Palmitoylcarnitine affects localization of growth associated protein GAP-43 in plasma membrane subdomains and its interaction with Gα o in neuroblastoma NB-2a cells

Neurochemical Research

Volumn 38, Issue 3, 2013, Pages 519-529

  Tułodziecka, Karolina ^a   Czeredys, Magdalena ^a   Nałęcz, Katarzyna A ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

Cholesterol; GAP 43; Palmitoylcarnitine; Phosphatidylinositol

Indexed keywords

2 BROMOPALMITIC ACID; CELL PROTEIN; CHOLESTEROL; ETOMOXIR; G ALPHA O PROTEIN; METHYL BETA CYCLODEXTRIN; NEOMYCIN; NEUROMODULIN; PALMITOYLCARNITINE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRAIN; CELL STRAIN NB 2A; CONTROLLED STUDY; LIPID RAFT; MOUSE; NERVE CELL DIFFERENTIATION; NEUROBLASTOMA CELL; NONHUMAN; PALMITOYLATION; PRECIPITATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION;

EID: 84876411116     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-012-0944-5     Document Type: Article

References (63)

1. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569-572
2. Brown DA (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 21:430-439
3. Resh MD (1999) Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1451:1-16
4. Resh MD (2004) Membrane targeting of lipid modified signal transduction proteins. Subcell Biochem 37:217-232
5. Aicart-Ramos C, Valero RA, Rodriguez-Crespo I (2011) Protein palmitoylation and subcellular trafficking. Biochim Biophys Acta 1808:2981-2994
6. Smotrys JE, Linder ME (2004) Palmitoylation of intracellular signaling proteins: regulation and function. Annu Rev Biochem 73:559-587
7. Skene JH (1989) Axonal growth-associated proteins. Annu Rev Neurosci 12:127-156
8. Skene JH, Virag I (1989) Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J Cell Biol 108:613-624
9. Strittmatter SM, Valenzuela D, Kennedy TE, Neer EJ, Fishman MC (1990) G0 is a major growth cone protein subject to regulation by GAP-43. Nature 344:836-841
10. Coggins PJ, Zwiers H (1989) Evidence for a single protein kinase C-mediated phosphorylation site in rat brain protein B-50. J Neurochem 53:1895-1901
11. 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 149:1455-1472
12. Hope HR, Pike LJ (1996) Phosphoinositides and phosphoinositide-utilizing enzymes in detergent-insoluble lipid domains. Mol Biol Cell 7:843-851
13. Klopfenstein DR, Tomishige M, Stuurman N, Vale RD (2002) Role of phosphatidylinositol(4,5)bisphosphate organization in membrane transport by the Unc104 kinesin motor. Cell 109:347-358
14. van Rheenen J, Achame EM, Janssen H, Calafat J, Jalink K (2005) PIP2 signaling in lipid domains: a critical re-evaluation. EMBO J 24:1664-1673
15. Tong J, Nguyen L, Vidal A, Simon SA, Skene JH, McIntosh TJ (2008) Role of GAP-43 in sequestering phosphatidylinositol 4,5-bisphosphate to raft bilayers. Biophys J 94:125-133
16. Nałȩcz KA, Mroczkowska JE, Berent U, Nałȩcz MJ (1997) Effect of palmitoylcarnitine on the cellular differentiation, proliferation and protein kinase C activity in neuroblastoma nb-2a cells. Acta Neurobiol Exp (Wars) 57:263-274
17. Kerner J, Hoppel C (2000) Fatty acid import into mitochondria. Biochim Biophys Acta 1486:1-17
18. Lee K, Kerner J, Hoppel CL (2011) Mitochondrial carnitine palmitoyltransferase 1a (CPT1a) is part of an outer membrane fatty acid transfer complex. J Biol Chem 286:25655-25662
19. Ebert D, Haller RG, Walton ME (2003) Energy contribution of octanoate to intact rat brain metabolism measured by 13C nuclear magnetic resonance spectroscopy. J Neurosci 23:5928-5935
20. Nałȩcz KA, Szczepankowska D, Czeredys M, Kulikova N, Grześkiewicz S (2007) Palmitoylcarnitine regulates estrification of lipids and promotes palmitoylation of GAP-43. FEBS Lett 581:3950-3954
21. Tamai I, Ohashi R, Nezu J, Yabuuchi H, Oku A, Shimane M, Sai Y, Tsuji A (1998) Molecular and functional identification of sodium ion-dependent, high affinity human carnitine transporter OCTN2. J Biol Chem 273:20378-20382
22. Tamai I, Ohashi R, Nezu JI, Sai Y, Kobayashi D, Oku A, Shimane M, Tsuji A (2000) Molecular and functional characterization of organic cation/carnitine transporter family in mice. J Biol Chem 275:40064-40072
23. Januszewicz E, Bekisz M, Mozrzymas JW, Nałȩcz KA (2010) High affinity carnitine transporters from OCTN family in neural cells. Neurochem Res 35:743-748
24. Shinawi M, Gruener N, Lerner A (1998) CSF levels of carnitine in children with meningitis, neurologic disorders, acute gastroenteritis, and seizure. Neurology 50:1869-1871
25. Szczepankowska D, Nałȩcz KA (2003) Palmitoylcarnitine modulates palmitoylation of proteins: implication for differentiation of neural cells. Neurochem Res 28:645-651
26. Sobiesiak-Mirska J, Nałȩcz MJ, Nałȩcz KA (2003) Interaction of palmitoylcarnitine with protein kinase C in neuroblastoma NB-2a cells. Neurochem Int 42:45-55
27. Sobiesiak-Mirska J, Nałȩcz KA (2006) Palmitoylcarnitine modulates interaction between protein kinase C betaII and its receptor RACK1. FEBS J 273:1300-1311
28. Mizgalska JA, Berent U, Mac M, Oestreicher B, De Graan PNE, Gispen WH, Nałȩcz MJ, Nałȩcz KA (1998) Accumulation of palmitoylcarnitine in neuroblastoma NB-2a cells affects the expression, phosphorylation and localization of B-50 protein. Neurosci Res Commun 22:73-82
29. Milligan G, Parenti M, Magee AI (1995) The dynamic role of palmitoylation in signal transduction. Trends Biochem Sci 20:181-187
30. Igarashi M, Strittmatter SM, Vartanian T, Fishman MC (1993) Mediation by G proteins of signals that cause collapse of growth cones. Science 259:77-79
31. Sudo Y, Valenzuela D, Beck-Sickinger AG, Fishman MC, Strittmatter SM (1992) Palmitoylation alters protein activity: blockade of G(o) stimulation by GAP-43. EMBO J 11:2095-2102
32. Brockenbrough JS, Korc M (1987) Inhibition of epidermal growth factor binding in rat pancreatic acini by palmitoyl carnitine: evidence for Ca2+ and protein kinase C independent regulation. Cancer Res 47:1805-1810
33. Lamprecht MR, Sabatini DM, Carpenter AE (2007) Cell Profiler: free, versatile software for automated biological image analysis. Biotechniques 42:71-75
34. Vokes MS, Carpenter AE (2008) Using CellProfiler for automatic identification and measurement of biological objects in images. Curr Protoc Mol Biol Chapter 14, Unit 14 17
35. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
36. Miecz D, Januszewicz E, Czeredys M, Hinton BT, Berezowski V, Cecchelli R, Nałȩcz KA (2008) Localization of organic cation/carnitine transporter (OCTN2) in cells forming the blood-brain barrier. J Neurochem 104:113-123
37. Gray MC, Plant AL, Nicholson JM, May WE (1995) Microenzymatic fluorescence assay for serum cholesterol. Anal Biochem 224:286-292
38. Gorodinsky A, Harris DA (1995) Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin. J Cell Biol 129:619-627
39. Sargiacomo M, Scherer PE, Tang Z, Kubler E, Song KS, Sanders MC, Lisanti MP (1995) Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc Natl Acad Sci USA 92:9407-9411
40. Fukata M, Fukata Y, Adesnik H, Nicoll RA, Bredt DS (2004) Identification of PSD-95 palmitoylating enzymes. Neuron 44:987-996
41. Arduini A, Mancinelli G, Radatti GL, Dottori S, Molajoni F, Ramsay RR (1992) Role of carnitine and carnitine palmitoyltransferase as integral components of the pathway for membrane phospholipid fatty acid turnover in intact human erythrocytes. J Biol Chem 267:12673-12681
42. Ramsay RR (2000) The carnitine acyltransferases: modulators of acyl-CoA-dependent reactions. Biochem Soc Trans 28:182-186
43. Ramsay RR, Gandour RD, van der Leij FR (2001) Molecular enzymology of carnitine transfer and transport. Biochim Biophys Acta 1546:21-43
44. Kiorpes TC, Hoerr D, Ho W, Weaner LE, Inman MG, Tutwiler GF (1984) Identification of 2-tetradecylglycidyl coenzyme A as the active form of methyl 2-tetradecylglycidate (methyl palmoxirate) and its characterization as an irreversible, active site-directed inhibitor of carnitine palmitoyltransferase A in isolated rat liver mitochondria. J Biol Chem 259:9750-9755
45. Kerner J, Zaluzec E, Gage D, Bieber LL (1994) Characterization of the malonyl-CoA-sensitive carnitine palmitoyltransferase (CPTo) of a rat heart mitochondrial particle. Evidence that the catalytic unit is CPTi. J Biol Chem 269:8209-8219
46. Hao M, Mukherjee S, Maxfield FR (2001) Cholesterol depletion induces large scale domain segregation in living cell membranes. Proc Natl Acad Sci USA 98:13072-13077
47. Adkins EM, Samuvel DJ, Fog JU, Eriksen J, Jayanthi LD, Vaegter CB, Ramamoorthy S, Gether U (2007) Membrane mobility and microdomain association of the dopamine transporter studied with fluorescence correlation spectroscopy and fluorescence recovery after photobleaching. Biochemistry 46:10484-10497
48. Wu J, McNicholas CM, Bevensee MO (2009) Phosphatidylinositol 4,5-bisphosphate (PIP2) stimulates the electrogenic Na/HCO3 cotransporter NBCe1-A expressed in Xenopus oocytes. Proc Natl Acad Sci USA 106:14150-14155
49. Strittmatter SM, Valenzuela D, Sudo Y, Linder ME, Fishman MC (1991) An intracellular guanine nucleotide release protein for G0. GAP-43 stimulates isolated alpha subunits by a novel mechanism. J Biol Chem 266:22465-22471
50. Strittmatter SM, Valenzuela D, Vartanian T, Sudo Y, Zuber MX, Fishman MC (1991) Growth cone transduction: Go and GAP-43. J Cell Sci Suppl 15:27-33
51. Yang H, Qu L, Ni J, Wang M, Huang Y (2008) Palmitoylation participates in G protein coupled signal transduction by affecting its oligomerization. Mol Membr Biol 25:58-71
52. Carter BD, Medzihradsky F (1993) Go mediates the coupling of the mu opioid receptor to adenylyl cyclase in cloned neural cells and brain. Proc Natl Acad Sci USA 90:4062-4066
53. Brown DA, Sihra TS (2008) Presynaptic signaling by heterotrimeric G-proteins. Handb Exp Pharmacol 184:207-260
54. Koenig JA, Edwardson JM, Humphrey PP (1997) Somatostatin receptors in Neuro2A neuroblastoma cells: operational characteristics. Br J Pharmacol 120:45-51
55. Arduini A, Denisova N, Virmani A, Avrova N, Federici G, Arrigoni-Martelli E (1994) Evidence for the involvement of carnitine-dependent long-chain acyltransferases in neuronal triglyceride and phospholipid fatty acid turnover. J Neurochem 62:1530-1538
56. Yang H, Wan L, Song F, Wang M, Huang Y (2009) Palmitoylation modification of Galpha o depresses its susceptibility to GAP-43 activation. Int J Biochem Cell Biol 41:1495-1501
57. Bates CA, Meyer RL (1996) Heterotrimeric G protein activation rapidly inhibits outgrowth of optic axons from adult and embryonic mouse, and goldfish retinal explants. Brain Res 714:65-75
58. Li S, Okamoto T, Chun M, Sargiacomo M, Casanova JE, Hansen SH, Nishimoto I, Lisanti MP (1995) Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem 270:15693-15701
59. Chisari M, Saini DK, Kalyanaraman V, Gautam N (2007) Shuttling of G protein subunits between the plasma membrane and intracellular membranes. J Biol Chem 282:24092-24098
60. Jia L, Linder ME, Blumer KJ (2011) Gi/o signaling and the palmitoyltransferase DHHC2 regulate palmitate cycling and shuttling of RGS7 family-binding protein. J Biol Chem 286:13695-13703
61. Tsutsumi R, Fukata Y, Noritake J, Iwanaga T, Perez F, Fukata M (2009) Identification of G protein alpha subunit-palmitoylating enzyme. Mol Cell Biol 29:435-447
62. Duncan JA, Gilman AG (1998) A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21(RAS). J Biol Chem 273:15830-15837
63. 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:e15045