Infection of porcine enteroids and 2D differentiated intestinal epithelial cells with rotavirus A to study cell tropism and polarized immune response

Reference

• Estes MK, Palmer EL, Obijeski JF. Rotaviruses - a review. Curr Top Microbiol Immunol. 1983;105:123–184. doi:10.1007/978-3-642-69159-1_3
   PubMed Web of Science ®Google Scholar
• Amimo JO, Raev SA, Chepngeno J, et al. Rotavirus interactions with host intestinal epithelial cells. Front Immunol. 2021 Dec 22;12:793841. doi:10.3389/fimmu.2021.793841
   PubMed Web of Science ®Google Scholar
• Banyai K, Kemenesi G, Budinski I, et al. Candidate new rotavirus species in Schreiber's bats, Serbia. Infect Genet Evol. 2017 Mar;48:19–26. doi:10.1016/j.meegid.2016.12.002
   PubMed Web of Science ®Google Scholar
• Matthijnssens J, Otto PH, Ciarlet M, et al. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol. 2012 Jun;157(6):1177–1182. doi:10.1007/s00705-012-1273-3
   PubMed Web of Science ®Google Scholar
• Janke BH, Nelson JK, Benfield DA, et al. Relative prevalence of typical and atypical strains among rotaviruses from diarrheic pigs in conventional swine herds. J Vet Diagn Invest. 1990;2(4):308–311. doi:10.1177/104063879000200410
   PubMedGoogle Scholar
• Marthaler D, Rossow K, Culhane M, et al. Widespread rotavirus H in commercially raised pigs, United States. Emerg Infect Dis. 2014 Jul;20(7):1195–1198. doi:10.3201/eid2007.140034
   PubMed Web of Science ®Google Scholar
• Smitalova R, Rodak L, Smid B, et al. Detection of nongroup A rotaviruses in faecal samples of pigs in the Czech Republic. Vet Med (Praha). 2009 Jan;54(1):12–18. doi:10.17221/3081-VETMED
   Web of Science ®Google Scholar
• Wakuda M, Ide T, Sasaki J, et al. Porcine rotavirus closely related to novel group of human rotaviruses. Emerg Infect Dis. 2011 Aug;17(8):1491–1493. doi:10.3201/eid1708.101466
   PubMed Web of Science ®Google Scholar
• Vlasova AN, Amimo JO, Saif LJ. Porcine rotaviruses: epidemiology, immune responses and control strategies. Viruses. 2017 Mar 18;9(3):48. doi:10.3390/v9030048
   PubMed Web of Science ®Google Scholar
• Ward RL, Bernstein DI, Young EC, et al. Human rotavirus studies in volunteers: determination of infectious dose and serological response to infection. J Infect Dis. 1986 Nov;154(5):871–880. doi:10.1093/infdis/154.5.871
   PubMed Web of Science ®Google Scholar
• Cui T, Theuns S, Xie J, et al. Porcine rotavirus mainly infects primary porcine enterocytes at the basolateral surface. Vet Res. 2019 Dec 19;50(1):110. doi:10.1186/s13567-019-0728-x
   PubMed Web of Science ®Google Scholar
• Obert G, Peiffer I, Servin AL. Rotavirus-induced structural and functional alterations in tight junctions of polarized intestinal Caco-2 cell monolayers. J Virol. 2000 May;74(10):4645–4651. doi:10.1128/JVI.74.10.4645-4651.2000
   PubMed Web of Science ®Google Scholar
• Liu F, Li G, Wen K, et al. Porcine small intestinal epithelial cell line (IPEC-J2) of rotavirus infection as a new model for the study of innate immune responses to rotaviruses and probiotics. Viral Immunol. 2010;23(2):135-49. doi:10.1089/vim.2009.0088
   PubMed Web of Science ®Google Scholar
• Estes MK, Graham DY, Gerba CP, et al. Simian rotavirus SAl replication in cell cultures. J Virol. 1979;31(3):810–815. doi:10.1128/jvi.31.3.810-815.1979
   PubMed Web of Science ®Google Scholar
• Co JY, Margalef-Catala M, Li X, et al. Controlling epithelial polarity: a human enteroid model for host-pathogen interactions. Cell Rep. 2019 Feb 26;26(9):2509–2520e4. doi:10.1016/j.celrep.2019.01.108
   PubMed Web of Science ®Google Scholar
• Kayisoglu O, Schlegel N, Bartfeld S. Gastrointestinal epithelial innate immunity-regionalization and organoids as new model. J Mol Med (Berl). 2021 Apr;99(4):517–530. doi:10.1007/s00109-021-02043-9
   PubMed Web of Science ®Google Scholar
• Kretzschmar K, Clevers H. Organoids: modeling development and the stem cell niche in a dish. Dev Cell. 2016 Sep 26;38(6):590–600. doi:10.1016/j.devcel.2016.08.014
   PubMed Web of Science ®Google Scholar
• Lancaster MA, Knoblich JA. Organogenesis in a dish: modeling development and disease using organoid technologies. Science. 2014 Jul 18;345(6194):1247125. doi:10.1126/science.1247125
   PubMed Web of Science ®Google Scholar
• Sato T, Clevers H. Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science. 2013 Jun 7;340(6137):1190–1194. doi:10.1126/science.1234852
   PubMed Web of Science ®Google Scholar
• de Lau W, Kujala P, Schneeberger K, et al. Peyer's patch M cells derived from Lgr5(+) stem cells require SpiB and are induced by RankL in cultured “miniguts”. Mol Cell Biol. 2012 Sep;32(18):3639–3647. doi:10.1128/MCB.00434-12
   PubMed Web of Science ®Google Scholar
• Sato T, Vries RG, Snippert HJ, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009 May 14;459(7244):262–265. doi:10.1038/nature07935
   PubMed Web of Science ®Google Scholar
• Blutt SE, Estes MK. Organoid models for infectious disease. Annu Rev Med. 2022 Jan 27;73:167–182. doi:10.1146/annurev-med-042320-023055
   PubMed Web of Science ®Google Scholar
• Verma S, Senger S, Cherayil BJ, et al. Spheres of influence: insights into salmonella pathogenesis from intestinal organoids. Microorganisms. 2020 Apr 1;8(4):504. doi:10.3390/microorganisms8040504
   PubMed Web of Science ®Google Scholar
• VanDussen KL, Marinshaw JM, Shaikh N, et al. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut. 2015 Jun;64(6):911–920. doi:10.1136/gutjnl-2013-306651
   PubMed Web of Science ®Google Scholar
• Wang X, Yamamoto Y, Wilson LH, et al. Cloning and variation of ground state intestinal stem cells. Nature. 2015 Jun 11;522(7555):173–178. doi:10.1038/nature14484
   PubMed Web of Science ®Google Scholar
• Drurey C, Lindholm HT, Coakley G, et al. Intestinal epithelial tuft cell induction is negated by a murine helminth and its secreted products. J Exp Med. 2022 Jan 3;219(1):e20211140. doi:10.1084/jem.20211140
   PubMed Web of Science ®Google Scholar
• Heo I, Dutta D, Schaefer DA, et al. Modelling cryptosporidium infection in human small intestinal and lung organoids. Nat Microbiol. 2018 Jul;3(7):814–823. doi:10.1038/s41564-018-0177-8
   PubMed Web of Science ®Google Scholar
• Finkbeiner SR, Zeng XL, Utama B, et al. Stem cell-derived human intestinal organoids as an infection model for rotaviruses. mBio. 2012;3(4):e00159–12. doi:10.1128/mBio.00159-12
   PubMed Web of Science ®Google Scholar
• Saxena K, Blutt SE, Ettayebi K, et al. Human intestinal enteroids: a New model To study human rotavirus infection, host restriction, and pathophysiology. J Virol. 2016 Jan 1;90(1):43–56. doi:10.1128/JVI.01930-15
   PubMed Web of Science ®Google Scholar
• Stanifer ML, Mukenhirn M, Muenchau S, et al. Asymmetric distribution of TLR3 leads to a polarized immune response in human intestinal epithelial cells. Nat Microbiol. 2020 Jan;5(1):181–191. doi:10.1038/s41564-019-0594-3
   PubMed Web of Science ®Google Scholar
• Lin SC, Qu L, Ettayebi K, et al. Human norovirus exhibits strain-specific sensitivity to host interferon pathways in human intestinal enteroids. Proc Natl Acad Sci USA. 2020 Sep 22;117(38):23782–23793. doi:10.1073/pnas.2010834117
   PubMed Web of Science ®Google Scholar
• Ettayebi K, Crawford S E, Murakami K, et al. Replication of human noroviruses in stem cell–derived human enteroids. Science. 2016;353(6306):1387–1393. doi:10.1126/science.aaf5211
   PubMed Web of Science ®Google Scholar
• Holly MK, Smith JG. Adenovirus infection of human enteroids reveals interferon sensitivity and preferential infection of goblet cells. J Virol. 2018 May 1;92(9):e00250-18. doi:10.1128/JVI.00250-18
   PubMed Web of Science ®Google Scholar
• Huang L, Hou Q, Ye L, et al. Crosstalk between H9N2 avian influenza virus and crypt-derived intestinal organoids. Vet Res. 2017 Nov 2;48(1):71. doi:10.1186/s13567-017-0478-6
   PubMedGoogle Scholar
• Zhou J, Li C, Liu X, et al. Infection of bat and human intestinal organoids by SARS-CoV-2. Nat Med. 2020 Jul;26(7):1077–1083. doi:10.1038/s41591-020-0912-6
   PubMed Web of Science ®Google Scholar
• Li Y, Yang N, Chen J, et al. Next-Generation porcine intestinal organoids: an apical-out organoid model for swine enteric virus infection and immune response investigations. J Virol. 2020 Oct 14;94(21):e01006-20. doi:10.1128/JVI.01006-20
   PubMed Web of Science ®Google Scholar
• Yang N, Zhang Y, Fu Y, et al. Transmissible gastroenteritis virus infection promotes the self-renewal of porcine intestinal stem cells via Wntβ-catenin pathway. J Virol. 2022;96(18):e0096222. doi:10.1128/jvi.00962-22
   PubMed Web of Science ®Google Scholar
• Li L, Fu F, Guo S, et al. Porcine intestinal enteroids: a new model for studying enteric coronavirus porcine epidemic diarrhea virus infection and the host innate response. J Virol. 2019 Feb 19;93(5):e01682-18. doi:10.1128/JVI.01682-18
   PubMed Web of Science ®Google Scholar
• Wang AZ, Ojakian GK WJN. Steps in the morphogenesis of a polarized epithelium II. disassembly and assembly of plasma membrane domains during reversal of epithelial cell polarity in multicellular epithelial (MDCK) cysts. J Cell Sci. 1990;95(Pt 1):153–165. doi:10.1242/jcs.95.1.153
   PubMedGoogle Scholar
• Pavasutthipaisit S, Stoff M, Ebbecke T, et al. CARD9 deficiency increases hippocampal injury following acute neurotropic picornavirus infection but does not affect pathogen elimination. Int J Mol Sci. 2021 Jun 29;22(13):6982. doi:10.3390/ijms22136982
   PubMed Web of Science ®Google Scholar
• Su A, Yan M, Pavasutthipaisit S, et al. Infection studies with airway organoids from carollia perspicillata indicate that the respiratory epithelium Is Not a barrier for interspecies transmiss. Microbiol Spectr. 2023 Mar 14;11(2):e0309822. doi:10.1128/spectrum.03098-22.
   PubMed Web of Science ®Google Scholar
• Pang XL, Lee B, Boroumand N, et al. Increased detection of rotavirus using a real time reverse transcription-polymerase chain reaction (RT-PCR) assay in stool specimens from children with diarrhea. J Med Virol. 2004 Mar;72(3):496–501. doi:10.1002/jmv.20009
   PubMed Web of Science ®Google Scholar
• Gonzalez LM, Williamson I, Piedrahita JA, et al. Cell lineage identification and stem cell culture in a porcine model for the study of intestinal epithelial regeneration. PLoS One. 2013;8(6):e66465. doi:10.1371/journal.pone.0066465
   PubMed Web of Science ®Google Scholar
• Lundgren O, Svensson L. Pathogenesis of rotavirus diarrhea. Microbes Infect. 2001 Nov;3(13):1145–1156. doi:10.1016/S1286-4579(01)01475-7
   PubMed Web of Science ®Google Scholar
• Crawford SE, Ramani S, Tate JE, et al. Rotavirus infection. Nat Rev Dis Primers. 2017 Nov 9;3:17083. doi:10.1038/nrdp.2017.83
   PubMed Web of Science ®Google Scholar
• Saxena K, Simon LM, Zeng XL, et al. A paradox of transcriptional and functional innate interferon responses of human intestinal enteroids to enteric virus infection. Proc Natl Acad Sci USA. 2017 Jan 24;114(4):E570–E579. doi:10.1073/pnas.1615422114
   PubMed Web of Science ®Google Scholar
• Pott J, Mahlakoiv T, Mordstein M, et al. IFN-lambda determines the intestinal epithelial antiviral host defense. Proc Natl Acad Sci USA. 2011 May 10;108(19):7944–7949. doi:10.1073/pnas.1100552108
   PubMed Web of Science ®Google Scholar
• Blutt SE, Crawford SE, Ramani S, et al. Engineered human gastrointestinal cultures to study the microbiome and infectious diseases. Cell Mol Gastroenterol Hepatol. 2018 Mar;5(3):241–251. doi:10.1016/j.jcmgh.2017.12.001
   PubMed Web of Science ®Google Scholar
• Blake R, Jensen K, Mabbott N, et al. The development of 3D bovine intestinal organoid derived models to investigate Mycobacterium avium ssp Paratuberculosis pathogenesis. Front Vet Sci. 2022;9:921160. doi:10.3389/fvets.2022.921160
   PubMed Web of Science ®Google Scholar
• Svensson L, Finlay BB, Bass D, et al. Symmetric infection of rotavirus on polarized human intestinal epithelial (Caco-2) cells. J Virol. 1991 Aug;65(8):4190–4197. doi:10.1128/jvi.65.8.4190-4197.1991
   PubMed Web of Science ®Google Scholar
• Porta DC, Lopez S, Arias CF, et al. Polarized rotavirus entry and release from differentiated small intestinal cells. Virology. 2016 Dec;499:65–71. doi:10.1016/j.virol.2016.09.010
   PubMed Web of Science ®Google Scholar
• Ciarlet M, Crawford SE, Estes MK. Differential infection of polarized epithelial cell lines by sialic acid-dependent and sialic acid-independent rotavirus strains. J Virol. 2001 Dec;75(23):11834–11850. doi:10.1128/JVI.75.23.11834-11850.2001
   PubMed Web of Science ®Google Scholar
• Mahlakoiv T, Hernandez P, Gronke K, et al. Leukocyte-derived IFN-alpha/beta and epithelial IFN-lambda constitute a compartmentalized mucosal defense system that restricts enteric virus infections. PLoS Pathog. 2015 Apr;11(4):e1004782. doi:10.1371/journal.ppat.1004782
   PubMed Web of Science ®Google Scholar
• Doldan P, Dai J, Metz-Zumaran C, et al. Type III and not type I interferons efficiently prevent the spread of rotavirus in human intestinal epithelial cells. J Virol. 2022 Sep 14;96(17):e0070622. doi:10.1128/jvi.00706-22
   PubMed Web of Science ®Google Scholar
• Lin JD, Feng N, Sen A, et al. Distinct roles of type I and type III interferons in intestinal immunity to homologous and heterologous rotavirus infections. PLoS Pathog. 2016 Apr;12(4):e1005600. doi:10.1371/journal.ppat.1005600
   PubMed Web of Science ®Google Scholar
• Lazear HM, Schoggins JW, Diamond MS. Shared and distinct functions of type I and type III interferons. Immunity. 2019 Apr 16;50(4):907–923. doi:10.1016/j.immuni.2019.03.025
   PubMed Web of Science ®Google Scholar
• Stanifer ML, Guo C, Doldan P, et al. Importance of type I and III interferons at respiratory and intestinal barrier surfaces. Front Immunol. 2020;11:608645. doi:10.3389/fimmu.2020.608645
   PubMed Web of Science ®Google Scholar