Stem cell-derived models of viral infections in the gastrointestinal tract

Viruses

Volumn 10, Issue 3, 2018, Pages

  Lanik, Wyatt E ^a   Mara, Madison A ^a   Mihi, Belgacem ^a   Coyne, Carolyn B ^b,c   Good, Misty ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

Enteroids; Enteroviruses; Intestinal stem cells; Mini guts; Organoids

Indexed keywords

ADENOVIRUS INFECTION; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; CELL STRUCTURE; DISEASE MODEL; ENTEROID; ENTEROVIRUS INFECTION; GASTROINTESTINAL INFECTION; HOST PATHOGEN INTERACTION; HUMAN; IN VITRO STUDY; INTESTINAL STEM CELL; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; INTESTINE TISSUE; INTESTINE VILLUS; NONHUMAN; NOROVIRUS INFECTION; ORGANOID; REVIEW; ROTAVIRUS INFECTION; SMALL INTESTINE; VIRUS INFECTION; VIRUS PATHOGENESIS; BIOLOGICAL MODEL; GASTROINTESTINAL TRACT; GENETICS; INTESTINE; METABOLISM; STEM CELL; VIROLOGY;

ENTEROVIRUS INFECTIONS; GASTROINTESTINAL TRACT; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; MODELS, BIOLOGICAL; ORGANOIDS; STEM CELLS;

EID: 85044289168     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v10030124     Document Type: Review

References (72)

1. Sato, T.; Vries, R.G.; Snippert, H.J.; van de Wetering, M.; Barker, N.; Stange, D.E.; van Es, J.H.; Abo, A.; Kujala, P.; Peters, P.J.; et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 2009, 459, 262–265. [CrossRef] [PubMed]
2. Sinagoga, K.L.; Wells, J.M. Generating human intestinal tissues from pluripotent stem cells to study development and disease. EMBO J. 2015, 34, 1149–1163. [CrossRef] [PubMed]
3. Buczacki, S.J.; Zecchini, H.I.; Nicholson, A.M.; Russell, R.; Vermeulen, L.; Kemp, R.; Winton, D.J. Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 2013, 495, 65–69. [CrossRef] [PubMed]
4. Goto, Y.; Kiyono, H. Epithelial barrier: An interface for the cross-communication between gut flora and immune system. Immunol. Rev. 2012, 245, 147–163. [CrossRef] [PubMed]
5. Bevins, C.L.; Salzman, N.H. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat. Rev. Microbiol. 2011, 9, 356–368. [CrossRef] [PubMed]
6. O’Ryan, M.; Prado, V.; Pickering, L.K. A millennium update on pediatric diarrheal illness in the developing world. Semin. Pediatr. Infect. Dis. 2005, 16, 125–136. [CrossRef] [PubMed]
7. Spence, J.R.; Mayhew, C.N.; Rankin, S.A.; Kuhar, M.F.; Vallance, J.E.; Tolle, K.; Hoskins, E.E.; Kalinichenko, V.V.; Wells, S.I.; Zorn, A.M.; et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 2011, 470, 105–109. [CrossRef] [PubMed]
8. McCracken, K.W.; Howell, J.C.; Wells, J.M.; Spence, J.R. Generating human intestinal tissue from pluripotent stem cells in vitro. Nat. Protoc. 2011, 6, 1920–1928. [CrossRef] [PubMed]
9. Stelzner, M.; Helmrath, M.; Dunn, J.C.; Henning, S.J.; Houchen, C.W.; Kuo, C.; Lynch, J.; Li, L.; Magness, S.T.; Martin, M.G.; et al. A nomenclature for intestinal in vitro cultures. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302, G1359–G1363. [CrossRef] [PubMed]
10. Finkbeiner, S.R.; Hill, D.R.; Altheim, C.H.; Dedhia, P.H.; Taylor, M.J.; Tsai, Y.H.; Chin, A.M.; Mahe, M.M.; Watson, C.L.; Freeman, J.J.; et al. Transcriptome-wide Analysis Reveals Hallmarks of Human Intestine Development and Maturation In Vitro and In Vivo. Stem Cell Rep. 2015, 4, 1140–1155. [CrossRef] [PubMed]
11. Hill, D.R.; Spence, J.R. Gastrointestinal Organoids: Understanding the Molecular Basis of the Host-Microbe Interface. Cell. Mol. Gastroenterol. Hepatol. 2017, 3, 138–149. [CrossRef] [PubMed]
12. Dye, B.R.; Hill, D.R.; Ferguson, M.A.; Tsai, Y.H.; Nagy, M.S.; Dyal, R.; Wells, J.M.; Mayhew, C.N.; Nattiv, R.; Klein, O.D.; et al. In vitro generation of human pluripotent stem cell derived lung organoids. Elife 2015, 4, e05098. [CrossRef] [PubMed]
13. Watson, C.L.; Mahe, M.M.; Munera, J.; Howell, J.C.; Sundaram, N.; Poling, H.M.; Schweitzer, J.I.; Vallance, J.E.; Mayhew, C.N.; Sun, Y.; et al. An in vivo model of human small intestine using pluripotent stem cells. Nat. Med. 2014, 20, 1310–1314. [CrossRef] [PubMed]
14. Aurora, M.; Spence, J.R. hPSC-derived lung and intestinal organoids as models of human fetal tissue. Dev. Biol. 2016, 420, 230–238. [CrossRef] [PubMed]
15. Finkbeiner, S.R.; Freeman, J.J.; Wieck, M.M.; El-Nachef, W.; Altheim, C.H.; Tsai, Y.H.; Huang, S.; Dyal, R.; White, E.S.; Grikscheit, T.C.; et al. Generation of tissue-engineered small intestine using embryonic stem cell-derived human intestinal organoids. Biol. Open 2015, 4, 1462–1472. [CrossRef] [PubMed]
16. Matano, M.; Date, S.; Shimokawa, M.; Takano, A.; Fujii, M.; Ohta, Y.; Watanabe, T.; Kanai, T.; Sato, T. Modeling colorectal cancer using CRISPR-Cas9-mediated engineering of human intestinal organoids. Nat. Med. 2015, 21, 256–262. [CrossRef] [PubMed]
17. Fujii, M.; Shimokawa, M.; Date, S.; Takano, A.; Matano, M.; Nanki, K.; Ohta, Y.; Toshimitsu, K.; Nakazato, Y.; Kawasaki, K.; et al. A colorectal tumor organoid library demonstrates progressive loss of niche factor requirements during tumorigenesis. Cell Stem Cell 2016, 18, 827–838. [CrossRef] [PubMed]
18. Drost, J.; van Jaarsveld, R.H.; Ponsioen, B.; Zimberlin, C.; van Boxtel, R.; Buijs, A.; Sachs, N.; Overmeer, R.M.; Offerhaus, G.J.; Begthel, H.; et al. Sequential cancer mutations in cultured human intestinal stem cells. Nature 2015, 521, 43–47. [CrossRef] [PubMed]
19. Van de Wetering, M.; Francies, H.E.; Francis, J.M.; Bounova, G.; Iorio, F.; Pronk, A.; van Houdt, W.; van Gorp, J.; Taylor-Weiner, A.; Kester, L.; et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell 2015, 161, 933–945. [CrossRef] [PubMed]
20. Koo, B.K.; Stange, D.E.; Sato, T.; Karthaus, W.; Farin, H.F.; Huch, M.; van Es, J.H.; Clevers, H. Controlled gene expression in primary Lgr5 organoid cultures. Nat. Methods 2011, 9, 81–83. [CrossRef] [PubMed]
21. Saxena, K.; Blutt, S.E.; Ettayebi, K.; Zeng, X.L.; Broughman, J.R.; Crawford, S.E.; Karandikar, U.C.; Sastri, N.P.; Conner, M.E.; Opekun, A.R.; et al. Human Intestinal Enteroids: A New Model to Study Human Rotavirus Infection, Host Restriction, and Pathophysiology. J. Virol. 2015, 90, 43–56. [CrossRef] [PubMed]
22. Ootani, A.; Li, X.; Sangiorgi, E.; Ho, Q.T.; Ueno, H.; Toda, S.; Sugihara, H.; Fujimoto, K.; Weissman, I.L.; Capecchi, M.R.; et al. Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat. Med. 2009, 15, 701–706. [CrossRef] [PubMed]
23. Pinto, D.; Gregorieff, A.; Begthel, H.; Clevers, H. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 2003, 17, 1709–1713. [CrossRef] [PubMed]
24. Kuhnert, F.; Davis, C.R.; Wang, H.T.; Chu, P.; Lee, M.; Yuan, J.; Nusse, R.; Kuo, C.J. Essential requirement for Wnt signaling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1. Proc. Natl. Acad. Sci. USA 2004, 101, 266–271. [CrossRef] [PubMed]
25. Carmon, K.S.; Gong, X.; Lin, Q.; Thomas, A.; Liu, Q. R-spondins function as ligands of the orphan receptors LGR4 and LGR5 to regulate Wnt/β-catenin signaling. Proc. Natl. Acad. Sci. USA 2011, 108, 11452–11457. [CrossRef] [PubMed]
26. Dignass, A.U.; Sturm, A. Peptide growth factors in the intestine. Eur. J. Gastroenterol. Hepatol. 2001, 13, 763–770. [CrossRef] [PubMed]
27. Haramis, A.P.; Begthel, H.; van den Born, M.; van Es, J.; Jonkheer, S.; Offerhaus, G.J.; Clevers, H. De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 2004, 303, 1684–1686. [CrossRef] [PubMed]
28. Qi, Z.; Li, Y.; Zhao, B.; Xu, C.; Liu, Y.; Li, H.; Zhang, B.; Wang, X.; Yang, X.; Xie, W.; et al. Bmp restricts stemness of intestinal lgr5(+) stem cells by directly suppressing their signature genes. Nat. Commun. 2017, 8, 13824. [CrossRef] [PubMed]
29. Sasaki, T.; Giltay, R.; Talts, U.; Timpl, R.; Talts, J.F. Expression and distribution of laminin α1 and α2 chains in embryonic and adult mouse tissues: An immunochemical approach. Exp. Cell Res. 2002, 275, 185–199. [CrossRef] [PubMed]
30. Fuller, M.K.; Faulk, D.M.; Sundaram, N.; Mahe, M.M.; Stout, K.M.; von Furstenberg, R.J.; Smith, B.J.; McNaughton, K.K.; Shroyer, N.F.; Helmrath, M.A.; et al. Intestinal stem cells remain viable after prolonged tissue storage. Cell Tissue Res. 2013, 354, 441–450. [CrossRef] [PubMed]
31. Sato, T.; Clevers, H. Primary mouse small intestinal epithelial cell cultures. In Epithelial Cell Culture Protocols; Humana Press: Totowa, NJ, USA, 2013; pp. 319–328.
32. Yu, H.; Hasan, N.M.; In, J.G.; Estes, M.K.; Kovbasnjuk, O.; Zachos, N.C.; Donowitz, M. The Contributions of Human Mini-Intestines to the Study of Intestinal Physiology and Pathophysiology. Annu. Rev. Physiol. 2017, 79, 291–312. [CrossRef] [PubMed]
33. VanDussen, K.L.; Marinshaw, J.M.; Shaikh, N.; Miyoshi, H.; Moon, C.; Tarr, P.I.; Ciorba, M.A.; Stappenbeck, T.S. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut 2015, 64, 911–920. [CrossRef] [PubMed]
34. Ameri, J.; Stahlberg, A.; Pedersen, J.; Johansson, J.K.; Johannesson, M.M.; Artner, I.; Semb, H. FGF2 specifies hESC-derived definitive endoderm into foregut/midgut cell lineages in a concentration-dependent manner. Stem Cells 2010, 28, 45–56. [CrossRef] [PubMed]
35. Cao, L.; Gibson, J.D.; Miyamoto, S.; Sail, V.; Verma, R.; Rosenberg, D.W.; Nelson, C.E.; Giardina, C. Intestinal lineage commitment of embryonic stem cells. Differentiation 2011, 81, 1–10. [CrossRef] [PubMed]
36. Wells, J.M.; Spence, J.R. How to make an intestine. Development 2014, 141, 752–760. [CrossRef] [PubMed]
37. McKie, A.T.; Barrow, D.; Latunde-Dada, G.O.; Rolfs, A.; Sager, G.; Mudaly, E.; Mudaly, M.; Richardson, C.; Barlow, D.; Bomford, A.; et al. An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 2001, 291, 1755–1759. [CrossRef] [PubMed]
38. Krasinski, S.D.; Upchurch, B.H.; Irons, S.J.; June, R.M.; Mishra, K.; Grand, R.J.; Verhave, M. Rat lactase-phlorizin hydrolase/human growth hormone transgene is expressed on small intestinal villi in transgenic mice. Gastroenterology 1997, 113, 844–855. [CrossRef]
39. Colombo, V.; Lorenz-Meyer, H.; Semenza, G. Small intestinal phlorizin hydrolase: The “beta-glycosidase complex”. Biochim. Biophys. Acta 1973, 327, 412–424. [CrossRef]
40. Dawson, P.A.; Lan, T.; Rao, A. Bile acid transporters. J. Lipid Res. 2009, 50, 2340–2357. [CrossRef] [PubMed]
41. Middendorp, S.; Schneeberger, K.; Wiegerinck, C.L.; Mokry, M.; Akkerman, R.D.; van Wijngaarden, S.; Clevers, H.; Nieuwenhuis, E.E. Adult stem cells in the small intestine are intrinsically programmed with their location-specific function. Stem Cells 2014, 32, 1083–1091. [CrossRef] [PubMed]
42. Nijenhuis, T.; Hoenderop, J.G.; van der Kemp, A.W.; Bindels, R.J. Localization and regulation of the epithelial Ca2+ channel TRPV6 in the kidney. J. Am. Soc. Nephrol. 2003, 14, 2731–2740. [CrossRef] [PubMed]
43. Wang, X.; Yamamoto, Y.; Wilson, L.H.; Zhang, T.; Howitt, B.E.; Farrow, M.A.; Kern, F.; Ning, G.; Hong, Y.; Khor, C.C.; et al. Cloning and variation of ground state intestinal stem cells. Nature 2015, 522, 173–178. [CrossRef] [PubMed]
44. Shaffiey, S.A.; Jia, H.; Keane, T.; Costello, C.; Wasserman, D.; Quidgley, M.; Dziki, J.; Badylak, S.; Sodhi, C.P.; March, J.C.; et al. Intestinal stem cell growth and differentiation on a tubular scaffold with evaluation in small and large animals. Regen. Med. 2016, 11, 45–61. [CrossRef] [PubMed]
45. Wang, Y.; Gunasekara, D.B.; Reed, M.I.; DiSalvo, M.; Bultman, S.J.; Sims, C.E.; Magness, S.T.; Allbritton, N.L. A microengineered collagen scaffold for generating a polarized crypt-villus architecture of human small intestinal epithelium. Biomaterials 2017, 128, 44–55. [CrossRef] [PubMed]
46. Chen, Y.; Zhou, W.; Roh, T.; Estes, M.K.; Kaplan, D.L. In vitro enteroid-derived three-dimensional tissue model of human small intestinal epithelium with innate immune responses. PLoS ONE 2017, 12, e0187880. [CrossRef] [PubMed]
47. Kim, H.J.; Lee, J.; Choi, J.H.; Bahinski, A.; Ingber, D.E. Co-culture of Living Microbiome with Microengineered Human Intestinal Villi in a Gut-on-a-Chip Microfluidic Device. J. Vis. Exp. 2016. [CrossRef] [PubMed]
48. Kasendra, M.; Tovaglieri, A.; Sontheimer-Phelps, A.; Jalili-Firoozinezhad, S.; Bein, A.; Chalkiadaki, A.; Scholl, W.; Zhang, C.; Rickner, H.; Richmond, C.A.; et al. Development of a primary human Small Intestine-on-a-Chip using biopsy-derived organoids. Sci. Rep. 2018, 8, 2871. [CrossRef] [PubMed]
49. Cheng, H.; Leblond, C.P. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am. J. Anat. 1974, 141, 461–479. [CrossRef] [PubMed]
50. Bjerknes, M.; Cheng, H. Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 1999, 116, 7–14. [CrossRef]
51. Bjerknes, M.; Cheng, H. Intestinal epithelial stem cells and progenitors. Methods Enzymol. 2006, 419, 337–383. [PubMed]
52. Tetteh, P.W.; Basak, O.; Farin, H.F.; Wiebrands, K.; Kretzschmar, K.; Begthel, H.; van den Born, M.; Korving, J.; de Sauvage, F.; van Es, J.H. et al. Replacement of lost lgr5-positive stem cells through plasticity of their enterocyte-lineage daughters. Cell Stem Cell 2016, 18, 203–213. [CrossRef] [PubMed]
53. Van Es, J.H.; Sato, T.; van de Wetering, M.; Lyubimova, A.; Yee Nee, A.N.; Gregorieff, A.; Sasaki, N.; Zeinstra, L.; vandenBorn, M.; Korving, J. et al. Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol. 2012, 14, 1099–1104. [CrossRef] [PubMed]
54. Jadhav, U.; Saxena, M.; O’Neill, N.K.; Saadatpour, A.; Yuan, G.C.; Herbert, Z.; Murata, K.; Shivdasani, R.A. Dynamic reorganization of chromatin accessibility signatures during dedifferentiation of secretory precursors into lgr5+ intestinal stem cells. Cell Stem Cell 2017, 21, 65–77. [CrossRef] [PubMed]
55. Metcalfe, C.; Kljavin, N.M.; Ybarra, R.; de Sauvage, F.J. Lgr5+ stem cells are indispensable for radiation-induced intestinal regeneration. Cell Stem Cell 2014, 14, 149–159. [CrossRef] [PubMed]
56. Sato, T.; van Es, J.H.; Snippert, H.J.; Stange, D.E.; Vries, R.G.; van den Born, M.; Barker, N.; Shroyer, N.F.; van de Wetering, M.; Clevers, H. Paneth cells constitute the niche for LGR5 stem cells in intestinal crypts. Nature 2011, 469, 415–418. [CrossRef] [PubMed]
57. Greenberg, H.B.; Estes, M.K. Rotaviruses: From pathogenesis to vaccination. Gastroenterology 2009, 136, 1939–1951. [CrossRef] [PubMed]
58. Tate, J.E.; Burton, A.H.; Boschi-Pinto, C.; Steele, A.D.; Duque, J.; Parashar, U.D. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: A systematic review and meta-analysis. Lancet Infect. Dis. 2012, 12, 136–141. [CrossRef]
59. Arnold, M.; Patton, J.T.; McDonald, S.M. Culturing, storage, and quantification of rotavirus. Curr. Protoc. Microbiol. 2009. [CrossRef]
60. Sheth, R.; Anderson, J.; Sato, T.; Oh, B.; Hempson, S.J.; Rollo, E.; Mackow, E.R.; Shaw, R.D. Rotavirus stimulates IL-8 secretion from cultured epithelial cells. Virology 1996, 221, 251–259. [CrossRef] [PubMed]
61. Pedron, T.; Thibault, C.; Sansonetti, P.J. The invasive phenotype of Shigella flexneri directs a distinct gene expression pattern in the human intestinal epithelial cell line Caco-2. J. Biol. Chem. 2003, 278, 33878–33886. [CrossRef] [PubMed]
62. Drummond, C.G.; Bolock, A.M.; Ma, C.; Luke, C.J.; Good, M.; Coyne, C.B. Enteroviruses infect human enteroids and induce antiviral signaling in a cell lineage-specific manner. Proc. Natl. Acad. Sci. USA 2017, 114, 1672–1677. [CrossRef] [PubMed]
63. Ward, R.L.; Clemens, J.D.; Sack, D.A.; Knowlton, D.R.; McNeal, M.M.; Huda, N.; Ahmed, F.; Rao, M.; Schiff, G.M. Culture adaptation and characterization of group A rotaviruses causing diarrheal illnesses in Bangladesh from 1985 to 1986. J. Clin. Microbiol. 1991, 29, 1915–1923. [PubMed]
64. Finkbeiner, S.R.; Zeng, X.L.; Utama, B.; Atmar, R.L.; Shroyer, N.F.; Estes, M.K. Stem cell-derived human intestinal organoids as an infection model for rotaviruses. MBio 2012, 3, e00159-12. [CrossRef] [PubMed]
65. Hale, A.; Mattick, K.; Lewis, D.; Estes, M.; Jiang, X.; Green, J.; Eglin, R.; Brown, D. Distinct epidemiological patterns of Norwalk-like virus infection. J. Med. Virol. 2000, 62, 99–103. [CrossRef]
66. Jones, M.K.; Watanabe, M.; Zhu, S.; Graves, C.L.; Keyes, L.R.; Grau, K.R.; Gonzalez-Hernandez, M.B.; Iovine, N.M.; Wobus, C.E.; Vinje, J.; et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 2014, 346, 755–759. [CrossRef] [PubMed]
67. Ramani, S.; Atmar, R.L.; Estes, M.K. Epidemiology of human noroviruses and updates on vaccine development. Curr. Opin. Gastroenterol. 2014, 30, 25–33. [CrossRef] [PubMed]
68. Ettayebi, K.; Crawford, S.E.; Murakami, K.; Broughman, J.R.; Karandikar, U.; Tenge, V.R.; Neill, F.H.; Blutt, S.E.; Zeng, X.L.; Qu, L.; et al. Replication of human noroviruses in stem cell-derived human enteroids. Science 2016, 353, 1387–1393. [CrossRef] [PubMed]
69. Choi, J.M.; Hutson, A.M.; Estes, M.K.; Prasad, B.V. Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proc. Natl. Acad. Sci. USA 2008, 105, 9175–9180. [CrossRef] [PubMed]
70. Wilson, S.S.; Bromme, B.A.; Holly, M.K.; Wiens, M.E.; Gounder, A.P.; Sul, Y.; Smith, J.G. Alpha-defensin-dependent enhancement of enteric viral infection. PLoS Pathog. 2017, 13, e1006446. [CrossRef] [PubMed]
71. Smith, J.G.; Silvestry, M.; Lindert, S.; Lu, W.; Nemerow, G.R.; Stewart, P.L. Insight into the mechanisms of adenovirus capsid disassembly from studies of defensin neutralization. PLoS Pathog. 2010, 6, e1000959. [CrossRef] [PubMed]
72. Bohm, R.; Fleming, F.E.; Maggioni, A.; Dang, V.T.; Holloway, G.; Coulson, B.S.; von Itzstein, M.; Haselhorst, T. Revisiting the role of histo-blood group antigens in rotavirus host-cell invasion. Nat. Commun. 2015, 6, 5907. [CrossRef] [PubMed]