Induction of an antiviral state and attenuated coxsackievirus replication in type III interferon-treated primary human pancreatic islets

Journal of Virology

Volumn 87, Issue 13, 2013, Pages 7646-7654

  Lind, Katharina ^a   Richardson, Sarah J ^b   Leete, Pia ^b   Morgan, Noel G ^b   Korsgren, Olle ^c   Flodström Tullberga, Malin ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERFERON RECEPTOR; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 10 RECEPTOR 2; LAMBDA INTERFERON; LAMBDA INTERFERON RECEPTOR 1; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; COXSACKIE VIRUS; COXSACKIE VIRUS INFECTION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; UPREGULATION; VIRUS REPLICATION;

EID: 84880336910     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03431-12     Document Type: Article

References (42)

1. Isaacs A, Lindenmann J. 1957. Virus interference. I. The interferon. Proc. R. Soc. Lond. B Biol. Sci. 147:258-267.
2. de Weerd NA, Nguyen T. 2012. The interferons and their receptors- distribution and regulation. Immunol. Cell Biol. 90:483-491.
3. Stetson DB, Medzhitov R. 2006. Type I interferons in host defense. Immunity 25:373-381.
4. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP. 2003. IFNlambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4:69-77.
5. Sheppard P, Kindsvogel W, Xu W, Henderson K, Schlutsmeyer S, Whitmore TE, Kuestner R, Garrigues U, Birks C, Roraback J, Ostrander C, Dong D, Shin J, Presnell S, Fox B, Haldeman B, Cooper E, Taft D, Gilbert T, Grant FJ, Tackett M, Krivan W, Mc-Knight G, Clegg C, Foster D, Klucher KM. 2003. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 4:63-68.
6. Kotenko SV. 2011. IFN-lambdas. Curr. Opin. Immunol. 23:583-590.
7. Li M, Liu X, Zhou Y, Su SB. 2009. Interferon-lambdas: the modulators of antivirus, antitumor, and immune responses. J. Leukoc. Biol. 86:23-32.
8. Hou W, Wang X, Ye L, Zhou L, Yang ZQ, Riedel E, Ho WZ. 2009. Lambda interferon inhibits human immunodeficiency virus type 1 infection of macrophages. J. Virol. 83:3834-3842.
9. Vareille M, Kieninger E, Alves MP, Kopf BS, Moller A, Geiser T, Johnston SL, Edwards MR, Regamey N. 2012. Impaired type I and type III interferon induction and rhinovirus control in human cystic fibrosis airway epithelial cells. Thorax 67:517-525.
10. Sommereyns C, Paul S, Staeheli P, Michiels T. 2008. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 4:e1000017. doi:10.1371 /journal.ppat.1000017.
11. Witte K, Gruetz G, Volk HD, Looman AC, Asadullah K, Sterry W, Sabat R, Wolk K. 2009. Despite IFN-lambda receptor expression, bloodimmune cells, but not keratinocytes or melanocytes, have an impaired response to type III interferons: implications for therapeutic applications of these cytokines. Genes Immun. 10:702-714.
12. Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed). 2007. Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
13. Knip M, Simell O. 2012. Environmental triggers of type 1 diabetes. Cold Spring Harbor Perspect. Med. 2:a007690. doi:10.1101/cshperspect.a007690.
14. Yeung WC, Rawlinson WD, Craig ME. 2011. Enterovirus infection and type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. BMJ 342:d35. doi:10.1136/bmj.d35.
15. Dotta F, Censini S, van Halteren AG, Marselli L, Masini M, Dionisi S, Mosca F, Boggi U, Muda AO, Prato SD, Elliott JF, Covacci A, Rappuoli R, Roep BO, Marchetti P. 2007. Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc. Natl. Acad. Sci. U.S.A. 104:5115-5120.
16. Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG. 2009. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia 52:1143-1151.
17. Ylipaasto P, Klingel K, Lindberg AM, Otonkoski T, Kandolf R, Hovi T, Roivainen M. 2004. Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet beta cells. Diabetologia 47:225-239.
18. Roivainen M, Ylipaasto P, Savolainen C, Galama J, Hovi T, Otonkoski T. 2002. Functional impairment and killing of human beta cells by enteroviruses: the capacity is shared by a wide range of serotypes, but the extent is a characteristic of individual virus strains. Diabetologia 45:693-702.
19. Flodstrom M, Maday A, Balakrishna D, Cleary MM, Yoshimura A, Sarvetnick N. 2002. Target cell defense prevents the development of diabetes after viral infection. Nat. Immunol. 3:373-382.
20. Flodstrom M, Tsai D, Fine C, Maday A, Sarvetnick N. 2003. Diabetogenic potential of human pathogens uncovered in experimentally permissive beta-cells. Diabetes 52:2025-2034.
21. Horwitz MS, Fine C, Ilic A, Sarvetnick N. 2001. Requirements for viral-mediated autoimmune diabetes: beta-cell damage and immune infiltration. J. Autoimmun. 16:211-217.
22. Kanno T, Kim K, Kono K, Drescher KM, Chapman NM, Tracy S. 2006. Group B coxsackievirus diabetogenic phenotype correlates with replication efficiency. J. Virol. 80:5637-5643.
23. Lind K, Huhn MH, Flodstrom-Tullberg M. 2012. Immunology in the clinic review series; focus on type 1 diabetes and viruses: the innate immune response to enteroviruses and its possible role in regulating type 1 diabetes. Clin. Exp. Immunol. 168:30-38.
24. Hultcrantz M, Huhn MH, Wolf M, Olsson A, Jacobson S, Williams BR, Korsgren O, Flodstrom-Tullberg M. 2007. Interferons induce an antiviral state in human pancreatic islet cells. Virology 367:92-101.
25. Goto M, Eich TM, Felldin M, Foss A, Kallen R, Salmela K, Tibell A, Tufveson G, Fujimori K, Engkvist M, Korsgren O. 2004. Refinement of the automated method for human islet isolation and presentation of a closed system for in vitro islet culture. Transplantation 78:1367-1375.
26. Johansson U, Olsson A, Gabrielsson S, Nilsson B, Korsgren O. 2003. Inflammatory mediators expressed in human islets of Langerhans: implications for islet transplantation. Biochem. Biophys. Res. Commun. 308: 474-479.
27. Tian RR, Guo HX, Wei JF, Yang CK, He SH, Wang JH. 2012. IFNlambda inhibits HIV-1 integration and post-transcriptional events in vitro, but there is only limited in vivo repression of viral production. Antiviral Res. 95:57-65.
28. Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N. 1998. Diabetes induced by coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat. Med. 4:781-785.
29. Diegelmann J, Beigel F, Zitzmann K, Kaul A, Goke B, Auernhammer CJ, Bartenschlager R, Diepolder HM, Brand S. 2010. Comparative analysis of the lambda-interferons IL-28A and IL-29 regarding their transcriptome and their antiviral properties against hepatitis C virus. PLoS One 5:e15200. doi:10.1371/journal.pone.0015200.
30. Ylipaasto P, Smura T, Gopalacharyulu P, Paananen A, Seppanen-Laakso T, Kaijalainen S, Ahlfors H, Korsgren O, Lakey JR, Lahesmaa R, Piemonti L, Oresic M, Galama J, Roivainen M. 2012. Enterovirusinduced gene expression profile is critical for human pancreatic islet destruction. Diabetologia 55:3273-3283.
31. Rosenthal LA, Szakaly RJ, Amineva SP, Xing Y, Hill MR, Palmenberg AC, Gern JE, Sorkness RL. 2012. Lower respiratory tract infection induced by a genetically modified picornavirus in its natural murine host. PLoS One 7:e32061. doi:10.1371/journal.pone.0032061.
32. Thomas E, Gonzalez VD, Li Q, Modi AA, Chen W, Noureddin M, Rotman Y, Liang TJ. 2012. HCV infection induces a unique hepatic innate immune response associated with robust production of type III interferons. Gastroenterology 142:978-988.
33. Diaz-San Segundo F, Weiss M, Perez-Martin E, Koster MJ, Zhu J, Grubman MJ, de los Santos T. 2011. Antiviral activity of bovine type III interferon against foot-and-mouth disease virus. Virology 413:283-292.
34. Perez-Martin E, Weiss M, Diaz-San Segundo F, Pacheco JM, Arzt J, Grubman MJ, de los Santos T. 2012. Bovine type III interferon significantly delays and reduces the severity of foot-and-mouth disease in cattle. J. Virol. 86: 4477-4487.
35. Goodbourn S, Didcock L, Randall RE. 2000. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81:2341-2364.
36. Flodstrom-Tullberg M, Hultcrantz M, Stotland A, Maday A, Tsai D, Fine C, Williams B, Silverman R, Sarvetnick N. 2005. RNase L and double-stranded RNA-dependent protein kinase exert complementary roles in islet cell defense during coxsackievirus infection. J. Immunol. 174:1171-1177.
37. Haller O, Kochs G. 2011. Human MxA protein: an interferon-induced dynamin-like GTPase with broad antiviral activity. J. Interferon Cytokine Res. 31:79-87.
38. Nejentsev S, Walker N, Riches D, Egholm M, Todd JA. 2009. Rare variants of IFIH1, a gene implicated in antiviral responses, protect against type 1 diabetes. Science 324:387-389.
39. Smyth DJ, Cooper JD, Bailey R, Field S, Burren O, Smink LJ, Guja C, Ionescu-Tirgoviste C, Widmer B, Dunger DB, Savage DA, Walker NM, Clayton DG, Todd JA. 2006. A genome-wide association study of nonsynonymous SNPs identifies a type 1 diabetes locus in the interferoninduced helicase (IFIH1) region. Nat. Genet. 38:617-619.
40. Huhn MH, Mc-Cartney SA, Lind K, Svedin E, Colonna M, Flodstrom-Tullberg M. 2010. Melanoma differentiation-associated protein-5 (MDA-5) limits early viral replication but is not essential for the induction of type 1 interferons after coxsackievirus infection. Virology 401:42-48.
41. Wang JP, Cerny A, Asher DR, Kurt-Jones EA, Bronson RT, Finberg RW. 2010. MDA5 and MAVS mediate type I interferon responses to coxsackie B virus. J. Virol. 84:254-260.
42. Shigemoto T, Kageyama M, Hirai R, Zheng J, Yoneyama M, Fujita T. 2009. Identification of loss of function mutations in human genes encoding RIG-I and MDA5: implications for resistance to type I diabetes. J. Biol. Chem. 284:13348-13354.