1932

Abstract

Viruses face a multitude of challenges when they infect a host cell. Cells have evolved innate defenses to protect against pathogens, and an infecting virus may induce a stress response that antagonizes viral replication. Further, the metabolic, oxidative, and cell cycle state may not be conducive to the viral infection. But viruses are fabulous manipulators, inducing host cells to use their own characteristic mechanisms and pathways to provide what the virus needs. This article centers on the manipulation of host cell metabolism by human cytomegalovirus (HCMV). We review the features of the metabolic program instituted by the virus, discuss the mechanisms underlying these dramatic metabolic changes, and consider how the altered program creates a synthetic milieu that favors efficient HCMV replication and spread.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-031413-085425
2014-09-29
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/virology/1/1/annurev-virology-031413-085425.html?itemId=/content/journals/10.1146/annurev-virology-031413-085425&mimeType=html&fmt=ahah

Literature Cited

  1. Murphy E, Yu D, Grimwood J, Schmutz J, Dickson M. 1.  et al. 2003. Coding potential of laboratory and clinical strains of human cytomegalovirus. Proc. Natl. Acad. Sci. USA 25:14976–81 [Google Scholar]
  2. Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY. 2.  et al. 2012. Decoding human cytomegalovirus. Science 338:1088–93 [Google Scholar]
  3. Goodrum F, Caviness K, Zagallo P. 3.  2012. Human cytomegalovirus persistence. Cell. Microbiol. 14:644–55 [Google Scholar]
  4. Wallace DL, Masters JE, de Lara CM, Henson SM, Worth A. 4.  et al. 2011. Human cytomegalovirus–specific CD8+ T-cell expansions contain long-lived cells that retain functional capacity in both young and elderly subjects. Immunology 132:27–38 [Google Scholar]
  5. Fish KN, Soderberg-Naucler C, Mills LK, Stenglein S, Nelson JA. 5.  1998. Human cytomegalovirus persistently infects aortic endothelial cells. J. Virol. 72:5661–68 [Google Scholar]
  6. Cobbs CS. 6.  2013. Cytomegalovirus and brain tumor: epidemiology, biology and therapeutic aspects. Curr. Opin. Oncol. 25:682–88 [Google Scholar]
  7. Dziurzynski K, Chang SM, Heimberger AB, Kalejta RF, McGregor Dallas SR. 7.  et al. 2012. Consensus on the role of human cytomegalovirus in glioblastoma. Neuro-Oncology 14:246–55 [Google Scholar]
  8. Reaves ML, Rabinowitz JD. 8.  2011. Metabolomics in systems microbiology. Curr. Opin. Biotechnol. 22:17–25 [Google Scholar]
  9. Yu Y, Clippinger AJ, Alwine JC. 9.  2011. Viral effects on metabolism: changes in glucose and glutamine utilization during human cytomegalovirus infection. Trends Microbiol. 19:360–67 [Google Scholar]
  10. Yu Y, Maguire TG, Alwine JC. 10.  2011. Human cytomegalovirus activates glucose transporter 4 expression to increase glucose uptake during infection. J. Virol. 85:1573–80 [Google Scholar]
  11. Yuneva M, Zamboni N, Oefner P, Sachidanandam R, Lazebnik Y. 11.  2007. Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J. Cell Biol. 178:93–105 [Google Scholar]
  12. Chambers JW, Maguire TG, Alwine JC. 12.  2010. Glutamine metabolism is essential for human cytomegalovirus infection. J. Virol. 84:1867–73 [Google Scholar]
  13. DeBerardinis RJ, Sayed N, Ditsworth D, Thompson CB. 13.  2008. Brick by brick: metabolism and tumor cell growth. Curr. Opin. Genet. Dev. 18:54–61 [Google Scholar]
  14. Warburg O, Posener K, Negelein E. 14.  1924. Über den Stoffwechsel der Carcinomzelle. Biochem. Z. 152:319–44 [Google Scholar]
  15. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M. 15.  et al. 2007. Beyond aerobic glycolysis: Transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc. Natl. Acad. Sci. USA 104:19345–50 [Google Scholar]
  16. Owen OE, Kalhan SC, Hanson RW. 16.  2002. The key role of anaplerosis and cataplerosis for citric acid cycle function. J. Biol. Chem. 277:30409–12 [Google Scholar]
  17. Marin-Valencia I, Yang C, Mashimo T, Cho S, Baek H. 17.  et al. 2012. Analysis of tumor metabolism reveals mitochondrial glucose oxidation in genetically diverse human glioblastomas in the mouse brain in vivo. Cell Metab. 15:827–37 [Google Scholar]
  18. Munger J, Bajad SU, Coller HA, Shenk T, Rabinowitz JD. 18.  2006. Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathog. 2:1165–75 [Google Scholar]
  19. Munger J, Bennett BD, Parikh A, Feng XJ, McArdle J. 19.  et al. 2008. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 26:1179–86 [Google Scholar]
  20. Spencer CM, Schafer XL, Moorman NJ, Munger J. 20.  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]
  21. Dang CV. 21.  2011. Therapeutic targeting of Myc-reprogrammed cancer cell metabolism. Cold Spring Harb. Symp. Quant. Biol. 76:369–74 [Google Scholar]
  22. Hagemeier C, Walker SM, Sissons PJ, Sinclair JH. 22.  1992. The 72K IE1 and 80K IE2 proteins of human cytomegalovirus independently trans-activate the c-fos, c-myc and hsp70 promoters via basal promoter elements. J. Gen. Virol. 73:2385–93 [Google Scholar]
  23. Alwine JC. 23.  2012. The human cytomegalovirus assembly compartment: a masterpiece of viral manipulation of cellular processes that facilitate assembly and egress. PLoS Pathog. 8:e1002878 [Google Scholar]
  24. Koyuncu E, Purdy JG, Rabinowitz JD, Shenk T. 24.  2013. Saturated very long chain fatty acids are required for the production of infectious human cytomegalovirus progeny. PLoS Pathog. 9:e1003333 [Google Scholar]
  25. Alwine JC. 25.  2008. Modulation of host cell stress responses by human cytomegalovirus. Curr. Top. Microbiol. Immunol. 325:263–79 [Google Scholar]
  26. Hardie DG. 26.  2011. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 25:1895–908 [Google Scholar]
  27. Sanli T, Steinberg GR, Singh G, Tsakiridis T. 27.  2014. AMP-activated protein kinase (AMPK) beyond metabolism: a novel genomic stress sensor participating in the DNA damage response pathway. Cancer Biol. Ther. 15:156–69 [Google Scholar]
  28. Kurth-Kraczek EJ, Hirshman MF, Goodyear LJ, Winder WW. 28.  1999. 5′ AMP–activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48:1667–71 [Google Scholar]
  29. Marsin AS, Bouzin C, Bertrand L, Hue L. 29.  2002. The stimulation of glycolysis by hypoxia in activated monocytes is mediated by AMP-activated protein kinase and inducible 6-phosphofructo-2-kinase. J. Biol. Chem. 277:30778–83 [Google Scholar]
  30. Proud CG. 30.  2004. Role of mTOR signalling in the control of translation initiation and elongation by nutrients. Curr. Top. Microbiol. Immunol. 279:215–44 [Google Scholar]
  31. Terry LJ, Vastag L, Rabinowitz JD, Shenk T. 31.  2012. Human kinome profiling identifies a requirement for AMP-activated protein kinase during human cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 109:3071–76 [Google Scholar]
  32. McArdle J, Moorman NJ, Munger J. 32.  2012. HCMV targets the metabolic stress response through activation of AMPK whose activity is important for viral replication. PLoS Pathog. 8:e1002502 [Google Scholar]
  33. McArdle J, Schafer XL, Munger J. 33.  2011. Inhibition of calmodulin-dependent kinase kinase blocks human cytomegalovirus–induced glycolytic activation and severely attenuates production of viral progeny. J. Virol. 85:705–14 [Google Scholar]
  34. Sharon-Friling R, Goodhouse J, Colberg-Poley AM, Shenk T. 34.  2006. Human cytomegalovirus pUL37x1 induces the release of endoplasmic reticulum calcium stores. Proc. Natl. Acad. Sci. USA 103:19117–22 [Google Scholar]
  35. Sharon-Friling R, Shenk T. 35.  2014. Human cytomegalovirus pUL37x1-induced calcium flux activates PKCα, inducing altered cell shape and accumulation of cytoplasmic vesicles. Proc. Natl. Acad. Sci. USA 111:E1140–48 [Google Scholar]
  36. Isler JA, Maguire TG, Alwine JC. 36.  2005. Production of infectious human cytomegalovirus virions is inhibited by drugs that disrupt calcium homeostasis in the endoplasmic reticulum. J. Virol. 79:15388–97 [Google Scholar]
  37. Hardie DG. 37.  1992. Regulation of fatty acid and cholesterol metabolism by the AMP-activated protein kinase. Biochim. Biophys. Acta 1123:231–38 [Google Scholar]
  38. Potena L, Frascaroli G, Grigioni F, Lazzarotto T, Magnani G. 38.  et al. 2004. Hydroxymethyl-glutaryl coenzyme A reductase inhibition limits cytomegalovirus infection in human endothelial cells. Circulation 109:532–36 [Google Scholar]
  39. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR. 39.  et al. 2002. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110:163–75 [Google Scholar]
  40. Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR. 40.  et al. 2004. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14:1296–302 [Google Scholar]
  41. Clippinger AJ, Maguire TG, Alwine JC. 41.  2011. The changing role of mTOR kinase in the maintenance of protein synthesis during human cytomegalovirus infection. J. Virol. 85:3930–39 [Google Scholar]
  42. Moorman NJ, Shenk T. 42.  2010. Rapamycin-resistant mTORC1 kinase activity is required for herpesvirus replication. J. Virol. 84:5260–69 [Google Scholar]
  43. Appenzeller-Herzog C, Hall MN. 43.  2012. Bidirectional crosstalk between endoplasmic reticulum stress and mTOR signaling. Trends Cell Biol. 22:274–82 [Google Scholar]
  44. Wang X, Proud CG. 44.  2011. mTORC1 signaling: what we still don't know. J. Mol. Cell Biol. 3:206–20 [Google Scholar]
  45. Wong PM, Puente C, Ganley IG, Jiang X. 45.  2013. The ULK1 complex: sensing nutrient signals for autophagy activation. Autophagy 9:124–37 [Google Scholar]
  46. Peterson TR, Sengupta SS, Harris TH, Carmack AE, Kang SA. 46.  et al. 2011. mTOR complex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 146:408–20 [Google Scholar]
  47. Agani F, Jiang BH. 47.  2013. Oxygen-independent regulation of HIF-1: novel involvement of PI3K/AKT/mTOR pathway in cancer. Curr. Cancer Drug Targets 13:245–51 [Google Scholar]
  48. McFarlane S, Nicholl MJ, Sutherland JS, Preston CM. 48.  2011. Interaction of the human cytomegalovirus particle with the host cell induces hypoxia-inducible factor 1 alpha. Virology 414:83–90 [Google Scholar]
  49. Sancak Y, Thoreen C, Peterson T, Lindquist R, Kang S. 49.  et al. 2007. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol. Cell 25:903–15 [Google Scholar]
  50. Kudchodkar SB, Yu Y, Maguire TG, Alwine JC. 50.  2004. Human cytomegalovirus infection induces rapamycin insensitive phosphorylation of downstream effectors of mTOR kinase. J. Virol. 78:11030–39 [Google Scholar]
  51. Kudchodkar SB, Del Prete GQ, Maguire TG, Alwine JC. 51.  2007. AMPK-mediated inhibition of mTOR kinase is circumvented during immediate-early times of human cytomegalovirus infection. J. Virol. 81:3649–51 [Google Scholar]
  52. Moorman NJ, Cristea IM, Terhune SS, Rout MP, Chait BT, Shenk T. 52.  2008. Human cytomegalovirus protein UL38 inhibits host cell stress responses by antagonizing the tuberous sclerosis protein complex. Cell Host Microbe 3:1–10 [Google Scholar]
  53. Johnson RA, Wang X, Ma XL, Huong SM, Huang ES. 53.  2001. 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. 75:6022–32 [Google Scholar]
  54. Nobukuni T, Kozma SC, Thomas G. 54.  2007. hVps34, an ancient player, enters a growing game: mTOR complex1/S6K1 signaling. Curr. Opin. Cell Biol. 19:135–41 [Google Scholar]
  55. Smith EM, Finn SG, Tee AR, Browne GJ, Proud CG. 55.  2005. The tuberous sclerosis protein TSC2 is not required for the regulation of the mammalian target of rapamycin by amino acids and certain cellular stresses. J. Biol. Chem. 280:18717–27 [Google Scholar]
  56. Tilton C, Clippinger AJ, Maguire T, Alwine JC. 56.  2011. Human cytomegalovirus induces multiple means to combat reactive oxygen species. J. Virol. 85:12585–93 [Google Scholar]
  57. Clippinger AJ, Maguire TG, Alwine JC. 57.  2011. Human cytomegalovirus infection maintains mTOR activity and its perinuclear localization during amino acid deprivation. J. Virol. 85:9369–76 [Google Scholar]
  58. Kim E, Goraksha-Hicks P, Li L, Neufeld T, Guan KL. 58.  2008. Regulation of TORC1 by Rag GTPases in nutrient response. Nat. Cell Biol. 10:935–45 [Google Scholar]
  59. Sancak Y, Peterson T, Shaul Y, Lindquist R, Thoreen C. 59.  et al. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496–501 [Google Scholar]
  60. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. 60.  2010. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141:290–303 [Google Scholar]
  61. Clippinger AJ, Alwine JC. 61.  2012. Dynein mediates the localization and activation of mTOR in normal and human cytomegalovirus–infected cells. Genes Dev. 26:2015–26 [Google Scholar]
  62. Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen J. 62.  2001. Phosphatidic acid–mediated mitogenic activation of mTOR signaling. Science 294:1942–45 [Google Scholar]
  63. Sun Y, Chen J. 63.  2008. mTOR signaling: PLD takes center stage. Cell Cycle 7:3118–23 [Google Scholar]
  64. Toschi A, Lee E, Xu L, Garcia A, Gadir N, Foster DA. 64.  2009. Regulation of mTORC1 and mTORC2 complex assembly by phosphatidic acid: competition with rapamycin. Mol. Cell. Biol. 29:1411–20 [Google Scholar]
  65. Foster DA. 65.  2013. Phosphatidic acid and lipid-sensing by mTOR. Trends Endocrinol. Metab. 24:272–78 [Google Scholar]
  66. Liu ST, Sharon-Friling R, Ivanova P, Milne SB, Myers DS. 66.  et al. 2011. Synaptic vesicle–like lipidome of human cytomegalovirus virions reveals a role for SNARE machinery in virion egress. Proc. Natl. Acad. Sci. USA 108:12869–74 [Google Scholar]
  67. Harding HP, Calfon M, Urano F, Novoa I, Ron D. 67.  2002. Transcriptional and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18:575–99 [Google Scholar]
  68. Kaufman RJ. 68.  1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcription and translational controls. Gen. Dev. 13:1211–33 [Google Scholar]
  69. Lee DY, Lee J, Sugden B. 69.  2009. The unfolded protein response and autophagy: Herpesviruses rule!. J. Virol. 83:1168–72 [Google Scholar]
  70. Lee AS. 70.  1992. Mammalian stress response: induction of the glucose-regulated protein family. Curr. Opin. Cell Biol. 4:267–73 [Google Scholar]
  71. Tardif KD, Mori K, Siddiqui A. 71.  2002. Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway. J. Virol. 76:7453–59 [Google Scholar]
  72. Rutkowski DR, Kaufman RJ. 72.  2004. A trip to the ER: coping with stress. Trends Cell Biol. 14:20–28 [Google Scholar]
  73. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. 73.  2000. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2:326–32 [Google Scholar]
  74. Shen J, Chen X, Hendershot LM, Prywes R. 74.  2002. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3:99–111 [Google Scholar]
  75. Buchkovich NJ, Maguire TG, Alwine JC. 75.  2010. Role of the endoplasmic reticulum chaperone BiP, SUN domain proteins, and dynein in altering nuclear morphology during human cytomegalovirus infection. J. Virol. 84:7005–17 [Google Scholar]
  76. Buchkovich NJ, Maguire TG, Paton AW, Paton JC, Alwine JC. 76.  2008. Human cytomegalovirus specifically controls the levels of the endoplasmic reticulum chaperone BiP/GRP78 which is required for virion assembly. J. Virol. 82:31–39 [Google Scholar]
  77. Buchkovich NJ, Maguire TG, Paton AW, Paton JC, Alwine JC. 77.  2009. The endoplasmic reticulum chaperone BiP/GRP78 is important in the structure and function of the HCMV assembly compartment. J. Virol. 83:11421–28 [Google Scholar]
  78. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P. 78.  2013. Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb. Perspect. Biol. 5:a013169 [Google Scholar]
  79. Isler JA, Skalet AH, Alwine JC. 79.  2005. Human cytomegalovirus infection activates and regulates the unfolded protein response. J. Virol. 79:6890–99 [Google Scholar]
  80. Bobrovnikova-Marjon E, Grigoriadou C, Pytel D, Zhang F, Ye J. 80.  et al. 2010. PERK promotes cancer cell proliferation and tumor growth by limiting oxidative DNA damage. Oncogene 29:3881–95 [Google Scholar]
  81. Yu Y, Pierciey FJ Jr, Maguire TG, Alwine JC. 81.  2013. PKR-like endoplasmic reticulum kinase is necessary for lipogenic activation in HCMV-infected cells. J. Virol. 9:e1003266 [Google Scholar]
  82. Hetz C. 82.  2012. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13:89–102 [Google Scholar]
  83. Harding HP, Zhang Y, Ron D. 83.  1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271–74 [Google Scholar]
  84. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. 84.  2000. PERK is essential for translation regulation and cell survival during unfolded protein response. Mol. Cell 5:897–904 [Google Scholar]
  85. Proud CG. 85.  2005. eIF2 and the control of cell physiology. Semin. Cell Dev. Biol. 16:3–12 [Google Scholar]
  86. Hakki M, Marshall EE, De Niro KL, Geballe AP. 86.  2006. Binding and nuclear relocalization of protein kinase R by human cytomegalovirus TRS1. J. Virol. 80:11817–26 [Google Scholar]
  87. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R. 87.  et al. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099–108 [Google Scholar]
  88. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD. 88.  et al. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11:619–33 [Google Scholar]
  89. Xuan B, Qian Z, Torigoi E, Yu D. 89.  2009. Human cytomegalovirus protein pUL38 induces ATF4 expression, inhibits persistent JNK phosphorylation, and suppresses endoplasmic reticulum stress–induced cell death. J. Virol 83:3463–74 [Google Scholar]
  90. Wang C, Huang Z, Du Y, Cheng Y, Chen S, Guo F. 90.  2010. ATF4 regulates lipid metabolism and thermogenesis. Cell Res. 20:174–84 [Google Scholar]
  91. Shao W, Espenshade PJ. 91.  2012. Expanding roles for SREBP in metabolism. Cell Metab. 16:414–19 [Google Scholar]
  92. Yu Y, Maguire T, Alwine JC. 92.  2012. Human cytomegalovirus infection induces adipocyte-like lipogenesis through activation of sterol regulatory element binding protein 1. J. Virol. 86:2942–49 [Google Scholar]
  93. Yu Y, Maguire TG, Alwine JC. 93.  2014. ChREBP, a glucose responsive transcriptional factor, redirects glucose metabolism to support biosynthesis in HCMV-infected cells. Proc. Natl. Acad. Sci. USA. 1111951–56 [Google Scholar]
  94. Seo JY, Cresswell P. 94.  2013. Viperin regulates cellular lipid metabolism during human cytomegalovirus infection. PLoS Pathog. 9:e1003497 [Google Scholar]
  95. Rauwel B, Mariame B, Martin H, Nielsen R, Allart S. 95.  et al. 2010. Activation of peroxisome proliferator–activated receptor gamma by human cytomegalovirus for de novo replication impairs migration and invasiveness of cytotrophoblasts from early placentas. J. Virol. 84:2946–54 [Google Scholar]
  96. Siersbaek R, Nielsen R, Mandrup S. 96.  2010. PPARγ in adipocyte differentiation and metabolism—novel insights from genome-wide studies. FEBS Lett. 584:3242–49 [Google Scholar]
  97. Vastag L, Koyuncu E, Grady SL, Shenk TE, Rabinowitz JD. 97.  2011. Divergent effects of human cytomegalovirus and herpes simplex virus-1 on cellular metabolism. PLoS Pathog. 7:e1002124 [Google Scholar]
  98. Roe B, Kensicki E, Mohney R, Hall WW. 98.  2011. Metabolomic profile of hepatitis C virus–infected hepatocytes. PLoS ONE 6:e23641 [Google Scholar]
  99. Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA. 99.  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]
  100. Cheung AK, Abendroth A, Cunningham AL, Slobedman B. 100.  2006. Viral gene expression during the establishment of human cytomegalovirus latent infection in myeloid progenitor cells. Blood 108:3691–99 [Google Scholar]
  101. Goodrum FD, Jordan CT, High K, Shenk T. 101.  2002. Human cytomegalovirus gene expression during infection of primary hematopoietic progenitor cells: a model for latency. Proc. Natl. Acad. Sci. USA 99:16255–60 [Google Scholar]
  102. Ecker J, Liebisch G, Englmaier M, Grandl M, Robenek H, Schmitz G. 102.  2010. Induction of fatty acid synthesis is a key requirement for phagocytic differentiation of human monocytes. Proc. Natl. Acad. Sci. USA 107:7817–22 [Google Scholar]
  103. Schneiter R, Brugger B, Amann CM, Prestwich GD, Epand RF. 103.  et al. 2004. Identification and biophysical characterization of a very-long-chain-fatty-acid-substituted phosphatidylinositol in yeast subcellular membranes. Biochem. J. 381:941–49 [Google Scholar]
  104. Ho JK, Moser H, Kishimoto Y, Hamilton JA. 104.  1995. Interactions of a very long chain fatty acid with model membranes and serum albumin. Implications for the pathogenesis of adrenoleukodystrophy. J. Clin. Investig. 96:1455–63 [Google Scholar]
  105. Gaigg B, Toulmay A, Schneiter R. 105.  2006. Very long-chain fatty acid–containing lipids rather than sphingolipids per se are required for raft association and stable surface transport of newly synthesized plasma membrane ATPase in yeast. J. Biol. Chem. 281:34135–45 [Google Scholar]
/content/journals/10.1146/annurev-virology-031413-085425
Loading
/content/journals/10.1146/annurev-virology-031413-085425
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