APOBEC3G inhibits microRNA-mediated repression of translation by interfering with the interaction between Argonaute-2 and MOV10

Journal of Biological Chemistry

Volumn 287, Issue 35, 2012, Pages 29373-29383

  Liu, Chao ^a   Zhang, Xue ^a   Huang, Feng ^a   Yang, Bin ^b   Li, Jun ^a   Liu, Bingfeng ^a   Luo, Haihua ^a   Zhang, Ping ^a   Zhang, Hui ^a,b  

^a SUN YAT SEN UNIVERSITY   (China)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C TERMINUS; CELLULAR FUNCTION; CYTIDINE DEAMINASE; HUMAN IMMUNODEFICIENCY VIRUS TYPE-1; MICRORNA (MIRNA); SMALL RNA;

ASSOCIATION REACTIONS; DISEASES; ONCOGENIC VIRUSES;

RNA;

7SL RNA; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; ARGONAUTE 2 PROTEIN; CARBOXY TERMINAL TELOPEPTIDE; INTERFERON; MICRORNA; MICRORNA INDUCED SILENCING COMPLEX; MOLONEY LEUKEMIA VIRUS 10 PROTEIN; RNA INDUCED SILENCING COMPLEX; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; GENE DELETION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLONEY LEUKEMIA ONCOVIRUS; MOLONEY LEUKEMIA VIRUS 10; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RETROVIRUS; RNA ANALYSIS; RNA TRANSLATION;

ARGONAUTE PROTEINS; CYTIDINE DEAMINASE; HIV-1; HUMANS; MICRORNAS; PROTEIN BIOSYNTHESIS; RNA HELICASES; RNA, SMALL CYTOPLASMIC; SIGNAL RECOGNITION PARTICLE;

HUMAN IMMUNODEFICIENCY VIRUS 1; MOLONEY MURINE LEUKEMIA VIRUS;

EID: 84865473920     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.354001     Document Type: Article

References (44)

1. Ambros, V., and Chen, X. (2007) The regulation of genes and genomes by small RNAs. Development 134, 1635-1641
2. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
3. Rana, T. M. (2007) Illuminating the silence: understanding the structure and function of small RNAs. Nat. Rev. Mol. Cell Biol. 8, 23-36
4. Carmell, M. A., Xuan, Z., Zhang, M. Q., and Hannon, G. J. (2002) The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16, 2733-2742
5. Caudy, A. A., Myers, M., Hannon, G. J., and Hammond, S. M. (2002) Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16, 2491-2496
6. Gregory, R. I., Chendrimada, T. P., Cooch, N., and Shiekhattar, R. (2005) Human RISC couples microRNA biogenesis and post-transcriptional gene silencing. Cell 123, 631-640
7. Liu, J., Carmell, M. A., Rivas, F. V., Marsden, C. G., Thomson, J. M., Song, J. J., Hammond, S. M., Joshua-Tor, L., and Hannon, G. J. (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305, 1437-1441
8. Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G., and Tuschl, T. (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15, 185-197
9. Meister, G., Landthaler, M., Peters, L., Chen, P. Y., Urlaub, H., Lührmann, R., and Tuschl, T. (2005) Identification of novel argonaute-associated proteins. Curr. Biol. 15, 2149-2155
10. Chiu, Y. L., Witkowska, H. E., Hall, S. C., Santiago, M., Soros, V. B., Esnault, C., Heidmann, T., and Greene, W. C. (2006) High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition. Proc. Natl. Acad. Sci. U.S.A. 103, 15588-15593
11. Gallois-Montbrun, S., Kramer, B., Swanson, C. M., Byers, H., Lynham, S., Ward, M., and Malim, M. H. (2007) Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J. Virol. 81, 2165-2178
12. Huang, J., Liang, Z., Yang, B., Tian, H., Ma, J., and Zhang, H. (2007) Derepression of microRNA-mediated protein translation inhibition by apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3G (APOBEC3G) and its family members. J. Biol. Chem. 282, 33632-33640
13. Kozak, S. L., Marin, M., Rose, K. M., Bystrom, C., and Kabat, D. (2006) The anti-HIV-1 editing enzyme APOBEC3G binds HIV-1 RNA and messenger RNAs that shuttle between polysomes and stress granules. J. Biol. Chem. 281, 29105-29119
14. Wichroski, M. J., Robb, G. B., and Rana, T. M. (2006) Human retroviral host restriction factors APOBEC3G and APOBEC3F localize to mRNA processing bodies. PLoS Pathog. 2, e41
15. Zhang, H., Yang, B., Pomerantz, R. J., Zhang, C., Arunachalam, S. C., and Gao, L. (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424, 94-98
16. Zhang, H., Dornadula, G., Alur, P., Laughlin, M. A., and Pomerantz, R. J. (1996) Amphipathic domains in the C terminus of the transmembrane protein (gp41) permeabilize HIV-1 virions: a molecular mechanism underlying natural endogenous reverse transcription. Proc. Natl. Acad. Sci. U.S.A. 93, 12519-12524
17. Pei, Y., Wang, X., and Zhang, X. (2009) Predicting the fate of microRNA target genes based on sequence features. J. Theor. Biol. 261, 17-22
18. Kumar, M., Lu, Z., Takwi, A. A., Chen, W., Callander, N. S., Ramos, K. S., Young, K. H., and Li, Y. (2011) Negative regulation of the tumor suppressor p53 gene by microRNAs. Oncogene 30, 843-853
19. Lakkaraju, A. K., Luyet, P. P., Parone, P., Falguières, T., and Strub, K. (2007) Inefficient targeting to the endoplasmic reticulum by the signal recognition particle elicits selective defects in post-ER membrane trafficking. Exp. Cell Res. 313, 834-847
20. Lakkaraju, A. K., Mary, C., Scherrer, A., Johnson, A. E., and Strub, K. (2008) SRP keeps polypeptides translocation-competent by slowing translation to match limiting ER-targeting sites. Cell 133, 440-451
21. Peng, G., Lei, K. J., Jin, W., Greenwell-Wild, T., and Wahl, S. M. (2006) Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J. Exp. Med. 203, 41-46
22. Yang, S., Sun, Y., and Zhang, H. (2001) The multimerization of human immunodeficiency virus type I Vif protein: a requirement for Vif function in the viral life cycle. J. Biol. Chem. 276, 4889-4893
23. Wang, T., Tian, C., Zhang, W., Luo, K., Sarkis, P. T., Yu, L., Liu, B., Yu, Y., and Yu, X. F. (2007) 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J. Virol. 81, 13112-13124
24. Bach, D., Peddi, S., Mangeat, B., Lakkaraju, A., Strub, K., and Trono, D. (2008) Characterization of APOBEC3G binding to 7SL RNA. Retrovirology 5, 54
25. Mary, C., Scherrer, A., Huck, L., Lakkaraju, A. K., Thomas, Y., Johnson, A. E., and Strub, K. (2010) Residues in SRP9/14 essential for elongation arrest activity of the signal recognition particle define a positively charged functional domain on one side of the protein. Rna 16, 969-979
26. Moore, M. J. (2005) From birth to death: the complex lives of eukaryotic mRNAs. Science 309, 1514-1518
27. Wolin, S. L., and Steitz, J. A. (1983) Genes for two small cytoplasmic Ro RNAs are adjacent and appear to be single-copy in the human genome. Cell 32, 735-744
28. Tian, C., Wang, T., Zhang, W., and Yu, X. F. (2007) Virion packaging determinants and reverse transcription of SRP RNA in HIV-1 particles. Nucleic Acids Res. 35, 7288-7302
29. Tomari, Y., Du, T., Haley, B., Schwarz, D. S., Bennett, R., Cook, H. A., Koppetsch, B. S., Theurkauf, W. E., and Zamore, P. D. (2004) RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 116, 831-841
30. Eystathioy, T., Chan, E. K., Tenenbaum, S. A., Keene, J. D., Griffith, K., and Fritzler, M. J. (2002) A phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol. Biol. Cell 13, 1338-1351
31. Eystathioy, T., Jakymiw, A., Chan, E. K., Séraphin, B., Cougot, N., and Fritzler, M. J. (2003) The GW182 protein colocalizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies. Rna 9, 1171-1173
32. Liu, J., Rivas, F. V., Wohlschlegel, J., Yates, J. R., 3rd, Parker, R., and Hannon, G. J. (2005) A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7, 1261-1266
33. Behm-Ansmant, I., Rehwinkel, J., Doerks, T., Stark, A., Bork, P., and Izaurralde, E. (2006) mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 20, 1885-1898
34. Gehring, N. H., Neu-Yilik, G., Schell, T., Hentze, M. W., and Kulozik, A. E. (2003) Y14 and hUpf3b form an NMD-activating complex. Mol. Cell 11, 939-949
35. Pillai, R. S., Artus, C. G., and Filipowicz, W. (2004) Tethering of human Ago proteins to mRNA mimics the miRNA-mediated repression of protein synthesis. Rna 10, 1518-1525
36. Haase, A. D., Fenoglio, S., Muerdter, F., Guzzardo, P. M., Czech, B., Pappin, D. J., Chen, C., Gordon, A., and Hannon, G. J. (2010) Probing the initiation and effector phases of the somatic piRNA pathway in Drosophila. Genes Dev. 24, 2499-2504
37. Zamore, P. D. (2010) Somatic piRNA biogenesis. EMBO J. 29, 3219-3221
38. Burdick, R., Smith, J. L., Chaipan, C., Friew, Y., Chen, J., Venkatachari, N. J., Delviks-Frankenberry, K. A., Hu, W. S., and Pathak, V. K. (2010) P body-associated protein Mov10 inhibits HIV-1 replication at multiple stages. J. Virol. 84, 10241-10253
39. Furtak, V., Mulky, A., Rawlings, S. A., Kozhaya, L., Lee, K., Kewalramani, V. N., and Unutmaz, D. (2010) Perturbation of the P-body component Mov10 inhibits HIV-1 infectivity. PLoS One 5, e9081
40. Wang, X., Han, Y., Dang, Y., Fu, W., Zhou, T., Ptak, R. G., and Zheng, Y. H. (2010) Moloney leukemia virus 10 (MOV10) protein inhibits retrovirus replication. J. Biol. Chem. 285, 14346-14355
41. Cook, H. A., Koppetsch, B. S., Wu, J., and Theurkauf, W. E. (2004) The Drosophila SDE3 homolog armitage is required for oskar mRNA silencing and embryonic axis specification. Cell 116, 817-829
42. Lim, A. K., and Kai, T. (2007) Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 104, 6714-6719
43. Ashraf, S. I., McLoon, A. L., Sclarsic, S. M., and Kunes, S. (2006) Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124, 191-205
44. Chendrimada, T. P., Finn, K. J., Ji, X., Baillat, D., Gregory, R. I., Liebhaber, S. A., Pasquinelli, A. E., and Shiekhattar, R. (2007) MicroRNA silencing through RISC recruitment of eIF6. Nature 447, 823-828