Caffeine inhibits human immunodeficiency virus type 1 transduction of nondividing cells

Journal of Virology

Volumn 79, Issue 4, 2005, Pages 2058-2065

  Daniel, René ^a   Marusich, Elena ^a   Argyris, Elias ^a   Zhao, Richard Y ^c   Skalka, Anna Marie ^b   Pomerantz, Roger J ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; CAFFEINE; NOCODAZOLE; PROTEIN KINASE; VIRUS PROTEIN; VIRUS VECTOR; VPR PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL GROWTH; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME INHIBITION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MACROPHAGE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; TARGET CELL;

CAFFEINE; CELL CYCLE PROTEINS; CELL LINE; GENETIC VECTORS; HIV-1; HUMANS; TRANSDUCTION, GENETIC; VIRUS INTEGRATION;

ANIMALIA; ATAXIA; ATAXIA TELANGIECTASIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

EID: 13444306242     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.4.2058-2065.2005     Document Type: Article

References (57)

1. Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177-2196.
2. Agostini, I., S. Popov, T. Hao, J. H. Li, L. Dubrovsky, O. Chaika, N. Chaika, R. Lewis, and M. Bukrinsky. 2002. Phosphorylation of Vpr regulates HIV type 1 nuclear import and macrophage infection. AIDS Res. Hum. Retrovir. 18:283-288.
3. Boothman, D. A., R. Schlegel, and A. B. Pardee. 1988. Anticarcinogenic potential of DNA-repair modulators. Mutat. Res. 202:393-411.
4. Brown, E. J., and D. Baltimore. 2000. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14:397-402.
5. Buchmann, A. M., J. R. Skaar, and J. A. DeCaprio. 2004. Activation of a DNA damage checkpoint response in a TAF1-defective cell line. Mol. Cell. Biol. 24:5332-5339.
6. Cliby, W. A., C. J. Roberts, K. A. Cimprich, C. M. Stringer, J. R. Lamb, S. L. Schreiber, and S. H. Friend. 1998. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17:159-169.
7. Collman, R., N. F. Hassan, R. Walker, B. Godfrey, J. Cutilli, J. C. Hastings, H. Friedman, S. D. Douglas, and N. Nathanson. 1989. Infection of monocyte-derived macrophages with human immunodeficiency virus type 1 (HIV-1). Monocyte-tropic and lymphocyte-tropic strains of HIV-1 show distinctive patterns of replication in a panel of cell types. J. Exp. Med. 170:1149-1163.
8. Cortez, D. 2003. Caffeine inhibits checkpoint responses without inhibiting the ataxia-telangiectasia-mutated (ATM) and ATM- and Rad3-related (ATR) protein kinases. J. Biol. Chem. 278:37139-37145.
9. Cortez, D., S. Guntuku, J. Qin, and S. J. Elledge. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294:1713-1716.
10. Costanzo, V., D. Shechter, P. J. Lupardus, K. A. Cimprich, M. Gottesman, and J. Gautier. 2003. An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell 11:203-213.
11. Crosio, C., G. M. Fimia, R. Loury, M. Kimura, Y. Okano, H. Zhou, S. Sen, C. D. Allis, and P. Sassone-Corsi. 2002. Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol. Cell. Biol. 22:874-885.
12. Daniel, R., J. G. Greger, R. A. Katz, K. D. Taganov, X. Wu, J. C. Kappes, and A. M. Skalka. 2004. Evidence that stable retroviral transduction and cell survival following DNA integration depend on components of the nonhomologous end joining repair pathway. J. Virol. 78:8573-8581.
13. Daniel, R., G. Kao, K. Taganov, J. G. Greger, O. Favorova, G. Merkel, T. J. Yen, R. A. Katz, and A. M. Skalka. 2003. Evidence that the retroviral DNA integration process triggers an ATR-dependent DNA damage response. Proc. Natl. Acad.Sci. USA 100:4778-4783.
14. Daniel, R., R. A. Katz, G. Merkel, J. C. Kittle, T. J. Yen, and A. M. Skalka. 2001. Wortmannin potentiates integrase-mediated killing of lymphocytes and reduces the efficiency of stable transduction by retroviruses. Mol. Cell. Biol. 21:1164-1172.
15. Daniel, R., R. A. Katz, and A. M. Skalka. 1999. A role for DNA-PK in retroviral DNA integration. Science 284:644-647.
16. Daniel, R., C. B. Myers, J. Kulkosky, K. Taganov, J. G. Greger, G. Merkel, I. T. Weber, R. W. Harrison, and A. M. Skalka. 2004. Characterization of a naphthalene derivative inhibitor of retroviral integrases. AIDS Res. Hum. Retrovir. 20:135-144.
17. de Klein, A., M. Muijtjens, R. van Os, Y. Verhoeven, B. Smit, A. M. Carr, A. R. Lehmann, and J. H. Hoeijmakers. 2000. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10:479-482.
18. Florensa, R., O. Bachs, and N. Agell. 2003. ATM/ATR-independent inhibition of cyclin B accumulation in response to hydroxyurea in nontransformed cell lines is altered in tumour cell lines. Oncogene 22:8283-8292.
19. Golding, S. E., E. Rosenberg, A. Khalil, A. McEwen, M. Holmes, S. Neill, L. F. Povirk, and K. Valerie. 2004. Double strand break repair by homologous recombination is regulated by cell cycle-independent signaling via ATM in human glioma cells. J. Biol. Chem. 279:15402-15410.
20. Griffiths, T. D., J. G. Carpenter, and D. B. Dahle. 1978. DNA synthesis and cell survival after X-irradiation of mammalian cells treated with caffeine or adenine. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 33:493-505.
21. Hall-Jackson, C. A., D. A. Cross, N. Morrice, and C. Smythe. 1999. ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene 18:6707-6713.
22. Heffernan, T. P., D. A. Simpson, A. R. Frank, A. N. Heinloth, R. S. Paules, M. Cordeiro-Stone, and W. K. Kaufmann. 2002. An ATR- and Chk1-dependent S checkpoint inhibits replicon initiation following UVC-induced DNA damage. Mol. Cell. Biol. 22:8552-8561.
23. Jung, T., and C. Streffer. 1992. Effects of caffeine on protein phosphorylation and cell cycle progression in X-irradiated two-cell mouse embryos. Int. J. Radiat. Biol. 62:161-168.
24. Kastan, M. B., O. Onyekwere, D. Sidransky, B. Vogelstein, and R. W. Craig. 1991. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304-6311.
25. Katz, R. A., J. G. Greger, K. Darby, P. Boimel, G. F. Rall, and A. M. Skalka. 2002. Transduction of interphase cells by avian sarcoma virus. J. Virol. 76:5422-5434.
26. Kimler, B. F., D. B. Leeper, M. H. Snyder, R. Rowley, and M. H. Schneiderman. 1982. Modification of radiation-induced division delay by caffeine analogues and dibutyryl cyclic AMP. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 41:47-58.
27. Lau, C. C., and A. B. Pardee. 1982. Mechanism by which caffeine potentiates lethality of nitrogen mustard. Proc. Natl. Acad. Sci. USA 79:2942-2946.
28. Lucke-Huhle, C. 1982. Alpha-irradiation-induced G2 delay: a period of cell recovery. Radiat. Res. 89:298-308.
29. Marheineke, K., and O. Hyrien. 2004. Control of replication origin density and firing time in Xenopus egg extracts: role of a caffeine-sensitive, ATR-dependent checkpoint. J. Biol. Chem. 279:28071-28081.
30. Murnane, J. P. 1995. Cell cycle regulation in response to DNA damage in mammalian cells: a historical perspective. Cancer Metastasis Rev. 14:17-29.
31. Murnane, J. P., J. E. Byfield, J. F. Ward, and P. Calabro-Jones. 1980. Effects of methylated xanthines on mammalian cells treated with bifunctional alkylating agents. Nature 285:326-329.
32. Naldini, L., U. Blomer, P. Gallay, D. Ory, R. Mulligan, F. H. Gage, I. M. Verma, and D. Trono. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
33. Osborn, A. J., S. J. Elledge, and L. Zou. 2002. Checking on the fork: the DNA-replication stress-response pathway. Trends Cell Biol. 12:509-516.
34. Painter, R. B. 1980. Effect of caffeine on DNA synthesis in irradiated and unirradiated mammalian cells. J. Mol. Biol. 143:289-301.
35. Patel, C. A., M. Mukhtar, S. Harley, J. Kulkosky, and R. J. Pomerantz. 2002. Lentiviral expression of HIV-1 Vpr induces apoptosis in human neurons. J. Neurovirol. 8:85-99.
36. Patel, C. A., M. Mukhtar, and R. J. Pomerantz. 2000. Human immunodeficiency virus type 1 Vpr induces apoptosis in human neuronal cells. J. Virol. 74:9717-9726.
37. Pleasure, S. J., and V. M. Lee. 1993. NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J. Neurosci. Res. 35:585-602.
38. Pleasure, S. J., C. Page, and V. M. Lee. 1992. Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J. Neurosci. 12:1802-1815.
39. Powell, S. N., J. S. DeFrank, P. Connell, M. Eogan, F. Preffer, D. Dombkowski, W. Tang, and S. Friend. 1995. Differential sensitivity of p53(-) and p53(+) cells to caffeine-induced radiosensitization and override of G2 delay. Cancer Res. 55:1643-1648.
40. Ribeiro, J. C., A. R. Barnetson, P. Jackson, K. Ow, M. Links, and P. J. Russell. 1999. Caffeine-increased radiosensitivity is not dependent on a loss of G2/M arrest or apoptosis in bladder cancer cell lines. Int. J. Radiat. Biol. 75:481-492.
41. Roshal, M., B. Kim, Y. Zhu, P. Nghiem, and V. Planelles. 2003. Activation of the ATR-mediated DNA damage response by the HIV-1 viral protein R. J. Biol. Chem. 278:25879-25886.
42. Rowley, R. 1992. Reduction of radiation-induced G2 arrest by caffeine. Radiat. Res. 129:224-227.
43. Saenz, D. T., N. Loewen, M. Peretz, T. Whitwam, R. Barraza, K. G. Howell, J. M. Holmes, M. Good, and E. M. Poeschla. 2004. Unintegrated lentivirus DNA persistence and accessibility to expression in nondividing cells: analysis with class I integrase mutants. J. Virol. 78:2906-2920.
44. Sage, J., G. J. Mulligan, L. D. Attardi, A. Miller, S. Chen, B. Williams, E. Theodorou, and T. Jacks. 2000. Targeted disruption of the three Rb-related genes leads to loss of G(1) control and immortalization. Genes Dev. 14:3037-3050.
45. Sarkaria, J. N., E. C. Busby, R. S. Tibbetts, P. Roos, Y. Taya, L. M. Karnitz, and R. T. Abraham. 1999. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59:4375-4382.
46. Shiloh, Y. 2001. ATM and ATR: networking cellular responses to DNA damage. Curr. Opin. Genet. Dev. 11:71-77.
47. Takai, H., A. Smogorzewska, and T. de Lange. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:1549-1556.
48. Takase, K., M. Sawai, K. Yamamoto, J. Yata, Y. Takasaki, H. Teraoka, and K. Tsukada. 1992. Reversible G1 arrest induced by dimethyl sulfoxide in human lymphoid cell lines: kinetics of the arrest and expression of the cell cycle marker proliferating cell nuclear antigen in Raji cells. Cell Growth Differ. 3:515-521.
49. Tibbetts, R. S., D. Cortez, K. M. Brumbaugh, R. Scully, D. Livingston, S. J. Elledge, and R. T. Abraham. 2000. Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev. 14:2989-3002.
50. Tolmach, L. J., R. W. Jones, and P. M. Busse. 1977. The action of caffeine on X-irradiated HeLa cells. I. Delayed inhibition of DNA synthesis. Radiat. Res. 71:653-665.
51. Tomasovic, S. P., and W. C. Dewey. 1978. Comparative studies of the effects of drugs on X-ray-induced G2 delay. Radiat. Res. 74:112-128.
52. Valenzuela, M. T., S. Mateos, J. M. Ruiz de Almodovar, and T. J. McMillan. 2000. Variation in sensitizing effect of caffeine in human tumour cell lines after gamma-irradiation. Radiother. Oncol. 54:261-271.
53. Waldren, C. A., and I. Rasko. 1978. Caffeine enhancement of X-ray killing in cultured human and rodent cells. Radiat. Res. 73:95-110.
54. Wang, H., J. Guan, A. R. Perrault, Y. Wang, and G. Iliakis. 2001. Replication protein A2 phosphorylation after DNA damage by the coordinated action of ataxia telangiectasia-mutated and DNA-dependent protein kinase. Cancer Res. 61:8554-8563.
55. Zhou, B. B., P. Chaturvedi, K. Spring, S. P. Scott, R. A. Johanson, R. Mishra, M. R. Mattern, J. D. Winkler, and K. K. Khanna. 2000. Caffeine abolishes the mammalian G(2)/M DNA damage checkpoint by inhibiting ataxia-telangiectasia- mutated kinase activity. J. Biol. Chem. 275:10342-10348.
56. Zhou, K., M. L. Cordeiro, J. Atienza, W. E. Robinson, Jr., and S. A. Chow. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433-439.
57. Zufferey, R., D. Nagy, R. J. Mandel, L. Naldini, and D. Trono. 1997. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15:871-875.