Bone and the innate immune system

Current Osteoporosis Reports

Volumn 12, Issue 1, 2014, Pages 1-8

  Charles, Julia F ^a   Nakamura, Mary C ^b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Autophagy; Bone; Innate immunity; Necroptosis; Osteoclast; Osteocyte; Osteomac

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1; INTERLEUKIN 6; OSTEOCLAST DIFFERENTIATION FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANTIGEN RECOGNITION; APOPTOSIS; AUTOIMMUNITY; AUTOPHAGY; BONE DEVELOPMENT; BONE REGENERATION; BONE REMODELING; BONE TURNOVER; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINE RELEASE; DENDRITIC CELL; HEMATOPOIESIS; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; MACROPHAGE; NONHUMAN; OSTEOCLAST; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; OSTEOLYSIS; PHAGOCYTOSIS; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; RHEUMATOID ARTHRITIS; TISSUE INJURY; TISSUE REPAIR;

APOPTOSIS; AUTOPHAGY; BONE AND BONES; BONE REMODELING; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; OSTEOCLASTS;

EID: 84893205545     PISSN: 15441873     EISSN: 15442241     Source Type: Journal    
DOI: 10.1007/s11914-014-0195-2     Document Type: Review

References (94)

1. Mori G, D'Amelio P, Faccio R, Brunetti G. The interplay between the bone and the immune system. Clin Dev Immunol. 2013:720504.
2. Takayanagi H. Osteoimmunology and the effects of the immune system on bone. Nat Rev Rheumatol. 2009;5:667-76.
3. Takayanagi H. New developments in osteoimmunology. Nat Rev Rheumatol. 2012;8:684-9.
4. Jones D, Glimche LH, Aliprantis AO. Osteoimmunology at the nexus of arthritis, osteoporosis, cancer, and infection. J Clin Invest. 2011;121:2534-42.
5. Pacifici R. Role of T cells in ovariectomy induced bone loss-revisited. J Bone Miner Res. 2012;27:231-9.
6. Baker-LePain JC, Nakamura MC, Lane NE. Effects of inflammation on bone: an update. Curr Opin Rheumatol. 2011;23:389-95.
7. Braun T, Zwerina J. Positive regulators of osteoclastogenesis and bone resorption in rheumatoid arthritis. Arthritis Res Ther. 2011;13:235.
8. Zhao B, Ivashkiv LB. Negative regulation of osteoclastogenesis and bone resorption by cytokines and transcriptional repressors. Arthritis Res Ther. 2011;13:234.
9. Soderstrom K, Stein E, Colmenero P, Purath U, Muller-Ladner U, de Matos CT, et al. Natural killer cells trigger osteoclastogenesis and bone destruction in arthritis. Proc Natl Acad Sci U S A. 2010;107:13028-33.
10. Chakravarti A, Raquil MA, Tessier P, Poubelle PE. Surface RANKL of toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood. 2009;114:1633-44.
11. • Charles JF, Hsu LY, Niemi EC, Weiss A, Aliprantis AO, Nakamura MC. Inflammatory arthritis increases mouse osteoclast precursors with myeloid suppressor function. J Clin Invest. 2012;122:4592-605. First demonstration of shared relationship of osteoclast precursors and myeloid dervied suppressor cells.
12. Jacome-Galarza CE, Lee SK, Lorenzo JA, Aguila HL. Identification, characterization, and isolation of a common progenitor for osteoclasts, macrophages, and dendritic cells from murine bone marrow and periphery. J Bone Miner Res. 2013;28:1203-13.
13. Rivollier A, Mazzorana M, Tebib J, Piperno M, Aitsiselmi T, Rabourdin-Combe C, et al. Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment. Blood. 2004;104:4029-37. (Pubitemid 39620153)
14. Alnaeeli M, Penninger JM, Teng YT. Immune interactions with CD4+ T cells promote the development of functional osteoclasts from murine CD11c+dendritic cells. J Immunol. 2006;177:3314-26. (Pubitemid 44277851)
15. Wakkach A, Mansour A, Dacquin R, Coste E, Jurdic P, Carle GF, et al. Bone marrow microenvironment controls the in vivo differentiation of murine dendritic cells into osteoclasts. Blood. 2008;112:5074-83.
16. McKenna HJ, Stocking KL, Miller RE, Brasel K, De Smedt T, Maraskovsky E, et al. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood. 2000;95:3489-97. (Pubitemid 30428482)
17. Tucci M, Stucci S, Savonarola A, Ciavarella S, Cafforio P, Dammacco F, et al. Immature dendritic cells in multiple myeloma are prone to osteoclast-like differentiation through interleukin-17A stimulation. Br J Haematol. 2013;161:821-31.
18. Bar-Shavit Z. Taking a toll on the bones: regulation of bone metabolism by innate immune regulators. Autoimmunity. 2008;41:195-203. (Pubitemid 351454989)
19. Takami M, Kim N, Rho J, Choi Y. Stimulation by toll-like receptors inhibits osteoclast differentiation. J Immunol. 2002;169:1516-23. (Pubitemid 34809198)
20. Seeling M, Hillenhoff U, David JP, Schett G, Tuckermann J, Lux A, et al. Inflammatory monocytes and Fcgamma receptor IV on osteoclasts are critical for bone destruction during inflammatory arthritis in mice. Proc Natl Acad Sci U S A. 2013;110:10729-34.
21. Wu Y, Humphrey MB, Nakamura MC. Osteoclasts - the innate immune cells of the bone. Autoimmunity. 2008;41:183-94. (Pubitemid 351454988)
22. Boyce BF, Rosenberg E, de Papp AE, le Duong T. The osteoclast, bone remodelling, and treatment of metabolic bone disease. Eur J Clin Invest. 2012;42:1332-41.
23. Del Fattore A, Cappariello A, Teti A. Genetics, pathogenesis and complications of osteopetrosis. Bone. 2008;42:19-29. (Pubitemid 350297169)
24. Chazaud B. Macrophages: supportive cells for tissue repair and regeneration. Immunobiology. 2013.
25. Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013;13:722-37.
26. •• Chang MK, Raggatt LJ, Alexander KA, Kuliwaba JS, Fazzalari NL, Schroder K, et al. Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol. 2008;181:1232-44. First demonstration of the "osteomac" cells as tissue resident macrophages in the bone.
27. Alexander KA, Chang MK, Maylin ER, Kohler T, Muller R, Wu AC, et al. Osteal macrophages promote in vivo intramembranous bone healing in a mouse tibial injury model. J Bone Miner Res. 2011;26:1517-32.
28. Jilka RL, Weinstein RS, Bellido T, Parfitt AM, Manolagas SC. Osteoblast programmed cell death (apoptosis): modulation by growth factors and cytokines. J Bone Miner Res. 1998;13:793-802. (Pubitemid 28224195)
29. Hochreiter-Hufford A, Ravichandran KS. Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol. 2013;5:a008748.
30. Lin YL, de Villiers WJ, Garvy B, Post SR, Nagy TR, Safadi FF, et al. The effect of class a scavenger receptor deficiency in bone. J Biol Chem. 2007;282:4653-60. (Pubitemid 47100985)
31. Takemura K, Sakashita N, Fujiwara Y, Komohara Y, Lei X, Ohnishi K, et al. Class A scavenger receptor promotes osteoclast differentiation via the enhanced expression of receptor activator of NF-kappaB (RANK). Biochem Biophys Res Comm. 2010;391:1675-80.
32. Kevorkova O, Martineau C, Martin-Falstrault L, Sanchez-Dardon J, Brissette L, Moreau R. Low-bone-mass phenotype of deficient mice for the Cluster of Differentiation 36 (CD36). PloS One. 2013;8:e77701.
33. Jilka RL, Noble B, Weinstein RS. Osteocyte apoptosis. Bone. 2013;54:264-71.
34. Kennedy OD, Herman BC, Laudier DM, Majeska RJ, Sun HB, Schaffler MB. Activation of resorption in fatigue-loaded bone involves both apoptosis and active pro-osteoclastogenic signaling by distinct osteocyte populations. Bone. 2012;50:1115-22.
35. Verborgt O, Gibson GJ, Schaffler MB. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res. 2000;15:60-7. (Pubitemid 30026933)
36. Cardoso L, Herman BC, Verborgt O, Laudier D, Majeska RJ, Schaffler MB. Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue. J Bone Miner Res. 2009;24:597-605.
37. Noble BS, Peet N, Stevens HY, Brabbs A, Mosley JR, Reilly GC, et al. Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am J Physiol Cell Physiol. 2003;284:C934-43. (Pubitemid 36336949)
38. Aguirre JI, Plotkin LI, Stewart SA, Weinstein RS, Parfitt AM, Manolagas SC, et al. Osteocyte apoptosis is induced by weightlessness in mice and precedes osteoclast recruitment and bone loss. J Bone Miner Res. 2006;21:605-15.
39. Cabahug PCLD. Kennedy OD. Tuthill A, Judex S, Shaffler MB. Inhibition of osteocyte apoptosis prevents trabecular bone loss after unloading of mouse long bone. Orthopaedic Research Society: Majeska RJ; 2013.
40. Emerton KB, Hu B, Woo AA, Sinofsky A, Hernandez C, Majeska RJ, et al. Osteocyte apoptosis and control of bone resorption following ovariectomy in mice. Bone. 2010;46:577-83.
41. •• Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-Hora M, Feng JQ, et al. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nature Med. 2011;17:1231-4. First demonstration of the importance of osteocyte produced RANKL in bone turnover regulation.
42. •• Xiong J, Onal M, Jilka RL, Weinstein RS, Manolagas SC, O'Brien CA. Matrix-embedded cells control osteoclast formation. Nature Med. 2011;17:1235-41. First demonstration of the importance of osteocyte produced RANKL in bone turnover regulation and demonstration the bone loss with skeletal unloading requires osteocyte produced RANKL
43. Elliott MR, Ravichandran KS. Clearance of apoptotic cells: implications in health and disease. J Cell Biol. 2010;189:1059-70.
44. Harre U, Keppeler H, Ipseiz N, Derer A, Poller K, Aigner M, et al. Moonlighting osteoclasts as undertakers of apoptotic cells. Autoimmunity. 2012;45:612-9.
45. Bronckers AL, Goei W, van Heerde WL, Dumont EA, Reutelingsperger CP, van den Eijnde SM. Phagocytosis of dying chondrocytes by osteoclasts in the mouse growth plate as demonstrated by annexin-V labelling. Cell Tissue Res. 2000;301:267-72. (Pubitemid 30601560)
46. Kaczmarek A, Vandenabeele P, Krysko DV. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity. 2013;38:209-23.
47. Moriwaki K, Chan FK. RIP3: a molecular switch for necrosis and inflammation. Genes Dev. 2013;27:1640-9.
48. Chan FK. Fueling the flames: mammalian programmed necrosis in inflammatory diseases. Cold Spring Harb Perspect Biol. 2012;4.
49. Tang D, Kang R, Coyne CB, Zeh HJ, Lotze MT. PAMPs and DAMPs: signal 0 s that spur autophagy and immunity. Immunol Rev. 2012;249:158-75.
50. Einhorn TA, Majeska RJ, Rush EB, Levine PM, Horowitz MC. The expression of cytokine activity by fracture callus. J Bone Miner Res. 1995;10:1272-81.
51. Gerstenfeld LC, Cho TJ, Kon T, Aizawa T, Tsay A, Fitch J, et al. Impaired fracture healing in the absence of TNF-alpha signaling: the role of TNF-alpha in endochondral cartilage resorption. J Bone Miner Res. 2003;18:1584-92. (Pubitemid 37022916)
52. Wallace A, Cooney TE, Englund R, Lubahn JD. Effects of interleukin-6 ablation on fracture healing in mice. J Orthopaed Res. 2011;29:1437-42.
53. Schoengraf P, Lambris JD, Recknagel S, Kreja L, Liedert A, Brenner RE, et al. Does complement play a role in bone development and regeneration? Immunobiology. 2013;218:1-9.
54. Ignatius A, Schoengraf P, Kreja L, Liedert A, Recknagel S, Kandert S, et al. Complement C3a and C5a modulate osteoclast formation and inflammatory response of osteoblasts in synergism with IL-1beta. J Cell Biochem. 2011;112:2594-605.
55. Tu Z, Bu H, Dennis JE, Lin F. Efficient osteoclast differentiation requires local complement activation. Blood. 2010;116:4456-63.
56. Claes L, Recknagel S, Ignatius A. Fracture healing under healthy and inflammatory conditions. Nat Rev Rheumatol. 2012;8:133-43.
57. Taniguchi N, Yoshida K, Ito T, Tsuda M, Mishima Y, Furumatsu T, et al. Stage-specific secretion of HMGB1 in cartilage regulates endochondral ossification. Mol Cell Biol. 2007;27:5650-63. (Pubitemid 47257823)
58. Charoonpatrapong K, Shah R, Robling AG, Alvarez M, Clapp DW, Chen S, et al. HMGB1 expression and release by bone cells. J Cell Physiol. 2006;207:480-90.
59. Yang J, Shah R, Robling AG, Templeton E, Yang H, Tracey KJ, et al. HMGB1 is a bone-active cytokine. J Cell Physiol. 2008;214:730-9. (Pubitemid 351224218)
60. Zhou Z, Han JY, Xi CX, Xie JX, Feng X, Wang CY, et al. HMGB1 regulates RANKL-induced osteoclastogenesis in a manner dependent on RAGE. J Bone Miner Res. 2008;23:1084-96. (Pubitemid 351915731)
61. Hamada Y, Kitazawa S, Kitazawa R, Kono K, Goto S, Komaba H, et al. The effects of the receptor for advanced glycation end products (RAGE) on bone metabolism under physiological and diabetic conditions. Endocrine. 2010;38:369-76.
62. Ding KH, Wang ZZ, Hamrick MW, Deng ZB, Zhou L, Kang B, et al. Disordered osteoclast formation in RAGE-deficient mouse establishes an essential role for RAGE in diabetes related bone loss. Biochem Biophys Res Comm. 2006;340:1091-7. (Pubitemid 43083390)
63. Zhou Z, Immel D, Xi CX, Bierhaus A, Feng X, Mei L, et al. Regulation of osteoclast function and bone mass by RAGE. J Exp Med. 2006;203:1067-80.
64. Redlich K, Smolen JS. Inflammatory bone loss: pathogenesis and therapeutic intervention. Nat Rev Drug Discov. 2012;11:234-50.
65. Weitzmann MN, Pacifici R. Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest. 2006;116:1186-94.
66. Ollivere B, Wimhurst JA, Clark IM, Donell ST. Current concepts in osteolysis. J Bone Joint Surg Br. 2012;94:10-5.
67. Abu-Amer Y, Darwech I, Clohisy JC. Aseptic loosening of total joint replacements: mechanisms underlying osteolysis and potential therapies. Arthritis Res Ther. 2007;9 Suppl 1:S6.
68. Goodman SB, Gibon E, Yao Z. The basic science of periprosthetic osteolysis. Instr Course Lect. 2013;62:201-6.
69. Hallab NJ, Jacobs JJ. Biologic effects of implant debris. Bull NYU Hosp Jt Dis. 2009;67:182-8.
70. • Burton L, Paget D, Binder NB, Bohnert K, Nestor BJ, Sculco TP, et al. Orthopedic wear debris mediated inflammatory osteolysis is mediated in part by NALP3 inflammasome activation. J Orthopaed Res. 2013;31:73-80. Demonstration that particle induced osteolysis is mediated by inflammasome activation.
71. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature. 2006;440:237-41. (Pubitemid 43372104)
72. Valladares RD, Nich C, Zwingenberger S, Li C, Swank KR, Gibon E, et al. Toll-like receptors-2 and 4 are overexpressed in an experimental model of particle-induced osteolysis. J Biomed Mater Res. Part A. 2013.
73. Frick C, Dietz AC, Merritt K, Umbreit TH, Tomazic-Jezic VJ. Effects of prosthetic materials on the host immune response: evaluation of polymethyl-methacrylate (PMMA), polyethylene (PE), and polystyrene (PS) particles. J Long-Term Eff Med Implants. 2006;16:423-33. (Pubitemid 351234875)
74. Atkins GJ, Haynes DR, Howie DW, Findlay DM. Role of polyethylene particles in peri-prosthetic osteolysis: a review. World J Orthop. 2011;2:93-101.
75. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol. 2008;9:847-56.
76. Ortega-Gomez A, Perretti M, Soehnlein O. Resolution of inflammation: an integrated view. EMBO Mol Med. 2013;5:661-74.
77. Tang Y, Wu X, Lei W, Pang L, Wan C, Shi Z, et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med. 2009;15:757-65.
78. Wan M, Li C, Zhen G, Jiao K, He W, Jia X, et al. Injury-activated transforming growth factor beta controls mobilization of mesenchymal stem cells for tissue remodeling. Stem Cells. 2012;30:2498-511.
79. Molina PE. Neurobiology of the stress response: contribution of the sympathetic nervous system to the neuroimmune axis in traumatic injury. Shock. 2005;24:3-10. (Pubitemid 40946588)
80. Xing L, Schwarz EM, Boyce BF. Osteoclast precursors, RANKL/RANK, and immunology. Immunol Rev. 2005;208:19-29. (Pubitemid 41746382)
81. Sawant A, Deshane J, Jules J, Lee CM, Harris BA, Feng X, et al. Myeloid-derived suppressor cells function as novel osteoclast progenitors enhancing bone loss in breast cancer. Cancer Res. 2013;73:672-82.
82. Zhuang J, Zhang J, Lwin ST, Edwards JR, Edwards CM, Mundy GR, et al. Osteoclasts in multiple myeloma are derived from Gr-1+ CD11b+myeloid-derived suppressor cells. PloS One. 2012;7:e48871.
83. Grassi F, Manferdini C, Cattini L, Piacentini A, Gabusi E, Facchini A, et al. T cell suppression by osteoclasts in vitro. J Cell Physiol. 2011;226:982-90.
84. Funderburk SF, Marcellino BK, Yue Z. Cell "self-eating" (autophagy) mechanism in Alzheimer's disease. Mt Sinai J Med. 2010;77:59-68.
85. Bincoletto C, Bechara A, Pereira GJ, Santos CP, Antunes F. Peixoto da-Silva J, et al. Interplay between apoptosis and autophagy, a challenging puzzle: new perspectives on antitumor chemotherapies. Chem Biol Interact. 2013;206:279-88.
86. Onal M, Piemontese M, Xiong J, Wang Y, Han L, Ye S, et al. Suppression of autophagy in osteocytes mimics skeletal aging. J Biol Chem. 2013;288:17432-40.
87. Xia X, Kar R, Gluhak-Heinrich J, Yao W, Lane NE, Bonewald LF, et al. Glucocorticoid-induced autophagy in osteocytes. J Bone Miner Res. 2010;25:2479-88.
88. Jia J, Yao W, Guan M, Dai W, Shahnazari M, Kar R, et al. Glucocorticoid dose determines osteocyte cell fate. FASEB J. 2011;25:3366-76.
89. • DeSelm CJ, Miller BC, Zou W, Beatty WL, van Meel E, Takahata Y, et al. Autophagy proteins regulate the secretory component of osteoclastic bone resorption. Dev Cell. 2011;21:966-74. First demonstration of the role for autophagy proteins in osteoclast development.
90. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell. 2007;131:1149-63. (Pubitemid 350235021)
91. Laurin N, Brown JP, Morissette J, Raymond V. Recurrent mutation of the gene encoding sequestosome 1 (SQSTM1/p62) in Paget disease of bone. Am J Human Genet. 2002;70:1582-8. (Pubitemid 34533906)
92. Hocking LJ, Lucas GJ, Daroszewska A, Mangion J, Olavesen M, Cundy T, et al. Domain-specific mutations in sequestosome 1 (SQSTM1) cause familial and sporadic Paget's disease. Hum Mol Genet. 2002;11:2735-9. (Pubitemid 35214900)
93. Duran A, Serrano M, Leitges M, Flores JM, Picard S, Brown JP, et al. The atypical PKC-interacting protein p62 is an important mediator of RANK-activated osteoclastogenesis. Dev Cell. 2004;6:303-9. (Pubitemid 38190368)
94. Kurihara N, Hiruma Y, Zhou H, Subler MA, Dempster DW, Singer FR, et al. Mutation of the sequestosome 1 (p62) gene increases osteoclastogenesis but does not induce Paget disease. J Clin Invest. 2007;117:133-42. (Pubitemid 46048460)