1932

Abstract

Over the past decades, there have been tremendous efforts to understand the cross-talk between viruses and host metabolism. Several studies have elucidated the mechanisms through which viral infections manipulate metabolic pathways including glucose, fatty acid, protein, and nucleotide metabolism. These pathways are evolutionarily conserved across the tree of life and extremely important for the host's nutrient utilization and energy production. In this review, we focus on host glucose, glutamine, and fatty acid metabolism and highlight the pathways manipulated by the different classes of viruses to increase their replication. We also explore a new system of viral hormones in which viruses mimic host hormones to manipulate the host endocrine system. We discuss viral insulin/IGF-1-like peptides and their potential effects on host metabolism. Together, these pathogenesis mechanisms targeting cellular signaling pathways create a multidimensional network of interactions between host and viral proteins. Defining and better understanding these mechanisms will help us to develop new therapeutic tools to prevent and treat viral infections.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-091919-102416
2021-09-29
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/virology/8/1/annurev-virology-091919-102416.html?itemId=/content/journals/10.1146/annurev-virology-091919-102416&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Pan D, Nolan J, Williams KH, Robbins MJ, Weber KA. 2017. Abundance and distribution of microbial cells and viruses in an alluvial aquifer. Front. Microbiol 8:1199
    [Google Scholar]
  2. 2. 
    Sanchez EL, Lagunoff M. 2015. Viral activation of cellular metabolism. Virology 479–480:609–18
    [Google Scholar]
  3. 3. 
    Mayer KA, Stockl J, Zlabinger GJ, Gualdoni GA. 2019. Hijacking the supplies: metabolism as a novel facet of virus-host interaction. Front. Immunol. 10:1533
    [Google Scholar]
  4. 4. 
    Thaker SK, Ch'ng J, Christofk HR. 2019. Viral hijacking of cellular metabolism. BMC Biol 17:59
    [Google Scholar]
  5. 5. 
    Ketter E, Randall G. 2019. Virus impact on lipids and membranes. Annu. Rev. Virol 6:319–40
    [Google Scholar]
  6. 6. 
    Fothergill-Gilmore LA, Michels PA. 1993. Evolution of glycolysis. Prog. Biophys. Mol. Biol. 59:105–235
    [Google Scholar]
  7. 7. 
    Fernie AR, Carrari F, Sweetlove LJ. 2004. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 7:254–61
    [Google Scholar]
  8. 8. 
    Lin SC, Hardie DG. 2018. AMPK: sensing glucose as well as cellular energy status. Cell Metab 27:299–313
    [Google Scholar]
  9. 9. 
    Hung YP, Teragawa C, Kosaisawe N, Gillies TE, Pargett M et al. 2017. Akt regulation of glycolysis mediates bioenergetic stability in epithelial cells. eLife 6:e27293
    [Google Scholar]
  10. 10. 
    Liberti MV, Locasale JW. 2016. The Warburg effect: How does it benefit cancer cells?. Trends Biochem. Sci. 41:211–18
    [Google Scholar]
  11. 11. 
    He ST, Lee DY, Tung CY, Li CY, Wang HC. 2019. Glutamine metabolism in both the oxidative and reductive directions is triggered in shrimp immune cells (hemocytes) at the WSSV genome replication stage to benefit virus replication. Front. Immunol. 10:2102
    [Google Scholar]
  12. 12. 
    Zwerschke W, Mazurek S, Massimi P, Banks L, Eigenbrodt E, Jansen-Durr P 1999. Modulation of type M2 pyruvate kinase activity by the human papillomavirus type 16 E7 oncoprotein. PNAS 96:1291–96
    [Google Scholar]
  13. 13. 
    Munger J, Bajad SU, Coller HA, Shenk T, Rabinowitz JD. 2006. Dynamics of the cellular metabolome during human cytomegalovirus infection. PLOS Pathog 2:e132
    [Google Scholar]
  14. 14. 
    Delgado T, Carroll PA, Punjabi AS, Margineantu D, Hockenbery DM, Lagunoff M 2010. Induction of the Warburg effect by Kaposi's sarcoma herpesvirus is required for the maintenance of latently infected endothelial cells. PNAS 107:10696–701
    [Google Scholar]
  15. 15. 
    Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA et al. 2010. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLOS Pathog 6:e1000719
    [Google Scholar]
  16. 16. 
    Ajaz S, McPhail MJ, Singh KK, Mujib S, Trovato FM et al. 2021. Mitochondrial metabolic manipulation by SARS-CoV-2 in peripheral blood mononuclear cells of patients with COVID-19. Am. J. Physiol. Cell Physiol. 320:C57–65
    [Google Scholar]
  17. 17. 
    Guo X, Wu S, Li N, Lin Q, Liu L et al. 2019. Accelerated metabolite levels of aerobic glycolysis and the pentose phosphate pathway are required for efficient replication of infectious spleen and kidney necrosis virus in Chinese perch brain cells. Biomolecules 9:440
    [Google Scholar]
  18. 18. 
    Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A et al. 2008. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 30:214–26
    [Google Scholar]
  19. 19. 
    Yuan HX, Xiong Y, Guan KL. 2013. Nutrient sensing, metabolism, and cell growth control. Mol. Cell 49:379–87
    [Google Scholar]
  20. 20. 
    Jiang S, Wang Y, Luo L, Shi F, Zou J et al. 2019. AMP-activated protein kinase regulates cancer cell growth and metabolism via nuclear and mitochondria events. J. Cell. Mol. Med. 23:3951–61
    [Google Scholar]
  21. 21. 
    Lyu X, Wang J, Guo X, Wu G, Jiao Y et al. 2018. EBV-miR-BART1-5P activates AMPK/mTOR/HIF1 pathway via a PTEN independent manner to promote glycolysis and angiogenesis in nasopharyngeal carcinoma. PLOS Pathog 14:e1007484
    [Google Scholar]
  22. 22. 
    Singh S, Singh PK, Suhail H, Arumugaswami V, Pellett PE et al. 2020. AMP-activated protein kinase restricts Zika virus replication in endothelial cells by potentiating innate antiviral responses and inhibiting glycolysis. J. Immunol. 204:1810–24
    [Google Scholar]
  23. 23. 
    Thai M, Graham NA, Braas D, Nehil M, Komisopoulou E et al. 2014. Adenovirus E4ORF1-induced MYC activation promotes host cell anabolic glucose metabolism and virus replication. Cell Metab 19:694–701
    [Google Scholar]
  24. 24. 
    Passalacqua KD, Lu J, Goodfellow I, Kolawole AO, Arche JR et al. 2019. Glycolysis is an intrinsic factor for optimal replication of a norovirus. mBio 10:2e02175-18
    [Google Scholar]
  25. 25. 
    Chi PI, Huang WR, Chiu HC, Li JY, Nielsen BL, Liu HJ. 2018. Avian reovirus σA-modulated suppression of lactate dehydrogenase and upregulation of glutaminolysis and the mTOC1/eIF4E/HIF-1α pathway to enhance glycolysis and the TCA cycle for virus replication. Cell. Microbiol. 20:e12946
    [Google Scholar]
  26. 26. 
    Chi PI, Huang WR, Lai IH, Cheng CY, Liu HJ. 2013. The p17 nonstructural protein of avian reovirus triggers autophagy enhancing virus replication via activation of phosphatase and tensin deleted on chromosome 10 (PTEN) and AMP-activated protein kinase (AMPK), as well as dsRNA-dependent protein kinase (PKR)/eIF2α signaling pathways. J. Biol. Chem. 288:3571–84
    [Google Scholar]
  27. 27. 
    Navale AM, Paranjape AN. 2016. Glucose transporters: physiological and pathological roles. Biophys. Rev. 8:5–9
    [Google Scholar]
  28. 28. 
    Loisel-Meyer S, Swainson L, Craveiro M, Oburoglu L, Mongellaz C et al. 2012. Glut1-mediated glucose transport regulates HIV infection. PNAS 109:2549–54
    [Google Scholar]
  29. 29. 
    Sorbara LR, Maldarelli F, Chamoun G, Schilling B, Chokekijcahi S et al. 1996. Human immunodeficiency virus type 1 infection of H9 cells induces increased glucose transporter expression. J. Virol. 70:7275–79
    [Google Scholar]
  30. 30. 
    Gualdoni GA, Mayer KA, Kapsch AM, Kreuzberg K, Puck A et al. 2018. Rhinovirus induces an anabolic reprogramming in host cell metabolism essential for viral replication. PNAS 115:E7158–65
    [Google Scholar]
  31. 31. 
    Chaudhary N, Gonzalez E, Chang SH, Geng F, Rafii S et al. 2016. Adenovirus protein E4-ORF1 activation of PI3 kinase reveals differential regulation of downstream effector pathways in adipocytes. Cell Rep 17:3305–18
    [Google Scholar]
  32. 32. 
    Heinz DW, Baase WA, Matthews BW 1992. Folding and function of a T4 lysozyme containing 10 consecutive alanines illustrate the redundancy of information in an amino acid sequence. PNAS 89:3751–55
    [Google Scholar]
  33. 33. 
    Dai L, Hu WW, Xia L, Xia M, Yang Q 2016. Transmissible gastroenteritis virus infection enhances SGLT1 and GLUT2 expression to increase glucose uptake. PLOS ONE 11:e0165585
    [Google Scholar]
  34. 34. 
    Dyer A, Schoeps B, Frost S, Jakeman P, Scott EM et al. 2019. Antagonism of glycolysis and reductive carboxylation of glutamine potentiates activity of oncolytic adenoviruses in cancer cells. Cancer Res 79:331–45
    [Google Scholar]
  35. 35. 
    Thai M, Thaker SK, Feng J, Du Y, Hu H et al. 2015. MYC-induced reprogramming of glutamine catabolism supports optimal virus replication. Nat. Commun. 6:8873
    [Google Scholar]
  36. 36. 
    Sanchez EL, Pulliam TH, Dimaio TA, Thalhofer AB, Delgado T, Lagunoff M. 2017. Glycolysis, glutaminolysis, and fatty acid synthesis are required for distinct stages of Kaposi's sarcoma-associated herpesvirus lytic replication. J. Virol. 91:10e02237-16
    [Google Scholar]
  37. 37. 
    Sanchez EL, Carroll PA, Thalhofer AB, Lagunoff M. 2015. Latent KSHV infected endothelial cells are glutamine addicted and require glutaminolysis for survival. PLOS Pathog 11:e1005052
    [Google Scholar]
  38. 38. 
    Rosado-Sanchez I, Rodriguez-Gallego E, Peraire J, Vilades C, Herrero P et al. 2019. Glutaminolysis and lipoproteins are key factors in late immune recovery in successfully treated HIV-infected patients. Clin. Sci. (Lond.) 133:997–1010
    [Google Scholar]
  39. 39. 
    Ye X, Zhou Q, Matsumoto Y, Moriyama M, Kageyama S et al. 2016. Inhibition of glutaminolysis inhibits cell growth via down-regulating mTORC1 signaling in lung squamous cell carcinoma. Anticancer Res 36:6021–29
    [Google Scholar]
  40. 40. 
    Wakil SJ, Abu-Elheiga LA. 2009. Fatty acid metabolism: target for metabolic syndrome. J. Lipid Res. 50:Suppl.S138–43
    [Google Scholar]
  41. 41. 
    Hiltunen JK, Qin Y. 2000. β-Oxidation—strategies for the metabolism of a wide variety of acyl-CoA esters. Biochim. Biophys. Acta 1484:117–28
    [Google Scholar]
  42. 42. 
    Wolfe RR. 1998. Metabolic interactions between glucose and fatty acids in humans. Am. J. Clin. Nutr. 67:519S–26S
    [Google Scholar]
  43. 43. 
    Lee G, Zheng Y, Cho S, Jang C, England C et al. 2017. Post-transcriptional regulation of de novo lipogenesis by mTORC1-S6K1-SRPK2 signaling. Cell 171:1545–58.e18
    [Google Scholar]
  44. 44. 
    Shimano H, Sato R. 2017. SREBP-regulated lipid metabolism: convergent physiology—divergent pathophysiology. Nat. Rev. Endocrinol. 13:710–30
    [Google Scholar]
  45. 45. 
    Madison BB. 2016. Srebp2: a master regulator of sterol and fatty acid synthesis. J. Lipid Res. 57:333–35
    [Google Scholar]
  46. 46. 
    Sakai J, Nohturfft A, Goldstein JL, Brown MS. 1998. Cleavage of sterol regulatory element-binding proteins (SREBPs) at site-1 requires interaction with SREBP cleavage-activating protein: evidence from in vivo competition studies. J. Biol. Chem. 273:5785–93
    [Google Scholar]
  47. 47. 
    Ye J, DeBose-Boyd RA. 2011. Regulation of cholesterol and fatty acid synthesis. Cold Spring Harb. Perspect. Biol. 3:a004754
    [Google Scholar]
  48. 48. 
    Chen G, Zhang X. 2010. New insights into S2P signaling cascades: regulation, variation, and conservation. Protein Sci 19:2015–30
    [Google Scholar]
  49. 49. 
    Goldstein JL, DeBose-Boyd RA, Brown MS. 2006. Protein sensors for membrane sterols. Cell 124:135–46
    [Google Scholar]
  50. 50. 
    Li S, Ogawa W, Emi A, Hayashi K, Senga Y et al. 2011. Role of S6K1 in regulation of SREBP1c expression in the liver. Biochem. Biophys. Res. Commun. 412:197–202
    [Google Scholar]
  51. 51. 
    Peterson TR, Sengupta SS, Harris TE, Carmack AE, Kang SA et al. 2011. mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 146:408–20
    [Google Scholar]
  52. 52. 
    Yu Y, Maguire TG, Alwine JC. 2012. Human cytomegalovirus infection induces adipocyte-like lipogenesis through activation of sterol regulatory element binding protein 1. J. Virol. 86:2942–49
    [Google Scholar]
  53. 53. 
    Spencer CM, Schafer XL, Moorman NJ, Munger J. 2011. Human cytomegalovirus induces the activity and expression of acetyl-coenzyme A carboxylase, a fatty acid biosynthetic enzyme whose inhibition attenuates viral replication. J. Virol. 85:5814–24
    [Google Scholar]
  54. 54. 
    Yuan S, Chu H, Chan JF, Ye ZW, Wen L et al. 2019. SREBP-dependent lipidomic reprogramming as a broad-spectrum antiviral target. Nat. Commun. 10:120
    [Google Scholar]
  55. 55. 
    Hulse M, Johnson SM, Boyle S, Caruso LB, Tempera I. 2020. Epstein-Barr virus-encoded latent membrane protein 1 and B-cell growth transformation induces lipogenesis through fatty acid synthase. J. Virol. 95:4e01857-20
    [Google Scholar]
  56. 56. 
    Wilsky S, Sobotta K, Wiesener N, Pilas J, Althof N et al. 2012. Inhibition of fatty acid synthase by amentoflavone reduces coxsackievirus B3 replication. Arch. Virol. 157:259–69
    [Google Scholar]
  57. 57. 
    Ohol YM, Wang Z, Kemble G, Duke G. 2015. Direct inhibition of cellular fatty acid synthase impairs replication of respiratory syncytial virus and other respiratory viruses. PLOS ONE 10:e0144648
    [Google Scholar]
  58. 58. 
    Kapadia SB, Chisari FV 2005. Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. PNAS 102:2561–66
    [Google Scholar]
  59. 59. 
    Long S, Zhou Y, Bai D, Hao W, Zheng B et al. 2019. Fatty acids regulate porcine reproductive and respiratory syndrome virus infection via the AMPK-ACC1 signaling pathway. Viruses 11:1145
    [Google Scholar]
  60. 60. 
    Fujimoto T, Parton RG. 2011. Not just fat: the structure and function of the lipid droplet. Cold Spring Harb. Perspect. Biol. 3:a004838
    [Google Scholar]
  61. 61. 
    Olzmann JA, Carvalho P. 2019. Dynamics and functions of lipid droplets. Nat. Rev. Mol. Cell Biol. 20:137–55
    [Google Scholar]
  62. 62. 
    Walther TC, Chung J, Farese RV Jr. 2017. Lipid droplet biogenesis. Annu. Rev. Cell Dev. Biol. 33:491–510
    [Google Scholar]
  63. 63. 
    Takahashi Y, Shinoda A, Furuya N, Harada E, Arimura N et al. 2013. Perilipin-mediated lipid droplet formation in adipocytes promotes sterol regulatory element-binding protein-1 processing and triacylglyceride accumulation. PLOS ONE 8:e64605
    [Google Scholar]
  64. 64. 
    Herker E, Ott M. 2012. Emerging role of lipid droplets in host/pathogen interactions. J. Biol. Chem. 287:2280–87
    [Google Scholar]
  65. 65. 
    Dias SSG, Soares VC, Ferreira AC, Sacramento CQ, Fintelman-Rodrigues N et al. 2020. Lipid droplets fuel SARS-CoV-2 replication and production of inflammatory mediators. PLOS Pathog 16:e1009127
    [Google Scholar]
  66. 66. 
    Jassey A, Liu CH, Changou CA, Richardson CD, Hsu HY, Lin LT. 2019. Hepatitis C virus non-structural protein 5A (NS5A) disrupts mitochondrial dynamics and induces mitophagy. Cells 8:4290
    [Google Scholar]
  67. 67. 
    Vogt DA, Camus G, Herker E, Webster BR, Tsou CL et al. 2013. Lipid droplet-binding protein TIP47 regulates hepatitis C virus RNA replication through interaction with the viral NS5A protein. PLOS Pathog 9:e1003302
    [Google Scholar]
  68. 68. 
    Hou W, Cruz-Cosme R, Armstrong N, Obwolo LA, Wen F et al. 2017. Molecular cloning and characterization of the genes encoding the proteins of Zika virus. Gene 628:117–28
    [Google Scholar]
  69. 69. 
    Samsa MM, Mondotte JA, Iglesias NG, Assuncao-Miranda I, Barbosa-Lima G et al. 2009. Dengue virus capsid protein usurps lipid droplets for viral particle formation. PLOS Pathog 5:e1000632
    [Google Scholar]
  70. 70. 
    Martins AS, Carvalho FA, Faustino AF, Martins IC, Santos NC. 2019. West Nile virus capsid protein interacts with biologically relevant host lipid systems. Front. Cell. Infect. Microbiol. 9:8
    [Google Scholar]
  71. 71. 
    Cheung W, Gill M, Esposito A, Kaminski CF, Courousse N et al. 2010. Rotaviruses associate with cellular lipid droplet components to replicate in viroplasms, and compounds disrupting or blocking lipid droplets inhibit viroplasm formation and viral replication. J. Virol. 84:6782–98
    [Google Scholar]
  72. 72. 
    Episcopio D, Aminov S, Benjamin S, Germain G, Datan E et al. 2019. Atorvastatin restricts the ability of influenza virus to generate lipid droplets and severely suppresses the replication of the virus. FASEB J 33:9516–25
    [Google Scholar]
  73. 73. 
    Tanner LB, Chng C, Guan XL, Lei Z, Rozen SG, Wenk MR. 2014. Lipidomics identifies a requirement for peroxisomal function during influenza virus replication. J. Lipid Res. 55:1357–65
    [Google Scholar]
  74. 74. 
    Keshavarz M, Solaymani-Mohammadi F, Namdari H, Arjeini Y, Mousavi MJ, Rezaei F. 2020. Metabolic host response and therapeutic approaches to influenza infection. Cell. Mol. Biol. Lett. 25:15
    [Google Scholar]
  75. 75. 
    Ayres JS. 2020. A metabolic handbook for the COVID-19 pandemic. Nat. Metab. 2:572–85
    [Google Scholar]
  76. 76. 
    Amako Y, Munakata T, Kohara M, Siddiqui A, Peers C, Harris M. 2015. Hepatitis C virus attenuates mitochondrial lipid β-oxidation by downregulating mitochondrial trifunctional-protein expression. J. Virol. 89:4092–101
    [Google Scholar]
  77. 77. 
    Seo JY, Cresswell P. 2013. Viperin regulates cellular lipid metabolism during human cytomegalovirus infection. PLOS Pathog 9:e1003497
    [Google Scholar]
  78. 78. 
    Kao YT, Chang BL, Liang JJ, Tsai HJ, Lee YL et al. 2015. Japanese encephalitis virus nonstructural protein NS5 interacts with mitochondrial trifunctional protein and impairs fatty acid β-oxidation. PLOS Pathog 11:e1004750
    [Google Scholar]
  79. 79. 
    Heaton NS, Randall G 2010. Dengue virus-induced autophagy regulates lipid metabolism. Cell Host Microbe 8:422–32
    [Google Scholar]
  80. 80. 
    Greseth MD, Traktman P. 2014. De novo fatty acid biosynthesis contributes significantly to establishment of a bioenergetically favorable environment for vaccinia virus infection. PLOS Pathog 10:e1004021
    [Google Scholar]
  81. 81. 
    Alcami A. 2003. Viral mimicry of cytokines, chemokines and their receptors. Nat. Rev. Immunol. 3:36–50
    [Google Scholar]
  82. 82. 
    Amara A, Mercer J 2015. Viral apoptotic mimicry. Nat. Rev. Microbiol. 13:461–69
    [Google Scholar]
  83. 83. 
    Elde NC, Malik HS. 2009. The evolutionary conundrum of pathogen mimicry. Nat. Rev. Microbiol. 7:787–97
    [Google Scholar]
  84. 84. 
    Huang Q, Kahn CR, Altindis E 2019. Viral hormones: expanding dimensions in endocrinology. Endocrinology 160:2165–79
    [Google Scholar]
  85. 85. 
    Elde NC, Child SJ, Geballe AP, Malik HS. 2009. Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457:485–89
    [Google Scholar]
  86. 86. 
    Shafee TM, Lay FT, Phan TK, Anderson MA, Hulett MD. 2017. Convergent evolution of defensin sequence, structure and function. Cell. Mol. Life Sci. 74:663–82
    [Google Scholar]
  87. 87. 
    Sackton TB, Clark N. 2019. Convergent evolution in the genomics era: new insights and directions. Philos. Trans. R. Soc. B 374:20190102
    [Google Scholar]
  88. 88. 
    Altindis E, Cai W, Sakaguchi M, Zhang F, GuoXiao W et al. 2018. Viral insulin-like peptides activate human insulin and IGF-1 receptor signaling: a paradigm shift for host-microbe interactions. PNAS 115:2461–66
    [Google Scholar]
  89. 89. 
    Huang Q, Chow I-T, Brady C, Raisingani A, Li D et al. 2020. Parabacteroides distasonis enhances type 1 diabetes autoimmunity via molecular mimicry. bioRxiv 2020.10.22.350801. https://doi.org/10.1101/2020.10.22.350801
    [Crossref]
  90. 90. 
    Smith CA, Davis T, Wignall JM, Din WS, Farrah T et al. 1991. T2 open reading frame from the shope fibroma virus encodes a soluble form of the TNF receptor. Biochem. Biophys. Res. Commun. 176:335–42
    [Google Scholar]
  91. 91. 
    Benedict CA, Butrovich KD, Lurain NS, Corbeil J, Rooney I et al. 1999. Cutting edge: a novel viral TNF receptor superfamily member in virulent strains of human cytomegalovirus. J. Immunol. 162:6967–70
    [Google Scholar]
  92. 92. 
    Tidona CA, Darai G. 1997. The complete DNA sequence of lymphocystis disease virus. Virology 230:207–16
    [Google Scholar]
  93. 93. 
    Alcamí A, Smith GL. 1992. A soluble receptor for interleukin-1β encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 71:153–67
    [Google Scholar]
  94. 94. 
    Spriggs MK, Hruby DE, Maliszewski CR, Pickup DJ, Sims JE et al. 1992. Vaccinia and cowpox viruses encode a novel secreted interleukin-1-binding protein. Cell 71:145–52
    [Google Scholar]
  95. 95. 
    Upton C, Mossman K, McFadden G. 1992. Encoding of a homolog of the IFN-gamma receptor by myxoma virus. Science 258:1369–72
    [Google Scholar]
  96. 96. 
    Song WJ, Qin QW, Qiu J, Huang CH, Wang F, Hew CL 2004. Functional genomics analysis of Singapore grouper iridovirus: complete sequence determination and proteomic analysis. J. Virol. 78:12576–90
    [Google Scholar]
  97. 97. 
    Tsai CT, Ting JW, Wu MH, Wu MF, IC Guo, Chang CY. 2005. Complete genome sequence of the grouper iridovirus and comparison of genomic organization with those of other iridoviruses. J. Virol. 79:2010–23
    [Google Scholar]
  98. 98. 
    Lopez-Bueno A, Mavian C, Labella AM, Castro D, Borrego JJ et al. 2016. Concurrence of iridovirus, polyomavirus, and a unique member of a new group of fish papillomaviruses in lymphocystis disease-affected gilthead sea bream. J. Virol. 90:8768–79
    [Google Scholar]
  99. 99. 
    Kramna L, Kolarova K, Oikarinen S, Pursiheimo JP, Ilonen J et al. 2015. Gut virome sequencing in children with early islet autoimmunity. Diabetes Care 38:930–33
    [Google Scholar]
  100. 100. 
    Monaco CL, Gootenberg DB, Zhao G, Handley SA, Ghebremichael MS et al. 2016. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome. Cell Host Microbe 19:311–22
    [Google Scholar]
  101. 101. 
    Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD, Bushman FD 2013. Rapid evolution of the human gut virome. PNAS 110:12450–55
    [Google Scholar]
  102. 102. 
    Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY et al. 2015. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160:447–60
    [Google Scholar]
  103. 103. 
    Breitbart M, Haynes M, Kelley S, Angly F, Edwards RA et al. 2008. Viral diversity and dynamics in an infant gut. Res. Microbiol. 159:367–73
    [Google Scholar]
  104. 104. 
    Chrudinova M, Moreau F, Noh HL, Panikova T, Zakova L et al. 2020. Characterization of viral insulins reveals white adipose tissue-specific effects in mice. Mol. Metab. 44:101121
    [Google Scholar]
  105. 105. 
    Moreau F, Brandao B, Cederquist C, Batista TM, Dimarchi R et al. 2020. 1725-P: viral insulins as agonists and antagonists on insulin/IGF-1 receptors. Diabetes 69:1725-P
    [Google Scholar]
  106. 106. 
    Yan Y, Cui H, Guo C, Li J, Huang X et al. 2013. An insulin-like growth factor homologue of Singapore grouper iridovirus modulates cell proliferation, apoptosis and enhances viral replication. J. Gen. Virol. 94:2759–70
    [Google Scholar]
  107. 107. 
    Taniguchi CM, Emanuelli B, Kahn CR. 2006. Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 7:85–96
    [Google Scholar]
  108. 108. 
    Annunziata M, Granata R, Ghigo E. 2011. The IGF system. Acta Diabetol 48:1–9
    [Google Scholar]
  109. 109. 
    Kang S, Song J, Kang H, Kim S, Lee Y, Park D. 2003. Insulin can block apoptosis by decreasing oxidative stress via phosphatidylinositol 3-kinase- and extracellular signal-regulated protein kinase-dependent signaling pathways in HepG2 cells. Eur. J. Endocrinol. 148:147–55
    [Google Scholar]
  110. 110. 
    Zhang M, Liu J, Li M, Zhang S, Lu Y et al. 2018. Insulin-like growth factor 1/insulin-like growth factor 1 receptor signaling protects against cell apoptosis through the PI3K/AKT pathway in glioblastoma cells. Exp. Ther. Med. 16:1477–82
    [Google Scholar]
  111. 111. 
    Gendrault JL, Steffan AM, Bingen A, Kirn A. 1981. Penetration and uncoating of frog virus 3 (FV3) in cultured rat Kupffer cells. Virology 112:375–84
    [Google Scholar]
  112. 112. 
    Grayfer L, Edholm E-S, De Jesús Andino F, Chinchar VG, Robert J 2015. Ranavirus host immunity and immune evasion. Ranaviruses: Lethal Pathogens of Ectothermic Vertebrates MJ Gray, VG Chinchar 141–70 Cham, Switz: Springer
    [Google Scholar]
  113. 113. 
    Ahlers LR, Bastos RG, Hiroyasu A, Goodman AG. 2016. Invertebrate iridescent virus 6, a DNA virus, stimulates a mammalian innate immune response through RIG-I-like receptors. PLOS ONE 11:e0166088
    [Google Scholar]
  114. 114. 
    Gut JP, Anton M, Bingen A, Vetter JM, Kirn A 1981. Frog virus 3 induces a fatal hepatitis in rats. Lab. Invest. 45:218–28
    [Google Scholar]
  115. 115. 
    Lopez C, Aubertin AM, Tondre L, Kirn A. 1986. Thermosensitivity of frog virus 3 genome expression: defect in early transcription. Virology 152:365–74
    [Google Scholar]
  116. 116. 
    Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM et al. 2013. A strategy to estimate unknown viral diversity in mammals. mBio 4:e00598-13
    [Google Scholar]
/content/journals/10.1146/annurev-virology-091919-102416
Loading
/content/journals/10.1146/annurev-virology-091919-102416
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error