A palmitoylation cycle dynamically regulates partitioning of the GABA-synthesizing enzyme GAD65 between ER-Golgi and post-Golgi membranes

Journal of Cell Science

Volumn 121, Issue 4, 2008, Pages 437-449

  Kanaani, Jamil ^a   Patterson, George ^b   Schaufele, Fred ^a   Lippincott Schwartz, Jennifer ^b   Baekkeskov, Steinunn ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

ER Golgi trafficking; FRAP analysis; Glutamic acid decarboxylase; Golgi post Golgi cycling; Membrane trafficking; Palmitoylation cycle; Palmitoylation signals

Indexed keywords

GLUTAMATE DECARBOXYLASE 65;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL CYCLE; CELL GROWTH; CELL MEMBRANE; CELL MIGRATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME REGULATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GOLGI COMPLEX; HYDROPHOBICITY; IMMUNOFLUORESCENCE; MOLECULAR IMAGING; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; RAT; SEQUENCE ANALYSIS;

ANIMALS; CELLS, CULTURED; ENDOPLASMIC RETICULUM; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GLUTAMATE DECARBOXYLASE; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; INTRACELLULAR MEMBRANES; KINETICS; LIPOYLATION; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS;

EID: 40949117546     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.011916     Document Type: Article

References (50)

1. Asada, H., Kawamura, Y., Maruyama, K., Kume, H., Ding, R., Ji, F. Y., Kanbara, N., Kuzume, H., Sambo, M., Yagi, T. et al. (1996). Mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) maintain normal levels of GAD67 and GABA in their brains but susceptible to seizures. Biochem. Biophys. Res. Commun. 229, 891-895.
2. Asada, H., Kawamura, Y., Maruyama, K., Kume, H., Ding, R. G., Kanbara, N., Kuzume, H., Sanbo, M., Yagi, T. and Obata, K. (1997). Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. USA 94, 6496-6499.
3. Baekkeskov, S., Aanstoot, H. J., Christgau, S., Reetz, A., Solimena, M., Cascalho, M., Folli, F. and Richter-Olesen, H. (1990). Identification of the 64K autoantigen in insulin-dependent diabetes as the GABA-synthesizing enzyme glutamic acid decarboxylase. Nature 347, 151-156.
4. Battaglioli, G. H., Liu, H. and Martin, D. L. (2003). Kinetic differences between the isoforms of glutamate decarboxylase: implications for the regulation of GABA synthesis. J. Neurochem. 86, 879-887.
5. Battaglioli, G., Liu, H., Hauer, C. R. and Martin, D. L. (2005). Glutamate decarboxylase: Loss of N-terminal segment does not affect homodimerization and determination of the oxidation state of cysteine residues. Neurochem. Res. 30, 989-1001.
6. Bijlmakers, M. and Marsh, M. (2003). The on-off story of palmitoylation. Trends Cell. Biol. 13, 32-42.
7. Brewer, G. J., Torricelli, J. R., Evege, E. K. and Price, P. J. (1993). Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576.
8. Chege, N. W. and Pfeffer, S. R. (1990). Compartmentation of the Golgi complex: brefeldin-A distinguishes trans-Golgi cisternae from the trans-Golgi network. J. Cell Biol. 111, 893-899.
9. Choy, E., Chiu, V. K., Silletti, J., Feoktistov, M., Morimoto, T., Michaelson, D., Ivanov, I. E. and Philips, M. R. (1999). Endomembrane trafficking of Ras: The CAAX motif targets proteins to the ER and Golgi. Cell 98, 69-80.
10. Christgau, S., Schierbeck, H., Aanstoot, H. J., Aagaard, L, Begley, K., Kofod, H., Hejnaes, K. and Baekkeskov, S. (1991). Pancreatic β-cells express two autoantigenic forms of glutamic acid decarboxylase, a 65kDa hydrophilic form and a 64kDa amphiphilic form which can be both membrane-bound and soluble. J. Biol. Chem. 266, 21257-21264.
11. Christgau, S., Aanstoot, H. J., Schierbeck, H., Begley, K., Tullin, S., Hejnaes, H. and Baekkeskov, S. (1992). Membrane anchoring of the autoantigen GAD65 to microvesicles in pancreatic β-cells by palmitoylation in the N-terminal domain. J. Cell Biol. 118, 309-320.
12. Cole, N. B., Sciaky, N., Marotta, A., Song, T. and Lippincott-Schwartz, J. (1996). Golgi dispersal during microtubule disruption regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell 7, 631-650.
13. Condie, B. G., Bain, G., Gottlieb, D. I. and Capecchi, M. R. (1997). Cleft palate in mice with a targeted mutation in the gamma-aminobutyric acid-producing enzyme glutamic acid decarboxylase 67. Proc. Natl. Acad. Sci. USA 94, 11451-11455.
14. RAS. J. Biol. Chem. 273, 15830-15837.
15. Duncan, J. A. and Gilman, A. G. (2002). Characterization of Saccharomyces cerevisiae acyl-protein thioesterase 1, the enzyme responsible for G protein alpha subunit deacylation in vivo. J. Biol. Chem. 277, 31740-31752.
16. Gillingham, A. K., Pfeifer, A. C. and Munro, S. (2002). CASP, the alternatively spliced product of the gene encoding the CCAAT-displacement protein transcription factor, is a Golgi membrane protein related to Giantin. Mol. Biol. Cell 13, 3761-3774.
17. Goodwin, J. S., Drake, K. R., Rogers, C., Wright, L., Lippincott-Schwartz, J., Philips, M. R. and Kenworthy, A. K. (2005). Depalmitoylated Ras traffics to and from the Golgi complex via a nonvesicular pathway. J. Cell Biol. 170, 261-272.
18. Hancock, J. F., Magee, A. I., Childs, J. E. and Marshall, C. J. (1989). All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57, 1167-1177.
19. Hancock, J. F., Paterson, H. and Marshall, C. J. (1990). A polybasic domain or palmitylation is required in addition to the CAAX motif to localize p21ras to the plasma membrance. Cell 63, 133-139.
20. Hensch, T. K., Fagiolini, M., Mataga, N., Stryker, M. P., Baekkeskov, S. and Kash, S. (1998). Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504-1508.
21. Hirschberg, K., Miller, C. M., Ellenberg, J., Presley, J. F., Siggia, E. D., Phair, R. D. and Lippincott-Schwartz, J. (1998). Kinetic analysis of secretary protein traffic and characterization of Golgi to plasma membrance transport intermediates in living cells. J. Cell Biol. 143, 1485-1503.
22. Huang, K., Yanai, A., Kang, R., Arstikaitis, P., Singaraja, R. R., Metzler, M., Mullard, A., Haigh, B., Guathier-Campbell, C., Gutekunst, C. et al. (2004). Huntingtin-Interacting Protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins. Neuron 44, 977-986.
23. Kanaani, J., El-Husseini, A. E., Aguilera-Moreno, A., Diacovo, M. J., Bredt, D. S. and Baekkeskov, S. (2002). A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65. J. Cell Biol. 158, 1229-1238.
24. Kanaani, J., Diacovo, M. J., El-Husseini, A. E., Bredt, D. and Baekkeskov, S. (2004). Palmitoylation controls trafficking of GAD65 from Golgi membranes to axon-specific endosomes and a Rab5a-dependent pathway to presynaptic clusters. J. Cell Sci. 117, 2001-2013.
25. Kash, S. F., Johnson, R. S., Tecott, L. H., Noebels, J. L., Mayfield, R. D., Hanahan, D. and Baekkeskov, S. (1997). Epilepsy in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. USA 94, 14060-14065.
26. Kash, S. F., Tecott, L. H., Hodge, C. and Baekkeskov, S. (1999). Increased anxiety and altered responses to anxiolytics in mice deficient in the 65 kDa isoform of glutamic acid decarboxylase. Proc. Natl. Acad. Sci. USA 96, 1698-1703.
27. Klausner, R. D., Donaldson, J. G. and Lippincott-Schwartz, J. (1992). Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116, 1071-1080.
28. Lippincott-Schwartz, J., Yuan, L., Tipper, C., Amherdt, M., Orci, L. and Klausner, R. D. (1991). Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67, 601-616.
29. Michaelson, D., Aheran, I., Bergo, M., Young, S. and Phillips, M. (2002). Membrane trafficking of heterotrimeric G proteins via the endoplasmic reticulum and Golgi. Mol. Biol. Cell 13, 3294-3302.
30. Miesenböck, G., De Angelis, D. A. and Rothman, J. E. (1998). Visualizing secretion and synaptic transmission with pH-sensititve green fluorescent proteins. Nature 394, 192-195.
31. Namchuk, M., Lindsay, L. A., Turck, C. W., Kanaani, J. and Baekkeskov, S. (1997). Phosphorylation of Serine Residues 3, 6, 10, and 13 distinguishes membrane anchored from soluble glutamic acid decarboxylase 65 and is restricted to glutamic acid decarboxylase 65α. J. Biol. Chem. 272, 1548-1557.
32. Nichols, B. J., Kenworthy, A. K., Polishchuk, R. S., Lodge, R., Roberts, T. H., Hirschberg, K., Phair, R. D. and Lippincott-Schwartz, J. (2001). Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153, 529-541.
33. Patel, A. B., deGraaf, R. A., Martin, D. L., Battaglioli, G. and Behar, K. L. (2006). Evidence that GAD65 mediates increased GABA synthesis during intense neuronal activity in vivo. J. Neurochem. 97, 385-396.
34. Prior, I. A., Harding, A., Yan, J., Sluimer, J., Parton, R. G. and Hancock, J. F. (2001). GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat. Cell Biol. 3, 368-375.
35. Reetz, A., Solimena, M., Matteoli, M., Folli, F., Takei, K. and DeCamilli, P. (1991). GABA and pancreatic β-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic like microvesicles suggests their role in GABA storage and secretion. EMBO J. 10, 1275-1284.
36. Rocks, O., Peyker, A, Kahms, M., Verveer, P. J., Koerner, C., Lumbierres, M., Kuhlmann, J., Waldmann, H., Wittinghofer, A. and Bastiaens, P. I. H. (2005). An acylation cycle regulates localization and activity of palmitoylated ras isoforms. Science 307, 1746-1752.
37. Shahinian, S. and Silvius, J. R. (1995). Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membrances. Biochemistry 34, 3813-3822.
38. Shi, Y., Veit, B. and Baekkeskov, S. (1994). Amino acid residues 24-31 but not palmitoylation of cysteines 30 and 45 are required for membrane anchoring of glutamic acid decarboxylase, GAD65. J. Cell Biol. 124, 927-934.
39. Shimura, T., Watanabe, U., Yanagawa, Y. and Yamamoto, Y. (2004). Altered taste function in mice deficient in the 65-kDa isoform of glutamate. Neurosci. Lett. 356, 171-174.
40. Smotrys, J. E. and Linder, M. E. (2004). Palmitoylation of intracellular signaling proteins: regulation and function. Annu. Rev. Biochem. 73, 559-587.
41. Solimena, M., Folli, F., Aparisi, G., Pozza, G. and De Camilli, P. (1990). Autoantibodies to GABA-ergic neurons and pancreatic beta cells in stiff-man syndrome. N. Engl. J. Med. 322, 1555-1560.
42. Solimena, M., Dirkx, R., Radzynski, M., Mundigl, O. and De Camilli, P. (1994). A signal located within amino acids 1-27 of GAD65 is required for its targeting to the Golgi complex region. J. Cell Biol. 126, 331-341.
43. Stork, O., Ji, F. Y., Kaneko, K., Stork, S., Yoshinobu, Y., Moriya, T., Shibata, S. and Obata, K. (2000). Postnatal development of a GABA deficit and disturbance of neural functions in mice lacking GAD65. Brain Res. 865, 45-58.
44. Stork, O., Yamanaka, H., Stork, S., Kume, N. and Obata, K. (2003). Altered conditioned fear behavior in glutamate decarboxylase 65 null mutant mice. Genes Brain Behav. 2, 65-70.
45. Tian, N., Petersen, C., Kash, S., Baekkeskov, S., Copenhagen, D. and Nicoll, R. (1999). The role of the synthetic enzyme GAD65 in the control of neuronal γ-aminobutyric acid release. Proc. Natl. Acad. Sci. USA 96, 12911-12916.
46. Vasudevan, C., Han, W., Tan, Y., Nie, Y., Li, D., Shome, K., Watkins, S. C., Levitan, E. S. and Romero, G. (1998). The distribution and translocation of the G protein ADP-Ribosylation factor 1 in live cells is determined by its GTPase activity. J. Cell Sci. 111, 1277-1285.
47. Veit, M. and Schmidt, M. F. G. (2001). Enzymatic depalmitoylation of viral glycoproteins with acyl-protein thioesterase 1 in vitro. Virology 288, 89-95.
48. Ward, T. H., Polishchuk, R. S., Caplan, S., Hirschberg, K. and Lippincott-Schwartz, J. (2001). Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155, 557-570.
49. Wood, S. A., Park, J. E. and Brown, W. J. (1991). Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell 67, 591-600.
50. 2+ - calmodulin. J. Biol. Chem. 274, 33148-33154.