A systematic analysis of protein palmitoylation in Caenorhabditis elegans

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Edmonds, Matthew J ^a   Morgan, Alan ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

DHHC; Neuronal ceroid lipofuscinosis; Palmitoyl acyl transferase; Palmitoyl protein thioesterase

Indexed keywords

ACYLTRANSFERASE; PALMITOYL ACYL TRANSFERASE; PALMITOYL PROTEIN THIOESTERASE; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BODY SIZE; CAENORHABDITIS ELEGANS; CELL FUNCTION; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ANALYSIS; GENOME ANALYSIS; GENOMICS; IN VIVO STUDY; LONGEVITY; MOTONEURON; MUTANT; NONHUMAN; PALMITOYLATION; PHENOTYPE; PLASMID; PROTEIN DOMAIN; PROTEIN PALMITOYLATION; PROTEIN PROCESSING; RNA INTERFERENCE; SENSORY NERVE CELL; SEQUENCE HOMOLOGY; AGING; AMINO ACID SEQUENCE; ANIMAL; BIOLOGY; CHEMISTRY; DEFICIENCY; GENE SILENCING; GENETICS; HUMAN; LIPOYLATION; LOCOMOTION; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; SEQUENCE ANALYSIS;

CAENORHABDITIS ELEGANS;

ACYLTRANSFERASES; AGING; AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; COMPUTATIONAL BIOLOGY; GENE KNOCKDOWN TECHNIQUES; HUMANS; LIPOYLATION; LOCOMOTION; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA INTERFERENCE; SEQUENCE ANALYSIS;

EID: 84907969440     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-841     Document Type: Article

References (73)

1. 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. 10.1194/jlr.R600007-JLR200, 16582420.
2. Camp LA, Verkruyse LA, Afendis SJ, Slaughter CA, Hofmann SL. Molecular cloning and expression of palmitoyl-protein thioesterase. J Biol Chem 1994, 269:23212-23219.
3. 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. 10.1074/jbc.272.43.27456, 9341199.
4. Fukata Y, Fukata M. Protein palmitoylation in neuronal development and synaptic plasticity. Nat Rev Neurosci 2010, 11:161-175.
5. Greaves J, Chamberlain LH. DHHC palmitoyl transferases: substrate interactions and (patho)physiology. Trends Biochem Sci 2011, 36:245-253. 10.1016/j.tibs.2011.01.003, 21388813.
6. Korycka J, Lach A, Heger E, Boguslawska DM, Wolny M, Toporkiewicz M, Augoff K, Korzeniewski J, Sikorski AF. Human DHHC proteins: a spotlight on the hidden player of palmitoylation. Eur J Cell Biol 2012, 91:107-117. 10.1016/j.ejcb.2011.09.013, 22178113.
7. Omary MB, Trowbridge IS. Covalent binding of fatty acid to the transferrin receptor in cultured human cells. J Biol Chem 1981, 256:4715-4718.
8. Bohm S, Frishman D, Mewes HW. Variations of the C2H2 zinc finger motif in the yeast genome and classification of yeast zinc finger proteins. Nucleic Acids Res 1997, 25:2464-2469. 10.1093/nar/25.12.2464, 146766, 9171100.
9. Fukata M, Fukata Y, Adesnik H, Nicoll RA, Bredt DS. Identification of PSD-95 palmitoylating enzymes. Neuron 2004, 44:987-996. 10.1016/j.neuron.2004.12.005, 15603741.
10. 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. 10.1083/jcb.200206120, 2173492, 12370247.
11. 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 (Austin) 2008, 2:198-214. 10.4161/fly.6621, 2898910, 18719403.
12. Mitchell DA, Mitchell G, Ling Y, Budde C, Deschenes RJ. Mutational analysis of Saccharomyces cerevisiae Erf2 reveals a two-step reaction mechanism for protein palmitoylation by DHHC enzymes. J Biol Chem 2010, 285:38104-38114. 10.1074/jbc.M110.169102, 2992244, 20851885.
13. Ohno Y, Kashio A, Ogata R, Ishitomi A, Yamazaki Y, Kihara A. Analysis of substrate specificity of human DHHC protein acyltransferases using a yeast expression system. Mol Biol Cell 2012, 23:4543-4551. 10.1091/mbc.E12-05-0336, 3510016, 23034182.
14. Duncan JA, Gilman AG. A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21(RAS). J Biol Chem 1998, 273:15830-15837. 10.1074/jbc.273.25.15830, 9624183.
15. 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.
16. Verkruyse LA, Hofmann SL. Lysosomal targeting of palmitoyl-protein thioesterase. J Biol Chem 1996, 271:15831-15836. 10.1074/jbc.271.26.15831, 8663305.
17. Lehtovirta M, Kyttala A, Eskelinen EL, Hess M, Heinonen O, Jalanko A. Palmitoyl protein thioesterase (PPT) localizes into synaptosomes and synaptic vesicles in neurons: implications for infantile neuronal ceroid lipofuscinosis (INCL). Hum Mol Genet 2001, 10:69-75. 10.1093/hmg/10.1.69, 11136716.
18. Calero G, Gupta P, Nonato MC, Tandel S, Biehl ER, Hofmann SL, Clardy J. The crystal structure of palmitoyl protein thioesterase-2 (PPT2) reveals the basis for divergent substrate specificities of the two lysosomal thioesterases, PPT1 and PPT2. J Biol Chem 2003, 278:37957-37964. 10.1074/jbc.M301225200, 12855696.
19. Kang R, Wan J, Arstikaitis P, Takahashi H, Huang K, Bailey AO, Thompson JX, Roth AF, Drisdel RC, Mastro R, Green WN, Yates JR, Davis NG, El-Husseini A. Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 2008, 456:904-909. 10.1038/nature07605, 2610860, 19092927.
20. Roth AF, Wan J, Bailey AO, Sun B, Kuchar JA, Green WN, Phinney BS, Yates JR, Davis NG. Global analysis of protein palmitoylation in yeast. Cell 2006, 125:1003-1013. 10.1016/j.cell.2006.03.042, 2246083, 16751107.
21. Yang W, Di Vizio D, Kirchner M, Steen H, Freeman MR. Proteome scale characterization of human S-acylated proteins in lipid raft-enriched and non-raft membranes. Mol Cell Proteomics 2010, 9:54-70. 10.1074/mcp.M800448-MCP200, 2808267, 19801377.
22. Dowal L, Yang W, Freeman MR, Steen H, Flaumenhaft R. Proteomic analysis of palmitoylated platelet proteins. Blood 2011, 118:e62-73. 10.1182/blood-2011-05-353078, 3186346, 21813449.
23. Marin EP, Derakhshan B, Lam TT, Davalos A, Sessa WC. Endothelial cell palmitoylproteomic identifies novel lipid-modified targets and potential substrates for protein acyl transferases. Circ Res 2012, 110:1336-1344. 10.1161/CIRCRESAHA.112.269514, 3428238, 22496122.
24. Merrick BA, Dhungana S, Williams JG, Aloor JJ, Peddada S, Tomer KB, Fessler MB. Proteomic profiling of S-acylated macrophage proteins identifies a role for palmitoylation in mitochondrial targeting of phospholipid scramblase 3. Mol Cell Proteomics 2011, 10:M110 006007. 10.1074/mcp.M110.006007, 3205854, 21785166.
25. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2001, 2. RESEARCH0002. http://www.ncbi.nlm.nih.gov/pubmed.
26. Timmons L, Fire A. Specific interference by ingested dsRNA. Nature 1998, 395:854. 10.1038/27579, 9804418.
27. Gleason EJ, Lindsey WC, Kroft TL, Singson AW, L'Hernault SW. spe-10 encodes a DHHC-CRD zinc-finger membrane protein required for endoplasmic reticulum/Golgi membrane morphogenesis during Caenorhabditis elegans spermatogenesis. Genetics 2006, 172:145-158. 1456142, 16143610.
28. Shakes DC, Ward S. Mutations that disrupt the morphogenesis and localization of a sperm-specific organelle in Caenorhabditis elegans. Dev Biol 1989, 134:307-316. 10.1016/0012-1606(89)90103-6, 2744235.
29. Cypser JR, Johnson TE. The spe-10 mutant has longer life and increased stress resistance. Neurobiol Aging 1999, 20:503-512. 10.1016/S0197-4580(99)00085-8, 10638523.
30. Porter MY, Turmaine M, Mole SE. Identification and characterization of Caenorhabditis elegans palmitoyl protein thioesterase1. J Neurosci Res 2005, 79:836-848. 10.1002/jnr.20403, 15672447.
31. 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. 10.1038/376584a0, 7637805.
32. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94. 1213120, 4366476.
33. Chalfie M, Sulston J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 1981, 82:358-370. 10.1016/0012-1606(81)90459-0, 7227647.
34. Prescott GR, Gorleku OA, Greaves J, Chamberlain LH. Palmitoylation of the synaptic vesicle fusion machinery. J Neurochem 2009, 110:1135-1149. 10.1111/j.1471-4159.2009.06205.x, 19508429.
35. Kihara A, Kurotsu F, Sano T, Iwaki S, Igarashi Y. Long-chain base kinase Lcb4 Is anchored to the membrane through its palmitoylation by Akr1. Mol Cell Biol 2005, 25:9189-9197. 10.1128/MCB.25.21.9189-9197.2005, 1265802, 16227572.
36. Gonzalez Montoro A, Quiroga R, Maccioni HJ, Valdez Taubas J. A novel motif at the C-terminus of palmitoyltransferases is essential for Swf1 and Pfa3 function in vivo. Biochem J 2009, 419:301-308. 10.1042/BJ20080921, 19138168.
37. Huang K, Sanders S, Singaraja R, Orban P, Cijsouw T, Arstikaitis P, Yanai A, Hayden MR, El-Husseini A. Neuronal palmitoyl acyl transferases exhibit distinct substrate specificity. FASEB J 2009, 23:2605-2615. 10.1096/fj.08-127399, 2717768, 19299482.
38. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691. 10.1038/nature02026, 14562095.
39. Rual JF, Ceron J, Koreth J, Hao T, Nicot AS, Hirozane-Kishikawa T, Vandenhaute J, Orkin SH, Hill DE, van den Heuvel S, Vidal M. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 2004, 14:2162-2168. 10.1101/gr.2505604, 528933, 15489339.
40. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811. 10.1038/35888, 9486653.
41. Simmer F, Tijsterman M, Parrish S, Koushika SP, Nonet ML, Fire A, Ahringer J, Plasterk RH. Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr Biol 2002, 12:1317-1319. 10.1016/S0960-9822(02)01041-2, 12176360.
42. Brown AE, Yemini EI, Grundy LJ, Jucikas T, Schafer WR. A dictionary of behavioral motifs reveals clusters of genes affecting Caenorhabditis elegans locomotion. Proc Natl Acad Sci U S A 2013, 110:791-796. 10.1073/pnas.1211447110, 3545781, 23267063.
43. Yemini E, Jucikas T, Grundy LJ, Brown AE, Schafer WR. A database of Caenorhabditis elegans behavioral phenotypes. Nat Methods 2013, 10:877-879. 10.1038/nmeth.2560, 3962822, 23852451.
44. Johnson JR, Ferdek P, Lian LY, Barclay JW, Burgoyne RD, Morgan A. Binding of UNC-18 to the N-terminus of syntaxin is essential for neurotransmission in Caenorhabditis elegans. Biochem J 2009, 418:73-80. 10.1042/BJ20081956, 19032153.
45. Miller KG, Emerson MD, Rand JB. Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron 1999, 24:323-333. 10.1016/S0896-6273(00)80847-8, 10571227.
46. Rush DB, Leon RT, McCollum MH, Treu RW, Wei J. Palmitoylation and trafficking of GAD65 are impaired in a cellular model of Huntington's disease. Biochem J 2012, 442:39-48. 10.1042/BJ20110679, 22103299.
47. Velinov M, Dolzhanskaya N, Gonzalez M, Powell E, Konidari I, Hulme W, Staropoli JF, Xin W, Wen GY, Barone R, Coppel SH, Sims K, Brown WT, Zuchner S. Mutations in the gene DNAJC5 cause autosomal dominant Kufs disease in a proportion of cases: study of the Parry family and 8 other families. PLoS One 2012, 7:e29729. 10.1371/journal.pone.0029729, 3250487, 22235333.
48. Vetrivel KS, Meckler X, Chen Y, Nguyen PD, Seidah NG, Vassar R, Wong PC, Fukata M, Kounnas MZ, Thinakaran G. Alzheimer disease Abeta production in the absence of S-palmitoylation-dependent targeting of BACE1 to lipid rafts. J Biol Chem 2009, 284:3793-3803. 10.1074/jbc.M808920200, 2635050, 19074428.
49. Das AK, Lu JY, Hofmann SL. Biochemical analysis of mutations in palmitoyl-protein thioesterase causing infantile and late-onset forms of neuronal ceroid lipofuscinosis. Hum Mol Genet 2001, 10:1431-1439. 10.1093/hmg/10.13.1431, 11440996.
50. Singaraja RR, Huang K, Sanders SS, Milnerwood AJ, Hines R, Lerch JP, Franciosi S, Drisdel RC, Vaid K, Young FB, Doty C, Wan J, Bissada N, Henkelman RM, Green WN, Davis NG, Raymond LA, Hayden MR. Altered palmitoylation and neuropathological deficits in mice lacking HIP14. Hum Mol Genet 2011, 20:3899-3909. 10.1093/hmg/ddr308, 3177655, 21775500.
51. Sutton LM, Sanders SS, Butland SL, Singaraja RR, Franciosi S, Southwell AL, Doty CN, Schmidt ME, Mui KK, Kovalik V, Young FB, Zhang W, Hayden MR. Hip14l-deficient mice develop neuropathological and behavioural features of Huntington disease. Hum Mol Genet 2013, 22:452-465. 10.1093/hmg/dds441, 23077216.
52. Gouda K, Matsunaga Y, Iwasaki T, Kawano T. An altered method of feeding RNAi that knocks down multiple genes simultaneously in the nematode Caenorhabditis elegans. Biosci Biotechnol Biochem 2010, 74:2361-2365. 10.1271/bbb.100579, 21071832.
53. Min K, Kang J, Lee J. A modified feeding RNAi method for simultaneous knock-down of more than one gene in Caenorhabditis elegans. Biotechniques 2010, 48:229-232. 10.2144/000113365, 20359305.
54. Lobo S, Greentree WK, Linder ME, Deschenes RJ. Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J Biol Chem 2002, 277:41268-41273. 10.1074/jbc.M206573200, 12193598.
55. Simmer F, Moorman C, van der Linden AM, Kuijk E, van den Berghe PV, Kamath RS, Fraser AG, Ahringer J, Plasterk RH. Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol 2003, 1:E12. 212692, 14551910.
56. Greaves J, Gorleku OA, Salaun C, Chamberlain LH. Palmitoylation of the SNAP25 protein family: specificity and regulation by DHHC palmitoyl transferases. J Biol Chem 2010, 285:24629-24638. 10.1074/jbc.M110.119289, 2915699, 20519516.
57. Hou H, John PAT, Meiringer C, Subramanian K, Ungermann C. Analysis of DHHC acyltransferases implies overlapping substrate specificity and a two-step reaction mechanism. Traffic 2009, 10:1061-1073. 10.1111/j.1600-0854.2009.00925.x, 19453970.
58. 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. J Neurosci 2007, 27:12874-12883. 10.1523/JNEUROSCI.2464-07.2007, 18032660.
59. 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. 10.1083/jcb.200710061, 2373489, 18158335.
60. Zinsmaier KE, Eberle KK, Buchner E, Walter N, Benzer S. Paralysis and early death in cysteine string protein mutants of Drosophila. Science 1994, 263:977-980. 10.1126/science.8310297, 8310297.
61. Kashyap SS, Johnson JR, McCue HV, Chen X, Edmonds MJ, Ayala M, Graham ME, Jenn RC, Barclay JW, Burgoyne RD, Morgan A. Caenorhabditis elegans dnj-14, the orthologue of the DNAJC5 gene mutated in adult onset neuronal ceroid lipofuscinosis, provides a new platform for neuroprotective drug screening and identifies a SIR-2.1-independent action of resveratrol. Hum Mol Genet 2014, in press.
62. Bellizzi JJ, Widom J, Kemp C, Lu JY, Das AK, Hofmann SL, Clardy J. The crystal structure of palmitoyl protein thioesterase 1 and the molecular basis of infantile neuronal ceroid lipofuscinosis. Proc Natl Acad Sci U S A 2000, 97:4573-4578. 10.1073/pnas.080508097, 18274, 10781062.
63. Devedjiev Y, Dauter Z, Kuznetsov SR, Jones TL, Derewenda ZS. Crystal structure of the human acyl protein thioesterase I from a single X-ray data set to 1.5 A. Structure 2000, 8:1137-1146. 10.1016/S0969-2126(00)00529-3, 11080636.
64. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934. 10.1126/science.1075762, 12471243.
65. Sacco F, Perfetto L, Castagnoli L, Cesareni G. The human phosphatase interactome: An intricate family portrait. FEBS Lett 2012, 586:2732-2739. 10.1016/j.febslet.2012.05.008, 3437441, 22626554.
66. Li W, Bengtson MH, Ulbrich A, Matsuda A, Reddy VA, Orth A, Chanda SK, Batalov S, Joazeiro CA. Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. PLoS One 2008, 3:e1487. 10.1371/journal.pone.0001487, 2198940, 18213395.
67. Clague MJ, Coulson JM, Urbe S. Cellular functions of the DUBs. J Cell Sci 2012, 125:277-286. 10.1242/jcs.090985, 22357969.
68. 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. 10.1074/jbc.M202505200, 12080046.
69. Dekker FJ, Rocks O, Vartak N, Menninger S, Hedberg C, Balamurugan R, Wetzel S, Renner S, Gerauer M, Scholermann B, Rusch M, Kramer JW, Rauh D, Coates GW, Brunsveld L, Bastiaens PI, Waldmann H. Small-molecule inhibition of APT1 affects Ras localization and signaling. Nat Chem Biol 2010, 6:449-456. 10.1038/nchembio.362, 20418879.
70. Tian L, McClafferty H, Knaus HG, Ruth P, Shipston MJ. Distinct acyl protein transferases and thioesterases control surface expression of calcium-activated potassium channels. J Biol Chem 2012, 287:14718-14725. 10.1074/jbc.M111.335547, 3340283, 22399288.
71. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 2007, 23:127-128. 10.1093/bioinformatics/btl529, 17050570.
72. Timmons L, Court DL, Fire A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 2001, 263:103-112. 10.1016/S0378-1119(00)00579-5, 11223248.
73. Yang JS, Nam HJ, Seo M, Han SK, Choi Y, Nam HG, Lee SJ, Kim S. OASIS: online application for the survival analysis of lifespan assays performed in aging research. PLoS One 2011, 6:e23525. 10.1371/journal.pone.0023525, 3156233, 21858155.