Viral effects on metabolism: Changes in glucose and glutamine utilization during human cytomegalovirus infection

Trends in Microbiology

Volumn 19, Issue 7, 2011, Pages 360-367

  Yu, Yongjun ^a   Clippinger, Amy J ^a   Alwine, James C ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; ADENOSINE TRIPHOSPHATE; CITRIC ACID; GLUCOSE; GLUTAMINE;

AMINO ACID TRANSPORT; ANAPLEROSIS; CATAPLEROSIS; CELL METABOLISM; CITRIC ACID CYCLE; CYTOMEGALOVIRUS INFECTION; ENERGY RESOURCE; ENZYME INDUCTION; FATTY ACID SYNTHESIS; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; GLYCOLYSIS; HOST CELL; HUMAN; METABOLIC PARAMETERS; MICROBIAL METABOLISM; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR CELL; VIRUS CARCINOGENESIS; VIRUS METABOLISM; VIRUS PATHOGENESIS;

CARBON; CELLS, CULTURED; CITRIC ACID; CITRIC ACID CYCLE; CYTOMEGALOVIRUS; ENERGY METABOLISM; FATTY ACIDS; GLUCOSE; GLUTAMINE; GLYCOLYSIS; HOST-PATHOGEN INTERACTIONS; HUMANS; KETOGLUTARIC ACIDS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NEOPLASMS; PHOSPHORYLATION;

HUMAN HERPESVIRUS 5;

EID: 79959868193     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2011.04.002     Document Type: Review

References (86)

1. DeBerardinis R.J., et al. 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. 2007, 104:19345-19350.
2. DeBerardinis R.J., et al. Brick by brick: metabolism and tumor cell growth. Curr. Opin. Genet. Dev. 2008, 18:54-61.
3. Wise D.R., et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18782-18787.
4. Wellen K.E., et al. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 2009, 324:1076-1080.
5. Vander Heiden M.G., et al. Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 2010, 329:1492-1499.
6. Ward P.S., et al. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 2010, 17:225-234.
7. Warburg O., et al. Über den Stoffwechsel der Carcinomzelle. Biochem. Z. 1924, 152:319-344.
8. Van der Heiden M.G., et al. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
9. Kuhajda F.P. Fatty acid synthase and cancer: new application of an old pathway. Cancer Res. 2006, 66:5977-5980.
10. Menendez J.A., Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat. Rev. Cancer 2007, 7:763-777.
11. Swinnen J.V., et al. Increased lipogenesis in cancer cells: new players, novel targets. Curr. Opin. Clin. Nutr. Metab. Care 2006, 9:358-365.
12. Newsholme E.A., et al. The role of high rates of glycolysis and glutamine utilization in rapidly dividing cells. Biosci. Rep. 1985, 5:393-400.
13. zur Hausen H. The search for infectious causes of human cancers: where and why. Virology 2009, 392:1-10.
14. O'Shea C.C. DNA tumor viruses - the spies who lyse us. Curr. Opin. Genet. Dev. 2005, 15:18-26.
15. Chen H.R., Barker W.C. Nucleic acid sequence database VI: retroviral oncogenes and cellular proto-oncogenes. DNA 1985, 42:171-182.
16. Murphy E., et al. Coding potential of laboratory and clinical strains of human cytomegalovirus. Proc. Natl. Acad. Sci. U.S.A. 2003, 25:14976-14981.
17. Mocarski E.S., Courcelle C.T. Cytomegaloviruses and their replication. Fields Virol. 2001, 2:2629-2673.
18. Goodrum F., et al. Human cytomegalovirus sequences expressed in latently infected individuals promote a latent infection in vitro. Blood 2007, 110:937-945.
19. Mendelson M., et al. Detection of endogenous human cytomegalovirus in CD34+ bone marrow progenitors. J. Gen. Virol. 1966, 77:3099-3102.
20. Reeves M.B., et al. Latency, chromatin remodeling, and reactivation of human cytomegalovirus in the dendritic cells of healthy carriers. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4140-4145.
21. Kudchodkar S.B., et al. Human cytomegalovirus infection alters the substrate specificities and rapamycin sensitivities of raptor- and rictor-containing complexes. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:14182-14187.
22. Kudchodkar S., et al. Human cytomegalovirus infection induces rapamycin insensitive phosphorylation of downstream effectors of mTOR kinase. J. Virol. 2004, 78:11030-11039.
23. Kudchodkar S.B., et al. AMPK-mediated inhibition of mTOR kinase is circumvented during immediate-early times of human cytomegalovirus infection. J. Virol. 2007, 81:3649-3651.
24. Yu Y., Alwine J.C. Human cytomegalovirus major immediate-early proteins and simian virus 40 large T antigen can inhibit apoptosis through activation of the phosphatidylinositide 3′-OH kinase pathway and cellular kinase Akt. J. Virol. 2002, 76:3731-3738.
25. Alwine J.C. Modulation of host cell stress responses by human cytomegalovirus. Current Topics in Microbiology and Immunology, Human Cytomegalovirus 2008, 263-279. Springer. T.E. Shenk, M.F. Stinski (Eds.).
26. Isler J.A., et al. Human cytomegalovirus infection activates and regulates the unfolded protein response. J. Virol. 2005, 79:6890-6899.
27. Isler J.A., et al. Production of infectious HCMV virions is inhibited by drugs that disrupt calcium homeostasis in the endoplasmic reticulum. J. Virol. 2005, 79:15338-15397.
28. Yu Y., et al. Effects of simian virus 40 large and small tumor antigens on mammalian target of rapamycin (mTOR) signaling: small tumor antigen mediates hypophosphorylation of eIF4E-binding protein 1 late in infection. J. Virol. 2005, 79:6882-6889.
29. Chambers J.W., et al. Glutamine metabolism is essential for human cytomegalovirus infection. J. Virol. 2010, 84:1867-1873.
30. Hakki M., et al. Binding and nuclear relocalization of protein kinase R by human cytomegalovirus TRS1. J. Virol. 2006, 80:11817-11826.
31. Walsh D., et al. Regulation of the translation initiation factor eIF4F by multiple mechanisms in human cytomegalovirus-infected cells. J. Virol. 2005, 79:8057-8064.
32. Moorman N.J., et al. Human cytomegalovirus protein UL38 inhibits host cell stress responses by antagonizing the tuberous sclerosis protein complex. Cell Host Microbe 2008, 3:1-10.
33. Xuan B., et al. Human cytomegalovirus protein pUL38 induces ATF4 expression, inhibits persistent JNK phosphorylation, and suppresses endoplasmic reticulum stress-induced cell death. J. Virol. 2009, 83:3463-3474.
34. Munger J., et al. Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathogens 2006, 2:1165-1175.
35. Munger J., et al. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 2008, 26:1179-1186.
36. Yu Y., et al. Human cytomegalovirus activates glucose transporter 4 expression to increase glucose uptake during infection. J. Virol. 2011, 85:1573-1580.
37. McArdle J., et al. Inhibition of calmodulin-dependent kinase kinase blocks human cytomegalovirus-induced glycolytic activation and severely attenuates production of viral progeny. J. Virol. 2011, 85:705-714.
38. Buchkovich N.J., et al. Role of the endoplasmic reticulum chaperone BiP SUN domain proteins, and dynein in altering nuclear morphology during human cytomegalovirus infection. J. Virol. 2010, 84:7005-7017.
39. Buchkovich N.J., et al. Human cytomegalovirus specifically controls the levels of the endoplasmic reticulum chaperone BiP/GRP78 which is required for virion assembly. J. Virol. 2008, 82:31-39.
40. Buchkovich N.J., et al. The endoplasmid reticulum chaperone BiP/GRP78 is important in the structure and function of the HCMV assembly compartment. J. Virol. 2009, 83:11421-11428.
41. Buchkovich N.J., et al. Human cytomegalovirus induces the endoplasmic reticulum chaperone BiP through increased transcription and activation of translation by using the BiP internal ribosome entry site. J. Virol. 2010, 84:11479-11486.
42. Buchkovich N.J., et al. The TORrid affairs of viruses: effects of mammalian DNA viruses on the PI3K-Akt-mTOR signaling pathway. Nat. Rev. Microbiol. 2008, 6:265-275.
43. Melnick J.L., et al. Cytomegalovirus and atherosclerosis. Arch. Immunol. Ther. Exp. 1996, 44:297-302.
44. Speir E. Cytomegalovirus gene regulation by reactive oxygen species. Agents of atherosclerosis. Ann. N. Y. Acad. Sci. 2000, 889:363-374.
45. Mattila K.J., et al. Role of infection as a risk factor for atherosclerosis, myocardial infarction, and stroke. Clin. Infect. Dis. 1998, 26:719-734.
46. Cinatl J., et al. Modulatory effects of human cytomegalovirus infection on malignant properties of cancer cells. Intervirology 1997, 39:259-269.
47. Streblow D.N., et al. Mechanisms of cytomegalovirus-accelerated vascular disease: induction of paracrine factors that promote angiogenesis and wound healing. Curr. Top. Microbiol. Immunol. 2008, 325:397-415.
48. Cobbs C.S., et al. Modulation of oncogenic phenotype in human glioma cells by cytomegalovirus IE1-mediated mitogenicity. Cancer Res. 2008, 68:724-730.
49. Mitchell D.A., et al. Sensitive detection of human cytomegalovirus in tumors and peripheral blood of patients diagnosed with glioblastoma. Neuro Oncol. 2008, 10:10-18.
50. Harkins L., et al. Specific localisation of human cytomegalovirus nucleic acids and proteins in human colorectal cancer. Lancet 2002, 360:1557-1563.
51. Samanta M., et al. High prevalence of human cytomegalovirus in prostatic intraepithelial neoplasia and prostatic carcinoma. J. Urol. 2003, 170:998-1002.
52. Shen Y., et al. Human cytomegalovirus IE1 and IE2 proteins are mutagenic and mediate " hit-and-run" oncogenic transformation in cooperation with the adenovirus E1A proteins. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:3341-3345.
53. Michaelis M., et al. The story of human cytomegalovirus and cancer: increasing evidence and open questions. Neoplasia 2009, 11:1-9.
54. Michaelis M., et al. Oncomodulation by human cytomegalovirus: evidence becomes stronger. Med. Microbiol. Immunol. 2009, 198:79-81.
55. Landini M.P. Early enhanced glucose uptake in human cytomegalovirus-infected cells. J. Gen. Virol. 1984, 65:1229-1232.
56. Joost H.G., et al. Nomenclature of the GLUT/SLC2A family of sugar/polyol transport facilitators. Am. J. Physiol. Endocrinol. Metab. 2002, 282:E974-E976.
57. Uldry M., Thorens B. The SLC2 family of facilitated hexose and polyol transporters. Pflugers Arch. 2004, 447:480-489.
58. Birnbaum M.J., et al. Cloning and characterization of a cDNA encoding the rat brain glucose-transporter protein. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:5784-5788.
59. Fukumoto H., et al. Sequence, tissue distribution, and chromosomal localization of mRNA encoding a human glucose transporter-like protein. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:5434-5438.
60. Pardridge W.M., et al. Brain-type glucose transporter (GLUT-1) is selectively localized to the blood-brain barrier Studies with quantitative western blotting and in situ hybridization. J. Biol. Chem. 1990, 265:18035-18040.
61. Thorens B., et al. Cloning and functional expression in bacteria of a novel glucose transporter present in liver, intestine, kidney, and beta-pancreatic islet cells. Cell 1988, 55:281-290.
62. Haber R.S., et al. Tissue distribution of the human GLUT3 glucose transporter. Endocrinology 1993, 132:2538-2543.
63. Birnbaum M.J. Identification of a novel gene encoding an insulin-responsive glucose transporter protein. Cell 1989, 57:305-315.
64. Langfort J., et al. Time course of GLUT4 and AMPK protein expression in human skeletal muscle during one month of physical training. Scand. J. Med. Sci. Sports 2003, 13:169-174.
65. Carvalho E., et al. GLUT4 overexpression or deficiency in adipocytes of transgenic mice alters the composition of GLUT4 vesicles and the subcellular localization of GLUT4 and insulin-responsive aminopeptidase. J. Biol. Chem. 2004, 279:21598-21605.
66. Yuneva M., et al. Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J. Cell Biol. 2007, 178:93-105.
67. Hue L., et al. Insulin and ischemia stimulate glycolysis by acting on the same targets through different and opposing signaling pathways. J. Mol. Cell. Cardiol. 2002, 34:1091-1097.
68. Rider M.H., et al. 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis. Biochem. J. 2004, 381:561-579.
69. Johnson R.A., et al. 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. 2001, 75:6022-6032.
70. Sharon-Friling R., et al. Human cytomegalovirus pUL37x1 induces the release of endoplasmic reticulum calcium stores. Proc. Natl. Acad. Sci. U.S.A. 2006, 130:19117-19122.
71. Monick M.M., et al. The immediate early genes of human cytomegalovirus upregulate expression of the cellular genes myc and fos. Am. J. Respir. Cell Mol. Biol. 1992, 7:251-256.
72. Boldogh I., et al. Transcriptional activation of cellular oncogenes fos, jun, and myc by human cytomegalovirus. J. Virol. 1991, 65:1568-1571.
73. Blaheta R.A., et al. Human cytomegalovirus infection alters PC3 prostate carcinoma cell adhesion to endothelial cells and extracellular matrix. Neoplasia 2006, 8:807-816.
74. Eboli M.L., Galeotti T. Evidence for the occurrence of the malate-citrate shuttle in intact Ehrlich ascites tumor cells. Biochim. Biophys. Acta 1981, 638:75-79.
75. Farfari S., et al. Glucose-regulated anaplerosis and cataplerosis in pancreatic beta-cells: possible implication of a pyruvate/citrate shuttle in insulin secretion. Diabetes 2000, 49:718-726.
76. Williamson C.D., Colberg-Poley A.M. Access of viral proteins to mitochondria via mitochondria-associated membranes. Rev. Med. Virol. 2009, 19:147-164.
77. Muruganandan S., et al. Adipocyte differentiation of bone marrow-derived mesenchymal stem cells: cross talk with the osteoblastogenic program. Cell. Mol. Life Sci. 2009, 66:236-253.
78. Sanchez V., et al. Accumulation of virion tegument and envelope proteins in a stable cytoplasmic compartment during human cytomegalovirus replication: characterization of a potential site of virus assembly. J. Virol. 2000, 74:975-986.
79. Sanchez V., et al. Human cytomegalovirus pp28 (UL99) localizes to a cytoplasmic compartment which overlaps the endoplasmic reticulum-golgi-intermediate compartment. J. Virol. 2000, 74:3842-3851.
80. Das S., et al. Three-dimensional structure of the human cytomegalovirus cytoplasmic virion assembly complex includes a reoriented secretory apparatus. J. Virol. 2007, 81:11861-11869.
81. Das S., Pellett P.E. Members of the HCMV US12 family of predicted heptaspanning membrane proteins have unique intracellular distributions, including association with the cytoplasmic virion assembly complex. Virology 2007, 361:263-273.
82. Homman-Loudiyi M., et al. Envelopment of human cytomegalovirus occurs by budding into Golgi-derived vacuole compartments positive for gB Rab 3, trans Golgi network 46, and mannosidase II. J. Virol. 2003, 77:3191-3203.
83. Theiler R.N., Compton T. Distinct glycoprotein O complexes arise in a post-Golgi compartment of cytomegalovirus-infected cells. J. Virol. 2002, 76:2890-2898.
84. Pignatelli S., et al. Cytomegalovirus primary envelopment at large nuclear membrane infoldings: what's new?. J. Virol. 2007, 81:7320-7321.
85. Severi B., et al. Human cytomegalovirus morphogenesis: an ultrastructural study of the late cytoplasmic phases. Arch. Virol. 1988, 98:51-64.
86. Severi B., et al. A study of the passage of human cytomegalovirus from the nucleus to the cytoplasm. Microbiologica 1979, 2:265-273.