A shift in protein S-palmitoylation, with persistence of growth- associated substrates, marks a critical period for synaptic plasticity in developing brain

Journal of Neurobiology

Volumn 39, Issue 3, 1999, Pages 423-437

  Patterson, Sean I ^a,b   Skene, J H P ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b FACULTAD DE CIENCIAS MÉDICAS   (Argentina)

Author keywords

Critical period; Development; Growth cone; Protein S palmitoylation; Synaptogenesis

Indexed keywords

NEUROMODULIN;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; ELECTRON MICROSCOPY; GROWTH CONE; NERVE CELL PLASTICITY; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN MODIFICATION; SYNAPTOGENESIS;

AGING; ANIMALS; ANIMALS, NEWBORN; BRAIN; GROWTH; GROWTH CONES; NERVE ENDINGS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PALMITIC ACID; RATS; RATS, SPRAGUE-DAWLEY; SUBSTRATE SPECIFICITY; SYNAPSES; SYNAPTOSOMES;

EID: 0033526552     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(19990605)39:3<423::AID-NEU8>3.0.CO;2-Z     Document Type: Article

References (90)

1. rho proteins. J Cell Biol 119:617-627.
2. Bark IC, Wilson MC. 1994. Regulated vesicular fusion in neurons: snapping together the details. Proc Natl Acad Sci USA 91:4621-4624.
3. Bixby JL, Jhabvala P. 1993. Tyrosine phosphorylation in early embryonic growth cones. J Neurosci 13:3421-3432.
4. Blue ME, Parnavelas JG. 1983a. The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis. J Neurocytol 12:599-616.
5. Blue ME, Parnavelas JG. 1983b. The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. J Neurocytol 12:687-712.
6. Bokoch GM. 1993. Biology of the rap proteins, members of the ras superfamily of GTP-binding proteins. Biochem J 289:17-24.
7. Bonhoeffer T. 1996. Neurotrophins and activity-dependent development of the neocortex. Curr Opin Neurobiol 6:119-126.
8. Bourguignon LYW, Kalomiris EL, Lokeshwar VB. 1991. Acylation of the lymphoma transmembrane glycoprotein, GP85, may be required for GP85-ankyrin interaction. J Biol Chem 266:11761-11765.
9. Bredt DS, Snyder SH. 1994. Nitric oxide: a physiologic messenger molecule. Annu Rev Biochem 63:175-195.
10. Burry RW. 1991. Transitional elements with characteristics of both growth cones and presynaptic terminals observed in cell cultures of cerebellar neurons. J Neurocytol 20: 124-132.
11. Casey PJ. 1995. Protein lipidation in cell signaling. Science 268:221-225.
12. Chapman ER, Blasi J, An S, Brose N, Johnston PA, Südhof TC, Jahn R. 1996. Fatty acylation of synpatotagmin in PC12 cells and synaptosomes. Biochem Biophys Res Commun 225:326-332.
13. Couve A, Protopopov V, Gerst JE. 1995. Yeast synaptobrevin homologs are modified posttranslationally by the addition of palmitate. Proc Natl Acad Sci USA 92:5987-5991.
14. Devoto SH, Barnstable CJ. 1989. Expression of growth cone specific epitope CDA 1 and the synaptic vesicle protein SVP38 in the developing mammalian cerebral cortex. J Comp Neurol 290:154-168.
15. Donaldson JG, Klausner RD. 1994. ARF: a key regulatory switch in membrane traffic and organelle structure. Curr Opin Cell Biol 6:527-532.
16. Dudler T, Gelb MH. 1996. Palmitoylation of Ha-ras facilitates membrane binding, activation of downstream effectors, and meiotic maturation in Xenopus oocytes. J Biol hem 271:11541-11547.
17. Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L. 1994. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vis Res 34:709-720.
18. Feron O, Saldana F, Michel JB, Michel T. 1998. The endothelial nitric-oxide synthase-caveolin regulatory cycle. J Biol Chem 273:3125-3128.
19. 2+-dependent routes to ras: mechanisms for neuronal survival, differentiation and plasticity? Neuron 16:233-236.
20. Friedrichson T, Kurzchalia TV. 1998. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking .Nature 394:802-805.
21. Futerman AH, Banker GA. 1996. The economics of neurite outgrowth - the addition of new membrane to growing axons. Trends Neurosci 19:144-149.
22. fyn src homology 4 domain define a motif for immune-receptor tyrosine-based activation motif (ITAM) binding and for plasma membrane localization. J Cell Biol 133:1007-1015.
23. Gonatas NK, Autilio-Gambetti L, Gambetti P, Shafer B. 1971. morphological and biochemical changes in rat synaptosome fractions during neonatal development. J Cell Biol 51:484-498.
24. Gordon-Weeks PR. 1987a. The cytoskeletons of isolated, neuronal growth cones. Neuroscience 21:977-989.
25. Gordon-Weeks PR. 1987b. Isolation of synaptosomes, growth cones and their subcellular compartments. In: Turner AJ, Bachelard HS, editors. Neurochemistry: a practical approach. Oxford: IRL Press, p. 1-26.
26. Gorodinsky A, Harris DA. 1995. Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin. J cell Biol 129:619-627.
27. Grove WE, Johnson TC, Kelly P, Luttges M. 1973. qualitative and quantitative morphological changes in subcellular fractions from mouse cerebral cortex during postnatal development. J Cell Biol 58:676-688.
28. Guo YJ, Lin SC, Wang JH, Bigby M, Sy MS. 1994. Palmitoylation of CD44 interferes with CD3-mediated signaling in human T lymphocytes. Int Immunol 6:213-221.
29. Harder T, Simons K. 1997. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr Opin Cell Biol 9:534-542.
30. Haruta T, Takami N, Ohmura M, Ikehara Y. 1997. Ca2+-dependent interaction of the growth-associated protein GAP-43 with the synaptic core complex. Biochem J 325:455-463.
31. Henderson CE. 1996. Role of neurotrophic factors in neuronal development. Curr Opin Neurobiol 6:64-70.
32. Hess DT, Lin LH, Freeman JA, Norden JJ. 1994. Modification of cysteine residues within Go and other neuronal proteins by exposure to nitric oxide. Neuropharmacology 33:1283-1292.
33. Hess DT, Patterson SI, Smith DS, Skene JHP. 1993. Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature 366:562-565.
34. Hess DT, Slater TM, Wilson MC, Skene JHP. 1992. The 25kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS. J Neurosci 12:4634-4641.
35. Hess DT, Smith DS, Patterson SI, Kahn RA, Skene JHP, Norden JJ. 1999. Rapid arrest of axon elongation by brefeldin A: a role for the small GTP-binding protein ARF in neuronal growth cones. J Neurobiol 38:105-115.
36. Hirschberg K, Zisling R, Echten-Deckert GV, Futerman AH. 1996. Ganglioside synthesis during the development of neuronal polarity. J Biol Chem 25:14876-14882.
37. 2-terminal myristoylation and palmitoylation at cysteine-3. J Cell Biol 136:1023-1035.
38. Huang MM, Bolen JB, Barnwell JW, Shattil SJ, Brugge JS. 1991. Membrane glycoprotein IV (CD36) is physically associated with the Fyn, Lyn and Yes protein-tyrosine kinases in human platelets. Proc Natl Acad Sci USA 88:7844-7848.
39. Huber LA, Ullrich O, Takai Y, Lütcke A, Dupree P, Okllonen V, Virta H, Hoop MJD, Alexandrov K, Peter M, Zerial M, Simons K. 1994. Mapping of ras-related GTP-binding proteins by GTP overlay following two-dimensional gel electrophoresis. Proc Natl Acad Sci USA 91: 7874-7878.
40. Igarishi M, Kozaki S, Terakawa S, Kawano S, Ide C, Komiya Y. 1996. Growth cone collapse and inhibition of neunte growth by Botulinum neurotoxin Cl: a t-SNARE is involved in axonal growth. J Cell Biol 134:205-215.
41. Igarishi M, Tagaya M, Komiya Y. 1997. The soluble Nethylmaleimide-sensitive factor attached protein receptor complex in growth cones: molecular aspects of the axon terminal development. J Neurosci 15:1460-1470.
42. Igarashi M, Waki H, Hirota M, Hirabayashi Y, Obata K, Ando S. 1990. Difference in lipid composition between isolated growth cones from the forebrain and those from the brainstem in the fetal rat. Dev Brain Res 51:1-9.
43. Ikonen E, Tagaya M, Ullrich O, Montecucco C, Simons K. 1995. Different requirements for NSF, SNAP, and Rab proteins in apical and basolateral transport in MDCK cells. Cell 81:571-580.
44. Kageyama GH, Robertson RT. 1993. Development of geniculocortical projections to visual cortex in rat: evidence for early ingrowth and synaptogenesis. J Comp Neurol 335:123-148.
45. Katz LC, Schatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
46. Kremer NE, D'Arcangelo G, Thomas SM, DeMarco M, Brugge JS, Halegoua S. 1991. Signal transduction by nerve growth factor and fibroblast growth factor in PC12 cells requires a sequence of src and ras actions. J Cell Biol 115:809-819.
47. Leclerc N, Beesley PW, Brown I, Colonnier M, Gurd JW, Paladino T, Hawkes R. 1989. Synaptophysin expression during synaptogenesis in the rat cerebellar cortex. J Comp Neurol 280:197-212.
48. Liu J, Hughes TE, Sessa WC. 1997. The first 35 amino acids and fatty acylation sites determine the molecular targeting of endothelial nitric oxide synthase into the Golgi region of cells: a green fluorescent protein study. J Cell Biol 137:1525-1535.
49. Liu L, Dudler T, Gelb MH. 1996. Purification of a protein palmitoyltransferase that acts on H-ras protein and on a C-terminal N-ras peptide. J Biol Chem 271:23269-23276.
50. Mackay DJG, Nobes CD, Hall A. 1995. The rho's progress: a potential role during neuritogenesis for the rho family of GTPases. Trends Neurosci 18:496-501.
51. Maekawa S, Kumnogoh H, Funatsu N, Takei N, Inoue K, Endo Y, Hamada K, Sokawa Y. 1997. Identification of NAP-22 and GAP-43 (neuromodulin) as major protein components in a Triton insoluble low density fraction of rat brain. Biochim Biophys Acta 1323:1-5.
52. Maness PF. 1992. Nonreceptor protein tyrosine kinases associated with neuronal development. Dev Neurosci 14: 257-270.
53. ras. Trends Biochem 18:250-254.
54. Martin RE, Bazan NG. 1992. Changing fatty acid content of growth cone lipids prior to synaptogenesis. J Neurochem 59:318-325.
55. Milligan G, Parenti M, Magee AI. 1995. The dynamic role of palmitoylation in signal transduction. Trends Biochem 5:181-186.
56. Mumby SM. 1997. Reversible palmitoylation of signaling proteins. Curr Opin Cell Biol 9:148-154.
57. Okamoto T, Schlegel A, Scherer PE, Lisanti MP. 1998. Caveolins, a family of scaffolding proteins for organizing "presassembled signaling complexes" at the plasma membrane. J Biol Chem 273:5419-5422.
58. Orike N, Pini A. 1996. Axon guidance: following the eph plan. Curr Biol 6:108-110.
59. Osen-Sand A, Catsicas M, Staple JK, Jones KA, Ayala G, Knowles J, Grenningloh G, Catsicas S. 1993. Inhibition of axonal growth by SNAP-25 antisense oligonucleotides in vitro and in vivo. Nature 364:445-448.
60. Oyler GA, Polli JW, Wilson MC, Billingsley ML. 1991. Developmental expression of the 25-kDa synaptosomal-associated protein (SNAP-25) in rat brain. Proc Natl Acad Sci USA 88:5247-5251.
61. Patterson SI, Skene JHP. 1994. Novel inhibitory action of tunicamycin homologues suggests a role for dynamic protein fatty acylation in growth cone-mediated neurite extension. J Cell Biol 124:521-536.
62. Patterson SI, Skene JHP. 1997. Long-chain fatty acylation of proteins. In: Boulton AA, Baker GB, Hemmings HC, editors. Posttranslational modification: techniques and protocols. Vol. 30. Totowa, NJ: Humana Press, p. 335-364.
63. Peunova N, Enikolopov G. 1995. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 375:68-73.
64. Pfenninger KH, Houssaye BADL, Helmke SM, Quiroga S. 1991. Growth-regulated proteins and neuronal plasticity. Mol Neurobiol 5:143-151.
65. Resh MD. 1994. Myristylation and palmitylation of src family members: the fats of the matter. Cell 76:411-413.
66. Ridley AJ. 1996. Rho: theme and variations. Curr Biol 6:1256-1264.
67. Rodriguez-Viciana P, Warne PH, Dhand R, Vanhaesebroeck B, Gout I, Fry MJ, Waterfield MD, Downward J. 1994. Phosphatidylinositol-3-OH kinase as a direct target of ras. Nature 370:527-532.
68. Rogers W, Crise B, Rose JK. 1994. Signals of determining protein tyrosine kinase and glycosyl-phosphatidylinositol-anchored protein targeting to a glycolipid-enriched membrane fraction. Mol Cell Biol 14:5384-5391.
69. Rothman JE. 1994. Mechanisms of intracellular protein transport Nature 372:55-63.
70. Schnitzer JE, Liu J, Oh P. 1995. Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSE, SNAP, annexins, and GTPases. J Biol Chem 270:14399-14404.
71. Schreyer DJ, Skene JHP. 1991. Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: delayed accumulation and correlation with regenerative potential. J Neurosci 11:3738-3751.
72. Schroeder H, Leeventis R, Shahinian S, Walton PA, Silvius JR. 1996. Lipid-modified, cysteinyl-containing peptides of diverse structures are efficiently S-acylated at the plasma membrane of mammalian cells. J Cell Biol 134: 647-660.
73. Shahinian S, Silvius JR. 1995. Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes. Biochemistry 34:3813-3822.
74. Shaul PW, Smart EJ, Robinson LJ, German Z, Yuhanna IS, Ying Y, Anderson GW, Michel T. 1996. Acylation targets endothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem 271:6518-6522.
75. Skene JHP. 1989. Axonal growth-associated proteins. Annu Rev Neurosci 12:127-156.
76. Skene JHP, Virag I. 1989. Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J Cell Biol 108:613-624.
77. Song KS, Sargiacomo M, Galbiati F, Parenti M, Lisanti MP. 1997. Targeting of a G alpha subunit (Gil alpha) and c-Src tyrosine kinase to caveolae membranes: clarifying the role of N-myristoylation. Cell Mol Biol 43:293-303.
78. Sretavan DW, Feng L, Pur3́ E, Reichardt LF. 1994. Embryonic neurons of the developing optic chiasm express L1 and CD44, cell surface molecules with opposing effects on retinal axon growth. Neuron 12:957-975.
79. Staufenbiel M. 1989. Fatty acylation of erythrocyte proteins. Biochem Soc Trans 17:863-864.
80. Südhof TC. 1995. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375:645-643.
81. Symons M. 1996. Rho family GTPases: the cytoskeleton and beyond. Trends Biochem 21:178-181.
82. Tabata H, Bell JM, Miller JC, Rapaport SI. 1986. Incorporation of plasma palmitate into the brain of rat during development. Dev Brain Res 29:1-8.
83. Takai Y, Sasaki T, Tanaka K, Nakanishi H. 1995. Rho as a regulator of the cytoskeleton. Trends Biochem 20:227-231.
84. Taylor J, Gordon-Weeks PR. 1989. Developmental changes in the calcium dependency of α-aminobutyric acid release from isolated growth cones: correlation with growth cone morphology. J Neurochem 53:834-843.
85. Varma R, Mayor S. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394:798-801.
86. Vizzard MA, Erdman SL, Groat WCD. 1995. Increased expression of neuronal nitric oxide synthase (NOS) in visceral neurons after injury. J Neurosci 15:4033-4045.
87. Wedegaertner PB, Wilson PT, Bourne HR. 1995. Lipid modifications of trimeric G proteins. J Biol Chem 270: 503-506.
88. Worley T, Holt C. 1996. Inhibition of protein tyrosine kinases impairs axon extension in the embryonic axon tract. J Neurosci 16:2294-2306.
89. Wu HH, Williams CV, McLoon SC. 1994. Involvement of nitric oxide in the elimination of a transient retinotectal projection in development. Science 265:1593-1596.
90. Zisch AH, D'Allesandri L, Amrein K, Ranscht B, Winterhalter KH, Vaughan L. 1995. The glypiated neuronal cell adhesion molecule contactin/F11 complexes with src family protein tyrosine kinase fyn. Mol Cell Neurosci 6:263-279.