Effects of interferons and viruses on metabolism

Frontiers in Immunology

Volumn 7, Issue DEC, 2016, Pages

  Fritsch, Stephanie Deborah ^a   Weichhart, Thomas ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Cholesterol synthesis; Fatty acid oxidation; Fatty acid synthesis; Glycolysis; Immunometabolism; MTOR; Oxidative phosphorylation

Indexed keywords

25 HYDROXYCHOLESTEROL; ARGININE; FLAVINE ADENINE NUCLEOTIDE; FRUCTOSE 6 PHOSPHATE; GUANOSINE TRIPHOSPHATE; INTERFERON; MAMMALIAN TARGET OF RAPAMYCIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; STAT PROTEIN; TRYPTOPHAN; URIDINE DIPHOSPHATE N ACETYLMURAMIC ACID;

AMINO ACID METABOLISM; ANAEROBIC METABOLISM; CELL METABOLISM; CELL PROLIFERATION; CHIKUNGUNYA VIRUS; ENERGY METABOLISM; FATTY ACID OXIDATION; HUMAN; LIPID HOMEOSTASIS; LIPOGENESIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICROENVIRONMENT; MULTIPLE SCLEROSIS; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVIEW; VIRUS INFECTION; VIRUS REPLICATION; ZIKA VIRUS;

EID: 85009376389     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00630     Document Type: Review

References (150)

1. Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev (2001) 14:778-809. doi:10.1128/CMR.14.4.778-809.2001
2. McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A. Type I interferons in infectious disease. Nat Rev Immunol (2015) 15:87-103. doi:10.1038/nri3787
3. Hu X, Ivashkiv LB. Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity (2009) 31:539-50. doi:10.1016/j.immuni.2009.09.002
4. Fensterl V, Sen GC. Interferons and viral infections. Biofactors (2009) 35:14-20. doi:10.1002/biof.6
5. Weichhart T, Hengstschlager M, Linke M. Regulation of innate immune cell function by mTOR. Nat Rev Immunol (2015) 15:599-614. doi:10.1038/nri3901
6. Cao W, Manicassamy S, Tang H, Kasturi SP, Pirani A, Murthy N, et al. Toll-like receptor-mediated induction of type I interferon in plasmacytoid dendritic cells requires the rapamycin-sensitive PI(3)K-mTOR-p70S6K pathway. Nat Immunol (2008) 9:1157-64. doi:10.1038/ni.1645
7. Schmitz F, Heit A, Dreher S, Eisenacher K, Mages J, Haas T, et al. Mammalian target of rapamycin (mTOR) orchestrates the defense program of innate immune cells. Eur J Immunol (2008) 38:2981-92. doi:10.1002/eji.200838761
8. Jaramillo M, Gomez MA, Larsson O, Shio MT, Topisirovic I, Contreras I, et al. Leishmania repression of host translation through mTOR cleavage is required for parasite survival and infection. Cell Host Microbe (2011) 9:331-41. doi:10.1016/j.chom.2011.03.008
9. Colina R, Costa-Mattioli M, Dowling RJ, Jaramillo M, Tai LH, Breitbach CJ, et al. Translational control of the innate immune response through IRF-7. Nature (2008) 452:323-8. doi:10.1038/nature06730
10. Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nat Rev Immunol (2014) 14:36-49. doi:10.1038/nri3581
11. Chow KT, Gale M Jr. SnapShot: interferon signaling. Cell (2015) 163:1808-e1. doi:10.1016/j.cell.2015.12.008
12. Levy DE, Garcia-Sastre A. The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine Growth Factor Rev (2001) 12:143-56. doi:10.1016/S1359-6101(00)00027-7
13. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol (2008) 8:559-68. doi:10.1038/nri2314
14. Haller O, Staeheli P, Schwemmle M, Kochs G. Mx GTPases: dynamin-like antiviral machines of innate immunity. Trends Microbiol (2015) 23:154-63. doi:10.1016/j.tim.2014.12.003
15. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science (2009) 324:1029-33. doi:10.1126/science.1160809
16. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab (2008) 7:11-20. doi:10.1016/j.cmet.2007.10.002
17. Rich PR. The molecular machinery of Keilin's respiratory chain. Biochem Soc Trans (2003) 31:1095-105. doi:10.1042/
18. DeBerardinis RJ, Cheng T. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene (2010) 29:313-24. doi:10.1038/onc.2009.358
19. Abo Alrob O, Lopaschuk GD. Role of CoA and acetyl-CoA in regulating cardiac fatty acid and glucose oxidation. Biochem Soc Trans (2014) 42:1043-51. doi:10.1042/BST20140094
20. Cantor JR, Sabatini DM. Cancer cell metabolism: one hallmark, many faces. Cancer Discov (2012) 2:881-98. doi:10.1158/2159-8290.CD-12-0345
21. Lunt SY, Vander Heiden MG. Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol (2011) 27:441-64. doi:10.1146/annurev-cellbio-092910-154237
22. Warburg O. On the origin of cancer cells. Science (1956) 123:309-14. doi:10.1126/science.123.3191.309
23. Hosios AM, Hecht VC, Danai LV, Johnson MO, Rathmell JC, Steinhauser ML, et al. Amino acids rather than glucose account for the majority of cell mass in proliferating mammalian cells. Dev Cell (2016) 36:540-9. doi:10.1016/j.devcel.2016.02.012
24. Wellen KE, Thompson CB. A two-way street: reciprocal regulation of metabolism and signalling. Nat Rev Mol Cell Biol (2012) 13:270-6. doi:10.1038/nrm3305
25. Derynck R, Content J, DeClercq E, Volckaert G, Tavernier J, Devos R, et al. Isolation and structure of a human fibroblast interferon gene. Nature (1980) 285:542-7. doi:10.1038/285542a0
26. Vigerust DJ, Shepherd VL. Virus glycosylation: role in virulence and immune interactions. Trends Microbiol (2007) 15:211-8. doi:10.1016/j.tim.2007.03.003
27. Yang C, Ko B, Hensley CT, Jiang L, Wasti AT, Kim J, et al. Glutamine oxidation maintains the TCA cycle and cell survival during impaired mitochondrial pyruvate transport. Mol Cell (2014) 56:414-24. doi:10.1016/j.molcel.2014.09.025
28. Le A, Lane AN, Hamaker M, Bose S, Gouw A, Barbi J, et al. Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab (2012) 15:110-21. doi:10.1016/j.cmet.2011.12.009
29. Jones RG, Thompson CB. Tumor suppressors and cell metabolism: a recipe for cancer growth. Genes Dev (2009) 23:537-48. doi:10.1101/gad.1756509
30. Infantino V, Convertini P, Cucci L, Panaro MA, Di Noia MA, Calvello R, et al. The mitochondrial citrate carrier: a new player in inflammation. Biochem J (2011) 438:433-6. doi:10.1042/BJ20111275
31. Infantino V, Iacobazzi V, Palmieri F, Menga A. ATP-citrate lyase is essential for macrophage inflammatory response. Biochem Biophys Res Commun (2013) 440:105-11. doi:10.1016/j.bbrc.2013.09.037
32. Burke JD, Platanias LC, Fish EN. Beta interferon regulation of glucose metabolism is PI3K/Akt dependent and important for antiviral activity against coxsackievirus B3. J Virol (2014) 88:3485-95. doi:10.1128/JVI.02649-13
33. Pantel A, Teixeira A, Haddad E, Wood EG, Steinman RM, Longhi MP. Direct type I IFN but not MDA5/TLR3 activation of dendritic cells is required for maturation and metabolic shift to glycolysis after poly IC stimulation. PLoS Biol (2014) 12:e1001759. doi:10.1371/journal.pbio.1001759
34. Grunert T, Leitner NR, Marchetti-Deschmann M, Miller I, Wallner B, Radwan M, et al. A comparative proteome analysis links tyrosine kinase 2 (Tyk2) to the regulation of cellular glucose and lipid metabolism in response to poly(I:C). J Proteomics (2011) 74:2866-80. doi:10.1016/j.jprot.2011.07.006
35. Hedl M, Yan J, Abraham C. IRF5 and IRF5 disease-risk variants increase glycolysis and human M1 macrophage polarization by regulating proximal signaling and Akt2 activation. Cell Rep (2016) 16:2442-55. doi:10.1016/j.celrep.2016.07.060
36. Pitroda SP, Wakim BT, Sood RF, Beveridge MG, Beckett MA, MacDermed DM, et al. STAT1-dependent expression of energy metabolic pathways links tumour growth and radioresistance to the Warburg effect. BMC Med (2009) 7:68. doi:10.1186/1741-7015-7-68
37. Lewis JA, Huq A, Najarro P. Inhibition of mitochondrial function by interferon. J Biol Chem (1996) 271:13184-90. doi:10.1074/jbc.271.22.13184
38. Haghikia A, Faissner S, Pappas D, Pula B, Akkad DA, Arning L, et al. Interferon-beta affects mitochondrial activity in CD4+ lymphocytes: implications for mechanism of action in multiple sclerosis. Mult Scler (2015) 21:1262-70. doi:10.1177/1352458514561909
39. Swiecki M, Colonna M. The multifaceted biology of plasmacytoid dendritic cells. Nat Rev Immunol (2015) 15:471-85. doi:10.1038/nri3865
40. Wu D, Sanin DE, Everts B, Chen Q, Qiu J, Buck MD, et al. Type 1 interferons induce changes in core metabolism that are critical for immune function. Immunity (2016) 44:1325-36. doi:10.1016/j.immuni.2016.06.006
41. Bajwa G, DeBerardinis RJ, Shao B, Hall B, Farrar JD, Gill MA. Cutting edge: critical role of glycolysis in human plasmacytoid dendritic cell antiviral responses. J Immunol (2016) 196:2004-9. doi:10.4049/jimmunol.1501557
42. Memon RA, Feingold KR, Moser AH, Doerrler W, Grunfeld C. In vivo effects of interferon-alpha and interferon-gamma on lipolysis and ketogenesis. Endocrinology (1992) 131:1695-702. doi:10.1210/endo.131.4.1396316
43. Vazquez A, Liu J, Zhou Y, Oltvai ZN. Catabolic efficiency of aerobic glycolysis: the Warburg effect revisited. BMC Syst Biol (2010) 4:58. doi:10.1186/1752-0509-4-58
44. Jha AK, Huang SC, Sergushichev A, Lampropoulou V, Ivanova Y, Loginicheva E, et al. Network integration of parallel metabolic and transcriptional data reveals metabolic modules that regulate macrophage polarization. Immunity (2015) 42:419-30. doi:10.1016/j.immuni.2015.02.005
45. Chouchani ET, Pell VR, Gaude E, Aksentijevic D, Sundier SY, Robb EL, et al. Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature (2014) 515:431-5. doi:10.1038/nature13909
46. Paiva CN, Bozza MT. Are reactive oxygen species always detrimental to pathogens? Antioxid Redox Signal (2014) 20:1000-37. doi:10.1089/ars.2013.5447
47. Vlahos R, Stambas J, Selemidis S. Suppressing production of reactive oxygen species (ROS) for influenza A virus therapy. Trends Pharmacol Sci (2012) 33:3-8. doi:10.1016/j.tips.2011.09.001
48. Naujoks J, Tabeling C, Dill BD, Hoffmann C, Brown AS, Kunze M, et al. IFNs modify the proteome of Legionella-containing vacuoles and restrict infection via IRG1-derived itaconic acid. PLoS Pathog (2016) 12:e1005408. doi:10.1371/journal.ppat.1005408
49. Strelko CL, Lu W, Dufort FJ, Seyfried TN, Chiles TC, Rabinowitz JD, et al. Itaconic acid is a mammalian metabolite induced during macrophage activation. J Am Chem Soc (2011) 133:16386-9. doi:10.1021/ja2070889
50. Michelucci A, Cordes T, Ghelfi J, Pailot A, Reiling N, Goldmann O, et al. Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production. Proc Natl Acad Sci U S A (2013) 110:7820-5. doi:10.1073/pnas.1218599110
51. Lampropoulou V, Sergushichev A, Bambouskova M, Nair S, Vincent EE, Loginicheva E, et al. Itaconate links inhibition of succinate dehydrogenase with macrophage metabolic remodeling and regulation of inflammation. Cell Metab (2016) 24:158-66. doi:10.1016/j.cmet.2016.06.004
52. Nemeth B, Doczi J, Csete D, Kacso G, Ravasz D, Adams D, et al. Abolition of mitochondrial substrate-level phosphorylation by itaconic acid produced by LPS-induced Irg1 expression in cells of murine macrophage lineage. FASEB J (2016) 30:286-300. doi:10.1096/fj.15-279398
53. Yu Y, Clippinger AJ, Alwine JC. Viral effects on metabolism: changes in glucose and glutamine utilization during human cytomegalovirus infection. Trends Microbiol (2011) 19:360-7. doi:10.1016/j.tim.2011.04.002
54. Inoue T, Tsai B. How viruses use the endoplasmic reticulum for entry, replication, and assembly. Cold Spring Harb Perspect Biol (2013) 5:a013250. doi:10.1101/cshperspect.a013250
55. Miller S, Krijnse-Locker J. Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol (2008) 6:363-74. doi:10.1038/nrmicro1890
56. den Boon JA, Ahlquist P. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol (2010) 64:241-56. doi:10.1146/annurev.micro.112408.134012
57. Chukkapalli V, Heaton NS, Randall G. Lipids at the interface of virus-host interactions. Curr Opin Microbiol (2012) 15:512-8. doi:10.1016/j.mib.2012.05.013
58. Heaton NS, Randall G. Multifaceted roles for lipids in viral infection. Trends Microbiol (2011) 19:368-75. doi:10.1016/j.tim.2011.03.007
59. Munger J, Bennett BD, Parikh A, Feng XJ, McArdle J, Rabitz HA, et al. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat Biotechnol (2008) 26:1179-86. doi:10.1038/nbt.1500
60. Spencer CM, Schafer XL, Moorman NJ, Munger J. 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) 85:5814-24. doi:10.1128/JVI.02630-10
61. Zaidi N, Swinnen JV, Smans K. ATP-citrate lyase: a key player in cancer metabolism. Cancer Res (2012) 72:3709-14. doi:10.1158/0008-5472.CAN-11-4112
62. Abramson HN. The lipogenesis pathway as a cancer target. J Med Chem (2011) 54:5615-38. doi:10.1021/jm2005805
63. Gaunt ER, Cheung W, Richards JE, Lever A, Desselberger U. Inhibition of rotavirus replication by downregulation of fatty acid synthesis. J Gen Virol (2013) 94:1310-7. doi:10.1099/vir.0.050146-0
64. Merino-Ramos T, Vazquez-Calvo A, Casas J, Sobrino F, Saiz JC, Martin-Acebes MA. Modification of the host cell lipid metabolism induced by hypolipidemic drugs targeting the acetyl coenzyme A carboxylase impairs West Nile virus replication. Antimicrob Agents Chemother (2016) 60:307-15. doi:10.1128/AAC.01578-15
65. Sanchez EL, Lagunoff M. Viral activation of cellular metabolism. Virology (2015) 47(9-480):609-18. doi:10.1016/j.virol.2015.02.038
66. Moser TS, Schieffer D, Cherry S. AMP-activated kinase restricts Rift Valley fever virus infection by inhibiting fatty acid synthesis. PLoS Pathog (2012) 8:e1002661. doi:10.1371/journal.ppat.1002661
67. Xie W, Wang L, Dai Q, Yu H, He X, Xiong J, et al. Activation of AMPK restricts coxsackievirus B3 replication by inhibiting lipid accumulation. J Mol Cell Cardiol (2015) 85:155-67. doi:10.1016/j.yjmcc.2015.05.021
68. Coulombe F, Jaworska J, Verway M, Tzelepis F, Massoud A, Gillard J, et al. Targeted prostaglandin E2 inhibition enhances antiviral immunity through induction of type I interferon and apoptosis in macrophages. Immunity (2014) 40:554-68. doi:10.1016/j.immuni.2014.02.013
69. Greseth MD, 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. doi:10.1371/journal.ppat.1004021
70. Heaton NS, Randall G. Dengue virus-induced autophagy regulates lipid metabolism. Cell Host Microbe (2010) 8:422-32. doi:10.1016/j.chom.2010.10.006
71. Heaton NS, Perera R, Berger KL, Khadka S, Lacount DJ, Kuhn RJ, 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) 107:17345-50. doi:10.1073/pnas.1010811107
72. Mackenzie JM, Khromykh AA, Parton RG. Cholesterol manipulation by West Nile virus perturbs the cellular immune response. Cell Host Microbe (2007) 2:229-39. doi:10.1016/j.chom.2007.09.003
73. Park CY, Jun HJ, Wakita T, Cheong JH, Hwang SB. Hepatitis C virus nonstructural 4B protein modulates sterol regulatory element-binding protein signaling via the AKT pathway. J Biol Chem (2009) 284:9237-46. doi:10.1074/jbc.M808773200
74. Robinzon S, Dafa-Berger A, Dyer MD, Paeper B, Proll SC, Teal TH, et al. Impaired cholesterol biosynthesis in a neuronal cell line persistently infected with measles virus. J Virol (2009) 83:5495-504. doi:10.1128/JVI.01880-08
75. Zheng YH, Plemenitas A, Fielding CJ, Peterlin BM. Nef increases the synthesis of and transports cholesterol to lipid rafts and HIV-1 progeny virions. Proc Natl Acad Sci U S A (2003) 100:8460-5. doi:10.1073/pnas.1437453100
76. Rothwell C, Lebreton A, Young Ng C, Lim JY, Liu W, Vasudevan S, et al. Cholesterol biosynthesis modulation regulates dengue viral replication. Virology (2009) 389:8-19. doi:10.1016/j.virol.2009.03.025
77. Mohan KV, Muller J, Atreya CD. Defective rotavirus particle assembly in lovastatin-treated MA104 cells. Arch Virol (2008) 153:2283-90. doi:10.1007/s00705-008-0261-0
78. Bader T, Fazili J, Madhoun M, Aston C, Hughes D, Rizvi S, et al. Fluvastatin inhibits hepatitis C replication in humans. Am J Gastroenterol (2008) 103:1383-9. doi:10.1111/j.1572-0241.2008.01876.x
79. Cohen JI. HMG CoA reductase inhibitors (statins) to treat Epstein-Barr virus-driven lymphoma. Br J Cancer (2005) 92:1593-8. doi:10.1038/sj.bjc.6602561
80. del Real G, Jimenez-Baranda S, Mira E, Lacalle RA, Lucas P, Gomez-Mouton C, et al. Statins inhibit HIV-1 infection by down-regulating Rho activity. J Exp Med (2004) 200:541-7. doi:10.1084/jem.20040061
81. Potena L, Frascaroli G, Grigioni F, Lazzarotto T, Magnani G, Tomasi L, et al. Hydroxymethyl-glutaryl coenzyme a reductase inhibition limits cytomegalovirus infection in human endothelial cells. Circulation (2004) 109:532-6. doi:10.1161/01.CIR.0000109485.79183.81
82. Dorobantu C, Macovei A, Lazar C, Dwek RA, Zitzmann N, Branza-Nichita N. Cholesterol depletion of hepatoma cells impairs hepatitis B virus envelopment by altering the topology of the large envelope protein. J Virol (2011) 85:13373-83. doi:10.1128/JVI.05423-11
83. Blanc M, Hsieh WY, Robertson KA, Watterson S, Shui G, Lacaze P, et al. Host defense against viral infection involves interferon mediated down-regulation of sterol biosynthesis. PLoS Biol (2011) 9:e1000598. doi:10.1371/journal.pbio.1000598
84. York AG, Williams KJ, Argus JP, Zhou QD, Brar G, Vergnes L, et al. Limiting cholesterol biosynthetic flux spontaneously engages type I IFN signaling. Cell (2015) 163:1716-29. doi:10.1016/j.cell.2015.11.045
85. Brown MS, Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell (1997) 89:331-40. doi:10.1016/S0092-8674(00)80213-5
86. Hornung V, Hartmann R, Ablasser A, Hopfner KP. OAS proteins and cGAS: unifying concepts in sensing and responding to cytosolic nucleic acids. Nat Rev Immunol (2014) 14:521-8. doi:10.1038/nri3719
87. Pfeffer LM, Kwok BC, Landsberger FR, Tamm I. Interferon stimulates cholesterol and phosphatidylcholine synthesis but inhibits cholesterol ester synthesis in HeLa-S3 cells. Proc Natl Acad Sci U S A (1985) 82:2417-21. doi:10.1073/pnas.82.8.2417
88. Cyster JG, Dang EV, Reboldi A, Yi T. 25-Hydroxycholesterols in innate and adaptive immunity. Nat Rev Immunol (2014) 14:731-43. doi:10.1038/nri3755
89. Blanc M, Hsieh WY, Robertson KA, Kropp KA, Forster T, Shui G, et al. The transcription factor STAT-1 couples macrophage synthesis of 25-hydroxycholesterol to the interferon antiviral response. Immunity (2013) 38:106-18. doi:10.1016/j.immuni.2012.11.004
90. Anggakusuma, Romero-Brey I, Berger C, Colpitts CC, Boldanova T, Engelmann M, et al. Interferon-inducible cholesterol-25-hydroxylase restricts hepatitis C virus replication through blockage of membranous web formation. Hepatology (2015) 62:702-14. doi:10.1002/hep.27913
91. Liu SY, Aliyari R, Chikere K, Li G, Marsden MD, Smith JK, et al. Interferon-inducible cholesterol-25-hydroxylase broadly inhibits viral entry by production of 25-hydroxycholesterol. Immunity (2013) 38:92-105. doi:10.1016/j.immuni.2012.11.005
92. Bougnoux P, Salem N, Lyons C, Hoffman T. Alteration in the membrane fatty acid composition of human lymphocytes and cultured transformed cells induced by interferon. Mol Immunol (1985) 22:1107-13. doi:10.1016/0161-5890(85)90114-2
93. Pfeffer LM, Landsberger FR, Tamm I. Beta-interferon-induced time-dependent changes in the plasma membrane lipid bilayer of cultured cells. J Interferon Res (1981) 1:613-20. doi:10.1089/jir.1981.1.613
94. Furlong ST, Mednis A, Remold HG. Interferon-gamma stimulates lipid metabolism in human monocytes. Cell Immunol (1992) 143:108-17. doi:10.1016/0008-8749(92)90009-E
95. Chatterjee S, Cheung HC, Hunter E. Interferon inhibits Sendai virus-induced cell fusion: an effect on cell membrane fluidity. Proc Natl Acad Sci U S A (1982) 79:835-9. doi:10.1073/pnas.79.3.835
96. Tanaka H, Miyano M, Ueda H, Fukui K, Ichinose M. Changes in serum and red blood cell membrane lipids in patients treated with interferon ribavirin for chronic hepatitis C. Clin Exp Med (2005) 5:190-5. doi:10.1007/s10238-005-0085-0
97. Reboldi A, Dang EV, McDonald JG, Liang G, Russell DW, Cyster JG. Inflammation. 25-hydroxycholesterol suppresses interleukin-1-driven inflammation downstream of type I interferon. Science (2014) 345:679-84. doi:10.1126/science.1254790
98. Guarda G, Braun M, Staehli F, Tardivel A, Mattmann C, Forster I, et al. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity (2011) 34:213-23. doi:10.1016/j.immuni.2011.02.006
99. Jamieson AM, Yu S, Annicelli CH, Medzhitov R. Influenza virus-induced glucocorticoids compromise innate host defense against a secondary bacterial infection. Cell Host Microbe (2010) 7:103-14. doi:10.1016/j.chom.2010.01.010
100. Zwaferink H, Stockinger S, Hazemi P, Lemmens-Gruber R, Decker T. IFN-beta increases listeriolysin O-induced membrane permeabilization and death of macrophages. J Immunol (2008) 180:4116-23. doi:10.4049/jimmunol.180.6.4116
101. Koberlin MS, Heinz LX, Superti-Furga G. Functional crosstalk between membrane lipids and TLR biology. Curr Opin Cell Biol (2016) 39:28-36. doi:10.1016/j.ceb.2016.01.010
102. Ramani D, De Bandt JP, Cynober L. Aliphatic polyamines in physiology and diseases. Clin Nutr (2014) 33:14-22. doi:10.1016/j.clnu.2013.09.019
103. Minois N, Carmona-Gutierrez D, Madeo F. Polyamines in aging and disease. Aging (Albany NY) (2011) 3:716-32. doi:10.18632/aging.100361
104. Mounce BC, Poirier EZ, Passoni G, Simon-Loriere E, Cesaro T, Prot M, et al. Interferon-induced spermidine-spermine acetyltransferase and polyamine depletion restrict Zika and chikungunya viruses. Cell Host Microbe (2016) 20:167-77. doi:10.1016/j.chom.2016.06.011
105. Bogdan C. Nitric oxide synthase in innate and adaptive immunity: an update. Trends Immunol (2015) 36:161-78. doi:10.1016/j.it.2015.01.003
106. Reiss CS, Komatsu T. Does nitric oxide play a critical role in viral infections? J Virol (1998) 72:4547-51.
107. Uehara EU, Shida Bde S, de Brito CA. Role of nitric oxide in immune responses against viruses: beyond microbicidal activity. Inflamm Res (2015) 64:845-52. doi:10.1007/s00011-015-0857-2
108. Colasanti M, Persichini T, Venturini G, Ascenzi P. S-nitrosylation of viral proteins: molecular bases for antiviral effect of nitric oxide. IUBMB Life (1999) 48:25-31. doi:10.1080/713803459
109. Saura M, Zaragoza C, McMillan A, Quick RA, Hohenadl C, Lowenstein JM, et al. An antiviral mechanism of nitric oxide: inhibition of a viral protease. Immunity (1999) 10:21-8. doi:10.1016/S1074-7613(00)80003-5
110. Hu J, Mahmoud MI, el-Fakahany EE. Polyamines inhibit nitric oxide synthase in rat cerebellum. Neurosci Lett (1994) 175:41-5. doi:10.1016/0304-3940(94)91073-1
111. Dorhoi A, Yeremeev V, Nouailles G, Weiner J III, Jorg S, Heinemann E, et al. Type I IFN signaling triggers immunopathology in tuberculosis-susceptible mice by modulating lung phagocyte dynamics. Eur J Immunol (2014) 44:2380-93. doi:10.1002/eji.201344219
112. Monteleone G, Pender SL, Wathen NC, MacDonald TT. Interferon-alpha drives T cell-mediated immunopathology in the intestine. Eur J Immunol (2001) 31:2247-55. doi:10.1002/1521-4141(200108)31:8<2247::AID-IMMU2247>3.0.CO;2-4
113. Yim HY, Yang Y, Lim JS, Lee MS, Zhang DE, Kim KI. The mitochondrial pathway and reactive oxygen species are critical contributors to interferon-alpha/beta-mediated apoptosis in Ubp43-deficient hematopoietic cells. Biochem Biophys Res Commun (2012) 423:436-40. doi:10.1016/j.bbrc.2012.05.154
114. Watanabe Y, Suzuki O, Haruyama T, Akaike T. Interferon-gamma induces reactive oxygen species and endoplasmic reticulum stress at the hepatic apoptosis. J Cell Biochem (2003) 89:244-53. doi:10.1002/jcb.10501
115. Burrack KS, Morrison TE. The role of myeloid cell activation and arginine metabolism in the pathogenesis of virus-induced diseases. Front Immunol (2014) 5:428. doi:10.3389/fimmu.2014.00428
116. Pryor WA, Squadrito GL. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am J Physiol (1995) 268:L699-722.
117. Bhattacharya A, Hegazy AN, Deigendesch N, Kosack L, Cupovic J, Kandasamy RK, et al. Superoxide dismutase 1 protects hepatocytes from type I interferon-driven oxidative damage. Immunity (2015) 43:974-86. doi:10.1016/j.immuni.2015.10.013
118. Miao L, St Clair DK. Regulation of superoxide dismutase genes: implications in disease. Free Radic Biol Med (2009) 47:344-56. doi:10.1016/j.freeradbiomed.2009.05.018
119. Yeung AW, Terentis AC, King NJ, Thomas SR. Role of indoleamine 2, 3-dioxygenase in health and disease. Clin Sci (Lond) (2015) 129:601-72. doi:10.1042/CS20140392
120. Pfefferkorn ER. Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc Natl Acad Sci U S A (1984) 81:908-12. doi:10.1073/pnas.81.3.908
121. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol (2004) 4:762-74. doi:10.1038/nri1457
122. Yoshida R, Imanishi J, Oku T, Kishida T, Hayaishi O. Induction of pulmonary indoleamine 2, 3-dioxygenase by interferon. Proc Natl Acad Sci U S A (1981) 78:129-32. doi:10.1073/pnas.78.1.129
123. Yasui H, Takai K, Yoshida R, Hayaishi O. Interferon enhances tryptophan metabolism by inducing pulmonary indoleamine 2, 3-dioxygenase: its possible occurrence in cancer patients. Proc Natl Acad Sci U S A (1986) 83:6622-6. doi:10.1073/pnas.83.17.6622
124. Schmidt SV, Schultze JL. New insights into IDO biology in bacterial and viral infections. Front Immunol (2014) 5:384. doi:10.3389/fimmu.2014.00384
125. Blohmke CJ, Darton TC, Jones C, Suarez NM, Waddington CS, Angus B, et al. Interferon-driven alterations of the host's amino acid metabolism in the pathogenesis of typhoid fever. J Exp Med (2016) 213:1061-77. doi:10.1084/jem.20151025
126. Yoshida R, Urade Y, Tokuda M, Hayaishi O. Induction of indoleamine 2, 3-dioxygenase in mouse lung during virus infection. Proc Natl Acad Sci U S A (1979) 76:4084-6. doi:10.1073/pnas.76.8.4084
127. Huang L, Li L, Klonowski KD, Tompkins SM, Tripp RA, Mellor AL. Induction and role of indoleamine 2, 3 dioxygenase in mouse models of influenza a virus infection. PLoS One (2013) 8:e66546. doi:10.1371/journal.pone.0066546
128. Hoshi M, Saito K, Hara A, Taguchi A, Ohtaki H, Tanaka R, et al. The absence of IDO upregulates type I IFN production, resulting in suppression of viral replication in the retrovirus-infected mouse. J Immunol (2010) 185:3305-12. doi:10.4049/jimmunol.0901150
129. Silvera D, Formenti SC, Schneider RJ. Translational control in cancer. Nat Rev Cancer (2010) 10:254-66. doi:10.1038/nrc2824
130. Jovanovic M, Rooney MS, Mertins P, Przybylski D, Chevrier N, Satija R, et al. Immunogenetics. Dynamic profiling of the protein life cycle in response to pathogens. Science (2015) 347:1259038. doi:10.1126/science.1259038
131. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature (2011) 472:481-5. doi:10.1038/nature09907
132. Platanias LC. Mechanisms of type-I-and type-II-interferon-mediated signalling. Nat Rev Immunol (2005) 5:375-86. doi:10.1038/nri1604
133. Kroczynska B, Mehrotra S, Arslan AD, Kaur S, Platanias LC. Regulation of interferon-dependent mRNA translation of target genes. J Interferon Cytokine Res (2014) 34:289-96. doi:10.1089/jir.2013.0148
134. Kaur S, Kroczynska B, Sharma B, Sassano A, Arslan AD, Majchrzak-Kita B, et al. Critical roles for Rictor/Sin1 complexes in interferon-dependent gene transcription and generation of antiproliferative responses. J Biol Chem (2014) 289:6581-91. doi:10.1074/jbc.M113.537852
135. Kroczynska B, Rafidi RL, Majchrzak-Kita B, Kosciuczuk EM, Blyth GT, Jemielity J, et al. Interferon gamma (IFNgamma) signaling via mechanistic target of rapamycin complex 2 (mTORC2) and regulatory effects in the generation of type II interferon biological responses. J Biol Chem (2016) 291:2389-96. doi:10.1074/jbc.M115.664995
136. Su X, Yu Y, Zhong Y, Giannopoulou EG, Hu X, Liu H, et al. Interferon-gamma regulates cellular metabolism and mRNA translation to potentiate macrophage activation. Nat Immunol (2015) 16:838-49. doi:10.1038/ni.3205
137. Cheng SC, Scicluna BP, Arts RJ, Gresnigt MS, Lachmandas E, Giamarellos-Bourboulis EJ, et al. Broad defects in the energy metabolism of leukocytes underlie immunoparalysis in sepsis. Nat Immunol (2016) 17:406-13. doi:10.1038/ni.3398
138. Shimobayashi M, Hall MN. Making new contacts: the mTOR network in metabolism and signalling crosstalk. Nat Rev Mol Cell Biol (2014) 15:155-62. doi:10.1038/nrm3757
139. Herdy B, Jaramillo M, Svitkin YV, Rosenfeld AB, Kobayashi M, Walsh D, et al. Translational control of the activation of transcription factor NF-kappaB and production of type I interferon by phosphorylation of the translation factor eIF4E. Nat Immunol (2012) 13:543-50. doi:10.1038/ni.2291
140. Schott J, Reitter S, Philipp J, Haneke K, Schafer H, Stoecklin G. Translational regulation of specific mRNAs controls feedback inhibition and survival during macrophage activation. PLoS Genet (2014) 10:e1004368. doi:10.1371/journal.pgen.1004368
141. Ivanov SS, Roy CR. Pathogen signatures activate a ubiquitination pathway that modulates the function of the metabolic checkpoint kinase mTOR. Nat Immunol (2013) 14:1219-28. doi:10.1038/ni.2740
142. Efeyan A, Zoncu R, Sabatini DM. Amino acids and mTORC1: from lysosomes to disease. Trends Mol Med (2012) 18:524-33. doi:10.1016/j.molmed.2012.05.007
143. Hara K, Yonezawa K, Weng QP, Kozlowski MT, Belham C, Avruch J. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J Biol Chem (1998) 273:14484-94. doi:10.1074/jbc.273.23.14484
144. Li P, Zhao Y, Wu X, Xia M, Fang M, Iwasaki Y, et al. Interferon gamma (IFN-gamma) disrupts energy expenditure and metabolic homeostasis by suppressing SIRT1 transcription. Nucleic Acids Res (2012) 40:1609-20. doi:10.1093/nar/gkr984
145. Mentch SJ, Mehrmohamadi M, Huang L, Liu X, Gupta D, Mattocks D, et al. Histone methylation dynamics and gene regulation occur through the sensing of one-carbon metabolism. Cell Metab (2015) 22:861-73. doi:10.1016/j.cmet.2015.08.024
146. Choudhary C, Weinert BT, Nishida Y, Verdin E, Mann M. The growing landscape of lysine acetylation links metabolism and cell signalling. Nat Rev Mol Cell Biol (2014) 15:536-50. doi:10.1038/nrm3841
147. O'Neill LA, Kishton RJ, Rathmell J. A guide to immunometabolism for immunologists. Nat Rev Immunol (2016) 16:553-65. doi:10.1038/nri.2016.70
148. Nomura M, Liu J, Rovira II, Gonzalez-Hurtado E, Lee J, Wolfgang MJ, et al. Fatty acid oxidation in macrophage polarization. Nat Immunol (2016) 17:216-7. doi:10.1038/ni.3366
149. Assmann N, Finlay DK. Metabolic regulation of immune responses: therapeutic opportunities. J Clin Invest (2016) 126:2031-9. doi:10.1172/JCI83005
150. Coe DJ, Kishore M, Marelli-Berg F. Metabolic regulation of regulatory T cell development and function. Front Immunol (2014) 5:590. doi:10.3389/fimmu.2014.00590