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Review

Toward the identification of ZDHHC enzymes required for palmitoylation of viral protein as potential drug targets

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Pages 159-177 | Received 23 Jul 2019, Accepted 19 Nov 2019, Published online: 06 Dec 2019

References

  • Schmidt MF. The transfer of myristic and other fatty acids on lipid and viral protein acceptors in cultured cells infected with Semliki Forest and influenza virus. Embo J. 1984 Oct;3(10):2295–2300. PubMed PMID: 6094180; eng.
  • Towler D, Glaser L. Acylation of cellular proteins with endogenously synthesized fatty acids. Biochemistry. 1986 Feb 25;25(4):878–884. PubMed PMID: 3964651.
  • Veit M, Herrler G, Schmidt MF, et al. The hemagglutinating glycoproteins of influenza B and C viruses are acylated with different fatty acids. Virology. 1990 Aug;177(2):807–811. PubMed PMID: 2371783; eng.
  • Hemsley PA. An outlook on protein S-acylation in plants: what are the next steps? J Exp Bot. 2017 Jun 1;68(12):3155–3164. PubMed PMID: 28158736; eng.
  • Blanc M, Blaskovic S, van der Goot FG. Palmitoylation, pathogens and their host. Biochem Soc Trans. 2013 Feb 1;41(1):84–88. PubMed PMID: 23356263; eng.
  • Brown RW, Sharma AI, Engman DM. Dynamic protein S-palmitoylation mediates parasite life cycle progression and diverse mechanisms of virulence. Crit Rev Biochem Mol Biol. 2017 Apr;52(2):145–162. PubMed PMID: 28228066; eng
  • Corvi MM, Turowski VR. Palmitoylation in apicomplexan parasites: from established regulatory roles to putative new functions. Mol Biochem Parasitol. 2019 Jun;230:16–23. PubMed PMID: 30978365; eng.
  • Ivanov SS, Roy C. Host lipidation: a mechanism for spatial regulation of Legionella effectors. Curr Top Microbiol Immunol. 2013;376:135–154. . PubMed PMID: 23918175; eng.
  • Resh MD. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta. 1999 Aug 12;1451(1):1–16. PubMed PMID: 10446384; eng.
  • Resh MD. Trafficking and signaling by fatty-acylated and prenylated proteins. Nat Chem Biol. 2006 Nov;2(11):584–590. PubMed PMID: 17051234; eng
  • Daniotti JL, Pedro MP, Valdez Taubas J. The role of S-acylation in protein trafficking. Traffic. 2017 Nov;18(11):699–710. PubMed PMID: 28837239; eng
  • Ernst AM, Toomre D, Bogan JS. Acylation - a new means to control traffic through the Golgi. Front Cell Dev Biol. 2019;7:109. . PubMed PMID: 31245373; eng.
  • Zaballa ME, van der Goot FG. The molecular era of protein S-acylation: spotlight on structure, mechanisms, and dynamics. Crit Rev Biochem Mol Biol. 2018 Aug;53(4):420–451. PubMed PMID: 29999430; eng
  • Fukata Y, Bredt DS, Fukata M. Protein palmitoylation by DHHC protein family, Chapter 5. In: Kittler JT, Moss SJ, editors. The dynamic synapse: molecular methods in ionotropic receptor biology. Boca Raton (FL): Frontiers in Neuroscience; 2006.
  • Mitchell DA, Vasudevan A, Linder ME, et al. Protein palmitoylation by a family of DHHC protein S-acyltransferases. J Lipid Res. 2006 Jun;47(6):1118–1127. PubMed PMID: 16582420.
  • Won SJ, Cheung See Kit M, Martin BR. Protein depalmitoylases. Crit Rev Biochem Mol Biol. 2017 Feb;53(1):83–98. PubMed PMID: 29239216; eng
  • Fukata Y, Fukata M. Protein palmitoylation in neuronal development and synaptic plasticity. Nat Rev Neurosci. 2010 Mar;11(3):161–175. . PubMed PMID: 20168314; eng
  • Globa AK, Bamji SX. Protein palmitoylation in the development and plasticity of neuronal connections. Curr Opin Neurobiol. 2017 Aug;45:210–220. PubMed PMID: 28366531; eng.
  • Huang K, El-Husseini A. Modulation of neuronal protein trafficking and function by palmitoylation. Curr Opin Neurobiol. 2005 Oct;15(5):527–535. . PubMed PMID: 16125924; eng
  • Cho E, Park M. Palmitoylation in Alzheimer’s disease and other neurodegenerative diseases. Pharmacol Res. 2016 Sep;111:133–151. PubMed PMID: 27293050; eng.
  • Sanders SS, Hayden MR. Aberrant palmitoylation in Huntington disease. Biochem Soc Trans. 2015 Apr;43(2):205–210. PubMed PMID: 25849918; eng
  • Ko PJ, Dixon SJ. Protein palmitoylation and cancer. EMBO Rep. 2018 Oct;19(10). DOI:10.15252/embr.201846666. PubMed PMID: 30232163; eng.
  • Resh MD. Palmitoylation of proteins in cancer. Biochem Soc Trans. 2017 Apr 15;45(2):409–416. PubMed PMID: 28408481; eng.
  • Chavda B, Arnott JA, Planey SL. Targeting protein palmitoylation: selective inhibitors and implications in disease. Expert Opin Drug Discov. 2014 Sep;99:1005–1019. PubMed PMID: 24967607; eng.
  • Chen B, Sun Y, Niu J, et al. Protein lipidation in cell signaling and diseases: function, regulation, and therapeutic opportunities. Cell Chem Biol. 2018 Jul 19;25(7):817–831. PubMed PMID: 29861273; eng.
  • Cox AD, Der CJ, Philips MR. Targeting RAS membrane association: back to the future for anti-RAS drug discovery? Clin Cancer Res. 2015 Apr 15;21(8):1819–1827. . PubMed PMID: 25878363; eng.
  • Lanyon-Hogg T, Faronato M, Serwa RA, et al. Dynamic protein acylation: new substrates, mechanisms, and drug targets. Trends Biochem Sci. 2017 Jul;42(7):566–581. PubMed PMID: 28602500; eng.
  • Lin DTS, Davis NG, Conibear E. Targeting the Ras palmitoylation/depalmitoylation cycle in cancer. Biochem Soc Trans. 2017 Aug 15;45(4):913–921. PubMed PMID: 28630138; eng.
  • Chamberlain LH, Shipston MJ. The physiology of protein S-acylation. Physiol Rev. 2015 Apr;95(2):341–376. . PubMed PMID: 25834228; eng
  • Linder ME, Deschenes RJ. Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol. 2007 Jan;8(1):74–84. PubMed PMID: 17183362
  • Veit M, Siche S. S-acylation of influenza virus proteins: are enzymes for fatty acid attachment promising drug targets? Vaccine. 2015 Dec 8;33(49):7002–7007. . PubMed PMID: 26387429; eng.
  • Schmidt MF, Schlesinger MJ. Fatty acid binding to vesicular stomatitis virus glycoprotein: a new type of post-translational modification of the viral glycoprotein. Cell. 1979 Aug;17(4):813–819. PubMed PMID: 226266.
  • Schmidt MF. Acylation of viral spike glycoproteins: a feature of enveloped RNA viruses. Virology. 1982 Jan 15;116(1):327–338. . PubMed PMID: 6278712; eng.
  • Schmidt MF, Bracha M, Schlesinger MJ. Evidence for covalent attachment of fatty acids to Sindbis virus glycoproteins. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1687–1691. . PubMed PMID: 287008; eng
  • Veit M, Schmidt MF, Rott R. Different palmitoylation of paramyxovirus glycoproteins. Virology. 1989 Jan;168(1):173–176. PubMed PMID: 2535902; eng
  • Berger M, Schmidt MF. Cell-free fatty acid acylation of Semliki Forest viral polypeptides with microsomal membranes from eukaryotic cells. J Biol Chem. 1984 Jun 10;259(11):7245–7252. PubMed PMID: 6725287; eng
  • Berger M, Schmidt MF. Identification of acyl donors and acceptor proteins for fatty acid acylation in BHK cells infected with Semliki Forest virus. Embo J. 1984 Apr;3(4):713–719. PubMed PMID: 6723626; eng
  • Kordyukova LV, Serebryakova MV, Baratova LA, et al. S acylation of the hemagglutinin of influenza viruses: mass spectrometry reveals site-specific attachment of stearic acid to a transmembrane cysteine. J Virol. 2008 Sep;82(18):9288–9292. PubMed PMID: 18596092; eng.
  • Kordyukova LV, Serebryakova MV, Polyansky AA, et al. Linker and/or transmembrane regions of influenza A/Group-1, A/Group-2, and type B virus hemagglutinins are packed differently within trimers. Biochim Biophys Acta. 2011 Jul;1808(7):1843–1854. PubMed PMID: 21420932.
  • Brett K, Kordyukova LV, Serebryakova MV, et al. Site-specific S-acylation of influenza virus hemagglutinin: the location of the acylation site relative to the membrane border is the decisive factor for attachment of stearate. J Biol Chem. 2014 Dec 12;289(50):34978–34989. PubMed PMID: 25349209; eng.
  • Kordyukova LV, Serebryakova MV, Baratova LA, et al. Site-specific attachment of palmitate or stearate to cytoplasmic versus transmembrane cysteines is a common feature of viral spike proteins. Virology. 2009 Mar 1;398(1):49–56. PubMed PMID: 20006369; eng.
  • Peitzsch RM, McLaughlin S. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry. 1993 Oct 5;32(39):10436–10443. . PubMed PMID: 8399188; eng.
  • Shahinian S, Silvius JR. Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes. Biochemistry. 1995 Mar 21;34(11):3813–3822. PubMed PMID: 7893678; eng.
  • Kokame K, Fukada Y, Yoshizawa T, et al. Lipid modification at the N terminus of photoreceptor G-protein alpha-subunit. Nature. 1992 Oct 22;359(6397):749–752. PubMed PMID: 1436039; eng.
  • Gerl MJ, Sampaio JL, Urban S, et al. Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. J Cell Biol. 2012 Jan 23;196(2):213–221. PubMed PMID: 22249292; PubMed Central PMCID: PMCPMC3265945.
  • Engel S, Scolari S, Thaa B, et al. FLIM-FRET and FRAP reveal association of influenza virus haemagglutinin with membrane rafts. Biochem J. 2009 Jan 15;425(3):567–573. PubMed PMID: 19888915; eng.
  • McBride CE, Machamer CE. Palmitoylation of SARS-CoV S protein is necessary for partitioning into detergent-resistant membranes and cell-cell fusion but not interaction with M protein. Virology. 2010 Sep 15;405(1):139–148. . PubMed PMID: 20580052; eng.
  • Melkonian KA, Ostermeyer AG, Chen JZ, et al. Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. many raft proteins are acylated, while few are prenylated. J Biol Chem. 1999 Feb 5;274(6):3910–3917. PubMed PMID: 9920947.
  • Ernst AM, Syed SA, Zaki O, et al. S-palmitoylation sorts membrane cargo for anterograde transport in the Golgi. Dev Cell. 2018 Nov 19;47(4):479–493 e7. PubMed PMID: 30458139; eng.
  • Engel S, de Vries M, Herrmann A, et al. Mutation of a raft-targeting signal in the transmembrane region retards transport of influenza virus hemagglutinin through the Golgi. FEBS Lett. 2012 Feb 3;586(3):277–282. PubMed PMID: 22245151; eng.
  • Veit M, Kretzschmar E, Kuroda K, et al. Site-specific mutagenesis identifies three cysteine residues in the cytoplasmic tail as acylation sites of influenza virus hemagglutinin. J Virol. 1991 May;65(5):2491–2500. PubMed PMID: 1901916; eng.
  • de Vries M, Herrmann A, Veit M. A cholesterol consensus motif is required for efficient intracellular transport and raft association of a group 2 HA from influenza virus. Biochem J. 2014 Jan 15;465(2):305–314. . PubMed PMID: 25330796; eng.
  • Hu B, Hofer CT, Thiele C, et al. Cholesterol binding to the transmembrane region of a group 2 HA of Influenza virus is essential for virus replication affecting both virus assembly and HA’s fusion activity. J Virol. 2019 May 22;93. DOI:10.1128/JVI.00555-19 PubMed PMID: 31118253; eng.
  • Baird NL, Starkey JL, Hughes DJ, et al. Myristylation and palmitylation of HSV-1 UL11 are not essential for its function. Virology. 2010 Feb 5;397(1):80–88. PubMed PMID: 19944438; eng.
  • Sobocinska J, Roszczenko-Jasinska P, Ciesielska A, et al. Protein palmitoylation and its role in bacterial and viral infections. Front Immunol. 2018;8:2003. . PubMed PMID: 29403483; eng.
  • Veit M. Palmitoylation of virus proteins. Biol Cell. 2012 Sep;104(9):493–515. . PubMed PMID: 22548323
  • Veit M, Serebryakova MV, Kordyukova LV. Palmitoylation of influenza virus proteins. Biochem Soc Trans. 2013 Feb 1;41(1):50–55. PubMed PMID: 23356257; eng.
  • Chen BJ, Takeda M, Lamb RA. Influenza virus hemagglutinin (H3 subtype) requires palmitoylation of its cytoplasmic tail for assembly: M1 proteins of two subtypes differ in their ability to support assembly. J Virol. 2005 Nov;79(21):13673–13684. PubMed PMID: 16227287; eng.
  • Siche S, Brett K, Moller L, et al. Two cytoplasmic acylation sites and an adjacent hydrophobic residue, but no other conserved amino acids in the cytoplasmic tail of HA from Influenza A virus are crucial for virus replication. Viruses. 2015 Dec 8;7(12):6458–6475. PubMed PMID: 26670246; eng.
  • Wagner R, Herwig A, Azzouz N, et al. Acylation-mediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity. J Virol. 2005 May;79(10):6449–6458. PubMed PMID: 15858028; PubMed Central PMCID: PMCPMC1091681.
  • Zurcher T, Luo G, Palese P. Mutations at palmitylation sites of the influenza virus hemagglutinin affect virus formation. J Virol. 1994 Sep;68(9):5748–5754. PubMed PMID: 8057456; eng
  • Ujike M, Nakajima K, Nobusawa E. Influence of acylation sites of influenza B virus hemagglutinin on fusion pore formation and dilation. J Virol. 2004 Nov;78(21):11536–11543. . PubMed PMID: 15479794; eng
  • Wang M, Ludwig K, Bottcher C, et al. The role of stearate attachment to the hemagglutinin-esterase-fusion glycoprotein HEF of influenza C virus. Cell Microbiol. 2015 May;18(5):692–704. PubMed PMID: 26518983; eng.
  • Grantham ML, Wu WH, Lalime EN, et al. Palmitoylation of the influenza A virus M2 protein is not required for virus replication in vitro but contributes to virus virulence. J Virol. 2009 Sep;83(17):8655–8661. PubMed PMID: 19553312; eng.
  • Thaa B, Tielesch C, Moller L, et al. Growth of influenza A virus is not impeded by simultaneous removal of the cholesterol-binding and acylation sites in the M2 protein. J Gen Virol. 2012 Feb;93(Pt 2):282–292. PubMed PMID: 22012459; eng.
  • Muraki Y, Okuwa T, Furukawa T, et al. Palmitoylation of CM2 is dispensable to influenza C virus replication. Virus Res. 2011 Apr;157(1):99–105. PubMed PMID: 21352864; eng.
  • Demers A, Ran Z, Deng Q, et al. Palmitoylation is required for intracellular trafficking of influenza B virus NB protein and efficient influenza B virus growth in vitro. J Gen Virol. 2014 Jun;95(Pt 6):1211–1220. PubMed PMID: 24671751; PubMed Central PMCID: PMCPMC4027035.
  • Hatta M, Kawaoka Y. The NB protein of influenza B virus is not necessary for virus replication in vitro. J Virol. 2003 May;77(10):6050–6054. . PubMed PMID: 12719596; PubMed Central PMCID: PMCPMC154028
  • Branigan PJ, Day ND, Liu C, et al. The cytoplasmic domain of the F protein of human respiratory syncytial virus is not required for cell fusion. J Gen Virol. 2006 Feb;87(Pt 2):395–398. PubMed PMID: 16432027; eng.
  • Caballero M, Carabana J, Ortego J, et al. Measles virus fusion protein is palmitoylated on transmembrane-intracytoplasmic cysteine residues which participate in cell fusion. J Virol. 1998 Oct;72(10):8198–8204. PubMed PMID: 9733862; eng.
  • Gaudin Y, Tuffereau C, Benmansour A, et al. Fatty acylation of rabies virus proteins. Virology. 1991 Sep;184(1):441–444. PubMed PMID: 1871978; eng.
  • Whitt MA, Rose JK. Fatty acid acylation is not required for membrane fusion activity or glycoprotein assembly into VSV virions. Virology. 1991 Dec;185(2):875–878. . PubMed PMID: 1660205; eng
  • Funke C, Becker S, Dartsch H, et al. Acylation of the marburg virus glycoprotein. Virology. 1995 Apr 1;208(1):289–297. PubMed PMID: 11831710; eng.
  • Ito H, Watanabe S, Takada A, et al. Ebola virus glycoprotein: proteolytic processing, acylation, cell tropism, and detection of neutralizing antibodies. J Virol. 2001 Feb;75(3):1576–1580. PubMed PMID: 11152533; eng.
  • Petit CM, Chouljenko VN, Iyer A, et al. Palmitoylation of the cysteine-rich endodomain of the SARS-coronavirus spike glycoprotein is important for spike-mediated cell fusion. Virology. 2007 Apr 10;360(2):264–274. PubMed PMID: 17134730; eng.
  • Shulla A, Gallagher T. Role of spike protein endodomains in regulating coronavirus entry. J Biol Chem. 2009 Nov 20;284(47):32725–32734. PubMed PMID: 19801669; eng.
  • Boscarino JA, Logan HL, Lacny JJ, et al. Envelope protein palmitoylations are crucial for murine coronavirus assembly. J Virol. 2008 Mar;82(6):2989–2999. PubMed PMID: 18184706; eng.
  • Lopez LA, Riffle AJ, Pike SL, et al. Importance of conserved cysteine residues in the coronavirus envelope protein. J Virol. 2008 Mar;82(6):3000–3010. PubMed PMID: 18184703; eng.
  • Gaedigk-Nitschko K, Ding MX, Levy MA, et al. Site-directed mutations in the Sindbis virus 6K protein reveal sites for fatty acylation and the underacylated protein affects virus release and virion structure. Virology. 1990 Mar;175(1):282–291. PubMed PMID: 2309447; eng.
  • Gaedigk-Nitschko K, Schlesinger MJ. The Sindbis virus 6K protein can be detected in virions and is acylated with fatty acids. Virology. 1990 Mar;175(1):274–281. PubMed PMID: 2408229; eng
  • Ivanova L, Schlesinger MJ. Site-directed mutations in the Sindbis virus E2 glycoprotein identify palmitoylation sites and affect virus budding. J Virol. 1993 May;67(5):2546–2551. PubMed PMID: 8474160; eng
  • Ryan C, Ivanova L, Schlesinger MJ. Effects of site-directed mutations of transmembrane cysteines in sindbis virus E1 and E2 glycoproteins on palmitylation and virus replication. Virology. 1998 Sep 15;249(1):62–67. PubMed PMID: 9740777; eng.
  • Ramsey J, Chavez M, Mukhopadhyay S. Domains of the TF protein important in regulating its own palmitoylation. Virology. 2019 May;531:31–39. PubMed PMID: 30852269; eng.
  • Ramsey J, Renzi EC, Arnold RJ, et al. Palmitoylation of Sindbis virus TF protein regulates its plasma membrane localization and subsequent incorporation into virions. J Virol. 2017 Feb 1;91(3). PubMed PMID: 27852864; PubMed Central PMCID: PMCPMC5244351. DOI:10.1128/JVI.02000-16.
  • Kiiver K, Tagen I, Zusinaite E, et al. Properties of non-structural protein 1 of Semliki Forest virus and its interference with virus replication. J Gen Virol. 2008 Jun;89(Pt 6):1457–1466. PubMed PMID: 18474562; eng.
  • Zhang N, Zhao H, Zhang L. Fatty acid synthase promotes the palmitoylation of chikungunya virus nsP1. J Virol. 2019 Feb 1;93(3). PubMed PMID: 30404808; PubMed Central PMCID: PMCPMC6340048. DOI:10.1128/JVI.01747-18
  • Majeau N, Fromentin R, Savard C, et al. Palmitoylation of hepatitis C virus core protein is important for virion production. J Biol Chem. 2009 Dec 4;284(49):33915–33925. PubMed PMID: 19783655; PubMed Central PMCID: PMCPMC2797162.
  • Paul D, Bartenschlager R, McCormick C. The predominant species of nonstructural protein 4B in hepatitis C virus-replicating cells is not palmitoylated. J Gen Virol. 2015 Jul;96(Pt 7):1696–1701. PubMed PMID: 25740959; PubMed Central PMCID: PMCPMC4635453
  • Yu GY, Lee KJ, Gao L, et al. Palmitoylation and polymerization of hepatitis C virus NS4B protein. J Virol. 2006 Jun;80(12):6013–6023. PubMed PMID: 16731940; PubMed Central PMCID: PMCPMC1472571.
  • Bhattacharya J, Peters PJ, Clapham PR. Human immunodeficiency virus type 1 envelope glycoproteins that lack cytoplasmic domain cysteines: impact on association with membrane lipid rafts and incorporation onto budding virus particles. J Virol. 2004 May;78(10):5500–5506. PubMed PMID: 15113929; eng
  • Rousso I, Mixon MB, Chen BK, et al. Palmitoylation of the HIV-1 envelope glycoprotein is critical for viral infectivity. Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13523–13525. PubMed PMID: 11095714; eng.
  • Chan WE, Lin HH, Chen SS. Wild-type-like viral replication potential of human immunodeficiency virus type 1 envelope mutants lacking palmitoylation signals. J Virol. 2005 Jul;79(13):8374–8387. PubMed PMID: 15956582; eng
  • Chopard C, Tong PBV, Toth P, et al. Cyclophilin A enables specific HIV-1 Tat palmitoylation and accumulation in uninfected cells. Nat Commun. 2018 Jun 8;9(1):2251. PubMed PMID: 29884859; eng.
  • Persing DH, Varmus HE, Ganem D. The preS1 protein of hepatitis B virus is acylated at its amino terminus with myristic acid. J Virol. 1987 May;61(5):1672–1677. PubMed PMID: 3573147; eng
  • Patrone M, Coroadinha AS, Teixeira AP, et al. Palmitoylation strengthens cholesterol-dependent multimerization and fusion activity of human cytomegalovirus glycoprotein B (gB). J Biol Chem. 2015 Feb 26;291(9):4711–4722. PubMed PMID: 26694613; eng.
  • Mach M, Osinski K, Kropff B, et al. The carboxy-terminal domain of glycoprotein N of human cytomegalovirus is required for virion morphogenesis. J Virol. 2007 May;81(10):5212–5224. PubMed PMID: 17229708; eng.
  • Serwa RA, Abaitua F, Krause E, et al. Systems analysis of protein fatty acylation in herpes simplex virus-infected cells using chemical proteomics. Chem Biol. 2015 Aug 20;22(8):1008–1017. PubMed PMID: 26256475; PubMed Central PMCID: PMCPMC4543063.
  • Gouttenoire J, Pollan A, Abrami L, et al. Palmitoylation mediates membrane association of hepatitis E virus ORF3 protein and is required for infectious particle secretion. PLoS Pathog. 2018 Dec;14(12):e1007471. PubMed PMID: 30532200; PubMed Central PMCID: PMCPMC6307819.
  • Peng T, Thinon E, Hang HC. Proteomic analysis of fatty-acylated proteins. Curr Opin Chem Biol. 2015 Feb;30:77–86. PubMed PMID: 26656971; eng.
  • Chan P, Han X, Zheng B, et al. Autopalmitoylation of TEAD proteins regulates transcriptional output of the Hippo pathway. Nat Chem Biol. 2016 Apr;12(4):282–289. PubMed PMID: 26900866; eng.
  • Kummel D, Heinemann U, Veit M. Unique self-palmitoylation activity of the transport protein particle component Bet3: a mechanism required for protein stability. Proc Natl Acad Sci U S A. 2006 Aug 22;103(34):12701–12706. . PubMed PMID: 16908848; eng.
  • Lobo S, Greentree WK, Linder ME, et al. Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J Biol Chem. 2002 Oct 25;277(43):41268–41273. PubMed PMID: 12193598.
  • Roth AF, Feng Y, Chen L, et al. The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J Cell Biol. 2002 Oct 14;159(1):23–28. PubMed PMID: 12370247; PubMed Central PMCID: PMCPMC2173492.
  • Gonzalez Montoro A, Quiroga R, Valdez Taubas J. Zinc co-ordination by the DHHC cysteine-rich domain of the palmitoyltransferase Swf1. Biochem J. 2013 Sep 15;454(3):427–435. PubMed PMID: 23790227; eng.
  • Putilina T, Wong P, Gentleman S. The DHHC domain: a new highly conserved cysteine-rich motif. Mol Cell Biochem. 1999 May;195(1–2):219–226. . PubMed PMID: 10395086; eng
  • Fukata M, Fukata Y, Adesnik H, et al. Identification of PSD-95 palmitoylating enzymes. Neuron. 2004 Dec 16;44(6):987–996. PubMed PMID: 15603741.
  • Ohno Y, Kihara A, Sano T, et al. Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim Biophys Acta. 2006 Apr;1761(4):474–483. PubMed PMID: 16647879.
  • Wittouck S, van Noort V. Correlated duplications and losses in the evolution of palmitoylation writer and eraser families. BMC Evol Biol. 2017 Mar 20;17(1):83. . PubMed PMID: 28320309; eng.
  • Lemonidis K, Sanchez-Perez MC, Chamberlain LH. Identification of a novel sequence motif recognized by the ankyrin repeat domain of zDHHC17/13 S-acyltransferases. J Biol Chem. 2015 Sep 4;290(36):21939–21950. PubMed PMID: 26198635; PubMed Central PMCID: PMCPMC4571948.
  • Fredericks GJ, Hoffmann FW, Rose AH, et al. Stable expression and function of the inositol 1,4,5-triphosphate receptor requires palmitoylation by a DHHC6/selenoprotein K complex. Proc Natl Acad Sci U S A. 2014 Nov 18;111(46):16478–16483. PubMed PMID: 25368151; PubMed Central PMCID: PMCPMC4246275.
  • Ebsen H, Lettau M, Kabelitz D, et al. Identification of SH3 domain proteins interacting with the cytoplasmic tail of the a disintegrin and metalloprotease 10 (ADAM10). PLoS One. 2014;9(7):e102899. . PubMed PMID: 25036101; PubMed Central PMCID: PMCPMC4103893.
  • Thomas GM, Hayashi T, Chiu SL, et al. Palmitoylation by DHHC5/8 targets GRIP1 to dendritic endosomes to regulate AMPA-R trafficking. Neuron. 2012 Feb 9;73(3):482–496. PubMed PMID: 22325201; PubMed Central PMCID: PMCPMC3345505.
  • Li Y, Hu J, Hofer K, et al. DHHC5 interacts with PDZ domain 3 of post-synaptic density-95 (PSD-95) protein and plays a role in learning and memory. J Biol Chem. 2010 Apr 23;285(17):13022–13031. PubMed PMID: 20178993; eng.
  • Thomas GM, Hayashi T, Huganir RL, et al. DHHC8-dependent PICK1 palmitoylation is required for induction of cerebellar long-term synaptic depression. J Neurosci. 2013 Sep 25;33(39):15401–15407. PubMed PMID: 24068808; eng.
  • Abrami L, Dallavilla T, Sandoz PA, et al. Identification and dynamics of the human ZDHHC16-ZDHHC6 palmitoylation cascade. Elife. 2017 Aug 15; 6 DOI:10.7554/eLife.27826. PubMed PMID: 28826475; PubMed Central PMCID: PMCPMC5582869.
  • Gorleku OA, Barns AM, Prescott GR, et al. Endoplasmic reticulum localization of DHHC palmitoyltransferases mediated by lysine-based sorting signals. J Biol Chem. 2011 Nov 11;286(45):39573–39584. PubMed PMID: 21926431; eng.
  • Salaun C, Ritchie L, Greaves J, et al. The C-terminal domain of zDHHC2 contains distinct sorting signals that regulate intracellular localisation in neurons and neuroendocrine cells. Mol Cell Neurosci. 2017 Dec;85:235–246. PubMed PMID: 28768144; eng.
  • Jennings BC, Linder ME. DHHC protein S-acyltransferases use similar ping-pong kinetic mechanisms but display different acyl-CoA specificities. J Biol Chem. 2012 Mar 2;287(10):7236–7245. PubMed PMID: 22247542; PubMed Central PMCID: PMCPMC3293542.
  • Lai J, Linder ME. Oligomerization of DHHC protein S-acyltransferases. J Biol Chem. 2013 Aug 2;288(31):22862–22870. PubMed PMID: 23793055; eng.
  • Greaves J, Munro KR, Davidson SC, et al. Molecular basis of fatty acid selectivity in the zDHHC family of S-acyltransferases revealed by click chemistry. Proc Natl Acad Sci U S A. 2017 Feb 21;114(8):E1365–E1374. PubMed PMID: 28167757; PubMed Central PMCID: PMCPMC5338407.
  • Rana MS, Kumar P, Lee CJ, et al. Fatty acyl recognition and transfer by an integral membrane S-acyltransferase. Science. 2018 Jan 12;359(6372):eaao6326. PubMed PMID: 29326245; PubMed Central PMCID: PMCPMC6317078.
  • Brown MS, Radhakrishnan A, Goldstein JL. Retrospective on cholesterol homeostasis: the central role of scap. Annu Rev Biochem. 2018 Jun 20;87:783–807. PubMed PMID: 28841344; eng.
  • Yuan S, Chu H, Chan JF, et al. SREBP-dependent lipidomic reprogramming as a broad-spectrum antiviral target. Nat Commun. 2019 Jan 10;10(1):120. PubMed PMID: 30631056; eng.
  • Ohol YM, Wang Z, Kemble G, et al. Direct inhibition of cellular fatty acid synthase impairs replication of respiratory syncytial virus and other respiratory viruses. PLoS One. 2015;10(12):e0144648. . PubMed PMID: 26659560; PubMed Central PMCID: PMCPMC4684246.
  • Yang W, Hood BL, Chadwick SL, et al. Fatty acid synthase is up-regulated during hepatitis C virus infection and regulates hepatitis C virus entry and production. Hepatology. 2008 Nov;48(5):1396–1403. PubMed PMID: 18830996; PubMed Central PMCID: PMCPMC2614928.
  • Kulkarni MM, Ratcliff AN, Bhat M, et al. Cellular fatty acid synthase is required for late stages of HIV-1 replication. Retrovirology. 2017 Sep 29;14(1):45. PubMed PMID: 28962653; PubMed Central PMCID: PMCPMC5622536.
  • Fukata Y, Iwanaga T, Fukata M. Systematic screening for palmitoyl transferase activity of the DHHC protein family in mammalian cells. Methods. 2006 Oct;40(2):177–182. PubMed PMID: 17012030
  • Lakkaraju AK, Abrami L, Lemmin T, et al. Palmitoylated calnexin is a key component of the ribosome-translocon complex. Embo J. 2012 Apr 4;31(7):1823–1835. PubMed PMID: 22314232; PubMed Central PMCID: PMCPMC3321195.
  • Tian L, McClafferty H, Jeffries O, et al. Multiple palmitoyltransferases are required for palmitoylation-dependent regulation of large conductance calcium- and voltage-activated potassium channels. J Biol Chem. 2010 Jul 30;285(31):23954–23962. PubMed PMID: 20507996; PubMed Central PMCID: PMCPMC2911306.
  • Roth AF, Wan J, Bailey AO, et al. Global analysis of protein palmitoylation in yeast. Cell. 2006 Jun 2;125(5):1003–1013. PubMed PMID: 16751107; PubMed Central PMCID: PMCPMC2246083.
  • Kordyukova L, Krabben L, Serebryakova M, et al. S-acylation of proteins. Methods Mol Biol. 2019;1934:265–291. . PubMed PMID: 31256385; eng.
  • Gao X, Hannoush RN. A decade of click chemistry in protein palmitoylation: impact on discovery and new biology. Cell Chem Biol. 2018 Mar 15;25(3):236–246. PubMed PMID: 29290622; eng.
  • Drisdel RC, Green WN. Labeling and quantifying sites of protein palmitoylation. Biotechniques. 2004 Feb;36(2):276–285. PubMed PMID: 14989092; eng.
  • Forrester MT, Hess DT, Thompson JW, et al. Site-specific analysis of protein S-acylation by resin-assisted capture. J Lipid Res. 2010 Feb;52(2):393–398. PubMed PMID: 21044946; eng.
  • Wang S, Mott KR, Cilluffo M, et al. The absence of DHHC3 affects primary and latent herpes simplex virus 1 infection. J Virol. 2018 Feb 15;92(4). PubMed PMID: 29187538; PubMed Central PMCID: PMCPMC5790959. DOI:10.1128/JVI.01599-17.
  • Wang S, Mott KR, Wawrowsky K, et al. Binding of herpes simplex virus 1 UL20 to GODZ (DHHC3) affects its palmitoylation and is essential for infectivity and proper targeting and localization of UL20 and glycoprotein K. J Virol. 2017 Oct 1;91(19). PubMed PMID: 28724772; PubMed Central PMCID: PMCPMC5599753. DOI:10.1128/JVI.00945-17.
  • Zhou Q, Lin H, Wang S, et al. The ER-associated protein ZDHHC1 is a positive regulator of DNA virus-triggered, MITA/STING-dependent innate immune signaling. Cell Host Microbe. 2014 Oct 8;16(4):450–461. PubMed PMID: 25299331; eng.
  • Mukai K, Konno H, Akiba T, et al. Activation of STING requires palmitoylation at the Golgi. Nat Commun. 2016 Jun 21;7:11932. . PubMed PMID: 27324217; eng.
  • Hansen AL, Mukai K, Schopfer FJ, et al. STING palmitoylation as a therapeutic target. Cell Mol Immunol. 2019 Mar;16(3):236–241. PubMed PMID: 30796349; eng.
  • Yount JS, Karssemeijer RA, Hang HC. S-palmitoylation and ubiquitination differentially regulate interferon-induced transmembrane protein 3 (IFITM3)-mediated resistance to influenza virus. J Biol Chem. 2012 Jun 1;287(23):19631–19641. PubMed PMID: 22511783; PubMed Central PMCID: PMCPMC3365998.
  • Yount JS, Moltedo B, Yang YY, et al. Palmitoylome profiling reveals S-palmitoylation-dependent antiviral activity of IFITM3. Nat Chem Biol. 2010 Aug;6(8):610–614. PubMed PMID: 20601941; eng.
  • McMichael TM, Zhang L, Chemudupati M, et al. The palmitoyltransferase ZDHHC20 enhances interferon-induced transmembrane protein 3 (IFITM3) palmitoylation and antiviral activity. J Biol Chem. 2017 Dec 29;292(52):21517–21526. PubMed PMID: 29079573; PubMed Central PMCID: PMCPMC5766958.
  • Gottlieb CD, Zhang S, Linder ME. The cysteine-rich domain of the DHHC3 palmitoyltransferase is palmitoylated and contains tightly bound zinc. J Biol Chem. 2015 Dec 4;290(49):29259–29269. PubMed PMID: 26487721; eng.
  • Neess D, Bek S, Engelsby H, et al. Long-chain acyl-CoA esters in metabolism and signaling: role of acyl-CoA binding proteins. Prog Lipid Res. 2015 Jul;59:1–25. PubMed PMID: 25898985; eng.
  • Verardi R, Kim JS, Ghirlando R, et al. structural basis for substrate recognition by the ankyrin repeat domain of human DHHC17 palmitoyltransferase. Structure. 2017 Sep 5;25(9):1337–1347 e6. PubMed PMID: 28757145; eng.
  • Greaves J, Gorleku OA, Salaun C, et al. Palmitoylation of the SNAP25 protein family: specificity and regulation by DHHC palmitoyl transferases. J Biol Chem. 2010 Aug 6;285(32):24629–24638. PubMed PMID: 20519516; PubMed Central PMCID: PMCPMC2915699.
  • Greaves J, Prescott GR, Fukata Y, et al. The hydrophobic cysteine-rich domain of SNAP25 couples with downstream residues to mediate membrane interactions and recognition by DHHC palmitoyl transferases. Mol Biol Cell. 2009 Mar;20(6):1845–1854. PubMed PMID: 19158383; eng.
  • Gamsjaeger R, Liew CK, Loughlin FE, et al. Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem Sci. 2007 Feb;32(2):63–70. PubMed PMID: 17210253; eng.
  • Rodenburg RNP, Snijder J, van de Waterbeemd M, et al. Stochastic palmitoylation of accessible cysteines in membrane proteins revealed by native mass spectrometry. Nat Commun. 2017 Nov 3;8(1):1280. PubMed PMID: 29097667; eng.
  • Benton DJ, Nans A, Calder LJ, et al. Influenza hemagglutinin membrane anchor. Proc Natl Acad Sci U S A. 2018 Oct 2;115(40):10112–10117. PubMed PMID: 30224494; eng.
  • Mineev KS, Lyukmanova EN, Krabben L, et al. Structural investigation of influenza virus hemagglutinin membrane-anchoring peptide. Protein Eng Des Sel. 2013 Sep;26(9):547–552. PubMed PMID: 23873663; eng.
  • Plain F, Congreve SD, Yee RSZ, et al. An amphipathic alpha-helix directs palmitoylation of the large intracellular loop of the sodium/calcium exchanger. J Biol Chem. 2017 Jun 23;292(25):10745–10752. PubMed PMID: 28432123; eng.
  • Lin YH, Doms AG, Cheng E, et al. Host cell-catalyzed S-palmitoylation mediates Golgi targeting of the legionella ubiquitin ligase GobX. J Biol Chem. 2015 Oct 16;290(42):25766–25781. PubMed PMID: 26316537; eng.
  • Thaa B, Levental I, Herrmann A, et al. Intrinsic membrane association of the cytoplasmic tail of influenza virus M2 protein and lateral membrane sorting regulated by cholesterol binding and palmitoylation. Biochem J. 2011 Aug 1;437(3):389–397. PubMed PMID: 21592088; eng.
  • Sharma M, Yi M, Dong H, et al. Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer. Science. 2010 Oct 22;330(6003):509–512. PubMed PMID: 20966252; eng.
  • Howie J, Reilly L, Fraser NJ, et al. Substrate recognition by the cell surface palmitoyl transferase DHHC5. Proc Natl Acad Sci U S A. 2014 Dec 9;111(49):17534–17539. PubMed PMID: 25422474; eng.
  • Nadolski MJ, Linder ME. Molecular recognition of the palmitoylation substrate Vac8 by its palmitoyltransferase Pfa3. J Biol Chem. 2009 Jun 26;284(26):17720–17730. PubMed PMID: 19416974; eng.
  • Gottlieb CD, Linder ME. Structure and function of DHHC protein S-acyltransferases. Biochem Soc Trans. 2017 Aug 15;45(4):923–928. PubMed PMID: 28630137; eng.
  • Lemonidis K, Salaun C, Kouskou M, et al. Substrate selectivity in the zDHHC family of S-acyltransferases. Biochem Soc Trans. 2017 Jun 15;45(3):751–758. PubMed PMID: 28620036; eng.
  • Lemonidis K, Werno MW, Greaves J, et al. The zDHHC family of S-acyltransferases. Biochem Soc Trans. 2015 Apr;43(2):217–221. PubMed PMID: 25849920; eng.
  • Rana MS, Lee CJ, Banerjee A. The molecular mechanism of DHHC protein acyltransferases. Biochem Soc Trans. 2019 Feb 28;47(1):157–167. PubMed PMID: 30559274.
  • Duncan JA, Gilman AG. A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21(RAS). J Biol Chem. 1998 Jun 19;273(25):15830–15837. PubMed PMID: 9624183.
  • Rusch M, Zimmermann TJ, Burger M, et al. Identification of acyl protein thioesterases 1 and 2 as the cellular targets of the Ras-signaling modulators palmostatin B and M. Angew Chem Int Ed Engl. 2011 Oct 10;50(42):9838–9842. PubMed PMID: 21905186.
  • Tian L, McClafferty H, Knaus HG, et al. Distinct acyl protein transferases and thioesterases control surface expression of calcium-activated potassium channels. J Biol Chem. 2012 Apr 27;287(18):14718–14725. PubMed PMID: 22399288; PubMed Central PMCID: PMCPMC3340283.
  • Tomatis VM, Trenchi A, Gomez GA, et al. Acyl-protein thioesterase 2 catalyzes the deacylation of peripheral membrane-associated GAP-43. PLoS One. 2010 Nov 30;5(11):e15045. PubMed PMID: 21152083; PubMed Central PMCID: PMCPMC2994833.
  • Yeh DC, Duncan JA, Yamashita S, et al. Depalmitoylation of endothelial nitric-oxide synthase by acyl-protein thioesterase 1 is potentiated by Ca(2+)-calmodulin. J Biol Chem. 1999 Nov 12;274(46):33148–33154. PubMed PMID: 10551886.
  • Won SJ, Davda D, Labby KJ, et al. Molecular mechanism for isoform-selective inhibition of acyl protein thioesterases 1 and 2 (APT1 and APT2). ACS Chem Biol. 2016 Dec 16;11(12):3374–3382. PubMed PMID: 27748579; eng.
  • Chen S, Han C, Miao X, et al. Targeting MC1R depalmitoylation to prevent melanomagenesis in redheads. Nat Commun. 2019 Feb 20;10(1):877. PubMed PMID: 30787281; eng.
  • Kong E, Peng S, Chandra G, et al. Dynamic palmitoylation links cytosol-membrane shuttling of acyl-protein thioesterase-1 and acyl-protein thioesterase-2 with that of proto-oncogene H-ras product and growth-associated protein-43. J Biol Chem. 2013 Mar 29;288(13):9112–9125. PubMed PMID: 23396970; PubMed Central PMCID: PMCPMC3610984.
  • Kathayat RS, Cao Y, Elvira PD, et al. Active and dynamic mitochondrial S-depalmitoylation revealed by targeted fluorescent probes. Nat Commun. 2018 Jan 23;9(1):334. PubMed PMID: 29362370; eng.
  • Kostiuk MA, Corvi MM, Keller BO, et al. Identification of palmitoylated mitochondrial proteins using a bio-orthogonal azido-palmitate analogue. Faseb J. 2008 Mar;22(3):721–732. PubMed PMID: 17971398; eng.
  • Lin DT, Conibear E. ABHD17 proteins are novel protein depalmitoylases that regulate N-Ras palmitate turnover and subcellular localization. Elife. 2015 Dec 23;4:e11306. PubMed PMID: 26701913; eng.
  • Veit M, Schmidt MF. Timing of palmitoylation of influenza virus hemagglutinin. FEBS Lett. 1993 Dec 27;336(2):243–247. . PubMed PMID: 8262238; eng.
  • Veit M, Schmidt MF. Enzymatic depalmitoylation of viral glycoproteins with acyl-protein thioesterase 1 in vitro. Virology. 2001 Sep 15;288(1):89–95. . PubMed PMID: 11543661; eng.
  • Dallavilla T, Abrami L, Sandoz PA, et al. Model-driven understanding of palmitoylation dynamics: regulated acylation of the endoplasmic reticulum chaperone calnexin. PLoS Comput Biol. 2016 Feb;12(2):e1004774. PubMed PMID: 26900856; eng.
  • Collins MO, Woodley KT, Choudhary JS. Global, site-specific analysis of neuronal protein S-acylation. Sci Rep. 2017 Jul 5;7(1):4683. PubMed PMID: 28680068; eng.
  • Yang W, Di Vizio D, Kirchner M, et al. Proteome scale characterization of human S-acylated proteins in lipid raft-enriched and non-raft membranes. Mol Cell Proteomics. 2009 Jan;9(1):54–70. PubMed PMID: 19801377; eng.
  • Jennings BC, Nadolski MJ, Ling Y, et al. 2-bromopalmitate and 2-(2-hydroxy-5-nitro-benzylidene)-benzo[b]thiophen-3-one inhibit DHHC-mediated palmitoylation in vitro. J Lipid Res. 2009 Feb;50(2):233–242. PubMed PMID: 18827284; eng.
  • Hutchinson EC, Charles PD, Hester SS, et al. Conserved and host-specific features of influenza virion architecture. Nat Commun. 2014 Sep 16;5:4816. . PubMed PMID: 25226414; eng.
  • Plotch SJ, Bouloy M, Ulmanen I, et al. A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell. 1981 Mar;23(3):847–858. PubMed PMID: 6261960; eng.
  • Hein MY, Hubner NC, Poser I, et al. A human interactome in three quantitative dimensions organized by stoichiometries and abundances. Cell. 2015 Oct 22;163(3):712–723. PubMed PMID: 26496610; eng.
  • Nagaraj N, Wisniewski JR, Geiger T, et al. Deep proteome and transcriptome mapping of a human cancer cell line. Mol Syst Biol. 2011 Nov 8;7:548. PubMed PMID: 22068331; eng.
  • De I, Sadhukhan S. Emerging roles of DHHC-mediated protein S-palmitoylation in physiological and pathophysiological context. Eur J Cell Biol. 2018 Jun;97(5):319–338. PubMed PMID: 29602512; eng
  • el-Husseini Ael D, Bredt DS. Protein palmitoylation: a regulator of neuronal development and function. Nat Rev Neurosci. 2002 Oct;3(10):791–802. PubMed PMID: 12360323
  • Ducker CE, Griffel LK, Smith RA, et al. Discovery and characterization of inhibitors of human palmitoyl acyltransferases. Mol Cancer Ther. 2006 Jul;5(7):1647–1659. PubMed PMID: 16891450; eng.
  • Hamel LD, Deschenes RJ, Mitchell DA. A fluorescence-based assay to monitor autopalmitoylation of zDHHC proteins applicable to high-throughput screening. Anal Biochem. 2014 Sep 1;460:1–8. PubMed PMID: 24878334; eng.
  • Hamel LD, Lenhart BJ, Mitchell DA, et al. Identification of protein palmitoylation inhibitors from a scaffold ranking library. Comb Chem High Throughput Screen. 2016;19(4):262–274. PubMed PMID: 27009891; eng.
  • Sliwoski G, Kothiwale S, Meiler J, et al. Computational methods in drug discovery. Pharmacol Rev. 2014;66(1):334–395. PubMed PMID: 24381236; eng.
  • Lonsdale R, Ward RA. Structure-based design of targeted covalent inhibitors. Chem Soc Rev. 2018 Jun 5;47(11):3816–3830. . PubMed PMID: 29620097; eng.
  • Neumann G, Watanabe T, Ito H, et al. Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9345–9350. PubMed PMID: 10430945; eng.
  • De Clercq E, Li G. Approved antiviral drugs over the past 50 Years. Clin Microbiol Rev. 2016 Jul;29(3):695–747. . PubMed PMID: 27281742; eng
  • Lemonidis K, Gorleku OA, Sanchez-Perez MC, et al. The Golgi S-acylation machinery comprises zDHHC enzymes with major differences in substrate affinity and S-acylation activity. Mol Biol Cell. 2014 Dec 1;25(24):3870–3883. PubMed PMID: 25253725; eng.
  • Renaud JP, Chari A, Ciferri C, et al. Cryo-EM in drug discovery: achievements, limitations and prospects. Nat Rev Drug Discov. 2018 Jul;17(7):471–492. PubMed PMID: 29880918; eng.
  • Cheng Y. Single-Particle Cryo-EM at Crystallographic Resolution. Cell. 2015 Apr 23;161(3):450–457. . PubMed PMID: 25910205; eng.

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