Bone metastasis in prostate cancer: Molecular and cellular mechanisms (Review)

International Journal of Molecular Medicine

Volumn 20, Issue 1, 2007, Pages 103-111

  Ye, Lin ^a   Kynaston, Howard G ^b   Jiang, Wen G ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY HOSPITAL OF WALES   (United Kingdom)

Author keywords

Bone metastasis; Cancer biology; Prostate cancer

Indexed keywords

BONE MORPHOGENETIC PROTEIN;

BIOLOGICAL MODEL; BONE DEVELOPMENT; BONE TUMOR; FORECASTING; GENETICS; HUMAN; MALE; METABOLISM; METASTASIS; OSTEOBLAST; OSTEOCLAST; PATHOLOGY; PROSTATE TUMOR; REVIEW;

BONE MORPHOGENETIC PROTEINS; BONE NEOPLASMS; FORECASTING; HUMANS; MALE; MODELS, BIOLOGICAL; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; PROSTATIC NEOPLASMS;

EID: 34548066096     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.20.1.103     Document Type: Review

References (105)

1. CancerStats: CancerStats Incidence UK. Cancer Research UK, 2005.
2. Bubendorf L, Schopfer A, Wagner U, Sauter G, Moch H, Willi N, Gasser TC and Mihatsch MJ: Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 31: 578-583, 2000.
3. Paget S: The distribution of secondary growths in cancer of the breast. Cancer Metastasis Rev 8: 98-101, 1989.
4. Wawroschek F, Vogt H, Weckermann D, Wagner T and Harzmann R: The sentinel lymph node concept in prostate cancer - first results of gamma probe-guided sentinel lymph node identification. Eur Urol 36: 595-600, 1999.
5. Raubenheimer EJ and Noffke CE: Pathogenesis of bone metastasis: a review. J Oral Pathol Med 35: 129-135, 2006.
6. Roodman GD: Mechanisms of bone metastasis. N Engl J Med 350: 1655-1664, 2004.
7. Cooper CR, Chay CH, Gendernalik JD, Lee HL, Bhatia J, Taichman RS, McCauley LK, Keller ET and Pienta KJ: Stromal factors involved in prostate carcinoma metastasis to bone. Cancer 97: 739-747, 2003.
8. Jiang WG, Martin TA, Parr C, Davies G, Matsumoto K and Nakamura T: Hepatocyte growth factor, its receptor, and their potential value in cancer therapies. Crit Rev Oncol Hematol 53: 35-69, 2005.
9. Batson OV: The function of the vertebral veins and their role in the spread of metastases. Clin Orthop Relat Res 312: 4-9, 1995.
10. Masuda H, Fukabori Y, Nakano K, Takezawa Y, T CS and Yamanaka H: Increased expression of bone morphogenetic protein-7 in bone metastatic prostate cancer. Prostate 54: 268-274, 2003.
11. De Pinieux G, Flam T, Zerbib M, Taupin P, Bellahcene A, Waltregny D, Vieillefond A and Poupon MF: Bone sialoprotein, bone morphogenetic protein 6 and thymidine phosphorylase expression in localized human prostatic adenocarcinoma as predictors of clinical outcome: a clinicopathological and immunohistochemical study of 43 cases. J Urol 166: 1924-1930, 2001.
12. Shariat SF, Shalev M, Menesses-Diaz A, Kim IY, Kattan MW, Wheeler TM and Slawin KM: Preoperative plasma levels of transforming growth factor beta(1) (TGF-beta(1)) strongly predict progression in patients undergoing radical prostatectomy. J Clin Oncol 19: 2856-2864, 2001. (Pubitemid 32538195)
13. Autzen P, Robson CN, Bjartell A, Malcolm AJ, Johnson MI, Neal DE and Hamdy FC: Bone morphogenetic protein 6 in skeletal metastases from prostate cancer and other common human malignancies. Br J Cancer 78: 1219-1223, 1998.
14. Lehr JE and Pienta KJ: Preferential adhesion of prostate cancer cells to a human bone marrow endothelial cell line. J Natl Cancer Inst 90: 118-123, 1998.
15. Chay CH, Cooper CR, Gendernalik JD, Dhanasekaran SM, Chinnaiyan AM, Rubin MA, Schmaier AH and Pienta KJ: A functional thrombin receptor (PAR1) is expressed on bone-derived prostate cancer cell lines. Urology 60: 760-765, 2002.
16. Kumar CC: Integrin alpha v beta 3 as a therapeutic target for blocking tumor-induced angiogenesis. Curr Drug Targets 4: 123-131, 2003.
17. Cooper CR, Chay CH and Pienta KJ: The role of alpha(v)beta(3) in prostate cancer progression. Neoplasia 4: 191-194, 2002.
18. Dai J, Kitagawa Y, Zhang J, Yao Z, Mizokami A, Cheng S, Nor J, McCauley LK, Taichman RS and Keller ET: Vascular endothelial growth factor contributes to the prostate cancer-induced osteoblast differentiation mediated by bone morphogenetic protein. Cancer Res 64: 994-999, 2004.
19. Krupski T, Harding MA, Herce ME, Gulding KM, Stoler MH and Theodorescu D: The role of vascular endothelial growth factor in the tissue-specific in vivo growth of prostate cancer cells. Growth Factors 18: 287-302, 2001.
20. Chen J, De S, Brainard J and Byzova TV: Metastatic properties of prostate cancer cells are controlled by VEGF. Cell Commun Adhes 11: 1-11, 2004.
21. Khodavirdi AC, Song Z, Yang S, Zhong C, Wang S, Wu H, Pritchard C, Nelson PS and Roy-Burman P: Increased expression of osteopontin contributes to the progression of prostate cancer. Cancer Res 66: 883-888, 2006.
22. Fizazi K, Yang J, Peleg S, Sikes CR, Kreimann EL, Daliani D, Olive M, Raymond KA, Janus TJ, Logothetis CJ, Karsenty G and Navone NM: Prostate cancer cell-osteoblast interaction shifts expression of growth/survival-related genes in prostate cancer and reduces expression of osteoprotegerin in osteoblasts. Clin Cancer Res 9: 2587-2597, 2003.
23. Jacob K, Webber M, Benayahu D and Kleinman HK: Osteonectin promotes prostate cancer cell migration and invasion: a possible mechanism for metastasis to bone. Cancer Res 59: 4453-4457, 1999.
24. Zhang JH, Tang J, Wang J, Ma W, Zheng W, Yoneda T and Chen J: Over-expression of bone sialoprotein enhances bone metastasis of human breast cancer cells in a mouse model. Int J Oncol 23: 1043-1048, 2003.
25. Denhardt DT, Giachelli CM and Rittling SR: Role of osteopontin in cellular signaling and toxicant injury. Annu Rev Pharmacol Toxicol 41: 723-749, 2001.
26. Rosol TJ: Pathogenesis of bone metastases: role of tumor-related proteins. J Bone Miner Res 15: 844-850, 2000.
27. Moursi AM, Damsky CH, Lull J, Zimmerman D, Doty SB, Aota S and Globus RK: Fibronectin regulates calvarial osteoblast differentiation. J Cell Sci 109: 1369-1380, 1996.
28. Moursi AM, Globus RK and Damsky CH: Interactions between integrin receptors and fibronectin are required for calvarial osteoblast differentiation in vitro. J Cell Sci 110: 2187-2196, 1997.
29. Globus RK, Doty SB, Lull JC, Holmuhamedov E, Humphries MJ and Damsky CH: Fibronectin is a survival factor for differentiated osteoblasts. J Cell Sci 111: 1385-1393, 1998.
30. Termine JD, Kleinman HK, Whitson SW, Conn KM, McGarvey ML and Martin GR: Osteonectin, a bone-specific protein linking mineral to collagen. Cell 26: 99-105, 1981.
31. Delany AM, Amling M, Priemel M, Howe C, Baron R and Canalis E: Osteopenia and decreased bone formation in osteonectin-deficient mice. J Clin Invest 105: 915-923, 2000.
32. Bornstein P, Armstrong LC, Hankenson KD, Kyriakides TR and Yang Z: Thrombospondin 2, a matricellular protein with diverse functions. Matrix Biol 19: 557-568, 2000.
33. Hankenson KD and Bornstein P: The secreted protein thrombospondin 2 is an autocrine inhibitor of marrow stromal cell proliferation. J Bone Miner Res 17: 415-425, 2002.
34. Hankenson KD, James IE, Apone S, Stroup GB, Blake SM, Liang X, Lark MW and Bornstein P: Increased osteoblasto-genesis and decreased bone resorption protect against ovariectomy-induced bone loss in thrombospondin-2-null mice. Matrix Biol 24: 362-370, 2005.
35. Thapa N, Kang KB and Kim IS: Beta ig-h3 mediates osteoblast adhesion and inhibits differentiation. Bone 36: 232-242, 2005.
36. Skonier J, Bennett K, Rothwell V, Kosowski S, Plowman G, Wallace P, Edelhoff S, Disteche C, Neubauer M, Marquardt H, et al: Beta ig-h3: a transforming growth factor-beta-responsive gene encoding a secreted protein that inhibits cell attachment in vitro and suppresses the growth of CHO cells in nude mice. DNA Cell Biol 13: 571-584, 1994.
37. Ducy P, Desbois C, Boyce B, Pinero G, Story B, Dunstan C, Smith E, Bonadio J, Goldstein S, Gundberg C, Bradley A and Karsenty G: Increased bone formation in osteocalcin-deficient mice. Nature 382: 448-452, 1996.
38. Luo G, Ducy P, McKee MD, Pinero GJ, Loyer E, Behringer RR and Karsenty G: Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386: 78-81, 1997.
39. Hunter GK and Goldberg HA: Nucleation of hydroxyapatite by bone sialoprotein. Proc Natl Acad Sci USA 90: 8562-8565, 1993.
40. Ganss B, Kim RH and Sodek J: Bone sialoprotein. Crit Rev Oral Biol Med 10: 79-98, 1999.
41. Hultenby K, Reinholt FP and Heinegard D: Distribution of integrin subunits on rat metaphyseal osteoclasts and osteoblasts. Eur J Cell Biol 62: 86-93, 1993.
42. Reinholt FP, Hultenby K, Oldberg A and Heinegard D: Osteopontin - a possible anchor of osteoclasts to bone. Proc Natl Acad Sci USA 87: 4473-4475, 1990.
43. Ishijima M, Tsuji K, Rittling SR, Yamashita T, Kurosawa H, Denhardt DT, Nifuji A and Noda M: Resistance to unloading-induced three-dimensional bone loss in osteopontin-deficient mice. J Bone Miner Res 17: 661-667, 2002.
44. Ihara H, Denhardt DT, Furuya K, Yamashita T, Muguruma Y, Tsuji K, Hruska KA, Higashio K, Enomoto S, Nifuji A, Rittling SR and Noda M: Parathyroid hormone-induced bone resorption does not occur in the absence of osteopontin. J Biol Chem 276: 13065-13071, 2001.
45. Young MF: Bone matrix proteins: their function, regulation, and relationship to osteoporosis. Osteoporos Int 14 (suppl 3): 35-42, 2003.
46. Wadhwa S, Embree MC, Bi Y and Young MF: Regulation, regulatory activities, and function of biglycan. Crit Rev Eukaryot Gene Expr 14: 301-315, 2004.
47. Mochida Y, Parisuthiman D and Yamauchi M: Biglycan is a positive modulator of BMP-2 induced osteoblast differentiation. Adv Exp Med Biol 585: 101-113, 2006.
48. Chen XD, Fisher LW, Robey PG and Young MF: The small leucine-rich proteoglycan biglycan modulates BMP-4-induced osteoblast differentiation. FASEB J 18: 948-958, 2004.
49. Sommerfeldt DW and Rubin CT: Biology of bone and how it orchestrates the form and function of the skeleton. Eur Spine J 10 (suppl 2): 86-95, 2001.
50. Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Boyle WJ and Riggs BL: The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption. J Bone Miner Res 15: 2-12, 2000.
51. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Luthy R, Nguyen HQ, Wooden S, Bennett L, Boone T, Shimamoto G, DeRose M, Elliott R, Colombero A, Tan HL, Trail G, Sullivan J, Davy E, Bucay N, Renshaw-Gegg L, Hughes TM, Hill D, Pattison W, Campbell P, Sander S, Van G, Tarpley J, Derby P, Lee R and Boyle WJ: Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89: 309-319, 1997.
52. Guise TA, Mohammad KS, Clines G, Stebbins EG, Wong DH, Higgins LS, Vessella R, Corey E, Padalecki S, Suva L and Chirgwin JM: Basic mechanisms responsible for osteolytic and osteoblastic bone metastases. Clin Cancer Res 12: 6213s-6216s, 2006.
53. Lee SK and Lorenzo J: Cytokines regulating osteoclast formation and function. Curr Opin Rheumatol 18: 411-418, 2006.
54. Mehrotra M, Krane SM, Walters K and Pilbeam C: Differential regulation of platelet-derived growth factor stimulated migration and proliferation in osteoblastic cells. J Cell Biochem 93: 741-752, 2004.
55. Yi B, Williams PJ, Niewolna M, Wang Y and Yoneda T: Tumor-derived platelet-derived growth factor-BB plays a critical role in osteosclerotic bone metastasis in an animal model of human breast cancer. Cancer Res 62: 917-923, 2002.
56. Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, Hennekens CH and Pollak M: Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 279: 563-566, 1998.
57. Shariat SF, Lamb DJ, Kattan MW, Nguyen C, Kim J, Beck J, Wheeler TM and Slawin KM: Association of preoperative plasma levels of insulin-like growth factor I and insulin-like growth factor binding proteins-2 and -3 with prostate cancer invasion, progression, and metastasis. J Clin Oncol 20: 833-841, 2002.
58. Chan JM, Stampfer MJ, Ma J, Gann P, Gaziano JM, Pollak M and Giovannucci E: Insulin-like growth factor-I (IGF-I) and IGF binding protein-3 as predictors of advanced-stage prostate cancer. J Natl Cancer Inst 94: 1099-1106, 2002.
59. Rubin J, Fan X, Rahnert J, Sen B, Hsieh CL, Murphy TC, Nanes MS, Horton LG, Beamer WG and Rosen CJ: IGF-I secretion by prostate carcinoma cells does not alter tumor-bone cell interactions in vitro or in vivo. Prostate 66: 789-800, 2006.
60. Mansson PE, Adams P, Kan M and McKeehan WL: Heparin-binding growth factor gene expression and receptor characteristics in normal rat prostate and two transplantable rat prostate tumors. Cancer Res 49: 2485-2494, 1989.
61. Dunstan CR, Boyce R, Boyce BF, Garrett IR, Izbicka E, Burgess WH and Mundy GR: Systemic administration of acidic fibroblast growth factor (FGF-1) prevents bone loss and increases new bone formation in ovariectomized rats. J Bone Miner Res 14: 953-959, 1999.
62. Gerber HP, Vu TH, Ryan AM, Kowalski J, Werb Z and Ferrara N: VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med 5: 623-628, 1999.
63. Street J, Bao M, deGuzman L, Bunting S, Peale FV Jr, Ferrara N, Steinmetz H, Hoeffel J, Cleland JL, Daugherty A, van Bruggen N, Redmond HP, Carano RA and Filvaroff EH: Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA 99: 9656-9661, 2002.
64. Midy V and Plouet J: Vasculotropin/vascular endothelial growth factor induces differentiation in cultured osteoblasts. Biochem Biophys Res Commun 199: 380-386, 1994.
65. Chen G, Shukeir N, Potti A, Sircar K, Aprikian A, Goltzman D and Rabbani SA: Up-regulation of Wnt-1 and beta-catenin production in patients with advanced metastatic prostate carcinoma: potential pathogenetic and prognostic implications. Cancer 101: 1345-1356, 2004.
66. Hall CL, Kang S, MacDougald OA and Keller ET: Role of Wnts in prostate cancer bone metastases. J Cell Biochem 97: 661-672, 2006.
67. Tian E, Zhan F, Walker R, Rasmussen E, Ma Y, Barlogie B and Shaughnessy JD Jr: The role of the Wnt-signaling antagonist DKK1 in the development of osteolytic lesions in multiple myeloma. N Engl J Med 349: 2483-2494, 2003.
68. Schluter KD, Katzer C and Piper HM: An N-terminal PTHrP peptide fragment void of a PTH/PTHrP-receptor binding domain activates cardiac ET(A) receptors. Br J Pharmacol 132: 427-432, 2001.
69. Cramer SD, Chen Z and Peehl DM: Prostate specific antigen cleaves parathyroid hormone-related protein in the PTH-like domain: inactivation of PTHrP-stimulated cAMP accumulation in mouse osteoblasts. J Urol 156: 526-531, 1996.
70. Achbarou A, Kaiser S, Tremblay G, Ste-Marie LG, Brodt P, Goltzman D and Rabbani SA: Urokinase overproduction results in increased skeletal metastasis by prostate cancer cells in vivo. Cancer Res 54: 2372-2377, 1994.
71. Rabbani SA, Desjardins J, Bell AW, Banville D, Mazar A, Henkin J and Goltzman D: An amino-terminal fragment of urokinase isolated from a prostate cancer cell line (PC-3) is mitogenic for osteoblast-like cells. Biochem Biophys Res Commun 173: 1058-1064, 1990.
72. Koutsilieris M: Osteoblastic metastasis in advanced prostate cancer. Anticancer Res 13: 443-449, 1993.
73. Killian CS, Corral DA, Kawinski E and Constantine RI: Mitogenic response of osteoblast cells to prostate-specific antigen suggests an activation of latent TGF-beta and a proteolytic modulation of cell adhesion receptors. Biochem Biophys Res Commun 192: 940-947, 1993.
74. Cohen P, Graves HC, Peehl DM, Kamarei M, Giudice LC and Rosenfeld RG: Prostate-specific antigen (PSA) is an insulin-like growth factor binding protein-3 protease found in seminal plasma. J Clin Endocrinol Metab 75: 1046-1053, 1992.
75. Cohen P, Peehl DM, Graves HC and Rosenfeld RG: Biological effects of prostate specific antigen as an insulin-like growth factor binding protein-3 protease. J Endocrinol 142: 407-415, 1994.
76. Vakar-Lopez F, Cheng CJ, Kim J, Shi GG, Troncoso P, Tu SM, Yu-Lee LY and Lin SH: Up-regulation of MDA-BF-1, a secreted isoform of ErbB3, in metastatic prostate cancer cells and activated osteoblasts in bone marrow. J Pathol 203: 688-695, 2004.
77. Liang AK, Liu J, Mao SA, Siu VS, Lee YC and Lin SH: Expression of recombinant MDA-BF-1 with a kinase recognition site and a 7-histidine tag for receptor binding and purification. Protein Expr Purif 44: 58-64, 2005.
78. Choueiri MB, Tu SM, Yu-Lee LY and Lin SH: The central role of osteoblasts in the metastasis of prostate cancer. Cancer Metastasis Rev 25: 601-609, 2006.
79. Takuwa Y, Masaki T and Yamashita K: The effects of the endothelin family peptides on cultured osteoblastic cells from rat calvariae. Biochem Biophys Res Commun 170: 998-1005, 1990.
80. Nelson JB, Hedican SP, George DJ, Reddi AH, Piantadosi S, Eisenberger MA and Simons JW: Identification of endothelin-1 in the pathophysiology of metastatic adenocarcinoma of the prostate. Nat Med 1: 944-949, 1995.
81. Granchi S, Brocchi S, Bonaccorsi L, Baldi E, Vinci MC, Forti G, Serio M and Maggi M: Endothelin-1 production by prostate cancer cell lines is up-regulated by factors involved in cancer progression and down-regulated by androgens. Prostate 49: 267-277, 2001.
82. Chiao JW, Moonga BS, Yang YM, Kancherla R, Mittelman A, Wu-Wong JR and Ahmed T: Endothelin-1 from prostate cancer cells is enhanced by bone contact which blocks osteoclastic bone resorption. Br J Cancer 83: 360-365, 2000.
83. Mohammad KS and Guise TA: Mechanisms of osteoblastic metastases: role of endothelin-1. Clin Orthop Relat Res 415: S67-S74, 2003.
84. Yin JJ, Mohammad KS, Kakonen SM, Harris S, Wu-Wong JR, Wessale JL, Padley RJ, Garrett IR, Chirgwin JM and Guise TA: A causal role for endothelin-1 in the pathogenesis of osteoblastic bone metastases. Proc Natl Acad Sci USA 100: 10954-10959, 2003.
85. Carducci MA, Padley RJ, Breul J, Vogelzang NJ, Zonnenberg BA, Daliani DD, Schulman CC, Nabulsi AA, Humerickhouse RA, Weinberg MA, Schmitt JL and Nelson JB: Effect of endothelin-A receptor blockade with atrasentan on tumor progression in men with hormone-refractory prostate cancer: a randomized, phase II, placebo-controlled trial. J Clin Oncol 21: 679-689, 2003.
86. Nelson JB, Chan-Tack K, Hedican SP, Magnuson SR, Opgenorth TJ, Bova GS and Simons JW: Endothelin-1 production and decreased endothelin B receptor expression in advanced prostate cancer. Cancer Res 56: 663-668, 1996.
87. Clines GA, Mohammad KS, Bao Y, Stephens OW, Suva LJ, Shaughnessy JD Jr, Fox JW, Chirgwin JM and Guise TA: Dickkopf homolog 1 mediates endothelin-1-stimulated new bone formation. Mol Endocrinol 21: 486-498, 2007.
88. Reddi AH, Roodman D, Freeman C and Mohla S: Mechanisms of tumor metastasis to the bone: challenges and opportunities. J Bone Miner Res 18: 190-194, 2003.
89. Oades GM, Coxon J and Colston KW: The potential role of bisphosphonates in prostate cancer. Prostate Cancer Prostatic Dis 5: 264-272, 2002.
90. Yonou H, Ochiai A, Goya M, Kanomata N, Hokama S, Morozumi M, Sugaya K, Hatano T and Ogawa Y: Intraosseous growth of human prostate cancer in implanted adult human bone: relationship of prostate cancer cells to osteoclasts in osteoblastic metastatic lesions. Prostate 58: 406-413, 2004. (Pubitemid 38295034)
91. Garnero P, Buchs N, Zekri J, Rizzoli R, Coleman RE and Delmas PD: Markers of bone turnover for the management of patients with bone metastases from prostate cancer. Br J Cancer 82: 858-864, 2000.
92. Lipton A, Small E, Saad F, Gleason D, Gordon D, Smith M, Rosen L, Kowalski MO, Reitsma D and Seaman J: The new bisphosphonate, Zometa (zoledronic acid), decreases skeletal complications in both osteolytic and osteoblastic lesions: a comparison to pamidronate. Cancer Invest 20 (suppl 2): 45-54, 2002.
93. Vessella RL and Corey E: Targeting factors involved in bone remodeling as treatment strategies in prostate cancer bone metastasis. Clin Cancer Res 12: 6285s-6290s, 2006.
94. Smith MR, Lee WC, Brandman J, Wang Q, Botteman M and Pashos CL: Gonadotropin-releasing hormone agonists and fracture risk: a claims-based cohort study of men with nonmetastatic prostate cancer. J Clin Oncol 23: 7897-7903, 2005.
95. Krupski TL, Smith MR, Lee WC, Pashos CL, Brandman J, Wang Q, Botteman M and Litwin MS: Natural history of bone complications in men with prostate carcinoma initiating androgen deprivation therapy. Cancer 101: 541-549, 2004.
96. Smith MR, McGovern FJ, Zietman AL, Fallon MA, Hayden DL, Schoenfeld DA, Kantoff PW and Finkelstein JS: Pamidronate to prevent bone loss during androgen-deprivation therapy for prostate cancer. N Engl J Med 345: 948-955, 2001.
97. Ye L, Lewis-Russell JM, Kynaston H and Jiang WG: Bone morphogenetic proteins and their receptor signaling in prostate cancer. Histol Histopathol (In press).
98. Ide H, Yoshida T, Matsumoto N, Aoki K, Osada Y, Sugimura T and Terada M: Growth regulation of human prostate cancer cells by bone morphogenetic protein-2. Cancer Res 57: 5022-5027, 1997.
99. Thomas R, Anderson WA, Raman V and Reddi AH: Androgen-dependent gene expression of bone morphogenetic protein 7 in mouse prostate. Prostate 37: 236-245, 1998.
100. Kakehi Y, Segawa T, Wu XX, Kulkarni P, Dhir R and Getzenberg RH: Down-regulation of macrophage inhibitory cytokine-1/prostate derived factor in benign prostatic hyperplasia. Prostate 59: 351-356, 2004.
101. Tamada H, Kitazawa R, Gohji K and Kitazawa S: Epigenetic regulation of human bone morphogenetic protein 6 gene expression in prostate cancer. J Bone Miner Res 16: 487-496, 2001.
102. Kim IY, Lee DH, Lee DK, Ahn HJ, Kim MM, Kim SJ and Morton RA: Loss of expression of bone morphogenetic protein receptor type II in human prostate cancer cells. Oncogene 23: 7651-7659, 2004.
103. Thomas R, True LD, Lange PH and Vessella RL: Placental bone morphogenetic protein (PLAB) gene expression in normal, pre-malignant and malignant human prostate: relation to tumor development and progression. Int J Cancer 93: 47-52, 2001.
104. Ye L, Lewis-Russell JM, Davies G, Sanders AJ, Kynaston H and Jiang WG: Hepatocyte growth factor up-regulates the expression of the bone morphogenetic protein (BMP) receptors, BMPR-IB and BMPR-II, in human prostate cancer cells. Int J Oncol 30: 521-529, 2007.
105. Ye L, Lewis-Russell JM, Kynaston H and Jiang WG: Endogenous BMP-7 controls the motility of prostate cancer cells through regulation of BMP antagonists. J Urol (In press).