Abstract
The gut microbiota has a profound impact on the resistance, pathogenesis, and immunity of enteric viral pathogens. Commensal microbes may prevent the host from infection or enhance infection by altering virus stability, attachment or cellular entry. Additionally, microbiota members can stimulate or suppress host immune responses to the viral infection. In most cases, the gut microbiota plays a role in host resistance against invading enteric viral pathogens; hence, germ-free animals are more susceptible to infection of various enteric pathogens. However, increasing evidence has demonstrated that certain commensal bacteria can enhance enteric viral infection. Exact mechanisms by which specific bacteria carry out these effects are not clearly understood in most instances. In this chapter, human norovirus (HuNoV) and human rotavirus (HRV), the two most important viral pathogens causing gastroenteritis, are chosen for the discussion of the impacts and mechanisms of microbiome–host interactions on viral gastroenteritis. The pathogenesis and immunity of HuNoV and HRV in humans and in germ-free animal models, particularly gnotobiotic (Gn) mice and pigs, and Gn pigs transplanted with human gut microbiota are reviewed. Findings from studies on host–microbiome interactions on the pathogenesis and immunity of the two viruses, and mechanisms of probiotics/prebiotics in ameliorating their infection and diseases, are summarized. Unraveling the role of microbiome and specific probiotics in the infectivity, pathogenesis, and immunity of HuNoV and HRV facilitates the development of strategies for manipulating the microbiome against viral infections. Further studies are needed to improve our understanding of mechanisms underlying host–microbiome interactions in the pathophysiology of enteric viral diseases.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- ASC:
-
Antibody-secreting cells
- AttHRV:
-
Attenuated human rotavirus
- Dpi:
-
Days post-inoculation
- EcN:
-
Escherichia coli Nissle 1917
- Gn:
-
Gnotobiotic
- HBGA:
-
Histo-blood group antigen
- HHGM:
-
Healthy human gut microbiota
- HRV:
-
Human rotavirus
- HuNoV:
-
Human norovirus
- LGG:
-
Lactobacillus rhamnosus GG
- MNCs:
-
Mononuclear cells
- NHPs:
-
Nonhuman primates
- UHGM:
-
Unhealthy human gut microbiota
- VirHRV:
-
Virulent human rotavirus
References
Agus SG, Dolin R, Wyatt RG, Tousimis AJ, Northrup RS (1973) Acute infectious nonbacterial gastroenteritis: intestinal histopathology. Histologic and enzymatic alterations during illness produced by the Norwalk agent in man. Ann Intern Med 79(1):18–25
Aoki-Yoshida A, Saito S, Fukiya S, Aoki R, Takayama Y, Suzuki C, Sonoyama K (2016) Lactobacillus rhamnosus GG increases Toll-like receptor 3 gene expression in murine small intestine ex vivo and in vivo. Benefic Microbes 7(3):421–429. https://doi.org/10.3920/BM2015.0169
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(6219):266–269. https://doi.org/10.1126/science.1258025
Barnes GL, Townley RR (1973) Duodenal mucosal damage in 31 infants with gastroenteritis. Arch Dis Child 48(5):343–349
Basic M, Keubler LM, Buettner M, Achard M, Breves G, Schroder B, Smoczek A, Jorns A, Wedekind D, Zschemisch NH, Gunther C, Neumann D, Lienenklaus S, Weiss S, Hornef MW, Mahler M, Bleich A (2014) Norovirus triggered microbiota-driven mucosal inflammation in interleukin 10-deficient mice. Inflamm Bowel Dis 20(3):431–443. https://doi.org/10.1097/01.MIB.0000441346.86827.ed
Bok K, Green KY (2012) Norovirus gastroenteritis in immunocompromised patients. N Engl J Med 367(22):2126–2132. https://doi.org/10.1056/NEJMra1207742
Bok K, Parra GI, Mitra T, Abente E, Shaver CK, Boon D, Engle R, Yu C, Kapikian AZ, Sosnovtsev SV, Purcell RH, Green KY (2011) Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc Natl Acad Sci USA 108(1):325–330. https://doi.org/10.1073/pnas.1014577107
Brown JR, Gilmour K, Breuer J (2016) Norovirus infections occur in B-cell-deficient patients. Clin Infect Dis 62(9):1136–1138. https://doi.org/10.1093/cid/ciw060
Buccigrossi V, Laudiero G, Russo C, Miele E, Sofia M, Monini M, Ruggeri FM, Guarino A (2014) Chloride secretion induced by rotavirus is oxidative stress-dependent and inhibited by Saccharomyces boulardii in human enterocytes. PLoS One 9(6):e99830. https://doi.org/10.1371/journal.pone.0099830
Bui T, Kocher J, Li Y, Wen K, Li G, Liu F, Yang X, LeRoith T, Tan M, Xia M, Zhong W, Jiang X, Yuan L (2013) Median infectious dose of human norovirus GII.4 in gnotobiotic pigs is decreased by simvastatin treatment and increased by age. J Gen Virol 94(Pt 9):2005–2016. https://doi.org/10.1099/vir.0.054080-0
Chattha KS, Vlasova AN, Kandasamy S, Rajashekara G, Saif LJ (2013) Divergent immunomodulating effects of probiotics on T cell responses to oral attenuated human rotavirus vaccine and virulent human rotavirus infection in a neonatal gnotobiotic piglet disease model. J Immunol 191(5):2446–2456. https://doi.org/10.4049/jimmunol.1300678
Cheetham S, Souza M, Meulia T, Grimes S, Han MG, Saif LJ (2006) Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J Virol 80(21):10372–10381. https://doi.org/10.1128/JVI.00809-06
Chenoll E, Casinos B, Bataller E, Buesa J, Ramon D, Genoves S, Fabrega J, Rivero Urgell M, Moreno Munoz JA (2016) Identification of a peptide produced by Bifidobacterium longum CECT 7210 with antirotaviral activity. Front Microbiol 7:655. https://doi.org/10.3389/fmicb.2016.00655
Das S, Gupta PK, Das RR (2016) Efficacy and safety of Saccharomyces boulardii in acute rotavirus diarrhea: double blind randomized controlled trial from a developing country. J Trop Pediatr 62:464–470. https://doi.org/10.1093/tropej/fmw032
Davidson GP, Barnes GL (1979) Structural and functional abnormalities of the small intestine in infants and young children with rotavirus enteritis. Acta Paediatr Scand 68(2):181–186
Desselberger U (2014) Rotaviruses. Virus Res 190:75–96. https://doi.org/10.1016/j.virusres.2014.06.016
Desselberger U, Huppertz HI (2011) Immune responses to rotavirus infection and vaccination and associated correlates of protection. J Infect Dis 203(2):188–195. https://doi.org/10.1093/infdis/jiq031
Dolin R, Levy AG, Wyatt RG, Thornhill TS, Gardner JD (1975) Viral gastroenteritis induced by the Hawaii agent. Jejunal histopathology and serologic response. Am J Med 59(6):761–768
Ettayebi K, Crawford SE, Murakami K, Broughman JR, Karandikar U, Tenge VR, Neill FH, Blutt SE, Zeng XL, Qu L, Kou B, Opekun AR, Burrin D, Graham DY, Ramani S, Atmar RL, Estes MK (2016) Replication of human noroviruses in stem cell-derived human enteroids. Science 353(6306):1387–1393. https://doi.org/10.1126/science.aaf5211
Fang H, Tan M, Xia M, Wang L, Jiang X (2013) Norovirus P particle efficiently elicits innate, humoral and cellular immunity. PLoS One 8(4):e63269. https://doi.org/10.1371/journal.pone.0063269
Gagnon M, Vimont A, Darveau A, Fliss I, Jean J (2016) Study of the ability of bifidobacteria of human origin to prevent and treat rotavirus infection using colonic cell and mouse models. PLoS One 11(10):e0164512. https://doi.org/10.1371/journal.pone.0164512
Green KY (2014) Norovirus infection in immunocompromised hosts. Clin Microbiol Infect 20(8):717–723. https://doi.org/10.1111/1469-0691.12761
Guandalini S, Pensabene L, Zikri MA, Dias JA, Casali LG, Hoekstra H, Kolacek S, Massar K, Micetic-Turk D, Papadopoulou A, de Sousa JS, Sandhu B, Szajewska H, Weizman Z (2000) Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. J Pediatr Gastroenterol Nutr 30(1):54–60
Harris VC, Armah G, Fuentes S, Korpela KE, Parashar U, Victor JC, Tate J, de Weerth C, Giaquinto C, Wiersinga WJ, Lewis KD, de Vos WM (2016) The infant gut microbiome correlates significantly with rotavirus vaccine response in rural Ghana. J Infect Dis 215:34–41. https://doi.org/10.1093/infdis/jiw518
Hemming M, Rasanen S, Huhti L, Paloniemi M, Salminen M, Vesikari T (2013) Major reduction of rotavirus, but not norovirus, gastroenteritis in children seen in hospital after the introduction of RotaTeq vaccine into the National Immunization Programme in Finland. Eur J Pediatr 172(6):739–746. https://doi.org/10.1007/s00431-013-1945-3
Heyman M, Corthier G, Petit A, Meslin JC, Moreau C, Desjeux JF (1987) Intestinal absorption of macromolecules during viral enteritis: an experimental study on rotavirus-infected conventional and germ-free mice. Pediatr Res 22(1):72–78
Iosef C, Chang KO, Azevedo MS, Saif LJ (2002) Systemic and intestinal antibody responses to NSP4 enterotoxin of Wa human rotavirus in a gnotobiotic pig model of human rotavirus disease. J Med Virol 68(1):119–128. https://doi.org/10.1002/jmv.10178
Islek A, Sayar E, Yilmaz A, Baysan BO, Mutlu D, Artan R (2014) The role of Bifidobacterium lactis B94 plus inulin in the treatment of acute infectious diarrhea in children. Turk J Gastroenterol 25(6):628–633. https://doi.org/10.5152/tjg.2014.14022
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(6210):755–759. https://doi.org/10.1126/science.1257147
Jones MK, Grau KR, Costantini V, Kolawole AO, de Graaf M, Freiden P, Graves CL, Koopmans M, Wallet SM, Tibbetts SA, Schultz-Cherry S, Wobus CE, Vinje J, Karst SM (2015) Human norovirus culture in B cells. Nat Protoc 10(12):1939–1947. https://doi.org/10.1038/nprot.2015.121
Kandasamy S, Chattha KS, Vlasova AN, Rajashekara G, Saif LJ (2014) Lactobacilli and bifidobacteria enhance mucosal B cell responses and differentially modulate systemic antibody responses to an oral human rotavirus vaccine in a neonatal gnotobiotic pig disease model. Gut Microbes 5(5):639–651. https://doi.org/10.4161/19490976.2014.969972
Kandasamy S, Vlasova AN, Fischer D, Kumar A, Chattha KS, Rauf A, Shao L, Langel SN, Rajashekara G, Saif LJ (2016) Differential effects of Escherichia coli Nissle and Lactobacillus rhamnosus strain GG on human rotavirus binding, infection, and B cell immunity. J Immunol 196(4):1780–1789. https://doi.org/10.4049/jimmunol.1501705
Kane M, Case LK, Kopaskie K, Kozlova A, MacDearmid C, Chervonsky AV, Golovkina TV (2011) Successful transmission of a retrovirus depends on the commensal microbiota. Science 334(6053):245–249. https://doi.org/10.1126/science.1210718
Kang JY, Lee DK, Ha NJ, Shin HS (2015) Antiviral effects of Lactobacillus ruminis SPM0211 and Bifidobacterium longum SPM1205 and SPM1206 on rotavirus-infected Caco-2 cells and a neonatal mouse model. J Microbiol 53(11):796–803. https://doi.org/10.1007/s12275-015-5302-2
Karandikar UC, Crawford SE, Ajami NJ, Murakami K, Kou B, Ettayebi K, Papanicolaou GA, Jongwutiwes U, Perales MA, Shia J, Mercer D, Finegold MJ, Vinje J, Atmar RL, Estes MK (2016) Detection of human norovirus in intestinal biopsies from immunocompromised transplant patients. J Gen Virol 97(9):2291–2300. https://doi.org/10.1099/jgv.0.000545
Karst SM (2010) Pathogenesis of noroviruses, emerging RNA viruses. Viruses 2(3):748–781. https://doi.org/10.3390/v2030748
Karst SM, Wobus CE, Lay M, Davidson J, HWt V (2003) STAT1-dependent innate immunity to a Norwalk-like virus. Science 299(5612):1575–1578. https://doi.org/10.1126/science.1077905
Karst SM, Wobus CE, Goodfellow IG, Green KY, Virgin HW (2014) Advances in norovirus biology. Cell Host Microbe 15(6):668–680. https://doi.org/10.1016/j.chom.2014.05.015
Kehrer-Sawatzki H, Cooper DN (2007) Understanding the recent evolution of the human genome: insights from human-chimpanzee genome comparisons. Hum Mutat 28(2):99–130. https://doi.org/10.1002/humu.20420
Knowles NJ, Reuter G (2012) Porcine caliciviruses. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW (eds) Diseases of swine, 10th edn. Wiley, New York, pp 493–500
Kocher J, Yuan L (2015) Norovirus vaccines and potential antinorovirus drugs: recent advances and future perspectives. Futur Virol 10(7):899–913. https://doi.org/10.2217/fvl.15.57
Kocher J, Bui T, Giri-Rachman E, Wen K, Li G, Yang X, Liu F, Tan M, Xia M, Zhong W, Jiang X, Yuan L (2014) Intranasal P particle vaccine provided partial cross-variant protection against human GII.4 norovirus diarrhea in gnotobiotic pigs. J Virol 88(17):9728–9743. https://doi.org/10.1128/JVI.01249-14
Kolawole AO, Rocha-Pereira J, Elftman MD, Neyts J, Wobus CE (2016) Inhibition of human norovirus by a viral polymerase inhibitor in the B cell culture system and in the mouse model. Antiviral Res 132:46–49. https://doi.org/10.1016/j.antiviral.2016.05.011
Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM, Hooper LV, Dermody TS, Pfeiffer JK (2011) Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334(6053):249–252. https://doi.org/10.1126/science.1211057
Lee H, Ko G (2016) Antiviral effect of vitamin A on norovirus infection via modulation of the gut microbiome. Sci Rep 6:25835. https://doi.org/10.1038/srep25835
Lei S, Ramesh A, Twitchell E, Wen K, Bui T, Weiss M, Yang X, Kocher J, Li G, Giri-Rachman E, Trang NV, Jiang X, Ryan EP, Yuan L (2016a) High protective efficacy of probiotics and rice bran against human norovirus infection and diarrhea in gnotobiotic pigs. Front Microbiol 7:1699. https://doi.org/10.3389/fmicb.2016.01699
Lei S, Ryu J, Wen K, Twitchell E, Bui T, Ramesh A, Weiss M, Li G, Samuel H, Clark-Deener S, Jiang X, Lee K, Yuan L (2016b) Increased and prolonged human norovirus infection in RAG2/IL2RG deficient gnotobiotic pigs with severe combined immunodeficiency. Sci Rep 6:25222. https://doi.org/10.1038/srep25222
Lei S, Samuel H, Twitchell E, Bui T, Ramesh A, Wen K, Weiss M, Li G, Yang X, Jiang X, Yuan L (2016c) Enterobacter cloacae inhibits human norovirus infectivity in gnotobiotic pigs. Sci Rep 6:25017. https://doi.org/10.1038/srep25017
Li D, Breiman A, le Pendu J, Uyttendaele M (2016) Anti-viral Effect of Bifidobacterium adolescentis against noroviruses. Front Microbiol 7:864. https://doi.org/10.3389/fmicb.2016.00864
Licciardi PV, Tang ML (2011) Vaccine adjuvant properties of probiotic bacteria. Discov Med 12(67):525–533
Liu F, Li G, Wen K, Wu S, Zhang Y, Bui T, Yang X, Kocher J, Sun J, Jortner B, Yuan L (2013) Lactobacillus rhamnosus GG on rotavirus-induced injury of ileal epithelium in gnotobiotic pigs. J Pediatr Gastroenterol Nutr 57(6):750–758. https://doi.org/10.1097/MPG.0b013e3182a356e1
Liu F, Wen K, Li G, Yang X, Kocher J, Bui T, Jones D, Pelzer K, Clark-Deener S, Yuan L (2014) Dual functions of Lactobacillus acidophilus NCFM as protection against rotavirus diarrhea. J Pediatr Gastroenterol Nutr 58(2):169–176. https://doi.org/10.1097/MPG.0000000000000197
Maitra U, Gan L, Chang S, Li L (2011) Low-dose endotoxin induces inflammation by selectively removing nuclear receptors and activating CCAAT/enhancer-binding protein delta. J Immunol 186(7):4467–4473. https://doi.org/10.4049/jimmunol.1003300
Mao X, Gu C, Hu H, Tang J, Chen D, Yu B, He J, Yu J, Luo J, Tian G (2016) Dietary Lactobacillus rhamnosus GG supplementation improves the mucosal barrier function in the intestine of weaned piglets challenged by porcine rotavirus. PLoS One 11(1):e0146312. https://doi.org/10.1371/journal.pone.0146312
McNeal MM, Sestak K, Choi AH, Basu M, Cole MJ, Aye PP, Bohm RP, Ward RL (2005) Development of a rotavirus-shedding model in rhesus macaques, using a homologous wild-type rotavirus of a new P genotype. J Virol 79(2):944–954
Mebus CA, Wyatt RG, Kapikian AZ (1977) Intestinal lesions induced in gnotobiotic calves by the virus of human infantile gastroenteritis. Vet Pathol 14(3):273–282
Nagata S, Asahara T, Ohta T, Yamada T, Kondo S, Bian L, Wang C, Yamashiro Y, Nomoto K (2011) Effect of the continuous intake of probiotic-fermented milk containing Lactobacillus casei strain Shirota on fever in a mass outbreak of norovirus gastroenteritis and the faecal microflora in a health service facility for the aged. Br J Nutr 106(4):549–556. https://doi.org/10.1017/S000711451100064X
Nelson AM, Walk ST, Taube S, Taniuchi M, Houpt ER, Wobus CE, Young VB (2012) Disruption of the human gut microbiota following norovirus infection. PLoS One 7(10):e48224. https://doi.org/10.1371/journal.pone.0048224
Nelson AM, Elftman MD, Pinto AK, Baldridge M, Hooper P, Kuczynski J, Petrosino JF, Young VB, Wobus CE (2013) Murine norovirus infection does not cause major disruptions in the murine intestinal microbiota. Microbiome 1(1):7. https://doi.org/10.1186/2049-2618-1-7
O’Neil SP, Novembre FJ, Hill AB, Suwyn C, Hart CE, Evans-Strickfaden T, Anderson DC, deRosayro J, Herndon JG, Saucier M, McClure HM (2000) Progressive infection in a subset of HIV-1-positive chimpanzees. J Infect Dis 182(4):1051–1062. https://doi.org/10.1086/315823
O’Ryan ML, Pena A, Vergara R, Diaz J, Mamani N, Cortes H, Lucero Y, Vidal R, Osorio G, Santolaya ME, Hermosilla G, Prado VJ (2010) Prospective characterization of norovirus compared with rotavirus acute diarrhea episodes in chilean children. Pediatr Infect Dis J 29(9):855–859. https://doi.org/10.1097/INF.0b013e3181e8b346
Olaya Galan NN, Ulloa Rubiano JC, Velez Reyes FA, Fernandez Duarte KP, Salas Cardenas SP, Gutierrez Fernandez MF (2016) In vitro antiviral activity of Lactobacillus casei and Bifidobacterium adolescentis against rotavirus infection monitored by NSP4 protein production. J Appl Microbiol 120(4):1041–1051. https://doi.org/10.1111/jam.13069
Patel MM, Hall AJ, Vinje J, Parashar UD (2009) Noroviruses: a comprehensive review. J Clin Virol: the official publication of the Pan American Society for Clinical Virology 44(1):1–8. https://doi.org/10.1016/j.jcv.2008.10.009
Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, Hall CB, Chappell J, Bernstein DI, Curns AT, Wikswo M, Shirley SH, Hall AJ, Lopman B, Parashar UD (2013) Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med 368(12):1121–1130. https://doi.org/10.1056/NEJMsa1206589
Pfaender S, Brown RJ, Pietschmann T, Steinmann E (2014) Natural reservoirs for homologs of hepatitis C virus. Emerg Microbes Infect 3(3):e21. https://doi.org/10.1038/emi.2014.19
Pringle K, Lopman B, Vega E, Vinje J, Parashar UD, Hall AJ (2015) Noroviruses: epidemiology, immunity and prospects for prevention. Futur Microbiol 10(1):53–67. https://doi.org/10.2217/fmb.14.102
Purcell RH, Emerson SU (2001) Animal models of hepatitis A and E. ILAR J 42(2):161–177
Ramig RF (2004) Pathogenesis of intestinal and systemic rotavirus infection. J Virol 78(19):10213–10220
Ramig RF (2007) Systemic rotavirus infection. Expert Rev Anti-Infect Ther 5(4):591–612
Rubio-del-Campo A, Coll-Marques JM, Yebra MJ, Buesa J, Perez-Martinez G, Monedero V, Rodriguez-Diaz J (2014) Noroviral p-particles as an in vitro model to assess the interactions of noroviruses with probiotics. PLoS One 9(2):e89586. https://doi.org/10.1371/journal.pone.0089586
Saif LJ, Ward LA, Yuan L, Rosen BI, To TL (1996) The gnotobiotic piglet as a model for studies of disease pathogenesis and immunity to human rotaviruses. Arch Virol Suppl 12:153–161
Saif L, Yuan L, Ward L, To T (1997) Comparative studies of the pathogenesis, antibody immune responses, and homologous protection to porcine and human rotaviruses in gnotobiotic piglets. Adv Exp Med Biol 412:397–403
Schnadower D, Finkelstein Y, Freedman SB (2015) Ondansetron and probiotics in the management of pediatric acute gastroenteritis in developed countries. Curr Opin Gastroenterol 31(1):1–6. https://doi.org/10.1097/MOG.0000000000000132
Schreiber DS, Blacklow NR, Trier JS (1973) The mucosal lesion of the proximal small intestine in acute infectious nonbacterial gastroenteritis. N Engl J Med 288(25):1318–1323. https://doi.org/10.1056/NEJM197306212882503
Schreiber DS, Blacklow NR, Trier JS (1974) The small intestinal lesion induced by Hawaii agent acute infectious nonbacterial gastroenteritis. J Infect Dis 129(6):705–708
Sindhu KN, Sowmyanarayanan TV, Paul A, Babji S, Ajjampur SS, Priyadarshini S, Sarkar R, Balasubramanian KA, Wanke CA, Ward HD, Kang G (2014) Immune response and intestinal permeability in children with acute gastroenteritis treated with Lactobacillus rhamnosus GG: a randomized, double-blind, placebo-controlled trial. Clin Infect Dis: an official publication of the Infectious Diseases Society of America 58(8):1107–1115. https://doi.org/10.1093/cid/ciu065
Souza M, Cheetham SM, Azevedo MS, Costantini V, Saif LJ (2007a) Cytokine and antibody responses in gnotobiotic pigs after infection with human norovirus genogroup II.4 (HS66 strain). J Virol 81(17):9183–9192. https://doi.org/10.1128/JVI.00558-07
Souza M, Costantini V, Azevedo MS, Saif LJ (2007b) A human norovirus-like particle vaccine adjuvanted with ISCOM or mLT induces cytokine and antibody responses and protection to the homologous GII.4 human norovirus in a gnotobiotic pig disease model. Vaccine 25(50):8448–8459. https://doi.org/10.1016/j.vaccine.2007.09.040
Souza M, Azevedo MS, Jung K, Cheetham S, Saif LJ (2008) Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-HS66 strain of human norovirus. J Virol 82(4):1777–1786. https://doi.org/10.1128/JVI.01347-07
Szajewska H, Urbanska M, Chmielewska A, Weizman Z, Shamir R (2014) Meta-analysis: Lactobacillus reuteri strain DSM 17938 (and the original strain ATCC 55730) for treating acute gastroenteritis in children. Benefic Microbes 5(3):285–293. https://doi.org/10.3920/BM2013.0056
Taube S, Kolawole AO, Hohne M, Wilkinson JE, Handley SA, Perry JW, Thackray LB, Akkina R, Wobus CE (2013) A mouse model for human norovirus. MBio 4(4):e00450–e00413. https://doi.org/10.1128/mBio.00450-13
Tin CM, Yuan L, Dexter RJ, Parra GI, Bui T, Green KY, Sosnovtsev SV (2017) A Luciferase Immunoprecipitation System (LIPS) assay for profiling human norovirus antibodies. J Virol Methods 248:116–129
Troeger H, Loddenkemper C, Schneider T, Schreier E, Epple HJ, Zeitz M, Fromm M, Schulzke JD (2009) Structural and functional changes of the duodenum in human norovirus infection. Gut 58(8):1070–1077. https://doi.org/10.1136/gut.2008.160150
Twitchell EL, Tin C, Wen K, Zhang H, Becker-Dreps S, Azcarate-Peril MA, Vilchez S, Li G, Ramesh A, Weiss M, Lei S, Bui T, Yang X, Schultz-Cherry S, Yuan L (2016) Modeling human enteric dysbiosis and rotavirus immunity in gnotobiotic pigs. Gut Pathog 8:51. https://doi.org/10.1186/s13099-016-0136-y
Tzipori SR, Makin TJ, Smith ML (1980) The clinical response of gnotobiotic calves, pigs and lambs to inoculation with human, calf, pig and foal rotavirus isolates. Aust J Exp Biol Med Sci 58(3):309–318
Uchiyama R, Chassaing B, Zhang B, Gewirtz AT (2014) Antibiotic treatment suppresses rotavirus infection and enhances specific humoral immunity. J Infect Dis 210(2):171–182. https://doi.org/10.1093/infdis/jiu037
Varyukhina S, Freitas M, Bardin S, Robillard E, Tavan E, Sapin C, Grill JP, Trugnan G (2012) Glycan-modifying bacteria-derived soluble factors from Bacteroides thetaiotaomicron and Lactobacillus casei inhibit rotavirus infection in human intestinal cells. Microbes Infect 14(3):273–278. https://doi.org/10.1016/j.micinf.2011.10.007
Vlasova AN, Chattha KS, Kandasamy S, Liu Z, Esseili M, Shao L, Rajashekara G, Saif LJ (2013) Lactobacilli and bifidobacteria promote immune homeostasis by modulating innate immune responses to human rotavirus in neonatal gnotobiotic pigs. PLoS One 8(10):e76962. https://doi.org/10.1371/journal.pone.0076962
Vlasova AN, Shao L, Kandasamy S, Fischer DD, Rauf A, Langel SN, Chattha KS, Kumar A, Huang HC, Rajashekara G, Saif LJ (2016) Escherichia coli Nissle 1917 protects gnotobiotic pigs against human rotavirus by modulating pDC and NK-cell responses. Eur J Immunol 46(10):2426–2437. https://doi.org/10.1002/eji.201646498
Wang M, Donovan SM (2015) Human microbiota-associated swine: current progress and future opportunities. ILAR J 56(1):63–73. https://doi.org/10.1093/ilar/ilv006
Wang QH, Han MG, Cheetham S, Souza M, Funk JA, Saif LJ (2005) Porcine noroviruses related to human noroviruses. Emerg Infect Dis 11(12):1874–1881
Wang H, Gao K, Wen K, Allen IC, Li G, Zhang W, Kocher J, Yang X, Giri-Rachman E, Li GH, Clark-Deener S, Yuan L (2016) Lactobacillus rhamnosus GG modulates innate signaling pathway and cytokine responses to rotavirus vaccine in intestinal mononuclear cells of gnotobiotic pigs transplanted with human gut microbiota. BMC Microbiol 16(1):109. https://doi.org/10.1186/s12866-016-0727-2
Ward RL, McNeal MM, Sheridan JF (1990) Development of an adult mouse model for studies on protection against rotavirus. J Virol 64(10):5070–5075
Ward LA, Rosen BI, Yuan L, Saif LJ (1996a) Pathogenesis of an attenuated and a virulent strain of group A human rotavirus in neonatal gnotobiotic pigs. J Gen Virol 77(Pt 7):1431–1441
Ward LA, Yuan L, Rosen BI, To TL, Saif LJ (1996b) Development of mucosal and systemic lymphoproliferative responses and protective immunity to human group A rotaviruses in a gnotobiotic pig model. Clin Diagn Lab Immunol 3(3):342–350
Wen K, Azevedo MS, Gonzalez A, Zhang W, Saif LJ, Li G, Yousef A, Yuan L (2009) Toll-like receptor and innate cytokine responses induced by lactobacilli colonization and human rotavirus infection in gnotobiotic pigs. Vet Immunol Immunopathol 127(3–4):304–315. https://doi.org/10.1016/j.vetimm.2008.10.322
Wen K, Tin C, Wang H, Yang X, Li G, Giri-Rachman E, Kocher J, Bui T, Clark-Deener S, Yuan L (2014) Probiotic Lactobacillus rhamnosus GG enhanced Th1 cellular immunity but did not affect antibody responses in a human gut microbiota transplanted neonatal gnotobiotic pig model. PLoS One 9(4):e94504. https://doi.org/10.1371/journal.pone.0094504
Wen K, Liu F, Li G, Bai M, Kocher J, Yang X, Wang H, Clark-Deener S, Yuan L (2015) Lactobacillus rhamnosus GG dosage affects the adjuvanticity and protection against rotavirus diarrhea in gnotobiotic pigs. J Pediatr Gastroenterol Nutr 60(6):834–843. https://doi.org/10.1097/MPG.0000000000000694
Wilks J, Lien E, Jacobson AN, Fischbach MA, Qureshi N, Chervonsky AV, Golovkina TV (2015) Mammalian lipopolysaccharide receptors incorporated into the retroviral envelope augment virus transmission. Cell Host Microbe 18(4):456–462. https://doi.org/10.1016/j.chom.2015.09.005
Wyatt RG, Greenberg HB, Dalgard DW, Allen WP, Sly DL, Thornhill TS, Chanock RM, Kapikian AZ (1978) Experimental infection of chimpanzees with the Norwalk agent of epidemic viral gastroenteritis. J Med Virol 2(2):89–96
Yang X, Wen K, Tin C, Li G, Wang H, Kocher J, Pelzer K, Ryan E, Yuan L (2014) Dietary rice bran protects against rotavirus diarrhea and promotes Th1-type immune responses to human rotavirus vaccine in gnotobiotic pigs. Clin Vaccine Immunol 21(10):1396–1403. https://doi.org/10.1128/CVI.00210-14
Yang X, Twitchell E, Li G, Wen K, Weiss M, Kocher J, Lei S, Ramesh A, Ryan EP, Yuan L (2015) High protective efficacy of rice bran against human rotavirus diarrhea via enhancing probiotic growth, gut barrier function, and innate immunity. Sci Rep 5:15004. https://doi.org/10.1038/srep15004
Yuan L, Saif LJ (2002) Induction of mucosal immune responses and protection against enteric viruses: rotavirus infection of gnotobiotic pigs as a model. Vet Immunol Immunopathol 87(3–4):147–160
Yuan L, Wen K (2017) Rotavirus. In: Liu D (ed) Laboratory models for foodborne infections, Food microbiology. CRC Press/Taylor & Francis, Boca Raton, pp 95–107
Yuan L, Ward LA, Rosen BI, To TL, Saif LJ (1996) Systematic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J Virol 70(5):3075–3083
Yuan L, Kang SY, Ward LA, To TL, Saif LJ (1998) Antibody-secreting cell responses and protective immunity assessed in gnotobiotic pigs inoculated orally or intramuscularly with inactivated human rotavirus. J Virol 72(1):330–338
Zhang M, Zhang M, Zhang C, Du H, Wei G, Pang X, Zhou H, Liu B, Zhao L (2009) Pattern extraction of structural responses of gut microbiota to rotavirus infection via multivariate statistical analysis of clone library data. FEMS Microbiol Ecol 70(2):21–29. https://doi.org/10.1111/j.1574-6941.2009.00694.x
Zhang H, Wang H, Shepherd M, Wen K, Li G, Yang X, Kocher J, Giri-Rachman E, Dickerman A, Settlage R, Yuan L (2014) Probiotics and virulent human rotavirus modulate the transplanted human gut microbiota in gnotobiotic pigs. Gut Pathog 6:39. https://doi.org/10.1186/s13099-014-0039-8
Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS (2006) Norovirus classification and proposed strain nomenclature. Virology 346(2):312–323. https://doi.org/10.1016/j.virol.2005.11.015
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 The American Physiological Society
About this chapter
Cite this chapter
Lei, S., Twitchell, E., Yuan, L. (2018). Pathogenesis, Immunity and the Role of Microbiome/Probiotics in Enteric Virus Infections in Humans and Animal Models. In: Sun, J., Dudeja, P. (eds) Mechanisms Underlying Host-Microbiome Interactions in Pathophysiology of Human Diseases. Physiology in Health and Disease. Springer, Boston, MA. https://doi.org/10.1007/978-1-4939-7534-1_3
Download citation
DOI: https://doi.org/10.1007/978-1-4939-7534-1_3
Published:
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4939-7533-4
Online ISBN: 978-1-4939-7534-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)