Skip to main content

Advertisement

SpringerLink
Log in

Molecular pathology of tumor metastasis

I. Predictive pathology

  • Seminar
  • Published:
Pathology Oncology Research

Abstract

Millenium reviews of oncology agreed that the last century produced major developments mainly in the management of the primary tumor, but despite all of these results, cancer still remains among the leading causes of death due to the failure of clinical management of disseminated disease. This failure is primarily due to the lack of detailed information on the molecular mechanisms of tumor metastasis. Therefore, one of the hottest fields in experimental oncology is metastasis research, which provides more and more information about the molecular mechanisms. However, this information is fragmented and is not yet exploited in clinical practice. A new field of diagnostic pathology recently emerged, which translates basic research data to diagnostic practice to provide clinically relevant information on the biological potential (in this case metastatic potential) of the malignant tumors. Since tumor cell-extracellular matrix interactions are key features of tumor dissemination, expression of genes responsible for them can define the metastatic potential of malignant tumors. This review summarizes our recent knowledge on the metastatic geno-and phenotype of major human solid tumors: lung, colon, breast, prostate cancers and malignant melanoma.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Adachi M, Taki T, Haung C, et al; Reduced integrin alpha3 expression as a factor of poor prognosis of patients with adenocarcinoma of the lung. J Clin Oncol 16:1060–1067, 1998.

    PubMed  CAS  Google Scholar 

  2. Balch ChM, Reintgen DS, Kirkwood JM, et al: Cutaneous melanoma. In: (DeVita, VT, Hellman S, Rosenberg SA (eds)): Principles & Practice of Oncology, Fifth Edition, Lippincott-Raven Publ. Philadelphia, Vol.1. 1947–94, 1997.

    Google Scholar 

  3. Bánkfalvi A, Terpe HJ, Breukelmann D et al; Gains and losses of CD44 expression during breast carcinogenesis and tumour progression. Histopathology 33:107–116, 1998.

    Article  PubMed  Google Scholar 

  4. Barnes DM, Gillett CE; Cyclin D1 in breast cancer. Breast Cancer Res Treat 52:1–15, 1998.

    Article  PubMed  CAS  Google Scholar 

  5. Bellahcene A, Albert V, Pollina L, et al; Ectopic expression of bone sialoprotein in human tyroid cancer. Thyroid 8:637–641, 1998.

    Article  PubMed  CAS  Google Scholar 

  6. Bishop NJA; Molecular pathology of melanoma. Cancer Metast Rev 16:141–154, 1997.

    Article  Google Scholar 

  7. Caputi M, Greoger AM, Esposito Y et al; Prognostic role of cyclin D1 in lung cancer. Relationship to proliferating cell nuclear antigen. Am J Respir Cell Mol Biol. 20:746–750, 1999.

    PubMed  CAS  Google Scholar 

  8. Chana JS, Wilson GD, Cree IA et al: c-myc, p53, and Bcl-2 expression and clinical outcome in uveal melanoma. Br J Ophthalmol 83:110–114, 1999.

    Article  PubMed  CAS  Google Scholar 

  9. Clezardin P; Recent insights into the role of integrins in cancer metastasis. CMLS Cell. Mol Life Sci 53:5412–548, 1998.

    Google Scholar 

  10. Cochran A, Bailly Ch, Paul E, et al: Characteristics that relate to prognosis. In: (Cochran AJ, Bailly Ch, Paul E, Remotti F, Bhuta S (Eds.): Melanocytic tumors. A guide to diagnosis. Lippincott-Raven Publishers, Philadelphia, New York, pp. 261–286, 1997.

    Google Scholar 

  11. Cohen AM, Minsky BR, Schilsky RI: Cancer of the colon. In: (De Vita VT, Hellman S, Rosenberg, SA (eds)): Principles Practice of Oncology, Fifth Edition, Lippincott-Raven Publ. Philadelphia, Vol.1. 1144–1162, 1997.

    Google Scholar 

  12. Coppola D, Hyacinthe H, Fu L, et al; CD44V6 expression in human colorectal carcinoma. Hum Pathol 29:627–635, 1998.

    Article  PubMed  CAS  Google Scholar 

  13. Cox LA, Chen G, Le EY; Tumor suppressor genes and their role in breast cancer. Breast Cancer Res Treat 32:19–38, 1994.

    Article  PubMed  CAS  Google Scholar 

  14. D’Amico TA, Masse M, Herndon JE et al; A biologic risk model for stage I lung cancer: immunohistochemical analysis of 408 patients with the use of ten molecular markers. J Thorac Cardiovasc Surg 117:736–743, 1999.

    Article  PubMed  CAS  Google Scholar 

  15. De Wit PEJ, Van Muijen GNP, De Wall; Pathology of malignant melanoma, including new markers and techniques in diagnosis and prognosis. Curr Op Oncol 8:143–151, 1996.

    Article  Google Scholar 

  16. Döme B, Somlai B, Ladányi A, et al. Expression of CD44v3 splice variant is associated with the visceral metastatic phenotype of human melanoma. Virchows Arch (in press)

  17. Dong JT, Rinker-Schaeffer CW, Ichikawa T, et al; Prostate cancer-biology of metastasis and its clinical implications. World J Urol 14:182–189, 1996.

    Article  PubMed  CAS  Google Scholar 

  18. Duffy MJ; Proteases as prognostic markers in cancer. Clin Cancer Res 2:613–618, 1996.

    PubMed  CAS  Google Scholar 

  19. Ewing J: Neoplatic diseases. WB Saunders, Philadelphia, 1928, 1928.

    Google Scholar 

  20. Fazekas K, Csuka O, Köves I, et al.; Experimental and clinicopathological studies on the function of the HGF receptor in human colon cancer metastasis. Clin Exp Metast 2001 (in press)

  21. Fidler IJ: Molecular Biology of Cancer: Invasion and Metastasis. Cancer In: (DeVita VT, Hellman S, Rosenberg SA (eds)): Principles & Practice of Oncology, Fifth Edition, Lippincott-Raven Publ. Philadelphia, 1:135–152, 1997.

    Google Scholar 

  22. Fidler IJ, Radinsky R; Search for genes that suppress cancer metastasis. J Natl Cancer Inst 88:1700–1703, 1996.

    Article  PubMed  CAS  Google Scholar 

  23. Fleisch H: Osteolytic tumor bone disease In: Felisch H (ed): Bisphosphonates in bone disease. The Parthenon Publishing Group, New York, London, pp. 86–106, 1997.

    Google Scholar 

  24. Foekens JA, Dall P, Klijn JG, et al; Prognostic value of CD44 variant expression in primary breast cancer. Int J Cancer 84:209–215, 1999.

    Article  PubMed  CAS  Google Scholar 

  25. Folkman J; How is blood vessel growth regulated in normal and neoplastic tissue? Cancer Res 46:467–477, 1986.

    PubMed  CAS  Google Scholar 

  26. Fredersdorf S, Burns J, Milne AM, et al; High level expression of p27(kip1) and cyclin D1 in some human breast cancer cells: inverse correlation between the expression of p27 (kip1) and degree of malignancy in human breast and colorectal cancers. Proc Natl Acad Sci USA 93:6380–6385, 1997.

    Article  Google Scholar 

  27. Freije JM, MacDonald NJ, Steeg PS; Nm23 and tumour metastasis: basic and translational advances. Biochem Soc Symp 63:261–271, 1998.

    PubMed  CAS  Google Scholar 

  28. Gasparini G, Brooks PC, Biganzoli E, et al; Vascular integrin alpha(v)beta3: a new prognostic indicator in breast cancer. Clin Cancer Res 4:2625–2634, 1998.

    PubMed  CAS  Google Scholar 

  29. Ghoussoub RA, Dillon DA, D’Aquila T, et al; Expression of cmet is a strong independent prognostic factor in breast carcinoma. Cancer 82:1513–1520, 1998.

    Article  PubMed  CAS  Google Scholar 

  30. Gillespie MT, Thoma RJ, Pu ZY, et al; Calcitonin receptors, bone sialoprotein and osteopontin are expresswed in primary breast cancer. Int J Cancer 73:812–815, 1997.

    Article  PubMed  CAS  Google Scholar 

  31. Ginsberg RJ, Vokes, EE, Raben A: Non-Small Cell Lung Cancer. In: (De Vita, VT, Hellman, S, Rosenberg, SA (eds)): Principles & Practice of Oncology, Fifth Edition, Lippincott-Raven Publ. Philadelphia, Vol.1. pp. 852–911, 1997.

    Google Scholar 

  32. Glinsky GV; Cell adhesion and metastasis: is the site specificity of cancer metastasis determined by leukocyte-endothelial cell recognition and adhesion. Clin Rev Oncol/Hematol 14:229–278, 1993.

    CAS  Google Scholar 

  33. Glinsky GV; Apoptosis in metastatic cancer cells. Clin Rev Oncol/Hematol 24:175–186, 1997.

    Google Scholar 

  34. Gohji K, Fujimoto N, Hara I, et al; Serum matrix metalloproteinase-2 and its density in men with prostate cancer as a new predictor of disease extension. Int J Cancer 79:96–101, 1998.

    Article  PubMed  CAS  Google Scholar 

  35. Goldmann T, Ribbert D, Suter L, et al; Tumor characteristics involved in the metastatic behaviour as an improvement in primary cutaneous melanoma prognostics. J Exp Clin Cancer Res 17:483–489, 1998.

    PubMed  CAS  Google Scholar 

  36. Gui GP, Puddefoot JP, Vinson GP, et al; Alterd cell-matrix contact: a prerequisite for breast cancer metastasis? Br J Cancer 75:623–633, 1997.

    PubMed  CAS  Google Scholar 

  37. Guilford P; E-cadherin downregulation in cancer: fuel on the fire: Mol Medicine Today 5:172–177, 1999.

    Article  CAS  Google Scholar 

  38. Harris Y, Marrow M, Norton L: Malignant tumor of the breast. In: (DeVita VT, Hellman S, Rosenberg SA (eds)): Principles Practice of Oncology, Fifth Edition, Lippincott-Raven Publ. Philadelphia, Vol.1. 1557–1616, 1997.

    Google Scholar 

  39. Hart IR; Perspective: tumour spread—the problems of latency. J Pathology 187:91–94, 1999.

    Article  CAS  Google Scholar 

  40. Hashimoto S, Koji T, Kohara N, et al; Frequency of apoptosis relates inversely to invasiveness and metastatic activity in human colorectal cancer. Virchows Arch 43:241–248, 1997.

    Article  Google Scholar 

  41. Hofmann M, Rudy W, Zoller M, et al; CD44 splice variants confer metastatic behaviour in rats: homologous sequences are expressed in human tumor cell lines. Cancer Res 51:5292–5297, 1991.

    PubMed  CAS  Google Scholar 

  42. Honn KV, Aref A, Chen Q, et al; Prostate cancer old problems and new approaches. Pathology Oncology Research 2:191–211, 1996a.

    Article  PubMed  CAS  Google Scholar 

  43. Honn KV, Aref A, Chen YQ et al; Prostate Cancer. Old problems and new approaches. Part III. Prevention and Treatment. Pathol Oncol Res 2:276–292, 1996b.

    Article  PubMed  Google Scholar 

  44. Houston SJ, Plunkett TA, Barnes, DM, et al; Overexpression of c-erbB2 is an independent marker of resistance to endocrine therapy in advanced breast cancer. Br J Cancer 79:1220–1226, 1999.

    Article  PubMed  CAS  Google Scholar 

  45. Ishigami SI, Arii S, Furutani M, et al; Predictive value of vascular endothelial growth factor (VEGF) in metastasis and prognosis of human colorectal cancer. Br J Cancer 78:1379–1384, 1998.

    PubMed  CAS  Google Scholar 

  46. Jalkanen S, Reichert RA, Gallatin WM, et al; Homing receptors and the control of lymphocyte migration. Immunol Rev 91:39–60, 1986.

    Article  PubMed  CAS  Google Scholar 

  47. Jansen RL, Hupperets PS, Arends JW, et al; MIB-1 labelling index is an independent prognostic marker in primary breast cancer. Br J Cancer 78:460–465, 1998.

    PubMed  CAS  Google Scholar 

  48. Juliano RL, Varner JA; Adhesion molecules in cancer: the role of integrins. Curr Op Cell Biol 5:812–818, 1993.

    Article  PubMed  CAS  Google Scholar 

  49. Kim YC, Park KO, Kern JA, et al; The interactive effect of Ras, HER2, P53, and Bcl-2 expression in predicting the survival of non-small cell lung cancer patients. Lung Cancer 22:181–190, 1998.

    Article  PubMed  CAS  Google Scholar 

  50. Koeneman KS, Yeung F, Chung LW; Osteomimetic properties of prostate cancer cells: a hypothesis supporting the predilection of prostate cancer metastasis and growth in the bone environment. Prostate 39:246–261, 1999.

    Article  PubMed  CAS  Google Scholar 

  51. Kumar S, Ghellal A, Li C, et al; Breast carcinoma: vascular density determined using CD105 antibody correlates with tumor prognosis. Cancer Res 59:856–861, 1999.

    PubMed  CAS  Google Scholar 

  52. Lee J-H, Miele ME, Hicks DJ, et al; KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J Natl Cancer Inst 88:1731–1737, 1996.

    Article  PubMed  CAS  Google Scholar 

  53. Liapis H, Flath A, Kitazawa S; Integrin alphav beta3 expression by bone resident breast cancer metastases. Diagn Mol Pathol 5:127–135, 1996.

    Article  PubMed  CAS  Google Scholar 

  54. Liotta LA; Tumor invasion and metastasis: role extracellular matrix. Cancer Res 46:1–14, 1986.

    Article  PubMed  CAS  Google Scholar 

  55. Maguire TM, Shering SG, Duggan CM, et al; High levels of cathepsin B predict poor aoutcome in patients with breast cancer. Int J Biol Markers 13:139–144, 1998.

    PubMed  CAS  Google Scholar 

  56. Menard S, Tagliabue E, Colnaghi MI; The 67 kDa laminin receptor as a prognostic factor in human cancer. Breast Cancer Res Treat 52:137–145, 1998.

    Article  PubMed  CAS  Google Scholar 

  57. Meyer T, Hart IR; Mechanisms of tumour metastasis. Eur J Cancer 34:214–221, 1998.

    Article  PubMed  CAS  Google Scholar 

  58. Miyake H, Hara I, Yamanaka K, et al; Elevation of serum levels of urokinase-type plasminogen activator and its receptor is associated with disease progression and prognosis in patients with prostate cancer. Prostate 39:123–129, 1999.

    Article  PubMed  CAS  Google Scholar 

  59. Miyake M, Adachi M, Huang C, et al; A novel molecular staging protocol for non-small cell lung cancer. Oncogene 18:2397–2404, 1999.

    Article  PubMed  CAS  Google Scholar 

  60. Nakamori S, Kameyama M, Imaoka S, et al; Involvement of carbohydrate antigen sialyl Lewis(x) in colorectal cancer metastasis. Dis Colon Rectum 40:420–431, 1997.

    Article  PubMed  CAS  Google Scholar 

  61. Nakamori S, Watanabe H, Kameyama M, et al; Expression of autocrine motility factor receptor in colorectal cancer as a predictor for disease recurrence. Cancer 74:1855–1862, 1994.

    Article  PubMed  CAS  Google Scholar 

  62. Nicolson GL; Paracrine and autocrine growth mechanisms in tumor metastasis to specific sites with particular emphasis on brain and lung metastasis. Cancer Metast Rev 12:325–343, 1993.

    Article  CAS  Google Scholar 

  63. Nihei Z, Ichikawa W, Kojima K et al; The positive relationship between the expression of CD44 variant 6 and prognosis in colorectal cancer. Surg Today 26:760–761, 1996.

    Article  PubMed  CAS  Google Scholar 

  64. Noordzij MA, van Steenbrugge GJ, Verkaik NS, et al; The prognostic value of CD44 isoforms in prostate cancer patients treated by radical prostatectomy. Clin Cancer Res 3:805–815, 1997.

    PubMed  CAS  Google Scholar 

  65. Oesterling J, Fuks ZVI, Lee CT, Scher HI: In: (DeVita VT, Hellman S, Rosenberg SA (eds)): Principles & Practice of Oncology, Fifth Edition, Lippincott-Raven Publ. Philadelphia, Vol. 1. 1222–1385, 1997.

    Google Scholar 

  66. Ohta Y, Endo Y, Tanaka M, et al; Significance of vascular endothelial growth factor messenger RNA expression in primary lung cancer. Clin Cancer Res 2:1411–1416, 1996.

    PubMed  CAS  Google Scholar 

  67. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 1:571–573, 1889.

    Article  Google Scholar 

  68. Pappot H, Francis D, Brunner N, et al; p53 protein in nonsmall cell lung cancer as quantitated by enzyme-linked immunosorbent assay: relation to prognosis. Clin Cancer Res 2:155–160, 1996.

    PubMed  CAS  Google Scholar 

  69. Parsons SL, Watson SA, Collins HM et al; Gelatinase (MMP-2 and -9) expression in gastrointestinal malignancy. Br J Cancer 78:1495–502, 1998.

    PubMed  CAS  Google Scholar 

  70. Pegram DM, Pauletti G, Slamon DJ; HER-2/neu as a predictive marker of response to breast cancer therapy. Breast Cancer Res Treat 52:65–77, 1998.

    Article  PubMed  CAS  Google Scholar 

  71. Ponta H, Sleeman J, Herrlich P; Tumor metastasis formation: cell-surface proteins confer metastasis-promoting or -suppressisng properties. Biochem Biophys Acta 1198:1–10, 1994.

    PubMed  CAS  Google Scholar 

  72. Radinsky R; Paracrine growth regulation of human colon carcinoma organ-specifric metastasis. Cancer Metast Rev 12:345–361, 1993.

    Article  CAS  Google Scholar 

  73. Rásó E, Tóvári J, Tóth K, et al. Ectopic αIIbβ3 integrin signaling involves 12-lipoxygenase and PKC-mediated serine phosphorylation events in melanoma cells. Thromb Haemostas 85:1037–1042, 2001.

    Google Scholar 

  74. Ravioli A, Bagli L, Zucchini A, et al; Prognosis and prediction of response in breast cancer: the current role of the main biological markers. Cell Prolif 31:113–126, 1998.

    Article  Google Scholar 

  75. Ropponen KM, Eskelinen MJ, Lipponen PK, et al; Expression of CD44 and variant proteins in human colorectal cancer and its relevance for prognosis. Scand J Gastroenterol 33:301–309, 1998.

    Article  PubMed  CAS  Google Scholar 

  76. Rudolph P, Alm P, Heidebrecht HJ, et al; Immunologic proliferation marker Ki-S2 as prognostic indicator for lymph nodenegative breast cancer. J Natl Cancer Inst 91:271–278, 1999.

    Article  PubMed  CAS  Google Scholar 

  77. Saito M, Yamaguchi A, Goi T, et al; Expression of DCC protein in colorectal tumors and its relationship to tumor progression and metastasis. Oncology 56:134–141, 1999.

    Article  PubMed  CAS  Google Scholar 

  78. Saitoh K, Takasashi H, Sawada N; Detection of the c-met proto-oncogene product in normal skin and tumours of melanocytic origin. J Pathology 174:191–199, 1994.

    Article  CAS  Google Scholar 

  79. Satoh Y, Higashi T, Nouso K, et al; Cathepsin B in the growth of colorectal cancer: increased activity of cathepsin B in human colorectal cancer. Acta Med Okayama 50:305–311, 1996.

    PubMed  CAS  Google Scholar 

  80. Seiki M, Sato H, Liotta LA, et al; Comparison of autocrine mechanisms promoting motility in two metastatic cell lines: human melanoma and ras-transfected NH3T3 cells. Int J Cancer 49:717–720, 1991.

    Article  PubMed  CAS  Google Scholar 

  81. Shiina H, Igawa M, Shigeno K, et al; Relationship of serum testosterone level with proliferating cell nuclear antigen and nm23 protein in human prostatic carcinoma tissue. Oncology 54:482–489, 1997.

    PubMed  CAS  Google Scholar 

  82. Shivers SC, Wang X, Li W, et al; Molecular staging of malignant melanoma: correlation with clinical outcome. JAMA 280:1410–1415, 1998.

    Article  PubMed  CAS  Google Scholar 

  83. Siegfried JM, Weissfeld LA, Luketich JD, et al; The clinical significance of hepatocyte growth factor for non-small cell lung cancer. Ann Thorac Surg 66:1915–1918, 1998.

    Article  PubMed  CAS  Google Scholar 

  84. Silletti S, Paku S, Raz A; Tumor cell motility and metastasis. Autocrine motility factor as an example of ecto/exoenzyme cytokines. Pathology Oncology Research 3:230–254, 1997.

    Article  PubMed  CAS  Google Scholar 

  85. Sloane BF, Moin K, Krepela E, et al; Cathepsin B and its endogenous inhibitors: the role in tumor malignancy. Cancer Metastasis Rev 9:333–352, 1990.

    Article  PubMed  CAS  Google Scholar 

  86. Smythe WR, Wasf, D, Bavaria JE et al; Loss of alpha-v integrin expression and recurrence in node-negative lung carcinoma. Ann Thorac Surg 64:949–953, 1997.

    Article  PubMed  CAS  Google Scholar 

  87. Steeg PS, Bevilacqua G, Kopper L, et al; Evidence for a novel gene associated with low tumor metastatic potential. J Natl Cancer Inst 80:200–204, 1988.

    Article  PubMed  CAS  Google Scholar 

  88. Stephens RW, Nielsen HJ, Christensen IJ, et al; Plasma urokinase receptor levels in patients with colorectal cancer: relationship to prognosis. J Natl Cancer Inst 91:869–874, 1999.

    Article  PubMed  CAS  Google Scholar 

  89. Sun XF, Ekberg H, Zhanh H, et al; Overexpression of ras is an independent prognostic factor in colorectal adenocarcinoma. APMIS 106:657–664, 1998.

    Article  PubMed  CAS  Google Scholar 

  90. Takanami I, Tanaka F, Hashizume T, et al; Tumor angiogenesis in pulmonary adenocarcinomas: relationship with basic fibroblast growth factor, its receptor, and survival. Neoplasma 44:295–298, 1997.

    PubMed  CAS  Google Scholar 

  91. Tan P, Cody B, Wanner M, et al; The cell cycle inhibitor p27 is an independent prognostic marker in small (T1a,b) invasive breast carcinomas. Cancer Res 57:1259–1263, 1997.

    PubMed  CAS  Google Scholar 

  92. Tang DG, Honn KV; Adhesion molecules and tumor metastasis: an update. Invasion Metast 14:109–122, 1995.

    CAS  Google Scholar 

  93. Tanigawa S, Hirokazu A, Matsumura M, et al; Tumor angiogenesis and mode of metastasis in Patients with colorectal cancer. Cancer Res 57:1043–1046, 1997.

    PubMed  CAS  Google Scholar 

  94. Telvensaari-Mattila A, Paakk, P, Hoyhtya M, et al; Matrix metalloproteinase-2 immunoreactive protein: a marker of aggressiveness in breast carcinoma. Camcer 83:1153–1162, 1998.

    Google Scholar 

  95. Tímár J, Silletti S, Bazaz R, et al; Regulation of melanoma-cell motility by the lipoxygenase metabolite 12-(S)-HETE. Int J Cancer 55:1003–1010, 1993.

    Article  PubMed  Google Scholar 

  96. Tímár J, Tóth Sz, Tóvári J, et al. Autocrine motility factor (neuroleukin, phosphohexose isomerase) induces cell movement through 12-lipoxygenase-dependent tyrosine phosphorylation and serine dephosphorylation events. Clin Exp Metast 17:809–816, 1999.

    Article  Google Scholar 

  97. Tímár J, Rásó E, Gilde K, et al. Expression and function of the AMR-AMFR system in human melanoma in experimental and clinical systems. Clin Exp Metast (in press).

  98. Tóvári J, Paku S, Rásó E, et al; Role of sinusoidal heparan sulfate proteoglycan in liver metastasis formation Int J Cancer 71:825–831, 1997.

    Article  PubMed  Google Scholar 

  99. Trikha M, Tímár J, Lundy SK, et al; Human prostate carcinoma cells express functional αIIbβ3 integrin. Cancer Res 56:5071–5078, 1996.

    PubMed  CAS  Google Scholar 

  100. Trikha M, Cai Y, Grignon D, et al.; Identification of a novel truncated αIIb integrin. Canc Res 58:4771–4775, 1998.

    CAS  Google Scholar 

  101. Vaisanen A, Tuominen H, Kallioinen M, Turpeenniemi-Hujanen T: Matrix metallo-proteinase-2 (72 kD type IV collagenase) expression occurs in the early stage of human melanocytic tumour progression and may have prognostic value. J Pathol 180:283–289, 1996.

    Article  PubMed  CAS  Google Scholar 

  102. Volm M, Mattern J, Koomagi R; Association between nm23-H1 expression, proliferation and apoptosis in non-small cell lung carcinomas. Clin Exp Metastasis 16:595–602, 1998.

    Article  PubMed  CAS  Google Scholar 

  103. Watanabe H, Takehana K, Date M, et al; Tumor cell autocrine motility factor is the neuroleukin / phosphohexose isomerase polypeptide. Cancer Res 46:2960–2963, 1996.

    Google Scholar 

  104. Yamaguchi A, Ding K, Maehara M, et al; Expression of nm23H1gene and Sialyl Lewis X antigen in breast cancer. Oncology 55:357–362, 1998.

    Article  PubMed  CAS  Google Scholar 

  105. Yu H, Levesque MA, Clark GM, et al; Prognostic value of prostate-specific antigen for women with breast cancer: a large United States cohort study. Clin Cancer Res 4:1489–1497, 1997.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National Institute of Oncology, Budapest

    József Tímár, Orsolya Csuka & Zsolt Orosz

  2. 1st Institute of Pathology Experimental Cancer Research, Semmelweis University, Budapest, Hungary

    József Tímár, András Jeney & László Kopper

Authors
  1. József Tímár
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Orsolya Csuka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zsolt Orosz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. András Jeney
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. László Kopper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to József Tímár.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tímár, J., Csuka, O., Orosz, Z. et al. Molecular pathology of tumor metastasis. Pathol. Oncol. Res. 7, 217–230 (2001). https://doi.org/10.1007/BF03032353

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03032353

Keywords

Search

Navigation