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Genetic analysis of breast cancer progression

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Abstract

At the histological level, breast tumors display a variety of morphologic lesions which suggest the existence of an increasingly aberrant pathway of intermediate steps leading to the invasive primary tumor and its metastatic dissemination. In order to obtain direct evidence for this presumed progression, underlying genetic changes must be identified. Analyses of primary breast tumors have revealed a large number of dominant and recessive gene alterations encompassing several cellular attributes and activities. It is quite likely that some of these alterations are of a causal nature and thus enable the tumor to attain distinctive malignant phenotypes, such as, dysregulated proliferation, invasion, angiogenesis, and ability to metastasize. Considerable heterogeneity has been observed in the sequence of acquisition of these genetic changes, which is substantiated by recent comparative analyses between carefully microdissected preinvasive and invasive tumor. The data are evaluated here in the context of existing models of breast cancer progression. Implications and prospects for translational application to the clinic are also discussed.

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References

  1. E. R. Fearon and B. Vogelstein (1990). A genetic model for colorectal tumorigenesis.Cell 61:759–767.

    PubMed  Google Scholar 

  2. D. L. Page and W. D. Dupont (1990). Anatomical markers of human premalignancy and risk of breast cancer.Cancer 66:1326–1335.

    PubMed  Google Scholar 

  3. P. O'Connell, V. Pekkel, S. Fuqua, C. K. Osborne, and D. C. Allred (1994). Molecular genetic studies of early breast cancer evolution.Br. Cancer Res. Treat. 32:5–12.

    Google Scholar 

  4. D.C. Allred, P. O'Connell, S. A. W. Fuqua, and C. K. Osborne (1994). Immunohistochemical studies of early breast cancer.Br. Cancer Res. Treat. 32:13–18.

    Google Scholar 

  5. H. S. Smith, Y. Lu, G. Deng, O. Martinez, S. Krams, B-M. Ljung, A. Thor, and M. Lagios (1993). Molecular aspects of early stages of breast cancer progression.J. Cell. Biochem. 17G:144–152.

    Google Scholar 

  6. E. Liu, C. Dollbaum, C. Rochlitz, C. Benz, and H. S. Smith (1988). Molecular lesions involved in the progression of breast cancer.Oncogene 3:323–327.

    PubMed  Google Scholar 

  7. H. S. Smith, S. R. Wolman, S. H. Dairkee, M. C. Hancock, M. Lippman, A. Leff, and A. J. Hackett (1987). Immortalization in culture: Occurrence at a late stage in progression of breast cancer.J. Natl. Cancer Inst. 78:611–615.

    PubMed  Google Scholar 

  8. Z. Zhuang, M. J. Merino, R. Chuaqui, L. Liotta, and M. R. Emmert-Buck (1995). Identical allelic loss on chromosome 11q13 in microdissectedin situ and invasive human breast cancer.Cancer Res. 55:467–471.

    PubMed  Google Scholar 

  9. C. M. Aldaz, T. Chen, A. Sahin, J. Cunningham, and M. Bondy (1995). Comparative allelotype ofin situ and invasive human breast cancer: high frequency of microsatellite instability in lobular breast carcinomas.Cancer Res. 55:3976–3981.

    PubMed  Google Scholar 

  10. B. Zafrani, M. Gerbault-Seureau, V. Mosseri, and B. Dutrillaux (1992). Cytogenetic study of breast cancer: clinicopathologic significance of homogeneously staining regions in 84 patients.Hum. Pathol. 23:542–547.

    PubMed  Google Scholar 

  11. J.M. Trent (1995). Cytogenetic and molecular biologic alterations in human breast cancer: A review.Br. Cancer Res. Treat. 5:221–229.

    Google Scholar 

  12. D. J. Slamon, G. M. Clark, S. G. Wong, W. J. Levin, A. Ullrich, and W. L. McGuire (1987). Human breast cancer: correlation of relapse and survival with amplification of theHER2/neu oncogene.Science 235:177–182.

    PubMed  Google Scholar 

  13. S. V. Machotka, C. T. Garret, A. M. Schwartz, and R. Callahan (1989). Amplification of the proto-oncogenesint-2, c-erbB-2 and c-myc in human breast cancer.Clin. Chim. Acta 4:207–218.

    Google Scholar 

  14. G. A. Lammie and G. Peters (1991). Chromosome 11q13 abnormalities in human cancer.Cancer Cells 3:413–420.

    PubMed  Google Scholar 

  15. J. Adnane, P. Gaudray, C. A. Dionne, G. Crumley, M. Jaye, J. Schlessinger, P. Jeanteur, D. Bimbaum, and C. Theillet (1991). BEK and FLG, two receptors to members of the FGF family, are amplified in subsets of human breast cancers.Oncogene 6:659–663.

    Google Scholar 

  16. E. M. Berns, J. G. Klijn, I. L. van Staveren, H. Portengen, and J. A. Foekens (1992). Sporadic amplification of the insulin-like growth factor 1 receptor gene in human breast tumors.Cancer Res. 52:1036–1039.

    PubMed  Google Scholar 

  17. A. Kallioniemi, O. P. Kallioniemi, F. Waldman, L. Chen, L. C. Yu, Fung, H. S. Smith, D. Pinke, and J. Gray (1991). Comparative genomic hybridization: A powerful new method for cytogenetic analysis of solid tumors.Science 258:818–820.

    Google Scholar 

  18. A. Kallioniemi, O. P. Kallioniemi, J. Piper, M. Tanner, T. Stokke, L. Chen, H. S. Smith, D. Pinkel, J. W. Gray, and F. Waldman (1994). Detection and mapping of amplified DNA sequences in breast cancer by comparative genomic hybridization.PNAS 91:2156–2160.

    PubMed  Google Scholar 

  19. O. P. Kallioniemi, A. Kallioniemi, W. Kurisu, A. Thor, L. C. Chen, H. S. Smith, F. M. Waldman, D. Pinkel, and J. W. Gray (1992).erbB2 amplification in breast cancer analyzed by fluorescencein situ hybridization.PNAS 89:5321–5325.

    PubMed  Google Scholar 

  20. J. R. C. Sainsbury, J. R. Farndon, G. K. Needham, A. J. Malcolm, and H. L. Harris (1987). Epidermal growth factor receptor status as predictor of early recurrence of and death from breast cancer.Lancet 1(8547):1398–1402.

    PubMed  Google Scholar 

  21. J. Lundy, A. Scuss, D. Stanick, E. S. McCormack, S. Kramer, and J. M. Sorvillo (1991). Expression of neu protein, EGF and TGFα in breast cancer.Am. J. Pathol. 138:1527–1534.

    PubMed  Google Scholar 

  22. Y. Umekita, N. Enokizono, Y. Sagara, K. Kuriwaki, T. Takasaki, A. Yoshida, and H. Yoshida (1992). Immunohistochemical studies on TGFα in human breast cancer: their relationship to estrogen receptor status, histological grade, mitogenic index and nodal status.Arch. Pathol. Histol. 420:325–351.

    Google Scholar 

  23. N. E. Hynes (1996). ErbB2 activation and signal transduction in normal and malignant mammary cells.J. Mam. Gland Biol. Neoplasia,1(2):199–206.

    Google Scholar 

  24. G. Gasparini, W. J. Gullick, S. Maluta, P. D. Palma, O. Caffo, S. Meli, E. Leonardi, P. Boracchi, F. Pozza, N. R. Lemoine, and P. Bevilacqua (1994). c-erbB3 and c-erbB2 gene expression in node-negative breast carcinoma.Eur. J. Cancer 30A:16–22.

    PubMed  Google Scholar 

  25. N. R. Lemoine, D. M. Barnes, D. P. Hollywood, C. M. Hughes, P. Smith, E. Dublin, S. A. Prigent, W. J. Gullick, and H. C. Hurst (1992). Expression oferbB3 gene product in breast cancer.Br. J. Cancer 66:1116–1122.

    PubMed  Google Scholar 

  26. G. D. Plowman, J. M. Culouscou, G. S. Whitney, J. M. Green, G. W. Carlton, L. Foy, M. G. Neubauer, and M. Shoyab (1993). Ligand specific activation ofHER4/p180erbB4, a fourth member of the epidermal growth factor receptor family.PNAS 90:1746–1750.

    PubMed  Google Scholar 

  27. E. M. J. J. Berns, J. G. M. Klijn, W. L. J. Van Putten, I. L. Van Staveren, H. Portengen, and J. A. Foekens (1992). c-myc amplification is a better prognostic factor thanHER2/neu amplification in primary breast cancer.Cancer Res. 52:1107–1113.

    PubMed  Google Scholar 

  28. H. Kreipe, H. Feist, L. Fischer, J. Felgner, K. Heidorn, L. Mettler, and R. Parwaresch (1993). Amplification of c-myc but not of c-erbB2 is associated with high proliferative capacity in breast cancer.Cancer Res. 53:1956–1961.

    PubMed  Google Scholar 

  29. I. L. Lee, V. W. Raymond, M. S. Tsao, D. C. Lee, H. S. Earp, and J. W. Grisham (1991). Clonal cosegregation of tumorigenicity with overexpression of c-myc and transforming growth factor α genes in chemically transformed rat liver epithelial cells.Cancer Res. 51:5238–5244.

    PubMed  Google Scholar 

  30. I. Bieche, M. H. Champeme, and R. Lidereau (1994). A tumor suppressor gene on chromosome 1p32-1pter controls the amplification ofmyc family genes in breast cancer.Cancer Res. 54:4274–4276.

    PubMed  Google Scholar 

  31. G. Peters, V. Fantl, R. Smith, S. Brookes, and C. Dickson (1995). Chromosome 11q13 markers and D-type cyclins in breast cancer.Breast Cancer Res. Treat. 33:125–135.

    PubMed  Google Scholar 

  32. C. Gillett, V. Fantl, R. Smith, C. Fisher, J. Bartek, C. Dickson, D. Barnes, and G. Peters (1994). Amplification and overexpression of cyclin D1 in breast cancer detected by immunohistochemical staining.Cancer Res. 54:1812–1817.

    PubMed  Google Scholar 

  33. D. Bellet (1992). Tumor-susceptibility markers. Monographs.Natl. Cancer Inst. 12:115–121.

    Google Scholar 

  34. R. J. Stanbridge (1990). Human tumor suppressor genes.Ann. Rev. Genet. 24:615–657.

    PubMed  Google Scholar 

  35. R. Sager (1989). Tumor Suppressor Genes: The puzzle and the promise.Science 246:1406–1412.

    PubMed  Google Scholar 

  36. B. Groner and N. E. Hynes (1990). Chapter III, 1. Mutations in human breast cancer cells: dominantly-acting oncogenes and tumor suppressor genes suggest strategies for targeted interference.Int. J. Cancer 4:40–46.

    Google Scholar 

  37. G. P. Studzinski, D. C. Moore, and D. L. Carter (1990). Editorial, Suppressor genes; restraint of growth or of tumor progression?Lab. Invest. 63:279–282.

    PubMed  Google Scholar 

  38. R. E. Hollingsworth and W-H. Lee (1991). Tumor suppressor genes: new prospects for cancer research.JNCI 83:91–96.

    PubMed  Google Scholar 

  39. R. A. Weinberg (1991). Tumor suppressor genes.Science 254:1138–1146.

    PubMed  Google Scholar 

  40. R. Callahan and G. Campbell (1989). Mutations in human breast cancer: an overview.JNCI 81:1780–1786.

    PubMed  Google Scholar 

  41. A. J. Levine and J. Momand (1990). Tumor suppressor genes: The p53 and retinoblastoma sensitivity genes and gene products.Biochim. Biophys. Acta 1032:119–136.

    PubMed  Google Scholar 

  42. A. G. Knudson, Jr. (1971). Mutation and cancer: Statistical study of retinoblastoma.PNAS 68:820–823.

    PubMed  Google Scholar 

  43. P. Devilee and C. J. Cornelisse (1990). Genetics of human breast cancer.Cancer Surv. 9:605–630.

    PubMed  Google Scholar 

  44. J. Mackay, A. M. Thompson, C. Coles, and C. M. Steel (1990). Molecular lesions in breast cancer.Int. J. Cancer 5:47–50.

    Google Scholar 

  45. R. Callahan, C. S. Cropp, G. R. Merlo, D. S. Liscia, A. P. M. Cappa, and R. Lidereau (1992). Somatic mutations and human breast cancer.Cancer 69:1582–1588.

    PubMed  Google Scholar 

  46. L. C. Chen, W. Kurisu, B. M. Ljung, E. S. Goldman, D. Moore, and H. S. Smith (1992). Heterogeneity for allelic loss in human breast cancer.JNCI 84:506–510.

    PubMed  Google Scholar 

  47. M. Balaz, K. Matdumara, D. Moore, D. Pinkel, J. W. Gray, and F. M. Waldman (1995). Karyotypic heterogeneity and its relationship to labeling index in interphase breast tumor cells.Cytometry 20:62–73.

    PubMed  Google Scholar 

  48. P. Devilee, M. van Vliet, A. Bardoel, T. Kievits, N. Kuipers-Diujkshoorn, P. L. Pearson, and C. J. Cornelisse (1991). Frequent somatic imbalance of marker alleles for chromosome 1 in human primary breast carcinoma.Cancer Res. 51:1020–1025.

    PubMed  Google Scholar 

  49. K. Takita, T. Sato, M. Miyagi, M. Watatani, F. Akiyama, G. Sakamoto, F. Kasumi, R. Abe, and Y. Nakamura (1992). Correlation of loss of alleles on the Short arm of chromosome 11 and 17 with metastasis of primary breast cancer to lymph nodes.Cancer Res. 52:3914–3917.

    PubMed  Google Scholar 

  50. T. Sato, A. Tanigami, K. Yamakawa, F. Akiyama, F. Kasumi, G. Sakamoto, and Y. Nakamura (1990). Allelotype of breast cancer. Cumulative allele losses promote tumor progression in primary breast cancer.Cancer Res. 50:7184–7189.

    PubMed  Google Scholar 

  51. I. U. Ali, R. Lidereau, C. Theillet, and R. Callahan (1987). Reduction to homozygosity of genes on chromosome 11 in human breast neoplasia.Science 238:185–188.

    PubMed  Google Scholar 

  52. P. Devilee, P. L. Pearson, and C. J. Cornelisse (1989). Allele losses in breast cancer.Lancet 154.

  53. I. Beiche, M. H. Champeme, G. Merlo, C-J. Larsen, R. Callahan, and R. Lideraeau (1990). Loss of heterozygosity of the L-myc oncogene in human breast tumors.Hum. Genet. 85:101–105.

    PubMed  Google Scholar 

  54. C. Lundberg, C. L. Skoog, W. Cavenee, M. Nordenskjold (1987). Loss of heterozygosity in human ductal breast tumors indicates a recessive mutation on chromosome 13.Proc. Natl. Acad. Sci. U.S.A. 84:2372–2376.

    PubMed  Google Scholar 

  55. P. A. Futreal, P. Soderkvist, J. R. Marks, J. D. Iglehart, C. Cochran, J. C. Barrett, and R. W. Wiseman (1992). Detection of frequent allelic loss on proximal chromosome 17q in sporadic breast carcinoma using microsatellite length polymorphisms.Cancer Res. 52:2624–2627.

    PubMed  Google Scholar 

  56. J. Mackay, P. A. Elder, C. M. Steel, and A. P. M. Forrest (1988). Allele loss on short arm of chromosome 17 in breast cancers.Lancet 2(8625):1384–1385.

    PubMed  Google Scholar 

  57. C. Coles, A. M. Thompson, P. A. Elder, B. Cohen, I. M. Mackenzie, G. Cranston, U. Chetty, J. Mackay, M. Macdonald, Y. Nakamura, B. Hoyheim, and C. M. Steel (1990). Evidence implicating at least two genes on chromosome 17p in breast carcinogenesis.Lancet 336:761–763.

    PubMed  Google Scholar 

  58. P. Devilee, M. van Vliet, P. van Sloun, N. Dijkshoorn, J. Hermans, P. L. Pearson, and C. J. Cornelisse (1991). Allelotype of human breast carcinoma: a second major site for loss of heterozygosity is on chromosome 6q.Oncogene 6:1705–1711.

    Google Scholar 

  59. L. C. Chen, C. Dollbaum, and H. S. Smith. (1986). Loss of heterozygosity on chromosome 1q in human breast cancer.PNAS 86:7204–7207.

    Google Scholar 

  60. L. C. Chen, A. Neubauer, W. Kurisu, F. Waldman, B-M. Ljung, W. Goodson III, E. Goldman, D. Moore, E. Liu, B. Mayall, and H. S. Smith (1991). Loss of heterozygosity on the short arm of chromosome 17 is associated with high proliferative capacity and DNA aneuploidy in primary human breast cancer.PNAS 88:3847–3851.

    PubMed  Google Scholar 

  61. S. Gendler, E. Cohen, A. Craston, T. Duhig, G. Johnstone, and D. Barnes (1990). The locus of the polymorphic epithelial mucin (pem) tumour antigen on chromosome 1q21 shows a high frequency of alteration in primary human breast tumors.Int. J. Cancer 45:431–435.

    PubMed  Google Scholar 

  62. G. Merlo, J. Siddiqui, C. Cropp, D. Liscia, R. Lidereau, R. Callahan, and D. Kufe (1989). Frequent alteration of the DF3 tumor-associated antigen gene in primary human breast carcinomas.Cancer Res. 49:6966–6971.

    PubMed  Google Scholar 

  63. C. J. Cornelisse (1992). Loss of heterozygosity, chromosome 7q, and breast cancer.Lancet 339:1423.

    PubMed  Google Scholar 

  64. I. Bieche and R. Lidereau (1992). Reply to loss of heterozygosity, chromosome 7q, and breast cancer.Lancet 339:1423–1424.

    PubMed  Google Scholar 

  65. I. U. Ali, R. Lidereau, and R. Callahan (1989). Presence of two members of c-erbA receptor gene family (c-erbAb and c-erbA2) in smallest region of somatic homozygosity on chromosome 3p21-p25 in human breast carcinoma.J. Natl. Cancer Inst. 81:1815–1820.

    PubMed  Google Scholar 

  66. M. Genuardi, H. Tsihira, D. E. Anderson, and G. F. Saunders (1989). Distal deletion of chromosome 1p in ductal carcinoma of the breast:Am. J. Hum. Genet. 45:73–82.

    PubMed  Google Scholar 

  67. P. Devilee, M. Van Den Broek, N. Kulpers-Dukshoorn, R. Kolluri, P. M. Khan, P. L. Pearson, and C. J. Cornelisse (1989). At least four different chromosomal regions are involved in loss of heterozygosity in human breast carcinoma.Genomics 5:554–560.

    PubMed  Google Scholar 

  68. P. Devilee, M. van Vliet, N. Kuipers-Dijkshoorn, P. L. Pearson, and C. J. Cornelisse (1991). Somatic genetic changes on chromosome 18 in breast carcinomas: is the DCC gene involved?Oncogene 6:311–315.

    PubMed  Google Scholar 

  69. S. Thorlacius, O. Jonasdottir, and J. E. Eyfjord (1991). Loss of heterozygosity at selective sites on chromosomes 13 and 17 in human breast carcinoma.Anticancer Res. 11:1501–1507.

    PubMed  Google Scholar 

  70. T. I. Andersen, A. Gaustad, L. Ottestad, G. W. Farrants, J. M. Nesland, K. M. Tveit, and A. L. Borresen (1992). Genetic alterations of the tumor suppressor gene regions 3p, 11p, 13q, 17p, and 17q in human breast carcinomas.Genes, Chromosomes Cancer 4:113–121.

    Google Scholar 

  71. T. Sato, F. Akiyama, G. Sakamoto, F. Kasumi, and Y. Nakamura (1991). Accumulation of genetic alterations and progression of primary breast cancer.Cancer Res. 51:5794–5799.

    PubMed  Google Scholar 

  72. L. C. Chen, K. Matsumara, G. Deng, W. Kurisu, B. M. Ljung, M. Lerman, F. M. Waldman, and H. S. Smith (1994). Deletion of two separate regions on chromosome 3p in breast cancers.Cancer Res. 54:3021–3024.

    PubMed  Google Scholar 

  73. K. Matsumura, A. Kallioniemi, O. Kallioniemi, L. Chen, H. S. Smith, D. Pinkel, J. Gray, and F. M. Waldman (1992). Deletion of chromosome 17p loci in breast cancer cells detected by fluorescencein situ hybridization.Cancer Res. 52:3474–3477.

    PubMed  Google Scholar 

  74. A. Kallioniemi, O. Kallioniemi, F. Waldman, L. Chen, L. Yu, Y. Fung, H. S. Smith, D. Pinkel, and J. Gray (1992). Detection of retinoblastoma gene deletions in metaphase chromosomes and interphase nuclei by fluorescencein situ hybridization.Cytogenet. Cell Genet. 60:190–193.

    PubMed  Google Scholar 

  75. H. S. Smith (1990). Stochastic model for interpreting the data on loss of heterozygosity in breast cancer.JNCI 82:793–794.

    PubMed  Google Scholar 

  76. W. McGuire and S. L. Naylor (1989). Loss of heterozygosity in breast cancer: cause or effect?JNCI 81:1764–1765.

    PubMed  Google Scholar 

  77. I. Ito, M. Yoshimoto, T. Iwase, S. Watanabe, T. Katagiri, Y. Harada, F. Kasumi, S. Yasuda, T. Mitomi, M. Emi, and Y. Nakamura (1995). Association of genetic alterations on chromosome 17 and loss of hormone receptors in breast cancer.Br. J. Cancer 71:438–441.

    PubMed  Google Scholar 

  78. C. S. Cropp, R. Lidereau, G. Campbell, M. H. Champene, and R. Callahan (1990). Loss of heterozygosity on chromosomes 17 and 18 in breast carcinoma: two additional regions identified.PNAS 87:7737–7741.

    PubMed  Google Scholar 

  79. D. M. Radford, K. Fair, A. M. Thompson, J. H. Ritter, M. Holt, T. Steinbrueck, M. Wallace, S. A. Wells, and H. R. Donis-Keller (1993). Allelic loss on chromosome 17 in ductal carcinomain situ of the Breast.Cancer Res. 53:2947–2950.

    PubMed  Google Scholar 

  80. T. I. Andersen, A. Gaustad, and L. Ottestad (1992). Genetic alterations of the tumor suppressor gene regions 3p, 11p, 13q, 17p, and 17q in human breast carcinomas.Genes Chromosomes Cancer 4:113–121.

    PubMed  Google Scholar 

  81. J. Koreth, P. B. Bethwaite, and J. O'D. McGee (1995). Mutation at chromosome 11q23 in human non-familial breast cancer: a microdissection microsatellite analysis.J. Pathol. 176:11–18.

    PubMed  Google Scholar 

  82. R. J. Osborne, G. R. Merlo, T. Mitsudomi, T. Venesio, D. S. Liscia, A. P. M. Cappa, I. Chiba, T. Takahashi, M. M. Nau, R. Callahan, and J. D. Minna (1991). Mutations in the p53 gene in primary human breast cancers.Cancer Res. 51:6194–6198.

    PubMed  Google Scholar 

  83. D. M. Barnes and R. S. Camplejohn (1996). P53, apoptosis and breast cancer.J. Mam. Gland Biol. Neoplasia 1:(2)163–175.

    Google Scholar 

  84. R. Bookstein and W.-H. Lee (1991). Molecular genetics of the retinoblastoma suppressor gene.Crit. Rev. Oncol. 2:211–227.

    Google Scholar 

  85. J. M. Varley, J. Armour, J. E. Swallow, A. J. Jeffreys, B. A. J. Ponder, A. T'Ang, Y. K. T. Fung, W. J. Brammar, and R. A. Walker (1989). The retinoblastoma gene is frequently altered leading to loss of expression in primary breast tumors.Oncogene 4:725–729.

    Google Scholar 

  86. A. Borg, Q. X. Zhang, P. Alm, H. Olsson, and G. Sellberg (1992). The retinoblastoma gene in breast cancer: allele loss is not correlated with loss of gene protein expression.Cancer Res. 52:2991–2994.

    PubMed  Google Scholar 

  87. J. Geradts, S-X. Hu, C. E. Lincoln, W. F. Benedict, and H-J. Xu (1994). Aberrant RB gene expression in routinely processed, archival tumor tissues determined by three different anti-RB antibodies.Int. J. Cancer 58:161–167.

    PubMed  Google Scholar 

  88. T. Pietilainen, P. Lipponen, S. Aaltomaa, M. Eskelinen, V-M. Kosma, and K. Syrjanen (1995). Expression of retinoblastoma gene protein (RB) in breast cancer as related to established prognostic factors and survival.Eur. J. Cancer 31A:329–333.

    PubMed  Google Scholar 

  89. D. R. Schott, J. N. Chang, G. Deng, W. Kurisu, W-L. Kuo, J. Gray, and H. S. Smith (1994). A candidate tumor suppressor gene in human breast cancers.Cancer Res. 54:1393–1396.

    PubMed  Google Scholar 

  90. P. A. Futreal, Q. Liu, D. Shattuck-Eidens, C. Cochran, K. Harshman, S. Tavtigian, L. M. Bennett, A. Haugen-Strano, J. Swensen, Y. Miki, K. Eddington, M. McClure, C. Frye, J. Weaver-Feldhaus, W. Ding, Z. Gholami, P. Söderkvist, L. Terry, S. Jhanwar, A. Berchuck, J. D. Iglehart, J. Marks, D. G. Ballinger, J. C. Barrett, M. H. Skolnick, A. Kamb, and R. Wiseman (1994).BRCA1 mutations in primary breast and ovarian carcinomas.Science 266:120–122.

    PubMed  Google Scholar 

  91. Y. Chen, C-F. Chen, D. J. Riley, C. Allred, P-L. Chen, D. Von Hoff, C. K. Osborne, and W-H. Lee (1995). Aberrant subcellular localization ofBRCA1 in breast cancer.Science 270:789–791.

    PubMed  Google Scholar 

  92. R. Wooster, S. L. Neuhausen, J. Mangion, Y. Quirk, D. Ford, N. Collins, K. Nguyen, S. Seal, T. Tran, D. Averill, P. Fields, G. Marshall, S. Narod, G. M. Lenoir, H. Lynch, J. Feunteun, P. Devilee, C. J. Cornelisse, F. H. Menko, P. A. Daly, W. Ormiston, R. McManus, C. Pye, C. M. Lewis, L. A. Cannon-Albright, J. Peto, B. A. J. Ponder, M. H. Skolnick, D. F. Easton, D. E. Goldgar, and M. R. Stratton (1994). Localization of a breast cancer susceptibility gene,BRCA2, to chromosome 13q12–13.Science 265:2088–2092.

    PubMed  Google Scholar 

  93. J. E. Garber, A. M. Goldstein, A. F. Kantor, M. G. Dreyfus, J. F. Fraumeni, Jr., and F. P. Li (1991). Follow-up study of twenty-four families with Li-Fraumeni syndrome.Cancer Res. 51:6094–6097.

    PubMed  Google Scholar 

  94. D. Malkin, F. P. Li, L. C. Strong, J. F. Fraumeni, Jr., C. E. Nelson, D. H. Kim, J. Kassel, M. A. Gryka, F. Z. Bischoff, and M. A. Tainsky (1990). Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms.Science 250:1233–1238.

    PubMed  Google Scholar 

  95. D. Sidransky, T. Tokino, K. Helzlsouer, B. Zehnbauer, G. Rausch, B. Shelton, L. Prestigiacomo, B. Vogelstein, and N. Davidson (1992). Inherited p53 gene mutations in breast cancer.Cancer Res. 52:2984–2986.

    PubMed  Google Scholar 

  96. M. Swift, P. Reitnauer, D. Morrell, and C. Chase (1987). Breast and other cancers in families with ataxia-telanguctasia.The New Engl. J. Med. 316:1289–1294.

    Google Scholar 

  97. Z. Zou, A. Anisowicz, M. J. Hendrix, A. Thor, M. Neveu, S. Sheng, K. Rafidi, E. Seftor, and R. Sager (1994). Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells.Science 263:526–529.

    PubMed  Google Scholar 

  98. P. A. Pemberton, D. T. Wong, H. L. Gibson, M. C. Kiefer, P. A. Fitzpatrick, R. Sager, and P. J. Barr (1995). The tumor suppressor maspin does not undergo the stressed to relaxed transition orinhibit trpsin-like serine proteases. Evidence that maspin is not a protease inhibitory serpin.J. Biol. Chem. 270:15832–15837.

    PubMed  Google Scholar 

  99. A. Leone, O. W. McBride, A. Weston, M. G. Wang, P. Anglard, C. S. Cropp, J. R. Goepel, R. Lidereau, R. Callahan, W. M. Linehan, R. C. Rees, C. C. Harris, L. A. Liotta, and P. S. Steeg (1991). Somatic allelic deletion ofnm23-H1 in human cancer.Cancer Res. 51:2490–2493.

    PubMed  Google Scholar 

  100. J. A. Stahl, A. Leone, A. M. Rosengard, L. Potter, C. R. King, and P. S. Steeg (1991). Identification of a second humannm23 gene,nm23-H2.Cancer Res. 51:445–449.

    PubMed  Google Scholar 

  101. A. Gilles, E. Presecan, A. Vonica, and I. Lascu (1991). Nucleoside diphosphate kinase from human erythrocytes.J. Biol. Chem. 266:8784–8789.

    PubMed  Google Scholar 

  102. P. S. Steeg, A. De La Rosa, U. Flatow, N. J. MacDonald, M. Benedict, and A. Leone (1993).Nm23 and breast cancer metastasis.Br. Cancer Res. Treat. 25:175–187.

    Google Scholar 

  103. G. Bevilacqua, M. E. Sobel, L. A. Liotta, and P. S. Steeg (1989). Association of lownm23 RNA levels in human primary infiltrating ductal breast carcinomas with lymph node involvement and other histopathological indicators of high metastatic potential.Cancer Res. 49:5185–5190.

    PubMed  Google Scholar 

  104. R. Barnes, S. Masood, E. Barker, A. M. Rosengard, D. L. Coggin, T. Crowell, C. R. King, K. Porter-Jordan, E. S. Wargotz, L. A. Liotta, and P. S. Steeg (1991). Lownm23 protein expression in infiltrating ductal breast carcinomas correlates with reduced patient survival.Am. J. Pathol. 139:245–250.

    PubMed  Google Scholar 

  105. C. Hennessy, J. A. Henry, F. E. B. May, B. R. Westley, B. Angus, and T. W. J. Lennard (1991). Expression of antimetastatic genenm23.Br. J. Cancer 63:1024.

    PubMed  Google Scholar 

  106. R. J. Goodall, H. J. Dawkins, P. D. Robbins, E. Hahnel, M. Sarna, R. Hahnel, J. M. Papadimitriou, J. M. Harvey, and G. F. Sterrett (1994). Evaluation of the expression levels ofnm23-H1 mRNA in primary breast cancer, benign breast disease, axillary lymph nodes and normal breast tissue.Pathology 26:423–428.

    PubMed  Google Scholar 

  107. A. Sawan, I. Lascu, M. Veron, J. J. Anderson, C. Wright, C. H. Horne, and B. Angus (1994). NDP-K/nm23 expression in human breast cancer in relation to relapse, survival and other prognostic factors: an immunohistochemical study.J. Pathol. 172:27–34.

    PubMed  Google Scholar 

  108. S. W. Lee, C. Tomasettio, and R. Sager (1991). Positive selection of candidate tumor-suppressor genes by subtractive hybridization.PNAS 88:2825–2829.

    PubMed  Google Scholar 

  109. L. C. Chen, J. P. O'Bryan, H. S. Smith, and E. Liu (1990). Overexpression of matrix Gla protein mRNA in malignant human breast cells: isolation by differential cDNA hybridization.Oncogene 5:1391–1395.

    PubMed  Google Scholar 

  110. P. Yaswen, A. Smoll, J. Hosoda, G. Parry, and M. R. Stampfer (1992). Protein product of a human intronless calmodulin-like gene shows tissue-specific expression and reduced abundance in transformed cells.Cell Growth Diff. 3:335–345.

    PubMed  Google Scholar 

  111. H. B. Muss, A. Thor, D. A. Berry, T. M. Kute, E. T. Liu, F. Koemer, C. T. Ciirrincione, D. R. Budman, W. C. Wood, M. Barcos, and I. C. Henderson (1994). c-erbB-2 expression and s-phase activity predict response to adjuvant therapy in women with node positive early breast cancer. A Comparison Study of the Cancer and Acute Leukemia Group B.New Engl. J. Med. 330:1260–1266.

    PubMed  Google Scholar 

  112. K. Smith, S. Houlbrook, M. Greenall, J. Carmichael, and A. L. Harris (1993). Topoisomerase I alpha co-amplification witherbB-2 in human primary breast cancer and breast cancer cell lines: relationship to m-AMSA and mitoxantrone sensitivity.Oncogene 8:933–938.

    PubMed  Google Scholar 

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Correspondence to Helene S. Smith.

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Dairkee, S.H., Smith, H.S. Genetic analysis of breast cancer progression. J Mammary Gland Biol Neoplasia 1, 139–151 (1996). https://doi.org/10.1007/BF02013638

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