Modeling Host-Virus Interactions in Viral Infectious Diseases Using Stem-Cell-Derived Systems and CRISPR/Cas9 Technology
Abstract
:1. Introduction
2. Modeling of Viral Disease Using iPSC Technology
3. Modeling of Viral Pathogenesis Using Adult Stem-Cell-Derived Organoid Systems
4. Uses of Adult Stem-Cell-Derived Organoid Systems in Modeling Viral Pathogenesis
5. Applications of CRISPR/Cas9 Technologies in iPSC- and Adult Stem-Cell-Derived Systems for Viral Research
6. Targeted Approaches to Identify Host Factors Regulating Infection
7. CRISPR/Cas9-Mediated Genome Editing in Adult Stem-Cell-Derived Organoid Systems
8. Applications of Genome-Wide CRISPR/Cas9 Screening
9. Conclusions and Future Perspectives
Funding
Acknowledgments
Conflicts of Interest
References
- Mogensen, T.H. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin. Microbiol. Rev. 2009, 22, 240–273. [Google Scholar] [CrossRef] [PubMed]
- Zur Wiesch, P.A.; Kouyos, R.; Engelstadter, J.; Regoes, R.R.; Bonhoeffer, S. Population biological principles of drug-resistance evolution in infectious diseases. Lancet Infect. Dis. 2011, 11, 236–247. [Google Scholar] [CrossRef]
- Shaw, T.; Bartholomeusz, A.; Locarnini, S. HBV drug resistance: Mechanisms, detection and interpretation. J. Hepatol. 2006, 44, 593–606. [Google Scholar] [CrossRef] [PubMed]
- Sarrazin, C.; Kieffer, T.L.; Bartels, D.; Hanzelka, B.; Muh, U.; Welker, M.; Wincheringer, D.; Zhou, Y.; Chu, H.M.; Lin, C.; et al. Dynamic hepatitis c virus genotypic and phenotypic changes in patients treated with the protease inhibitor telaprevir. Gastroenterology 2007, 132, 1767–1777. [Google Scholar] [CrossRef] [PubMed]
- Cairns, R.A.; Harris, I.S.; Mak, T.W. Regulation of cancer cell metabolism. Nat. Rev. Cancer 2011, 11, 85–95. [Google Scholar] [CrossRef] [PubMed]
- Pan, C.; Kumar, C.; Bohl, S.; Klingmueller, U.; Mann, M. Comparative proteomic phenotyping of cell lines and primary cells to assess preservation of cell type-specific functions. Mol. Cell. Proteom. 2009, 8, 443–450. [Google Scholar] [CrossRef]
- Taylor, G. Animal models of respiratory syncytial virus infection. Vaccine 2017, 35, 469–480. [Google Scholar] [CrossRef] [Green Version]
- Warren, H.S.; Tompkins, R.G.; Moldawer, L.L.; Seok, J.; Xu, W.; Mindrinos, M.N.; Maier, R.V.; Xiao, W.; Davis, R.W. Mice are not men. Proc. Natl. Acad. Sci. USA 2015, 112, E345. [Google Scholar] [CrossRef]
- Takahashi, K.; Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126, 663–676. [Google Scholar] [CrossRef]
- Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131, 861–872. [Google Scholar] [CrossRef]
- Yu, J.; Vodyanik, M.A.; Smuga-Otto, K.; Antosiewicz-Bourget, J.; Frane, J.L.; Tian, S.; Nie, J.; Jonsdottir, G.A.; Ruotti, V.; Stewart, R.; et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318, 1917–1920. [Google Scholar] [CrossRef] [PubMed]
- Stadtfeld, M.; Hochedlinger, K. Induced pluripotency: History, mechanisms, and applications. Genes Dev. 2010, 24, 2239–2263. [Google Scholar] [CrossRef]
- Takahashi, K.; Yamanaka, S. A decade of transcription factor-mediated reprogramming to pluripotency. Nat. Rev. Mol. Cell Biol. 2016, 17, 183–193. [Google Scholar] [CrossRef] [PubMed]
- Passier, R.; Orlova, V.; Mummery, C. Complex tissue and disease modeling using hipscs. Cell Stem Cell 2016, 18, 309–321. [Google Scholar] [CrossRef] [PubMed]
- Avior, Y.; Sagi, I.; Benvenisty, N. Pluripotent stem cells in disease modelling and drug discovery. Nat. Rev. Mol. Cell Biol. 2016, 17, 170–182. [Google Scholar] [CrossRef] [PubMed]
- Clevers, H. Modeling development and disease with organoids. Cell 2016, 165, 1586–1597. [Google Scholar] [CrossRef]
- Pasca, S.P. The rise of three-dimensional human brain cultures. Nature 2018, 553, 437–445. [Google Scholar]
- Qian, X.; Nguyen, H.N.; Song, M.M.; Hadiono, C.; Ogden, S.C.; Hammack, C.; Yao, B.; Hamersky, G.R.; Jacob, F.; Zhong, C.; et al. Brain-region-specific organoids using mini-bioreactors for modeling zikv exposure. Cell 2016, 165, 1238–1254. [Google Scholar] [CrossRef]
- Ramani, S.; Crawford, S.E.; Blutt, S.E.; Estes, M.K. Human organoid cultures: Transformative new tools for human virus studies. Curr. Opin. Virol. 2018, 29, 79–86. [Google Scholar] [CrossRef]
- Hsu, P.D.; Lander, E.S.; Zhang, F. Development and applications of crispr-cas9 for genome engineering. Cell 2014, 157, 1262–1278. [Google Scholar] [CrossRef]
- Freiermuth, J.L.; Powell-Castilla, I.J.; Gallicano, G.I. Toward a crispr picture: Use of crispr/cas9 to model diseases in human stem cells in vitro. J. Cell. Biochem. 2018, 119, 62–68. [Google Scholar] [CrossRef]
- Hockemeyer, D.; Jaenisch, R. Induced pluripotent stem cells meet genome editing. Cell Stem Cell 2016, 18, 573–586. [Google Scholar] [CrossRef]
- Artegiani, B.; Clevers, H. Use and application of 3d-organoid technology. Hum. Mol. Genet. 2018, 27, R99–R107. [Google Scholar]
- Bayat, H.; Naderi, F.; Khan, A.H.; Memarnejadian, A.; Rahimpour, A. The impact of crispr-cas system on antiviral therapy. Adv. Pharm. Bull. 2018, 8, 591–597. [Google Scholar] [CrossRef]
- Carlin, A.F.; Shresta, S. Genome-wide approaches to unravelling host-virus interactions in dengue and zika infections. Curr. Opin. Virol. 2018, 34, 29–38. [Google Scholar] [CrossRef]
- Jiang, D.J.; Xu, C.L.; Tsang, S.H. Revolution in gene medicine therapy and genome surgery. Genes (Basel) 2018, 9, 575. [Google Scholar] [CrossRef]
- Davila, S.; Hibberd, M.L. Genome-wide association studies are coming for human infectious diseases. Genome Med. 2009, 1, 19. [Google Scholar] [CrossRef] [Green Version]
- Newport, M.J.; Finan, C. Genome-wide association studies and susceptibility to infectious diseases. Brief. Funct. Genom. 2011, 10, 98–107. [Google Scholar] [CrossRef] [Green Version]
- Fumagalli, M.; Pozzoli, U.; Cagliani, R.; Comi, G.P.; Bresolin, N.; Clerici, M.; Sironi, M. Genome-wide identification of susceptibility alleles for viral infections through a population genetics approach. PLoS Genet. 2010, 6, e1000849. [Google Scholar] [CrossRef]
- Kim, D.S.; Ross, P.J.; Zaslavsky, K.; Ellis, J. Optimizing neuronal differentiation from induced pluripotent stem cells to model asd. Front. Cell. Neurosci. 2014, 8, 109. [Google Scholar] [CrossRef]
- Palakkan, A.A.; Nanda, J.; Ross, J.A. Pluripotent stem cells to hepatocytes, the journey so far. Biomed. Rep. 2017, 6, 367–373. [Google Scholar] [CrossRef] [Green Version]
- Pickl, M.; Ries, C.H. Comparison of 3d and 2d tumor models reveals enhanced her2 activation in 3d associated with an increased response to trastuzumab. Oncogene 2009, 28, 461–468. [Google Scholar] [CrossRef]
- Langhans, S.A. Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front. Pharmacol. 2018, 9, 6. [Google Scholar] [CrossRef]
- Dutta, D.; Heo, I.; Clevers, H. Disease modeling in stem cell-derived 3d organoid systems. Trends Mol. Med. 2017, 23, 393–410. [Google Scholar] [CrossRef]
- Trevisan, M.; Sinigaglia, A.; Desole, G.; Berto, A.; Pacenti, M.; Palu, G.; Barzon, L. Modeling viral infectious diseases and development of antiviral therapies using human induced pluripotent stem cell-derived systems. Viruses 2015, 7, 3835–3856. [Google Scholar] [CrossRef]
- Nie, Y.Z.; Zheng, Y.W.; Miyakawa, K.; Murata, S.; Zhang, R.R.; Sekine, K.; Ueno, Y.; Takebe, T.; Wakita, T.; Ryo, A.; et al. Recapitulation of hepatitis b virus-host interactions in liver organoids from human induced pluripotent stem cells. EBioMedicine 2018, 35, 114–123. [Google Scholar] [CrossRef]
- Heymann, D.L.; Hodgson, A.; Sall, A.A.; Freedman, D.O.; Staples, J.E.; Althabe, F.; Baruah, K.; Mahmud, G.; Kandun, N.; Vasconcelos, P.F.; et al. Zika virus and microcephaly: Why is this situation a pheic? Lancet 2016, 387, 719–721. [Google Scholar] [CrossRef]
- Barkovich, A.J.; Guerrini, R.; Kuzniecky, R.I.; Jackson, G.D.; Dobyns, W.B. A developmental and genetic classification for malformations of cortical development: Update 2012. Brain 2012, 135, 1348–1369. [Google Scholar] [CrossRef]
- Calvet, G.; Aguiar, R.S.; Melo, A.S.O.; Sampaio, S.A.; de Filippis, I.; Fabri, A.; Araujo, E.S.M.; de Sequeira, P.C.; de Mendonca, M.C.L.; de Oliveira, L.; et al. Detection and sequencing of zika virus from amniotic fluid of fetuses with microcephaly in brazil: A case study. Lancet Infect. Dis. 2016, 16, 653–660. [Google Scholar] [CrossRef]
- Mlakar, J.; Korva, M.; Tul, N.; Popovic, M.; Poljsak-Prijatelj, M.; Mraz, J.; Kolenc, M.; Resman Rus, K.; Vesnaver Vipotnik, T.; Fabjan Vodusek, V.; et al. Zika virus associated with microcephaly. N. Engl. J. Med. 2016, 374, 951–958. [Google Scholar] [CrossRef]
- Tang, H.; Hammack, C.; Ogden, S.C.; Wen, Z.; Qian, X.; Li, Y.; Yao, B.; Shin, J.; Zhang, F.; Lee, E.M.; et al. Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 2016, 18, 587–590. [Google Scholar] [CrossRef]
- Oh, Y.; Zhang, F.; Wang, Y.; Lee, E.M.; Choi, I.Y.; Lim, H.; Mirakhori, F.; Li, R.; Huang, L.; Xu, T.; et al. Zika virus directly infects peripheral neurons and induces cell death. Nat. Neurosci. 2017, 20, 1209–1212. [Google Scholar] [CrossRef] [Green Version]
- Yoon, K.J.; Song, G.; Qian, X.; Pan, J.; Xu, D.; Rho, H.S.; Kim, N.S.; Habela, C.; Zheng, L.; Jacob, F.; et al. Zika-virus-encoded ns2a disrupts mammalian cortical neurogenesis by degrading adherens junction proteins. Cell Stem Cell 2017, 21, 349–358. [Google Scholar] [CrossRef]
- Garcez, P.P.; Loiola, E.C.; Madeiro da Costa, R.; Higa, L.M.; Trindade, P.; Delvecchio, R.; Nascimento, J.M.; Brindeiro, R.; Tanuri, A.; Rehen, S.K. Zika virus impairs growth in human neurospheres and brain organoids. Science 2016, 352, 816–818. [Google Scholar] [CrossRef] [Green Version]
- Watanabe, M.; Buth, J.E.; Vishlaghi, N.; de la Torre-Ubieta, L.; Taxidis, J.; Khakh, B.S.; Coppola, G.; Pearson, C.A.; Yamauchi, K.; Gong, D.; et al. Self-organized cerebral organoids with human-specific features predict effective drugs to combat zika virus infection. Cell Rep. 2017, 21, 517–532. [Google Scholar] [CrossRef]
- Gabriel, E.; Ramani, A.; Karow, U.; Gottardo, M.; Natarajan, K.; Gooi, L.M.; Goranci-Buzhala, G.; Krut, O.; Peters, F.; Nikolic, M.; et al. Recent zika virus isolates induce premature differentiation of neural progenitors in human brain organoids. Cell Stem Cell 2017, 20, 397–406. [Google Scholar] [CrossRef]
- Dang, J.; Tiwari, S.K.; Lichinchi, G.; Qin, Y.; Patil, V.S.; Eroshkin, A.M.; Rana, T.M. Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor tlr3. Cell Stem Cell 2016, 19, 258–265. [Google Scholar] [CrossRef]
- Lui, J.H.; Hansen, D.V.; Kriegstein, A.R. Development and evolution of the human neocortex. Cell 2011, 146, 18–36. [Google Scholar] [CrossRef]
- Cugola, F.R.; Fernandes, I.R.; Russo, F.B.; Freitas, B.C.; Dias, J.L.; Guimaraes, K.P.; Benazzato, C.; Almeida, N.; Pignatari, G.C.; Romero, S.; et al. The brazilian zika virus strain causes birth defects in experimental models. Nature 2016, 534, 267–271. [Google Scholar] [CrossRef]
- Zhang, F.; Hammack, C.; Ogden, S.C.; Cheng, Y.; Lee, E.M.; Wen, Z.; Qian, X.; Nguyen, H.N.; Li, Y.; Yao, B.; et al. Molecular signatures associated with zikv exposure in human cortical neural progenitors. Nucleic Acids Res. 2016, 44, 8610–8620. [Google Scholar] [CrossRef]
- Janssens, S.; Schotsaert, M.; Karnik, R.; Balasubramaniam, V.; Dejosez, M.; Meissner, A.; Garcia-Sastre, A.; Zwaka, T.P. Zika virus alters DNA methylation of neural genes in an organoid model of the developing human brain. mSystems 2018, 3, e00219-17. [Google Scholar] [CrossRef]
- Liang, Q.; Luo, Z.; Zeng, J.; Chen, W.; Foo, S.S.; Lee, S.A.; Ge, J.; Wang, S.; Goldman, S.A.; Zlokovic, B.V.; et al. Zika virus ns4a and ns4b proteins deregulate akt-mtor signaling in human fetal neural stem cells to inhibit neurogenesis and induce autophagy. Cell Stem Cell 2016, 19, 663–671. [Google Scholar] [CrossRef]
- Xu, M.; Lee, E.M.; Wen, Z.; Cheng, Y.; Huang, W.K.; Qian, X.; Tcw, J.; Kouznetsova, J.; Ogden, S.C.; Hammack, C.; et al. Identification of small-molecule inhibitors of zika virus infection and induced neural cell death via a drug repurposing screen. Nat. Med. 2016, 22, 1101–1107. [Google Scholar] [CrossRef]
- Schwartz, R.E.; Trehan, K.; Andrus, L.; Sheahan, T.P.; Ploss, A.; Duncan, S.A.; Rice, C.M.; Bhatia, S.N. Modeling hepatitis c virus infection using human induced pluripotent stem cells. Proc. Natl. Acad. Sci. USA 2012, 109, 2544–2548. [Google Scholar] [CrossRef]
- Wu, X.; Robotham, J.M.; Lee, E.; Dalton, S.; Kneteman, N.M.; Gilbert, D.M.; Tang, H. Productive hepatitis c virus infection of stem cell-derived hepatocytes reveals a critical transition to viral permissiveness during differentiation. PLoS Pathog. 2012, 8, e1002617. [Google Scholar] [CrossRef]
- Nelson, C.T.; Demmler, G.J. Cytomegalovirus infection in the pregnant mother, fetus, and newborn infant. Clin. Perinatol. 1997, 24, 151–160. [Google Scholar] [CrossRef]
- D’Aiuto, L.; Di Maio, R.; Heath, B.; Raimondi, G.; Milosevic, J.; Watson, A.M.; Bamne, M.; Parks, W.T.; Yang, L.; Lin, B.; et al. Human induced pluripotent stem cell-derived models to investigate human cytomegalovirus infection in neural cells. PLoS ONE 2012, 7, e49700. [Google Scholar] [CrossRef]
- Kretzschmar, K.; Clevers, H. Organoids: Modeling development and the stem cell niche in a dish. Dev. Cell 2016, 38, 590–600. [Google Scholar] [CrossRef]
- Rotavirus vaccines. WHO position paper—January 2013. Wkly. Epidemiol. Rec. 2013, 88, 49–64. [PubMed]
- Macartney, K.K.; Baumgart, D.C.; Carding, S.R.; Brubaker, J.O.; Offit, P.A. Primary murine small intestinal epithelial cells, maintained in long-term culture, are susceptible to rotavirus infection. J. Virol. 2000, 74, 5597–5603. [Google Scholar] [CrossRef]
- 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. 2016, 90, 43–56. [Google Scholar] [CrossRef]
- Yin, Y.; Bijvelds, M.; Dang, W.; Xu, L.; van der Eijk, A.A.; Knipping, K.; Tuysuz, N.; Dekkers, J.F.; Wang, Y.; de Jonge, J.; et al. Modeling rotavirus infection and antiviral therapy using primary intestinal organoids. Antiviral Res. 2015, 123, 120–131. [Google Scholar] [CrossRef]
- Ramani, S.; Atmar, R.L.; Estes, M.K. Epidemiology of human noroviruses and updates on vaccine development. Curr. Opin. Gastroenterol. 2014, 30, 25–33. [Google Scholar] [CrossRef] [Green Version]
- Belliot, G.; Lopman, B.A.; Ambert-Balay, K.; Pothier, P. The burden of norovirus gastroenteritis: An important foodborne and healthcare-related infection. Clin. Microbiol. Infect. 2014, 20, 724–730. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [Green Version]
- 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. [Google Scholar] [CrossRef] [Green Version]
- Van der Sanden, S.M.G.; Sachs, N.; Koekkoek, S.M.; Koen, G.; Pajkrt, D.; Clevers, H.; Wolthers, K.C. Enterovirus 71 infection of human airway organoids reveals vp1-145 as a viral infectivity determinant. Emerg. Microbes Infect. 2018, 7, 84. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Holly, M.K.; Smith, J.G. Adenovirus infection of human enteroids reveals interferon sensitivity and preferential infection of goblet cells. J. Virol. 2018. [Google Scholar] [CrossRef]
- To, K.K.; Chan, J.F.; Chen, H.; Li, L.; Yuen, K.Y. The emergence of influenza a h7n9 in human beings 16 years after influenza a h5n1: A tale of two cities. Lancet Infect. Dis. 2013, 13, 809–821. [Google Scholar] [CrossRef]
- Klenk, H.D. Influenza viruses en route from birds to man. Cell Host Microbe 2014, 15, 653–654. [Google Scholar] [CrossRef]
- Zhou, J.; Li, C.; Sachs, N.; Chiu, M.C.; Wong, B.H.; Chu, H.; Poon, V.K.; Wang, D.; Zhao, X.; Wen, L.; et al. Differentiated human airway organoids to assess infectivity of emerging influenza virus. Proc. Natl. Acad. Sci. USA 2018, 115, 6822–6827. [Google Scholar] [CrossRef]
- Sachs, N.; Zomer-van Ommen, D.D.; Papaspyropoulos, A.; Heo, I.; Bottinger, L.; Klay, D.; Weeber, F.; Huelsz-Prince, G.; Iakobachvili, N.; Viveen, M.C.; et al. Long-term expanding human airway organoids for disease modelling. EMBO J. 2018, 38, e100300. [Google Scholar] [CrossRef]
- Van der Oost, J.; Westra, E.R.; Jackson, R.N.; Wiedenheft, B. Unravelling the structural and mechanistic basis of crispr-cas systems. Nat. Rev. Microbiol. 2014, 12, 479–492. [Google Scholar] [CrossRef]
- Deltcheva, E.; Chylinski, K.; Sharma, C.M.; Gonzales, K.; Chao, Y.; Pirzada, Z.A.; Eckert, M.R.; Vogel, J.; Charpentier, E. Crispr rna maturation by trans-encoded small rna and host factor RNAse III. Nature 2011, 471, 602–607. [Google Scholar] [CrossRef]
- Barrangou, R. Diversity of crispr-cas immune systems and molecular machines. Genome Biol. 2015, 16, 247. [Google Scholar] [CrossRef]
- Brault, J.B.; Khou, C.; Basset, J.; Coquand, L.; Fraisier, V.; Frenkiel, M.P.; Goud, B.; Manuguerra, J.C.; Pardigon, N.; Baffet, A.D. Comparative analysis between flaviviruses reveals specific neural stem cell tropism for zika virus in the mouse developing neocortex. EBioMedicine 2016, 10, 71–76. [Google Scholar] [CrossRef]
- Nowakowski, T.J.; Pollen, A.A.; Di Lullo, E.; Sandoval-Espinosa, C.; Bershteyn, M.; Kriegstein, A.R. Expression analysis highlights axl as a candidate zika virus entry receptor in neural stem cells. Cell Stem Cell 2016, 18, 591–596. [Google Scholar] [CrossRef]
- Wells, M.F.; Salick, M.R.; Wiskow, O.; Ho, D.J.; Worringer, K.A.; Ihry, R.J.; Kommineni, S.; Bilican, B.; Klim, J.R.; Hill, E.J.; et al. Genetic ablation of axl does not protect human neural progenitor cells and cerebral organoids from zika virus infection. Cell Stem Cell 2016, 19, 703–708. [Google Scholar] [CrossRef]
- Broder, C.C.; Collman, R.G. Chemokine receptors and HIV. J. Leukoc Biol. 1997, 62, 20–29. [Google Scholar] [CrossRef]
- Kang, H.; Minder, P.; Park, M.A.; Mesquitta, W.T.; Torbett, B.E.; Slukvin, I.I. Ccr5 disruption in induced pluripotent stem cells using crispr/cas9 provides selective resistance of immune cells to ccr5-tropic HIV-1 virus. Mol. Ther. Nucleic Acids 2015, 4, e268. [Google Scholar] [CrossRef]
- Ye, L.; Wang, J.; Beyer, A.I.; Teque, F.; Cradick, T.J.; Qi, Z.; Chang, J.C.; Bao, G.; Muench, M.O.; Yu, J.; et al. Seamless modification of wild-type induced pluripotent stem cells to the natural ccr5delta32 mutation confers resistance to hiv infection. Proc. Natl. Acad. Sci. USA 2014, 111, 9591–9596. [Google Scholar] [CrossRef]
- Schwank, G.; Koo, B.K.; Sasselli, V.; Dekkers, J.F.; Heo, I.; Demircan, T.; Sasaki, N.; Boymans, S.; Cuppen, E.; van der Ent, C.K.; et al. Functional repair of cftr by crispr/cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell 2013, 13, 653–658. [Google Scholar] [CrossRef]
- Longmire, T.A.; Ikonomou, L.; Hawkins, F.; Christodoulou, C.; Cao, Y.; Jean, J.C.; Kwok, L.W.; Mou, H.; Rajagopal, J.; Shen, S.S.; et al. Efficient derivation of purified lung and thyroid progenitors from embryonic stem cells. Cell Stem Cell 2012, 10, 398–411. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Fessler, E.; Drost, J.; van Hooff, S.R.; Linnekamp, J.F.; Wang, X.; Jansen, M.; de Sousa, E.M.F.; Prasetyanti, P.R.; JE, I.J.; Franitza, M.; et al. Tgfbeta signaling directs serrated adenomas to the mesenchymal colorectal cancer subtype. EMBO Mol. Med. 2016, 8, 745–760. [Google Scholar] [CrossRef]
- Gao, X.; Bali, A.S.; Randell, S.H.; Hogan, B.L. Grhl2 coordinates regeneration of a polarized mucociliary epithelium from basal stem cells. J. Cell Biol. 2015, 211, 669–682. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Huch, M.; Gehart, H.; van Boxtel, R.; Hamer, K.; Blokzijl, F.; Verstegen, M.M.; Ellis, E.; van Wenum, M.; Fuchs, S.A.; de Ligt, J.; et al. Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell 2015, 160, 299–312. [Google Scholar] [CrossRef]
- Andersson-Rolf, A.; Merenda, A.; Mustata, R.C.; Li, T.; Dietmann, S.; Koo, B.K. Simultaneous paralogue knockout using a crispr-concatemer in mouse small intestinal organoids. Dev. Biol. 2016, 420, 271–277. [Google Scholar] [CrossRef]
- Andersson-Rolf, A.; Mustata, R.C.; Merenda, A.; Kim, J.; Perera, S.; Grego, T.; Andrews, K.; Tremble, K.; Silva, J.C.; Fink, J.; et al. One-step generation of conditional and reversible gene knockouts. Nat. Methods 2017, 14, 287–289. [Google Scholar] [CrossRef] [Green Version]
- Ramage, H.; Cherry, S. Virus-host interactions: From unbiased genetic screens to function. Annu. Rev. Virol. 2015, 2, 497–524. [Google Scholar] [CrossRef]
- Shalem, O.; Sanjana, N.E.; Hartenian, E.; Shi, X.; Scott, D.A.; Mikkelson, T.; Heckl, D.; Ebert, B.L.; Root, D.E.; Doench, J.G.; et al. Genome-scale crispr-cas9 knockout screening in human cells. Science 2014, 343, 84–87. [Google Scholar] [CrossRef]
- CRISPR Pooled Libraries. Available online: https://www.addgene.org/crispr/libraries/ (accessed on 25 May 2018).
- Savidis, G.; McDougall, W.M.; Meraner, P.; Perreira, J.M.; Portmann, J.M.; Trincucci, G.; John, S.P.; Aker, A.M.; Renzette, N.; Robbins, D.R.; et al. Identification of zika virus and dengue virus dependency factors using functional genomics. Cell Rep. 2016, 16, 232–246. [Google Scholar] [CrossRef]
- Zhang, R.; Miner, J.J.; Gorman, M.J.; Rausch, K.; Ramage, H.; White, J.P.; Zuiani, A.; Zhang, P.; Fernandez, E.; Zhang, Q.; et al. A crispr screen defines a signal peptide processing pathway required by flaviviruses. Nature 2016, 535, 164–168. [Google Scholar] [CrossRef]
- Marceau, C.D.; Puschnik, A.S.; Majzoub, K.; Ooi, Y.S.; Brewer, S.M.; Fuchs, G.; Swaminathan, K.; Mata, M.A.; Elias, J.E.; Sarnow, P.; et al. Genetic dissection of flaviviridae host factors through genome-scale crispr screens. Nature 2016, 535, 159–163. [Google Scholar] [CrossRef]
- Ma, H.; Dang, Y.; Wu, Y.; Jia, G.; Anaya, E.; Zhang, J.; Abraham, S.; Choi, J.G.; Shi, G.; Qi, L.; et al. A crispr-based screen identifies genes essential for west-nile-virus-induced cell death. Cell Rep. 2015, 12, 673–683. [Google Scholar] [CrossRef]
- Park, R.J.; Wang, T.; Koundakjian, D.; Hultquist, J.F.; Lamothe-Molina, P.; Monel, B.; Schumann, K.; Yu, H.; Krupzcak, K.M.; Garcia-Beltran, W.; et al. A genome-wide crispr screen identifies a restricted set of hiv host dependency factors. Nat. Genet. 2017, 49, 193–203. [Google Scholar] [CrossRef]
- Chakrabarti, J.; Holokai, L.; Syu, L.; Steele, N.; Chang, J.; Dlugosz, A.; Zavros, Y. Mouse-derived gastric organoid and immune cell co-culture for the study of the tumor microenvironment. Methods Mol. Biol. 2018, 1817, 157–168. [Google Scholar]
- Dijkstra, K.K.; Cattaneo, C.M.; Weeber, F.; Chalabi, M.; van de Haar, J.; Fanchi, L.F.; Slagter, M.; van der Velden, D.L.; Kaing, S.; Kelderman, S.; et al. Generation of tumor-reactive t cells by co-culture of peripheral blood lymphocytes and tumor organoids. Cell 2018, 174, 1586–1598. [Google Scholar] [CrossRef]
- Nie, J.; Hashino, E. Organoid technologies meet genome engineering. EMBO Rep. 2017, 18, 367–376. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Knott, G.J.; Doudna, J.A. Crispr-cas guides the future of genetic engineering. Science 2018, 361, 866–869. [Google Scholar] [CrossRef]
- Chen, H.; Ye, F.; Tang, W.; He, J.; Yin, M.; Wang, Y.; Xie, F.; Bi, E.; Yang, X.; Gratzel, M.; et al. A solvent- and vacuum-free route to large-area perovskite films for efficient solar modules. Nature 2017, 550, 92–95. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.S.; Dagdas, Y.S.; Kleinstiver, B.P.; Welch, M.M.; Sousa, A.A.; Harrington, L.B.; Sternberg, S.H.; Joung, J.K.; Yildiz, A.; Doudna, J.A. Enhanced proofreading governs crispr-cas9 targeting accuracy. Nature 2017, 550, 407–410. [Google Scholar] [CrossRef] [PubMed]
- Yin, H.; Song, C.Q.; Suresh, S.; Kwan, S.Y.; Wu, Q.; Walsh, S.; Ding, J.; Bogorad, R.L.; Zhu, L.J.; Wolfe, S.A.; et al. Partial DNA-guided cas9 enables genome editing with reduced off-target activity. Nat. Chem. Biol. 2018, 14, 311–316. [Google Scholar] [CrossRef] [PubMed]
- Fujii, M.; Matano, M.; Nanki, K.; Sato, T. Efficient genetic engineering of human intestinal organoids using electroporation. Nat. Protoc. 2015, 10, 1474–1485. [Google Scholar] [CrossRef] [PubMed]
- Glass, Z.; Lee, M.; Li, Y.; Xu, Q. Engineering the delivery system for crispr-based genome editing. Trends Biotechnol. 2018, 36, 173–185. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [PubMed]
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Kim, J.; Koo, B.-K.; Yoon, K.-J. Modeling Host-Virus Interactions in Viral Infectious Diseases Using Stem-Cell-Derived Systems and CRISPR/Cas9 Technology. Viruses 2019, 11, 124. https://doi.org/10.3390/v11020124
Kim J, Koo B-K, Yoon K-J. Modeling Host-Virus Interactions in Viral Infectious Diseases Using Stem-Cell-Derived Systems and CRISPR/Cas9 Technology. Viruses. 2019; 11(2):124. https://doi.org/10.3390/v11020124
Chicago/Turabian StyleKim, Jihoon, Bon-Kyoung Koo, and Ki-Jun Yoon. 2019. "Modeling Host-Virus Interactions in Viral Infectious Diseases Using Stem-Cell-Derived Systems and CRISPR/Cas9 Technology" Viruses 11, no. 2: 124. https://doi.org/10.3390/v11020124
APA StyleKim, J., Koo, B. -K., & Yoon, K. -J. (2019). Modeling Host-Virus Interactions in Viral Infectious Diseases Using Stem-Cell-Derived Systems and CRISPR/Cas9 Technology. Viruses, 11(2), 124. https://doi.org/10.3390/v11020124