Importin α-mediated nuclear import of cytoplasmic Poly(A) binding protein occurs as a direct consequence of cytoplasmic mRNA depletion

Molecular and Cellular Biology

Volumn 31, Issue 15, 2011, Pages 3113-3125

  Renuka Kumar, G ^a   Shum, Leona ^a   Glaunsinger, Britt A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTIC POLYPEPTIDE CHAIN RELEASING FACTOR 3; INITIATION FACTOR 4F; INITIATION FACTOR 4G; KARYOPHERIN ALPHA; MESSENGER RNA; MUTANT PROTEIN; PAIP1 PROTEIN; PAIP2A PROTEIN; POLYADENYLATED RNA; POLYADENYLIC ACID BINDING PROTEIN; POLYPEPTIDE; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR SOX; UNCLASSIFIED DRUG; VIRION HOST SHUTOFF PROTEIN; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOPLASM; FEMALE; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR IMPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA METABOLISM;

ACTIVE TRANSPORT, CELL NUCLEUS; ALPHA KARYOPHERINS; ANIMALS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOPLASM; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNOPRECIPITATION; PLASMIDS; POLY(A)-BINDING PROTEIN I; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; VIRAL PROTEINS;

EID: 79960328660     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05402-11     Document Type: Article

References (79)

1. Adam, S. A., T. Nakagawa, M. S. Swanson, T. K. Woodruff, and G. Dreyfuss. 1986. mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol. Cell. Biol. 6:2932-2943.
2. Afonina, E., R. Stauber, and G. N. Pavlakis. 1998. The human poly(A)-binding protein 1 shuttles between the nucleus and the cytoplasm. J. Biol. Chem. 273:13015-13021.
3. Akerfelt, M., R. I. Morimoto, and L. Sistonen. 2010. Heat shock factors: integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell Biol. 11:545-555.
4. Bag, J. 2001. Feedback inhibition of poly(A)-binding protein mRNA translation. A possible mechanism of translation arrest by stalled 40 S ribosomal subunits. J. Biol. Chem. 276:47352-47360.
5. Bechtel, J. T., Y. Liang, J. Hvidding, and D. Ganem. 2003. Host range of Kaposi's sarcoma-associated herpesvirus in cultured cells. J. Virol. 77:6474-6481.
6. Behm-Ansmant, I., D. Gatfield, J. Rehwinkel, V. Hilgers, and E. Izaurralde. 2007. A conserved role for cytoplasmic poly(A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA decay. EMBO J. 26:1591-1601.
7. Blakqori, G., I. van Knippenberg, and R. M. Elliott. 2009. Bunyamwera orthobunyavirus S-segment untranslated regions mediate poly(A) tail-independent translation. J. Virol. 83:3637-3646.
8. Blanco, P., et al. 2001. A novel poly(A)-binding protein gene (PABPC5) maps to an X-specific subinterval in the Xq21.3/Yp11.2 homology block of the human sex chromosomes. Genomics 74:1-11.
9. Brune, C., S. E. Munchel, N. Fischer, A. V. Podtelejnikov, and K. Weis. 2005. Yeast poly(A)-binding protein Pab1 shuttles between the nucleus and the cytoplasm and functions in mRNA export. RNA 11:517-531.
10. Burd, C. G., E. L. Matunis, and G. Dreyfuss. 1991. The multiple RNAbinding domains of the mRNA poly(A)-binding protein have different RNAbinding activities. Mol. Cell. Biol. 11:3419-3424.
11. Cassola, A., and A. C. Frasch. 2009. An RNA recognition motif mediates the nucleocytoplasmic transport of a trypanosome RNA-binding protein. J. Biol. Chem. 284:35015-35028.
12. Cassola, A., G. Noe, and A. C. Frasch. 2010. RNA recognition motifs involved in nuclear import of RNA-binding proteins. RNA Biol. 7:339-344.
13. Cosson, B., et al. 2002. Poly(A)-binding protein and eRF3 are associated in vivo in human and Xenopus cells. Biol. Cell 94:205-216.
14. Covarrubias, S., J. M. Richner, K. Clyde, Y. J. Lee, and B. A. Glaunsinger. 2009. Host shutoff is a conserved phenotype of gammaherpesvirus infection and is orchestrated exclusively from the cytoplasm. J. Virol. 83:9554-9566.
15. Craig, A. W., A. Haghighat, A. T. Yu, and N. Sonenberg. 1998. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature 392:520-523.
16. Deakin, N. O., and C. E. Turner. 2008. Paxillin comes of age. J. Cell Sci. 121:2435-2444.
17. de Melo Neto, O. P., N. Standart, and C. Martins de Sa. 1995. Autoregulation of poly(A)-binding protein synthesis in vitro. Nucleic Acids Res. 23: 2198-2205.
18. Doller, A., J. Pfeilschifter, and W. Eberhardt. 2008. Signalling pathways regulating nucleo-cytoplasmic shuttling of the mRNA-binding protein HuR. Cell Signal. 20:2165-2173.
19. D'Orso, I., and A. C. Frasch. 2002. TcUBP-1, an mRNA destabilizing factor from trypanosomes, homodimerizes and interacts with novel AU-rich element-and poly(A)-binding proteins forming a ribonucleoprotein complex. J. Biol. Chem. 277:50520-50528.
20. Eberle, A. B., L. Stalder, H. Mathys, R. Z. Orozco, and O. Muhlemann. 2008. Posttranscriptional gene regulation by spatial rearrangement of the 3' untranslated region. PLoS Biol. 6:e92.
21. Everly, D. N., Jr., P. Feng, I. S. Mian, and G. S. Read. 2002. mRNA degradation by the virion host shutoff (Vhs) protein of herpes simplex virus: genetic and biochemical evidence that Vhs is a nuclease. J. Virol. 76:8560-8571.
22. Ezzeddine, N., et al. 2007. Human TOB, an antiproliferative transcription factor, is a poly(A)-binding protein-dependent positive regulator of cytoplasmic mRNA deadenylation. Mol. Cell. Biol. 27:7791-7801.
23. Fabian, M. R., et al. 2009. Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol. Cell 35:868-880.
24. Feral, C., G. Guellaen, and A. Pawlak. 2001. Human testis expresses a specific poly(A)-binding protein. Nucleic Acids Res. 29:1872-1883.
25. Glaunsinger, B., L. Chavez, and D. Ganem. 2005. The exonuclease and host shutoff functions of the SOX protein of Kaposi's sarcoma-associated herpesvirus are genetically separable. J. Virol. 79:7396-7401.
26. Glaunsinger, B., and D. Ganem. 2004. Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol. Cell 13:713-723.
27. Gorlach, M., C. G. Burd, and G. Dreyfuss. 1994. The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp. Cell Res. 211:400-407.
28. Harb, M., et al. 2008. Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN. J. Virol. 82:11283-11293.
29. Hayden, M. S., and S. Ghosh. 2008. Shared principles in NF-kappaB signaling. Cell 132:344-362.
30. Hayden, M. S., and S. Ghosh. 2004. Signaling to NF-kappaB. Genes Dev. 18:2195-2224.
31. Hoshino, S., M. Imai, T. Kobayashi, N. Uchida, and T. Katada. 1999. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3'-poly(A) tail of mRNA. Direct association of erf3/GSPT with polyadenylate-binding protein. J. Biol. Chem. 274:16677-16680.
32. Hosoda, N., F. Lejeune, and L. E. Maquat. 2006. Evidence that poly(A) binding protein C1 binds nuclear pre-mRNA poly(A) tails. Mol. Cell. Biol. 26:3085-3097.
33. Imataka, H., A. Gradi, and N. Sonenberg. 1998. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 17:7480-7489.
34. Ivanov, P. V., N. H. Gehring, J. B. Kunz, M. W. Hentze, and A. E. Kulozik. 2008. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 27:736-747.
35. Jones, F. E., C. A. Smibert, and J. R. Smiley. 1995. Mutational analysis of the herpes simplex virus virion host shutoff protein: evidence that vhs functions in the absence of other viral proteins. J. Virol. 69:4863-4871.
36. Kamitani, W., C. Huang, K. Narayanan, K. G. Lokugamage, and S. Makino. 2009. A two-pronged strategy to suppress host protein synthesis by SARS coronavirus Nsp1 protein. Nat. Struct. Mol. Biol. 16:1134-1140.
37. Kamitani, W., et al. 2006. Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc. Natl. Acad. Sci. U. S. A. 103:12885-12890.
38. Karim, M. M., et al. 2006. A mechanism of translational repression by competition of Paip2 with eIF4G for poly(A) binding protein (PABP) binding. Proc. Natl. Acad. Sci. U. S. A. 103:9494-9499.
39. Khaleghpour, K., et al. 2001. Dual interactions of the translational repressor Paip2 with poly(A) binding protein. Mol. Cell. Biol. 21:5200-5213.
40. Khaleghpour, K., et al. 2001. Translational repression by a novel partner of human poly(A) binding protein, Paip2. Mol. Cell 7:205-216.
41. Kuhn, U., and T. Pieler. 1996. Xenopus poly(A) binding protein: functional domains in RNA binding and protein-protein interaction. J. Mol. Biol. 256: 20-30.
42. Kuhn, U., and E. Wahle. 2004. Structure and function of poly(A) binding proteins. Biochim. Biophys. Acta 1678:67-84.
43. Kumar, G. R., and B. A. Glaunsinger. 2010. Nuclear import of cytoplasmic poly(A) binding protein restricts gene expression via hyperadenylation and nuclear retention of mRNA. Mol. Cell. Biol. 30:4996-5008.
44. Kumar, K. P., K. M. McBride, B. K. Weaver, C. Dingwall, and N. C. Reich. 2000. Regulated nuclear-cytoplasmic localization of interferon regulatory factor 3, a subunit of double-stranded RNA-activated factor 1. Mol. Cell. Biol. 20:4159-4168.
45. Lange, A., et al. 2007. Classical nuclear localization signals: definition, function, and interaction with importin alpha. J. Biol. Chem. 282:5101-5105.
46. Lee, Y. J., and B. A. Glaunsinger. 2009. Aberrant herpesvirus-induced polyadenylation correlates with cellular mRNA destruction. PLoS Biol. 7:e1000107.
47. Liang, S. H., and M. F. Clarke. 1999. A bipartite nuclear localization signal is required for p53 nuclear import regulated by a carboxyl-terminal domain. J. Biol. Chem. 274:32699-32703.
48. Liang, S. H., and M. F. Clarke. 2001. Regulation of p53 localization. Eur. J. Biochem. 268:2779-2783.
49. Ma, S., R. B. Bhattacharjee, and J. Bag. 2009. Expression of poly(A)-binding protein is upregulated during recovery from heat shock in HeLa cells. FEBS J. 276:552-570.
50. Madrid, A. S., and K. Weis. 2006. Nuclear transport is becoming crystal clear. Chromosoma 115:98-109.
51. Mangus, D. A., M. C. Evans, and A. Jacobson. 2003. Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4:223.
52. Melo, E. O., R. Dhalia, C. Martins de Sa, N. Standart, and O. P. de Melo Neto. 2003. Identification of a C-terminal poly(A)-binding protein (PABP)-PABP interaction domain: role in cooperative binding to poly(A) and efficient cap distal translational repression. J. Biol. Chem. 278:46357-46368.
53. O'Brate, A., and P. Giannakakou. 2003. The importance of p53 location: nuclear or cytoplasmic zip code? Drug Resist. Updat. 6:313-322.
54. Peng, S. S., C. Y. Chen, N. Xu, and A. B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17:3461-3470.
55. Reich, N. C. 2002. Nuclear/cytoplasmic localization of IRFs in response to viral infection or interferon stimulation. J. Interferon Cytokine Res. 22:103-109.
56. Richner, J., et al. Global mRNA degradation during lytic gammaherpesvirus infection contributes to establishment of viral latency. PLoS Pathog., in press.
57. Richter, K., M. Haslbeck, and J. Buchner. 2010. The heat shock response: life on the verge of death. Mol. Cell 40:253-266.
58. Rosenblum, J. S., L. F. Pemberton, and G. Blobel. 1997. A nuclear import pathway for a protein involved in tRNA maturation. J. Cell Biol. 139:1655-1661.
59. Rosenblum, J. S., L. F. Pemberton, N. Bonifaci, and G. Blobel. 1998. Nuclear import and the evolution of a multifunctional RNA-binding protein. J. Cell Biol. 143:887-899.
60. Roy, G., et al. 2002. Paip1 interacts with poly(A) binding protein through two independent binding motifs. Mol. Cell. Biol. 22:3769-3782.
61. Sachs, A. B., M. W. Bond, and R. D. Kornberg. 1986. A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell 45:827-835.
62. Sachs, A. B., R. W. Davis, and R. D. Kornberg. 1987. A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol. Cell. Biol. 7:3268-3276.
63. Saffran, H. A., G. S. Read, and J. R. Smiley. 2010. Evidence for translational regulation by the herpes simplex virus virion host shutoff protein. J. Virol. 84:6041-6049.
64. Salaun, C., et al. 2010. Poly(A)-binding protein 1 partially relocalizes to the nucleus during herpes simplex virus type 1 infection in an ICP27-independent manner and does not inhibit virus replication. J. Virol. 84:8539-8548.
65. Sarkar, N. 1997. Polyadenylation of mRNA in prokaryotes. Annu. Rev. Biochem. 66:173-197.
66. Schek, N., and S. L. Bachenheimer. 1985. Degradation of cellular mRNAs induced by a virion-associated factor during herpes simplex virus infection of Vero cells. J. Virol. 55:601-610.
67. Servant, M. J., B. Tenoever, and R. Lin. 2002. Overlapping and distinct mechanisms regulating IRF-3 and IRF-7 function. J. Interferon Cytokine Res. 22:49-58.
68. Simeonidis, S., D. Stauber, G. Chen, W. A. Hendrickson, and D. Thanos. 1999. Mechanisms by which IkappaB proteins control NF-kappaB activity. Proc. Natl. Acad. Sci. U. S. A. 96:49-54.
69. Sorokin, A. V., E. R. Kim, and L. P. Ovchinnikov. 2007. Nucleocytoplasmic transport of proteins. Biochemistry (Mosc.) 72:1439-1457.
70. Strom, T., and N. Frenkel. 1987. Effects of herpes simplex virus on mRNA stability. J. Virol. 61:2198-2207.
71. Terry, L. J., E. B. Shows, and S. R. Wente. 2007. Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport. Science 318:1412-1416.
72. Vujanac, M., A. Fenaroli, and V. Zimarino. 2005. Constitutive nuclear import and stress-regulated nucleocytoplasmic shuttling of mammalian heatshock factor 1. Traffic 6:214-229.
73. Wagner, E., S. L. Clement, and J. Lykke-Andersen. 2007. An unconventional human Ccr4-Caf1 deadenylase complex in nuclear Cajal bodies. Mol. Cell. Biol. 27:1686-1695.
74. Wells, S. E., P. E. Hillner, R. D. Vale, and A. B. Sachs. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell 2:135-140.
75. Woods, A. J., T. Kantidakis, H. Sabe, D. R. Critchley, and J. C. Norman. 2005. Interaction of paxillin with poly(A)-binding protein 1 and its role in focal adhesion turnover and cell migration. Mol. Cell. Biol. 25:3763-3773.
76. Woods, A. J., et al. 2002. Paxillin associates with poly(A)-binding protein 1 at the dense endoplasmic reticulum and the leading edge of migrating cells. J. Biol. Chem. 277:6428-6437.
77. Wu, J., and J. Bag. 1998. Negative control of the poly(A)-binding protein mRNA translation is mediated by the adenine-rich region of its 5'-untranslated region. J. Biol. Chem. 273:34535-34542.
78. Yamashita, A., et al. 2005. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat. Struct. Mol. Biol. 12:1054-1063.
79. Yang, H., C. S. Duckett, and T. Lindsten. 1995. iPABP, an inducible poly(A)-binding protein detected in activated human T cells. Mol. Cell. Biol. 15: 6770-6776.