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Original Articles

Down-regulation of cell membrane localized NTCP expression in proliferating hepatocytes prevents hepatitis B virus infection

, , , , , , , , , , , , , & ORCID Icon show all
Pages 879-894 | Received 06 Feb 2019, Accepted 26 Apr 2019, Published online: 09 Jun 2019

References

  • Lozano R, Naghavi M, Foreman K, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the global burden of disease study 2010. Lancet. 2012 Dec 15;380(9859):2095–2128. doi:10.1016/S0140-6736(12)61728-0. PubMed PMID: 23245604.
  • Collaborators GBDCoD. Global, regional, and national age-sex specific mortality for 264 causes of death, 1980–2016: a systematic analysis for the global burden of disease study 2016. Lancet. 2017 Sep 16;390(10100):1151–1210. doi:10.1016/S0140-6736(17)32152-9. PubMed PMID: 28919116; PubMed Central PMCID: PMCPMC5605883.
  • Trepo C, Chan HL, Lok A. Hepatitis B virus infection. Lancet. 2014 Dec 6;384(9959):2053–2063. doi:10.1016/S0140-6736(14)60220-8. PubMed PMID: 24954675.
  • Mason WS, Litwin S, Xu C, et al. Hepatocyte turnover in transient and chronic hepadnavirus infections. J Viral Hepat. 2007 Nov;14(Suppl 1):22–28. doi:10.1111/j.1365-2893.2007.00911.x. PubMed PMID: 17958639.
  • Summers J, Jilbert AR, Yang W, et al. Hepatocyte turnover during resolution of a transient hepadnaviral infection. Proc Natl Acad Sci USA. 2003 Sep 30;100(20):11652–9. doi:10.1073/pnas.1635109100. PubMed PMID: 14500915; PubMed Central PMCID: PMC208813.
  • Nakai K, Tanaka H, Hanada K, et al. Decreased expression of cytochromes P450 1A2, 2E1, and 3A4 and drug transporters Na+-taurocholate-cotransporting polypeptide, organic cation transporter 1, and organic anion-transporting peptide-C correlates with the progression of liver fibrosis in chronic hepatitis C patients. Drug Metab Dispos. 2008 Sep;36(9):1786–1793. doi:10.1124/dmd.107.020073. PubMed PMID: 18515332.
  • Zollner G, Fickert P, Zenz R, et al. Hepatobiliary transporter expression in percutaneous liver biopsies of patients with cholestatic liver diseases. Hepatology. 2001 Mar;33(3):633–646. doi:10.1053/jhep.2001.22646. PubMed PMID: 11230744.
  • Allweiss L, Dandri M. The role of cccDNA in HBV Maintenance. Viruses. 2017 Jun 21;9(6). doi:10.3390/v9060156. PubMed PMID: 28635668; PubMed Central PMCID: PMC5490831.
  • Mason WS, Liu C, Aldrich CE, et al. Clonal expansion of normal-appearing human hepatocytes during chronic hepatitis B virus infection. J Virol. 2010 Aug;84(16):8308–8315. doi:10.1128/JVI.00833-10. PubMed PMID: 20519397; PubMed Central PMCID: PMC2916518.
  • Allweiss L, Volz T, Giersch K, et al. Proliferation of primary human hepatocytes and prevention of hepatitis B virus reinfection efficiently deplete nuclear cccDNA in vivo. Gut. 2018 Mar;67(3):542–552. doi:10.1136/gutjnl-2016-312162. PubMed PMID: 28428345.
  • Dienes HP, Purcell RH, Popper H, et al. The significance of infections with two types of viral hepatitis demonstrated by histologic features in chimpanzees. J Hepatol. 1990 Jan;10(1):77–84. PubMed PMID: 2106549. doi: 10.1016/0168-8278(90)90076-4
  • Keeffe EB. Is hepatitis A more severe in patients with chronic hepatitis B and other chronic liver diseases? Am J Gastroenterol. 1995 Feb;90(2):201–205. PubMed PMID: 7847285.
  • Tassopoulos N, Papaevangelou G, Roumeliotou-Karayannis A, et al. Double infections with hepatitis A and B viruses. Liver. 1985 Dec;5(6):348–353. PubMed PMID: 4088008. doi: 10.1111/j.1600-0676.1985.tb00258.x
  • Guo JT, Zhou H, Liu C, et al. Apoptosis and regeneration of hepatocytes during recovery from transient hepadnavirus infections. J Virol. 2000 Feb;74(3):1495–1505. PubMed PMID: 10627561; PubMed Central PMCID: PMCPMC111485. doi: 10.1128/JVI.74.3.1495-1505.2000
  • Alrefai WA, Gill RK. Bile acid transporters: structure, function, regulation and pathophysiological implications. Pharm Res. 2007 Oct;24(10):1803–1823. doi:10.1007/s11095-007-9289-1. PubMed PMID: 17404808.
  • Bouezzedine F, Fardel O, Gripon P. Interleukin 6 inhibits HBV entry through NTCP down regulation. Virology. 2015 Jul;481:34–42. doi:10.1016/j.virol.2015.02.026 . PubMed PMID: 25765005.
  • Song M, Sun Y, Tian J, et al. Silencing retinoid X receptor alpha expression enhances early-stage hepatitis B virus infection in cell cultures. J Virol. 2018 Apr 15;92(8). doi:10.1128/JVI.01771-17. PubMed PMID: 29437960; PubMed Central PMCID: PMCPMC5874418.
  • Donkers JM, Zehnder B, van Westen GJP, et al. Reduced hepatitis B and D viral entry using clinically applied drugs as novel inhibitors of the bile acid transporter NTCP. Sci Rep. 2017 Nov 10;7(1):15307. doi:10.1038/s41598-017-15338-0. PubMed PMID: 29127322; PubMed Central PMCID: PMCPMC5681660.
  • Miura T, Kimura N, Yamada T, et al. Sustained repression and translocation of Ntcp and expression of Mrp4 for cholestasis after rat 90% partial hepatectomy. J Hepatol. 2011 Aug;55(2):407–414. doi:10.1016/j.jhep.2010.11.023. PubMed PMID: 21167233.
  • Kang J, Wang J, Cheng J, et al. Down-regulation of NTCP expression by cyclin D1 in hepatitis B virus-related hepatocellular carcinoma has clinical significance. Oncotarget. 2017 Aug 22;8(34):56041–56050. doi:10.18632/oncotarget.10241. PubMed PMID: 28915572; PubMed Central PMCID: PMCPMC5593543.
  • He W, Cao Z, Mao F, et al. Modification of three amino acids in sodium taurocholate cotransporting polypeptide renders mice susceptible to infection with hepatitis D virus In vivo. J Virol. 2016 Oct 1;90(19):8866–8874. doi:10.1128/JVI.00901-16. PubMed PMID: 27466423; PubMed Central PMCID: PMC5021397.
  • Wang J, Ding S, Duan Z, et al. Role of p14ARF-HDM2-p53 axis in SOX6-mediated tumor suppression. Oncogene. 2016 Mar 31;35(13):1692–1702. doi:10.1038/onc.2015.234. PubMed PMID: 26119940; PubMed Central PMCID: PMC4820682.
  • Appelman MD, Chakraborty A, Protzer U, et al. N-Glycosylation of the Na+-taurocholate cotransporting polypeptide (NTCP) determines Its trafficking and stability and is required for hepatitis B virus infection. PLoS One. 2017;12(1):e0170419. doi:10.1371/journal.pone.0170419. PubMed PMID: 28125599; PubMed Central PMCID: PMC5268470.
  • Roncalli M, Sciarra A, Tommaso LD. Benign hepatocellular nodules of healthy liver: focal nodular hyperplasia and hepatocellular adenoma. Clin Mol Hepatol. 2016 Jun;22(2):199–211. doi:10.3350/cmh.2016.0101. PubMed PMID: 27189732; PubMed Central PMCID: PMC4946404.
  • Zhang F, Yao S, Zhang M, et al. Roles of circulating soluble interleukin (IL)-6 receptor and IL-6 receptor expression on CD4+ T cells in patients with chronic hepatitis B. Int J Infect Dis. 2011 Apr;15(4):e267–e271. doi:10.1016/j.ijid.2010.12.008. PubMed PMID: 21295508.
  • Kao JT, Lai HC, Tsai SM, et al. Rather than interleukin-27, interleukin-6 expresses positive correlation with liver severity in naive hepatitis B infection patients. Liver Int. 2012 Jul;32(6):928–936. doi:10.1111/j.1478-3231.2011.02742.x. PubMed PMID: 22230324.
  • Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature. 2001 May 17;411(6835):342–348. doi:10.1038/35077213. PubMed PMID: 11357141.
  • Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, et al. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem. 2004;73:39–85. doi:10.1146/annurev.biochem.73.011303.073723. PubMed PMID: 15189136.
  • Huibregtse JM, Scheffner M, Howley PM. Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins. Mol Cell Biol. 1993 Aug;13(8):4918–4927. PubMed PMID: 8393140; PubMed Central PMCID: PMC360130. doi: 10.1128/MCB.13.8.4918
  • Foster JS, Fernando RI, Ishida N, et al. Estrogens down-regulate p27Kip1 in breast cancer cells through Skp2 and through nuclear export mediated by the ERK pathway. J Biol Chem. 2003 Oct 17;278(42):41355–41366. doi:10.1074/jbc.M302830200. PubMed PMID: 12904306.
  • Ciznadija D, Zhu XH, Koff A. Hdm2- and proteasome-dependent turnover limits p21 accumulation during S phase. Cell Cycle. 2011 Aug 15;10(16):2714–2723. doi:10.4161/cc.10.16.16725. PubMed PMID: 21768776; PubMed Central PMCID: PMC3219540.
  • Hu R, Aplin AE. Skp2 regulates G2/M progression in a p53-dependent manner. Mol Biol Cell. 2008 Nov;19(11):4602–4610. doi:10.1091/mbc.E07-11-1137. PubMed PMID: 18716061; PubMed Central PMCID: PMC2575176.
  • Lu F, Gladden AB, Diehl JA. An alternatively spliced cyclin D1 isoform, cyclin D1b, is a nuclear oncogene. Cancer Res. 2003 Nov 1;63(21):7056–7061. PubMed PMID: 14612495.
  • Cattori V, Eckhardt U, Hagenbuch B. Molecular cloning and functional characterization of two alternatively spliced Ntcp isoforms from mouse liver1. Biochim Biophys Acta. 1999 Apr 14;1445(1):154–159. PubMed PMID: 10209268. doi: 10.1016/S0167-4781(99)00029-9
  • Hagenbuch B, Meier PJ. Molecular cloning, chromosomal localization, and functional characterization of a human liver Na+/bile acid cotransporter. J Clin Invest. 1994 Mar;93(3):1326–1331. doi:10.1172/JCI117091. PubMed PMID: 8132774; PubMed Central PMCID: PMC294097.
  • Yan H, Zhong G, Xu G, et al. Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. eLife. 2012 Nov 13;1:e00049. doi:10.7554/eLife.00049. PubMed PMID: 23150796; PubMed Central PMCID: PMC3485615.
  • Konig A, Doring B, Mohr C, et al. Kinetics of the bile acid transporter and hepatitis B virus receptor Na+/taurocholate cotransporting polypeptide (NTCP) in hepatocytes. J Hepatol. 2014 Oct;61(4):867–875. doi:10.1016/j.jhep.2014.05.018. PubMed PMID: 24845614.
  • Stross C, Kluge S, Weissenberger K, et al. A dileucine motif is involved in plasma membrane expression and endocytosis of rat sodium taurocholate cotransporting polypeptide (Ntcp). Am J Physiol Gastrointestinal Liver Physiol. 2013 Nov 15;305(10):G722–G730. doi:10.1152/ajpgi.00056.2013. PubMed PMID: 24008362.
  • Kuhlkamp T, Keitel V, Helmer A, et al. Degradation of the sodium taurocholate cotransporting polypeptide (NTCP) by the ubiquitin-proteasome system. Biol Chem. 2005 Oct;386(10):1065–1074. doi:10.1515/BC.2005.122 . PubMed PMID: 16218878.
  • Anwer MS, Stieger B. Sodium-dependent bile salt transporters of the SLC10A transporter family: more than solute transporters. Pflugers Archiv: Eur J Physiolo. 2014 Jan;466(1):77–89. doi:10.1007/s00424-013-1367-0 . PubMed PMID: 24196564; PubMed Central PMCID: PMC3877701.
  • Anwer MS. Role of protein kinase C isoforms in bile formation and cholestasis. Hepatology. 2014 Sep;60(3):1090–1097. doi:10.1002/hep.27088. PubMed PMID: 24700589; PubMed Central PMCID: PMC4141907.
  • Thimme R, Wieland S, Steiger C, et al. CD8(+) t cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J Virol. 2003 Jan;77(1):68–76. PubMed PMID: 12477811; PubMed Central PMCID: PMC140637. doi: 10.1128/JVI.77.1.68-76.2003
  • Xia Y, Protzer U. Control of hepatitis B virus by cytokines. Viruses. 2017 Jan 20;9(1). doi:10.3390/v9010018. PubMed PMID: 28117695; PubMed Central PMCID: PMC5294987.
  • Kim DH, Kang HS, Kim KH. Roles of hepatocyte nuclear factors in hepatitis B virus infection. World J Gastroenterol. 2016 Aug 21;22(31):7017–7029. doi:10.3748/wjg.v22.i31.7017. PubMed PMID: 27610013; PubMed Central PMCID: PMCPMC4988315.
  • Duncan AW, Dorrell C, Grompe M. Stem cells and liver regeneration. Gastroenterology. 2009 Aug;137(2):466–481. doi:10.1053/j.gastro.2009.05.044. PubMed PMID: 19470389; PubMed Central PMCID: PMC3136245.
  • Ori A, Zauberman A, Doitsh G, et al. P53 binds and represses the HBV enhancer: an adjacent enhancer element can reverse the transcription effect of p53. EMBO J. 1998 Jan 15;17(2):544–553. doi:10.1093/emboj/17.2.544. PubMed PMID: 9430645; PubMed Central PMCID: PMC1170404.