Skip to main content

Nuclear Hormone Receptors and Host-Virus Interactions

  • Chapter
  • First Online:
Nuclear Receptors
  • 853 Accesses

Abstract

Viruses are a diverse class of obligate parasites that require a host to propagate. Viruses have evolved to exploit host signaling pathways to promote propagation and facilitation of their life cycle. Host-virus interactions are a complex network that can enable the viral life cycle within the host. These interactions also allow for the host’s immune system to overcome the infection. Successful viral infection and the resultant antiviral response are highly dependent on the dynamic molecular interactions between the viral components/factors and the host’s antiviral and cellular signaling pathways. These interactions are also modulated by the cellular microenvironment that can be beneficial or detrimental to the viral life cycle. Recently, increasing evidence has emerged highlighting the role of the nuclear hormone receptor superfamily in facilitating host-virus interactions. The nuclear hormone receptor family is a diverse group of transcription factors that share analogous structure and architectures. They can be activated or repressed depending on the upstream signal. This chapter will focus on the diverse roles that nuclear hormone receptors play in modulating host-virus interactions, as well as highlighting the crosstalk between viruses and specific subtypes of nuclear receptors, namely, peroxisome proliferator-activated receptors (PPARs), liver X receptor (LXRs), and retinoid X receptors (FXRs).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Adler B, Sattler C, Adler H. Herpesviruses and their host cells: a successful liaison. Trends Microbiol. Elsevier Ltd,. 2017;25(3):229–41. https://doi.org/10.1016/j.tim.2016.11.009.

    Article  CAS  PubMed  Google Scholar 

  2. Agarwal N, et al. HIV-1 viral protein R (Vpr) induces fatty liver in mice via LXRα and PPARα dysregulation: implications for HIV-specific pathogenesis of NAFLD. Sci Rep. Springer US,. 2017;7(1):1–15. https://doi.org/10.1038/s41598-017-13835-w.

    Article  CAS  Google Scholar 

  3. Altmann R, et al. 13-Oxo-ODE is an endogenous ligand for PPARγ in human colonic epithelial cells. Biochem Pharmacol. 2007;74(4):612–22. https://doi.org/10.1016/j.bcp.2007.05.027.

    Article  CAS  PubMed  Google Scholar 

  4. André P, et al. Role of nuclear receptors in hepatitis B and C infections. Clin Res Hepatol Gastroenterol. 2011;35(3):169–75. https://doi.org/10.1016/j.clinre.2011.01.001.

    Article  CAS  PubMed  Google Scholar 

  5. Aranda A, Pascual A. Nuclear hormone receptors and gene expression. Physiol Rev. 2001;81(3):1269–304. https://doi.org/10.1152/physrev.2001.81.3.1269.

    Article  CAS  PubMed  Google Scholar 

  6. Barba G, et al. Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci U S A. 1997;94(4):1200–5. https://doi.org/10.1073/pnas.94.4.1200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Barrows NJ, et al. Biochemistry and molecular biology of flaviviruses. Chem Rev. 2018;118(8):4448–82. https://doi.org/10.1021/acs.chemrev.7b00719.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bartenschlager R, et al. Assembly of infectious hepatitis C virus particles. Trends Microbiol. 2011;19(2):95–103. https://doi.org/10.1016/j.tim.2010.11.005.

    Article  CAS  PubMed  Google Scholar 

  9. Bassaganya-Riera J, et al. PPAR-γ activation as an anti-inflammatory therapy for respiratory virus infections. Viral Immunol. 2010;23(4):343–52. https://doi.org/10.1089/vim.2010.0016.

    Article  CAS  PubMed  Google Scholar 

  10. Bastard JP, et al. Association between altered expression of adipogenic factor SREBP1 in lipoatrophic adipose tissue from HIV-1-infected patients and abnormal adipocyte differentiation and insulin resistance. Lancet. 2002;359(9311):1026–31. https://doi.org/10.1016/S0140-6736(02)08094-7.

    Article  CAS  PubMed  Google Scholar 

  11. Behrens GMN, Grinspoon S, Carr A. Cardiovascular risk and body-fat abnormalities in HIV-infected adults [4] (multiple letters). N Engl J Med. 2005;352(16):1721–2. https://doi.org/10.1056/NEJM200504213521620.

    Article  CAS  PubMed  Google Scholar 

  12. Berger KL, et al. Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication. Proc Natl Acad Sci U S A. 2009;106(18):7577–82. https://doi.org/10.1073/pnas.0902693106.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Bernier A, et al. Transcriptional profiling reveals molecular signatures associated with HIV permissiveness in th1th17 cells and identifies peroxisome proliferator-activated receptor gamma as an intrinsic negative regulator of viral replication. Retrovirology. 2013;10(1) https://doi.org/10.1186/1742-4690-10-160.

  14. Berrodin TJ, et al. Identification of 5α,6α-epoxycholesterol as a novel modulator of liver X receptor activity. Mol Pharmacol. 2010;78(6):1046–58. https://doi.org/10.1124/mol.110.065193.

    Article  CAS  PubMed  Google Scholar 

  15. Bocchetta S, et al. Up-regulation of the ATP-binding cassette transporter A1 inhibits hepatitis C virus infection. PLoS One. 2014;9(3) https://doi.org/10.1371/journal.pone.0092140.

  16. Bong S, et al. Expression of liver X receptor correlates with intrahepatic inflammation and fibrosis in patients with nonalcoholic fatty liver disease. Dig Dis Sci. 2014;59:2975–82. https://doi.org/10.1007/s10620-014-3289-x.

    Article  CAS  Google Scholar 

  17. Bougarne N, et al. Molecular actions of PPARα in lipid metabolism and inflammation. Endocr Rev. 2018;39(5):760–802. https://doi.org/10.1210/er.2018-00064.

    Article  PubMed  Google Scholar 

  18. Brügger B, et al. The HIV lipidome: a raft with an unusual composition. Proc Natl Acad Sci U S A. 2006;103(8):2641–6. https://doi.org/10.1073/pnas.0511136103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Cagno V, et al. Inhibition of herpes simplex-1 virus replication by 25-hydroxycholesterol and 27-hydroxycholesterol. Redox Biol. Elsevier B.V.,. 2017;12(March):522–7. https://doi.org/10.1016/j.redox.2017.03.016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Carro AC, Damonte EB. Requirement of cholesterol in the viral envelope for dengue virus infection. Virus Res. Elsevier B.V.,. 2013;174(1–2):78–87. https://doi.org/10.1016/j.virusres.2013.03.005.

    Article  CAS  PubMed  Google Scholar 

  21. Castrillo A, et al. Crosstalk between LXR and Toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol Cell. 2003;12(4):805–16. https://doi.org/10.1016/S1097-2765(03)00384-8.

    Article  CAS  PubMed  Google Scholar 

  22. Chandra V, et al. Structure of the intact PPAR-γ-RXR-α nuclear receptor complex on DNA. Nature. 2008;456(7220):350–6. https://doi.org/10.1038/nature07413.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Chang K-O, George DW. Bile acids promote the expression of hepatitis C virus in replicon-harboring cells. J Virol. 2007;81(18):9633–40. https://doi.org/10.1128/jvi.00795-07.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chen SL, Morgan TR. The natural history of hepatitis C virus (HCV) infection. Int J Med Sci. 2006:47–52. https://doi.org/10.7150/ijms.3.47.

  25. Cheng Y, et al. Hepatitis C virus infection down-regulates the expression of peroxisome proliferator-activated receptor α and carnitine palmitoyl acyl-CoA transferase 1A. World J Gastroenterol. 2005;11(48):7591–6. https://doi.org/10.3748/wjg.v11.i48.7591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Chiang JYL. Bile acid metabolism and signaling. Compr Physiol. 2013;3(3):1191–212. https://doi.org/10.1002/cphy.c120023.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Choi YH, et al. Hepatitis B virus X protein modulates peroxisome proliferator-activated receptor γ through protein-protein interaction. FEBS Lett. 2004;557(1–3):73–80. https://doi.org/10.1016/S0014-5793(03)01449-2.

    Article  CAS  PubMed  Google Scholar 

  28. Claudel T, Staels B, Kuipers F. The Farnesoid X receptor: a molecular link between bile acid and lipid and glucose metabolism. Arterioscler Thromb Vasc Biol. 2005;25(10):2020–31. https://doi.org/10.1161/01.ATV.0000178994.21828.a7.

    Article  CAS  PubMed  Google Scholar 

  29. Dalgleish AG, et al. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature. 1984;321:763–7.

    Article  Google Scholar 

  30. Deng HK, et al. Identification of a major co-receptor for primary isolates of HIV-1. Nature. 1996;381(6584):661–6. https://doi.org/10.1038/381661a0.

    Article  CAS  PubMed  Google Scholar 

  31. Devchand PR, Ziouzenkova O, Plutzky J. Oxidative stress and peroxisome proliferator-activated receptors reversing the curse? Circ Res. 2004;95(12):1137–9. https://doi.org/10.1161/01.RES.0000151331.69399.b2.

    Article  CAS  PubMed  Google Scholar 

  32. Dharancy S, et al. Impaired expression of the peroxisome proliferator-activated receptor alpha during hepatitis C virus infection. Gastroenterology. 2005;128(2):334–42. https://doi.org/10.1053/j.gastro.2004.11.016.

    Article  CAS  PubMed  Google Scholar 

  33. Dreyer C, et al. Control of the peroxisomal β-oxidation pathway by a novel family of nuclear hormone receptors. Cell. 1992;68(5):879–87. https://doi.org/10.1016/0092-8674(92)90031-7.

    Article  CAS  PubMed  Google Scholar 

  34. Du L, et al. Peroxisome Proliferators Activated Receptor (PPAR) agonists activate hepatitis B virus replication in vivo. Virol J. 2017;14(1):1–9. https://doi.org/10.1186/s12985-017-0765-x.

    Article  CAS  Google Scholar 

  35. Dubrovsky L, et al. Liver X receptor agonist inhibits HIV-1 replication and prevents HIV-induced reduction of plasma HDL in humanized mouse model of HIV infection. Biochem Biophys Res Commun. Elsevier Inc.,. 2012;419(1):95–8. https://doi.org/10.1016/j.bbrc.2012.01.137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Eslam M, Khattab MA, Harrison SA. Peroxisome proliferator-activated receptors and hepatitis C virus. Ther Adv Gastroenterol. 2011;4(6):419–31. https://doi.org/10.1177/1756283X11405251.

    Article  CAS  Google Scholar 

  37. Fedson DS. Treating influenza with statins and other immunomodulatory agents. Antivir Res. Elsevier B.V.,. 2013;99(3):417–35. https://doi.org/10.1016/j.antiviral.2013.06.018.

    Article  CAS  PubMed  Google Scholar 

  38. Fujita N, et al. Effects of bezafibrate in patients with chronic hepatitis C virus infection: combination with interferon and ribavirin. J Viral Hepat. 2006;13(7):441–8. https://doi.org/10.1111/j.1365-2893.2005.00718.x.

    Article  CAS  PubMed  Google Scholar 

  39. Gan SK, et al. Altered myocellular and abdominal fat partitioning predict disturbance in insulin action in HIV protease inhibitor-related lipodystrophy. Diabetes. 2002;51(11):3163–9. https://doi.org/10.2337/diabetes.51.11.3163.

    Article  CAS  PubMed  Google Scholar 

  40. Ganguli G, Mukherjee U, Sonawane A. Peroxisomes and oxidative stress: their implications in the modulation of cellular immunity during mycobacterial infection. Front Microbiol. 2019;10(JUN):1–17. https://doi.org/10.3389/fmicb.2019.01121.

    Article  Google Scholar 

  41. Gavrilova O, et al. Liver peroxisome proliferator-activated receptor γ contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass. J Biol Chem. 2003;278(36):34268–76. https://doi.org/10.1074/jbc.M300043200.

    Article  CAS  PubMed  Google Scholar 

  42. Gearing KL, et al. Interaction of the peroxisome-proliferator-activated receptor and retinoid X receptor. Proc Natl Acad Sci U S A. 1993;90(4):1440–4. https://doi.org/10.1073/pnas.90.4.1440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Georgel P, et al. Virus-host interactions in hepatitis C virus infection: implications for molecular pathogenesis and antiviral strategies. Trends Mol Med. 2010;16(6):277–86. https://doi.org/10.1016/j.molmed.2010.04.003.

    Article  CAS  PubMed  Google Scholar 

  44. Goldwasser J, et al. Naringenin inhibits the assembly and long-term production of infectious hepatitis C virus particles through a PPAR-mediated mechanism. J Hepatol. European Association for the Study of the Liver,. 2011;55(5):963–71. https://doi.org/10.1016/j.jhep.2011.02.011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. De Gottardi A, et al. Peroxisome proliferator-activated receptor-α and -γ mRNA levels are reduced in chronic hepatitis C with steatosis and genotype 3 infection. Aliment Pharmacol Ther. 2006;23(1):107–14. https://doi.org/10.1111/j.1365-2036.2006.02729.x.

    Article  CAS  PubMed  Google Scholar 

  46. Grassi G, et al. Hepatitis C virus relies on lipoproteins for its life cycle. World J Gastroenterol. 2016;22(6):1953–65. https://doi.org/10.3748/wjg.v22.i6.1953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Grimm, D., Thimme, R. & Blum, H. E. ‘HBV life cycle and novel drug targets’, Hepatology International. 2011;5(2):644–653. https://doi.org/10.1007/s12072-011-9261-3.

  48. Guidotti LG, et al. In vivo regulation of hepatitis B virus replication by peroxisome proliferators. J Virol. 1999;73(12):10377–86. https://doi.org/10.1128/jvi.73.12.10377-10386.1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Gupta S, Pandak WM, Hylemon PB. Lxrα is the dominant regulator of CYP7A1 transcription. Biochem Biophys Res Commun. 2002;293(1):338–43. https://doi.org/10.1016/S0006-291X(02)00229-2.

    Article  CAS  PubMed  Google Scholar 

  50. Gustafsson JA. Historical overview of nuclear receptors. J Steroid Biochem Mol Biol. Elsevier Ltd,. 2016;157:3–6. https://doi.org/10.1016/j.jsbmb.2015.03.004.

    Article  CAS  PubMed  Google Scholar 

  51. Guyader M, et al. Role for human immunodeficiency virus type 1 membrane cholesterol in viral internalization. J Virol. 2002;76(20):10356–64. https://doi.org/10.1128/jvi.76.20.10356-10364.2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Hadigan C, et al. Increased rates of lipolysis among human immunodeficiency virus-infected men receiving highly active antiretroviral therapy. Metab Clin Exp. 2002;51(9):1143–7. https://doi.org/10.1053/meta.2002.34704.

    Article  CAS  PubMed  Google Scholar 

  53. Hanley TM, et al. PPARγ and LXR signaling inhibit dendritic cell-mediated HIV-1 capture and trans-infection. PLoS Pathog. 2010;6(7):1–16. https://doi.org/10.1371/journal.ppat.1000981.

    Article  CAS  Google Scholar 

  54. Hanley TM, Viglianti GA. Nuclear receptor signaling inhibits HIV-1 replication in macrophages through multiple trans-repression mechanisms. J Virol. 2011;85(20):10834–50. https://doi.org/10.1128/jvi.00789-11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Hayes MM, et al. Peroxisome proliferator-activated receptor γ agonists inhibit HIV-1 replication in macrophages by transcriptional and post-transcriptional effects. J Biol Chem. 2002;277(19):16913–9. https://doi.org/10.1074/jbc.M200875200.

    Article  CAS  PubMed  Google Scholar 

  56. Heaton NS, Randall G. Dengue virus-induced autophagy regulates lipid metabolism. Cell Host Microbe. Elsevier Inc.,. 2010;8(5):422–32. https://doi.org/10.1016/j.chom.2010.10.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hirokane H, et al. Bile acid reduces the secretion of very low density lipoprotein by repressing microsomal triglyceride transfer protein gene expression mediated by hepatocyte nuclear factor-4. J Biol Chem. 2004;279(44):45685–92. https://doi.org/10.1074/jbc.M404255200.

    Article  CAS  PubMed  Google Scholar 

  58. Huan B, Kosovsky MJ, Siddiqui A. Retinoid X receptor alpha transactivates the hepatitis B virus enhancer 1 element by forming a heterodimeric complex with the peroxisome proliferator-activated receptor. J Virol. 1995;69(1):547–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Huang H, et al. Human herpesvirus 6 envelope cholesterol is required for virus entry. J Gen Virol. 2006;87(2):277–85. https://doi.org/10.1099/vir.0.81551-0.

    Article  CAS  PubMed  Google Scholar 

  60. Huang H, et al. Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins. Proc Natl Acad Sci U S A. 2007;104(14):5848–53. https://doi.org/10.1073/pnas.0700760104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Huang P, Chandra V, Rastinejad F. Structural overview of the nuclear receptor superfamily: insights into physiology and therapeutics. Annu Rev Physiol. 2010;72(1):247–72. https://doi.org/10.1146/annurev-physiol-021909-135917.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Huang S, Zhu B, et al. PPAR-γ in macrophages limits pulmonary inflammation and promotes host recovery following respiratory viral infection. J Virol. 2019a;93(9):1–15.

    Article  Google Scholar 

  63. Huang S, Goplen NP, et al. Macrophage PPAR-γ suppresses long-term lung fibrotic sequelae following acute influenza infection. PLoS One. 2019b;14(10):1–17. https://doi.org/10.1371/journal.pone.0223430.

    Article  CAS  Google Scholar 

  64. Huang W, et al. PPARα and PPARγ attenuate HIV-induced dysrégulation of tight junction proteins by modulations of matrix metalloproteinase and proteasome activities. FASEB J. 2009;23(5):1596–606. https://doi.org/10.1096/fj.08-121624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Huang W, et al. PPARα and PPARγ protect against HIV-1-induced MMP-9 overexpression via caveolae-associated ERK and Akt signaling. FASEB J. 2011;25(11):3979–88. https://doi.org/10.1096/fj.11-188607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Huang W, et al. PPAR agonist-mediated protection against HIV Tat-induced cerebrovascular toxicity is enhanced in MMP-9-deficient mice. J Cereb Blood Flow Metab. 2014;34(4):646–53. https://doi.org/10.1038/jcbfm.2013.240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Hummasti S, Tontonoz P. The peroxisome proliferator-activated receptor N-terminal domain controls isotype-selective gene expression and adipogenesis. Mol Endocrinol. 2006;20(6):1261–75. https://doi.org/10.1210/me.2006-0025.

    Article  CAS  PubMed  Google Scholar 

  68. Issemann I, Green S. Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature. 1990;347(6294):645–50. https://doi.org/10.1038/347645a0.

    Article  CAS  PubMed  Google Scholar 

  69. Janowski BA, et al. An oxysterol signalling pathway mediated by the nuclear receptor LXRa. Lett Nat. 1996;96(1):266–71.

    Google Scholar 

  70. Jones DM, McLauchlan J. Hepatitis C virus: assembly and release of virus particles. J Biol Chem. 2010;285(30):22733–9. https://doi.org/10.1074/jbc.R110.133017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Joseph SB, et al. Direct and indirect mechanisms for regulation of fatty acid synthase gene expression by liver X receptors. J Biol Chem. 2002;277(13):11019–25. https://doi.org/10.1074/jbc.M111041200.

    Article  CAS  PubMed  Google Scholar 

  72. Kalaany NY, Mangelsdorf DJ. LXRS AND FXR: the Yin and Yang of cholesterol and fat metabolism. Annu Rev Physiol. 2006;68(1):159–91. https://doi.org/10.1146/annurev.physiol.68.033104.152158.

    Article  CAS  PubMed  Google Scholar 

  73. Kandathil AJ, Sugawara S, Balagopal A. Are T cells the only HIV-1 reservoir. Retrovirology. BioMed Central,. 2016;13(1):1–10. https://doi.org/10.1186/s12977-016-0323-4.

    Article  Google Scholar 

  74. Kast HR, et al. Farnesoid X-activated receptor induces apolipoprotein C-II transcription: a molecular mechanism linking plasma triglyceride levels to bile acids. Mol Endocrinol. 2001;15(10):1720–8. https://doi.org/10.1210/mend.15.10.0712.

    Article  CAS  PubMed  Google Scholar 

  75. Kersten S. Peroxisome proliferator activated receptors and lipoprotein metabolism. PPAR Res. 2008, 2008; https://doi.org/10.1155/2008/132960.

  76. Kim HY, et al. Bile acids increase hepatitis B virus gene expression and inhibit interferon-α activity. FEBS J. 2010;277(13):2791–802. https://doi.org/10.1111/j.1742-4658.2010.07695.x.

    Article  CAS  PubMed  Google Scholar 

  77. Kim KH, et al. Hepatitis B virus X protein induces hepatic steatosis via transcriptional activation of SREBP1 and PPARγ. Gastroenterology. 2007;132(5):1955–67. https://doi.org/10.1053/j.gastro.2007.03.039.

    Article  CAS  PubMed  Google Scholar 

  78. Kim KJ, et al. Hepatitis C virus NS5A protein increases hepatic lipid accumulation via induction of activation and expression of PPARgamma. FEBS Letters. Federation of European Biochemical Societies,. 2009;583(17):2720–6. https://doi.org/10.1016/j.febslet.2009.07.034.

    Article  CAS  PubMed  Google Scholar 

  79. Korach-André M, et al. Liver x receptors regulate de novo lipogenesis in a tissue-specific manner in c57bl/6 female mice. Am J Physiol Endocrinol Metab. 2011;301(1):210–22. https://doi.org/10.1152/ajpendo.00541.2010.

    Article  CAS  Google Scholar 

  80. Lange PT, et al. Liver X receptors suppress activity of cholesterol and fatty acid synthesis pathways to oppose gammaherpesvirus replication. mBio. 2018;9(4):1–15. https://doi.org/10.1128/mBio.01115-18.

    Article  Google Scholar 

  81. Lange PT, et al. LXR alpha restricts gammaherpesvirus reactivation from latently infected peritoneal cells. J Virol. 2019;93(6):1–16. https://doi.org/10.1128/jvi.02071-18.

    Article  CAS  Google Scholar 

  82. Lehmann JM, et al. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J Biol Chem. 1997;272(6):3137–40. https://doi.org/10.1074/jbc.272.6.3137.

    Article  CAS  PubMed  Google Scholar 

  83. León-Juárez M, et al. Recombinant Dengue virus protein NS2B alters membrane permeability in different membrane models. Virology Journal. 2016;13(1):1–11. https://doi.org/10.1186/s12985-015-0456-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Levin N, et al. Macrophage liver X receptor is required for antiatherogenic activity of LXR agonists. Arterioscler Thromb Vasc Biol. 2005;25(1):135–42. https://doi.org/10.1161/01.ATV.0000150044.84012.68.

    Article  CAS  PubMed  Google Scholar 

  85. Li H, et al. The metabolic responses to hepatitis B virus infection shed new light on pathogenesis and targets for treatment. Sci Rep. 2015;5:8421. https://doi.org/10.1038/srep08421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Li X, Yeh V, Molteni V. Liver X receptor modulators: a review of recently patented compounds (2007–2009). Expert Opin Ther Pat. 2010a;20(4):535–62. https://doi.org/10.1517/13543771003621269.

    Article  CAS  PubMed  Google Scholar 

  87. Li ZH, et al. Hepatitis C virus core protein induces malignant transformation of biliary epithelial cells by activating nuclear factor-κB pathway. J Gastroenterol and Hepatol (Australia). 2010b;25(7):1315–20. https://doi.org/10.1111/j.1440-1746.2009.06201.x.

    Article  CAS  Google Scholar 

  88. Lin YM, et al. Calcitriol inhibits HCV infection via blockade of activation of PPAR and interference with endoplasmic reticulum-associated degradation. Viruses. 2018;10(2) https://doi.org/10.3390/v10020057.

  89. Liu Y, et al. Activation of liver X receptor plays a central role in antiviral actions of 25-hydroxycholesterol. J Lipid Res. 2018;59(12):2287–96. https://doi.org/10.1194/jlr.M084558.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Lu TT, Repa JJ, Mangelsdorf DJ. Orphan nuclear receptors as eLiXiRs and FiXeRs of sterol metabolism. J Biol Chem. 2001;276(41):37735–8. https://doi.org/10.1074/jbc.R100035200.

    Article  CAS  PubMed  Google Scholar 

  91. Lyn RK, et al. Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism. Virology. Elsevier B.V.,. 2009;394(1):130–42. https://doi.org/10.1016/j.virol.2009.08.022.

    Article  CAS  PubMed  Google Scholar 

  92. Ma X, et al. Deciphering the roles of PPARγ in adipocytes via dynamic change of transcription complex. Front Endocrinol. 2018;9(AUG):1–10. https://doi.org/10.3389/fendo.2018.00473.

    Article  Google Scholar 

  93. Makishima M, et al. Identification of a nuclear receptor for bile acids. Science. 1999;284(5418):1362–5. https://doi.org/10.1126/science.284.5418.1362.

    Article  CAS  PubMed  Google Scholar 

  94. Michalik L, et al. International Union of Pharmacology. LXI. Peroxisome Proliferator-Activated Receptors. Pharmacol Rev. 2006;58(4):726–41. https://doi.org/10.1124/pr.58.4.5.(NR1C1).

    Article  CAS  PubMed  Google Scholar 

  95. Moriishi K, et al. Critical role of PA28γ in hepatitis C virus-associated steatogenesis and hepatocarcinogenesis. Proc Natl Acad Sci U S A. 2007;104(5):1661–6. https://doi.org/10.1073/pnas.0607312104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Moriya K, et al. Hepatitis C virus core protein induces hepatic steatosis in transgenic mice. J Gen Virol. 1997;78(7):1527–31. https://doi.org/10.1099/0022-1317-78-7-1527.

    Article  CAS  PubMed  Google Scholar 

  97. Morrow MP, et al. Stimulation of the liver X receptor pathway inhibits HIV-1 replication via induction of ATP-binding cassette transporter A1. Mol Pharmacol. 2010;78(2):215–25. https://doi.org/10.1124/mol.110.065029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Moseley CE, Webster RG, Aldridge JR. Peroxisome proliferator-activated receptor and AMP-activated protein kinase agonists protect against lethal influenza virus challenge in mice. Influenza Other Respir Viruses. 2010;4(5):307–11. https://doi.org/10.1111/j.1750-2659.2010.00155.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Motojima K, et al. Expression of putative fatty acid transporter genes are regulated by peroxisome proliferator-activated receptor α and γ activators in a tissue- and inducer-specific manner. J Biol Chem. 1998;273(27):16710–4. https://doi.org/10.1074/jbc.273.27.16710.

    Article  CAS  PubMed  Google Scholar 

  100. Mouzannar K, et al. Farnesoid X receptor-α is a proviral host factor for hepatitis B virus that is inhibited by ligands in vitro and in vivo. FASEB J. 2019;33(2):2472–83. https://doi.org/10.1096/fj.201801181R.

    Article  CAS  PubMed  Google Scholar 

  101. Mujawar Z, et al. Human immunodeficiency virus impairs reverse cholesterol transport from macrophages. Retrovirology. 2006;3(Suppl 1):S82. https://doi.org/10.1186/1742-4690-3-S1-S82.

    Article  PubMed Central  Google Scholar 

  102. Nakajima S, et al. Fungus-derived Neoechinulin B as a novel antagonist of liver X receptor, identified by chemical genetics using a hepatitis C virus cell culture system. J Virol. 2016;90(20):9058–74. https://doi.org/10.1128/jvi.00856-16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Narala VR, et al. Leukotriene B4 is a physiologically relevant endogenous peroxisome proliferator-activated receptor-α agonist. J Biol Chem. 2010;285(29):22067–74. https://doi.org/10.1074/jbc.M109.085118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Nasheri N, et al. Modulation of fatty acid synthase enzyme activity and expression during hepatitis C virus replication. Chem Biol. Elsevier Ltd,. 2013;20(4):570–82. https://doi.org/10.1016/j.chembiol.2013.03.014.

    Article  CAS  PubMed  Google Scholar 

  105. Neufeldt CJ, et al. Rewiring cellular networks by members of the Flaviviridae family. Nat Rev Microbiol. Nature Publishing Group,. 2018;16(3):125–42. https://doi.org/10.1038/nrmicro.2017.170.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Niu Y, et al. Farnesoid X receptor ablation sensitizes mice to hepatitis b virus X protein–induced hepatocarcinogenesis. Hepatology. 2017;65(3):893–906. https://doi.org/10.1002/hep.28924.

    Article  CAS  PubMed  Google Scholar 

  107. O’Flaherty JT, et al. 5-Oxo-ETE analogs and the proliferation of cancer cells. Biochim Biophys Acta Mol Cell Biol Lipids. 2005;1736(3):228–36. https://doi.org/10.1016/j.bbalip.2005.08.009.

    Article  CAS  Google Scholar 

  108. Oehler N, et al. Binding of hepatitis B virus to its cellular receptor alters the expression profile of genes of bile acid metabolism. Hepatology. 2014;60(5):1483–93. https://doi.org/10.1002/hep.27159.

    Article  CAS  PubMed  Google Scholar 

  109. de Oliveira DN, et al. Inflammation markers in the saliva of infants born from Zika-infected mothers: exploring potential mechanisms of microcephaly during fetal development. Sci Rep. 2019;9(1):1–7. https://doi.org/10.1038/s41598-019-49796-5.

    Article  CAS  Google Scholar 

  110. Omeragic A, et al. Peroxisome proliferator-activated receptor-gamma: potential molecular therapeutic target for HIV-1-associated brain inflammation. J Neuroinflammation. 2017;14(1):1–13. https://doi.org/10.1186/s12974-017-0957-8.

    Article  CAS  Google Scholar 

  111. Omeragic A, et al. Peroxisome Proliferator-Activated Receptor-gamma agonists exhibit anti-inflammatory and antiviral effects in an EcoHIV mouse model. Sci Rep. 2019;9(1):1–12. https://doi.org/10.1038/s41598-019-45878-6.

    Article  CAS  Google Scholar 

  112. Ono A, Freed EO. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc Natl Acad Sci U S A. 2001;98(24):13925–30. https://doi.org/10.1073/pnas.241320298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Oram JF, Heinecke JW. ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol Rev. 2005;85(4):1343–72. https://doi.org/10.1152/physrev.00005.2005.

    Article  CAS  PubMed  Google Scholar 

  114. Patrone M, et al. Palmitoylation strengthens cholesterol-dependent multimerization and fusion activity of human cytomegalovirus glycoprotein B (Gb). J Biol Chem. 2016;291(9):4711–22. https://doi.org/10.1074/jbc.M115.682252.

    Article  CAS  PubMed  Google Scholar 

  115. Paul D, Bartenschlager R. Flaviviridae replication organelles: oh, what a tangled web we weave. Ann Rev Virol. 2015;2(1):289–310. https://doi.org/10.1146/annurev-virology-100114-055007.

    Article  CAS  Google Scholar 

  116. Pawlak M, Lefebvre P, Staels B. Molecular mechanism of PPARα action and its impact on lipid metabolism, inflammation and fibrosis in non-alcoholic fatty liver disease. J Hepatol. European Association for the Study of the Liver,. 2015;62(3):720–33. https://doi.org/10.1016/j.jhep.2014.10.039.

    Article  CAS  PubMed  Google Scholar 

  117. Pazienza V, et al. Hepatitis C virus core protein genotype 3a increases SOCS-7 expression through PPAR-γ in Huh-7 cells. J Gen Virol. 2010;91(7):1678–86. https://doi.org/10.1099/vir.0.020644-0.

    Article  CAS  PubMed  Google Scholar 

  118. Perera R, et al. Dengue virus infection perturbs lipid homeostasis in infected mosquito cells. PLoS Pathog. 2012;8(3) https://doi.org/10.1371/journal.ppat.1002584.

  119. Petruzziello A, et al. Global epidemiology of hepatitis C virus infection: an up-date of the distribution and circulation of hepatitis C virus genotypes. World J Gastroenterol. 2016;22(34):7824–40. https://doi.org/10.3748/wjg.v22.i34.7824.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Poirier H, et al. Differential involvement of peroxisome-proliferator-activated receptors α and δ in fibrate and fatty-acid-mediated inductions of the gene encoding liver fatty-acid-binding protein in the liver and the small intestine. Biochem J. 2001;355(2):481–8. https://doi.org/10.1042/0264-6021:3550481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Porter BA, et al. Structure and function of the nuclear receptor superfamily and current targeted therapies of prostate cancer. Cancers. 2019;11(12) https://doi.org/10.3390/cancers11121852.

  122. Potena L, et al. Hydroxymethyl-glutaryl coenzyme a reductase inhibition limits cytomegalovirus infection in human endothelial cells. Circulation. 2004;109(4):532–6. https://doi.org/10.1161/01.CIR.0000109485.79183.81.

    Article  CAS  PubMed  Google Scholar 

  123. Potula R, et al. Peroxisome proliferator-activated receptor-γ activation suppresses HIV-1 replication in an animal model of encephalitis. AIDS. 2008;22(13):1539–49. https://doi.org/10.1097/QAD.0b013e3283081e08.

    Article  CAS  PubMed  Google Scholar 

  124. Raboud JM, et al. A meta-analysis of six placebo-controlled trials of thiazolidinedione therapy for HIV lipoatrophy. HIV Clin Trials. 2010;11(1):39–50. https://doi.org/10.1310/hct1101-39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Radreau P, et al. Reciprocal regulation of farnesoid X receptor α activity and hepatitis B virus replication in differentiated HepaRG cells and primary human hepatocytes. FASEB J. 2016;30(9):3146–54. https://doi.org/10.1096/fj.201500134.

    Article  CAS  PubMed  Google Scholar 

  126. Rakic B, et al. Peroxisome proliferator-activated receptor α antagonism inhibits hepatitis C virus replication. Chem Biol. 2006;13(1):23–30. https://doi.org/10.1016/j.chembiol.2005.10.006.

    Article  CAS  PubMed  Google Scholar 

  127. Ramezani A, et al. Stimulation of liver X receptor has potent anti-HIV effects in a humanized mouse model of HIV infection. J Pharmacol Exp Ther. 2015;354(3):376–83. https://doi.org/10.1124/jpet.115.224485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Ramiere C, et al. Transactivation of the hepatitis B virus core promoter by the nuclear receptor FXR. J Virol. 2008;82(21):10832–40. https://doi.org/10.1128/jvi.00883-08.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Ramirez SH, et al. Activation of peroxisome proliferator-activated receptor γ (PPARγ) suppresses rho GTPases in human brain microvascular endothelial cells and inhibits adhesion and transendothelial migration of HIV-1 infected monocytes. J Immunol. 2008;180(3):1854–65. https://doi.org/10.4049/jimmunol.180.3.1854.

    Article  CAS  PubMed  Google Scholar 

  130. Raney, A. K. et al. ‘Members of the nuclear receptor superfamily regulate transcription from the hepatitis B virus nucleocapsid promoter.’, Journal of virology. 1997;71(2):1058–1071. https://doi.org/10.1128/jvi.71.2.1058-1071.1997.

  131. Raney AK, et al. Transcription and replication of a natural hepatitis B virus nucleocapsid promoter variant is regulated in Vivo by peroxisome proliferators. Virology. 2001;289(2):239–51. https://doi.org/10.1006/viro.2001.1169.

    Article  CAS  PubMed  Google Scholar 

  132. Rauwel B, et al. 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. 2010;84(6):2946–54. https://doi.org/10.1128/jvi.01779-09.

    Article  CAS  PubMed  Google Scholar 

  133. Reese VC, Oropeza CE, McLachlan A. Independent activation of hepatitis B virus biosynthesis by retinoids, peroxisome proliferators, and bile acids. J Virol. 2013;87(2):991–7. https://doi.org/10.1128/jvi.01562-12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Repa JJ, et al. Regulation of mouse sterol regulatory by oxysterol receptors, LXR ␣ and LXR ␤. Genes Dev. 2000;14(22):2819–30. https://doi.org/10.1101/gad.844900.four.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Repa JJ, et al. Regulation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 by the liver X receptors α and β. J Biol Chem. 2002;277(21):18793–800. https://doi.org/10.1074/jbc.M109927200.

    Article  CAS  PubMed  Google Scholar 

  136. Repa JJ, Mangelsdorf DJ. The role of orphan nuclear receptors in the regulation of cholesterol homeostasis. Annu Rev Cell Dev Biol. 2000;16:459–81.

    Article  CAS  PubMed  Google Scholar 

  137. Ricote M, Glass CK. PPARs and molecular mechanisms of transrepression. Biochim Biophys Acta Mol Cell Biol Lipids. 2007;1771(8):926–35. https://doi.org/10.1016/j.bbalip.2007.02.013.

    Article  CAS  Google Scholar 

  138. del Rio C. The global HIV epidemic: what the pathologist needs to know. Semin Diagn Pathol. 2017;34(4):314–7. https://doi.org/10.1053/j.semdp.2017.05.001.

    Article  PubMed  PubMed Central  Google Scholar 

  139. Robbins GT, Nie D. PPAR gamma, bioactive lipids, and cancer progression. Frontiers in Bioscience. 2012:1816–34. https://doi.org/10.2741/4021.

  140. Rolland M, et al. PPARγ is activated during congenital cytomegalovirus infection and inhibits neuronogenesis from human neural stem cells. PLoS Pathog. 2016;12(4):1–30. https://doi.org/10.1371/journal.ppat.1005547.

    Article  CAS  Google Scholar 

  141. Rothwell C, et al. Cholesterol biosynthesis modulation regulates dengue viral replication. Virology. Elsevier Inc.,. 2009;389(1–2):8–19. https://doi.org/10.1016/j.virol.2009.03.025.

    Article  CAS  PubMed  Google Scholar 

  142. Sagan SM, et al. The influence of cholesterol and lipid metabolism on host cell structure and hepatitis C virus replication. Biochem Cell Biol. 2006;84(1):67–79. https://doi.org/10.1139/o05-149.

    Article  CAS  PubMed  Google Scholar 

  143. Schadinger SE, et al. PPARγ2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes. Am J Physiol Endocrinol Metabol. 2005;288(6 51-6):1195–205. https://doi.org/10.1152/ajpendo.00513.2004.

    Article  CAS  Google Scholar 

  144. Scholtes C, et al. Enhancement of genotype 1 hepatitis C virus replication by bile acids through FXR. J Hepatol. 2008;48(2):192–9. https://doi.org/10.1016/j.jhep.2007.09.015.

    Article  CAS  PubMed  Google Scholar 

  145. Serfaty L, et al. Hepatitis C virus induced hypobetalipoproteinemia: a possible mechanism for steatosis in chronic hepatitis C. J Hepatol. 2001;34(3):428–34. https://doi.org/10.1016/S0168-8278(00)00036-2.

    Article  CAS  PubMed  Google Scholar 

  146. Sever R, Glass CK. Signaling by nuclear receptors. Cold Spring Harb Perspect Biol. 2013;5(3):1–5. https://doi.org/10.1101/cshperspect.a016709.

    Article  CAS  Google Scholar 

  147. Sheng X, Xiang, et al. The LXR ligand GW3965 inhibits Newcastle disease virus infection by affecting cholesterol homeostasis. Arch Virol. Springer Vienna,. 2016;161(9):2491–501. https://doi.org/10.1007/s00705-016-2950-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Shi YX, Huang CJ, Yang ZG. Impact of hepatitis B virus infection on hepatic metabolic signaling pathway. World J Gastroenterol. 2016;22(36):8161–7. https://doi.org/10.3748/wjg.v22.i36.8161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Shimano H, et al. Isoform 1c of sterol regulatory element binding protein is less active than isoform 1a in livers of transgenic mice and in cultured cells. J Clin Investig. 1997;99(5):846–54. https://doi.org/10.1172/JCI119248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Sinal CJ, et al. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell. 2000;102(6):731–44. https://doi.org/10.1016/S0092-8674(00)00062-3.

    Article  CAS  PubMed  Google Scholar 

  151. Singaravelu R, et al. MicroRNAs regulate the immunometabolic response to viral infection in the liver. Nat Chem Biol. 2015;11(12):988–93. https://doi.org/10.1038/nchembio.1940.

    Article  CAS  PubMed  Google Scholar 

  152. Singaravelu R, et al. Soraphen a: a probe for investigating the role of de novo lipogenesis during viral infection. ACS Infect Dis. 2016;1(3):130–4. https://doi.org/10.1021/acsinfecdis.5b00019.

    Article  CAS  Google Scholar 

  153. Sirvent A, Verhoeven AJM, et al. Farnesoid X receptor represses hepatic lipase gene expression. J Lipid Res. 2004a;45(11):2110–5. https://doi.org/10.1194/jlr.M400221-JLR200.

    Article  CAS  PubMed  Google Scholar 

  154. Sirvent A, Claudel T, et al. The farnesoid X receptor induces very low density lipoprotein receptor gene expression. FEBS Lett. 2004b;566(1–3, 173):–177. https://doi.org/10.1016/j.febslet.2004.04.026.

  155. Skolnik PR, et al. Stimulation of peroxisome proliferator-activated receptors α and γ blocks HIV-1 replication and TNFα production in acutely infected primary blood cells, chronically infected U1 cells, and alveolar macrophages from HIV-infected subjects. J Acquir Immune Defic Syndr. 2002;31(1):1–10. https://doi.org/10.1097/00126334-200209010-00001.

    Article  CAS  PubMed  Google Scholar 

  156. Soto-Acosta R, et al. The increase in cholesterol levels at early stages after dengue virus infection correlates with an augment in LDL particle uptake and HMG-CoA reductase activity. Virology. Elsevier,. 2013;442(2):132–47. https://doi.org/10.1016/j.virol.2013.04.003.

    Article  CAS  PubMed  Google Scholar 

  157. Sparrow CP, et al. A potent synthetic LXR agonist is more effective than cholesterol loading at inducing ABCA1 mRNA and stimulating cholesterol efflux. J Biol Chem. 2002;277(12):10021–7. https://doi.org/10.1074/jbc.M108225200.

    Article  CAS  PubMed  Google Scholar 

  158. Sreenarasimhaiah J. Lack of optimal T-cell reactivity against the hepatitis C virus is associated with the development of fibrosis/cirrhosis during chronic hepatitis. Hum Immunol. 2002;8859(02) https://doi.org/10.1016/s1098-8859(02)00781-4.

  159. Stieger B. The role of the sodium-taurocholate cotransporting polypeptide (NTCP) and of the bile salt export pump (BSEP) in physiology and pathophysiology of bile formation. Handb Exp Pharmacol. 2011; https://doi.org/10.1007/978-3-642-14541-4_5.

  160. Su AI, et al. Genomic analysis of the host response to hepatitis C virus infection. Proc Natl Acad Sci U S A. 2002;99(24):15669–74. https://doi.org/10.1073/pnas.202608199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Sviridov D, et al. Comorbidities of HIV infection: role of Nef-induced impairment of cholesterol metabolism and lipid raft functionality. AIDS. 2020;34(1):1–13. https://doi.org/10.1097/QAD.0000000000002385.

    Article  CAS  PubMed  Google Scholar 

  162. Syed GH, Amako Y, Siddiqui A. Hepatitis C virus hijacks host lipid metabolism. Trends Endocrinol Metab. 2010;21(1):33–40. https://doi.org/10.1016/j.tem.2009.07.005.

    Article  CAS  PubMed  Google Scholar 

  163. Tanaka N, et al. PPARα activation is essential for HCV core protein–induced hepatic steatosis and hepatocellular carcinoma in mice. J Clin Invest. 2008;118(2):683–94. https://doi.org/10.1172/JCI33594.The.

    Article  PubMed  PubMed Central  Google Scholar 

  164. Tang C, Oram JF. The cell cholesterol exporter ABCA1 as a protector from cardiovascular disease and diabetes. Biochim Biophys Acta Mol Cell Biol Lipids. Elsevier B.V.,. 2009;1791(7):563–72. https://doi.org/10.1016/j.bbalip.2009.03.011.

    Article  CAS  Google Scholar 

  165. Tang H, et al. Human herpesvirus-6 infection induces the reorganization of membrane microdomains in target cells, which are required for virus entry. Virology. Elsevier Inc.,. 2008;378(2):265–71. https://doi.org/10.1016/j.virol.2008.05.028.

    Article  CAS  PubMed  Google Scholar 

  166. Tang H, McLachlan A. Transcriptional regulation of hepatitis B virus by nuclear hormone receptors is a critical determinant of viral tropism. Proc Natl Acad Sci U S A. 2001;98(4):1841–6. https://doi.org/10.1073/pnas.98.4.1841.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Tongluan N, et al. Involvement of fatty acid synthase in dengue virus infection. Virol J. 2017;14(1):1–18. https://doi.org/10.1186/s12985-017-0685-9.

    Article  CAS  Google Scholar 

  168. Torchia J, Glass C, Rosenfeld MG. Co-activators and co-repressors in the integration of transcriptional responses. Curr Opin Cell Biol. 1998;10(3):373–83. https://doi.org/10.1016/S0955-0674(98)80014-8.

    Article  CAS  PubMed  Google Scholar 

  169. Torra IP, et al. Bile acids induce the expression of the human peroxisome proliferator-activated receptor α gene via activation of the farnesoid X receptor. Mol Endocrinol. 2003;17(2):259–72. https://doi.org/10.1210/me.2002-0120.

    Article  CAS  Google Scholar 

  170. Trabattoni D, et al. Thiazolides elicit anti-viral innate immunity and reduce HIV replication. Sci Rep. Nature Publishing Group,. 2016;6(June):1–10. https://doi.org/10.1038/srep27148.

    Article  CAS  Google Scholar 

  171. Tu H, Okamoto AY, Shan B. FXR, a bile acid receptor and biological sensor. Trends Cardiovasc Med. 2000;10(1):30–5. https://doi.org/10.1016/S1050-1738(00)00043-8.

    Article  CAS  PubMed  Google Scholar 

  172. Vastag L, et al. Divergent effects of human cytomegalovirus and herpes simplex virus-1 on cellular metabolism. PLoS Pathog. 2011;7(7) https://doi.org/10.1371/journal.ppat.1002124.

  173. Vieira FS, et al. Host-cell lipid rafts: a safe door for micro-organisms? Biol Cell. 2010;102(7):391–407. https://doi.org/10.1042/bc20090138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Wakui Y, et al. Inhibitory effect on hepatitis B virus in vitro by a peroxisome proliferator-activated receptor-γ ligand, rosiglitazone. Biochem Biophys Res Commun. Elsevier Inc.,. 2010;396(2):508–14. https://doi.org/10.1016/j.bbrc.2010.04.128.

    Article  CAS  PubMed  Google Scholar 

  175. Wang L, et al. A comprehensive data mining study shows that most nuclear receptors act as newly proposed homeostasis-associated molecular pattern receptors. J Hematol Oncol. 2017;10(1):168. https://doi.org/10.1186/s13045-017-0526-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Wang YX. PPARs: diverse regulators in energy metabolism and metabolic diseases. Cell Res. 2010;20(2):124–37. https://doi.org/10.1038/cr.2010.13.

    Article  CAS  PubMed  Google Scholar 

  177. Watanabe M, et al. Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J Clin Investig. 2004;113(10):1408–18. https://doi.org/10.1172/JCI21025.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Welsch S, et al. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe. Elsevier Ltd,. 2009;5(4):365–75. https://doi.org/10.1016/j.chom.2009.03.007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. White MK, et al. Zika virus: an emergent neuropathological agent. Ann Neurol. 2016;80(4):479–89. https://doi.org/10.1002/ana.24748.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Winter PM, et al. Proinflammatory cytokines and chemokines in humans with Japanese encephalitis. J Infect Dis. 2004;190(9):1618–26. https://doi.org/10.1086/423328.

    Article  CAS  PubMed  Google Scholar 

  181. Wu ZY, et al. Farnesoid X receptor agonist GW4064 indirectly inhibits HCV entry into cells via down-regulating scavenger receptor class B type I. Eur J Pharmacol. 2019;853(March):111–20. https://doi.org/10.1016/j.ejphar.2019.03.033.

    Article  CAS  PubMed  Google Scholar 

  182. Xu J, et al. Epigallocatechin gallate inhibits hepatitis B virus via farnesoid X receptor alpha. J Nat Med. Springer Japan,. 2016;70(3):584–91. https://doi.org/10.1007/s11418-016-0980-6.

    Article  CAS  PubMed  Google Scholar 

  183. Yan H, et al. Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. eLife. 2012;2012(1):1–28. https://doi.org/10.7554/eLife.00049.

    Article  CAS  Google Scholar 

  184. Yan H, et al. Viral entry of hepatitis B and D viruses and bile salts transportation share common molecular determinants on sodium taurocholate cotransporting polypeptide. J Virol. 2014;88(6):3273–84. https://doi.org/10.1128/jvi.03478-13.

    Article  PubMed  PubMed Central  Google Scholar 

  185. Yang J-M. Effect of HCV infection on expression of several cancer-associated gene products in HCC. World J Gastroenterol. 1999;5(1):25. https://doi.org/10.3748/wjg.v5.i1.25.

    Article  PubMed  PubMed Central  Google Scholar 

  186. Yoon S, et al. Adiponectin, a downstream target gene of peroxisome proliferator-activated receptor γ, controls hepatitis B virus replication. Virology. Elsevier Inc.,. 2011;409(2):290–8. https://doi.org/10.1016/j.virol.2010.10.024.

    Article  CAS  PubMed  Google Scholar 

  187. Yoshikawa T, et al. Identification of liver X receptor-retinoid X receptor as an activator of the sterol regulatory element-binding protein 1c gene promoter. Mol Cell Biol. 2001;21(9):2991–3000. https://doi.org/10.1128/mcb.21.9.2991-3000.2001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Yu K, et al. Differential activation of peroxisome proliferator-activated receptors by eicosanoids. J Biol Chem. 1995;270(41):23975–83. https://doi.org/10.1074/jbc.270.41.23975.

    Article  CAS  PubMed  Google Scholar 

  189. Zelcer N, et al. LXR regulates cholesterol uptake through idol-dependent ubiquitination of the LDL receptor cellular. Life Sci. 2009;325(July):100–4. https://doi.org/10.1126/science.1168974.

    Article  CAS  Google Scholar 

  190. Zeng J, et al. Liver X receptors agonists impede hepatitis C virus infection in an Idol-dependent manner. Antivir Res. Elsevier B.V.,. 2012;95(3):245–56. https://doi.org/10.1016/j.antiviral.2012.06.004.

    Article  CAS  PubMed  Google Scholar 

  191. Zeng J, et al. Activation of the liver X receptor pathway inhibits HBV replication in primary human hepatocytes. Hepatology. 2020:0–2. https://doi.org/10.1002/hep.31217.

  192. Zhao C, Dahlman-Wright K. Liver X receptor in cholesterol metabolism. J Endocrinol. 2010;204(3):233–40. https://doi.org/10.1677/JOE-09-0271.

    Article  CAS  PubMed  Google Scholar 

  193. Zhao Q, et al. DNA methylation patterns of peroxisome proliferator-activated receptor gamma gene associated with liver fibrosis and inflammation in chronic hepatitis B. J Viral Hepat. 2013;20(6):430–7. https://doi.org/10.1111/jvh.12048.

    Article  CAS  PubMed  Google Scholar 

  194. Zhao Z-H, et al. Promoter methylation status and expression of PPAR-γ gene are associated with prognosis of acute-on-chronic hepatitis B liver failure. Clin Epigenetics. 2015;7(1):115. https://doi.org/10.1186/s13148-015-0149-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. Zheng YH, et al. Nef increases infectivity of HIV via lipid rafts. Curr Biol. 2001;11(11):875–9. https://doi.org/10.1016/S0960-9822(01)00237-8.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

N.A. and N.A. are supported by a NSERC Postgraduate Scholarship-Doctoral (PGS-D). R.F. is supported by NSERC Canada Graduate Scholarship- Doctoral (CGS-D). This work is supported by funding from a Natural Sciences and Engineering Research Council (NSERC) grant (298496) and a Canadian Institutes of Health Research (CIHR) grant (136807). Figures in this chapter are created using Biorender.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John Paul Pezacki .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ahmed, N., Ahmed, N., Filip, R., Pezacki, J.P. (2021). Nuclear Hormone Receptors and Host-Virus Interactions. In: Badr, M.Z. (eds) Nuclear Receptors. Springer, Cham. https://doi.org/10.1007/978-3-030-78315-0_13

Download citation

Publish with us

Policies and ethics