Estrogen deficiency induces the differentiation of IL-17 secreting Th17 cells: A new candidate in the pathogenesis of osteoporosis

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Tyagi, Abdul M ^a   Srivastava, Kamini ^a   Mansoori, Mohd Nizam ^a   Trivedi, Ritu ^a   Chattopadhyay, Naibedya ^a   Singh, Divya ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ESTROGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 6; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; RETINOID RELATED ORPHAN RECEPTOR ALPHA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; ESTRADIOL; MESSENGER RNA; TNFSF11 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW STROMA CELL; CALVARIA; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; ESTROGEN DEFICIENCY; HEMATOPOIETIC STEM CELL; IMMUNOREGULATION; IN VIVO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPOROSIS; OVARIECTOMY; TH17 CELL; TRABECULAR BONE; ANIMAL; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; GENETICS; HELPER CELL; METABOLISM; OSTEOCLAST; SECRETION (PROCESS);

ANIMALS; CELL DIFFERENTIATION; CELL LINE; ESTRADIOL; INTERLEUKIN-17; MICE; NF-KAPPA B; OSTEOBLASTS; OSTEOCLASTS; OSTEOPOROSIS; OSTEOPROTEGERIN; OVARIECTOMY; RANK LIGAND; RNA, MESSENGER; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84872336610     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044552     Document Type: Article

References (62)

1. Clowes JA, Riggs BL, Khosla S (2005) The role of the immune system in the pathophysiology of osteoporosis. Immunol Rev 208:207-227.
2. Ginaldi L, Di Benedetto MC, De Martinis M (2005) Osteoporosis, inflammation and ageing. Immun Ageing 2:14.
3. Arron JR, Choi Y (2000) Bone versus immune system. Nature 408:535-536.
4. Oostlander AE, Everts V, Schoenmaker T, Bravenboer N, van Vliet SJ, et al (2012) T cell-mediated increased osteoclast formation from peripheral blood as a mechanism for Crohn's disease-associated bone loss. J Cell Biochem 113:260-268.
5. Manolagas SC (2000) Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 21:115-137.
6. Clarke B (2008) Normal bone anatomy and physiology. Clin J Am Soc Nephrol 3 Suppl 3:S131-139.
7. Roggia C, Gao Y, Cenci S, Weitzmann MN, Toraldo G, et al (2001) Upregulation 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 98:13960-13965.
8. Pacifici R (2007) T cells and post menopausal osteoporosis in murine models. Arthritis Res Ther 9:102.
9. Tyagi AM, Srivastava K, Sharan K, Yadav D, Maurya R, et al (2011) Daidzein prevents the increase in CD4+CD28null T cells and B lymphopoesis in ovariectomized mice: a key mechanism for anti-osteoclastogenic effect. PLoS One 6:e21216.
10. Weitzmann MN, Pacifici R (2005) The role of T lymphocytes in bone metabolism. Immunol Rev 208:154-168.
11. Kong YY, Penninger JM (2000) Molecular control of bone remodeling and osteoporosis. Exp Gerontol 35:947-956.
12. Kotake S, Udagawa N, Hakoda M, Mogi M, Yano K, et al (2001) Activated human T cells directly induce osteoclastogenesis from human monocytes: possible role of T cells in bone destruction in rheumatoid arthritis patients. Arthritis Rheum 44:1003-1012.
13. Weitzmann MN, Cenci S, Rifas L, Haug J, Dipersio J, et al (2001) T cell activation induces human osteoclast formation via receptor activator of nuclear factor kappaB ligand-dependent and -independent mechanisms. J Bone Miner Res 16:328-337.
14. Kong YY FU, Sarosi I, Bolon B, Tafuri A, Morony S (1999) Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402:304-309.
15. Yuan FL, Li X, Lu WG, Zhao YQ, Li CW, et al (2012) Type 17 T-helper cells might be a promising therapeutic target for osteoporosis. Mol Biol Rep 39:771-774.
16. Kramer JM, Gaffen SL (2007) Interleukin-17: a new paradigm in inflammation, autoimmunity, and therapy. J Periodontol 78:1083-1093.
17. Annunziato F, Cosmi L, Liotta F, Maggi E, Romagnani S (2009) Type 17 T helper cells-origins, features and possible roles in rheumatic disease. Nat Rev Rheumatol 5:325-331.
18. Yu JJ, Gaffen SL (2008) Interleukin-17: a novel inflammatory cytokine that bridges innate and adaptive immunity. Front Biosci 13:170-177.
19. Kosmaczewska A, Swierkot J, Ciszak L, Wiland P (2011) The role of Th1, Th17, and Treg cells in the pathogenesis of rheumatoid arthritis including antiinflammatory action of Th1 cytokines. Postepy Hig Med Dosw (Online) 65:397-403.
20. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, et al (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103:1345-1352.
21. Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, et al (2006) Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 203:2673-2682.
22. Kamiya S, Nakamura C, Fukawa T, Ono K, Ohwaki T, et al (2007) Effects of IL-23 and IL-27 on osteoblasts and osteoclasts: inhibitory effects on osteoclast differentiation. J Bone Miner Metab 25:277-285.
23. Yu JJ, Ruddy MJ, Conti HR, Boonanantanasarn K, Gaffen SL (2008) The interleukin-17 receptor plays a gender-dependent role in host protection against Porphyromonas gingivalis-induced periodontal bone loss. Infect Immun 76:4206-4213.
24. Won HY, Lee JA, Park ZS, Song JS, Kim HY, et al (2011) Prominent bone loss mediated by RANKL and IL-17 produced by CD4+ T cells in TallyHo/JngJ mice. PLoS One 6:e18168.
25. Miossec P, Korn T, Kuchroo VK (2009) Interleukin-17 and type 17 helper T cells. N Engl J Med 361:888-898.
26. Goswami J, Hernandez-Santos N, Zuniga LA, Gaffen SL (2009) A boneprotective role for IL-17 receptor signaling in ovariectomy-induced bone loss. Eur J Immunol 39:2831-2839.
27. Abdul Tyagi DS (2011) Estrogen deficiency leads to increased differentiation of IL-17 secreting Th17 cells which might adversely affect bone formation Osteoporos Int 22 S214
28. Deselm CJ, Takahata Y, Warren J, Chappel JC, Khan T (2012) IL-17 mediates estrogen-deficient osteoporosis in an Act1-dependent manner J Cell Biochem Apr. 17. doi: 10.1002/jcb.24165.
29. Tyagi AM, Gautam AK, Kumar A, Srivastava K, Bhargavan B, et al (2010) Medicarpin inhibits osteoclastogenesis and has nonestrogenic bone conserving effect in ovariectomized mice. Mol Cell Endocrinol 325:101-109.
30. Yago T, Nanke Y, Ichikawa N, Kobashigawa T, Mogi M, et al (2009) IL-17 induces osteoclastogenesis from human monocytes alone in the absence of osteoblasts, which is potently inhibited by anti-TNF-alpha antibody: a novel mechanism of osteoclastogenesis by IL-17. J Cell Biochem 108:947-955.
31. Ariyoshi W, Takahashi T, Kanno T, Ichimiya H, Shinmyouzu K, et al (2008) Heparin inhibits osteoclastic differentiation and function. J Cell Biochem 103:1707-1717.
32. Bhargavan B, Gautam AK, Singh D, Kumar A, Chaurasia S, et al (2009) Methoxylated isoflavones, cajanin and isoformononetin, have non-estrogenic bone forming effect via differential mitogen activated protein kinase (MAPK) signaling. J Cell Biochem 108:388-399.
33. Gautam AK, Bhargavan B, Tyagi AM, Srivastava K, Yadav DK, et al (2011) Differential effects of formononetin and cladrin on osteoblast function, peak bone mass achievement and bioavailability in rats. J Nutr Biochem 22:318-327.
34. Kumar A, Singh AK, Gautam AK, Chandra D, Singh D, et al (2010) Identification of kaempferol-regulated proteins in rat calvarial osteoblasts during mineralization by proteomics. Proteomics 10:1730-1739.
35. Tyagi AM, Srivastava K, Kureel J, Kumar A, Raghuvanshi A, et al (2011) Premature T cell senescence in Ovx mice is inhibited by repletion of estrogen and medicarpin: a possible mechanism for alleviating bone loss. Osteoporos Int 23:1151-1161.
36. Gregory CA, Gunn WG, Peister A, Prockop DJ (2004) An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem 329:77-84.
37. Maurya R, Yadav DK, Singh G, Bhargavan B, Narayana Murthy PS, et al (2009) Osteogenic activity of constituents from Butea monosperma. Bioorg Med Chem Lett 19:610-613.
38. Kim SH, Shin TY (2005) Amomum xanthiodes inhibits mast cell-mediated allergic reactions through the inhibition of histamine release and inflammatory cytokine production. Exp Biol Med (Maywood) 230:681-687.
39. Cenci S, Toraldo G, Weitzmann MN, Roggia C, Gao Y, et al (2003) 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 100:10405-10410.
40. Baker PJ, Dixon M, Evans RT, Dufour L, Johnson E, et al (1999) CD4 (+) T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 67:2804-2809.
41. Tarjanyi O, Boldizsar F, Nemeth P, Mikecz K, Glant TT (2009) Age-related changes in arthritis susceptibility and severity in a murine model of rheumatoid arthritis. Immun Ageing 6:8.
42. Kozlowska E, Biernacka M, Ciechomska M, Drela N (2007) Age-related changes in the occurrence and characteristics of thymic CD4 (+) CD25 (+) T cells in mice. Immunology 122:445-453.
43. Lubberts E, Koenders MI, Oppers-Walgreen B, van den Bersselaar L, Coenende Roo CJ, et al (2004) Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum 50:650-659.
44. Sarkar S, Cooney LA, White P, Dunlop DB, Endres J, et al (2009) Regulation of pathogenic IL-17 responses in collagen-induced arthritis: roles of endogenous interferon-gamma and IL-4. Arthritis Res Ther 11:R158.
45. Yang W, Ding X, Deng J, Lu Y, Matsuda Z, et al (2011) Interferon-gamma negatively regulates Th17-mediated immunopathology during mouse hepatitis virus infection. J Mol Med (Berl) 89:399-409.
46. Bianchi F, Bernardini N, Marchetti P, Navalesi R, Giannarelli R, et al (1993) In vitro morpho-functional analysis of pancreatic islets isolated from the domestic chicken. Tissue Cell 25:817-824.
47. Marchetti P, Giannarelli, Villani G, Andreozzi M, Cruschelli L, et al (1994) Collagenase distension, two-step sequential filtration, and histopaque gradient purification for consistent isolation of pure pancreatic islets from the market-age (6-month-old) pig. Transplantation 57:1532-1535.
48. Bryl E, Vallejo AN, Matteson EL, Witkowski JM, Weyand CM, et al (2005) Modulation of CD28 expression with anti-tumor necrosis factor alpha therapy in rheumatoid arthritis. Arthritis Rheum 52:2996-3003.
49. Pandey R, Gautam AK, Bhargavan B, Trivedi R, Swarnkar G, et al (2010) Total extract and standardized fraction from the stem bark of Butea monosperma have osteoprotective action: evidence for the nonestrogenic osteogenic effect of the standardized fraction. Menopause 17:602-610.
50. Stamp LK, James MJ, Cleland LG (2004) Interleukin-17: the missing link between T-cell accumulation and effector cell actions in rheumatoid arthritis? Immunol Cell Biol 82:1-9.
51. Witowski J, Ksiazek K, Jorres A (2004) Interleukin-17: a mediator of inflammatory responses. Cell Mol Life Sci 61:567-579.
52. Burger HG (2001) Physiological principles of endocrine replacement: estrogen. Horm Res 56 Suppl 1:82-85.
53. Kitami S, Tanaka H, Kawato T, Tanabe N, Katono-Tani T, et al (2010) IL-17A suppresses the expression of bone resorption-related proteinases and osteoclast differentiation via IL-17RA or IL-17RC receptors in RAW264.7 cells. Biochimie 92:398-404.
54. Huang H, Kim HJ, Chang EJ, Lee ZH, Hwang SJ, et al (2009) IL-17 stimulates the proliferation and differentiation of human mesenchymal stem cells: implications for bone remodeling. Cell Death Differ 16:1332-1343.
55. Kocic J, Santibanez JF, Krstic A, Mojsilovic S, Dordevic IO, et al (2012) Interleukin 17 inhibits myogenic and promotes osteogenic differentiation of C2C12 myoblasts by activating ERK1, 2. Biochim Biophys Acta 1823:838-849.
56. Dong C (2008) TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol 8:337-348.
57. Lelu K, Laffont S, Delpy L, Paulet PE, Perinat T, et al (2011) Estrogen receptor alpha signaling in T lymphocytes is required for estradiol-mediated inhibition of Th1 and Th17 cell differentiation and protection against experimental autoimmune encephalomyelitis. J Immunol 187:2386-2393.
58. Luo CY, Wang L, Sun C, Li DJ (2011) Estrogen enhances the functions of CD4 (+) CD25 (+) Foxp3 (+) regulatory T cells that suppress osteoclast differentiation and bone resorption in vitro. Cell Mol Immunol 8:50-58.
59. Calvo MS, Eyre DR, Gundberg CM (1996) Molecular basis and clinical application of biological markers of bone turnover. Endocr Rev 17:333-368.
60. Garnero P, Dargent-Molina P, Hans D, Schott AM, Breart G, et al. (1998) Do markers of bone resorption add to bone mineral density and ultrasonographic heel measurement for the prediction of hip fracture in elderly women? The EPIDOS prospective study. Osteoporos Int 8:563-569.
61. Mainini G, Incoronato M, Urso L, Scaffa C Serum (2011) osteoprotegerin correlates with age and bone mass in postmenopausal, but not in fertile age women. Clin Exp Obstet Gynecol 38:355-359.
62. Holland JC, Brennan O, Kennedy OD, Rackard SM, O'Brien FJ, et al (2011) Subchondral trabecular structural changes in the proximal tibia in an ovine model of increased bone turnover. J Anat 218:619-624.