Expanding regulatory T cells alleviates Chikungunya virus-induced pathology in mice

Journal of Virology

Volumn 89, Issue 15, 2015, Pages 7893-7904

  Lee, Wendy W L ^a,b   Teo, Teck Hui ^a,b   Her, Zhisheng ^a,f   Lum, Fok Moon ^a,c   Kam, Yiu Wing ^a   Haase, Doreen ^a   Rénia, Laurent ^a   Rötzschke, Olaf ^a,c,d   Ng, Lisa F P ^a,c,e  

^a AGENCY FOR SCIENCE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e UNIVERSITY OF LIVERPOOL   (United Kingdom)

^f INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; JES 6 1 ANTIBODY; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CHIKUNGUNYA; CHIKUNGUNYA VIRUS; CLONAL ANERGY; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; FLOW CYTOMETRY; IMMUNOPHENOTYPING; IN VIVO STUDY; INNATE IMMUNITY; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VIREMIA; VIRUS LOAD;

CHIKUNGUNYA VIRUS; MUS;

EID: 84932644792     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00998-15     Document Type: Article

References (67)

1. Kennedy A, Fleming J, Solomon L. 1979. Chikungunya viral arthropathy: a clinical description. J Rheumatol 7:231-236.
2. Pfefferkorn ER, Shapiro D. 1974. Reproduction of togaviruses, p 171-230. In Fraenkel-Conrat H, Wagner RR (ed), Reproduction: small and intermediate RNA viruses. Springer, New York, NY.
3. Renault P, Solet J-L, Sissoko D, Balleydier E, Larrieu S, Filleul L, Lassalle C, Thiria J, Rachou E, de Valk H, Ilef D, Ledrans M, Quatresous I, Quenel P, Pierre V. 2007. A major epidemic of chikungunya virus infection on Réunion Island, France, 2005-2006. Am J Trop Med Hyg 77:727-731.
4. Pialoux G, Gaüzère B-A, Jauréguiberry S, Strobel M. 2007. Chikungunya, an epidemic arbovirosis. Lancet Infect Dis 7:319-327. http://dx.doi.org/10.1016/S1473-3099(07)70107-X.
5. Powers AM, Logue CH. 2007. Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus. J Gen Virol 88:2363-2377. http://dx.doi.org/10.1099/vir.0.82858-0.
6. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC, Cassone A. 2007. Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370:1840-1846. http://dx.doi.org/10.1016/S0140-6736(07)61779-6.
7. Grandadam M, Caro V, Plumet S, Thiberge JM, Souarès Y, Failloux AB, Tolou HJ, Budelot M, Cosserat D, Leparc-Goffart I, Desprès P. 2011. Chikungunya virus, southeastern France. Emerg Infect Dis 17:910. http://dx.doi.org/10.3201/eid1705.101873.
8. Cagney H. 2014. Infectious disease surveillance update. Lancet Infect Dis 14:377. http://dx.doi.org/10.1016/S1473-3099(14)70762-5.
9. Leparc-Goffart I, Nougairede A, Cassadou S, Prat C, de Lamballerie X. 2014. Chikungunya in the Americas. Lancet 383:514. http://dx.doi.org/10.1016/S0140-6736(14)60185-9.
10. Pan American Health Organization. 31 Oct 2014. Number of reported cases of chikungunya fever in the Americas, by country or territory. http://www.paho.org/hq/index.php?option=com_docman&task=doc_download&Itemid=&gid=27998&lang=en. Accessed 6 November 2014.
11. Roth A, Hoy D, Horwood PF, Ropa B, Hancock T, Guillaumot L, Rickart K, Frison P, Pavlin B, Souares Y. 2014. Preparedness for threat of chikungunya in the Pacific. Emerg Infect Dis, vol 20. http://dx.doi.org/10.3201/eid2008.130696.
12. Simon F, Parola P, Grandadam M, Fourcade S, Oliver M, Brouqui P, Hance P, Kraemer P, Mohamed AA, de Lamballerie X, Charrel R, Tolou H. 2007. Chikungunya infection: an emerging rheumatism among travelers returned from Indian Ocean islands. Report of 47 cases. Medicine 86:123-137. http://dx.doi.org/10.1097/MD/0b013e31806010a5.
13. Chow A, Her Z, Ong EKS, Chen J-M, Dimatatac F, Kwek DJC, Barkham T, Yang H, Rénia L, Leo Y-S, Ng LFP. 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. http://dx.doi.org/10.1093/infdis/jiq042.
14. Borgherini G, Poubeau P, Jossaume A, Gouix A, Cotte L, Michault A, Arvin-Berod C, Paganin F. 2008. Persistent arthralgia associated with chikungunya virus: a study of 88 adult patients on Reunion Island. Clin Infect Dis 47:469-475. http://dx.doi.org/10.1086/590003.
15. Ng LFP, Chow A, Sun Y-J, Kwek DJC, Lim P-L, Dimatatac F, Ng L-C, Ooi E-E, Choo K-H, Her Z, Kourilsky P, Leo Y-S. 2009. IL-1β, IL-6, and RANTES as biomarkers of chikungunya severity. PLoS One 4:e4261. http://dx.doi.org/10.1371/journal.pone.0004261.
16. Teo TH, Lum FM, Claser C, Lulla V, Lulla A, Merits A, Rénia L, Ng LFP. 2013. A pathogenic role for CD4+ T cells during chikungunya virus infection in mice. J Immunol 190:259-269. http://dx.doi.org/10.4049/jimmunol.1202177.
17. Hoarau J-J, Jaffar Bandjee M-C, Krejbich Trotot P, Das T, Li-Pat-Yuen G, Dassa B, Denizot M, Guichard E, Ribera A, Henni T, Tallet F, Moiton MP, Gauzère BA, Bruniquet S, Jaffar Bandjee Z, Morbidelli P, Martigny G, Jolivet M, Gay F, Grandadam M, Tolou H, Vieillard V, Debré P, Autran B, Gasque P. 2010. Persistent chronic inflammation and infection by chikungunya arthritogenic alphavirus in spite of a robust host immune response. J Immunol 184:5914-5927. http://dx.doi.org/10.4049/jimmunol.0900255.
18. Morrison TE, Oko L, Montgomery SA, Whitmore AC, Lotstein AR, Gunn BM, Elmore SA, Heise MT. 2011. A mouse model of chikungunya virus-induced musculoskeletal inflammatory disease: evidence of arthritis, tenosynovitis, myositis, and persistence. Am J Pathol 178:32-40. http://dx.doi.org/10.1016/j.ajpath.2010.11.018.
19. Nakaya HI, Gardner J, Poo Y-S, Major L, Pulendran B, Suhrbier A. 2012. Gene profiling of Chikungunya virus arthritis in a mouse model reveals significant overlap with rheumatoid arthritis. Arthritis Rheum 64: 3553-3563. http://dx.doi.org/10.1002/art.34631.
20. Poo YS, Rudd PA, Gardner J, Wilson JAC, Larcher T, Colle M-A, Le TT, Nakaya HI, Warrilow D, Allcock R, Bielefeldt-Ohmann H, Schroder WA, Khromykh AA, Lopez JA, Suhrbier A. 2014. Multiple immune factors are involved in controlling acute and chronic chikungunya virus infection. PLoS Negl Trop Dis 8:e3354. http://dx.doi.org/10.1371/journal.pntd.0003354.
21. Lundgren A, Suri-Payer E, Enarsson K, Svennerholm A-M, Lundin BS. 2003. Helicobacter pylori-specific CD4+ CD25high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals. Infect Immun 71:1755-1762. http://dx.doi.org/10.1128/IAI.71.4.1755-1762.2003.
22. Suvas S, Azkur AK, Kim BS, Kumaraguru U, Rouse BT. 2004. CD4+CD25+ regulatory T cells control the severity of viral immunoinflammatory lesions. J Immunol 172:4123-4132. http://dx.doi.org/10.4049/jimmunol.172.7.4123.
23. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. 1995. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of selftolerance causes various autoimmune diseases. J Immunol 155:1151-1164.
24. McKinley L, Logar AJ, McAllister F, Zheng M, Steele C, Kolls JK. 2006. Regulatory T cells dampen pulmonary inflammation and lung injury in an animal model of Pneumocystis pneumonia. J Immunol 177:6215-6226. http://dx.doi.org/10.4049/jimmunol.177.9.6215.
25. Centers for Disease Control and Prevention. 3 Oct 2014. West Nile virus disease cases and presumptive viremic blood donors by state-United States. http://www.cdc.gov/westnile/statsMaps/preliminaryMapsData/histatedate.html. Accessed 7 Oct 2014.
26. Lanteri MC, Brien KM, Purtha WE, Cameron MJ, Lund JM, Owen RE, Heitman JW, Custer B, Hirschkorn DF, Tobler LH, Kiely N, Prince HE, Ndhlovu LC, Nixon DF, Kamel HT, Kelvin DJ, Busch MP, Rudensky AY, Diamond MS, Norris PJ. 2009. Tregs control the development of symptomatic West Nile virus infection in humans and mice. J Clin Invest 119:3266-3277. http://dx.doi.org/10.1172/JCI39387.
27. Gardner J, Anraku I, Le TT, Larcher T, Major L, Roques P, Schroder WA, Higgs S, Suhrbier A. 2010. Chikungunya virus arthritis in adult wild-type mice. J Virol 84:8021-8032. http://dx.doi.org/10.1128/JVI.02603-09.
28. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. 2008. Regulatory T cells and immune tolerance. Cell 133:775-787. http://dx.doi.org/10.1016/j.cell.2008.05.009.
29. Boyman O, Kovar M, Rubinstein MP, Surh CD, Sprent J. 2006. Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science 311:1924-1927. http://dx.doi.org/10.1126/science.1122927.
30. Her Z, Malleret B, Chan M, Ong EKS, Wong S-C, Kwek DJC, Tolou H, Lin RTP, Tambyah PA, Rénia L, Ng LFP. 2010. Active infection of human blood monocytes by chikungunya virus triggers an innate immune response. J Immunol 184:5903-5913. http://dx.doi.org/10.4049/jimmunol.0904181.
31. Kam YW, Lum FM, Teo TH, Lee WWL, Simarmata D, Harjanto S, Chua CL, Chan YF, Wee JK, Chow A, Lin RTP, Leo YS, Le Grand R, Sam IC, Tong JC, Roques P, Wiesmüller KH, Rénia L, Rötzschke O, Ng LFP. 2012. Early neutralizing IgG response to chikungunya virus in infected patients targets a dominant linear epitope on the E2 glycoprotein. EMBO Mol Med 4:330-343. http://dx.doi.org/10.1002/emmm.201200213.
32. Lum FM, Teo TH, Lee WWL, Kam Y-W, Rénia L, Ng LFP. 2013. An essential role of antibodies in the control of chikungunya virus infection. J Immunol 190:6295-6302. http://dx.doi.org/10.4049/jimmunol.1300304.
33. Teng T-S, Foo S-S, Simamarta D, Lum F-M, Teo T-H, Lulla A, Yeo NKW, Koh EGL, Chow A, Leo Y-S, Merits A, Chin K-C, Ng LFP. 2012. Viperin restricts chikungunya virus replication and pathology. J Clin Invest 122:4447-4460. http://dx.doi.org/10.1172/JCI63120.
34. Plaskon NE, Adelman ZN, Myles KM. 2009. Accurate strand-specific quantification of viral RNA. PLoS One 4:e7468. http://dx.doi.org/10.1371/journal.pone.0007468.
35. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. http://dx.doi.org/10.1038/nmeth.2089.
36. Lahl K, Sparwasser T. 2011. In vivo depletion of FoxP3+ Tregs using the DEREG mouse model, p 157-172. In Kassiotis G, Liston A (ed), Regulatory T cells, vol 707. Humana Press, Totowa, NJ.
37. Rulli NE, Rolph MS, Srikiatkhachorn A, Anantapreecha S, Guglielmotti A, Mahalingam S. 2011. Protection from arthritis and myositis in a mouse model of acute chikungunya virus disease by bindarit, an inhibitor of monocyte chemotactic protein-1 synthesis. J Infect Dis 204:1026-1030. http://dx.doi.org/10.1093/infdis/jir470.
38. Endl E, Steinbach P, Knüchel R, Hofstädter F. 1997. Analysis of cell cycle-related Ki-67 and p120 expression by flow cytometric BrdUHoechst/7AAD and immunolabeling technique. Cytometry 29:233-241. http://dx.doi.org/10.1002/(SICI)1097-0320(19971101)29:3<233::AID-CYTO6>3.0.CO;2-C.
39. Schwartz R. 1990. A cell culture model for T lymphocyte clonal anergy. Science 248:1349-1356. http://dx.doi.org/10.1126/science.2113314.
40. Schwartz RH. 1996. Models of T cell anergy: is there a common molecular mechanism?. J Exp Med 184:1-8. http://dx.doi.org/10.1084/jem.184.1.1.
41. Fathman CG, Lineberry NB. 2007. Molecular mechanisms of CD4+ T-cell anergy. Nat Rev Immunol 7:599-609. http://dx.doi.org/10.1038/nri2131.
42. Venken K, Thewissen M, Hellings N, Somers V, Hensen K, Rummens J-L, Stinissen P. 2007. A CFSE based assay for measuring CD4+CD25+ regulatory T cell mediated suppression of auto-antigen specific and polyclonal T cell responses. J Immunol Methods 322:1-11. http://dx.doi.org/10.1016/j.jim.2007.01.025.
43. Lyons AB, Parish CR. 1994. Determination of lymphocyte division by flow cytometry. J Immunol Methods 171:131-137. http://dx.doi.org/10.1016/0022-1759(94)90236-4.
44. Mahnke K, Ring S, Johnson TS, Schallenberg S, Schönfeld K, Storn V, Bedke T, Enk AH. 2007. Induction of immunosuppressive functions of dendritic cells in vivo by CD4+CD25+ regulatory T cells: role of B7-H3 expression and antigen presentation. Eur J Immunol 37:2117-2126. http://dx.doi.org/10.1002/eji.200636841.
45. Kuklina EM. 2013. Molecular mechanisms of T-cell anergy. Biochemistry (Mosc) 78:144-156. http://dx.doi.org/10.1134/S000629791302003X.
46. Boussiotis VA, Freeman GJ, Taylor PA, Berezovskaya A, Grass I, Blazar BR, Nadler LM. 2000. p27kip1 functions as an anergy factor inhibiting interleukin 2 transcription and clonal expansion of alloreactive human and mouse helper T lymphocytes. Nat Med 6:290-297. http://dx.doi.org/10.1038/73144.
47. Kang SM, Beverly B, Tran AC, Brorson K, Schwartz RH, Lenardo MJ. 1992. Transactivation by AP-1 is a molecular target of T cell clonal anergy. Science 257:1134-1138. http://dx.doi.org/10.1126/science.257.5073.1134.
48. Vermaelen KY, Carro-Muino I, Lambrecht BN, Pauwels RA. 2001. Specific migratory dendritic cells rapidly transport antigen from the airways to the thoracic lymph nodes. J Exp Med 193:51-60.
49. Hänig J, Lutz MB. 2008. Suppression of mature dendritic cell function by regulatory T cells in vivo is abrogated by CD40 licensing. J Immunol 180:1405-1413. http://dx.doi.org/10.4049/jimmunol.180.3.1405.
50. Onishi Y, Fehervari Z, Yamaguchi T, Sakaguchi S. 2008. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc Natl Acad Sci USA 105:10113-10118. http://dx.doi.org/10.1073/pnas.0711106105.
51. Misra N, Bayry J, Lacroix-Desmazes S, Kazatchkine MD, Kaveri SV. 2004. Cutting edge: human CD4+CD25+T cells restrain the maturation and antigen-presenting function of dendritic cells. J Immunol 172:4676-4680. http://dx.doi.org/10.4049/jimmunol.172.8.4676.
52. Cederbom L, Hall H, Ivars F. 2000. CD4+CD25+ regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur J Immunol 30:1538-1543. http://dx.doi.org/10.1002/1521-4141(200006)30:6<1538::AID-IMMU1538>3.0.CO;2-X.
53. Suhrbier A, La Linn M. 2004. Clinical and pathologic aspects of arthritis due to Ross River virus and other alphaviruses. Curr Opin Rheumatol 16:374-379. http://dx.doi.org/10.1097/01.bor.0000130537.76808.26.
54. Licon Luna RM, Lee E, Müllbacher A, Blanden RV, Langman R, Lobigs M. 2002. Lack of both Fas ligand and perforin protects from flavivirusmediated encephalitis in mice. J Virol 76:3202-3211. http://dx.doi.org/10.1128/JVI.76.7.3202-3211.2002.
55. Gagnon SJ, Ennis FA, Rothman AL. 1999. Bystander target cell lysis and cytokine production by dengue virus-specific human CD4+ cytotoxic T-lymphocyte clones. J Virol 73:3623-3629.
56. Wang Y, Lobigs M, Lee E, Müllbacher A. 2003. CD8+ T cells mediate recovery and immunopathology in West Nile virus encephalitis. J Virol 77:13323-13334. http://dx.doi.org/10.1128/JVI.77.24.13323-13334.2003.
57. King NJC, Getts DR, Getts MT, Rana S, Shrestha B, Kesson AM. 2007. Immunopathology of flavivirus infections. Immunol Cell Biol 85:33-42. http://dx.doi.org/10.1038/sj.icb.7100012.
58. Kurane I, Ennis FE. 1992. Immunity and immunopathology in dengue virus infections. Semin Immunol 4:121-127.
59. Powell JD, Lerner CG, Schwartz RH. 1999. Inhibition of cell cycle progression by rapamycin induces T cell clonal anergy even in the presence of costimulation. J Immunol 162:2775-2784.
60. Rudd CE. 2006. Cell cycle 'check points' T cell anergy. Nat Immunol 7:1130-1132. http://dx.doi.org/10.1038/ni1106-1130.
61. Jenkins MK. 1992. The role of cell division in the induction of clonal anergy. Immunol Today 13:69-73. http://dx.doi.org/10.1016/0167-5699(92)90137-V.
62. Lombardi G, Riffo-Vasquez Y. 2008. Dendritic cells. Springer, New York, NY.
63. Powers AM. 2013. Infection patterns and emergence of O'nyong'nyong virus, p 433-444. In Singh SK (ed), Viral infections and global change. John Wiley & Sons, Inc., New York, NY.
64. Yu W, Mengersen K, Dale P, Mackenzie JS, Toloo G, Wang X, Tong S. 2014. Epidemiologic patterns of Ross River virus disease in Queensland, Australia, 2001-2011. Am J Trop Med Hyg 91:109-118. http://dx.doi.org/10.4269/ajtmh.13-0455.
65. San Martín JL, Brathwaite O, Zambrano B, Solórzano JO, Bouckenooghe A, Dayan GH, Guzmán MG. 2010. The epidemiology of dengue in the Americas over the last three decades: a worrisome reality. Am J Trop Med Hyg 82:128-135. http://dx.doi.org/10.4269/ajtmh.2010.09-0346.
66. Suhrbier A, Jaffar-Bandjee M-C, Gasque P. 2012. Arthritogenic alphaviruses-an overview. Nat Rev Rheumatol 8:420-429. http://dx.doi.org/10.1038/nrrheum.2012.64.
67. Allison AC. 2000. Immunosuppressive drugs: the first 50 years and a glance forward. Immunopharmacology 47:63-83. http://dx.doi.org/10.1016/S0162-3109(00)00186-7.