The role of megakaryocytes in skeletal homeostasis and rheumatoid arthritis

Current Opinion in Rheumatology

Volumn 18, Issue 4, 2006, Pages 405-410

  Kacena, Melissa A ^a   Horowitz, Mark C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytokines; Fibroblasts; Megakaryocytes; Osteoblasts; Osteoclasts; Osteoprotegerin; Rheumatoid arthritis; Thrombopoietin

Indexed keywords

CYTOKINE;

BONE DENSITY; BONE DEVELOPMENT; BONE EROSION; HOMEOSTASIS; HUMAN; MEGAKARYOCYTE; OSSIFICATION; OSTEOLYSIS; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SYNOVIAL FLUID; THROMBOCYTOSIS; UPREGULATION;

ARTHRITIS, RHEUMATOID; BONE AND BONES; BONE DEVELOPMENT; BONE RESORPTION; CYTOKINES; HUMANS; INFLAMMATION; MEGAKARYOCYTES; MODELS, BIOLOGICAL; THROMBOPOIESIS;

EID: 33748065968     PISSN: 10408711     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.bor.0000231910.42666.31     Document Type: Review

References (86)

1. Walsh NC, Crotti TN, Goldring SR, Gravallese EM. Rheumatic diseases: the effects of inflammation on bone. Immunol Rev 2005; 208:228-251. This paper does an excellent job at reviewing bone resorption in the context of the pro-inflammatory cytokines associated with RA and other rheumatic diseases.
2. Roodman GD. Advances in bone biology: the osteoclast. Endocr Rev 1996; 17:308-332.
3. Udagawa N, Takahashi N, Akatsu T, et al. Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells. Proc Natl Acad Sci U S A 1990; 87:7260-7264.
4. Suda T, Takahashi N, Udagawa N, et al. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr Rev 1999; 20:345-357.
5. Wiktor-Jedrzejczak W, Bartocci A, Ferrante AW Jr, et al. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc Natl Acad Sci U S A 1990; 87:4828-4832.
6. Felix R, Cecchini MG, Fleisch H. Macrophage colony stimulating factor restores in vivo bone resorption in the op/op osteopetrotic mouse. Endocrinology 1990; 127:2592-2594.
7. Hamilton JA. CSF-1 signal transduction. J Leukoc Biol 1997; 62:145-155.
8. Simonet WS, Lacey DL, Dunstan CR, et al. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 1997; 89:309-319.
9. Kim N, Kadono Y, Takami M, et al. Osteoclast differentiation independent of the TRANCE-RANK-TRAF6 axis. J Exp Med 2005; 202:589-595.
10. Bord S, Frith E, Ireland DC, et al. Megakaryocytes modulate osteoblast synthesis of type-I collagen, osteoprotegerin, and RANKL. Bone 2005; 36:812-819. This research demonstrates that megakaryocytes stimulate both OPG and RANKL expression in cells of the osteoblast lineage.
11. Kartsogiannis V, Zhou H, Horwood NJ, et al. Localization of RANKL (receptor activator of NF kappa B ligand) mRNA and protein in skeletal and extraskeletal tissues. Bone 1999; 25:525-534.
12. Kong YY, Feige U, Sarosi I, et al. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 1999; 402:304-309.
13. Manabe N, Kawaguchi H, Chikuda H, et al. Connection between B lymphocyte and osteoclast differentiation pathways. J Immunol 2001; 167:2625-2631.
14. Bord S, Ireland DC, Beavan SR, Compston JE. The effects of estrogen on osteoprotegerin, RANKL, and estrogen receptor expression in human osteoblasts. Bone 2003; 32:136-141.
15. Bord S, Frith E, Ireland DC, et al. Synthesis of osteoprotegerin and RANKL by megakaryocytes is modulated by oestrogen. Br J Haematol 2004; 126:244-251.
16. 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 U S A 2001; 98:11581-11586.
17. Chagraoui H, Sabri S, Capron C, et al. Expression of osteoprotegerin mRNA and protein in murine megakaryocytes. Exp Hematol 2003; 31:1081-1088.
18. Kacena MA, Gundberg CM, Horowitz MC. A novel role for megakaryocytes in the inhibition of osteoclast formation. J Bone Miner Res 2004; 19:S155.
19. Jiang S, Levine JD, Fu Y, et al. Cytokine production by primary bone marrow megakaryocytes. Blood 1994; 84:4151-4156.
20. Soslau G, Morgan DA, Jaffe JS, et al. Cytokine mRNA expression in human platelets and a megakaryocytic cell line and cytokine modulation of platelet function. Cytokine 1997; 9:405-411.
21. Wickenhauser C, Hillienhof A, Jungheim K, et al. Detection and quantification of transforming growth factor beta (TGF-beta) and platelet-derived growth factor (PDGF) release by normal human megakaryocytes. Leukemia 1995; 9:310-315.
22. Wickenhauser C, Lorenzen J, Thiele J, et al. Secretion of cytokines (interleukins-1 alpha, -3, and -6 and granulocyte-macrophage colony-stimulating factor) by normal human bone marrow megakaryocytes. Blood 1995; 85:685-691.
23. Wakikawa T, Shioi A, Hino M, et al. Thrombopoietin inhibits in vitro osteoclastogenesis from murine bone marrow cells. Endocrinology 1997; 138:4160-4166.
24. Kacena MA, Shivdasani RA, Wilson K, et al. Megakaryocyte-osteoblast interaction revealed in mice deficient in transcription factors GATA-1 and NF-E2. J Bone Miner Res 2004; 19:652-660.
25. Miao D, Murant S, Scutt N, et al. Megakaryocyte-bone marrow stromal cell aggregates demonstrate increased colony formation and alkaline phosphatase expression in vitro. Tissue Eng 2004; 10:807-817.
26. Schmitz B, Thiele J, Otto F, et al. Interactions between endogeneous lectins and fucosylated oligosaccharides in megakaryocyte-dependent fibroblast growth of the normal bone marrow. Leukemia 1996; 10:1604-1614.
27. Schmitz B, Thiele J, Witte O, et al. Influence of cytokines (IL-1 alpha, IL-3, IL-11, GM-CSF) on megakaryocyte-fibroblast interactions in normal human bone marrow. Eur J Haematol 1995; 55:24-32.
28. Schmitz B, Wickenhauser C, Thiele J, et al. Megakaryocyte induced fibroblast proliferation is enhanced by costimulation with IL-6/IL-3 and dependent on secretory and adhesion events. Leuk Res 1999; 23:723-729.
29. Gao YH, Shinki T, Yuasa T, et al. Potential role of cbfa1, an essential transcriptional factor for osteoblast differentiation, in osteoclastogenesis: regulation of mRNA expression of osteoclast differentiation factor (ODF). Biochem Biophys Res Commun 1998; 252:697-702.
30. Hofbauer LC, Dunstan CR, Spelsberg TC, et al. Osteoprotegerin production by human osteoblast lineage cells is stimulated by vitamin D, bone morphogenetic protein-2, and cytokines. Biochem Biophys Res Commun 1998; 250:776-781.
31. Hofbauer LC, Heufelder AE. Osteoprotegerin and its cognate ligand: a new paradigm of osteoclastogenesis. Eur J Endocrinol 1998; 139:152-154.
32. Vidal ON, Sjogren K, Eriksson BI, et al. Osteoprotegerin mRNA is increased by interleukin-1 alpha in the human osteosarcoma cell line MG-63 and in human osteoblast-like cells. Biochem Biophys Res Commun 1998; 248:696-700.
33. Udagawa N, Takahashi N, Jimi E, et al. Osteoblasts/stromal cells stimulate osteoclast activation through expression of osteoclast differentiation factor/RANKL but not macrophage colony-stimulating factor: receptor activator of NF-kappa B ligand. Bone 1999; 25:517-523.
34. Nakano K, Okada Y, Saito K, Tanaka Y. Induction of RANKL expression and osteoclast maturation by the binding of fibroblast growth factor 2 to heparan sulfate proteoglycan on rheumatoid synovial fibroblasts. Arthritis Rheum 2004; 50:2450-2458.
35. Mitani M, Miura Y, Saura R, et al. Estrogen specifically stimulates expression and production of osteoprotegerin from rheumatoid synovial fibroblasts. Int J Mol Med 2005; 15:827-832.
36. Wei X, Zhang X, Zuscik MJ, et al. Fibroblasts express RANKL and support osteoclastogenesis in a COX-2-dependent manner after stimulation with titanium particles. J Bone Miner Res 2005; 20:1136-1148.
37. Thiede MA, Smock SL, Petersen DN, et al. Presence of messenger ribonucleic acid encoding osteocalcin, a marker of bone turnover, in bone marrow megakaryocytes and peripheral blood platelets. Endocrinology 1994; 135:929-937.
38. Kelm RJ Jr, Hair GA, Mann KG, Grant BW. Characterization of human osteoblast and megakaryocyte-derived osteonectin (SPARC). Blood 1992; 80:3112-3119.
39. Breton-Gorius J, Clezardin P, Guichard J, et al. Localization of platelet osteonectin at the internal face of the alpha-granule membranes in platelets and megakaryocytes. Blood 1992; 79:936-941.
40. Chenu C, Delmas PD. Platelets contribute to circulating levels of bone sialoprotein in human. J Bone Miner Res 1992; 7:47-54.
41. Frank JD, Balena R, Masarachia P, et al. The effects of three different demineralization agents on osteopontin localization in adult rat bone using immunohistochemistry. Histochemistry 1993; 99:295-301.
42. Sipe JB, Zhang J, Waits C, et al. Localization of bone morphogenetic proteins (BMPs)-2, -4, and -6 within megakaryocytes and platelets. Bone 2004; 35:1316-1322.
43. Vannucchi AM, Bianchi L, Cellai C, et al. Development of myelofibrosis in mice genetically impaired for GATA-1 expression (GATA-1(low) mice). Blood 2002; 100:1123-1132.
44. Frey BM, Rafii S, Crystal RG, Moore MA. Adenovirus long-term expression of thrombopoietin in vivo: a new model for myeloproliferative syndrome and osteomyelofibrosis. Schweiz Med Wochenschr 1998; 128:1587-1592.
45. Yan XQ, Lacey D, Fletcher F, et al. Chronic exposure to retroviral vector encoded MGDF (mpl-ligand) induces lineage-specific growth and differentiation of megakaryocytes in mice. Blood 1995; 86:4025-4033.
46. Yan XQ, Lacey D, Hill D, et al. A model of myelofibrosis and osteosclerosis in mice induced by overexpressing thrombopoietin (mpl ligand): reversal of disease by bone marrow transplantation. Blood 1996; 88:402-409.
47. Villeval JL, Cohen-Solal K, Tulliez M, et al. High thrombopoietin production by hematopoietic cells induces a fatal myeloproliferative syndrome in mice. Blood 1997; 90:4369-4383.
48. McDevitt MA, Shivdasani RA, Fujiwara Y, et al. A "knockdown" mutation created by cis-element gene targeting reveals the dependence of erythroid cell maturation on the level of transcription factor GATA-1. Proc Natl Acad Sci USA 1997; 94:6781-6785.
49. Shivdasani RA, Rosenblatt MF, Zucker-Franklin D, et al. Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/MGDF in megakaryocyte development. Cell 1995; 81: 695-704.
50. Kacena MA, Gundberg CM, Nelson T, Horowitz MC. Loss of the transcription factor p45 NF-E2 results in a developmental arrest of megakaryocyte differentiation and the onset of a high bone mass phenotype. Bone 2005; 36:215-223.
51. Haznedaroglu IC, Benekli M, Dundar S. Thrombopoietin, megakaryocytopoietic cytokines, and reactive versus clonal megakaryocytopoiesis: an enigma complex. Blood 1996; 87:1654.
52. Joffe I, Epstein S. Osteoporosis associated with rheumatoid arthritis: pathogenesis and management. Semin Arthritis Rheum 1991; 20:256-272.
53. Peel NF, Eastell R, Russell RG. Osteoporosis in rheumatoid arthritis - the laboratory perspective. Br J Rheumatol 1991; 30:84-85.
54. Neva MH, Isomaki P, Hannonen P, et al. Early and extensive erosiveness in peripheral joints predicts atlantoaxial subluxations in patients with rheumatoid arthritis. Arthritis Rheum 2003; 48:1808-1813.
55. Neva MH, Kotaniemi A, Kaarela K, et al. Atlantoaxial disorders in rheumatoid arthritis associate with the destruction of peripheral and shoulder joints, and decreased bone mineral density. Clin Exp Rheumatol 2003; 21:179-184.
56. Woolf AD. Osteoporosis in rheumatoid arthritis - the clinical viewpoint. Br J Rheumatol 1991; 30:82-84.
57. Ertenli I, Kiraz S, Ozturk MA, et al. Pathologic thrombopoiesis of rheumatoid arthritis. Rheumatol Int 2003; 23:49-60.
58. Hermann JA, Hall MA, Maini RN, et al. Important immunoregulatory role of interleukin-11 in the inflammatory process in rheumatoid arthritis. Arthritis Rheum 1998; 41:1388-1397.
59. Okamoto H, Yamamura M, Morita Y, et al. The synovial expression and serum levels of interleukin-6, interleukin-11, leukemia inhibitory factor, and oncostatin M in rheumatoid arthritis. Arthritis Rheum 1997; 40:1096-1105.
60. Trepicchio WL, Wang L, Bozza M, Dorner AJ. IL-11 regulates macrophage effector function through the inhibition of nuclear factor-kappaB. J Immunol 1997; 159:5661-5670.
61. Kaushansky K. Thrombopoietin: the primary regulator of platelet production. Blood 1995; 86:419-431.
62. Horwood NJ, Elliott J, Martin TJ, Gillespie MT. Osteotropic agents regulate the expression of osteoclast differentiation factor and osteoprotegerin in osteoblastic stromal cells. Endocrinology 1998; 139:4743-4746.
63. Carsons SE, Santiago-Schwarz F, Diola C. Detection and quantitation of stem cell factor (kit ligand) in the synovial fluid of patients with rheumatic disease. J Rheumatol 2000; 27:2798-2800.
64. Avraham H, Vannier E, Cowley S, et al. Effects of the stem cell factor, c-kit ligand, on human megakaryocytic cells. Blood 1992; 79:365-371.
65. Demulder A, Suggs SV, Zsebo KM, et al. Effects of stem cell factor on osteoclast-like cell formation in long-term human marrow cultures. J Bone Miner Res 1992; 7:1337-1344.
66. Waring PM, Carroll GJ, Kandiah DA, et al. Increased levels of leukemia inhibitory factor in synovial fluid from patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum 1993; 36:911-915.
67. Atkins GJ, Haynes DR, Geary SM, et al. Coordinated cytokine expression by stromal and hematopoietic cells during human osteoclast formation. Bone 2000; 26:653-661.
68. Gorny G, Shaw A, Oursler MJ, IL-6. LIF, and TNF-alpha regulation of GM-CSF inhibition of osteoclastogenesis in vitro. Exp Cell Res 2004; 294:149-158.
69. Houssiau FA, Devogelaer JP, Van Damme J, et al. Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum 1988; 31:784-788.
70. Gewirtz AM. Megakaryocytopoiesis: the state of the art. Thromb Haemost 1995; 74:204-209.
71. Ishibashi T, Kimura H, Shikama Y, et al. Interleukin-6 is a potent thrombopoietic factor in vivo in mice. Blood 1989; 74:1241-1244.
72. Ishibashi T, Kimura H, Uchida T, et al. Human interleukin 6 is a direct promoter of maturation of megakaryocytes in vitro. Proc Natl Acad Sci U S A 1989; 86:5953-5957.
73. Liu XH, Kirschenbaum A, Yao S, Levine AC. Cross-talk between the interleukin-6 and prostaglandin E(2) signaling systems results in enhancement of osteoclastogenesis through effects on the osteoprotegerin/receptor activator of nuclear factor-{kappa}B (RANK) ligand/RANK system. Endocrinology 2005; 146:1991-1998.
74. Nakamura H, Ueki Y, Sakito S, et al. High serum and synovial fluid granulocyte colony stimulating factor (G-CSF) concentrations in patients with rheumatoid arthritis. Clin Exp Rheumatol 2000; 18:713-718.
75. Kokai Y, Wada T, Oda T, et al. Overexpression of granulocyte colony-stimulating factor induces severe osteopenia in developing mice that is partially prevented by a diet containing vitamin K2 (menatetrenone). Bone 2002; 30:880-885.
76. Lee MY, Fevold KL, Muguruma Y, Lottsfeldt JL. Conditions that support long-term production of osteoclast progenitors in vitro. Stem Cells 1997; 15:340-346.
77. Kaushansky K, Broudy VC, Lin N, et al. Thrombopoietin, the Mp1 ligand, is essential for full megakaryocyte development. Proc Natl Acad Sci USA 1995; 92:3234-3238.
78. Kaushansky K. Thrombopoietin. N Engl J Med 1998; 339:746-754.
79. Kiraz S, Ertenli I, Ozturk MA, et al. Bloodstream thrombopoietin in rheumatoid arthritis with thrombocytosis. Clin Rheumatol 2002; 21:453-456.
80. Chagraoui H, Tulliez M, Smayra T, et al. Stimulation of osteoprotegerin production is responsible for osteosclerosis in mice overexpressing TPO. Blood 2003; 101:2983-2989.
81. Kakumitsu H, Kamezaki K, Shimoda K, et al. Transgenic mice overexpressing murine thrombopoietin develop myelofibrosis and osteosclerosis. Leuk Res 2005; 29:761-769.
82. Chagraoui H, Komura E, Tulliez M, et al. Prominent role of TGF-beta 1 in thrombopoietin-induced myelofibrosis in mice. Blood 2002; 100:3495-3503.
83. Ertenli I, Kiraz S, Arici M, et al. P-selectin as a circulating molecular marker in rheumatoid arthritis with thrombocytosis. J Rheumatol 1998; 25:1054-1058.
84. Farr M, Scott DL, Constable TJ, et al. Thrombocytosis of active rheumatoid disease. Ann Rheum Dis 1983; 42:545-549.
85. Gough A, Sambrook P, Devlin J, et al. Osteoclastic activation is the principal mechanism leading to secondary osteoporosis in rheumatoid arthritis. J Rheumatol 1998; 25:1282-1289.
86. Hirayama T, Danks L, Sabokbar A, Athanasou NA. Osteoclast formation and activity in the pathogenesis of osteoporosis in rheumatoid arthritis. Rheumatology (Oxford) 2002; 41:1232-1239.