1932

Abstract

Infectious diseases are the second leading cause of death worldwide. Although the host multitropism of some pathogens has rendered their manipulation possible in animal models, the human-restricted tropism of numerous viruses, bacteria, fungi, and parasites has seriously hampered our understanding of these pathogens. Hence, uncovering the genetic basis underlying the narrow tropism of such pathogens is critical for understanding their mechanisms of infection and pathogenesis. Moreover, such genetic dissection is essential for the generation of permissive animal models that can serve as critical tools for the development of therapeutics or vaccines against challenging human pathogens. In this review, we describe different experimental approaches utilized to uncover the genetic foundation regulating pathogen host tropism as well as their relevance for studying the tropism of several important human pathogens. Finally, we discuss the current and future uses of this knowledge for generating genetically modified animal models permissive for these pathogens.

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2015-11-23
2024-04-18
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Literature Cited

  1. Agarwal V, Hammerschmidt S, Malm S, Bergmann S, Riesbeck K, Blom AM. 1.  2012. Enolase of Streptococcus pneumoniae binds human complement inhibitor C4b-binding protein and contributes to complement evasion. J. Immunol. 189:3575–84 [Google Scholar]
  2. Ashour J, Morrison J, Laurent-Rolle M, Belicha-Villanueva A, Plumlee CR. 2.  et al. 2010. Mouse STAT2 restricts early dengue virus replication. Cell Host Microbe 8:410–21 [Google Scholar]
  3. Assiri A, McGeer A, Perl TM, Price CS, Al Rabeeah AA. 3.  et al. 2013. Hospital outbreak of Middle East respiratory syndrome coronavirus. N. Engl. J. Med. 369:407–16 [Google Scholar]
  4. Benga WJ, Krieger SE, Dimitrova M, Zeisel MB, Parnot M. 4.  et al. 2010. Apolipoprotein E interacts with hepatitis C virus nonstructural protein 5A and determines assembly of infectious particles. Hepatology 51:43–53 [Google Scholar]
  5. Berger KL, Cooper JD, Heaton NS, Yoon R, Oakland TE. 5.  et al. 2009. Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication. PNAS 106:7577–82 [Google Scholar]
  6. Bility MT, Cheng L, Zhang Z, Luan Y, Li F. 6.  et al. 2014. Hepatitis B virus infection and immunopathogenesis in a humanized mouse model: induction of human-specific liver fibrosis and M2-like macrophages. PLOS Pathog. 10:e1004032 [Google Scholar]
  7. Bitzegeio J, Bankwitz D, Hueging K, Haid S, Brohm C. 7.  et al. 2010. Adaptation of hepatitis C virus to mouse CD81 permits infection of mouse cells in the absence of human entry factors. PLOS Pathog. 6:e1000978 [Google Scholar]
  8. Bradfute SB, Warfield KL, Bray M. 8.  2012. Mouse models for filovirus infections. Viruses 4:1477–508 [Google Scholar]
  9. Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A. 9.  et al. 2008. Identification of host proteins required for HIV infection through a functional genomic screen. Science 319:921–26 [Google Scholar]
  10. Bray M, Davis K, Geisbert T, Schmaljohn C, Huggins J. 10.  1998. A mouse model for evaluation of prophylaxis and therapy of Ebola hemorrhagic fever. J. Infect. Dis. 178:651–61 [Google Scholar]
  11. Brehm MA, Shultz LD, Luban J, Greiner DL. 11.  2013. Overcoming current limitations in humanized mouse research. J. Infect. Dis. 208:Suppl. 2S125–30 [Google Scholar]
  12. Bushman FD, Malani N, Fernandes J, D'Orso I, Cagney G. 12.  et al. 2009. Host cell factors in HIV replication: meta-analysis of genome-wide studies. PLOS Pathog. 5:e1000437 [Google Scholar]
  13. Carette JE, Guimaraes CP, Varadarajan M, Park AS, Wuethrich I. 13.  et al. 2009. Haploid genetic screens in human cells identify host factors used by pathogens. Science 326:1231–35 [Google Scholar]
  14. Carette JE, Guimaraes CP, Wuethrich I, Blomen VA, Varadarajan M. 14.  et al. 2011. Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Nat. Biotechnol. 29:542–46 [Google Scholar]
  15. Carette JE, Raaben M, Wong AC, Herbert AS, Obernosterer G. 15.  et al. 2011. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477:340–43 [Google Scholar]
  16. Carlson DF, Tan W, Lillico SG, Stverakova D, Proudfoot C. 16.  et al. 2012. Efficient TALEN-mediated gene knockout in livestock. PNAS 109:17382–87 [Google Scholar]
  17. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H. 17.  et al. 2008. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455:757–63 [Google Scholar]
  18. Chen J, Zhao Y, Zhang C, Chen H, Feng J. 18.  et al. 2014. Persistent hepatitis C virus infections and hepatopathological manifestations in immune-competent humanized mice. Cell Res. 24:1050–66 [Google Scholar]
  19. Chen Q, Khoury M, Chen J. 19.  2009. Expression of human cytokines dramatically improves reconstitution of specific human-blood lineage cells in humanized mice. PNAS 106:21783–88 [Google Scholar]
  20. Cheng Y, Ma Z, Kim BH, Wu W, Cayting P. 20.  et al. 2014. Principles of regulatory information conservation between mouse and human. Nature 515:371–75 [Google Scholar]
  21. Cho A, Haruyama N, Kulkarni AB. 21.  2009. Generation of transgenic mice. Curr. Protoc. Cell Biol. doi: 10.1002/0471143030.cb1911s42
  22. Cowan S, Hatziioannou T, Cunningham T, Muesing MA, Gottlinger HG, Bieniasz PD. 22.  2002. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. PNAS 99:11914–19 [Google Scholar]
  23. Cui D, Li J, Zhang L, Liu S, Wen X. 23.  et al. 2015. Generation of bi-transgenic pigs overexpressing human lactoferrin and lysozyme in milk. Transgenic Res. 24:365–73 [Google Scholar]
  24. Darmstadt GL, Mentele L, Podbielski A, Rubens CE. 24.  2000. Role of group A streptococcal virulence factors in adherence to keratinocytes. Infect. Immun. 68:1215–21 [Google Scholar]
  25. Dave S, Brooks-Walter A, Pangburn MK, McDaniel LS. 25.  2001. PspC, a pneumococcal surface protein, binds human factor H. Infect. Immun. 69:3435–37 [Google Scholar]
  26. de Jong YP, Dorner M, Mommersteeg MC, Xiao JW, Balazs AB. 26.  et al. 2014. Broadly neutralizing antibodies abrogate established hepatitis C virus infection. Sci. Transl. Med. 6:254ra129 [Google Scholar]
  27. de Jong YP, Rice CM, Ploss A. 27.  2010. New horizons for studying human hepatotropic infections. J. Clin. Investig. 120:650–53 [Google Scholar]
  28. Del Prete GQ, Ailers B, Moldt B, Keele BF, Estes JD. 28.  et al. 2014. Selection of unadapted, pathogenic SHIVs encoding newly transmitted HIV-1 envelope proteins. Cell Host Microbe 16:412–18 [Google Scholar]
  29. Disson O, Grayo S, Huillet E, Nikitas G, Langa-Vives F. 29.  et al. 2008. Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis. Nature 455:1114–18 [Google Scholar]
  30. Do Carmo S, Cuello AC. 30.  2013. Modeling Alzheimer's disease in transgenic rats. Mol. Neurodegener. 8:37 [Google Scholar]
  31. Dorner M, Horwitz JA, Donovan BM, Labitt RN, Budell WC. 31.  et al. 2013. Completion of the entire hepatitis C virus life cycle in genetically humanized mice. Nature 501:237–41 [Google Scholar]
  32. Dorner M, Horwitz JA, Robbins JB, Barry WT, Feng Q. 32.  et al. 2011. A genetically humanized mouse model for hepatitis C virus infection. Nature 474:208–11 [Google Scholar]
  33. Dragunsky E, Nomura T, Karpinski K, Furesz J, Wood DJ. 33.  et al. 2003. Transgenic mice as an alternative to monkeys for neurovirulence testing of live oral poliovirus vaccine: validation by a WHO collaborative study. Bull. World Health Organ. 81:251–60 [Google Scholar]
  34. Elde NC, Child SJ, Geballe AP, Malik HS. 34.  2009. Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457:485–89 [Google Scholar]
  35. Etemad-Moghadam B, Sun Y, Nicholson EK, Fernandes M, Liou K. 35.  et al. 2000. Envelope glycoprotein determinants of increased fusogenicity in a pathogenic simian-human immunodeficiency virus (SHIV-KB9) passaged in vivo. J. Virol. 74:4433–40 [Google Scholar]
  36. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M. 36.  et al. 2007. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801–5 [Google Scholar]
  37. Frentzen A, Anggakusuma, Gurlevik E, Hueging K, Knocke S. 37.  et al. 2014. Cell entry, efficient RNA replication, and production of infectious hepatitis C virus progeny in mouse liver-derived cells. Hepatology 59:78–88 [Google Scholar]
  38. Frentzen A, Huging K, Bitzegeio J, Friesland M, Haid S. 38.  et al. 2011. Completion of hepatitis C virus replication cycle in heterokaryons excludes dominant restrictions in human non-liver and mouse liver cell lines. PLOS Pathog.e1002029
  39. Gaska JM, Ploss A. 39.  2015. Study of viral pathogenesis in humanized mice. Curr. Opin. Virol. 11C:14–20 [Google Scholar]
  40. Gottlinger HG, Dorfman T, Cohen EA, Haseltine WA. 40.  1993. Vpu protein of human immunodeficiency virus type 1 enhances the release of capsids produced by gag gene constructs of widely divergent retroviruses. PNAS 90:7381–85 [Google Scholar]
  41. Graef KM, Vreede FT, Lau YF, McCall AW, Carr SM. 41.  et al. 2010. The PB2 subunit of the influenza virus RNA polymerase affects virulence by interacting with the mitochondrial antiviral signaling protein and inhibiting expression of beta interferon. J. Virol. 84:8433–45 [Google Scholar]
  42. Grant D, Tan GK, Qing M, Ng JKW, Yip A. 42.  et al. 2011. A single amino acid in nonstructural protein NS4B confers virulence to dengue virus in AG129 mice through enhancement of viral RNA synthesis. J. Virol. 85:7775–87 [Google Scholar]
  43. Guidotti LG, Matzke B, Schaller H, Chisari FV. 43.  1995. High-level hepatitis B virus replication in transgenic mice. J. Virol. 69:6158–69 [Google Scholar]
  44. Gutti TL, Knibbe JS, Makarov E, Zhang J, Yannam GR. 44.  et al. 2014. Human hepatocytes and hematolymphoid dual reconstitution in treosulfan-conditioned uPA-NOG mice. Am. J. Pathol. 184:101–9 [Google Scholar]
  45. Hammerschmidt S, Tillig MP, Wolff S, Vaerman JP, Chhatwal GS. 45.  2000. Species-specific binding of human secretory component to SpsA protein of Streptococcus pneumoniae via a hexapeptide motif. Mol. Microbiol. 36:726–36 [Google Scholar]
  46. Harouse JM, Gettie A, Eshetu T, Tan RC, Bohm R. 46.  et al. 2001. Mucosal transmission and induction of simian AIDS by CCR5-specific simian/human immunodeficiency virus SHIV(SF162P3). J. Virol. 75:1990–95 [Google Scholar]
  47. Hatziioannou T, Cowan S, Goff SP, Bieniasz PD, Towers GJ. 47.  2003. Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J. 22:385–94 [Google Scholar]
  48. Hatziioannou T, Cowan S, Von Schwedler UK, Sundquist WI, Bieniasz PD. 48.  2004. Species-specific tropism determinants in the human immunodeficiency virus type 1 capsid. J. Virol. 78:6005–12 [Google Scholar]
  49. Hatziioannou T, Del Prete GQ, Keele BF, Estes JD, McNatt MW. 49.  et al. 2014. HIV-1-induced AIDS in monkeys. Science 344:1401–5 [Google Scholar]
  50. Hatziioannou T, Princiotta M, Piatak M Jr, Yuan F, Zhang F. 50.  et al. 2006. Generation of simian-tropic HIV-1 by restriction factor evasion. Science 314:95 [Google Scholar]
  51. Hauschild J, Petersen B, Santiago Y, Queisser AL, Carnwath JW. 51.  et al. 2011. Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. PNAS 108:12013–17 [Google Scholar]
  52. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E. 52.  et al. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534–41 [Google Scholar]
  53. Horvat B, Rivailler P, Varior-Krishnan G, Cardoso A, Gerlier D, Rabourdin-Combe C. 53.  1996. Transgenic mice expressing human measles virus (MV) receptor CD46 provide cells exhibiting different permissivities to MV infections. J. Virol. 70:6673–81 [Google Scholar]
  54. Hsu M, Ho SH, Balfe P, Gettie A, Harouse J. 54.  et al. 2005. A CCR5-tropic simian-HIV molecular clone capable of inducing AIDS in rhesus macaques. J. Acquir. Immune Defic. Syndr. 40:383–87 [Google Scholar]
  55. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M. 55.  et al. 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420–28 [Google Scholar]
  56. Iwai A, Shiozaki T, Kawai T, Akira S, Kawaoka Y. 56.  et al. 2010. Influenza A virus polymerase inhibits type I interferon induction by binding to interferon beta promoter stimulator 1. J. Biol. Chem. 285:32064–74 [Google Scholar]
  57. Jae LT, Raaben M, Herbert AS, Kuehne AI, Wirchnianski AS. 57.  et al. 2014. Virus entry. Lassa virus entry requires a trigger-induced receptor switch. Science 344:1506–10 [Google Scholar]
  58. Jae LT, Raaben M, Riemersma M, van Beusekom E, Blomen VA. 58.  et al. 2013. Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry. Science 340:479–83 [Google Scholar]
  59. Johansson L, Rytkonen A, Bergman P, Albiger B, Kallstrom H. 59.  et al. 2003. CD46 in meningococcal disease. Science 301:373–75 [Google Scholar]
  60. Jones JM, Meisler MH. 60.  2014. Modeling human epilepsy by TALEN targeting of mouse sodium channel Scn8a. Genesis 52:141–48 [Google Scholar]
  61. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. 61.  2005. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309:1577–81 [Google Scholar]
  62. Kilian M, Mestecky J, Schrohenloher RE. 62.  1979. Pathogenic species of the genus Haemophilus and Streptococcus pneumoniae produce immunoglobulin A1 protease. Infect. Immun. 26:143–49 [Google Scholar]
  63. Kim H, Kim JS. 63.  2014. A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 15:321–34 [Google Scholar]
  64. Klimkait T, Strebel K, Hoggan MD, Martin MA, Orenstein JM. 64.  1990. The human immunodeficiency virus type 1–specific protein vpu is required for efficient virus maturation and release. J. Virol. 64:621–29 [Google Scholar]
  65. Kohaar I, Ploss A, Korol E, Mu K, Schoggins JW. 65.  et al. 2010. Splicing diversity of the human OCLN gene and its biological significance for hepatitis C virus entry. J. Virol. 84:6987–94 [Google Scholar]
  66. Koike S, Taya C, Kurata T, Abe S, Ise I. 66.  et al. 1991. Transgenic mice susceptible to poliovirus. PNAS 88:951–55 [Google Scholar]
  67. Konig R, Zhou YY, Elleder D, Diamond TL, Bonamy GMC. 67.  et al. 2008. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 135:49–60 [Google Scholar]
  68. Kootstra NA, Munk C, Tonnu N, Landau NR, Verma IM. 68.  2003. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. PNAS 100:1298–303 [Google Scholar]
  69. Krishnan MN, Ng A, Sukumaran B, Gilfoy FD, Uchil PD. 69.  et al. 2008. RNA interference screen for human genes associated with West Nile virus infection. Nature 455:242–44 [Google Scholar]
  70. Lecuit M, Vandormael-Pournin S, Lefort J, Huerre M, Gounon P. 70.  et al. 2001. A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292:1722–25 [Google Scholar]
  71. Leeb M, Wutz A. 71.  2011. Derivation of haploid embryonic stem cells from mouse embryos. Nature 479:131–34 [Google Scholar]
  72. Legrand N, Ploss A, Balling R, Becker PD, Borsotti C. 72.  et al. 2009. Humanized mice for modeling human infectious disease: challenges, progress, and outlook. Cell Host Microbe 6:5–9 [Google Scholar]
  73. Li K, Foy E, Ferreon JC, Nakamura M, Ferreon AC. 73.  et al. 2005. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. PNAS 102:2992–97 [Google Scholar]
  74. Li Q, Brass AL, Ng A, Hu Z, Xavier RJ. 74.  et al. 2009. A genome-wide genetic screen for host factors required for hepatitis C virus propagation. PNAS 106:16410–15 [Google Scholar]
  75. Li Q, Zhang YY, Chiu S, Hu Z, Lan KH. 75.  et al. 2014. Integrative functional genomics of hepatitis C virus infection identifies host dependencies in complete viral replication cycle. PLOS Pathog. 10:e1004163 [Google Scholar]
  76. Long G, Hiet MS, Windisch MP, Lee JY, Lohmann V, Bartenschlager R. 76.  2011. Mouse hepatic cells support assembly of infectious hepatitis C virus particles. Gastroenterology 141:1057–66 [Google Scholar]
  77. Lovkvist L, Sjolinder H, Wehelie R, Aro H, Norrby-Teglund A. 77.  et al. 2008. CD46 contributes to the severity of group A streptococcal infection. Infect. Immun. 76:3951–58 [Google Scholar]
  78. Lu L, Lamm ME, Li H, Corthesy B, Zhang JR. 78.  2003. The human polymeric immunoglobulin receptor binds to Streptococcus pneumoniae via domains 3 and 4. J. Biol. Chem. 278:48178–87 [Google Scholar]
  79. Lu L, Ma Y, Zhang JR. 79.  2006. Streptococcus pneumoniae recruits complement factor H through the amino terminus of CbpA. J. Biol. Chem. 281:15464–74 [Google Scholar]
  80. Lu L, Ma Z, Jokiranta TS, Whitney AR, DeLeo FR, Zhang JR. 80.  2008. Species-specific interaction of Streptococcus pneumoniae with human complement factor H. J. Immunol. 181:7138–46 [Google Scholar]
  81. Madani N, Kabat D. 81.  1998. An endogenous inhibitor of human immunodeficiency virus in human lymphocytes is overcome by the viral Vif protein. J. Virol. 72:10251–55 [Google Scholar]
  82. Mailly L, Robinet E, Meuleman P, Baumert TF, Zeisel MB. 82.  2013. Hepatitis C virus infection and related liver disease: the quest for the best animal model. Front. Microbiol. 4:213 [Google Scholar]
  83. Malim MH. 83.  2009. APOBEC proteins and intrinsic resistance to HIV-1 infection. Philos. Trans. R. Soc. Lond. Series B 364:675–87 [Google Scholar]
  84. Malim MH, Bieniasz PD. 84.  2012. HIV restriction factors and mechanisms of evasion. Cold Spring Harb. Perspect. Med. 2:a006940 [Google Scholar]
  85. Malimas T, Yukphan P, Takahashi M, Muramatsu Y, Kaneyasu M. 85.  et al. 2009. Gluconobacter japonicus sp. nov., an acetic acid bacterium in the Alphaproteobacteria. Int. J. Syst. Evol. Microbiol. 59:466–71 [Google Scholar]
  86. Manz B, Schwemmle M, Brunotte L. 86.  2013. Adaptation of avian influenza A virus polymerase in mammals to overcome the host species barrier. J. Virol. 87:7200–9 [Google Scholar]
  87. Matsui H, Sekiya Y, Nakamura M, Murayama SY, Yoshida H. 87.  et al. 2009. CD46 transgenic mouse model of necrotizing fasciitis caused by Streptococcus pyogenes infection. Infect. Immun. 77:4806–14 [Google Scholar]
  88. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M. 88.  et al. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167–72 [Google Scholar]
  89. Miller EH, Obernosterer G, Raaben M, Herbert AS, Deffieu MS. 89.  et al. 2012. Ebola virus entry requires the host-programmed recognition of an intracellular receptor. EMBO J. 31:1947–60 [Google Scholar]
  90. Moncorge O, Mura M, Barclay WS. 90.  2010. Evidence for avian and human host cell factors that affect the activity of influenza virus polymerase. J. Virol. 84:9978–86 [Google Scholar]
  91. Morrison J, Laurent-Rolle M, Maestre AM, Rajsbaum R, Pisanelli G. 91.  et al. 2013. Dengue virus co-opts UBR4 to degrade STAT2 and antagonize type I interferon signaling. PLOS Pathog. 9:e1003265 [Google Scholar]
  92. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J. 92.  et al. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918–21 [Google Scholar]
  93. Neil SJ, Eastman SW, Jouvenet N, Bieniasz PD. 93.  2006. HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLOS Pathog. 2:e39 [Google Scholar]
  94. Neil SJ, Sandrin V, Sundquist WI, Bieniasz PD. 94.  2007. An interferon-alpha-induced tethering mechanism inhibits HIV-1 and Ebola virus particle release but is counteracted by the HIV-1 Vpu protein. Cell Host Microbe 2:193–203 [Google Scholar]
  95. Neil SJ, Zang T, Bieniasz PD. 95.  2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425–30 [Google Scholar]
  96. Ngampasutadol J, Ram S, Blom AM, Jarva H, Jerse AE. 96.  et al. 2005. Human C4b-binding protein selectively interacts with Neisseria gonorrhoeae and results in species-specific infection. PNAS 102:17142–47 [Google Scholar]
  97. Niu Y, Shen B, Cui Y, Chen Y, Wang J. 97.  et al. 2014. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156:836–43 [Google Scholar]
  98. Ohka S, Igarashi H, Nagata N, Sakai M, Koike S. 98.  et al. 2007. Establishment of a poliovirus oral infection system in human poliovirus receptor-expressing transgenic mice that are deficient in alpha/beta interferon receptor. J. Virol. 81:7902–12 [Google Scholar]
  99. Okada N, Liszewski MK, Atkinson JP, Caparon M. 99.  1995. Membrane cofactor protein (CD46) is a keratinocyte receptor for the M protein of the group A streptococcus. PNAS 92:2489–93 [Google Scholar]
  100. Oldstone MB, Lewicki H, Thomas D, Tishon A, Dales S. 100.  et al. 1999. Measles virus infection in a transgenic model: virus-induced immunosuppression and central nervous system disease. Cell 98:629–40 [Google Scholar]
  101. Owens CA, Yang PC, Gottlinger H, Sodroski J. 101.  2003. Human and simian immunodeficiency virus capsid proteins are major viral determinants of early, postentry replication blocks in simian cells. J. Virol. 77:726–31 [Google Scholar]
  102. Patel MR, Loo YM, Horner SM, Gale M Jr, Malik HS. 102.  2012. Convergent evolution of escape from hepaciviral antagonism in primates. PLOS Biol. 10:e1001282 [Google Scholar]
  103. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F. 103.  et al. 1998. Binding of hepatitis C virus to CD81. Science 282:938–41 [Google Scholar]
  104. Platt RJ, Chen S, Zhou Y, Yim MJ, Swiech L. 104.  et al. 2014. CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 159:440–55 [Google Scholar]
  105. Plaut AG, Gilbert JV, Artenstein MS, Capra JD. 105.  1975. Neisseria gonorrhoeae and Neisseria meningitidis: extracellular enzyme cleaves human immunoglobulin A. Science 190:1103–5 [Google Scholar]
  106. Ploss A, Dubuisson J. 106.  2012. New advances in the molecular biology of hepatitis C virus infection: towards the identification of new treatment targets. Gut 61:Suppl. 1i25–35 [Google Scholar]
  107. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H. 107.  et al. 2009. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457:882–86 [Google Scholar]
  108. Ploss A, Khetani SR, Jones CT, Syder AJ, Trehan K. 108.  et al. 2010. Persistent hepatitis C virus infection in microscale primary human hepatocyte cultures. PNAS 107:3141–45 [Google Scholar]
  109. Plummer EM, Shresta S. 109.  2014. Mouse models for dengue vaccines and antivirals. J. Immunol. Methods 410:34–38 [Google Scholar]
  110. Raj VS, Mou HH, Smits SL, Dekkers DHW, Muller MA. 110.  et al. 2013. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251–54 [Google Scholar]
  111. Randall G, Panis M, Cooper JD, Tellinghuisen TL, Sukhodolets KE. 111.  et al. 2007. Cellular cofactors affecting hepatitis C virus infection and replication. PNAS 104:12884–89 [Google Scholar]
  112. Raney AK, Eggers CM, Kline EF, Guidotti LG, Pontoglio M. 112.  et al. 2001. Nuclear covalently closed circular viral genomic DNA in the liver of hepatocyte nuclear factor 1 alpha-null hepatitis B virus transgenic mice. J. Virol. 75:2900–11 [Google Scholar]
  113. Reimann KA, Li JT, Voss G, Lekutis C, Tenner-Racz K. 113.  et al. 1996. An env gene derived from a primary human immunodeficiency virus type 1 isolate confers high in vivo replicative capacity to a chimeric simian/human immunodeficiency virus in rhesus monkeys. J. Virol. 70:3198–206 [Google Scholar]
  114. Ren RB, Costantini F, Gorgacz EJ, Lee JJ, Racaniello VR. 114.  1990. Transgenic mice expressing a human poliovirus receptor: a new model for poliomyelitis. Cell 63:353–62 [Google Scholar]
  115. Rezcallah MS, Hodges K, Gill DB, Atkinson JP, Wang B, Cleary PP. 115.  2005. Engagement of CD46 and alpha5beta1 integrin by group A streptococci is required for efficient invasion of epithelial cells. Cell. Microbiol. 7:645–53 [Google Scholar]
  116. Rouet P, Smih F, Jasin M. 116.  1994. Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell. Biol. 14:8096–106 [Google Scholar]
  117. Saeed M, Shiina M, Date T, Akazawa D, Watanabe N. 117.  et al. 2011. In vivo adaptation of hepatitis C virus in chimpanzees for efficient virus production and evasion of apoptosis. Hepatology 54:425–33 [Google Scholar]
  118. Saito S, Heller T, Yoneda M, Takahashi H, Nakajima A, Liang JT. 118.  2007. Lifestyle-related diseases of the digestive system: a new in vitro model of hepatitis C virion production: application of basic research on hepatitis C virus to clinical medicine. J. Pharmacol. Sci. 105:138–44 [Google Scholar]
  119. Sanjana NE, Shalem O, Zhang F. 119.  2014. Improved vectors and genome-wide libraries for CRISPR screening. Nat. Methods 11:783–84 [Google Scholar]
  120. Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S. 120.  et al. 2002. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 21:5017–25 [Google Scholar]
  121. Schieck A, Schulze A, Gahler C, Muller T, Haberkorn U. 121.  et al. 2013. Hepatitis B virus hepatotropism is mediated by specific receptor recognition in the liver and not restricted to susceptible hosts. Hepatology 58:43–53 [Google Scholar]
  122. Schoggins JW, Dorner M, Feulner M, Imanaka N, Murphy MY. 122.  et al. 2012. Dengue reporter viruses reveal viral dynamics in interferon receptor-deficient mice and sensitivity to interferon effectors in vitro. PNAS 109:14610–15 [Google Scholar]
  123. Sessions OM, Barrows NJ, Souza-Neto JA, Robinson TJ, Hershey CL. 123.  et al. 2009. Discovery of insect and human dengue virus host factors. Nature 458:1047–50 [Google Scholar]
  124. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA. 124.  et al. 2014. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87 [Google Scholar]
  125. Sheahan T, Jones CT, Ploss A. 125.  2010. Advances and challenges in studying hepatitis C virus in its native environment. Expert Rev. Gastroenterol. Hepatol. 4:541–50 [Google Scholar]
  126. Sheehy AM, Gaddis NC, Choi JD, Malim MH. 126.  2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646–50 [Google Scholar]
  127. Shresta S, Kyle JL, Snider HM, Basavapatna M, Beatty PR, Harris E. 127.  2004. Interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas T- and B-cell-dependent immunity are less critical. J. Virol. 78:2701–10 [Google Scholar]
  128. Shresta S, Sharar KL, Prigozhin DM, Beatty PR, Harris E. 128.  2006. Murine model for dengue virus-induced lethal disease with increased vascular permeability. J. Virol. 80:10208–17 [Google Scholar]
  129. Shultz LD, Brehm MA, Garcia-Martinez JV, Greiner DL. 129.  2012. Humanized mice for immune system investigation: progress, promise and challenges. Nat. Rev. Immunol. 12:786–98 [Google Scholar]
  130. Silvie O, Greco C, Franetich JF, Dubart-Kupperschmitt A, Hannoun L. 130.  et al. 2006. Expression of human CD81 differently affects host cell susceptibility to malaria sporozoites depending on the Plasmodium species. Cell. Microbiol. 8:1134–46 [Google Scholar]
  131. Simon JH, Gaddis NC, Fouchier RA, Malim MH. 131.  1998. Evidence for a newly discovered cellular anti-HIV-1 phenotype. Nat. Med. 4:1397–400 [Google Scholar]
  132. Smith BL, Hostetter MK. 132.  2000. C3 as substrate for adhesion of Streptococcus pneumoniae. J. Infect. Dis. 182:497–508 [Google Scholar]
  133. Soll SJ, Wilson SJ, Kutluay SB, Hatziioannou T, Bieniasz PD. 133.  2013. Assisted evolution enables HIV-1 to overcome a high TRIM5α-imposed genetic barrier to rhesus macaque tropism. PLOS Pathog. 9:e1003667 [Google Scholar]
  134. Steel J, Lowen AC, Mubareka S, Palese P. 134.  2009. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLOS Pathog. 5:e1000252 [Google Scholar]
  135. Steinhauer DA, Skehel JJ. 135.  2002. Genetics of influenza viruses. Annu. Rev. Genet. 36:305–32 [Google Scholar]
  136. Stergachis AB, Neph S, Sandstrom R, Haugen E, Reynolds AP. 136.  et al. 2014. Conservation of trans-acting circuitry during mammalian regulatory evolution. Nature 515:365–70 [Google Scholar]
  137. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. 137.  2004. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427:848–53 [Google Scholar]
  138. Sun H, Ringdahl U, Homeister JW, Fay WP, Engleberg NC. 138.  et al. 2004. Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 305:1283–86 [Google Scholar]
  139. Supekova L, Supek F, Lee J, Chen S, Gray N. 139.  et al. 2008. Identification of human kinases involved in hepatitis C virus replication by small interference RNA library screening. J. Biol. Chem. 283:29–36 [Google Scholar]
  140. Tai AW, Benita Y, Peng LF, Kim SS, Sakamoto N. 140.  et al. 2009. A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host Microbe 5:298–307 [Google Scholar]
  141. Tesson L, Usal C, Menoret S, Leung E, Niles BJ. 141.  et al. 2011. Knockout rats generated by embryo microinjection of TALENs. Nat. Biotechnol. 29:695–96 [Google Scholar]
  142. Tjoumakaris SI, Chalouhi N, Ghobrial GM, Jabbour P, Dumont AS. 142.  et al. 2012. Efficacy of endovascular stroke management in elderly patients. J. Neurointerv. Surg. doi: neurintsurg-2012-010525
  143. Uprichard SL, Chung J, Chisari FV, Wakita T. 143.  2006. Replication of a hepatitis C virus replicon clone in mouse cells. Virol. J. 3:89 [Google Scholar]
  144. Urnov FD, Miller JC, Lee YL, Beausejour CM, Rock JM. 144.  et al. 2005. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435:646–51 [Google Scholar]
  145. Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD. 145.  2010. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 11:636–46 [Google Scholar]
  146. Varble A, Benitez AA, Schmid S, Sachs D, Shim JV. 146.  et al. 2013. An in vivo RNAi screening approach to identify host determinants of virus replication. Cell Host Microbe 14:346–56 [Google Scholar]
  147. Varthakavi V, Smith RM, Bour SP, Strebel K, Spearman P. 147.  2003. Viral protein U counteracts a human host cell restriction that inhibits HIV-1 particle production. PNAS 100:15154–59 [Google Scholar]
  148. Vogt A, Scull MA, Friling T, Horwitz JA, Donovan BM. 148.  et al. 2013. Recapitulation of the hepatitis C virus life-cycle in engineered murine cell lines. Virology 444:1–11 [Google Scholar]
  149. von Schaewen M, Ploss A. 149.  2014. Murine models of hepatitis C: What can we look forward to?. Antivir. Res. 104:15–22 [Google Scholar]
  150. Wanaguru M, Liu W, Hahn BH, Rayner JC, Wright GJ. 150.  2013. RH5-Basigin interaction plays a major role in the host tropism of Plasmodium falciparum. PNAS 110:20735–40 [Google Scholar]
  151. Wang F, Ma Y, Barrett JW, Gao X, Loh J. 151.  et al. 2004. Disruption of Erk-dependent type I interferon induction breaks the myxoma virus species barrier. Nat. Immunol. 5:1266–74 [Google Scholar]
  152. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW. 152.  et al. 2013. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–18 [Google Scholar]
  153. Washburn ML, Bility MT, Zhang L, Kovalev GI, Buntzman A. 153.  et al. 2011. A humanized mouse model to study hepatitis C virus infection, immune response, and liver disease. Gastroenterology 140:1334–44 [Google Scholar]
  154. 154. WHO 2008. Introduction. Global Burden of Disease: 2004 Update. Geneva, Switz: WHO [Google Scholar]
  155. Wilson EM, Bial J, Tarlow B, Bial G, Jensen B. 155.  et al. 2014. Extensive double humanization of both liver and hematopoiesis in FRGN mice. Stem Cell Res. 13:404–12 [Google Scholar]
  156. Yan H, Zhong G, Xu G, He W, Jing Z. 156.  et al. 2012. Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. eLife 1:e00049 [Google Scholar]
  157. Yang H, Liu Z, Ma Y, Zhong C, Yin Q. 157.  et al. 2013. Generation of haploid embryonic stem cells from Macaca fascicularis monkey parthenotes. Cell Res. 23:1187–200 [Google Scholar]
  158. Yasunaga A, Hanna SL, Li J, Cho H, Rose PP. 158.  et al. 2014. Genome-wide RNAi screen identifies broadly-acting host factors that inhibit arbovirus infection. PLOS Pathog. 10:e1003914 [Google Scholar]
  159. Yeung ML, Houzet L, Yedavalli VS, Jeang KT. 159.  2009. A genome-wide short hairpin RNA screening of Jurkat T-cells for human proteins contributing to productive HIV-1 replication. J. Biol. Chem. 284:19463–73 [Google Scholar]
  160. Yue F, Cheng Y, Breschi A, Vierstra J, Wu W. 160.  et al. 2014. A comparative encyclopedia of DNA elements in the mouse genome. Nature 515:355–64 [Google Scholar]
  161. Yin Z, Chen YL, Schul W, Wang QY, Gu F. 161.  et al. 2009. An adenosine nucleoside inhibitor of dengue virus. PNAS 106:20435–39 [Google Scholar]
  162. Zellweger RM, Shresta S. 162.  2014. Mouse models to study dengue virus immunology and pathogenesis. Front. Immunol. 5:151 [Google Scholar]
  163. Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D. 163.  et al. 2009. Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6:54–67 [Google Scholar]
  164. Zhang JR, Mostov KE, Lamm ME, Nanno M, Shimida S. 164.  et al. 2000. The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell 102:827–37 [Google Scholar]
  165. Zhao J, Li K, Wohlford-Lenane C, Agnihothram SS, Fett C. 165.  et al. 2014. Rapid generation of a mouse model for Middle East respiratory syndrome. PNAS 111:4970–75 [Google Scholar]
  166. Zhou H, Xu M, Huang Q, Gates AT, Zhang XD. 166.  et al. 2008. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 4:495–504 [Google Scholar]
  167. Zust R, Toh YX, Valdes I, Cerny D, Heinrich J. 167.  et al. 2014. Type I interferon signals in macrophages and dendritic cells control dengue virus infection: implications for a new mouse model to test dengue vaccines. J. Virol. 88:7276–85 [Google Scholar]
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