Upregulation of Nrf2 expression by human cytomegalovirus infection protects host cells from oxidative stress

Journal of General Virology

Volumn 94, Issue PART7, 2013, Pages 1658-1668

  Lee, Junsub ^a   Koh, Kyungmi ^a   Kim, Young Eui ^b   Ahn, Jin Hyun ^b   Kim, Sunyoung ^a  

^a Seoul National University   (South Korea)

^b Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BUTHIONINE SULFOXIMINE; CASEIN KINASE II; HEME OXYGENASE 1; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; ENZYME ACTIVITY; FIBROBLAST; HOST CELL; HUMAN; HUMAN CELL; INFLAMMATION; OXIDATIVE STRESS; PREPUCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL RATE; UPREGULATION;

BUTHIONINE SULFOXIMINE; CELL SURVIVAL; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; CYTOPROTECTION; FIBROBLASTS; HEME OXYGENASE-1; HUMANS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; UP-REGULATION;

HUMAN HERPESVIRUS 5;

EID: 84879144629     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.052142-0     Document Type: Article

References (40)

1. Afonyushkin, T., Oskolkova, O. V., Binder, B. R. & Bochkov, V. N. (2011). Involvement of CK2 in activation of electrophilic genes in endothelial cells by oxidized phospholipids. J Lipid Res 52, 98-103.
2. Britt, W. (2008). Manifestations of human cytomegalovirus infection: proposed mechanisms of acute and chronic disease. Curr Top Microbiol Immunol 325, 417-470.
3. Browne, E. P., Wing, B., Coleman, D. & Shenk, T. (2001). Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J Virol 75, 12319-12330.
4. Buchkovich, N. J., Maguire, T. G., Paton, A. W., Paton, J. C. & Alwine, J. C. (2009). The endoplasmic reticulum chaperone BiP/GRP78 is important in the structure and function of the human cytomegalovirus assembly compartment. J Virol 83, 11421-11428.
5. Burdette, D., Olivarez, M. & Waris, G. (2010). Activation of transcription factor Nrf2 by hepatitis C virus induces the cell-survival pathway. J Gen Virol 91, 681-690.
6. Calkins, M. J., Vargas, M. R., Johnson, D. A. & Johnson, J. A. (2010). Astrocyte-specific overexpression of Nrf2 protects striatal neurons from mitochondrial complex II inhibition. Toxicol Sci 115, 557-568.
7. Carvajal-Yepes, M., Himmelsbach, K., Schaedler, S., Ploen, D., Krause, J., Ludwig, L., Weiss, T., Klingel, K. & Hildt, E. (2011). Hepatitis C virus impairs the induction of cytoprotective Nrf2 target genes by delocalization of small Maf proteins. J Biol Chem 286, 8941-8951.
8. Chan, K., Lu, R., Chang, J. C. & Kan, Y. W. (1996). NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci U S A 93, 13943-13948.
9. Cope, A. V., Sabin, C., Burroughs, A., Rolles, K., Griffiths, P. D. & Emery, V. C. (1997). Interrelationships among quantity of human cytomegalovirus (HCMV) DNA in blood, donor-recipient serostatus, and administration of methylprednisolone as risk factors for HCMV disease following liver transplantation. J Infect Dis 176, 1484-1490.
10. Deayton, J. R., Sabin, C. A., Johnson, M. A., Emery, V. C., Wilson, P. & Griffiths, P. D. (2004). Importance of cytomegalovirus viraemia in risk of disease progression and death in HIV-infected patients receiving highly active antiretroviral therapy. Lancet 363, 2116-2121.
11. Emery, V. C., Cope, A. V., Bowen, E. F., Gor, D. & Griffiths, P. D. (1999). The dynamics of human cytomegalovirus replication in vivo. J Exp Med 190, 177-182.
12. Emery, V. C., Sabin, C. A., Cope, A. V., Gor, D., Hassan-Walker, A. F. & Griffiths, P. D. (2000). Application of viral-load kinetics to identify patients who develop cytomegalovirus disease after transplantation. Lancet 355, 2032-2036.
13. Fehr, A. R. & Yu, D. (2011). Human cytomegalovirus early protein pUL21a promotes efficient viral DNA synthesis and the late accumulation of immediate-early transcripts. J Virol 85, 663-674.
14. Gharbi, S. I., Zvelebil, M. J., Shuttleworth, S. J., Hancox, T., Saghir, N., Timms, J. F. & Waterfield, M. D. (2007). Exploring the specificity of the PI3K family inhibitor LY294002. Biochem J 404, 15-21.
15. Huh, Y. H., Kim, Y. E., Kim, E. T., Park, J. J., Song, M. J., Zhu, H., Hayward, G. S. & Ahn, J. H. (2008). Binding STAT2 by the acidic domain of human cytomegalovirus IE1 promotes viral growth and is negatively regulated by SUMO. J Virol 82, 10444-10454.
16. Jang, J., Yoon, K., Hwang, D. W., Lee, D. S. & Kim, S. (2012). A retroviral vector suitable for ultrasound image-guided gene delivery to mouse brain. Gene Ther 19, 396-403.
17. Johnson, R. A., Wang, X., Ma, X. L., Huong, S. M. & Huang, E. S. (2001). Human cytomegalovirus up-regulates the phosphatidylinositol 3-kinase (PI3-K) pathway: inhibition of PI3-K activity inhibits viral replication and virus-induced signaling. J Virol 75, 6022-6032.
18. Joyce, M. A., Walters, K. A., Lamb, S. E., Yeh, M. M., Zhu, L. F., Kneteman, N., Doyle, J. S., Katze, M. G. & Tyrrell, D. L. (2009). HCV induces oxidative and ER stress, and sensitizes infected cells to apoptosis in SCID/Alb-uPA mice. PLoS Pathog 5, e1000291.
19. Jung, G. S., Kim, Y. Y., Kim, J. I., Ji, G. Y., Jeon, J. S., Yoon, H. W., Lee, G. C., Ahn, J. H., Lee, K. M. & Lee, C. H. (2011). Full genome sequencing and analysis of human cytomegalovirus strain JHC isolated from a Korean patient. Virus Res 156, 113-120.
20. Kesic, M. J., Simmons, S. O., Bauer, R. & Jaspers, I. (2011). Nrf2 expression modifies influenza A entry and replication in nasal epithelial cells. Free Radic Biol Med 51, 444-453.
21. Kim, K. M., Song, J. D., Chung, H. T. & Park, Y. C. (2012). Protein kinase CK2 mediates peroxynitrite-induced heme oxygenase-1 expression in articular chondrocytes. Int J Mol Med 29, 1039-1044.
22. Liu, Z. M., Li, L. Q., Peng, M. H., Liu, T. W., Qin, Z., Guo, Y., Xiao, K. Y., Ye, X. P., Mo, X. S. & other authors (2008). Hepatitis B virus infection contributes to oxidative stress in a population exposed to aflatoxin B1 and high-risk for hepatocellular carcinoma. Cancer Lett 263, 212-222.
23. Nakaso, K., Yano, H., Fukuhara, Y., Takeshima, T., Wada-Isoe, K. & Nakashima, K. (2003). PI3K is a key molecule in the Nrf2-mediated regulation of antioxidative proteins by hemin in human neuroblastoma cells. FEBS Lett 546, 181-184.
24. Niture, S. K. & Jaiswal, A. K. (2010). Hsp90 interaction with INrf2(Keap1) mediates stress-induced Nrf2 activation. J Biol Chem 285, 36865-36875.
25. Niture, S. K., Jain, A. K. & Jaiswal, A. K. (2009). Antioxidant-induced modification of INrf2 cysteine 151 and PKC-d-mediated phosphorylation of Nrf2 serine 40 are both required for stabilization and nuclear translocation of Nrf2 and increased drug resistance. J Cell Sci 122, 4452-4464.
26. Niture, S. K., Kaspar, J. W., Shen, J. & Jaiswal, A. K. (2010). Nrf2 signaling and cell survival. Toxicol Appl Pharmacol 244, 37-42.
27. Schaedler, S., Krause, J., Himmelsbach, K., Carvajal-Yepes, M., Lieder, F., Klingel, K., Nassal, M., Weiss, T. S., Werner, S. & Hildt, E. (2010). Hepatitis B virus induces expression of antioxidant response element-regulated genes by activation of Nrf2. J Biol Chem 285, 41074-41086.
28. Söderberg-Nauclér, C. (2006). Does cytomegalovirus play a causative role in the development of various inflammatory diseases and cancer? J Intern Med 259, 219-246.
29. Speir, E., Shibutani, T., Yu, Z. X., Ferrans, V. & Epstein, S. E. (1996). Role of reactive oxygen intermediates in cytomegalovirus gene expression and in the response of human smooth muscle cells to viral infection. Circ Res 79, 1143-1152.
30. Stanton, R. J., McSharry, B. P., Rickards, C. R., Wang, E. C., Tomasec, P. & Wilkinson, G. W. (2007). Cytomegalovirus destruction of focal adhesions revealed in a high-throughput Western blot analysis of cellular protein expression. J Virol 81, 7860-7872.
31. Steininger, C. (2007). Clinical relevance of cytomegalovirus infection in patients with disorders of the immune system. Clin Microbiol Infect 13, 953-963.
32. Streblow, D. N., Orloff, S. L. & Nelson, J. A. (2007). Acceleration of allograft failure by cytomegalovirus. Curr Opin Immunol 19, 577-582.
33. Sykiotis, G. P. & Bohmann, D. (2010). Stress-activated cap'n'collar transcription factors in aging and human disease. Sci Signal 3, re3.
34. Tilton, C., Clippinger, A. J., Maguire, T. & Alwine, J. C. (2011). Human cytomegalovirus induces multiple means to combat reactive oxygen species. J Virol 85, 12585-12593.
35. Tsutsui, Y. (2009). Effects of cytomegalovirus infection on embryogenesis and brain development. Congenit Anom (Kyoto) 49, 47-55.
36. Valyi-Nagy, T. & Dermody, T. S. (2005). Role of oxidative damage in the pathogenesis of viral infections of the nervous system. Histol Histopathol 20, 957-967.
37. van de Berg, P. J., Heutinck, K. M., Raabe, R., Minnee, R. C., Young, S. L., van Donselaar-van der Pant, K. A., Bemelman, F. J., van Lier, R. A. & ten Berge, I. J. (2010). Human cytomegalovirus induces systemic immune activation characterized by a type 1 cytokine signature. J Infect Dis 202, 690-699.
38. Varani, S. & Landini, M. P. (2011). Cytomegalovirus-induced immunopathology and its clinical consequences. Herpesviridae 2, 6.
39. Wang, L., Chen, Y., Sternberg, P. & Cai, J. (2008). Essential roles of the PI3 kinase/Akt pathway in regulating Nrf2-dependent antioxidant functions in the RPE. Invest Ophthalmol Vis Sci 49, 1671-1678.
40. Yu, S. S., Han, E., Hong, Y., Lee, J. T., Kim, S. & Kim, S. (2003). Construction of a retroviral vector production system with the minimum possibility of a homologous recombination. Gene Ther 10, 706-711.