Role of RANKL/RANK in primary and secondary breast cancer

World Journal of Orthopedics

Volumn 4, Issue 4, 2013, Pages 178-185

  Yoneda, Toshiyuki ^a,b   Tanaka, Soichi ^b   Hata, Kenji ^b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Bone metastasis; Bone pain; Bone resorption; Epithelial mesenchymal transition; Osteoblasts; Osteoclasts; Stromal cells

Indexed keywords

EID: 84893019097     PISSN: None     EISSN: 22185836     Source Type: Journal    
DOI: 10.5312/wjo.v4.i4.178     Document Type: Article

References (65)

1. Coleman RE. Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res 2006; 12: 6243s-6249s [PMID: 17062708 DOI: 10.1158/1078-0432. CCR-06-0931]
2. Schulman KL, Kohles J. Economic burden of metastatic bone disease in the U.S. Cancer 2007; 109: 2334-2342 [PMID: 17450591]
3. Talmadge JE, Fidler IJ. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 2010; 70: 5649-5669 [PMID: 20610625 DOI: 10.1158/0008-5472. CAN-10-1040]
4. Mego M, Mani SA, Cristofanilli M. Molecular mechanisms of metastasis in breast cancer--clinical applications. Nat Rev Clin Oncol 2010; 7: 693-701 [PMID: 20956980 DOI: 10.1038/nrclinonc.2010.171]
5. Ross JS, Slodkowska EA. Circulating and disseminated tumor cells in the management of breast cancer. Am J Clin Pathol 2009; 132: 237-245 [PMID: 19605818 DOI: 10.1309/AJCPJI7DEOLKCS6F]
6. Yoneda T, Williams PJ, Hiraga T, Niewolna M, Nishimura R. A bone-seeking clone exhibits different biological properties from the MDA-MB-231 parental human breast cancer cells and a brain-seeking clone in vivo and in vitro. J Bone Miner Res 2001; 16: 1486-1495 [PMID: 11499871 DOI: 10.1359/jbmr.2001.16.8.1486]
7. Yoneda T, Hiraga T. Crosstalk between cancer cells and bone microenvironment in bone metastasis. Biochem Biophys Res Commun 2005; 328: 679-687 [PMID: 15694401 DOI: 10.1016/j.bbrc.2004.11.070]
8. Hauschka PV, Mavrakos AE, Iafrati MD, Doleman SE, Klagsbrun M. Growth factors in bone matrix. Isolation of multiple types by affinity chromatography on heparin-Sepharose. J Biol Chem 1986; 261: 12665-12674 [PMID: 3745206]
9. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 1889; 1: 571-573 [DOI: 10.1016/S0140-6736(00)49915-0]
10. Hiraga T, Myoui A, Hashimoto N, Sasaki A, Hata K, Morita Y, Yoshikawa H, Rosen CJ, Mundy GR, Yoneda T. Bone-derived IGF mediates crosstalk between bone and breast cancer cells in bony metastases. Cancer Res 2012; 72: 4238-4249 [PMID: 22738911 DOI: 10.1158/0008-5472.CAN-11-3061]
11. Yin JJ, Selander K, Chirgwin JM, Dallas M, Grubbs BG, Wieser R, Massagué J, Mundy GR, Guise TA. TGF-beta signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J Clin Invest 1999; 103: 197-206 [PMID: 9916131 DOI: 10.1172/JCI3523]
12. Hiraga T, Myoui A, Choi ME, Yoshikawa H, Yoneda T. Stimulation of cyclooxygenase-2 expression by bone-derived transforming growth factor-beta enhances bone metastases in breast cancer. Cancer Res 2006; 66: 2067-2073 [PMID: 16489006 DOI: 10.1158/0008-5472.CAN-05-2012]
13. Morinaga Y, Fujita N, Ohishi K, Tsuruo T. Stimulation of interleukin-11 production from osteoblast-like cells by transforming growth factor-beta and tumor cell factors. Int J Cancer 1997; 71: 422-428 [PMID: 9139879 DOI: 3.0.CO; ]
14. Mundy GR. Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Cancer 2002; 2: 584-593 [PMID: 12154351 DOI: 10.1038/nrc867]
15. Roodman GD. Mechanisms of bone metastasis. N Engl J Med 2004; 350: 1655-1664 [PMID: 15084698 DOI: 10.1056/NEJMra030831]
16. Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: a fatal attraction. Nat Rev Cancer 2011; 11: 411-425 [PMID: 21593787 DOI: 10.1038/nrc3055]
17. Thomas RJ, Guise TA, Yin JJ, Elliott J, Horwood NJ, Martin TJ, Gillespie MT. Breast cancer cells interact with osteoblasts to support osteoclast formation. Endocrinology 1999; 140: 4451-4458 [PMID: 10499498 DOI: 10.1210/en.140.10.4451]
18. Kearns AE, Khosla S, Kostenuik PJ. Receptor activator of nuclear factor kappaB ligand and osteoprotegerin regulation of bone remodeling in health and disease. Endocr Rev 2008; 29: 155-192 [PMID: 18057140 DOI: 10.1210/er.2007-0014]
19. Lacey DL, Boyle WJ, Simonet WS, Kostenuik PJ, Dougall WC, Sullivan JK, San Martin J, Dansey R. Bench to bedside: elucidation of the OPG-RANK-RANKL pathway and the development of denosumab. Nat Rev Drug Discov 2012; 11: 401-419 [PMID: 22543469 DOI: 10.1038/nrd3705]
20. Dougall WC. Molecular pathways: osteoclast-dependent and osteoclast-independent roles of the RANKL/RANK/OPG pathway in tumorigenesis and metastasis. Clin Cancer Res 2012; 18: 326-335 [PMID: 22031096 DOI: 10.1158/1078-0432. CCR-10-2507]
21. Fata JE, Kong YY, Li J, Sasaki T, Irie-Sasaki J, Moorehead RA, Elliott R, Scully S, Voura EB, Lacey DL, Boyle WJ, Khokha R, Penninger JM. The osteoclast differentiation factor osteoprotegerin-ligand is essential for mammary gland development. Cell 2000; 103: 41-50 [PMID: 11051546 DOI: 10.1016/S0092-8674(00)00103-3]
22. Fernandez-Valdivia R, Mukherjee A, Ying Y, Li J, Paquet M, DeMayo FJ, Lydon JP. The RANKL signaling axis is sufficient to elicit ductal side-branching and alveologenesis in the mammary gland of the virgin mouse. Dev Biol 2009; 328: 127-139 [PMID: 19298785 DOI: 10.1016/j.ydbio.2009.01.019]
23. Gonzalez-Suarez E, Branstetter D, Armstrong A, Dinh H, Blumberg H, Dougall WC. RANK overexpression in transgenic mice with mouse mammary tumor virus promotercontrolled RANK increases proliferation and impairs alveolar differentiation in the mammary epithelia and disrupts lumen formation in cultured epithelial acini. Mol Cell Biol 2007; 27: 1442-1454 [PMID: 17145767 DOI: 10.1128/MCB.01298-06]
24. Cao Y, Bonizzi G, Seagroves TN, Greten FR, Johnson R, Schmidt EV, Karin M. IKKalpha provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell 2001; 107: 763-775 [PMID: 11747812 DOI: 10.1016/S0092-8674(01)00599-2]
25. Schramek D, Sigl V, Penninger JM. RANKL and RANK in sex hormone-induced breast cancer and breast cancer metastasis. Trends Endocrinol Metab 2011; 22: 188-194 [PMID: 21470874 DOI: 10.1016/j.tem.2011.02.007]
26. Schramek D, Leibbrandt A, Sigl V, Kenner L, Pospisilik JA, Lee HJ, Hanada R, Joshi PA, Aliprantis A, Glimcher L, Pasparakis M, Khokha R, Ormandy CJ, Widschwendter M, Schett G, Penninger JM. Osteoclast differentiation factor RANKL controls development of progestin-driven mammary cancer. Nature 2010; 468: 98-102 [PMID: 20881962 DOI: 10.1038/nature09387]
27. Gonzalez-Suarez E, Jacob AP, Jones J, Miller R, Roudier-Meyer MP, Erwert R, Pinkas J, Branstetter D, Dougall WC. RANK ligand mediates progestin-induced mammary epithelial proliferation and carcinogenesis. Nature 2010; 468: 103-107 [PMID: 20881963 DOI: 10.1038/nature09495]
28. Shapiro S, Farmer RD, Stevenson JC, Burger HG, Mueck AO. Does hormone replacement therapy cause breast cancer? An application of causal principles to three studies. Part 4: the Million Women Study. J Fam Plann Reprod Health Care 2012; 38: 102-109 [PMID: 22262621 DOI: 10.1136/jfprhc-2011-100229]
29. Joshi PA, Jackson HW, Beristain AG, Di Grappa MA, Mote PA, Clarke CL, Stingl J, Waterhouse PD, Khokha R. Progesterone induces adult mammary stem cell expansion. Nature 2010; 465: 803-807 [PMID: 20445538 DOI: 10.1038/nature09091]
30. Palafox M, Ferrer I, Pellegrini P, Vila S, Hernandez-Ortega S, Urruticoechea A, Climent F, Soler MT, Muñoz P, Viñals F, Tometsko M, Branstetter D, Dougall WC, González-Suárez E. RANK induces epithelial-mesenchymal transition and stemness in human mammary epithelial cells and promotes tumorigenesis and metastasis. Cancer Res 2012; 72: 2879-2888 [PMID: 22496457 DOI: 10.1158/0008-5472.CAN-12-0044]
31. Tan W, Zhang W, Strasner A, Grivennikov S, Cheng JQ, Hoffman RM, Karin M. Tumour-infiltrating regulatory T cells stimulate mammary cancer metastasis through RANKL-RANK signalling. Nature 2011; 470: 548-553 [PMID: 21326202 DOI: 10.1038/nature09707]
32. Atanackovic D, Cao Y, Luetkens T, Panse J, Faltz C, Arfsten J, Bartels K, Wolschke C, Eiermann T, Zander AR, Fehse B, Bokemeyer C, Kroger N. CD4+CD25+FOXP3+ T regulatory cells reconstitute and accumulate in the bone marrow of patients with multiple myeloma following allogeneic stem cell transplantation. Haematologica 2008; 93: 423-430 [PMID: 18287134 DOI: 10.3324/haematol.11897]
33. Zhao E, Wang L, Dai J, Kryczek I, Wei S, Vatan L, Altuwaijri S, Sparwasser T, Wang G, Keller ET, Zou W. Regulatory T cells in the bone marrow microenvironment in patients with prostate cancer. Oncoimmunology 2012; 1: 152-161 [PMID: 22720236 DOI: 10.4161/onci.1.2.18480]
34. El Saghir NS, Seoud M, Khalil MK, Charafeddine M, Salem ZK, Geara FB, Shamseddine AI. Effects of young age at presentation on survival in breast cancer. BMC Cancer 2006; 6: 194 [PMID: 16857060 DOI: 10.1186/1471-2407-6-194]
35. Fredholm H, Eaker S, Frisell J, Holmberg L, Fredriksson I, Lindman H. Breast cancer in young women: poor survival despite intensive treatment. PLoS One 2009; 4: e7695 [PMID: 19907646 DOI: 10.1371/journal.pone.0007695]
36. Cancello G, Maisonneuve P, Rotmensz N, Viale G, Mastropasqua MG, Pruneri G, Veronesi P, Torrisi R, Montagna E, Luini A, Intra M, Gentilini O, Ghisini R, Goldhirsch A, Colleoni M. Prognosis and adjuvant treatment effects in selected breast cancer subtypes of very young women (< 35 years) with operable breast cancer. Ann Oncol 2010; 21: 1974-1981 [PMID: 20332136 DOI: 10.1093/annonc/mdq072]
37. Azim HA, Michiels S, Bedard PL, Singhal SK, Criscitiello C, Ignatiadis M, Haibe-Kains B, Piccart MJ, Sotiriou C, Loi S. Elucidating prognosis and biology of breast cancer arising in young women using gene expression profiling. Clin Cancer Res 2012; 18: 1341-1351 [PMID: 22261811 DOI: 10.1158/1078-0432.CCR-11-2599]
38. Canon J, Bryant R, Roudier M, Branstetter DG, Dougall WC. RANKL inhibition combined with tamoxifen treatment increases anti-tumor efficacy and prevents tumor-induced bone destruction in an estrogen receptor-positive breast cancer bone metastasis model. Breast Cancer Res Treat 2012; 135: 771-780 [PMID: 22926264 DOI: 10.1007/s10549-012-2222-2]
39. Ibrahim T, Sacanna E, Gaudio M, Mercatali L, Scarpi E, Zoli W, Serra P, Ricci R, Serra L, Kang Y, Amadori D. Role of RANK, RANKL, OPG, and CXCR4 tissue markers in predicting bone metastases in breast cancer patients. Clin Breast Cancer 2011; 11: 369-375 [PMID: 21764390 DOI: 10.1016/j.clbc.2011.05.001]
40. Mercatali L, Ibrahim T, Sacanna E, Flamini E, Scarpi E, Calistri D, Ricci M, Serra P, Ricci R, Zoli W, Kang Y, Amadori D. Bone metastases detection by circulating biomarkers: OPG and RANK-L. Int J Oncol 2011; 39: 255-261 [PMID: 21491082]
41. Huang L, Cheng YY, Chow LT, Zheng MH, Kumta SM. Tumour cells produce receptor activator of NF-kappaB ligand (RANKL) in skeletal metastases. J Clin Pathol 2002; 55: 877-878 [PMID: 12401833 DOI: 10.1136/jcp.55.11.877]
42. Santini D, Schiavon G, Vincenzi B, Gaeta L, Pantano F, Russo A, Ortega C, Porta C, Galluzzo S, Armento G, La Verde N, Caroti C, Treilleux I, Ruggiero A, Perrone G, Addeo R, Clezardin P, Muda AO, Tonini G. Receptor activator of NFkB (RANK) expression in primary tumors associates with bone metastasis occurrence in breast cancer patients. PLoS One 2011; 6: e19234 [PMID: 21559440 DOI: 10.1371/journal. pone.0019234]
43. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674 [PMID: 21376230 DOI: 10.1016/j.cell.2011.02.013]
44. Gao D, Vahdat LT, Wong S, Chang JC, Mittal V. Microenvironmental regulation of epithelial-mesenchymal transitions in cancer. Cancer Res 2012; 72: 4883-4889 [PMID: 23002209 DOI: 10.1158/0008-5472.CAN-12-1223]
45. Dave B, Mittal V, Tan NM, Chang JC. Epithelial-mesenchymal transition, cancer stem cells and treatment resistance. Breast Cancer Res 2012; 14: 202 [PMID: 22264257 DOI: 10.1186/bcr2938]
46. de Herreros AG, Peiró S, Nassour M, Savagner P. Snail family regulation and epithelial mesenchymal transitions in breast cancer progression. J Mammary Gland Biol Neoplasia 2010; 15: 135-147 [PMID: 20455012 DOI: 10.1007/s10911-010-9179-8]
47. Heldin CH, Vanlandewijck M, Moustakas A. Regulation of EMT by TGFß in cancer. FEBS Lett 2012; 586: 1959-1970 [PMID: 22710176 DOI: 10.1016/j.febslet.2012.02.037]
48. Kohno N, Aogi K, Minami H, Nakamura S, Asaga T, Iino Y, Watanabe T, Goessl C, Ohashi Y, Takashima S. Zoledronic acid significantly reduces skeletal complications compared with placebo in Japanese women with bone metastases from breast cancer: a randomized, placebo-controlled trial. J Clin Oncol 2005; 23: 3314-3321 [PMID: 15738536 DOI: 10.1200/JCO.2005.05.116]
49. Brisson L, Reshkin SJ, Goré J, Roger S. pH regulators in invadosomal functioning: proton delivery for matrix tasting. Eur J Cell Biol 2012; 91: 847-860 [PMID: 22673002 DOI: 10.1016/j.ejcb.2012.04.004]
50. Sherwood TW, Frey EN, Askwith CC. Structure and activity of the acid-sensing ion channels. Am J Physiol Cell Physiol 2012; 303: C699-C710 [PMID: 22843794 DOI: 10.1152/ajpcell.00188.2012]
51. Nagae M, Hiraga T, Wakabayashi H, Wang L, Iwata K, Yoneda T. Osteoclasts play a part in pain due to the inflammation adjacent to bone. Bone 2006; 39: 1107-1115 [PMID: 16769263 DOI: 10.1016/j.bone.2006.04.033]
52. Yoneda T, Hata K, Nakanishi M, Nagae M, Nagayama T, Wakabayashi H, Nishisho T, Sakurai T, Hiraga T. Involvement of acidic microenvironment in the pathophysiology of cancer-associated bone pain. Bone 2011; 48: 100-105 [PMID: 20637323 DOI: 10.1016/j.bone.2010.07.009]
53. Yoneda T, Hata K, Nakanishi M, Nagae M, Nagayama T, Wakabayashi H, Nishisho T, Sakurai T, Hiraga T. Molecular events of acid-induced bone pain. IBMS BoneKey 2011; 8: 195-204 [DOI: 10.1138/20110507]
54. Clohisy DR, Mantyh PW. Bone cancer pain and the role of RANKL/OPG. J Musculoskelet Neuronal Interact 2004; 4: 293-300 [PMID: 15615497]
55. Roudier MP, Bain SD, Dougall WC. Effects of the RANKL inhibitor, osteoprotegerin, on the pain and histopathology of bone cancer in rats. Clin Exp Metastasis 2006; 23: 167-175 [PMID: 16912914 DOI: 10.1007/s10585-006-9026-x]
56. Nagae M, Hiraga T, Yoneda T. Acidic microenvironment created by osteoclasts causes bone pain associated with tumor colonization. J Bone Miner Metab 2007; 25: 99-104 [PMID: 17323179 DOI: 10.1007/s00774-006-0734-8]
57. Cleeland CS, Body JJ, Stopeck A, von Moos R, Fallowfield L, Mathias SD, Patrick DL, Clemons M, Tonkin K, Masuda N, Lipton A, de Boer R, Salvagni S, Oliveira CT, Qian Y, Jiang Q, Dansey R, Braun A, Chung K. Pain outcomes in patients with advanced breast cancer and bone metastases: results from a randomized, double-blind study of denosumab and zoledronic acid. Cancer 2013; 119: 832-838 [PMID: 22951813]
58. Mould DR, Green B. Pharmacokinetics and pharmacodynamics of monoclonal antibodies: concepts and lessons for drug development. BioDrugs 2010; 24: 23-39 [PMID: 20055530 DOI: 10.2165/11530560-000000000-00000]
59. Baron R, Ferrari S, Russell RG. Denosumab and bisphosphonates: different mechanisms of action and effects. Bone 2011; 48: 677-692 [PMID: 21145999 DOI: 10.1016/j.bone.2010.11.020]
60. Lipton A, Steger GG, Figueroa J, Alvarado C, Solal-Celigny P, Body JJ, de Boer R, Berardi R, Gascon P, Tonkin KS, Coleman R, Paterson AH, Peterson MC, Fan M, Kinsey A, Jun S. Randomized active-controlled phase II study of denosumab efficacy and safety in patients with breast cancer-related bone metastases. J Clin Oncol 2007; 25: 4431-4437 [PMID: 17785705 DOI: 10.1200/JCO.2007.11.8604]
61. Body JJ, Lipton A, Gralow J, Steger GG, Gao G, Yeh H, Fizazi K. Effects of denosumab in patients with bone metastases with and without previous bisphosphonate exposure. J Bone Miner Res 2010; 25: 440-446 [PMID: 19653815 DOI: 10.1359/jbmr.090810]
62. Stopeck AT, Lipton A, Body JJ, Steger GG, Tonkin K, de Boer RH, Lichinitser M, Fujiwara Y, Yardley DA, Viniegra M, Fan M, Jiang Q, Dansey R, Jun S, Braun A. Denosumab compared with zoledronic acid for the treatment of bone metastases in patients with advanced breast cancer: a randomized, double-blind study. J Clin Oncol 2010; 28: 5132-5139 [PMID: 21060033 DOI: 10.1200/JCO.2010.29.7101]
63. Coleman RE. Bone cancer in 2011: Prevention and treatment of bone metastases. Nat Rev Clin Oncol 2012; 9: 76-78 [PMID: 22182971 DOI: 10.1038/nrclinonc.2011.198]
64. Saad F, Brown JE, Van Poznak C, Ibrahim T, Stemmer SM, Stopeck AT, Diel IJ, Takahashi S, Shore N, Henry DH, Barrios CH, Facon T, Senecal F, Fizazi K, Zhou L, Daniels A, Carrière P, Dansey R. Incidence, risk factors, and outcomes of osteonecrosis of the jaw: integrated analysis from three blinded active-controlled phase III trials in cancer patients with bone metastases. Ann Oncol 2012; 23: 1341-1347 [PMID: 21986094 DOI: 10.1093/annonc/mdr435]
65. Lipton A, Fizazi K, Stopeck AT, Henry DH, Brown JE, Yardley DA, Richardson GE, Siena S, Maroto P, Clemens M, Bilynskyy B, Charu V, Beuzeboc P, Rader M, Viniegra M, Saad F, Ke C, Braun A, Jun S. Superiority of denosumab to zoledronic acid for prevention of skeletal-related events: a combined analysis of 3 pivotal, randomised, phase 3 trials. Eur J Cancer 2012; 48: 3082-3092 [PMID: 22975218 DOI: 10.1016/j.ejca.2012.08.002]