Palmitoylation and depalmitoylation defects

Journal of Inherited Metabolic Disease

Volumn 38, Issue 1, 2015, Pages 179-186

  Hornemann, Thorsten ^a,b  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; CARBON; PALMITIC ACID DERIVATIVE; PALMITOYL COENZYME A HYDROLASE;

ALZHEIMER DISEASE; ANIMAL; CHEMISTRY; GENETICS; GOLTZ SYNDROME; HUMAN; HUNTINGTON CHOREA; METABOLISM; NERVE CELL; NEURONAL CEROID LIPOFUSCINOSIS; SCHIZOPHRENIA;

ACYLTRANSFERASES; ALZHEIMER DISEASE; ANIMALS; CARBON; FOCAL DERMAL HYPOPLASIA; HUMANS; HUNTINGTON DISEASE; NEURONAL CEROID-LIPOFUSCINOSES; NEURONS; PALMITIC ACIDS; PALMITOYL-COA HYDROLASE; SCHIZOPHRENIA;

EID: 84934293835     PISSN: 01418955     EISSN: 15732665     Source Type: Journal    
DOI: 10.1007/s10545-014-9753-0     Document Type: Review

References (105)

1. Arstikaitis P, Gauthier-Campbell C, Carolina Gutierrez Herrera R et al (2008) Paralemmin-1, a modulator of filopodia induction is required for spine maturation. Mol Biol Cell 19(5):2026–2038
2. Barrott JJ, Cash GM, Smith AP, Barrow JR, Murtaugh LC (2011) Deletion of mouse Porcn blocks Wnt ligand secretion and reveals an ectodermal etiology of human focal dermal hypoplasia/Goltz syndrome. Proc Natl Acad Sci U S A 108(31):12752–12757
3. Bartels DJ, Mitchell DA, Dong X, Deschenes RJ (1999) Erf2, a novel gene product that affects the localization and palmitoylation of Ras2 in Saccharomyces cerevisiae. Mol Cell Biol 19(10):6775–6787
4. Bellizzi JJ 3rd, Widom J, Kemp C et al (2000) The crystal structure of palmitoyl protein thioesterase 1 and the molecular basis of infantile neuronal ceroid lipofuscinosis. Proc Natl Acad Sci U S A 97(9):4573–4578
5. Benjannet S, Elagoz A, Wickham L et al (2001) Post-translational processing of beta-secretase (beta-amyloid-converting enzyme) and its ectodomain shedding. The pro- and transmembrane/cytosolic domains affect its cellular activity and amyloid-beta production. J Biol Chem 276(14):10879–10887
6. Biechele S, Cox BJ, Rossant J (2011) Porcupine homolog is required for canonical Wnt signaling and gastrulation in mouse embryos. Dev Biol 355(2):275–285
7. Brown DA (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology 21:430–439
8. Callier P, Calvel P, Matevossian A et al (2014) Loss of function mutation in the palmitoyl-transferase HHAT leads to syndromic 46, XY disorder of sex development by impeding Hedgehog protein palmitoylation and signaling. PLoS Genet 10(5):e1004340
9. Cattaneo E, Zuccato C, Tartari M (2005) Normal huntingtin function: an alternative approach to Huntington’s disease. Nat Rev Neurosci 6(12):919–930
10. Charollais J, Van Der Goot FG (2009) Palmitoylation of membrane proteins (Review). Mol Membr Biol 26(1):55–66
11. Chen MH, Li YJ, Kawakami T, Xu SM, Chuang PT (2004a) Palmitoylation is required for the production of a soluble multimeric Hedgehog protein complex and long-range signaling in vertebrates. Genes Dev 18(6):641–659
12. Chen WY, Shi YY, Zheng YL et al (2004b) Case–control study and transmission disequilibrium test provide consistent evidence for association between schizophrenia and genetic variation in the 22q11 gene ZDHHC8. Hum Mol Genet 13(23):2991–2995
13. Cho S, Dawson G (2000) Palmitoyl protein thioesterase 1 protects against apoptosis mediated by Ras-Akt-caspase pathway in neuroblastoma cells. J Neurochem 74(4):1478–1488
14. Cho S, Dawson PE, Dawson G (2000) Antisense palmitoyl protein thioesterase 1 (PPT1) treatment inhibits PPT1 activity and increases cell death in LA-N-5 neuroblastoma cells. J Neurosci Res 62(2):234–240
15. Conibear E, Davis NG (2010) Palmitoylation and depalmitoylation dynamics at a glance. J Cell Sci 123(Pt 23):4007–4010
16. Demily C, Legallic S, Bou J et al (2007) ZDHHC8 single nucleotide polymorphism rs175174 is not associated with psychiatric features of the 22q11 deletion syndrome or schizophrenia. Psychiatr Genet 17(5):311–312
17. Doubravska L, Krausova M, Gradl D et al (2011) Fatty acid modification of Wnt1 and Wnt3a at serine is prerequisite for lipidation at cysteine and is essential for Wnt signalling. Cell Signal 23(5):837–848
18. Ducker CE, Stettler EM, French KJ, Upson JJ, Smith CD (2004) Huntingtin interacting protein 14 is an oncogenic human protein: palmitoyl acyltransferase. Oncogene 23(57):9230–9237
19. Duncan JA, Gilman AG (1998) A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21 (RAS). J Biol Chem 273(25):15830–15837
20. El-Husseini AE, Bredt DS (2002) Protein palmitoylation: a regulator of neuronal development and function. Nat Rev Neurosci 3(10):791–802
21. El-Husseini AE, Craven SE, Chetkovich DM et al (2000) Dual palmitoylation of PSD-95 mediates its vesiculotubular sorting, postsynaptic targeting, and ion channel clustering. J Cell Biol 148(1):159–172
22. El-Husseini AE, Schnell E, Dakoji S et al (2002) Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108(6):849–863
23. Fukata Y, Fukata M (2010) Protein palmitoylation in neuronal development and synaptic plasticity. Nat Rev Neurosci 11(3):161–175
24. Fukata M, Fukata Y, Adesnik H, Nicoll RA, Bredt DS (2004) Identification of PSD-95 palmitoylating enzymes. Neuron 44(6):987–996
25. Galli LM, Barnes TL, Secrest SS, Kadowaki T, Burrus LW (2007) Porcupine-mediated lipid-modification regulates the activity and distribution of Wnt proteins in the chick neural tube. Development 134(18):3339–3348
26. Gauthier-Campbell C, Bredt DS, Murphy TH AEE-H (2004) Regulation of dendritic branching and filopodia formation in hippocampal neurons by specific acylated protein motifs. Mol Biol Cell 15(5):2205–2217
27. Glaser B, Schumacher J, Williams HJ et al (2005) No association between the putative functional ZDHHC8 single nucleotide polymorphism rs175174 and schizophrenia in large European samples. Biol Psychiatry 58(1):78–80
28. Glaser B, Moskvina V, Kirov G et al (2006) Analysis of ProDH, COMT and ZDHHC8 risk variants does not support individual or interactive effects on schizophrenia susceptibility. Schizophr Res 87(1–3):21–27
29. Greaves J, Chamberlain LH (2011) DHHC palmitoyl transferases: substrate interactions and (patho) physiology. Trends Biochem Sci 36(5):245–253
30. Greaves J, Prescott GR, Gorleku OA, Chamberlain LH (2009) The fat controller: roles of palmitoylation in intracellular protein trafficking and targeting to membrane microdomains (Review). Mol Membr Biol 26(1):67–79
31. Greaves J, Gorleku OA, Salaun C, Chamberlain LH (2010) Palmitoylation of the SNAP25 protein family: specificity and regulation by DHHC palmitoyl transferases. J Biol Chem 285(32):24629–24638
32. Gupta P, Soyombo AA, Shelton JM et al (2003) Disruption of PPT2 in mice causes an unusual lysosomal storage disorder with neurovisceral features. Proc Natl Acad Sci U S A 100(21):12325–12330
33. Haltia M (2006) The neuronal ceroid-lipofuscinoses: from past to present. Bba-Mol Basis Dis 1762(10):850–856
34. Hellsten E, Vesa J, Olkkonen VM, Jalanko A, Peltonen L (1996) Human palmitoyl protein thioesterase: evidence for lysosomal targeting of the enzyme and disturbed cellular routing in infantile neuronal ceroid lipofuscinosis. The EMBO j 15(19):5240–5245
35. Hofmann K (2000) A superfamily of membrane-bound O-acyltransferases with implications for wnt signaling. Trends Biochem Sci 25(3):111–112
36. Huang K, El-Husseini AE (2005) Modulation of neuronal protein trafficking and function by palmitoylation. Curr Opin Neurobiol 15(5):527–535
37. Huang K, Yanai A, Kang R et al (2004) Huntingtin-interacting protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins. Neuron 44(6):977–986
38. Huang K, Sanders S, Singaraja R et al (2009) Neuronal palmitoyl acyl transferases exhibit distinct substrate specificity. FASEB j: off pub of the Fed of Am Soc for Exp Biol 23(8):2605–2615
39. Kalchman MA, Graham RK, Xia G et al (1996) Huntingtin is ubiquitinated and interacts with a specific ubiquitin-conjugating enzyme. J Biol Chem 271(32):19385–19394
40. Kang R, Wan J, Arstikaitis P et al (2008) Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456(7224):904–909
41. Kato H, Allen ND, Emson PC, Kiyama H (2000) GAP-43 N-terminal translocation signal targets beta-galactosidase to developing axons in a pan-neuronal transgenic mouse line. Brain Res Dev Brain Res 121(1):109–112
42. Kim E, Sheng M (2004) PDZ domain proteins of synapses. Nat Rev Neurosci 5(10):771–781
43. Kutzleb C, Sanders G, Yamamoto R et al (1998) Paralemmin, a prenyl-palmitoyl-anchored phosphoprotein abundant in neurons and implicated in plasma membrane dynamics and cell process formation. J Cell Biol 143(3):795–813
44. Laux T, Fukami K, Thelen M, Golub T, Frey D, Caroni P (2000) GAP43, MARCKS, and CAP23 modulate PI (4,5) P (2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 149(7):1455–1472
45. Levental I, Grzybek M, Simons K (2010) Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49(30):6305–6316
46. Levin SW, Baker EH, Zein WM et al (2014) Oral cysteamine bitartrate and N-acetylcysteine for patients with infantile neuronal ceroid lipofuscinosis: a pilot study. Lancet Neurol doi:10.1016/S1474-4422(14)70142-5
47. Linder ME, Deschenes RJ (2007) Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol 8(1):74–84
48. Liu H, Abecasis GR, Heath SC et al (2002) Genetic variation in the 22q11 locus and susceptibility to schizophrenia. Proc Natl Acad Sci U S A 99(26):16859–16864
49. Lobo S, Greentree WK, Linder ME, Deschenes RJ (2002) Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J Biol Chem 277(43):41268–41273
50. Lyly A, Marjavaara SK, Kyttala A et al (2008) Deficiency of the INCL protein Ppt1 results in changes in ectopic F1-ATP synthase and altered cholesterol metabolism. Hum Mol Genet 17(10):1406–1417
51. Mansilla F, Birkenkamp-Demtroder K, Kruhoffer M et al (2007) Differential expression of DHHC9 in microsatellite stable and instable human colorectal cancer subgroups. Br J Cancer 96(12):1896–1903
52. Mansouri MR, Marklund L, Gustavsson P et al (2005) Loss of ZDHHC15 expression in a woman with a balanced translocation t (X;15) (q13.3;cen) and severe mental retardation. EJHG 13(8):970–977
53. Mill P, Lee AW, Fukata Y et al (2009) Palmitoylation regulates epidermal homeostasis and hair follicle differentiation. PLoS Genet 5(11):e1000748
54. Mitchell DA, Vasudevan A, Linder ME, Deschenes RJ (2006) Protein palmitoylation by a family of DHHC protein S-acyltransferases. J Lipid Res 47(6):1118–1127
55. Mitchison HM, Hofmann SL, Becerra CH et al (1998) Mutations in the palmitoyl-protein thioesterase gene (PPT; CLN1) causing juvenile neuronal ceroid lipofuscinosis with granular osmiophilic deposits. Hum Mol Genet 7(2):291–297
56. Mizumaru C, Saito Y, Ishikawa T et al (2009) Suppression of APP-containing vesicle trafficking and production of beta-amyloid by AID/DHHC-12 protein. J Neurochem 111(5):1213–1224
57. Mukai J, Liu H, Burt RA et al (2004) Evidence that the gene encoding ZDHHC8 contributes to the risk of schizophrenia. Nat Genet 36(7):725–731
58. Mukai J, Dhilla A, Drew LJ et al (2008) Palmitoylation-dependent neurodevelopmental deficits in a mouse model of 22q11 microdeletion. Nat Neurosci 11(11):1302–1310
59. Nadolski MJ, Linder ME (2007) Protein lipidation. FEBS J 274(20):5202–5210
60. Nasir J, Floresco SB, O’Kusky JR et al (1995) Targeted disruption of the Huntington’s disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell 81(5):811–823
61. Ohno Y, Kihara A, Sano T, Igarashi Y (2006) Intracellular localization and tissue-specific distribution of human and yeast DHHC cysteine-rich domain-containing proteins. Biochim Biophys Acta 1761(4):474–483
62. Otani K, Ujike H, Tanaka Y et al (2005) The ZDHHC8 gene did not associate with bipolar disorder or schizophrenia. Neurosci Lett 390(3):166–170
63. Oyama T, Miyoshi Y, Koyama K et al (2000) Isolation of a novel gene on 8p21.3-22 whose expression is reduced significantly in human colorectal cancers with liver metastasis. Genes Chromosomes Cancer 29(1):9–15
64. Polakis P (2007) The many ways of Wnt in cancer. Curr Opin Genet Dev 17(1):45–51
65. Politis EG, Roth AF, Davis NG (2005) Transmembrane topology of the protein palmitoyl transferase Akr1. J Biol Chem 280(11):10156–10163
66. Prescott GR, Gorleku OA, Greaves J, Chamberlain LH (2009) Palmitoylation of the synaptic vesicle fusion machinery. J Neurochem 110(4):1135–1149
67. Putilina T, Wong P, Gentleman S (1999) The DHHC domain: a new highly conserved cysteine-rich motif. Mol Cell Biochem 195(1–2):219–226
68. Raymond FL, Tarpey PS, Edkins S et al (2007) Mutations in ZDHHC9, which encodes a palmitoyltransferase of NRAS and HRAS, cause X-linked mental retardation associated with a Marfanoid habitus. Am J Hum Genet 80(5):982–987
69. Resh MD (2006) Palmitoylation of ligands, receptors, and intracellular signaling molecules. Science’s STKE: signal transduction knowledge environment 2006 (359): re14
70. Rocks O, Peyker A, Bastiaens PI (2006) Spatio-temporal segregation of Ras signals: one ship, three anchors, many harbors. Curr Opin Cell Biol 18(4):351–357
71. Rocks O, Gerauer M, Vartak N et al (2010) The palmitoylation machinery is a spatially organizing system for peripheral membrane proteins. Cell 141(3):458–471
72. Roos RA (2010) Huntington’s disease: a clinical review. Orphanet j of rare dis 5(1):40
73. Roth AF, Feng Y, Chen L, Davis NG (2002) The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J Cell Biol 159(1):23–28
74. Rusch M, Zimmermann TJ, Burger M et al (2011) 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 50(42):9838–9842
75. Saito S, Ikeda M, Iwata N et al (2005) No association was found between a functional SNP in ZDHHC8 and schizophrenia in a Japanese case–control population. Neurosci Lett 374(1):21–24
76. Salaun C, Greaves J, Chamberlain LH (2010) The intracellular dynamic of protein palmitoylation. J Cell Biol 191(7):1229–1238
77. Saleem AN, Chen YH, Baek HJ et al (2010) Mice with alopecia, osteoporosis, and systemic amyloidosis due to mutation in Zdhhc13, a gene coding for palmitoyl acyltransferase. PLoS Genet 6(6):e1000985
78. Santavuori P (2011) The Neuronal ceroid lipofuscinoses, Mole, Sara/ Williams, Ruth/ Goebel, Hans Oxford University Press ELT
79. Schlesinger MJ, Magee AI, Schmidt MF (1980) Fatty acid acylation of proteins in cultured cells. J Biol Chem 255(21):10021–10024
80. Schmidt MF, Schlesinger MJ (1979) Fatty acid binding to vesicular stomatitis virus glycoprotein: a new type of post-translational modification of the viral glycoprotein. Cell 17(4):813–819
81. Shin HD, Park BL, Bae JS et al (2010) Association of ZDHHC8 polymorphisms with smooth pursuit eye movement abnormality. Am j of med genet Part B, Neuropsychiatr genet: the official publication of the Int Soc of Psychiatr Genet 153B(6):1167–1172
82. Shindou H, Shimizu T (2009) Acyl-CoA:lysophospholipid acyltransferases. J Biol Chem 284(1):1–5
83. Singaraja RR, Hadano S, Metzler M et al (2002) HIP14, a novel ankyrin domain-containing protein, links huntingtin to intracellular trafficking and endocytosis. Hum Mol Genet 11(23):2815–2828
84. Singaraja RR, Huang K, Sanders SS et al (2011) Altered palmitoylation and neuropathological deficits in mice lacking HIP14. Hum Mol Genet 20(20):3899–3909
85. Slow EJ, van Raamsdonk J, Rogers D et al (2003) Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum Mol Genet 12(13):1555–1567
86. Soyombo AA, Hofmann SL (1997) 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 272(43):27456–27463
87. Sturrock A, Leavitt BR (2010) The clinical and genetic features of Huntington disease. J Geriatr Psychiatry Neurol 23(4):243–259
88. Takada R, Satomi Y, Kurata T et al (2006) Monounsaturated fatty acid modification of Wnt protein: its role in Wnt secretion. Dev Cell 11(6):791–801
89. Tian L, McClafferty H, Jeffries O, Shipston MJ (2010) Multiple palmitoyltransferases are required for palmitoylation-dependent regulation of large conductance calcium- and voltage-activated potassium channels. J Biol Chem 285(31):23954–23962
90. Tomatis VM, Trenchi A, Gomez GA, Daniotti JL (2010) Acyl-protein thioesterase 2 catalyzes the deacylation of peripheral membrane-associated GAP-43. PLoS ONE 5(11):e15045
91. Tyynela J, Palmer DN, Baumann M, Haltia M (1993) Storage of saposins A and D in infantile neuronal ceroid-lipofuscinosis. FEBS Lett 330(1):8–12
92. Veit M, Serebryakova MV, Kordyukova LV (2013) Palmitoylation of influenza virus proteins. Biochem Soc Trans 41(1):50–55
93. Verkruyse LA, Hofmann SL (1996) Lysosomal targeting of palmitoyl-protein thioesterase. J Biol Chem 271(26):15831–15836
94. Vesa J, Hellsten E, Verkruyse LA et al (1995) Mutations in the palmitoyl protein thioesterase gene causing infantile neuronal ceroid lipofuscinosis. Nature 376(6541):584–587
95. Vetrivel KS, Meckler X, Chen Y et al (2009) Alzheimer disease Abeta production in the absence of S-palmitoylation-dependent targeting of BACE1 to lipid rafts. J Biol Chem 284(6):3793–3803
96. Wang X, Reid Sutton V, Omar Peraza-Llanes J et al (2007) Mutations in X-linked PORCN, a putative regulator of Wnt signaling, cause focal dermal hypoplasia. Nat Genet 39(7):836–838
97. Warby SC, Visscher H, Collins JA et al (2011) HTT haplotypes contribute to differences in Huntington disease prevalence between Europe and East Asia. EJHG 19(5):561–566
98. Willert K, Brown JD, Danenberg E et al (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423(6938):448–452
99. Xu M, St Clair D, He L (2010) Testing for genetic association between the ZDHHC8 gene locus and susceptibility to schizophrenia: an integrated analysis of multiple datasets. Am j of med genet Part B, Neuropsychiatr genet: the official publication of the Int Soc of Psychiatr Genet 153B(7):1266–1275
100. Yamamoto Y, Chochi Y, Matsuyama H et al (2007) Gain of 5p15.33 is associated with progression of bladder cancer. Oncology 72(1–2):132–138
101. Yanai A, Huang K, Kang R et al (2006) Palmitoylation of huntingtin by HIP14 is essential for its trafficking and function. Nat Neurosci 9(6):824–831
102. Yeh DC, Duncan JA, Yamashita S, Michel T (1999) Depalmitoylation of endothelial nitric-oxide synthase by acyl-protein thioesterase 1 is potentiated by Ca (2+)-calmodulin. J Biol Chem 274(46):33148–33154
103. Zeidman R, Jackson CS, Magee AI (2009) Protein acyl thioesterases (Review). Mol Membr Biol 26(1):32–41
104. Zhang Z, Lee YC, Kim SJ et al (2006) Palmitoyl-protein thioesterase-1 deficiency mediates the activation of the unfolded protein response and neuronal apoptosis in INCL. Hum Mol Genet 15(2):337–346
105. Zhang J, Planey SL, Ceballos C, Stevens SM Jr, Keay SK, Zacharias DA (2008) Identification of CKAP4/p63 as a major substrate of the palmitoyl acyltransferase DHHC2, a putative tumor suppressor, using a novel proteomics method. Mol & cel proteomics: MCP 7(7):1378–1388