Disruption of PTH receptor 1 in t cells protects against PTH-induced bone loss

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Tawfeek, Hesham ^a   Bedi, Brahmchetna ^a   Li, Jau Yi ^a   Adams, Jonathan ^a   Kobayashi, Tatsuya ^c   Weitzmann, M Neale ^a,d   Kronenberg, Henry M ^c   Pacifici, Roberto ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C PEPTIDE; CD40 ANTIGEN; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE RECEPTOR 1; PROTEIN KINASE LCK; TUMOR NECROSIS FACTOR ALPHA; OSTEOPROTEGERIN; PARATHYROID HORMONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; BONE MASS; CATABOLISM; CELL DIFFERENTIATION; CELL DISRUPTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE SILENCING; HOMOZYGOSITY; MORPHOMETRICS; MOUSE; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRABECULAR BONE; UPREGULATION; ANIMAL; BIOSYNTHESIS; BONE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; OSTEOBLAST; OSTEOCLAST; PATHOLOGY; STROMA CELL;

MUS;

ANIMALS; BONE AND BONES; BONE RESORPTION; FEMALE; GENE SILENCING; HUMANS; MALE; MICE; OSTEOBLASTS; OSTEOCLASTS; OSTEOPROTEGERIN; PARATHYROID HORMONE; RANK LIGAND; RECEPTOR, PARATHYROID HORMONE, TYPE 1; SIGNAL TRANSDUCTION; STROMAL CELLS; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77957891185     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012290     Document Type: Article

References (49)

1. Riggs BL, Melton LJ, 3rd (1986) Involutional osteoporosis. N Engl J Med 314: 1676-1686.
2. Grey AB, Stapleton JP, Evans MC, Reid IR (1996) Accelerated bone loss in postmenopausal women with mild primary hyperparathyroidism. Clin Endocrinol (Oxf) 44: 697-702.
3. Parisien M, Dempster DW, Shane E, Bilezikian JP (2001) Histomorphometric analysis of bone in primary hyperparathyroidism. The parathyroids Basic and clinical concepts. San Diego: Academic Press. pp 423-436.
4. Potts J (1998) Primary hyperparathyroidism. In: Avioli LV, Krane S, eds. Metabolic Bone Diseases. #rd ed. San Diego: Academic Press. pp 411-442.
5. Silverberg SJ, Shane E, de la Cruz L, Dempster DW, Feldman F, et al. (1989) Skeletal disease in primary hyperparathyroidism. J Bone Miner Res 4: 283-291.
6. Zaidi M (2007) Skeletal remodeling in health and disease. Nat Med 13: 791-801.
7. Canalis E, Giustina A, Bilezikian JP (2007) Mechanisms of anabolic therapies for osteoporosis. N Engl J Med 357: 905-916.
8. Iida-Klein A, Lu SS, Kapadia R, Burkhart M, Moreno A, et al. (2005) Shortterm 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.
9. Lotinun S, Evans GL, Bronk JT, Bolander ME, Wronski TJ, et al. (2004) Continuous parathyroid hormone induces cortical porosity in the rat: effects on bone turnover and mechanical properties. J Bone Miner Res 19: 1165-1171.
10. Hock JM, Gera I (1992) Effects of continuous and intermittent administration and inhibition of resorption on the anabolic response of bone to parathyroid hormone. J Bone Miner Res 7: 65-72.
11. Gao Y, Wu X, Terauchi M, Li JY, Grassi F, et al. (2008) T cells potentiate PTHinduced cortical bone loss through CD40L signaling. Cell Metab 8: 132-145.
12. Dempster DW, Parisien M, Silverberg SJ, Liang XG, Schnitzer M, et al. (1999) On the mechanism of cancellous bone preservation in postmenopausal women with mild primary hyperparathyroidism. J Clin Endocrinol Metab 84: 1562-1566.
13. Qin L, Raggatt LJ, Partridge NC (2004) Parathyroid hormone: a double-edged sword for bone metabolism. Trends Endocrinol Metab 15: 60-65.
14. Calvi LM, Sims NA, Hunzelman JL, Knight MC, Giovannetti A, et al. (2001) Activated parathyroid hormone/parathyroid hormone-related protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. J Clin Invest 107: 277-286.
15. Lanske B, Amling M, Neff L, Guiducci J, Baron R, et al. (1999) Ablation of the PTHrP gene or the PTH/PTHrP receptor gene leads to distinct abnormalities in bone development. J Clin Invest 104: 399-407.
16. Ma YL, Cain RL, Halladay DL, Yang X, Zeng Q, et al. (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.
17. Weir EC, Lowik CW, Paliwal I, Insogna KL (1996) Colony stimulating factor-1 plays a role in osteoclast formation and function in bone resorption induced by parathyroid hormone and parathyroid hormone-related protein. J Bone Miner Res 11: 1474-1481.
18. McCauley LK, Rosol TJ, Merryman JI, Capen CC (1992) Parathyroid hormone-related protein binding to human T-cell lymphotropic virus type Iinfected lymphocytes. Endocrinology 130: 300-306.
19. Terauchi M, Li JY, Bedi B, Baek KH, Tawfeek H, et al. (2009) T lymphocytes amplify the anabolic activity of parathyroid hormone through Wnt10b signaling. Cell Metab 10: 229-240.
20. Young N, Mikhalkevich N, Yan Y, Chen D, Zheng WP (2005) Differential regulation of osteoblast activity by Th cell subsets mediated by parathyroid hormone and IFN-gamma. J Immunol 175: 8287-8295.
21. Geffner ME, Bersch N, Cortez AB, Bailey RC, Golde DW (1995) Growthpromoting actions of parathyroid hormone, adrenocorticotrophic hormone, and thyroid-stimulating hormone: in vitro studies in normal and pygmy Tlymphoblast cell lines. Pediatr Res 37: 507-511.
22. Stojceva-Taneva O, Fadda GZ, Smogorzewski M, Massry SG (1993) Parathyroid hormone increases cytosolic calcium of thymocytes. Nephron 64: 592-599.
23. Ahuja SS, Zhao S, Bellido T, Plotkin LI, Jimenez F, et al. (2003) 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 144: 1761-1769.
24. Hory BG, Roussanne MC, Rostand S, Bourdeau A, Drueke TB, et al. (2000) 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 23: 273-279.
25. Kobayashi T, Chung UI, Schipani E, Starbuck M, Karsenty G, et al. (2002) PTHrP and Indian hedgehog control differentiation of growth plate chondrocytes at multiple steps. Development 129: 2977-2986.
26. Lee PP, Fitzpatrick DR, Beard C, Jessup HK, Lehar S, et al. (2001) A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15: 763-774.
27. Brodt MD, Ellis CB, Silva MJ (1999) Growing C57Bl/6 mice increase whole bone mechanical properties by increasing geometric and material properties. J Bone Miner Res 14: 2159-2166.
28. Pacifici R (2010) T cells: Critical bone regulators in health and disease. Bone.
29. 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.
30. Eichinger A, Fiaschi-Taesch N, Massfelder T, Fritsch S, Barthelmebs M, et al. (2002) Transcript expression of the tuberoinfundibular peptide (TIP)39/PTH2 receptor system and non-PTH1 receptor-mediated tonic effects of TIP39 and other PTH2 receptor ligands in renal vessels. Endocrinology 143: 3036-3043.
31. Hoare SR, Clark JA, Usdin TB (2000) Molecular determinants of tuberoinfundibular peptide of 39 residues (TIP39) selectivity for the parathyroid hormone-2 (PTH2) receptor. N-terminal truncation of TIP39 reverses PTH2 receptor/ PTH1 receptor binding selectivity. J Biol Chem 275: 27274-27283.
32. Usdin TB, Hoare SR, Wang T, Mezey E, Kowalak JA (1999) TIP39: a new neuropeptide and PTH2-receptor agonist from hypothalamus. Nat Neurosci 2: 941-943.
33. Divieti P, Geller AI, Suliman G, Juppner H, Bringhurst FR (2005) Receptors specific for the carboxyl-terminal region of parathyroid hormone on bonederived cells: determinants of ligand binding and bioactivity. Endocrinology 146: 1863-1870.
34. Bellido T, Ali AA, Gubrij I, Plotkin LI, Fu Q, et al. (2005) Chronic elevation of parathyroid hormone in mice reduces expression of sclerostin by osteocytes: a novel mechanism for hormonal control of osteoblastogenesis. Endocrinology 146: 4577-4583.
35. O'Brien CA, Plotkin LI, Galli C, Goellner JJ, Gortazar AR, et al. (2008) Control of bone mass and remodeling by PTH receptor signaling in osteocytes. PLoS ONE 3: e2942.
36. Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, et al. (2005) Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci U S A 102: 3324-3329.
37. Kimble RB, Srivastava S, Ross FP, Matayoshi A, Pacifici R (1996) 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 271: 28890-28897.
38. Galli C, Fu Q, Wang W, Olsen BR, Manolagas SC, et al. (2009) Commitment to the osteoblast lineage is not required for RANKL gene expression. J Biol Chem 284: 12654-12662.
39. Tanaka Y, Maruo A, Fujii K, Nomi M, Nakamura T, et al. (2000) Intercellular adhesion molecule 1 discriminates functionally different populations of human osteoblasts: characteristic involvement of cell cycle regulators. J Bone Miner Res 15: 1912-1923.
40. Everts V, Delaisse JM, Korper W, Jansen DC, Tigchelaar-Gutter W, et al. (2002) The bone lining cell: its role in cleaning Howship's lacunae and initiating bone formation. J Bone Miner Res 17: 77-90.
41. Weitzmann MN, Pacifici R (2006) Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 116: 1186-1194.
42. Grey A, Mitnick MA, Shapses S, Ellison A, Gundeberg C, et al. (1996) Circulating levels of Intreleukin-6 and tumor necrosis factor α are elevated in primary hyperparathyroidism and correlate with markers of bone resorption. JClinEndoMetab 81: 3450-3468.
43. Cenci S, Weitzmann MN, Roggia C, Namba N, Novack D, et al. (2000) Estrogen deficiency induces bone loss by enhancing T-cell production of TNFalpha. J Clin Invest 106: 1229-1237.
44. Lam J, Takeshita S, Barker JE, Kanagawa O, Ross FP, et al. (2000) TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J Clin Invest 106: 1481-1488.
45. Khosla S (2001) Minireview: the OPG/RANKL/RANK system. Endocrinology 142: 5050-5055.
46. Corbi AL, Lopez-Rodriguez C (1997) CD11c integrin gene promoter activity during myeloid differentiation. Leuk Lymphoma 25: 415-425.
47. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, et al. (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2: 595-610.
48. Grassi F, Tell G, Robbie-Ryan M, Gao Y, Terauchi M, et al. (2007) Oxidative stress causes bone loss in estrogen-deficient mice through enhanced bone marrow dendritic cell activation. Proc Natl Acad Sci U S A 104: 15087-15092.
49. 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.