Osteoblastogenesis and tumor growth in myeloma

Leukemia and Lymphoma

Volumn 51, Issue 2, 2010, Pages 213-220

  Yaccoby, Shmuel ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Bone formation; Bortezomib; Myeloma; Osteoblasts; Proteoglycans; Wnt

Indexed keywords

BORTEZOMIB; PROTEASOME INHIBITOR;

BONE ATROPHY; BONE DEVELOPMENT; CANCER INHIBITION; MYELOMA; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; PRIORITY JOURNAL; REVIEW; TUMOR GROWTH;

ANIMALS; ANTINEOPLASTIC AGENTS; BORONIC ACIDS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; MULTIPLE MYELOMA; OSTEOBLASTS; OSTEOCLASTS; PYRAZINES; TUMOR BURDEN;

EID: 76349110797     PISSN: 10428194     EISSN: 10292403     Source Type: Journal    
DOI: 10.3109/10428190903503438     Document Type: Review

References (85)

1. Datta HK, Ng WF, Walker JA, Tuck SP, Varanasi SS. The cell biology of bone metabolism. J Clin Pathol 2008;61:577-587.
2. Bataille R, Chappard D, Marcelli C, et al. Recruitment of new osteoblasts and osteoclasts is the earliest critical event in the pathogenesis of human multiple myeloma. J Clin Invest 1991;88:62-66.
3. Taube T, Beneton MN, McCloskey EV, et al. Abnormal bone remodelling in patients with myelomatosis and normal biochemical indices of bone resorption. Eur J Haematol 1992;49:192-198.
4. Roodman GD. Pathogenesis of myeloma bone disease. Leukemia 2009;23:435-441.
5. Kyle RA, Therneau TM, Rajkumar SV, et al. A long-term study of prognosis in monoclonal gammopathy of undetermined significance. N Engl J Med 2002;346:564-569.
6. Drake M, Ng A, Kumar S, et al. Increases in serum levels of dickkopf 1 are associated with alterations in skeletal microstructure in monoclonal gammopathy of undetermined significance [abstract]. In: The 31st Annual Meeting of the American Society for Bone and Mineral Research, September 2009, Denver USA.
7. Landgren O, Kyle RA, Pfeiffer RM, et al. Monoclonal gammopathy of undetermined significance (MGUS) consistently precedes multiple myeloma: a prospective study. Blood 2009;113:5412-5417.
8. Evans CE, Galasko CS, Ward C. Does myeloma secrete an osteoblast inhibiting factor? J Bone Joint Surg Br 1989;71: 288-290.
9. Barille S, Collette M, Bataille R, Amiot M. Myeloma cells upregulate interleukin-6 secretion in osteoblastic cells through cell-to-cell contact but downregulate osteocalcin. Blood 1995; 86:3151-3159.
10. Tian E, Zhan F, Walker R, et al. The role of the Wnt-signaling antagonist DKK1 in the development of osteolytic lesions in multiple myeloma. N Engl J Med 2003;349:2483-2494.
11. Oshima T, Abe M, Asano J, et al. Myeloma cells suppress bone formation by secreting a soluble Wnt inhibitor, sFRP-2. Blood 2005;106:3160-3165.
12. Giuliani N, Colla S, Morandi F, et al. Myeloma cells block RUNX2/CBFA1 activity in human bone marrow osteoblast progenitors and inhibit osteoblast formation and differentiation. Blood 2005;106:2472-2483.
13. Standal T, Abildgaard N, Fagerli UM, et al. HGF inhibits BMP-induced osteoblastogenesis: possible implications for the bone disease of multiple myeloma. Blood 2007;109:3024-3030.
14. Lee JW, Chung HY, Ehrlich LA, et al. IL-3 expression by myeloma cells increases both osteoclast formation and growth of myeloma cells. Blood 2004;103:2308-2315.
15. Ehrlich LA, Chung HY, Ghobrial I, et al. IL-3 is a potential inhibitor of osteoblast differentiation in multiple myeloma. Blood 2005;106:1407-1414.
16. Roodman GD.Mechanisms of bone metastasis. N Engl JMed 2004;350:1655-1664.
17. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008;133:38-52.
18. Edwards CM,Mundy GR. Eph receptors and ephrin signaling pathways: a role in bone homeostasis. Int J Med Sci 2008;5: 263-272.
19. Zhao C, Irie N, Takada Y, et al. Bidirectional ephrinB2- EphB4 signaling controls bone homeostasis. Cell Metab 2006;4:111-121.
20. Allan EH, Hausler KD, Wei T, et al. EphrinB2 regulation by parathyroid hormone (PTH) and PTHrP revealed by molecular profiling in differentiating osteoblasts. J Bone Miner Res 2008;23:1170-1181.
21. Pennisi A, Ling W, Li X, et al. The ephrinB2/EphB4 axis is dysregulated in osteoprogenitors from myeloma patients and its activation affects myeloma bone disease and tumor growth. Blood 2009;114:1803-1812.
22. Gunn WG, Conley A, Deininger L, et al. A crosstalk between myeloma cells and marrow stromal cells stimulates production of DKK1 and IL-6: a potential role in the development of lytic bone disease and tumor progression in multiple myeloma. Stem Cells 2006;24:986-991.
23. Podar K, Anderson KC. The pathophysiologic role of VEGF in hematologic malignancies: therapeutic implications. Blood 2005;105:1383-1395.
24. Pearse RN, Sordillo EM, Yaccoby S, et al. Multiple myeloma disrupts the TRANCE/ osteoprotegerin cytokine axis to trigger bone destruction and promote tumor progression. Proc Natl Acad Sci USA 2001;98:11581-11586.
25. Qiang YW, Chen Y, Stephens O, et al. Myeloma-derived Dickkopf-1 disrupts Wnt-regulated osteoprotegerin and RANKL production by osteoblasts: a potential mechanism underlying osteolytic bone lesions in multiple myeloma. Blood 2008;112:196-207.
26. Corre J, Mahtouk K, Attal M, et al. Bone marrow mesenchymal stem cells are abnormal in multiple myeloma. Leukemia 2007;21:1079-1088.
27. Stewart JP, Shaughnessy JD, Jr. Role of osteoblast suppression in multiple myeloma. J Cell Biochem 2006;98:1-13.
28. Yaccoby S, Wezeman MJ, Henderson A, et al. Cancer and the microenvironment: myeloma-osteoclast interactions as a model. Cancer Res 2004;64:2016-2023.
29. Yaccoby S, Wezeman MJ, Zangari M, 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.
30. Glass DA, Bialek P, Ahn JD, et al. Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 2005;8:751-764.
31. Spencer GJ, Utting JC, Etheridge SL, Arnett TR, Genever PG. Wnt signalling in osteoblasts regulates expression of the receptor activator of NFkB ligand and inhibits osteoclastogenesis in vitro. J Cell Sci 2006;119:1283-1296.
32. Canalis E. Growth factor control of bone mass. J Cell Biochem 2009;108:769-777.
33. Podar K, Chauhan D, Anderson KC. Bone marrow microenvironment and the identification of new targets for myeloma therapy. Leukemia 2009;23:10-24.
34. Li X, Pennisi A, Yaccoby S. Role of decorin in the antimyeloma effects of osteoblasts. Blood 2008;112:159-168.
35. Waddington RJ, Roberts HC, Sugars RV, Schonherr E. Differential roles for small leucine-rich proteoglycans in bone formation. Eur Cell Mater 2003;6:12-21.
36. Balint E, Lapointe D, Drissi H, et al. Phenotype discovery by gene expression profiling: mapping of biological processes linked to BMP-2-mediated osteoblast differentiation. J Cell Biochem 2003;89:401-426.
37. Ameye L, Young MF. Mice deficient in small leucine-rich proteoglycans: novel in vivo models for osteoporosis, osteoarthritis, Ehlers-Danlos syndrome, muscular dystrophy, and corneal diseases. Glycobiology 2002;12:107R-116R.
38. De LA, Santra M, Baldi A, Giordano A, Iozzo RV. Decorininduced growth suppression is associated with up-regulation of p21, an inhibitor of cyclin-dependent kinases. J Biol Chem 1996;271:18961-18965.
39. Moscatello DK, Santra M, Mann DM, et al. Decorin suppresses tumor cell growth by activating the epidermal growth factor receptor. J Clin Invest 1998;101:406-412.
40. Reed CC, Gauldie J, Iozzo RV. Suppression of tumorigenicity by adenovirus-mediated gene transfer of decorin. Oncogene 2002;21:3688-3695.
41. Reed CC, Waterhouse A, Kirby S, et al. Decorin prevents metastatic spreading of breast cancer. Oncogene 2005;24: 1104-1110.
42. Zhu JX, Goldoni S, Bix G, et al. Decorin evokes protracted internalization and degradation of the epidermal growth factor receptor via caveolar endocytosis. J Biol Chem 2005;280: 32468-32479.
43. Naito Z. Role of the small leucine-rich proteoglycan (SLRP) family in pathological lesions and cancer cell growth. J Nippon Med.Sch 2005;72:137-145.
44. Li Y, Aoki T, Mori Y, et al. Cleavage of lumican by membrane-type matrix metalloproteinase-1 abrogates this proteoglycan-mediated suppression of tumor cell colony formation in soft agar. Cancer Res 2004;64:7058-7064.
45. Troup S, Njue C, Kliewer EV, et al. Reduced expression of the small leucine-rich proteoglycans, lumican, and decorin is associated with poor outcome in node-negative invasive breast cancer. Clin Cancer Res 2003;9:207-214.
46. Zafiropoulos A, Nikitovic D, Katonis P, et al. Decorininduced growth inhibition is overcome through protracted expression and activation of epidermal growth factor receptors in osteosarcoma cells. Mol Cancer Res 2008;6:785-794.
47. Goldoni S, Iozzo RV. Tumor microenvironment: modulation by decorin and related molecules harboring leucine-rich tandem motifs. Int J Cancer 2008;123:2473-2479.
48. Borset M, Seidel C, Hjorth-Hansen H, Waage A, Sundan A. The role of hepatocyte growth factor and its receptor c-Met in multiple myeloma and other blood malignancies. Leuk Lymphoma 1999;32:249-256.
49. Qiang YW, Shaughnessy JD, Jr., Yaccoby S. Wnt3a signaling within bone inhibits multiple myeloma bone disease and tumor growth. Blood 2008;112:374-382.
50. Edwards CM, Edwards JR, Lwin ST, et al. Increasing Wnt signaling in the bone marrow microenvironment inhibits the development of myeloma bone disease and reduces tumor burden in bone in vivo. Blood 2008;111:2833-2842.
51. Garrett IR, Chen D, Gutierrez G, et al. Selective inhibitors of the osteoblast proteasome stimulate bone formation in vivo and in vitro. J Clin Invest 2003;111:1771-1782.
52. Pennisi A, Li X, Ling W, et al. The proteasome inhibitor, bortezomib suppresses primary myeloma and stimulates bone formation in myelomatous and nonmyelomatous bones in vivo. Am J Hematol 2009;84:6-14.
53. Zangari M, Esseltine D, Lee CK, et al. Response to bortezomib is associated to osteoblastic activation in patients with multiple myeloma. Br J Haematol 2005;131:71-73. (Pubitemid 43899710)
54. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006;127:469-480.
55. Pinzone JJ, Hall BM, Thudi NK, et al. The role of Dickkopf-1 in bone development, homeostasis, and disease. Blood 2009;113:517-525.
56. Kaiser M, Mieth M, Liebisch P, 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.
57. Qiang YW, Barlogie B, Rudikoff S, Shaughnessy JD, Jr. Dkk1- induced inhibition of Wnt signaling in osteoblast differentiation is an underlying mechanism of bone loss in multiple myeloma. Bone 2008;42:669-680.
58. Yaccoby S, Ling W, Zhan F, et al. Antibody-based inhibition of DKK1 suppresses tumor-induced bone resorption and multiple myeloma growth in vivo. Blood 2007;109:2106-2111.
59. Yaccoby S, Pearse RN, Johnson CL, et al. Myeloma interacts with the bone marrow microenvironment to induce osteoclastogenesis and is dependent on osteoclast activity. Br J Haematol 2002;116:278-290.
60. Yaccoby S, Epstein J. The proliferative potential of myeloma plasma cells manifest in the SCID-hu host. Blood 1999;94: 3576-3582.
61. Yaccoby S, Barlogie B, Epstein J. Primary myeloma cells growing in SCID-hu mice: a model for studying the biology and treatment of myeloma and its manifestations. Blood 1998;92:2908-2913.
62. Yata K, Yaccoby S. The SCID-rab model: a novel in vivo system for primary human myeloma demonstrating growth of CD138-expressing malignant cells. Leukemia 2004;18:1891-1897.
63. Fulciniti M, Tassone P, Hideshima T et al. Anti-DKK1 mAb (BHQ880) as a potential therapeutic agent for multiple myeloma. Blood 2009;114:371-379.
64. Heath DJ, Chantry AD, Buckle CH, et al. Inhibiting Dickkopf-1 (Dkk1) removes suppression of bone formation and prevents the development of osteolytic bone disease in multiple myeloma. J Bone Miner Res 2009;24:425-436.
65. Derksen PW, Tjin E, Meijer HP, et al. Illegitimate WNT signaling promotes proliferation of multiple myeloma cells. Proc Natl Acad Sci USA 2004;101:6122-6127.
66. Dutta-Simmons J, Zhang Y, Gorgun G, et al. Aurora kinase A is a target of Wnt/{beta}-catenin involved in multiple myeloma disease progression. Blood 2009;114:2699-2708.
67. Richardson PG, Barlogie B, Berenson J, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 2003;348:2609-2617.
68. Bellido T, Ali AA, Plotkin LI, et al. Proteasomal degradation of Runx2 shortens parathyroid hormone-induced anti-apoptotic signaling in osteoblasts. A putative explanation for why intermittent administration is needed for bone anabolism. J Biol Chem 2003;278:50259-50272.
69. Giuliani N, Morandi F, Tagliaferri S, et al. The proteasome inhibitor bortezomib affects osteoblast differentiation in vitro and in vivo in multiple myeloma patients. Blood 2007;110: 334-338.
70. Qiang YW, Hu B, Chen Y, et al. Bortezomib induces osteoblast differentiation via Wnt-independent activation of beta-catenin/TCF signaling. Blood 2009;113:4319-4330.
71. Oyajobi BO, Garrett IR, Gupta A, et al. Stimulation of new bone formation by the proteasome inhibitor, bortezomib: implications for myeloma bone disease. Br J Haematol 2007; 139:434-438.
72. Zavrski I, Krebbel H, Wildemann B, et al. Proteasome inhibitors abrogate osteoclast differentiation and osteoclast function. Biochem Biophys Res Commun 2005;333:200-205.
73. Edwards CM, Lwin ST, Fowler JA, et al. Myeloma cells exhibit an increase in proteasome activity and an enhanced response to proteasome inhibition in the bone marrow microenvironment in vivo. Am J Hematol 2009;84:268-272.
74. Zangari M, Yaccoby S, Cavallo F, Esseltine D, Tricot G. Response to bortezomib and activation of osteoblasts in multiple myeloma. Clin Lymphoma Myeloma 2006;7:109-114. (Pubitemid 44596593)
75. Zangari M, Pappas L, Zhan F, et al. Parathyroid hormones (PTH) serum variations are associated with bortezomib response in multiple myeloma patients. In: The 50th Annual Meeting of the American Society of Hematology, December 2008, San Francisco, USA (Abstract 2783).
76. Zangari M, Esseltine D, Cavallo F, et al. Predictive value of alkaline phosphatase for response and time to progression in bortezomib-treated multiple myeloma patients. Am J Hematol 2007;82:831-833.
77. Terpos E, Heath DJ, Rahemtulla A, et al. Bortezomib reduces serum dickkopf-1 and receptor activator of nuclear factor-kB ligand concentrations and normalises indices of bone remodelling in patients with relapsed multiple myeloma. Br J Haematol 2006;135:688-692.
78. Heider U, Kaiser M, Muller C, et al. Bortezomib increases osteoblast activity in myeloma patients irrespective of response to treatment. Eur J Haematol 2006;77:233-238.
79. Garayoa M, Garcia JL, Santamaria C, et al. Mesenchymal stem cells from multiple myeloma patients display distinct genomic profile as compared with those from normal donors. Leukemia 2009;23:1515-1527.
80. Wallace SR, Oken MM, Lunetta KL, Panoskaltsis-Mortari A, Masellis AM. Abnormalities of bone marrow mesenchymal cells in multiple myeloma patients. Cancer 2001;91:1219-1230.
81. Prockop DJ, Gregory CA, Spees JL. One strategy for cell and gene therapy: harnessing the power of adult stem cells to repair tissues. Proc Natl Acad Sci USA 2003;100 (Suppl 1):11917-11923.
82. Prockop DJ, Olson SD. Clinical trials with adult stem/ progenitor cells for tissue repair: let's not overlook some essential precautions. Blood 2007;109:3147-3151.
83. Rabin N, Kyriakou C, Coulton L, et al. A new xenograft model of myeloma bone disease demonstrating the efficacy of human mesenchymal stem cells expressing osteoprotegerin by lentiviral gene transfer. Leukemia 2007;21:2181-2191.
84. Weinstein RS, Jilka RL, Parfitt AM,Manolagas SC. Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids. Potential mechanisms of their deleterious effects on bone. J Clin Invest 1998; 102:274-282.
85. Weinstein RS, Chen JR, Powers CC, et al. Promotion of osteoclast survival and antagonism of bisphosphonate-induced osteoclast apoptosis by glucocorticoids. J Clin Invest 2002; 109:1041-1048.