Gastrointestinal organoid technology advances studies of enteric virus biology

English version

Autoři: Abimbola O. Kolawole ^aff001; Christiane E. Wobus ^aff001
Působiště autorů: Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, United States of America ^aff001
Vyšlo v časopise: Gastrointestinal organoid technology advances studies of enteric virus biology. PLoS Pathog 16(1): e32767. doi:10.1371/journal.ppat.1008212
Kategorie: Pearls
doi: https://doi.org/10.1371/journal.ppat.1008212

Zdroje

1. Wobus CE, Cunha JB, Elftman MD, Kolawole AO. Animal Models of Norovirus Infection. In: Svensson L, Desselberger U., Greenberg HB, Estes MK, editor. Viral Gastroenteritis: Molecular Epidemiology and Pathogenesis. 1: Elsevier; 2016. p. 397–422.

2. Taube S, Kolawole AO, Hohne M, Wilkinson JE, Handley SA, Perry JW, et al. A mouse model for human norovirus. MBio. 2013;4(4). doi: 10.1128/mBio.00450-13 23860770; PubMed Central PMCID: PMC3735125.

3. Hill DR, Huang S, Nagy MS, Yadagiri VK, Fields C, Mukherjee D, et al. Bacterial colonization stimulates a complex physiological response in the immature human intestinal epithelium. Elife. 2017;6. doi: 10.7554/eLife.29132 PubMed Central PMCID: PMC5711377. 29110754

4. Finkbeiner SR, Hill DR, Altheim CH, Dedhia PH, Taylor MJ, Tsai YH, et al. Transcriptome-wide Analysis Reveals Hallmarks of Human Intestine Development and Maturation In Vitro and In Vivo. Stem Cell Reports. 2015. doi: 10.1016/j.stemcr.2015.04.010 26050928; PubMed Central PMCID: PMC4471827.

5. Takahashi Y, Sato S, Kurashima Y, Yamamoto T, Kurokawa S, Yuki Y, et al. A Refined Culture System for Human Induced Pluripotent Stem Cell-Derived Intestinal Epithelial Organoids. Stem Cell Reports. 2018;10(1):314–28. doi: 10.1016/j.stemcr.2017.11.004 29233552; PubMed Central PMCID: PMC5768885.

6. Spence JR, Mayhew CN, Rankin SA, Kuhar MF, Vallance JE, Tolle K, et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature. 2011;470(7332):105–9. doi: 10.1038/nature09691 21151107; PubMed Central PMCID: PMC3033971.

7. Middendorp S, Schneeberger K, Wiegerinck CL, Mokry M, Akkerman RD, van Wijngaarden S, et al. Adult stem cells in the small intestine are intrinsically programmed with their location-specific function. Stem Cells. 2014;32(5):1083–91. doi: 10.1002/stem.1655 24496776.

8. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009;459(7244):262–5. doi: 10.1038/nature07935 19329995.

9. Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH, Van den Brink S, et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology. 2011;141(5):1762–72. doi: 10.1053/j.gastro.2011.07.050 21889923.

10. VanDussen KL, Marinshaw JM, Shaikh N, Miyoshi H, Moon C, Tarr PI, et al. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut. 2015;64(6):911–20. doi: 10.1136/gutjnl-2013-306651 25007816; PubMed Central PMCID: PMC4305344.

11. Costantini V, Morantz EK, Browne H, Ettayebi K, Zeng XL, Atmar RL, et al. Human Norovirus Replication in Human Intestinal Enteroids as Model to Evaluate Virus Inactivation. Emerging infectious diseases. 2018;24(8):1453–64. doi: 10.3201/eid2408.180126 30014841; PubMed Central PMCID: PMC6056096.

12. Drummond CG, Bolock AM, Ma C, Luke CJ, Good M, Coyne CB. Enteroviruses infect human enteroids and induce antiviral signaling in a cell lineage-specific manner. Proceedings of the National Academy of Sciences of the United States of America. 2017;114(7):1672–7. doi: 10.1073/pnas.1617363114 28137842; PubMed Central PMCID: PMC5320971.

13. Ettayebi K, Crawford SE, Murakami K, Broughman JR, Karandikar U, Tenge VR, et al. Replication of human noroviruses in stem cell-derived human enteroids. Science (New York, NY. 2016;353(6306):1387–93. doi: 10.1126/science.aaf5211 27562956; PubMed Central PMCID: PMC5305121.

14. Chang-Graham AL, Danhof HA, Engevik MA, Tomaro-Duchesneau C, Karandikar UC, Estes MK, et al. Human Intestinal Enteroids With Inducible Neurogenin-3 Expression as a Novel Model of Gut Hormone Secretion. Cell Mol Gastroenterol Hepatol. 2019;8(2):209–29. doi: 10.1016/j.jcmgh.2019.04.010 31029854; PubMed Central PMCID: PMC6664234.

15. Rouch JD, Scott A, Lei NY, Solorzano-Vargas RS, Wang J, Hanson EM, et al. Development of Functional Microfold (M) Cells from Intestinal Stem Cells in Primary Human Enteroids. PLoS ONE. 2016;11(1):e0148216. doi: 10.1371/journal.pone.0148216 26820624; PubMed Central PMCID: PMC4731053.

16. Fasciano AC, Blutt SE, Estes MK, Mecsas J. Induced Differentiation of M Cell-like Cells in Human Stem Cell-derived Ileal Enteroid Monolayers. J Vis Exp. 2019;(149). doi: 10.3791/59894 31403623.

17. Fujii M, Matano M, Toshimitsu K, Takano A, Mikami Y, Nishikori S, et al. Human Intestinal Organoids Maintain Self-Renewal Capacity and Cellular Diversity in Niche-Inspired Culture Condition. Cell Stem Cell. 2018;23(6):787–93 e6. doi: 10.1016/j.stem.2018.11.016 30526881.

18. Finkbeiner SR, Zeng XL, Utama B, Atmar RL, Shroyer NF, Estes MK. Stem cell-derived human intestinal organoids as an infection model for rotaviruses. MBio. 2012;3(4):e00159–12. doi: 10.1128/mBio.00159-12 22761392; PubMed Central PMCID: PMC3398537.

19. Saxena K, Blutt SE, Ettayebi K, Zeng XL, Broughman JR, Crawford SE, et al. Human Intestinal Enteroids: a New Model To Study Human Rotavirus Infection, Host Restriction, and Pathophysiology. Journal of virology. 2016;90(1):43–56. doi: 10.1128/JVI.01930-15 26446608; PubMed Central PMCID: PMC4702582.

20. Jones MK, Grau KR, Costantini V, Kolawole AO, de Graaf M, Freiden P, et al. Human norovirus culture in B cells. Nat Protoc. 2015;10(12):1939–47. doi: 10.1038/nprot.2015.121 PubMed Central PMCID: PMC4689599. 26513671

21. Sato S, Hisaie K, Kurokawa S, Suzuki A, Sakon N, Uchida Y, et al. Human Norovirus Propagation in Human Induced Pluripotent Stem Cell-Derived Intestinal Epithelial Cells. Cell Mol Gastroenterol Hepatol. 2019;7(3):686–8 e5. doi: 10.1016/j.jcmgh.2018.11.001 30543870; PubMed Central PMCID: PMC6477164.

22. Holly MK, Smith JG. Adenovirus Infection of Human Enteroids Reveals Interferon Sensitivity and Preferential Infection of Goblet Cells. Journal of virology. 2018;92(9). doi: 10.1128/JVI.00250-18 29467318; PubMed Central PMCID: PMC5899204.

23. Kolawole AO, Mirabelli C, Hill DR, Svoboda SA, Janowski AB, Passalacqua KD, et al. Astrovirus replication in human intestinal enteroids reveals multi-cellular tropism and an intricate host innate immune landscape. PLoS Pathog. 2019;15(10):e1008057. doi: 10.1371/journal.ppat.1008057 31671153

24. Good C, Wells AI, Coyne CB. Type III interferon signaling restricts enterovirus 71 infection of goblet cells. Sci Adv. 2019;5(3):eaau4255. doi: 10.1126/sciadv.aau4255 30854425; PubMed Central PMCID: PMC6402847.

25. Hagbom M, Istrate C, Engblom D, Karlsson T, Rodriguez-Diaz J, Buesa J, et al. Rotavirus stimulates release of serotonin (5-HT) from human enterochromaffin cells and activates brain structures involved in nausea and vomiting. PLoS Pathog. 2011;7(7):e1002115. doi: 10.1371/journal.ppat.1002115 21779163; PubMed Central PMCID: PMC3136449.

26. Nikitas G, Deschamps C, Disson O, Niault T, Cossart P, Lecuit M. Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin. J Exp Med. 2011;208(11):2263–77. doi: 10.1084/jem.20110560 21967767; PubMed Central PMCID: PMC3201198.

27. Knoop KA, Newberry RD. Goblet cells: multifaceted players in immunity at mucosal surfaces. Mucosal Immunol. 2018;11(6):1551–7. doi: 10.1038/s41385-018-0039-y 29867079.

28. Rausell A, Munoz M, Martinez R, Roger T, Telenti A, Ciuffi A. Innate immune defects in HIV permissive cell lines. Retrovirology. 2016;13(1):43. doi: 10.1186/s12977-016-0275-8 27350062; PubMed Central PMCID: PMC4924258.

29. Saxena K, Simon LM, Zeng XL, Blutt SE, Crawford SE, Sastri NP, 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;114(4):E570–E9. doi: 10.1073/pnas.1615422114 28069942; PubMed Central PMCID: PMC5278484.

30. Ding S, Mooney N, Li B, Kelly MR, Feng N, Loktev AV, et al. Comparative Proteomics Reveals Strain-Specific beta-TrCP Degradation via Rotavirus NSP1 Hijacking a Host Cullin-3-Rbx1 Complex. PLoS Pathog. 2016;12(10):e1005929. doi: 10.1371/journal.ppat.1005929 27706223; PubMed Central PMCID: PMC5051689.

31. Pfeiffer JK, Virgin HW. Viral immunity. Transkingdom control of viral infection and immunity in the mammalian intestine. Science. 2016;351(6270). doi: 10.1126/science.aad5872 26816384; PubMed Central PMCID: PMC4751997.

32. Holloway EM, Capeling MM, Spence JR. Biologically inspired approaches to enhance human organoid complexity. Development. 2019;146(8). doi: 10.1242/dev.166173 30992275; PubMed Central PMCID: PMC6503984.

33. Yin Y, Bijvelds M, Dang W, Xu L, van der Eijk AA, Knipping K, et al. Modeling rotavirus infection and antiviral therapy using primary intestinal organoids. Antiviral Res. 2015;123 : 120–31. doi: 10.1016/j.antiviral.2015.09.010 26408355.

34. Kasendra M, Tovaglieri A, Sontheimer-Phelps A, Jalili-Firoozinezhad S, Bein A, Chalkiadaki A, et al. Development of a primary human Small Intestine-on-a-Chip using biopsy-derived organoids. Sci Rep. 2018;8(1):2871. doi: 10.1038/s41598-018-21201-7 29440725; PubMed Central PMCID: PMC5811607.

35. Williamson IA, Arnold JW, Samsa LA, Gaynor L, DiSalvo M, Cocchiaro JL, et al. A High-Throughput Organoid Microinjection Platform to Study Gastrointestinal Microbiota and Luminal Physiology. Cell Mol Gastroenterol Hepatol. 2018;6(3):301–19. doi: 10.1016/j.jcmgh.2018.05.004 30123820; PubMed Central PMCID: PMC6092482.

36. Chang-Graham AL, Perry JL, Strtak AC, Ramachandran NK, Criglar JM, Philip AA, et al. Rotavirus Calcium Dysregulation Manifests as Dynamic Calcium Signaling in the Cytoplasm and Endoplasmic Reticulum. Sci Rep. 2019;9(1):10822. doi: 10.1038/s41598-019-46856-8 31346185; PubMed Central PMCID: PMC6658527.

37. Yin Y, Wang Y, Dang W, Xu L, Su J, Zhou X, et al. Mycophenolic acid potently inhibits rotavirus infection with a high barrier to resistance development. Antiviral Res. 2016;133 : 41–9. doi: 10.1016/j.antiviral.2016.07.017 27468950.

38. Lulla V, Dinan AM, Hosmillo M, Chaudhry Y, Sherry L, Irigoyen N, et al. An upstream protein-coding region in enteroviruses modulates virus infection in gut epithelial cells. Nat Microbiol. 2019;4(2):280–92. doi: 10.1038/s41564-018-0297-1 30478287; PubMed Central PMCID: PMC6443042.

Článek Agricultural and geographic factors shaped the North American 2015 highly pathogenic avian influenza H5N2 outbreak

Článek A kinesin-3 recruitment complex facilitates axonal sorting of enveloped alpha herpesvirus capsids

Článek Broad dengue neutralization in mosquitoes expressing an engineered antibody

Článek Signatures of oral microbiome in HIV-infected individuals with oral Kaposi's sarcoma and cell-associated KSHV DNA

Článek The C. elegans CHP1 homolog, pbo-1, functions in innate immunity by regulating the pH of the intestinal lumen

Článek G protein α subunit suppresses sporangium formation through a serine/threonine protein kinase in Phytophthora sojae

Článek Phosphoinositide signaling and regulation in Trypanosoma brucei: Specialized functions in a protozoan pathogen

Článek Targeting resident memory T cell immunity culminates in pulmonary and systemic protection against Brucella infection

Článek USP44 positively regulates innate immune response to DNA viruses through deubiquitinating MITA

Článek An RNA thermometer dictates production of a secreted bacterial toxin

Článek Quantifying within-host diversity of H5N1 influenza viruses in humans and poultry in Cambodia

Článek The CRISPR toolbox in medical mycology: State of the art and perspectives