T cells: Critical bone regulators in health and disease

Bone

Volumn 47, Issue 3, 2010, Pages 461-471

  Pacifici, Roberto ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

Estrogen; Osteoporosis; Postmenopausal; PTH; T cells

Indexed keywords

ABATACEPT; B7 ANTIGEN; CD40 LIGAND; ESTROGEN; GAMMA INTERFERON; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE; PARATHYROID HORMONE RECEPTOR 1; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR; WNT PROTEIN;

ANTIGEN PRESENTATION; APOPTOSIS; BONE MARROW CELL; BONE METABOLISM; CALCIUM METABOLISM; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; ESTROGEN DEFICIENCY; HUMAN; HYPERPARATHYROIDISM; LIGAND BINDING; LYMPHOCYTE HOMING; MENOPAUSE; MOLECULAR INTERACTION; NONHUMAN; OSSIFICATION; OSTEOCLAST; OSTEOLYSIS; OVARY FUNCTION; OXIDATIVE STRESS; POSTMENOPAUSE OSTEOPOROSIS; REVIEW; SIGNAL TRANSDUCTION; STROMA CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH17 CELL; TH2 CELL;

ANIMALS; BONE AND BONES; BONE DISEASES, METABOLIC; ESTROGENS; HOMEOSTASIS; HUMANS; MENOPAUSE; PARATHYROID HORMONE; SIGNAL TRANSDUCTION; STROMAL CELLS; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77955842458     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2010.04.611     Document Type: Review

References (139)

1. Kong Y.Y., Feige U., Sarosi I., Bolon B., Tafuri A., Morony S., et al. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 1999, 402(6759):304-309.
2. Mak T.W., Ferrick D.A. The gammadelta T-cell bridge: linking innate and acquired immunity. Nat Med 1998, 4(7):764-765.
3. Haas W., Pereira P., Tonegawa S. Gamma/delta cells. Annu Rev Immunol 1993, 11:637-685.
4. Godfrey D.I., MacDonald H.R., Kronenberg M., Smyth M.J., Van Kaer L. NKT cells: what's in a name?. Nat Rev Immunol 2004, 4(3):231-237.
5. Volpe E., Servant N., Zollinger R., Bogiatzi S.I., Hupe P., Barillot E., et al. A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses. Nat Immunol 2008, 9(6):650-657.
6. Sato K., Suematsu A., Okamoto K., Yamaguchi A., Morishita Y., Kadono Y., et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 2006, 203(12):2673-2682.
7. Kotake S., Nanke Y., Mogi M., Kawamoto M., Furuya T., Yago T., et al. IFN-gamma-producing human T cells directly induce osteoclastogenesis from human monocytes via the expression of RANKL. Eur J Immunol 2005, 35(11):3353-3363.
8. Di Rosa F., Pabst R. The bone marrow: a nest for migratory memory T cells. Trends Immunol 2005, 26(7):360-366.
9. Di Rosa F., Santoni A. Memory T-cell competition for bone marrow seeding. Immunology 2003, 108(3):296-304.
10. Wilson A., Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 2006, 6(2):93-106.
11. Tokoyoda K., Zehentmeier S., Chang H.D., Radbruch A. Organization and maintenance of immunological memory by stroma niches. Eur J Immunol 2009, 39(8):2095-2099.
12. Uccelli A., Moretta L., Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008, 8(9):726-736.
13. Ren G., Zhang L., Zhao X., Xu G., Zhang Y., Roberts A.I., et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008, 2(2):141-150.
14. Le Blanc K., Frassoni F., Ball L., Locatelli F., Roelofs H., Lewis I., et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008, 371(9624):1579-1586.
15. Huang W., La Russa V., Alzoubi A., Schwarzenberger P. Interleukin-17A: a T-cell-derived growth factor for murine and human mesenchymal stem cells. Stem Cells 2006, 24(6):1512-1518.
16. Yamaza T., Miura Y., Bi Y., Liu Y., Akiyama K., Sonoyama W., et al. Pharmacologic stem cell based intervention as a new approach to osteoporosis treatment in rodents. PLoS ONE 2008, 3(7):e2615.
17. Grewal I.S., Flavell R.A. CD40 and CD154 in cell-mediated immunity. Annu Rev Immunol 1998, 16:111-135.
18. Quezada S.A., Jarvinen L.Z., Lind E.F., Noelle R.J. CD40/CD154 interactions at the interface of tolerance and immunity. Annu Rev Immunol 2004, 22:307-328.
19. Andre P., Prasad K.S., Denis C.V., He M., Papalia J.M., Hynes R.O., et al. CD40L stabilizes arterial thrombi by a beta3 integrin-dependent mechanism. Nat Med 2002, 8(3):247-252.
20. Leveille C., Bouillon M., Guo W., Bolduc J., Sharif-Askari E., El-Fakhry Y., et al. CD40 ligand binds to alpha5beta1 integrin and triggers cell signaling. J Biol Chem 2007, 282(8):5143-5151.
21. Ahuja S.S., Zhao S., Bellido T., Plotkin L.I., Jimenez F., Bonewald L.F. CD40 ligand blocks apoptosis induced by tumor necrosis factor alpha, glucocorticoids, and etoposide in osteoblasts and the osteocyte-like cell line murine long bone osteocyte-Y4. Endocrinology 2003, 144(5):1761-1769.
22. Li Y., Toraldo G., Li A., Yang X., Zhang H., Qian W.P., et al. B cells and T cells are critical for the preservation of bone homeostasis and attainment of peak bone mass in vivo. Blood 2007, 109(9):3839-3848.
23. Lopez-Granados E., Temmerman S.T., Wu L., Reynolds J.C., Follmann D., Liu S., et al. Osteopenia in X-linked hyper-IgM syndrome reveals a regulatory role for CD40 ligand in osteoclastogenesis. Proc Natl Acad Sci U S A 2007, 104(12):5056-5061.
24. Gao Y., Wu X., Terauchi M., Li J.Y., Grassi F., Galley S., et al. T cells potentiate PTH-induced cortical bone loss through CD40L signaling. Cell Metab 2008, 8(2):132-145.
25. Teng Y.T., Nguyen H., Gao X., Kong Y.Y., Gorczynski R.M., Singh B., et al. Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. J Clin Invest 2000, 106(6):R59-R67.
26. Weitzmann M.N., Pacifici R. Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 2006, 116(5):1186-1194.
27. John V., Hock J.M., Short L.L., Glasebrook A.L., Galvin R.J. A role for CD8+ T lymphocytes in osteoclast differentiation in vitro. Endocrinology 1996, 137(6):2457-2463.
28. Grcevic D., Lee S.K., Marusic A., Lorenzo J.A. Depletion of CD4 and CD8 T lymphocytes in mice In vivo enhances 1, 25-dihydroxyvitamin D(3)-stimulated osteoclast-like cell formation In vitro by a mechanism that is dependent on prostaglandin synthesis. J Immunol 2000, 165(8):4231-4238.
29. Toraldo G., Roggia C., Qian W.-P., Pacifici R., Weitzmann M.N. IL-7 induces bone loss in vivo by induction of receptor activator of nuclear factor kappa B ligand and tumor necrosis factor alpha from T cells 2003, vol. 100:125-130.
30. Riggs B.L., Melton L.J. Medical progress: involutional osteoporosis. N. Eng. J. Med. 1986, 314:1676-1684.
31. Potts J. Primary hyperparathyroidism. Metabolic Bone Diseases 1998, vol. 1:411-442. Academic Press, San Diego. #rd ed. L.V. Avioli, S. Krane (Eds.).
32. Canalis E., Giustina A., Bilezikian J.P. Mechanisms of anabolic therapies for osteoporosis. N Engl J Med 2007, 357(9):905-916.
33. Qin L., Raggatt L.J., Partridge N.C. Parathyroid hormone: a double-edged sword for bone metabolism. Trends Endocrinol Metab 2004, 15(2):60-65.
34. Lanske B., Amling M., Neff L., Guiducci J., Baron R., Kronenberg H.M. Ablation of the PTHrP gene or the PTH/PTHrP receptor gene leads to distinct abnormalities in bone development. J Clin Invest 1999, 104(4):399-407.
35. Calvi L.M., Sims N.A., Hunzelman J.L., Knight M.C., Giovannetti A., Saxton J.M., et al. Activated parathyroid hormone/parathyroid hormone-related protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. J Clin Invest 2001, 107(3):277-286.
36. O'Brien C.A., Plotkin L.I., Galli C., Goellner J.J., Gortazar A.R., Allen M.R., et al. Control of bone mass and remodeling by PTH receptor signaling in osteocytes. PLoS ONE 2008, 3(8):e2942.
37. Lindsay R., Cosman F., Zhou H., Bostrom M.P., Shen V.W., Cruz J.D., et al. A novel tetracycline labeling schedule for longitudinal evaluation of the short-term effects of anabolic therapy with a single iliac crest bone biopsy: early actions of teriparatide. J Bone Miner Res 2006, 21(3):366-373.
38. Ma Y.L., Zeng Q., Donley D.W., Ste-Marie L.G., Gallagher J.C., Dalsky G.P., et al. Teriparatide increases bone formation in modeling and remodeling osteons and enhances IGF-II immunoreactivity in postmenopausal women with osteoporosis. J Bone Miner Res 2006, 21(6):855-864.
39. Dobnig H., Turner R.T. Evidence that intermittent treatment with parathyroid hormone increases bone formation in adult rats by activation of bone lining cells. Endocrinology 1995, 136(8):3632-3638.
40. Pettway G.J., Meganck J.A., Koh A.J., Keller E.T., Goldstein S.A., McCauley L.K. Parathyroid hormone mediates bone growth through the regulation of osteoblast proliferation and differentiation. Bone 2008, 42:806-818.
41. Meng X.W., Liang X.G., Birchman R., Wu D.D., Dempster D.W., Lindsay R., et al. Temporal expression of the anabolic action of PTH in cancellous bone of ovariectomized rats. J Bone Miner Res 1996, 11(4):421-429.
42. Jilka R.L., Weinstein R.S., Bellido T., Roberson P., Parfitt A.M., Manolagas S.C. Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest 1999, 104(4):439-446.
43. Bellido T., Ali A.A., Plotkin L.I., Fu Q., Gubrij I., Roberson P.K., 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(50):50259-50272.
44. Kato M., Patel M.S., Levasseur R., Lobov I., Chang B.H., Glass D.A., et al. Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol 2002, 157(2):303-314.
45. Jilka R.L. Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 2007, 40(6):1434-1446.
46. Almeida M., Han L., Bellido T., Manolagas S.C., Kousteni S. Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent and -independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J Biol Chem 2005, 280(50):41342-41351.
47. Glass D.A., Bialek P., Ahn J.D., Starbuck M., Patel M.S., Clevers H., et al. Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 2005, 8(5):751-764.
48. Choi H.Y., Dieckmann M., Herz J., Niemeier A. Lrp4, a novel receptor for Dickkopf 1 and sclerostin, is expressed by osteoblasts and regulates bone growth and turnover in vivo. PLoS ONE 2009, 4(11):e7930.
49. Behrens J., von Kries J.P., Kuhl M., Bruhn L., Wedlich D., Grosschedl R., et al. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 1996, 382(6592):638-642.
50. Kulkarni N.H., Halladay D.L., Miles R.R., Gilbert L.M., Frolik C.A., Galvin R.J., et al. Effects of parathyroid hormone on Wnt signaling pathway in bone. J Cell Biochem 2005, 95(6):1178-1190.
51. Wan M., Yang C., Li J., Wu X., Yuan H., Ma H., et al. Parathyroid hormone signaling through low-density lipoprotein-related protein 6. Genes Dev 2008, 22(21):2968-2979.
52. Bellido T., Ali A.A., Gubrij I., Plotkin L.I., Fu Q., O'Brien C.A., et al. Chronic elevation of parathyroid hormone in mice reduces expression of sclerostin by osteocytes: a novel mechanism for hormonal control of osteoblastogenesis. Endocrinology 2005, 146(11):4577-4583.
53. Keller H., Kneissel M. SOST is a target gene for PTH in bone. Bone 2005, 37(2):148-158.
54. Qin L., Qiu P., Wang L., Li X., Swarthout J.T., Soteropoulos P., et al. Gene expression profiles and transcription factors involved in parathyroid hormone signaling in osteoblasts revealed by microarray and bioinformatics. J Biol Chem 2003, 278(22):19723-19731.
55. Terauchi M., Li J.Y., Bedi B., Baek K.H., Tawfeek H., Galley S., et al. T lymphocytes amplify the anabolic activity of parathyroid hormone through Wnt10b signaling. Cell Metab 2009, 10(3):229-240.
56. Stojceva-Taneva O., Fadda G.Z., Smogorzewski M., Massry S.G. Parathyroid hormone increases cytosolic calcium of thymocytes. Nephron 1993, 64(4):592-599.
57. Rifas L. T-cell cytokine induction of BMP-2 regulates human mesenchymal stromal cell differentiation and mineralization. J Cell Biochem 2006, 98(4):706-714.
58. Guise T.A., Chirgwin J.M., Favarato G., Boyce B.F., Mundy G.R. Chinese hamster ovarian cells transfected with human parathyroid hormone-related protein cDNA cause hypercalcemia in nude mice. Lab Invest 1992, 67(4):477-485.
59. Hory B.G., Roussanne M.C., Rostand S., Bourdeau A., Drueke T.B., Gogusev J. Absence of response to human parathyroid hormone in athymic mice grafted with human parathyroid adenoma, hyperplasia or parathyroid cells maintained in culture. J Endocrinol Invest 2000, 23(5):273-279.
60. O'Brien C., Fu Q., Mommsen L., Dusevich V., Bonewald L., Manolagas S.C., et al. Osteoblasts are not the source of RANKL and OPG in bone but are required for maintenance of osteoclast function. J Bone Miner Res 2006, 22(Supplement 1). abstract.
61. Tanaka Y., Maruo A., Fujii K., Nomi M., Nakamura T., Eto S., et al. Intercellular adhesion molecule 1 discriminates functionally different populations of human osteoblasts: characteristic involvement of cell cycle regulators. J Bone Miner Res 2000, 15(10):1912-1923.
62. Everts V., Delaisse J.M., Korper W., Jansen D.C., Tigchelaar-Gutter W., Saftig P., et al. The bone lining cell: its role in cleaning Howship's lacunae and initiating bone formation. J Bone Miner Res 2002, 17(1):77-90.
63. Young N., Mikhalkevich N., Yan Y., Chen D., Zheng W.P. Differential regulation of osteoblast activity by Th cell subsets mediated by parathyroid hormone and IFN-gamma. J Immunol 2005, 175(12):8287-8295.
64. Cheng X., Li J., Lu Y., Keyak J., Lang T. Proximal femoral density and geometry measurements by quantitative computed tomography: Association with hip fracture. Bone 2007, 40:169-174.
65. Grassi F., Tell G., Robbie-Ryan M., Gao Y., Terauchi M., Yang X., et al. Oxidative stress causes bone loss in estrogen-deficient mice through enhanced bone marrow dendritic cell activation. Proc Natl Acad Sci U S A 2007, 104(38):15087-15092.
66. Pettway G.J., Schneider A., Koh A.J., Widjaja E., Morris M.D., Meganck J.A., et al. Anabolic actions of PTH (1-34): use of a novel tissue engineering model to investigate temporal effects on bone. Bone 2005, 36(6):959-970.
67. Di Rosa F. T-lymphocyte interaction with stromal, bone and hematopoietic cells in the bone marrow. Immunol Cell Biol 2008, 87:20-29.
68. Rawadi G., Vayssiere B., Dunn F., Baron R., Roman-Roman S. BMP-2 controls alkaline phosphatase expression and osteoblast mineralization by a Wnt autocrine loop. J Bone Miner Res 2003, 18(10):1842-1853.
69. Luo Q., Kang Q., Si W., Jiang W., Park J.K., Peng Y., et al. Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J Biol Chem 2004, 279(53):55958-55968.
70. Spencer G.J., Utting J.C., Etheridge S.L., Arnett T.R., Genever P.G. Wnt signalling in osteoblasts regulates expression of the receptor activator of NFkappaB ligand and inhibits osteoclastogenesis in vitro. J Cell Sci 2006, 119(Pt 7):1283-1296.
71. Moon R.T., Bowerman B., Boutros M., Perrimon N. The promise and perils of Wnt signaling through beta-catenin. Science 2002, 296(5573):1644-1646.
72. Kimble R.B., Srivastava S., Ross F.P., Matayoshi A., Pacifici R. Estrogen deficiency increases the ability of stromal cells to support murine osteoclastogenesis via an interleukin-1and tumor necrosis factor-mediated stimulation of macrophage colony-stimulating factor production. J Biol Chem 1996, 271(46):28890-28897.
73. Zaidi M. Skeletal remodeling in health and disease. Nat Med 2007, 13(7):791-801.
74. Nakamura T., Imai Y., Matsumoto T., Sato S., Takeuchi K., Igarashi K., et al. Estrogen prevents bone loss via estrogen receptor alpha and induction of Fas ligand in osteoclasts. Cell 2007, 130(5):811-823.
75. Krum S.A., Miranda-Carboni G.A., Hauschka P.V., Carroll J.S., Lane T.F., Freedman L.P., et al. Estrogen protects bone by inducing Fas ligand in osteoblasts to regulate osteoclast survival. EMBO J 2008, 27(3):535-545.
76. Jilka R.L., Takahashi K., Munshi M., Williams D.C., Roberson P.K., Manolagas S.C. Loss of estrogen upregulates osteoblastogenesis in the murine bone marrow. Evidence for autonomy from factors released during bone resorption. J Clin Invest 1998, 101(9):1942-1950.
77. Di Gregorio G.B., Yamamoto M., Ali A.A., Abe E., Roberson P., Manolagas S.C., et al. Attenuation of the self-renewal of transit-amplifying osteoblast progenitors in the murine bone marrow by 17beta-estradiol. J Clin Invest 2001, 107(7):803-812.
78. Kousteni S., Bellido T., Plotkin L.I., O'Brien C.A., Bodenner D.L., Han L., et al. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 2001, 104(5):719-730.
79. Kousteni S., Han L., Chen J.R., Almeida M., Plotkin L.I., Bellido T., et al. Kinase-mediated regulation of common transcription factors accounts for the bone-protective effects of sex steroids. J Clin Invest 2003, 111(11):1651-1664.
80. Parfitt A.M. Bone remodeling: relationship to the amount and structure of bone, and the pathogenesis and prevention of fractures. Osteoporosis 1988, 45-93. Raven Press, New York. 1 ed. B.L. Riggs (Ed.).
81. Manolagas S.C. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr Rev 2010, 31:1-35.
82. Roggia C., Gao Y., Cenci S., Weitzmann M.N., Toraldo G., Isaia G., et al. Up-regulation of TNF-producing T cells in the bone marrow: A key mechanism by which estrogen deficiency induces bone loss in vivo. Proc Natl Acad Sci U S A 2001, 98(24):13960-13965.
83. Ammann P., Rizzoli R., Bonjour J.P., Bourrin S., Meyer J.M., Vassalli P., et al. Transgenic mice expressing soluble tumor necrosis factor-receptor are protected against bone loss caused by estrogen deficiency. J Clin Invest 1997, 99:1699-1703.
84. Kimble R., Bain S., Pacifici R. The functional block of TNF but not of IL-6 prevents bone loss in ovariectomized mice. J Bone Miner Res 1997, 12:935-941.
85. Pacifici R., Brown C., Puscheck E., Friedrich E., Slatopolsky E., Maggio D., et al. Effect of surgical menopause and estrogen replacement on cytokine release from human blood mononuclear cells. Proc Natl Acad Sci 1991, 88:5134-5138.
86. Ralston S.H., Russell R.G.G., Gowen M. Estrogen inhibits release of tumor necrosis factor from peripheral blood mononuclear cells in postmenopausal women. J Bone Miner Res 1990, 5:983-988.
87. Shanker G., Sorci-Thomas M., Adams M.R. Estrogen modulates the expression of tumor necrosis factor alpha mRNA in phorbol ester-stimulated human monocytic THP-1 cells. Lymphokine Cytokine Res 1994, 13:377-382.
88. Cenci S., Weitzmann M.N., Roggia C., Namba N., Novack D., Woodring J., et al. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J Clin Invest 2000, 106(10):1229-1237.
89. Gao Y., Qian W.-P., Dark K., Toraldo G., Lin A.S.P., Guldberg R.E., et al. Estrogen prevents bone loss through transforming growth factor {beta} signaling in T cells 2004, vol. 101:16618-16623.
90. Gao Y., Grassi F., Ryan M.R., Terauchi M., Page K., Yang X., et al. IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation. J Clin Invest 2007, 117(1):122-132.
91. Robbie-Ryan M., Grassi F., Gao Y., Page K., Yang X., Weitzmann M.N., et al. Silencing of T cell function in wild-type mice by immunodepletion or treatment with abatacept prevents the loss of cortical and trabecular bone and the increase in bone resorption induced by ovariectomy. J Bone Miner Res 2006, 21(Supplement 1). Abs. 1095.
92. Moreland L., Bate G., Kirkpatrick P. Abatacept. Nat Rev Drug Discov 2006, 5(3):185-186.
93. Ruderman E.M., Pope R.M. The evolving clinical profile of abatacept (CTLA4-Ig): a novel co-stimulatory modulator for the treatment of rheumatoid arthritis. Arthritis Res Ther 2005, 7(Suppl 2):S21-S25.
94. D'Amelio P., Grimaldi A., Di Bella S., Brianza S.Z., Cristofaro M.A., Tamone C., et al. Estrogen deficiency increases osteoclastogenesis up-regulating T cells activity: a key mechanism in osteoporosis. Bone 2008, 43(1):92-100.
95. Lee S.K., Kadono Y., Okada F., Jacquin C., Koczon-Jaremko B., Gronowicz G., et al. T lymphocyte-deficient mice lose trabecular bone mass with ovariectomy. J Bone Miner Res 2006, 21(11):1704-1712.
96. Cenci S., Toraldo G., Weitzmann M.N., Roggia C., Gao Y., Qian W.P., et al. Estrogen deficiency induces bone loss by increasing T cell proliferation and lifespan through IFN-gamma-induced class II transactivator. Proc Natl Acad Sci U S A 2003, 100(18):10405-10410.
97. Grassi F., Pacifici R. Ovariectomy increases the formation of T cell niches at the resorption surfaces. J Bone Miner Res 2005, 20(Suppl. 1). Abs.
98. Adamski J., Ma Z., Nozell S., Benveniste E.N. 17beta-Estradiol inhibits class II major histocompatibility complex (MHC) expression: influence on histone modifications and cbp recruitment to the class II MHC promoter. Mol Endocrinol 2004, 18(8):1963-1974.
99. Robey E.A., Ramsdell F., Gordon J.W., Mamalaki C., Kioussis D., Youn H.J., et al. A self-reactive T cell population that is not subject to negative selection. Int Immunol 1992, 4(9):969-974.
100. Grossman Z., Paul W.E. Self-tolerance: context dependent tuning of T cell antigen recognition. Semin Immunol 2000, 12(3):197-203. discussion 257-344.
101. Tanchot C., Lemonnier F.A., Perarnau B., Freitas A.A., Rocha B. Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science 1997, 276(5321):2057-2062.
102. Boss J.M., Jensen P.E. Transcriptional regulation of the MHC class II antigen presentation pathway. Curr Opin Immunol 2003, 15(1):105-111.
103. Takayanagi H., Ogasawara K., Hida S., Chiba T., Murata S., Sato K., et al. T-cell-mediated regulation of osteoclastogenesis by signalling cross- talk between RANKL and IFN-gamma. Nature 2000, 408(6812):600-605.
104. Vermeire K., Heremans H., Vandeputte M., Huang S., Billiau A., Matthys P. Accelerated collagen-induced arthritis in IFN-gamma receptor-deficient mice. J Immunol 1997, 158(11):5507-5513.
105. Sato K., Satoh T., Shizume K., Yamakawa Y., Ono Y., Demura H., et al. Prolonged decrease of serum calcium concentration by murine gamma-interferon in hypercalcemic, human tumor (EC-GI)-bearing nude mice. Cancer Res 1992, 52(2):444-449.
106. Baker P.J., Dixon M., Evans R.T., Dufour L., Johnson E., Roopenian D.C. CD4(+) T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 1999, 67(6):2804-2809.
107. Arnoldi J., Gerdes J., Flad H.D. Immunohistologic assessment of cytokine production of infiltrating cells in various forms of leprosy. Am J Pathol 1990, 137(4):749-753.
108. Cannon G.W., Pincus S.H., Emkey R.D., Denes A., Cohen S.A., Wolfe F., et al. Double-blind trial of recombinant gamma-interferon versus placebo in the treatment of rheumatoid arthritis. Arthritis Rheum 1989, 32(8):964-973.
109. Mann G.N., Jacobs T.W., Buchinsky F.J., Armstrong E.C., Li M., Ke H.Z., et al. Interferon-gamma causes loss of bone volume in vivo and fails to ameliorate cyclosporin A-induced osteopenia. Endocrinology 1994, 135:1077-1083.
110. Key L.L., Rodriguiz R.M., Willi S.M., Wright N.M., Hatcher H.C., Eyre D.R., et al. Long-term treatment of osteopetrosis with recombinant human interferon gamma. N Engl J Med 1995, 332(24):1594-1599.
111. Rodriguiz R.M., Key L.L., Ries W.L. Combination macrophage-colony stimulating factor and interferon-gamma administration ameliorates the osteopetrotic condition in microphthalmic (mi/mi) mice. Pediatr Res 1993, 33(4 Pt 1):384-389.
112. Takayanagi H., Kim S., Taniguchi T. Signaling crosstalk between RANKL and interferons in osteoclast differentiation. Arthritis Res 2002, 4(Suppl 3):S227-S232.
113. Yang N.N., Venugopalan M., Hardikar S., Glasebrook A. Identification of an estrogen response element activated by metabolites of 17'-estradiol and raloxifene. Science 1996, 273:1222-1225.
114. Miyaura C., Onoe Y., Inada M., Maki K., Ikuta K., Ito M., et al. Increased B-lymphopoiesis by interleukin 7 induces bone loss in mice with intact ovarian function: similarity to estrogen deficiency. Proc Natl Acad Sci USA 1997, 19:9360-9365.
115. Weitzmann M.N., Roggia C., Toraldo G., Weitzmann L., Pacifici R. Increased production of IL-7 uncouples bone formation from bone resorption during estrogen deficiency. J Clin Invest 2002, 110(11):1643-1650.
116. Ryan M.R., Shepherd R., Leavey J.K., Gao Y., Grassi F., Schnell F.J., et al. An IL-7-dependent rebound in thymic T cell output contributes to the bone loss induced by estrogen deficiency. Proc Natl Acad Sci U S A 2005, 102(46):16735-16740.
117. Lindberg M.K., Svensson J., Venken K., Chavoshi T., Andersson N., Moverare Skrtic S., et al. Liver-derived IGF-I is permissive for ovariectomy-induced trabecular bone loss. Bone 2006, 38(1):85-92.
118. Lee SK, Kalinowski JF, Jacquin C, Adams DJ, Gronowicz G, Lorenzo JA. Interleukin-7 influences osteoclast function in vivo but is not a critical factor in ovariectomy-induced bone loss. J Bone Miner Res 2006;21:695-702.
119. Huang M., Sharma S., Zhu L.X., Keane M.P., Luo J., Zhang L., et al. IL-7 inhibits fibroblast TGF-beta production and signaling in pulmonary fibrosis. J Clin Invest 2002, 109(7):931-937.
120. Dubinett S.M., Huang M., Dhanani S., Economou J.S., Wang J., Lee P., et al. Down-regulation of murine fibrosarcoma transforming growth factor-beta 1 expression by interleukin 7. J Natl Cancer Inst 1995, 87(8):593-597.
121. Basu S., Michaelsson K., Olofsson H., Johansson S., Melhus H. Association between oxidative stress and bone mineral density. Biochem Biophys Res Commun 2001, 288(1):275-279.
122. Maggio D., Barabani M., Pierandrei M., Polidori M.C., Catani M., Mecocci P., et al. Marked decrease in plasma antioxidants in aged osteoporotic women: results of a cross-sectional study. J Clin Endocrinol Metab 2003, 88(4):1523-1527.
123. Lean J.M., Davies J.T., Fuller K., Jagger C.J., Kirstein B., Partington G.A., et al. A crucial role for thiol antioxidants in estrogen-deficiency bone loss. J Clin Invest 2003, 112(6):915-923.
124. Muthusami S., Ramachandran I., Muthusamy B., Vasudevan G., Prabhu V., Subramaniam V., et al. Ovariectomy induces oxidative stress and impairs bone antioxidant system in adult rats. Clin Chim Acta 2005, 360(1-2):81-86.
125. Almeida M., Han L., Martin-Millan M., Plotkin L.I., Stewart S.A., Roberson P.K., et al. Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 2007, 282(37):27285-27297.
126. Jagger C.J., Lean J.M., Davies J.T., Chambers T.J. Tumor necrosis factor-alpha mediates osteopenia caused by depletion of antioxidants. Endocrinology 2005, 146(1):113-118.
127. Almeida M., Ambrogini E., Han L., Manolagas S.C., Jilka R.L. Increased lipid oxidation causes oxidative stress, increased peroxisome proliferator-activated receptor-gamma expression, and diminished pro-osteogenic Wnt signaling in the skeleton. J Biol Chem 2009, 284(40):27438-27448.
128. Almeida M., Martin-Millan M., Ambrogini E., Bradsher R., Han L., Chen X.D., et al. Estrogens attenuate oxidative stress and the differentiation and apoptosis of osteoblasts by DNA binding-independent actions of the ERalpha. J Bone Miner Res 2009.
129. Martin-Millan M., Almeida M., Ambrogini E., Han L., Zhao H., Weinstein R.S., et al. The estrogen receptor-alpha in osteoclasts mediates the protective effects of estrogens on cancellous but not cortical bone. Mol Endocrinol 2010, 24(2):323-334.
130. Ambrogini E., Almeida M., Martin-Millan M., Paik J.H., Depinho R.A., Han L. et al., FoxO-mediated defense against oxidative stress in osteoblasts is indispensable for skeletal homeostasis in mice. Cell Metab 11(2):136-46.
131. Mizuashi M., Ohtani T., Nakagawa S., Aiba S. Redox imbalance induced by contact sensitizers triggers the maturation of dendritic cells. J Invest Dermatol 2005, 124(3):579-586.
132. Rutault K., Alderman C., Chain B.M., Katz D.R. Reactive oxygen species activate human peripheral blood dendritic cells. Free Radic Biol Med 1999, 26(1-2):232-238.
133. Maemura K., Zheng Q., Wada T., Ozaki M., Takao S., Aikou T., et al. Reactive oxygen species are essential mediators in antigen presentation by Kupffer cells. Immunol Cell Biol 2005, 83(4):336-343.
134. Vosters O., Neve J., De Wit D., Willems F., Goldman M., Verhasselt V. Dendritic cells exposed to nacystelyn are refractory to maturation and promote the emergence of alloreactive regulatory t cells. Transplantation 2003, 75(3):383-389.
135. Verhasselt V., Vanden Berghe W., Vanderheyde N., Willems F., Haegeman G., Goldman M. N-acetyl-L-cysteine inhibits primary human T cell responses at the dendritic cell level: association with NF-kappaB inhibition. J Immunol 1999, 162(5):2569-2574.
136. Matsue H., Edelbaum D., Shalhevet D., Mizumoto N., Yang C., Mummert M.E., et al. Generation and function of reactive oxygen species in dendritic cells during antigen presentation. J Immunol 2003, 171(6):3010-3018.
137. Hildeman D.A., Mitchell T., Teague T.K., Henson P., Day B.J., Kappler J., et al. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 1999, 10(6):735-744.
138. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol 2003, 15(2):247-254.
139. Ozaki M., Suzuki S., Irani K. Redox factor-1/APE suppresses oxidative stress by inhibiting the rac1 GTPase. FASEB J 2002, 16(8):889-890.