Coculture with prostate cancer cells alters endoglin expression and attenuates transforming growth factor-β signaling in reactive bone marrow stromal cells

Molecular Cancer Research

Volumn 5, Issue 6, 2007, Pages 585-603

  O'Connor, John C ^a,c   Farach Carson, Mary C ^a,c   Schneider, Charles J ^b,c,d   Carson, Daniel D ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b HELEN F GRAHAM CANCER CENTER   (United States)

^c Center for Translational Cancer Research   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOGLIN; GLYCOPROTEIN; INHIBITORY SMAD PROTEIN; MEMBRANE RECEPTOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1;

ARTICLE; BONE MARROW CELL; BONE METASTASIS; CANCER CELL CULTURE; CELL PROLIFERATION; COCULTURE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC SCREENING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MALE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN FAMILY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STROMA CELL;

ANTIGENS, CD; APOPTOSIS; BONE AND BONES; BONE MARROW CELLS; CELL LINE, TUMOR; CELL PROLIFERATION; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; HUMANS; MALE; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; STROMAL CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 34250856921     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-06-0408     Document Type: Article

References (65)

1. Reddi AH, Roodman D, Freeman C, Mohla S. Mechanisms of tumor metastasis to the bone: challenges and opportunities. J Bone Miner Res 2003;18:190-4.
2. Dorkin TJ, Neal DE. Basic science aspects of prostate cancer. Semin Cancer Biol 1997;8:21-7.
3. Gopalkrishnan RV, Kang DC, Fisher PB. Molecular markers and determinants of prostate cancer metastasis. J Cell Physiol 2001;189:245-56.
4. Yoneda T. Cellular and molecular mechanisms of breast and prostate cancer metastasis to bone. Eur J Cancer 1998;34:240-5.
5. Greenlee RT, Hill-Harmon MB, Murray T, Thun M. Cancer statistics, 2001. CA Cancer J Clin 2001;51:15-36.
6. Lalani el N, Laniado ME, Abel PD. Molecular and cellular biology of prostate cancer. Cancer Metastasis Rev 1997;16:29-66.
7. Chung LW. Prostate carcinoma bone-stroma interaction and its biologic and therapeutic implications. Cancer 2003;97:772-8.
8. Chung LWK, Baseman A, Assikis V, Zhau HE. Molecular insights into prostate cancer progression: the missing linkof tumor microenvironment. J Urol 2005;173:10-20.
9. Chackal-Roy M, Niemeyer C, Moore M, Zetter BR. Stimulation of human prostatic carcinoma cell growth by factors present in human bone marrow. J Clin Invest 1989;84:43-50.
10. Goltzman D. Mechanisms of the development of osteoblastic metastases. Cancer 1997;80:1581-7.
11. Yoneda T. Cellular and molecular basis of preferential metastasis of breast cancer to bone. J Orthop Sci 2000;5:75-81.
12. Weber MH, Goltzman D, Kostenuik P, et al. Mechanisms of tumor metastasis to bone. Crit Rev Eukaryot Gene Expr 2000;10:281-302.
13. Camps JL, Chang SM, Hsu TC, et al. Fibroblast-mediated acceleration of human epithelial tumor growth in vivo. Proc Natl Acad Sci U S A 1990;87:75-9.
14. Chung LW, Chang SM, Bell C, Zhau HE, Ro JY, von Eschenbach AC. Coinoculation of tumorigenic rat prostate mesenchymal cells with non-tumorigenic epithelial cells results in the development of carcinosarcoma in syngeneic and athymic animals. Int J Cancer 1989;43:1179-87.
15. Chung LW, Matsuura J, Rocco AK, Thompson TC, Miller GJ, Runner MN. Tissue interactions and prostatic growth: a new mouse model for prostatic hyperplasia. Ann N Y Acad Sci 1984;438:394-404.
16. Gleave M, Hsieh JT, Gao CA, von Eschenbach AC, Chung LW. Acceleration of human prostate cancer growth in vivo by factors produced by prostate and bone fibroblasts. Cancer Res 1991;51:3753-61.
17. Gleave ME, Hsieh JT, von Eschenbach AC, Chung LW. 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 1992;147:1151-9.
18. Miller GJ, Runner MN, Chung LW. Tissue interactions and prostatic growth: II. Morphological and biochemical characterization of adult mouse prostatic hyperplasia induced by fetal urogenital sinus implants. Prostate 1985;6:241-53.
19. Wong YC, Wang YZ. Growth factors and epithelial-stromal interactions in prostate cancer development. Int Rev Cytol 2000;199:65-116.
20. Wu HC, Hsieh JT, Gleave ME, Brown NM, Pathak S, Chung LW. Derivation of androgen-independent human LNCaP prostatic cancer cell sublines: role of bone stromal cells. Int J Cancer 1994;57:406-12.
21. Wu TT, Sikes RA, Cui Q, et al. Establishing human prostate cancer cell xenografts in bone: induction of osteoblastic reaction by prostate-specific antigen-producing tumors in athymic and SCID/bg mice using LNCaP and lineagederived metastatic sublines. Int J Cancer 1998;77:887-94.
22. Olumi AF, Dazin P, Tlsty TD. A novel coculture technique demonstrates that normal human prostatic fibroblasts contribute to tumor formation of LNCaP cells by retarding cell death. Cancer Res 1998;58:4525-30.
23. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 1999;59:5002-11.
24. Thalmann GN, Anezinis PE, Chang SM, et al. Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res 1994;54:2577-81.
25. Thalmann GN, Sikes RA, Wu TT, et al. LNCaP progression model of human prostate cancer: androgen-independence and osseous metastasis. Prostate 2000;44:91-103.
26. Ozen M, Multani AS, Kuniyasu H, Chung LW, von Eschenbach AC, Pathak S. Specific histologic and cytogenetic evidence for in vivo malignant transformation of murine host cells by three human prostate cancer cell lines. Oncol Res 1997;9:433-8.
27. Pathak S, Nemeth MA, Multani AS, Thalmann GN, von Eschenbach AC, Chung LW. Can cancer cells transform normal host cells into malignant cells? Br J Cancer 1997;76:1134-8.
28. Tlsty TD, Hein PW. Know thy neighbor: stromal cells can contribute oncogenic signals. Curr Opin Genet Dev 2001;11:54-9.
29. 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 1999;39:246-61.
30. Pece-Barbara N, Wrana JL, Letarte M. Endoglin is an accessory protein that interacts with the signaling receptor complex of multiple members of the transforming growth factor-β superfamily. J Biol Chem 1999;274:584-94.
31. Blanco FJ, Santibanez JF, Guerrero-Esteo M, Langa C, Vary CP, Bernabeu C. Interaction and functional interplay between endoglin and ALK-1, two components of the endothelial transforming growth factor-β receptor complex. J Cell Physiol 2005;204:574-84.
32. Lebrin F, Deckers M, Bertolino P, tenDijke P. TGF-β receptor function in the endothelium. Cardiovasc Res 2005;65:599-608.
33. Itoh S, Itoh F, Goumans M-J, tenDijke P. Signaling of transforming growth factor-β family members through Smad proteins. Eur J Biochem 2000;267:6954-67.
34. Walther HE. Krebsmetastasen. Verlag, Basel: Benno Schwabe & Co.; 1948.
35. Chung LW, Davies R. Prostate epithelial differentiation is dictated by its surrounding stroma. Mol Biol Rep 1996;23:13-9.
36. Gmyrek GA, Walburg M, Webb CP, et al. Normal and malignant prostate epithelial cells differ in their response to hepatocyte growth factor/scatter factor. Am J Pathol 2001;159:579-90.
37. Krupski T, Harding MA, Herce ME, Gulding KM, Stoler MH, Theodorescu D. The role of vascular endothelial growth factor in the tissue specific in vivo growth of prostate cancer cells. Growth Factors 2001;18:287-302.
38. Mansson PE, Adams P, Kan M, McKeehan WL. Heparin-binding growth factor gene expression and receptor characteristics in normal rat prostate and two transplantable rat prostate tumors. Cancer Res 1989;49:2485-94.
39. Shain SA, Saric T, Ke LD, Nannen D, Yoas S. Endogenous fibroblast growth factor-1 or fibroblast growth factor-2 modulate prostate cancer cell proliferation. Cell Growth Differ 1996;7:573-86.
40. Boyce BF, Yoneda T, Guise TA. Factors regulating the growth of metastatic cancer in bone. Endocr Relat Cancer 1999;6:333-47.
41. Axelrod R, Axelrod DE, Pienta KJ. From the Cover: Evolution of cooperation among tumor cells. Proc Natl Acad Sci U S A 2006;103:13474-9.
42. Balooch G, Balooch M, Nalla RK, et al. TGF-β regulates the mechanical properties and composition of bone matrix. Proc Natl Acad Sci U S A 2005;102:18813-8.
43. Rich JN, Borton AJ, Wang X-F. Transforming growth factor-β signaling in cancer. Microsc Res Tech 2001;52:363-73.
44. Massague J, Blain SW, Lo RS. TGFβ signaling in growth control, cancer, and heritable disorders. Cell 2000;103:295-309.
45. Blobe GC, Schiemann WP, Lodish HF. Role of transforming growth factor β in human disease. N Engl J Med 2000;342:1350-8.
46. Koutsilieris M, Rabani SA, Goltzman D. Selective osteoblast mitogens can be extracted from prostatic tissue. Prostate 1986;9:109-15.
47. Koutsilieris M, Rabani SA, Goltzman D. Effects of human prostatic mitogens on rat bone cells and fibroblasts. Endocrinology 1986;115:447-54.
48. Koutsilieris M, Rabani SA, Bennet HP, Goltzman D. Characteristics of prostate derived growth factors for cells of the osteoblastic phenotype. J Clin Invest 1987;80:941-6.
49. Perkel VS, Mohan S, Herring SJ, Baylink DJ, Linkhart TA. Human prostatic cancer cells, PC3, elaborate mitogenic activity which selectively stimulates human bone cells. Cancer Res 1990;50:6902-7.
50. Katagiri T, Imada M, Yanai T, Suda T, Takahashi N, Kamijo R. Identification of a BMP-responsive element in Id1, the gene for inhibition of myogenesis. Genes Cells 2002;7:949-60.
51. Wong YC, Wang X, Ling M-T. Id-1 expression and cell survival. Apoptosis 2004;9:279-89.
52. Datta PK, Blake MC, Moses HL. Regulation of plasminogenactivator inhibitor-1 expression by transforming growth factor-β-induced physical and functional interactions between Smads and Sp1. J Biol Chem 2000;275:40014-9.
53. Peng Y, Kang Q, Luo Q, et al. Inhibitor of DNA binding/differentiation helix-loop-helix proteins mediate bone morphogenetic protein-induced osteoblast differentiation of mesenchymal stem cells. J Biol Chem 2004;279:32941-9.
54. Cheng S, Yang J, Rifas L, Zhang S, Avioli L. Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone. Endocrinology 1994;134:277-86.
55. Thies R, Bauduy M, Ashton B, Kurtzberg L, Wozney J, Rosen V. Recombinant human bone morphogenetic protein-2 induces osteoblastic differentiation in W-20-17 stromal cells. Endocrinology 1992;130:1318-24.
56. Osyczka AM, Diefenderfer DL, Bhargave G, Leboy PS. Different effects of BMP-2 on marrow stromal cells from human and rat bone. Cells Tissues Organs 2004;176:109-19.
57. TerBrugge PJ, Jansen JA. In vitro osteogenic differentiation of rat bone marrow cells subcultured with and without dexamethasone. Tissue Eng 2002;8:321-31.
58. Walsh S, Jefferiss C, Stewart K, Beresford JN. TGFβ1 limits the expansion of the osteoprogenitor fraction in cultures of human bone marrow stromal cells. Cell Tissue Res 2003;311:187-98.
59. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-75.
60. Roecklein B, Torok-Storb B. Functionally distinct human marrow stromal cell lines immortalized by transduction with the human papilloma virus E6/E7 genes. Blood 1995;85:997-1005.
61. Amit M, Margulets V, Segev H, et al. Human feeder layers for human embryonic stem cells. Biol Reprod 2003;68:2150-6.
62. Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF, Jones LW. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol 1979;17:16-23.
63. Stone KR, Mickey DD, Wunderli H, Mickey GH, Paulson DF. Isolation of a human prostate carcinoma cell line (DU-145). Int J Cancer 1978;21:274-81.
64. Horoszewicz JS, Leong SS, Kawinski E, et al. LNCaP model of human prostatic carcinoma. Cancer Res 1983;43:1809-18.
65. Engel LW, Young NA, Tralka TS, Lippman ME, O'Brien SJ, Joyce MJ. Establishment and characterization of three new continuous cell lines derived from human breast carcinomas. Cancer Res 1978;38:3352-64.