Inducible APOBEC3G-Vif double stable cell line as a high-throughput screening platform to identify antiviral compounds

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 1, 2010, Pages 78-87

  Nowotny, Boris ^a   Schneider, Thomas ^b   Pradel, Gabriele ^a   Schirmeister, Tanja ^b   Rethwilm, Axel ^a   Kirschner, Marc ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b Institute of Pharmacy and Food Chemistry   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; CYTIDINE DEAMINASE; DOXYCYCLINE; HYBRID PROTEIN; PROTEASOME; RN 18; UBIQUITIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; YELLOW FLUORESCENT PROTEIN;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; TRANSGENE; UBIQUITINATION; UPREGULATION; VIRION;

ANTI-BACTERIAL AGENTS; ANTI-HIV AGENTS; ANTIVIRAL AGENTS; BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE; COST-BENEFIT ANALYSIS; CULTURE MEDIA; CYTIDINE DEAMINASE; DNA, VIRAL; DOXYCYCLINE; DRUG EVALUATION, PRECLINICAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME INDUCTION; FLOW CYTOMETRY; FLUORESCENT DYES; GENE EXPRESSION REGULATION, VIRAL; GENETIC VECTORS; HUMANS; LENTIVIRUS; MOLECULAR SEQUENCE DATA; PLASMIDS; REPRODUCIBILITY OF RESULTS; TRANSFECTION;

EID: 73849140020     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00775-09     Document Type: Article

References (52)

1. Alce, T. M., and W. Popik. 2004. APOBEC3G is incorporated into virus-like particles by a direct interaction with HIV-1 Gag nucleocapsid protein. J. Biol. Chem. 279:34083-34086.
2. Beckham, C. J., and R. Parker. 2008. P bodies, stress granules, and viral life cycles. Cell Host Microbe 3:206-212.
3. Bishop, K. N., R. K. Holmes, and M. H. Malim. 2006. Antiviral potency of APOBEC proteins does not correlate with cytidine deamination. J. Virol. 80:8450-8458.
4. Bishop, K. N., R. K. Holmes, A. M. Sheehy, N. O. Davidson, S. J. Cho, and M. H. Malim. 2004. Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr. Biol. 14:1392-1396.
5. Carter, R. E., and A. Sorkin. 1998. Endocytosis of functional epidermal growth factor receptor-green fluorescent protein chimera. J. Biol. Chem. 273:35000-35007.
6. Cen, S., F. Guo, M. Niu, J. Saadatmand, J. Deflassieux, and L. Kleiman. 2004. The interaction between HIV-1 Gag and APOBEC3G. J. Biol. Chem. 279:33177-33184.
7. Conticello, S. G., R. S. Harris, and M. S. Neuberger. 2003. The Vif Protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr. Biol. 13:2009-2013.
8. Cowan, S., T. Hatziioannou, T. Cunningham, M. A. Muesing, H. G. Gottlinger, and P. D. Bieniasz. 2002. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc. Natl. Acad. Sci. U. S. A. 99:11914-11919.
9. Cullen, B. R. 1991. Regulation of HIV-1 gene expression. FASEB J. 5:2361-2368.
10. Cullen, B. R. 2006. Role and mechanism of action of the APOBEC3 family of antiretroviral resistance factors. J. Virol. 80:1067-1076.
11. Cullen, B. R., and W. C. Greene. 1990. Functions of the auxiliary gene products of the human immunodeficiency virus type 1. Virology 178:1-5.
12. De Clercq, E. 2009. Anti-HIV drugs: 25 compounds approved within 25 years after the discovery of HIV. Int. J. Antimicrob. Agents 33:307-320.
13. Gallois-Montbrun, S., B. Kramer, C. M. Swanson, H. Byers, S. Lynham, M. Ward, and M. H. Malim. 2007. Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J. Virol. 81:2165-2178.
14. Goila-Gaur, R., and K. Strebel. 2008. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 5:51.
15. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. U. S. A. 89:5547-5551.
16. Greene, W. C., Z. Debyser, Y. Ikeda, E. O. Freed, E. Stephens, W. Yonemoto, R. W. Buckheit, J. A. Este, and T. Cihlar. 2008. Novel targets for HIV therapy. Antivir. Res. 80:251-265.
17. Han, Y., X. Wang, Y. Dang, and Y. H. Zheng. 2008. APOBEC3G and APOBEC3F require an endogenous cofactor to block HIV-1 replication. PLoS Pathog 4:e1000095.
18. Harris, R. S., K. N. Bishop, A. M. Sheehy, H. M. Craig, S. K. Petersen-Mahrt, I. N. Watt, M. S. Neuberger, and M. H. Malim. 2003. DNA deamination mediates innate immunity to retroviral infection. Cell 113:803-809.
19. Iwatani, Y., D. S. Chan, F. Wang, K. S. Maynard, W. Sugiura, A. M. Gronenborn, I. Rouzina, M. C. Williams, K. Musier-Forsyth, and J. G. Levin. 2007. Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res. 35:7096-7108.
20. Izumi, T., K. Shirakawa, and A. Takaori-Kondo. 2008. Cytidine deaminases as a weapon against retroviruses and a new target for antiviral therapy. Mini Rev. Med. Chem. 8:231-238.
21. Kerppola, T. K. 2006. Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat. Protoc. 1:1278-1286.
22. Kieffer, T. L., P. Kwon, R. E. Nettles, Y. Han, S. C. Ray, and R. F. Siliciano. 2005. G → A hypermutation in protease and reverse transcriptase regions of human immunodeficiency virus type 1 residing in resting CD4+ T cells in vivo. J. Virol. 79:1975-1980.
23. Kirschner, M., V. Monrose, M. Paluch, N. Techodamrongsin, A. Rethwilm, and J. P. Moore. 2006. The production of cleaved, trimeric human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein vaccine antigens and infectious pseudoviruses using linear polyethylenimine as a transfection reagent. Protein Expr. Purif. 48:61-68.
24. Kobayashi, M., A. Takaori-Kondo, Y. Miyauchi, K. Iwai, and T. Uchiyama. 2005. Ubiquitination of APOBEC3G by an HIV-1 Vif-Cullin5-Elongin BElongin C complex is essential for Vif function. J. Biol. Chem. 280:18573-18578.
25. Kootstra, N. A., C. Munk, N. Tonnu, N. R. Landau, and I. M. Verma. 2003. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc. Natl. Acad. Sci. U. S. A. 100:1298-1303.
26. Leurs, C., M. Jansen, K. E. Pollok, M. Heinkelein, M. Schmidt, M. Wissler, D. Lindemann, C. Von Kalle, A. Rethwilm, D. A. Williams, and H. Hanenberg. 2003. Comparison of three retroviral vector systems for transduction of nonobese diabetic/severe combined immunodeficiency mice repopulating human CD34+ cord blood cells. Hum. Gene Ther. 14:509-519.
27. Levy, J. A. 2006. HIV pathogenesis: knowledge gained after two decades of research. Adv. Dent. Res. 19:10-16.
28. Li, X.-Y., F. Guo, L. Zhang, L. Kleiman, and S. Cen. 2007. APOBEC3G inhibits DNA strand transfer during HIV-1 reverse transcription. J. Biol. Chem. 282:32065-32074.
29. Liddament, M. T., W. L. Brown, A. J. Schumacher, and R. S. Harris. 2004. APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr. Biol. 14:1385-1391.
30. Luo, K., T. Wang, B. Liu, C. Tian, Z. Xiao, J. Kappes, and X.-F. Yu. 2007. Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. J. Virol. 81:7238-7248.
31. Lv, W., Z. Liu, H. Jin, X. Yu, and L. Zhang. 2007. Three-dimensional structure of HIV-1 VIF constructed by comparative modeling and the function characterization analyzed by molecular dynamics simulation. Org. Biomol. Chem. 5:617-626.
32. Malim, M. H. 2006. Natural resistance to HIV infection: the Vif-APOBEC interaction. C. R. Biol. 329:871-875.
33. Mangeat, B., P. Turelli, G. Caron, M. Friedli, L. Perrin, and D. Trono. 2003. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424:99-103.
34. Marin, M., K. M. Rose, S. L. Kozak, and D. Kabat. 2003. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 9:1398-1403.
35. Nathans, R., H. Cao, N. Sharova, A. Ali, M. Sharkey, R. Stranska, M. Stevenson, and T. M. Rana. 2008. Small-molecule inhibition of HIV-1 Vif. Nat. Biotechnol. 26:1187-1192.
36. Nguyen, D. H., S. Gummuluru, and J. Hu. 2007. Deamination- independent inhibition of hepatitis B virus reverse transcription by APOBEC3G. J. Virol. 81:4465-4472.
37. Owens, C. M., P. C. Yang, H. Gottlinger, and J. Sodroski. 2003. Human and simian immunodeficiency virus capsid proteins are major viral determinants of early, postentry replication blocks in simian cells. J. Virol. 77:726-731.
38. Rana, T. M. 19 April 2007. Composition and synthesis of new reagents for inhibition of HIV replication. IPC patent A61K 31/42 (2006.01), C07D 263/02 (2006.01). WIPO publication WO/2007/044565.
39. Sheehy, A. M., N. C. Gaddis, J. D. Choi, and M. H. Malim. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650.
40. Sheehy, A. M., N. C. Gaddis, and M. H. Malim. 2003. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat. Med. 9:1404-1407.
41. Soros, V. B., W. Yonemoto, and W. C. Greene. 2007. Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA, and subsequently activated by RNase H. PLoS Pathog. 3:e15.
42. Stopak, K., C. de Noronha, W. Yonemoto, and W. C. Greene. 2003. HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol. Cell 12:591-601.
43. Stremlau, M., C. M. Owens, M. J. Perron, M. Kiessling, P. Autissier, and J. Sodroski. 2004. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427:848-853.
44. Turelli, P., B. Mangeat, S. Jost, S. Vianin, and D. Trono. 2004. Inhibition of hepatitis B virus replication by APOBEC3G. Science 303:1829.
45. Wichroski, M. J., K. Ichiyama, and T. M. Rana. 2005. Analysis of HIV-1 viral infectivity factor-mediated proteasome-dependent depletion of APOB EC3G: correlating function and subcellular localization. J. Biol. Chem. 280: 8387-8396.
46. Wichroski, M. J., G. B. Robb, and T. M. Rana. 2006. Human retroviral host restriction factors APOBEC3G and APOBEC3F localize to mRNA processing bodies. PLoS Pathog. 2:e41.
47. Xu, H., E. Chertova, J. Chen, D. E. Ott, J. D. Roser, W.-S. Hu, and V. K. Pathak. 2007. Stoichiometry of the antiviral protein APOBEC3G in HIV-1 virions. Virology 360:247-256.
48. Yu, X., Y. Yu, B. Liu, K. Luo, W. Kong, P. Mao, and X.-F. Yu. 2003. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302:1056-1060.
49. Zennou, V., D. Perez-Caballero, H. Gottlinger, and P. D. Bieniasz. 2004. APOBEC3G incorporation into human immunodeficiency virus type 1 particles. J. Virol. 78:12058-12061.
50. Zhang, H., B. Yang, R. J. Pomerantz, C. Zhang, S. C. Arunachalam, and L. Gao. 2003. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424:94-98.
51. Zhang, J., D. T. Scadden, and C. S. Crumpacker. 2007. Primitive hematopoietic cells resist HIV-1 infection via p21. J. Clin. Invest. 117:473-481.
52. Zhang, J. H., T. D. Chung, and K. R. Oldenburg. 1999. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen. 4:67-73.