IL-17A Is Increased in Humans with Primary Hyperparathyroidism and Mediates PTH-Induced Bone Loss in Mice

Cell Metabolism

Volumn 22, Issue 5, 2015, Pages 799-810

  Li, Jau Yi ^a   D'Amelio, Patrizia ^b   Robinson, Jerid ^a   Walker, Lindsey D ^a   Vaccaro, Chiara ^a   Luo, Tao ^a   Tyagi, Abdul Malik ^a   Yu, Mingcan ^a   Reott, Michael ^a   Sassi, Francesca ^b   Buondonno, Ilaria ^b   Adams, Jonathan ^a   Weitzmann, M Neale ^a,c   Isaia, Giovanni Carlo ^b   Pacifici, Roberto ^a,d  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TURIN   (Italy)

^c ATLANTA VA MEDICAL CENTER   (United States)

^d EMORY UNIVERSITY   (United States)

Author keywords

bone; hyperparathyroidism; IL 17; IL 17 antibody; IL 17R; PTH; T cells; Th17 cells

Indexed keywords

CALCIUM; DILTIAZEM; INTERLEUKIN 17; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE; TUMOR NECROSIS FACTOR ALPHA; CALCIUM CHANNEL BLOCKING AGENT; IL17A PROTEIN, HUMAN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM BLOOD LEVEL; CALCIUM SIGNALING; CATABOLISM; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; HUMAN; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MORPHOMETRICS; MOUSE; NONHUMAN; OSTEOLYSIS; PARATHYROID FUNCTION; PARATHYROIDECTOMY; PERIPHERAL CIRCULATION; POSTMENOPAUSE; PRIMARY HYPERPARATHYROIDISM; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; ANIMAL; BIOSYNTHESIS; BONE DISEASES, METABOLIC; COMPLICATION; HYPERPARATHYROIDISM, PRIMARY; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BONE DISEASES, METABOLIC; CALCIUM CHANNEL BLOCKERS; HUMANS; HYPERPARATHYROIDISM, PRIMARY; INTERLEUKIN-17; MICE; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84948397950     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.09.012     Document Type: Article

References (58)

1. Adamopoulos, I. E., Chao, C. C., Geissler, R., Laface, D., Blumenschein, W., Iwakura, Y., McClanahan, T., and Bowman, E. P. (2010). Interleukin-17A upregulates receptor activator of NF-kappaB on osteoclast precursors. Arthritis Res. Ther. 12, R29.
2. Basu, R., Hatton, R. D., and Weaver, C. T. (2013). The Th17 family: flexibility follows function. Immunol. Rev. 252, 89-103.
3. Bedi, B., Li, J. Y., Tawfeek, H., Baek, K. H., Adams, J., Vangara, S. S., Chang, M. K., Kneissel, M., Weitzmann, M. N., and Pacifici, R. (2012). Silencing of parathyroid hormone (PTH) receptor 1 in T cells blunts the bone anabolic activity of PTH. Proc. Natl. Acad. Sci. USA 109, E725-E733.
4. Ben-awadh, A. N., Delgado-Calle, J., Tu, X., Kuhlenschmidt, K., Allen, M. R., Plotkin, L. I., and Bellido, T. (2014). Parathyroid hormone receptor signaling induces bone resorption in the adult skeleton by directly regulating the RANKL gene in osteocytes. Endocrinology 155, 2797-2809.
5. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., Weiner, H. L., and Kuchroo, V. K. (2006). Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238.
6. Calvi, L. M., Sims, N. A., Hunzelman, J. L., Knight, M. C., Giovannetti, A., Saxton, J. M., Kronenberg, H. M., Baron, R., and Schipani, E. (2001). Activated parathyroid hormone/parathyroid hormone-related protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. J. Clin. Invest. 107, 277-286.
7. Chen, D. Y., Chen, Y. M., Chen, H. H., Hsieh, C. W., Lin, C. C., and Lan, J. L. (2011). Increasing levels of circulating Th17 cells and interleukin-17 in rheumatoid arthritis patients with an inadequate response to anti-TNF-a therapy. Arthritis Res. Ther. 13, R126.
8. Cho, S. W., Soki, F. N., Koh, A. J., Eber, M. R., Entezami, P., Park, S. I., van Rooijen, N., and McCauley, L. K. (2014). Osteal macrophages support physiologic skeletal remodeling and anabolic actions of parathyroid hormone in bone. Proc. Natl. Acad. Sci. USA 111, 1545-1550.
9. Datta, N. S., and Abou-Samra, A. B. (2009). PTH and PTHrP signaling in osteoblasts. Cell. Signal. 21, 1245-1254.
10. Dempster, D. W., Compston, J. E., Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M., Recker, R. R., and Parfitt, A. M. (2013). Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 28, 2-17.
11. DeSelm, C. J., Takahata, Y., Warren, J., Chappel, J. C., Khan, T., Li, X., Liu, C., Choi, Y., Kim, Y. F., Zou, W., and Teitelbaum, S. L. (2012). IL-17 mediates estrogen-deficient osteoporosis in an Act1-dependent manner. J. Cell. Biochem. 113, 2895-2902.
12. Gao, Y., Wu, X., Terauchi, M., Li, J. Y., Grassi, F., Galley, S., Yang, X., Weitzmann, M. N., and Pacifici, R. (2008). T cells potentiate PTH-induced cortical bone loss through CD40L signaling. Cell Metab. 8, 132-145.
13. Hell, J. W. (2010). Beta-adrenergic regulation of the L-type Ca2+ channel Ca(V) 1. 2 by PKA rekindles excitement. Sci. Signal. 3, pe33.
14. Iida-Klein, A., Lu, S. S., Kapadia, R., Burkhart, M., Moreno, A., Dempster, D. W., and Lindsay, R. (2005). Short-term continuous infusion of human parathyroid hormone 1-34 fragment is catabolic with decreased trabecular connectivity density accompanied by hypercalcemia in C57BL/J6 mice. J. Endocrinol. 186, 549-557.
15. Iwakura, Y., Ishigame, H., Saijo, S., and Nakae, S. (2011). Functional specialization of interleukin-17 family members. Immunity 34, 149-162.
16. Jovanovic, D. V., Di Battista, J. A., Martel-Pelletier, J., Jolicoeur, F. C., He, Y., Zhang, M., Mineau, F., and Pelletier, J. P. (1998). IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J. Immunol. 160, 3513-3521.
17. Kappel, L. W., Goldberg, G. L., King, C. G., Suh, D. Y., Smith, O. M., Ligh, C., Holland, A. M., Grubin, J., Mark, N. M., Liu, C., et al. (2009). IL-17 contributes to CD4-mediated graft-versus-host disease. Blood 113, 945-952.
18. Koh, A. J., Novince, C. M., Li, X., Wang, T., Taichman, R. S., and McCauley, L. K. (2011). An irradiation-altered bone marrow microenvironment impacts anabolic actions of PTH. Endocrinology 152, 4525-4536.
19. Komatsu, N., and Takayanagi, H. (2012). Autoimmune arthritis: the interface between the immune system and joints. Adv. Immunol. 115, 45-71.
20. Korn, T., Bettelli, E., Oukka, M., and Kuchroo, V. K. (2009). IL-17 and Th17 Cells. Annu. Rev. Immunol. 27, 485-517.
21. Kotake, S., Udagawa, N., Takahashi, N., Matsuzaki, K., Itoh, K., Ishiyama, S., Saito, S., Inoue, K., Kamatani, N., Gillespie, M. T., 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.
22. Lang, C. L., Wang, M. H., Hung, K. Y., Hsu, S. H., Chiang, C. K., and Lu, K. C. (2014). Correlation of interleukin-17-producing effector memory T cells and CD4+CD25+Foxp3 regulatory T cells with the phosphate levels in chronic hemodialysis patients. ScientificWorldJournal 2014, 593170.
23. Leonardi, C., Matheson, R., Zachariae, C., Cameron, G., Li, L., Edson-Heredia, E., Braun, D., and Banerjee, S. (2012). Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N. Engl. J. Med. 366, 1190-1199.
24. Li, X., Murray, F., Koide, N., Goldstone, J., Dann, S. M., Chen, J., Bertin, S., Fu, G., Weinstein, L. S., Chen, M., et al. (2012). Divergent requirement for Gas and cAMP in the differentiation and inflammatory profile of distinct mouse Th subsets. J. Clin. Invest. 122, 963-973.
25. Lockhart, E., Green, A. M., and Flynn, J. L. (2006). IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J. Immunol. 177, 4662-4669.
26. Löwik, C. W. G. M., van der Pluijm, G., Bloys, H., Hoekman, K., Bijvoet, O. L., Aarden, L. A., and Papapoulos, S. E. (1989). Parathyroid hormone (PTH) and PTH-like protein (PLP) stimulate interleukin-6 production by osteogenic cells: a possible role of interleukin-6 in osteoclastogenesis. Biochem. Biophys. Res. Commun. 162, 1546-1552.
27. Ma, Y. L., Cain, R. L., Halladay, D. L., Yang, X., Zeng, Q., Miles, R. R., Chandrasekhar, S., Martin, T. J., and Onyia, J. E. (2001). Catabolic effects of continuous human PTH (1-38) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and gene-associated bone formation. Endocrinology 142, 4047-4054.
28. Martin, D. A., Churchill, M., Flores-Suarez, L., Cardiel, M. H., Wallace, D., Martin, R., Phillips, K., Kaine, J. L., Dong, H., Salinger, D., et al. (2013). A phase Ib multiple ascending dose study evaluating safety, pharmacokinetics, and early clinical response of brodalumab, a human anti-IL-17R antibody, in methotrexate-resistant rheumatoid arthritis. Arthritis Res. Ther. 15, R164.
29. Martinez, G. J., Nurieva, R. I., Yang, X. O., and Dong, C. (2008). Regulation and function of proinflammatory TH17 cells. Ann. N Y Acad. Sci. 1143, 188-211.
30. Mease, P. J., Genovese, M. C., Greenwald, M. W., Ritchlin, C. T., Beaulieu, A. D., Deodhar, A., Newmark, R., Feng, J., Erondu, N., and Nirula, A. (2014). Brodalumab, an anti-IL17RA monoclonal antibody, in psoriatic arthritis. N. Engl. J. Med. 370, 2295-2306.
31. Mieth, A., Revermann, M., Babelova, A., Weigert, A., Schermuly, R. T., and Brandes, R. P. (2013). L-type calcium channel inhibitor diltiazem prevents aneurysm formation by blood pressure-independent anti-inflammatory effects. Hypertension 62, 1098-1104.
32. Miossec, P., Korn, T., and Kuchroo, V. K. (2009). Interleukin-17 and type 17 helper T cells. N. Engl. J. Med. 361, 888-898.
33. Molnár, I., Bohaty, I., and Somogyiné-Vári, É. (2014). IL-17A-mediated sRANK ligand elevation involved in postmenopausal osteoporosis. Osteoporos. Int. 25, 783-786.
34. Nakae, S., Suto, H., Berry, G. J., and Galli, S. J. (2007). Mast cell-derived TNF can promote Th17 cell-dependent neutrophil recruitment in ovalbumin-challenged OTII mice. Blood 109, 3640-3648.
35. Nakashima, T., Kobayashi, Y., Yamasaki, S., Kawakami, A., Eguchi, K., Sasaki, H., and Sakai, H. (2000). Protein expression and functional difference of membrane-bound and soluble receptor activator of NF-kappaB ligand: modulation of the expression by osteotropic factors and cytokines. Biochem. Biophys. Res. Commun. 275, 768-775.
36. Oh-hora, M. (2009). Calcium signaling in the development and function of Tlineage cells. Immunol. Rev. 231, 210-224.
37. Pacifici, R. (2013). Role of T cells in the modulation of PTH action: physiological and clinical significance. Endocrine 44, 576-582.
38. Parisien, M., Dempster, D. W., Shane, E., and Bilezikian, J. P. (2001). Histomorphometric analysis of bone in primary hyperparathyroidism. In The Parathyroids: Basic and Clinical Concepts, J. P. Bilezikian, R. Marcus, and M. A. Levine, eds. (Academic Press), pp. 423-436.
39. Potts, J. (1998). Primary hyperparathyroidism. In Metabolic Bone Diseases, L. V. Avioli and S. Krane, eds. (Academic Press), pp. 411-442.
40. Qin, L., Raggatt, L. J., and Partridge, N. C. (2004). Parathyroid hormone: a double-edged sword for bone metabolism. Trends Endocrinol. Metab. 15, 60-65.
41. Qin, J., Shang, L., Ping, A. S., Li, J., Li, X. J., Yu, H., Magdalou, J., Chen, L. B., and Wang, H. (2012). TNF/TNFR signal transduction pathway-mediated antiapoptosis and anti-inflammatory effects of sodium ferulate on IL-1b-induced rat osteoarthritis chondrocytes in vitro. Arthritis Res. Ther. 14, R242.
42. Robinson, J. W., Li, J. Y., Walker, L. D., Tyagi, A. M., Reott, M. A., Yu, M., Adams, J., Weitzmann, M. N., and Pacifici, R. (2015). T cell-expressed CD40L potentiates the bone anabolic activity of intermittent PTH treatment. J. Bone Miner. Res. 30, 695-705.
43. Saini, V., Marengi, D. A., Barry, K. J., Fulzele, K. S., Heiden, E., Liu, X., Dedic, C., Maeda, A., Lotinun, S., Baron, R., and Pajevic, P. D. (2013). Parathyroid hormone (PTH)/PTH-related peptide type 1 receptor (PPR) signaling in osteocytes regulates anabolic and catabolic skeletal responses to PTH. J. Biol. Chem. 288, 20122-20134.
44. Sato, K., Suematsu, A., Okamoto, K., Yamaguchi, A., Morishita, Y., Kadono, Y., Tanaka, S., Kodama, T., Akira, S., Iwakura, 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.
45. Semsarian, C., Ahmad, I., Giewat, M., Georgakopoulos, D., Schmitt, J. P., McConnell, B. K., Reiken, S., Mende, U., Marks, A. R., Kass, D. A., et al. (2002). The L-type calcium channel inhibitor diltiazem prevents cardiomyopathy in a mouse model. J. Clin. Invest. 109, 1013-1020.
46. Silverberg, S. J., Shane, E., de la Cruz, L., Dempster, D. W., Feldman, F., Seldin, D., Jacobs, T. P., Siris, E. S., Cafferty, M., Parisien, M. V., et al. (1989). Skeletal disease in primary hyperparathyroidism. J. Bone Miner. Res. 4, 283-291.
47. Sugita, S., Kawazoe, Y., Imai, A., Yamada, Y., Horie, S., and Mochizuki, M. (2012). Inhibition of Th17 differentiation by anti-TNF-alpha therapy in uveitis patients with Behçet's disease. Arthritis Res. Ther. 14, R99.
48. Sutton, C. E., Lalor, S. J., Sweeney, C. M., Brereton, C. F., Lavelle, E. C., and Mills, K. H. (2009). Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31, 331-341.
49. Tawfeek, H., Bedi, B., Li, J. Y., Adams, J., Kobayashi, T., Weitzmann, M. N., Kronenberg, H. M., and Pacifici, R. (2010). Disruption of PTH receptor 1 in T cells protects against PTH-induced bone loss. PLoS ONE 5, e12290.
50. Terauchi, M., Li, J. Y., Bedi, B., Baek, K. H., Tawfeek, H., Galley, S., Gilbert, L., Nanes, M. S., Zayzafoon, M., Guldberg, R., et al. (2009). T lymphocytes amplify the anabolic activity of parathyroid hormone through Wnt10b signaling. Cell Metab. 10, 229-240.
51. Tyagi, A. M., Srivastava, K., Mansoori, M. N., Trivedi, R., Chattopadhyay, N., and Singh, D. (2012). Estrogen deficiency induces the differentiation of IL-17 secreting Th17 cells: a new candidate in the pathogenesis of osteoporosis. PLoS ONE 7, e44552.
52. Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M., and Stockinger, B. (2006). TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24, 179-189.
53. Waisman, A. (2011). T helper cell populations: as flexible as the skin? Eur. J. Immunol. 41, 2539-2543.
54. Xiong, J., Piemontese, M., Thostenson, J. D., Weinstein, R. S., Manolagas, S. C., and O'Brien, C. A. (2014). Osteocyte-derived RANKL is a critical mediator of the increased bone resorption caused by dietary calcium deficiency. Bone 66, 146-154.
55. Ye, P., Rodriguez, F. H., Kanaly, S., Stocking, K. L., Schurr, J., Schwarzenberger, P., Oliver, P., Huang, W., Zhang, P., Zhang, J., et al. (2001). Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colonystimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194, 519-527.
56. Yeremenko, N., Paramarta, J. E., and Baeten, D. (2014). The interleukin-23/ interleukin-17 immune axis as a promising new target in the treatment of spondyloarthritis. Curr. Opin. Rheumatol. 26, 361-370.
57. Zepp, J., Wu, L., and Li, X. (2011). IL-17 receptor signaling and T helper 17-mediated autoimmune demyelinating disease. Trends Immunol. 32, 232-239.
58. Zhang, J., Fu, Q., Ren, Z., Wang, Y., Wang, C., Shen, T., Wang, G., and Wu, L. (2015). Changes of serum cytokines-related Th1/Th2/Th17 concentration in patients with postmenopausal osteoporosis. Gynecol. Endocrinol. 31, 183-190.