Enhanced immunoprotective effects by anti-il-17 antibody translates to improved skeletal parameters under estrogen deficiency compared with anti-RANKL and anti-TNF-α antibodies

Journal of Bone and Mineral Research

Volumn 29, Issue 9, 2014, Pages 1981-1992

  Tyagi, Abdul M ^a   Mansoori, Mohd N ^a   Srivastava, Kamini ^a   Khan, Mohd P ^a   Kureel, Jyoti ^a   Dixit, Manisha ^a   Shukla, Priyanka ^a   Trivedi, Ritu ^a   Chattopadhyay, Naibedya ^a   Singh, Divya ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

B LYMPHOPOESIS; ESTROGEN DEFICIENCY; IMMUNE SYSTEM; PROINFLAMMATORY CYTOKINES; T CELLS

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; CD28 ANTIGEN; CYTOKINE ANTIBODY; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 6; OSTEOCLAST DIFFERENTIATION FACTOR ANTIBODY; STAT3 PROTEIN; STAT5 PROTEIN; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; UNCLASSIFIED DRUG; WNT10B PROTEIN; ANTIBODY; AUTACOID; CYTOKINE; ESTROGEN; LEUKOCYTE ANTIGEN; OSTEOCLAST DIFFERENTIATION FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPSY; B LYMPHOCYTE; BIOMECHANICS; BONE MARROW CELL; BONE MASS; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; CORTICAL BONE; CYTOKINE PRODUCTION; DIAPHYSIS; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESTROGEN DEFICIENCY; ESTROGEN THERAPY; FEMALE; FEMUR; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; MORPHOMETRICS; MOUSE; NICK END LABELING; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; OVARIECTOMY; PROTEIN BLOOD LEVEL; REGULATORY T LYMPHOCYTE; RNA ANALYSIS; TH17 CELL; TRABECULAR BONE; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BONE; COMPARATIVE STUDY; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; HUMAN; IMMUNOLOGY; LYMPHOPOIESIS; METABOLISM; PHYSIOLOGY; T LYMPHOCYTE;

ANIMALS; ANTIBODIES; ANTIGENS, CD; B-LYMPHOCYTES; BONE AND BONES; CELL PROLIFERATION; CYTOKINES; ESTROGENS; FEMALE; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-17; LYMPHOPOIESIS; MICE, INBRED BALB C; OSTEOCLASTS; OVARIECTOMY; RANK LIGAND; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84906355830     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2228     Document Type: Article

References (66)

1. Clowes JA, Riggs BL, Khosla S,. The role of the immune system in the pathophysiology of osteoporosis. Immunol Rev. 2005; 208: 207-27.
2. Picherit C, Bennetau-Pelissero C, Chanteranne B, et al. Soybean isoflavones dose-dependently reduce bone turnover but do not reverse established osteopenia in adult ovariectomized rats. J Nutr. 2001; 131 (3): 723-8.
3. Chwan-Li S, Iin-Sook K, Wang S, et al. Functions and mechanisms of green tea catechins in regulating bone remodeling. Curr Drug Targets. 2013; 14 (13): 1619-30.
4. Xu M, Choudhary S, Voznesensky O, et al. Basal bone phenotype and increased anabolic responses to intermittent parathyroid hormone in healthy male COX-2 knockout mice. Bone. 2010; 47 (2): 341-52.
5. Raisz LG,. Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J Clin Invest. 2005; 115 (12): 3318-25.
6. Raisz LG,. Physiology and pathophysiology of bone remodeling. Clin Chem. 1999; 45 (8 Pt 2): 1353-8.
7. Lerner UH,. 2006 Bone remodeling in post-menopausal osteoporosis. J Dent Res. 2006; 85 (7): 584-95.
8. Pinkerton JV, Thomas S, Dalkin AC,. Osteoporosis treatment and prevention for postmenopausal women: current and future therapeutic options. Clin Obstet Gynecol. 2013; 56 (4): 711-21.
9. Ginaldi L, Di Benedetto MC, De Martinis M,. Osteoporosis, inflammation and ageing. Immun Ageing. 2005; 2: 14.
10. Pacifici R,. T cells and post menopausal osteoporosis in murine models. Arthritis Res Ther. 2007; 9 (2): 102.
11. Roggia C, Gao Y, Cenci S, 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 USA. 2001; 98 (24): 13960-5.
12. Tyagi AM, Srivastava K, Kureel J, et al. Premature T cell senescence in Ovx mice is inhibited by repletion of estrogen and medicarpin: a possible mechanism for alleviating bone loss. Osteoporos Int. 2012; 23 (3): 1151-61.
13. Tyagi AM, Srivastava K, Mansoori MN, Trivedi R, Chattopadhyay N, Singh D,. Estrogen deficiency induces the differentiation of IL-17 secreting Th17 cells: a new candidate in the pathogenesis of osteoporosis. PLoS One. 2012; 7 (9): e44552.
14. Tyagi AM, Srivastava K, Sharan K, Yadav D, Maurya R, Singh D,. Daidzein prevents the increase in CD4 + CD28null T cells and B lymphopoesis in ovariectomized mice: a key mechanism for anti-osteoclastogenic effect. PLoS One. 2011; 6 (6): e21216.
15. Kimble RB, 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 (6): 935-41.
16. Furuya Y, Inagaki A, Khan M, et al. Stimulation of bone formation in cortical bone of mice treated with a receptor activator of nuclear factor-kappaB ligand (RANKL)-binding peptide that possesses osteoclastogenesis inhibitory activity. J Biol Chem. 2013; 288 (8): 5562-71.
17. Miller PD,. A review of the efficacy and safety of denosumab in postmenopausal women with osteoporosis. Ther Adv Musculoskelet Dis. 2011; 3 (6): 271-82.
18. Anastasilakis AD, Toulis KA, Polyzos SA, Anastasilakis CD, Makras P,. Long-term treatment of osteoporosis: safety and efficacy appraisal of denosumab. Ther Clin Risk Manag. 2012; 8: 295-306.
19. Reginster JY, Pelousse F, Bruyere O,. Safety concerns with the long-term management of osteoporosis. Expert Opin Drug Saf. 2013; 12 (4): 507-22.
20. Kawai VK, Stein CM, Perrien DS, Griffin MR,. Effects of anti-tumor necrosis factor alpha agents on bone. Curr Opin Rheumatol. 2012; 24 (5): 576-85.
21. McMahon MS, Ueki Y,. Does anti-TNF-alpha have a role in the treatment of osteoporosis ? Bull NYU Hosp Jt Dis. 2008; 66 (4): 280-1.
22. Atzeni F, Talotta R, Salaffi F, et al. Immunogenicity and autoimmunity during anti-TNF therapy. Autoimmun Rev. 2013; 12 (7): 703-8.
23. Cairns AP, Taggart AJ,. Anti-tumour necrosis factor therapy for severe inflammatory arthritis: two years of experience in Northern Ireland. Ulster Med J. 2002; 71 (2): 101-5.
24. Rosenblum H, Amital H,. Anti-TNF therapy: safety aspects of taking the risk. Autoimmun Rev. 2011; 10 (9): 563-8.
25. Navarra SV, Tang B, Lu L, et al. Risk of tuberculosis with anti-tumor necrosis factor-alpha therapy: substantially higher number of patients at risk in Asia. Int J Rheum Dis. 2014; 17 (3): 291-8.
26. Sugita S, Kawazoe Y, Imai A, Yamada Y, Horie S, Mochizuki M,. Inhibition of Th17 differentiation by anti-TNF-alpha therapy in uveitis patients with Behcet's disease. Arthritis Res. Ther. 2012; 14 (3): R99.
27. Dahlen R, Strid H, Lundgren A, et al. Infliximab inhibits activation and effector functions of peripheral blood T cells in vitro from patients with clinically active ulcerative colitis. Scand J Immunol. 2013; 78 (3): 275-84.
28. Shen H, Xia L, Lu J, Xiao W,. Infliximab reduces the frequency of interleukin 17-producing cells and the amounts of interleukin 17 in patients with rheumatoid arthritis. J Investig Med. 2010; 58 (7): 905-8.
29. Yuan FL, Li X, Lu WG, et al. Type 17 T-helper cells might be a promising therapeutic target for osteoporosis. Mol Biol Rep. 2012; 39 (1): 771-4.
30. Sato K, Suematsu A, Okamoto K, 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): 2673-82.
31. Kramer JM, Gaffen SL,. Interleukin-17: a new paradigm in inflammation, autoimmunity, and therapy. J Periodontol. 2007; 78 (6): 1083-93.
32. Miossec P, Korn T, Kuchroo VK,. Interleukin-17 and type 17 helper T cells. N Engl J Med. 2009; 361 (9): 888-98.
33. Ominsky MS, Stouch B, Schroeder J, et al. Denosumab, a fully human RANKL antibody, reduced bone turnover markers and increased trabecular and cortical bone mass, density, and strength in ovariectomized cynomolgus monkeys. Bone. 2011; 49 (2): 162-73.
34. Kostenuik PJ, Nguyen HQ, McCabe J, et al. Denosumab, a fully human monoclonal antibody to RANKL, inhibits bone resorption and increases BMD in knock-in mice that express chimeric (murine/human) RANKL. J Bone Miner Res. 2009; 24 (2): 182-95.
35. Ominsky MS, Li X, Asuncion FJ, et al. RANKL inhibition with osteoprotegerin increases bone strength by improving cortical and trabecular bone architecture in ovariectomized rats. J Bone Miner Res. 2008; 23 (5): 672-82.
36. Furuya Y, Mori K, Ninomiya T, et al. Increased bone mass in mice after single injection of anti-receptor activator of nuclear factor-kappaB ligand-neutralizing antibody: evidence for bone anabolic effect of parathyroid hormone in mice with few osteoclasts. J Biol Chem. 2011; 286 (42): 37023-31.
37. Wada T, Nakashima T, Hiroshi N, Penninger JM,. RANKL-RANK signaling in osteoclastogenesis and bone disease. Trends Mol Med. 2006; 12 (1): 17-25.
38. Tomimori Y, Mori K, Koide M, et al. Evaluation of pharmaceuticals with a novel 50-hour animal model of bone loss. J Bone Miner Res. 2009; 24 (7): 1194-205.
39. Kim BJ, Bae SJ, Lee SY, et al. TNF-alpha mediates the stimulation of sclerostin expression in an estrogen-deficient condition. Biochem Biophys Res. Commun. 2012; 424 (1): 170-5.
40. Cenci S, Toraldo G, Weitzmann MN, 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 USA. 2003; 100 (18): 10405-10.
41. Baker PJ, Dixon M, Evans RT, Dufour L, Johnson E, Roopenian DC,. CD4(+) T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun. 1999; 67 (6): 2804-9.
42. Tarjanyi O, Boldizsar F, Nemeth P, Mikecz K, Glant TT,. Age-related changes in arthritis susceptibility and severity in a murine model of rheumatoid arthritis. Immun Ageing. 2009; 6: 8.
43. Kozlowska E, Biernacka M, Ciechomska M, Drela N,. Age-related changes in the occurrence and characteristics of thymic CD4(+) CD25(+) T cells in mice. Immunology. 2007; 122 (3): 445-53.
44. Kamijo S, Nakajima A, Ikeda K, et al. Amelioration of bone loss in collagen-induced arthritis by neutralizing anti-RANKL monoclonal antibody. Biochem Biophys Res Commun. 2006; 347 (1): 124-32.
45. Bianchi F, Bernardini N, Marchetti P, et al. In vitro morpho-functional analysis of pancreatic islets isolated from the domestic chicken. Tissue Cell. 1993; 25 (6): 817-24.
46. Marchetti P, Giannarelli Villani G, et al. 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. 1994; 57 (10): 1532-5.
47. Sharan K, Mishra JS, Swarnkar G, et al. A novel quercetin analogue from a medicinal plant promotes peak bone mass achievement and bone healing after injury and exerts an anabolic effect on osteoporotic bone: the role of aryl hydrocarbon receptor as a mediator of osteogenic action. J Bone Miner Res. 2011; 26 (9): 2096-111.
48. Bhargavan B, Gautam AK, Singh D, et al. Methoxylated isoflavones, cajanin and isoformononetin, have non-estrogenic bone forming effect via differential mitogen activated protein kinase (MAPK) signaling. J Cell Biochem. 2009; 108 (2): 388-99.
49. Vallejo AN, Weyand CM, Goronzy JJ,. T-cell senescence: a culprit of immune abnormalities in chronic inflammation and persistent infection. Trends Mol Med. 2004; 10 (3): 119-24.
50. Kawai T, Matsuyama T, Hosokawa Y, et al. B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol. 2006; 169 (3): 987-98.
51. Horowitz MC, Bothwell AL, Hesslein DG, Pflugh DL, Schatz DG,. B cells and osteoblast and osteoclast development. Immunol Rev. 2005; 208: 141-53.
52. Ziegler SF, Buckner JH,. FOXP3 and the regulation of Treg/Th17 differentiation. Microbes Infect. 2009; 11 (5): 594-8.
53. Dong C,. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat Rev Immunol. 2008; 8 (5): 337-48.
54. Bennett CN, Ouyang H, Ma YL, et al. Wnt10b increases postnatal bone formation by enhancing osteoblast differentiation. J Bone Miner Res. 2007; 22 (12): 1924-32.
55. Schnoke M, Midura SB, Midura RJ,. Parathyroid hormone suppresses osteoblast apoptosis by augmenting DNA repair. Bone. 2009; 45 (3): 590-602.
56. Terauchi M, Li JY, Bedi B, et al. T lymphocytes amplify the anabolic activity of parathyroid hormone through Wnt10b signaling. Cell Metab. 2009; 10 (3): 229-40.
57. Silvestrini G, Ballanti P, Leopizzi M, et al. Effects of intermittent parathyroid hormone (PTH) administration on SOST mRNA and protein in rat bone. J Mol Histol. 2007; 38 (4): 261-9.
58. Dobnig H, Turner RT,. Evidence that intermittent treatment with parathyroid hormone increases bone formation in adult rats by activation of bone lining cells. Endocrinology. 1995; 136 (8): 3632-8.
59. Hale LV, Galvin RJ, Risteli J, et al. PINP: a serum biomarker of bone formation in the rat. Bone. 2007; 40 (4): 1103-9.
60. Rosen CJ, Usiskin K, Owens M, Barlascini CO, Belsky M, Adler RA,. T lymphocyte surface antigen markers in osteoporosis. J Bone Miner Res. 1990; 5 (8): 851-5.
61. Masuzawa T, Miyaura C, Onoe Y, et al. Estrogen deficiency stimulates B lymphopoiesis in mouse bone marrow. J Clin Invest. 1994; 94 (3): 1090-7.
62. Li Y, Li A, Yang X, Weitzmann MN,. Ovariectomy-induced bone loss occurs independently of B cells. J Cell Biochem. 2007; 100 (6): 1370-5.
63. Dasgupta A, Saxena R,. Regulatory T cells: a review. Natl Med J India. 2012; 25 (6): 341-51.
64. Duong le T,. Therapeutic inhibition of cathepsin K-reducing bone resorption while maintaining bone formation. Bonekey Rep. 2012; 1: 67.
65. Li JY, Walker LD, Tyagi AM, Adams J, Weitzmann MN, Pacifici R,. The sclerostin-independent bone anabolic activity of intermittent PTH treatment is mediated by T-cell-produced Wnt10b. J Bone Miner Res. 2014; 29 (1): 43-54.
66. Yasuda H,. RANKL, a necessary chance for clinical application to osteoporosis and cancer-related bone diseases. World J Orthop. 2013; 4 (4): 207-17.