Uncovering the global host cell requirements for influenza virus replication via RNAi screening

Microbes and Infection

Volumn 13, Issue 5, 2011, Pages 516-525

  Stertz, Silke ^a   Shaw, Megan L ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Influenza virus; RNA interference; Virus host interactions

Indexed keywords

SMALL INTERFERING RNA; VIRUS RNA;

ANIMAL CELL; DROSOPHILA; GENETIC TRANSCRIPTION; GENOME; HOST CELL; HUMAN; HUMAN CELL; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SHORT SURVEY; VIRUS CELL INTERACTION; VIRUS REPLICATION;

ANIMALS; CELL LINE; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; ORTHOMYXOVIRIDAE; PROTEINS; RNA INTERFERENCE; VIRAL PROTEINS; VIRUS REPLICATION;

ORTHOMYXOVIRIDAE;

EID: 79953288103     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2011.01.012     Document Type: Short Survey

References (65)

1. Palese P., Shaw M.L. Orthomyxoviridae: the viruses and their replication. Fields Virology 2007, 1647-1689. Lippincott Williams & Wilkins, Philadelphia. fifth ed. D.M. Knipe, P.M. Howley (Eds.).
2. De Clercq E. Antiviral agents active against influenza A viruses. Nat. Rev. Drug Discov. 2006, 5:1015-1025.
3. König R., Stertz S., Zhou Y., Inoue A., Hoffmann H.H., Bhattacharyya S., Alamares J.G., Tscherne D.M., Ortigoza M.B., Liang Y., Gao Q., Andrews S.E., Bandyopadhyay S., De Jesus P., Tu B.P., Pache L., Shih C., Orth A., Bonamy G., Miraglia L., Ideker T., Garcia-Sastre A., Young J.A., Palese P., Shaw M.L., Chanda S.K. Human host factors required for influenza virus replication. Nature 2010, 463:813-817.
4. Karlas A., Machuy N., Shin Y., Pleissner K.P., Artarini A., Heuer D., Becker D., Khalil H., Ogilvie L.A., Hess S., Maurer A.P., Muller E., Wolff T., Rudel T., Meyer T.F. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 2010, 463:818-822.
5. 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., Adams D.J., Xavier R.J., Farzan M., Elledge S.J. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009, 139:1243-1254.
6. Shapira S.D., Gat-Viks I., Shum B.O., Dricot A., de Grace M.M., Wu L., Gupta P.B., Hao T., Silver S.J., Root D.E., Hill D.E., Regev A., Hacohen N. A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 2009, 139:1255-1267.
7. Hao L., Sakurai A., Watanabe T., Sorensen E., Nidom C.A., Newton M.A., Ahlquist P., Kawaoka Y. Drosophila RNAi screen identifies host genes important for influenza virus replication. Nature 2008, 454:890-893.
8. O'Neill R.E., Palese P. NPI-1, the human homolog of SRP-1, interacts with influenza virus nucleoprotein. Virology 1995, 206:116-125.
9. Nemeroff M.E., Barabino S.M., Li Y., Keller W., Krug R.M. Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3'end formation of cellular pre-mRNAs. Mol. Cell 1998, 1:991-1000.
10. Mayer D., Molawi K., Martinez-Sobrido L., Ghanem A., Thomas S., Baginsky S., Grossmann J., Garcia-Sastre A., Schwemmle M. Identification of cellular interaction partners of the influenza virus ribonucleoprotein complex and polymerase complex using proteomic-based approaches. J. Proteome Res. 2007, 6:672-682.
11. Jorba N., Juarez S., Torreira E., Gastaminza P., Zamarreno N., Albar J.P., Ortin J. Analysis of the interaction of influenza virus polymerase complex with human cell factors. Proteomics 2008, 8:2077-2088.
12. Deng T., Engelhardt O.G., Thomas B., Akoulitchev A.V., Brownlee G.G., Fodor E. Role of ran binding protein 5 in nuclear import and assembly of the influenza virus RNA polymerase complex. J. Virol. 2006, 80:11911-11919.
13. Momose F., Naito T., Yano K., Sugimoto S., Morikawa Y., Nagata K. Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J. Biol. Chem. 2002, 277:45306-45314.
14. Naito T., Momose F., Kawaguchi A., Nagata K. Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J. Virol. 2007, 81:1339-1349.
15. Chase G., Deng T., Fodor E., Leung B.W., Mayer D., Schwemmle M., Brownlee G. Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 2008, 377:431-439.
16. Hutchinson E.C., von Kirchbach J.C., Gog J.R., Digard P. Genome packaging in influenza A virus. J. Gen. Virol. 2010, 91:313-328.
17. Fodor E., Devenish L., Engelhardt O.G., Palese P., Brownlee G.G., Garcia-Sastre A. Rescue of influenza A virus from recombinant DNA. J. Virol. 1999, 73:9679-9682.
18. Neumann G., Watanabe T., Ito H., Watanabe S., Goto H., Gao P., Hughes M., Perez D.R., Donis R., Hoffmann E., Hobom G., Kawaoka Y. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:9345-9350.
19. Rameix-Welti M.A., Tomoiu A., Dos Santos Afonso E., van der Werf S., Naffakh N. Avian Influenza A virus polymerase association with nucleoprotein, but not polymerase assembly, is impaired in human cells during the course of infection. J. Virol. 2009, 83:1320-1331.
20. Manicassamy B., Manicassamy S., Belicha-Villanueva A., Pisanelli G., Pulendran B., Garcia-Sastre A. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11531-11536.
21. Shaw M.L., Stone K.L., Colangelo C.M., Gulcicek E.E., Palese P. Cellular proteins in influenza virus particles. PLoS Pathog. 2008, 4:e1000085.
22. Geiss G.K., An M.C., Bumgarner R.E., Hammersmark E., Cunningham D., Katze M.G. Global impact of influenza virus on cellular pathways is mediated by both replication-dependent and -independent events. J. Virol. 2001, 75:4321-4331.
23. Kash J.C., Tumpey T.M., Proll S.C., Carter V., Perwitasari O., Thomas M.J., Basler C.F., Palese P., Taubenberger J.K., Garcia-Sastre A., Swayne D.E., Katze M.G. Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 2006, 443:578-581.
24. Zhang H., Su Y.A., Hu P., Yang J., Zheng B., Wu P., Peng J., Tang Y., Zhang L. Signature patterns revealed by microarray analyses of mice infected with influenza virus A and Streptococcus pneumoniae. Microbes Infect. 2006, 8:2172-2185.
25. Fornek J.L., Gillim-Ross L., Santos C., Carter V., Ward J.M., Cheng L.I., Proll S., Katze M.G., Subbarao K. A single-amino-acid substitution in a polymerase protein of an H5N1 influenza virus is associated with systemic infection and impaired T-cell activation in mice. J. Virol. 2009, 83:11102-11115.
26. Rowe T., Leon A.J., Crevar C.J., Carter D.M., Xu L., Ran L., Fang Y., Cameron C.M., Cameron M.J., Banner D., Ng D.C., Ran R., Weirback H.K., Wiley C.A., Kelvin D.J., Ross T.M. Modeling host responses in ferrets during A/California/07/2009 influenza infection. Virology 2010, 401:257-265.
27. Cameron C.M., Cameron M.J., Bermejo-Martin J.F., Ran L., Xu L., Turner P.V., Ran R., Danesh A., Fang Y., Chan P.K., Mytle N., Sullivan T.J., Collins T.L., Johnson M.G., Medina J.C., Rowe T., Kelvin D.J. Gene expression analysis of host innate immune responses during Lethal H5N1 infection in ferrets. J. Virol. 2008, 82:11308-11317.
28. Reemers S.S., van Leenen D., Koerkamp M.J., van Haarlem D., van de Haar P., van Eden W., Vervelde L. Early host responses to avian influenza A virus are prolonged and enhanced at transcriptional level depending on maturation of the immune system. Mol. Immunol. 2010, 47:1675-1685.
29. Baskin C.R., Garcia-Sastre A., Tumpey T.M., Bielefeldt-Ohmann H., Carter V.S., Nistal-Villan E., Katze M.G. Integration of clinical data, pathology, and cDNA microarrays in influenza virus-infected pigtailed macaques (Macaca nemestrina). J. Virol. 2004, 78:10420-10432.
30. Cilloniz C., Shinya K., Peng X., Korth M.J., Proll S.C., Aicher L.D., Carter V.S., Chang J.H., Kobasa D., Feldmann F., Strong J.E., Feldmann H., Kawaoka Y., Katze M.G. Lethal influenza virus infection in macaques is associated with early dysregulation of inflammatory related genes. PLoS Pathog. 2009, 5:e1000604.
31. Baskin C.R., Bielefeldt-Ohmann H., Tumpey T.M., Sabourin P.J., Long J.P., Garcia-Sastre A., Tolnay A.E., Albrecht R., Pyles J.A., Olson P.H., Aicher L.D., Rosenzweig E.R., Murali-Krishna K., Clark E.A., Kotur M.S., Fornek J.L., Proll S., Palermo R.E., Sabourin C.L., Katze M.G. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3455-3460.
32. Kash J.C., Basler C.F., Garcia-Sastre A., Carter V., Billharz R., Swayne D.E., Przygodzki R.M., Taubenberger J.K., Katze M.G., Tumpey T.M. Global host immune response: pathogenesis and transcriptional profiling of type A influenza viruses expressing the hemagglutinin and neuraminidase genes from the 1918 pandemic virus. J. Virol. 2004, 78:9499-9511.
33. Geiss G.K., Salvatore M., Tumpey T.M., Carter V.S., Wang X., Basler C.F., Taubenberger J.K., Bumgarner R.E., Palese P., Katze M.G., Garcia-Sastre A. Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:10736-10741.
34. Ehrhardt C., Marjuki H., Wolff T., Nurnberg B., Planz O., Pleschka S., Ludwig S. Bivalent role of the phosphatidylinositol-3-kinase (PI3K) during influenza virus infection and host cell defence. Cell. Microbiol. 2006, 8:1336-1348.
35. Pleschka S., Wolff T., Ehrhardt C., Hobom G., Planz O., Rapp U.R., Ludwig S. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signaling cascade. Nat. Cell Biol. 2001, 3:301-305.
36. Sieczkarski S.B., Brown H.A., Whittaker G.R. Role of protein kinase C betaII in influenza virus entry via late endosomes. J. Virol. 2003, 77:460-469.
37. Naito T., Kiyasu Y., Sugiyama K., Kimura A., Nakano R., Matsukage A., Nagata K. An influenza virus replicon system in yeast identified Tat-SF1 as a stimulatory host factor for viral RNA synthesis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:18235-18240.
38. Sui B., Bamba D., Weng K., Ung H., Chang S., Van Dyke J., Goldblatt M., Duan R., Kinch M.S., Li W.B. The use of random homozygous gene perturbation to identify novel host-oriented targets for influenza. Virology 2009, 387:473-481.
39. Bullock A.N., Das S., Debreczeni J.E., Rellos P., Fedorov O., Niesen F.H., Guo K., Papagrigoriou E., Amos A.L., Cho S., Turk B.E., Ghosh G., Knapp S. Kinase domain insertions define distinct roles of CLK kinases in SR protein phosphorylation. Structure 2009, 17:352-362.
40. Hagiwara M. Alternative splicing: a new drug target of the post-genome era. Biochim. Biophys. Acta 2005, 1754:324-331.
41. 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.
42. König R., Zhou Y., Elleder D., Diamond T.L., Bonamy G.M., Irelan J.T., Chiang C.Y., Tu B.P., De Jesus P.D., Lilley C.E., Seidel S., Opaluch A.M., Caldwell J.S., Weitzman M.D., Kuhen K.L., Bandyopadhyay S., Ideker T., Orth A.P., Miraglia L.J., Bushman F.D., Young J.A., Chanda S.K. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 2008, 135:49-60.
43. Zhou H., Xu M., Huang Q., Gates A.T., Zhang X.D., Castle J.C., Stec E., Ferrer M., Strulovici B., Hazuda D.J., Espeseth A.S. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 2008, 4:495-504.
44. Bushman F.D., Malani N., Fernandes J., D'Orso I., Cagney G., Diamond T.L., Zhou H., Hazuda D.J., Espeseth A.S., König R., Bandyopadhyay S., Ideker T., Goff S.P., Krogan N.J., Frankel A.D., Young J.A., Chanda S.K. Host cell factors in HIV replication: meta-analysis of genome-wide studies. PLoS Pathog. 2009, 5:e1000437.
45. Guinea R., Carrasco L. Concanamycin A blocks influenza virus entry into cells under acidic conditions. FEBS Lett. 1994, 349:327-330.
46. Guinea R., Carrasco L. Requirement for vacuolar proton-ATPase activity during entry of influenza virus into cells. J. Virol. 1995, 69:2306-2312.
47. Beck R., Rawet M., Wieland F.T., Cassel D. The COPI system: molecular mechanisms and function. FEBS Lett. 2009, 583:2701-2709.
48. Aniento F., Gu F., Parton R.G., Gruenberg J. An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 1996, 133:29-41.
49. Whitney J.A., Gomez M., Sheff D., Kreis T.E., Mellman I. Cytoplasmic coat proteins involved in endosome function. Cell 1995, 83:703-713.
50. Reed R., Cheng H. TREX, SR proteins and export of mRNA. Curr. Opin. Cell. Biol. 2005, 17:269-273.
51. Read E.K., Digard P. Individual influenza A virus mRNAs show differential dependence on cellular NXF1/TAP for their nuclear export. J. Gen. Virol. 2010, 91:1290-1301.
52. Satterly N., Tsai P.L., van Deursen J., Nussenzveig D.R., Wang Y., Faria P.A., Levay A., Levy D.E., Fontoura B.M. Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1853-1858.
53. Wang P., Palese P., O'Neill R.E. The NPI-1/NPI-3 (karyopherin alpha) binding site on the influenza a virus nucleoprotein NP is a nonconventional nuclear localization signal. J. Virol. 1997, 71:1850-1856.
54. Gabriel G., Herwig A., Klenk H.D. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog. 2008, 4:e11.
55. Tarendeau F., Boudet J., Guilligay D., Mas P.J., Bougault C.M., Boulo S., Baudin F., Ruigrok R.W., Daigle N., Ellenberg J., Cusack S., Simorre J.P., Hart D.J. Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat. Struct. Mol. Biol. 2007, 14:229-233.
56. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., Lempicki R.A. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 2003, 4:P3.
57. Hoffmann H.H., Palese P., Shaw M.L. Modulation of influenza virus replication by alteration of sodium ion transport and protein kinase C activity. Antivir. Res. 2008, 80:124-134.
58. Arora D.J., Gasse N. Influenza virus hemagglutinin stimulates the protein kinase C activity of human polymorphonuclear leucocytes. Arch. Virol. 1998, 143:2029-2037.
59. Mehle A., Doudna J.A. A host of factors regulating influenza virus replication. Viruses 2010, 566-573.
60. Min J.Y., Subbarao K. Cellular targets for influenza drugs. Nat. Biotechnol. 2010, 28:239-240.
61. Watanabe T., Watanabe S., Kawaoka Y. Cellular networks involved in the influenza virus life-cycle. Cell Host Microbe 2010, 7:427-439.
62. Krishnan M.N., Ng A., Sukumaran B., Gilfoy F.D., Uchil P.D., Sultana H., Brass A.L., Adametz R., Tsui M., Qian F., Montgomery R.R., Lev S., Mason P.W., Koski R.A., Elledge S.J., Xavier R.J., Agaisse H., Fikrig E. RNA interference screen for human genes associated with west Nile virus infection. Nature 2008, 455:242-245.
63. Sessions O.M., Barrows N.J., Souza-Neto J.A., Robinson T.J., Hershey C.L., Rodgers M.A., Ramirez J.L., Dimopoulos G., Yang P.L., Pearson J.L., Garcia-Blanco M.A. Discovery of insect and human dengue virus host factors. Nature 2009, 458:1047-1050.
64. 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. U.S.A. 2009, 106:16410-16415.
65. Tai A.W., Benita Y., Peng L.F., Kim S.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.