Directionality of nucleocytoplasmic transport of the retroviral gag protein depends on sequential binding of karyopherins and viral RNA

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 20, 2010, Pages 9358-9363

  Gudleski, Nicole ^a   Flanagan, John M ^a   Ryan, Eileen P ^a,b   Bewley, Maria C ^a   Parent, Leslie J ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

CRM1; Importin ; Importin 11; Protein RNA binding; Retrovirus assembly

Indexed keywords

EXPORTIN 1; GAG PROTEIN; GENOMIC RNA; HETERODIMER; KARYOPHERIN ALPHA; KARYOPHERIN BETA;

ANIMAL CELL; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FIBROBLAST; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; QUAIL; RETROVIRUS; VIRION; VIRUS PARTICLE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL NUCLEUS; GENE PRODUCTS, GAG; IMMUNOPRECIPITATION; KARYOPHERINS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; QUAIL; RIBONUCLEOPROTEINS; RNA, VIRAL; ROUS SARCOMA VIRUS; VIRUS ASSEMBLY;

ROUS SARCOMA VIRUS;

EID: 77952733968     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1000304107     Document Type: Article

References (61)

1. Terry LJ, Shows EB, Wente SR (2007) Crossing the nuclear envelope: Hierarchical regulation of nucleocytoplasmic transport. Science 318:1412-1416.
2. Pemberton LF, Paschal BM (2005) Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6:187-198.
3. Gardiner FC, Costa R, Ayscough KR (2007) Nucleocytoplasmic trafficking is required for functioning of the adaptor protein Sla1p in endocytosis. Traffic 8: 347-358.
4. Behrens J, et al. (1996) Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382:638-642.
5. Itoh K, Brott BK, Bae GU, Ratcliffe MJ, Sokol SY (2005) Nuclear localization is required for Dishevelled function in Wnt/beta-catenin signaling. J Biol, 10.1186/jbiol20.
6. Scheifele LZ, Garbitt RA, Rhoads JD, Parent LJ (2002) Nuclear entry and CRM1- dependent nuclear export of the Rous sarcoma virus Gag polyprotein. Proc Natl Acad Sci USA 99:3944-3949.
7. Swanstrom R, Wills JW (1997) Retroviruses, eds Coffin JM, Hughes SH, Varmus HE (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY), pp 263-334.
8. Garbitt-Hirst R, Kenney SP, Parent LJ (2009) Genetic evidence for a connection between Rous sarcoma virus gag nuclear trafficking and genomic RNA packaging. J Virol 83:6790-6797.
9. Dupont S, et al. (1999) A novel nuclear export activity in HIV-1 matrix protein required for viral replication. Nature 402:681-685. (Pubitemid 129516340)
10. Nash MA, Meyer MK, Decker GL, Arlinghaus RB (1993) A subset of Pr65gag is nucleus associated in murine leukemia virus-infected cells. J Virol 67:1350-1356.
11. Balasundaram D, Benedik MJ, Morphew M, Dang VD, Levin HL (1999) Nup124p is a nuclear pore factor of Schizosaccharomyces pombe that is important for nuclear import and activity of retrotransposon Tf1. Mol Cell Biol 19:5768-5784. (Pubitemid 29339932)
12. Schliephake AW, Rethwilm A (1994) Nuclear localization of foamy virus Gag precursor protein. J Virol 68:4946-4954.
13. Butterfield-Gerson KL, Scheifele LZ, Ryan EP, Hopper AK, Parent LJ (2006) Importin-beta family members mediate alpharetrovirus gag nuclear entry via interactions with matrix and nucleocapsid. J Virol 80:1798-1806.
14. Scheifele LZ, Ryan EP, Parent LJ (2005) Detailed mapping of the nuclear export signal in the Rous sarcoma virus Gag protein. J Virol 79:8732-8741.
15. Verderame MF, Nelle TD, Wills JW (1996) The membrane-binding domain of the Rous sarcoma virus Gag protein. J Virol 70:2664-2668.
16. Weldon RA, Jr, Wills JW (1993) Characterization of a small (25-kilodalton) derivative of the Rous sarcoma virus Gag protein competent for particle release. J Virol 67: 5550-5561.
17. Nandhagopal N, et al. (2004) Dimeric rous sarcoma virus capsid protein structure relevant to immature Gag assembly. J Mol Biol 335:275-282. (Pubitemid 37494978)
18. Scheifele LZ, Kenney SP, Cairns TM, Craven RC, Parent LJ (2007) Overlapping roles of the Rous sarcoma virus Gag p10 domain in nuclear export and virion core morphology. J Virol 81:10718-10728.
19. Timney BL, et al. (2006) Simple kinetic relationships and nonspecific competition govern nuclear import rates in vivo. J Cell Biol 175:579-593.
20. Plafker SM, Macara IG (2000) Importin-11, a nuclear import receptor for the ubiquitin-conjugating enzyme, UbcM2. EMBO J 19:5502-5513.
21. Yang W, Musser SM (2006) Nuclear import time and transport efficiency depend on importin beta concentration. J Cell Biol 174:951-961. (Pubitemid 44455184)
22. Conti E, Uy M, Leighton L, Blobel G, Kuriyan J (1998) Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell 94:193-204. (Pubitemid 28348007)
23. Banks JD, Linial ML (2000) Secondary structure analysis of a minimal avian leukosis-sarcoma virus packaging signal. J Virol 74:456-464.
24. Zhou J, McAllen JK, Tailor Y, Summers MF (2005) High affinity nucleocapsid protein binding to the muPsi RNA packaging signal of Rous sarcoma virus. J Mol Biol 349: 976-988. (Pubitemid 40779620)
25. Steeg CM, Vogt VM (1990) RNA-binding properties of the matrix protein (p19gag) of avian sarcoma and leukemia viruses. J Virol 64:847-855.
26. Darlix JL, Spahr PF (1982) Binding sites of viral protein P19 onto Rous sarcoma virus RNA and possible controls of viral functions. J Mol Biol 160:147-161.
27. Leis JP, McGinnis J, Green RW (1978) Rous sarcoma virus p19 binds to specific double-stranded regions of viral RNA: Effect of p19 on cleavage of viral RNA by RNase III. Virology 84:87-98. (Pubitemid 8268922)
28. Hutten S, Kehlenbach RH (2007) CRM1-mediated nuclear export: To the pore and beyond. Trends Cell Biol 17:193-201. (Pubitemid 46507806)
29. Bischoff FR, Klebe C, Kretschmer J, Wittinghofer A, Ponstingl H (1994) RanGAP1 induces GTPase activity of nuclear Ras-related Ran. Proc Natl Acad Sci USA 91: 2587-2591.
30. Kenney SP, Lochmann TL, Schmid CL, Parent LJ (2008) Intermolecular interactions between retroviral Gag proteins in the nucleus. J Virol 82:683-691.
31. Rulli SJ, Jr, et al. (2007) Selective and nonselective packaging of cellular RNAs in retrovirus particles. J Virol 81:6623-6631.
32. Giles KE, Caputi M, Beemon KL (2004) Packaging and reverse transcription of snRNAs by retroviruses may generate pseudogenes. RNA 10:299-307.
33. Chen PJ, Cywinski A, Taylor JM (1985) Reverse transcription of 7S L RNA by an avian retrovirus. J Virol 54:278-284.
34. Garcia EL, et al. (2009) Packaging of host mY RNAs by murine leukemia virus may occur early in Y RNA biogenesis. J Virol 83:12526-12534.
35. Fritz J, et al. (2009) RNA-regulated interaction of transportin-1 and exportin-5 with the double-stranded RNA-binding domain regulates nucleocytoplasmic shuttling of ADAR1. Mol Cell Biol 29:1487-1497.
36. Ma YM, Vogt VM (2004) Nucleic acid binding-induced Gag dimerization in the assembly of Rous sarcoma virus particles in vitro. J Virol 78:52-60.
37. Wodrich H, et al. (2006) Adenovirus core protein pVII is translocated into the nucleus by multiple import receptor pathways. J Virol 80:9608-9618.
38. Luo M, Pang CW, Gerken AE, Brock TG (2004) Multiple nuclear localization sequences allow modulation of 5-lipoxygenase nuclear import. Traffic 5:847-854.
39. Pemberton LF, Rosenblum JS, Blobel G (1999) Nuclear import of the TATA-binding protein: Mediation by the karyopherin Kap114p and a possible mechanism for intranuclear targeting. J Cell Biol 145:1407-1417.
40. Campbell S, Vogt VM (1995) Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1. J Virol 69:6487-6497.
41. Svarovskaia ES, et al. (2004) Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J Biol Chem 279:35822-35828.
42. Ma YM, Vogt VM (2002) Rous sarcoma virus Gag protein-oligonucleotide interaction suggests a critical role for protein dimer formation in assembly. J Virol 76:5452-5462.
43. Garbitt RA, Albert JA, Kessler MD, Parent LJ (2001) trans-acting inhibition of genomic RNA dimerization by Rous sarcoma virus matrix mutants. J Virol 75:260-268.
44. Craven RC, Leure-duPree AE, Erdie CR, Wilson CB, Wills JW (1993) Necessity of the spacer peptide between CA and NC in the Rous sarcoma virus gag protein. J Virol 67: 6246-6252.
45. Callahan EM, Wills JW (2000) Repositioning basic residues in the M domain of the Rous sarcoma virus Gag protein. J Virol 74:11222-11229.
46. Callahan EM, Wills JW (2003) Link between genome packaging and rate of budding for Rous sarcoma virus. J Virol 77:9388-9398.
47. Palmeri D, Malim MH (1999) Importin beta can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin alpha. Mol Cell Biol 19:1218-1225.
48. Yang J, Cullen BR (1999) Structural and functional analysis of the avian leukemia virus constitutive transport element. RNA 5:1645-1655.
49. Chen MH, et al. (2005) Phospholipid scramblase 1 contains a nonclassical nuclear localization signal with unique binding site in importin alpha. J Biol Chem 280: 10599-10606.
50. Yaseen NR, Blobel G (1997) Cloning and characterization of human karyopherin beta3. Proc Natl Acad Sci USA 94:4451-4456.
51. Stewart-Maynard KM, et al. (2008) Retroviral nucleocapsid proteins display nonequivalent levels of nucleic acid chaperone activity. J Virol 82:10129-10142.
52. Purdy JG, Flanagan JM, Ropson IJ, Rennoll-Bankert KE, Craven RC (2008) Critical role of conserved hydrophobic residues within the major homology region in mature retroviral capsid assembly. J Virol 82:5951-5961.
53. Weldon RA, Jr, Erdie CR, Oliver MG, Wills JW (1990) Incorporation of chimeric Gag protein into retroviral particles. J Virol 64:4169-4179.
54. Bonanno JB, et al. (2001) Structural genomics of enzymes involved in sterol/isoprenoid biosynthesis. Proc Natl Acad Sci USA 98:12896-12901.
55. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expression Purif 41:207-234.
56. Hieda M, et al. (1999) A monoclonal antibody to the COOH-terminal acidic portion of Ran inhibits both the recycling of Ran and nuclear protein import in living cells. J Cell Biol 144:645-655.
57. Lischka P, Sorg G, Kann M, Winkler M, Stamminger T (2003) A nonconventional nuclear localization signal within the UL84 protein of human cytomegalovirus mediates nuclear import via the importin alpha/beta pathway. J Virol 77:3734-3748.
58. O'Regan KJ, Murphy MA, Bucks MA, Wills JW, Courtney RJ (2007) Incorporation of the herpes simplex virus type 1 tegument protein VP22 into the virus particle is independent of interaction with VP16. Virology 369:263-280.
59. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36-42.
60. Guichet A, et al. (1997) The nuclear receptor homologue Ftz-F1 and the homeodomain protein Ftz are mutually dependent cofactors. Nature 385:548-552.
61. Schwartz CJ, et al. (2001) FTZ-Factor1 and Fushi tarazu interact via conserved nuclear receptor and coactivator motifs. EMBO J 20:510-519.