New insights into the nuclear localization of retroviral gag proteins

Nucleus

Volumn 2, Issue 2, 2011, Pages 92-97

  Parent, Leslie J ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Gag proteins; Nucleocytoplasmic trafficking; Retroviral assembly; Viral RNA packaging

Indexed keywords

GAG PROTEIN; NUCLEOPROTEIN; VIRUS RNA;

AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE TRANSPORT; FELINE LEUKEMIA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS; MURINE LEUKEMIA VIRUS; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR PORE COMPLEX; PROTEIN LOCALIZATION; RETROPOSON; ROUS SARCOMA ONCOVIRUS; SPUMA VIRUS;

BORNA DISEASE VIRUS; CORONAVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN SPUMARETROVIRUS; MURINE LEUKEMIA VIRUS; RICE STRIPE VIRUS; ROUS SARCOMA VIRUS; SCHIZOSACCHAROMYCES POMBE;

EID: 79953325166     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.2.2.15018     Document Type: Article

References (59)

1. Arnold M, Nath A, Hauber J, Kehlenbach RH. Multiple importins function as nuclear transport receptors for the rev protein of human immunodeficiency virus type 1. J Biol Chem 2006; 281:20883-90.
2. Balasundaram D, Benedik MJ, Morphew M, Dang VD, Levin HL. Nup124p Is a nuclear pore factor of schizosaccharomyces pombe that is important for nuclear import and activity of retrotransposon Tf1. Mol Cell Biol 1999; 19:5768-84.
3. Berkowitz R, Fisher J, Goff SP. RNA packaging. Curr Top Microbiol Immunol 1996; 214:177-218.
4. Bohl CR, Brown SM, Weldon RA Jr. The Pp24 phosphoprotein of mason-pfizer monkey virus contributes to viral genome packaging. Retrovirology 2005; 2:68.
5. Bowzard JB, Bennett RP, Krishna NK, Ernst SM, Rein A, Wills JW. Importance of basic residues in the nucleocapsid sequence for retrovirus Gag assembly and complementation rescue. J Virol 1998; 72:9034-44.
6. Bui M, Wills EG, Helenius A, Whittaker G. Role of the infeluenza virus M1 protein in nuclear export of viral ribonucleoproteins. J Virol 2000; 74:1781-6.
7. Butterfield-Gerson KL, Scheifele LZ, Ryan EP, Hopper AK, Parent LJ. Importin beta family members mediate alpharetrovirus Gag nuclear entry via interactions with MA and NC. J Virol 2006; 80:1798-806.
8. Carmody SR, Wente SR. Mrna nuclear export at a glance. J Cell Sci 2009; 122:1933-7.
9. Cullen BR. Nuclear RNA export pathways. Mol Cell Biol 2000; 20:4181-7.
10. D'Souza V, Summers MF. How retroviruses select their genomes. Nat Rev Microbiol 2005; 3:643-55.
11. Dang VD, Levin HL. Nuclear import of the ret-rotransposon Tf1 is governed by a nuclear localization signal that possesses a unique requirement for the FXFG nuclear pore factor Nup124p. Mol Cell Biol 2000; 20:7798-812.
12. Demirov DG, Freed EO. Retrovirus budding. Virus Res 2004; 106:87-102.
13. Doye V, Hurt E. From nucleoporins to nuclear pore complexes. Curr Opin Cell Biol 1997; 9:401-11.
14. Dupont S, Sharova N, DeHoratius C, Virbasius CM, Zhu X, Bukrinskaya AG, et al. A novel nuclear export activity in HIV-1 matrix protein required for viral replication. Nature 1999; 402:681-5.
15. Elton D, Simpson-Holley M, Archer K, Medcalf L, Hallam R, McCauley J, et al. Interaction of the influenza virus nucleoprotein with the cellular Crm1-mediated nuclear export pathway. J Virol 2001; 75:408-19.
16. Freed EO. Viral late domains. J Virol 2002; 76:4679-87.
17. Fries T, Betz C, Sohn K, Caesar S, Schlenstedt G, Bailer SM. A novel conserved nuclear localization signal is recognized by a group of yeast importins. J Biol Chem 2007; 282:19292-301.
18. Fukuda M, Asano S, Nakamura T, Adachi M, Yoshida M, Yanagida M, et al. Crm1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 1997; 390:308-11.
19. Garbitt-Hirst R, Kenney SP, Parent LJ. Genetic evidence for a connection between rous sarcoma virus Gag nuclear trafficking and genomic RNA packaging. J Virol 2009; 83:6790-7
20. Garcia EL, Onafuwa-Nuga A, Sim S, King SR, Wolin SL, Telesnitsky A. Packaging of host My RNAs by Murine leukemia virus may occur early in Y RNA biogenesis. J Virol 2009; 83:12526-34.
21. Grigorov B, Decimo D, Smagulova F, Pechoux C, Mougel M, Muriaux D, et al. Intracellular HIV-1 Gag localization is impaired by mutations in the nucleocapsid zinc fingers. Retrovirology 2007; 4:54.
22. Gudleski N, Flanagan JM, Ryan EP, Bewley MC, Parent LJ. Directionality of nucleocytoplasmic transport of the retroviral Gag protein depends on sequential binding of karyopherins and viral RNA. Proc Natl Acad Sci USA 2010; 107:9358-63.
23. Hsieh PK, Chang SC, Huang CC, Lee TT, Hsiao CW, Kou YH, et al. Assembly of severe acute respiratory syndrome coronavirus RNA packaging signal into virus-like particles is nucleocapsid dependent. J Virol 2005; 79:13848-55.
24. Huang X, Liu T, Muller J, Levandowski RA, Ye Z. Effect of influenza virus matrix protein and viral RNA on ribonucleoprotein formation and nuclear export. Virology 2001; 287:405-16.
25. Jewell NA, Mansky LM. In the beginning: Genome recognition, RNA encapsidation and the initiation of complex retrovirus assembly. J Gen Virol 2000; 81:1889-99.
26. Kemler I, Meehan A, Poeschla EM. Live-cell coimaging of the genomic rnas and Gag proteins of two lentiviruses. J Virol 2010; 84:6352-66.
27. Kim MK, Claiborn KC, Levin HL. The long terminal repeat-containing retro transposon Tf1 possesses amino acids in Gag that regulate nuclear localization and particle formation. J Virol 2005; 79:9540-55.
28. Kobayashi T, Kamitani W, Zhang G, Watanabe M, Tomonaga K, Ikuta K. Borna disease virus nucleoprotein requires both nuclear localization and export activities for viral nucleocytoplasmic shuttling. J Virol 2001; 75:3404-12.
29. Larsen LS, Beliakova-Bethell N, Bilanchone V, Zhang M, Lamsa A, Dasilva R, et al. Ty3 nucleocapsid controls localization of particle assembly. J Virol 2008; 82:2501-14.
30. Ma K, Roy AMM, Whittaker GR. Nuclear export of influenza virus ribonucleoproteins: Identification of an export intermediate at the nuclear periphery. Virology 2001; 282:215-20.
31. Macara IG. Transport into and out of the nucleus. Microbiol Mol Biol Rev 2001; 65:570-94.
32. Martin K, Helenius A. Nuclear transport of influenza virus ribonucleoproteins: The viral matrix protein (M1) promotes export and inhibits import. Cell 1991; 67:117-30.
33. Mattaj IW, Englmeier L. Nucleocytoplasmic transport: The soluble phase. Annu Rev Biochem 1998; 67:265-306.
34. Moore MJ. From birth to death: The complex lives of eukaryotic MRNAs. Science 2005; 309:1514-8.
35. Moore MJ, Schwartzfarb EM, Silver PA, Yu MC. Differential recruitment of the splicing machinery during transcription predicts genome-wide patterns of mRNA splicing. Molecular Cell 2006; 24:903-15.
36. Nandhagopal N, Simpson AA, Johnson MC, Francisco AB, Schatz GW, Rossmann MG, et al. Dimeric Rous Sarcoma virus capsid protein structure relevant to immature Gag assembly. J Mol Biol 2004; 335:275-82.
37. Nash MA, Meyer MK, Decker GL, Arlinghaus RB. A subset of pr65gag is nucleus associated in Murine leukemia virus-infected cells. J Virol 1993; 67:1350-6.
38. Nayak DP, Hui EKW, Barman S. Assembly and budding of influenza virus. Virus Research 2004; 106:147-65.
39. Nikolaev I, Cochet MF, Felenbok B. Nuclear import of zinc binuclear cluster proteins proceeds through multiple, overlapping transport pathways. Eukaryotic Cell 2003; 2:209-21.
40. Onafuwa-Nuga AA, King SR, Telesnitsky A. Non-random packaging of host RNAs in moloney Murine leukemia virus. J Virol 79:13528-37
41. Pardue ML, Rashkova S, Casacuberta E, DeBaryshe PG, George JA, Traverse KL. Two retrotransposons maintain telomeres in drosophila. Chromosome Res 2005; 13:443-53.
42. Parent LJ, Bennett RP, Craven RC, Nelle TD, Krishna NK, Bowzard J B, et al. Positionally independent and exchangeable late budding functions of the Rous Sarcoma virus and human immunodeficiency virus Gag proteins. J Virol 1995; 69: 5455-60.
43. Poole E, Strappe P, Mok HP, Hicks R, Lever AM. HIV-1 Gag-RNA interaction occurs at a perinuclear/ centrosomal site; analysis by confocal microscopy and fret. Traffic 2005; 6:741-55.
44. Rashkova S, Karam SE, Kellum R, Pardue ML. Gag proteins of the two drosophila telomeric retrotransposons are targeted to chromosome ends. J Cell Biol 2002; 159:397-402.
45. Rein A. Retroviral RNA packaging: A review. Arch Virol 1994; 9:513-22.
46. Scheifele LZ, Garbitt RA, Rhoads JD, Parent LJ. Nuclear entry and Crm1-dependent nuclear export of the Rous Sarcoma virus Gag polyprotein. Proc Natl Acad Sci USA 2002; 99:3944-9.
47. Scheifele LZ, Kenney SP, Cairns TM, Craven RC, Parent LJ. Overlapping roles of the Rous Sarcoma virus Gag P10 domain in nuclear export and virion core morphology. J Virol 2007; 81:10718-28.
48. Scheifele LZ, Ryan EP, Parent LJ. Detailed mapping of the nuclear export signal in the Rous Sarcoma virus Gag protein. J Virol 2005; 79:8732-41.
49. Schliephake AW, Rethwilm A. Nuclear localization of foamy virus Gag precursor protein. J Virol 1994; 68:4946-54.
50. Swanstrom R, Wills JW. Synthesis, Assembly and Processing of Viral Proteins. In: Retroviruses JM, Coffin SH, Hughes, Varmus HE, Eds. Cold Spring Harbor Laboratory Press 1997; 263-334.
51. Terry LJ, Shows EB, Wente SR. Crossing the nuclear envelope: Hierarchical regulation of nucleocytoplasmic transport. Science 2007; 318:1412-6.
52. Verderame MF, Nelle TD, Wills JW. The membrane-binding domain of the Rous Sarcoma virus Gag protein. J Virol 1996; 70:2664-8.
53. Vogt VM. Retroviral Virions and Genomes. In: Retroviruses JM, Coffin SH, Hughes, Varmus HE, Eds. Cold Spring Harbor NY, Cold Spring Harbor Press 1997; 27-69.
54. Weldon RA Jr, Sarkar P, Brown SM, Weldon SK. Mason-Pfizer monkey virus Gag proteins interact with the human sumo conjugating enzyme, hUbc9. Virology 2003; 314:62-73.
55. Wills JW, Craven RC. Form, function and use of retroviral Gag proteins. AIDS 1991; 5:639-54.
56. Yanai H, Kobayashi T, Hayashi Y, Watanabe Y, Ohtaki N, Zhang G, et al. A methioninerich domain mediates Crm1-dependent nuclear export activity of borna disease virus phosphoprotein. J Virol 2006; 80:1121-9.
57. You J, Dove BK, Enjuanes L, DeDiego ML, Alvarez E, Howell G, et al. Subcellular localization of the severe acute respiratory syndrome coronavirus nucleocapsid protein. J Gen Virol 2005; 86:3303-10.
58. Yu SF, Edelmann K, Strong RK, Moebes A, Rethwilm A, Linial ML. The Carboxyl Terminus of the Human Foamy Virus Gag Protein Contains Separable Nucleic Acid Binding and Nuclear Transport Domains. J Virol 1996; 70:8255-62.
59. Zhou J, McAllen JK, Tailor Y, Summers MF. High affinity nucleocapsid protein binding to the mupsi RNA packaging signal of Rous Sarcoma virus. J Mol Biol 2005; 349:976-88.