1932

Abstract

Viruses manipulate cellular lipids and membranes at each stage of their life cycle. This includes lipid-receptor interactions, the fusion of viral envelopes with cellular membranes during endocytosis, the reorganization of cellular membranes to form replication compartments, and the envelopment and egress of virions. In addition to the physical interactions with cellular membranes, viruses have evolved to manipulate lipid signaling and metabolism to benefit their replication. This review summarizes the strategies that viruses use to manipulate lipids and membranes at each stage in the viral life cycle.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-092818-015748
2019-09-29
2024-10-07
Loading full text...

Full text loading...

/deliver/fulltext/virology/6/1/annurev-virology-092818-015748.html?itemId=/content/journals/10.1146/annurev-virology-092818-015748&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Kielian M, Rey FA. 2006. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4:167–76
    [Google Scholar]
  2. 2. 
    Taube S, Jiang M, Wobus CE 2010. Glycosphingolipids as receptors for non-enveloped viruses. Viruses 2:41011–49
    [Google Scholar]
  3. 3. 
    Yang S-T, Kiessling V, Simmons JA, White JM, Tamm LK 2015. HIV gp41–mediated membrane fusion occurs at edges of cholesterol-rich lipid domains. Nat. Chem. Biol. 11:6424–31
    [Google Scholar]
  4. 4. 
    Yang S-T, Kiessling V, Tamm LK 2016. Line tension at lipid phase boundaries as driving force for HIV fusion peptide-mediated fusion. Nat. Commun. 7:11401
    [Google Scholar]
  5. 5. 
    Aigal S, Claudinon J, Römer W 2015. Plasma membrane reorganization: a glycolipid gateway for microbes. Biochim. Biophys. Acta 1853:4858–71
    [Google Scholar]
  6. 6. 
    Otsuki N, Sakata M, Saito K, Okamoto K, Mori Y et al. 2017. Both sphingomyelin and cholesterol in the host cell membrane are essential for rubella virus entry. J. Virol. 92:1e01130-17
    [Google Scholar]
  7. 7. 
    Amara A, Mercer J. 2015. Viral apoptotic mimicry. Nat. Rev. Microbiol. 13:8461–69
    [Google Scholar]
  8. 8. 
    Meertens L, Labeau A, Dejarnac O, Cipriani S, Sinigaglia L et al. 2017. Axl mediates ZIKA virus entry in human glial cells and modulates innate immune responses. Cell Rep 18:2324–33
    [Google Scholar]
  9. 9. 
    Wells MF, Salick MR, Wiskow O, Ho DJ, Worringer KA et al. 2016. Genetic ablation of AXL does not protect human neural progenitor cells and cerebral organoids from Zika virus infection. Cell Stem Cell 19:6703–8
    [Google Scholar]
  10. 10. 
    Hastings AK, Yockey LJ, Jagger BW, Hwang J, Uraki R et al. 2017. TAM receptors are not required for Zika virus infection in mice. Cell Rep 19:3558–68
    [Google Scholar]
  11. 11. 
    Bhattacharyya S, Zagórska A, Lew ED, Shrestha B, Rothlin CV et al. 2013. Enveloped viruses disable innate immune responses in dendritic cells by direct activation of TAM receptors. Cell Host Microbe 14:2136–47
    [Google Scholar]
  12. 12. 
    Younan P, Iampietro M, Santos RI, Ramanathan P, Popov VL, Bukreyev A 2018. Disruption of phosphatidylserine synthesis or trafficking reduces infectivity of Ebola virus. J. Infect. Dis. 218:Suppl. 5S475–85
    [Google Scholar]
  13. 13. 
    Younan P, Iampietro M, Santos RI, Ramanathan P, Popov VL, Bukreyev A 2018. Role of transmembrane protein 16F in the incorporation of phosphatidylserine into budding Ebola virus virions. J. Infect. Dis. 218:Suppl. 5S335–45
    [Google Scholar]
  14. 14. 
    Cheshenko N, Pierce C, Herold BC 2018. Herpes simplex viruses activate phospholipid scramblase to redistribute phosphatidylserines and Akt to the outer leaflet of the plasma membrane and promote viral entry. PLOS Pathog 14:1e1006766
    [Google Scholar]
  15. 15. 
    Zaitseva E, Yang S-T, Melikov K, Pourmal S, Chernomordik LV 2010. Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLOS Pathog 6:10e1001131
    [Google Scholar]
  16. 16. 
    Nour AM, Li Y, Wolenski J, Modis Y 2013. Viral membrane fusion and nucleocapsid delivery into the cytoplasm are distinct events in some flaviviruses. PLOS Pathog 9:9e1003585
    [Google Scholar]
  17. 17. 
    Qian M, Cai D, Verhey KJ, Tsai B 2009. A lipid receptor sorts polyomavirus from the endolysosome to the endoplasmic reticulum to cause infection. PLOS Pathog 5:6e1000465
    [Google Scholar]
  18. 18. 
    Munger J, Bajad SU, Coller HA, Shenk T, Rabinowitz JD 2006. Dynamics of the cellular metabolome during human cytomegalovirus infection. PLOS Pathog 2:12e132
    [Google Scholar]
  19. 19. 
    Munger J, Bennett BD, Parikh A, Feng X-J, McArdle J et al. 2008. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 26:101179–86
    [Google Scholar]
  20. 20. 
    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. 85:125814–24
    [Google Scholar]
  21. 21. 
    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]
  22. 22. 
    Ferguson D, Zhang J, Davis MA, Helsley RN, Vedin L-L et al. 2017. The lipid droplet-associated protein perilipin 3 facilitates hepatitis C virus-driven hepatic steatosis. J. Lipid Res. 58:2420–32
    [Google Scholar]
  23. 23. 
    Perera R, Riley C, Isaac G, Hopf-Jannasch AS, Moore RJ et al. 2012. Dengue virus infection perturbs lipid homeostasis in infected mosquito cells. PLOS Pathog 8:3e1002584
    [Google Scholar]
  24. 24. 
    Heaton NS, Randall G. 2010. Dengue virus-induced autophagy regulates lipid metabolism. Cell Host Microbe 8:5422–32
    [Google Scholar]
  25. 25. 
    Jordan TX, Randall G. 2017. Dengue virus activates the AMP kinase-mTOR axis to stimulate a proviral lipophagy. J. Virol. 91:11e02020-16
    [Google Scholar]
  26. 26. 
    Zhang J, Lan Y, Li MY, Lamers MM, Fusade-Boyer M et al. 2018. Flaviviruses exploit the lipid droplet protein AUP1 to trigger lipophagy and drive virus production. Cell Host Microbe 23:6819–31
    [Google Scholar]
  27. 27. 
    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 10:3e1004021
    [Google Scholar]
  28. 28. 
    Wang L, Xie W, Zhang L, Li D, Yu H et al. 2018. CVB3 nonstructural 2A protein modulates SREBP1a signaling via the MEK/ERK pathway. J. Virol. 92:24e01060-18
    [Google Scholar]
  29. 29. 
    Li J, Zeng C, Zheng B, Liu C, Tang M et al. 2018. HMGB1-induced autophagy facilitates hepatic stellate cells activation: a new pathway in liver fibrosis. Clin. Sci. 132:151645–67
    [Google Scholar]
  30. 30. 
    Wang Y, Wu T, Hu D, Weng X, Wang X et al. 2018. Intracellular hepatitis B virus increases hepatic cholesterol deposition in alcoholic fatty liver via hepatitis B core protein. J. Lipid Res. 59:158–68
    [Google Scholar]
  31. 31. 
    Chu Z, Ma J, Wang C, Lu K, Li X et al. 2018. Newcastle disease virus V protein promotes viral replication in HeLa cells through the activation of MEK/ERK signaling. Viruses 10:9489
    [Google Scholar]
  32. 32. 
    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 146:3408–20
    [Google Scholar]
  33. 33. 
    Mingorance L, Castro V, Ávila-Pérez G, Calvo G, Rodriguez MJ et al. 2018. Host phosphatidic acid phosphatase lipin1 is rate limiting for functional hepatitis C virus replicase complex formation. PLOS Pathog 14:9e1007284
    [Google Scholar]
  34. 34. 
    Zhang Z, He G, Han G-S, Zhang J, Catanzaro N et al. 2018. Host Pah1p phosphatidate phosphatase limits viral replication by regulating phospholipid synthesis. PLOS Pathog 14:4e1006988
    [Google Scholar]
  35. 35. 
    Chuang C, Barajas D, Qin J, Nagy PD 2014. Inactivation of the host lipin gene accelerates RNA virus replication through viral exploitation of the expanded endoplasmic reticulum membrane. PLOS Pathog 10:2e1003944
    [Google Scholar]
  36. 36. 
    Lodhi IJ, Semenkovich CF. 2014. Peroxisomes: a nexus for lipid metabolism and cellular signaling. Cell Metab 19:3380–92
    [Google Scholar]
  37. 37. 
    Coyaud E, Ranadheera C, Cheng D, Gonçalves J, Dyakov BJA et al. 2018. Global interactomics uncovers extensive organellar targeting by Zika virus. Mol. Cell. Proteom. 17:112242–55
    [Google Scholar]
  38. 38. 
    Jean Beltran PM, Cook KC, Hashimoto Y, Galitzine C, Murray LA et al. 2018. Infection-induced peroxisome biogenesis is a metabolic strategy for herpesvirus replication. Cell Host Microbe 24:4526–41.e7
    [Google Scholar]
  39. 39. 
    Sychev ZE, Hu A, DiMaio TA, Gitter A, Camp ND et al. 2017. Integrated systems biology analysis of KSHV latent infection reveals viral induction and reliance on peroxisome mediated lipid metabolism. PLOS Pathog 13:3e1006256
    [Google Scholar]
  40. 40. 
    Romero-Brey I, Bartenschlager R. 2015. Viral infection at high magnification: 3D electron microscopy methods to analyze the architecture of infected cells. Viruses 7:126316–45
    [Google Scholar]
  41. 41. 
    Ahlquist P. 2006. Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat. Rev. Microbiol. 4:5371–82
    [Google Scholar]
  42. 42. 
    Tai AW, Benita Y, Peng LF, Kim S-S, Sakamoto N et al. 2009. A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host Microbe 5:3298–307
    [Google Scholar]
  43. 43. 
    Berger KL, Cooper JD, Heaton NS, Yoon R, Oakland TE et al. 2009. Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication. PNAS 106:187577–82
    [Google Scholar]
  44. 44. 
    Reiss S, Rebhan I, Backes P, Romero-Brey I, Erfle H et al. 2011. Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe 9:132–45
    [Google Scholar]
  45. 45. 
    Berger KL, Kelly SM, Jordan TX, Tartell MA, Randall G 2011. Hepatitis C virus stimulates the phosphatidylinositol 4-kinase III alpha-dependent phosphatidylinositol 4-phosphate production that is essential for its replication. J. Virol. 85:178870–83
    [Google Scholar]
  46. 46. 
    Tai AW, Salloum S. 2011. The role of the phosphatidylinositol 4-kinase PI4KA in hepatitis C virus-induced host membrane rearrangement. PLOS ONE 6:10e26300
    [Google Scholar]
  47. 47. 
    Chukkapalli V, Berger KL, Kelly SM, Thomas M, Deiters A, Randall G 2015. Daclatasvir inhibits hepatitis C virus NS5A motility and hyper-accumulation of phosphoinositides. Virology 476:168–79
    [Google Scholar]
  48. 48. 
    Berger C, Romero-Brey I, Radujkovic D, Terreux R, Zayas M et al. 2014. Daclatasvir-like inhibitors of NS5A block early biogenesis of hepatitis C virus–induced membranous replication factories, independent of RNA replication. Gastroenterology 147:51094–105.e25
    [Google Scholar]
  49. 49. 
    Dorobantu CM, Albulescu L, Harak C, Feng Q, van Kampen M et al. 2015. Modulation of the host lipid landscape to promote RNA virus replication: The picornavirus encephalomyocarditis virus converges on the pathway used by hepatitis C virus. PLOS Pathog 11:9e1005185
    [Google Scholar]
  50. 50. 
    Hsu N-Y, Ilnytska O, Belov G, Santiana M, Chen Y-H et al. 2010. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141:5799–811
    [Google Scholar]
  51. 51. 
    Arita M, Kojima H, Nagano T, Okabe T, Wakita T, Shimizu H 2011. Phosphatidylinositol 4-kinase III beta is a target of enviroxime-like compounds for antipoliovirus activity. J. Virol. 85:52364–72
    [Google Scholar]
  52. 52. 
    Ishikawa-Sasaki K, Sasaki J, Taniguchi K 2014. A complex comprising phosphatidylinositol 4-kinase IIIβ, ACBD3, and Aichi virus proteins enhances phosphatidylinositol 4-phosphate synthesis and is critical for formation of the viral replication complex. J. Virol. 88:126586–98
    [Google Scholar]
  53. 53. 
    Roulin PS, Murer L, Greber UF 2018. A single point mutation in the rhinovirus 2B protein reduces the requirement for phosphatidylinositol 4-kinase class III beta in viral replication. J. Virol. 92:23e01462-18
    [Google Scholar]
  54. 54. 
    Martín-Acebes MA, Blázquez A-B, Jiménez de Oya N, Escribano-Romero E, Saiz J-C 2011. West Nile virus replication requires fatty acid synthesis but is independent on phosphatidylinositol-4-phosphate lipids. PLOS ONE 6:9e24970
    [Google Scholar]
  55. 55. 
    Heaton NS, Perera R, Berger KL, Khadka S, Lacount DJ et al. 2010. Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis. PNAS 107:4017345–50
    [Google Scholar]
  56. 56. 
    Tang W-C, Lin R-J, Liao C-L, Lin Y-L 2014. Rab18 facilitates dengue virus infection by targeting fatty acid synthase to sites of viral replication. J. Virol. 88:126793–804
    [Google Scholar]
  57. 57. 
    Gullberg RC, Steel JJ, Pujari V, Rovnak J, Crick DC, Perera R 2018. Stearoly-CoA desaturase 1 differentiates early and advanced dengue virus infections and determines virus particle infectivity. PLOS Pathog 14:8e1007261
    [Google Scholar]
  58. 58. 
    Nguyen LN, Lim Y-S, Pham LV, Shin H-Y, Kim Y-S, Hwang SB 2014. Stearoyl coenzyme A desaturase 1 is associated with hepatitis C virus replication complex and regulates viral replication. J. Virol. 88:2112311–25
    [Google Scholar]
  59. 59. 
    Lyn RK, Singaravelu R, Kargman S, O'Hara S, Chan H et al. 2014. Stearoyl-CoA desaturase inhibition blocks formation of hepatitis C virus-induced specialized membranes. Sci. Rep. 4:4549
    [Google Scholar]
  60. 60. 
    Lee WM, Ishikawa M, Ahlquist P 2001. Mutation of host Δ9 fatty acid desaturase inhibits brome mosaic virus RNA replication between template recognition and RNA synthesis. J. Virol. 75:52097–106
    [Google Scholar]
  61. 61. 
    Mesmin B, Bigay J, Moser von Filseck J, Lacas-Gervais S, Drin G, Antonny B 2013. A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP. Cell 155:4830–43
    [Google Scholar]
  62. 62. 
    Arita M. 2014. Phosphatidylinositol-4 kinase III beta and oxysterol-binding protein accumulate unesterified cholesterol on poliovirus-induced membrane structure. Microbiol. Immunol. 58:4239–56
    [Google Scholar]
  63. 63. 
    Barajas D, Xu K, de Castro Martín IF, Sasvari Z, Brandizzi F et al. 2014. Co-opted oxysterol-binding ORP and VAP proteins channel sterols to RNA virus replication sites via membrane contact sites. PLOS Pathog 10:10e1004388
    [Google Scholar]
  64. 64. 
    Wang H, Perry JW, Lauring AS, Neddermann P, De Francesco R, Tai AW 2014. Oxysterol-binding protein is a phosphatidylinositol 4-kinase effector required for HCV replication membrane integrity and cholesterol trafficking. Gastroenterology 146:51373–85.e11
    [Google Scholar]
  65. 65. 
    Strating JRPM, van der Linden L, Albulescu L, Bigay J, Arita M et al. 2015. Itraconazole inhibits enterovirus replication by targeting the oxysterol-binding protein. Cell Rep 10:4600–15
    [Google Scholar]
  66. 66. 
    McCune BT, Tang W, Lu J, Eaglesham JB, Thorne L et al. 2017. Noroviruses co-opt the function of host proteins VAPA and VAPB for replication via a phenylalanine–phenylalanine-acidic-tract-motif mimic in nonstructural viral protein Ns1/2. mBio 8:4e00668-17
    [Google Scholar]
  67. 67. 
    Mackenzie JM, Khromykh AA, Parton RG 2007. Cholesterol manipulation by West Nile virus perturbs the cellular immune response. Cell Host Microbe 2:4229–39
    [Google Scholar]
  68. 68. 
    Xu K, Nagy PD. 2017. Sterol binding by the tombusviral replication proteins is essential for replication in yeast and plants. J. Virol. 91:7e01984-16
    [Google Scholar]
  69. 69. 
    Stoeck IK, Lee J-Y, Tabata K, Romero-Brey I, Paul D et al. 2018. Hepatitis C virus replication depends on endosomal cholesterol homeostasis. J. Virol. 92:1e01196-17
    [Google Scholar]
  70. 70. 
    Ilnytska O, Santiana M, Hsu N-Y, Du W-L, Chen Y-H et al. 2013. Enteroviruses harness the cellular endocytic machinery to remodel the host cell cholesterol landscape for effective viral replication. Cell Host Microbe 14:3281–93
    [Google Scholar]
  71. 71. 
    Belov GA, Sztul E. 2014. Rewiring of cellular membrane homeostasis by picornaviruses. J. Virol. 88:179478–89
    [Google Scholar]
  72. 72. 
    Zhang J, Zhang Z, Chukkapalli V, Nchoutmboube JA, Li J et al. 2016. Positive-strand RNA viruses stimulate host phosphatidylcholine synthesis at viral replication sites. PNAS 113:8E1064–73
    [Google Scholar]
  73. 73. 
    Viktorova EG, Nchoutmboube JA, Ford-Siltz LA, Iverson E, Belov GA 2018. Phospholipid synthesis fueled by lipid droplets drives the structural development of poliovirus replication organelles. PLOS Pathog 14:8e1007280
    [Google Scholar]
  74. 74. 
    Banerjee S, Aponte-Diaz D, Yeager C, Sharma SD, Ning G et al. 2018. Hijacking of multiple phospholipid biosynthetic pathways and induction of membrane biogenesis by a picornaviral 3CD protein. PLOS Pathog 14:5e1007086
    [Google Scholar]
  75. 75. 
    Nchoutmboube JA, Viktorova EG, Scott AJ, Ford LA, Pei Z et al. 2013. Increased long chain acyl-Coa synthetase activity and fatty acid import is linked to membrane synthesis for development of picornavirus replication organelles. PLOS Pathog 9:6e1003401
    [Google Scholar]
  76. 76. 
    Zhang J, Diaz A, Mao L, Ahlquist P, Wang X 2012. Host acyl coenzyme A binding protein regulates replication complex assembly and activity of a positive-strand RNA virus. J. Virol. 86:95110–21
    [Google Scholar]
  77. 77. 
    Liebscher S, Ambrose RL, Aktepe TE, Mikulasova A, Prier JE et al. 2018. Phospholipase A2 activity during the replication cycle of the flavivirus West Nile virus. PLOS Pathog 14:4e1007029
    [Google Scholar]
  78. 78. 
    Xu K, Nagy PD. 2015. RNA virus replication depends on enrichment of phosphatidylethanolamine at replication sites in subcellular membranes. PNAS 112:14E1782–91
    [Google Scholar]
  79. 79. 
    Xu K, Nagy PD. 2016. Enrichment of phosphatidylethanolamine in viral replication compartments via co-opting the endosomal Rab5 small GTPase by a positive-strand RNA virus. PLOS Biol 14:10e2000128
    [Google Scholar]
  80. 80. 
    Hyodo K, Taniguchi T, Manabe Y, Kaido M, Mise K et al. 2015. Phosphatidic acid produced by phospholipase D promotes RNA replication of a plant RNA virus. PLOS Pathog 11:5e1004909
    [Google Scholar]
  81. 81. 
    Khan I, Katikaneni DS, Han Q, Sanchez-Felipe L, Hanada K et al. 2014. Modulation of hepatitis C virus genome replication by glycosphingolipids and four-phosphate adaptor protein 2. J. Virol. 88:2112276–95
    [Google Scholar]
  82. 82. 
    Roe B, Kensicki E, Mohney R, Hall WW 2011. Metabolomic profile of hepatitis C virus-infected hepatocytes. PLOS ONE 6:8e23641
    [Google Scholar]
  83. 83. 
    Hirata Y, Ikeda K, Sudoh M, Tokunaga Y, Suzuki A et al. 2012. Self-enhancement of hepatitis C virus replication by promotion of specific sphingolipid biosynthesis. PLOS Pathog 8:8e1002860
    [Google Scholar]
  84. 84. 
    Aktepe TE, Pham H, Mackenzie JM 2015. Differential utilisation of ceramide during replication of the flaviviruses West Nile and dengue virus. Virology 484:241–50
    [Google Scholar]
  85. 85. 
    Kato T, Date T, Miyamoto M, Furusaka A, Tokushige K et al. 2003. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 125:61808–17
    [Google Scholar]
  86. 86. 
    Huang H, Chen Y, Ye J 2007. Inhibition of hepatitis C virus replication by peroxidation of arachidonate and restoration by vitamin E. PNAS 104:4718666–70
    [Google Scholar]
  87. 87. 
    Yamane D, McGivern DR, Wauthier E, Yi M, Madden VJ et al. 2014. Regulation of the hepatitis C virus RNA replicase by endogenous lipid peroxidation. Nat. Med. 20:8927–35
    [Google Scholar]
  88. 88. 
    Saeed M, Andreo U, Chung H-Y, Espiritu C, Branch AD et al. 2015. SEC14L2 enables pan-genotype HCV replication in cell culture. Nature 524:7566471–75
    [Google Scholar]
  89. 89. 
    Harak C, Meyrath M, Romero-Brey I, Schenk C, Gondeau C et al. 2016. Tuning a cellular lipid kinase activity adapts hepatitis C virus to replication in cell culture. Nat. Microbiol. 2:16247
    [Google Scholar]
  90. 90. 
    Aktepe TE, Liebscher S, Prier JE, Simmons CP, Mackenzie JM 2017. The host protein Reticulon 3.1A is utilized by flaviviruses to facilitate membrane remodelling. Cell Rep 21:61639–54
    [Google Scholar]
  91. 91. 
    Tang W-F, Yang S-Y, Wu B-W, Jheng J-R, Chen Y-L et al. 2007. Reticulon 3 binds the 2C protein of enterovirus 71 and is required for viral replication. J. Biol. Chem. 282:85888–98
    [Google Scholar]
  92. 92. 
    Cui X, Lu L, Wang Y, Yuan X, Chen X 2018. The interaction of soybean reticulon homology domain protein (GmRHP) with Soybean mosaic virus encoded P3 contributes to the viral infection. Biochem. Biophys. Res. Commun. 495:32105–10
    [Google Scholar]
  93. 93. 
    Diaz A, Wang X, Ahlquist P 2010. Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. PNAS 107:3716291–96
    [Google Scholar]
  94. 94. 
    Erlandson KJ, Bisht H, Weisberg AS, Hyun S-I, Hansen BT et al. 2016. Poxviruses encode a reticulon-like protein that promotes membrane curvature. Cell Rep 14:92084–91
    [Google Scholar]
  95. 95. 
    Tabata K, Arimoto M, Arakawa M, Nara A, Saito K et al. 2016. Unique requirement for ESCRT factors in flavivirus particle formation on the endoplasmic reticulum. Cell Rep 16:92339–47
    [Google Scholar]
  96. 96. 
    Barbosa NS, Mendonça LR, Dias MVS, Pontelli MC, da Silva EZM et al. 2018. ESCRT machinery components are required for Orthobunyavirus particle production in Golgi compartments. PLOS Pathog 14:5e1007047
    [Google Scholar]
  97. 97. 
    Diaz A, Zhang J, Ollwerther A, Wang X, Ahlquist P 2015. Host ESCRT proteins are required for bromovirus RNA replication compartment assembly and function. PLOS Pathog 11:3e1004742
    [Google Scholar]
  98. 98. 
    Barajas D, Jiang Y, Nagy PD 2009. A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLOS Pathog 5:12e1000705
    [Google Scholar]
  99. 99. 
    Kovalev N, de Castro Martín IF, Pogany J, Barajas D, Pathak K et al. 2016. Role of viral RNA and co-opted cellular ESCRT-I and ESCRT-III factors in formation of tombusvirus spherules harboring the tombusvirus replicase. J. Virol. 90:73611–26
    [Google Scholar]
  100. 100. 
    Gong X, Qian H, Zhou X, Wu J, Wan T et al. 2016. Structural insights into the Niemann-Pick C1 (NPC1)-mediated cholesterol transfer and Ebola infection. Cell 165:61467–78
    [Google Scholar]
  101. 101. 
    Kaufusi PH, Kelley JF, Yanagihara R, Nerurkar VR 2014. Induction of endoplasmic reticulum-derived replication-competent membrane structures by West Nile virus non-structural protein 4B. PLOS ONE 9:1e84040
    [Google Scholar]
  102. 102. 
    Li MY, Grandadam M, Kwok K, Lagache T, Siu YL et al. 2015. KDEL receptors assist dengue virus exit from the endoplasmic reticulum. Cell Rep 10:91496–507
    [Google Scholar]
  103. 103. 
    Lee Y-R, Kuo S-H, Lin C-Y, Fu P-J, Lin Y-S et al. 2018. Dengue virus-induced ER stress is required for autophagy activation, viral replication, and pathogenesis both in vitro and in vivo. Sci. Rep 8:1489
    [Google Scholar]
  104. 104. 
    Ward AM, Calvert MEK, Read LR, Kang S, Levitt BE et al. 2016. The Golgi associated ERI3 is a Flavivirus host factor. Sci. Rep. 6:34379
    [Google Scholar]
  105. 105. 
    Ramsey J, Renzi EC, Arnold RJ, Trinidad JC, Mukhopadhyay S 2017. Palmitoylation of Sindbis virus TF protein regulates its plasma membrane localization and subsequent incorporation into virions. J. Virol. 91:3e02000-16
    [Google Scholar]
  106. 106. 
    Corbic Ramljak I, Stanger J, Real-Hohn A, Dreier D, Wimmer L et al. 2018. Cellular N-myristoyltransferases play a crucial picornavirus genus-specific role in viral assembly, virion maturation, and infectivity. PLOS Pathog 14:8e1007203
    [Google Scholar]
  107. 107. 
    Zhu Y, Luo S, Sabo Y, Wang C, Tong L, Goff SP 2017. Heme oxygenase 2 binds myristate to regulate retrovirus assembly and TLR4 signaling. Cell Host Microbe 21:2220–30
    [Google Scholar]
  108. 108. 
    Carluccio AV, Prigigallo MI, Rosas-Diaz T, Lozano-Duran R, Stavolone L 2018. S-acylation mediates Mungbean yellow mosaic virus AC4 localization to the plasma membrane and in turns gene silencing suppression. PLOS Pathog 14:8e1007207
    [Google Scholar]
  109. 109. 
    Dick RA, Zadrozny KK, Xu C, Schur FKM, Lyddon TD et al. 2018. Inositol phosphates are assembly co-factors for HIV-1. Nature 560:7719509–12
    [Google Scholar]
  110. 110. 
    Yandrapalli N, Lubart Q, Tanwar HS, Picart C, Mak J et al. 2016. Self assembly of HIV-1 Gag protein on lipid membranes generates PI(4,5)P2/cholesterol nanoclusters. Sci. Rep. 6:39332
    [Google Scholar]
  111. 111. 
    Liu Q, Chen L, Aguilar HC, Chou KC 2018. A stochastic assembly model for Nipah virus revealed by super-resolution microscopy. Nat. Commun. 9:13050
    [Google Scholar]
  112. 112. 
    Salamango DJ, Alam KK, Burke DH, Johnson MC 2016. In vivo analysis of infectivity, fusogenicity, and incorporation of a mutagenic viral glycoprotein library reveals determinants for virus incorporation. J. Virol. 90:146502–14
    [Google Scholar]
  113. 113. 
    Blazevic J, Rouha H, Bradt V, Heinz FX, Stiasny K 2016. Membrane anchors of the structural flavivirus proteins and their role in virus assembly. J. Virol. 90:146365–78
    [Google Scholar]
  114. 114. 
    DuRaine G, Wisner TW, Howard P, Williams M, Johnson DC 2017. Herpes simplex virus gE/gI and US9 promote both envelopment and sorting of virus particles in the cytoplasm of neurons, two processes that precede anterograde transport in axons. J. Virol. 91:11e00050-17
    [Google Scholar]
  115. 115. 
    Therkelsen MD, Klose T, Vago F, Jiang W, Rossmann MG, Kuhn RJ 2018. Flaviviruses have imperfect icosahedral symmetry. PNAS 115:4511608–12
    [Google Scholar]
  116. 116. 
    Chojnacki J, Waithe D, Carravilla P, Huarte N, Galiani S et al. 2017. Envelope glycoprotein mobility on HIV-1 particles depends on the virus maturation state. Nat. Commun. 8:1545
    [Google Scholar]
  117. 117. 
    Lorizate M, Sachsenheimer T, Glass B, Habermann A, Gerl MJ et al. 2013. Comparative lipidomics analysis of HIV-1 particles and their producer cell membrane in different cell lines. Cell. Microbiol. 15:2292–304
    [Google Scholar]
  118. 118. 
    Brügger B, Glass B, Haberkant P, Leibrecht I, Wieland FT, Kräusslich H-G 2006. The HIV lipidome: a raft with an unusual composition. PNAS 103:82641–46
    [Google Scholar]
  119. 119. 
    Nieto-Garai JA, Glass B, Bunn C, Giese M, Jennings G et al. 2018. Lipidomimetic compounds act as HIV-1 entry inhibitors by altering viral membrane structure. Front. Immunol. 9:1983
    [Google Scholar]
  120. 120. 
    Kawaguchi A, Hirohama M, Harada Y, Osari S, Nagata K 2015. Influenza virus induces cholesterol-enriched endocytic recycling compartments for budozone formation via cell cycle-independent centrosome maturation. PLOS Pathog 11:11e1005284
    [Google Scholar]
  121. 121. 
    Zawada KE, Wrona D, Rawle RJ, Kasson PM 2016. Influenza viral membrane fusion is sensitive to sterol concentration but surprisingly robust to sterol chemical identity. Sci. Rep. 6:29842
    [Google Scholar]
  122. 122. 
    Martín-Acebes MA, Merino-Ramos T, Blázquez A-B, Casas J, Escribano-Romero E et al. 2014. The composition of West Nile virus lipid envelope unveils a role of sphingolipid metabolism in flavivirus biogenesis. J. Virol. 88:2012041–54
    [Google Scholar]
  123. 123. 
    Martín-Acebes MA, Gabandé-Rodríguez E, García-Cabrero AM, Sánchez MP, Ledesma MD et al. 2016. Host sphingomyelin increases West Nile virus infection in vivo. J. Lipid Res. 57:3422–32
    [Google Scholar]
  124. 124. 
    Liu STH, Sharon-Friling R, Ivanova P, Milne SB, Myers DS et al. 2011. Synaptic vesicle-like lipidome of human cytomegalovirus virions reveals a role for SNARE machinery in virion egress. PNAS 108:3112869–74
    [Google Scholar]
  125. 125. 
    Coller KE, Berger KL, Heaton NS, Cooper JD, Yoon R, Randall G 2009. RNA interference and single particle tracking analysis of hepatitis C virus endocytosis. PLOS Pathog 5:12e1000702
    [Google Scholar]
  126. 126. 
    Merz A, Long G, Hiet M-S, Brügger B, Chlanda P et al. 2011. Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome. J. Biol. Chem. 286:43018–32
    [Google Scholar]
  127. 127. 
    Lavie M, Dubuisson J. 2017. Interplay between hepatitis C virus and lipid metabolism during virus entry and assembly. Biochimie 141:62–69
    [Google Scholar]
  128. 128. 
    Fujii K, Hurley JH, Freed EO 2007. Beyond Tsg101: the role of Alix in “ESCRTing” HIV-1. Nat. Rev. Microbiol. 5:12912–16
    [Google Scholar]
  129. 129. 
    Gordon TB, Hayward JA, Marsh GA, Baker ML, Tachedjian G 2019. Host and viral proteins modulating Ebola and Marburg virus egress. Viruses 11:125
    [Google Scholar]
  130. 130. 
    Rossman JS, Jing X, Leser GP, Lamb RA 2010. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142:6902–13
    [Google Scholar]
  131. 131. 
    Feng Z, Hensley L, McKnight KL, Hu F, Madden V et al. 2013. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496:7445367–71
    [Google Scholar]
  132. 132. 
    González-López O, Rivera-Serrano EE, Hu F, Hensley L, McKnight KL et al. 2018. Redundant late domain functions of tandem VP2 YPX3l motifs in nonlytic cellular egress of quasi-enveloped hepatitis A virus. J. Virol. 92:23e01308-1
    [Google Scholar]
  133. 133. 
    Hirai-Yuki A, Hensley L, Whitmire JK, Lemon SM 2016. Biliary secretion of quasi-enveloped human hepatitis A virus. mBio 7:6e01998-16
    [Google Scholar]
  134. 134. 
    Raab-Traub N, Dittmer DP. 2017. Viral effects on the content and function of extracellular vesicles. Nat. Rev. Microbiol. 15:9559–72
    [Google Scholar]
  135. 135. 
    Bird SW, Maynard ND, Covert MW, Kirkegaard K 2014. Nonlytic viral spread enhanced by autophagy components. PNAS 111:3613081–86
    [Google Scholar]
  136. 136. 
    Corona AK, Saulsbery HM, Corona Velazquez AF, Jackson WT 2018. Enteroviruses remodel autophagic trafficking through regulation of host SNARE proteins to promote virus replication and cell exit. Cell Rep 22:123304–14
    [Google Scholar]
  137. 137. 
    Robinson SM, Tsueng G, Sin J, Mangale V, Rahawi S et al. 2014. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLOS Pathog 10:4e1004045
    [Google Scholar]
  138. 138. 
    Mohamud Y, Shi J, Qu J, Poon T, Xue YC et al. 2018. Enteroviral infection inhibits autophagic flux via disruption of the SNARE complex to enhance viral replication. Cell Rep 22:123292–303
    [Google Scholar]
  139. 139. 
    Jansens RJJ, Van den Broeck W, De Pelsmaeker S, Lamote JAS, Van Waesberghe C et al. 2017. Pseudorabies virus US3-induced tunneling nanotubes contain stabilized microtubules, interact with neighbouring cells via cadherins and allow intercellular molecular communication. J. Virol. 91:19e00749-17
    [Google Scholar]
  140. 140. 
    Chen Y-H, Du W, Hagemeijer MC, Takvorian PM, Pau C et al. 2015. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 160:4619–30
    [Google Scholar]
  141. 141. 
    Cuevas JM, Durán-Moreno M, Sanjuán R 2017. Multi-virion infectious units arise from free viral particles in an enveloped virus. Nat. Microbiol. 2:17078
    [Google Scholar]
  142. 142. 
    Santiana M, Ghosh S, Ho BA, Rajasekaran V, Du W-L et al. 2018. Vesicle-cloaked virus clusters are optimal units for inter-organismal viral transmission. Cell Host Microbe 24:2208–20.e8
    [Google Scholar]
  143. 143. 
    Schoggins JW, Randall G. 2013. Lipids in innate antiviral defense. Cell Host Microbe 14:4379–85
    [Google Scholar]
  144. 144. 
    Fagone P, Jackowski S. 2009. Membrane phospholipid synthesis and endoplasmic reticulum function. J. Lipid Res. 50:Suppl.S311–16
    [Google Scholar]
/content/journals/10.1146/annurev-virology-092818-015748
Loading
/content/journals/10.1146/annurev-virology-092818-015748
Loading

Data & Media loading...

  • 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