Role of Pentraxin 3 in Shaping Arthritogenic Alphaviral Disease: From Enhanced Viral Replication to Immunomodulation

English version České info

Chikungunya virus (CHIKV) and Ross River virus (RRV) are arthropod-borne viruses associated with massive epidemics affecting millions of people worldwide, causing widespread distribution of alphaviral-induced arthritis. The rising prevalence of alphavirus infections and, critically, the lack of therapeutic treatments warrant urgent attention to elucidate the innate immune responses elicited, which serves as the first line of host defense against alphavirus. Ironically, robust innate immune responses have been associated with both protective and pathogenic outcomes. Here, we identified PTX3 as an innate protein involved in acute CHIKV and RRV infection in humans. Using an established acute RRV disease mouse model, we revealed a pathogenic immunoregulatory role of PTX3 which led to enhanced viral infectivity and prolonged disease. Transient overexpression of PTX3 in a human epithelial cell line identified the importance of PTX3 N-terminus in binding RRV and modulating viral entry and replication. Collectively, our study identified a previously undescribed pathogenic role of PTX3 during virus infection and shed insights into the sophisticated innate immune responses launched against virus invasion.

Vyšlo v časopise: Role of Pentraxin 3 in Shaping Arthritogenic Alphaviral Disease: From Enhanced Viral Replication to Immunomodulation. PLoS Pathog 11(2): e32767. doi:10.1371/journal.ppat.1004649
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004649

Souhrn

Zdroje

1. Taubitz W, Cramer JP, Kapaun A, Pfeffer M, Drosten C, et al. (2007) Chikungunya fever in travelers: clinical presentation and course. Clin Infect Dis 45: e1–4. 17554689

2. Bi P, Hiller JE, Cameron AS, Zhang Y, Givney R (2009) Climate variability and Ross River virus infections in Riverland, South Australia, 1992–2004. Epidemiol Infect 137 : 1486–1493. doi: 10.1017/S0950268809002441 19296873

3. Aaskov JG, Mataika JU, Lawrence GW, Rabukawaqa V, Tucker MM, et al. (1981) An epidemic of Ross River virus infection in Fiji, 1979. Am J Trop Med Hyg 30 : 1053–1059. 7283004

4. Suhrbier A, Jaffar-Bandjee MC, Gasque P (2012) Arthritogenic alphaviruses—an overview. Nat Rev Rheumatol 8 : 420–429. doi: 10.1038/nrrheum.2012.64 22565316

5. Pan American Health Oganization WHO (2014) Number of Reported Cases of Chikungunya Fever in the Americas, by Country or Territory 2013–2014 (Updated 25 July 2014).

6. Russell RC (2002) Ross River virus: ecology and distribution. Annual Review of Entomology 47 : 1–31. 11729067

7. Burt FJ, Rolph MS, Rulli NE, Mahalingam S, Heise MT (2012) Chikungunya: a re-emerging virus. Lancet 379 : 662–671. doi: 10.1016/S0140-6736(11)60281-X 22100854

8. Schwartz O, Albert ML (2010) Biology and pathogenesis of chikungunya virus. Nat Rev Microbiol 8 : 491–500. doi: 10.1038/nrmicro2368 20551973

9. Proll S, Dobler G, Pfeffer M, Jelinek T, Nothdurft HD, et al. (1999) [Persistent arthralgias in Ross-River-Virus disease after travel to the South Pacific]. Dtsch Med Wochenschr 124 : 759–762. 10412359

10. Chen W, Foo SS, Rulli NE, Taylor A, Sheng KC, et al. (2014) Arthritogenic alphaviral infection perturbs osteoblast function and triggers pathologic bone loss. Proc Natl Acad Sci U S A 111 : 6040–6045. doi: 10.1073/pnas.1318859111 24733914

11. Bouquillard E, Combe B (2009) A report of 21 cases of rheumatoid arthritis following Chikungunya fever. A mean follow-up of two years. Joint Bone Spine 76 : 654–657. doi: 10.1016/j.jbspin.2009.08.005 19945329

12. Mylonas AD, Brown AM, Carthew TL, McGrath B, Purdie DM, et al. (2002) Natural history of Ross River virus-induced epidemic polyarthritis. Med J Aust 177 : 356–360. 12358577

13. Burt FJ, Chen W, Mahalingam S (2014) Chikungunya virus and arthritic disease: Mechanism and potential risk factor for sever disease. Lancet Infect Dis: in press.

14. Schilte C, Staikowsky F, Couderc T, Madec Y, Carpentier F, et al. (2013) Chikungunya virus-associated long-term arthralgia: a 36-month prospective longitudinal study. PLoS Negl Trop Dis 7: e2137. doi: 10.1371/journal.pntd.0002137 23556021

15. Chow A, Her Z, Ong EK, Chen JM, Dimatatac F, et al. (2011) Persistent Arthralgia Induced by Chikungunya Virus Infection is Associated with Interleukin-6 and Granulocyte Macrophage Colony-Stimulating Factor. J Infect Dis 203 : 149–157. doi: 10.1093/infdis/jiq042 21288813

16. Daigo K, Hamakubo T (2012) Host-protective effect of circulating pentraxin 3 (PTX3) and complex formation with neutrophil extracellular traps. Front Immunol 3 : 378. doi: 10.3389/fimmu.2012.00378 23248627

17. Herrero LJ, Nelson M, Srikiatkhachorn A, Gu R, Anantapreecha S, et al. (2011) Critical role for macrophage migration inhibitory factor (MIF) in Ross River virus-induced arthritis and myositis. Proc Natl Acad Sci U S A 108 : 12048–12053. doi: 10.1073/pnas.1101089108 21730129

18. Morrison TE, Fraser RJ, Smith PN, Mahalingam S, Heise MT (2007) Complement contributes to inflammatory tissue destruction in a mouse model of Ross River virus-induced disease. J Virol 81 : 5132–5143. 17314163

19. Gunn BM, Morrison TE, Whitmore AC, Blevins LK, Hueston L, et al. (2012) Mannose binding lectin is required for alphavirus-induced arthritis/myositis. PLoS Pathog 8: e1002586. doi: 10.1371/journal.ppat.1002586 22457620

20. Bottazzi B, Doni A, Garlanda C, Mantovani A (2010) An integrated view of humoral innate immunity: pentraxins as a paradigm. Annu Rev Immunol 28 : 157–183. doi: 10.1146/annurev-immunol-030409-101305 19968561

21. Jaillon S, Peri G, Delneste Y, Fremaux I, Doni A, et al. (2007) The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J Exp Med 204 : 793–804. 17389238

22. Alles VV, Bottazzi B, Peri G, Golay J, Introna M, et al. (1994) Inducible expression of PTX3, a new member of the pentraxin family, in human mononuclear phagocytes. Blood 84 : 3483–3493. 7949102

23. Lee GW, Lee TH, Vilcek J (1993) TSG-14, a tumor necrosis factor -⁠ and IL-1-inducible protein, is a novel member of the pentaxin family of acute phase proteins. J Immunol 150 : 1804–1812. 7679696

24. Bottazzi B, Garlanda C, Cotena A, Moalli F, Jaillon S, et al. (2009) The long pentraxin PTX3 as a prototypic humoral pattern recognition receptor: interplay with cellular innate immunity. Immunol Rev 227 : 9–18. doi: 10.1111/j.1600-065X.2008.00719.x 19120471

25. He X, Han B, Liu M (2007) Long pentraxin 3 in pulmonary infection and acute lung injury. Am J Physiol Lung Cell Mol Physiol 292: L1039–1049. 17277044

26. Baldini M, Maugeri N, Ramirez GA, Giacomassi C, Castiglioni A, et al. (2011) Selective upregulation of the soluble pattern recognition receptor PTX3 and of VEGF in giant cell arteritis: Relevance for recent optic nerve ischemia. Arthritis Rheum.

27. Rolph MS, Zimmer S, Bottazzi B, Garlanda C, Mantovani A, et al. (2002) Production of the long pentraxin PTX3 in advanced atherosclerotic plaques. Arterioscler Thromb Vasc Biol 22: e10–14. 12006411

28. Luchetti MM, Piccinini G, Mantovani A, Peri G, Matteucci C, et al. (2000) Expression and production of the long pentraxin PTX3 in rheumatoid arthritis (RA). Clin Exp Immunol 119 : 196–202. 10606983

29. Bozza S, Bistoni F, Gaziano R, Pitzurra L, Zelante T, et al. (2006) Pentraxin 3 protects from MCMV infection and reactivation through TLR sensing pathways leading to IRF3 activation. Blood 108 : 3387–3396. 16840729

30. Reading PC, Bozza S, Gilbertson B, Tate M, Moretti S, et al. (2008) Antiviral activity of the long chain pentraxin PTX3 against influenza viruses. J Immunol 180 : 3391–3398. 18292565

31. Souza DG, Amaral FA, Fagundes CT, Coelho FM, Arantes RM, et al. (2009) The long pentraxin PTX3 is crucial for tissue inflammation after intestinal ischemia and reperfusion in mice. Am J Pathol 174 : 1309–1318. doi: 10.2353/ajpath.2009.080240 19286566

32. Deban L, Russo RC, Sironi M, Moalli F, Scanziani M, et al. (2010) Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat Immunol 11 : 328–334. doi: 10.1038/ni.1854 20208538

33. Morrison TE, Whitmore AC, Shabman RS, Lidbury BA, Mahalingam S, et al. (2006) Characterization of Ross River virus tropism and virus-induced inflammation in a mouse model of viral arthritis and myositis. J Virol 80 : 737–749. 16378976

34. Mantovani A, Valentino S, Gentile S, Inforzato A, Bottazzi B, et al. (2013) The long pentraxin PTX3: a paradigm for humoral pattern recognition molecules. Ann N Y Acad Sci 1285 : 1–14. doi: 10.1111/nyas.12043 23527487

35. Herrero LJ, Sheng KC, Jian P, Taylor A, Her Z, et al. (2013) Macrophage migration inhibitory factor receptor CD74 mediates alphavirus-induced arthritis and myositis in murine models of alphavirus infection. Arthritis Rheum 65 : 2724–2736. doi: 10.1002/art.38090 23896945

36. Wang YF, Sawicki SG, Sawicki DL (1994) Alphavirus nsP3 functions to form replication complexes transcribing negative-strand RNA. J Virol 68 : 6466–6475. 8083984

37. Lidbury BA, Rulli NE, Suhrbier A, Smith PN, McColl SR, et al. (2008) Macrophage-derived proinflammatory factors contribute to the development of arthritis and myositis after infection with an arthrogenic alphavirus. J Infect Dis 197 : 1585–1593. doi: 10.1086/587841 18433328

38. Ng LF, Chow A, Sun YJ, Kwek DJ, Lim PL, et al. (2009) IL-1beta, IL-6, and RANTES as biomarkers of Chikungunya severity. PLoS One 4: e4261. doi: 10.1371/journal.pone.0004261 19156204

39. Inforzato A, Doni A, Barajon I, Leone R, Garlanda C, et al. (2013) PTX3 as a paradigm for the interaction of pentraxins with the complement system. Semin Immunol 25 : 79–85. doi: 10.1016/j.smim.2013.05.002 23747040

40. Hossain I, Tambyah PA, Wilder-Smith A (2009) Ross River virus disease in a traveler to Australia. J Travel Med 16 : 420–423. doi: 10.1111/j.1708-8305.2009.00345.x 19930384

41. Chopra A, Anuradha V, Lagoo-Joshi V, Kunjir V, Salvi S, et al. (2008) Chikungunya virus aches and pains: an emerging challenge. Arthritis Rheum 58 : 2921–2922. doi: 10.1002/art.23753 18759351

42. Hollan I, Bottazzi B, Cuccovillo I, Forre OT, Mikkelsen K, et al. (2010) Increased levels of serum pentraxin 3, a novel cardiovascular biomarker, in patients with inflammatory rheumatic disease. Arthritis Care Res (Hoboken) 62 : 378–385. doi: 10.1002/acr.20094 20391484

43. Garlanda C, Hirsch E, Bozza S, Salustri A, De Acetis M, et al. (2002) Non-redundant role of the long pentraxin PTX3 in anti-fungal innate immune response. Nature 420 : 182–186. 12432394

44. Moalli F, Paroni M, Veliz Rodriguez T, Riva F, Polentarutti N, et al. (2011) The therapeutic potential of the humoral pattern recognition molecule PTX3 in chronic lung infection caused by Pseudomonas aeruginosa. J Immunol 186 : 5425–5434. doi: 10.4049/jimmunol.1002035 21441447

45. Jaillon S, Moalli F, Ragnarsdottir B, Bonavita E, Puthia M, et al. (2014) The humoral pattern recognition molecule PTX3 is a key component of innate immunity against urinary tract infection. Immunity 40 : 621–632. doi: 10.1016/j.immuni.2014.02.015 24745336

46. Souza DG, Soares AC, Pinho V, Torloni H, Reis LF, et al. (2002) Increased mortality and inflammation in tumor necrosis factor-stimulated gene-14 transgenic mice after ischemia and reperfusion injury. Am J Pathol 160 : 1755–1765. 12000727

47. Soares AC, Souza DG, Pinho V, Vieira AT, Nicoli JR, et al. (2006) Dual function of the long pentraxin PTX3 in resistance against pulmonary infection with Klebsiella pneumoniae in transgenic mice. Microbes Infect 8 : 1321–1329. 16697676

48. Chen W, Foo SS, Taylor A, Lulla A, Merits A, et al. (2014) Bindarit, an inhibitor of monocyte chemotactic proteins (MCPs) synthesis, protects against bone loss induced by Chikungunya virus infection. J Virol.

49. Nauta AJ, Bottazzi B, Mantovani A, Salvatori G, Kishore U, et al. (2003) Biochemical and functional characterization of the interaction between pentraxin 3 and C1q. Eur J Immunol 33 : 465–473. 12645945

50. Rigamonti E, Touvier T, Clementi E, Manfredi AA, Brunelli S, et al. (2013) Requirement of inducible nitric oxide synthase for skeletal muscle regeneration after acute damage. J Immunol 190 : 1767–1777. doi: 10.4049/jimmunol.1202903 23335752

51. Foo SS, Chen W, Herrero L, Bettadapura J, Narayan J, et al. (2011) The genetics of alphaviruses. Future Virol 6 : 1407.

52. Inforzato A, Rivieccio V, Morreale AP, Bastone A, Salustri A, et al. (2008) Structural characterization of PTX3 disulfide bond network and its multimeric status in cumulus matrix organization. J Biol Chem 283 : 10147–10161. doi: 10.1074/jbc.M708535200 18223257

53. Han B, Ma X, Zhang J, Zhang Y, Bai X, et al. (2012) Protective effects of long pentraxin PTX3 on lung injury in a severe acute respiratory syndrome model in mice. Lab Invest 92 : 1285–1296. doi: 10.1038/labinvest.2012.92 22732935

54. Win MK, Chow A, Dimatatac F, Go CJ, Leo YS (2010) Chikungunya fever in Singapore: acute clinical and laboratory features, and factors associated with persistent arthralgia. J Clin Virol 49 : 111–114. doi: 10.1016/j.jcv.2010.07.004 20674479

55. Tsetsarkin K, Higgs S, McGee CE, De Lamballerie X, Charrel RN, et al. (2006) Infectious clones of Chikungunya virus (La Reunion isolate) for vector competence studies. Vector Borne Zoonotic Dis 6 : 325–337. 17187566

56. Salmon AB, Murakami S, Bartke A, Kopchick J, Yasumura K, et al. (2005) Fibroblast cell lines from young adult mice of long-lived mutant strains are resistant to multiple forms of stress. Am J Physiol Endocrinol Metab 289: E23–29. 15701676

57. Bottazzi B, Vouret-Craviari V, Bastone A, De Gioia L, Matteucci C, et al. (1997) Multimer formation and ligand recognition by the long pentraxin PTX3. Similarities and differences with the short pentraxins C-reactive protein and serum amyloid P component. J Biol Chem 272 : 32817–32823. 9407058

58. Camozzi M, Rusnati M, Bugatti A, Bottazzi B, Mantovani A, et al. (2006) Identification of an antiangiogenic FGF2-binding site in the N terminus of the soluble pattern recognition receptor PTX3. J Biol Chem 281 : 22605–22613. 16769728

59. Lidbury BA, Simeonovic C, Maxwell GE, Marshall ID, Hapel AJ (2000) Macrophage-induced muscle pathology results in morbidity and mortality for Ross River virus-infected mice. J Infect Dis 181 : 27–34. 10608747

60. Shabman RS, Rogers KM, Heise MT (2008) Ross River virus envelope glycans contribute to type I interferon production in myeloid dendritic cells. J Virol 82 : 12374–12383. doi: 10.1128/JVI.00985-08 18922878