Vaccinia virus requires glutamine but not glucose for efficient replication

Journal of Virology

Volumn 88, Issue 8, 2014, Pages 4366-4374

  Fontaine, Krystal A ^a   Camarda, Roman ^a,b   Lagunoff, Michael ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUTAMINE;

AMINO ACID METABOLISM; ARTICLE; CARBON SOURCE; CELL METABOLISM; CITRIC ACID CYCLE; CONTROLLED STUDY; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; VACCINIA VIRUS; VIRION; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

GLUCOSE; GLUTAMINE; GLYCOLYSIS; HUMANS; VACCINIA; VACCINIA VIRUS; VIRUS REPLICATION;

EID: 84896926285     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03134-13     Document Type: Article

References (40)

1. Munger J, Bajad SU, Coller HA, Shenk T, Rabinowitz JD. 2006. Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathog. 2:e132. http://dx.doi.org/10.1371/journal.ppat.0020132.
2. Munger J, Bennett BD, Parikh A, Feng XJ, McArdle J, Rabitz HA, Shenk T, Rabinowitz JD. 2008. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 26:1179-1186. http://dx.doi.org/10.1038/nbt.1500.
3. Delgado T, Sanchez EL, Camarda R, LagunoffM. 2012. Global metabolic profiling of infection by an oncogenic virus: KSHV induces and requires lipogenesis for survival of latent infection. PLoS Pathog. 8:e1002866. http://dx.doi.org/10.1371/journal.ppat.1002866.
4. Vastag L, Koyuncu E, Grady SL, Shenk TE, Rabinowitz JD. 2011. Divergent effects of human cytomegalovirus and herpes simplex virus-1 on cellular metabolism. PLoS Pathog. 7:e1002124. http://dx.doi.org/10.1371/journal.ppat.1002124.
5. Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA, Proll SC, McDermott JE, Gritsenko MA, Zhang Q, Zhao R, Metz TO, Camp DG, II, Waters KM, Smith RD, Rice CM, Katze MG. 2010. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog. 6:e1000719. http://dx.doi.org/10.1371/journal.ppat.1000719.
6. Hollenbaugh JA, Munger J, Kim B. 2011. Metabolite profiles of human immunodeficiency virus infected CD4+ T cells and macrophages using LC-MS/MS analysis. Virology 415:153-159. http://dx.doi.org/10.1016/j.virol.2011.04.007.
7. Birungi G, Chen SM, Loy BP, Ng ML, Li SF. 2010. Metabolomics approach for investigation of effects of dengue virus infection using the EA.hy926 cell line. J. Proteome Res. 9:6523-6534. http://dx.doi.org/10.1021/pr100727m.
8. Chambers JW, Maguire TG, Alwine JC. 2010. Glutamine metabolism is essential for human cytomegalovirus infection. J. Virol. 84:1867-1873. http://dx.doi.org/10.1128/JVI.02123-09.
9. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, YudkoffM, Wehrli S, Thompson CB. 2007. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc. Natl. Acad. Sci. U. S. A. 104:19345-19350. http://dx.doi.org/10.1073/pnas.0709747104.
10. Deberardinis RJ, Sayed N, Ditsworth D, Thompson CB. 2008. Brick by brick: metabolism and tumor cell growth. Curr. Opin. Genet. Dev. 18:54-61. http://dx.doi.org/10.1016/j.gde.2008.02.003.
11. Wise DR, DeBerardinis RJ, Mancuso A, Sayed N, Zhang XY, Pfeiffer HK, Nissim I, Daikhin E, YudkoffM, McMahon SB, Thompson CB. 2008. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc. Natl. Acad. Sci. U. S. A. 105: 18782-18787. http://dx.doi.org/10.1073/pnas.0810199105.
12. Lewis VJ, Jr, Scott LV. 1962. Nutritional requirements for the production of herpes simplex virus. I. Influence of glucose and glutamine of herpes simplex virus production by HeLa cells. J. Bacteriol. 83:475-482.
13. Eagle H, Habel K. 1956. The nutritional requirements for the propagation of poliomyelitis virus by the HeLa cell. J. Exp. Med. 104:271-287. http://dx.doi.org/10.1084/jem.104.2.271.
14. Moss B. 2001. Poxviridae: the viruses and their replication, p 2849-2883. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
15. Lewis-Jones S. 2004. Zoonotic poxvirus infections in humans. Curr. Opin. Infect. Dis. 17:81-89. http://dx.doi.org/10.1097/00001432-200404000-00003.
16. Frey SE, Belshe RB. 2004. Poxvirus zoonoses-putting pocks into context. N. Engl. J. Med. 350:324-327. http://dx.doi.org/10.1056/NEJM p038208.
17. Esposito JJ. 2001. Poxviruses, p 2885-2921. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
18. Hutin YJ, Williams RJ, Malfait P, Pebody R, Loparev VN, Ropp SL, Rodriguez M, Knight JC, Tshioko FK, Khan AS, Szczeniowski MV, Esposito JJ. 2001. Outbreak of human monkeypox, Democratic Republic of Congo, 1996 to 1997. Emerg. Infect. Dis. 7:434-438. http://dx.doi.org/10.3201/eid0703.017311.
19. Meyer H, Perrichot M, Stemmler M, Emmerich P, Schmitz H, Varaine F, Shungu R, Tshioko F, Formenty P. 2002. Outbreaks of disease suspected of being due to human monkeypox virus infection in the Democratic Republic of Congo in 2001. J. Clin. Microbiol. 40:2919-2921. http://dx.doi.org/10.1128/JCM.40.8.2919-2921.2002.
20. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
21. DiMaio TA, Gutierrez KD, LagunoffM. 2011. Latent KSHV infection of endothelial cells induces integrin beta3 to activate angiogenic phenotypes. PLoS Pathog. 7:e1002424. http://dx.doi.org/10.1371/journal.ppat.1002424.
22. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671-675. http://dx.doi.org/10.1038/nmeth.2089.
23. Vander Heiden MG, Cantley LC, Thompson CB. 2009. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324:1029-1033. http://dx.doi.org/10.1126/science.1160809.
24. Munoz-Pinedo C, El Mjiyad N, Ricci JE. 2012. Cancer metabolism: current perspectives and future directions. Cell Death Dis. 3:e248. http://dx.doi.org/10.1038/cddis.2011.123.
25. Kim JW, Dang CV. 2006. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 66:8927-8930. http://dx.doi.org/10.1158/0008-5472.CAN-06-1501.
26. Pelicano H, Martin DS, Xu RH, Huang P. 2006. Glycolysis inhibition for anticancer treatment. Oncogene 25:4633-4646. http://dx.doi.org/10.1038/sj.onc.1209597.
27. Yu Y, Clippinger AJ, Alwine JC. 2011. Viral effects on metabolism: changes in glucose and glutamine utilization during human cytomegalovirus infection. Trends Microbiol. 19:360-367. http://dx.doi.org/10.1016/j.tim.2011.04.002.
28. Vanslyke JK, Whitehead SS, Wilson EM, Hruby DE. 1991. The multistep proteolytic maturation pathway utilized by vaccinia virus P4a protein: a degenerate conserved cleavage motif within core proteins. Virology 183:467-478. http://dx.doi.org/10.1016/0042-6822(91)90976-I.
29. Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, LagunoffM. 2010. Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 107:10696-10701. http://dx.doi.org/10.1073/pnas.1004882107.
30. McArdle J, Schafer XL, Munger J. 2011. Inhibition of calmodulindependent kinase kinase blocks human cytomegalovirus-induced glycolytic activation and severely attenuates production of viral progeny. J. Virol. 85:705-714. http://dx.doi.org/10.1128/JVI.01557-10.
31. Radsak KD, Weder D. 1981. Effect of 2-deoxy-D-glucose on cytomegalovirus-induced DNA synthesis in human fibroblasts. J. Gen. Virol. 57:33-42. http://dx.doi.org/10.1099/0022-1317-57-1-33.
32. Courtney RJ, Steiner SM, Benyesh-Melnick M. 1973. Effects of 2-deoxy-D-glucose on herpes simplex virus replication. Virology 52:447-455. http://dx.doi.org/10.1016/0042-6822(73)90340-1.
33. Mazzon M, Peters NE, Loenarz C, Krysztofinska EM, Ember SW, Ferguson BJ, Smith GL. 2013. A mechanism for induction of a hypoxic response by vaccinia virus. Proc. Natl. Acad. Sci. U. S. A. 110:12444-12449. http://dx.doi.org/10.1073/pnas.1302140110.
34. Cory J. 2006. Purine and pyrimidine nucleotide metabolism, p 789-822. In Devlin T (ed), Textbook of biochemistry with clinical correlations, 6th ed. Wiley-Liss, Hoboken, NJ.
35. Pestova TV, Kolupaeva VG. 2002. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev. 16:2906-2922. http://dx.doi.org/10.1101/gad.1020902.
36. Jackson RJ. 1991. The ATP requirement for initiation of eukaryotic translation varies according to the mRNA species. Eur. J. Biochem. 200:285-294. http://dx.doi.org/10.1111/j.1432-1033.1991.tb16184.x.
37. Alberts B, Johnson A, Lewis J, RaffM, Roberts K, Walter P. 2002. Molecular biology of the cell, 4th ed. Garland Science, New York, NY.
38. Berg JM, Tymoczko JL, Stryer L. 2002. Biochemistry, 5th ed. WH Freeman, New York, NY.
39. Lu W, Pelicano H, Huang P. 2010. Cancer metabolism: is glutamine sweeter than glucose? Cancer Cell 18:199-200. http://dx.doi.org/10.1016/j.ccr.2010.08.017.
40. Shukla K, Ferraris DV, Thomas AG, Stathis M, Duvall B, Delahanty G, Alt J, Rais R, Rojas C, Gao P, Xiang Y, Dang CV, Slusher BS, Tsukamoto T. 2012. Design, synthesis, and pharmacological evaluation of bis-2-(5-phenylacetamido-1,2,4-thiadiazol-2-yl)ethyl sulfide 3 (BPTES) analogs as glutaminase inhibitors. J. Med. Chem. 55:10551-10563. http://dx.doi.org/10.1021/jm301191p.