Targeting of the osteoclastogenic RANKL-RANK axis prevents osteoporotic bone loss and soft tissue calcification in coxsackievirus B3-infected mice

Journal of Immunology

Volumn 190, Issue 4, 2013, Pages 1623-1630

  Lee, Kyunghee ^a   Kim, Hyunsoo ^a,g   Park, Ho Sun ^a   Kim, Keuk Jun ^b   Song, Hoogeun ^c   Shin, Hong In ^d   Kim, Han Sung ^e   Seo, Donghyun ^e   Kook, Hyun ^f   Ko, Jeong Hyeon ^f   Jeong, Daewon ^a  

^a Yeungnam University College of Medicine   (South Korea)

^b TaeKyeung University   (South Korea)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^d Kyungpook National University   (South Korea)

^e Yonsei University Wonju   (South Korea)

^f Chonnam National University Medical School   (South Korea)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; BONE MORPHOGENETIC PROTEIN 2; CALCIUM; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; DECAY ACCELERATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEONECTIN; OSTEOPROTEGERIN; PHOSPHATE; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; RECOMBINANT PROTEIN; RECOMBINANT RECEPTOR ACTIVATOR OF NF KAPPA B FC FUSION PROTEIN; TARTRATE RESISTANT ACID PHOSPHATASE 5B; TRANSCRIPTION FACTOR FRA 1; TRANSCRIPTION FACTOR RUNX2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DESTRUCTION; BONE DEVELOPMENT; CALCIFICATION; CALCIUM DEPLETION; CARDIAC FIBROBLAST CALCIFICATION; CELL COUNT; CONTROLLED STUDY; COXSACKIE VIRUS INFECTION; CYTOKINE PRODUCTION; HEART CALCIFICATION; IMMUNE RESPONSE; IN VITRO STUDY; INTRACELLULAR SIGNALING; LUNG CALCIFICATION; MALE; MOLECULAR PATHOLOGY; MOUSE; NEWBORN; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLASTOGENESIS; OSTEOPOROSIS; PANCREAS CALCIFICATION; PHOSPHATE BLOOD LEVEL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN TARGETING; RAT; SOFT TISSUE CALCIFICATION; TISSUE DISTRIBUTION; UPREGULATION;

ANIMALS; CALCINOSIS; COXSACKIEVIRUS INFECTIONS; DISEASE MODELS, ANIMAL; HELA CELLS; HUMANS; MALE; MICE; MICE, INBRED BALB C; OSSIFICATION, HETEROTOPIC; OSTEOBLASTS; OSTEOCLASTS; OSTEOPOROSIS; RANK LIGAND; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RECOMBINANT FUSION PROTEINS;

EID: 84873545703     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201479     Document Type: Article

References (49)

1. Peacock, M. 2010. Calcium metabolism in health and disease. Clin. J. Am. Soc. Nephrol. 5(Suppl 1): S23-S30.
2. Zaidi, M. 2007. Skeletal remodeling in health and disease. Nat. Med. 13: 791-801.
3. Boskey, A. L., and R. Coleman. 2010. Aging and bone. J. Dent. Res. 89: 1333-1348.
4. Robinson, L. J., H. C. Blair, J. B. Barnett, M. Zaidi, and C. L. Huang. 2010. Regulation of bone turnover by calcium-regulated calcium channels. Ann. N. Y. Acad. Sci. 1192: 351-357.
5. Murshed, M., and M. D. McKee. 2010. Molecular determinants of extracellular matrix mineralization in bone and blood vessels. Curr. Opin. Nephrol. Hypertens. 19: 359-365.
6. Kirsch, T. 2006. Determinants of pathological mineralization. Curr. Opin. Rheumatol. 18: 174-180.
7. Esfandiarei, M., and B. M. McManus. 2008. Molecular biology and pathogenesis of viral myocarditis. Annu. Rev. Pathol. 3: 127-155.
8. Mena, I., C. M. Perry, S. Harkins, F. Rodriguez, J. Gebhard, and J. L. Whitton. 1999. The role of B lymphocytes in coxsackievirus B3 infection. Am. J. Pathol. 155: 1205-1215.
9. Chatterjee, N. K., D. W. Moore, S. S. Monroe, R. I. Glass, M. J. Cambridge, S. F. Kondracki, and D. L. Morse. 2004. Molecular epidemiology of outbreaks of viral gastroenteritis in New York State, 1998-1999. Clin. Infect. Dis. 38(Suppl 3): S303-S310.
10. Monto, A. S., A. M. Fendrick, and M. W. Sarnes. 2001. Respiratory illness caused by picornavirus infection: a review of clinical outcomes. Clin. Ther. 23: 1615-1627.
11. Muir, P., and A. M. van Loon. 1997. Enterovirus infections of the central nervous system. Intervirology 40: 153-166.
12. Oka, K., K. Oohira, Y. Yatabe, T. Tanaka, K. Kurano, R. Kosugi, M. Murata, H. Hakozaki, T. Nishikawa, and Y. Tsutsumi. 2005. Fulminant myocarditis demonstrating uncommon morphology-α report of two autopsy cases. Virchows Arch. 446: 259-264.
13. Konen, O., V. Rathaus, S. Bauer, T. Dolfin, and M. Shapiro. 2000. Progressive liver calcifications in neonatal coxsackievirus infection. Pediatr. Radiol. 30: 343-345.
14. Seko, Y., Y. Shinkai, A. Kawasaki, H. Yagita, K. Okumura, F. Takaku, and Y. Yazaki. 1991. Expression of perforin in infiltrating cells in murine hearts with acute myocarditis caused by coxsackievirus B3. Circulation 84: 788-795.
15. Lane, J. R., D. A. Neumann, A. Lafond-Walker, A. Herskowitz, and N. R. Rose. 1992. Interleukin 1 or tumor necrosis factor can promote Coxsackie B3-induced myocarditis in resistant B10.A mice. J. Exp. Med. 175: 1123-1129.
16. Fairweather, D., S. Frisancho-Kiss, S. Gatewood, D. Njoku, R. Steele, M. Barrett, and N. R. Rose. 2004. Mast cells and innate cytokines are associated with susceptibility to autoimmune heart disease following coxsackievirus B3 infection. Autoimmunity 37: 131-145.
17. Persy, V., and P. D'Haese. 2009. Vascular calcification and bone disease: the calcification paradox. Trends Mol. Med. 15: 405-416.
18. Hyder, J. A., M. A. Allison, M. H. Criqui, and C. M. Wright. 2007. Association between systemic calcified atherosclerosis and bone density. Calcif. Tissue Int. 80: 301-306.
19. Schulz, E., K. Arfai, X. Liu, J. Sayre, and V. Gilsanz. 2004. Aortic calcification and the risk of osteoporosis and fractures. J. Clin. Endocrinol. Metab. 89: 4246-4253.
20. Price, P. A., S. A. Faus, and M. K. Williamson. 2001. Bisphosphonates alendronate and ibandronate inhibit artery calcification at doses comparable to those that inhibit bone resorption. Arterioscler. Thromb. Vasc. Biol. 21: 817-824.
21. Callister, T. Q., P. Raggi, B. Cooil, N. J. Lippolis, and D. J. Russo. 1998. Effect of HMG-CoA reductase inhibitors on coronary artery disease as assessed by electron-beam computed tomography. N. Engl. J. Med. 339: 1972-1978.
22. Edwards, C. J., D. J. Hart, and T. D. Spector. 2000. Oral statins and increased bone-mineral density in postmenopausal women. Lancet 355: 2218-2219.
23. Sordillo, E. M., and R. N. Pearse. 2003. RANK-Fc: a therapeutic antagonist for RANK-L in myeloma. Cancer 97(Suppl): 802-812.
24. Kee, H. J., G. H. Eom, H. Joung, S. Shin, J. R. Kim, Y. K. Cho, N. Choe, B.W. Sim, D. Jo, M. H. Jeong, et al. 2008. Activation of histone deacetylase 2 by inducible heat shock protein 70 in cardiac hypertrophy. Circ. Res. 103: 1259-1269.
25. Kim, H., H. J. Kim, K. Lee, J. M. Kim, H. S. Kim, J. R. Kim, C. M. Ha, Y. K. Choi, S. J. Lee, J. Y. Kim, et al. 2012. α-Lipoic acid attenuates vascular calcification via reversal of mitochondrial function and restoration of Gas6/Axl/Akt survival pathway. J. Cell. Mol. Med. 16: 273-286.
26. Shafren, D. R., D. T. Williams, and R. D. Barry. 1997. A decay-accelerating factor-binding strain of coxsackievirus B3 requires the coxsackievirusadenovirus receptor protein to mediate lytic infection of rhabdomyosarcoma cells. J. Virol. 71: 9844-9848.
27. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275: 1320-1323.
28. Shi, Y., C. Chen, U. Lisewski, U. Wrackmeyer, M. Radke, D. Westermann, M. Sauter, C. Tschöpe, W. Poller, K. Klingel, and M. Gotthardt. 2009. Cardiac deletion of the Coxsackievirus-adenovirus receptor abolishes Coxsackievirus B3 infection and prevents myocarditis in vivo. J. Am. Coll. Cardiol. 53: 1219-1226.
29. Halleen, J. M., S. L. Alatalo, H. Suominen, S. Cheng, A. J. Janckila, and H. K. Väänänen. 2000. Tartrate-resistant acid phosphatase 5b: a novel serum marker of bone resorption. J. Bone Miner. Res. 15: 1337-1345.
30. 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.
31. Reynolds, J. L., A. J. Joannides, J. N. Skepper, R. McNair, L. J. Schurgers, D. Proudfoot, W. Jahnen-Dechent, P. L. Weissberg, and C. M. Shanahan. 2004. Human vascular smooth muscle cells undergo vesicle-mediated calcification in response to changes in extracellular calcium and phosphate concentrations: a potential mechanism for accelerated vascular calcification in ESRD. J. Am. Soc. Nephrol. 15: 2857-2867.
32. Panizo, S., A. Cardus, M. Encinas, E. Parisi, P. Valcheva, S. López-Ongil, B. Coll, E. Fernandez, and J. M. Valdivielso. 2009. RANKL increases vascular smooth muscle cell calcification through a RANK-BMP4-dependent pathway. Circ. Res. 104: 1041-1048.
33. Hofbauer, L. C., C. C. Brueck, C. M. Shanahan, M. Schoppet, and H. Dobnig. 2007. Vascular calcification and osteoporosis-from clinical observation towards molecular understanding. Osteoporos. Int. 18: 251-259.
34. Chan, E. D., D. V. Morales, C. H. Welsh, M. T. McDermott, and M. I. Schwarz. 2002. Calcium deposition with or without bone formation in the lung. Am. J. Respir. Crit. Care Med. 165: 1654-1669.
35. Abedin, M., Y. Tintut, and L. L. Demer. 2004. Vascular calcification: mechanisms and clinical ramifications. Arterioscler. Thromb. Vasc. Biol. 24: 1161-1170.
36. Tintut, Y., J. Patel, F. Parhami, and L. L. Demer. 2000. Tumor necrosis factoralpha promotes in vitro calcification of vascular cells via the cAMP pathway. Circulation 102: 2636-2642.
37. Giachelli, C. M. 2004. Vascular calcification mechanisms. J. Am. Soc. Nephrol. 15: 2959-2964.
38. Delany, A. M., I. Kalajzic, A. D. Bradshaw, E. H. Sage, and E. Canalis. 2003. Osteonectin-null mutation compromises osteoblast formation, maturation, and survival. Endocrinology 144: 2588-2596.
39. Tanaka, T., H. Sato, H. Doi, C. A. Yoshida, T. Shimizu, H. Matsui, M. Yamazaki, H. Akiyama, K. Kawai-Kowase, T. Iso, et al. 2008. Runx2 represses myocardinmediated differentiation and facilitates osteogenic conversion of vascular smooth muscle cells. Mol. Cell. Biol. 28: 1147-1160.
40. Nakagawa, Y., K. Ikeda, Y. Akakabe, M. Koide, M. Uraoka, K. T. Yutaka, R. Kurimoto-Nakano, T. Takahashi, S. Matoba, H. Yamada, et al. 2010. Paracrine osteogenic signals via bone morphogenetic protein-2 accelerate the atherosclerotic intimal calcification in vivo. Arterioscler. Thromb. Vasc. Biol. 30: 1908-1915.
41. Jochum, W., J. P. David, C. Elliott, A. Wutz, H. Plenk, Jr., K. Matsuo, and E. F. Wagner. 2000. Increased bone formation and osteosclerosis in mice overexpressing the transcription factor Fra-1. Nat. Med. 6: 980-984.
42. Ilbäck, N. G., L. Wesslén, K. Pauksen, T. Sta°lhandske, G. Friman, and J. Fohlman. 1993. Effects of the antiviral WIN 54954 and the immune modulator LS 2616 on cachectin/TNF and gamma-interferon responses during viral heart disease. Scand. J. Infect. Dis. Suppl. 88: 117-123.
43. 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.
44. Jimi, E., I. Nakamura, T. Ikebe, S. Akiyama, N. Takahashi, and T. Suda. 1998. Activation of NF-kappaB is involved in the survival of osteoclasts promoted by interleukin-1. J. Biol. Chem. 273: 8799-8805.
45. Boyle, W. J., W. S. Simonet, and D. L. Lacey. 2003. Osteoclast differentiation and activation. Nature 423: 337-342.
46. Lam, J., S. Takeshita, J. E. Barker, O. Kanagawa, F. P. Ross, and S. L. Teitelbaum. 2000. TNF-alpha induces osteoclastogenesis by direct stimulation of macrophages exposed to permissive levels of RANK ligand. J. Clin. Invest. 106: 1481-1488.
47. Kudo, O., Y. Fujikawa, I. Itonaga, A. Sabokbar, T. Torisu, and N. A. Athanasou. 2002. Proinflammatory cytokine (TNFalpha/IL-1alpha) induction of human osteoclast formation. J. Pathol. 198: 220-227.
48. Bucay, N., I. Sarosi, C. R. Dunstan, S. Morony, J. Tarpley, C. Capparelli, S. Scully, H. L. Tan, W. Xu, D. L. Lacey, et al. 1998. osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 12: 1260-1268.
49. Helas, S., C. Goettsch, M. Schoppet, U. Zeitz, U. Hempel, H. Morawietz, P. J. Kostenuik, R. G. Erben, and L. C. Hofbauer. 2009. Inhibition of receptor activator of NF-kappaB ligand by denosumab attenuates vascular calcium deposition in mice. Am. J. Pathol. 175: 473-478.