Palmitoylation cycles and regulation of protein function (Review)

References

• Greaves J, Chamberlain LH. Palmitoylation-dependent protein sorting. J Cell Biol 2007; 176: 249–254
   PubMed Web of Science ®Google Scholar
• Linder ME, Deschenes RJ. Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol 2007; 8: 74–84
   PubMed Web of Science ®Google Scholar
• Resh, MD. 2006. Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci STKE. re14.
   PubMedGoogle Scholar
• Skene JH, Virág I. Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J Cell Biol 1989; 108: 613–624
   PubMed Web of Science ®Google Scholar
• Craven SE, El-Husseini AE, Bredt DS. Synaptic targeting of the postsynaptic density protein PSD-95 mediated by lipid and protein motifs. Neuron 1999; 22: 497–509
   PubMed Web of Science ®Google Scholar
• Degtyarev MY, Spiegel AM, Jones TL. The G protein alpha s subunit incorporates [3H]palmitic acid and mutation of cysteine-3 prevents this modification. Biochemistry 1993; 32: 8057–8061
   PubMedGoogle Scholar
• Linder ME, Middleton P, Hepler JR, Taussig R, Gilman AG, Mumby SM. Lipid modifications of G proteins: alpha subunits are palmitoylated. Proc Natl Acad Sci USA 1993; 90: 3675–3679
   PubMed Web of Science ®Google Scholar
• Hancock JF, Paterson H, Marshall CJ. A polybasic domain or palmitylation is required in addition to the CAAX motif to localize p21ras to the plasma membrance. Cell 1990; 63: 133–139
   PubMed Web of Science ®Google Scholar
• Choy E, Chiu VK, Silletti J, Feoktistov M, Morimoto T, Michaelson D, Ivanov IE, Philips MR. Endomembrane trafficking of Ras: the CAAX motif targets proteins to the ER and Golgi. Cell 1999; 98: 69–80
   PubMed Web of Science ®Google Scholar
• Magee AI, Gutierrez L, McKay IA, Marshall CJ, Hall A. Dynamic fatty acylation of p21N-Ras. EMBO J. 1987; 6: 3353–3357
   PubMed Web of Science ®Google Scholar
• Christgau S, Schierbeck H, Aanstoot HJ, Aagaard L, Begley K, Kofod H, Hejnaes K, Baekkeskov S. Pancreatic β-cells express two autoantigenic forms of glutamic acid decarboxylase, a 65kDa hydrophilic form and a 64kDa amphiphilic form which can be both membrane-bound and soluble. J Biol Chem 1991; 266: 21257–21264
   PubMed Web of Science ®Google Scholar
• Christgau S, Aanstoot HJ, Schierbeck H, Begley K, Tullin S, Hejnaes H, Baekkeskov S. Membrane anchoring of the autoantigen GAD65 to microvesicles in pancreatic ß-cells by palmitoylation in the N-terminal domain. J Cell Biol 1992; 118: 309–320
   PubMed Web of Science ®Google Scholar
• Shi Y, Veit B, Baekkeskov S. Amino acid residues 24-31 but not palmitoylation of cysteines 30 and 45 are required for membrane anchoring of glutamic acid decarboxylase, GAD65. J Cell Biol 1994; 124: 927–934
   PubMed Web of Science ®Google Scholar
• Rocks O, Peyker A, Kahms M, Verveer PJ, Koerner C, Lumbierres M, Kuhlmann J, Waldmann H, Wittinghofer A, Bastiaens PIH. An acylation cycle regulates localization and activity of palmitoylated ras isoforms. Science 2005; 307: 1746–1752
   PubMed Web of Science ®Google Scholar
• Goodwin JS, Drake KR, Rogers C, Wright L, Lippincott-Schwartz J, Philips MR, Kenworthy AK. Depalmitoylated Ras traffics to and from the Golgi complex via a nonvesicular pathway. J Cell Biol 2005; 170: 261–272
   PubMed Web of Science ®Google Scholar
• Karnoub AE, Weinberg RA. Ras oncogenes: split personalities. Nat Rev Mol Cell Biol 2008; 9: 517–531
   PubMed Web of Science ®Google Scholar
• Apolloni A, Prior IA, Lindsay M, Parton RG, Hancock JF. H-Ras but not K-ras traffics to the plasma membrane through the exocytic pathway. Mol Cell Biol 2000; 20: 2475–2487
   PubMed Web of Science ®Google Scholar
• Chiu VK, Bivona T, Hach A, Sajous JB, Silletti J, Wiener H, Johnson RL 2nd, Cox AD, Philips MR. Ras signalling on the endoplasmic reticulum and the Golgi. Nat Cell Biol 2002; 4: 343–350
   PubMed Web of Science ®Google Scholar
• Kanaani J, Patterson G, Schaufele F, Lippincott-Schwartz J, Baekkeskov S. A palmitoylation cycle dynamically regulates partitioning of the GABA-synthesizing enzyme GAD65 between ER-Golgi and post-Golgi membranes. J Cell Sci 2008; 121: 437–449
   PubMed Web of Science ®Google Scholar
• Battaglioli GH, Liu H, Martin DL. Kinetic differences between the isoforms of glutamate decarboxylase: Implications for the regulation of GABA synthesis. J Neurochem 2003; 86: 879–887
   PubMedGoogle Scholar
• Condie BG, Bain G, Gottlieb DI, Capecchi MR. Cleft palate in mice with a targeted mutation in the gamma-aminobutyric acid-producing enzyme glutamic acid decarboxylase 67. Proc Natl Acad Sci USA 1997; 94: 11451–11455
   PubMed Web of Science ®Google Scholar
• Reetz A, Solimena M, Matteoli M, Folli F, Takei K, DeCamilli P. GABA and pancreatic ß-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic like microvesicles suggests their role in GABA storage and secretion. EMBO J 1991; 10: 1275–1284
   PubMed Web of Science ®Google Scholar
• Kanaani J, El-Husseini AE, Aguilera-Moreno A, Diacovo MJ, Bredt DS, Baekkeskov S. A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65. J Cell Biol 2002; 158: 1229–1238
   PubMed Web of Science ®Google Scholar
• Solimena M, Dirkx R, Radzynski M, Mundigl O, De Camilli P. A signal located within amino acids 1-27 of GAD65 is required for its targeting to the Golgi complex region. J Cell Biol 1994; 126: 331–341
   PubMed Web of Science ®Google Scholar
• Kanaani J, Diacovo MJ, El-Husseini AE, Bredt D, Baekkeskov S. Palmitoylation controls trafficking of GAD65 from Golgi membranes to axon-specific endosomes and a Rab5a-dependent pathway to presynaptic clusters. J Cell Sci 2004; 117: 2001–2013
   PubMedGoogle Scholar
• Hirschberg K, Miller CM, Ellenberg J, Presley JF, Siggia ED, Phair RD, Lippincott-Schwartz J. Kinetic analyses of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells. J Cell Biol 1998; 143: 1485–1503
   PubMed Web of Science ®Google Scholar
• Ward TH, Polishchuk RS, Caplan S, Hirschberg K, Lippincott-Schwartz J. Maintenance of Golgi structure and function depends on the integrity of ER export. J Cell Biol 2001; 155: 557–570
   PubMed Web of Science ®Google Scholar
• Duncan JA, Gilman AG. A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21RAS. J Biol Chem 1998; 273: 15830–15837
   PubMed Web of Science ®Google Scholar
• Duncan JA, Gilman AG. Characterization of Saccharomyces cerevisiae acyl-protein thioesterase 1, the enzyme responsible for G protein alpha subunit deacylation in vivo. J Biol Chem 2002; 277: 31740–31752
   PubMed Web of Science ®Google Scholar
• Yeh DC, Duncan JA, Yamashita S, Michel T. Depalmitoylation of endothelial nitric-oxide synthase by acyl-protein thioesterase 1 is potentiated by Ca2 + -calmodulin. J Biol Chem 1999; 274: 33148–33154
   PubMed Web of Science ®Google Scholar
• Chisari M, Saini DK, Kalyanaraman V, Gautam N. Shuttling of G protein subunits between the plasma membrane and intracellular membranes. J Biol Chem 2007; 282: 24092–24098
   PubMedGoogle Scholar
• Meder D, Simons K. Cell biology. Ras on the roundabout. Science. 2005; 307(5716)1731–1733
   PubMedGoogle Scholar
• Quatela SE, Philips MR. Ras signaling on the Golgi. Curr Opin Cell Biol 2006; 18(2)162–167
   PubMedGoogle Scholar
• Rocks O, Peyker A, Bastiaens PI. Spatio-temporal segregation of Ras signals: one ship, three anchors, many harbors. Curr Opin Cell Biol 2006; 18: 351–357
   PubMedGoogle Scholar
• Qanbar R, Bouvier M. Role of palmitoylation/depalmitoylation reactions in G-protein-coupled receptor function. Pharmacol Ther 2003; 97: 1–33
   PubMedGoogle Scholar
• Huang K, El-Husseini A. Modulation of neuronal protein trafficking and function by palmitoylation. Curr Opin Neurobiol 2005; 15: 527–535
   PubMed Web of Science ®Google Scholar
• Horton AC, Rácz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 2005; 48(5)757–771
   PubMedGoogle Scholar
• Lobo, S, Greentree, WK, Linder, ME, Deschenes, RJ.. Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J Biol Chem, 277:41268–41273.
   PubMedGoogle Scholar
• Zhao L, Lobo S, Dong X, Ault AD, Deschenes RJ. Erf4p and Erf2p form an endoplasmic reticulum-associated complex involved in the plasma membrane localization of yeast Ras proteins. J Biol Chem 2002; 277: 49352–49359
   PubMedGoogle Scholar
• Roth AF, Feng Y, Chen L, Davis NG. The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J Cell Biol 2002; 159: 23–28
   PubMed Web of Science ®Google Scholar
• Keller CA, Yuan X, Panzanelli P, Martin ML, Alldred M, Sassoè-Pognetto M, Lüscher B. The gamma2 subunit of GABA(A) receptors is a substrate for palmitoylation by GODZ. J Neurosci 2004; 24: 5881–5891
   PubMed Web of Science ®Google Scholar
• Roth AF, Wan J, Bailey AO, Sun B, Kuchar JA, Green WN, Phinney BS, Yates JR III, Davis NG. Global analysis of protein palmitoylation in yeast. Cell 2006; 125: 1003–1013
   PubMed Web of Science ®Google Scholar
• Bannan BA, Van Etten J, Kohler JA, Tsoi Y, Hansen NM, Sigmon S, Fowler E, Buff H, Williams TS, Ault JG, Glaser RL, Korey CA. The Drosophila protein palmitoylome: characterizing palmitoyl-thioesterases and DHHC palmitoyl-transferases. Fly 2008; 2: 198–214
   PubMed Web of Science ®Google Scholar
• Fukata M, Fukata Y, Adesnik H, Nicoll RA, Bredt DS. Identification of PSD-95 palmitoylating enzymes. Neuron 2004; 44: 987–996
   PubMed Web of Science ®Google Scholar
• Huang K, Yanai A, Kang R, Arstikaitis P, Singaraja RR, Metzler M, Mullard A, Haigh B, Guathier-Campbell C, Gutekunst C, Hayden MR, El-Husseini A. Huntingtin-Interacting Protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins. Neuron 2004; 44: 977–986
   PubMed Web of Science ®Google Scholar
• Swarthout JT, Lobo S, Farh L, Croke MR, Greentree WK, Deschenes RJ, Linder ME. DHHC9 and GCP16 constitute a human protein fatty acyltransferase with specificity for H- and N-Ras. J Biol Chem 2005; 280: 31141–31148
   PubMed Web of Science ®Google Scholar
• Mitchell DA, Vasudevan A, Linder ME, Deschenes RJ. Protein palmitoylation by a family of DHHC protein S-acyltransferases. J Lipid Res 2006; 47: 1118–1127
   PubMed Web of Science ®Google Scholar
• Shahinian S, Silvius JR. Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membrances. Biochemistry 1995; 34: 3813–3822
   PubMed Web of Science ®Google Scholar
• Michaelsons D, Aheran I, Bergo M, Young S, Phillips M. Membrane trafficking of heterotrimeric G proteins via the endoplasmic reticulum and Golgi. Mol Biol Cell 2002; 13: 3294–3302
   PubMedGoogle Scholar
• Camp LA, Hofmann SL. Purification and properties of a palmitoyl-protein thioesterase that cleaves palmitate from H-Ras. J Biol Chem 1993; 268: 22566–22574
   PubMed Web of Science ®Google Scholar
• Hellsten E, Vesa J, Olkkonen VM, Jalanko A, Peltonen L. Human palmitoyl protein thioesterase: evidence for lysosomal targeting of the enzyme and disturbed cellular routing in infantile neuronal ceroid lipofuscinosis. EMBO J 1996; 15: 5240–5245
   PubMed Web of Science ®Google Scholar
• Kim SJ, Zhang Z, Sarkar C, Tsai PC, Lee YC, Dye L, Mukherjee AB. Palmitoyl protein thioesterase-1 deficiency impairs synaptic vesicle recycling at nerve terminals, contributing to neuropathology in humans and mice. J Clin Invest 2008; 118: 3075–3086
   PubMed Web of Science ®Google Scholar
• Vesa J, Hellsten E, Verkruyse LA, Camp LA, Rapola J, Santavuori P, Hofmann SL, Peltonen L. Mutations in the palmitoyl protein thioesterase gene causing infantile neuronal ceroid lipofuscinosis. Nature 1995; 376: 584–587
   PubMed Web of Science ®Google Scholar
• Soyombo AA, Hofmann SL. Molecular cloning and expression of palmitoyl-protein thioesterase 2 (PPT2), a homolog of lysosomal palmitoyl-protein thioesterase with a distinct substrate specificity. J Biol Chem 1997; 272: 27456–27463
   PubMed Web of Science ®Google Scholar
• Gupta P, Soyombo AA, Atashband A, Wisniewski KE, Shelton JM, Richardson JA, Hammer RE, Hofmann SL. Disruption of PPT1 or PPT2 causes neuronal ceroid lipofuscinosis in knockout mice. Proc Natl Acad Sci USA 2001; 98: 13566–13571
   PubMed Web of Science ®Google Scholar
• Veit M, Schmidt MFG. Enzymatic depalmitoylation of viral glycoproteins with acyl-protein thioesterase 1 in vitro. Virology 2001; 288: 89–95
   PubMed Web of Science ®Google Scholar
• Fukata Y, Iwanaga T, Fukata M. Systematic screening for palmitoyl transferase activity of the DHHC protein family in mammalian cells. Methods 2006; 40: 177–182
   PubMed Web of Science ®Google Scholar
• Tsutsumi R, Fukata Y, Fukata M. Discovery of protein-palmitoylating enzymes. Pflugers Arch – Eur J Physiol 2008; 456: 1199–1206
   PubMed Web of Science ®Google Scholar
• Fernández-Hernando C, Fukata M, Bernatchez PN, Fukata Y, Lin MI, Bredt DS, Sessa WC. Identification of Golgi-localized acyl transferases that palmitoylate and regulate endothelial nitric oxide synthase. J Cell Biol 2006; 174: 369–377
   PubMed Web of Science ®Google Scholar
• Fang C, Deng L, Keller CA, Fukata M, Fukata Y, Chen G, Lüscher B. GODZ-mediated palmitoylation of GABA(A) receptors is required for normal assembly and function of GABAergic inhibitory synapses. J Neurosci 2006; 26: 12758–12768
   PubMed Web of Science ®Google Scholar
• Drisdel RC, Green WN. Labeling and quantifying sites of protein palmitoylation. Biotechniques 2004; 36: 276–285
   PubMed Web of Science ®Google Scholar
• Kümmel 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 USA 2006; 103: 12701–12706
   PubMed Web of Science ®Google Scholar
• Zhang J, Planey SL, Ceballos C, Stevens SM, Jr, Keay SK, Zacharias DA. Identification of CKAP4/p63 as a major substrate of the palmitoyl acyltransferase DHHC2, a putative tumor suppressor, using a novel proteomics method. Mol Cell Proteomics 2008; 7: 1378–1388
   PubMed Web of Science ®Google Scholar
• Sharma C, Yang XH, Hemler ME. DHHC2 affects palmitoylation, stability, and functions of tetraspanins CD9 and CD151. Mol Biol Cell 2008; 19: 3415–3425
   PubMed Web of Science ®Google Scholar
• Ohno Y, Kihara A, Sano T, Igarashi Y. Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim Biophys Acta 2006; 1761: 474–483
   PubMed Web of Science ®Google Scholar
• Stowers RS, Isacoff EY. Drosophila huntingtin-interacting protein 14 is a presynaptic protein required for photoreceptor synaptic transmission and expression of the palmitoylated proteins synaptosome-associated protein 25 and cysteine string protein. Neuroscience 2007; 27: 12874–12883
   PubMedGoogle Scholar
• Mukai J, Liu H, Burt RA, Swor DE, Lai WS, Karayiorgou M, Gogos JA. Evidence that the gene encoding ZDHHC8 contributes to the risk of schizophrenia. Nat Genet 2004; 36: 725–731
   PubMed Web of Science ®Google Scholar
• Yanai A, Huang K, Kang R, Singaraja RR, Arstikaitis P, Gan L, Orban PC, Mullard A, Cowan CM, Raymond LA, Drisdel RC, Green WN, Ravikumar B, Rubinsztein DC, El-Husseini A, Hayden MR. Palmitoylation of huntingtin by HIP14 is essential for its trafficking and function. Nat Neurosci 2006; 9: 824–831
   PubMed Web of Science ®Google Scholar
• Ohyama T, Verstreken P, Ly CV, Rosenmund T, Rajan A, Tien AC, Haueter C, Schulze KL, Bellen HJ. Huntingtin-interacting protein 14, a palmitoyl transferase required for exocytosis and targeting of CSP to synaptic vesicles. J Cell Biol 2007; 179: 1481–1496
   PubMed Web of Science ®Google Scholar
• Greaves J, Salaun C, Fukata Y, Fukata M, Chamberlain LH. Palmitoylation and membrane interactions of the neuroprotective chaperone cysteine-string protein. J Biol Chem 2008; 283: 25014–25026
   PubMed Web of Science ®Google Scholar
• Matakatsu H, Blair SS. The DHHC palmitoyltransferase approximated regulates Fat signaling and Dachs localization and activity. Curr Biol 2008; 18: 1390–1395
   PubMedGoogle Scholar
• El-Husseini Ael-D, Bredt DS. Protein palmitoylation: a regulator of neuronal development and function. Nat Rev Neurosci 2002; 3: 791–802
   PubMed Web of Science ®Google Scholar
• El-Husseini Ael-D, Schnell E, Dakoji S, Sweeney N, Zhou Q, Prange O, Gauthier-Campbell C, Aguilera-Moreno A, Nicoll RA, Bredt DS. Synaptic strength regulated by palmitate cycling on PSD-95. Cell 2002; 108: 849–863
   PubMed Web of Science ®Google Scholar
• Oyama T, Miyoshi Y, Koyama K, Nakagawa H, Yamori T, Ito T, Matsuda H, Arakawa H, Nakamura Y. Isolation of a novel gene on 8p21.3-22 whose expression is reduced significantly in human colorectal cancers with liver metastasis. Genes Chromosomes Cancer. 2000; 29: 9–15
   PubMed Web of Science ®Google Scholar
• Raymond FL, Tarpey PS, Edkins S, Tofts C, O'Meara S, Teague J, Butler A, Stevens C, Barthorpe S, Buck G, Cole J, Dicks E, Gray K, Halliday K, Hills K, Hinton J, Jones D, Menzies A, Perry J, Raine K, Shepherd R, Small A, Varian J, Widaa S, Mallya U, Moon J, Luo Y, Shaw M, Boyle J, Kerr B, Turner G, Quarrell O, Cole T, Easton DF, Wooster R, Bobrow M, Schwartz CE, Gecz J, Stratton MR, Futreal PA. Mutations in ZDHHC9, which encodes a palmitoyltransferase of N-RAS and H-RAS, cause X-linked mental retardation associated with a Marfanoid habitus. Am J Hum Genet 2007; 80: 982–987
   PubMed Web of Science ®Google Scholar
• Mansilla F, Birkenkamp-Demtroder K, Kruhøffer M, Sørensen FB, Andersen CL, Laiho P, Aaltonen LA, Verspaget HW, Orntoft TF. Differential expression of DHHC9 in microsatellite stable and instable human colorectal cancer subgroups. Br J Cancer 2007; 96: 1896–1903
   PubMed Web of Science ®Google Scholar
• Yamamoto Y, Chochi Y, Matsuyama H, Eguchi S, Kawauchi S, Furuya T, Oga A, Kang JJ, Naito K, Sasaki K. Gain of 5p15.33 is associated with progression of bladder cancer. Oncology 2007; 72: 132–138
   PubMed Web of Science ®Google Scholar
• Mansouri MR, Marklund L, Gustavsson P, Davey E, Carlsson B, Larsson C, White I, Gustavson KH, Dahl N. Loss of ZDHHC15 expression in a woman with a balanced translocation t(X;15)(q13.3;cen) and severe mental retardation. Eur J Hum Genet 2005; 13: 970–977
   PubMed Web of Science ®Google Scholar
• Wedegaertner PB, Bourne HR. Activation and depalmitoylation of Gs alpha. Cell 1994; 77: 1063–1070
   PubMed Web of Science ®Google Scholar
• Ponimaskin E, Dityateva G, Ruonala MO, Fukata M, Fukata Y, Kobe F, Wouters FS, Delling M, Bredt DS, Schachner M, Dityatev A. Fibroblast growth factor-regulated palmitoylation of the neural cell adhesion molecule determines neuronal morphogenesis. J Neurosci 2008; 28: 8897–8907
   PubMed Web of Science ®Google Scholar