Translational regulation of viral secretory proteins by the 5' coding regions and a viral RNA-binding protein

Journal of Cell Biology

Volumn 216, Issue 8, 2017, Pages 2283-2293

  Nordholm, Johan ^a   Petitou, Jeanne ^a   Östbye, Henrik ^a   da Silva, Diogo V ^a   Dou, Dan ^a   Wang, Hao ^a   Daniels, Robert ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; GLYCOPROTEIN HA; GLYCOPROTEIN NA; MESSENGER RNA; NONSTRUCTURAL PROTEIN 1; RNA BINDING PROTEIN; SECRETORY PROTEIN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS RNA; 3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; H1N1 VIRUS HEMAGGLUTININ; INFLUENZA VIRUS HEMAGGLUTININ; INS1 PROTEIN, INFLUENZA VIRUS; NA PROTEIN, INFLUENZA A VIRUS; PROTEIN BINDING; SIALIDASE; SIGNAL RECOGNITION PARTICLE; VIRAL PROTEIN;

5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE CONTROL; GENE SEQUENCE; GENE TARGETING; GENETIC CODE; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA SEQUENCE; 3' UNTRANSLATED REGION; A-549 CELL LINE; ANIMAL; BINDING SITE; BIOSYNTHESIS; CHLOROCEBUS AETHIOPS; CV-1 CELL LINE; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HUMAN; INFLUENZA A VIRUS (H1N1); METABOLISM; PROTEIN DOMAIN; PROTEIN SYNTHESIS; VERO CELL LINE;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; A549 CELLS; ANIMALS; BINDING SITES; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOPLASMIC RETICULUM; HEK293 CELLS; HELA CELLS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; NEURAMINIDASE; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN DOMAINS; RNA, MESSENGER; RNA, VIRAL; SIGNAL RECOGNITION PARTICLE; TRANSFECTION; VERO CELLS; VIRAL NONSTRUCTURAL PROTEINS; VIRAL PROTEINS;

EID: 85027281678     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201702102     Document Type: Article

References (51)

1. Aragón, T., S. de la Luna, I. Novoa, L. Carrasco, J. Ortín, and A. Nieto. 2000. Eukaryotic translation initiation factor 4GI is a cellular target for NS1 protein, a translational activator of influenza virus. Mol. Cell. Biol. 20:6259-6268. http ://dx.doi.org/10.1128/MCB.20.17.6259-6268.2000
2. Barreau, C., L. Paillard, and H.B. Osborne. 2005. AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33:7138-7150. http ://dx.doi.org/10.1093/nar/gki1012
3. Bendtsen, J.D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795. http ://dx.doi.org/10.1016/j.jmb.2004.05.028
4. Blobel, G., and B. Dobberstein. 1975. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol. 67:835-851. http ://dx.doi.org/10.1083/jcb.67.3.835
5. Bos, T.J., A.R. Davis, and D.P. Nayak. 1984. NH2-terminal hydrophobic region of influenza virus neuraminidase provides the signal function in translocation. Proc. Natl. Acad. Sci. USA. 81:2327-2331. http ://dx.doi.org/10.1073/pnas.81.8.2327
6. Carmody, S.R., and S.R. Wente. 2009. mRNA nuclear export at a glance. J. Cell Sci. 122:1933-1937. http ://dx.doi.org/10.1242/jcs.041236
7. Chlanda, P., O. Schraidt, S. Kummer, J. Riches, H. Oberwinkler, S. Prinz, H.G. Kräusslich, and J.A. Briggs. 2015. Structural analysis of the roles of influenza A virus membrane-associated proteins in assembly and morphology. J. Virol. 89:8957-8966. http ://dx.doi.org/10.1128/JVI.00592-15
8. Daniels, R., B. Kurowski, A.E. Johnson, and D.N. Hebert. 2003. N-linked glycans direct the cotranslational folding pathway of Influenza hemagglutinin. Mol. Cell. 11:79-90. http ://dx.doi.org/10.1016/S1097-2765(02)00821-3
9. Daniels, R., P. Mellroth, A. Bernsel, F. Neiers, S. Normark, G. von Heijne, and B. Henriques-Normark. 2010. Disulfide bond formation and cysteine exclusion in gram-positive bacteria. J. Biol. Chem. 285:3300-3309. http ://dx.doi.org/10.1074/jbc.M109.081398
10. da Silva, D.V., J. Nordholm, U. Madjo, A. Pfeiffer, and R. Daniels. 2013. Assembly of subtype 1 influenza neuraminidase is driven by both the transmembrane and head domains. J. Biol. Chem. 288:644-653. http ://dx.doi.org/10.1074/jbc.M112.424150
11. de la Luna, S., P. Fortes, A. Beloso, and J. Ortín. 1995. Influenza virus NS1 protein enhances the rate of translation initiation of viral mRNAs. J. Virol. 69:2427-2433
12. Dou, D., D.V. da Silva, J. Nordholm, H. Wang, and R. Daniels. 2014. Type II transmembrane domain hydrophobicity dictates the cotranslational dependence for inversion. Mol. Biol. Cell. 25:3363-3374. http ://dx.doi.org/10.1091/mbc.E14-04-0874
13. Enami, K., T.A. Sato, S. Nakada, and M. Enami. 1994. Influenza virus NS1 protein stimulates translation of the M1 protein. J. Virol. 68:1432-1437
14. Francis, E., R. Daniels, and D.N. Hebert. 2002. Analysis of protein folding and oxidation in the endoplasmic reticulum. Curr. Protoc. Cell Biol. 15:16. http ://dx.doi.org/10.1002/047114303.cb1506s14
15. Gerstberger, S., M. Hafner, and T. Tuschl. 2014. A census of human RNAbinding proteins. Nat. Rev. Genet. 15:829-845. http ://dx.doi.org/10.1038/nrg3813
16. Gilmore, R., P. Walter, and G. Blobel. 1982. Protein translocation across the endoplasmic reticulum. II. Isolation and characterization of the signal recognition particle receptor. J. Cell Biol. 95:470-477. http ://dx.doi.org/10.1083/jcb.95.2.470
17. Greenspan, D., P. Palese, and M. Krystal. 1988. Two nuclear location signals in the influenza virus NS1 nonstructural protein. J. Virol. 62:3020-3026
18. Hale, B.G., R.E. Randall, J. Ortín, and D. Jackson. 2008. The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol. 89:2359-2376. http ://dx.doi.org/10.1099/vir.0.2008/004606-0
19. Heaton, N.S., N. Moshkina, R. Fenouil, T.J. Gardner, S. Aguirre, P.S. Shah, N. Zhao, L. Manganaro, J.F. Hultquist, J. Noel, et al. 2016. Targeting viral proteostasis limits influenza virus, HIV, and dengue virus infection. Immunity. 44:46-58. (published erratum appears in Immunity. 44:438) http ://dx.doi.org/10.1016/j.immuni.2015.12.017
20. Helder, S., A.J. Blythe, C.S. Bond, and J.P. Mackay. 2016. Determinants of affinity and specificity in RNA-binding proteins. Curr. Opin. Struct. Biol. 38:83-91. http ://dx.doi.org/10.1016/j.sbi.2016.05.005
21. Hessa, T., N.M. Meindl-Beinker, A. Bernsel, H. Kim, Y. Sato, M. Lerch-Bader, I. Nilsson, S.H. White, and G. von Heijne. 2007. Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature. 450:1026-1030. http ://dx.doi.org/10.1038/nature06387
22. Hoffmann, E., G. Neumann, Y. Kawaoka, G. Hobom, and R.G. Webster. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. USA. 97:6108-6113. http ://dx.doi.org/10.1073/pnas.100133697
23. Hull, J.D., R. Gilmore, and R.A. Lamb. 1988. Integration of a small integral membrane protein, M2, of influenza virus into the endoplasmic reticulum: analysis of the internal signal-anchor domain of a protein with an ectoplasmic NH2 terminus. J. Cell Biol. 106:1489-1498. http ://dx.doi.org/10.1083/jcb.106.5.1489
24. Jackson, R.J., C.U. Hellen, and T.V. Pestova. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11:113-127. http ://dx.doi.org/10.1038/nrm2838
25. Kang, S.W., N.S. Rane, S.J. Kim, J.L. Garrison, J. Taunton, and R.S. Hegde. 2006. Substrate-specific translocational attenuation during ER stress defines a pre-emptive quality control pathway. Cell. 127:999-1013. http ://dx.doi.org/10.1016/j.cell.2006.10.032
26. Karamyshev, A.L., A.E. Patrick, Z.N. Karamysheva, D.S. Griesemer, H. Hudson, S. Tjon-Kon-Sang, I. Nilsson, H. Otto, Q. Liu, S. Rospert, et al. 2014. Inefficient SRP interaction with a nascent chain triggers a mRNA quality control pathway. Cell. 156:146-157. http ://dx.doi.org/10.1016/j.cell.2013.12.017
27. Kawakami, E., T. Watanabe, K. Fujii, H. Goto, S. Watanabe, T. Noda, and Y. Kawaoka. 2011. Strand-specific real-time RT-PCR for distinguishing influenza vRNA, cRNA, and mRNA. J. Virol. Methods. 173:1-6. http ://dx.doi.org/10.1016/j.jviromet.2010.12.014
28. Kertesz, M., Y. Wan, E. Mazor, J.L. Rinn, R.C. Nutter, H.Y. Chang, and E. Segal. 2010. Genome-wide measurement of RNA secondary structure in yeast. Nature. 467:103-107. http ://dx.doi.org/10.1038/nature09322
29. Kurzchalia, T.V., M. Wiedmann, A.S. Girshovich, E.S. Bochkareva, H. Bielka, and T.A. Rapoport. 1986. The signal sequence of nascent preprolactin interacts with the 54K polypeptide of the signal recognition particle. Nature. 320:634-636. http ://dx.doi.org/10.1038/320634a0
30. Lamb, R.A., and P.W. Choppin. 1976. Synthesis of influenza virus proteins in infected cells: Translation of viral polypeptides, including three P polypeptides, from RNA produced by primary transcription. Virology. 74:504-519. http ://dx.doi.org/10.1016/0042-6822(76)90356-1
31. Lee, A.S., P.J. Kranzusch, and J.H. Cate. 2015. eIF3 targets cell-proliferation messenger RNAs for translational activation or repression. Nature. 522:111-114. http ://dx.doi.org/10.1038/nature14267
32. Lin, L., Y. Li, H.M. Pyo, X. Lu, S.N. Raman, Q. Liu, E.G. Brown, and Y. Zhou. 2012. Identification of RNA helicase A as a cellular factor that interacts with influenza A virus NS1 protein and its role in the virus life cycle. J. Virol. 86:1942-1954. http ://dx.doi.org/10.1128/JVI.06362-11
33. Mellroth, P., R. Daniels, A. Eberhardt, D. Rönnlund, H. Blom, J. Widengren, S. Normark, and B. Henriques-Normark. 2012. LytA, major autolysin of Streptococcus pneumoniae, requires access to nascent peptidoglycan. J. Biol. Chem. 287:11018-11029. http ://dx.doi.org/10.1074/jbc.M111.318584
34. Mor, A., A. White, K. Zhang, M. Thompson, M. Esparza, R. Muñoz-Moreno, K. Koide, K.W. Lynch, A. García-Sastre, and B.M. Fontoura. 2016. Influenza virus mRNA trafficking through host nuclear speckles. Nat. Microbiol. 1:16069. http ://dx.doi.org/10.1038/nmicrobiol.2016.69
35. Mortimer, S.A., M.A. Kidwell, and J.A. Doudna. 2014. Insights into RNA structure and function from genome-wide studies. Nat. Rev. Genet. 15:469-479. http ://dx.doi.org/10.1038/nrg3681
36. Muckenthaler, M., N.K. Gray, and M.W. Hentze. 1998. IRP-1 binding to ferritin mRNA prevents the recruitment of the small ribosomal subunit by the cap-binding complex eIF4F. Mol. Cell. 2:383-388. http ://dx.doi.org/10.1016/S1097-2765(00)80282-8
37. Nordholm, J., D.V. da Silva, J. Damjanovic, D. Dou, and R. Daniels. 2013. Polar residues and their positional context dictate the transmembrane domain interactions of influenza A neuraminidases. J. Biol. Chem. 288:10652-10660. http ://dx.doi.org/10.1074/jbc.M112.440230
38. Park, Y.W., and M.G. Katze. 1995. Translational control by influenza virus. Identification of cis-acting sequences and trans-acting factors which may regulate selective viral mRNA translation. J. Biol. Chem. 270:28433-28439
39. Park, Y.W., J. Wilusz, and M.G. Katze. 1999. Regulation of eukaryotic protein synthesis: Selective influenza viral mRNA translation is mediated by the cellular RNA-binding protein GRSF-1. Proc. Natl. Acad. Sci. USA. 96:6694-6699. http ://dx.doi.org/10.1073/pnas.96.12.6694
40. Qian, X.Y., C.Y. Chien, Y. Lu, G.T. Montelione, and R.M. Krug. 1995. An amino-terminal polypeptide fragment of the influenza virus NS1 protein possesses specific RNA-binding activity and largely helical backbone structure. RNA. 1:948-956
41. Ray, D., H. Kazan, K.B. Cook, M.T. Weirauch, H.S. Najafabadi, X. Li, S. Gueroussov, M. Albu, H. Zheng, A. Yang, et al. 2013. A compendium of RNA-binding motifs for decoding gene regulation. Nature. 499:172-177. http ://dx.doi.org/10.1038/nature12311
42. Richardson, S.M., S.J. Wheelan, R.M. Yarrington, and J.D. Boeke. 2006. GeneDesign: Rapid, automated design of multikilobase synthetic genes. Genome Res. 16:550-556. http ://dx.doi.org/10.1101/gr.4431306
43. Shapiro, G.I., T. Gurney Jr., and R.M. Krug. 1987. Influenza virus gene expression: control mechanisms at early and late times of infection and nuclear-cytoplasmic transport of virus-specific RNAs. J. Virol. 61:764-773
44. Skehel, J.J. 1973. Early polypeptide synthesis in influenza virus-infected cells. Virology. 56:394-399. http ://dx.doi.org/10.1016/0042-6822(73)90320-6
45. Treanor, J.J., M.H. Snyder, W.T. London, and B.R. Murphy. 1989. The B allele of the NS gene of avian influenza viruses, but not the A allele, attenuates a human influenza A virus for squirrel monkeys. Virology. 171:1-9. http ://dx.doi.org/10.1016/0042-6822(89)90504-7
46. Vester, D., A. Lagoda, D. Hoffmann, C. Seitz, S. Heldt, K. Bettenbrock, Y. Genzel, and U. Reichl. 2010. Real-time RT-qPCR assay for the analysis of human influenza A virus transcription and replication dynamics. J. Virol. Methods. 168:63-71. http ://dx.doi.org/10.1016/j.jviromet.2010.04.017
47. Walter, P., and G. Blobel. 1981. Translocation of proteins across the endoplasmic reticulum III. Signal recognition protein (SRP) causes signal sequencedependent and site-specific arrest of chain elongation that is released by microsomal membranes. J. Cell Biol. 91:557-561. http ://dx.doi.org/10.1083/jcb.91.2.557
48. Walter, P., and A.E. Johnson. 1994. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10:87-119. http ://dx.doi.org/10.1146/annurev.cb.10.110194.000511
49. Walter, P., I. Ibrahimi, and G. Blobel. 1981. Translocation of proteins across the endoplasmic reticulum. I. Signal recognition protein (SRP) binds to invitro-assembled polysomes synthesizing secretory protein. J. Cell Biol. 91:545-550. http ://dx.doi.org/10.1083/jcb.91.2.545
50. Wang, W., K. Riedel, P. Lynch, C.Y. Chien, G.T. Montelione, and R.M. Krug. 1999. RNA binding by the novel helical domain of the influenza virus NS1 protein requires its dimer structure and a small number of specific basic amino acids. RNA. 5:195-205. http ://dx.doi.org/10.1017/S1355838299981621
51. Zurek, N., L. Sparks, and G. Voeltz. 2011. Reticulon short hairpin transmembrane domains are used to shape ER tubules. Traffic. 12:28-41. http ://dx.doi.org/10.1111/j.1600-0854.2010.01134.x