Stealing the Keys to the Kitchen: Viral Manipulation of the Host Cell Metabolic Network

Trends in Microbiology

Volumn 23, Issue 12, 2015, Pages 789-798

  Goodwin, Christopher M ^a   Xu, Shihao ^a   Munger, Joshua ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Citric acid cycle; Energy; Fatty acid; Glycolysis; Immunity; Infection; Lipid; Metabolism; Virus

Indexed keywords

ABACAVIR; ACICLOVIR; CIDOFOVIR; EMTRICITABINE; ENTECAVIR; GANCICLOVIR; LAMIVUDINE; RIBAVIRIN; SOFOSBUVIR; TELBIVUDINE; TENOFOVIR; VALACICLOVIR; ZIDOVUDINE;

BIOMASS; CARCINOGENESIS; CATABOLISM; ENZYME ACTIVITY; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HERPES SIMPLEX VIRUS; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN CYTOMEGALOVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; METABOLIC REGULATION; METABOLISM; NONHUMAN; NUTRIENT UPTAKE; PRIORITY JOURNAL; REVIEW; VARICELLA ZOSTER VIRUS; VIRAL TROPISM; VIRION; VIRUS INFECTION; VIRUS REPLICATION; CHEMISTRY; CITRIC ACID CYCLE; GLYCOLYSIS; HUMAN; PROTEIN SYNTHESIS; VIRAL PHENOMENA AND FUNCTIONS; VIRUS;

CARCINOGENESIS; CITRIC ACID CYCLE; GLYCOLYSIS; HOST-PATHOGEN INTERACTIONS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; METABOLISM; PROTEIN BIOSYNTHESIS; VIRAL TROPISM; VIRION; VIRUS PHYSIOLOGICAL PHENOMENA; VIRUS REPLICATION; VIRUSES;

EID: 84945936970     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2015.08.007     Document Type: Review

References (97)

1. Das K., Arnold E. HIV-1 reverse transcriptase and antiviral drug resistance. Part 1. Curr. Opin. Virol. 2013, 3:111-118.
2. Menendez-Arias L., et al. Nucleoside/nucleotide analog inhibitors of hepatitis B virus polymerase: mechanism of action and resistance. Curr. Opin. Virol. 2014, 8:1-9.
3. Lee W.A., Martin J.C. Perspectives on the development of acyclic nucleotide analogs as antiviral drugs. Antivir. Res. 2006, 71:254-259.
4. Andrei G., et al. Novel inhibitors of human CMV. Curr. Opin. Investig. Drugs 2008, 9:132-145.
5. Li H.C., Lo S.Y. Hepatitis C virus: Virology, diagnosis and treatment. World J. Hepatol. 2015, 7:1377-1389.
6. Yogev O., et al. Kaposi's sarcoma herpesvirus microRNAs induce metabolic transformation of infected cells. PLoS Pathog. 2014, 10:e1004400.
7. 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.
8. Thai M., et al. Adenovirus E4ORF1-induced MYC activation promotes host cell anabolic glucose metabolism and virus replication. Cell Metab. 2014, 19:694-701.
9. Xiao L., et al. Targeting Epstein-Barr virus oncoprotein LMP1-mediated glycolysis sensitizes nasopharyngeal carcinoma to radiation therapy. Oncogene 2014, 33:4568-4578.
10. Fontaine K.A., et al. Dengue virus induces and requires glycolysis for optimal replication. J. Virol. 2015, 89:2358-2366.
11. Diamond D.L., et al. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog. 2010, 6:e1000719.
12. Ritter J., et al. Metabolic effects of influenza virus infection in cultured animal cells: Intra- and extracellular metabolite profiling. BMC Syst. Biol. 2010, 4:61.
13. Fontaine K.A., et al. Vaccinia virus requires glutamine but not glucose for efficient replication. J. Virol. 2014, 88:4366-4374.
14. Vastag L., et al. Divergent effects of human cytomegalovirus and herpes simplex virus-1 on cellular metabolism. PLoS Pathog. 2011, 7:e1002124.
15. Ramière C., et al. Hexokinase activity is increased by its interaction with Hepatitis C virus protein NS5A. J. Virol. 2014, 88:3246-3254.
16. McArdle J., et al. HCMV Targets the metabolic stress response through activation of AMPK whose activity is important for viral replication. PLoS Pathog. 2012, 8:e1002502.
17. Towler M.C., Hardie D.G. AMP-activated protein kinase in metabolic control and insulin signaling. Circ. Res. 2007, 100:328-341.
18. Yu Y., et al. ChREBP, a glucose-responsive transcriptional factor, enhances glucose metabolism to support biosynthesis in human cytomegalovirus-infected cells. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:1951-1956.
19. Chambers J.W., et al. Glutamine metabolism is essential for human cytomegalovirus infection. J. Virol. 2010, 84:1867-1873.
20. Khan M., et al. Mitochondrial dynamics and viral infections: A close nexus. Biochim. Biophys. Acta 2015, Published online January 13 2015. 10.1016/j.bbamcr.2014.12.040.
21. Yogev O., et al. Kaposi's sarcoma herpesvirus microRNAs induce metabolic transformation of infected cells. Plos Pathog. 2014, 10:e1004400.
22. Kim S.J., et al. Hepatitis C virus triggers mitochondrial fission and attenuates apoptosis to promote viral persistence. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:6413-6418.
23. Kim S.J., et al. Hepatitis B virus disrupts mitochondrial dynamics: induces fission and mitophagy to attenuate apoptosis. PLoS Pathog. 2013, 9:e1003722.
24. Arnoult D., et al. Cytomegalovirus cell death suppressor vMIA blocks Bax- but not Bak-mediated apoptosis by binding and sequestering Bax at mitochondria. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:7988-7993.
25. Spencer C.M., et al. Human cytomegalovirus induces the activity and expression of acetyl-coenzyme a carboxylase, a fatty acid biosynthetic enzyme whose inhibition attenuates viral replication. J. Virol. 2011, 85:5814-5824.
26. Greseth M.D., Traktman P. De novo fatty acid biosynthesis contributes significantly to establishment of a bioenergetically favorable environment for vaccinia virus infection. PLoS Pathog. 2014, 10:e1004021.
27. Yu Y., et al. Human cytomegalovirus infection induces adipocyte-like lipogenesis through activation of sterol regulatory element binding protein 1. J. Virol. 2012, 86:2942-2949.
28. Herker E., Ott M. Unique ties between hepatitis C virus replication and intracellular lipids. Trends Endocrinol. Metab. 2011, 22:241-248.
29. Syed G.H., et al. Hepatitis C virus hijacks host lipid metabolism. Trends Endocrinol. Metab. 2010, 21:33-40.
30. Kim Y., et al. Novel triacsin C analogs as potential antivirals against rotavirus infections. Eur. J. Med. Chem. 2012, 50:311-318.
31. Heaton N.S., et al. Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17345-17350.
32. Xu K., Nagy P.D. Expanding use of multi-origin subcellular membranes by positive-strand RNA viruses during replication. Curr. Opin. Virol. 2014, 9:119-126.
33. Kao Y.T., et al. Japanese encephalitis virus nonstructural protein NS5 interacts with mitochondrial trifunctional protein and impairs fatty acid beta-oxidation. PLoS Pathog. 2015, 11:e1004750.
34. Seo J.Y., Cresswell P. Viperin regulates cellular lipid metabolism during human cytomegalovirus infection. PLoS Pathog. 2013, 9:e1003497.
35. Rasmussen A.L., et al. Systems virology identifies a mitochondrial fatty acid oxidation enzyme, dodecenoyl coenzyme A delta isomerase, required for hepatitis C virus replication and likely pathogenesis. J. Virol. 2011, 85:11646-11654.
36. Tang W.C., et al. Rab18 facilitates dengue virus infection by targeting fatty acid synthase to sites of viral replication. J. Virol. 2014, 88:6793-6804.
37. Berger K.L., et al. Hepatitis C virus stimulates the phosphatidylinositol 4-kinase III alpha-dependent phosphatidylinositol 4-phosphate production that is essential for its replication. J. Virol. 2011, 85:8870-8883.
38. Roulin P.S., et al. Rhinovirus uses a phosphatidylinositol 4-phosphate/cholesterol counter-current for the formation of replication compartments at the ER-Golgi interface. Cell Host Microbe 2014, 16:677-690.
39. Chatel-Chaix L., Bartenschlager R. Dengue virus- and hepatitis C virus-induced replication and assembly compartments: the enemy inside--caught in the web. J. Virol. 2014, 88:5907-5911.
40. Xu K., Nagy P.D. RNA virus replication depends on enrichment of phosphatidylethanolamine at replication sites in subcellular membranes. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:E1782-E1791.
41. Barajas D., et al. Co-opted oxysterol-binding ORP and VAP proteins channel sterols to RNA virus replication sites via membrane contact sites. PLoS Pathog. 2014, 10:e1004388.
42. Liefhebber J.M., et al. Modulation of triglyceride and cholesterol ester synthesis impairs assembly of infectious hepatitis C virus. J. Biol. Chem. 2014, 289:21276-21288.
43. Soni S.P., Stahelin R.V. The Ebola virus matrix protein VP40 selectively induces vesiculation from phosphatidylserine-enriched membranes. J. Biol. Chem. 2014, 289:33590-33597.
44. Chen Y.H., et al. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 2015, 160:619-630.
45. Koyuncu E., et al. Saturated very long chain fatty acids are required for the production of infectious human cytomegalovirus progeny. PLoS Pathog. 2013, 9:e1003333.
46. Purdy J.G., et al. Fatty acid elongase 7 catalyzes lipidome remodeling essential for human cytomegalovirus replication. Cell Rep. 2015, 10:1375-1385.
47. Lalonde M.S., Sundquist W.I. How HIV finds the door. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18631-18632.
48. Saad J.S., et al. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:11364-11369.
49. Tang C., et al. Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:517-522.
50. Silva M.C., et al. Human cytomegalovirus UL99-encoded pp28 is required for the cytoplasmic envelopment of tegument-associated capsids. J. Virol. 2003, 77:10594-10605.
51. Seo J.Y., Britt W.J. Cytoplasmic envelopment of human cytomegalovirus requires the postlocalization function of tegument protein pp28 within the assembly compartment. J. Virol. 2007, 81:6536-6547.
52. Jones T.R., Lee S.W. An acidic cluster of human cytomegalovirus UL99 tegument protein is required for trafficking and function. J. Virol. 2004, 78:1488-1502.
53. Boscarino J.A., et al. Envelope protein palmitoylations are crucial for murine coronavirus assembly. J. Virol. 2008, 82:2989-2999.
54. Demers A., et al. Palmitoylation is required for intracellular trafficking of influenza B virus NB protein and efficient influenza B virus growth in vitro. J. Gen. Virol. 2014, 95:1211-1220.
55. Grantham M.L., et al. Palmitoylation of the influenza A virus M2 protein is not required for virus replication in vitro but contributes to virus virulence. J. Virol. 2009, 83:8655-8661.
56. Majeau N., et al. Palmitoylation of hepatitis C virus core protein is important for virion production. J. Biol. Chem. 2009, 284:33915-33925.
57. Naik N.G., Wu H.N. Mutation of putative N-glycosylation sites on dengue NS4B decreases RNA replication. J. Virol. 2015, 89:6746-6760.
58. Julithe R., et al. Modification of the hepatitis B virus envelope protein glycosylation pattern interferes with secretion of viral particles, infectivity, and susceptibility to neutralizing antibodies. J. Virol. 2014, 88:9049-9059.
59. Nakamura K., Compans R.W. Effects of glucosamine, 2-deoxyglucose, and tunicamycin on glycosylation, sulfation, and assembly of influenza viral proteins. Virology 1978, 84:303-319.
60. Luo S., et al. Contribution of N-linked glycans on HSV-2 gB to cell-cell fusion and viral entry. Virology 2015, 483:72-82.
61. DeVito S.R., et al. Cytomegalovirus-mediated activation of pyrimidine biosynthesis drives UDP-sugar synthesis to support viral protein glycosylation. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:18019-18024.
62. Machesky N.J., et al. Human Cytomegalovirus Regulates Bioactive Sphingolipids. J. Biol. Chem. 2008, 283:26148-26160.
63. Hirata Y., et al. Self-enhancement of hepatitis C virus replication by promotion of specific sphingolipid biosynthesis. PLoS Pathog. 2012, 8:e1002860.
64. Martín-Acebes M.A., et al. The composition of West Nile Virus lipid envelope unveils a role of sphingolipid metabolism in flavivirus biogenesis. J. Virol. 2014, 88:12041-12054.
65. Maceyka M., Spiegel S. Sphingolipid metabolites in inflammatory disease. Nature 2014, 510:58-67.
66. Santoro M.G. Antiviral activity of cyclopentenone prostanoids. Trends Microbiol. 1997, 5:276-281.
67. Clemente M.I., et al. Prostaglandin E2 reduces the release and infectivity of new cell-free virions and cell-to-cell HIV-1 transfer. PLoS ONE 2014, 9:e85230.
68. Speir E., et al. Aspirin attenuates cytomegalovirus infectivity and gene expression mediated by cyclooxygenase-2 in coronary artery smooth muscle cells. Circ. Res. 1998, 83:210-216.
69. Zhu H., et al. Inhibition of cyclooxygenase 2 blocks human cytomegalovirus replication. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:3932-3937.
70. Rue C.A., et al. A cyclooxygenase-2 homologue encoded by rhesus cytomegalovirus is a determinant for endothelial cell tropism. J. Virol. 2004, 78:12529-12536.
71. Coulombe F., et al. Targeted prostaglandin E2 inhibition enhances antiviral immunity through induction of type I interferon and apoptosis in macrophages. Immunity 2014, 40:554-568.
72. Diamond T.L., et al. Macrophage tropism of HIV-1 depends on efficient cellular dNTP utilization by reverse transcriptase. J. Biol. Chem. 2004, 279:51545-51553.
73. Amie S.M., et al. Intracellular nucleotide levels and the control of retroviral infections. Virology 2013, 436:247-254.
74. Goujon C., et al. Characterization of simian immunodeficiency virus SIVSM/human immunodeficiency virus type 2 Vpx function in human myeloid cells. J. Virol. 2008, 82:12335-12345.
75. Goujon C., et al. SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells. Retrovirology 2007, 4:2.
76. Laguette N., et al. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 2011, 474:654-657.
77. Lahouassa H., et al. SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat. Immunol. 2012, 13:223-228.
78. Koyuncu E., et al. Sirtuins are evolutionarily conserved viral restriction factors. mBio 2014, 5. e02249-02214.
79. Yamamoto H., et al. Sirtuin functions in health and disease. Mol. Endocrinol. 2007, 21:1745-1755.
80. Hallows W.C., et al. Regulation of glycolytic enzyme phosphoglycerate mutase-1 by Sirt1 protein-mediated deacetylation. J. Biol. Chem. 2012, 287:3850-3858.
81. Purushotham A., et al. Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab. 2009, 9:327-338.
82. Chalmin F., et al. Oxysterols regulate encephalitogenic CD4(+) T cell trafficking during central nervous system autoimmunity. J. Autoimmun. 2015, 56:45-55.
83. Gold E.S., et al. 25-Hydroxycholesterol acts as an amplifier of inflammatory signaling. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:10666-10671.
84. Xiang Y., et al. Identification of cholesterol 25-hydroxylase as a Novel Host restriction factor and a part of the primary innate immune responses against hepatitis C virus infection. J. Virol. 2015, 89:6805-6816.
85. Chen Y., et al. Interferon-inducible cholesterol-25-hydroxylase inhibits hepatitis C virus replication via distinct mechanisms. Sci. Rep. 2014, 4:7242.
86. Elliott M.R., et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009, 461:282-286.
87. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
88. Tong X., et al. The molecular determinants of de novo nucleotide biosynthesis in cancer cells. Curr. Opin. Genet. Dev. 2009, 19:32-37.
89. Kuhajda F.P. Fatty-acid synthase and human cancer: new perspectives on its role in tumor biology. Nutrition (Burbank Los Angeles County Calif.) 2000, 16:202-208.
90. Teng C.F., et al. Activation of ATP citrate lyase by mTOR signal induces disturbed lipid metabolism in hepatitis B virus pre-S2 mutant tumorigenesis. J. Virol. 2015, 89:605-614.
91. Lai D., et al. Localization of HPV-18 E2 at mitochondrial membranes induces ROS release and modulates host cell metabolism. PLoS ONE 2013, 8:e75625.
92. Mazurek S., et al. Effects of the human papilloma virus HPV-16 E7 oncoprotein on glycolysis and glutaminolysis: role of pyruvate kinase type M2 and the glycolytic-enzyme complex. Biochem. J. 2001, 356:247-256.
93. Mazurek S., et al. Metabolic cooperation between different oncogenes during cell transformation: interaction between activated ras and HPV-16 E7. Oncogene 2001, 20:6891-6898.
94. Ripoli M., et al. Hepatitis C virus-linked mitochondrial dysfunction promotes hypoxia-inducible factor 1 alpha-mediated glycolytic adaptation. J. Virol. 2010, 84:647-660.
95. Delgado T., et al. 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. 2010, 107:10696-10701.
96. Delgado T., et al. Global metabolic profiling of infection by an oncogenic virus: KSHV induces and requires lipogenesis for survival of latent infection. PLoS Pathog. 2012, 8:e1002866.
97. Boroughs L.K., DeBerardinis R.J. Metabolic pathways promoting cancer cell survival and growth. Nat. Cell Biol. 2015, 17:351-359.