Regulation of the Trafficking and Antiviral Activity of IFITM3 by Post-Translational Modifications

References

• Siegrist F , EbelingM , CertaU . The small interferon-induced transmembrane genes and proteins . J. Interferon Cytokine Res.31 ( 1 ), 183 – 197 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Sallman Almen M , BringelandN , FredrikssonR , SchiothHB . The dispanins: a novel gene family of ancient origin that contains 14 human members . PLoS ONE7 ( 2 ), e31961 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Brass AL , HuangIC , BenitaYet al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus . Cell139 ( 7 ), 1243 – 1254 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Yount JS , MoltedoB , YangYYet al. Palmitoylome profiling reveals S-palmitoylation-dependent antiviral activity of IFITM3 . Nat. Chem. Biol.6 ( 8 ), 610 – 614 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Weidner JM , JiangD , PanXB , ChangJ , BlockTM , GuoJT . Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms . J. Virol.84 ( 24 ), 12646 – 12657 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Huang IC , BaileyCC , WeyerJLet al. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus . PLoS Pathog.7 ( 1 ), e1001258 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Schoggins JW , WilsonSJ , PanisMet al. A diverse range of gene products are effectors of the type I interferon antiviral response . Nature472 ( 7344 ), 481 – 485 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Schoggins JW , MacDuffDA , ImanakaNet al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity . Nature505 ( 7485 ), 691 – 695 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Anafu AA , BowenCH , ChinCR , BrassAL , HolmGH . Interferon-inducible transmembrane protein 3 (IFITM3) restricts reovirus cell entry . J. Biol. Chem.288 ( 24 ), 17261 – 17271 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Lu J , PanQ , RongL , HeW , LiuSL , LiangC . The IFITM proteins inhibit HIV-1 infection . J. Virol.85 ( 5 ), 2126 – 2137 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Raychoudhuri A , ShrivastavaS , SteeleR , KimH , RayR , RayRB . ISG56 and IFITM1 proteins inhibit hepatitis C virus replication . J. Virol.85 ( 24 ), 12881 – 12889 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Wilkins C , WoodwardJ , LauDTYet al. IFITM1 is a tight junction protein that inhibits hepatitis virus entry . Hepatology57 ( 2 ), 461 – 469 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Mudhasani R , TranJP , RettererCet al. IFITM-2 and IFITM-3 but not IFITM-1 restrict Rift Valley fever virus . J. Virol.87 ( 15 ), 8451 – 8464 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Smith RA , YoungJ , WeisJJ , WeisJH . Expression of the mouse fragilis gene products in immune cells and association with receptor signaling complexes . Genes Immun.7 ( 2 ), 113 – 121 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Smith SE , GibsonMS , WashRSet al. Chicken interferon-inducible transmembrane protein 3 restricts influenza viruses and lyssaviruses in vitro . J. Virol.87 ( 23 ), 12957 – 12966 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Zhu R , WangJ , LeiXY , GuiJF , ZhangQY . Evidence for Paralichthys olivaceus IFITM1 antiviral effect by impeding viral entry into target cells . Fish Shellfish Immunol.35 ( 3 ), 918 – 926 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Zhang Z , LiuJ , LiM , YangH , ZhangCY . Evolutionary dynamics of the interferon-induced transmembrane gene family in vertebrates . PLoS ONE7 ( 11 ) ( 2012 ).
   Web of Science ®Google Scholar
• Yount JS , KarssemeijerRA , HangHC . S-palmitoylation and ubiquitination differentially regulate interferon-induced transmembrane protein 3 (IFITM3)-mediated resistance to influenza virus . J. Biol. Chem.287 , 19631 – 19641 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Shan Z , HanQ , NieJet al. Negative regulation of interferon-induced transmembrane protein 3 by SET7-mediated lysine monomethylation . J. Biol. Chem.288 ( 49 ), 35093 – 35103 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Jia R , PanQ , DingSet al. The N-terminal region of IFITM3 modulates its antiviral activity by regulating IFITM3 cellular localization . J. Virol.86 ( 24 ), 13697 – 13707 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Chesarino NM , McMichaelTM , HachJC , YountJS . Phosphorylation of the antiviral protein IFITM3 dually regulates its endocytosis and ubiquitination . J. Biol. Chem.289 ( 17 ), 11986 – 11992 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Hickford D , FrankenbergS , ShawG , RenfreeMB . Evolution of vertebrate interferon inducible transmembrane proteins . BMC Genom.13 , 155 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Diamond MS , FarzanM . The broad-spectrum antiviral functions of IFIT and IFITM proteins . Nat. Rev. Immunol.13 ( 1 ), 46 – 57 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Moffatt P , GaumondMH , SaloisPet al. Bril: a novel bone–specific modulator of mineralization . J. Bone Miner Res.23 ( 9 ), 1497 – 1508 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Semler O , GarbesL , KeuppKet al. A mutation in the 5′-UTR of IFITM5 creates an in-frame start codon and causes autosomal-dominant osteogenesis imperfecta type with hyperplastic callus . Am. J. Hum. Genet.91 ( 2 ), 349 – 357 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Hanagata N , LiXL , MoritaH , TakemuraT , LiJ , MinowaT . Characterization of the osteoblast-specific transmembrane protein IFITM5 and analysis of IFITM5-deficient mice . J. Bone Miner. Metab.29 ( 3 ), 279 – 290 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Everitt AR , ClareS , PertelTet al. IFITM3 restricts the morbidity and mortality associated with influenza . Nature484 ( 7395 ), 519 – 523 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Bailey CC , HuangIC , KamC , FarzanM . Ifitm3 limits the severity of acute influenza in mice . PLoS Pathog.8 ( 9 ), e1002909 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Wang Z , ZhangA , WanYet al. Early hypercytokinemia is associated with interferon-induced transmembrane protein-3 dysfunction and predictive of fatal H7N9 infection . Proc. Natl Acad. Sci. USA111 ( 2 ), 769 – 774 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Zhang YH , ZhaoY , LiNet al. Interferon-induced transmembrane protein-3 genetic variant rs12252-C is associated with severe influenza in Chinese individuals . Nat. Commun.4 , 1418 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Feeley EM , SimsJS , JohnSPet al. IFITM3 inhibits influenza A virus infection by preventing cytosolic entry . PLoS Pathog.7 ( 10 ), e1002337 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Li K , MarkosyanRM , ZhengYMet al. IFITM proteins restrict viral membrane hemifusion . PLoS Pathog.9 ( 1 ), e1003124 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Desai TM , MarinM , ChinCR , SavidisG , BrassAL , MelikyanGB . IFITM3 restricts influenza A virus entry by blocking the formation of fusion pores following ViruS-endosome hemifusion . PLoS Pathog.10 ( 4 ), e1004048 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Perreira JM , ChinCR , FeeleyEM , BrassAL . IFITMs restrict the replication of multiple pathogenic viruses . J. Mol. Biol.425 ( 24 ), 4937 – 4955 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Smith S , WestonS , KellamP , MarshM . IFITM proteinS-cellular inhibitors of viral entry . Curr. Opin. Virol.4C , 71 – 77 ( 2014 ).
   Google Scholar
• Hach JC , McMichaelT , ChesarinoNM , YountJS . Palmitoylation on conserved and non-conserved cysteines of murine IFITM1 regulates its stability and anti-influenza A virus activity . J. Virol.87 ( 17 ), 9923 – 9927 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• John SP , ChinCR , PerreiraJMet al. The CD225 domain of IFITM3 is required for both IFITM protein association and inhibition of influenza A virus and dengue virus replication . J. Virol.87 ( 14 ), 7837 – 7852 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Wee YS , RoundyKM , WeisJJ , WeisJH . Interferon-inducible transmembrane proteins of the innate immune response act as membrane organizers by influencing clathrin and v-ATPase localization and function . Innate Immunol.18 ( 6 ), 834 – 845 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Amini-Bavil-Olyaee S , ChoiYJ , LeeJHet al. The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry . Cell Host Microbe.13 ( 4 ), 452 – 464 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Lin TY , ChinCR , EverittARet al. Amphotericin B increases influenza A virus infection by preventing IFITM3-mediated restriction . Cell Rep.5 ( 4 ), 895 – 908 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Kohn A . Early interactions of viruses with cellular membranes . Adv. Virus Res.24 , 223 – 276 ( 1979 ).
   PubMedGoogle Scholar
• Schoggins JW , RandallG . Lipids in innate antiviral defense . Cell Host Microbe.14 ( 4 ), 379 – 385 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Liu SY , SanchezDJ , ChengG . New developments in the induction and antiviral effectors of type I interferon . Curr. Opin. Immunol.23 ( 1 ), 57 – 64 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Tom CT , MartinBR . Fat chance! Getting a grip on a slippery modification . ACS Chem. Biol.8 ( 1 ), 46 – 57 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Linder ME , DeschenesRJ . Palmitoylation: policing protein stability and traffic . Nat. Rev. Mol. Cell Biol.8 ( 1 ), 74 – 84 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Resh MD . Palmitoylation of ligands, receptors, and intracellular signaling molecules . Sci. STKE2006 ( 359 ), re14 ( 2006 ).
   PubMedGoogle Scholar
• Blaskovic S , BlancM , van der GootFG . What does S-palmitoylation do to membrane proteins?FEBS J.280 ( 12 ), 2766 – 2774 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Yount JS , ZhangMM , HangHC . Emerging roles for protein S-palmitoylation in immunity from chemical proteomics . Curr. Opin. Chem. Biol.17 ( 1 ), 27 – 33 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Lewin AR , ReidLE , McMahonM , StarkGR , KerrIM . Molecular analysis of a human interferon-inducible gene family . Eur. J. Biochem.199 ( 2 ), 417 – 423 ( 1991 ).
   PubMedGoogle Scholar
• Friedman RL , ManlySP , McMahonM , KerrIM , StarkGR . Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells . Cell38 ( 3 ), 745 – 755 ( 1984 ).
   PubMed Web of Science ®Google Scholar
• Yount JS , CharronG , HangHC . Bioorthogonal proteomics of 15-hexadecynyloxyacetic acid chemical reporter reveals preferential targeting of fatty acid modified proteins and biosynthetic enzymes . Bioorg. Med. Chem.20 ( 2 ), 650 – 654 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Jiang D , WeidnerJM , QingMet al. Identification of five interferon-induced cellular proteins that inhibit west nile virus and dengue virus infections . J. Virol.84 ( 16 ), 8332 – 8341 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Tsukamoto T , LiX , MoritaHet al. Role of S-palmitoylation on IFITM5 for the interaction with FKBP11 in osteoblast cells . PLoS ONE8 ( 9 ), e75831 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Wagner SA , BeliP , WeinertBTet al. A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles . Mol. Cell. Proteomics10 ( 10 ), M111 013284 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Wagner SA , BeliP , WeinertBTet al. Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues . Mol. Cell. Proteomics11 ( 12 ), 1578 – 1585 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Kim W , BennettEJ , HuttlinELet al. Systematic and quantitative assessment of the ubiquitin-modified proteome . Mol. Cell44 ( 2 ), 325 – 340 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Chen T , ZhouT , HeBet al. mUbiSiDa: a comprehensive database for protein ubiquitination sites in mammals . PLoS ONE9 ( 1 ), e85744 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Kulathu Y , KomanderD . Atypical ubiquitylation – the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages . Nat. Rev. Mol. Cell Biol.13 ( 8 ), 508 – 523 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Wang H , CaoR , XiaLet al. Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase . Mol. Cell8 ( 6 ), 1207 – 1217 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Kurash JK , LeiH , ShenQet al. Methylation of p53 by Set7/9 mediates p53 acetylation and activity in vivo . Mol. Cell29 ( 3 ), 392 – 400 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Munro S , KhaireN , IncheA , CarrS , La ThangueNB . Lysine methylation regulates the pRb tumour suppressor protein . Oncogene29 ( 16 ), 2357 – 2367 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Pagans S , SakaneN , SchnolzerM , OttM . Characterization of HIV Tat modifications using novel methyl-lysine-specific antibodies . Methods53 ( 1 ), 91 – 96 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Esteve PO , ChangY , SamaranayakeMet al. A methylation and phosphorylation switch between an adjacent lysine and serine determines human DNMT1 stability . Nat. Struct. Mol. Biol.18 ( 1 ), 42 – 48 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Liu X , WangD , ZhaoYet al. Methyltransferase Set7/9 regulates p53 activity by interacting with Sirtuin 1 (SIRT1) . Proc. Natl Acad. Sci. USA108 ( 5 ), 1925 – 1930 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Jia R , XuF , QianJet al. Identification of an endocytic signal essential for the antiviral action of IFITM3 . Cell. Microbiol.16 ( 7 ), 1080 – 1093 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Hunter T . The age of crosstalk: phosphorylation, ubiquitination, and beyond . Mol. Cell28 ( 5 ), 730 – 738 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Alland L , PeseckisSM , AthertonRE , BerthiaumeL , ReshMD . Dual myristylation and palmitylation of Src family member p59fyn affects subcellular localization . J. Biol. Chem.269 ( 24 ), 16701 – 16705 ( 1994 ).
   PubMed Web of Science ®Google Scholar
• van’t Hof W , ReshMD . Rapid plasma membrane anchoring of newly synthesized p59fyn: selective requirement for NH2–terminal myristoylation and palmitoylation at cysteine-3 . J. Cell Biol.136 ( 5 ), 1023 – 1035 ( 1997 ).
   PubMed Web of Science ®Google Scholar
• Lancki DW , QianD , FieldsP , GajewskiT , FitchFW . Differential requirement for protein tyrosine kinase Fyn in the functional activation of antigen–specific T lymphocyte clones through the TCR or Thy-1 . J. Immunol.154 ( 9 ), 4363 – 4370 ( 1995 ).
   PubMed Web of Science ®Google Scholar
• Tang X , FengY , YeK . SrC-family tyrosine kinase fyn phosphorylates phosphatidylinositol 3-kinase enhancer-activating Akt, preventing its apoptotic cleavage and promoting cell survival . Cell Death Differ.14 ( 2 ), 368 – 377 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Peters DJ , McGrewBR , PerronDC , LiptakLM , LaudanoAP . In vivo phosphorylation and membrane association of the fyn proto-oncogene product in IM–9 human lymphoblasts . Oncogene5 ( 9 ), 1313 – 1319 ( 1990 ).
   PubMed Web of Science ®Google Scholar
• Mustelin T , Pessa–MorikawaT , AuteroMet al. Regulation of the p59fyn protein tyrosine kinase by the CD45 phosphotyrosine phosphatase . Eur. J. Immunol.22 ( 5 ), 1173 – 1178 ( 1992 ).
   PubMed Web of Science ®Google Scholar
• Bailey CC , KondurHR , HuangIC , FarzanM . Interferon-induced transmembrane protein 3 is a type II transmembrane protein . J. Biol. Chem.288 ( 45 ), 32184 – 32193 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Uittenbogaard A , YingY , SmartEJ . Characterization of a cytosolic heat–shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking . J. Biol. Chem.273 ( 11 ), 6525 – 6532 ( 1998 ).
   PubMed Web of Science ®Google Scholar
• Kalashnikova E , LorcaRA , KaurIet al. SynDIG1: an activity-regulated, AMPA- receptor-interacting transmembrane protein that regulates excitatory synapse development . Neuron65 ( 1 ), 80 – 93 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Patoine A , GaumondMH , JaiswalPK , FassierF , RauchF , MoffattP . Topological mapping of BRIL reveals a type II orientation and effects of osteogenesis imperfecta mutations on its cellular destination . J. Bone Miner. Res. doi: 10.1002/jbmr.2243 ( 2014 ) ( Epub ahead of print ).
   PubMed Web of Science ®Google Scholar
• Voeltz GK , PrinzWA . Sheets, ribbons and tubules – how organelles get their shape . Nat. Rev. Mol. Cell Biol.8 ( 3 ), 258 – 264 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Chutiwitoonchai N , HiyoshiM , Hiyoshi-YoshidomiY , HashimotoM , TokunagaK , SuzuS . Characteristics of IFITM, the newly identified IFN-inducible anti-HIV-1 family proteins . Microbes Infect.15 ( 4 ), 280 – 290 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Everitt AR , ClareS , McDonaldJUet al. Defining the range of pathogens susceptible to ifitm3 restriction using a knockout mouse model . PLoS ONE8 ( 11 ), e80723 ( 2013 ).
   PubMed Web of Science ®Google Scholar