Breast Cancer Research and Treatment

, Volume 83, Issue 3, pp 249–289 | Cite as

Relevance of Breast Cancer Cell Lines as Models for Breast Tumours: An Update

  • Marc Lacroix
  • Guy Leclercq


The number of available breast cancer cell (BCC) lines is small, and only a very few of them have been extensively studied. Whether they are representative of the tumours from which they originated remains a matter of debate. Whether their diversity mirrors the well-known inter-tumoural heterogeneity is another essential question. While numerous similarities have long been found between cell lines and tumours, recent technical advances, including the use of micro-arrays and comparative genetic analysis, have brought new data to the discussion. This paper presents most of the BCC lines that have been described in some detail to date. It evaluates the accuracy of the few of them widely used (MCF-7, T-47D, BT-474, SK-BR-3, MDA-MB-231, Hs578T) as tumour models. It is concluded that BCC lines are likely to reflect, to a large extent, the features of cancer cells in vivo. The importance of oestrogen receptor-alpha (gene ESR1) and Her-2/neu (ERBB2) as classifiers for cell lines and tumours is underlined. The recourse to a larger set of cell lines is suggested since the exact origin of some of the widely used lines remains ambiguous. Investigations on additional specific lines are expected to improve our knowledge of BCC and of the dialogue that these maintain with their surrounding normal cells in vivo.

breast cancer cell lines classification estrogen receptor gene expression Her-2/neu markers models tumours 


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  1. 1.
    Lasfargues EY, Ozzello L: Cultivation of human breast carcinomas. J Natl Cancer Inst 21: 1131–1147, 1958Google Scholar
  2. 2.
    Gazdar AF, Kurvari V, Virmani A, Gollahon L, Sakaguchi M, Westerfield M, Kodagoda D, Stasny V, Cunningham HT, Wistuba II, Tomlinson G, Tonk V, Ashfaq R, Leitch AM, Minna JD, Shay JW: Characterization of paired tumor and non-tumor cell lines established from patients with breast cancer. Int J Cancer 78: 766–774, 1998Google Scholar
  3. 3.
    Amadori D, Bertoni L, Flamingi A, Savini S, De Giovanni C, Casanova S, De Paola F, Amadori A, Giulotto E, Zoli W: Establishment and characterization of a new cell line from primary breast carcinoma. Breast Cancer Res Treat 28: 251–260, 1993Google Scholar
  4. 4.
    Cailleau R, Olivé M, Cruciger QV: Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In vitro 14: 911–915, 1978Google Scholar
  5. 5.
    Meltzer P, Leibovitz A, Dalton W, Villar H, Kute T, Davis J, Nagle R, Trent J: Establishment of two new cell lines derived from human breast carcinomas with Her-2/neu amplification. Br J Cancer 63: 727–735, 1991Google Scholar
  6. 6.
    Band V, Zajchowski D, Swisshelm K, Trask D, Kulesa V, Cohen C, Connolly J, Sager R: Tumor progression in four mammary epithelial cell lines derived from the same patient. Cancer Res 50: 7351–7357, 1990Google Scholar
  7. 7.
    Bacus SS, Kiguchi K, Chin D, King CR, Huberman E: Differentiation of cultured human breast cancer cells (AU-565 and MCF-7) associated with loss of cell surface Her-2/neu antigen. Mol Carcinogen 3: 350–362, 1990Google Scholar
  8. 8.
    Nordquist RE, Ishmael R, Lovig CA, Hyder DM, Hoge AF: The tissue culture and morphology of human breast tumor cell line BOT-2. Cancer Res 35: 3100–3105, 1975Google Scholar
  9. 9.
    Möbus VJ, Moll R, Gerharz CD, Kieback DG, Merk O, Runnebaum IB, Linner S, Dreher L, Grill HJ, Kreienberg R: Differential characteristics of two new tumorigenic cell lines of human breast carcinoma origin. Int J Cancer 77: 415–423, 1998Google Scholar
  10. 10.
    Watanabe M, Tanaka H, Kamada M, Okano JH, Takahashi H, Uchida K, Iwamura A, Zeniya M, Ohno T: Establishment of the human BSMZ breast cancer cell line, which overexpresses the erbB-2 and c-myc genes. Cancer Res 52: 5178–5182, 1992Google Scholar
  11. 11.
    Engel LW, Young NA: Human breast carcinoma in continuous culture: a review. Cancer Res 38: 4327–4339, 1978Google Scholar
  12. 12.
    Lasfargues EY, Coutinho WG, Redfield ES: Isolation of two human tumor epithelial cell lines from solid breast carcinomas. J Natl Cancer Inst 61: 967–978, 1978Google Scholar
  13. 13.
    Gioanni J, Courdi A, Lalanne CM, Fischel JL, Zanghellini E, Lambert JC, Ettore F, Namer M: Establishment, characterization, chemosensitivity, and radiosensitivity of two different cell lines derived from a human breast cancer biopsy. Cancer Res 45: 1246–1258, 1985Google Scholar
  14. 14.
    Gioanni J, Le François D, Zanghellini E, Mazeau C, Ettore F, Lambert JC, Schneider M: Establishment and characterisation of a new tumorigenic cell line with a normal karyotype derived from a human breast adenocarcinoma. Br J Cancer 62: 8–13, 1990Google Scholar
  15. 15.
    Fogh J, Wright WC, Loveless JD: Absence of HeLa cell contamination in 169 cell lines derived from human tumors. J Natl Cancer Inst 58: 209–214, 1977Google Scholar
  16. 16.
    Langlois AJ, Holder Jr WD, Iglehart JD, Nelson-Rees WA, Wells Jr SA, Bolognesi DP: Morphological and biochemical properties of a new human breast cancer cell line. Cancer Res 39: 2604–2613, 1979Google Scholar
  17. 17.
    Simon WE, Hansel M, Dietel M, Matthiesen L, Albrecht M, Holzel F: Alteration of steroid hormone sensitivity during the cultivation of human mammary carcinoma cells. In vitro 20: 157–166, 1984Google Scholar
  18. 18.
    Clayton SJ, May FE, Westley BR: Insulin-like growth factors control the regulation of oestrogen and progesterone receptor expression by oestrogens. Mol Cell Endocrinol 128: 57–68, 1997Google Scholar
  19. 19.
    Chu MY, Hagerty MG, Wiemann MC, Tibbetts LM, Sato S, Cummings FJ, Bogaars HA, Leduc EH, Calabresi P: Differential characteristics of two newly established human breast carcinoma cell lines. Cancer Res 45: 1357–1366, 1985Google Scholar
  20. 20.
    Lippman M, Bolan G, Huff K: The effects of estrogens and antiestrogens on hormone-responsive human breast cancer in long-term tissue culture. Cancer Res 36: 4595–4601, 1976Google Scholar
  21. 21.
    Borras M, Lacroix M, Legros N, Leclercq G: Estrogen receptor-negative/progesterone receptor-positive Evsa-T mammary tumor cells: a model for assessing the biological property of this peculiar phenotype of breast cancers. Cancer Lett 120: 23–30, 1997Google Scholar
  22. 22.
    Hurst J, Maniar N, Tombarkiewicz J, Lucas F, Roberson C, Steplewski Z, James W, Perras J: A novel model of a metastatic human breast tumour xenograft line. Br J Cancer 68: 274–276, 1993Google Scholar
  23. 23.
    Calaf G, Abarca-Quinones J, Feuilhade F, Beaune J, Dupre G, Orrico M, Barnabas-Sohi N, Kouyoumdjian JC: New cell lines of human breast cancer origin. Breast Cancer Res Treat 21: 63–75, 1992Google Scholar
  24. 24.
    Gaffney EV: A cell line (HBL-100) established from human breast milk. Cell Tissue Res 227: 563–568, 1982Google Scholar
  25. 25.
    Caron de Fromentel C, Nardeux PC, Soussi T, Lavialle C, Estrade S, Carloni G, Chandrasekaran K, Cassingena R: Epithelial HBL-100 cell line derived from milk of an apparently healthy woman harbours SV40 genetic information. Exp Cell Res 160: 83–94, 1985Google Scholar
  26. 26.
    Wang CS, Goulet F, Lavoie J, Drouin R, Auger F, Champetier S, Germain L, Tetu B: Establishment and characterization of a new cell line derived from a primary breast carcinoma. Cancer Genet Cytogenet 120: 58–72, 2000Google Scholar
  27. 27.
    Nayak SK, Kakati S, Harvey SR, Malone CC, Cornforth AN, Dillman RO: Characterization of cancer cell lines established from two human metastatic breast cancers. In vitro Cell Dev Biol Anim 36: 188–193, 2000Google Scholar
  28. 28.
    Briand P, Lykkesfeldt AE: An in vitro model of human breast carcinogenesis: epigenetic aspects. Breast Cancer Res Treat 65: 179–187, 2001Google Scholar
  29. 29.
    Hackett AJ, Smith HS, Springer EL, Owens RB, Nelson-Rees WA, Riggs JL, Gardner MB: Two syngeneic cell lines from human breast tissue: the aneuploid mammary epithelial (Hs578T) and the diploid myoepithelial (Hs578Bst) cell lines. J Natl Cancer Inst 58: 1795–1806, 1977Google Scholar
  30. 30.
    Loh PM, Clamon G, MacIndoe J, White M, Urdaneta L, Hukku B, Peterson WD: Development of a new human breast cancer cell line Ia-270. Breast Cancer Res Treat 5: 23–29, 1985Google Scholar
  31. 31.
    Siwek B, Larsimont D, Lacroix M, Body JJ: Establishment and characterization of three new breast-cancer cell lines. Int J Cancer 76: 677–683, 1998Google Scholar
  32. 32.
    Bover L, Barrio M, Slavutsky I, Bravo AI, Quintans C, Bagnati A, Lema B, Schiaffi J, Yomha R, Mordoh J: Description of a new human breast cancer cell line, IIB-BR-G, established from a primary undifferentiated tumor. Breast Cancer Res Treat 19: 47–56, 1991Google Scholar
  33. 33.
    Kurebayashi J, Kurosumi M, Sonoo H: A new human breast cancer cell line, KPL-1, secretes tumour-associated antigens and grows rapidly in female athymic nude mice. Br J Cancer 71: 845–853, 1995Google Scholar
  34. 34.
    Kurebayashi J, Kurosumi M, Sonoo H: A new human breast cancer cell line, KPL-3C, secretes parathyroid hormone-related protein and produces tumours associated with microcalcifications in nude mice. Br J Cancer 74: 200–207, 1996Google Scholar
  35. 35.
    Kurebayashi J, Otsuki T, Tang CK, Kurosumi M, Yamamoto S, Tanaka K, Mochizuki M, Nakamura H, Sonoo H: Isolation and characterization of a new human breast cancer cell line, KPL-4, expressing the Erb B family receptors and interleukin-6. Br J Cancer 79: 707–717, 1999Google Scholar
  36. 36.
    Thompson EW, Sung V, Lavigne M, Baumann K, Azumi N, Aaron AD, Clarke R: LCC15-MB: a vimentin-positive human breast cancer cell line from a femoral bone metastasis. Clin Exp Metastasis 17: 193–204, 1999Google Scholar
  37. 37.
    Rye PD, Norum L, Olsen DR, Garman-Vik S, Kaul S, Fodstad O: Brain metastasis model in athymic nude mice using a novelMUC1-secreting human breast-cancer cell line, MA11. Int J Cancer 68: 682–687, 1996Google Scholar
  38. 38.
    Micci F, Teixeira MR, Heim S: Complete cytogenetic characterization of the human breast cancer cell line MA11 combining G-banding, comparative genomic hybridization, multicolor fluorescence in situ hybridization, RxFISH, and chromosome-specific painting. Cancer Genet Cytogenet 131: 25–30, 2001Google Scholar
  39. 39.
    Zoli W, Roncuzzi L, Flamingi A, Gruppioni R, Sensi A, Zini N, Amadori D, Gasperi-Campani A: A new cell line from human infiltrating ductal carcinoma of the breast: establishment and characterization. J Cancer Res Clin Oncol 122: 237–242, 1996Google Scholar
  40. 40.
    Hambly RJ, Double JA, Thompson MJ, Bibby MC: Establishment and characterization of new cell lines from human breast tumours initially established as tumour xenografts in NMRI nude mice. Breast Cancer Res Treat 43: 247–258, 1997Google Scholar
  41. 41.
    Soule HD, Vazquez J, Long A, Albert S, Brennan M: A human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst 51: 1409–1416, 1973Google Scholar
  42. 42.
    Cailleau R, Young R, Olivé M, Reeves Jr WJ: Breast tumor cell lines from pleural effusions. J Natl Cancer Inst 53: 661–674, 1974Google Scholar
  43. 43.
    Young RK, Cailleau RM, Mackay B, Reeves Jr WJ: Establishment of epithelial cell line MDA-MB-157 from metastatic pleural effusion of human breast carcinoma. In vitro 9: 239–245, 1974Google Scholar
  44. 44.
    Hackenberg R, Luttchens S, Hofmann J, Kunzmann R, Holzel F, Schulz KD: Androgen sensitivity of the new human breast cancer cell line MFM-223. Cancer Res 51: 5722–5727, 1991Google Scholar
  45. 45.
    Naundorf H, Rewasowa EC, Fichtner I, Buttner B, Becker M, Gorlich M: Characterization of two human mammary carcinomas, MT-1 and MT-3, suitable for in vivo testing of ether lipids and their derivatives. Breast Cancer Res Treat 23: 87–95, 1992Google Scholar
  46. 46.
    Whitehead RH, Monaghan P, Webber LM, Bertoncello I, Vitali AA: A new human breast carcinoma cell line (PMC42) with stem cell characteristics. II. Characterization of cells growing as organoids. J Natl Cancer Inst 71: 1193–1203, 1983Google Scholar
  47. 47.
    Ethier SP, Mahacek ML, Gullick WJ, Frank TS, Weber BL: Differential isolation of normal luminal mammary epithelial cells and breast cancer cells from primary and metastatic sites using selective media. Cancer Res 53: 627–635, 1993Google Scholar
  48. 48.
    Keydar I, Chen L, Karby S, Weiss FR, Delarea J, Radu M, Chaitcik S, Brenner HJ: Establishment and characterization of a cell line of human breast carcinoma origin. Eur J Cancer 15: 659–670, 1979Google Scholar
  49. 49.
    Mehta RR, Bratescu L, Graves JM, Hart GD, Shilkaitis A, Green A, Beattie CW, Das Gupta TK: Human breast carcinoma cell lines: ultrastructural, genotypic, and immunocytochemical characterization. Anticancer Res 12: 683–692, 1992Google Scholar
  50. 50.
    Vandewalle B, Collyn d'Hooghe M, Savary JB, Vilain MO, Peyrat JP, Deminatti M, Delobelle-Deroide A, Lefebvre J: Establishment and characterization of a new cell line (VHB-1) derived from a primary breast carcinoma. J Cancer Res Clin Oncol 113: 550–558, 1987Google Scholar
  51. 51.
    Engel LW, Young NA, Tralka TS, Lippman ME, O'Brien SJ, Joyce MJ: Establishment and characterization of three new continuous cell lines derived from human breast carcinomas. Cancer Res 38: 3352–3364, 1978Google Scholar
  52. 52.
    Kytola S, Rummukainen J, Nordgren A, Karhu R, Farnebo F, Isola J, Larsson C: Chromosomal alterations in 15 breast cancer cell lines by comparative genomic hybridization and spectral karyotyping. Genes Chromosomes Cancer 28: 308–317, 2000Google Scholar
  53. 53.
    Davidson JM, Gorringe KL, Chin SF, Orsetti B, Besret C, Courtay-Cahen C, Roberts I, Theillet C, Caldas C, Edwards PA: Molecular cytogenetic analysis of breast cancer cell lines. Br J Cancer 83: 1309–1317, 2000Google Scholar
  54. 54.
    Lacroix M, Marie PJ, Body JJ: Protein production by osteoblasts: modulation by breast cancer cell-derived factors. Breast Cancer Res Treat 61: 59–67, 2000Google Scholar
  55. 55.
    DeFazio A, Chiew YE, Sini RL, Janes PW, Sutherland RL: Expression of c-erbB receptors, heregulin and oestrogen receptor in human breast cell lines. Int J Cancer 87: 487–498, 2000Google Scholar
  56. 56.
    Sartor CI, Dziubinski ML, Yu CL, Jove R, Ethier SP: Role of epidermal growth factor receptor and STAT-3 activation in autonomous proliferation of SUM-102PT human breast cancer cells. Cancer Res 57: 978–987, 1997Google Scholar
  57. 57.
    Berquin IM, Dziubinski ML, Nolan GP, Ethier SP: A functional screen for genes inducing epidermal growth factor autonomy of human mammary epithelial cells confirms the role of amphiregulin. Oncogene 20: 4019–4028, 2001Google Scholar
  58. 58.
    Forozan F, Veldman R, Ammerman CA, Parsa NZ, Kallioniemi A, Kallioniemi OP, Ethier SP: Molecular cytogenetic analysis of 11 new breast cancer cell lines. Br J Cancer 81: 1328–1334, 1999Google Scholar
  59. 59.
    McLeskey SW, Ding IY, Lippman ME, Kern FG: MDAMB-134 breast carcinoma cells overexpress fibroblast growth factor (FGF) receptors and are growth-inhibited by FGF ligands. Cancer Res 54: 523–530, 1994Google Scholar
  60. 60.
    Tannheimer SL, Rehemtulla A, Ethier SP: Characterization of fibroblast growth factor receptor 2 overexpression in the human breast cancer cell line SUM-52PE. Breast Cancer Res 2: 311–320, 2000Google Scholar
  61. 61.
    Jarvinen TA, Tanner M, Rantanen V, Barlund M, Borg A, Grenman S, Isola J: Amplification and deletion of topoisomerase II alpha associate with ErbB-2 amplification and affect sensitivity to topoisomerase II inhibitor doxorubicin in breast cancer. Am J Pathol 156: 839–847, 2000Google Scholar
  62. 62.
    Kauraniemi P, Barlund M, Monni O, Kallioniemi A: New amplified and highly expressed genes discovered in the ERBB2 amplicon in breast cancer by cDNA microarrays. Cancer Res 61: 8235–8240, 2001Google Scholar
  63. 63.
    Ackland ML, Michalczyk A, Whitehead RH: PMC42, a novel model for the differentiated human breast. Exp Cell Res 263: 14–22, 2001Google Scholar
  64. 64.
    Ackland ML, Newgreen DF, Fridman M, Waltham MC, Arvanitis A, Minichiello J, Price JT, Thompson EW: Epidermal growth factor-induced epithelio-mesenchymal transition in human breast carcinoma cells. Lab Invest 83: 435–448, 2003Google Scholar
  65. 65.
    Engebraaten O, Fodstad O: Site-specific experimental metastasis patterns of two human breast cancer cell lines in nude rats. Int J Cancer 82: 219–225, 1999Google Scholar
  66. 66.
    Wistuba II, Behrens C, Milchgrub S, Syed S, Ahmadian M, Virmani AK, Kurvari V, Cunningham TH, Ashfaq R, Minna JD, Gazdar AF: Comparison of features of human breast cancer cell lines and their corresponding tumors. Clin Cancer Res 4: 2931–2938, 1998Google Scholar
  67. 67.
    Jones C, Payne J, Wells D, Delhanty JD, Lakhani SR, Kortenkamp A: Comparative genomic hybridization reveals extensive variation among different MCF-7 cell stocks. Cancer Genet Cytogenet 117: 153–158, 2000Google Scholar
  68. 68.
    Rooney PH, Stevenson DA, Marsh S, Johnston PG, Haites NE, Cassidy J, McLeod HL: Comparative genomic hybridization analysis of chromosomal alterations induced by the development of resistance to thymidylate synthase inhibitors. Cancer Res 58: 5042–5045, 1998Google Scholar
  69. 69.
    Wosikowski K, Schuurhuis D, Kops GJ, Saceda M, Bates SE: Altered gene expression in drug-resistant human breast cancer cells. Clin Cancer Res 3: 2405–2414, 1997Google Scholar
  70. 70.
    Turton NJ, Judah DJ, Riley J, Davies R, Lipson D, Styles JA, Smith AG, Gant TW: Gene expression and amplification in breast carcinoma cells with intrinsic and acquired doxorubicin resistance. Oncogene 20: 1300–1306, 2001Google Scholar
  71. 71.
    Hansen CM, Rohde L, Madsen MW, Hansen D, Colston KW, Pirianov G, Holm PK, Binderup L: MCF-7/VD(R): a new vitamin D resistant cell line. J Cell Biochem 82: 422–436, 2001Google Scholar
  72. 72.
    Clarke R, Brünner N: Acquired estrogen independence and antiestrogen resistance in breast cancer. Trends Endocrinol Metab 7: 291–301, 1996Google Scholar
  73. 73.
    Brünner N, Boysen B, Jirus S, Skaar TC, Holst-Hansen C, Lippman J, Frandsen T, Spang-Thomsen M, Fuqua SAW, Clarke R: MCF7/LCC9: an antiestrogen ICI 182,780 confers an early cross-resistance to the nonsteroidal antiestrogen tamoxifen. Cancer Res 57: 3486–3493, 1997Google Scholar
  74. 74.
    Leonessa F, Green D, Licht T, Wright A, Wingate-Legette K, Lippman J, Gottesman MM, Clarke R: MDA435/LCC6 and MDA435/LCC6MDR1: ascites models of human breast cancer. Br J Cancer 73: 154–161, 1996Google Scholar
  75. 75.
    Yoneda T, Williams PJ, Hiraga T, Niewolna M, Nishimura R: A bone-seeking clone exhibits different biological properties from the MDA-MB-231 parental human breast cancer cells and a brain-seeking clone in vivo and in vitro. J Bone Miner Res 16: 1486–1495, 2001Google Scholar
  76. 76.
    Tomlinson GE, Chen TT, Stastny VA, Virmani AK, Spillman MA, Tonk V, Blum JL, Schneider NR, Wistuba II, Shay JW, Minna JD, Gazdar AF: Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res 58: 3237–3242, 1998Google Scholar
  77. 77.
    Scully R, Ganesan S, Vlasakova K, Chen J, Socolovsky M, Livingston DM: Genetic analysis of BRCA1 function in a defined tumor cell line. Mol Cell 4: 1093–1099, 1999Google Scholar
  78. 78.
    Lee JS, Collins KM, Brown AL, Lee CH, Chung JH: hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature 404: 201–204, 2000Google Scholar
  79. 79.
    Lu M, Arrick BA: Transactivation of the p21 promoter by BRCA1 splice variants in mammary epithelial cells: evidence for both common and distinct activities of wildtype and mutant forms. Oncogene 19: 6351–6360, 2000Google Scholar
  80. 80.
    Fan S, Ma YX, Wang C, Yuan RQ, Meng Q, Wang JA, Erdos M, Goldberg ID, Webb P, Kushner PJ, Pestell RG, Rosen EM: Role of direct interaction in BRCA1 inhibition of estrogen receptor activity. Oncogene 20: 77–87, 2001Google Scholar
  81. 81.
    Ruffner H, Joazeiro CA, Hemmati D, Hunter T, Verma IM: Cancer predisposing mutations within the RING domain of BRCA1: loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. Proc Natl Acad Sci USA 98: 5134–5139, 2001Google Scholar
  82. 82.
    Berns EM, van Staveren IL, Verhoog L, van de Ouweland AM, Meijer-van Gelder M, Meijers-Heijboer H, Portengen H, Foekens JA, Dorssers LC, Klijn JG: Molecular profiles of BRCA1-mutated and matched sporadic breast tumours: relation with clinico-pathological features. Br J Cancer 85: 538–545, 2001Google Scholar
  83. 83.
    Fan S, Yuan R, Ma YX, Meng Q, Goldberg ID, Rosen EM: Mutant BRCA1 genes antagonize phenotype of wild-type BRCA1. Oncogene 20: 8215–8235, 2001Google Scholar
  84. 84.
    Andrews HN, Mullan PB, McWilliams S, Sebelova S, Quinn JE, Gilmore PM, McCabe N, Pace A, Koller B, Johnston PG, Haber DA, Harkin DP: BRCA1 regulates the interferon gamma-mediated apoptotic response. J Biol Chem 277: 26225–26232, 2002Google Scholar
  85. 85.
    Okada S, Ouchi T: Cell cycle differences in DNA damage-induced BRCA1 phosphorylation affect its subcellular localization. J Biol Chem 278: 2015–2020, 2003Google Scholar
  86. 86.
    Tassone P, Tagliaferri P, Perricelli A, Blotta S, Quaresima B, Martelli ML, Goel A, Barbieri V, Costanzo F, Boland CR, Venuta S: BRCA1 expression modulates chemosensitivity of BRCA1-defective HCC1937 human breast cancer cells. Br J Cancer 88: 1285–12891, 2003Google Scholar
  87. 87.
    Shattuck-Eidens D, Oliphant A, McClure M, McBride C, Gupte J, Rubano T, Pruss D, Tavtigian SV, Teng DH, Adey N, Staebell M, Gumpper K, Lundstrom R, Hulick M, Kelly M, Holmen J, Lingenfelter B, Manley S, Fujimura F, Luce M, Ward B, Cannon-Albright L, Steele L, Offit K, Gilewski T, Norton L, Brown K, Schulz C, Hampel H, Schluger A, Giulotto E, Zoli W, Ravaioli A, Nevanlinna H, Pyrhonen S, Rowley P, Scalia J, Michaelson R, Scottt R, Radice P, Pierotti M, Garber J, Isaacs C, Peshkin B, Lippman M, Dosik M, Caligo M, Greenstein R, Pilarski R, Weber B, Burgemeister R, Frank T, Skolnick M, Thomas A: BRCA1 sequence analysis in women at high risk for susceptibility mutations. Risk factor analysis and implications for genetic testing. JAMA 278: 1242–1250, 1997Google Scholar
  88. 88.
    Annab LA, Terry L, Cable PL, Brady J, Stampfer MR, Barrett JC, Afshari CA: Establishment and characterization of a breast cell strain containing a BRCA1 185delAG mutation. Gynecol Oncol 77: 121–128, 2000Google Scholar
  89. 89.
    Ahmadian M, Wistuba II, Fong KM, Behrens C, Kodagoda DR, Saboorian MH, Shay J, Tomlinson GE, Blum J, Minna JD, Gazdar AF: Analysis of the FHIT gene and FRA3B region in sporadic breast cancer, preneoplastic lesions, and familial breast cancer probands. Cancer Res 57: 3664–3668, 1997Google Scholar
  90. 90.
    Shay JW, Tomlinson G, Piatyszek MA, Gollahon LS: Spontaneous in vitro immortalization of breast epithelial cells from a patient with Li-Fraumeni syndrome. Mol Cell Biol 15: 425–432, 1995Google Scholar
  91. 91.
    Nathanson KL, Weber BL: 'Other' breast cancer susceptibility genes: searching for more holy grail. Hum Mol Genet 10: 715–720, 2001Google Scholar
  92. 92.
    Jaiyesimi IA, Buzdar AU, Hortobagyi G: Inflammatory breast cancer: a review. J Clin Oncol 10: 1014–1024, 1992Google Scholar
  93. 93.
    Kleer CG, van Golen KL, Merajver SD: Molecular biology of breast cancer metastasis. Inflammatory breast cancer: clinical syndrome and molecular determinants. Breast Cancer Res 2: 423–429, 2000Google Scholar
  94. 94.
    Turpin E, Bieche I, Bertheau P, Plassa LF, Lerebours F, de Roquancourt A, Olivi M, Espie M, Marty M, Lidereau R, Vidaud M, de The H: Increased incidence of ERBB2 overexpression and TP53 mutation in inflammatory breast cancer. Oncogene 21: 7593–7597, 2002Google Scholar
  95. 95.
    Colpaert CG, Vermeulen PB, Benoy I, Soubry A, van Roy F, van Beest P, Goovaerts G, Dirix LY, van Dam P, Fox SB, Harris AL, van Marck EA: Inflammatory breast cancer shows angiogenesis with high endothelial proliferation rate and strong E-cadherin expression. Br J Cancer 88: 718–725, 2003Google Scholar
  96. 96.
    van Golen KL, Davies S, Wu ZF, Wang Y, Bucana CD, Root H, Chandrasekharappa S, Strawderman M, Ethier SP, Merajver SD: A novel putative low-affinity insulin-like growth factor-binding protein, LIBC (lost in inflammatory breast cancer), and RhoC GTPase correlate with the inflammatory breast cancer phenotype. Clin Cancer Res 5: 2511–2519, 1999Google Scholar
  97. 97.
    van Golen KL, Wu ZF, Qiao XT, Bao LW, Merajver SD: RhoC GTPase, a novel transforming oncogene for human mammary epithelial cells that partially recapitulates the inflammatory breast cancer phenotype. Cancer Res 60: 5832–5838, 2000Google Scholar
  98. 98.
    van Golen KL, Wu ZF, Qiao XT, Bao L, Merajver SD: RhoC GTPase overexpression modulates induction of angiogenic factors in breast cells. Neoplasia 2: 418–425, 2000Google Scholar
  99. 99.
    van Golen KL, Bao LW, Pan Q, Miller FR, Wu ZF, Merajver SD: Mitogen activated protein kinase pathway is involved in RhoC GTPase induced motility, invasion and angiogenesis in inflammatory breast cancer. Clin Exp Metastasis 19: 301–311, 2002Google Scholar
  100. 100.
    van Golen KL, Bao L, DiVito MM, Wu Z, Prendergast GC, Merajver SD: Reversion of RhoC GTPase-induced inflammatory breast cancer phenotype by treatment with a farnesyl transferase inhibitor. Mol Cancer Ther 1: 575–583, 2002Google Scholar
  101. 101.
    van Golen KL: Inflammatory breast cancer: relationship between growth factor signaling and motility in aggressive cancers. Breast Cancer Res 5: 174–179, 2003Google Scholar
  102. 102.
    Kleer CG, Zhang Y, Pan Q, van Golen KL, Wu ZF, Livant D, Merajver SD: WISP3 is a novel tumor suppressor gene of inflammatory breast cancer. Oncogene 21: 3172–3180, 2002Google Scholar
  103. 103.
    Alpaugh ML, Tomlinson JS, Shao ZM, Barsky SH: A novel human xenograft model of inflammatory breast cancer. Cancer Res 59: 5079–5084, 1999Google Scholar
  104. 104.
    Alpaugh ML, Tomlinson JS, Ye Y, Barsky SH: Relationship of sialyl-Lewis(x/a) underexpression and E-cadherin overexpression in the lymphovascular embolus of inflammatory breast carcinoma. Am J Pathol 161: 619–628, 2002Google Scholar
  105. 105.
    Alpaugh ML, Tomlinson JS, Kasraeian S, Barsky SH: Cooperative role of E-cadherin and sialyl-Lewis X/A-deficient MUC1 in the passive dissemination of tumor emboli in inflammatory breast carcinoma. Oncogene 21: 3631–3643, 2002Google Scholar
  106. 106.
    Shirakawa K, Tsuda H, Heike Y, Kato K, Asada R, Inomata M, Sasaki H, Kasumi F, Yoshimoto M, Iwanaga T, Konishi F, Terada M, Wakasugi H: Absence of endothelial cells, central necrosis, and fibrosis are associated with aggressive inflammatory breast cancer. Cancer Res 61: 445–451, 2001Google Scholar
  107. 107.
    Leclercq G: Molecular forms of the estrogen receptor in breast cancer. J Steroid Biochem Mol Biol 80: 259–272, 2002Google Scholar
  108. 108.
    Palmieri C, Cheng GJ, Saji S, Zelada-Hedman M, Warri A, Weihua Z, Van Noorden S, Wahlstrom T, Coombes RC, Warner M, Gustafsson JA: Estrogen receptor beta in breast cancer. Endocr Relat Cancer 9: 1–13, 2002Google Scholar
  109. 109.
    Lacroix M, Querton G, Hennebert P, Larsimont D, Leclercq G: Estrogen receptor analysis in primary breast tumors by ligand-binding assay, immunocytochemical assay, and northern blot: a comparison. Breast Cancer Res Treat 67: 263–271, 2001Google Scholar
  110. 110.
    Jensen EV, Cheng G, Palmieri C, Saji S, Makela S, Van Noorden S, Wahlstrom T, Warner M, Coombes RC, Gustafsson JA: Estrogen receptors and proliferation markers in primary and recurrent breast cancer. Proc Natl Acad Sci USA 98: 15197–15202, 2001Google Scholar
  111. 111.
    Ethier SP: Growth factor synthesis and human breast cancer progression. J Natl Cancer Inst 87: 964–973, 1995Google Scholar
  112. 112.
    Thompson EW, Paik S, Brunner N, Sommers CL, Zugmaier G, Clarke R, Shima TB, Torri J, Donahue S, Lippman ME, Martin GR, Dickson RB: Association of increased basement membrane invasiveness with absence of estrogen receptor and expression of vimentin in human breast cancer cell lines. J Cell Physiol 150: 534–544, 1992Google Scholar
  113. 113.
    Sommers CL, Byers SW, Thompson EW, Torri JA, Gelmann EP: Differentiation state and invasiveness of human breast cancer cell lines. Breast Cancer Res Treat 31: 325–335, 1994Google Scholar
  114. 114.
    Boyer B, Valles AM, Edme N: Induction and regulation of epithelial-mesenchymal transitions. Biochem Pharmacol 60: 1091–1099, 2000Google Scholar
  115. 115.
    Sommers CL, Heckford SE, Skerker JM, Worland P, Torri JA, Thompson EW, Byers SW, Gelmann EP: Loss of epithelial markers and acquisition of vimentin expression in adriamycin-and vinblastine-resistant human breast cancer cell lines. Cancer Res 52: 5190–5197, 1992Google Scholar
  116. 116.
    Vickers PJ, Dickson RB, Shoemaker R, Cowan KH: A multidrug-resistant MCF-7 human breast cancer cell line which exhibits cross-resistance to antiestrogens and hormone-independent tumor growth in vivo. Mol Endocrinol 2: 886–892, 1988Google Scholar
  117. 117.
    Hendrix MJ, Seftor EA, Seftor RE, Trevor KT: Experimental co-expression of vimentin and keratin intermediate filaments in human breast cancer cells results in phenotypic interconversion and increased invasive behavior. Am J Pathol 150: 483–495, 1997Google Scholar
  118. 118.
    Fuqua SA: The role of estrogen receptors in breast cancer metastasis. J Mamm Gland Biol Neoplasia 6: 407–417, 2001Google Scholar
  119. 119.
    Gilles C, Polette M, Zahm JM, Tournier JM, Volders L, Foidart JM, Birembaut P: Vimentin contributes to human mammary epithelial cell migration. J Cell Sci 112: 4615–4625, 1999Google Scholar
  120. 120.
    D'souza B, Taylor-Papadimitriou J: Overexpression of ERBB2 in human mammary epithelial cells signals inhibition of transcription of the E-cadherin gene. Proc Natl Acad Sci USA 91: 7202–7206, 1994Google Scholar
  121. 121.
    Grunt TW, Saceda M, Martin MB, Lupu R, Dittrich E, Krupitza G, Harant H, Huber H, Dittrich C: Bidirectional interactions between the estrogen receptor and the cerbB-2 signaling pathways: heregulin inhibits estrogenic effects in breast cancer cells. Int J Cancer 63: 560–567, 1995Google Scholar
  122. 122.
    de Cremoux P, Gauville C, Closson V, Linares G, Calvo F, Tavitian A, Olofsson B: EGF modulation of the ras-related rhoB gene expression in human breast-cancer cell lines. Int J Cancer 59: 408–415, 1994Google Scholar
  123. 123.
    Kuang WW, Thompson DA, Hoch RV, Weigel RJ: Differential screening and suppression subtractive hybridization identified genes differentially expressed in an estrogen receptor-positive breast carcinoma cell line. Nucl Acids Res 26: 1116–1123, 1998Google Scholar
  124. 124.
    Kirschmann DA, Lininger RA, Gardner LM, Seftor EA, Odero VA, Ainsztein AM, Earnshaw WC, Wallrath LL, Hendrix MJ: Down-regulation of HP1Hsalpha expression is associated with the metastatic phenotype in breast cancer. Cancer Res 60: 3359–3363, 2000Google Scholar
  125. 125.
    Parker C, Rampaul RS, Pinder SE, Bell JA, Wencyk PM, Blamey RW, Nicholson RI, Robertson JF, Ellis IO: E-cadherin as a prognostic indicator in primary breast cancer. Br J Cancer 85: 1958–1963, 2001Google Scholar
  126. 126.
    Swisshelm K, Machl A, Planitzer S, Robertson R, Kubbies M, Hosier S: SEMP1, a senescence-associated cDNA isolated from human mammary epithelial cells, is a member of an epithelial membrane protein superfamily. Gene 226: 285–295, 1999Google Scholar
  127. 127.
    Kominsky SL, Argani P, Korz D, Evron E, Raman V, Garrett E, Rein A, Sauter G, Kallioniemi OP, Sukumar S: Loss of the tight junction protein claudin-7 correlates with histological grade in both ductal carcinoma in situ and invasive ductal carcinoma of the breast. Oncogene 22: 2021–2033, 2003Google Scholar
  128. 128.
    Davies EL, Gee JM, Cochrane RA, Jiang WG, Sharma AK, Nicholson RI, Mansel RE: The immunohistochemical expression of desmoplakin and its role in vivo in the progression and metastasis of breast cancer. Eur J Cancer 35: 902–907, 1999Google Scholar
  129. 129.
    Zafrani B, Aubriot MH, Mouret E, De Cremoux P, De Rycke Y, Nicolas A, Boudou E, Vincent-Salomon A, Magdelenat H, Sastre-Garau X: High sensitivity and specificity of immunohistochemistry for the detection of hormone receptors in breast carcinoma: comparison with biochemical determination in a prospective study of 793 cases. Histopathology 37: 536–545, 2000Google Scholar
  130. 130.
    Tong D, Schneeberger C, Czerwenka K, Schmutzler RK, Speiser P, Kucera E, Concin N, Kubista E, Leodolter S, Zeillinger R: Messenger RNA determination of estrogen receptor, progesterone receptor, pS2, and plasminogen activator inhibitor-1 by competitive reverse transcription-polymerase chain reaction in human breast cancer. Clin Cancer Res 5: 1497–1502, 1999Google Scholar
  131. 131.
    Ringberg A, Anagnostaki L, Anderson H, Idvall I, Ferno M; South Sweden Breast Cancer Group: cell biological factors in ductal carcinoma in situ (DCIS) of the breast-relationship to ipsilateral local recurrence and histopathological characteristics. Eur J Cancer 37: 1514–1522, 2001Google Scholar
  132. 132.
    Hoch RV, Thompson DA, Baker RJ, Weigel RJ: GATA-3 is expressed in association with estrogen receptor in breast cancer. Int J Cancer 84: 122–128, 1999Google Scholar
  133. 133.
    Xiang YY, Ladeda V, Filmus J: Glypican-3 expression is silenced in human breast cancer. Oncogene 20: 7408–7412, 2001Google Scholar
  134. 134.
    Daly RJ, Sanderson GM, Janes PW, Sutherland RL: Cloning and characterization of GRB14, a novel member of the GRB7 gene family. J Biol Chem 271: 12502–12510, 1996Google Scholar
  135. 135.
    Ghosh MG, Thompson DA, Weigel RJ: PDZK1 and GREB1 are estrogen-regulated genes expressed in hormone-responsive breast cancer. Cancer Res 60: 6367–6375, 2000Google Scholar
  136. 136.
    Yee D, Favoni RE, Lippman ME, Powell DR: Identification of insulin-like growth factor binding proteins in breast cancer cells. Breast Cancer Res Treat 18: 3–10, 1991Google Scholar
  137. 137.
    Figueroa JA, Jackson JG, McGuire WL, Krywicki RF, Yee D: Expression of insulin-like growth factor binding proteins in human breast cancer correlates with estrogen receptor status. J Cell Biochem 52: 196–205, 1993Google Scholar
  138. 138.
    Foster KW, Frost AR, McKie-Bell P, Lin CY, Engler JA, Grizzle WE, Ruppert JM: Increase of GKLF messenger RNA and protein expression during progression of breast cancer. Cancer Res 60: 6488–6495, 2000Google Scholar
  139. 139.
    Schaller G, Fuchs I, Pritze W, Ebert A, Herbst H, Pantel K, Weitzel H, Lengyel E: Elevated keratin 18 protein expression indicates a favorable prognosis in patients with breast cancer. Clin Cancer Res 2: 1879–1885, 1996Google Scholar
  140. 140.
    Gudas JM, Nguyen H, Klein RC, Katayose D, Seth P, Cowan KH: Differential expression of multiple MDM2 messenger RNAs and proteins in normal and tumorigenic breast epithelial cells. Clin Cancer Res 1: 71–80, 1995Google Scholar
  141. 141.
    Hori M, Shimazaki J, Inagawa S, Itabashi M, Hori M: Overexpression of MDM2 oncoprotein correlates with possession of estrogen receptor alpha and lack of MDM2 mRNA splice variants in human breast cancer. Breast Cancer Res Treat 71: 77–83, 2002Google Scholar
  142. 142.
    Hartsough MT, Clare SE, Mair M, Elkahloun AG, Sgroi D, Osborne CK, Clark G, Steeg PS: Elevation of breast carcinoma Nm23-H1 metastasis suppressor gene expression and reduced motility by DNA methylation inhibition. Cancer Res 61: 2320–2327, 2001Google Scholar
  143. 143.
    Hartsough MT, Steeg PS: Nm23/nucleoside diphosphate kinase in human cancers. J Bioenerg Biomem 32: 301–308, 2000Google Scholar
  144. 144.
    Hall RE, Lee CS, Alexander IE, Shine J, Clarke CL, Sutherland RL: Steroid hormone receptor gene expression in human breast cancer cells: inverse relationship between oestrogen and glucocorticoid receptor messenger RNA levels. Int J Cancer 46: 1081–1087, 1990Google Scholar
  145. 145.
    Tong D, Czerwenka K, Sedlak J, Schneeberger C, Schiebel I, Concin N, Leodolter S, Zeillinger R: Association of in vitro invasiveness and gene expression of estrogen receptor, progesterone receptor, pS2 and plasminogen activator inhibitor-1 in human breast cancer cell lines. Breast Cancer Res Treat 56: 91–97, 1999Google Scholar
  146. 146.
    Du Y, Carling T, Fang W, Piao Z, Sheu JC, Huang S: Hypermethylation in human cancers of the RIZ1 tumor suppressor gene, a member of a histone/protein methyltransferase superfamily. Cancer Res 61: 8094–8099, 2001Google Scholar
  147. 147.
    Peirce SK, Chen WY, Chen WY: Quantification of prolactin receptor mRNA in multiple human tissues and cancer cell lines by real time RT-PCR. J Endocrinol 171: R1–R4, 2001Google Scholar
  148. 148.
    Gill S, Peston D, Vonderhaar BK, Shousha S: Expression of prolactin receptors in normal, benign, and malignant breast tissue: an immunohistological study. J Clin Pathol 54: 956–960, 2001Google Scholar
  149. 149.
    Yip SS, Crew AJ, Gee JM, Hui R, Blamey RW, Robertson JF, Nicholson RI, Sutherland RL, Daly RJ: Up-regulation of the protein tyrosine phosphatase SHP-1 in human breast cancer and correlation with GRB2 expression. Int J Cancer 88: 363–368, 2000Google Scholar
  150. 150.
    Finlin BS, Gau CL, Murphy GA, Shao H, Kimel T, Seitz RS, Chiu YF, Botstein D, Brown PO, Der CJ, Tamanoi F, Andres DA, Perou CM: RERG is a novel ras-related, estrogen-regulated and growth-inhibitory gene in breast cancer. J Biol Chem 276: 42259–42267, 2001Google Scholar
  151. 151.
    Stemmer-Rachamimov AO, Wiederhold T, Nielsen GP, James M, Pinney-Michalowski D, Roy JE, Cohen WA, Ramesh V, Louis DN: NHE-RF, a merlin-interacting protein, is primarily expressed in luminal epithelia, proliferative endometrium, and estrogen receptor-positive breast carcinomas. Am J Pathol 158: 57–62, 2001Google Scholar
  152. 152.
    Oberst M, Anders J, Xie B, Singh B, Ossandon M, Johnson M, Dickson RB, Lin CY: Matriptase and HAI-1 are expressed by normal and malignant epithelial cells in vitro and in vivo. Am J Pathol 158: 1301–1311, 2001Google Scholar
  153. 153.
    Bouras T, Southey MC, Chang AC, Reddel RR, Willhite D, Glynne R, Henderson MA, Armes JE, Venter DJ: Stanniocalcin 2 is an estrogen-responsive gene coexpressed with the estrogen receptor in human breast cancer. Cancer Res 62: 1289–1295, 2002Google Scholar
  154. 154.
    Yuan Y, Mendez R, Sahin A, Dai JL: Hypermethylation leads to silencing of the SYK gene in human breast cancer. Cancer Res 61: 5558–5561, 2001Google Scholar
  155. 155.
    Gillesby BE, Zacharewski TR: pS2 (TFF1) levels in human breast cancer tumor samples: correlation with clinical and histological prognostic markers. Breast Cancer Res Treat 56: 253–265, 1999Google Scholar
  156. 156.
    Hoover KB, Liao SY, Bryant PJ: Loss of the tight junction MAGUK ZO-1 in breast cancer: relationship to glandular differentiation and loss of heterozygosity. Am J Pathol 153: 1767–1773, 1998Google Scholar
  157. 157.
    Byrne JA, Tomasetto C, Garnier JM, Rouyer N, Mattei MG, Bellocq JP, Rio MC, Basset P: A screening method to identify genes commonly overexpressed in carcinomas and the identification of a novel complementary DNA sequence. Cancer Res 55: 2896–2903, 1995Google Scholar
  158. 158.
    Nakatani K, Thompson DA, Barthel A, Sakaue H, Liu W, Weigel RJ, Roth RA: Up-regulation of Akt3 in estrogen receptor-deficient breast cancers and androgen-independent prostate cancer lines. J Biol Chem 274: 21528–21532, 1999Google Scholar
  159. 159.
    Hayes AJ, Huang WQ, Yu J, Maisonpierre PC, Liu A, Kern FG, Lippman ME, McLeskey SW, Li LY: Expression and function of angiopoietin-1 in breast cancer. Br J Cancer 83: 1154–1160, 2000Google Scholar
  160. 160.
    Hardwick M, Fertikh D, Culty M, Li H, Vidic B, Papadopoulos V: Peripheral-type benzodiazepine receptor (PBR) in human breast cancer: correlation of breast cancer cell aggressive phenotype with PBR expression, nuclear localization, and PBR-mediated cell proliferation and nuclear transport of cholesterol. Cancer Res 59: 831–842, 1999Google Scholar
  161. 161.
    Paredes J, Milanezi F, Viegas L, Amendoeira I, Schmitt F: P-cadherin expression is associated with high-grade ductal carcinoma in situ of the breast. Virchows Arch 440: 16–21, 2002Google Scholar
  162. 162.
    Pishvaian MJ, Feltes CM, Thompson P, Bussemakers MJ, Schalken JA, Byers SW: Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Res 59: 947–952, 1999Google Scholar
  163. 163.
    Hui R, Macmillan RD, Kenny FS, Musgrove EA, Blamey RW, Nicholson RI, Robertson JF, Sutherland RL: INK4a gene expression and methylation in primary breast cancer: overexpression of p16INK4a messenger RNA is a marker of poor prognosis. Clin Cancer Res 6: 2777–2787, 2000Google Scholar
  164. 164.
    Yee LD, Liu L: The constitutive production of colony stimulating factor 1 by invasive human breast cancer cells. Anticancer Res 20: 4379–4383, 2000Google Scholar
  165. 165.
    Thompson DA, Weigel RJ: Characterization of a gene that is inversely correlated with estrogen receptor expression (ICERE-1) in breast carcinomas. Eur J Biochem 252: 169–177, 1998Google Scholar
  166. 166.
    Klijn JG, Berns PM, Schmitz PI, Foekens JA: The clinical significance of epidermal growth factor receptor (EGF-R) in human breast cancer: a review on 5232 patients. Endocr Rev 13: 3–17, 1992Google Scholar
  167. 167.
    Walker RA, Dearing SJ: Expression of epidermal growth factor receptor mRNA and protein in primary breast carcinomas. Breast Cancer Res Treat 53: 167–176, 1999Google Scholar
  168. 168.
    Spizzo G, Obrist P, Ensinger C, Theurl I, Dunser M, Ramoni A, Gunsilius E, Eibl G, Mikuz G, Gastl G: Prognostic significance of Ep-CAM AND Her-2/neu overexpression in invasive breast cancer. Int J Cancer 98: 883–888, 2002Google Scholar
  169. 169.
    Tagliabue E, Menard S, Robertson JF, Harris L: c-erbB-2 expression in primary breast cancer. Int J Biol Markers 14: 16–26, 1999Google Scholar
  170. 170.
    Tsuda H, Hirohashi S, Shimosato Y, Hirota T, Tsugane S, Watanabe S, Terada M, Yamamoto H: Correlation between histologic grade of malignancy and copy number of c-erbB-2 gene in breast carcinoma. A retrospective analysis of 176 cases. Cancer 65: 1794–1800, 1990Google Scholar
  171. 171.
    Rilke F, Colnaghi MI, Cascinelli N, Andreola S, Baldini MT, Bufalino R, Della Porta G, Menard S, Pierotti MA, Testori A: Prognostic significance of Her-2/neu expression in breast cancer and its relationship to other prognostic factors. Int J Cancer 49: 44–49, 1991Google Scholar
  172. 172.
    Hoque A, Sneige N, Sahin AA, Menter DG, Bacus JW, Hortobagyi GN, Lippman SM: Her-2/neu gene amplification in ductal carcinoma in situ of the breast. Cancer Epidemiol Biomarkers Prev 11: 587–590, 2002Google Scholar
  173. 173.
    Hoff ER, Tubbs RR, Myles JL, Procop GW: HER2/neu amplification in breast cancer: stratification by tumor type and grade. Am J Clin Pathol 117: 916–921, 2002Google Scholar
  174. 174.
    Gilles C, Polette M, Birembaut P, Brunner N, Thompson EW: Expression of c-ets-1 mRNA is associated with an invasive, EMT-derived phenotype in breast carcinoma cell lines. Clin Exp Metastasis 15: 519–526, 1997Google Scholar
  175. 175.
    Esworthy RS, Baker MA, Chu FF: Expression of selenium-dependent glutathione peroxidase in human breast tumor cell lines. Cancer Res 55: 957–962, 1995Google Scholar
  176. 176.
    Townsend AJ, Morrow CS, Sinha BK, Cowan KH: Selenium-dependent glutathione peroxidase expression is inversely related to estrogen receptor content of human breast cancer cells. Cancer Commun 3: 265–270, 1991Google Scholar
  177. 177.
    Moscow JA, Townsend AJ, Goldsmith ME, Whang-Peng J, Vickers PJ, Poisson R, Legault-Poisson S, Myers CE, Cowan KH: Isolation of the human anionic glutathione S-transferase cDNA and the relation of its gene expression to estrogen-receptor content in primary breast cancer. Proc Natl Acad Sci USA 85: 6518–6522, 1988Google Scholar
  178. 178.
    Liu WM, Guerra-Vladusic FK, Kurakata S, Lupu R, Kohwi-Shigematsu T: HMG-I(Y) recognizes base-unpairing regions of matrix attachment sequences and its increased expression is directly linked to metastatic breast cancer phenotype. Cancer Res 59: 5695–5703, 1999Google Scholar
  179. 179.
    Dandachi N, Hauser-Kronberger C, More E, Wiesener B, Hacker GW, Dietze O, Wirl G: Co-expression of tenascin-C and vimentin in human breast cancer cells indicates phenotypic transdifferentiation during tumour progression: correlation with histopathological parameters, hormone receptors, and oncoproteins. J Pathol 193: 181–189, 2001Google Scholar
  180. 180.
    Lacroix M, Siwek B, Marie PJ, Body JJ: Production and regulation of interleukin-11 by breast cancer cells. Cancer Lett 127: 29–35, 1998Google Scholar
  181. 181.
    De Larco JE, Wuertz BR, Rosner KA, Erickson SA, Gamache DE, Manivel JC, Furcht LT: A potential role for interleukin-8 in the metastatic phenotype of breast carcinoma cells. Am J Pathol 158: 639–646, 2001Google Scholar
  182. 182.
    Kirschmann DA, Seftor EA, Fong SF, Nieva DR, Sullivan CM, Edwards EM, Sommer P, Csiszar K, Hendrix MJ: A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res 62: 4478–4483, 2002Google Scholar
  183. 183.
    Beviglia L, Matsumoto K, Lin CS, Ziober BL, Kramer RH: Expression of the c-Met/HGF receptor in human breast carcinoma: correlation with tumor progression. Int J Cancer 74: 301–309, 1997Google Scholar
  184. 184.
    Pulyaeva H, Bueno J, Polette M, Birembaut P, Sato H, Seiki M, Thompson EW: MT1-MMP correlates with MMP-2 activation potential seen after epithelial to mesenchymal transition in human breast carcinoma cells. Clin Exp Metastasis 15: 111–120, 1997Google Scholar
  185. 185.
    Gilles C, Polette M, Seiki M, Birembaut P, Thompson EW: Implication of collagen type I-induced membrane-type 1-matrix metalloproteinase expression and matrix metalloproteinase-2 activation in the metastatic progression of breast carcinoma. Lab Invest 76: 651–660, 1997Google Scholar
  186. 186.
    Carmeci C, Thompson DA, Kuang WW, Lightdale N, Furthmayr H, Weigel RJ: Moesin expression is associated with the estrogen receptor-negative breast cancer phenotype. Surgery 124: 211–217, 1998Google Scholar
  187. 187.
    Friedline JA, Garrett SH, Somji S, Todd JH, Sens DA: Differential expression of the MT-1E gene in estrogen-receptor-positive and-negative human breast cancer cell lines. Am J Pathol 152: 23–27, 1998Google Scholar
  188. 188.
    Jin R, Bay BH, Chow VT, Tan PH, Lin VC: Metallothionein 1E mRNA is highly expressed in oestrogen receptor-negative human invasive ductal breast cancer. Br J Cancer 83: 319–323, 2000Google Scholar
  189. 189.
    Tsai MS, Hornby AE, Lakins J, Lupu R: Expression and function of CYR61, an angiogenic factor, in breast cancer cell lines and tumor biopsies. Cancer Res 60: 5603–5607, 2000Google Scholar
  190. 190.
    Look MP, van Putten WL, Duffy MJ, Harbeck N, Christensen IJ, Thomssen C, Kates R, Spyratos F, Ferno M, Eppenberger-Castori S, Sweep CG, Ulm K, Peyrat JP, Martin PM, Magdelenat H, Brunner N, Duggan C, Lisboa BW, Bendahl PO, Quillien V, Daver A, Ricolleau G, Meijer-van Gelder ME, Manders P, Fiets WE, Blankenstein MA, Broet P, Romain S, Daxenbichler G, Windbichler G, Cufer T, Borstnar S, Kueng W, Beex LV, Klijn JG, O'Higgins N, Eppenberger U, Janicke F, Schmitt M, Foekens JA: Pooled analysis of prognostic impact of urokinase-type plasminogen activator and its inhibitor PAI-1 in 8377 breast cancer patients. J Natl Cancer Inst 94: 116–128, 2002Google Scholar
  191. 191.
    Tetu B, Brisson J, Wang CS, Lapointe H, Beaudry G, Blanchette C: Expression of cathepsin D, stromelysin-3, and urokinase by reactive stromal cells on breast carcinoma prognosis. Cancer 92: 2957–2964, 2001Google Scholar
  192. 192.
    Grøndahl-Hansen J, Christensen IJ, Rosenquist C, Brunner N, Mouridsen HT, Dano K, Blichert-Toft M: High levels of urokinase-type plasminogen activator and its inhibitor PAI-1 in cytosolic extracts of breast carcinomas are associated with poor prognosis. Cancer Res 53: 2513–2521, 1993Google Scholar
  193. 193.
    Riegel AT, Wellstein A: The potential role of the heparin-binding growth factor pleiotrophin in breast cancer. Breast Cancer Res Treat 31: 309–314, 1994Google Scholar
  194. 194.
    Widschwendter M, Berger J, Hermann M, Muller HM, Amberger A, Zeschnigk M, Widschwendter A, Abendstein B, Zeimet AG, Daxenbichler G, Marth C: Methylation and silencing of the retinoic acid receptor-beta2 gene in breast cancer. J Natl Cancer Inst 92: 826–832, 2000Google Scholar
  195. 195.
    Pedrocchi M, Schafer BW, Mueller H, Eppenberger U, Heizmann CW: Expression of Ca(2+)-binding proteins of the S100 family in malignant human breast-cancer cell lines and biopsy samples. Int J Cancer 57: 684–690, 1994Google Scholar
  196. 196.
    Sherbet GV, Lakshmi MS: S100A4 (MTS1) calcium binding protein in cancer growth, invasion and metastasis. Anticancer Res 18: 2415–2421, 1998Google Scholar
  197. 197.
    Blanco MJ, Moreno-Bueno G, Sarrio D, Locascio A, Cano A, Palacios J, Nieto MA: Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 21: 3241–3246, 2002Google Scholar
  198. 198.
    Hajra KM, Chen DYS, Fearon ER: The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 62: 1613–1618, 2002Google Scholar
  199. 199.
    Curmi PA, Nogues C, Lachkar S, Carelle N, Gonthier MP, Sobel A, Lidereau R, Bieche I: Overexpression of stathmin in breast carcinomas points out to highly proliferative tumours. Br J Cancer 82: 142–150, 2000Google Scholar
  200. 200.
    Yoshiji H, Harris SR, Raso E, Gomez DE, Lindsay CK, Shibuya M, Sinha CC, Thorgeirsson UP: Mammary carcinoma cells over-expressing tissue inhibitor of metalloproteinases-1 show enhanced vascular endothelial growth factor expression. Int J Cancer 75: 81–87, 1998Google Scholar
  201. 201.
    McCarthy K, Maguire T, McGreal G, McDermott E, O'Higgins N, Duffy MJ: High levels of tissue inhibitor of metalloproteinase-1 predict poor outcome in patients with breast cancer. Int J Cancer 84: 44–48, 1999Google Scholar
  202. 202.
    Remacle A, McCarthy K, Noel A, Maguire T, McDermott E, O'Higgins N, Foidart JM, Duffy MJ: High levels of TIMP-2 correlate with adverse prognosis in breast cancer. Int J Cancer 89: 118–121, 2000Google Scholar
  203. 203.
    Bundy LM, Sealy L: CCAAT/enhancer binding protein beta (C/EBPbeta)-2 transforms normal mammary epithelial cells and induces epithelial to mesenchymal transition in culture. Oncogene 22: 869–883, 2003Google Scholar
  204. 204.
    Reeves R, Edberg DD, Li Y: Architectural transcription factor HMGI(Y) promotes tumor progression and mesenchymal transition of human epithelial cells. Mol Cell Biol 21: 575–594, 2001Google Scholar
  205. 205.
    Lin CQ, Singh J, Murata K, Itahana Y, Parrinello S, Liang SH, Gillett CE, Campisi J, Desprez PY: A role for Id-1 in the aggressive phenotype and steroid hormone response of human breast cancer cells. Cancer Res 60: 1332–1340, 2000Google Scholar
  206. 206.
    Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, Wade PA: MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113: 207–219, 2003Google Scholar
  207. 207.
    Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A: The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2: 84–89, 2000Google Scholar
  208. 208.
    Castles CG, Klotz DM, Fuqua SA, Hill SM: Coexpression of wild-type and variant oestrogen receptor mRNAs in a panel of human breast cancer cell lines. Br J Cancer 71: 974–980, 1995Google Scholar
  209. 209.
    van Agthoven T, Timmermans M, Foekens JA, Dorssers LC, Henzen-Logmans SC: Differential expression of estrogen, progesterone, and epidermal growth factor receptors in normal, benign, and malignant human breast tissues using dual staining immunohistochemistry. Am J Pathol 144: 1238–1246, 1994Google Scholar
  210. 210.
    Elston CW, Ellis IO: Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Elston CW, Ellis IO (eds), Histopathology 19: 403–410, 1991, Histopathology 41: 151, 2002Google Scholar
  211. 211.
    Polyak K: On the birth of breast cancer. Biochim Biophys Acta 1552: 1–13, 2001Google Scholar
  212. 212.
    Cserni G: Tumour histological grade may progress between primary and recurrent invasive mammary carcinoma. J Clin Pathol 55: 293–297, 2002Google Scholar
  213. 213.
    Warnberg F, Nordgren H, Bergkvist L, Holmberg L: Tumour markers in breast carcinoma correlate with grade rather than with invasiveness. Br J Cancer 85: 869–874, 2001Google Scholar
  214. 214.
    Iglehart JD, Kerns BJ, Huper G, Marks JR: Maintenance of DNA content and erbB-2 alterations in intraductal and invasive phases of mammary cancer. Breast Cancer Res Treat 34: 253–263, 1995Google Scholar
  215. 215.
    Millis RR, Barnes DM, Lampejo OT, Egan MK, Smith P: Tumour grade does not change between primary and recurrent mammary carcinoma. Eur J Cancer 34: 548–553, 1998Google Scholar
  216. 216.
    Moriya T, Silverberg SG: Intraductal carcinoma (ductal carcinoma in situ) of the breast. A comparison of pure noninvasive tumors with those including different proportions of infiltrating carcinoma. Cancer 74: 2972–2978, 1994Google Scholar
  217. 217.
    Lampejo OT, Barnes DM, Smith P, Millis RR: Evaluation of infiltrating ductal carcinomas with a DCIS component: correlation of the histologic type of the in situ component with grade of the infiltrating component. Semin Diag Pathol 11: 215–222, 1994Google Scholar
  218. 218.
    Douglas-Jones AG, Gupta SK, Attanoos RL, Morgan JM, Mansel RE: A critical appraisal of six modern classifications of ductal carcinoma in situ of the breast (DCIS): correlation with grade of associated invasive carcinoma. Histopathology 29: 397–409, 1996Google Scholar
  219. 219.
    Su L, Morgan PR, Lane EB: Expression of cytokeratin messenger RNA versus protein in the normal mammary gland and in breat cancer. Hum Pathol 27: 800–806, 1996Google Scholar
  220. 220.
    Briffod M, Hacene K, Le Doussal V: Immunohistochemistry on cell blocks from fine-needle cytopunctures of primary breast carcinomas and lymph node metastases. Mod Pathol 13: 841–850, 2000Google Scholar
  221. 221.
    Nedergaard L, Haerslev T, Jacobsen GK: Immunohistochemical study of estrogen receptors in primary breast carcinomas and their lymph node metastases including comparison of two monoclonal antibodies. APMIS 103: 20–24, 1995Google Scholar
  222. 222.
    Kayser K, Biechele U, Kayser G, Dienemann H, Andre S, Bovin NV, Gabius HJ: Pulmonary metastases of breast carcinomas: ligandohistochemical, nuclear, and structural analysis of primary and metastatic tumors with emphasis on period of occurrence of metastases and survival. J Surg Oncol 69: 137–146, 1998Google Scholar
  223. 223.
    Shimizu C, Fukutomi T, Tsuda H, Akashi-Tanaka S, Watanabe T, Nanasawa T, Sugihara K: c-erbB-2 protein overexpression and p53 immunoreaction in primary and recurrent breast cancer tissues. J Surg Oncol 73: 17–20, 2000Google Scholar
  224. 224.
    Barnes DM, Lammie GA, Millis RR, Gullick WL, Allen DS, Altman DG: An immunohistochemical evaluation of c-erbB-2 expression in human breast carcinoma. Br J Cancer 58: 448–452, 1988Google Scholar
  225. 225.
    van Agthoven T, Timmermans M, Dorssers LC, Henzen-Logmans SC: Expression of estrogen, progesterone and epidermal growth factor receptors in primary and metastatic breast cancer. Int J Cancer 63: 790–793, 1995Google Scholar
  226. 226.
    Bijker N, Peterse JL, Duchateau L, Robanus-Maandag EC, Bosch CA, Duval C, Pilotti S, van de Vijver MJ: Histological type and marker expression of the primary tumour compared with its local recurrence after breast-conserving therapy for ductal carcinoma in situ. Br J Cancer 84: 539–544, 2001Google Scholar
  227. 227.
    Horiguchi J, Iino Y, Takei H, Maemura M, Koibuchi Y, Takeyoshi I, Ohwada S, Yokoe T, Nakajima T, Oyama T, Morishita Y: Immunohistochemical study on primary and recurrent tumors in patients with local recurrence in the conserved breast. Oncol Rep 7: 295–298, 2000Google Scholar
  228. 228.
    Jojovic M, Adam E, Zangemeister-Wittke U, Schumacher U: Epithelial glycoprotein-2 expression is subject to regulatory processes in epithelial-mesenchymal transitions during metastases: an investigation of human cancers transplanted into severe combined immunodeficient mice. Histochem J 30: 723–729, 1998Google Scholar
  229. 229.
    Rennstam K, Baldetorp B, Kytola S, Tanner M, Isola J: Chromosomal rearrangements and oncogene amplification precede aneuploidization in the genetic evolution of breast cancer. Cancer Res 61: 1214–1219, 2001Google Scholar
  230. 230.
    Wenger CR, Beardslee S, Owens MA, Pounds G, Oldaker T, Vendely P, Pandian MR, Harrington D, Clark GM, McGuire WL: DNA ploidy, S-phase, and steroid receptors in more than 127,000 breast cancer patients. Breast Cancer Res Treat 28: 9–20, 1993Google Scholar
  231. 231.
    Teixeira MR, Pandis N, Heim S: Cytogenetic clues to breast carcinogenesis. Genes Chromosomes Cancer 33: 1–16, 2002Google Scholar
  232. 232.
    Pandis N, Idvall I, Bardi G, Jin Y, Gorunova L, Mertens F, Olsson H, Ingvar C, Beroukas K, Mitelman F, Heim S: Correlation between karyotypic pattern and clincopathologic features in 125 breast cancer cases. Int J Cancer 66: 191–196, 1996Google Scholar
  233. 233.
    Dellas A, Torhorst J, Schultheiss E, Mihatsch MJ, Moch H: DNA sequence losses on chromosomes 11p and 18q are associated with clinical outcome in lymph node-negative ductal breast cancer. Clin Cancer Res 8: 1210–1216, 2002Google Scholar
  234. 234.
    Zudaire I, Odero MD, Caballero C, Valenti C, Martinez-Penuela JM, Isola J, Calasanz MJ: Genomic imbalances detected by comparative genomic hybridization are prognostic markers in invasive ductal breast carcinomas. Histopathology 40: 547–555, 2002Google Scholar
  235. 235.
    Schwendel A, Richard F, Langreck H, Kaufmann O, Lage H, Winzer KJ, Petersen I, Dietel M: Chromosome alterations in breast carcinomas: frequent involvement of DNA losses including chromosomes 4q and 21q. Br J Cancer 78: 806–811, 1998Google Scholar
  236. 236.
    Roylance R, Gorman P, Harris W, Liebmann R, Barnes D, Hanby A, Sheer D: Comparative genomic hybridization of breast tumors stratified by histological grade reveals new insights into the biological progression of breast cancer. Cancer Res 59: 1433–1436, 1999Google Scholar
  237. 237.
    Adeyinka A, Mertens F, Idvall I, Bondeson L, Ingvar C, Mitelman F, Pandis N: Different patterns of chromosomal imbalances in metastasising and non-metastasising primary breast carcinomas. Int J Cancer 84: 370–375, 1999Google Scholar
  238. 238.
    Ried T, Just KE, Holtgreve-Grez H, du Manoir S, Speicher MR, Schrock E, Latham C, Blegen H, Zetterberg A, Cremer T, Auer G: Comparative genomic hybridization of formalin-fixed, paraffin-embedded breast tumors reveals different patterns of chromosomal gains and losses in fibroadenomas and diploid and aneuploid carcinomas. Cancer Res 55: 5415–5423, 1995Google Scholar
  239. 239.
    Forozan F, Mahlamaki EH, Monni O, Chen Y, Veldman R, Jiang Y, Gooden GC, Ethier SP, Kallioniemi A, Kallioniemi OP: Comparative genomic hybridization analysis of 38 breast cancer cell lines: a basis for interpreting complementary DNA microarray data. Cancer Res 60: 4519–4525, 2000Google Scholar
  240. 240.
    Larramendy ML, Lushnikova T, Bjorkqvist AM, Wistuba II, Virmani AK, Shivapurkar N, Gazdar AF, Knuutila S: Comparative genomic hybridization reveals complex genetic changes in primary breast cancer tumors and their cell lines. Cancer Genet Cytogenet 119: 132–138, 2000Google Scholar
  241. 241.
    Tirkkonen M, Tanner M, Karhu R, Kallioniemi A, Isola J, Kallioniemi OP: Molecular cytogenetics of primary breast cancer by CGH. Genes Chromosomes Cancer 21: 177–184, 1998Google Scholar
  242. 242.
    Loveday RL, Greenman J, Simcox DL, Speirs V, Drew PJ, Monson JR, Kerin MJ: Genetic changes in breast cancer detected by comparative genomic hybridisation. Int J Cancer 86: 494–500, 2000Google Scholar
  243. 243.
    Roylance R, Gorman P, Hanby A, Tomlinson I: Allelic imbalance analysis of chromosome 16q shows that grade I and grade III invasive ductal breast cancers follow different genetic pathways. J Pathol 196: 32–36, 2002Google Scholar
  244. 244.
    Richard F, Pacyna-Gengelbach M, Schlüns K, Fleige B, Winzer KJ, Szymas J, Dietel M, Petersen I, Schwendel A: Patterns of chromosomal imbalances in invasive breast cancer. Int J Cancer 89: 305–310, 2000Google Scholar
  245. 245.
    Glockner S, Lehmann U, Wilke N, Kleeberger W, Langer F, Kreipe H: Amplification of growth regulatory genes in intraductal breast cancer is associated with higher nuclear grade but not with the progression to invasiveness. Lab Invest 81: 565–571, 2001Google Scholar
  246. 246.
    Buerger H, Simon R, Schafer KL, Diallo R, Littmann R, Poremba C, van Diest PJ, Dockhorn-Dworniczak B, Bocker W: Genetic relation of lobular carcinoma in situ, ductal carcinoma in situ, and associated invasive carcinoma of the breast. Mol Pathol 53: 118–121, 2000Google Scholar
  247. 247.
    Anbazhagan R, Fujii H, Gabrielson E: Microsatellite instability is uncommon in breast cancer. Clin Cancer Res 5: 839–844, 1999Google Scholar
  248. 248.
    Teng DH, Hu R, Lin H, Davis T, Iliev D, Frye C, Swedlund B, Hansen KL, Vinson VL, Gumpper KL, Ellis L, El-Naggar A, Frazier M, Jasser S, Langford LA, Lee J, Mills GB, Pershouse MA, Pollack RE, Tornos C, Troncoso P, Yung WK, Fujii G, Berson A, Steck PA: MMAC1/PTEN mutations in primary tumor specimens and tumor cell lines. Cancer Res 57: 5221–5225, 1997Google Scholar
  249. 249.
    Achuthan R, Bell SM, Roberts P, Leek JP, Horgan K, Markham AF, MacLennan KA, Speirs V: Genetic events during the transformation of a tamoxifen-sensitive human breast cancer cell line into a drug-resistant clone. Cancer Genet Cytogenet 130: 166–172, 2001Google Scholar
  250. 250.
    Aubele M, Mattis A, Zitzelsberger H, Walch A, Kremer M, Hutzler P, Hofler H, Werner M: Intratumoral heterogeneity in breast carcinoma revealed by laser-microdissection and comparative genomic hybridization. Cancer Genet Cytogenet 110: 94–102, 1999Google Scholar
  251. 251.
    Hampl M, Hampl JA, Schwarz P, Frank S, Hahn M, Schackert G, Saeger HD, Schackert HK: Accumulation of genetic alterations in brain metastases of sporadic breast carcinomas is associated with reduced survival after metastasis. Invasion Metastasis 18: 81–95, 1998-1999Google Scholar
  252. 252.
    Lacroix M, Zammatteo N, Remacle J, Leclercq G: A low-density DNA microarray for analysis of markers in breast cancer. Int J Biol Markers 17: 5–23, 2002Google Scholar
  253. 253.
    Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO, Botstein D: Molecular portraits of human breast tumours. Nature 406: 747–752, 2000Google Scholar
  254. 254.
    Ross DT, Scherf U, Eisen MB, Perou CM, Rees C, Spellman P, Iyer V, Jeffrey SS, Van de Rijn M, Waltham M, Pergamenschikov A, Lee JC, Lashkari D, Shalon D, Myers TG, Weinstein JN, Botstein D, Brown PO: Systematic variation in gene expression patterns in human cancer cell lines. Nat Genet 24: 227–235, 2000Google Scholar
  255. 255.
    Lønning PE, Sørlie T, Perou CM, Brown PO, Botstein D, Borresen-Dale AL: Microarrays in primary breast cancer-lessons from chemotherapy studies. Endocr Relat Cancer 8: 259–263, 2001Google Scholar
  256. 256.
    Gruvberger S, Ringner M, Chen Y, Panavally S, Saal LH, Borg A, Ferno M, Peterson C, Meltzer PS: Estrogen receptor status in breast cancer is associated with remarkably distinct gene expression patterns. Cancer Res 61: 5979–5988, 2001Google Scholar
  257. 257.
    Ross DT, Perou CM: A comparison of gene expression signatures from breast tumors and breast tissue derived cell lines. Dis Markers 17: 99–109, 2001Google Scholar
  258. 258.
    Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van De Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Lønning PE, Borresen-Dale AL: Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 98: 10869–10874, 2001Google Scholar
  259. 259.
    Zajchowski DA, Bartholdi MF, Gong Y, Webster L, Liu HL, Munishkin A, Beauheim C, Harvey S, Ethier SP, Johnson PH: Identification of gene expression profiles that predict the aggressive behavior of breast cancer cells. Cancer Res 61: 5168–5178, 2001Google Scholar
  260. 260.
    van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH: Gene expression profiling predicts clinical outcome of breast cancer. Nature 415: 530–536, 2002Google Scholar
  261. 261.
    Sotiriou C, Neo SY, McShane LM, Korn EL, Long PM, Jazaeri A, Martiat P, Fox SB, Harris AL, Liu ET: Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci USA 100: 10393–10398, 2003Google Scholar
  262. 262.
    Jones C, Nonni AV, Fulford L, Merrett S, Chaggar R, Eusebi V, Lakhani SR: CGH analysis of ductal carcinoma of the breast with basaloid/myoepithelial cell differentiation. Br J Cancer 85: 422–427, 2001Google Scholar
  263. 263.
    Tsuda H, Takarabe T, Hasegawa T, Murata T, Hirohashi S: Myoepithelial differentiation in high-grade invasive ductal carcinomas with large central acellular zones. Hum Pathol 30: 1134–1139, 1999Google Scholar
  264. 264.
    Armes JE, Trute L, White D, Southey MC, Hammet F, Tesoriero A, Hutchins AM, Dite GS, McCredie MR, Giles GG, Hopper JL, Venter DJ: Distinct molecular pathogeneses of early-onset breast cancers in BRCA1 and BRCA2 mutation carriers: a population-based study. Cancer Res 59: 2011–2017, 1999Google Scholar
  265. 265.
    Grushko TA, Blackwood MA, Schumm PL, Hagos FG, Adeyanju MO, Feldman MD, Sanders MO, Weber BL, Olopade OI: Molecular-cytogenetic analysis of Her-2/neu gene in BRCA1-associated breast cancers. Cancer Res 62: 1481–1488, 2002Google Scholar
  266. 266.
    Price JE, Zhang RD: Studies of human breast cancer metastasis using nude mice. Cancer Metastasis Rev 8: 285–297, 1990Google Scholar
  267. 267.
    Ellison G, Klinowska T, Westwood RF, Docter E, French T, Fox JC: Further evidence to support the melanocytic origin of MDA-MB-435. Mol Pathol 55: 294–299, 2002Google Scholar
  268. 268.
    Malik K, Brown KW: Epigenetic gene deregulation in cancer. Br J Cancer 83: 1583–1588, 2000Google Scholar
  269. 269.
    Bird A: DNA methylation patterns and epigenetic memory. Genes Dev 16: 6–21, 2002Google Scholar
  270. 270.
    Widschwendter M, Jones PA: DNA methylation and breast carcinogenesis. Oncogene 21: 5462–5482, 2002Google Scholar
  271. 271.
    Yan PS, Chen CM, Shi H, Rahmatpanah F, Wei SH, Caldwell CW, Huang TH: Dissecting complex epigenetic alterations in breast cancer using CpG island microarrays. Cancer Res 61: 8375–8380, 2001Google Scholar
  272. 272.
    Elenbaas B, Weinberg RA: Heterotypic signaling between epithelial tumor cells and fibroblasts in carcinoma formation. Exp Cell Res 264: 169–184, 2001Google Scholar
  273. 273.
    Toillon RA, Chopin V, Jouy N, Fauquette W, Boilly B, Le Bourhis X: Normal breast epithelial cells induce p53-dependent apoptosis and p53-independent cell cycle arrest of breast cancer cells. Breast Cancer Res Treat 71: 269–280, 2002Google Scholar
  274. 274.
    Ben-Hur H, Cohen O, Schneider D, Gurevich P, Halperin R, Bala U, Mozes M, Zusman I: The role of lymphocytes and macrophages in human breast tumorigenesis: an immunohistochemical and morphometric study. Anticancer Res 22: 1231–1238, 2002Google Scholar
  275. 275.
    Moore MA: The role of chemoattraction in cancer metastases. Bioessays 23: 674–676, 2001Google Scholar
  276. 276.
    Yoneda T: Cellular and molecular basis of preferential metastasis of breast cancer to bone. J Orthop Sci 5: 75–81, 2000Google Scholar
  277. 277.
    Sierra A, Price JE, Garcia-Ramirez M, Mendez O, Lopez L, Fabra A: Astrocyte-derived cytokines contribute to the metastatic brain specificity of breast cancer cells. Lab Invest 77: 357–368, 1997Google Scholar
  278. 278.
    Lacroix M, Siwek B, Body JJ: Effects of secretory products of breast cancer cells on osteoblast-like cells. Breast Cancer Res Treat 38: 209–216, 1996Google Scholar
  279. 279.
    Deugnier MA, Teuliere J, Faraldo MM, Thiery JP, Glukhova MA: The importance of being a myoepithelial cell. Breast Cancer Res 4: 224–230, 2002Google Scholar
  280. 280.
    Barsky SH: Myoepithelial mRNA expression profiling reveals a common tumor-suppressor phenotype. Exp Mol Pathol 74: 113–122, 2003Google Scholar
  281. 281.
    Sternlicht MD, Barsky SH: Themyoepithelial defense: a host defense against cancer. Med Hypotheses 48: 37–46, 1997Google Scholar
  282. 282.
    Xiao G, Liu YE, Gentz R, Sang QA, Ni J, Goldberg ID, Shi YE: Suppression of breast cancer growth and metastasis by a serpin myoepithelium-derived serine proteinase inhibitor expressed in the mammary myoepithelial cells. Proc Natl Acad Sci USA 96: 3700–3705, 1999Google Scholar
  283. 283.
    Wang CS, Tetu B: Stromelysin-3 expression by mammary tumor-associated fibroblasts under in vitro breast cancer cell induction. Int J Cancer 99: 792–799, 2002Google Scholar
  284. 284.
    Schnack Nielsen B, Rank F, Engelholm LH, Holm A, Dano K, Behrendt N: Urokinase receptor-associated protein (uPARAP) is expressed in connection with malignant as well as benign lesions of the human breast and occurs in specific populations of stromal cells. Int J Cancer 98: 656–664, 2002Google Scholar
  285. 285.
    Heppner KJ, Matrisian LM, Jensen RA, Rodgers WH: Expression of most matrix metalloproteinase family members in breast cancer represents a tumor-induced host response. Am J Pathol 149: 273–282, 1996Google Scholar
  286. 286.
    Dano K, Romer J, Nielsen BS, Bjorn S, Pyke C, Rygaard J, Lund LR: Cancer invasion and tissue remodeling-cooperation of protease systems and cell types. APMIS 107: 120–127, 1999Google Scholar
  287. 287.
    Arnstein P, Taylor DO, Nelson-Rees WA, Huebner RJ, Lennette EH: Propagation of human tumors in antithymocyte serum-treated mice. J Natl Cancer Inst 52: 71–84, 1974Google Scholar
  288. 288.
    Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA: Creation of human tumour cells with defined genetic elements. Nature 400: 464–468, 1999Google Scholar
  289. 289.
    Whitehead RH, Bertoncello I, Webber LM, Pedersen JS: A new human breast carcinoma cell line (PMC42) with stem cell characteristics. I. Morphologic characterization. J Natl Cancer Inst 70: 649–661, 1983Google Scholar
  290. 290.
    Flanagan L, Van Weelden K, Ammerman C, Ethier SP, Welsh J: SUM-159PT cells: a novel estrogen independent human breast cancer model system. Breast Cancer Res Treat 58: 193–204, 1999Google Scholar
  291. 291.
    Blumenthal RD, Waskewich C, Goldenberg DM, Lew W, Flefleh C, Burton J: Chronotherapy and chronotoxicity of the cyclooxygenase-2 inhibitor, celecoxib, in athymic mice bearing human breast cancer xenografts. Clin Cancer Res 7: 3178–3185, 2001Google Scholar
  292. 292.
    Rosol TJ, Tannehill-Gregg SH, LeRoy BE, Mandl S, Contag CH: Animal models of bone metastasis. Cancer 97: 748–757, 2003Google Scholar
  293. 293.
    Leung CKH, Shiu RPC: Required presence of both oestrogen and pituitary factors for the growth of human breast cancer cells in athymic nude mice. Cancer Res 41: 546–551, 1981Google Scholar
  294. 294.
    Shafie SM, Grantham FH: Role of hormones in the growth and regression of human breast cancer cells (MCF-7) transplanted into athymic nude mice. J Natl Cancer Inst 67: 51–56, 1981Google Scholar
  295. 295.
    Osborne CK, Hobbs K, Clark GM: Effect of estrogens and antiestrogens on growth of human breast cancer cells in athymic nude mice. Cancer Res 45: 584–590, 1985Google Scholar
  296. 296.
    Clarke R: Human breast cancer cell line xenografts as models of breast cancer. The immunobiologies of recipient mice and the characteristics of several tumorigenic cell lines. Breast Cancer Res Treat 39: 69–86, 1996Google Scholar
  297. 297.
    Osborne CK, Hobbs K, Trent JM: Biological differences among MCF-7 human breast cancer cell lines from different laboratories. Breast Cancer Res Treat 9: 111–121, 1987Google Scholar
  298. 298.
    Madsen MW, Briand P: Relationship between tumorigenicity, in vitro invasiveness, and plasminogen activator production of human breast cell lines. Eur J Cancer 26: 793–797, 1990Google Scholar
  299. 299.
    van Slooten HJ, Bonsing BA, Hiller AJ, Colbern GT, van Dierendonck JH, Cornelisse CJ, Smith HS: Outgrowth of BT-474 human breast cancer cells in immune-deficient mice: a new in vivo model for hormone-dependent breast cancer. Br J Cancer 72: 22–30, 1995Google Scholar
  300. 300.
    Price J: Metastasis from human breast cancer cell lines. Breast Cancer Res Treat 39: 93–102, 1996Google Scholar
  301. 301.
    Giovanella BC, Vardeman DM, Williams LJ, Taylor DJ, De Ipolyi PD, Greeff PJ, Stehlin JS, Ullrich A, Cailleau R, Slamon DJ, Gary Jr HE: Heterotransplantation of human breast carcinomas in nude mice. Correlation between successful heterotransplants, poor prognosis, and amplification of the Her-2/neu oncogene. Int J Cancer 47: 66–71, 1991Google Scholar
  302. 302.
    Mullen P, Ritchie A, Langdon SP, Miller WR: Effect of Matrigel on the tumorigenicity of human breast and ovarian carcinoma cell lines. Int J Cancer 67: 816–820, 1996Google Scholar
  303. 303.
    Zhang RD, Fidler IJ, Price JE: Relative malignant potential of human breast carcinoma cell lines established from pleural effusions and a brain metastasis. Invasion Metastasis 11: 204–215, 1991Google Scholar
  304. 304.
    Negrini M, Sabbioni S, Possati L, Rattan S, Corallini A, Barbanti-Brodano G, Croce CM: Suppression of tumorigenicity of breast cancer cells by microcell-mediated chromosome transfer: studies on chromosomes 6 and 11. Cancer Res 54: 1331–1336, 1994Google Scholar
  305. 305.
    Negrini M, Sabbioni S, Haldar S, Possati L, Castagnoli A, Corallini A, Barbanti-Brodano G, Croce CM: Tumor and growth suppression of breast cancer cells by chromosome-17 associated functions. Cancer Res 54: 1818–1824, 1994Google Scholar
  306. 306.
    Mbalaviele G, Dunstan CR, Sasaki A, Williams PJ, Mundy GR, Yoneda T: E-cadherin expression in human breast cancer cells suppresses the development of osteolytic bone metastases in an experimental metastasis model. Cancer Res 56: 4063–4070, 1996Google Scholar
  307. 307.
    Butt AJ, Dickson KA, McDougall F, Baxter RC: Insulin-like growth factor-binding protein-5 inhibits the growth of human breast cancer cells in vitro and in vivo. J Biol Chem 278: 29676–29685, 2003Google Scholar
  308. 308.
    Tsai MS, Bogart DF, Castaneda JM, Li P, Lupu R: Cyr61 promotes breast tumorigenesis and cancer progression. Oncogene 21: 8178–8185, 2002Google Scholar
  309. 309.
    Akiri G, Sabo E, Dafni H, Vadasz Z, Kartvelishvily Y, Gan N, Kessler O, Cohen T, Resnick M, Neeman M, Neufeld G: Lysyl oxidase-related protein-1 promotes tumor fibrosis and tumor progression in vivo. Cancer Res 63: 1657–1666, 2003Google Scholar
  310. 310.
    Mattila MM, Ruohola JK, Karpanen T, Jackson DG, Alitalo K, Harkonen PL: VEGF-C induced lymphangiogenesis is associated with lymph node metastasis in orthotopic MCF-7 tumors. Int J Cancer 98: 946–951, 2002Google Scholar
  311. 311.
    Spiridon CI, Ghetie MA, Uhr J, Marches R, Li JL, Shen GL, Vitetta ES: Targeting multiple Her-2 epitopes with monoclonal antibodies results in improved antigrowth activity of a human breast cancer cell line in vitro and in vivo. Clin Cancer Res 8: 1720–1730, 2002Google Scholar
  312. 312.
    Zinda MJ, Johnson MA, Paul JD, Horn C, Konicek BW, Lu ZH, Sandusky G, Thomas JE, Neubauer BL, Lai MT, Graff JR: AKT-1,-2, and-3 are expressed in both normal and tumor tissues of the lung, breast, prostate, and colon. Clin Cancer Res 7: 2475–2479, 2001Google Scholar
  313. 313.
    Faridi J, Wang L, Endemann G, Roth RA: Expression of constitutively active Akt-3 in MCF-7 breast cancer cells reverses the estrogen and tamoxifen responsivity of these cells in vivo. Clin Cancer Res 9: 2933–2939, 2003Google Scholar
  314. 314.
    Garcia M, Derocq D, Freiss G, Rochefort H: Activation of estrogen receptor transfected into a receptor-negative breast cancer cell line decreases the metastatic and invasive potential of the cells. Proc Natl Acad Sci USA 89: 11538–11542, 1992Google Scholar
  315. 315.
    Bendre MS, Gaddy-Kurten D, Mon-Foote T, Akel NS, Skinner RA, Nicholas RW, Suva LJ: Expression of interleukin 8 and not parathyroid hormone-related protein by human breast cancer cells correlates with bone metastasis in vivo. Cancer Res 62: 5571–5579, 2002Google Scholar
  316. 316.
    Shimo T, Nakanishi T, Nishida T, Asano M, Sasaki A, Kanyama M, Kuboki T, Matsumura T, Takigawa M: Involvement of CTGF, a hypertrophic chondrocyte-specific gene product, in tumor angiogenesis. Oncology 61: 315–322, 2001Google Scholar
  317. 317.
    Sotiriou C, Lacroix M, Lespagnard L, Larsimont D, Paesmans M, Body JJ: Interleukins-6 and-11 expression in primary breast cancer and subsequent development of bone metastases. Cancer Lett 169: 87–95, 2001Google Scholar
  318. 318.
    Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J: A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3: 537–549, 2003Google Scholar
  319. 319.
    Coleman RE, Smith P, Rubens RD: Clinical course and prognostic factors following bone recurrence from breast cancer. Br J Cancer 77: 336–340, 1998Google Scholar
  320. 320.
    Hess KR, Pusztai L, Buzdar AU, Hortobagyi GN: Estrogen receptors and distinct patterns of breast cancer relapse. Breast Cancer Res Treat 78: 105–118, 2003Google Scholar
  321. 321.
    Kamby C, Andersen J, Ejlertsen B, Birkler NE, Rytter L, Zedeler K, Thorpe SM, Norgaard T, Rose C: Histological grade and steroid receptor content of primary breast cancer impact on prognosis and possible modes of action. Br J Cancer 58: 480–486, 1988Google Scholar
  322. 322.
    Guise TA, Yin JJ, Mohammad KS: Role of endothelin-1 in osteoblastic bone metastases. Cancer 97: 779–784, 2003Google Scholar
  323. 323.
    Yoneda T, Michigami T, Yi B, Williams PJ, Niewolna M, Hiraga T: Actions of bisphosphonate on bone metastasis in animal models of breast carcinoma. Cancer 88: 2979–2988, 2000Google Scholar
  324. 324.
    Morony S, Capparelli C, Sarosi I, Lacey DL, Dunstan CR, Kostenuik PJ: Osteoprotegerin inhibits osteolysis and decreases skeletal tumor burden in syngeneic and nude mouse models of experimental bone metastasis. Cancer Res 61: 4432–4436, 2001Google Scholar
  325. 325.
    Yang M, Baranov E, Li XM, Wang JW, Jiang P, Li L, Moossa AR, Penman S, Hoffman RM: Whole-body and intravital optical imaging of angiogenesis in orthotopically implanted tumors. Proc Natl Acad Sci USA 98: 2616–2621, 2001Google Scholar
  326. 326.
    Hoffman RM: Visualization of GFP-expressing tumors and metastasis in vivo. Biotechniques 30: 1016–1022 & 1024-1026, 2001Google Scholar
  327. 327.
    Harms JE, Welch DR: MDA-MB-435 human breast carcinoma metastasis to bone. Clin Exp Metastasis 20: 327–334, 2003Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Marc Lacroix
    • 1
  • Guy Leclercq
    • 1
  1. 1.Laboratoire Jean-Claude Heuson de Cancérologie Mammaire, Institut Jules BordetUniversité Libre de BruxellesBruxellesBelgium

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