Giant ankyrin-G stabilizes somatodendritic GABAergic synapses through opposing endocytosis of GABAA receptors

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 4, 2015, Pages 1214-1219

  Tseng, Wei Chou ^a   Jenkins, Paul M ^a,b   Tanaka, Masashi ^a   Mooney, Richard ^a   Bennett, Vann ^a,b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

Extrasynaptic membrane; GABAA receptor endocytosis; GABAergic synapses; GABARAP; Giant ankyrin G

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ANKYRIN; ANKYRIN G; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; ANK3 PROTEIN, MOUSE; CYTOSKELETON PROTEIN; GABARAP PROTEIN, MOUSE; MEMBRANE PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL MEMBRANE; CELL SPECIFICITY; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DENDRITIC CELL; ENDOCYTOSIS; GABAERGIC SYSTEM; INTERNEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY; PYRAMIDAL NERVE CELL; SYNAPSE; SYNAPTIC MEMBRANE; ANIMAL; GENETICS; HUMAN; MENTAL DISEASE; METABOLISM; PATHOLOGY;

ANIMALS; ANKYRINS; CYTOSKELETAL PROTEINS; ENDOCYTOSIS; GABAERGIC NEURONS; HUMANS; MEMBRANE PROTEINS; MENTAL DISORDERS; MICE; PYRAMIDAL CELLS; RECEPTORS, GABA-A; SYNAPTIC MEMBRANES;

EID: 84921932679     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1417989112     Document Type: Article

References (40)

1. + GABAergic interneurons: From cellular design to microcircuit function. Science 345(6196):1255263.
2. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science 321(5885):53-57.
3. Luscher B, Fuchs T, Kilpatrick CL (2011) GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 70(3):385-409.
4. Bogdanov Y, et al. (2006) Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J 25(18):4381-4389.
5. Kittler JT, et al. (2000) Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci 20(21):7972-7977.
6. Thomas P, Mortensen M, Hosie AM, Smart TG (2005) Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nat Neurosci 8(7):889-897.
7. Fuchs C, et al. (2013) GABA(A) receptors can initiate the formation of functional inhibitory GABAergic synapses. Eur J Neurosci 38(8):3146-3158.
8. Kole MH, Stuart GJ (2012) Signal processing in the axon initial segment. Neuron 73(2):235-247.
9. Muir J, Kittler JT (2014) Plasticity of GABAA receptor diffusion dynamics at the axon initial segment. Front Cell Neurosci 8:151.
10. Blot A, Barbour B (2014) Ultra-rapid axon-axon ephaptic inhibition of cerebellar Purkinje cells by the pinceau. Nat Neurosci 17(2):289-295.
11. Ango F, et al. (2004) Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119(2):257-272.
12. Kriebel M, et al. (2011) The cell adhesion molecule neurofascin stabilizes axo-axonic GABAergic terminals at the axon initial segment. J Biol Chem 286(27):24385-24393.
13. Zhou D, et al. (1998) AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol 143(5):1295-1304.
14. Bennett V, Lorenzo DN (2013) Spectrin- and ankyrin-based membrane domains and the evolution of vertebrates. Curr Top Membr 72:1-37.
15. Kordeli E, Lambert S, Bennett V (1995) Ankyrin G. A new ankyrin gene with neuralspecific isoforms localized at the axonal initial segment and node of Ranvier. J Biol Chem 270(5):2352-2359.
16. Jenkins PM, et al. (2014) Giant ankyrin-G was a critical innovation in vertebrate evolution of fast and integrated neuronal signaling. Proc Natl Acad Sci USA 112:957-964.
17. Jones SL, Korobova F, Svitkina T (2014) Axon initial segment cytoskeleton comprises a multiprotein submembranous coat containing sparse actin filaments. J Cell Biol 205(1):67-81.
18. Yoshimura T, Rasband MN (2014) Axon initial segments: Diverse and dynamic neuronal compartments. Curr Opin Neurobiol 27:96-102.
19. Iqbal Z, et al. (2013) Homozygous and heterozygous disruptions of ANK3: At the crossroads of neurodevelopmental and psychiatric disorders. Hum Mol Genet 22(10):1960-1970.
20. Jenkins PM, et al. (2013) E-cadherin polarity is determined by a multifunction motif mediating lateral membrane retention through ankyrin-G and apical-lateral transcytosis through clathrin. J Biol Chem 288(20):14018-14031.
21. Smith KR, et al. (2014) Psychiatric Risk Factor ANK3/Ankyrin-G Nanodomains Regulate the Structure and Function of Glutamatergic Synapses. Neuron 84(2):399-415.
22. He M, Abdi KM, Bennett V (2014) Ankyrin-G palmitoylation and βII-spectrin binding to phosphoinositide lipids drive lateral membrane assembly. J Cell Biol 206(2):273-288.
23. Leil TA, Chen ZW, Chang CS, Olsen RW (2004) GABAA receptor-associated protein traffics GABAA receptors to the plasma membrane in neurons. J Neurosci 24(50):11429-11438.
24. Wang H, Bedford FK, Brandon NJ, Moss SJ, Olsen RW (1999) GABA(A)-receptorassociated protein links GABA(A) receptors and the cytoskeleton. Nature 397(6714):69-72.
25. Chen L, Wang H, Vicini S, Olsen RW (2000) The gamma-aminobutyric acid type A (GABAA) receptor-associated protein (GABARAP) promotes GABAA receptor clustering and modulates the channel kinetics. Proc Natl Acad Sci USA 97(21):11557-11562.
26. Mansuy V, et al. (2004) GEC1, a protein related to GABARAP, interacts with tubulin and GABA(A) receptor. Biochem Biophys Res Commun 325(2):639-648.
27. Chen ZW, Olsen RW (2007) GABAA receptor associated proteins: A key factor regulating GABAA receptor function. J Neurochem 100(2):279-294.
28. Söderberg O, et al. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 3(12):995-1000.
29. Alemu EA, et al. (2012) ATG8 family proteins act as scaffolds for assembly of the ULK complex: Sequence requirements for LC3-interacting region (LIR) motifs. J Biol Chem 287(47):39275-39290.
30. Birgisdottir AB, Lamark T, Johansen T (2013) The LIR motif - crucial for selective autophagy. J Cell Sci 126(Pt 15):3237-3247.
31. Nusser Z, Sieghart W, Somogyi P (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18(5):1693-1703.
32. Chandra D, et al. (2006) GABAA receptor alpha 4 subunits mediate extrasynaptic inhibition in thalamus and dentate gyrus and the action of gaboxadol. Proc Natl Acad Sci USA 103(41):15230-15235.
33. Kittler JT, et al. (2005) Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci USA 102(41):14871-14876.
34. Goodkin HP, Yeh JL, Kapur J (2005) Status epilepticus increases the intracellular accumulation of GABAA receptors. J Neurosci 25(23):5511-5520.
35. O'Sullivan GA, Kneussel M, Elazar Z, Betz H (2005) GABARAP is not essential for GABA receptor targeting to the synapse. Eur J Neurosci 22(10):2644-2648.
36. Kneussel M, et al. (2000) The gamma-aminobutyric acid type A receptor (GABAAR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc Natl Acad Sci USA 97(15):8594-8599.
37. Lai HC, Jan LY (2006) The distribution and targeting of neuronal voltage-gated ion channels. Nat Rev Neurosci 7(7):548-562.
38. Mohrlüder J, Hoffmann Y, Stangler T, Hänel K, Willbold D (2007) Identification of clathrin heavy chain as a direct interaction partner for the gamma-aminobutyric acid type A receptor associated protein. Biochemistry 46(50):14537-14543.
39. Ferreira MA, et al.; Wellcome Trust Case Control Consortium (2008) Collaborative genome-wide association analysis supports a role for ANK3 and CACNA1C in bipolar disorder. Nat Genet 40(9):1056-1058.
40. He M, Tseng WC, Bennett V (2013) A single divergent exon inhibits ankyrin-B association with the plasma membrane. J Biol Chem 288(21):14769-14779.