Immunomodulation by Enteric Viruses

Literature Cited

1. 1.

   Aliabadi N, Tate JE, Haynes AK, Parashar UD. 2015. Sustained decrease in laboratory detection of rotavirus after implementation of routine vaccination—United States, 2000–2014. Morb. Mortal. Wkly. Rep. 64:13337–42
   [Google Scholar]
2. 2.

   Leshem E, Moritz RE, Curns AT, Zhou F, Tate JE et al. 2014. Rotavirus vaccines and health care utilization for diarrhea in the United States (2007–2011). Pediatrics 134:115–23
   [Google Scholar]
3. 3.

   Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L et al. 2015. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat. Med. 21:101228–34
   [Google Scholar]
4. 4.

   Liang G, Zhao C, Zhang H, Mattei L, Sherrill-Mix S et al. 2020. The stepwise assembly of the neonatal virome is modulated by breastfeeding. Nature 581:7809470–74
   [Google Scholar]
5. 5.

   Gogokhia L, Buhrke K, Bell R, Hoffman B, Brown DG et al. 2019. Expansion of bacteriophages is linked to aggravated intestinal inflammation and colitis. Cell Host Microbe 25:2285–99.e8
   [Google Scholar]
6. 6.

   Li Y, Handley SA, Baldridge MT. 2021. The dark side of the gut: virome-host interactions in intestinal homeostasis and disease. J. Exp. Med. 218:5e20201044
   [Google Scholar]
7. 7.

   Nishio J, Negishi H, Yasui-Kato M, Miki S, Miyanaga K et al. 2021. Identification and characterization of a novel Enterococcus bacteriophage with potential to ameliorate murine colitis. Sci. Rep. 11:120231
   [Google Scholar]
8. 8.

   Cadwell K, Marchiando AM. 2016. Function of epithelial barriers. Encyclopedia of Cell Biology, Vol. 3 RA Bradshaw, PD Stahl 687–94. Waltham, MA: Academic
   [Google Scholar]
9. 9.

   Vehik K, Lynch KF, Wong MC, Tian X, Ross MC et al. 2019. Prospective virome analyses in young children at increased genetic risk for type 1 diabetes. Nat. Med. 25:121865–72
   [Google Scholar]
10. 10.

    Reyes A, Blanton LV, Cao S, Zhao G, Manary M et al. 2015. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. PNAS 112:3811941–46
    [Google Scholar]
11. 11.

    Ghosh S, Kumar M, Santiana M, Mishra A, Zhang M et al. 2022. Enteric viruses replicate in salivary glands and infect through saliva. Nature 607:7918345–50
    [Google Scholar]
12. 12.

    Desselberger U. 2014. Rotaviruses. Virus Res. 190:75–96
    [Google Scholar]
13. 13.

    Petrie BL, Greenberg HB, Graham DY, Estes MK. 1984. Ultrastructural localization of rotavirus antigens using colloidal gold. Virus Res. 1:2133–52
    [Google Scholar]
14. 14.

    Chang-Graham AL, Perry JL, Engevik MA, Engevik KA, Scribano FJ et al. 2020. Rotavirus induces intercellular calcium waves through ADP signaling. Science 370:6519eabc3621
    [Google Scholar]
15. 15.

    Bomidi C, Robertson M, Coarfa C, Estes MK, Blutt SE. 2021. Single-cell sequencing of rotavirus-infected intestinal epithelium reveals cell-type specific epithelial repair and tuft cell infection. PNAS 118:45e2112814118
    [Google Scholar]
16. 16.

    Riddle MS, Chen WH, Kirkwood CD, MacLennan CA. 2018. Update on vaccines for enteric pathogens. Clin. Microbiol. Infect 24:101039–45
    [Google Scholar]
17. 17.

    Wu AG, Pruijssers AJ, Brown JJ, Stencel-Baerenwald JE, Sutherland DM et al. 2018. Age-dependent susceptibility to reovirus encephalitis in mice is influenced by maturation of the type-I interferon response. Pediatr. Res. 83:51057–66
    [Google Scholar]
18. 18.

    Winder N, Gohar S, Muthana M. 2022. Norovirus: an overview of virology and preventative measures. Viruses 14:122811
    [Google Scholar]
19. 19.

    Bok K, Green KY. 2012. Norovirus gastroenteritis in immunocompromised patients. N. Engl. J. Med. 367:222126–32
    [Google Scholar]
20. 20.

    Green KY, Kaufman SS, Nagata BM, Chaimongkol N, Kim DY et al. 2020. Human norovirus targets enteroendocrine epithelial cells in the small intestine. Nat. Commun. 11:12759
    [Google Scholar]
21. 21.

    Roth AN, Karst SM. 2016. Norovirus mechanisms of immune antagonism. Curr. Opin. Virol. 16:24–30
    [Google Scholar]
22. 22.

    Karst SM, Wobus CE, Goodfellow IG, Green KY, Virgin HW. 2014. Advances in norovirus biology. Cell Host Microbe 15:6668–80
    [Google Scholar]
23. 23.

    Thorne LG, Goodfellow IG. 2014. Norovirus gene expression and replication. J. Gen. Virol. 95:2278–91
    [Google Scholar]
24. 24.

    Ettayebi K, Crawford SE, Murakami K, Broughman JR, Karandikar U et al. 2016. Replication of human noroviruses in stem cell-derived human enteroids. Science 353:63061387–93
    [Google Scholar]
25. 25.

    Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR et al. 2014. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346:6210755–59
    [Google Scholar]
26. 26.

    Monedero V, Buesa J, Rodríguez-Díaz J. 2018. The interactions between host glycobiology, bacterial microbiota, and viruses in the gut. Viruses 10:296
    [Google Scholar]
27. 27.

    Lindesmith LC, Donaldson EF, LoBue AD, Cannon JL, Zheng DP et al. 2008. Mechanisms of GII.4 norovirus persistence in human populations. PLOS Med. 5:2e31
    [Google Scholar]
28. 28.

    Wilen CB, Lee S, Hsieh LL, Orchard RC, Desai C et al. 2018. Tropism for tuft cells determines immune promotion of norovirus pathogenesis. Science 360:6385204–8
    [Google Scholar]
29. 29.

    Strine MS, Alfajaro MM, Graziano VR, Song J, Hsieh LL et al. 2022. Tuft-cell-intrinsic and -extrinsic mediators of norovirus tropism regulate viral immunity. Cell Rep. 41:6111593
    [Google Scholar]
30. 30.

    Graziano VR, Alfajaro MM, Schmitz CO, Filler RB, Strine MS et al. 2021. CD300lf conditional knockout mouse reveals strain-specific cellular tropism of murine norovirus. J. Virol. 95:3e01652–20
    [Google Scholar]
31. 31.

    Orchard RC, Wilen CB, Doench JG, Baldridge MT, McCune BT et al. 2016. Discovery of a proteinaceous cellular receptor for a norovirus. Science 353:6302933–36
    [Google Scholar]
32. 32.

    Haga K, Fujimoto A, Takai-Todaka R, Miki M, Doan YH et al. 2016. Functional receptor molecules CD300lf and CD300ld within the CD300 family enable murine noroviruses to infect cells. PNAS 113:41E6248–55
    [Google Scholar]
33. 33.

    Mumphrey SM, Changotra H, Moore TN, Heimann-Nichols ER, Wobus CE et al. 2007. Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J. Virol. 81:73251–63
    [Google Scholar]
34. 34.

    Kahan SM, Liu G, Reinhard MK, Hsu CC, Livingston RS, Karst SM. 2011. Comparative murine norovirus studies reveal a lack of correlation between intestinal virus titers and enteric pathology. Virology 421:2202–10
    [Google Scholar]
35. 35.

    Roth AN, Helm EW, Mirabelli C, Kirsche E, Smith JC et al. 2020. Norovirus infection causes acute self-resolving diarrhea in wild-type neonatal mice. Nat. Commun. 11:12968
    [Google Scholar]
36. 36.

    Helm EW, Peiper AM, Phillips M, Williams CG, Sherman MB et al. 2022. Environmentally-triggered contraction of the norovirus virion determines diarrheagenic potential. Front. Immunol. 13:1043746
    [Google Scholar]
37. 37.

    Becker-Dreps S, González F, Bucardo F. 2020. Sapovirus: an emerging cause of childhood diarrhea. Curr. Opin. Infect. Dis. 33:5388–97
    [Google Scholar]
38. 38.

    Cortez V, Meliopoulos VA, Karlsson EA, Hargest V, Johnson C, Schultz-Cherry S. 2017. Astrovirus biology and pathogenesis. Annu. Rev. Virol. 4:327–48
    [Google Scholar]
39. 39.

    Cortez V, Boyd DF, Crawford JC, Sharp B, Livingston B et al. 2020. Astrovirus infects actively secreting goblet cells and alters the gut mucus barrier. Nat. Commun. 11:12097
    [Google Scholar]
40. 40.

    Ingle H, Hassan E, Gawron J, Mihi B, Li Y et al. 2021. Murine astrovirus tropism for goblet cells and enterocytes facilitates an IFN-λ response in vivo and in enteroid cultures. Mucosal Immunol. 14:3751–61
    [Google Scholar]
41. 41.

    Kolawole AO, Mirabelli C, Hill DR, Svoboda SA, Janowski AB et al. 2019. Astrovirus replication in human intestinal enteroids reveals multi-cellular tropism and an intricate host innate immune landscape. PLOS Pathog. 15:10e1008057
    [Google Scholar]
42. 42.

    Dhingra A, Hage E, Ganzenmueller T, Böttcher S, Hofmann J et al. 2019. Molecular evolution of human adenovirus (HAdV) species C. Sci. Rep. 9:11039
    [Google Scholar]
43. 43.

    Kosulin K. 2019. Intestinal HAdV infection: tissue specificity, persistence, and implications for antiviral therapy. Viruses 11:9804
    [Google Scholar]
44. 44.

    Wells AI, Coyne CB. 2019. Enteroviruses: a gut-wrenching game of entry, detection, and evasion. Viruses 11:5460
    [Google Scholar]
45. 45.

    Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM et al. 2011. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334:6053249–52
    [Google Scholar]
46. 46.

    Robinson CM, Jesudhasan PR, Pfeiffer JK. 2014. Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell Host Microbe 15:136–46
    [Google Scholar]
47. 47.

    Ida-Hosonuma M, Iwasaki T, Yoshikawa T, Nagata N, Sato Y et al. 2005. The alpha/beta interferon response controls tissue tropism and pathogenicity of poliovirus. J. Virol. 79:74460–69
    [Google Scholar]
48. 48.

    Hird TR, Grassly NC. 2012. Systematic review of mucosal immunity induced by oral and inactivated poliovirus vaccines against virus shedding following oral poliovirus challenge. PLOS Pathog. 8:4e1002599
    [Google Scholar]
49. 49.

    Odenwald MA, Paul S. 2022. Viral hepatitis: past, present, and future. World J. Gastroenterol. 28:141405–29
    [Google Scholar]
50. 50.

    Bird SW, Maynard ND, Covert MW, Kirkegaard K. 2014. Nonlytic viral spread enhanced by autophagy components. PNAS 111:3613081–86
    [Google Scholar]
51. 51.

    Chen Y-H, Du W, Hagemeijer MC, Takvorian PM, Pau C et al. 2015. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 160:4619–30
    [Google Scholar]
52. 52.

    Taylor MP, Burgon TB, Kirkegaard K, Jackson WT. 2009. Role of microtubules in extracellular release of poliovirus. J. Virol. 83:136599–609
    [Google Scholar]
53. 53.

    Feng Z, Hensley L, McKnight KL, Hu F, Madden V et al. 2013. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496:7445367–71
    [Google Scholar]
54. 54.

    Robinson SM, Tsueng G, Sin J, Mangale V, Rahawi S et al. 2014. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLOS Pathog. 10:4e1004045
    [Google Scholar]
55. 55.

    Dahmane S, Shankar K, Carlson L-A. 2023. A 3D view of how enteroviruses hijack autophagy. Autophagy 19:72156–58
    [Google Scholar]
56. 56.

    Santiana M, Ghosh S, Ho BA, Rajasekaran V, Du W-L et al. 2018. Vesicle-cloaked virus clusters are optimal units for inter-organismal viral transmission. Cell Host Microbe 24:2208–20.e8
    [Google Scholar]
57. 57.

    Patro ARK. 2019. Subversion of immune response by human cytomegalovirus. Front. Immunol. 10:1155
    [Google Scholar]
58. 58.

    Dennis EA, Smythies LE, Grabski R, Li M, Ballestas ME et al. 2018. Cytomegalovirus promotes intestinal macrophage-mediated mucosal inflammation through induction of Smad7. Mucosal Immunol. 11:61694–704
    [Google Scholar]
59. 59.

    Deeks SG, Overbaugh J, Phillips A, Buchbinder S. 2015. HIV infection. Nat. Rev. Dis. Primers 1:115035
    [Google Scholar]
60. 60.

    Cheung KS, Hung IFN, Chan PPY, Lung KC, Tso E et al. 2020. Gastrointestinal manifestations of SARS-CoV-2 infection and virus load in fecal samples from a Hong Kong cohort: systematic review and meta-analysis. Gastroenterology 159:181–95
    [Google Scholar]
61. 61.

    Redd WD, Zhou JC, Hathorn KE, McCarty TR, Bazarbashi AN et al. 2020. Prevalence and characteristics of gastrointestinal symptoms in patients with severe acute respiratory syndrome coronavirus 2 infection in the United States: a multicenter cohort study. Gastroenterology 159:2765–67.e2
    [Google Scholar]
62. 62.

    Ye L, Yang Z, Liu J, Liao L, Wang F. 2021. Digestive system manifestations and clinical significance of coronavirus disease 2019: a systematic literature review. J. Gastroenterol. Hepatol. 36:61414–22
    [Google Scholar]
63. 63.

    Livanos AE, Jha D, Cossarini F, Gonzalez-Reiche AS, Tokuyama M et al. 2021. Intestinal host response to SARS-CoV-2 infection and COVID-19 outcomes in patients with gastrointestinal symptoms. Gastroenterology 160:72435–50.e34
    [Google Scholar]
64. 64.

    Britton GJ, Chen-Liaw A, Cossarini F, Livanos AE, Spindler MP et al. 2021. Limited intestinal inflammation despite diarrhea, fecal viral RNA and SARS-CoV-2-specific IgA in patients with acute COVID-19. Sci. Rep. 11:113308
    [Google Scholar]
65. 65.

    Morone G, Palomba A, Iosa M, Caporaso T, de Angelis D et al. 2020. Incidence and persistence of viral shedding in COVID-19 post-acute patients with negativized pharyngeal swab: a systematic review. Front. Med. 7:562
    [Google Scholar]
66. 66.

    Lamers MM, Beumer J, van der Vaart J, Knoops K, Puschhof J et al. 2020. SARS-CoV-2 productively infects human gut enterocytes. Science 369:649950–54
    [Google Scholar]
67. 67.

    Stanifer ML, Kee C, Cortese M, Zumaran CM, Triana S et al. 2020. Critical role of type III interferon in controlling SARS-CoV-2 infection in human intestinal epithelial cells. Cell Rep. 32:1107863
    [Google Scholar]
68. 68.

    Jang KK, Kaczmarek ME, Dallari S, Chen Y-H, Tada T et al. 2022. Variable susceptibility of intestinal organoid-derived monolayers to SARS-CoV-2 infection. PLOS Biol. 20:3e3001592
    [Google Scholar]
69. 69.

    Karki R, Sharma BR, Tuladhar S, Williams EP, Zalduondo L et al. 2021. Synergism of TNF-α and IFN-γ triggers inflammatory cell death, tissue damage, and mortality in SARS-CoV-2 infection and cytokine shock syndromes. Cell 184:1149–68.e17
    [Google Scholar]
70. 70.

    Bernard-Raichon L, Venzon M, Klein J, Axelrad JE, Zhang C et al. 2022. Gut microbiome dysbiosis in antibiotic-treated COVID-19 patients is associated with microbial translocation and bacteremia. Nat. Commun. 13:15926
    [Google Scholar]
71. 71.

    Sencio V, Machado MG, Trottein F. 2021. The lung-gut axis during viral respiratory infections: the impact of gut dysbiosis on secondary disease outcomes. Mucosal Immunol. 14:2296–304
    [Google Scholar]
72. 72.

    Sencio V, Gallerand A, Machado MG, Deruyter L, Heumel S et al. 2021. Influenza virus infection impairs the gut's barrier properties and favors secondary enteric bacterial infection through reduced production of short-chain fatty acids. Infect. Immun. 89:9e0073420
    [Google Scholar]
73. 73.

    Peterson LW, Artis D. 2014. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 14:3141–53
    [Google Scholar]
74. 74.

    Delorme-Axford E, Coyne CB. 2011. The actin cytoskeleton as a barrier to virus infection of polarized epithelial cells. Viruses 3:122462–77
    [Google Scholar]
75. 75.

    Shi Z, Zou J, Zhang Z, Zhao X, Noriega J et al. 2019. Segmented filamentous bacteria prevent and cure rotavirus infection. Cell 179:3644–58.e13
    [Google Scholar]
76. 76.

    Bolsega S, Basic M, Smoczek A, Buettner M, Eberl C et al. 2019. Composition of the intestinal microbiota determines the outcome of virus-triggered colitis in mice. Front. Immunol. 10:1708
    [Google Scholar]
77. 77.

    Olmsted SS, Padgett JL, Yudin AI, Whaley KJ, Moench TR, Cone RA. 2001. Diffusion of macromolecules and virus-like particles in human cervical mucus. Biophys. J. 81:41930–37
    [Google Scholar]
78. 78.

    Boshuizen JA, Reimerink JHJ, Korteland-Van Male AM, van Ham VJJ, Bouma J et al. 2005. Homeostasis and function of goblet cells during rotavirus infection in mice. Virology 337:2210–21
    [Google Scholar]
79. 79.

    Engevik MA, Danhof HA, Auchtung J, Endres BT, Ruan W et al. 2021. Fusobacterium nucleatum adheres to Clostridioides difficile via the RadD adhesin to enhance biofilm formation in intestinal mucus. Gastroenterology 160:41301–14.e8
    [Google Scholar]
80. 80.

    Smith JG, Nemerow GR. 2008. Mechanism of adenovirus neutralization by human α-defensins. Cell Host Microbe 3:111–19
    [Google Scholar]
81. 81.

    Smith JG, Silvestry M, Lindert S, Lu W, Nemerow GR, Stewart PL. 2010. Insight into the mechanisms of adenovirus capsid disassembly from studies of defensin neutralization. PLOS Pathog. 6:6e1000959
    [Google Scholar]
82. 82.

    Wilson SS, Bromme BA, Holly MK, Wiens ME, Gounder AP et al. 2017. Alpha-defensin-dependent enhancement of enteric viral infection. PLOS Pathog. 13:6e1006446
    [Google Scholar]
83. 83.

    Gounder AP, Myers ND, Treuting PM, Bromme BA, Wilson SS et al. 2016. Defensins potentiate a neutralizing antibody response to enteric viral infection. PLOS Pathog. 12:3e1005474
    [Google Scholar]
84. 84.

    Turula H, Wobus C. 2018. The role of the polymeric immunoglobulin receptor and secretory immunoglobulins during mucosal infection and immunity. Viruses 10:5237
    [Google Scholar]
85. 85.

    Yel L. 2010. Selective IgA deficiency. J. Clin. Immunol. 30:110–16
    [Google Scholar]
86. 86.

    Metzger R, Krug A, Eisenächer K. 2018. Enteric virome sensing—its role in intestinal homeostasis and immunity. Viruses 10:4146
    [Google Scholar]
87. 87.

    Price AE, Shamardani K, Lugo KA, Deguine J, Roberts AW et al. 2018. A map of Toll-like receptor expression in the intestinal epithelium reveals distinct spatial, cell type-specific, and temporal patterns. Immunity 49:3560–75.e6
    [Google Scholar]
88. 88.

    Xing J, Zhou X, Fang M, Zhang E, Minze LJ, Zhang Z. 2021. DHX15 is required to control RNA virus-induced intestinal inflammation. Cell Rep. 35:12109205
    [Google Scholar]
89. 89.

    Wang P, Zhu S, Yang L, Cui S, Pan W et al. 2015. Nlrp6 regulates intestinal antiviral innate immunity. Science 350:6262826–30
    [Google Scholar]
90. 90.

    Zhu S, Ding S, Wang P, Wei Z, Pan W et al. 2017. Nlrp9b inflammasome restricts rotavirus infection in intestinal epithelial cells. Nature 546:7660667–70
    [Google Scholar]
91. 91.

    Lin JD, Feng N, Sen A, Balan M, Tseng HC et al. 2016. Distinct roles of type I and type III interferons in intestinal immunity to homologous and heterologous rotavirus infections. PLOS Pathog. 12:4e1005600
    [Google Scholar]
92. 92.

    van Winkle JA, Peterson ST, Kennedy EA, Wheadon MJ, Ingle H et al. 2022. Homeostatic interferon-lambda response to bacterial microbiota stimulates preemptive antiviral defense within discrete pockets of intestinal epithelium. eLife 11:e74072
    [Google Scholar]
93. 93.

    Lin S-C, Qu L, Ettayebi K, Crawford SE, Blutt SE et al. 2020. Human norovirus exhibits strain-specific sensitivity to host interferon pathways in human intestinal enteroids. PNAS 117:3823782–93
    [Google Scholar]
94. 94.

    Baldridge MT, Lee S, Brown JJ, McAllister N, Urbanek K et al. 2017. Expression of Ifnlr1 on intestinal epithelial cells is critical to the antiviral effects of interferon lambda against norovirus and reovirus. J. Virol. 91:7e02079–16
    [Google Scholar]
95. 95.

    Rocha-Pereira J, Jacobs S, Noppen S, Verbeken E, Michiels T, Neyts J. 2018. Interferon lambda (IFN-λ) efficiently blocks norovirus transmission in a mouse model. Antiviral Res. 149:7–15
    [Google Scholar]
96. 96.

    Mahlakõiv T, Hernandez P, Gronke K, Diefenbach A, Staeheli P. 2015. Leukocyte-derived IFN-α/β and epithelial IFN-λ constitute a compartmentalized mucosal defense system that restricts enteric virus infections. PLOS Pathog. 11:4e1004782
    [Google Scholar]
97. 97.

    Zhang Z, Zou J, Shi Z, Zhang B, Etienne-Mesmin L et al. 2020. IL-22-induced cell extrusion and IL-18-induced cell death prevent and cure rotavirus infection. Sci. Immunol. 5:52eabd2876
    [Google Scholar]
98. 98.

    Zhang B, Chassaing B, Shi Z, Uchiyama R, Zhang Z et al. 2014. Prevention and cure of rotavirus infection via TLR5/NLRC4-mediated production of IL-22 and IL-18. Science 346:6211861–65
    [Google Scholar]
99. 99.

    Schnepf D, Hernandez P, Mahlakõiv T, Crotta S, Sullender ME et al. 2021. Rotavirus susceptibility of antibiotic-treated mice ascribed to diminished expression of interleukin-22. PLOS ONE 16:8e0247738
    [Google Scholar]
100. 100.

     Hernández PP, Mahlakõiv T, Yang I, Schwierzeck V, Nguyen N et al. 2015. Interferon-λ and interleukin 22 act synergistically for the induction of interferon-stimulated genes and control of rotavirus infection. Nat. Immunol. 16:7698–707
     [Google Scholar]
101. 101.

     Gonzalez-Hernandez MB, Liu T, Payne HC, Stencel-Baerenwald JE, Ikizler M et al. 2014. Efficient norovirus and reovirus replication in the mouse intestine requires microfold (M) cells. J. Virol. 88:126934–43
     [Google Scholar]
102. 102.

     Franco MA, Greenberg HB. 1995. Role of B cells and cytotoxic T lymphocytes in clearance of and immunity to rotavirus infection in mice. J. Virol. 69:127800–6
     [Google Scholar]
103. 103.

     Mäkela M, Martilla J, Simell O, Ilonen J. 2004. Rotavirus-specific T-cell responses in young prospectively followed-up children. Clin. Exp. Immunol. 137:1173–78
     [Google Scholar]
104. 104.

     Dharakul T, Rott L, Greenberg HB. 1990. Recovery from chronic rotavirus infection in mice with severe combined immunodeficiency: virus clearance mediated by adoptive transfer of immune CD8⁺ T lymphocytes. J. Virol. 64:94375–82
     [Google Scholar]
105. 105.

     Chachu KA, Strong DW, LoBue AD, Wobus CE, Baric RS, Virgin HW. 2008. Antibody is critical for the clearance of murine norovirus infection. J. Virol. 82:136610–17
     [Google Scholar]
106. 106.

     Malm M, Uusi-Kerttula H, Vesikari T, Blazevic V. 2014. High serum levels of norovirus genotype-specific blocking antibodies correlate with protection from infection in children. J. Infect. Dis. 210:111755–62
     [Google Scholar]
107. 107.

     Mayassi T, Jabri B. 2018. Human intraepithelial lymphocytes. Mucosal Immunol. 11:51281–89
     [Google Scholar]
108. 108.

     Swamy M, Abeler-Dörner L, Chettle J, Mahlakõiv T, Goubau D et al. 2015. Intestinal intraepithelial lymphocyte activation promotes innate antiviral resistance. Nat. Commun. 6:17090
     [Google Scholar]
109. 109.

     Matsuzawa-Ishimoto Y, Yao X, Koide A, Ueberheide BM, Axelrad JE et al. 2022. The γδ IEL effector API5 masks genetic susceptibility to Paneth cell death. Nature 610:7932547–54
     [Google Scholar]
110. 110.

     Müller S, Bühler-Jungo M, Mueller C. 2000. Intestinal intraepithelial lymphocytes exert potent protective cytotoxic activity during an acute virus infection. J. Immunol. 164:41986–94
     [Google Scholar]
111. 111.

     Osborne LC, Monticelli LA, Nice TJ, Sutherland TE, Siracusa MC et al. 2014. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science 345:6196578–82
     [Google Scholar]
112. 112.

     Parsa R, London M, Rezende de Castro TB, Reis B, Buissant des Amorie J et al. 2022. Newly recruited intraepithelial Ly6A⁺CCR9⁺CD4⁺ T cells protect against enteric viral infection. Immunity 55:71234–1249.e6
     [Google Scholar]
113. 113.

     Zhu S, Jones MK, Hickman D, Han S, Reeves W, Karst SM. 2016. Norovirus antagonism of B-cell antigen presentation results in impaired control of acute infection. Mucosal Immunol. 9:61559–70
     [Google Scholar]
114. 114.

     Chachu KA, LoBue AD, Strong DW, Baric RS, Virgin HW. 2008. Immune mechanisms responsible for vaccination against and clearance of mucosal and lymphatic norovirus infection. PLOS Pathog. 4:12e1000236
     [Google Scholar]
115. 115.

     Tomov VT, Osborne LC, Dolfi DV, Sonnenberg GF, Monticelli LA et al. 2013. Persistent enteric murine norovirus infection is associated with functionally suboptimal virus-specific CD8 T cell responses. J. Virol. 87:127015–31
     [Google Scholar]
116. 116.

     Labarta-Bajo L, Nilsen SP, Humphrey G, Schwartz T, Sanders K et al. 2020. Type I IFNs and CD8 T cells increase intestinal barrier permeability after chronic viral infection. J. Exp. Med. 217:12e20192276
     [Google Scholar]
117. 117.

     Schorer M, Lambert K, Rakebrandt N, Rost F, Kao K-C et al. 2020. Rapid expansion of Treg cells protects from collateral colitis following a viral trigger. Nat. Commun. 11:11522
     [Google Scholar]
118. 118.

     Macleod BL, Elsaesser HJ, Snell LM, Dickson RJ, Guo M et al. 2020. A network of immune and microbial modifications underlies viral persistence in the gastrointestinal tract. J. Exp. Med. 217:12e20191473
     [Google Scholar]
119. 119.

     Kim B, Feng N, Narváez CF, He X-S, Eo SK et al. 2008. The influence of CD4⁺ CD25⁺ Foxp3⁺ regulatory T cells on the immune response to rotavirus infection. Vaccine 26:445601–11
     [Google Scholar]
120. 120.

     Bisaillon M, Sénéchal S, Bernier L, Lemay G. 1999. A glycosyl hydrolase activity of mammalian reovirus σ1 protein can contribute to viral infection through a mucus layer. J. Mol. Biol. 286:3759–73
     [Google Scholar]
121. 121.

     Diaz K, Hu CT, Sul Y, Bromme BA, Myers ND et al. 2020. Defensin-driven viral evolution. PLOS Pathog. 16:11e1009018
     [Google Scholar]
122. 122.

     Liu Y, Zhang Z, Zhao X, Yu R, Zhang X et al. 2014. Enterovirus 71 inhibits cellular type I interferon signaling by downregulating JAK1 protein expression. Viral Immunol. 27:6267–76
     [Google Scholar]
123. 123.

     Kane M, Case LK, Kopaskie K, Kozlova A, MacDearmid C et al. 2011. Successful transmission of a retrovirus depends on the commensal microbiota. Science 334:6053245–49
     [Google Scholar]
124. 124.

     Cornell CT, Kiosses WB, Harkins S, Whitton JL. 2007. Coxsackievirus B3 proteins directionally complement each other to downregulate surface major histocompatibility complex class I. J. Virol. 81:136785–97
     [Google Scholar]
125. 125.

     Kemball CC, Harkins S, Whitmire JK, Flynn CT, Feuer R, Whitton JL. 2009. Coxsackievirus B3 inhibits antigen presentation in vivo, exerting a profound and selective effect on the MHC class I pathway. PLOS Pathog. 5:10e1000618
     [Google Scholar]
126. 126.

     McFadden N, Bailey D, Carrara G, Benson A, Chaudhry Y et al. 2011. Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLOS Pathog. 7:12e1002413
     [Google Scholar]
127. 127.

     Borg C, Jahun AS, Thorne L, Sorgeloos F, Bailey D, Goodfellow IG. 2021. Murine norovirus virulence factor 1 (VF1) protein contributes to viral fitness during persistent infection. J. Gen. Virol. 102:9001651
     [Google Scholar]
128. 128.

     Emmott E, Sorgeloos F, Caddy SL, Vashist S, Sosnovtsev S et al. 2017. Norovirus-mediated modification of the translational landscape via virus and host-induced cleavage of translation initiation factors. Mol. Cell. Proteom. 16:4S215–29
     [Google Scholar]
129. 129.

     Fritzlar S, Jegaskanda S, Aktepe TE, Prier JE, Holz LE et al. 2018. Mouse norovirus infection reduces the surface expression of major histocompatibility complex class I proteins and inhibits CD8⁺ T cell recognition and activation. J. Virol. 92:18286–304
     [Google Scholar]
130. 130.

     Zhu S, Regev D, Watanabe M, Hickman D, Moussatche N et al. 2013. Identification of immune and viral correlates of norovirus protective immunity through comparative study of intra-cluster norovirus strains. PLOS Pathog. 9:9e1003592
     [Google Scholar]
131. 131.

     van Winkle JA, Robinson BA, Peters AM, Li L, Nouboussi RV et al. 2018. Persistence of systemic murine norovirus is maintained by inflammatory recruitment of susceptible myeloid cells. Cell Host Microbe 24:5665–76.e4
     [Google Scholar]
132. 132.

     Robinson BA, van Winkle JA, McCune BT, Peters AM, Nice TJ. 2019. Caspase-mediated cleavage of murine norovirus NS1/2 potentiates apoptosis and is required for persistent infection of intestinal epithelial cells. PLOS Pathog. 15:7e1007940
     [Google Scholar]
133. 133.

     Lee S, Wilen CB, Orvedahl A, McCune BT, Kim K-W et al. 2017. Norovirus cell tropism is determined by combinatorial action of a viral non-structural protein and host cytokine. Cell Host Microbe 22:4449–59.e4
     [Google Scholar]
134. 134.

     Lee S, Liu H, Wilen CB, Sychev ZE, Desai C et al. 2019. A secreted viral nonstructural protein determines intestinal norovirus pathogenesis. Cell Host Microbe 25:6845–57.e5
     [Google Scholar]
135. 135.

     Nice TJ, Baldridge MT, McCune BT, Norman JM, Lazear HM et al. 2015. Interferon-λ cures persistent murine norovirus infection in the absence of adaptive immunity. Science 347:6219269–73
     [Google Scholar]
136. 136.

     Sharon AJ, Filyk HA, Fonseca NM, Simister RL, Filler RB et al. 2022. Restriction of viral replication, rather than T cell immunopathology, drives lethality in murine norovirus CR6-infected STAT1-deficient mice. J. Virol. 96:6e0206521
     [Google Scholar]
137. 137.

     Tomov VT, Palko O, Lau CW, Pattekar A, Sun Y et al. 2017. Differentiation and protective capacity of virus-specific CD8⁺ T cells suggest murine norovirus persistence in an immune-privileged enteric niche. Immunity 47:4723–38.e5
     [Google Scholar]
138. 138.

     Baldridge MT, Nice TJ, McCune BT, Yokoyama CC, Kambal A et al. 2015. Commensal microbes and interferon-λ determine persistence of enteric murine norovirus infection. Science 347:6219266–69
     [Google Scholar]
139. 139.

     Grau KR, Zhu S, Peterson ST, Helm EW, Philip D et al. 2020. The intestinal regionalization of acute norovirus infection is regulated by the microbiota via bile acid-mediated priming of type III interferon. Nat. Microbiol. 5:184–92
     [Google Scholar]
140. 140.

     Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118:2229–41
     [Google Scholar]
141. 141.

     Neil JA, Matsuzawa-Ishimoto Y, Kernbauer-Hölzl E, Schuster SL, Sota S et al. 2019. IFN-I and IL-22 mediate protective effects of intestinal viral infection. Nat. Microbiol. 4:101737–49
     [Google Scholar]
142. 142.

     Kernbauer E, Ding Y, Cadwell K. 2014. An enteric virus can replace the beneficial function of commensal bacteria. Nature 516:752994–98
     [Google Scholar]
143. 143.

     Abt MC, Buffie CG, Sušac B, Becattini S, Carter RA et al. 2016. TLR-7 activation enhances IL-22-mediated colonization resistance against vancomycin-resistant enterococcus. Sci. Transl. Med. 8:327327ra25
     [Google Scholar]
144. 144.

     Dallari S, Heaney T, Rosas-Villegas A, Neil JA, Wong S-Y et al. 2021. Enteric viruses evoke broad host immune responses resembling those elicited by the bacterial microbiome. Cell Host Microbe 29:61014–29.e8
     [Google Scholar]
145. 145.

     Liu L, Gong T, Tao W, Lin B, Li C et al. 2019. Commensal viruses maintain intestinal intraepithelial lymphocytes via noncanonical RIG-I signaling. Nat. Immunol. 20:121681–91
     [Google Scholar]
146. 146.

     Yang JY, Kim MS, Kim E, Cheon JH, Lee YS et al. 2016. Enteric viruses ameliorate gut inflammation via Toll-like receptor 3 and Toll-like receptor 7-mediated interferon-β production. Immunity 44:4889–900
     [Google Scholar]
147. 147.

     Broggi A, Tan Y, Granucci F, Zanoni I. 2017. IFN-λ suppresses intestinal inflammation by non-translational regulation of neutrophil function. Nat. Immunol. 18:101084–93
     [Google Scholar]
148. 148.

     Sun L, Miyoshi H, Origanti S, Nice TJ, Barger AC et al. 2015. Type I interferons link viral infection to enhanced epithelial turnover and repair. Cell Host Microbe 17:185–97
     [Google Scholar]
149. 149.

     Ingle H, Lee S, Ai T, Orvedahl A, Rodgers R et al. 2019. Viral complementation of immunodeficiency confers protection against enteric pathogens via interferon-λ. Nat. Microbiol. 4:71120–28
     [Google Scholar]
150. 150.

     Thépaut M, Grandjean T, Hober D, Lobert PE, Bortolotti P et al. 2015. Protective role of murine norovirus against Pseudomonas aeruginosa acute pneumonia. Vet. Res. 46:191
     [Google Scholar]
151. 151.

     Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY et al. 2015. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160:3447–60
     [Google Scholar]
152. 152.

     Clooney AG, Sutton TDS, Shkoporov AN, Holohan RK, Daly KM et al. 2019. Whole-virome analysis sheds light on viral dark matter in inflammatory bowel disease. Cell Host Microbe 26:6764–78.e5
     [Google Scholar]
153. 153.

     Nakatsu G, Zhou H, Wu WKK, Wong SH, Coker OO et al. 2018. Alterations in enteric virome are associated with colorectal cancer and survival outcomes. Gastroenterology 155:2529–41.e5
     [Google Scholar]
154. 154.

     Legoff J, Resche-Rigon M, Bouquet J, Robin M, Naccache SN et al. 2017. The eukaryotic gut virome in hematopoietic stem cell transplantation: new clues in enteric graft-versus-host disease. Nat. Med. 23:91080–85
     [Google Scholar]
155. 155.

     Axelrad JE, Joelson A, Green PHR, Lawlor G, Lichtiger S et al. 2018. Enteric infections are common in patients with flares of inflammatory bowel disease. Am. J. Gastroenterol. 113:101530–39
     [Google Scholar]
156. 156.

     Axelrad JE, Olén O, Askling J, Lebwohl B, Khalili H et al. 2019. Gastrointestinal infection increases odds of inflammatory bowel disease in a nationwide case-control study. Clin. Gastroenterol. Hepatol. 17:71311–22.e7
     [Google Scholar]
157. 157.

     Adiliaghdam F, Amatullah H, Digumarthi S, Saunders TL, Rahman R-U et al. 2022. Human enteric viruses autonomously shape inflammatory bowel disease phenotype through divergent innate immunomodulation. Sci. Immunol. 7:70eabn6660
     [Google Scholar]
158. 158.

     Huang H, Fang M, Jostins L, Umićević Mirkov M, Boucher G et al. 2017. Fine-mapping inflammatory bowel disease loci to single-variant resolution. Nature 547:173–78
     [Google Scholar]
159. 159.

     Basic M, Keubler LM, Buettner M, Achard M, Breves G et al. 2014. Norovirus triggered microbiota-driven mucosal inflammation in interleukin 10-deficient mice. Inflamm. Bowel Dis. 20:3431–43
     [Google Scholar]
160. 160.

     Lencioni KC, Seamons A, Treuting PM, Maggio-Price L, Brabb T. 2008. Murine norovirus: an intercurrent variable in a mouse model of bacteria-induced inflammatory bowel disease. Comp. Med. 58:6522–33
     [Google Scholar]
161. 161.

     Cadwell K, Patel KK, Maloney NS, Liu T-C, Ng ACY et al. 2010. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 141:71135–45
     [Google Scholar]
162. 162.

     Matsuzawa-Ishimoto Y, Hwang S, Cadwell K. 2018. Autophagy and inflammation. Annu. Rev. Immunol. 36:73–101
     [Google Scholar]
163. 163.

     Cadwell K, Liu JY, Brown SL, Miyoshi H, Loh J et al. 2008. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456:7219259–63
     [Google Scholar]
164. 164.

     Matsuzawa-Ishimoto Y, Shono Y, Gomez LE, Hubbard-Lucey VM, Cammer M et al. 2017. Autophagy protein ATG16L1 prevents necroptosis in the intestinal epithelium. J. Exp. Med. 214:123687–705
     [Google Scholar]
165. 165.

     Matsuzawa-Ishimoto Y, Hine A, Shono Y, Rudensky E, Lazrak A et al. 2020. An intestinal organoid-based platform that recreates susceptibility to T-cell-mediated tissue injury. Blood 135:262388–401
     [Google Scholar]
166. 166.

     Shukla S, Kumari S, Bal SK, Monaco DC, Ribeiro SP et al. 2021.. “ Go”, “No Go,” or “Where to Go”; does microbiota dictate T cell exhaustion, programming, and HIV persistence?. Curr. Opin. HIV AIDS 16:4215–22
     [Google Scholar]
167. 167.

     Wang Y, Lifshitz L, Gellatly K, Vinton CL, Busman-Sahay K et al. 2020. HIV-1-induced cytokines deplete homeostatic innate lymphoid cells and expand TCF7-dependent memory NK cells. Nat. Immunol. 21:3274–86
     [Google Scholar]
168. 168.

     Nganou-Makamdop K, Talla A, Sharma AA, Darko S, Ransier A et al. 2021. Translocated microbiome composition determines immunological outcome in treated HIV infection. Cell 184:153899–914.e16
     [Google Scholar]
169. 169.

     Monaco CL, Gootenberg DB, Zhao G, Handley SA, Ghebremichael MS et al. 2016. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome. Cell Host Microbe 19:3311–22
     [Google Scholar]
170. 170.

     Hirao LA, Grishina I, Bourry O, Hu WK, Somrit M et al. 2014. Early mucosal sensing of SIV infection by Paneth cells induces IL-1β production and initiates gut epithelial disruption. PLOS Pathog. 10:8e1004311
     [Google Scholar]
171. 171.

     Zaragoza MM, Sankaran-Walters S, Canfield DR, Hung JKS, Martinez E et al. 2011. Persistence of gut mucosal innate immune defenses by enteric α-defensin expression in the simian immunodeficiency virus model of AIDS. J. Immunol. 186:31589–97
     [Google Scholar]
172. 172.

     Handley SA, Desai C, Zhao G, Droit L, Monaco CL et al. 2016. SIV infection-mediated changes in gastrointestinal bacterial microbiome and virome are associated with immunodeficiency and prevented by vaccination. Cell Host Microbe 19:3323–35
     [Google Scholar]
173. 173.

     Stene LC, Honeyman MC, Hoffenberg EJ, Haas JE, Sokol RJ et al. 2006. Rotavirus infection frequency and risk of celiac disease autoimmunity in early childhood: a longitudinal study. Am. J. Gastroenterol. 101:102333–40
     [Google Scholar]
174. 174.

     Bouziat R, Hinterleitner R, Brown JJ, Stencel-Baerenwald JE, Ikizler M et al. 2017. Reovirus infection triggers inflammatory responses to dietary antigens and development of celiac disease. Science 356:633344–50
     [Google Scholar]
175. 175.

     Bouziat R, Biering SB, Kouame E, Sangani KA, Kang S et al. 2018. Murine norovirus infection induces TH1 inflammatory responses to dietary antigens. Cell Host Microbe 24:5677–88.e5
     [Google Scholar]
176. 176.

     Brigleb PH, Kouame E, Fiske KL, Taylor GM, Urbanek K et al. 2022. NK cells contribute to reovirus-induced IFN responses and loss of tolerance to dietary antigen. JCI Insight 7:16e159823
     [Google Scholar]
177. 177.

     Pane JA, Coulson BS. 2015. Lessons from the mouse: potential contribution of bystander lymphocyte activation by viruses to human type 1 diabetes. Diabetologia 58:61149–59
     [Google Scholar]
178. 178.

     Krogvold L, Edwin B, Buanes T, Frisk G, Skog O et al. 2015. Detection of a low-grade enteroviral infection in the islets of Langerhans of living patients newly diagnosed with type 1 diabetes. Diabetes 64:51682–87
     [Google Scholar]
179. 179.

     Zargari Samani O, Mahmoodnia L, Izad M, Shirzad H, Jamshidian A et al. 2018. Alteration in CD8⁺ T cell subsets in enterovirus-infected patients: an alarming factor for type 1 diabetes mellitus. Kaohsiung J. Med. Sci. 34:5274–80
     [Google Scholar]
180. 180.

     Wang K, Ye F, Chen Y, Xu J, Zhao Y et al. 2021. Association between enterovirus infection and type 1 diabetes risk: a meta-analysis of 38 case-control studies. Front. Endocrinol. 12:706964
     [Google Scholar]
181. 181.

     Engelmann I, Alidjinou EK, Bertin A, Bossu J, Villenet C et al. 2017. Persistent coxsackievirus B4 infection induces microRNA dysregulation in human pancreatic cells. Cell. Mol. Life Sci. 74:203851–61
     [Google Scholar]
182. 182.

     Serreze DV, Ottendorfer EW, Ellis TM, Gauntt CJ, Atkinson MA. 2000. Acceleration of type 1 diabetes by a coxsackievirus infection requires a preexisting critical mass of autoreactive T-cells in pancreatic islets. Diabetes 49:5708–11
     [Google Scholar]
183. 183.

     Pane JA, Webster NL, Coulson BS. 2014. Rotavirus activates lymphocytes from non-obese diabetic mice by triggering Toll-like receptor 7 signaling and interferon production in plasmacytoid dendritic cells. PLOS Pathog. 10:3e1003998
     [Google Scholar]
184. 184.

     Graham KL, Sanders N, Tan Y, Allison J, Kay TWH, Coulson BS 2008. Rotavirus infection accelerates type 1 diabetes in mice with established insulitis. J. Virol. 82:136139–49
     [Google Scholar]
185. 185.

     Marroqui L, dos Santos RS, Op de beeck A, Coomans de Brachène A, Marselli L et al. 2017. Interferon-α mediates human beta cell HLA class I overexpression, endoplasmic reticulum stress and apoptosis, three hallmarks of early human type 1 diabetes. Diabetologia 60:4656–67
     [Google Scholar]
186. 186.

     Dou Y, Yim HC, Kirkwood CD, Williams BR, Sadler AJ. 2017. The innate immune receptor MDA 5 limits rotavirus infection but promotes cell death and pancreatic inflammation. EMBO J. 36:182742–57
     [Google Scholar]
187. 187.

     Alhazmi A, Nekoua MP, Michaux H, Sane F, Halouani A et al. 2021. Effect of coxsackievirus B4 infection on the thymus: elucidating its role in the pathogenesis of type 1 diabetes. Microorganisms 9:61177
     [Google Scholar]
188. 188.

     Pearson JA, Tai N, Ekanayake-Alper DK, Peng J, Hu Y et al. 2019. Norovirus changes susceptibility to type 1 diabetes by altering intestinal microbiota and immune cell functions. Front. Immunol. 10:2654
     [Google Scholar]
189. 189.

     Sankaran-Walters S, Macal M, Grishina I, Nagy L, Goulart L et al. 2013. Sex differences matter in the gut: effect on mucosal immune activation and inflammation. Biol. Sex Differ. 4:110
     [Google Scholar]
190. 190.

     Robinson CM, Wang Y, Pfeiffer JK. 2017. Sex-dependent intestinal replication of an enteric virus. J. Virol. 91:7e02101–16
     [Google Scholar]
191. 191.

     Kim AH, Armah G, Dennis F, Wang L, Rodgers R et al. 2022. Enteric virome negatively affects seroconversion following oral rotavirus vaccination in a longitudinally sampled cohort of Ghanaian infants. Cell Host Microbe 30:1110–23.e5
     [Google Scholar]
192. 192.

     Taniuchi M, Platts-Mills JA, Begum S, Uddin MJ, Sobuz SU et al. 2016. Impact of enterovirus and other enteric pathogens on oral polio and rotavirus vaccine performance in Bangladeshi infants. Vaccine 34:273068–75
     [Google Scholar]
193. 193.

     Kayisoglu Ö, Schlegel N, Bartfeld S. 2021. Gastrointestinal epithelial innate immunity—regionalization and organoids as new model. J. Mol. Med. 99:517–30
     [Google Scholar]
194. 194.

     Carty M, Guy C, Bowie AG. 2021. Detection of viral infections by innate immunity. Biochem. Pharmacol. 183:114316
     [Google Scholar]