Advertisement

Cell motility and breast cancer metastasis

  • Marc E. Bracke
  • Daan De Maeseneer
  • Veerle Van Marck
  • Lara Derycke
  • Barbara Vanhoecke
  • Olivier De Wever
  • Herman T. Depypere
Part of the Cancer Metastasis – Biology and Treatment book series (CMBT, volume 11)

Abstract

Motility and invasion of breast cancer cells are the result of the concerted action of a number of cell activities: directional migration underpinned by the dynamic organisation of cytoskeletal components (actin micro-filaments and microtubules), establishment and disruption of cell-matrix and homotypic/heterotypic cell-cell adhesions, and extracellular proteolysis. Metastasis formation is not only related to cancer cell motility, but also necessitates the collaboration of other, coined “host” cells. Newly discovered ligand-receptor interactions between cancer cells and these host elements offer a molecular explanation for Paget’s “seed and soil” hypothesis, and indicate new targets for possible anti-metastatic therapeutic agents

Keywords

motility metastasis breast cancer actin microtubles cytoskeleton extracellular matrix collagen laminin hyaluronate cadherin CXCL12/CXCR4 interaction integrin CD44 proteinases 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Billington WD, Weir BJ. Deportation of trophoblast in the chinchilla. J Reprod Fertil. 1967; 13: 593-595PubMedCrossRefGoogle Scholar
  2. 2.
    Insall RH, G. E. Jones GE. Moving matters: signals and mechanisms in directed cell migration. Nat Cell Biol. 2006; 8: 776-779PubMedCrossRefGoogle Scholar
  3. 3.
    Liotta LA. Tumor invasion and metastases - Role of the extracellular matrix: Rhoads Memorial Award Lecture., Cancer Res. 1986; 46: 1-7PubMedCrossRefGoogle Scholar
  4. 4.
    Paget P. The distribution of secondary growths in cancer of the breast. Lancet 1889; 1: 571-573CrossRefGoogle Scholar
  5. 5.
    Winston JS, Asch HL, Zhang P, Edge SB, Hyland A, Asch BB. Downregulation of gelsolin correlates with the progression to breast carcinoma. Breast Cancer Res. Treat. 2001; 65: 11-21Google Scholar
  6. 6.
    De Corte V, Bruyneel E, Boucherie C, Mareel C, Vandekerckhove J, Gettemans J. Gelsolin-induced epithelial cell invasion is dependent on Ras-Rac signalling. EMBO J. 2002; 21: 6781-6790PubMedCrossRefGoogle Scholar
  7. 7.
    Hu W, McCrea PD, Deavers M, Kavanagh JJ, Kudelka AP, Verschraegen CF. Increased expression of fascin, motility associated protein, in cell cultures derived from ovarian cancer and in borderline and carcinomatous ovarian tumors, Clin Exp Metastasis 2000; 18: 83-88PubMedCrossRefGoogle Scholar
  8. 8.
    Yoder BJ, Tso E, Skacel M, Pettay J, Tarr S, Budd S, Tubbs RR, Adams JC, Hicks DG. The expression of fascin, an actin-bundling motility protein, correlates with hormone receptor-negative breast cancer and a more aggressive clinical course. Clin Cancer Res. 2005; 11: 186-192PubMedGoogle Scholar
  9. 9.
    Lin YH, Park ZY, Lin D, Brahmbhatt AA, Rio MC, Yates JR 3rd, Klemke RL. Regulation of cell migration and survival by focal adhesion targeting of Lasp-1, J Cell Biol. 2004; 165: 421-432PubMedCrossRefGoogle Scholar
  10. 10.
    Van Impe K, De Corte V, Eichinger L, Bruyneel E, Mareel M, Vandekerckhove J, Gettemans J. The nucleo-cytoplasmic actin binding protein CapG lacks a nuclear export sequence present in structurally related proteins, J Biol Chem. 2003; 278: 17945-17952PubMedCrossRefGoogle Scholar
  11. 11.
    Betapudi V, Licate LS, Egelhoff TT. Distinct roles of nonmuscle myosin II isoforms in the regulation of MDA-MB-231 breast cancer cell spreading and migration, Cancer Res. 2006; 66: 4725-4733PubMedCrossRefGoogle Scholar
  12. 12.
    Jenkinson SR, Barraclough R, West CR, Rudland PS. S100A4 regulates cell motility and invasion in an in vitro model for breast cancer metastasis. Br J Cancer 2004; 90: 253-262PubMedCrossRefGoogle Scholar
  13. 13.
    Wang G, Zhang S, Fernig DG, Martin-Fernandez M, Rudland PS, Barraclough R. Mutually antagonistic actions of S100A4 and S100A1 on normal and metastatic phenotypes, Oncogene 2005; 24: 1445-1454PubMedCrossRefGoogle Scholar
  14. 14.
    Zhang S, Wang G, Liu D, Bao Z, Fernig DG, Rudland PS, Barraclough R. The C-terminal region of S100A4 is important for its metastasis-inducing properties. Oncogene 2005; 24: 4401-4411PubMedCrossRefGoogle Scholar
  15. 15.
    Mareel MMK, De Brabander MJ. Effect of microtubule inhibitors on malignant invasion in vitro. J Natl Cancer Inst. 1978; 61: 787-792PubMedGoogle Scholar
  16. 16.
    Atassi G, Dumont P, Vandendris M. Investigation of the in vivo anti-invasive and anti-metastatic effect of desacetyl vinblastine amide sulphate or vindesine, Invasion Metastasis 1982; 2: 217-231PubMedGoogle Scholar
  17. 17.
    Hall A. Ras-related GTPases and the cytoskeleton. Mol Biol Cell. 1992; 3: 475-479PubMedGoogle Scholar
  18. 18.
    Minard ME, Kim LS, Price JE, Gallick GE. The role of the guanine nucleotide exchange factor Tiam1 in cellular migration, invasion, adhesion and tumor progression. Breast Cancer Res Treat. 2004; 84: 21-32PubMedCrossRefGoogle Scholar
  19. 19.
    Goodison S, Yuan J, Sloan D, Kim R, Li C, Popescu N C, Urquidi V. The RhoGAP protein D LC-1 functions as a metastasis suppressor in breast cancer cells. Cancer Res. 2005; 65: 6042-6053PubMedCrossRefGoogle Scholar
  20. 20.
    Chan AY, Coniglio SJ, Chuang YY, Michaelson D, Knaus UG, Philips M R, Symons M. Roles of the Rac1 and Rac3 GTPases in human tumor cell invasion. Oncogene 2005; 24: 7821-7829PubMedCrossRefGoogle Scholar
  21. 21.
    Baugher PJ, Krishnamoorthy L, Price JE, Dharmawardhane SF. Rac1 and Rac3 isoform activation is involved in the invasive and metastatic phenotype of human breast cancer cells. Breast Cancer Res. 2005; 7: R965-R974PubMedCrossRefGoogle Scholar
  22. 22.
    Kleer CG, van Golen KL, Zhang Y, Wu ZF, Rubin MA, Merajver SD. Characteri- zation of RhoC expression in benign and malignant breast disease: a potential new marker for small breast carcinomas with metastatic ability. Am J Pathol. 2002; 160: 579-584PubMedGoogle Scholar
  23. 23.
    Jiang WG, Watkins G, Lane J, Cunnick GH, Douglas-Jones A, Mokbel K, Mansel RE. Prognostic value of rho GTPases and rho guanine nucleotide disso- ciation inhibitors in human breast cancers. Clin Cancer Res. 2003; 9: 6432-6440PubMedGoogle Scholar
  24. 24.
    Hordijk PL, ten Klooster JP, van der Kammen RA, Michiels F, Oomen LCJM, Collard JG. Inhibition of invasion of epithelial cells by Tiam1-Rac signalling. Science 1997; 278: 1464-1466PubMedCrossRefGoogle Scholar
  25. 25.
    Wang F, Reierstad S, Fishman DA. Matrilysin over-expression in MCF-7 cells enhances cellular invasiveness and pro-gelatinase activation. Cancer Lett. 2006; 236: 292-301PubMedCrossRefGoogle Scholar
  26. 26.
    Rolli M, Fransvea E, Pilch J, Saven A, Felding-Habermann B. Activated integrin alphavbeta3 cooperates with metalloproteinase MMP-9 in regulating migration of metastatic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 9482-9487PubMedCrossRefGoogle Scholar
  27. 27.
    Wang FM, Liu HQ, Liu SR, Tang SP, Yang L, Feng GS. SHP-2 promoting migration and metastasis of MCF-7 with loss of E-cadherin, dephosphorylation of FAK and secretion of MMP-9 induced by IL-1beta in vivo and in vitro, Breast Cancer Res Treat. 2005; 89: 5-14PubMedCrossRefGoogle Scholar
  28. 28.
    Lirdprapamongkol K, Sakurai H, Kawasaki N, Choo MK, Saitoh Y, Aozuka Y, Singhirunnusorn P, Ruchirawat S, Svasti J, Saiki I. Vanillin suppresses in vitro invasion and in vivo metastasis of mouse breast cancer cells. Eur J Pharm Sci. 2005; 25: 57-65PubMedCrossRefGoogle Scholar
  29. 29.
    Larkins TL, Nowell M, Singh S, Sanford GL. Inhibition of cyclooxygenase-2 decreases breast cancer cell motility, invasion and matrix metalloproteinase expression. BMC Cancer 2006; 6: 18CrossRefGoogle Scholar
  30. 30.
    Mahabeleshwar GH. Kundu GC. Syk, a protein-tyrosine kinase, suppresses the cell motility and nuclear factor kappa B-mediated secretion of urokinase type plasminogen activator by inhibiting the phosphatidylinositol 3’-kinase activity in breast cancer cells. J Biol Chem. 2003; 278: 6209-6221PubMedCrossRefGoogle Scholar
  31. 31.
    Li J and Sidell N Growth-related oncogene produced in human breast cancer cells and regulated by Syk protein-tyrosine kinase. Int J Cancer 2005; 117: 14-20PubMedCrossRefGoogle Scholar
  32. 32.
    Han B, Nakamura M, Zhou G, Ishii A, Nakamura A, Bai Y, Mori I, Kakudo K. Calcitonin inhibits invasion of breast cancer cells: involvement of urokinase-type plasminogen activator (uPA) and uPA receptor. Int J Oncol. 2006; 28: 807-814PubMedGoogle Scholar
  33. 33.
    Subramanian R, Gondi CS, Lakka SS, Jutla A, Rao JS. siRNA-mediated simul- taneous downregulation of uPA and its receptor inhibits angiogenesis and invasive- ness triggering apoptosis in breast cancer cells, Int J Oncol. 2006; 28: 831-839PubMedGoogle Scholar
  34. 34.
    Fauquette W, Dong-Le Bourhis X, Delannoy-Courdent A, Boilly B, and Desbiens X. Characterization of morphogenetic and invasive abilities of human mammary epithelial cells: correlation with variations of urokinase-type plasminogen activator activity and type-1 plasminogen activator inhibitor level. Biol Cell. 1997; 89: 453-465PubMedCrossRefGoogle Scholar
  35. 35.
    Palmieri D, Lee JW, Juliano RL, Church FC. Plasminogen activator inhibitor-1 and -3 increase cell adhesion and motility of MDA-MB-435 breast cancer cells. J Biol Chem. 2002; 277: 40950-40957PubMedCrossRefGoogle Scholar
  36. 36.
    Ahn SM, Jeong SJ, Kim YS, Sohn Y, Moon A. Retroviral delivery of TIMP-2 inhibits H-ras-induced migration and invasion in MCF10A human breast epithelial cells. Cancer Lett. 2004; 207: 49-57PubMedCrossRefGoogle Scholar
  37. 37.
    Jiang WG, Davies G, Martin TA, Parr C, Watkins G, Mason MD, Mansel RE. Expression of membrane type-1 matrix metalloproteinase, MT1-MMP in human breast cancer and its impact on invasiveness of breast cancer cells, Int J Mol Med. 2006; 17: 583-590PubMedGoogle Scholar
  38. 38.
    Felding-Habermann B, O’Toole TE, Smith JW, Fransvea E, Ruggeri ZM, Ginsberg MH, Hughes PE, Pampori N, Shattil SJ, Saven A, Mueller BM. Integrin activation controls metastasis in human breast cancer, Proc Natl Acad Sci USA 2001; 98: 1853-1858PubMedCrossRefGoogle Scholar
  39. 39.
    Morini M, Mottolese M, Ferrari N, Ghiorzo F, Buglioni S, Mortarini R, Noonan DM, Natali PG, Albini A. The alpha 3 beta 1 integrin is associated with mammary carcinoma cell metastasis, invasion, and gelatinase B (MMP-9) activity. Int J Cancer. 2000; 87: 336-342PubMedCrossRefGoogle Scholar
  40. 40.
    Wang HS, Hung Y, Su CH, Peng ST, Guo YJ , Lai MC, Liu CY, Hsu JW. CD44 cross-linking induces integrin-mediated adhesion and transendothelial migration in breast cancer cell line by up-regulation of LFA-1 (alpha L beta2) and VLA-4 (alpha4beta1). Exp Cell Res. 2005; 304: 116-126PubMedCrossRefGoogle Scholar
  41. 41.
    Jauliac S, Lopez-Rodriguez C, Shaw LM, Brown LF, Rao A, Toker A. The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nat Cell Biol. 2002; 4: 540-544PubMedCrossRefGoogle Scholar
  42. 42.
    Scherberich A, Tucker RP, Degen M, Brown-Luedi M, Andres AC, Chiquet- Ehrismann R. Tenascin-W is found in malignant mammary tumors, promotes alpha8 integrin-dependent motility and requires p38MAPK activity for BMP-2 and TNF-alpha induced expression in vitro. Oncogene 2005; 24: 1525-1532PubMedCrossRefGoogle Scholar
  43. 43.
    Sung V, Stubbs JT 3rd, Fisher L, Aaron AD, Thompson EW. Bone sialoprotein supports breast cancer cell adhesion proliferation and migration through differential usage of the alpha(v)beta3 and alpha(v)beta5 integrins, J Cell Physiol. 1998; 176: 482-494PubMedCrossRefGoogle Scholar
  44. 44.
    Pecheur I, Peyruchaud O, Serre, Guglielmi J, Voland C, Bourre F, Margue C, Cohen-Solal M, Buffet A, Kieffer N, Clezardin P. Integrin alpha(v)beta3 expression confers on tumor cells a greater propensity to metastasize to bone. FASEB J. 2002; 16: 1266-1268PubMedGoogle Scholar
  45. 45.
    Sturge J, Hamelin J, Jones GE. N-WASP activation by a beta1-integrin- dependent mechanism supports PI3K-independent chemotaxis stimulated by urokinase-type plasminogen activator. J Cell Sci. 2002; 115: 699-711PubMedGoogle Scholar
  46. 46.
    Arboleda MJ, Lyons JF, Kabbinavar FF, Bray MR, Snow BE, Ayala R, Danino M, Karlan BY, Slamon DJ. Overexpression of AKT2/protein kinase Bbeta leads to up-regulation of beta1 integrins, increased invasion, and metastasis of human breast and ovarian cancer cells. Cancer Res. 2003; 63: 196-206PubMedGoogle Scholar
  47. 47.
    Shannon KE, Keene JL, Settle SL, Duffin TD, Nickols MA, Westlin M, Schroeter S, Ruminski PG, Griggs DW. Anti-metastatic properties of RGD- peptidomimetic agents S137 and S247. Clin Exp Metastasis 2004; 21: 129-138PubMedCrossRefGoogle Scholar
  48. 48.
    Barsky SH, Rao CN, Grotendorst GR, Liotta LA. Increased content of Type V Collagen in desmoplasia of human breast carcinoma. Am J Pathol. 1982; 108: 276-283PubMedGoogle Scholar
  49. 49.
    Demou ZN, Awad M, McKee T, Perentes JY, Wang X, Munn LL, Jain RK, Boucher Y. Lack of telopeptides in fibrillar collagen I promotes the invasion of a metastatic breast tumor cell line, Cancer Res. 2005; 65: 5674-5682PubMedCrossRefGoogle Scholar
  50. 50.
    Bemis LT, Schedin P. Reproductive state of rat mammary gland stroma modulates human breast cancer cell migration and invasion. Cancer Res. 2000; 60: 3414-3418PubMedGoogle Scholar
  51. 51.
    Bracke ME, Castronovo V, Van Cauwenberge RM-L, Vakaet L Jr, Strojny P, Foidart J-M, Mareel MM. The anti-invasive flavonoid (+)-catechin binds to laminin and abrogates the effect of laminin on cell morphology and adhesion. Exp Cell Res. 1987; 173: 193-205PubMedCrossRefGoogle Scholar
  52. 52.
    Udabage L, Brownlee GR, Waltham M, Blick T, Walker EC, Heldin P, Nilsson SK, Thompson EW, Brown TJ. Antisense-mediated suppression of hyaluronan synthase 2 inhibits the tumorigenesis and progression of breast cancer. Cancer Res. 2005; 65: 6139-6150PubMedCrossRefGoogle Scholar
  53. 53.
    Chen P, Shen WZ, Karnik P. Suppression of malignant growth of human breast cancer cells by ectopic expression of integrin-linked kinase. Int J Cancer 2004; 111: 881-891PubMedCrossRefGoogle Scholar
  54. 54.
    Lee J-H, Welch DR. Suppression of metastasis in human breast carcinoma MDA- MB-435 cells after transfection wih the metastasis suppressor gene, KiSS-1. Cancer Res. 1997; 57: 2384-2387PubMedGoogle Scholar
  55. 55.
    Navenot JM, Wang Z, Chopin M, Fujii N, Peiper SC. Kisspeptin-10-induced signaling of GPR54 negatively regulates chemotactic responses mediated by CXCR4: a potential mechanism for the metastasis suppressor activity of kisspeptins. Cancer Res. 2005; 65: 10450-10456PubMedCrossRefGoogle Scholar
  56. 56.
    Takeichi M. Cadherins: a molecular family important in selective cell-cell adhesion. Annu Rev Biochem. 1990; 59: 237-252PubMedCrossRefGoogle Scholar
  57. 57.
    Bracke ME, Van Roy FM, Mareel MM. The E-cadherin/catenin complex in invasion and metastasis, in: Attempts to Understand Metastasis Formation I, edited by U. Günthert and W. Birchmeier (Springer, Berlin, 1996) pp. 123-161.Google Scholar
  58. 58.
    Vleminckx K, Vakaet L, Mareel M, Fiers W, Van Roy F. Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 1991; 66: 107-119PubMedCrossRefGoogle Scholar
  59. 59.
    Perl A-K, Wilgenbus P, Dahl U, Semb H, Christofori G. A causal role for E- cadherin in the transition from adenoma to carcinoma. Nature 1998; 392: 190-193PubMedCrossRefGoogle Scholar
  60. 60.
    Pagliarini RA, Xu T. A genetic screen in Drosophila for metastatic behaviour. Science. 2003; 302: 1227-1231PubMedCrossRefGoogle Scholar
  61. 61.
    Suriano G, Mulholland D, De Wever O, Ferreira P, Mateus AR, Bruyneel E, Nelson CC, Mareel MM, Yokota J, Huntsman D, Seruca R. The intracellular E- cadherin germline mutation V832M lacks the ability to mediate cell-cell adhesion and to suppress invasion. Oncogene 2003; 22: 5716-5719PubMedCrossRefGoogle Scholar
  62. 62.
    Sarrio D, Perez-Mies B, Hardisson D, Moreno-Bueno G, Suarez A, Cano A, Martin-Perez J, Gamallo C, Palacios J. Cytoplasmic localization of p120ctn and E-cadherin loss characterize lobular breast carcinoma from preinvasive to metastatic lesions. Oncogene. 2004; 23: 3272-3283PubMedCrossRefGoogle Scholar
  63. 63.
    Berx G, Cleton-Jansen A-M, Strumane K, de Leeuw WJF, Nollet F, Van Roy F, Cornelisse C. E-cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain. Oncogene 1996; 13: 1919-1925PubMedGoogle Scholar
  64. 64.
    Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morpho- genesis, plays an essential role in tumor metastasis. Cell 2004; 117: 927-939PubMedCrossRefGoogle Scholar
  65. 65.
    Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, Mareel M, Huylebroeck D, van Roy F. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 2001; 7: 1267-1278PubMedCrossRefGoogle Scholar
  66. 66.
    Bracke ME, Vyncke BM, Bruyneel EA, Vermeulen SJ, De Bruyne GK, Van Larebeke NA, Vleminckx K, Van Roy FM, Mareel MM. Insulin-like growth factor I activates the invasion suppressor function of E-cadherin in MCF-7 human mammary carcinoma cells in vitro. Br J Cancer 1993; 68: 282-289PubMedGoogle Scholar
  67. 67.
    Dollé L, Oliveira M-J, Bruyneel E, Hondermarck H, Bracke M. Nerve growth factor mediates its pro-invasive effect in parallel with the release of a soluble E- cadherin fragment from breast cancer MCF-7/AZ cells. J Dairy Res. 2005; 72: 20-26PubMedCrossRefGoogle Scholar
  68. 68.
    Stove C, Boterberg T, Van Marck V, Mareel M, Bracke M. Bowes melanoma cells secrete heregulin, which can promote aggregation and counteract invasion of human mammary cancer cells. Int J Cancer 2005; 114: 572-578PubMedCrossRefGoogle Scholar
  69. 69.
    Boterberg T, Vennekens KM, Thienpont M, Mareel MM, Bracke ME. Inter- nalization of the E-cadherin/catenin complex and scattering of human mammary carcinoma cells MCF-7/AZ after treatment with conditioned medium from human skin squamous carcinoma cells COLO 16. Cell Adhesion Commun. 2000; 7: 299-310CrossRefGoogle Scholar
  70. 70.
    Rong H, Boterberg T, Maubach J, Stove C, Depypere H, Van Slambrouck S, Serreyn R, De Keukeleire D, Mareel M, Bracke M. 8-Prenylnaringenin, the phyto- estrogen in hops and beer, upregulates the function of the E-cadherin/catenin complex in human mammary carcinoma cells. Eur J Cell Biol. 2001; 80: 580-585PubMedCrossRefGoogle Scholar
  71. 71.
    Van Slambrouck S, Parmar VS, Sharma SK, De Bondt B, Foré F, Coopman P, Vanhoecke BW, Boterberg T, Depypere HT, Leclercq G, MBracke ME. Tangeretin inhibits extacellular-signal-regulated kinase (ERK) phosphorylation. FEBS Lett. 2005; 579: 1665-1669PubMedCrossRefGoogle Scholar
  72. 72.
    Vanhoecke B, Derycke L, Van Marck V, Depypere H, De Keukeleire D, Bracke M. Antiinvasive effect of xanthohumol, a prenylated chalcone present in hops (Humulus lupulus L.) and beer. Int J Cancer 2005; 117: 889-895PubMedCrossRefGoogle Scholar
  73. 73.
    Vermeulen SJ, Bruyneel EA, Van Roy FM, Mareel MM, Bracke ME. Activation of the E-cadherin/catenin complex in human MCF-7 breast cancer cells by alltrans-retinoic acid. Br J Cancer 1995; 72: 1447-1453PubMedGoogle Scholar
  74. 74.
    Vanhoecke BW, Depypere HT, De Beyter A, Sharma SK, Parmar VS, De Keukeleire D, Bracke ME. New anti-invasive compounds: results from the IndoBelgian screening program. Pure Appl Chem. 2005; 77: 65-74CrossRefGoogle Scholar
  75. 75.
    Katritzky AL, Kuanar M, Dobchev DA, Vanhoecke BWA, Karelson M, Parmar VS, Stevens CV, Bracke ME. QSAR modeling of anti-invasive activity of organic compounds using structural descriptors. Bioorg Med Chem. 2006; 14: 6933-6939PubMedCrossRefGoogle Scholar
  76. 76.
    Derycke LDM, Bracke ME. N-cadherin in the spotlight of cell-cell adhesion, differentiation, embryogenesis, invasion and signalling. Int J Dev Biol. 2004; 48: 463-476PubMedCrossRefGoogle Scholar
  77. 77.
    Hazan RB, Qiao R, Keren R, Badano I, Suyama K. Cadherin switch in tumor pro- gression. Ann NY Acad Sci. 2004; 1014: 155-163PubMedCrossRefGoogle Scholar
  78. 78.
    Hazan RB, Phillips GR, Fang Qiao R, Norton L, Aaronson SA. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol. 2000; 148: 779-790PubMedCrossRefGoogle Scholar
  79. 79.
    Vandewalle C, Comijn J, De Craene B, Vermassen P, Bruyneel E, Andersen H, Tulchinsky E, Van Roy F, Berx G. SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res. 2005; 33: 6566-6578PubMedCrossRefGoogle Scholar
  80. 80.
    De Craene B, Gilbert B, Stove C, Bruyneel E, van Roy F, Berx G. The trans- cription factor Snail induces tumor cell invasion through modulation of the epithelial cell differentiation program. Cancer Res. 2005; 65: 6237-6244PubMedCrossRefGoogle Scholar
  81. 81.
    Van Marck VL, Bracke ME. Epithelial-mesenchymal transitions in human cancer, in: Rise and Fall of Epithelial Phenotype. Concepts of Epithelial-Mesenchymal Transition, edited by P. Savagner (Landes Bioscience, Georgetown, Texas, USA, 2005), Chapter 9, pp. 135-159.Google Scholar
  82. 82.
    Marine JC, Francoz S, Maetens M, Wahl G, Toledo F, Lozano G. Keeping p53 in check: essential and synergistic functions of Mdm2 and Mdm4. Cell Death Differ. 2006; 13: 927-234PubMedCrossRefGoogle Scholar
  83. 83.
    Derycke L, Morbidelli L, Ziche M, De Wever O, Bracke M, Van Aken E. Soluble N-cadherin fragment promotes angiogenesis. Clin Exp Metastasis 2006, In Press.Google Scholar
  84. 84.
    Derycke L, De Wever O, Stove V, Vanhoecke B, Delanghe J, Depypere H, Bracke M. Soluble N-cadherin in human biological fluids. Int J Cancer 2006 In PressGoogle Scholar
  85. 85.
    Van Marck V, Stove C, Van Den Bossche K, Stove V, Paredes J, Vander Haeghen Y, Bracke M. P-cadherin promotes cell-cell adhesion and counteracts invasion in human melanoma. Cancer Res. 2005; 65: 8774-8783PubMedCrossRefGoogle Scholar
  86. 86.
    Palacios J, Benito N, Pizarro A, Suarez A, Espada J, Cano A, Gamallo C. Anomalous expression of P-cadherin in breast carcinoma. Am J Pathol. 1995; 146: 605-612PubMedGoogle Scholar
  87. 87.
    Radice GL, Ferreira-Cornwell MC, Robinson SD, Rayburn H, Chodosh LA, Takeichi M, and Hynes RO. Precocious mammary gland development in P-cadherin-deficient mice. J Cell Biol. 1997; 139: 1025-1032PubMedCrossRefGoogle Scholar
  88. 88.
    Deugnier M-A, Faraldo MM, Rousselle P, Thiery JP, and Glukhova MA. Cell- extracellular matrix interactions and EGF are important regulators of the basal mammary epithelial cell phenotype. J Cell Sci. 1999; 112: 1035-1044PubMedGoogle Scholar
  89. 89.
    Peralta Soler A, Knudsen KA, Salazar H, Han AC, and Keshgegian AA. P- Cadherin expression in breast carcinoma indicates poor survival. Cancer 1999; 86: 1263-1272PubMedCrossRefGoogle Scholar
  90. 90.
    Knudsen KA, Lin CY, Johnson KR, Wheelock MJ, Keshgegian AA, and Soler AP. Lack of correlation between serum levels of E- and P-cadherin fragments and the presence of breast cancer. Hum Pathol. 2000; 31: 961-965PubMedCrossRefGoogle Scholar
  91. 91.
    Madhavan M, Srinivas P, Abraham E, Ahmed I, Mathew A, Vijayalekshmi NR, Balaram P. Cadherins as predictive markers of nodal metastasis in breast cancer. Mod Pathol. 2001; 14: 423-427PubMedCrossRefGoogle Scholar
  92. 92.
    Gamallo C, Moreno-Bueno G, Sarrio D, Calero F, Hardisson D, Palacios J. The prognostic significance of P-cadherin in infiltrating ductal breast carcinoma. Mod Pathol. 2001; 14: 650-654PubMedCrossRefGoogle Scholar
  93. 93.
    Kovacs A, Walker RA, Nagy A, Gomba S, Jones L, Dearing S. Immuno- histochemical study of P-cadherin in breast cancer. Orv Hetil. 2002; 143: 405-409PubMedGoogle Scholar
  94. 94.
    Paredes J, Milanezi F, Reis-Filho JS, Leitão D, Athanazio D, Schmitt F. Aberrant P-cadherin expression: is it associated with estrogen-independent growth in breast cancer? Pathol Res Pract. 2002; 198: 795-801PubMedCrossRefGoogle Scholar
  95. 95.
    Soler AP, Russo J, Russo IH, Knudsen KA. Soluble fragment of P-cadherin adhesion protein found in human milk. J Cell Biochem. 2002; 85: 180-184PubMedCrossRefGoogle Scholar
  96. 96.
    Kovacs A, Dhillon J, Walker RA. Expression of P-cadherin, but not E-cadherin or N-cadherin, relates to pathological and functional differentiation of breast carcinomas. J Clin Pathol.: Mol Pathol. 2003; 56: 318-322CrossRefGoogle Scholar
  97. 97.
    Kovács A, Walker RA. P-cadherin as a marker in the differential diagnosis of breast lesions. J Clin Pathol. 2003; 56: 139-141PubMedCrossRefGoogle Scholar
  98. 98.
    Palacios J, Honrado E, Osorio A, Cazorla A, Sarrió D, Barroso A, Rodríguez S, Cigudosa JC, Diez O, Alonso C, Lerma E, Sánchez L, Rivas C, Benítez J. Immuno- histochemical characteristics defined by tissue microarray of hereditary breast cancer not attributable to BRCA1 or BRCA2 mutations: differences from breast carcinomas arising in BRCA1 and BRCA2 mutation carriers. Clin Cancer Res. 2003; 9: 3606-3614PubMedGoogle Scholar
  99. 99.
    Radice GL, Sauer CL, Kostetskii I, Peralta Soler A, Knudsen KA. Inappropriate P-cadherin expression in the mouse mammary epithelium is compatible with normal mammary gland function. Differentiation 2003; 71: 361-373PubMedCrossRefGoogle Scholar
  100. 100.
    Paredes J, Stove C, Stove V, Milanezi F, Van Marck V, Derycke L, Mareel M, Bracke M, Schmitt F. P-cadherin is up-regulated by the antiestrogen ICI 182,780 and promotes invasion of human breast cancer cells. Cancer Res. 2004; 64: 8309-8317PubMedCrossRefGoogle Scholar
  101. 101.
    Arnes JB, Brunet J-S, Stefansson I, Bégin LR, Wong N, Chappuis PO, Akslen LA, Foulkes WD. Placental cadherin and the basal epithelial phenotype of BRCA1-related breast cancer. Clin Cancer Res. 2005; 11: 4003-4011PubMedCrossRefGoogle Scholar
  102. 102.
    Collett K, Stefansson IM, Eide J, Braaten A, Wang H, Eide GE, Thoresen S Ø, Foulkes WD, Akslen LA. A basal epithelial phenotype is more frequent in interval breast cancers compared with screen detected tumors. Cancer Epidemiol. Biomarkers Prev. 2005; 14: 1108-1112CrossRefGoogle Scholar
  103. 103.
    Jacquemier J, Padovani L, Rabayrol L, Lakhani SR, Penault-Llorca F, Denoux Y, Fiche M, Figueiro P, Maisongrosse V, Ledoussal V, Martinez Penuela J, Udvarhely N, ElMakdissi G, Ginestier C, Geneix J, Charafe-Jauffret E, Xerri L, Eisinger F, Birnbaum D, Sobol H. The European Working Group for Breast Screening Pathology, The Breast Cancer Linkage Consortium and Hagay Sobol, Typical medullary breast carcinomas have a basal/myoepithelial phenotype. J Pathol. 2005; 207: 260-268PubMedCrossRefGoogle Scholar
  104. 104.
    Paredes J, Albergaria A, Oliveira JT, Jeronimo C, Milanezi F, Schmitt FC. P-cadherin overexpression is an indicator of clinical outcome in invasive breast carcinomas and is associated with CDH3 promoter hypomethylation. Clin Cancer Res. 2005; 11: 5869-5877PubMedCrossRefGoogle Scholar
  105. 105.
    Müller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verástegui E, Zlotnik A. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001; 410: 50-56PubMedCrossRefGoogle Scholar
  106. 106.
    Darash-Yahana M, Pikarsky E, Abramovitch R, Zeira E, Pal B, Karplus R, Beider K, Avniel S, Kasem S, Galun E, Peled A. Role of high expression levels of CXCR4 in tumor growth, vascularization, and metastasis., FASEB J. 2004; 18: 1240-1242PubMedGoogle Scholar
  107. 107.
    Kang H, Mansel RE, Jiang WG. Genetic manipulation of stromal cell-derived factor-1 attests the pivotal role of the autocrine SDF-1-CXCR4 pathway in the aggressiveness of breast cancer cells. Int J Oncol. 2005; 26: 14291-434Google Scholar
  108. 108.
    Schmid BC, Rudas M, Rezniczek GA, Leodolter S, Zeillinger R. CXCR4 is expressed in ductal carcinoma in situ of the breast and in atypical ductal hyperplasia. Breast Cancer Res Treat. 2004; 84: 247-250PubMedCrossRefGoogle Scholar
  109. 109.
    Richard CL, Tan EY, Blay J. Adenosine upregulates CXCR4 and enhances the pro- liferative and migratory responses of human carcinoma cells to CXCL12/SDF-1α. Int J Cancer 2006; 119: 2044-2053PubMedCrossRefGoogle Scholar
  110. 110.
    Holland JD, Kochetkova M, Akekawatchai C, Dottore M, Lopez A, SMcColl SR. Differential functional activation of chemokine receptor CXCR4 is mediated by G proteins in breast cancer cells. Cancer Res. 2006; 66: 4117-4124PubMedCrossRefGoogle Scholar
  111. 111.
    Sun Y, Cheng Z, Ma L, Pei G. Beta-arrestin2 is critically involved in CXCR4-mediated chemotaxis, and this is mediated by its enhancement of p38 MAPK activation. J Biol Chem. 2003; 277: 49212-49219CrossRefGoogle Scholar
  112. 112.
    Fernandis AZ, Prasad A, Band H, Klosel R, Ganju RK. Regulation of CXCR4- mediated chemotaxis and chemoinvasion of breast cancer cells. Oncogene 2004; 23: 157-167PubMedCrossRefGoogle Scholar
  113. 113.
    Zijlstra A, Quigley JP. The DARC side of metastasis: shining a light on KAI1- mediated metastasis suppression in the vascular tunnel. Cancer Cell 2006; 10: 177-178PubMedCrossRefGoogle Scholar
  114. 114.
    Jiang WG, Raz A, Douglas-Jones A, Mansel RE. Expression of autocrine motility factor (AMF) and its receptor, AMFR, in human breast cancer. J. Histochem Cytochem. 2006; 54: 231-241PubMedCrossRefGoogle Scholar
  115. 115.
    Bellahcène A, Castronovo V. Expression of bone matrix proteins in human breast cancer: potential roles in microcalcification formation and in the genesis of bone metastases. Bull Cancer 1997; 84: 17-24PubMedGoogle Scholar
  116. 116.
    Aigner S, Ramos CL, Hafezi-Moghadam A, Lawrence MB, Friederichs J, Altevogt P, Ley K. CD24 mediates rolling of breast carcinoma cells on P-selectin. FASEB J. 1998; 12: 1241-1251PubMedGoogle Scholar
  117. 117.
    Baumann P, Cremers N, Kroese F, Orend G, Chiquet-Ehrismann T, Uede T, Yagita H, Sleeman JP. CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res. 2005; 65: 10783-10793PubMedCrossRefGoogle Scholar
  118. 118.
    Schabath H, Runz S, Joumaa S, Altevogt P. CD24 affects CXCR4 function in pre-B lymphocytes and breast carcinoma cells. J Cell Sci. 2006; 119: 314-325PubMedCrossRefGoogle Scholar
  119. 119.
    Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006; 107: 1761-1767PubMedCrossRefGoogle Scholar
  120. 120.
    Dittmar T, Husemann A, Schewe Y, Nofer JR, Niggemann B, Zanker KS, Brandt BH. Induction of cancer cell migration by epidermal growth factor is initiated by specific phosphorylation of tyrosine 1248 of c-erbB-2 receptor via EGFR. FASEB J. 2002; 16: 1823-1825PubMedGoogle Scholar
  121. 121.
    Wang SJ, Saadi W, Lin F, Minh-Canh Nguyen C, Li Jeon N. Differential effects of EGF gradient profiles on MDA-MB-231 breast cancer cell chemotaxis. Exp Cell Res. 2004; 300: 180-189PubMedCrossRefGoogle Scholar
  122. 122.
    Hart S, Fischer OM, Prenzel N, Zwick-Wallasch E, Schneider M, Hennighausen L, Ullrich A. GPCR-induced migration of breast carcinoma cells depends on both EGFR signal transactivation and EGFR-independent pathways. Biol Chem. 2005; 386: 845-855PubMedCrossRefGoogle Scholar
  123. 123.
    Sarkar S, Maceyka M, Hait NC, Paugh SW, Sankala H, Milstien S, Spiegel S. Sphingosine kinase 1 is required for migration, proliferation and survival of MCF-7 human breast cancer cells. FEBS Lett. 2005; 579: 5313-5317PubMedCrossRefGoogle Scholar
  124. 124.
    Korah R, Choi L, Barrios J, Wieder R. Expression of FGF-2 alters focal adhesion dynamics in migration-restricted MDA-MB-231 breast cancer cells. Breast Cancer Res Treat. 2004; 88: 17-28PubMedCrossRefGoogle Scholar
  125. 125.
    Stadler CR, Knyazev P, Bange J, Ullrich A. FGFR4 GLY388 isotype suppresses motility of MDA-MB-231 breast cancer cells by EDG-2 gene repression. Cell Signal 2006; 18: 783-794PubMedCrossRefGoogle Scholar
  126. 126.
    Mine S, Fujisaki T, Kawahara C, Tabata T, Iida T, Yasuda M, Yoneda T, Tanaka Y. Hepatocyte growth factor enhances adhesion of breast cancer cells to endo- thelial cells in vitro through up-regulation of CD44. Exp Cell Res. 2003; 288: 189-197PubMedCrossRefGoogle Scholar
  127. 127.
    Matteucci E, Locati M, Desiderio MA. Hepatocyte growth factor enhances CXCR4 expression favoring breast cancer cell invasiveness. Exp Cell Res. 2005; 310: 176-185PubMedCrossRefGoogle Scholar
  128. 128.
    Stove C, Bracke M. Roles for neuregulins in human cancer. Clin Exp Metastasis 2004; 21: 665-684PubMedCrossRefGoogle Scholar
  129. 129.
    Kalish ED, Iida N, Moffat FL, Bourguignon LY. A new CD44V3-containing isoform is involved in tumor cell growth and migration during human breast carcinoma progression. Front Biosci. 1999; 4: A1-A8PubMedCrossRefGoogle Scholar
  130. 130.
    Bourguignon LY, Singleton PA, Zhu H, Zhou B. Hyaluronan promotes signaling interaction between CD44 and the transforming growth factor beta receptor I in metastatic breast tumor cells. J Biol Chem. 2002; 277: 39703-39712PubMedCrossRefGoogle Scholar
  131. 131.
    Lopez JI, Camenisch TD, Stevens MV, Sands BJ, McDonald J, JSchroeder JA. CD44 attenuates metastatic invasion during breast cancer progression. Cancer Res. 2005; 65: 6755-6763PubMedCrossRefGoogle Scholar
  132. 132.
    Tzircotis G, Thorne RF, Isacke CM. Chemotaxis towards hyaluronan is dependent on CD44 expression and modulated by cell type variation in CD44- hyaluronan binding. J Cell Sci. 2005; 118: 5119-5128PubMedCrossRefGoogle Scholar
  133. 133.
    Mauro L, Salerno M, Morelli C, Boterberg T, Bracke ME, Surmacz E. Role of the IGF-I receptor in the regulation of cell-cell adhesion: implications in cancer development and progression. J Cell Physiol. 2002; 194: 108-116CrossRefGoogle Scholar
  134. 134.
    Jackson JG, Zhang X, Yoneda T, Yee D. Regulation of breast cancer cell motility by insulin receptor substrate-2 (IRS-2) in metastatic variants of human breast cancer cell lines. Oncogene 2001; 20: 7318-7325PubMedCrossRefGoogle Scholar
  135. 135.
    Guvakova MA, Adams JC, Boettiger D. Functional role of alpha-actinin, PI 3- kinase and MEK1/2 in insulin-like growth factor I receptor kinase regulated motility of human breast carcinoma cells. J Cell Sci. 2002; 115: 4149-4165PubMedCrossRefGoogle Scholar
  136. 136.
    Sachdev D, Hartell JS, Lee AV, Zhang X, Yee D. A dominant negative type I insulin-like growth factor receptor inhibits metastasis of human cancer cells. J Biol Chem. 2004; 79: 5017-5024Google Scholar
  137. 137.
    Akekawatchai C, Holland JD, Kochetkova M, Wallace JC, McCollSR. Transactivation of CXCR4 by the insulin-like growth factor-1 receptor (IGF-1R) in human MDA-MB-231 breast cancer epithelial cells. J Biol Chem. 2005; 280: 39701-39708PubMedCrossRefGoogle Scholar
  138. 138.
    Nozaki S, Sledge GW Jr, Nakshatri H. Cancer cell-derived interleukin 1alpha contributes to autocrine and paracrine induction of pro-metastatic genes in breast cancer. Biochem Biophys Res Commun. 2000; 275: 60-62PubMedCrossRefGoogle Scholar
  139. 139.
    Rahn JJ, Shen Q, Mah BK, Hugh JC. MUC1 initiates a calcium signal after ligation by intercellular adhesion molecule. J Biol Chem. 2004; 279: 29386-29390PubMedCrossRefGoogle Scholar
  140. 140.
    Rahn JJ, Chow JW, Horne GJ, Mah BK, Emerman JT, Hoffman P, Hugh JC. MUC1 mediates transendothelial migration in vitro by ligating endothelial cell ICAM-1. Clin Exp Metastasis 2005; 22: 475-483PubMedCrossRefGoogle Scholar
  141. 141.
    Campo McKnight DA, Sosnoski DM, Koblinski JE, Gay CV. Roles of osteonectin in the migration of breast cancer cells into bone. J Cell Biochem. 2006; 97: 288-302PubMedCrossRefGoogle Scholar
  142. 142.
    Renkonen J, Paavonen T, Renkonen R. Endothelial epithelial expression of sialyl Lewis(x) and sialyl Lewis(a) in lesions of breast carcinoma. Int J Cancer 1997; 74: 296-300PubMedCrossRefGoogle Scholar
  143. 143.
    Nguyen Q-D, De Wever O, Bruyneel E, Hendrix A, Xie W-Z, Lombet A, Leibl M, Mareel M, Gieseler F, Bracke M, Gespach C. Commutators of PAR-1 signaling in cancer cell invasion reveal an essential role of the Rho-Rho kinase axis and tumor microenvironment. Oncogene 2005; 24: 8240-8251PubMedCrossRefGoogle Scholar
  144. 144.
    Henrikson KP, Salazar SL, Fenton JW 2nd, Pentecost BT. Role of thrombin receptor in breast cancer invasiveness. Br J Cancer 1999; 79: 401-406PubMedCrossRefGoogle Scholar
  145. 145.
    Hjortoe GM, Petersen LC, Albrektsen T, Sorensen BB, Norby PL, Mandal SK, Pendurthi UR, Rao LV. Tissue factor-factor VIIa-specific up-regulation of IL-8 expression in MDA-MB-231 cells is mediated by PAR-2 and results in increased cell migration. Blood 2004; 103: 3029-3037PubMedCrossRefGoogle Scholar
  146. 146.
    Hatse S, Princen K, Bridger G, De Clercq E, Schols D. Chemokine receptor inhibition by AMD3100 is strictly confined to CXCR4. FEBS Lett. 2002; 527: 255-262PubMedCrossRefGoogle Scholar
  147. 147.
    Tamamura H, Hori A, Kanzaki N, Hiramatsu K, Mizumot Mo, Nakashima H, Yamamoto N, Otak Aa, Fujii N. T140 analogs as CXCR4 antagonists identified as anti-metastatic agents in the treatment of breast cancer. FEBS Lett. 2003; 550: 79-83PubMedCrossRefGoogle Scholar
  148. 148.
    Liang Z, Wu T, Lou H, Yu X, Taichman RS, Lau SK, Nie S, Umbreit J, Shim H. Inhibition of breast cancer metastasis by selective synthetic polypeptide against CXCR4. Cancer Res. 2004; 64: 4302-4308PubMedCrossRefGoogle Scholar
  149. 149.
    Rozic JG, Chakraborty C, Lala PK. Cyclooxygenase inhibitors retard murine mammary tumor progression by reducing tumor cell migration, invasiveness and angiogenesis. Int J Cancer 2001; 93: 497-506PubMedCrossRefGoogle Scholar
  150. 150.
    Singh B, Berry JA, Shoher A, Ramakrishnan V, Lucci A. COX-2 overexpression increases motility and invasion of breast cancer cells. Int J Oncol. 2005; 26: 1393-1399PubMedGoogle Scholar
  151. 151.
    Boissier S, Ferreras M, Peyruchaud O, Magnetto S, Ebetino FH, Colombel M, Delmas P, Delaissé J-M, Clézardin P. Bisphosphonates inhibit breast and prostate carcinoma cell invasion, an early event in the formation of bone metastases. Cancer Res. 2000; 60: 2949-2954PubMedGoogle Scholar
  152. 152.
    Denoyelle C, Hong L, Vannier JP, Soria J, Soria C. New insights into the actions of bisphosphonate zoledronic acid in breast cancer cells by dual RhoA-dependent and -independent effects. Br J Cancer 2003; 88: 1631-1640PubMedCrossRefGoogle Scholar
  153. 153.
    Hiraga T, Williams PJ, Ueda A, Tamura D, Yoneda T. Zoledronic acid inhibits visceral metastases in the 4T1/luc mouse breast cancer model. Clin Cancer Res. 2004; 10: 4559-4567 (2004).PubMedCrossRefGoogle Scholar
  154. 154.
    Valachovicova T, Slivova V, Bergman H, Shuherk J, Sliva D. Soy isoflavones suppress invasiveness of breast cancer cells by the inhibition of NF-kappaB/AP1-dependent and -independent pathways. Int J Oncol. 2004; 25: 1389-1395PubMedGoogle Scholar
  155. 155.
    Slivova V, Zaloga G, DeMichele SJ, Mukerji P, Huang YS, Siddiqui R, Harvey K, Valachovicova T, Sliva D. Green tea polyphenols modulate secretion of urokinase plasminogen activator (uPA) and inhibit invasive behavior of breast cancer cells. Nutr Cancer 2005; 52: 66-73PubMedCrossRefGoogle Scholar
  156. 156.
    Nangia-Makker P, Hogan V, Honjo Y, Baccarini S, Tait L, Bresalier R, Raz A. Inhibition of human cancer cell growth and metastasis in nude mice by oral intake of modified citrus pectin. J Natl Cancer Inst. 2002; 94: 1854-1862PubMedGoogle Scholar
  157. 157.
    Awad AB, Williams H, Fink CS. Phytosterols reduce in vitro metastatic ability of MDA-MB-231 human breast cancer cells. Nutr Cancer 2001; 40: 157-164PubMedCrossRefGoogle Scholar
  158. 158.
    Cai J, Jiang WG, Mansel RE. Inhibition of angiogenic factor- and tumour-induced angiogenesis by gamma linolenic acid. Prostaglandins Leukot Essent Fatty Acids 1999; 60: 21-29PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Marc E. Bracke
    • 1
  • Daan De Maeseneer
    • 2
  • Veerle Van Marck
    • 3
  • Lara Derycke
    • 4
  • Barbara Vanhoecke
    • 5
  • Olivier De Wever
    • 6
  • Herman T. Depypere
    • 7
  1. 1.Laboratory of Experimental Cancer Research, Department of Experimental CancUniversity HospitalBelgium
  2. 2.Laboratory of Experimental Cancer Research, Department of Experimental CancUniversity HospitalBelgium
  3. 3.Laboratory of Experimental Cancer Research, Department of Experimental CancUniversity HospitalBelgium
  4. 4.Laboratory of Experimental Cancer Research, Department of Experimental CancUniversity HospitalBelgium
  5. 5.Laboratory of Experimental Cancer Research, Department of Experimental CancUniversity HospitalBelgium
  6. 6.Laboratory of Experimental Cancer Research, Department of Experimental CancUniversity HospitalBelgium
  7. 7.Department of Gynaecological OncologyUniversity HospitalBelgium

Personalised recommendations