Differential regulation of osteoblast activity by Th cell subsets mediated by parathyroid hormone and IFN-γ

Journal of Immunology

Volumn 175, Issue 12, 2005, Pages 8287-8295

  Young, Nathan ^a,c   Mikhalkevich, Natallia ^a   Yan, Ying ^b   Chen, Di ^b   Zheng, Wei Ping ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; CYTOKINE; GAMMA INTERFERON; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PARATHYROID HORMONE;

ANIMAL CELL; ARTICLE; BONE MATRIX; BONE REMODELING; CELL ACTIVITY; CELL CULTURE; CELL FUNCTION; CULTURE MEDIUM; CYTOKINE PRODUCTION; ENZYME ACTIVITY; HORMONE SYNTHESIS; INFLAMMATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; TH1 CELL; TH2 CELL;

EID: 29144534586     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.12.8287     Document Type: Article

References (63)

1. Gruber, H. E. 1991. Bone and the immune system. Proc. Soc. Exp. Biol. Med. 197: 219-225.
2. Schulze-Koops, H., and J. R. Kalden. 2001. The balance of Th1/Th2 cytokines in rheumatoid arthritis. Best Pract. Res. Clin. Rheumatol. 15: 677-691.
3. Udagawa, N., S. Kotake, N. Kamatani, N. Takahashi, and T. Suda. 2002. The molecular mechanism of osteoclastogenesis in rheumatoid arthritis. Arthritis Res. 4: 281-289.
4. Manolagas, S. C. 2000. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr. Rev. 21: 115-137.
5. Whyte, M. P. 1994. Hypophosphatasia and the role of alkaline phosphatase in skeletal mineralization. Endocr. Rev. 15: 439-461.
6. Kotake, S., N. Udagawa, N. Takahashi, K. Matsuzaki, K. Itoh, S. Ishiyama, S. Saito, K. Inoue, N. Kamatani, M. T. Gillespie, 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.
7. Lacey, D. L., E. Timms, H. L. Tan, M. J. Kelley, C. R. Dunstan, T. Burgess, R. Elliott, A. Colombero, G. Elliott, S. Scully, et al. 1998. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93: 165-176.
8. Parfitt, A. M. 1994. Osteonal and hemi-osteonal remodeling: the spatial and temporal framework for signal traffic in adult human bone. J. Cell. Biochem. 55: 273-286.
9. Yasuda, H., N. Shima, N. Nakagawa, K. Yamaguchi, M. Kinosaki, S. Mochizuki, A. Tomoyasu, K. Yano, M. Goto, A. Murakami, et al. 1998. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis- inhibitory factor and is identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. USA 95: 3597-3602.
10. Aarden, E. M., E. H. Burger, and P. J. Nijweide. 1994. Function of osteocytes in bone. J. Cell. Biochem. 55: 287-299.
11. Luben, R. A., G. L. Wong, and D. V. Cohn. 1976. Biochemical characterization with parathormone and calcitonin of isolated bone cells: provisional identification of osteoclasts and osteoblasts. Endocrinology 99: 526-534.
12. Aagaard, L., G. Laible, P. Selenko, M. Schmid, R. Dorn, G. Schotta, S. Kuhfittig, A. Wolf, A. Lebersorger, P. B. Singh, et al. 1999. Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J. 18: 1923-1938.
13. Kong, Y. Y., U. Feige, I. Sarosi, B. Bolon, A. Tafuri, S. Morony, C. Capparelli, J. Li, R. Elliott, S. McCabe, et al. 1999. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402: 304-309.
14. Wong, B. R., J. Rho, J. Arron, E. Robinson, J. Orlinick, M. Chao, S. Kalachikov, E. Cayam, F. S. Bartlett III, W. N. Frankel, et al. 1997. TRANCE is a novel ligand of the tumor necrosis factor receptor family that activates c-Jun N-terminal kinase in T cells. J. Biol. Chem. 272: 25190-25194.
15. Mosmann, T. R., H. Cherwinski, M. W. Bond, M. A. Giedlin, and R. L. Coffman, 1986. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 136: 2348-2357.
16. Miltenburg, A. M., J. M. van Laar, R. de Kuiper, M. R. Daha, and F. C. Breedveld. 1992. T cells cloned from human rheumatoid synovial membrane functionally represent the Th1 subset. Scand. J. Immunol. 35: 603-610.
17. Schulze-Koops, H., P. E. Lipsky, A. F. Kavanaugh, and L. S. Davis. 1995. Elevated Th1- or Th0-like cytokine mRNA in peripheral circulation of patients with rheumatoid arthritis: modulation by treatment with anti-ICAM-1 correlates with clinical benefit. J. Immunol. 155: 5029-5037.
18. Gerli, R., O. Bistoni, A. Russano, S. Fiorucci, L. Borgato, M. E. Cesarotti, and C. Lunardi. 2002. In vivo activated T cells in rheumatoid synovitis: analysis of Th1- and Th2-type cytokine production at clonal level in different stages of disease. Clin. Exp. Immunol. 129: 549-555.
19. Guedez, Y. B., K. B. Whittington, J. L. Clayton, L. A. Joosten, F. A. van de Loo, W. B. van den Berg, and E. F. Rosloniec. 2001. Genetic ablation of interferon-7 up-regulates interleukin-1β expression and enables the elicitation of collagen-induced arthritis in a nonsusceptible mouse strain. Arthritis Rheum. 44: 2413-2424.
20. Manoury-Schwartz, B., G. Chiocchia, N. Bessis, O. Abehsira-Amar, F. Batteux, S. Muller, S. Huang, M. C. Boissier, and C. Foumier. 1997. High susceptibility to collagen-induced arthritis in mice lacking IFN-γ receptors. J. Immunol. 158: 5501-5506.
21. Ortmann, R. A., and E. M. Shevach. 2001. Susceptibility to collagen-induced arthritis: cytokine-mediated regulation. Clin. Immunol. 98: 109-118.
22. Vermeire, K., H. Heremans, M. Vandeputte, S. Huang, A. Billiau, and P. Matthys. 1997. Accelerated collagen-induced arthritis in IFN-γ receptor-deficient mice. J. Immunol. 158: 5507-5513.
23. Kaplan, C., J. C. Valdez, R. Chandrasekaran, H. Eibel, K. Mikecz, T. T. Glant, and A. Finnegan. 2002. Th1 and Th2 cytokines regulate proteoglycan-specific autoantibody isotypes and arthritis. Arthritis Res. 4: 54-58.
24. Chen, Y., E. Rosloniec, M, I. Goral, M. Boothby, and J. Chen. 2001. Redirection of T cell effector function in vivo and enhanced collagen-induced arthritis mediated by an IL-2Rβ/IL-4Rα chimeric cytokine receptor transgene. J. Immunol. 166: 4163-4169.
25. Horsfall, A. C., D. M. Butler, L. Marinova, P. J. Warden, R. O. Williams, R. N. Maini, and M. Feldmann. 1997. Suppression of collagen-induced arthritis by continuous administration of IL-4. J. Immunol. 159: 5687-5696.
26. Yoshino, S., Y. Murata, and M. Ohsawa. 1998. Successful induction of adjuvant arthritis in mice by treatment with a monoclonal antibody against IL-4. J. Immunol. 161: 6904-6908.
27. Hollo, K., T. T. Glant, M. Garzo, A. Finnegan, K. Mikecz, and E. Buzas. 2000. Complex pattern of Th1 and Th2 activation with a preferential increase of autoreactive Th1 cells in BALB/c mice with proteoglycan (aggrecan)-induced arthritis. Clin. Exp. Immunol. 120: 167-173.
28. Lee, D. M., D. S. Friend, M. F. Gurish, C. Benoist, D. Mathis, and M. B. Brenner. 2002. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 297: 1689-1692.
29. Matsumoto, I., A. Staub, C. Benoist, and D. Mathis. 1999. Arthritis provoked by linked T and B cell recognition of a glycolytic enzyme. Science 286: 1732-1735.
30. Terato, K., K. A. Hasty, R. A. Reife, M. A. Cremer, A. H. Kang, and J. M. Stuart, 1992. Induction of arthritis with monoclonal antibodies to collagen. J. Immunol. 148: 2103-2108.
31. Chen, N. J., M. W. Huang, and S. L. Hsieh. 2001. Enhanced secretion of IFN-γ by activated Th1 cells occurs via reverse signaling through TNF-related activation-induced cytokine. J. Immunol. 166: 270-276.
32. Takayanagi, H., K. Ogasawara, S. Hida, T. Chiba, S. Murata, K. Sato, A. Takaoka, T. Yokochi, H. Oda, K. Tanaka, et al. 2000. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-γ. Nature 408: 600-605.
33. Lubberts, E., L. A. Joosten, M. Chabaud, L. van Den Bersselaar, B. Oppers, C. J. Coenen-De Roo, C. D. Richards, P. Miossec, and W. B. van Den Berg. 2000. IL-4 gene therapy for collagen arthritis suppresses synovial IL-17 and osteoprotegerin ligand and prevents bone erosion. J. Clin. Invest. 105: 1697-1710.
34. Onoe, Y., C, Miyaura, T. Kaminakayashiki, Y. Nagai, K. Noguchi, Q. R. Chen, H. Seo, H. Ohta, S. Nozawa, I. Kudo, and T. Suda. 1996. IL-13 and IL-4 inhibit bone resorption by suppressing cyclooxygenase-2-dependent prostaglandin synthesis in osteoblasts. J. Immunol. 156: 758-764.
35. Zheng, W.-p., and R. A. Flavell. 1997. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89:587-596.
36. Zheng, W. P., Q. Zhao, X. Zhao, B. Li, M. Hubank, D. G. Schatz, and R. A. Flavell. 2004. Up-regulation of Hlx in immature Th cells induces IFN-γ expression. J. Immunol. 172: 114-122.
37. Reiner, S. L., S. Zheng, D. B. Corry, and R. M. Locksley. 1993. Constructing polycompetitor cDNAs for quantitative PCR. [Published errata appear in 1994 J. Immunol. Methods 173:133 and 175:275.] J. Immunol. Methods 165: 37-46.
38. Reiner, S. L., S. Zheng, D. B. Corry, and R. M. Locksley. 1994. Constructing polycompetitor cDNAs for quantitative PCR (J. Immunol. Methods 165 (1993) 37-46: 173(1994) 133). J. Immunol. Methods 175: 275.
39. -ΔΔCT method. Methods 25: 402-408.
40. Bost, K. L., W. K. Ramp, N. C. Nicholson, J. L. Bento, I. Marriott, and M. C. Hudson. 1999. Staphylococcus aureus infection of mouse or human osteoblasts induces high levels of interleukin-6 and interleukin-12 production. J. Infect. Dis. 180: 1912-1920.
41. Ouyang, W., S. H. Ranganath, K. Weindel, D. Bhattacharya, T. L. Murphy, W. C. Sha, and K. M. Murphy. 1998, Inhibition of Th1 development mediated by GATA-3 through an IL-4-independent mechanism. Immunity 9: 745-755.
42. Pai, S. Y., M. L. Truitt, and I. C. Ho. 2004. GATA-3 deficiency abrogates the development and maintenance of T helper type 2 cells. Proc. Natl. Acad. Sci. USA 101: 1993-1998.
43. H2 responses. Nat. Immunol. 5: 1157-1165.
44. Muroya, K., T. Hasegawa, Y. Ito, T. Nagai, H. Isotani, Y. Iwata, K. Yamamoto, S. Fujimoto, S. Seishu, Y. Fukushima, et al. 2001. GATA3 abnormalities and the phenotypic spectrum of HDR syndrome. J. Med. Genet. 38: 374-380.
45. Nesbit, M. A., M. R. Bowl, B. Harding, A. Ali, A. Ayala, C. Crowe, A. Dobbie, G. Hampson, I. Holdaway, M. A. Levine, et al. 2004. Characterization of GATA3 mutations in the hypoparathyroidism, deafness, and renal dysplasia (HDR) syndrome. J. Biol. Chem. 279: 22624-22634.
46. Van Esch, H., P. Groenen, M. A. Nesbit, S. Schuffenhauer, P. Lichtner, G. Vanderlinden, B. Harding, R. Beetz, R. W. Bilous, I. Holdaway, et al. 2000. GATA3 haplo-insufficiency causes human HDR syndrome. Nature 406: 419-422.
47. + T cells. J. Immunol. 158: 1085-1094.
48. lo thymocytes in vivo. Science 250: 1720-1723.
49. Silver, J., and H. M. Kronenberg. 1996. Parathyroid hormone-molecular biology and regulation. In Bone Biology. J. P. Bilezikian, L. G. Raisz, and G. A. Rodan, eds. Academic, New York, pp. 325-346.
50. Neer, R. M., C. D. Arnaud, J. R. Zanchetta, R. Prince, G. A. Gaich, J. Y. Reginster, A. B. Hodsman, E. F. Eriksen, S. Ish-Shalom, H. K. Genant, et al. 2001. Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N. Engl. J. Med. 344: 1434-1441.
51. Hukkanen, M., F. J. Hughes, L. D. Buttery, S. S. Gross, T. J. Evans, S. Seddon, V. Riveros-Moreno, I. MacIntyre, and J. M. Polak. 1995. Cytokine-stimulated expression of inducible nitric oxide synthase by mouse, rat, and human osteoblast-like cells and its functional role in osteoblast metabolic activity. Endocrinology 136: 5445-5453.
52. Candeliere, G. A., F. Liu, and J. E. Aubin. 2001. Individual osteoblasts in the developing calvaria express different gene repertoires. Bone 28: 351-361.
53. Bogdanovic, Z., Y. F. Huang, M. Dodig, S. H. Clark, A. C. Lichtler, and B. E. Kream. 2000. Parathyroid hormone inhibits collagen synthesis and the activity of rat col1a1 transgenes mainly by a cAMP-mediated pathway in mouse calvariae. J. Cell. Biochem. 77: 149-158.
54. Lee, S. K., and J. A. Lorenzo. 1999. Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation. Endocrinology 140: 3552-3561.
55. Horwood, N. J., J. Elliott, T. J. Martin, and M. T. Gillespie. 1998. Osteotropic agents regulate the expression of osteoclast differentiation factor and osteoprotegerin in osteoblastic stromal cells. Endocrinology 139: 4743-4746.
56. Locklin, R. M., S. Khosla, R. T. Turner, and B. L. Riggs. 2003. Mediators of the biphasic responses of bone to intermittent and continuously administered parathyroid hormone. J. Cell Biochem. 89: 180-190.
57. Tam, C. S., J. N. Heersche, T. M. Murray, and J. A. Parsons. 1982. Parathyroid hormone stimulates the bone apposition rate independently of its resorptive action: differential effects of intermittent and continuous administration. Endocrinology 110: 506-512.
58. Qin, L., L. J. Raggatt, and N. C. Partridge. 2004. Parathyroid hormone: a double-edged sword for bone metabolism. Trends Endocrinol. Metab. 15: 60-65.
59. Dempster, D., C. Hughes-Gegos, K. Plavetic-Chee, A. Brandao-Burch, F. Cosman, J. Nieves, S. Neubort, S. Lu, A. Iida-Klein, T. Arnett, and R. Lindsay. 2005. Normal human osteoclasts formed from peripheral blood monocytes express PTH type I receptors and are stimulated by PTH in the absence of osteoblasts. J. Cell. Biochem. 95: 139-148.
60. Halladay, D. L., R. R. Miles, K. Thirunavukkarasu, S. Chandrasekhar, T. J. Martin, and J. E. Onyia. 2001. Identification of signal transduction pathways and promoter sequences that mediate parathyroid hormone 1-38 inhibition of osteoprotegerin gene expression. J. Cell. Biochem. 84: 1-11.
61. Kanzawa, M., T. Sugimoto, M. Kanatani, and K. Chihara. 2000. Involvement of osteoprotegerin/osteoclastogenesis inhibitory factor in the stimulation of osteoclast formation by parathyroid hormone in mouse bone cells. Eur. J. Endocrinology 142: 661-664.
62. Debacker, C., M. Catala, and M. C. Labastie. 1999. Embryonic expression of the human GATA-3 gene. Mech. Dev. 85: 183-187.
63. Stock, J. L., J. A. Coderre, W. J. DeVito, and S. Baker. 1998, Effects of human lymphocyte-conditioned medium on MG-63 human osteosarcoma cell function. Cytokine 10: 603-612.