Expression of Ifnlr1 on intestinal epithelial cells is critical to the antiviral effects of interferon lambda against norovirus and reovirus

Journal of Virology

Volumn 91, Issue 7, 2017, Pages

  Baldridge, Megan T ^a   Lee, Sanghyun ^a   Brown, Judy J ^b   McAllister, Nicole ^c   Urbanek, Kelly ^c   Dermody, Terence S ^c   Nice, Timothy J ^d   Virgin, Herbert W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Innate immunity; Interferons; Mucosal immunity; Norovirus; Reovirus

Indexed keywords

INTERFERON LAMBDA; RECOMBINANT INTERFERON; UNCLASSIFIED DRUG; IFNLR1 PROTEIN, MOUSE; INTERFERON RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; C57BL 6 MOUSE; COLON; CONTROLLED STUDY; FECES; GENE EXPRESSION; GENE LOCUS; IFI44 GENE; IFIT1 GENE; IFNLR1 GENE; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; LAMINA PROPRIA; MOUSE; NONHUMAN; NOROVIRUS INFECTION; OAS1A GENE; RAG1-/- MOUSE; REOVIRUS INFECTION; SMALL INTESTINE; UPREGULATION; VIRUS GENE; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS SHEDDING; WILD TYPE; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CALICIVIRUS INFECTION; CELL LINE; EPITHELIUM CELL; IMMUNOLOGY; INTESTINE MUCOSA; KNOCKOUT MOUSE; LARGE INTESTINE; MAMMALIAN ORTHOREOVIRUS; METABOLISM; NOROVIRUS; PHYSIOLOGY; VIROLOGY;

ANIMALS; CALICIVIRIDAE INFECTIONS; CELL LINE; EPITHELIAL CELLS; IMMUNITY, INNATE; INTESTINAL MUCOSA; INTESTINE, LARGE; INTESTINE, SMALL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NOROVIRUS; ORGAN SPECIFICITY; ORTHOREOVIRUS, MAMMALIAN; RECEPTORS, INTERFERON; REOVIRIDAE INFECTIONS; VIRUS SHEDDING;

EID: 85015241826     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02079-16     Document Type: Article

References (58)

1. Karst SM. 2010. Pathogenesis of noroviruses, emerging RNA viruses. Viruses 2:748-781. https://doi.org/10.3390/v2030748.
2. Glass RI, Parashar UD, Estes MK. 2009. Norovirus gastroenteritis. N Engl J Med 361:1776-1785. https://doi.org/10.1056/NEJMra0804575.
3. Koo HL, Ajami N, Atmar RL, DuPont HL. 2010. Noroviruses: the leading cause of gastroenteritis worldwide. Discov Med 10:61-70.
4. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17:7-15. https://doi.org/10.3201/eid1701.P11101.
5. Lazear HM, Nice TJ, Diamond MS. 2015. Interferon-lambda: immune functions at barrier surfaces and beyond. Immunity 43:15-28. https://doi.org/10.1016/j.immuni.2015.07.001.
6. Hermant P, Michiels T. 2014. Interferon-lambda in the context of viral infections: production, response and therapeutic implications. J Innate Immun 6:563-574. https://doi.org/10.1159/000360084.
7. Egli A, Santer DM, O'Shea D, Tyrrell DL, Houghton M. 2014. The impact of the interferon-lambda family on the innate and adaptive immune response to viral infections. Emerg Microbes Infect 3:e51. https://doi.org/10.1038/emi.2014.51.
8. Nice TJ, Baldridge MT, McCune BT, Norman JM, Lazear HM, Artyomov M, Diamond MS, Virgin HW. 2015. Interferon-lambda cures persistent murine norovirus infection in the absence of adaptive immunity. Science 347:269-273. https://doi.org/10.1126/science.1258100.
9. Pott J, Mahlakoiv T, Mordstein M, Duerr CU, Michiels T, Stockinger S, Staeheli P, Hornef MW. 2011. IFN-lambda determines the intestinal epithelial antiviral host defense. Proc Natl Acad Sci U S A 108:7944-7949. https://doi.org/10.1073/pnas.1100552108.
10. Lazear HM, Daniels BP, Pinto AK, Huang AC, Vick SC, Doyle SE, Gale M, Jr, Klein RS, Diamond MS. 2015. Interferon-lambda restricts West Nile virus neuroinvasion by tightening the blood-brain barrier. Sci Transl Med 7:284ra259.
11. Muir AJ, Arora S, Everson G, Flisiak R, George J, Ghalib R, Gordon SC, Gray T, Greenbloom S, Hassanein T, Hillson J, Horga MA, Jacobson IM, Jeffers L, Kowdley KV, Lawitz E, Lueth S, Rodriguez-Torres M, Rustgi V, Shemanski L, Shiffman ML, Srinivasan S, Vargas HE, Vierling JM, Xu D, Lopez-Talavera JC, Zeuzem S, EMERGE Study Group. 2014. A randomized phase 2b study of peginterferon lambda-1a for the treatment of chronic HCV infection. J Hepatol 61:1238-1246. https://doi.org/10.1016/j.jhep .2014.07.022.
12. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP. 2003. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4:69-77. https://doi.org/10.1038/ni875.
13. 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, McKnight 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. https://doi.org/10.1038/ni873.
14. Bolen CR, Ding S, Robek MD, Kleinstein SH. 2014. Dynamic expression profiling of type I and type III interferon-stimulated hepatocytes reveals a stable hierarchy of gene expression. Hepatology 59:1262-1272. https://doi.org/10.1002/hep.26657.
15. Kohli A, Zhang X, Yang J, Russell RS, Donnelly RP, Sheikh F, Sherman A, Young H, Imamichi T, Lempicki RA, Masur H, Kottilil S. 2012. Distinct and overlapping genomic profiles and antiviral effects of Interferon-lambda and-alpha on HCV-infected and noninfected hepatoma cells. J Viral Hepat 19:843-853. https://doi.org/10.1111/j.1365-2893.2012.01610.x.
16. Baldridge MT, Nice TJ, McCune BT, Yokoyama CC, Kambal A, Wheadon M, Diamond MS, Ivanova Y, Artyomov M, Virgin HW. 2015. Commensal microbes and interferon-lambda determine persistence of enteric murine norovirus infection. Science 347:266-269. https://doi.org/10.1126/science.1258025.
17. Karst SM, Wobus CE, Goodfellow IG, Green KY, Virgin HW. 2014. Advances in norovirus biology. Cell Host Microbe 15:668-680. https://doi.org/10.1016/j.chom.2014.05.015.
18. Wobus CE, Thackray LB, Virgin HW. 2006. Murine norovirus: a model system to study norovirus biology and pathogenesis. J Virol 80: 5104-5112. https://doi.org/10.1128/JVI.02346-05.
19. Mahlakoiv T, Hernandez P, Gronke K, Diefenbach A, Staeheli P. 2015. Leukocyte-derived IFN-alpha/beta and epithelial IFN-lambda constitute a compartmentalized mucosal defense system that restricts enteric virus infections. PLoS Pathog 11:e1004782. https://doi.org/10.1371/journal.ppat.1004782.
20. Lin JD, Feng N, Sen A, Balan M, Tseng HC, McElrath C, Smirnov SV, Peng J, Yasukawa LL, Durbin RK, Durbin JE, Greenberg HB, Kotenko SV. 2016. Distinct roles of type I and type III interferons in intestinal immunity to homologous and heterologous rotavirus infections. PLoS Pathog 12: e1005600. https://doi.org/10.1371/journal.ppat.1005600.
21. Visel A, Thaller C, Eichele G. 2004. GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 32: D552-D556. https://doi.org/10.1093/nar/gkh029.
22. Diez-Roux G, Banfi S, Sultan M, Geffers L, Anand S, Rozado D, Magen A, Canidio E, Pagani M, Peluso I, Lin-Marq N, Koch M, Bilio M, Cantiello I, Verde R, De Masi C, Bianchi SA, Cicchini J, Perroud E, Mehmeti S, Dagand E, Schrinner S, Nurnberger A, Schmidt K, Metz K, Zwingmann C, Brieske N, Springer C, Hernandez AM, Herzog S, Grabbe F, Sieverding C, Fischer B, Schrader K, Brockmeyer M, Dettmer S, Helbig C, Alunni V, Battaini MA, Mura C, Henrichsen CN, Garcia-Lopez R, Echevarria D, Puelles E, Garcia-Calero E, Kruse S, Uhr M, Kauck C, Feng G, Milyaev N, Ong CK, Kumar L, Lam M, Semple CA, Gyenesei A, Mundlos S, Radelof U, Lehrach H, Sarmientos P, Reymond A, Davidson DR, Dolle P, Antonarakis SE, Yaspo ML, Martinez S, Baldock RA, Eichele G, Ballabio A. 2011. A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol 9:e1000582. https://doi.org/10.1371/journal.pbio.1000582.
23. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89:1-47. https://doi.org/10.1099/vir.0.83391-0.
24. de Weerd NA, Samarajiwa SA, Hertzog PJ. 2007. Type I interferon receptors: biochemistry and biological functions. J Biol Chem 282: 20053-20057. https://doi.org/10.1074/jbc.R700006200.
25. Sommereyns C, Paul S, Staeheli P, Michiels T. 2008. IFN-lambda (IFNlambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog 4:e1000017. https://doi.org/10.1371/journal.ppat.1000017.
26. Blazek K, Eames HL, Weiss M, Byrne AJ, Perocheau D, Pease JE, Doyle S, McCann F, Williams RO, Udalova IA. 2015. IFN-lambda resolves inflammation via suppression of neutrophil infiltration and IL-1beta production. J Exp Med 212:845-853. https://doi.org/10.1084/jem.20140995.
27. Witte K, Gruetz G, Volk HD, Looman AC, Asadullah K, Sterry W, Sabat R, Wolk K. 2009. Despite IFN-lambda receptor expression, blood immune 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. https://doi.org/10.1038/gene.2009.72.
28. Ank N, Iversen MB, Bartholdy C, Staeheli P, Hartmann R, Jensen UB, Dagnaes-Hansen F, Thomsen AR, Chen Z, Haugen H, Klucher K, Paludan SR. 2008. An important role for type III interferon (IFN-lambda/IL-28) in TLR-induced antiviral activity. J Immunol 180:2474-2485. https://doi.org/10.4049/jimmunol.180.4.2474.
29. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. 2002. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 277:33275-33283. https://doi.org/10.1074/jbc.M204935200.
30. Passegue E, Wagner EF, Weissman IL. 2004. JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell 119:431-443. https://doi.org/10.1016/j.cell.2004.10.010.
31. Stranges PB, Watson J, Cooper CJ, Choisy-Rossi CM, Stonebraker AC, Beighton RA, Hartig H, Sundberg JP, Servick S, Kaufmann G, Fink PJ, Chervonsky AV. 2007. Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity 26:629-641. https://doi.org/10.1016/j.immuni.2007.03.016.
32. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8:265-277. https://doi.org/10.1023/A:1008942828960.
33. Jakubzick C, Bogunovic M, Bonito AJ, Kuan EL, Merad M, Randolph GJ. 2008. Lymph-migrating, tissue-derived dendritic cells are minor constituents within steady-state lymph nodes. J Exp Med 205:2839-2850. https://doi.org/10.1084/jem.20081430.
34. Schwenk F, Baron U, Rajewsky K. 1995. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23:5080-5081. https://doi.org/10.1093/nar/23.24.5080.
35. Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV, Belliot G, Krug A, Mackenzie JM, Green KY, Virgin HW. 2004. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2:e432. https://doi.org/10.1371/journal.pbio.0020432.
36. Lefrancois L, Lycke N. 2001. Isolation of mouse small intestinal intraepithelial lymphocytes, Peyer's patch, and lamina propria cells. Curr Protoc Immunol Chapter 3:Unit 3.19.
37. Reference deleted.
38. Kanki H, Suzuki H, Itohara S. 2006. High-efficiency CAG-FLPe deleter mice in C57BL/6J background. Exp Anim 55:137-141. https://doi.org/10.1538/expanim.55.137.
39. Abram CL, Roberge GL, Hu Y, Lowell CA. 2014. Comparative analysis of the efficiency and specificity of myeloid-Cre deleting strains using ROSAEYFP reporter mice. J Immunol Methods 408:89-100. https://doi.org/10.1016/j.jim.2014.05.009.
40. Zhong Z, Baker JJ, Zylstra-Diegel CR, Williams BO. 2012. Lrp5 and Lrp6 play compensatory roles in mouse intestinal development. J Cell Biochem 113:31-38. https://doi.org/10.1002/jcb.23324.
41. Nice TJ, Strong DW, McCune BT, Pohl CS, Virgin HW. 2013. A singleamino-acid change in murine norovirus NS1/2 is sufficient for colonic tropism and persistence. J Virol 87:327-334. https://doi.org/10.1128/JVI.01864-12.
42. Elkhateeb E, Tag-El-Din-Hassan HT, Sasaki N, Torigoe D, Morimatsu M, Agui T. 2016. The role of mouse 2',5'-oligoadenylate synthetase 1 paralogs. Infect Genet Evol 45:393-401. https://doi.org/10.1016/j.meegid.2016.09.018.
43. Reynaud JM, Kim DY, Atasheva S, Rasalouskaya A, White JP, Diamond MS, Weaver SC, Frolova EI, Frolov I. 2015. IFIT1 differentially interferes with translation and replication of alphavirus genomes and promotes induction of type I interferon. PLoS Pathog 11:e1004863. https://doi.org/10.1371/journal.ppat.1004863.
44. Carlton-Smith C, Elliott RM. 2012. Viperin, MTAP44, and protein kinase R contribute to the interferon-induced inhibition of Bunyamwera Orthobunyavirus replication. J Virol 86:11548-11557. https://doi.org/10.1128/JVI.01773-12.
45. Crotta S, Davidson S, Mahlakoiv T, Desmet CJ, Buckwalter MR, Albert ML, Staeheli P, Wack A. 2013. Type I and type III interferons drive redundant amplification loops to induce a transcriptional signature in influenzainfected airway epithelia. PLoS Pathog 9:e1003773. https://doi.org/10.1371/journal.ppat.1003773.
46. Mordstein M, Kochs G, Dumoutier L, Renauld JC, Paludan SR, Klucher K, Staeheli P. 2008. Interferon-lambda contributes to innate immunity of mice against influenza A virus but not against hepatotropic viruses. PLoS Pathog 4:e1000151. https://doi.org/10.1371/journal.ppat.1000151.
47. Mordstein M, Neugebauer E, Ditt V, Jessen B, Rieger T, Falcone V, Sorgeloos F, Ehl S, Mayer D, Kochs G, Schwemmle M, Gunther S, Drosten C, Michiels T, Staeheli P. 2010. Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J Virol 84:5670-5677. https://doi.org/10.1128/JVI.00272-10.
48. Ank N, West H, Bartholdy C, Eriksson K, Thomsen AR, Paludan SR. 2006. Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol 80:4501-4509. https://doi.org/10.1128/JVI.80.9.4501-4509.2006.
49. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, Gonzalez-Hernandez MB, Iovine NM, Wobus CE, Vinje J, Tibbetts SA, Wallet SM, Karst SM. 2014. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346:755-759. https://doi.org/10.1126/science.1257147.
50. Zhang B, Chassaing B, Shi Z, Uchiyama R, Zhang Z, Denning TL, Crawford SE, Pruijssers AJ, Iskarpatyoti JA, Estes MK, Dermody TS, Ouyang W, Williams IR, Vijay-Kumar M, Gewirtz AT. 2014. Viral infection. Prevention and cure of rotavirus infection via TLR5/NLRC4-mediated production of IL-22 and IL-18. Science 346:861-865.
51. Strong DW, Thackray LB, Smith TJ, Virgin HW. 2012. Protruding domain of capsid protein is necessary and sufficient to determine murine norovirus replication and pathogenesis in vivo. J Virol 86:2950-2958. https://doi.org/10.1128/JVI.07038-11.
52. Kobayashi T, Antar AA, Boehme KW, Danthi P, Eby EA, Guglielmi KM, Holm GH, Johnson EM, Maginnis MS, Naik S, Skelton WB, Wetzel JD, Wilson GJ, Chappell JD, Dermody TS. 2007. A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell Host Microbe 1:147-157. https://doi.org/10.1016/j.chom.2007.03.003.
53. Kobayashi T, Ooms LS, Ikizler M, Chappell JD, Dermody TS. 2010. An improved reverse genetics system for mammalian orthoreoviruses. Virology 398:194-200. https://doi.org/10.1016/j.virol.2009.11.037.
54. Virgin HWT, Bassel-Duby R, Fields BN, Tyler KL. 1988. Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J Virol 62:4594-4604.
55. Furlong DB, Nibert ML, Fields BN. 1988. Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J Virol 62:246-256.
56. Smith RE, Zweerink HJ, Joklik WK. 1969. Polypeptide components of virions, top component and cores of reovirus type 3. Virology 39: 791-810. https://doi.org/10.1016/0042-6822(69)90017-8.
57. Cadwell K, Patel KK, Maloney NS, Liu TC, Ng AC, Storer CE, Head RD, Xavier R, Stappenbeck TS, Virgin HW. 2010. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 141:1135-1145. https://doi.org/10.1016/j.cell.2010.05.009.
58. Baert L, Wobus CE, Van Coillie E, Thackray LB, Debevere J, Uyttendaele M. 2008. Detection of murine norovirus 1 by using plaque assay, transfection assay, and real-time reverse transcription-PCR before and after heat exposure. Appl Environ Microbiol 74:543-546. https://doi.org/10.1128/AEM.01039-07.