Inhibition of calmodulin-dependent kinase kinase blocks human cytomegalovirus-induced glycolytic activation and severely attenuates production of viral progeny

Journal of Virology

Volumn 85, Issue 2, 2011, Pages 705-714

  McArdle, Jessica ^a   Schafer, Xenia L ^a   Munger, Joshua ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN DEPENDENT KINASE 2; CALMODULIN DEPENDENT KINASE KINASE; CALMODULIN DEPENDENT KINASE KINASE 1; CYCLIC AMP DEPENDENT PROTEIN KINASE; MESSENGER RNA; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG; VIRUS DNA;

ARTICLE; CYTOMEGALOVIRUS INFECTION; DNA REPLICATION; ENZYME INHIBITION; GENE EXPRESSION; GLYCOLYSIS; HERPES SIMPLEX VIRUS 1; HUMAN CYTOMEGALOVIRUS; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; VIRION; VIRUS ACTIVATION; VIRUS REPLICATION;

CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE KINASE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 1; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOMEGALOVIRUS; FIBROBLASTS; GENE EXPRESSION; GLYCOLYSIS; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; RNA, MESSENGER; VIRUS REPLICATION;

HERPESVIRIDAE; HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 5;

EID: 78650660123     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01557-10     Document Type: Article

References (40)

1. Andrei, G., E. De Clercq, and R. Snoeck. 2008. Novel inhibitors of human CMV. Curr. Opin. Invest. Drugs 9:132-145.
2. Beisser, P. S., H. Lavreysen, C. A. Bruggeman, and C. Vink. 2008. Chemokines and chemokine receptors encoded by cytomegaloviruses. Curr. Top. Microbiol. Immunol. 325:221-242.
3. Bito, H., and S. Takemoto-Kimura. 2003. Ca(2+)/CREB/CBP-dependent gene regulation: a shared mechanism critical in long-term synaptic plasticity and neuronal survival. Cell Calcium 34:425-430.
4. Bradley, P. L. 1957. Metabolism of pyruvate and alpha-ketoglutarate in virus-infected mouse brain. Nature 180:1418-1419.
5. Burny, W., C. Liesnard, C. Donner, and A. Marchant. 2004. Epidemiology, pathogenesis and prevention of congenital cytomegalovirus infection. Expert Rev. Anti Infect. Ther. 2:881-894.
6. Cochrane, A. B. 2006. Antiviral dosing and efficacy for prophylaxis of cytomegalovirus disease in solid organ transplant recipients. Am. J. Health Syst. Pharm. 63:S17-S21.
7. Courtney, R. J., S. M. Steiner, and M. Benyesh-Melnick. 1973. Effects of 2-deoxy-glucose on herpes simplex virus replication. Virology 52:447-455.
8. DeBerardinis, R. J., J. J. Lum, G. Hatzivassiliou, and C. B. Thompson. 2008. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 7:11-20.
9. Fioretti, A., T. Furukawa, D. Santoli, and S. A. Plotkin. 1973. Nonproductive infection of guinea pig cells with human cytomegalovirus. J. Virol. 11:998-1003.
10. Furukawa, T., S. Tanaka, and S. A. Plotkin. 1975. Resticted growth of human cytomegalovirus in UV-irradiated WI-38 human fibroblasts. Proc. Soc Exp. Biol. Med. 148:1249-1251.
11. Gerna, G., F. Baldanti, and M. G. Revello. 2004. Pathogenesis of human cytomegalovirus infection and cellular targets. Hum. Immunol. 65:381-386. (Pubitemid 38686760)
12. Goodrich, J. M., et al. 1993. Ganciclovir prophylaxis to prevent cytomegalovirus disease after allogeneic marrow transplant. Ann. Intern. Med. 118: 173-178.
13. Hidaka, H., M. Inagaki, S. Kawamoto, and Y. Sasaki. 1984. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 23:5036-5041.
14. Himpens, B., et al. 1995. Human cytomegalovirus modulates the Ca2+ response to vasopressin and ATP in fibroblast cultures. Cell Calcium 18: 111-119.
15. Huang, E. S. 1975. Human cytomegalovirus. IV. Specific inhibition of virusinduced DNA polymerase activity and viral DNA replication by phosphonoacetic acid. J. Virol. 16:1560-1565.
16. Jungmann, R. A., D. Huang, and D. Tian. 1998. Regulation of LDH-A gene expression by transcriptional and posttranscriptional signal transduction mechanisms. J. Exp. Zool. 282:188-195.
17. Kaplan, A. S., and T. Ben-Porat. 1961. The action of 5-fluorouracil on the nucleic acid metabolism of pseudorabies virus-infected and noninfected rabbit kidney cells. Virology 13:78-92.
18. Kinsella, T. M., and G. P. Nolan. 1996. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7:1405-1413.
19. Lee, M. G., and P. L. Pedersen. 2003. Glucose metabolism in cancer: importance of transcription factor-DNA interactions within a short segment of the proximal region og the type II hexokinase promoter. J. Biol. Chem. 278:41047-41058.
20. Lee, W. A., and J. C. Martin. 2006. Perspectives on the development of acyclic nucleotide analogs as antiviral drugs. Antiviral Res. 71:254-259.
21. Litman, R. M., and A. B. Pardee. 1956. Production of bacteriophage mutants by a disturbance of deoxyribonucleic acid metabolism. Nature 178:529-531.
22. Munger, J., S. U. Bajad, H. A. Coller, T. Shenk, and J. D. Rabinowitz. 2006. Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathog. 2:e132.
23. Munger, J., et al. 2008. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 26:1179-1186.
24. Pass, R. F. 2001. Cytomegalovirus, p. 2675-2705. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott-Williams and Wilkins, New York, NY.
25. Pearson, H. E., and R. J. Winzler. 1949. Oxidative and glycolytic metabolism of minced day-old mouse brain in relation to propagation of Theiler's GD VII virus. J. Biol. Chem. 181:577-582.
26. Qin, H., B. Raught, N. Sonenberg, E. G. Goldstein, and A. M. Edelman. 2003. Phosphorylation screening identifies translational initiation factor 4GII as an intracellular target of Ca(2+)/calmodulin-dependent protein kinase I. J. Biol. Chem. 278:48570-48579.
27. Radsak, K. D., and D. Weder. 1981. Effect of 2-deoxy-D-glucose on cytomegalovirus-induced DNA synthesis in human fibroblasts. J. Gen. Virol. 57:33-42.
28. Rider, M. H., et al. 2004. 6-Phosphofructo-2-kinase/fructose-2,6- bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis. Biochem. J. 381:561-579.
29. Robey, R. B., and N. Hay. 2009. Is Akt the "Warburg kinase"?-Akt-energy metabolism interactions and oncogenesis. Semin. Cancer Biol. 19:25-31.
30. Salzman, N. P., R. Z. Lockart, Jr., and E. D. Sebring. 1959. Alterations in HeLa cell metabolism resulting from poliovirus infection. Virology 9:244-259.
31. Sharon-Friling, R., J. Goodhouse, A. M. Colberg-Poley, and T. Shenk. 2006. Human cytomegalovirus pUL37x1 induces the release of endoplasmic reticulum calcium stores. Proc. Natl. Acad. Sci. U. S. A. 103:19117-19122.
32. Singh, P., M. Salih, J. J. Leddy, and B. S. Tuana. 2004. The muscle-specific calmodulin-dependent protein kinase assembles with the glycolytic enzyme complex at the sarcoplasmic reticulum and modulates the activity of glyceraldehyde-3-phosphate dehydrogenase in a Ca2+/calmodulin- dependent manner. J. Biol. Chem. 279:35176-35182.
33. Swulius, M. T., and M. N. Waxham. 2008. Ca(2+)/calmodulin-dependent protein kinases. Cell. Mol. Life Sci. 65:2637-2657.
34. Tokumitsu, H., et al. 1990. KN-62, 1-[N,O-bis(5-isoquinolinesulfonyl)- Nmethyl-L-tyrosyl]-4-phenylpiperazine, a specific inhibitor of Ca2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 265:4315-4320.
35. Tokumitsu, H., et al. 2002. STO-609, a specific inhibitor of the Ca(2+)/calmodulin-dependent protein kinase kinase. J. Biol. Chem. 277:15813-15818.
36. Towler, M. C., and D. G. Hardie. 2007. AMP-activated protein kinase in metabolic control and insulin signaling. Circ. Res. 100:328-341.
37. Yalcin, A., S. Telang, B. Clem, and J. Chesney. 2009. Regulation of glucose metabolism by 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatases in cancer. Exp. Mol. Pathol. 86:174-179.
38. Yano, S., H. Tokumitsu, and T. R. Soderling. 1998. Calcium promotes cell survival through CaM-K kinase activation of the protein-kinase-B pathway. Nature 396:584-587.
39. Yu, D., G. A. Smith, L. W. Enquist, and T. Shenk. 2002. Construction of a self-excisable bacterial artificial chromosome containing the human cytomegalovirus genome and mutagenesis of the diploid TRL/IRL13 gene. J. Virol. 76:2316-2328.
40. Yurochko, A. D. 2008. Human cytomegalovirus modulation of signal transduction. Curr. Top. Microbiol. Immunol. 325:205-220