Role of fas and treg cells in fracture healing as characterized in the fas-deficient (lpr) mouse model of lupus

Journal of Bone and Mineral Research

Volumn 29, Issue 6, 2014, Pages 1478-1491

  Al Sebaei, Maisa O ^a,b   Daukss, Dana M ^a   Belkina, Anna C ^a   Kakar, Sanjeev ^a   Wigner, Nathan A ^a   Cusher, Daniel ^a   Graves, Dana ^c   Einhorn, Thomas ^a   Morgan, Elise ^a,d   Gerstenfeld, Louis C ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d Boston University   (United States)

Author keywords

APOPTOSIS; CHONDROCYTES; FAS; OSTEOCLASTS; TREG CELLS

Indexed keywords

CALCITONIN RECEPTOR; CASPASE 3; FAS ANTIGEN; MESSENGER RNA; SCLEROPROTEIN; TUMOR NECROSIS FACTOR ALPHA; FAS PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; BONE CELL; BONE TISSUE; BONE TURNOVER; CALLUS; CARTILAGE CELL; CELL ACTIVITY; CELL FUNCTION; CHONDROLYSIS; CONTROLLED STUDY; ENCHONDRAL OSSIFICATION; FEMUR FRACTURE; FLUORESCENCE ACTIVATED CELL SORTING; FRACTURE HEALING; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; LIFESPAN; MALE; MECHANICAL TORSION; MORPHOMETRICS; MOUSE; NONHUMAN; OSSIFICATION; OSTEOCLAST ACTIVITY; OUTCOME ASSESSMENT; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTEIN DEPLETION; REGULATORY T LYMPHOCYTE; SPLEEN; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; UPREGULATION; ANIMAL; ANTIBODY SPECIFICITY; BIOMECHANICS; BONE; BONE DEVELOPMENT; BONE REMODELING; C57BL MOUSE; CARTILAGE; DEFICIENCY; DISEASE MODEL; FRACTURE; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; OSTEOCLAST; PATHOLOGY; PATHOPHYSIOLOGY; RADIOGRAPHY;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; BIOMECHANICAL PHENOMENA; BONE AND BONES; BONE REMODELING; BONY CALLUS; CARTILAGE; DISEASE MODELS, ANIMAL; FRACTURE HEALING; FRACTURES, BONE; INFLAMMATION; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE, INBRED C57BL; MICE, INBRED MRL LPR; ORGAN SPECIFICITY; OSTEOCLASTS; OSTEOGENESIS; RNA, MESSENGER; T-LYMPHOCYTES, REGULATORY; X-RAY MICROTOMOGRAPHY;

EID: 84901272669     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2169     Document Type: Article

References (57)

1. Kon T, Cho TJ, Aizawa T, et al. Expression of osteoprotegerin, receptor activator of NF-kappaB ligand (osteoprotegerin ligand) and related proinflammatory cytokines during fracture healing. J Bone Miner Res. 2001; 16 (6): 1004-14.
2. Gerstenfeld LC, Cho TJ, Kon T, 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 (9): 1584-92.
3. Lehmann W, Edgar CM, Wang K, et al. Tumor necrosis factor alpha (TNF-alpha) coordinately regulates the expression of specific matrix metalloproteinases (MMPS) and angiogenic factors during fracture healing. Bone. 2005; 36 (2): 300-10.
4. Gerstenfeld LC, Cho TJ, Kon T, et al. Impaired intramembranous bone formation during bone repair in the absence of tumor necrosis factor-alpha signaling. Cells Tissues Organs. 2001; 169 (3): 285-94.
5. Glass GE, Chan JK, Freidin A, Feldmann M, Horwood NJ, Nanchahal J., TNF-alpha promotes fracture repair by augmenting the recruitment and differentiation of muscle-derived stromal cells. Proc Natl Acad Sci USA. 2011; 108 (4): 1585-90.
6. Cho TJ, Lehmann W, Edgar C, et al. Tumor necrosis factor alpha activation of the apoptotic cascade in murine articular chondrocytes is associated with the induction of metalloproteinases and specific pro-resorptive factors. Arthritis Rheum. 2003; 48 (10): 2845.
7. Wallach D, Varfolomeev EE, Malinin NL, Goltsev YV, Kovalenko AV, Boldin MP., Tumor necrosis factor receptor and Fas signaling mechanisms. Annu Rev Immunol. 1999; 17: 331-3367.
8. Bazzoni F, Beutler B., The tumor necrosis factor ligand and receptor families. N Engl J Med. 1996; 334 (26): 1717-25.
9. Eugster HP, Muller M, LeHir M., Immunodeficiency of tumor necrosis factor and lymphotoxin-alpha double deficient mice. In:, Durum S, Muegge K, editors. Cytokine knockouts. Totowa (NJ): Humana Press; p. 103-27. 1998.
10. Nakamura T, Imai Y, Matsumoto T, et al. Estrogen prevents bone loss via estrogen receptor alpha and induction of Fas ligand in osteoclasts. Cell. 2007; 130 (5): 811-23.
11. Wu X, Pan G, McKenna MA, Zayzafoon M, Xiong WC, McDonald JM., RANKL regulates Fas expression and Fas-mediated apoptosis in osteoclasts. J Bone Miner Res. 2005; 20 (1): 107-16.
12. Gibson G., Active role of chondrocyte apoptosis in endochondral ossification. Microsc Res Tech. 1998; 43 (2): 191-204.
13. Roach HI, Erenpreisa J, Aigner T., Osteogenic differentiation of hypertrophic chondrocytes involves asymmetric cell divisions and apoptosis. J Cell Biol. 1995; 131 (2): 483-94.
14. Hashimoto S, Setareh M, Ochs RL, Lotz M., Fas/Fas ligand expression and induction of apoptosis in chondrocytes. Arthritis Rheum. 1997; 40 (10): 1749-55.
15. Aizawa T, Kokubun S, Tanaka Y., Apoptosis and proliferation of growth plate chondrocytes in rabbits. J Bone Joint Surg Br. 1997; 79 (3): 483-6.
16. Lee FY, Choi YW, Behrens FF, DeFouw DO, Einhorn TA., Programmed removal of chondrocytes during endochondral fracture healing. J Orthop Res. 1998; 16 (1): 144-50.
17. Aizawa T, Kon T, Einhorn TA, Gerstenfeld LC., Induction of apoptosis in chondrocytes by tumor necrosis factor-alpha. J Orthop Res. 2001; 19 (5): 785-96.
18. Chu JL, Drappa J, Parnassa A, Elkon KB., The defect in Fas mRNA expression in MRL/lpr mice is associated with insertion of the retrotransposon. ETn. J Exp Med. 1993; 178 (2): 723-30.
19. Watanabe-Fukunaga R, Brannan CI, Copeland NG, Jenkins NA, Nagata S., Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature. 1992; 356 (6367): 314-7.
20. Furukawa F, Kanauchi H, Wakita H, et al. Spontaneous autoimmune skin lesions of MRL/n mice: autoimmune disease-prone genetic background in relation to Fas-defect MRL/1pr mice. J Invest Dermatol. 1996; 107 (1): 95-100.
21. Alexander EL, Moyer C, Travlos GS, Roths JB, Murphy ED., Two histopathologic types of inflammatory vascular disease in MRL/Mp autoimmune mice. Model for human vasculitis in connective tissue disease. Arthritis Rheum. 1985; 28 (10): 1146-55.
22. Kelley VE, Roths JB., Interaction of mutant lpr gene with background strain influences renal disease. Clin Immunol Immunopathol. 1985; 37 (2): 220-9.
23. Jepsen KJ, Price C, Silkman LJ, et al. Genetic variation in the patterns of skeletal progenitor cell differentiation and progression during endochondral bone formation affects the rate of fracture healing. J Bone Miner Res. 2008; 23 (8): 1204-16.
24. Morgan EF, Mason ZD, Chien KB, et al. Micro-computed tomography assessment of fracture healing: relationships among callus structure, composition, and mechanical function. Bone. 2009; 44 (2): 335-44.
25. Gerstenfeld LC, Alkhiary YM, Krall EA, et al. Three-dimensional reconstruction of fracture callus morphogenesis. J Histochem Cytochem. 2006; 54 (11): 1215-28.
26. Parfitt AM, Drezner MK, Glorieux FH, et al. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res. 1987; 2 (6): 595-610.
27. Wang K, Vishwanath P, Eichler GS, et al. Analysis of fracture healing by large-scale transcriptional profile identified temporal relationships between metalloproteinase and ADAMTS mRNA expression. Matrix Biol. 2006; 25 (5): 271-81.
28. Cho TJ, Gerstenfeld LC, Einhorn TA., Differential temporal expression of members of the transforming growth factor beta superfamily during murine fracture healing. J Bone Miner Res. 2002; 17 (3): 513-20.
29. Basu R, Hatton RD, Weaver CT., The Th17 family: flexibility follows function. Immunol Rev. 2013; 252 (1): 89-103.
30. Miedlich SU, Zalutskaya A, Zhu ED, Demay MB., Phosphate-induced apoptosis of hypertrophic chondrocytes is associated with a decrease in mitochondrial membrane potential and is dependent upon Erk1/2 phosphorylation. J Biol Chem. 2010; 285 (24): 18270-5.
31. Kim J, Xu M, Xo R, et al. Mitochondrial DNA damage is involved in apoptosis caused by pro-inflammatory cytokines in human OA chondrocytes. Osteoarthritis Cartilage. 2010; 18 (3): 424-32.
32. Ouchi N, Uzuki M, Kamataki A, Miura Y, Sawai T., Cartilage destruction is partly induced by the internal proteolytic enzymes and apoptotic phenomenon of chondrocytes in relapsing polychondritis. J Rheumatol. 2011; 38 (4): 730-7.
33. Park D, Spencer JA, Koh BI, et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell. 2012; 10 (3): 259-72.
34. Iqbal J., Does TNF have anti-osteoclastogenic actions ? Ann NY Acad Sci. 2006; 1068: 234-9.
35. Kaplan DL, Eielson CM, Horowitz MC, Insogna KL, Weir EC., Tumor necrosis factor-alpha induces transcription of the colony-stimulating factor-1 gene in murine osteoblasts. J Cell Physiol. 1996; 168 (1): 199-208.
36. Cenci S, Weitzmann MN, Roggia C, et al. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest. 2000; 106 (10): 1229-37.
37. Zhang YH, Heulsmann A, Tondravi MM, Mukherjee A, Abu-Amer Y., Tumor necrosis factor-alpha (TNF) stimulates RANKL-induced osteoclastogenesis via coupling of TNF type 1 receptor and RANK signaling pathways. J Biol Chem. 2001; 276 (1): 563-8.
38. Yao Z, Li P, Zhang Q, et al. Tumor necrosis factor-alpha increases circulating osteoclast precursor numbers by promoting their proliferation and differentiation in the bone marrow through up-regulation of c-Fms expression. J Biol Chem. 2006; 281 (17): 11846-55.
39. Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, Teitelbaum SL., TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest. 2000; 106 (12): 1481-8.
40. Li P, Schwarz EM, O'Keefe RJ, et al. Systemic tumor necrosis factor alpha mediates an increase in peripheral CD11b high osteoclast precursors in tumor necrosis factor alpha-transgenic mice. Arthritis Rheum. 2004; 50 (1): 265-76.
41. Cullen CM, Bonventre PF, Heeg H, Bluethmann H, Mountz JD, Edwards CK 3rd., A fas antigen receptor mutation allows development of toxic shock syndrome toxin-1-induced lethal shock in V beta 8.2 T-cell receptor transgenic mice. Pathobiology. 1995; 63 (6): 293-304.
42. Anam K, Amare M, Naik S, Szabo KA, Davis TA., Severe tissue trauma triggers the autoimmune state systemic lupus erythematosus in the MRL/++ lupus-prone mouse. Lupus. 2009; 18 (4): 318-31.
43. Park H, Jung YK, Park OJ, Lee YJ, Choi JY, Choi Y., Interaction of Fas ligand and Fas expressed on osteoclast precursors increases osteoclastogenesis. J Immunol. 2005; 175 (11): 7193-201.
44. Roux S, Lambert-Comeau P, Saint-Pierre C, Lepine M, Sawan B, Parent JL., Death receptors, Fas and TRAIL receptors are involved in human osteoclast apoptosis. Biochem Biophys Res Commun. 2005; 333 (1): 42-50.
45. Imai Y, Youn MY, Kondoh S, et al. Estrogens maintain bone mass by regulating expression of genes controlling function and life span in mature osteoclasts. Ann NY Acad Sci. 2009; 1173 (Suppl 1): E31-9.
46. Krum SA, Miranda-Carboni GA, Hauschka PV, Carroll JS, Lane TF, Freedman LP, Brown M., Estrogen protects bone by inducing Fas ligand in osteoblasts to regulate osteoclast survival. EMBO J. 2008; 6; 27 (3): 535-45.
47. Hoang Tu-Rapp H, Hammermüller A, Mix E, et al. Aproinflammatory role for Fas in joints of mice with collagen-induced arthritis. Arthritis Res Ther. 2004; 6 (5): R404-14.
48. Nam D, Mau E, Wang Y, et al. T-lymphocytes enable osteoblast maturation via IL-17F during the early phase of fracture repair. PLoS One. 2012; 7 (6): e40044.
49. Adamik J, Henkel M, Ray A, Auron PE, Duerr R, Barrie A., The IL17A and IL17F loci have divergent histone modifications and are differentially regulated by prostaglandin E2 in Th17 cells. Cytokine. 2013; 64 (1): 404-12.
50. Gerstenfeld LC, Thiede M, Seibert K, et al. Differential inhibition of fracture healing by non-selective and cyclooxygenase-2 selective non-steroidal anti-inflammatory drugs. J Orthop Res. 2003; 21 (4): 670-5.
51. Gerstenfeld LC, Al-Ghawas M, Alkhiary YM, et al. Selective and nonselective cyclooxygenase-2 inhibitors and experimental fracture-healing. Reversibility of effects after short-term treatment J Bone Joint Surg Am. 2007; 89 (1): 114-25.
52. Lane NE., Therapy insight: osteoporosis and osteonecrosis in systemic lupus erythematosus. Nat Clin Pract Rheumatol. 2006; 2 (10): 562-9.
53. Houssiau FA, Lefebvre C, Depresseux G, et al. Trabecular and cortical bone loss in systemic lupus erythematosus. Br J Rheumatol. 1996; 35 (3): 244-7.
54. Bultink IE, Lems WF, Kostense PJ, Dijkmans BA, Voskuyl AE., Prevalence of and risk factors for low bone mineral density and vertebral fractures in patients with systemic lupus erythematosus. Arthritis Rheum. 2005; 52 (7): 2044-50.
55. Lee C, Almagor O, Dunlop DD, et al. Disease damage and low bone mineral density: an analysis of women with systemic lupus erythematosus ever and never receiving corticosteroids. Rheumatology (Oxford). 2006; 45 (1): 53-60.
56. Lee Y., The role of interleukin-17 in bone metabolism and inflammatory skeletal diseases. BMB Rep. 2013; 46 (10): 479-83.
57. Wu X, McKenna MA, Feng X, Nagy TR, McDonald JM., Osteoclast apoptosis: the role of Fas in vivo and in vitro. Endocrinology. 2003; 144 (12): 5545-55.