Castration-induced bone loss triggers growth of disseminated prostate cancer cells in bone

Endocrine-Related Cancer

Volumn 21, Issue 5, 2014, Pages 769-781

  Ottewell, Penelope D ^a   Wang, Ning ^b   Meek, Joshua ^a   Fowles, C Anne ^b   Croucher, Peter I ^c   Eaton, Colby L ^b   Holen, Ingunn ^a  

^a Academic Unit of Clinical Oncology   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Bone; Castration; Metastasis; Prostate cancer

Indexed keywords

BISPHOSPHONIC ACID DERIVATIVE; BONE DENSITY CONSERVATION AGENT; IMIDAZOLE DERIVATIVE; ZOLEDRONIC ACID;

ANIMAL; BAGG ALBINO MOUSE; BONE TUMOR; CASTRATION; HUMAN; MALE; METABOLISM; OSTEOLYSIS; PATHOLOGY; PREVENTION AND CONTROL; PROSTATE TUMOR; SECONDARY; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; BONE DENSITY CONSERVATION AGENTS; BONE NEOPLASMS; BONE RESORPTION; CASTRATION; CELL LINE, TUMOR; DIPHOSPHONATES; HUMANS; IMIDAZOLES; MALE; MICE, INBRED BALB C; PROSTATIC NEOPLASMS; TUMOR BURDEN;

EID: 84907479141     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-14-0199     Document Type: Article

References (58)

1. Aguirre-Ghiso JA 2007 Models, mechanisms and evidence for cancer dormancy. Nature Reviews. Cancer 7 834-846. (doi:10.1038/nrc2256)
2. American Cancer Society 2013 Survival rates for prostate cancer. Atlanta, GA, USA:American Cancer Society. (available at: http://www.cancer.org/cancer/prostatecancer/detailedguide/prostate-cancer-key-statistics).
3. Barkan D, Green JE & Chambers AF 2010 Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth. European Journal of Cancer 46 1181-1188. (doi:10.1016/j.ejca.2010.02.027)
4. Brown HK & Holen I 2009 Anti-tumour effects of bisphosphonates - what have we learned from in vivo models? Current Cancer Drug Targets 9 807-823. (doi:10.2174/156800909789760339)
5. Chu GC, Zhau HE, Wang R, Rogatko A, Feng X, Zayzafoon M, Liu Y, Farach-Carson MC, You S, Kim J et al. 2014 RANK- and c-Met-mediated signal network promotes prostate cancer metastatic colonization. Endocrine-Related Cancer 21 311-326. (doi:10.1530/ERC-13-0548)
6. Cole AA & Walters LM 1987 Tartrate-resistant acid phosphatase in bone and cartilage following decalcification and cold-embedding in plastic. Journal of Histochemistry and Cytochemistry 35 203-206. (doi:10.1177/35.2.3540104)
7. Coleman RE, Lipton A, Roodman GD, Guise TA, Boyce BF, Brufsky AM, Clézardin P, Croucher PI, Gralow JR, Hadji P et al. 2010 Metastasis and bone loss: advancing treatment and prevention. Cancer Treatment Reviews 36 615-620. (doi:10.1016/j.ctrv.2010.04.003)
8. Coleman RE, Rathbone E & Brown JE 2013 Management of cancer treatment-induced bone loss. Nature Reviews. Rheumatology 9 365-374.(doi:10.1038/nrrheum.2013.36)
9. Cook LM, Shay G, Aruajo A & Lynch CC 2014 Integrating new discoveries into the "vicious cycle" paradigm of prostate to bone metastases. Cancer Metastasis Reviews 33 511-525. (doi:10.1007/s10555-014-9494-4)
10. Corey E, Brown LG, Quinn JE, Poot M, Roudier MP, Higano CS & Vessella RL 2003 Zoledronic acid exhibits inhibitory effects on osteoblastic and osteolytic metastases of prostate cancer. Clinical Cancer Research 9 295-306.
11. Das K, Lorena PD, Ng LK, Lim D, Shen L, Siow WY, Teh M, Reichardt JK & Salto-Tellez M 2010 Differential expression of steroid 5α-reductase isozymes and association with disease severity and angiogenic genes predict their biological role in prostate cancer. Endocrine-Related Cancer17 757-770. (doi:10.1677/ERC-10-0022)
12. Daubiné F, Le Gall C, Gasser J, Green J & Clézardin P 2007 Antitumor effects of clinical dosing regimens of bisphosphonates in experimental breast cancer bone metastasis. Journal of the National Cancer Institute 21 322-330. (doi:10.1093/jnci/djk054)
13. Debes JD & Tindall DJ 2002 The role of androgens and the androgen receptor in prostate cancer. Cancer Letters 187 1-7. (doi:10.1016/S0304-3835(02)00413-5)
14. El-Amm J, Freeman A, Patel N & Aragon-Ching JB 2013 Bone-targeted therapies in metastatic castration-resistant prostate cancer: evolving paradigms. Prostate Cancer article 210686. (doi:10.1155/2013/210686)
15. Ellis SL, Grassinger J, Jones A, Borg J, Camenisch T, Haylock D, Bertoncello I & Nilsson SK 2011 The relationship between bone, hemopoietic stem cells and vasculature. Blood 11 1516-1524. (doi:10.1182/blood-2010-08-303800)
16. Garnero P, Buchs N, Zekri J, Rizzoli R, Coleman RE & Delmas PD 2000 Markers of bone turnover for the management of patients with bone metastases from prostate cancer. British Journal of Cancer 82 858-864.(doi:10.1054/bjoc.1999.1012)
17. Graham TJ, Box G, Tunariu N, Crespo M, Spinks TJ, Miranda S, Attard G, de Bono J, Eccles SA, Davies FE et al. 2014 Preclinical evaluation of imaging biomarkers for prostate cancer bone metastasis and response to cabozantinib. Journal of the National Cancer Institute 106 dju033.(doi:10.1093/jnci/dju033)
18. Guise T 2010 Examining the metastatic niche: targeting the micro-environment.Seminars in Oncology 37 (Suppl 2) S2-S14. (doi:10.1053/j.seminoncol.2010.10.007)
19. Han M, Partin AW, Zahurak M, Piantadosi S, Epstein JJ & Walsh PC 2003 Biochemical (prostate specific antigen) recurrence probability following radical prostatectomy for clinically localized prostate cancer. Journal of Urology 169 517-523. (doi:10.1016/S0022-5347(05)63946-8)
20. Hansen AG, Arnold SA, Jiang M, Palmer TD, Ketova T, Merkel A, Pickup M, Samaras S, Shyr Y, Moses HL et al. 2014 ALCAM/CD166 is a TGF-β-responsive marker and functional regulator of prostate cancer metastasis to bone. Cancer Research 74 1404-1415. (doi:10.1158/0008-5472.CAN-13-1296)
21. Harris WP, Mostaghel EA, Nelson PS & Montgomery B 2009 Androgen deprivation therapy: progress in understanding mechanisms of resistance and optimizing androgen depletion. Nature Clinical Practice. Urology 6 76-85. (doi:10.1038/ncpuro1296)
22. Herroon MK, Rajagurubandara E, Hardaway AL, Powell K, Turchick A, Feldmann D & Podgorski I 2013 Bone marrow adipocytes promote tumor growth in bone via FABP4-dependent mechanisms. Oncotarget 4 2108-2123.
23. van der Horst G, van den Hoogen C, Buijs JT, Cheung H, Bloys H, Pelger RC, Lorenzon G, Heckmann B, Feyen J, Pujuguet P et al. 2011 Targeting of α(v)-integrins in stem/progenitor cells and supportive microenvironment impairs bone metastasis in human prostate cancer. Neoplasia 13 516-525. (doi:10.1593/neo.11122)
24. Hung TT, Chan J, Russell PJ & Power CA 2011 Zoledronic acid preserves bone structure and increases survival but does not limit tumour incidence in a prostate cancer bone metastasis model. PLoS ONE 6 e19389. (doi:10.1371/journal.pone.0019389)
25. Kim JK, Jung Y, Wang J, Joseph J, Mishra A, Hill EE, Krebsbach PH, Pienta KJ, Shiozawa Y & Taichman RS 2013 TBK1 regulates prostate cancer dormancy through mTOR inhibition. Neoplasia 15 1064-1074.(doi:10.1593/neo.13402)
26. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, Tesio M, Samstein RM, Goichberg P, Spiegel A et al. 2006 Osteoclasts degrade endosteal components and promote mobilisation of hematopoietic progenitor cells. Nature Medicine 12 657-664. (doi:10.1038/nm1417)
27. Kollet O, Dar A & Lapidot T 2007 The multiple roles of osteoclasts in host defence: bone remodelling and hematopoietic stem cell mobilisation. Annual Review of Immunology 25 51-69. (doi:10.1146/annurev.immunol.25.022106.141631)
28. Lee YC, Bilen MA, Yu G, Lin SC, Huang CF, Ortiz A, Cho H, Song JH, Satcher RL, Kuang J et al. 2013 Inhibition of cell adhesion by a cadherin-11 antibody thwarts bone metastasis. Molecular Cancer Research 11 1401-1411. (doi:10.1158/1541-7786.MCR-13-0108)
29. Matsushima H, Goto T, Hosaka Y, Kitamura T & Kawabe K 1999 Correlation between proliferation, apoptosis, and angiogenesis in prostate carcinoma and their relation to androgen ablation. Cancer 85 1822-1827.(doi:10.1002/(SICI)1097-0142(19990415)85:8〈1822::AID-CNCR24〉3.0.CO;2-1)
30. Michaelson MD, Kaufman DS, Lee H, McGovern FJ, Kantoff PW, Fallon MA, Finkelstein JS & Smith MR 2007 Randomized controlled trial of annual zoledronic acid to prevent gonadotropin-releasing hormone agonist-induced bone loss in men with prostate cancer. Journal of Clinical Oncology 25 1038-1042. (doi:10.1200/JCO.2006.07.3361)
31. Morgans AK & Smith MR 2012 Bone-targeted agents: preventing skeletal complications in prostate cancer. Urologic Clinics of North America 39 533-546. (doi:10.1016/j.ucl.2012.07.009)
32. Morrissey C, Roudier MP, Dowell A, True LD, Ketchanji M, Welty C, Corey E, Lange PH, Higano CS & Vessella RL 2013 Effects of androgen deprivation therapy and bisphosphonate treatment on bone in patients with metastatic castration-resistant prostate cancer: results from the University of Washington Rapid Autopsy Series. Journal of Bone and Mineral Research 28 333-340. (doi:10.1002/jbmr.1749)
33. Ottewell PD, Mönkkönen H, Jones M, Lefley DV, Coleman RE & Holen I 2008 Antitumor effects of doxorubicin followed by zoledronic acid in a mouse model of breast cancer. Journal of the National Cancer Institute 100 1167-1178. (doi:10.1093/jnci/djn240)
34. Ottewell PD, Woodward JK, Lefley DV, Evans CA, Coleman RE & Holen I 2009 Anticancer mechanisms of doxorubicin and zoledronic acid in breast cancer tumor growth in bone. Molecular Cancer Therapeutics 8 2821-2832. (doi:10.1158/1535-7163.MCT-09-0462)
35. Ottewell PD, Brown HK, Jones M, Rogers TL, Cross SS, Brown NJ, Coleman RE & Holen I 2012 Combination therapy inhibits development and progression of mammary tumours in immunocompetent mice. Breast Cancer Research and Treatment 133 523-536. (doi:10.1007/s10549-011-1782-x)
36. Ottewell PD, Wang N, Brown HK, Reeves K, Fowles A, Croucher P, Eaton C & Holen I 2014 Zoledronic acid has differential anti-tumour activity in the pre-and post-menopausal bone microenvironment in vivo. Clinical Cancer Research 20 2922-2932. (doi:10.1158/1078-0432.CCR-13-1246)
37. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM & Recker RR 1987 Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. Journal of Bone and Mineral Research 2 595-610. (doi:10.1002/jbmr.5650020617)
38. Petrylak DP, Tangen CM, Hussain MH, Lara PN Jr, Jones JA, Taplin ME, Burch PA, Berry D, Moinpour C, Kohli M et al. 2004 Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. New England Journal of Medicine 351 1513-1520. (doi:10.1056/NEJMoa041318)
39. van der Pluijm G, Que I, Sijmons B, Buijs JT, Löwik CW, Wetterwald A, Thalmann GN, Papapoulos SE & Cecchini MG 2005 Interference with the microenvironmental support impairs the de novo formation of bone metastases in vivo. Cancer Research 65 7682-7690. (doi:10.1158/0008-5472.CAN-04-4118)
40. Reim NS, Breig B, Stahr K, Eberle J, Hoeflich A, Wolf E & Erben RG 2008 Cortical bone loss in androgen-deficient aged male rats is mainly caused by increased endocortical bone remodeling. Journal of Bone and Mineral Research 23 694-704. (doi:10.1359/jbmr.080202)
41. Renstrom J, Kroger M, Peschel C & Oostendorp RA 2010 How the niche regulates hematopoietic stem cells. Chemico-Biological Interactions 184 7-15. (doi:10.1016/j.cbi.2009.11.012)
42. Saylor PJ 2014 Bone targeted therapies for the prevention of skeletal morbidity in men with prostate cancer. Asian Journal of Andrology 16 341-347. (doi:10.4103/1008-682X.122591)
43. Seruga B, Ocana A & Tannock IF 2011 Drug resistance in metastatic castration-resistant prostate cancer. Nature Reviews. Clinical Oncology 8 12-23. (doi:10.1038/nrclinonc.2010.136)
44. Shahinian VB, Kuo YF, Freeman JL & Goodwin JS 2005 Risk of fracture after androgen deprivation for prostate cancer. New England Journal of Medicine 352 154-164. (doi:10.1056/NEJMoa041943)
45. Shiosawa Y, Pedersen EA, Havens AM, Jung Y, Mishra A, Joseph J, Kim JK, Patel LR, Ying C, Ziegler AM et al. 2011 Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. Journal of Clinical Investigation 121 1298-1312. (doi:10.1172/JCI43414)
46. Shiozawa Y, McGee S, Pienta MJ, McGregor N, Jung Y, Yumoto K, Wang J, Berry JE, Pienta KJ & Taichman RS 2013 Erythropoietin supports the survival of prostate cancer, but not growth and bone metastasis. Journal of Cellular Biochemistry 114 2471-2478. (doi:10.1002/jcb.24592)
47. Smith MR 2003 Bisphosphonates to prevent skeletal complications in men with metastatic prostate cancer. Journal of Urology 170 S55-S57. (doi:10.1097/01.ju.0000095102.34708.bc)
48. Smith MR, McGovern FJ, ZietmanAL, Fallon MA, Hayden DL, Schoenfeld DA, Kantoff PW & Finkelstein JS 2001 Pamidronate to prevent bone loss during androgen-deprivation therapy for prostate cancer. New England Journal of Medicine 345 948-955. (doi:10.1056/NEJMoa010845)
49. Smith MR, Eastham J, Gleason DM, Shasha D, Tchekmedyian S & Zinner N 2003 Randomized controlled trial of zoledronic acid to prevent bone loss in men receiving androgen deprivation therapy for nonmetastatic prostate cancer. Journal of Urology 169 2008-2012. (doi:10.1097/01.ju.0000063820.94994.95)
50. Smith MR, Kabbinavar F, Saad F, Hussain A, Gittelman MC, Bilhartz DL, Wynne C, Murray R, Zinner NR, Schulman C et al. 2005 Natural history of rising serum prostate-specific antigen in men with castrate nonmetastatic prostate cancer. Journal of Clinical Oncology 23 2918-2925. (doi:10.1200/JCO.2005.01.529)
51. Smith MR, Halabi S, Ryan CJ, Hussain A, Vogelzang N, Stadler W, Hauke RJ, Monk JP, Saylor P, Bhoopalam N et al. 2014 Randomized controlled trial of early zoledronic acid in men with castration-sensitive prostate cancer and bone metastases: results of CALGB 90202 (Alliance). Clinical Oncology 32 1143-1150. (doi:10.1200/JCO.2013.51.6500)
52. Sturge J, Caley MP & Waxman J 2011 Bone metastasis in prostate cancer: emerging therapeutic strategies. Nature Reviews. Clinical Oncology 8 357-368. (doi:10.1038/nrclinonc.2011.67)
53. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, Oudard S, Théodore C, James ND, Turesson I et al. 2004 Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. New England Journal of Medicine 351 1502-1512. (doi:10.1056/NEJMoa040720)
54. Thudi NK, Martin CK, Nadella MV, Fernandez SA, Werbeck JL, Pinzone JJ & Rosol TJ 2008 Zoledronic acid decreased osteolysis but not bone metastasis in a nude mouse model of canine prostate cancer with mixed bone lesions. Prostate 68 1116-1125. (doi:10.1002/pros.20776)
55. Townson JL & Chambers AF 2006 Dormancy of solitary metastatic cells. Cell Cycle 16 1744-1750. (doi:10.4161/cc.5.16.2864)
56. Veldscholte J, Voorhorst-Ogink MM, Bolt-de Vries J, van Rooij HC, Trapman J & Mulder E 1990 Unusual specificity of the androgen receptor in the human prostate tumor cell line LNCaP: high affinity for progestagenic and estrogenic steroids. Biochimica et Biophysica Acta 1052 187-194. (doi:10.1016/0167-4889(90)90075-O)
57. Verhas M, Schoutens A, L'hermite-Baleriaux M, Dourov N, Verschaeren A, Mone M & Heilporn A 1986 The effect of orchidectomy on bonemetabolism in aging rats. Calcified Tissue International 39 74-77. (doi:10.1007/BF02553294)
58. Weilbaecher KN, Guise TA & McCauley L 2011 Cancer to bone: a fatal attraction. Nature Reviews. Cancer 11 411-425. (doi:10.1038/nrc3055)