Mapping of nuclear import signal and importin α3 binding regions of 52K protein of bovine adenovirus-3

Virology

Volumn 432, Issue 1, 2012, Pages 63-72

  Paterson, Carolyn P ^a,b   Ayalew, Lisanework E ^a,b   Tikoo, Suresh K ^a,b  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

52K; Alpha importins; BAdV 3; NLS; Nucleus

Indexed keywords

HYBRID PROTEIN; IMPORTIN ALPHA3; KARYOPHERIN ALPHA; MUTANT PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; BINDING SITE; BOVINE ADENOVIRUS; BOVINE ADENOVIRUS 3; CELL NUCLEUS; CONTROLLED STUDY; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; NUCLEOLUS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOVIRIDAE; ALPHA KARYOPHERINS; ANIMALS; BINDING SITES; CATTLE; CELL LINE; CELL NUCLEUS; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN SORTING SIGNALS; VIRAL NONSTRUCTURAL PROTEINS;

BOVINE ADENOVIRUS 3;

EID: 84864015937     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.05.021     Document Type: Article

References (47)

1. Adam S.A., Marr R.S., Gerace L. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 1990, 111:807-816.
2. Bangari D.S., Sharma A., Mittal S.K. Bovine adenovirus type 3 internalization is independent of primary receptors of human adenovirus type 5 and porcine adenovirus type 3. Biochem. Biophys. Res. Commun. 2005, 331:1478-1484.
3. Christophe D., Christophe-Hobertus C., Pichon B. Nuclear targeting of proteins: how many different signals?. Cell Signal. 2000, 12:337-341.
4. Conti E., Uy M., Leighton L., Blobel G., Kurian J. Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin alpha. Cell 1998, 94:193-204.
5. Davison A.J., Benko M., Harrach B. Genetic content and evolution of adenoviruses. J. Gen. Virol. 2003, 84:2895-2908.
6. Depping R., Steinhoff A., Schindler S.G., Friedrich B., Fagerlund R., Metzen E., Hartmann E., Köhler M. Nuclear translocation of hypoxia-inducible factors (HIFs): involvement of the classical importin alpha/beta pathway. Biochim. Biophys. Acta 2008, 1783:394-404.
7. Efthymiadis A., Briggs L.J., Jans D.A. The HIV-1 Tat nuclear localization sequence confers novel nuclear import properties. J. Biol. Chem. 1998, 273:1623-1628.
8. Fonte M.R., Teh T., Kobe B. Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin alpha. J. Mol. Biol. 2000, 297:1183-1194.
9. Fried H., Kutay U. Nucleocytoplasmic transport: taking an inventory. Cell. Mol. Life Sci. 2003, 60:1659-1688.
10. Friedrich B., Quensel C., Sommer T., Hartmann E., Kohler M. Nuclear localization signal and protein context both mediate importin alpha specificity of nuclear import substrates. Mol. Cell. Biol. 2006, 26:8697-8709.
11. Ghildyal R., Ho A., Wagstaff K.M., Dias M.M., Barton C.L., Jans P., Bardin P., Jans D.A. Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry 2005, 44:12887-12895.
12. Görlich D., Henklein P., Laskey R.A., Hartmann E. A 41 amino acid motif in importin-alpha confers binding to importin-beta and hence transit into the nucleus. EMBO J. 1996, 15:1810-1817.
13. Gorlich D., Kostaka S., Kraft R., Dingwall C., Laskey R.A., Hartmann E., Prehn S. Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr. Biol. 1995, 5:383-392.
14. Görlich D., Kraft R., Kostka S., Vogel F., Hartmann E., Laskey R.A., Mattaj I.W., Izaurralde E. Importin provides a link between nuclear protein import and U snRNA export. Cell 1996, 87:21-32.
15. Gustin K.E., Imperiale M.J. Encapsidation of viral DNA requires the adenovirus L1 52/55-kilodalton protein. J. Virol. 1998, 72:7860-7870.
16. Hanover J.A., Love D.C., Prinz W.A. Calmodulin-driven nuclear entry: trigger for sex determination and terminal differentiation. J. Biol. Chem. 2009, 284:12593-12597.
17. Hasson T.B., Ornelles D.A., Shenk T. Adenovirus L1 52- and 55-kilodalton proteins are present within assembling virions and colocalize with nuclear structures distinct from replication centers. J. Virol. 1992, 66:6133-6142.
18. Hasson T.B., Soloway P.D., Ornelles D.A., Doerfler W., Shenk T. Adenovirus L1 52- and 55-kilodalton proteins are required for assembly of virions. J. Virol. 1989, 63:3612-3621.
19. Hearps A.C., Jans D.A. HIV-1 integrase is capable of targeting DNA to the nucleus via an importin alpha/beta-dependent mechanism. Biochem. J. 2006, 398:475-484.
20. Idamakanti N., Reddy P.S., Babiuk L.A., Tikoo S.K. Transcription mapping and characterization of 284R and 121R proteins produced from early region 3 of bovine adenovirus type 3. Virology 1999, 256:351-359.
21. Imamoto N., Shimamoto T., Takao T., Tachibana T., Kose S., Matsubae M., Sekimoto T., Shimonishi Y., Yoneda Y. In vivo evidence for involvement of a 58kDa component of nuclear pore-targeting complex in nuclear protein import. EMBO J. 1995, 14:3617-3626.
22. Kalderon D., Richardson W.D., Markham A.F., Smith A.E. Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature 1984, 311:33-38.
23. Köhler M., Speck C., Christiansen M., Bischoff F.R., Prehn S., Haller H., Görlich D., Hartmann E. Evidence for distinct substrate specificities of importin alpha family members in nuclear protein import. Mol. Cell. Biol. 1999, 19:7782-7791.
24. Kulshreshtha V., Babiuk L.A., Tikoo S.K. Role of bovine adenovirus-3 33K protein in viral replication. Virology 2004, 323:59-69.
25. Lai M.-C., Lin R.-I., Tarn W.-Y. Transportin-SR2 mediates nuclear import of phosphorylated SR proteins. Proc. Natl. Acad. Sci. USA 2001, 98:10154-10159.
26. Lim R.Y.H., Aebi U., Fahrenkrog B. Towards reconciling structure and function in the nuclear pore complex. Histochem. Cell Biol. 2008, 129:105-116.
27. Lucher L.A., Symington J.S., Green M. Biosynthesis and properties of the adenovirus 2 L1-encoded 52,000- and 55,000-Mr proteins. J. Virol. 1986, 57:839-847.
28. Michael W.M., Eder P.S., Dreyfuss G. The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein. EMBO J. 1997, 16:3587-3598.
29. Miyamoto Y., Imamoto N., Sekimoto T., Tachibana T., Seki T., Tada S., Enomoto T., Yoneda Y. Differential modes of nuclear localization signal (NLS) recognition by three distinct classes of NLS receptors. J. Biol. Chem. 1997, 272:26375-26381.
30. Palmeri D., Malim M.H. Importin beta can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin alpha. Mol. Cell. Biol. 1999, 19:1218-1225.
31. Pollard V.W., Michael W.M., Nakielny S., Siomi M.C., Wang F., Dreyfuss G. A novel receptor-mediated nuclear protein import pathway. Cell 1996, 86:985-994.
32. Rasmussen U.B., Benchaibi M., Meyer V., Schlesinger Y., Schughart K. Novel human gene transfer vectors: evaluation of wild-type and recombinant animal adenoviruses in human-derived cells. Hum. Gene Ther. 1999, 10:2587-2599.
33. Reddy P.S., Chen Y., Idamakanti N., Pyne C., Babiuk L.A., Tikoo S.K. Characterization of early region 1 and pIX of bovine adenovirus-3. Virology 1999, 253:299-308.
34. Reddy P.S., Idamakanti N., Zakhartchouk A.N., Baxi M.K., Lee J.B., Pyne C., Babiuk L.A., Tikoo S.K. Nucleotide sequence, genome organization, and transcription map of bovine adenovirus type 3. J. Virol. 1998, 72:1394-1402.
35. Robbins J., Dilworth S.M., Laskey R.A., Dingwall C. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 1991, 64:615-623.
36. Seki T., Tada S., Katada T., Enomoto T. Cloning of a cDNA encoding a novel importin-alpha homologue, Qip1: discrimination of Qip1 and Rch1 from hSrp1 by their ability to interact with DNA helicase Q1/RecQL. Biochem. Biophys. Res. Commun. 1997, 234:48-53.
37. Tachibana T., Hieda M., Miyamoto Y., Kose S., Imamoto N., Yoneda Y. Recycling of importin alpha from the nucleus is suppressed by loss of RCC1 function in living mammalian cells. Cell Struct. Funct. 2000, 25:115-123.
38. Truant R., Cullen B.R. The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin beta-dependent nuclear localization signals. Mol. Cell. Biol. 1999, 19:1210-1217.
39. Tsuji T., Sheehy N., Gautier V.W., Hayakawa H., Sawa H., Hall W.W. The nuclear import of the human T lymphotropic virus type I (HTLV-1) tax protein is carrier- and energy-independent. J. Biol. Chem. 2007, 282:13875-13883.
40. Welch K., Franke J., Kohler M., Macara I.G. RanBP3 contains an unusual nuclear localization signal that is imported preferentially by importin-α3. Mol. Cell. Biol. 1999, 19:8400-8411.
41. Wohl B.P., Hearing P. Role for the L1-52/55K protein in the serotype specificity of adenovirus DNA packaging. J. Virol. 2008, 82:5089-5092.
42. Wu Q., Chen Y., Kulshreshtha V., Tikoo S. Characterization and nuclear localization of the fiber protein encoded by the late region 7 of bovine adenovirus type 3. Arch. Virol. 2004, 149:1783-1799.
43. Xing L., Tikoo S.K. Characterization of cis-acting sequences involved in packaging porcine adenovirus type 3. Virology 2003, 314:650-661.
44. Xing L., Tikoo S.K. E1A promoter of bovine adenovirus type 3. J. Gen. Virol. 2006, 87:3539-3544.
45. Xing L., Tikoo S.K. Bovine adenovirus-3 E1A coding region contain cis-acting DNA packaging motifs. Virus Res. 2007, 130:315-320.
46. Yokoya F., Imamoto N., Tachibana T., Yoneda Y. Beta-catenin can be transported into the nucleus in a Ran-unassisted manner. Mol. Biol. Cell 1999, 10:1119-1131.
47. Zakhartchouk A.N., Pyne C., Mutwiri G.K., Papp Z., Baca-Estrada M.E., Griebel P., Babiuk L.A., Tikoo S.K. Mucosal immunization of calves with recombinant bovine adenovirus-3: induction of protective immunity to bovine herpesvirus-1. J. Gen. Virol. 1999, 80:1263-1269.