Making Bunyaviruses Talk: Interrogation Tactics to Identify Host Factors Required for Infection
Abstract
:1. Introduction
2. Genetic Approaches to Identify Bunyavirus Host Factors
3. Recent Advances in Genetic Screening Techniques
4. Small Molecule Screening
5. Biochemical Approaches: Viral Proteins as Bait for Host Factors
6. The Next Generation of Biochemical Screening Techniques
7. Diverse Screening Approaches are Highly Complementary
8. Future Perspectives: Expanding Cellular Targets and Bunyavirus Technical Resources
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Cherry, S.; Doukas, T.; Armknecht, S.; Whelan, S.; Wang, H.; Sarnow, P.; Perrimon, N. Genome-wide RNAi screen reveals a specific sensitivity of IRES-containing RNA viruses to host translation inhibition. Genes Dev. 2005, 19, 445–452. [Google Scholar] [CrossRef] [PubMed]
- Cherry, S.; Kunte, A.; Wang, H.; Coyne, C.; Rawson, R.B.; Perrimon, N. COPI activity coupled with fatty acid biosynthesis is required for viral replication. PLoS Pathog. 2006, 2, e120. [Google Scholar] [CrossRef] [PubMed]
- Brass, A.L.; Dykxhoorn, D.M.; Benita, Y.; Yan, N.; Engelman, A.; Xavier, R.J.; Lieberman, J.; Elledge, S.J. Identification of host proteins required for HIV infection through a functional genomic screen. Science 2008, 319, 921–926. [Google Scholar] [CrossRef] [PubMed]
- König, R.; Zhou, Y.; Elleder, D.; Diamond, T.L.; Bonamy, G.M.C.; Irelan, J.T.; Chiang, C.; Tu, B.P.; de Jesus, P.D.; Lilley, C.E.; et al. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 2008, 135, 49–60. [Google Scholar] [CrossRef] [PubMed]
- Zhou, H.; Xu, M.; Huang, Q.; Gates, A.T.; Zhang, X.D.; Castle, J.C.; Stec, E.; Ferrer, M.; Strulovici, B.; Hazuda, D.J.; et al. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 2008, 4, 495–504. [Google Scholar] [CrossRef] [PubMed]
- Brass, A.L.; Huang, I.C.; Benita, Y.; John, S.P.; Krishnan, M.N.; Feeley, E.M.; Ryan, B.J.; Weyer, J.L.; van der Weyden, L.; Fikrig, E.; et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009, 139, 1243–1254. [Google Scholar] [CrossRef] [PubMed]
- Hopkins, K.C.; McLane, L.M.; Maqbool, T.; Panda, D.; Gordesky-Gold, B.; Cherry, S. A genome-wide RNAi screen reveals that mRNA decapping restricts bunyaviral replication by limiting the pools of dcp2-accessible targets for cap-snatching. Genes Dev. 2013, 27, 1511–1525. [Google Scholar] [CrossRef] [PubMed]
- Meier, R.; Franceschini, A.; Horvath, P.; Tetard, M.; Mancini, R.; von Mering, C.; Helenius, A.; Lozach, P.-Y. Genome-wide small interfering RNA screens reveal VAMP3 as a novel host factor required for Uukuniemi virus late penetration. J. Virol. 2014, 88, 8565–8578. [Google Scholar] [CrossRef] [PubMed]
- White, J.; Matlin, K.; Helenius, A. Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses. J. Cell Biol. 1981, 89, 674–679. [Google Scholar] [CrossRef] [PubMed]
- Maeda, T.; Ohnishi, S. Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS Lett. 1980, 122, 283–287. [Google Scholar] [CrossRef]
- Huang, R.T.C.; Rott, R.; Klenk, H.D. Influenza viruses cause hemolysis and fusion of cells. Virology 1981, 110, 243–247. [Google Scholar] [CrossRef]
- Fader, C.M.; Sánchez, D.G.; Mestre, M.B.; Colombo, M.I. TI-VAMP/VAMP7 and VAMP3/cellubrevin: Two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim. Biophys. Acta 2009, 1793, 1901–1916. [Google Scholar] [CrossRef] [PubMed]
- Carette, J.E.; Guimaraes, C.P.; Varadarajan, M.; Park, A.S.; Wuethrich, I.; Godarova, A.; Kotecki, M.; Cochran, B.H.; Spooner, E.; Ploegh, H.L.; et al. Haploid genetic screens in human cells identify host factors used by pathogens. Science 2009, 326, 1231–1235. [Google Scholar] [CrossRef] [PubMed]
- Carette, J.E.; Guimaraes, C.P.; Wuethrich, I.; Blomen, V.A.; Sun, C.; Bell, G.; Yuan, B.; Muellner, M.K.; Nijman, M.; Ploegh, H.L.; et al. Global gene disruption in human cells to assign genes to phenotypes. Nat. Biotechnol. 2011, 29, 542–546. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carette, J.E.; Raaben, M.; Wong, A.C.; Herbert, A.S.; Obernosterer, G.; Mulherkar, N.; Kuehne, A.I.; Kranzusch, P.J.; Griffin, A.M.; Ruthel, G.; et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 2011, 477, 340–343. [Google Scholar] [CrossRef] [PubMed]
- Jae, L.T.; Raaben, M.; Riemersma, M.; van Beusekom, E.; Blomen, V.; Velds, A.; Kerkhoven, R.M.; Carette, J.E.; Topaloglu, H.; Meinecke, P.; et al. Deciphering the glycosylome of dystroglycanopathies using haploid screens for Lassa virus entry. Science 2013, 340, 479–483. [Google Scholar] [CrossRef] [PubMed]
- Jae, L.T.; Raaben, M.; Herbert, A.S.; Kuehne, A.I.; Wirchnianski, A.S.; Soh, T.K.; Stubbs, S.H.; Janssen, H.; Damme, M.; Saftig, P.; et al. Lassa virus entry requires a trigger-induced receptor switch. Science 2014, 344, 1506–1510. [Google Scholar] [CrossRef] [PubMed]
- Petersen, J.; Drake, M.J.; Bruce, E.A.; Riblett, A.M.; Didigu, C.A.; Wilen, C.B.; Malani, N.; Male, F.; Lee, F.-H.; Bushman, F.D.; et al. The major cellular sterol regulatory pathway is required for Andes virus infection. PLoS Pathog. 2014, 10, e1003911. [Google Scholar] [CrossRef] [PubMed]
- Kleinfelter, L.M.; Jangra, R.K.; Jae, L.T.; Herbert, A.S.; Mittler, E.; Stiles, K.M.; Wirchnianski, A.S.; Kielian, M.; Brummelkamp, T.R.; Dye, J.M. Haploid genetic screen reveals a profound and direct dependence on cholesterol for hantavirus membrane fusion. mBio 2015, 6, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Riblett, A.M.; Blomen, V.A.; Jae, L.T.; Altamura, L.A.; Doms, R.W.; Brummelkamp, T.R.; Wojcechowskyj, J.A. A haploid genetic screen identifies heparan sulfate proteoglycans supporting Rift Valley fever virus infection. J. Virol. 2016, 90, 1414–1423. [Google Scholar] [CrossRef] [PubMed]
- Ungar, D.; Oka, T.; Brittle, E.E.; Vasile, E.; Lupashin, V.; Chatterton, J.E.; Heuser, J.E.; Krieger, M.; Waters, M.G. Characterization of a mammalian Golgi-localized protein complex, COG, that is required for normal Golgi morphology and function. J. Cell Biol. 2002, 157, 405–415. [Google Scholar] [CrossRef]
- Kingsley, D.M.; Kozarsky, K.F.; Segal, M.; Krieger, M. Three types of low density lipoprotein receptor-deficient mutant have pleiotropic defects in the synthesis of N-linked, O-linked, and lipid-linked carbohydrate chains. J. Cell Biol. 1986, 102, 1576–1585. [Google Scholar] [CrossRef] [PubMed]
- Blomen, V.A.; Májek, P.; Jae, L.T.; Bigenzahn, J.W.; Nieuwenhuis, J.; Staring, J.; Sacco, R.; van Diemen, F.R.; Olk, N.; Stukalov, A.; et al. Gene essentiality and synthetic lethality in haploid human cells. Science 2015, 350, 1092–1096. [Google Scholar] [CrossRef] [PubMed]
- Yi, M.; Hong, N.; Hong, Y. Generation of medaka fish haploid embryonic stem cells. Science 2009, 326, 430–433. [Google Scholar] [CrossRef] [PubMed]
- Elling, U.; Taubenschmid, J.; Wirnsberger, G.; O’Malley, R.; Demers, S.P.; Vanhaelen, Q.; Shukalyuk, A.I.; Schmauss, G.; Schramek, D.; Schnuetgen, F.; et al. Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Cell Stem Cell 2011, 9, 563–574. [Google Scholar] [CrossRef] [PubMed]
- Leeb, M.; Wutz, A. Derivation of haploid embryonic stem cells from mouse embryos. Nature 2011, 479, 131–134. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.; Liu, Z.; Ma, Y.; Zhong, C.; Yin, Q.; Zhou, C.; Shi, L.; Cai, Y.; Zhao, H.; Wang, H.; et al. Generation of haploid embryonic stem cells from Macaca fascicularis monkey parthenotes. Cell Res. 2013, 23, 1187–1200. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Li, X.; Li, T.; Jiang, M.G.; Wan, H.; Luo, G.Z.; Feng, C.; Cui, X.; Teng, F.; Yuan, Y.; et al. Genetic modification and screening in rat using haploid embryonic stem cells. Cell Stem Cell 2014, 14, 404–414. [Google Scholar] [CrossRef] [PubMed]
- Essletzbichler, P.; Konopka, T.; Santoro, F.; Chen, D.; Gapp, B.V.; Kralovics, R.; Brummelkamp, T.R.; Nijman, S.M.B.; Bürckstümmer, T. Megabase-scale deletion using CRISPR/Cas9 to generate a fully haploid human cell line. Genome Res. 2014, 24, 2059–2065. [Google Scholar] [CrossRef] [PubMed]
- Wright, A.V.; Nunez, J.K.; Doudna, J.A. Biology and applications of CRISPR systems: Harnessing nature’s toolbox for genome engineering. Cell 2016, 164, 29–44. [Google Scholar] [CrossRef] [PubMed]
- 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] [PubMed]
- Sanjana, N.E.; Shalem, O.; Zhang, F. Improved vectors and genome-wide libraries for CRISPR screening. Nat. Methods 2014, 11, 006726. [Google Scholar] [CrossRef] [PubMed]
- Islam, M.K.; Baudin, M.; Eriksson, J.; Öberg, C.; Habjan, M.; Weber, F.; Överby, A.K.; Ahlm, C.; Evander, M. High-throughput screening using a whole-cell virus replication reporter gene assay to identify inhibitory compounds against Rift Valley fever virus infection. J. Biomol. Screen. 2016, 21, 354–362. [Google Scholar] [CrossRef] [PubMed]
- Tan, X.; Hu, L.; Luquette, L.J.; Gao, G.; Liu, Y.; Qu, H.; Xi, R.; Lu, Z.J.; Park, P.J.; Elledge, S.J. Systematic identification of synergistic drug pairs targeting HIV. Nat. Biotechnol. 2012, 30, 1125–1130. [Google Scholar] [CrossRef] [PubMed]
- Léonard, V.H.J.; Kohl, A.; Hart, T.J.; Elliott, R.M. Interaction of Bunyamwera orthobunyavirus NSs protein with Mediator protein MED8: A mechanism for inhibiting the interferon response. J. Virol. 2006, 80, 9667–9675. [Google Scholar] [CrossRef] [PubMed]
- Rönnberg, T.; Jääskeläinen, K.; Blot, G.; Parviainen, V.; Vaheri, A.; Renkonen, R.; Bouloy, M.; Plyusnin, A. Searching for cellular partners of hantaviral nonstructural protein NSs: Y2H screening of mouse cDNA library and analysis of cellular interactome. PLoS ONE 2012, 7. [Google Scholar] [CrossRef] [PubMed]
- Pichlmair, A.; Kandasamy, K.; Alvisi, G.; Mulhern, O.; Sacco, R.; Habjan, M.; Binder, M.; Stefanovic, A.; Eberle, C.-A.; Goncalves, A.; et al. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature 2012, 487, 486–490. [Google Scholar] [CrossRef] [PubMed]
- Kainulainen, M.; Habjan, M.; Hubel, P.; Busch, L.; Lau, S.; Colinge, J.; Superti-Furga, G.; Pichlmair, A.; Weber, F. Virulence factor NSs of Rift Valley fever virus recruits the F-box protein FBXO3 to degrade subunit p62 of general transcription factor TFIIH. J. Virol. 2014, 88, 3464–3473. [Google Scholar] [CrossRef] [PubMed]
- Martell, J.D.; Deerinck, T.J.; Sancak, Y.; Poulos, T.L.; Mootha, V.K.; Sosinsky, G.E.; Ellisman, M.H.; Ting, A.Y. Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat. Biotechnol. 2012, 30, 1143–1148. [Google Scholar] [PubMed]
- Rhee, H.; Zou, P.; Udeshi, N.D.; Martell, J.D.; Mootha, V.K.; Carr, S.A.; Ting, A.Y. Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science 2013, 339, 1328. [Google Scholar] [CrossRef] [PubMed]
- Lam, S.S.; Martell, J.D.; Kamer, K.J.; Deerinck, T.J.; Ellisman, M.H.; Mootha, V.K.; Ting, A.Y. Directed evolution of APEX2 for electron microscopy and proximity labeling. Nat. Methods 2014, 12, 51–54. [Google Scholar] [CrossRef] [PubMed]
- Roux, K.J.; Kim, D.I.; Raida, M.; Burke, B. A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J. Cell Biol. 2012, 196, 801–810. [Google Scholar] [CrossRef] [PubMed]
- Kim, D.I.; KC, B.; Zhu, W.; Motamedchaboki, K.; Doye, V.; Roux, K.J. Probing nuclear pore complex architecture with proximity-dependent biotinylation. Proc. Natl. Acad. Sci. USA 2014, 111, E2453–E2461. [Google Scholar] [CrossRef] [PubMed]
- Elzi, D.J.; Song, M.; Hakala, K.; Weintraub, S.T.; Shiio, Y. Proteomic analysis of the EWS-Fli-1 interactome reveals the role of the lysosome in EWS-Fli-1 turnover. J. Proteome Res. 2014, 13, 3783–3791. [Google Scholar] [CrossRef] [PubMed]
- Mojica, S.A.; Hovis, K.M.; Frieman, M.B.; Tran, B.; Hsia, R.C.; Ravel, J.; Jenkins-Houk, C.; Wilson, K.L.; Bavoil, P.M. SINC, a type III secreted protein of Chlamydia psittaci, targets the inner nuclear membrane of infected cells and uninfected neighbors. Mol. Biol. Cell 2015, 26, 1918–1934. [Google Scholar] [CrossRef] [PubMed]
- Le Sage, V.; Cinti, A.; Valiente-Echeverría, F.; Mouland, A.J. Proteomic analysis of HIV-1 Gag interacting partners using proximity-dependent biotinylation. Virol. J. 2015, 12, 138. [Google Scholar] [CrossRef] [PubMed]
- Kim, D.I.; Jensen, S.C.; Noble, K.A.; Kc, B.; Roux, K.H.; Motamedchaboki, K.; Roux, K.J. An improved smaller biotin ligase for BioID proximity labeling. Mol. Biol. Cell 2016, 27, 1188–1196. [Google Scholar] [CrossRef] [PubMed]
- Bushman, F.D.; Malani, N.; Fernandes, J.; D’Orso, I.; Cagney, G.; Diamond, T.L.; Zhou, H.; Hazuda, D.J.; Espeseth, A.S.; Konig, R.; et al. Host cell factors in HIV replication: Meta-analysis of genome-wide studies. PLoS Pathog. 2009, 5, e1000437. [Google Scholar] [CrossRef] [PubMed]
- Tai, A.W.; Benita, Y.; Peng, L.F.; Kim, S.; Sakamoto, N.; Xavier, R.J.; Chung, R.T. A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host Microbe 2009, 5, 298–307. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Brass, A.L.; Ng, A.; Hu, Z.; Xavier, R.J.; Liang, T.J.; Elledge, S.J. A genome-wide genetic screen for host factors required for hepatitis C virus propagation. Proc. Natl. Acad. Sci. USA 2009, 106, 16410–16415. [Google Scholar] [CrossRef] [PubMed]
- Rose, P.P.; Hanna, S.L.; Spiridigliozzi, A.; Wannissorn, N.; Beiting, D.P.; Ross, S.R.; Hardy, R.W.; Bambina, S.A.; Heise, M.T.; Cherry, S. Natural resistance-associated macrophage protein is a cellular receptor for Sindbis virus in both insect and mammalian hosts. Cell Host Microbe 2011, 10, 97–104. [Google Scholar] [CrossRef] [PubMed]
- Panda, D.; Rose, P.P.; Hanna, S.L.; Gold, B.; Hopkins, K.C.; Lyde, R.B.; Marks, M.S.; Cherry, S. Genome-wide RNAi screen identifies SEC61A and VCP as conserved regulators of Sindbis virus entry. Cell Rep. 2013, 5, 1737–1748. [Google Scholar] [PubMed]
- Ooi, Y.S.; Stiles, K.M.; Liu, C.Y.; Taylor, G.M.; Kielian, M. Genome-wide RNAi screen identifies novel host proteins required for alphavirus entry. PLoS Pathog. 2013, 9, e1003835. [Google Scholar] [CrossRef] [PubMed]
- Franceschini, A.; Meier, R.; Casanova, A.; Kreibich, S.; Daga, N.; Andritschke, D.; Dilling, S.; Rämö, P.; Emmenlauer, M.; Kaufmann, A.; et al. Specific inhibition of diverse pathogens in human cells by synthetic microRNA-like oligonucleotides inferred from RNAi screens. Proc. Natl. Acad. Sci. USA 2014, 111, 4548–4553. [Google Scholar] [CrossRef] [PubMed]
- Zhu, J.; Davoli, T.; Perriera, J.M.; Chin, C.R.; Gaiha, G.D.; John, S.P.; Sigiollot, F.D.; Gao, G.; Xu, Q.; Qu, H.; et al. Comprehensive identification of host modulators of HIV-1 replication using multiple orthologous RNAi reagents. Cell Rep. 2014, 9, 752–766. [Google Scholar] [CrossRef] [PubMed]
- Mohr, S.E.; Smith, J.A.; Shamu, C.E.; Neumüller, R.A.; Perrimon, N. RNAi screening comes of age: Improved techniques and complementary approaches. Nat. Rev. Mol. Cell Biol. 2014, 15, 591–600. [Google Scholar] [CrossRef] [PubMed]
- Baggen, J.; Jan, H.; Staring, J.; Jae, L.T.; Liu, Y.; Guo, H.; Slager, J.J.; de Bruin, J.W.; van Vliet, A.L.W.; Blomen, V.A.; et al. Enterovirus D68 receptor requirements unveiled by haploid genetics. Proc. Natl. Acad. Sci. USA 2015, 113, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Pillay, S.; Meyer, N.L.; Puschnik, A.S.; Davulcu, O.; Diep, J.; Ishikawa, Y.; Jae, L.T.; Wosen, J.E.; Nagamine, C.M.; Chapman, M.S.; et al. An essential receptor for adeno-associated virus infection. Nature 2016, 530, 108–112. [Google Scholar] [CrossRef] [PubMed]
- Schorch, B.; Song, S.; van Diemen, F.R.; Bock, H.H.; May, P.; Herz, J.; Brummelkamp, T.R.; Papatheodorou, P.; Aktories, K. LRP1 is a receptor for Clostridium perfringens TpeL toxin indicating a two-receptor model of clostridial glycosylating toxins. Proc. Natl. Acad. Sci. USA 2014, 111, 6431–6436. [Google Scholar] [CrossRef] [PubMed]
- Tafesse, F.G.; Guimaraes, C.P.; Maruyama, T.; Carette, J.E.; Lory, S.; Brummelkamp, T.R.; Ploegh, H.L. GPR107, a G-protein-coupled receptor essential for intoxication by Pseudomonas aeruginosa exotoxin A, localizes to the Golgi and is cleaved by furin. J. Biol. Chem. 2014, 289, 24005–24018. [Google Scholar] [CrossRef] [PubMed]
- Popov, L.M.; Marceau, C.D.; Starkl, P.M.; Lumb, J.H.; Shah, J.; Guerrera, D.; Cooper, R.L.; Merakou, C.; Bouley, D.M.; Meng, W.; et al. The adherens junctions control susceptibility to Staphylococcus aureus α-toxin. Proc. Natl. Acad. Sci. USA 2015, 112, 201510265. [Google Scholar] [CrossRef] [PubMed]
- Munger, J.; Bajad, S.U.; Coller, H.A.; Shenk, T.; Rabinowitz, J.D. Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathog. 2006, 2, 1165–1175. [Google Scholar] [CrossRef] [PubMed]
- Munger, J.; Bennett, B.D.; Parikh, A.; Feng, X.-J.; McArdle, J.; Rabitz, H.A.; Shenk, T.; Rabinowitz, J.D. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 2008, 26, 1179–1186. [Google Scholar] [CrossRef] [PubMed]
- Vastag, L.; Koyuncu, E.; Grady, S.L.; Shenk, T.E.; Rabinowitz, J.D. Divergent effects of human cytomegalovirus and herpes simplex virus-1 on cellular metabolism. PLoS Pathog. 2011, 7. [Google Scholar] [CrossRef] [PubMed]
- Morita, M.; Kuba, K.; Ichikawa, A.; Nakayama, M.; Katahira, J.; Iwamoto, R.; Watanebe, T.; Sakabe, S.; Daidoji, T.; Nakamura, S.; et al. The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza. Cell 2013, 153, 112–125. [Google Scholar] [CrossRef] [PubMed]
- SenGupta, D.J.; Zhang, B.; Kraemer, B.; Pochart, P.; Fields, S.; Wickens, M. A three-hybrid system to detect RNA-protein interactions in vivo. Proc. Natl. Acad. Sci. USA 1996, 93, 8496–8501. [Google Scholar] [CrossRef] [PubMed]
- Wood, J.; Frederickson, R.M.; Fields, S.; Patel, A.H. Hepatitis C virus 3’X region interacts with human ribosomal proteins. J. Virol. 2001, 75, 1348–1358. [Google Scholar] [CrossRef] [PubMed]
- Castello, A.; Fischer, B.; Eichelbaum, K.; Horos, R.; Beckmann, B.M.; Strein, C.; Davey, N.E.; Humphreys, D.T.; Preiss, T.; Steinmetz, L.M.; et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 2012, 149, 1393–1406. [Google Scholar] [CrossRef] [PubMed]
- Shi, X.; van Mierlo, J.T.; French, A.; Elliott, R.M. Visualizing the replication cycle of Bunyamwera orthobunyavirus expressing fluorescent protein-tagged Gc glycoprotein. J. Virol. 2010, 84, 8460–8469. [Google Scholar] [CrossRef] [PubMed]
- Shi, X.; Elliott, R.M. Generation and analysis of recombinant Bunyamwera orthobunyaviruses expressing V5 epitope-tagged L proteins. J. Gen. Virol. 2009, 90, 297–306. [Google Scholar] [CrossRef] [PubMed]
- Elliott, R.M.; Blakqori, G.; van Knippenberg, I.C.; Koudriakova, E.; Li, P.; McLees, A.; Shi, X.; Szemiel, A.M. Establishment of a reverse genetics system for Schmallenberg virus, a newly emerged orthobunyavirus in Europe. J. Gen. Virol. 2013, 94, 851–859. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Wu, S.; Song, S.; Lv, J.; Feng, C.; Lin, X. Preparation and characterization of a stable BHK-21 cell line constitutively expressing the Schmallenberg virus nucleocapsid protein. Mol. Cell. Probes 2015, 29, 244–253. [Google Scholar] [CrossRef] [PubMed]
- Acrani, G.O.; Tilston-Lunel, N.L.; Spiegel, M.; Weidmann, M.; Dilcher, M.; da Silva, D.E.A.; Nunes, M.R.T.; Elliott, R.M. Establishment of a minigenome system for oropouche virus reveals the S genome segment to be significantly longer than reported previously. J. Gen. Virol. 2015, 96, 513–523. [Google Scholar] [CrossRef] [PubMed]
- Takenaka-Uema, A.; Sugiura, K.; Bangphoomi, N.; Shioda, C.; Uchida, K.; Kato, K.; Haga, T.; Murakami, S.; Akashi, H.; Horimoto, T. Development of an improved reverse genetics system for Akabane bunyavirus. J. Virol. Methods 2016, 232, 16–20. [Google Scholar] [CrossRef] [PubMed]
- Ikegami, T.; Won, S.; Peters, C.J.; Makino, S. Rescue of infectious Rift Valley fever virus entirely from cDNA, analysis of virus lacking the NSs gene, and expression of a foreign gene. J. Virol. 2006, 80, 2933–2940. [Google Scholar] [CrossRef] [PubMed]
- Kortekaas, J.; Oreshkova, N.; Cobos-Jimenez, V.; Vloet, R.P.M.; Potgieter, C.A.; Moormann, R.J.M. Creation of a nonspreading Rift Valley fever virus. J. Virol. 2011, 85, 12622–12630. [Google Scholar] [CrossRef] [PubMed]
- Ray, N.; Whidby, J.; Stewart, S.; Hooper, J.W.; Bertolotti-Ciarlet, A. study of Andes virus entry and neutralization using a pseudovirion system. J. Virol. Methods 2010, 163, 416–423. [Google Scholar] [CrossRef] [PubMed]
- Higa, M.M.; Petersen, J.; Hooper, J.; Doms, R.W. Efficient production of Hantaan and Puumala pseudovirions for viral tropism and neutralization studies. Virology 2012, 423, 134–142. [Google Scholar] [CrossRef] [PubMed]
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Riblett, A.M.; Doms, R.W. Making Bunyaviruses Talk: Interrogation Tactics to Identify Host Factors Required for Infection. Viruses 2016, 8, 130. https://doi.org/10.3390/v8050130
Riblett AM, Doms RW. Making Bunyaviruses Talk: Interrogation Tactics to Identify Host Factors Required for Infection. Viruses. 2016; 8(5):130. https://doi.org/10.3390/v8050130
Chicago/Turabian StyleRiblett, Amber M., and Robert W. Doms. 2016. "Making Bunyaviruses Talk: Interrogation Tactics to Identify Host Factors Required for Infection" Viruses 8, no. 5: 130. https://doi.org/10.3390/v8050130