Calcium-modulating cyclophilin ligand regulates membrane trafficking of postsynaptic GABAA receptors

Molecular and Cellular Neuroscience

Volumn 38, Issue 2, 2008, Pages 277-289

  Yuan, Xu ^a   Yao, Jun ^a   Norris, David ^a   Tran, David D ^c,d   Bram, Richard J ^c,d   Chen, Gong ^a   Luscher, Bernhard ^a,b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

^d Mayo Clinic   (United States)

Author keywords

Calcium modulating cyclophilin ligand; Cyclophilin B; Endocytic recycling; Endoplasmic reticulum; Exocytosis; Inhibitory synapses; Protein trafficking

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BINDING PROTEIN; CALCIUM MODULATING CYCLOPHILIN LIGAND; CYCLOPHILIN; PROTEIN SUBUNIT;

ARTICLE; CONTROLLED STUDY; EMBRYO; GABAERGIC TRANSMISSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NERVE CELL; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CALCIUM; CELL LINE; CYCLOPHILINS; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HUMANS; KIDNEY; MICE; MICE, KNOCKOUT; NEURAL INHIBITION; NEURONS; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RECEPTORS, GABA-A; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 44649089921     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2008.03.002     Document Type: Article

References (41)

1. Alldred M.J., Mulder-Rosi J., Lingenfelter S.E., Chen G., and Luscher B. Distinct γ2 subunit domains mediate clustering and synaptic function of postsynaptic GABAA receptors and gephyrin. J. Neurosci. 25 (2005) 594-603
2. Baer K., Essrich C., Benson J.A., Benke D., Bluethmann H., Fritschy J.-M., and Luscher B. Postsynaptic clustering of GABAA receptors by the γ3 subunit in vivo. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 12860-12865
3. A receptor subtypes differentiated by their gamma-subunit variants: prevalence, pharmacology and subunit architecture. Neuropharmacology 35 (1996) 1413-1423
4. Benson J.A., Low K., Keist R., Mohler H., and Rudolph U. Pharmacology of recombinant γ-aminobutyric acidA receptors rendered diazepam-insensitive by point-mutated a-subunits. FEBS Lett. 431 (1998) 400-404
5. Bogdanov Y., Michels G., Armstrong-Gold C., Haydon P.G., Lindstrom J., Pangalos M., and Moss S.J. Synaptic GABA(A) receptors are directly recruited from their extrasynaptic counterparts. EMBO J. 25 (2006) 4381-4389
6. Bram R.J., and Crabtree G.R. Calcium signalling in T cells stimulated by a cyclophilin B-binding protein. Nature 371 (1994) 355-358
7. Chavas J., Forero M.E., Collin T., Llano I., and Marty A. Osmotic tension as a possible link between GABA(A) receptor activation and intracellular calcium elevation. Neuron 44 (2004) 701-713
8. Chen Z.W., and Olsen R.W. GABA Receptor Associated Proteins: a key factor regulating GABA receptor function. J. Neurochem. 100 (2007) 279-294
9. Chen Z.W., Chang C.S., Leil T.A., and Olsen R.W. C-terminal modification is required for GABARAP-mediated GABA(A) receptor trafficking. J. Neurosci. 27 (2007) 6655-6663
10. Crestani F., Lorez M., Baer K., Essrich C., Benke D., Laurent J.P., Belzung C., Fritschy J.M., Luscher B., and Mohler H. Decreased GABA(A)-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat. Neurosci. 2 (1999) 833-839
11. Earnheart J.C., Schweizer C., Crestani F., Iwasato T., Itohara S., Mohler H., and Luscher B. GABAergic control of adult hippocampal neurogenesis in relation to behavior indicative of trait anxiety and depression states. J. Neurosci. 27 (2007) 3845-3854
12. Ehlers M.D. Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28 (2000) 511-525
13. Essrich C., Lorez M., Benson J., Fritschy J.-M., and Luscher B. Postsynaptic clustering of major GABA(A) receptor subtypes requires the γ2 subunit and gephyrin. Nat. Neurosci. 1 (1998) 563-571
14. Fang C., Deng L., Keller C.A., Fukata M., Fukata Y., Chen G., and Luscher B. GODZ-mediated palmitoylation of GABA(A) receptors is required for normal assembly and function of GABAergic inhibitory synapses. J. Neurosci. 26 (2006) 12758-12768
15. Fritschy J.-M., and Brunig I. Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol. Ther. 98 (2003) 299-323
16. Harlow E., and Lane D. Antibodies: A Laboratory Manual (1988), Cold Spring Harbor Laboratory, Cold Spring Harbor
17. Hayashi S., and McMahon A.P. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244 (2002) 305-318
18. Holloway M.P., and Bram R.J. A hydrophobic domain of Ca2+-modulating cyclophilin ligand modulates calcium influx signaling in T lymphocytes. J. Biol. Chem. 271 (1996) 8549-8552
19. Holloway M.P., and Bram R.J. Co-localization of calcium-modulating cyclophilin ligand with intracellular calcium pools. J. Biol. Chem. 273 (1998) 16346-16350
20. Jiang M., and Chen G. High Ca2+-phosphate transfection efficiency in low-density neuronal cultures. Nat. Protoc. 1 (2006) 695-700
21. Kabeya Y., Mizushima N., Yamamoto A., Oshitani-Okamoto S., Ohsumi Y., and Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 117 (2004) 2805-2812
22. A receptors is a substrate for palmitoylation by GODZ. J. Neurosci. 24 (2004) 5881-5891
23. Kim H.S., Morales V.M., Dass C., Encinas J., Teitell M., and Blumberg R.S. Cloning of the gene encoding the mouse homologue of the human calcium signal-modulating ligand. Gene 163 (1995) 323-324
24. Kittler J.T., Thomas P., Tretter V., Bogdanov Y.D., Haucke V., Smart T.G., and Moss S.J. Huntingtin-associated protein 1 regulates inhibitory synaptic transmission by modulating gamma-aminobutyric acid type A receptor membrane trafficking. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 12736-12741
25. Lee S.J., Drabik K., and Benveniste E.N. Cloning of rat calcium-modulating cyclophilin ligand. DNA Seq. 12 (2001) 209-213
26. Li R.W., Yu W., Christie S., Miralles C.P., Bai J., Loturco J.J., and De Blas A.L. Disruption of postsynaptic GABA receptor clusters leads to decreased GABAergic innervation of pyramidal neurons. J. Neurochem. 95 (2005) 756-770
27. A receptor trafficking and channel activity in functional plasticity of inhibitory synapses. Pharmacol. Ther. 102 (2004) 195-221
28. A-receptor expressed from rat brain alpha- and beta-subunit cDNAs displays potentiation by benzodiazepine receptor ligands. Mol. Brain Res. 8 (1990) 199-208
29. Marsden K.C., Beattie J.B., Friedenthal J., and Carroll R.C. NMDA receptor activation potentiates inhibitory transmission through GABA receptor-associated protein-dependent exocytosis of GABA(A) receptors. J. Neurosci. 27 (2007) 14326-14337
30. Mattioni T., Louvion J.F., and Picard D. Regulation of protein activities by fusion to steroid binding domains. Methods Cell Biol. 43 (1994) 335-352 Pt A
31. Moss S.J., and Smart T.G. Constructing inhibitory synapses. Nat. Rev., Neurosci. 2 (2001) 240-250
32. Qi J., Yao J., Fang C., Luscher B., and Chen G. Downregulation of tonic GABA currents following epileptogenic stimulation of rat hippocampal cultures. J. Physiol. 577 (2006) 579-590
33. Rathenberg J., Kittler J.T., and Moss S.J. Palmitoylation regulates the clustering and cell surface stability of GABAA receptors. Mol. Cell. Neurosci. 26 (2004) 251-257
34. A receptors is required for maintenance of receptors at mature synapses. Mol. Cell. Neurosci. 24 (2003) 442-450
35. Tran D.D., Russell H.R., Sutor S.L., van Deursen J., and Bram R.J. CAML is required for efficient EGF receptor recycling. Dev. Cell 5 (2003) 245-256
36. Tran D.D., Edgar C.E., Heckman K.L., Sutor S.L., Huntoon C.J., van Deursen J., McKean D.L., and Bram R.J. CAML is a p56Lck-interacting protein that is required for thymocyte development. Immunity 23 (2005) 139-152
37. Tretter V., Jacob T.C., Mukherjee J., Fritschy J.M., Pangalos M.N., and Moss S.J. The clustering of GABA(A) receptor subtypes at inhibitory synapses is facilitated via the direct binding of receptor alpha2 subunits to gephyrin. J. Neurosci. 28 (2008) 1356-1365
38. von Bulow G.U., and Bram R.J. NF-AT activation induced by a CAML-interacting member of the tumor necrosis factor receptor superfamily. Science 278 (1997) 138-141
39. A-receptor-associated protein links GABAA receptors and the cytoskeleton. Nature 397 (1999) 69-72
40. Wang J., Liu S., Haditsch U., Tu W., Cochrane K., Ahmadian G., Tran L., Paw J., Wang Y., Mansuy I., Salter M.M., and Lu Y.M. Interaction of calcineurin and type-A GABA receptor gamma2 subunits produces long-term depression at CA1 inhibitory synapses. J. Neurosci. 23 (2003) 826-836
41. Yao J., Qi J., and Chen G. Actin-dependent activation of presynaptic silent synapses contributes to long-term synaptic plasticity in developing hippocampal neurons. J. Neurosci. 26 (2006) 8137-8147