Breast cancer metastasis: Markers and models

Nature Reviews Cancer

Volumn 5, Issue 8, 2005, Pages 591-602

  Weigelt, Britta ^a   Peterse, Johannes L ^a   Van't Veer, Laura J ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR 2; PLASMINOGEN ACTIVATOR INHIBITOR 1; PLASMINOGEN ACTIVATOR INHIBITOR 2; STEROID RECEPTOR; UROKINASE RECEPTOR;

ADRENAL METASTASIS; AXILLARY LYMPH NODE; BONE METASTASIS; BRAIN METASTASIS; BREAST CANCER; CANCER GRADING; CANCER INVASION; CANCER MORTALITY; CANCER RELAPSE; CANCER RISK; CANCER SURVIVAL; CARCINOGENESIS; CLINICAL FEATURE; CYTOTOXICITY; DISEASE MARKER; DNA MICROARRAY; GENE AMPLIFICATION; GENE EXPRESSION; HEART METASTASIS; HISTOPATHOLOGY; HUMAN; KIDNEY METASTASIS; LIVER METASTASIS; LUNG METASTASIS; LYMPH NODE METASTASIS; METASTASIS; NONHUMAN; OVARY METASTASIS; PERITONEUM METASTASIS; PHENOTYPE; PLEURA METASTASIS; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; REVIEW; SKIN METASTASIS; TUMOR EMBOLISM; TUMOR VOLUME; VISCERAL METASTASIS;

BREAST NEOPLASMS; FEMALE; HUMANS; MODELS, ANIMAL; NEOPLASM METASTASIS; TUMOR MARKERS, BIOLOGICAL;

EID: 23144442644     PISSN: 1474175X     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrc1670     Document Type: Review

References (106)

1. Early Breast Cancer Trialists' Collaborative Group (EBCTCG). Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365, 1687-1717 (2005). Gives an overview of the results of 194 randomized trials of adjuvant chemotherapy or hormonal therapy among women with early breast cancer.
2. Eifel, P. et al. National Institutes of Health Consensus Development Conference Statement: adjuvant therapy for breast cancer, November 1-3, 2000. J. Natl Cancer Inst. 93, 979-989 (2001). Provides an assessment of available data between January 1995 and July 2000 regarding the use of adjuvant therapy for breast cancer.
3. Fidler, I. J. & Kripke, M. L. Metastasis results from preexisting variant cells within a malignant tumour. Science 197, 893-895 (1977). The experimental data establish the longstanding model of metastasis, which indicates that metastatic cells are rare and arise late during tumorigenesis.
4. Milas, L., Peters, L. J. & Ito, H. Spontaneous metastasis: random or selective? Clin. Exp. Metastasis 1, 309-315 (1983).
5. Giavazzi, R., Alessandri, G., Spreafico, F., Garattini, S. & Mantovani, A. Metastasizing capacity of tumour cells from spontaneous metastases of transplanted murine tumours. Br. J. Cancer 42, 462-472 (1980).
6. Mantovani, A., Giavazzi, R., Alessandri, G., Spreafico, F. & Garattini, S. Characterization of tumour lines derived from spontaneous metastases of a transplanted murine sarcoma. Eur. J. Cancer 17, 71-76 (1981).
7. van't Veer, L. J. et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415, 530-536 (2002). Shows that a 70-gene expression profile of primary breast tumours can predict the later appearance or absence of distant metastases.
8. van de Vijver, M. J. et al. A gene-expression signature as a predictor of survival in breast cancer. N. Engl. J. Med. 347, 1999-2009 (2002).
9. Ramaswamy, S., Ross, K. N., Lander, E. S. & Golub, T. R. A molecular signature of metastasis in primary solid tumours. Nature Genet. 33, 49-54 (2003).
10. Bernards, R. & Weinberg, R. A. A progression puzzle. Nature 418, 823 (2002).
11. Hellman, S. & Harris, J. R. in Diseases of the Breast (eds Harris, J. R., Lippman, M. E., Morrow, M. & Osborne, C. K.), 407-423 (Lippincott Williams & Wilkins, Philadelphia, 2000). Describes the clinical behaviour of untreated breast cancer, including the incidences of regional lymph-node and distant metastasis.
12. Tavassoli, F. A. & Devilee, P. (eds) World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of the Breast and Female Genital Organs. (IARC press, Lyon, 2003).
13. Lee, Y. T. Breast carcinoma: pattern of metastasis at autopsy. J. Surg. Oncol. 23, 175-180 (1983).
14. Page, D. L. Prognosis and breast cancer. Recognition of lethal and favourable prognostic types. Am. J. Surg. Pathol. 15, 334-349 (1991).
15. Koscielny, S. et al. Breast cancer: relationship between the size of the primary tumour and the probability of metastatic dissemination. Br. J. Cancer 49, 709-715 (1984).
16. Rosen, P. P., Groshen, S., Saigo, P. E., Kinne, D. W. & Hellman, S. Pathological prognostic factors in stage I (T1N0M0) and stage II (T1N1M0) breast carcinoma: a study of 644 patients with median follow-up of 18 years. J. Clin. Oncol. 7, 1239-1251 (1989).
17. Carter, C. L., Allen, C. & Henson, D. E. Relation of tumour size, lymph node status, and survival in 24,740 breast cancer cases. Cancer 63, 181-187 (1989).
18. Elston, C. W. & Ellis, I. O. 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. Histopathology 19, 403-410 (1991).
19. Pinder, S. E. et al. Pathological prognostic factors in breast cancer. III. Vascular invasion: relationship with recurrence and survival in a large study with long-term follow-up. Histopathology 24, 41-47 (1994).
20. de Mascarel, I. et al. Obvious peritumoural emboli: an elusive prognostic factor reappraised. Multivariate analysis of 1320 node-negative breast cancers. Eur. J. Cancer 34, 58-65 (1998).
21. Hellman, S. Karnofsky Memorial Lecture. Natural history of small breast cancers. J. Clin. Oncol. 12, 2229-2234 (1994).
22. James, J. J. et al. Bone metastases from breast carcinoma: histopathological-radiological correlations and prognostic features. Br. J. Cancer 89, 660-665 (2003).
23. Borst, M. J. & Ingold, J. A. Metastatic patterns of invasive lobular versus invasive ductal carcinoma of the breast. Surgery 114, 637-641 (1993).
24. Arpino, G., Bardou, V. J., Clark, G. M. & Elledge, R. M. Infiltrating lobular carcinoma of the breast: tumour characteristics and clinical outcome. Breast Cancer Res. 6, R149-R156 (2004).
25. McGuire, W. L. & Clark, G. M. Prognostic factors and treatment decisions in axillary-node-negative breast cancer. N. Engl. J. Med. 326, 1756-1761 (1992).
26. Hayes, D. F. et al. Tumour marker utility grading system: a framework to evaluate clinical utility of tumour markers. J. Natl Cancer Inst. 88, 1456-1466 (1996).
27. Ransohoff, D. F. Bias as a threat to the validity of cancer molecular-marker research. Nature Rev. Cancer 5, 142-149 (2005).
28. Slamon, D. J. et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235, 177-182 (1987).
29. Slamon, D. J. et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N. Engl. J. Med. 344, 783-792 (2001).
30. Ross, J. S. et al. The Her-2/neu gene and protein in breast cancer 2003: biomarker and target of therapy. Oncologist 8, 307-325 (2003).
31. Yamauchi, H., Stearns, V. & Hayes, D. F. When is a tumour marker ready for prime time? A case study of c-erbB-2 as a predictive factor in breast cancer. J. Clin. Oncol. 19, 2334-2356 (2001).
32. Ross, J. S. et al. Targeted therapy in breast cancer: the HER-2/neu gene and protein. Mol. Cell Proteomics 3, 379-398 (2004).
33. Dvorak, H. F. Tumours: wounds that do not heal. Similarities between tumour stroma generation and wound healing. N. Engl. J. Med. 315, 1650-1659 (1986).
34. Ring, A., Smith, I. E. & Dowsett, M. Circulating tumour cells in breast cancer. Lancet Oncol. 5, 79-88 (2004).
35. Stathopoulou, A. et al. Molecular detection of cytokeratin-19-positive cells in the peripheral blood of patients with operable breast cancer: evaluation of their prognostic significance. J. Clin. Oncol. 20, 3404-3412 (2002).
36. Zach, O., Kasparu, H., Wagner, H., Krieger, O. & Lutz, D. Prognostic value of tumour cell detection in peripheral blood of breast cancer patients. Acta Med. Austriaca 59, 32-34 (2002).
37. Pierga, J. Y. et al. Clinical significance of immunocytochemical detection of tumour cells using digital microscopy in peripheral blood and bone marrow of breast cancer patients. Clin. Cancer Res. 10, 1392-1400 (2004).
38. Diel, I. J. et al. Micrometastatic breast cancer cells in bone marrow at primary surgery: prognostic value in comparison with nodal status. J. Natl Cancer Inst. 88, 1652-1658 (1996).
39. Landys, K., Persson, S., Kovarik, J., Hultborn, R. & Holmberg, E. Prognostic value of bone marrow biopsy in operable breast cancer patients at the time of initial diagnosis: results of a 20-year median follow-up. Breast Cancer Res. Treat. 49, 27-33 (1998).
40. Braun, S. et al. Cytokeratin-positive cells in the bone marrow and survival of patients with stage I, II, or III breast cancer. N. Engl. J. Med. 342, 525-533 (2000).
41. Wiedswang, G. et al. Detection of isolated tumour cells in bone marrow is an independent prognostic factor in breast cancer. J. Clin. Oncol. 21, 3469-3478 (2003).
42. Molino, A. et al. Bone marrow micrometastases in 109 breast cancer patients: correlations with clinical and pathological features and prognosis. Breast Cancer Res. Treat. 42, 23-30 (1997).
43. Ismail, M. S. et al. Detection of micrometastatic disease and monitoring of perioperative tumour cell dissemination in primary operable breast cancer patients using real-time quantitative reverse transcription-PCR. Clin. Cancer Res. 10, 196-201 (2004).
44. Gebauer, G., Fehm, T., Merkle, E., Jaeger, W. & Mitze, M. Micrometastases in axillary lymph nodes and bone marrow of lymph node-negative breast cancer patients - prognostic relevance after 10 years. Anticancer Res. 23, 4319-4324 (2003).
45. Funke, I. & Schraut, W. Meta-analyses of studies on bone marrow micrometastases: an independent prognostic impact remains to be substantiated. J. Clin. Oncol. 16, 557-566 (1998).
46. Fidler, I. J. Metastasis: quantitative analysis of distribution and fate of tumour embolilabeled with 125 I-5-iodo-2′-deoxyuridine. J. Natl Cancer Inst. 45, 773-782 (1970).
47. Gangnus, R., Langer, S., Breit, E., Pantel, K. & Speicher, M. R. Genomic profiling of viable and proliferate micrometastatic cells from early-stage breast cancer patients. Clin. Cancer Res. 10, 3457-3464 (2004).
48. Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J. & Clarke, M. F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100, 3983-3988 (2003). Describes the prospective isolation of candidate breast tumour stem cells and their ability to form tumours in mice.
49. Gudjonsson, T. et al. Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties. Genes Dev. 16, 693-706 (2002).
50. Clarke, R. B. et al. A putative human breast stem cell population is enriched for steroid receptor-positive cells. Dev. Biol. 277, 443-456 (2005).
51. Andreasen, P. A., Kjoller, L., Christensen, L. & Duffy, M. J. The urokinase-type plasminogen activator system in cancer metastasis: a review. Int. J. Cancer 72, 1-22 (1997).
52. Umeda, T., Eguchi, Y., Okino, K., Kodama, M. & Hattori, T. Cellular localization of urokinase-type plasminogen activator, its inhibitors, and their mRNAs in breast cancer tissues. J. Pathol. 183, 388-397 (1997).
53. Janicke, F., Schmitt, M. & Graeff, H. Clinical relevance of the urokinase-type and tissue-type plasminogen activators and of their type 1 inhibitor in breast cancer. Semin. Thromb. Hemost. 17, 303-312 (1991).
54. Bajou, K. et al. Host-derived plasminogen activator inhibitor-1 (PAI-1) concentration is critical for in vivo tumoural angiogenesis and growth. Oncogene 23, 6986-6990 (2004).
55. Foekens, J. A. et al. The urokinase system of plasminogen activation and prognosis in 2780 breast cancer patients. Cancer Res. 60, 636-643 (2000).
56. Konecny, G. et al. Her-2/neu and urokinase-type plasminogen activator and its inhibitor in breast cancer. Clin. Cancer Res. 7, 2448-2457 (2001).
57. Janicke, F. et al. Randomized adjuvant chemotherapy trial in high-risk, lymph node-negative breast cancer patients identified by urokinase-type plasminogen activator and plasminogen activator inhibitor type 1. J. Natl Cancer Inst. 93, 913-920 (2001).
58. Harbeck, N., Kates, R. E. & Schmitt, M. Clinical relevance of invasion factors urokinase-type plasminogen activator and plasminogen activator inhibitor type 1 for individualized therapy decisions in primary breast cancer is greatest when used in combination. J. Clin. Oncol. 20, 1000-1007 (2002).
59. Look, M. P. et al. 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 (2002). Confirms the prognostic value of uPA and PAI1 in primary breast cancer in a re-analysis of independent patient data provided by the members of the EORTC Receptor and Biomarker Group.
60. Harbeck, N. et al. Enhanced benefit from adjuvant chemotherapy in breast cancer patients classified high-risk according to urokinase-type plasminogen activator (uPA) and plasminogen activator inhibitor type 1 (n = 3424). Cancer Res. 62, 4617-4622 (2002).
61. Perou, C. M. et al. Molecular portraits of human breast tumours. Nature 406, 747-752 (2000). Classifies primary breast tumours into 5 subtypes on the basis of similarities in their gene-expression patterns.
62. Sorlie, T. et al. Gene expression patterns of breast carcinomas distinguish tumour subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98, 10869-10874 (2001).
63. Sorlie, T. et al. Repeated observation of breast tumour subtypes in independent gene expression data sets. Proc. Natl Acad. Sci. USA 100, 8418-8423 (2003).
64. Egeblad, M. & Werb, Z. New functions for the matrix metalloproteinases in cancer progression. Nature Rev. Cancer 2, 161-174 (2002).
65. Goldhirsch, A., Glick, J. H., Gelber, R. D., Coates, A. S. & Senn, H. J. Meeting highlights: international consensus panel on the treatment of primary breast cancer. Seventh international conference on adjuvant therapy of primary breast cancer. J. Clin. Oncol. 19, 3817-3827 (2001).
66. Tuma, R. S. A big trial for a new technology: TransBIG project takes microarrays into clinical trials. J. Natl Cancer Inst. 96, 648-689 (2004).
67. Wang, Y. et al. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365, 671-679 (2005).
68. Tan, P. K. et al. Evaluation of gene expression measurements from commercial microarray platforms. Nucleic Acids Res. 31, 5676-5684 (2003).
69. Huang, E. et al. Gene expression predictors of breast cancer outcomes. Lancet 361, 1590-1596 (2003).
70. Ma, X. J. et al. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell 5, 607-616 (2004).
71. Paik, S. et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N. Engl. J. Med. 351, 2817-2826 (2004).
72. Esteva, F. J. et al. Prognostic role of a multigene reverse transcriptase-PCR assay in patients with node-negative breast cancer not receiving adjuvant systemic therapy. Clin. Cancer Res. 11, 3315-3319 (2005).
73. Kang, Y. et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549 (2003).
74. Minn, A. J. et al. Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumours. J. Clin. Invest. 115, 44-55 (2005). Shows that organ-specific metastasis of a breast cancer cell line is determined by the poor-prognosis signature and an additional metastasis-specific gene set.
75. Chang, H. Y. et al. Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumours and wounds. PLoS Biol. 2, E7 (2004).
76. Chang, H. Y. et al. Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival. Proc. Natl Acad. Sci. USA 102, 3738-3743 (2005).
77. Ein-Dor, L., Kela, I., Getz, G., Givol, D. & Domany, E. Outcome signature genes in breast cancer: is there a unique set? Bioinformatics 21, 171-178 (2005).
78. Fidler, I. J. Selection of successive tumour lines for metastasis. Nature New Biol. 242, 148-149 (1973).
79. Leighton, J. Inherent malignancy of cancer cells possibly limited by genetically differing cells in the same tumour. Acta Cytol. 9, 138-140 (1965).
80. Stackpole, C. W. Distinct lung-colonizing and lung-metastasizing cell populations in B16 mouse melanoma. Nature 289, 798-800 (1981).
81. Vaage, J. Metastasizing potentials of mouse mammary tumours and their metastases. Int. J. Cancer 41, 855-858 (1988).
82. Eccles, S. A., Heckford, S. E. & Alexander, P. Effect of cyclosporin A on the growth and spontaneous metastasis of syngeneic animal tumours. Br. J. Cancer 42, 252-259 (1980).
83. Weiss, L., Holmes, J. C. & Ward, P. M. Do metastases arise from pre-existing subpopulations of cancer cells? Br. J. Cancer 47, 81-89 (1983).
84. Hill, R. P., Chambers, A. F., Ling, V. & Harris, J. F. Dynamic heterogeneity: rapid generation of metastatic variants in mouse B16 melanoma cells. Science 224, 998-1001 (1984).
85. Ling, V., Chambers, A. F., Harris, J. F. & Hill, R. P. Quantitative genetic analysis of tumour progression. Cancer Metastasis Rev. 4, 173-192 (1985).
86. Kerbel, R. S., Waghorne, C., Man, M. S., Elliott, B. & Breitman, M. L. Alteration of the tumorigenic and metastatic properties of neoplastic cells is associated with the process of calcium phosphate-mediated DNA transfection. Proc. Natl Acad. Sci. USA 84, 1263-1267 (1987).
87. Kerbel, R. S., Waghorne, C., Korczak, B., Lagarde, A. & Breitman, M. L. Clonal dominance of primary tumours by metastatic cells: genetic analysis and biological implications. Cancer Surv. 7, 597-629 (1988).
88. Garcia-Olmo, D., Garcia-Olmo, D. C., Ontanon, J., Martinez, E. & Vallejo, M. Tumour DNA circulating in the plasma might play a role in metastasis. The hypothesis of the genometastasis. Histol. Histopathol. 14, 1159-1164 (1999).
89. Garcia-Olmo, D. & Garcia-Olmo, D. C. Functionality of circulating DNA: the hypothesis of genometastasis. Ann. NY Acad. Sci. 945, 265-275 (2001).
90. Lancaster, M., Rouse, J. & Hunter, K. W. Modifiers of mammary tumour progression and metastasis on mouse chromosomes 7, 9, and 17. Mamm. Genome 16, 120-126 (2005).
91. Bissell, M. J. & Radisky, D. Putting tumours in context. Nature Rev. Cancer 1, 46-54 (2001).
92. Bhowmick, N. A., Neilson, E. G. & Moses, H. L. Stromal fibroblasts in cancer initiation and progression. Nature 432, 332-337 (2004).
93. Weigelt, B. et al. Gene expression profiles of primary breast tumours maintained in distant metastases. Proc. Natl Acad. Sci. USA 100, 15901-15905 (2003).
94. Ma, X. J. et al. Gene expression profiles of human breast cancer progression. Proc. Natl Acad. Sci. USA 100, 5974-5979 (2003).
95. Schmidt-Kittler, O. et al. From latent disseminated cells to overt metastasis: genetic analysis of systemic breast cancer progression. Proc. Natl Acad. Sci. USA 100, 7737-7742 (2003).
96. Reya, T., Morrison, S. J., Clarke, M. F. & Weissman, I. L. Stem cells, cancer, and cancer stem cells. Nature 414, 105-111 (2001).
97. Singh, S. K. et al. Identification of human brain tumour initiating cells. Nature 432, 396-401 (2004).
98. Bissell, M. J. & Labarge, M. A. Context, tissue plasticity, and cancer; are tumour stem cells also regulated by the microenvironment? Cancer Cell 7, 17-23 (2005).
99. Dontu, G., El-Ashry, D. & Wicha, M. S. Breast cancer, stem/progenitor cells and the estrogen receptor. Trends Endocrinol. Metab. 15, 193-197 (2004).
100. Chang, J. C. et al. Gene expression profiling for the prediction of therapeutic response to docetaxel in patients with breast cancer. Lancet 362, 362-369 (2003).
101. Ayers, M. et al. Gene expression profiles predict complete pathologic response to neoadjuvant paclitaxel and fluorouracil, doxorubicin, and cyclophosphamide chemotherapy in breast cancer. J. Clin. Oncol. 22, 2284-2293 (2004).
102. Quackenbush, J. Computational analysis of microarray data. Nature Rev. Genet. 2, 418-427 (2001).
103. Eisen, M. B., Spellman, P. T., Brown, P. O. & Botstein, D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl Acad. Sci. USA 95, 14863-14868 (1998).
104. Golub, T. R. et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286, 531-537 (1999).
105. Al-Hajj, M. & Clarke, M. F. Self-renewal and solid tumour stem cells Oncogene 23, 7274-7282 (2004).
106. Van't Veer, L. J., Weigelt, B. Road map to metastasis. Nature Med. 9, 999-1000 (2003).