The L1 major capsid protein of human papillomavirus type 11 interacts with Kap β2 and Kap β3 nuclear import receptors

Virology

Volumn 306, Issue 1, 2003, Pages 162-169

  Nelson, Lisa M ^a   Rose, Robert C ^b   Moroianu, Junona ^a  

^a BOSTON COLLEGE   (United States)

^b UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Kap 2; Kap 3; Karyopherins; L1; Papillomavirus

Indexed keywords

CAPSID PROTEIN; KARYOPHERIN BETA;

ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIRION; VIRUS STRAIN; WART VIRUS;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPES; PAPILLOMAVIRUS;

EID: 0037295145     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0042-6822(02)00025-9     Document Type: Article

References (43)

1. Adam E.J., Adam S.A. Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope. J. Cell Biol. 125:1994;547-555.
2. Belnap D.M., Olson N.H., Cladel N.M., Newcomb W.W., Brown J.C., Kreider J.W., Christensen N.D., Baker T.S. Conserved features in papillomavirus and polyomavirus capsids. J. Mol. Biol. 259:1996;249-263 doi:10.1006/jmbi.1996.0317.
3. Bonifaci N., Moroianu J., Radu A., Blobel G. Karyopherin beta2 mediates nuclear import of a mRNA binding protein. Proc. Natl. Acad. Sci. USA. 94:1997;5055-5060.
4. Chi N.C., Adam E.J., Adam S.A. Sequence and characterization of cytoplasmic nuclear protein import factor p97. J. Cell Biol. 130:1995;265-274.
5. Chi N.C., Adam E.J., Visser G.D., Adam S.A. RanBP1 stabilizes the interaction of Ran with p97 nuclear protein import. J. Cell Biol. 135:1996;559-569.
6. Chook Y.M., Blobel G. Structure of the nuclear transport complex karyopherin-beta2-Ran x GppNHp [see comments]. Nature. 399:1999;230-237.
7. Chook Y.M., Jung A., Rosen M.K., Blobel G. Uncoupling Kapbeta2 substrate dissociation and ran binding. Biochemistry. 41:2002;6955-6966.
8. Coutavas E., Ren M., Oppenheim J.D., D'Eustachio P., Rush M.G. Characterization of proteins that interact with the cell-cycle regulatory protein Ran/TC4. Nature. 366:1993;585-587.
9. Dreyfuss G., Matunis M.J., Pinol-Roma S., Burd C.G. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:1993;289-321.
10. Floer M., Blobel G. The nuclear transport factor karyopherin beta binds stoichiometrically to Ran-GTP and inhibits the Ran GTPase activating protein. J. Biol. Chem. 271:1996;5313-5316.
11. Gorlich D., Vogel F., Mills A.D., Hartmann E., Laskey R.A. Distinct functions for the two importin subunits in nuclear protein import. Nature. 377:1995;246-248.
12. Hagensee M.E., Olson N.H., Baker T.S., Galloway D.A. Three-dimensional structure of vaccinia virus-produced human papillomavirus type 1 capsids. J. Virol. 68:1994;4503-4505.
13. Izaurralde E., Jarmolowski A., Beisel C., Mattaj I.W., Dreyfuss G., Fischer U. A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J. Cell Biol. 137:1997;27-35.
14. Jakel S., Gorlich D. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 17:1998;4491-4502.
15. Kataoka N., Bachorik J.L., Dreyfuss G. Transportin-SR, a nuclear import receptor for SR proteins. J. Cell Biol. 145:1999;1145-1152.
16. Kirnbauer R., Booy F., Cheng N., Lowy D.R., Schiller J.T. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc. Natl. Acad. Sci. USA. 89:1992;12180-12184.
17. Li M., Beard P., Estes P.Q.A., Lyon M.K., Garcea R.L. Intercapsomeric disulfide bonds in papillomavirus assembly and disassembly. J. Virol. 72:1998;2160-2167.
18. McCarthy M.P., White W.I., Palmer-Hill F., Koenig S., Suzich J.A. Quantitative disassembly and reassembly of human papillomavirus type 11 viruslike particles in vitro. J. Virol. 72:1998;32-41.
19. Merle E., Rose R.C., LeRoux L., Moroianu J. Nuclear import of HPV11 L1 capsid protein is mediated by karyopherin alpha2beta1 heterodimers. J. Cell. Biochem. 74:1999;628-637.
20. Moroianu, J. (1999). Nuclear import and export pathways. J. Cell. Biochem. (Suppl.) 76-83.
21. Muhlhausser P., Muller E.C., Otto A., Kutay U. Multiple pathways contribute to nuclear import of core histones. EMBO Rep. 2:2001;690-696.
22. Nakielny S., Dreyfuss G. Transport of proteins and RNAs in and out of the nucleus. Cell. 99:1999;677-690.
23. Nelson L.M., Rose R.C., LeRoux L., Lane C., Bruya K., Moroianu J. Nuclear import and DNA binding of human papillomavirus type 45 L1 capsid protein. J. Cell. Biochem. 79:2000;225-238.
24. Nelson L.M., Rose R.C., Moroianu J. Nuclear import strategies of high risk HPV16 L1 major capsid protein. J. Biol. Chem. 277:2002;23958-23964.
25. Paschal B.M., Gerace L. Identification of NTF2, a cytosolic factor for nuclear import that interacts with nuclear pore complex protein p62. J. Cell Biol. 129:1995;925-937.
26. Pollard V.W., Michael W.M., Nakielny S., Siomi M.C., Wang F., Dreyfuss G. A novel receptor-mediated nuclear protein import pathway. Cell. 86:1996;985-994.
27. Ribbeck K., Kutay U., Paraskeva E., Gorlich D. The translocation of transportin-cargo complexes through nuclear pores is independent of both Ran and energy. Curr. Biol. 9:1999;47-50.
28. Ribbeck K., Lipowsky G., Kent H.M., Stewart M., Gorlich D. NTF2 mediates nuclear import of Ran. EMBO J. 17:1998;6587-6598.
29. Rose R.C., Bonnez W., Da Rin C., McCance D.J., Reichman R.C. Serological differentiation of human papillomavirus types 11, 16 and 18 using recombinant virus-like particles. J. Gen. Virol. 75:1994;2445-2449.
30. Rose R.C., Bonnez W., Reichman R.C., Garcea R.L. Expression of human papillomavirus type 11 L1 protein in insect cells In vivo and in vitro assembly of viruslike particles. J. Virol. 67:1993;1936-1944.
31. Rose R.C., Reichman R.C., Bonnez W. Human papillomavirus (HPV) type 11 recombinant virus-like particles induce the formation of neutralizing antibodies and detect HPV-specific antibodies in human sera. J. Gen. Virol. 75:1994;2075-2079.
32. Schwoebel E.D., Talcott B., Cushman I., Moore M.S. Ran-dependent signal-mediated nuclear import does not require GTP hydrolysis by Ran. J. Biol. Chem. 273:1998;35170-35175.
33. Siomi H., Dreyfuss G. A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 129:1995;551-560.
34. Siomi M.C., Eder P.S., Kataoka N., Wan L., Liu Q., Dreyfuss G. Transportin-mediated nuclear import of heterogeneous nuclear RNP proteins. J. Cell Biol. 138:1997;1181-1192.
35. Trus B.L., Roden R.B., Greenstone H.L., Vrhel M., Schiller J.T., Booy F.P. Novel structural features of bovine papillomavirus capsid revealed by a three-dimensional reconstruction to 9 A resolution. Nat. Struct. Biol. 4:1997;413-420.
36. Truant R., Kang Y., Cullen B.R. The human tap nuclear RNA export factor contains a novel transportin-dependent nuclear localization signal that lacks nuclear export signal function. J. Biol. Chem. 274:1999;32167-32172.
37. van der Houven van Oordt W., Diaz-Meco M.T., Lozano J., Krainer A.R., Moscat J., Caceres J.F. The MKK(3/6)-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J. Cell Biol. 149:2000;307-316.
38. Volpers C., Schirmacher P., Streeck R.E., Sapp M. Assembly of the major and the minor capsid protein of human papillomavirus type 33 into virus-like particles and tubular structures in insect cells. Virology. 200:1994;504-512 doi:10.1006/viro.1994.1213.
39. Weis K., Mattaj I.W., Lamond A.I. Identification of hSRP1 alpha as a functional receptor for nuclear localization sequences. Science. 268:1995;1049-1053.
40. Wente S.R. Gatekeepers of the nucleus. Science. 288:2000;1374-1377.
41. Yaseen N.R., Blobel G. Cloning and characterization of human karyopherin beta3. Proc. Natl. Acad. Sci. USA. 94:1997;4451-4456.
42. Zhou J., Stenzel D.J., Sun X.Y., Frazer I.H. Synthesis and assembly of infectious bovine papillomavirus particles in vitro. J. Gen. Virol. 74:1993;763-768.
43. zur Hausen H. Papillomaviruses causing cancer evasion from host-cell control in early events in carcinogenesis. J. Natl. Cancer Inst. 92:2000;690-698.