Thrombospondin-1 triggers cell migration and development of advanced prostate tumors

Cancer Research

Volumn 71, Issue 24, 2011, Pages 7649-7658

  Firlej, Virginie ^a   Mathieu, Jacques R R ^a   Gilbert, Cristèle ^a   Lemonnier, Loïc ^b   Nakhlé, Jessica ^a,c   Gallou Kabani, Catherine ^c   Guarmit, Basma ^d   Morin, Aurélie ^a   Prevarskaya, Natalia ^b   Delongchamps, Nicolas Barry ^a,e   Cabon, Florence ^a,c,f  

^a CNRS   (France)

^b Université des Sciences et Technologies de Lille   (France)

^c SeleXel   (France)

^d CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^e Paris Descartes University ^*  (France)

^f CANCER RESEARCH CENTER OF TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; THROMBOSPONDIN 1;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER TISSUE; CARCINOGENESIS; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROSTATECTOMY; PROTEIN EXPRESSION; TUMOR CELL; TUMOR XENOGRAFT;

ANIMALS; ANOXIA; ANTIGENS, CD36; CALCIUM; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL; NEOVASCULARIZATION, PATHOLOGIC; ORCHIECTOMY; PEPTIDES; PROSTATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; THROMBOSPONDIN 1; TRPV CATION CHANNELS; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84255192004     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-0833     Document Type: Article

References (55)

1. Aragon-Ching JB, Madan RA, Dahut WL. Angiogenesis inhibition in prostate cancer: current uses and future promises. J Oncol 2010;2010:361836.
2. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008;8:592-603.
3. Pàez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Viñals F, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009;15:220-31.
4. Ebos JML, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-9.
5. Tuszynski GP, Gasic TB, Rothman VL, Knudsen KA, Gasic GJ. Thrombospondin, a potentiator of tumor cell metastasis. Cancer Res 1987;47:4130-3. (Pubitemid 17108482)
6. Markovic SN, Suman VJ, Rao RA, Ingle JN, Kaur JS, Erickson LA, et al. A phase II study of ABT-510 (thrombospondin-1 analog) for the treatment of metastatic melanoma. Am J Clin Oncol 2007;30:303-9. (Pubitemid 46884153)
7. Baker LH, Rowinsky EK, Mendelson D, Humerickhouse RA, Knight RA, Qian J, et al. Randomized, phase ii study of the thrombospondin-1-mimetic angiogenesis inhibitor abt-510 in patients with advanced soft tissue sarcoma. J Clin Oncol 2008;26:5583-8.
8. Good DJ, Polverini PJ, Rastinejad F, Le BM, Lemons RS, Frazier WA, et al. A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci U S A 1990;87:6624-8.
9. Carlson CB, Lawler J, Mosher DF. Structures of thrombospondins. Cell Mol Life Sci 2008;65:672-86.
10. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 2000;6:41-8. (Pubitemid 30048524)
11. Colombel M, Filleur S, Fournier P, Merle C, Guglielmi J, Courtin A, et al. Androgens repress the expression of the angiogenesis inhibitor thrombospondin- 1 in normal and neoplastic prostate. Cancer Res 2005;65:300-8. (Pubitemid 40070822)
12. Fontana A, Filleur S, Guglielmi J, Frappart L, Bruno-Bossio G, Boissier S, et al. Human breast tumors override the antiangiogenic effect of stromal thrombospondin-1 in vivo. Int J Cancer 2005;116:686-91. (Pubitemid 41099699)
13. Kwak C, Jin RJ, Lee C, Park MS, Lee SE. Thrombospondin-1, vascular endothelial growth factor expression and their relationship with p53 status in prostate cancer and benign prostatic hyperplasia. BJU Int 2002;89:303-9. (Pubitemid 34158467)
14. Adams JC. Functions of the conserved thrombospondin carboxyterminal cassette in cell-extracellular matrix interactions and signaling. Int J Biochem Cell Biol 2004;36:1102-14. (Pubitemid 38501562)
15. Prevarskaya N, Zhang L, Barritt G. TRP channels in cancer. Biochim Biophys Acta 2007;1772:937-46.
16. Bidaux G, Flourakis M, Thebault S, Zholos A, Beck B, Gkika D, et al. Prostate cell differentiation status determines transient receptor potential melastatin member 8 channel subcellular localization and function. J Clin Invest 2007;117:1647-57. (Pubitemid 46871349)
17. Monet M, Lehen'kyi V, Gackiere F, Firlej V, Vandenberghe M, Roudbaraki M, et al. Role of cationic channel TRPV2 in promoting prostate cancer migration and progression to androgen resistance. Cancer Res 2010;70:1225-35.
18. Jariwala U, Prescott J, Jia L, Barski A, Pregizer S, Cogan JP, et al. Identification of novel androgen receptor target genes in prostate cancer. Mol Cancer 2007;6:39.
19. Grynkiewicz G, Poenie M, Tsien R. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985;260:3440-50. (Pubitemid 15114340)
20. Li Q, Ahuja N, Burger PC, Issa JP. Methylation and silencing of the Thrombospondin-1 promoter in human cancer. Oncogene 1999;18:3284-9. (Pubitemid 29286973)
21. Thalmann GN, Anezinis PE, Chang SM, Zhau HE, Kim EE, Hopwood VL, et al. Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res 1994;54:2577-81. (Pubitemid 24173741)
22. Compagno D, Merle C, Morin A, Gilbert C, Mathieu J, Bozec A, et al. SIRNA-directed in vivo silencing of androgen receptor inhibits the growth of castration-resistant prostate carcinomas. PLoS One 2007;2:e1006.
23. Busk M, Toustrup K, Sorensen BS, Alsner J, Horsman MR, Jakobsen S, et al. In vivo identification and specificity assessment of mRNA markers of hypoxia in human and mouse tumors. BMC Cancer 2011;11:63.
24. Filleur S, Volpert OV, Degeorges A, Voland C, Reiher F, Clezardin P, et al. In vivo mechanisms by which tumors producing thrombospondin 1 bypass its inhibitory effects. Genes Dev 2001;15:1373-82. (Pubitemid 32524644)
25. Tolsma SS, Volpert OV, Good DJ, Frazier WA, Polverini PJ, Bouck N. Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. J Cell Biol 1993;122:497-511. (Pubitemid 23210475)
26. Dawson DW, Volpert OV, Pearce SF, Schneider AJ, Silverstein RL, Henkin J, et al. Three distinct D-amino acid substitutions confer potent antiangiogenic activity on an inactive peptide derived from a thrombospondin-1 type 1 repeat. Mol Pharmacol 1999;55:332-8. (Pubitemid 29076031)
27. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP. CD36 mediates the In vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 1997;138:707-17. (Pubitemid 27349849)
28. Misenheimer TM, Mosher DF. Calcium ion binding to thrombospondin 1. J Biol Chem 1995;270:1729-33.
29. Fixemer T, Wissenbach U, Flockerzi V, Bonkhoff H. Expression of the Ca2+-selective cation channel TRPV6 in human prostate cancer: a novel prognostic marker for tumor progression. Oncogene 2003;22:7858-61. (Pubitemid 37485545)
30. Lehen'Kyi V, Flourakis M, Skryma R, Prevarskaya N. TRPV6 channel controls prostate cancer cell proliferation via Ca2+//NFAT-dependent pathways. Oncogene 2007;26:7380-5.
31. Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KS, et al. Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 2005;307:1468-72. (Pubitemid 40321945)
32. Vogt-Eisele AK, Weber K, Sherkheli MA, Vielhaber G, Panten J, Gisselmann G, et al. Monoterpenoid agonists of TRPV3. Br J Pharmacol 2007;151:530-40. (Pubitemid 46905006)
33. Toescu EC. Hypoxia sensing and pathways of cytosolic Ca2+ increases. Cell Calcium 2004;36:187-99. (Pubitemid 38992347)
34. Mehta R, Kyshtoobayeva A, Kurosaki T, Small EJ, Kim H, Stroup R, et al. Independent association of angiogenesis index with outcome in prostate cancer. Clin Cancer Res 2001;7:81-8. (Pubitemid 32110208)
35. Sargiannidou I, Qiu C, Tuszynski GP. Mechanisms of thrombospondin- 1-mediated metastasis and angiogenesis. Semin Thromb Hemost 2004;30:127-36. (Pubitemid 38457307)
36. Ohtani Y, Kijima H, Dowaki S, Kashiwagi H, Tobita K, Tsukui M, et al. Stromal expression of thrombospondin-1 is correlated with growth and metastasis of human gallbladder carcinoma. Int J Oncol 1999;15:453-7.
37. de Fraipont F, Keramidas M, El Atifi M, Chambaz EM, Berger F, Feige J-J. Expression of the thrombospondin 1 fragment 167-569 in C6 glioma cells stimulates tumorigenicity despite reduced neovascularization. Oncogene 2004;23:3642-9. (Pubitemid 38658431)
38. Yee KO, Connolly CM, Duquette M, Kazerounian S, Washington R, Lawler J. The effect of thrombospondin-1 on breast cancer metastasis. Breast Cancer Res Treat 2009;114:85-96.
39. Veliceasa D, Ivanovic M, Hoepfner FT, Thumbikat P, Volpert OV, Smith ND. Transient potential receptor channel 4 controls thrombospondin-1 secretion and angiogenesis in renal cell carcinoma. FEBS J 2007;274:6365-77. (Pubitemid 350215931)
40. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, et al. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 2006;444:1032-7. (Pubitemid 46018516)
41. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003;4:517-29. (Pubitemid 36773404)
42. Flourakis M, Prevarskaya N. Insights into Ca2+ homeostasis of advanced prostate cancer cells. Biochim Biophys Acta 2009;1793:1105-9.
43. Carnell DM, Smith RE, Daley FM, Saunders MI, Bentzen SM, Hoskin PJ. An immunohistochemical assessment of hypoxia in prostate carcinoma using pimonidazole: implications for radioresistance. Int J Radiat Oncol Biol Phys 2006;65:91-9.
44. Vergis R, Corbishley CM, Norman AR, Bartlett J, Jhavar S, Borre M, et al. Intrinsic markers of tumour hypoxia and angiogenesis in localised prostate cancer and outcome of radical treatment: a retrospective analysis of two randomised radiotherapy trials and one surgical cohort study. Lancet Oncol 2008;9:342-51.
45. Jans J, van Dijk JH, van Schelven S, van der Groep P, Willems SH, Jonges TN, et al. Expression and localization of hypoxia proteins in prostate cancer: prognostic implications after radical prostatectomy. Urology 2010;75:786-92.
46. Yao X, Garland CJ. Recent developments in vascular endothelial cell transient receptor potential channels. Circ Res 2005;97:853-63. (Pubitemid 41552670)
47. Meng F, To WKL, Gu Y. Role of TRP channels and NCX in mediating hypoxia-induced [Ca2+]i elevation in PC12 cells. Respir Physiol Neurobiol 2008;164:386-93.
48. Laklai H, Laval Sv, Dumartin L, Rochaix P, Hagedorn M, Bikfalvi A, et al. Thrombospondin-1 is a critical effector of oncosuppressive activity of sst2 somatostatin receptor on pancreatic cancer. Proc Natl Acad of Sci U S A 2009;106:17769-74.
49. Kyriakides TR, Maclauchlan S. The role of thrombospondins in wound healing, ischemia, and the foreign body reaction. J Cell Commun Signal 2009;3:215-25.
50. Favier J, Germain S, Emmerich J, Corvol P, Gasc J. Critical overexpression of thrombospondin 1 in chronic leg ischaemia. J Pathol 2005;207:358-66. (Pubitemid 41556458)
51. Osada-Oka M, Ikeda T, Akiba S, Sato T. Hypoxia stimulates the autocrine regulation of migration of vascular smooth muscle cells via HIF-1alpha-dependent expression of thrombospondin-1. J Cell Biochem 2008;104:1918-26.
52. Carron JA, Wagstaff SC, Gallagher JA, Bowler WB. A CD36-binding peptide from thrombospondin-1 can stimulate resorption by osteoclasts in vitro. Biochem Biophys Res Commun 2000;270:1124-7. (Pubitemid 30444842)
53. John AS, Hu X, Rothman VL, Tuszynski GP. Thrombospondin-1 (TSP-1) up-regulates tissue inhibitor of metalloproteinase-1 (TIMP-1) production in human tumor cells: Exploring the functional significance in tumor cell invasion. Exp Mol Pathol 2009;87:184-8.
54. Burchardt M, Burchardt T, Chen MW, Hayek OR, Knight C, Shabsigh A, et al. Vascular endothelial growth factor-A expression in the rat ventral prostate gland and the early effects of castration. Prostate 2000;43:184-94. (Pubitemid 30230454)
55. Fitchev PP, Wcislak SM, Lee C, Bergh A, Brendler CB, Stellmach VM, et al. Thrombospondin-1 regulates the normal prostate in vivo through angiogenesis and TGF-beta activation. Lab Invest 2010;90:1078-90.