A novel role for CCL3 (MIP-1α) in myeloma-induced bone disease via osteocalcin downregulation and inhibition of osteoblast function

Leukemia

Volumn 25, Issue 7, 2011, Pages 1174-1181

  Vallet, S ^a,b,c   Pozzi, S ^a,b   Patel, K ^a   Vaghela, N ^a   Fulciniti, M T ^b   Veiby, P ^d   Hideshima, T ^b   Santo, L ^b   Cirstea, D ^b   Scadden, D T ^a   Anderson, K C ^b   Raje, N ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d MILLENNIUM PHARMACEUTICALS INC   (United States)

Author keywords

CCL3; ERK; myeloma; osteoblast; osteocalcin; osterix

Indexed keywords

CHEMOKINE RECEPTOR CCR ANTAGONIST; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; MLN 3897; OSTEOCALCIN; TRANSCRIPTION FACTOR OSTERIX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE DISEASE; BONE MARROW CELL; BONE MINERALIZATION; CATABOLISM; CELL FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; MOUSE; MULTIPLE MYELOMA; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STROMA CELL; UPREGULATION;

ANIMALS; BONE MARROW CELLS; BONE REMODELING; CALCIFICATION, PHYSIOLOGIC; CELL LINE, TUMOR; CHEMOKINE CCL3; DOWN-REGULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MESENCHYMAL STEM CELLS; MICE; MICE, SCID; MULTIPLE MYELOMA; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; OSTEOBLASTS; OSTEOCALCIN; OSTEOCLASTS; OSTEOGENESIS; OSTEOLYSIS; RECEPTORS, CCR1; RECEPTORS, CCR5; STROMAL CELLS; TRANSCRIPTION FACTORS;

EID: 79960269049     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2011.43     Document Type: Article

References (31)

1. Saad F, Lipton A, Cook R, Chen YM, Smith M, Coleman R. Pathologic fractures correlate with reduced survival in patients with malignant bone disease. Cancer 2007; 110: 1860-1867. (Pubitemid 47557312)
2. Bataille R, Chappard D, Marcelli C, Dessauw P, Sany J, Baldet P et al. Mechanisms of bone destruction in multiple myeloma: the importance of an unbalanced process in determining the severity of lytic bone disease. J Clin Oncol 1989; 7: 1909-1914. (Pubitemid 20014340)
3. Han JH, Choi SJ, Kurihara N, Koide M, Oba Y, Roodman GD. Macrophage inflammatory protein-1alpha is an osteoclastogenic factor in myeloma that is independent of receptor activator of nuclear factor kappaB ligand. Blood 2001; 97: 3349-3353.
4. Lentzsch S, Gries M, Janz M, Bargou R, Dorken B, Mapara MY. Macrophage inflammatory protein 1-alpha (MIP-1 alpha) triggers migration and signaling cascades mediating survival and proliferation in multiple myeloma (MM) cells. Blood 2003; 101: 3568-3573. (Pubitemid 36857943)
5. Vallet S, Raje N, Ishitsuka K, Hideshima T, Podar K, Chhetri S et al. MLN3897, a novel CCR1 inhibitor, impairs osteoclastogenesis and inhibits the interaction of multiple myeloma cells and osteoclasts. Blood 2007; 110: 3744-3752. (Pubitemid 350159645)
6. Abbas S, Zhang YH, Clohisy JC, Abu-Amer Y. Tumor necrosis factor-alpha inhibits pre-osteoblast differentiation through its type-1. receptor. Cytokine 2003; 22: 33-41. (Pubitemid 37222300)
7. Yano S, Mentaverri R, Kanuparthi D, Bandyopadhyay S, Rivera A, Brown EM et al. Functional expression of beta-chemokine receptors in osteoblasts: role of regulated upon activation, normal T cell expressed and secreted (RANTES) in osteoblasts and regulation of its secretion by osteoblasts and osteoclasts. Endocrinology 2005; 146: 2324-2335. (Pubitemid 40577520)
8. Vincent C, Findlay DM, Welldon KJ, Wijenayaka AR, Zheng TS, Haynes DR et al. Pro-inflammatory cytokines TNF-related weak inducer of apoptosis (TWEAK) and TNFalpha induce the mitogenactivated protein kinase (MAPK)-dependent expression of sclerostin in human osteoblasts. J Bone Miner Res 2009; 24: 1434-1449.
9. Greenstein S, Krett NL, Kurosawa Y, Ma C, Chauhan D, Hideshima T et al. Characterization of the MM 1 human multiple myeloma (MM) cell lines: a model system to elucidate the characteristics, behavior, and signaling of steroid-sensitive and-resistant MM cells. Exp Hematol 2003; 31: 271-282. (Pubitemid 36407603)
10. Burger R, Guenther A, Bakker F, Schmalzing M, Bernand S, BaumWet al. Gp130 and ras mediated signaling in human plasma cell line INA-6: a cytokine-regulated tumor model for plasmacytoma. Hematol J 2001; 2: 42-53. (Pubitemid 32266385)
11. 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. Pro Natl Acad Sci USA 2010; 107: 5124-5129.
12. Derkx P, Nigg AL, Bosman FT, Birkenhager-Frenkel DH, Houtsmuller AB, Pols HA et al. Immunolocalization and quantification of noncollagenous bone matrix proteins in methylmethacrylateembedded adult human bone in combination with histomorphometry. Bone 1998; 22: 367-373. (Pubitemid 28177190)
13. Tassone P, Neri P, Carrasco DR, Burger R, Goldmacher VS, Fram R et al. A clinically relevant SCID-hu in vivo model of human multiple myeloma. Blood 2005; 106: 713-716. (Pubitemid 40981270)
14. Rasband WS. ImageJ. In: US National Institutes of Health B, Maryland U, (eds) US National Institutes of Health: Bethesda, Maryland, USA. http://rsb.info.nih.gov/ij/; 1997-2006.
15. Stein GS, Lian JB, Owen TA. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. Faseb J 1990; 4: 3111-3123.
16. Uneda S, Hata H, Matsuno F, Harada N, Mitsuya Y, Kawano F et al. Macrophage inflammatory protein-1 alpha is produced by human multiple myeloma (MM) cells and its expression correlates with bone lesions in patients with MM. Br J Haematol 2003; 120: 53-55. (Pubitemid 36056908)
17. Roecklein BA, Torok-Storb B. Functionally distinct human marrow stromal cell lines immortalized by transduction with the human papilloma virus E6/E7 genes. Blood 1995; 85: 997-1005.
18. Graf L, Iwata M, Torok-Storb B. Gene expression profiling of the functionally distinct human bone marrow stromal cell lines HS-5 and HS-27a. Blood 2002; 100: 1509-1511. (Pubitemid 34864317)
19. Boskey AL, Gadaleta S, Gundberg C, Doty SB, Ducy P, Karsenty G. Fourier transform infrared microspectroscopic analysis of bones of osteocalcin-deficient mice provides insight into the function of osteocalcin. Bone 1998; 23: 187-196. (Pubitemid 28434662)
20. Kavukcuoglu NB, Patterson-Buckendahl P, Mann AB. Effect of osteocalcin deficiency on the nanomechanics and chemistry of mouse bones. J Mechan Behav Biomed Materials 2009; 2: 348-354.
21. Terpos E, Politou M, Szydlo R, Goldman JM, Apperley JF, Rahemtulla A. Serum levels of macrophage inflammatory protein-1 alpha (MIP-1alpha) correlate with the extent of bone disease and survival in patients with multiple myeloma. Br J Haematol 2003; 123: 106-109. (Pubitemid 37222765)
22. Sordi V, Malosio ML, Marchesi F, Mercalli A, Melzi R, Giordano T et al. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 2005; 106: 419-427. (Pubitemid 40981232)
23. Honczarenko M, Le Y, Swierkowski M, Ghiran I, Glodek AM, Silberstein LE. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem cells (Dayton, Ohio) 2006; 24: 1030-1041. (Pubitemid 44464736)
24. Giuliani N, Colla S, Morandi F, Lazzaretti M, Sala R, Bonomini S 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. (Pubitemid 41510822)
25. Tian E, Zhan F, Walker R, Rasmussen E, Ma Y, Barlogie B 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. (Pubitemid 38010074)
26. Lu X, Gilbert L, He X, Rubin J, Nanes MS. Transcriptional regulation of the osterix (Osx, Sp7) promoter by tumor necrosis factor identifies disparate effects of mitogen-activated protein kinase and NF kappa B pathways. J Biol Chem 2006; 281: 6297-6306. (Pubitemid 43847561)
27. Roussou M, Tasidou A, Dimopoulos MA, Kastritis E, Migkou M, Christoulas D et al. Increased expression of macrophage inflammatory protein-1alpha on trephine biopsies correlates with extensive bone disease, increased angiogenesis and advanced stage in newly diagnosed patients with multiple myeloma. Leukemia 2009; 23: 2177-2181.
28. Hipskind RA, Bilbe G. MAP kinase signaling cascades and gene expression in osteoblasts. Front Biosci 1998; 3: d804-d816.
29. Higuchi C, Myoui A, Hashimoto N, Kuriyama K, Yoshioka K, Yoshikawa H et al. Continuous inhibition of MAPK signaling promotes the early osteoblastic differentiation and mineralization of the extracellular matrix. J Bone Miner Res 2002; 17: 1785-1794.
30. Kono SJ, Oshima Y, Hoshi K, Bonewald LF, Oda H, Nakamura K et al. Erk pathways negatively regulate matrix mineralization. Bone 2007; 40: 68-74. (Pubitemid 44839341)
31. Raucci A, Bellosta P, Grassi R, Basilico C, Mansukhani A. Osteoblast proliferation or differentiation is regulated by relative strengths of opposing signaling pathways. J Cell Physiol 2008; 215: 442-451. (Pubitemid 351468956)