Dynamic interplay between bone and multiple myeloma: Emerging roles of the osteoblast

Bone

Volumn 75, Issue , 2015, Pages 161-169

  Reagan, Michaela R ^a,b   Liaw, Lucy ^b,c   Rosen, Clifford J ^b,c   Ghobrial, Irene M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Maine Medical Center Research Institute   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bone; Multiple myeloma; Osteoblasts

Indexed keywords

DASATINIB; DECORIN; DKK1 ANTIBODY; PARATHYROID HORMONE; PROTEASOME INHIBITOR; PROTEIN ANTIBODY; SCLEROSTIN ANTIBODY; UNCLASSIFIED DRUG;

ADIPOCYTE; BONE DENSITY; CANCER GROWTH; CELL INTERACTION; CELLULAR IMMUNITY; DEVELOPMENTAL BIOLOGY; DRUG THERAPY; HUMAN; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MULTIPLE MYELOMA; MYELOMA CELL; NONHUMAN; ONTOGENY; OSTEOANABOLIC THERAPY; OSTEOBLAST; OSTEOCLAST; OSTEOCLAST ACTIVITY; OSTEOCYTE; OSTEOLYSIS; OSTEOPROGENITOR CELL; REVIEW; DISEASE COURSE; METABOLISM; PATHOLOGY;

DISEASE PROGRESSION; HUMANS; MULTIPLE MYELOMA; OSTEOBLASTS;

EID: 84924253484     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2015.02.021     Document Type: Review

References (125)

1. Drake M.T. Unveiling skeletal fragility in patients diagnosed with MGUS: no longer a condition of undetermined significance?. J Bone Miner Res 2014, 29:2529-2533. 10.1002/jbmr.2387.
2. Kingsley L.A., Fournier P.G.J., Chirgwin J.M., Guise T.A. Molecular biology of bone metastasis. Mol Cancer Ther 2007, 6:2609-2617. 10.1158/1535-7163.MCT-07-0234.
3. Guise T.A., Mohammad K.S., Clines G., Stebbins E.G., Wong D.H., Higgins L.S., et al. Basic mechanisms responsible for osteolytic and osteoblastic bone metastases. Clin Cancer Res 2006, 12:6213s-6216s. 10.1158/1078-0432.CCR-06-1007.
4. Fowler J.A., Edwards C.M., Croucher P.I. Tumor-host cell interactions in the bone disease of myeloma. Bone 2011, 48:121-128. 10.1016/j.bone.2010.06.029.
5. Kovacic N., Croucher P.I., McDonald M.M. Signaling between tumor cells and the host bone marrow microenvironment. Calcif Tissue Int 2013, 94:125-139. 10.1007/s00223-013-9794-7.
6. Taube T., Beneton M.N., McCloskey E.V., Rogers S., Greaves M., Kanis J.A. Abnormal bone remodelling in patients with myelomatosis and normal biochemical indices of bone resorption. Eur J Haematol 1992, 49:192-198.
7. A Double-blind, Placebo-controlled, Randomized Phase 2 Study of BHQ880, an Anti-Dickkopf1 (DKK1) Monoclonal Antibody (mAb), in Patients With Untreated Multiple Myeloma and Renal Insufficiency n.d. (accessed December 18, 2015). https://clinicaltrials.gov/ct2/show/record/NCT01337752.
8. A Phase Ib/II Multicenter Dose-determination Study, With an Adaptive, Randomized, Placebo-controlled, Double-blind Phase II, Using Various Repeated IV Doses of BHQ880 in Combination With Zoledronic Acid in Relapsed or Refractory Myeloma Patients With Prio n.d. (accessed January 18, 2015). https://clinicaltrials.gov/ct2/show/NCT00741377.
9. Krevvata M., Silva B.C., Manavalan J.S., Galan-Diez M., Kode A., Matthews B.G., et al. Inhibition of leukemia cell engraftment and disease progression in mice by osteoblasts. Blood 2014, 124:2834-2846. 10.1182/blood-2013-07-517219.
10. Ng A.C., Khosla S., Charatcharoenwitthaya N., Kumar S.K., Achenbach S.J., Holets M.F., et al. Bone microstructural changes revealed by high-resolution peripheral quantitative computed tomography imaging and elevated DKK1 and MIP-1α levels in patients with MGUS. Blood 2011, 118:6529-6534. 10.1182/blood-2011-04-351437.
11. Berenson J.R., Anderson K.C., Audell R.A., Boccia R.V., Coleman M., Dimopoulos M.A., et al. Monoclonal gammopathy of undetermined significance: a consensus statement. Br J Haematol 2010, 150:28-38. 10.1111/j.1365-2141.2010.08207.x.
12. Capulli M., Paone R., Rucci N. Osteoblast and osteocyte: games without frontiers. Arch Biochem Biophys 2014, 561:3-12. 10.1016/j.abb.2014.05.003.
13. Kronenberg H.M., Kobayashi T. Skeletal Development and Repair. Methods and Protocols 2014, Springer, London. 10.1007/978-1-62703-989-5.
14. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336. 10.1038/nature01657.
15. Baron R., Rawadi G., Roman-Roman S. Wnt signaling: a key regulator of bone mass. Curr Top Dev Biol 2006, 76:103-127. 10.1016/S0070-2153(06)76004-5.
16. Baron R., Kneissel M. WNT signaling in bone homeostasis and disease: from human mutations to treatments. Nat Med 2013, 19:179-192. 10.1038/nm.3074.
17. Colnot C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J Bone Miner Res 2009, 24:274-282. 10.1359/jbmr.081003.
18. Colnot C., Zhang X., Knothe Tate M.L. Current insights on the regenerative potential of the periosteum: molecular, cellular, and endogenous engineering approaches. J Orthop Res 2012, 30:1869-1878. 10.1002/jor.22181.
19. Movérare-Skrtic S., Henning P., Liu X., Nagano K., Saito H., Börjesson A.E., et al. Osteoblast-derived WNT16 represses osteoclastogenesis and prevents cortical bone fragility fractures. Nat Med 2014, 20:1279-1288. 10.1038/nm.3654.
20. Stevens J.R., Miranda-Carboni G.A., Singer M.A., Brugger S.M., Lyons K.M., Lane T.F. Wnt10b deficiency results in age-dependent loss of bone mass and progressive reduction of mesenchymal progenitor cells. J Bone Miner Res 2010, 25:2138-2147. 10.1002/jbmr.118.
21. Bennett C.N., Longo K.A., Wright W.S., Suva L.J., Lane T.F., Hankenson K.D., et al. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci U S A 2005, 102:3324-3329. 10.1073/pnas.0408742102.
22. Brommage R., Liu J., Hansen G.M., Kirkpatrick L.L., Potter D.G., Sands A.T., et al. High-throughput screening of mouse gene knockouts identifies established and novel skeletal phenotypes. Bone Res 2014, 2:14034. 10.1038/boneres.2014.34.
23. Pritchard J.M., Giangregorio L.M., Atkinson S.A., Beattie K.A., Inglis D., Ioannidis G., et al. Changes in trabecular bone microarchitecture in postmenopausal women with and without type 2 diabetes: a two year longitudinal study. BMC Musculoskelet Disord 2013, 14:114. 10.1186/1471-2474-14-114.
24. Reagan M.R., Mishima Y., Glavey S.V., Zhang Y., Manier S., Lu Z.N., et al. Investigating osteogenic differentiation in multiple myeloma using a novel 3D bone marrow niche model. Blood 2014, 124:3250-3259. 10.1182/blood-2014-02-558007.
25. Roccaro A.M., Sacco A., Purschke W.G., Moschetta M., Buchner K., Maasch C., et al. SDF-1 inhibition targets the bone marrow niche for cancer therapy. Cell Rep 2014, 9:118-128. 10.1016/j.celrep.2014.08.042.
26. Azab A.K., Runnels J.M., Pitsillides C., Moreau A.-S., Azab F., Leleu X., et al. CXCR4 inhibitor AMD3100 disrupts the interaction of multiple myeloma cells with the bone marrow microenvironment and enhances their sensitivity to therapy. Blood 2009, 113:4341-4351. 10.1182/blood-2008-10-186668.
27. Takeuchi K., Abe M., Hiasa M., Oda A., Amou H., Kido S., et al. Tgf-Beta inhibition restores terminal osteoblast differentiation to suppress myeloma growth. PLoS ONE 2010, 5:e9870. 10.1371/journal.pone.0009870.
28. Logothetis C.J., Lin S.-H. Osteoblasts in prostate cancer metastasis to bone. Nat Rev Cancer 2005, 5:21-28. 10.1038/nrc1528.
29. Langley G.R., Sabean H.B., Sorger K. Sclerotic lesions of bone in myeloma. Can Med Assoc J 1966, 94:940-946.
30. Morán Blanco L.M., Encinas Rodríguez C. Multiple myeloma with diffuse osteosclerosis: Distinct from POEMS syndrome. Radiologia 2013, 56:e29-e33. 10.1016/j.rx.2013.04.003.
31. Chen M., Green R. Circulating plasma cells with Russell bodies in osteosclerotic myeloma. Blood 2013, 122:160.
32. Kuo M.C., Shih L.Y. Primary plasma cell leukemia with extensive dense osteosclerosis: complete remission following combination chemotherapy. Ann Hematol 1995, 71:147-151.
33. Mulleman D., Gaxatte C., Guillerm G., Leroy X., Cotten A., Duquesnoy B., et al. Multiple myeloma presenting with widespread osteosclerotic lesions. Joint Bone Spine 2004, 71:79-83. 10.1016/S1297-319X(03)00152-0.
34. Olechnowicz S.W.Z., Edwards C.M. Contributions of the host microenvironment to cancer-induced bone disease. Cancer Res 2014, 74:1625-1631. 10.1158/0008-5472.CAN-13-2645.
35. Park D., Spencer J.A., Koh B.I., Kobayashi T., Fujisaki J., Clemens T.L., et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 2012, 10:259-272. 10.1016/j.stem.2012.02.003.
36. Kode A., Manavalan J.S., Mosialou I., Bhagat G., Rathinam C.V., Luo N., et al. Leukaemogenesis induced by an activating β-catenin mutation in osteoblasts. Nature 2014, 506:240-244. 10.1038/nature12883.
37. Li X., Pennisi A., Yaccoby S. Role of decorin in the antimyeloma effects of osteoblasts. Blood 2008, 112:159-168. 10.1182/blood-2007-11-124164.
38. Chen Z., Orlowski R.Z., Wang M., Kwak L., McCarty N. Osteoblastic niche supports the growth of quiescent multiple myeloma cells. Blood 2014, 123:2204-2208. 10.1182/blood-2013-07-517136.
39. Yaccoby S. Osteoblastogenesis and tumor growth in myeloma. Leuk Lymphoma 2010, 51:213-220. 10.3109/10428190903503438.
40. Yaccoby S., Wezeman M.J., Zangari M., Walker R., Cottler-Fox M., Gaddy D., et al. Inhibitory effects of osteoblasts and increased bone formation on myeloma in novel culture systems and a myelomatous mouse model. Haematologica 2006, 91:192-199.
41. Nash L.A., Sullivan P.J., Peters S.J., Ward W.E. Rooibos flavonoids, orientin and luteolin, stimulate mineralization in human osteoblasts through the Wnt pathway. Mol Nutr Food Res 2014, [Epub ahead]. 10.1002/mnfr.201400592.
42. Ishtiaq S., Edwards S., Sankaralingam A., Evans B.A.J., Elford C., Frost M.L., et al. The effect of nitrogen containing bisphosphonates, zoledronate and alendronate, on the production of pro-angiogenic factors by osteoblastic cells. Cytokine 2014, 71:154-160. 10.1016/j.cyto.2014.10.025.
43. Guo D., Li Q., Lv Q., Wei Q., Cao S., Gu J. MiR-27a targets sFRP1 in hFOB cells to regulate proliferation, apoptosis and differentiation. PLoS ONE 2014, 9:e91354. 10.1371/journal.pone.0091354.
44. Zhang W., Lee W.Y., Siegel D.S., Tolias P., Zilberberg J. Patient-specific 3D microfluidic tissue model for multiple myeloma. Tissue Eng Part C Methods 2014, 20:663-670. 10.1089/ten.TEC.2013.0490.
45. Tinhofer I., Biedermann R., Krismer M., Crazzolara R., Greil R. A role of TRAIL in killing osteoblasts by myeloma cells. FASEB J 2006, 20:759-761. 10.1096/fj.05-4329fje.
46. Kassen D., Moore S., Percy L., Herledan G., Bounds D., Rodriguez-Justo M., et al. The bone marrow stromal compartment in multiple myeloma patients retains capability for osteogenic differentiation in vitro: defining the stromal defect in myeloma. Br J Haematol 2014, 167:194-206. 10.1111/bjh.13020.
47. Rubin J., Fan X., Rahnert J., Sen B., Hsieh C.-L., Murphy T.C., et al. IGF-I secretion by prostate carcinoma cells does not alter tumor-bone cell interactions in vitro or in vivo. Prostate 2006, 66:789-800. 10.1002/pros.20379.
48. Standal T., Johnson R.W., McGregor N.E., Poulton I.J., Ho P.W.M., Martin T.J., et al. gp130 in late osteoblasts and osteocytes is required for PTH-induced osteoblast differentiation. J Endocrinol 2014, 223:181-190. 10.1530/JOE-14-0424.
49. Reagan M.R., Ghobrial I.M. Multiple myeloma-mesenchymal stem cells: characterization, origin, and tumor-promoting effects. Clin Cancer Res 2012, 18:342-349. 10.1158/1078-0432.CCR-11-2212.
50. Fu R., Liu H., Zhao S., Wang Y., Li L., Gao S., et al. Osteoblast inhibition by chemokine cytokine ligand3 in myeloma-induced bone disease. Cancer Cell Int 2014, 14:132. 10.1186/s12935-014-0132-6.
51. TM bioreactor allows the study of multiple myeloma biology and response to therapy. PLoS ONE 2013, 8:e71613. 10.1371/journal.pone.0071613.
52. Narayanan N.K., Duan B., Butcher J.T., Mazumder A., Narayanan B.A. Characterization of multiple myeloma clonal cell expansion and stromal Wnt/β-catenin signaling in hyaluronic acid-based 3D hydrogel. In Vivo (Brooklyn) 2014, 28:67-73.
53. Cappariello A., Maurizi A., Veeriah V., Teti A. The great beauty of the osteoclast. Arch Biochem Biophys 2014, 558:70-78. 10.1016/j.abb.2014.06.017.
54. Schmiedel B.J., Scheible C.A., Nuebling T., Kopp H.-G., Wirths S., Azuma M., et al. RANKL expression, function, and therapeutic targeting in multiple myeloma and chronic lymphocytic leukemia. Cancer Res 2013, 73:683-694. 10.1158/0008-5472.CAN-12-2280.
55. Clines G.A., Guise T.A. Hypercalcaemia of malignancy and basic research on mechanisms responsible for osteolytic and osteoblastic metastasis to bone. Endocr Relat Cancer 2005, 12:549-583. 10.1677/erc.1.00543.
56. Colaianni G., Brunetti G., Faienza M.F., Colucci S., Grano M. Osteoporosis and obesity: role of Wnt pathway in human and murine models. World J Orthop 2014, 5:242-246. 10.5312/wjo.v5.i3.242.
57. Berendsen A.D., Olsen B.R. Osteoblast-adipocyte lineage plasticity in tissue development, maintenance and pathology. Cell Mol Life Sci 2014, 71:493-497. 10.1007/s00018-013-1440-z.
58. Zhou B.O., Yue R., Murphy M.M., Peyer J.G., Morrison S.J. Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell 2014, 15:154-168. 10.1016/j.stem.2014.06.008.
59. Worthley D.L., Churchill M., Compton J.T., Tailor Y., Rao M., Si Y., et al. Gremlin 1 identifies a skeletal stem cell with bone, cartilage, and reticular stromal potential. Cell 2015, 160:269-284. 10.1016/j.cell.2014.11.042.
60. Chan C.K.F., Seo E.Y., Chen J.Y., Lo D., McArdle A., Sinha R., et al. Identification and specification of the mouse skeletal stem cell. Cell 2015, 160:285-298. 10.1016/j.cell.2014.12.002.
61. Pan S.Y., Johnson K.C., Ugnat A.-M., Wen S.W., Mao Y. Association of obesity and cancer risk in Canada. Am J Epidemiol 2004, 159:259-268.
62. Wallin A., Larsson S.C. Body mass index and risk of multiple myeloma: a meta-analysis of prospective studies. Eur J Cancer 2011, 47:1606-1615. 10.1016/j.ejca.2011.01.020.
63. Sola B., Poirot M., de Medina P., Bustany S., Marsaud V., Silvente-Poirot S., et al. Antiestrogen-binding site ligands induce autophagy in myeloma cells that proceeds through alteration of cholesterol metabolism. Oncotarget 2013, 4:911-922.
64. Wang X., Yan Z., Fulciniti M., Li Y., Gkotzamanidou M., Amin S.B., et al. Transcription factor-pathway coexpression analysis reveals cooperation between SP1 and ESR1 on dysregulating cell cycle arrest in non-hyperdiploid multiple myeloma. Leukemia 2014, 28:894-903. 10.1038/leu.2013.233.
65. Islam R., Altundag K., Kurt M., Altundag O., Turen S. Association between obesity and multiple myeloma in postmenopausal women may be attributed to increased aromatization of androgen in adipose tissue. Med Hypotheses 2005, 65:1001-1002. 10.1016/j.mehy.2005.05.014.
66. Hardaway A.L., Herroon M.K., Rajagurubandara E., Podgorski I. Bone marrow fat: linking adipocyte-induced inflammation with skeletal metastases. Cancer Metastasis Rev 2014, 33:527-543. 10.1007/s10555-013-9484-y.
67. Caers J., Deleu S., Belaid Z., De Raeve H., Van Valckenborgh E., De Bruyne E., et al. Neighboring adipocytes participate in the bone marrow microenvironment of multiple myeloma cells. Leukemia 2007, 21:1580-1584. 10.1038/sj.leu.2404658.
68. Adler B.J., Kaushansky K., Rubin C.T. Obesity-driven disruption of haematopoiesis and the bone marrow niche. Nat Rev Endocrinol 2014, 10:737-748. 10.1038/nrendo.2014.169.
69. Vogl D.T., Wang T., Pérez W.S., Stadtmauer E.A., Heitjan D.F., Lazarus H.M., et al. Effect of obesity on outcomes after autologous hematopoietic stem cell transplantation for multiple myeloma. Biol Blood Marrow Transplant 2011, 17:1765-1774. 10.1016/j.bbmt.2011.05.005.
70. Calvi L.M., Adams G.B., Weibrecht K.W., Weber J.M., Olson D.P., Knight M.C., et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425:841-846. 10.1038/nature02040.
71. Panaroni C., Tzeng Y.-S., Saeed H., Wu J.Y. Mesenchymal progenitors and the osteoblast lineage in bone marrow hematopoietic niches. Curr Osteoporos Rep 2014, 12:22-32. 10.1007/s11914-014-0190-7.
72. Wang L., Jin N., Schmitt A., Greiner J., Malcherek G., Hundemer M., et al. T cell-based targeted immunotherapies for patients with multiple myeloma. Int J Cancer 2014, 136:1751-1768. 10.1002/ijc.29190.
73. Ramachandran I.R., Martner A., Pisklakova A., Condamine T., Chase T., Vogl T., et al. Myeloid-derived suppressor cells regulate growth of multiple myeloma by inhibiting T cells in bone marrow. J Immunol 2013, 190:3815-3823. 10.4049/jimmunol.1203373.
74. Braga W.M.T., Atanackovic D., Colleoni G.W.B. The role of regulatory T cells and TH17 cells in multiple myeloma. Clin Dev Immunol 2012, 2012:293479. 10.1155/2012/293479.
75. Fu R., Gao S., Peng F., Li J., Liu H., Wang H., et al. Relationship between abnormal osteoblasts and cellular immunity in multiple myeloma. Cancer Cell Int 2014, 14:62. 10.1186/1475-2867-14-62.
76. McMillin D.W., Delmore J., Weisberg E., Negri J.M., Geer D.C., Klippel S., et al. Tumor cell-specific bioluminescence platform to identify stroma-induced changes to anticancer drug activity. Nat Med 2010, 16:483-489. 10.1038/nm.2112.
77. Roccaro A.M., Sacco A., Maiso P., Azab A.K., Tai Y.-T., Reagan M., et al. BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest 2013, 123:1542-1555. 10.1172/JCI66517.
78. Reagan M.R., Kaplan D.L. Concise review: mesenchymal stem cell tumor-homing: detection methods in disease model systems. Stem Cells 2011, 29:920. 10.1002/stem.645.
79. Houthuijzen J.M., Daenen L.G.M., Roodhart J.M.L., Voest E.E. The role of mesenchymal stem cells in anti-cancer drug resistance and tumour progression. Br J Cancer 2012, 106:1901-1906. 10.1038/bjc.2012.201.
80. Azab F., Vali S., Abraham J., Potter N., Muz B., de la Puente P., et al. PI3KCA plays a major role in multiple myeloma and its inhibition with BYL719 decreases proliferation, synergizes with other therapies and overcomes stroma-induced resistance. Br J Haematol 2014, 165:89-101. 10.1111/bjh.12734.
81. Corre J., Mahtouk K., Attal M., Gadelorge M., Huynh A., Fleury-Cappellesso S., et al. Bone marrow mesenchymal stem cells are abnormal in multiple myeloma. Leukemia 2007, 21:1079-1088. 10.1038/sj.leu.2404621.
82. Birmingham E., Niebur G.L., McHugh P.E., Shaw G., Barry F.P., McNamara L.M. Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche. Eur Cell Mater 2012, 23:13-27.
83. Sims N.A., Vrahnas C. Regulation of cortical and trabecular bone mass by communication between osteoblasts, osteocytes and osteoclasts. Arch Biochem Biophys 2014, 561C:22-28. 10.1016/j.abb.2014.05.015.
84. Compton J.T., Lee F.Y. A review of osteocyte function and the emerging importance of sclerostin. J Bone Joint Surg Am 2014, 96:1659-1668. 10.2106/JBJS.M.01096.
85. Giuliani N., Ferretti M., Bolzoni M., Storti P., Lazzaretti M., Dalla Palma B., et al. Increased osteocyte death in multiple myeloma patients: role in myeloma-induced osteoclast formation. Leukemia 2012, 26:1391-1401. 10.1038/leu.2011.381.
86. Delgado-Calle J., Bellido T., Roodman G.D. Role of osteocytes in multiple myeloma bone disease. Curr Opin Support Palliat Care 2014, 8:407-413. 10.1097/SPC.0000000000000090.
87. Del Fattore A., Teti A. The tight relationship between osteoclasts and the immune system. Inflamm Allergy Drug Targets 2012, 11:181-187.
88. Andersen T.L., Sondergaard T.E., Skorzynska K.E., Dagnaes-Hansen F., Plesner T.L., Hauge E.M., et al. A physical mechanism for coupling bone resorption and formation in adult human bone. Am J Pathol 2009, 174:239-247. 10.2353/ajpath.2009.080627.
89. Jensen P.R., Andersen T.L., Hauge E.-M., Bollerslev J., Delaissé J.-M. A joined role of canopy and reversal cells in bone remodeling-lessons from glucocorticoid-induced osteoporosis. Bone 2014, 73C:16-23. 10.1016/j.bone.2014.12.004.
90. Andersen T.L., Søe K., Sondergaard T.E., Plesner T., Delaisse J.-M. Myeloma cell-induced disruption of bone remodelling compartments leads to osteolytic lesions and generation of osteoclast-myeloma hybrid cells. Br J Haematol 2010, 148:551-561. 10.1111/j.1365-2141.2009.07980.x.
91. Kondoh S., Inoue K., Igarashi K., Sugizaki H., Shirode-Fukuda Y., Inoue E., et al. Estrogen receptor α in osteocytes regulates trabecular bone formation in female mice. Bone 2014, 60:68-77. 10.1016/j.bone.2013.12.005.
92. Hofbauer L.C., Rachner T.D., Coleman R.E., Jakob F. Endocrine aspects of bone metastases. Lancet Diabetes Endocrinol 2014, 2:500-512. 10.1016/S2213-8587(13)70203-1.
93. Patti A., Gennari L., Merlotti D., Dotta F., Nuti R. Endocrine actions of osteocalcin. Int J Endocrinol 2013, 2013:846480. 10.1155/2013/846480.
94. Hu B., Chen Y., Usmani S.Z., Ye S., Qiang W., Papanikolaou X., et al. Characterization of the molecular mechanism of the bone-anabolic activity of carfilzomib in multiple myeloma. PLoS ONE 2013, 8:e74191. 10.1371/journal.pone.0074191.
95. Swami A., Reagan M.R., Basto P., Mishima Y., Kamaly N., Glavey S., et al. Engineered nanomedicine for myeloma and bone microenvironment targeting. Proc Natl Acad Sci U S A 2014, 111:10287-10292. 10.1073/pnas.1401337111.
96. Zangari M., Terpos E., Zhan F., Tricot G. Impact of bortezomib on bone health in myeloma: a review of current evidence. Cancer Treat Rev 2012, 38:968-980. 10.1016/j.ctrv.2011.12.007.
97. Daoussis D., Andonopoulos A.P. The emerging role of Dickkopf-1 in bone biology: is it the main switch controlling bone and joint remodeling?. Semin Arthritis Rheum 2011, 41:170-177. 10.1016/j.semarthrit.2011.01.006.
98. Clarke B.L. Anti-sclerostin antibodies: utility in treatment of osteoporosis. Maturitas 2014, 78:199-204. 10.1016/j.maturitas.2014.04.016.
99. Colucci S., Brunetti G., Oranger A., Mori G., Sardone F., Specchia G., et al. Myeloma cells suppress osteoblasts through sclerostin secretion. Blood Cancer J 2011, 1:e27. 10.1038/bcj.2011.22.
100. Politou M.C., Heath D.J., Rahemtulla A., Szydlo R., Anagnostopoulos A., Dimopoulos M.A., et al. Serum concentrations of Dickkopf-1 protein are increased in patients with multiple myeloma and reduced after autologous stem cell transplantation. Int J Cancer 2006, 119:1728-1731. 10.1002/ijc.22033.
101. Kaiser M., Mieth M., Liebisch P., Oberländer R., Rademacher J., Jakob C., et al. Serum concentrations of DKK-1 correlate with the extent of bone disease in patients with multiple myeloma. Eur J Haematol 2008, 80:490-494. 10.1111/j.1600-0609.2008.01065.x.
102. Fulciniti M., Tassone P., Hideshima T., Vallet S., Nanjappa P., Ettenberg S.A., et al. Anti-DKK1 mAb (BHQ880) as a potential therapeutic agent for multiple myeloma. Blood 2009, 114:371-379. 10.1182/blood-2008-11-191577.
103. Zhou F., Meng S., Song H., Claret F.X. Dickkopf-1 is a key regulator of myeloma bone disease: opportunities and challenges for therapeutic intervention. Blood Rev 2013, 27:261-267. 10.1016/j.blre.2013.08.002.
104. Yaccoby S., Ling W., Zhan F., Walker R., Barlogie B., Shaughnessy J.D. Antibody-based inhibition of DKK1 suppresses tumor-induced bone resorption and multiple myeloma growth in vivo. Blood 2007, 109:2106-2111. 10.1182/blood-2006-09-047712.
105. Garcia-Gomez A., Ocio E.M., Crusoe E., Santamaria C., Hernández-Campo P., Blanco J.F., et al. Dasatinib as a bone-modifying agent: anabolic and anti-resorptive effects. PLoS ONE 2012, 7:e34914. 10.1371/journal.pone.0034914.
106. Silbermann R., Bolzoni M., Storti P., Guasco D., Bonomini S., Zhou D., et al. Bone marrow monocyte-/macrophage-derived activin A mediates the osteoclastogenic effect of IL-3 in multiple myeloma. Leukemia 2014, 28:951-954. 10.1038/leu.2013.385.
107. Vallet S., Mukherjee S., Vaghela N., Hideshima T., Fulciniti M., Pozzi S., et al. Activin A promotes multiple myeloma-induced osteolysis and is a promising target for myeloma bone disease. Proc Natl Acad Sci U S A 2010, 107:5124-5129. 10.1073/pnas.0911929107.
108. Chantry A.D., Heath D., Mulivor A.W., Pearsall S., Baud'huin M., Coulton L., et al. Inhibiting activin-A signaling stimulates bone formation and prevents cancer-induced bone destruction in vivo. J Bone Miner Res 2010, 25:2633-2646. 10.1002/jbmr.142.
109. Pennisi A., Ling W., Li X., Khan S., Wang Y., Barlogie B., et al. Consequences of daily administered parathyroid hormone on myeloma growth, bone disease, and molecular profiling of whole myelomatous bone. PLoS ONE 2010, 5:e15233. 10.1371/journal.pone.0015233.
110. Jilka R.L. Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 2007, 40:1434-1446. 10.1016/j.bone.2007.03.017.
111. Martin T.J. Bone biology and anabolic therapies for bone: current status and future prospects. J Bone Metab 2014, 21:8-20. 10.11005/jbm.2014.21.1.8.
112. Walker R.E., Lawson M.A., Buckle C.H., Snowden J.A., Chantry A.D. Myeloma bone disease: pathogenesis, current treatments and future targets. Br Med Bull 2014, 111:117-138. 10.1093/bmb/ldu016.
113. Coleman R., Gnant M., Morgan G., Clezardin P. Effects of bone-targeted agents on cancer progression and mortality. J Natl Cancer Inst 2012, 104:1059-1067. 10.1093/jnci/djs263.
114. Pozzi S., Raje N. The role of bisphosphonates in multiple myeloma: mechanisms, side effects, and the future. Oncologist 2011, 16:651-662. 10.1634/theoncologist. 2010-0225.
115. Mohty M., Malard F., Mohty B., Savani B., Moreau P., Terpos E. The effects of bortezomib on bone disease in patients with multiple myeloma. Cancer 2014, 120:618-623. 10.1002/cncr.28481.
116. Effect of Low Dose Bortezomib on Bone Formation in Smoldering Myeloma Patients n.d. (accessed January 04, 2015). https://clinicaltrials.gov/ct2/show/record/NCT00983346.
117. A Phase IIa Study of Sotatercept on Bone Mass and Turnover in Patients With Multiple Myeloma - Tabular View - ClinicalTrials.gov n.d. (accessed January 04, 2015). https://clinicaltrials.gov/ct2/show/NCT02230917.
118. Abdulkadyrov K.M., Salogub G.N., Khuazheva N.K., Sherman M.L., Laadem A., Barger R., et al. Sotatercept in patients with osteolytic lesions of multiple myeloma. Br J Haematol 2014, 165:814-823. 10.1111/bjh.12835.
119. Platt R.J., Chen S., Zhou Y., Yim M.J., Swiech L., Kempton H.R., et al. CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 2014, 159:440-455. 10.1016/j.cell.2014.09.014.
120. Lu G., Middleton R.E., Sun H., Naniong M., Ott C.J., Mitsiades C.S., et al. The myeloma drug lenalidomide promotes the cereblon-dependent destruction of Ikaros proteins. Science 2014, 343:305-309. 10.1126/science.1244917.
121. Eskildsen T., Taipaleenmäki H., Stenvang J., Abdallah B.M., Ditzel N., Nossent A.Y., et al. MicroRNA-138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells in vivo. Proc Natl Acad Sci U S A 2011, 108:6139-6144. 10.1073/pnas.1016758108.
122. Sung B., Oyajobi B., Aggarwal B.B. Plumbagin inhibits osteoclastogenesis and reduces human breast cancer-induced osteolytic bone metastasis in mice through suppression of RANKL signaling. Mol Cancer Ther 2012, 11:350-359. 10.1158/1535-7163.MCT-11-0731.
123. Roodman G.D. Genes associate with abnormal bone cell activity in bone metastasis. Cancer Metastasis Rev 2012, 31:569-578. 10.1007/s10555-012-9372-x.
124. Zhai Z., Qu X., Yan W., Li H., Liu G., Liu X., et al. Andrographolide prevents human breast cancer-induced osteoclastic bone loss via attenuated RANKL signaling. Breast Cancer Res Treat 2014, 144:33-45. 10.1007/s10549-014-2844-7.
125. Zinonos I., Luo K.-W., Labrinidis A., Liapis V., Hay S., Panagopoulos V., et al. Pharmacologic inhibition of bone resorption prevents cancer-induced osteolysis but enhances soft tissue metastasis in a mouse model of osteolytic breast cancer. Int J Oncol 2014, 45:532-540. 10.3892/ijo.2014.2468.