Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium

Cancer Research

Volumn 59, Issue 19, 1999, Pages 5002-5011

  Olumi, Aria F ^a   Grossfeld, Gary D ^a   Hayward, Simon W ^a   Carroll, Peter R ^a   Tlsty, Thea D ^a,b   Cunha, Gerald R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; COCULTURE; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; FIBROBLAST CULTURE; HUMAN; HUMAN CELL; KARYOTYPE; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROSTATE EPITHELIUM; TUMOR GROWTH;

NON-PROGRAMMATIC;

ANIMALS; CELL LINE; CELL SURVIVAL; COCULTURE TECHNIQUES; DISEASE PROGRESSION; EPITHELIAL CELLS; FIBROBLASTS; HUMANS; KARYOTYPING; KERATINS; MALE; MICE; MICE, NUDE; PROSTATE; PROSTATIC NEOPLASMS; RATS; RATS, NUDE; TRANSPLANTATION, HETEROLOGOUS; VIMENTIN;

EID: 0033215242     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Landis, S. H., Murray, T., Bolden, S., and Wingo, P. A. Cancer statistics, 1998. CA Cancer J. Clin., 48: 6-29, 1998.
2. Foulds, L. Neoplastic Development. London: Academic Press, 1969.
3. Ronnov-Jessen, L., Petersen, O. W., and Bissell, M. J. Cellular changes involved in conversion of normal to malignant breast: importance of the stromal reaction. Physiol. Rev., 76: 69-125, 1996.
4. Hong, W. K., and Sporn, M. B. Recent advances in chemoprevention of cancer. Science (Washington DC), 278: 1073-1077, 1997.
5. Kinzler, K. W., and Vogelstein, B. Landscaping the cancer terrain. Science (Washington DC), 280: 1036-1037, 1998.
6. Rinehart, C. A., and Torti, V. R. Aging and cancer: the role of stromal interactions with epithelial cells. Mol. Carcinog., 18: 187-192, 1997.
7. van den Hooff, A. Connective tissue changes in cancer. Int. Rev. Connective Tissue Res., 10: 395-431, 1983.
8. Cunha, G. R., Alarid, E. T., Turner, T., Donjacour, A. A., Boutin, E. L., and Foster, B. A. Normal and abnormal development of the male urogenital tract: role of androgens, mesenchymal-epithelial interactions and growth factors. J. Androl., 13: 465-475, 1992.
9. Haffen, K., Kedinger, M., Simon-Assmann, P. M., and Lacroix, B. Mesenchyme-dependent differentiation of intestinal brush-border enzymes in the gizzard endoderm of the chick embryo. In: M. Weber and M. Burger (eds.), Embryonic Development, Part B: Cellular Aspects, pp. 261-270. New York: A. R. Liss, 1982.
10. Kratochwil, K. Tissue combination and organ culture studies in the development of the embryonic mammary gland. In: R. B. L. Gwatkin (ed.), Developmental Biology: A Comprehensive Synthesis, Vol. 4, pp. 315-334. New York: Plenum Publishing Corp., 1987.
11. Adam, L., Crepin, M., Lelong, J. C., Spanakis, E., and Israel, L. Selective interactions between mammary epithelial cells and fibroblasts in co-culture. Int. J. Cancer, 59: 262-268, 1994.
12. Dong-Le Bourhis, X., Berthois, Y., Millot, G., Degeorges, A., Sylvi, M., Martin, P. M., and Calvo, F. Effect of stromal and epithelial cells derived from normal and tumorous breast tissue on the proliferation of human breast cancer cell lines in co-culture. Int. J. Cancer, 71: 42-48, 1997.
13. Skobe, M., and Fusenig, N. E. Tumorigenic conversion of immortal human keratinocytes through stromal cell activation. Proc. Natl. Acad. Sci. USA, 95: 1050-1055, 1998.
14. Basset, P., Bellocq, J. P., Wolf, C., Stoll, I., Hutin, P., Limacher, J. M., Podhajcer, O. L., Chenard, M. P., Rio, M. C., and Chambon, P. A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature (Lond.), 348: 699-704, 1990.
15. Chiquet-Ehrismann, R., Mackie, E. J., Pearson, C. A., and Sakakura, T. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell, 47: 131-139, 1986.
16. Singer, C., Rasmussen, A., Smith, H. S., Lippman, M. E., Lynch, H. T., and Cullen, K. J. Malignant breast epithelium selects for insulin-like growth factor II expression in breast stroma: evidence for paracrine function. Cancer Res., 55: 2448-2454, 1995.
17. Wright, J. H., McDonnell, S., Portella, G., Bowden, G. T., Balmain, A., and Matrisian, L. M. A switch from stromal to tumor cell expression of stromelysin-1 mRNA associated with the conversion of squamous to spindle carcinomas during mouse skin tumor progression. Mol. Carcinog., 10: 207-215, 1994.
18. Yee, D., Rosen, N., Favoni, R. E., and Cullen, K. J. The insulin-like growth factors, their receptors, and their binding proteins in human breast cancer. Cancer Treat. Res., 53: 93-106, 1991.
19. Ronnov-Jessen, L., Petersen, O. W., Koteliansky, V. E., and Bissell, M. J. The origin of the myofibroblasts in breast cancer. Recapitulation of tumor environment in culture unravels diversity and implicates converted fibroblasts and recruited smooth muscle cells. J. Clin. Investig., 95: 859-873, 1995.
20. Schor, S. L., Schor, A. M., Grey, A. M., and Rushton. G. Foetal and cancer patient fibroblasts produce an autocrine migration-stimulating factor not made by normal adult cells. J. Cell Sci., 90: 391-399, 1988.
21. Ellis, M. J., Singer, C., Hornby, A., Rasmussen, A., and Cullen, K. J. Insulin-like growth factor mediated stromal-epithelial interactions in human breast cancer. Breast Cancer Res. Treat., 31: 249-261, 1994.
22. Frazier, K. S., and Grotendorst, G. R. Expression of connective tissue growth factor mRNA in the fibrous stroma of mammary tumors. Int. J. Biochem. Cell Biol., 29: 153-161, 1997.
23. Nakamura, T., Matsumoto, K., Kiritoshi, A., Tano, Y., and Nakamura, T. Induction of hepatocyte growth factor in fibroblasts by tumor-derived factors affects invasive growth of tumor cells: in vitro analysis of tumor-stromal interactions. Cancer Res., 57: 3305-3313, 1997.
24. Ponten, F., Ren, Z., Nister, M., Westermark, B., and Ponten, J. Epithelial-stromal interactions in basal cell cancer: the PDGF system. J. Investig. Dermatol., 102: 304-309, 1994.
25. Yan, G., Fukabori, Y., McBride, G., Nikolaropolous, S., and McKeehan, W. L. Exon switching and activation of stromal and embryonic fibroblast growth factor (FGF)-FGF receptor genes in prostate epithelial cells accompany stromal independence and malignancy. Mol. Cell. Biol., 13: 4513-4522, 1993.
26. Hayward, S. W., Dahiya, R., Cunha, G. R., Bartek, J., Deshpande, N., and Narayan, P. Establishment and characterization of an immortalized but non-transformed human prostate epithelial cell line: BPH-1. In Vitro Cell Dev. Biol. Anim., 31: 14-24, 1995.
27. Hayward, S., Cox, S., Mitchell, I., Hallowes, R., Deshpande, N., and Towler, J. The effects of interferons on the activity of α-glycerolphosphate dehydrogenase in benign prostatic hyperplasia cells in primary culture. J. Urol., 138: 648-653, 1987.
28. Hayward, S. W., Del Buono, R., Hall, P. A., and Deshpande, N. A functional model of human prostate epithelium: the role of androgens and stroma in architectural organisation and the maintenance of differentiated secretory function. J. Cell Sci., 102: 361-372, 1992.
29. Hayward, S. W. A simple method for freezing and storing viable tissue fragments. In Vitro Cell Dev. Biol., A34: 28-29, 1998.
30. Hayward, S. W., Haughney, P. C., Rosen, M. A., Gruelich, K. M., Weier, H-U., Dahiya, R., and Cunha, G. R. Interactions between adult human prostatic epithelium and rat urogenital sinus mesenchyme in a tissue recombination model. Differentiation, 63: 31-40, 1998.
31. Hallowes, R. C., Bone, E. J., and Jones, W. A new dimension in the culture of human breast. In: R. J. Richards and K. T. Rajan (eds.), Tissue Culture in Medical Research, Vol. 2, pp. 213-220. Oxford: Pergamon Press, 1980.
32. Olumi, A. F., Dazin, P., and Tlsty, T. D. A novel co-culture technique demonstrates that normal human prostatic fibroblasts contribute to tumor formation of LNCaP cells by retarding cell death. Cancer Res., 58: 4528-4530, 1998.
33. Grossfeld, G. D., Ginsberg, D. A., Stein, J. P., Bochner, B. H., Esrig, D., Groshen, S., Dunn, M., Nichols, P. W., Taylor, C. R., Skinner, D. G., and Cote, R. J. Thrombospondin-1 expression in bladder cancer: association with p53 alterations, tumor angiogenesis, and tumor progression. J. Natl. Cancer Inst., 89: 219-227, 1997.
34. Belloc, F., Dumain, P., Boisseau, M. R., Jalloustre, C., Reiffers, J., Bernard, P., and Lacombe, F. A flow cytometric method using Hoechst 33342 and propidium iodide for simultaneous cell cycle analysis and apoptosis determination in unfixed cells. Cytometry, 17: 59-65, 1994.
35. Crompton, T., Peitsch, M. C., MacDonald, H. R., and Tschopp, J. Propidium iodide staining correlates with the extent of DNA degradation in isolated nuclei. Biochem. Biophys. Res. Commun., 183: 532-537, 1992.
36. Hamel, W., Dazin, P., and Israel, M. A. Adaptation of a simple flow cytometric assay to identify different stages during apoptosis. Cytometry, 25: 173-181, 1996.
37. Gerdes, J., Becker, M. H., Key, G., and Cattoretti, G. Immunohistological detection of tumour growth fraction (Ki-67 antigen) in formalin-fixed and routinely processed tissues. J. Pathol., 168: 85-86, 1992.
38. Grossfeld, G. D., Olumi, A. F., Connolly, J. A., Chew, K., Gibney, J., Bhargava, V., Waldman, F. M., and Carroll, P. R. Locally recurrent prostate tumors following either radiation therapy or radical prostatectomy have changes in Ki-67 labeling index, p53 and bcl-2 immunoreactivity. J. Urol., 159: 1437-1443, 1998.
39. White, A. E., Livanos, E. M., and Tlsty, T. D. Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins. Genes Dev., 8: 666-677, 1994.
40. Kallioniemi, A., Kallioniemi, O. P., Sudar, D., Rutovitz, D., Gray, J. W., Waldman, F., and Pinkel, D. Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors, Science (Washington DC), 258: 818-821, 1992.
41. Schmitt-Graff, A., Desmouliere, A., and Gabbiani, G. Heterogenity of myofibroblast phenotypic features: an example of fibroblastic cell plasticity. Virchows Arch., 425: 3-24, 1994.
42. Cunha, G. R. Role of mesenchymal-epithelial interactions in normal and abnormal development of the mammary gland and prostate. Cancer (Phila.), 74: 1030-1044, 1994.
43. Cunha, G. R. Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Mullerian ducts and urogenital sinus during development of the uterus and vagina in mice. J. Exp. Zool., 196: 361-370, 1976.
44. De Luca, M., Pellegrini, G., Zambruno, G., and Marchisio, P. C. Role of integrins in cell adhesion and polarity in normal keratinocytes and human skin pathologies. J. Dermatol., 21: 821-828, 1994.
45. Desmouliere, A., Geinoz, A., Gabbiani, F., and Gabbiani, G. Transforming growth factor-β1 induces α-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J. Cell Biol., 122: 103-111, 1993.
46. Grinnell, F. Fibroblasts, myofibroblasts, and wound contraction. J. Cell Biol., 124: 401-404, 1994.
47. Poulsom, R., Pignatelli, M., Stetler-Stevenson, W., Liotta, L. A., Wright, P. A., Jeffery, R. E., Longcroft, J. M., Rogers, L., and Stamp, G. W. H. Stromal expression of 72kDa type IV collagenase (MMP-2) and TIMP-2 mRNAs in colorectal neoplasia. Am. J. Pathol., 141: 389-396, 1992.
48. Knudson, C. B., and Knudson, W. Hyaluronan-binding proteins in development, tissue homeostasis, and disease. FASEB J., 7: 1233-1241, 1993.
49. Mareel, M., Behrens, J., Birchmeier, W., De Bruyne, G. K., Vleminckx, K., Hoogewus, A., Fiers, W. C., and Van Roy, F. Down-regulation of E-cadherin expression in Madin Darby canine kidney (MDCK) cells inside tumors of nude mice. Int. J. Cancer, 47: 922-928, 1991.
50. Camps, J. L., Chang, S. M., Hsu, T. C., Freeman, M. R., Hong, S. J., Zhau, H. E., von Eschenbach, A. C., and Chung, L. W. Fibroblast-mediated acceleration of human epithelial tumor growth in vivo. Proc. Natl. Acad. Sci. USA, 87: 75-79, 1990.
51. Chung, L. W., Chang, S. M., Bell, C., Zhau, H. E., Ro, J. Y., and von Eschenbach, A. C. Co-inoculation of tumorigenic rat prostate mesenchymal cells with nontumorigenic epithelial cells results in the development of carcinosarcoma in syngeneic and athymic animals. Int. J. Cancer, 43: 1179-1187, 1989.
52. Gleave, M. E., Hsieh, J. T., Von Eschenbach, A. C., and Chung, L. W. K. Prostate and bone fibroblasts induce human prostate cancer growth in vivo: implications for bidirectional tumor-stromal cell interaction in prostate carcinoma growth and metastasis. J. Urol., 147: 1151-1159, 1992.
53. Momose, H., Uchida, K., Kakinuma, H., Yura, Y., and Oyasu, R. Involvement of urine in epithelial-stromal interactions in urinary bladder carcinogenesis. Cancer Lett., 53: 91-96, 1990.
54. Noel, A., Hajitou, A., L'Hoir, C., Maquoi, E., Baramova, E., Lewalle, J. M., Remacle, A., Kebers, F., Brown, P., Calberg-Bacq, C. M., and Foidart, J. M. Inhibition of stromal matrix metalloproteases: effects on breast-tumor promotion by fibroblasts. Int. J. Cancer, 76: 267-273, 1998.
55. Thompson, T. C., Southgate, J., Kitchener, G., and Land, H. Multistage carcinogenesis induced by ras and myc oncogenes in a reconstituted organ. Cell, 56: 917-930, 1989.
56. Thompson, T. C., Timme, T. L., Kadmon, D., Park, S. H., Egawa, S., and Yoshida, K. Genetic predisposition and mesenchymal-epithelial interactions in ras+myc-induced carcinogenesis in reconstituted mouse prostate. Mol. Carcinog., 7: 165-179, 1993.
57. Uchida, K., Samma, S., Momose, H., Kashihara, N., Rademaker, A., and Oyasu, R. Stimulation of urinary bladder tumorigenesis by carcinogen-exposed stroma. J. Urol., 143: 618-621, 1990.
58. Fujii, H., Cunha, G. R., and Norman, J. T. The induction of adenocarcinomatous differentiation in neoplastic bladder epithelium by an embryonic prostatic inductor. J. Urol., 128: 858-861, 1982.
59. Hayashi, N., Cunha, G. R., and Wong, Y. C. Influence of male genital tract mesenchymes on differentiation of Dunning prostatic adenocarcinoma. Cancer Res., 50: 4747-4754, 1990.
60. Hayashi, N., Tsuji, M., Sugimura, Y., Kawamura, J., and Cunha, G. R. Change in the morphological and functional cytodifferentiation induced by seminal vesicle mesenchyme in cell suspensions of rat Dunning prostatic adenocarcinoma cells. Int. J. Cancer, 68: 788-794, 1996.
61. Nakamura, T., Nishizawa, T., Hagiya, M., Seki, T., Shimonishi, M., Sugimura, A., Tashiro, K., and Shimizu, S. Molecular cloning and expression of human hepatocyte growth factor. Nature (Lond.), 342: 440-443, 1989.
62. Olani, Y., Igarashi, N., Yokoyama, T., Kimita, M., Sakurai, Y., Kameyama, K., Kubota, T., Kumai, K., and Kitajima, M. Fibroblasts affect the malignant potential of gastric carcinoma. Am. Assoc. Cancer Res. Proc., 39: 494, 1998.
63. Picard, O., Rolland, Y., and Poupon, M. F. Fibroblast-dependent tumorigenicity of cells in nude mice: implication for implantation of metastases. Cancer Res., 46: 3290-3294, 1986.