Arthritogenic alphaviruses: New insights into arthritis and bone pathology

Trends in Microbiology

Volumn 23, Issue 1, 2015, Pages 35-43

  Chen, Weiqiang ^a   Foo, Suan Sin ^a   Sims, Natalie A ^b   Herrero, Lara J ^a   Walsh, Nicole C ^b   Mahalingam, Suresh ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Alphavirus; Arthritis; Bone loss; Chikungunya virus; Inflammation; Ross river virus

Indexed keywords

ADALIMUMAB; C REACTIVE PROTEIN; CYTOKINE ANTIBODY; DENOSUMAB; EOTAXIN; ETANERCEPT; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INFLIXIMAB; INTERLEUKIN 10; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 3; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; RANTES; REACTIVE NITROGEN SPECIES; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TOCILIZUMAB; TUMOR NECROSIS FACTOR ALPHA; TNFRSF11A PROTEIN, HUMAN;

AGE; ALPHAVIRUS INFECTION; ARTHRALGIA; ARTHROPATHY; BONE EROSION; CHIKUNGUNYA; CHIKUNGUNYA ALPHAVIRUS; DISEASE EXACERBATION; EPIDEMIC; HUMAN; INFECTION PREVENTION; INFECTIOUS ARTHRITIS; INNATE IMMUNITY; MACROPHAGE; NONHUMAN; OSTEOLYSIS; PROTEIN TARGETING; REVIEW; RHEUMATOID ARTHRITIS; RISK FACTOR; ROSS RIVER ALPHA VIRUS; ROSS RIVER VIRUS INFECTION; T LYMPHOCYTE ACTIVATION; TH17 CELL; VIRUS REPLICATION; ALPHAVIRUS; ANIMAL; COMPLICATION; DISEASE MODEL; ETIOLOGY; GENETICS; IMMUNOLOGY; INFLAMMATION; PATHOLOGY; VIROLOGY;

ALPHAVIRUS; CHIKUNGUNYA VIRUS; ROSS RIVER VIRUS;

ALPHAVIRUS; ANIMALS; ARTHRITIS, INFECTIOUS; BONE RESORPTION; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION; INTERLEUKIN-17; INTERLEUKIN-6; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; RISK FACTORS; TH17 CELLS;

EID: 84920522431     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2014.09.005     Document Type: Review

References (104)

1. Zacks M.A., Paessler S. Encephalitic alphaviruses. Vet. Microbiol. 2010, 140:281-286.
2. Rulli N., et al. The molecular and cellular aspects of arthritis due to alphavirus infections: lesson learned from Ross River virus. Ann. N. Y. Acad. Sci. 2007, 1102:96-108.
3. Suhrbier A., La Linn M. Clinical and pathologic aspects of arthritis due to Ross River virus and other alphaviruses. Curr. Opin. Rheumatol. 2004, 16:374-379.
4. Kiwanuka N., et al. O'nyong-nyong fever in south-central Uganda, 1996-1997: clinical features and validation of a clinical case definition for surveillance purposes. Clin. Infect. Dis. 1999, 29:1243-1250.
5. Laine M., et al. Sindbis viruses and other alphaviruses as cause of human arthritic disease. J. Intern. Med. 2004, 256:457-471.
6. Munoz M., Navarro J.C. Mayaro: a re-emerging arbovirus in Venezuela and Latin America. Biomedica 2012, 32:286-302. (in Spanish).
7. Phillips D.A., et al. Clinical and subclinical Barmah Forest virus infection in Queensland. Med. J. Aust. 1990, 152:463-466.
8. Paquet C., et al. Chikungunya outbreak in Reunion: epidemiology and surveillance, 2005 to early January 2006. Euro Surveill. 2006, 11:E060202-E060203.
9. Suhrbier A., Mahalingam S. The immunobiology of viral arthritides. Pharmacol. Ther. 2009, 124:301-308.
10. Parida M.M. Rapid and real-time detection technologies for emerging viruses of biomedical importance. J. Biosci. 2008, 33:617-628.
11. Aoyama I., et al. A case of chikungunya fever imported from India to Japan, follow-up of specific IgM and IgG antibodies over a 6-month period. Jpn. J. Infect. Dis. 2010, 63:65-66.
12. Robinson M.C. An epidemic of virus disease in Southern Province, Tanganyika Territory, in 1952-53. I. Clinical features. Trans. R. Soc. Trop. Med. Hyg. 1955, 49:28-32.
13. Josseran L., et al. Chikungunya disease outbreak, Reunion Island. Emerg. Infect. Dis. 2006, 12:1994-1995.
14. Krishnamoorthy K., et al. Burden of chikungunya in India: estimates of disability adjusted life years (DALY) lost in 2006 epidemic. J. Vector Borne Dis. 2009, 46:26-35.
15. Harley D., et al. Ross River virus disease in tropical Queensland: evolution of rheumatic manifestations in an inception cohort followed for six months. Med. J. Aust. 2002, 177:352-355.
16. Staikowsky F., et al. Prospective study of chikungunya virus acute infection in the Island of La Reunion during the 2005-2006 outbreak. PLoS ONE 2009, 4:e7603.
17. Sissoko D., et al. Post-epidemic chikungunya disease on Reunion Island: course of rheumatic manifestations and associated factors over a 15-month period. PLoS Negl. Trop. Dis. 2009, 3:e389.
18. Kurkela S., et al. Clinical and laboratory manifestations of Sindbis virus infection: prospective study, Finland, 2002-2003. J. Infect. Dis. 2005, 191:1820-1829.
19. Laine M., et al. Prolonged arthritis associated with sindbis-related (Pogosta) virus infection. Rheumatology (Oxford) 2000, 39:1272-1274.
20. Mylonas A.D., et al. Natural history of Ross River virus-induced epidemic polyarthritis. Med. J. Aust. 2002, 177:356-360.
21. Sims N.A., Vrahnas C. Regulation of cortical and trabecular bone mass by communication between osteoblasts, osteocytes and osteoclasts. Arch. Biochem. Biophys. 2014, 10.1016/j.abb.2014.05.015.
22. McHugh K.P., et al. The role of cell-substrate interaction in regulating osteoclast activation: potential implications in targeting bone loss in rheumatoid arthritis. Ann. Rheum. Dis. 2010, 69(Suppl. 1):i83-i85.
23. Danks L., Takayanagi H. Immunology and bone. J. Biochem. 2013, 154:29-39.
24. Deal C., et al. Bone loss in rheumatoid arthritis: systemic, periarticular, and focal. Curr. Rheumatol. Rep. 2012, 14:231-237.
25. Vis M., et al. Can bone loss in rheumatoid arthritis be prevented?. Osteoporos. Int. 2013, 24:2541-2553.
26. Gough A.K., et al. Generalised bone loss in patients with early rheumatoid arthritis. Lancet 1994, 344:23-27.
27. Gravallese E.M., et al. Identification of cell types responsible for bone resorption in rheumatoid arthritis and juvenile rheumatoid arthritis. Am. J. Pathol. 1998, 152:943-951.
28. Walsh N.C., et al. Osteoblast function is compromised at sites of focal bone erosion in inflammatory arthritis. J. Bone Miner. Res. 2009, 24:1572-1585.
29. Lacey D.L., et al. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 1998, 93:165-176.
30. Kong Y.Y., et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 1999, 397:315-323.
31. Dougall W.C., et al. RANK is essential for osteoclast and lymph node development. Genes Dev. 1999, 13:2412-2424.
32. Simonet W.S., et al. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 1997, 89:309-319.
33. Horwood N.J., et al. Osteotropic agents regulate the expression of osteoclast differentiation factor and osteoprotegerin in osteoblastic stromal cells. Endocrinology 1998, 139:4743-4746.
34. Fazzalari N.L., et al. The ratio of messenger RNA levels of receptor activator of nuclear factor kappaB ligand to osteoprotegerin correlates with bone remodeling indices in normal human cancellous bone but not in osteoarthritis. J. Bone Miner. Res. 2001, 16:1015-1027.
35. Gori F., et al. The expression of osteoprotegerin and RANK ligand and the support of osteoclast formation by stromal-osteoblast lineage cells is developmentally regulated. Endocrinology 2000, 141:4768-4776.
36. Atkins G.J., et al. RANKL expression is related to the differentiation state of human osteoblasts. J. Bone Miner. Res. 2003, 18:1088-1098.
37. Nakashima T., et al. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat. Med. 2011, 17:1231-1234.
38. Gravallese E.M., et al. Synovial tissue in rheumatoid arthritis is a source of osteoclast differentiation factor. Arthritis Rheum. 2000, 43:250-258.
39. Takayanagi H., et al. Involvement of receptor activator of nuclear factor kappaB ligand/osteoclast differentiation factor in osteoclastogenesis from synoviocytes in rheumatoid arthritis. Arthritis Rheum. 2000, 43:259-269.
40. Kong Y.Y., et al. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 1999, 402:304-309.
41. Haynes D., et al. Modulation of RANKL and osteoprotegerin expression in synovial tissue from patients with rheumatoid arthritis in response to disease-modifying antirheumatic drug treatment and correlation with radiologic outcome. Arthritis Rheum. 2008, 59:911-920.
42. Pettit A.R., et al. RANKL protein is expressed at the pannus-bone interface at sites of articular bone erosion in rheumatoid arthritis. Rheumatology (Oxford) 2006, 45:1068-1076.
43. Romas E., et al. Expression of osteoclast differentiation factor at sites of bone erosion in collagen-induced arthritis. Arthritis Rheum. 2000, 43:821-826.
44. Xu S., et al. Osteoprotegerin and RANKL in the pathogenesis of rheumatoid arthritis-induced osteoporosis. Rheumatol. Int. 2012, 32:3397-3403.
45. Chopra A., et al. Chikungunya virus aches and pains: an emerging challenge. Arthritis Rheum. 2008, 58:2921-2922.
46. Jaffar-Bandjee M.C., et al. Chikungunya virus takes centre stage in virally induced arthritis: possible cellular and molecular mechanisms to pathogenesis. Microbes Infect. 2009, 11(14-15):1206-1218.
47. Parola P., et al. Novel chikungunya virus variant in travelers returning from Indian Ocean islands. Emerg. Infect. Dis. 2006, 12:1493-1499.
48. Malvy D., et al. Destructive arthritis in a patient with chikungunya virus infection with persistent specific IgM antibodies. BMC Infect. Dis. 2009, 9:200.
49. Bouquillard E., Combe B. A report of 21 cases of rheumatoid arthritis following chikungunya fever. A mean follow-up of two years. Joint Bone Spine 2009, 76:654-657.
50. Manimunda S.P., et al. Clinical progression of chikungunya fever during acute and chronic arthritic stages and the changes in joint morphology as revealed by imaging. Trans. R. Soc. Trop. Med. Hyg. 2010, 104:392-399.
51. Lokireddy S., et al. Connective tissue metabolism in chikungunya patients. Virol. J. 2008, 5:31.
52. Chen W., et al. Arthritogenic alphaviral infection perturbs osteoblast function and triggers pathologic bone loss. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:6040-6045.
53. Noret M., et al. Interleukin 6, RANKL, and osteoprotegerin expression by chikungunya virus-infected human osteoblasts. J. Infect. Dis. 2012, 206:455-457.
54. Schett G., et al. High-sensitivity C-reactive protein and risk of nontraumatic fractures in the Bruneck study. Arch. Intern. Med. 2006, 166:2495-2501.
55. Soden M., et al. Detection of viral ribonucleic acid and histologic analysis of inflamed synovium in Ross River virus infection. Arthritis Rheum. 2000, 43:365-369.
56. Hoarau J.J., et al. Persistent chronic inflammation and infection by chikungunya arthritogenic alphavirus in spite of a robust host immune response. J. Immunol. 2010, 184:5914-5927.
57. Phuklia W., et al. Osteoclastogenesis induced by CHIKV-infected fibroblast-like synoviocytes: a possible interplay between synoviocytes and monocytes/macrophages in CHIKV-induced arthralgia/arthritis. Virus Res. 2013, 177:179-188.
58. Gardner J., et al. Chikungunya virus arthritis in adult wild-type mice. J. Virol. 2010, 84:8021-8032.
59. Morrison T.E., et al. A mouse model of chikungunya virus-induced musculoskeletal inflammatory disease: evidence of arthritis, tenosynovitis, myositis, and persistence. Am. J. Pathol. 2011, 178:32-40.
60. Heise M.T., et al. Sindbis-group alphavirus replication in periosteum and endosteum of long bones in adult mice. J. Virol. 2000, 74:9294-9299.
61. Labadie K., et al. Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages. J. Clin. Invest. 2010, 120:894-906.
62. Chow A., et al. Persistent arthralgia induced by chikungunya virus infection is associated with interleukin-6 and granulocyte macrophage colony-stimulating factor. J. Infect. Dis. 2011, 203:149-157.
63. Ng L.F., et al. IL-1beta, IL-6, and RANTES as biomarkers of chikungunya severity. PLoS ONE 2009, 4:e4261.
64. Lidbury B.A., et al. Macrophage-derived proinflammatory factors contribute to the development of arthritis and myositis after infection with an arthrogenic alphavirus. J. Infect. Dis. 2008, 197:1585-1593.
65. Poo Y.S., et al. CCR2 deficiency promotes exacerbated chronic erosive neutrophil-dominated chikungunya virus arthritis. J. Virol. 2014, 88:6862-6872.
66. Rulli N.E., et al. Amelioration of alphavirus-induced arthritis and myositis in a mouse model by treatment with bindarit, an inhibitor of monocyte chemotactic proteins. Arthritis Rheum. 2009, 60:2513-2523.
67. Boyle W.J., et al. Osteoclast differentiation and activation. Nature 2003, 423:337-342.
68. Suda T., et al. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr. Rev. 1999, 20:345-357.
69. Onan D., et al. The chemokine Cxcl1 is a novel target gene of parathyroid hormone (PTH)/PTH-related protein in committed osteoblasts. Endocrinology 2009, 150:2244-2253.
70. Abe M., et al. Vicious cycle between myeloma cell binding to bone marrow stromal cells via VLA-4-VCAM-1 adhesion and macrophage inflammatory protein-1alpha and MIP-1beta production. J. Bone Miner. Metab. 2009, 27:16-23.
71. Choi S.J., et al. Macrophage inflammatory protein 1-alpha is a potential osteoclast stimulatory factor in multiple myeloma. Blood 2000, 96:671-675.
72. Hueber W., et al. Proteomic analysis of secreted proteins in early rheumatoid arthritis: anti-citrulline autoreactivity is associated with up regulation of proinflammatory cytokines. Ann. Rheum. Dis. 2007, 66:712-719.
73. Wauquier N., et al. The acute phase of chikungunya virus infection in humans is associated with strong innate immunity and T CD8 cell activation. J. Infect. Dis. 2011, 204:115-123.
74. Gunn B.M., et al. Mannose binding lectin is required for alphavirus-induced arthritis/myositis. PLoS Pathog. 2012, 8:e1002586.
75. Herrero L.J., et al. Macrophage migration inhibitory factor receptor CD74 mediates alphavirus-induced arthritis and myositis in murine models of alphavirus infection. Arthritis Rheum. 2013, 65:2724-2736.
76. + T cells during chikungunya virus infection in mice. J. Immunol. 2013, 190:259-269.
77. Sato K., et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J. Exp. Med. 2006, 203:2673-2682.
78. Kularatne S.A., et al. Epidemiology, clinical manifestations, and long-term outcomes of a major outbreak of chikungunya in a hamlet in Sri Lanka, in 2007: a longitudinal cohort study. J. Trop. Med. 2012, 2012:639178.
79. Borgherini G., et al. Persistent arthralgia associated with chikungunya virus: a study of 88 adult patients on Reunion Island. Clin. Infect. Dis. 2008, 47:469-475.
80. Sane J., et al. Epidemic Sindbis virus infection in Finland: a population-based case-control study of risk factors. J. Infect. Dis. 2011, 204:459-466.
81. Ishimi Y., et al. IL-6 is produced by osteoblasts and induces bone resorption. J. Immunol. 1990, 145:3297-3303.
82. Guerne P-A., et al. Synovium as a source of interleukin 6 in vitro. Contribution to local and systemic manifestations of arthritis. J. Clin. Invest. 1989, 83:585.
83. Lems W.F., Dijkmans B.A. Should we look for osteoporosis in patients with rheumatoid arthritis?. Ann. Rheum. Dis. 1998, 57:325-327.
84. Zheng Y., et al. Direct cross-talk between cancer and osteoblast lineage cells fuels metastatic growth in bone via auto-amplification of IL-6 and RANKL signaling pathways. J. Bone Miner. Res. 2014, 29:1938-1949.
85. Yokota S., et al. Therapeutic efficacy of humanized recombinant anti-interleukin-6 receptor antibody in children with systemic-onset juvenile idiopathic arthritis. Arthritis Rheum. 2005, 52:818-825.
86. Smolen J.S., et al. Effect of interleukin-6 receptor inhibition with tocilizumab in patients with rheumatoid arthritis (OPTION study): a double-blind, placebo-controlled, randomised trial. Lancet 2008, 371:987-997.
87. Svensson C.I. Interleukin-6: a local pain trigger?. Arthritis Res. Ther. 2010, 12:145.
88. Schaible H.G., et al. Mechanisms of pain in arthritis. Ann. N. Y. Acad. Sci. 2002, 966:343-354.
89. Danning C.L., et al. Macrophage-derived cytokine and nuclear factor kappaB p65 expression in synovial membrane and skin of patients with psoriatic arthritis. Arthritis Rheum. 2000, 43:1244-1256.
90. MacNaul K.L., et al. Analysis of IL-1 and TNF-alpha gene expression in human rheumatoid synoviocytes and normal monocytes by in situ hybridization. J. Immunol. 1990, 145:4154-4166.
91. Fossiez F., et al. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J. Exp. Med. 1996, 183:2593-2603.
92. Schabert V.F., et al. Disability outcomes and dose escalation with etanercept, adalimumab, and infliximab in rheumatoid arthritis patients: a US-based retrospective comparative effectiveness study. Curr. Med. Res. Opin. 2012, 28:569-580.
93. Ungar W.J., et al. Cost-effectiveness of biologics in polyarticular-course juvenile idiopathic arthritis patients unresponsive to disease-modifying antirheumatic drugs. Arthritis Care Res. (Hoboken) 2011, 63:111-119.
94. Zaid A., et al. Disease exacerbation by etanercept in a mouse model of alphaviral arthritis and myositis. Arthritis Rheum. 2011, 63:488-491.
95. Zaid A., et al. Exacerbation of alphaviral arthritis and myositis in a mouse model after etanercept treatment is due to diminished levels of interferon α/β. Virol. Mycol. 2013, 2:122.
96. Chao C.C., et al. Anti-IL-17A therapy protects against bone erosion in experimental models of rheumatoid arthritis. Autoimmunity 2011, 44:243-252.
97. Lubberts E., et al. Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum. 2004, 50:650-659.
98. Koenders M.I., et al. Blocking of interleukin-17 during reactivation of experimental arthritis prevents joint inflammation and bone erosion by decreasing RANKL and interleukin-1. Am. J. Pathol. 2005, 167:141-149.
99. Miossec P., et al. Interleukin-17 and type 17 helper T cells. N. Engl. J. Med. 2009, 361:888-898.
100. Cummings S.R., et al. Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N. Engl. J. Med. 2009, 361:756-765.
101. Josse R., et al. Denosumab, a new pharmacotherapy option for postmenopausal osteoporosis. Curr. Med. Res. Opin. 2013, 29:205-216.
102. Tyagi A.M., et al. Enhanced immunoprotective effects by anti-IL17 antibody translates to improved skeletal parameters under estrogen deficiency compared to anti-RANKL and anti-TNFalpha antibodies. J. Bone Miner. Res. 2014, 29:1981-1992.
103. Rizzoli R., et al. Denosumab. Nature reviews. Drug Discov. 2010, 9:591-592.
104. Cohen S.B., et al. Denosumab treatment effects on structural damage, bone mineral density, and bone turnover in rheumatoid arthritis: a twelve-month, multicenter, randomized, double-blind, placebo-controlled, phase II clinical trial. Arthritis Rheum. 2008, 58:1299-1309.