Modulation of neuronal protein trafficking and function by palmitoylation

Current Opinion in Neurobiology

Volumn 15, Issue 5, 2005, Pages 527-535

  Huang, Kun ^a   El Husseini, Alaa ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ALPHA SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; AMPA RECEPTOR; G PROTEIN COUPLED RECEPTOR; GLUTAMATE DECARBOXYLASE 65; NERVE PROTEIN; NEUROMODULIN; PALMITIC ACID; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN; SNARE PROTEIN; SYNAPTOBREVIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN; UNCLASSIFIED DRUG;

ACYLATION; CELL VACUOLE; LIPID METABOLISM; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMITTER RELEASE; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MODIFICATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

ANIMALS; HUMANS; NEURONS; PALMITATES; PROTEIN TRANSPORT;

EID: 25844522857     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2005.08.001     Document Type: Review

References (51)

1. M.D. Resh Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins Biochim Biophys Acta 1451 1999 1 16
2. J.E. Smotrys, and M.E. Linder Palmitoylation of intracellular signaling proteins: regulation and function Annu Rev Biochem 73 2004 559 587
3. R. Qanbar, and M. Bouvier Role of palmitoylation/depalmitoylation reactions in G-protein-coupled receptor function Pharmacol Ther 97 2003 1 33
4. Ael-D El-Husseini, and D.S. Bredt Protein palmitoylation: a regulator of neuronal development and function Nat Rev Neurosci 3 2002 791 802
5. S.M. Strittmatter, M. Igarashi, and M.C. Fishman GAP43 amino terminal peptides modulate growth cone morphology and neurite outgrowth.PG - 5503-13 J Neurosci 14 1994 5503 5513
6. C. Kutzleb, G. Sanders, R. Yamamoto, X. Wang, B. Lichte, E. Petrasch-Parwez, and M.W. Kilimann Paralemmin, a prenyl-palmitoyl-anchored phosphoprotein abundant in neurons and implicated in plasma membrane dynamics and cell process formation J Cell Biol 143 1998 795 813
7. C. Gauthier-Campbell, D.S. Bredt, T.H. Murphy, and AE-D. El-Husseini Regulation of dendritic branching and filopodia formation in hippocampal neurons by specific acylated protein motifs Mol Biol Cell 15 2004 2205 2217 The authors find that the specific palmitoylated protein motifs of GAP43 and paralemmin are sufficient to increase the number of filopodia and the branching of dendrites and axons in neurons. This effect is palmitoylation-dependent and requires the action of ARF6 and cdc-42, two GTPases that regulate bulk membrane cycling and actin dynamics.
8. D. Raucher, and M.P. Sheetz Cell spreading and lamellipodial extension rate is regulated by membrane tension J Cell Biol 148 2000 127 136
9. Z. Herincs, V. Corset, N. Cahuzac, C. Furne, V. Castellani, A.O. Hueber, and P. Mehlen DCC association with lipid rafts is required for netrin-1-mediated axon guidance J Cell Sci 118 2005 1687 1692
10. M.E. Hemler Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain Annu Rev Cell Dev Biol 19 2003 397 422
11. X. Yang, O.V. Kovalenko, W. Tang, C. Claas, C.S. Stipp, and M.E. Hemler Palmitoylation supports assembly and function of integrin-tetraspanin complexes J Cell Biol 167 2004 1231 1240
12. E. Kim, and M. Sheng PDZ domain proteins of synapses Nat Rev Neurosci 5 2004 771 781
13. S.E. Craven, A.E. El-Husseini, and D.S. Bredt Synaptic targeting of the postsynaptic density protein PSD-95 mediated by lipid and protein motifs Neuron 22 1999 497 509
14. A.E. El-Husseini, E. Schnell, D.M. Chetkovich, R.A. Nicoll, and D.S. Bredt PSD-95 involvement in maturation of excitatory synapses Science 290 2000 1364 1368
15. K.S. Christopherson, N.T. Sweeney, S.E. Craven, R. Kang, D. El-Husseini Ael, and D.S. Bredt Lipid- and protein-mediated multimerization of PSD-95: implications for receptor clustering and assembly of synaptic protein networks J Cell Sci 116 2003 3213 3219
16. A.E. El-Husseini, S.E. Craven, D.M. Chetkovich, B.L. Firestein, E. Schnell, C. Aoki, and D.S. Bredt Dual palmitoylation of PSD-95 mediates its vesiculotubular sorting, postsynaptic targeting, and ion channel clustering J Cell Biol 148 2000 159 172
17. I. Ehrlich, and R. Malinow Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity J Neurosci 24 2004 916 927 The authors find that defects in PSD-95 palmitoylation block activity-dependent AMPAR incorporation at synapses during long term potentiation (LTP) and experience-driven synaptic strengthening.
18. M. Fukata, Y. Fukata, H. Adesnik, R.A. Nicoll, and D.S. Bredt Identification of PSD-95 palmitoylating enzymes Neuron 44 2004 987 996 Using a genetic approach, the authors isolated 23 mammalian DHHC proteins and found a subset, named P-PAT (PSD-95 palmitoyl acyl transferases), that specifically palmitoylate PSD-95. P-PATs can regulate synaptic function through PSD-95 palmitoylation.
19. R.D. Swayze, M.-F. Lise, J.N. Levinson, A. Phillips, and A. El-Husseini Modulation of dopamine mediated phosphorylation of AMPA receptors by PSD-95 and AKAP79/150 Neuropharmacology 47 2004 764 778
20. A.E. El-Husseini, J.R. Topinka, J.E. Lehrer-Graiwer, B.L. Firestein, S.E. Craven, C. Aoki, and D.S. Bredt Ion channel clustering by membrane-associated guanylate kinases. Differential regulation by N-terminal lipid and metal binding motifs J Biol Chem 275 2000 23904 23910
21. D. El-Husseini Ael, E. Schnell, S. Dakoji, N. Sweeney, Q. Zhou, O. Prange, C. Gauthier-Campbell, A. Aguilera-Moreno, R.A. Nicoll, and D.S. Bredt Synaptic strength regulated by palmitate cycling on PSD-95 Cell 108 2002 849 863
22. S. DeSouza, J. Fu, B.A. States, and E.B. Ziff Differential palmitoylation directs the AMPA receptor-binding protein ABP to spines or to intracellular clusters J Neurosci 22 2002 3493 3503
23. P. Washbourne, V. Cansino, J.R. Mathews, M. Graham, R.D. Burgoyne, and M.C. Wilson Cysteine residues of SNAP-25 are required for SNARE disassembly and exocytosis, but not for membrane targeting Biochem J 357 2001 625 634
24. R. Kang, R. Swayze, M.F. Lise, K. Gerrow, A. Mullard, W.G. Honer, and A. El-Husseini Presynaptic trafficking of synaptotagmin I is regulated by protein palmitoylation J Biol Chem 279 2004 50524 50536 The authors find that palmitoylation contributes to sorting of synaptotagmin I to an intracellular vesicular compartment at the presynaptic terminal and regulates its internalization.
25. W. Han, J.S. Rhee, A. Maximov, Y. Lao, T. Mashimo, C. Rosenmund, and T.C. Sudhof N-glycosylation is essential for vesicular targeting of synaptotagmin 1 Neuron 41 2004 85 99
26. M. Fukasawa, O. Varlamov, W.S. Eng, T.H. Sollner, and J.E. Rothman Localization and activity of the SNARE Ykt6 determined by its regulatory domain and palmitoylation Proc Natl Acad Sci USA 101 2004 4815 4820
27. J. Kanaani, M.J. Diacovo, D. El-Husseini Ael, D.S. Bredt, and S. Baekkeskov Palmitoylation controls trafficking of GAD65 from Golgi membranes to axon-specific endosomes and a Rab5a-dependent pathway to presynaptic clusters J Cell Sci 117 2004 2001 2013 The authors find that palmitoylation of GAD65 regulates its trafficking from Golgi membranes to axons in a Rab5a-dependent endosomal trafficking pathway.
28. J. Kanaani, D. el-Husseini Ael, A. Aguilera-Moreno, J.M. Diacovo, D.S. Bredt, and S. Baekkeskov A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65 J Cell Biol 158 2002 1229 1238
29. J. Rathenberg, J.T. Kittler, and S.J. Moss Palmitoylation regulates the clustering and cell surface stability of GABA(A) receptors Mol Cell Neurosci 26 2004 251 257
30. A receptor.
31. R.C. Drisdel, E. Manzana, and W.N. Green The role of palmitoylation in functional expression of nicotinic alpha7 receptors J Neurosci 24 2004 10502 10510
32. R.A. Gubitosi-Klug, D.J. Mancuso, and R.W. Gross The human Kv1.1 channel is palmitoylated, modulating voltage sensing: Identification of a palmitoylation consensus sequence Proc Natl Acad Sci USA 102 2005 5964 5968
33. P. Osten, L. Khatri, J.L. Perez, G. Kohr, G. Giese, C. Daly, T.W. Schulz, A. Wensky, L.M. Lee, and E.B. Ziff Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor Neuron 27 2000 313 325
34. O. Rocks, A. Peyker, M. Kahms, P.J. Verveer, C. Koerner, M. Lumbierres, J. Kuhlmann, H. Waldmann, A. Wittinghofer, and P.I. Bastiaens An acylation cycle regulates localization and activity of palmitoylated Ras isoforms Science 307 2005 1746 1752 Constitutive cycling of palmitate on H-Ras and N-Ras regulates rapid protein shuttling between the plasma membrane and the Golgi. This process might contribute to the differential effects of Ras isoforms in response to various extracellular stimuli.
35. R.M. Drenan, C.A. Doupnik, M.P. Boyle, L.J. Muglia, J.E. Huettner, M.E. Linder, and K.J. Blumer Palmitoylation regulates plasma membrane-nuclear shuttling of R7BP, a novel membrane anchor for the RGS7 family J Cell Biol 169 2005 623 633
36. U. Heindel, M.F. Schmidt, and M. Veit Palmitoylation sites and processing of synaptotagmin I, the putative calcium sensor for neurosecretion FEBS Lett 544 2003 57 62
37. R. Qanbar, and M. Bouvier Determination of protein-bound palmitate turnover rates using a three-compartment model that formally incorporates [3H]palmitate recycling Biochemistry 43 2004 12275 12288
38. R.C. Drisdel, and W.N. Green Labeling and quantifying sites of protein palmitoylation Biotechniques 36 2004 276 285 This work reports a novel non-radioactive method for detection of palmitoylated proteins that is more sensitive than conventional methods and enables quantitative estimation of palmitoylation.
39. M.E. Linder, and R.J. Deschenes Model organisms lead the way to protein palmitoyltransferases J Cell Sci 117 2004 521 526
40. Z. Chamoun, R.K. Mann, D. Nellen, D.P. von Kessler, M. Bellotto, P.A. Beachy, and K. Basler Skinny hedgehog, an acyltransferase required for palmitoylation and activity of the hedgehog signal Science 293 2001 2080 2084
41. R. Nusse Wnts and Hedgehogs: lipid-modified proteins and similarities in signaling mechanisms at the cell surface Development 130 2003 5297 5305
42. L. Zhai, D. Chaturvedi, and S. Cumberledge Drosophila wnt-1 undergoes a hydrophobic modification and is targeted to lipid rafts, a process that requires porcupine J Biol Chem 279 2004 33220 33227 The authors find that palmitoylation of wnt-1 is regulated by porcupine, a palmitoyl transferase in Drosophila.
43. S. Lobo, W.K. Greentree, M.E. Linder, and R.J. Deschenes Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae J Biol Chem 277 2002 41268 41273
44. A.F. Roth, Y. Feng, L. Chen, and N.G. Davis The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase J Cell Biol 159 2002 23 28 The authors of this study and Lobo et al. [43] identified Akr1 and Erf2-Erf4 protein complexes as palmitoyl-transferases. These studies led to the identification of a large family of mammalian palmitoyl transferases that contain the conserved DHHC domain.
45. R.R. Singaraja, S. Hadano, M. Metzler, S. Givan, C.L. Wellington, S. Warby, A. Yanai, C.A. Gutekunst, B.R. Leavitt, and H. Yi HIP14, a novel ankyrin domain-containing protein, links huntingtin to intracellular trafficking and endocytosis Hum Mol Genet 11 2002 2815 2828
46. K. Huang, A. Yanai, R. Kang, P. Arstikaitis, R.R. Singaraja, M. Metzler, A. Mullard, B. Haigh, C. Gauthier-Campbell, and C.A. Gutekunst Huntingtin-interacting protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins Neuron 44 2004 977 986 The authors identified HIP14 as a palmitoyl transferase involved in the palmitoylation and trafficking of multiple neuronal proteins.
47. E.G. Politis, A.F. Roth, and N.G. Davis Transmembrane topology of the protein palmitoyl transferase Akr1 J Biol Chem 280 2005 10156 10163
48. J. Mukai, H. Liu, R.A. Burt, D.E. Swor, W.S. Lai, M. Karayiorgou, and J.A. Gogos Evidence that the gene encoding ZDHHC8 contributes to the risk of schizophrenia Nat Genet 36 2004 725 731 The authors find that the palmitoyl transferase DHHC-8 is associated with susceptibility to schizophrenia.
49. D.C. Yeh, J.A. Duncan, S. Yamashita, and T. Michel Depalmitoylation of endothelial nitric-oxide synthase by acyl-protein thioesterase 1 is potentiated by Ca(2+)-calmodulin J Biol Chem 274 1999 33148 33154
50. M. Lehtovirta, A. Kyttala, E.L. Eskelinen, M. Hess, O. Heinonen, and A. Jalanko Palmitoyl protein thioesterase (PPT) localizes into synaptosomes and synaptic vesicles in neurons: implications for infantile neuronal ceroid lipofuscinosis (INCL) Hum Mol Genet 10 2001 69 75
51. 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, In press.