Regulation of GABA neurotransmission by glutamic acid decarboxylase (GAD)

Current Pharmaceutical Design

Volumn 21, Issue 34, 2015, Pages 4939-4942

  Modi, Jigar Pravinchandra ^a,b   Prentice, Howard ^a,b   Wu, Jang Yen ^a,b,c  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

^b FLORIDA ATLANTIC UNIVERSITY   (United States)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Calpain; GABA neurotransmission; Glutamic acid decarboxylase; Palmitoylation; Phosphorylation; Vesicular GABA release

Indexed keywords

4 AMINOBUTYRIC ACID; CALPAIN 1; CYSTEINE; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; CALPAIN; GLUTAMATE DECARBOXYLASE 1; GLUTAMATE DECARBOXYLASE 2; MU-CALPAIN;

ARTICLE; BRAIN INJURY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GABAERGIC TRANSMISSION; GENETIC TRANSCRIPTION; HUMAN; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROCESSING; RNA SPLICING; SYNAPSE VESICLE; ANIMAL; CEREBROVASCULAR ACCIDENT; METABOLISM; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; CALPAIN; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HUMANS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; STROKE; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 84947998102     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612821666150917094343     Document Type: Article

References (44)

1. Somogyi R, Wen X, Ma W, Barker JL. Developmental kinetics of GAD family mRNAs parallel neurogenesis in the rat spinal cord. J Neurosci 1995; 15: 2575-91.
2. Behar T, Schaffner A, Laing P, Hudson L, Komoly S, Barker J. Many spinal cord cells transiently express low molecular weight forms of glutamic acid decarboxylase during embryonic development. Brain Res Dev Brain Res 1993; 72: 203-18.
3. Pinal CS, Tobin AJ. Uniqueness and redundancy in GABA production. Perspect Dev Neurobiol 1998; 5: 109-18.
4. Wei J, Wu JY. Post-translational regulation of L-glutamic acid decarboxylase in the brain. Neurochem Res 2008; 33: 1459-65.
5. Wei J, Jin Y, Wu H, Sha D, Wu JY. Identification and functional analysis of truncated human glutamic acid decarboxylase 65. J Biomed Sci 2003; 10: 617-24.
6. Christgau S, Aanstoot HJ, Schierbeck H, et al. Membrane anchoring of the autoantigen GAD65 to microvesicles in pancreatic betacells by palmitoylation in the NH2-terminal domain. J Cell Biol 1992; 118: 309-20.
7. Sha D, Wei J, Wu H, Jin Y, Wu JY. Molecular cloning, expression, purification, and characterization of shorter forms of human glutamic decarboxylase 67 in an E. coli expression system. Brain Res Mol Brain Res 2005; 136: 255-61.
8. Sha D, Jin Y, Wu H, et al. Role of mu-calpain in proteolytic cleavage of brain L-glutamic acid decarboxylase. Brain Res 2008; 1207: 9-18.
9. Wei J, Lin CH, Wu H, Jin Y, Lee YH, Wu JY. Activity-dependent cleavage of brain glutamic acid decarboxylase 65 by calpain. J Neurochem 2006; 98: 1688-95.
10. Buddhala C, Suarez M, Modi J, et al. Calpain cleavage of brain glutamic acid decarboxylase 65 is pathological and impairs GABA neurotransmission. Smalheiser NR, editor. PLoS One 2012; 7: e33002.
11. De Graauw M, Hensbergen P, van de Water B. Phospho-proteomic analysis of cellular signaling. Electrophoresis 2006; 27: 2676-86.
12. Wei J, Davis KM, Wu H, Wu JY. Protein phosphorylation of human brain glutamic acid decarboxylase (GAD)65 and GAD67 and its physiological implications. Biochemistry 2004; 43: 6182-9.
13. Namchuk M, Lindsay L, Turck CW, Kanaani J, Baekkeskov S. 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 65alpha. J Biol Chem 1997; 272: 1548-57.
14. Wu JY, Roberts E. Properties of brain L-glutamate decarboxylase: inhibition studies. J Neurochem 1974; 23: 759-67.
15. Wei J, Wu J-Y. Structural and functional analysis of cysteine residues in human glutamate decarboxylase 65 (GAD65) and GAD67. J Neurochem 2005; 93: 624-33.
16. Fenalti G, Law RHP, Buckle AM, et al. GABA production by glutamic acid decarboxylase is regulated by a dynamic catalytic loop. Nat Struct Mol Biol 2007; 14: 280-6.
17. Battaglioli G, Liu H, Martin DL. Kinetic differences between the isoforms of glutamate decarboxylase: implications for the regulation of GABA synthesis. J Neurochem 2003; 86: 879-87.
18. Grattan DR, Rocca MS, Strauss KI, Sagrillo CA, Selmanoff M, McCarthy MM. GABAergic neuronal activity and mRNA levels for both forms of glutamic acid decarboxylase (GAD65 and GAD67) are reduced in the diagonal band of Broca during the afternoon of proestrus. Brain Res 1996; 733: 46-55.
19. Schmidli RS, Faulkner-Jones BE, Harrison LC, James RF, DeAizpurua HJ. Cytokine regulation of glutamate decarboxylase biosynthesis in isolated rat islets of Langerhans. Biochem J 1996; 317(Pt 3): 713-9.
20. Laprade N, Soghomonian JJ. Differential regulation of mRNA levels encoding for the two isoforms of glutamate decarboxylase (GAD65 and GAD67) by dopamine receptors in the rat striatum. Mol Brain Res 1995; 34: 65-74.
21. Laprade N, Soghomonian JJ. MK-801 decreases striatal and cortical GAD65 mRNA levels. Neuroreport 1995; 6: 1885-9.
22. Rimvall K, Martin DL. The level of GAD67 protein is highly sensitive to small increases in intraneuronal gamma-aminobutyric acid levels. J Neurochem 1994; 62: 1375-81.
23. Kanaani J, Diacovo MJ, El-Husseini AE-D, Bredt DS, Baekkeskov S. Palmitoylation controls trafficking of GAD65 from Golgi membranes to axon-specific endosomes and a Rab5a-dependent pathway to presynaptic clusters. J Cell Sci 2004; 117: 2001-13.
24. Kanaani J, Patterson G, Schaufele F, Lippincott-Schwartz J, Baekkeskov S. A palmitoylation cycle dynamically regulates partitioning of the GABA-synthesizing enzyme GAD65 between ER-Golgi and post-Golgi membranes. J Cell Sci 2008; 121: 437-49.
25. Dirkx R, Thomas A, Li L, Lernmark K, et al. Targeting of the 67- kDa isoform of glutamic acid decarboxylase to intracellular organelles is mediated by its interaction with the NH(2)-terminal region of the 65-kDa isoform of glutamic acid decarboxylase. J Biol Chem 1995; 270: 2241-6.
26. Kanaani J. The hydrophilic isoform of glutamate decarboxylase, GAD67, is targeted to membranes and nerve terminals independent of dimerization with the hydrophobic membrane-anchored isoform, GAD65. J Biol Chem 1999; 274: 37200-9.
27. Lernmark A. Glutamic acid decarboxylase--gene to antigen to disease. J Intern Med 1996; 240: 259-77.
28. Dietrich LEP, Ungermann C. On the mechanism of protein palmitoylation. EMBO Rep 2004; 5: 1053-7.
29. Noritake J, Fukata Y, Iwanaga T, et al. Mobile DHHC palmitoylating enzyme mediates activity-sensitive synaptic targeting of PSD- 95. J Cell Biol 2009; 186: 147-60.
30. Modi J, Prentice H, Wu J-Y. Regulation of GABA synthesis and transport. In: Vlainic J, Jembrek MJ, Eds. Gamma-Aminobutyric Acid (GABA): Biosynthesis, Medicinal Uses and Health Effects. New York: Nova Science Publishers, Inc. 2014; pp. 1-12.
31. Huang K, Sanders S, Singaraja R, et al. Neuronal palmitoyl acyl transferases exhibit distinct substrate specificity. FASEB J 2009; 23: 2605-15.
32. Singaraja RR. HIP14, a novel ankyrin domain-containing protein, links huntingtin to intracellular trafficking and endocytosis. Hum Mol Genet 2002; 11: 2815-28.
33. Huang K, Yanai A, Kang R, et al. Huntingtin-interacting protein HIP14 is a palmitoyl transferase involved in palmitoylation and trafficking of multiple neuronal proteins. Neuron 2004; 44: 977-86.
34. Rush DB, Leon RT, McCollum MH, Treu RW, Wei J. Palmitoylation and trafficking of GAD65 are impaired in a cellular model of Huntington's disease. Biochem J 2012; 442: 39-48.
35. Liu J, Liu MC, Wang KKW. Calpain in the CNS: from synaptic function to neurotoxicity. Sci Signal 2008; 1: re1.
36. Vosler PS, Brennan CS, Chen J. Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration. Mol Neurobiol 2008; 38: 78-100.
37. Wang K. Calpain and caspase: can you tell the difference?, by kevin K.W. WangVol. 23, pp. 20-26. Trends Neurosci 2000; 23: 59.
38. Blomgren K, Zhu C, Wang X, et al. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis"? J Biol Chem 2001; 276: 10191-8.
39. Bizat N, Hermel J-M, Humbert S, et al. In vivo calpain/caspase cross-talk during 3-nitropropionic acid-induced striatal degeneration: implication of a calpain-mediated cleavage of active caspase- 3. J Biol Chem 2003; 278: 43245-53.
40. Ray SK, Patel SJ, Welsh CT, Wilford GG, Hogan EL, Banik NL. Molecular evidence of apoptotic death in malignant brain tumors including glioblastoma multiforme: upregulation of calpain and caspase-3. J Neurosci Res 2002; 69: 197-206.
41. Blomgren K, Zhu C, Wang X, et al. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis"? J Biol Chem 2001; 276: 10191-8.
42. Jin H, Wu H, Osterhaus G, et al. Demonstration of functional coupling between gamma -aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc Natl Acad Sci USA 2003; 100: 4293-8.
43. Ray SK, Banik NL. Calpain and its involvement in the pathophysiology of CNS injuries and diseases: therapeutic potential of calpain inhibitors for prevention of neurodegeneration. Curr Drug Targets CNS Neurol Disord 2003; 2: 173-89.
44. Crocker SJ, Smith PD, Jackson-Lewis V, et al. Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of Parkinson's disease. J Neurosci 2003; 23: 4081-91.