Recent advances in bone-targeted therapies of metastatic prostate cancer

Cancer Treatment Reviews

Volumn 40, Issue 6, 2014, Pages 730-738

  Deng, Xiyun ^a,c   He, Guangchun ^a   Liu, Junwen ^b   Luo, Feijun ^b   Peng, Xiaoning ^a   Tang, Shigang ^a   Gao, Zhiyong ^a   Lin, Qinlu ^b   Keller, Jill M ^d   Yang, Tao ^b,c   Keller, Evan T ^d  

^a HUNAN NORMAL UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY OF FORESTRY AND TECHNOLOGY   (China)

^c Changsha Microworld Biotech Company   (China)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Bone metastasis; Molecular targeted therapy; Osteoblasts; Osteoclasts; Prostate cancer; RANKL

Indexed keywords

ANDROGEN; ATRASENTAN; BISPHOSPHONIC ACID DERIVATIVE; BOSUTINIB; CATHEPSIN K; CLODRONIC ACID; DASATINIB; DENOSUMAB; DOCETAXEL; ENDOTHELIN A RECEPTOR; ETARACIZUMAB; GELATINASE A; GELATINASE B; GLPG 0187; INTEGRIN; INTERSTITIAL COLLAGENASE; LEXIDRONAM SAMARIUM SM 153; LY 2109761; MATRILYSIN; MK 0429; OSTEOCLAST DIFFERENTIATION FACTOR; PHOSPHOTRANSFERASE INHIBITOR; PREDNISONE; PROTEIN TYROSINE KINASE; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; SARACATINIB; SPRTYCEL; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VILY 2109761TAXIN; ZIBOTENTAN;

BONE MATRIX; BONE METASTASIS; CANCER SURVIVAL; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; MOLECULARLY TARGETED THERAPY; NONHUMAN; OSSIFICATION; PROSTATE CANCER; QUALITY OF LIFE; REVIEW; TUMOR MICROENVIRONMENT;

BONE METASTASIS; MOLECULAR TARGETED THERAPY; OSTEOBLASTS; OSTEOCLASTS; PROSTATE CANCER; RANKL;

ANIMALS; ANTINEOPLASTIC AGENTS; BONE DENSITY CONSERVATION AGENTS; BONE NEOPLASMS; BONE RESORPTION; CATHEPSIN K; DIPHOSPHONATES; DISEASE MODELS, ANIMAL; HUMANS; MALE; MOLECULAR TARGETED THERAPY; OSTEOGENESIS; PROSTATIC NEOPLASMS; RADIOISOTOPES; RANK LIGAND; SIGNAL TRANSDUCTION; TISSUE INHIBITOR OF METALLOPROTEINASES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84899927795     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2014.04.003     Document Type: Review

References (78)

1. Siegel R., DeSantis C., Virgo K., Stein K., Mariotto A., Smith T., et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 2012, 62:220-241.
2. Dai B., Ye D.W., Kong Y.Y., Shen Y.J., Wang B.H. Individualized prostate biopsy strategy for Chinese patients with different prostate-specific antigen levels. Asian J Androl 2008, 10:325-331.
3. Clinicopathological statistics on registered prostate cancer patients in Japan: 2000 report from the Japanese Urological Association. Int J Urol 2005;12:46-61.
4. Bubendorf L., Schopfer A., Wagner U., Sauter G., Moch H., Willi N., et al. Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 2000, 31:578-583.
5. Yonou H., Ochiai A., Goya M., Kanomata N., Hokama S., Morozumi M., et al. Intraosseous growth of human prostate cancer in implanted adult human bone: relationship of prostate cancer cells to osteoclasts in osteoblastic metastatic lesions. Prostate 2004, 58:406-413.
6. Ye L., Kynaston H.G., Jiang W.G. Bone metastasis in prostate cancer: molecular and cellular mechanisms (Review). Int J Mol Med 2007, 20:103-111.
7. Madan R.A., Arlen P.M. Recent advances revolutionize treatment of metastatic prostate cancer. Future Oncol 2013, 9:1133-1144.
8. Yin L., Hu Q., Hartmann R.W. Recent progress in pharmaceutical therapies for castration-resistant prostate cancer. Int J Mol Sci 2013, 14:13958-13978.
9. Heidegger I., Massoner P., Eder I.E., Pircher A., Pichler R., Aigner F., et al. Novel therapeutic approaches for the treatment of castration-resistant prostate cancer. J Steroid Biochem Mol Biol 2013, 138:248-256.
10. Agarwal N., Sonpavde G., Sternberg C.N. Novel molecular targets for the therapy of castration-resistant prostate cancer. Eur Urol 2012, 61:950-960.
11. Cher M.L. Mechanisms governing bone metastasis in prostate cancer. Curr Opin Urol 2001, 11:483-488.
12. Fidler I.J., Kripke M.L. Metastasis results from preexisting variant cells within a malignant tumor. Science 1977, 197:893-895.
13. Trouvin A.P., Goeb V. Receptor activator of nuclear factor-kappaB ligand and osteoprotegerin: maintaining the balance to prevent bone loss. Clin Interv Aging 2010, 5:345-354.
14. Baud'huin M., Duplomb L., Ruiz Velasco C., Fortun Y., Heymann D., Padrines M. Key roles of the OPG-RANK-RANKL system in bone oncology. Expert Rev Anticancer Ther 2007, 7:221-232.
15. Chinni S.R., Yamamoto H., Dong Z., Sabbota A., Bonfil R.D., Cher M.L. CXCL12/CXCR4 transactivates HER2 in lipid rafts of prostate cancer cells and promotes growth of metastatic deposits in bone. Mol Cancer Res 2008, 6:446-457.
16. Bonfil R.D., Chinni S., Fridman R., Kim H.R., Cher M.L. Proteases, growth factors, chemokines, and the microenvironment in prostate cancer bone metastasis. Urol Oncol 2007, 25:407-411.
17. Brubaker K.D., Vessella R.L., True L.D., Thomas R., Corey E. Cathepsin K mRNA and protein expression in prostate cancer progression. J Bone Miner Res 2003, 18:222-230.
18. Smith H.W., Marshall C.J. Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol 2010, 11:23-36.
19. Edwards J. Src kinase inhibitors: an emerging therapeutic treatment option for prostate cancer. Expert Opin Investig Drugs 2010, 19:605-614.
20. Rosenthal M.A., Davidson P., Rolland F., Campone M., Xue L., Han T.H., et al. Evaluation of the safety, pharmacokinetics and treatment effects of an alpha(nu)beta(3) integrin inhibitor on bone turnover and disease activity in men with hormone-refractory prostate cancer and bone metastases. Asia Pac J Clin Oncol 2010, 6:42-48.
21. Clarke N.W., Hart C.A., Brown M.D. Molecular mechanisms of metastasis in prostate cancer. Asian J Androl 2009, 11:57-67.
22. Russell R.G., Xia Z., Dunford J.E., Oppermann U., Kwaasi A., Hulley P.A., et al. Bisphosphonates: an update on mechanisms of action and how these relate to clinical efficacy. Ann N Y Acad Sci 2007, 1117:209-257.
23. Ibrahim A., Scher N., Williams G., Sridhara R., Li N., Chen G., et al. Approval summary for zoledronic acid for treatment of multiple myeloma and cancer bone metastases. Clin Cancer Res 2003, 9:2394-2399.
24. Prakash G., Gautam G. Optimal bone health management strategies in patients with prostate cancer. Indian J Urol 2013, 29:89-99.
25. Rodrigues P., Hering F.O., Meller A. Adjuvant effect of IV clodronate on the delay of bone metastasis in high-risk prostate cancer patients: a prospective study. Cancer Res Treat 2011, 43:231-235.
26. Dearnaley D.P., Mason M.D., Parmar M.K., Sanders K., Sydes M.R. Adjuvant therapy with oral sodium clodronate in locally advanced and metastatic prostate cancer: long-term overall survival results from the MRC PR04 and PR05 randomised controlled trials. Lancet Oncol 2009, 10:872-876.
27. Goessl C., Katz L., Dougall W.C., Kostenuik P.J., Zoog H.B., Braun A., et al. The development of denosumab for the treatment of diseases of bone loss and cancer-induced bone destruction. Ann N Y Acad Sci 2012, 1263:29-40.
28. Smith M.R., Egerdie B., Hernandez Toriz N., Feldman R., Tammela T.L., Saad F., et al. Denosumab in men receiving androgen-deprivation therapy for prostate cancer. N Engl J Med 2009, 361:745-755.
29. Fizazi K., Carducci M., Smith M., Damiao R., Brown J., Karsh L., et al. Denosumab versus zoledronic acid for treatment of bone metastases in men with castration-resistant prostate cancer: a randomised, double-blind study. Lancet 2011, 377:813-822.
30. Smith M.R., Saad F., Coleman R., Shore N., Fizazi K., Tombal B., et al. Denosumab and bone-metastasis-free survival in men with castration-resistant prostate cancer: results of a phase 3, randomised, placebo-controlled trial. Lancet 2012, 379:39-46.
31. Ignatoski K.M., Escara-Wilke J.F., Dai J.L., Lui A., Dougall W., Daignault S., et al. RANKL inhibition is an effective adjuvant for docetaxel in a prostate cancer bone metastases model. Prostate 2008, 68:820-829.
32. Virk M.S., Petrigliano F.A., Liu N.Q., Chatziioannou A.F., Stout D., Kang C.O., et al. Influence of simultaneous targeting of the bone morphogenetic protein pathway and RANK/RANKL axis in osteolytic prostate cancer lesion in bone. Bone 2009, 44:160-167.
33. Virk M.S., Alaee F., Petrigliano F.A., Sugiyama O., Chatziioannou A.F., Stout D., et al. Combined inhibition of the BMP pathway and the RANK-RANKL axis in a mixed lytic/blastic prostate cancer lesion. Bone 2011, 48:578-587.
34. Armstrong A.P., Miller R.E., Jones J.C., Zhang J., Keller E.T., Dougall W.C. RANKL acts directly on RANK-expressing prostate tumor cells and mediates migration and expression of tumor metastasis genes. Prostate 2008, 68:92-104.
35. Miller R.E., Roudier M., Jones J., Armstrong A., Canon J., Dougall W.C. RANK ligand inhibition plus docetaxel improves survival and reduces tumor burden in a murine model of prostate cancer bone metastasis. Mol Cancer Ther 2008, 7:2160-2169.
36. Yu E.Y., Massard C., Gross M.E., Carducci M.A., Culine S., Hudes G., et al. Once-daily dasatinib: expansion of phase II study evaluating safety and efficacy of dasatinib in patients with metastatic castration-resistant prostate cancer. Urology 2011, 77:1166-1171.
37. Yu E.Y., Wilding G., Posadas E., Gross M., Culine S., Massard C., et al. Phase II study of dasatinib in patients with metastatic castration-resistant prostate cancer. Clin Cancer Res 2009, 15:7421-7428.
38. Araujo J.C., Mathew P., Armstrong A.J., Braud E.L., Posadas E., Lonberg M., et al. Dasatinib combined with docetaxel for castration-resistant prostate cancer: results from a phase 1-2 study. Cancer 2012, 118:63-71.
39. Antonarakis E.S., Heath E.I., Posadas E.M., Yu E.Y., Harrison M.R., Bruce J.Y., et al. A phase 2 study of KX2-391, an oral inhibitor of Src kinase and tubulin polymerization, in men with bone-metastatic castration-resistant prostate cancer. Cancer Chemother Pharmacol 2013, 71:883-892.
40. Rabbani S.A., Valentino M.L., Arakelian A., Ali S., Boschelli F. SKI-606 (Bosutinib) blocks prostate cancer invasion, growth, and metastasis in vitro and in vivo through regulation of genes involved in cancer growth and skeletal metastasis. Mol Cancer Ther 2010, 9:1147-1157.
41. Gupta A., Cao W., Chellaiah M.A. Integrin alphavbeta3 and CD44 pathways in metastatic prostate cancer cells support osteoclastogenesis via a Runx2/Smad 5/receptor activator of NF-kappaB ligand signaling axis. Mol Cancer 2012, 11:66.
42. ν integrins, in progressive castration-resistant prostate cancer with bone metastases after chemotherapy. Eur Urol 2013.
43. van der Horst G., van den Hoogen C., Buijs J.T., Cheung H., Bloys H., Pelger R.C., et al. Targeting of alpha(v)-integrins in stem/progenitor cells and supportive microenvironment impairs bone metastasis in human prostate cancer. Neoplasia 2011, 13:516-525.
44. Pinto A., Merino M., Zamora P., Redondo A., Castelo B., Espinosa E. Targeting the endothelin axis in prostate carcinoma. Tumour Biol 2012, 33:421-426.
45. Armstrong A.J., Creel P., Turnbull J., Moore C., Jaffe T.A., Haley S., et al. A phase I-II study of docetaxel and atrasentan in men with castration-resistant metastatic prostate cancer. Clin Cancer Res 2008, 14:6270-6276.
46. Carducci M.A., Saad F., Abrahamsson P.A., Dearnaley D.P., Schulman C.C., North S.A., et al. A phase 3 randomized controlled trial of the efficacy and safety of atrasentan in men with metastatic hormone-refractory prostate cancer. Cancer 2007, 110:1959-1966.
47. Nelson J.B., Love W., Chin J.L., Saad F., Schulman C.C., Sleep D.J., et al. Phase 3, randomized, controlled trial of atrasentan in patients with nonmetastatic, hormone-refractory prostate cancer. Cancer 2008, 113:2478-2487.
48. Warren R., Liu G. ZD4054: a specific endothelin A receptor antagonist with promising activity in metastatic castration-resistant prostate cancer. Expert Opin Investig Drugs 2008, 17:1237-1245.
49. James N.D., Caty A., Borre M., Zonnenberg B.A., Beuzeboc P., Morris T., et al. Safety and efficacy of the specific endothelin-A receptor antagonist ZD4054 in patients with hormone-resistant prostate cancer and bone metastases who were pain free or mildly symptomatic: a double-blind, placebo-controlled, randomised, phase 2 trial. Eur Urol 2009, 55:1112-1123.
50. James N.D., Caty A., Payne H., Borre M., Zonnenberg B.A., Beuzeboc P., et al. Final safety and efficacy analysis of the specific endothelin A receptor antagonist zibotentan (ZD4054) in patients with metastatic castration-resistant prostate cancer and bone metastases who were pain-free or mildly symptomatic for pain: a double-blind, placebo-controlled, randomized Phase II trial. BJU Int 2010, 106:966-973.
51. Nelson J.B., Fizazi K., Miller K., Higano C., Moul J.W., Akaza H., et al. Phase 3, randomized, placebo-controlled study of zibotentan (ZD4054) in patients with castration-resistant prostate cancer metastatic to bone. Cancer 2012, 118:5709-5718.
52. Fizazi K.S., Higano C.S., Nelson J.B., Gleave M., Miller K., Morris T., et al. Phase III, randomized, placebo-controlled study of docetaxel in combination with zibotentan in patients with metastatic castration-resistant prostate cancer. J Clin Oncol 2013, 31:1740-1747.
53. Vengalil S., O'Sullivan J.M., Parker C.C. Use of radionuclides in metastatic prostate cancer: pain relief and beyond. Curr Opin Support Palliat Care 2012, 6:310-315.
54. Longo J., Lutz S., Johnstone C. Samarium-153-ethylene diamine tetramethylene phosphonate, a beta-emitting bone-targeted radiopharmaceutical, useful for patients with osteoblastic bone metastases. Cancer Manag Res 2013, 5:235-242.
55. Sartor O., Reid R.H., Hoskin P.J., Quick D.P., Ell P.J., Coleman R.E., et al. Samarium-153-Lexidronam complex for treatment of painful bone metastases in hormone-refractory prostate cancer. Urology 2004, 63:940-945.
56. Fizazi K., Beuzeboc P., Lumbroso J., Haddad V., Massard C., Gross-Goupil M., et al. Phase II trial of consolidation docetaxel and samarium-153 in patients with bone metastases from castration-resistant prostate cancer. J Clin Oncol 2009, 27:2429-2435.
57. Morris M.J., Pandit-Taskar N., Carrasquillo J., Divgi C.R., Slovin S., Kelly W.K., et al. Phase I study of samarium-153 lexidronam with docetaxel in castration-resistant metastatic prostate cancer. J Clin Oncol. 2009, 27:2436-2442.
58. Tu S.M., Mathew P., Wong F.C., Jones D., Johnson M.M., Logothetis C.J. Phase I study of concurrent weekly docetaxel and repeated samarium-153 lexidronam in patients with castration-resistant metastatic prostate cancer. J Clin Oncol 2009, 27:3319-3324.
59. Jadvar H., Quinn D.I. Targeted alpha-particle therapy of bone metastases in prostate cancer. Clin Nucl Med 2013, 38:966-971.
60. Nilsson S., Franzen L., Parker C., Tyrrell C., Blom R., Tennvall J., et al. Bone-targeted radium-223 in symptomatic, hormone-refractory prostate cancer: a randomised, multicentre, placebo-controlled phase II study. Lancet Oncol 2007, 8:587-594.
61. Nilsson S., Strang P., Aksnes A.K., Franzen L., Olivier P., Pecking A., et al. A randomized, dose-response, multicenter phase II study of radium-223 chloride for the palliation of painful bone metastases in patients with castration-resistant prostate cancer. Eur J Cancer 2012, 48:678-686.
62. Parker C., Nilsson S., Heinrich D., Helle S.I., O'Sullivan J.M., Fossa S.D., et al. Alpha emitter radium-223 and survival in metastatic prostate cancer. N Engl J Med 2013, 369:213-223.
63. Okazaki I., Nabeshima K. Introduction: MMPs, ADAMs/ADAMTSs research products to achieve big dream. Anticancer Agents Med Chem 2012, 12:688-706.
64. Sottnik J.L., Zhang J., Macoska J.A., Keller E.T. The PCa tumor microenvironment. Cancer Microenviron 2011, 4:283-297.
65. Stellas D., Patsavoudi E. Inhibiting matrix metalloproteinases, an old story with new potentials for cancer treatment. Anticancer Agents Med Chem 2012, 12:707-717.
66. Annabi B., Bouzeghrane M., Currie J.C., Dulude H., Daigneault L., Garde S., et al. Inhibition of MMP-9 secretion by the anti-metastatic PSP94-derived peptide PCK3145 requires cell surface laminin receptor signaling. Anticancer Drugs 2006, 17:429-438.
67. Singh R.P., Raina K., Deep G., Chan D., Agarwal R. Silibinin suppresses growth of human prostate carcinoma PC-3 orthotopic xenograft via activation of extracellular signal-regulated kinase 1/2 and inhibition of signal transducers and activators of transcription signaling. Clin Cancer Res 2009, 15:613-621.
68. Deng X., He G., Levine A., Cao Y., Mullins C. Adenovirus-mediated expression of TIMP-1 and TIMP-2 in bone inhibits osteolytic degradation by human prostate cancer. Int J Cancer 2008, 122:209-218.
69. Shariat S.F., Roehrborn C.G., McConnell J.D., Park S., Alam N., Wheeler T.M., et al. Association of the circulating levels of the urokinase system of plasminogen activation with the presence of prostate cancer and invasion, progression, and metastasis. J Clin Oncol 2007, 25:349-355.
70. Fritz V., Noel D., Bouquet C., Opolon P., Voide R., Apparailly F., et al. Antitumoral activity and osteogenic potential of mesenchymal stem cells expressing the urokinase-type plasminogen antagonist amino-terminal fragment in a murine model of osteolytic tumor. Stem Cells 2008, 26:2981-2990.
71. Juarez P., Guise T.A. TGF-beta in cancer and bone: implications for treatment of bone metastases. Bone 2011, 48:23-29.
72. Mishra S., Tang Y., Wang L., deGraffenried L., Yeh I.T., Werner S., et al. Blockade of transforming growth factor-beta (TGFbeta) signaling inhibits osteoblastic tumorigenesis by a novel human prostate cancer cell line. Prostate 2011, 71:1441-1454.
73. Hu Z., Gupta J., Zhang Z., Gerseny H., Berg A., Chen Y.J., et al. Systemic delivery of oncolytic adenoviruses targeting transforming growth factor-beta inhibits established bone metastasis in a prostate cancer mouse model. Hum Gene Ther 2012, 23:871-882.
74. Wan X., Li Z.G., Yingling J.M., Yang J., Starbuck M.W., Ravoori M.K., et al. Effect of transforming growth factor beta (TGF-beta) receptor I kinase inhibitor on prostate cancer bone growth. Bone 2012, 50:695-703.
75. Cheng C.J., Ye X.C., Vakar-Lopez F., Kim J., Tu S.M., Chen D.T., et al. Bone microenvironment and androgen status modulate subcellular localization of ErbB3 in prostate cancer cells. Mol Cancer Res 2007, 5:675-684.
76. Fizazi K., Sikes C.R., Kim J., Yang J., Martinez L.A., Olive M.C., et al. High efficacy of docetaxel with and without androgen deprivation and estramustine in preclinical models of advanced prostate cancer. Anticancer Res 2004, 24:2897-2903.
77. Pfitzenmaier J., Quinn J.E., Odman A.M., Zhang J., Keller E.T., Vessella R.L., et al. Characterization of C4-2 prostate cancer bone metastases and their response to castration. J Bone Miner Res 2003, 18:1882-1888.
78. Rosol T.J., Tannehill-Gregg S.H., Corn S., Schneider A., McCauley L.K. Animal models of bone metastasis. Cancer Treat Res 2004, 118:47-81.