Dystroglycan mediates homeostatic synaptic plasticity at GABAergic synapses

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

Volumn 111, Issue 18, 2014, Pages 6810-6815

  Pribiag, Horia ^a   Peng, Huashan ^a   Shah, Waris Ali ^a   Stellwagen, David ^a   Carbonetto, Salvatore ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

AMPA receptors; Dystrophin; Excitation inhibition balance; Muscular dystrophy; Retardation

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; AGRIN; BICUCULLINE; DYSTROGLYCAN; GLYCOSYLTRANSFERASE; TETRODOTOXIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GABAERGIC SYSTEM; GLYCOSYLATION; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; RNA INTERFERENCE; SCALE UP; SYNAPSE; SYNAPTIC TRANSMISSION; UPREGULATION;

AMPA RECEPTORS; DYSTROPHIN; EXCITATION-INHIBITION BALANCE; MUSCULAR DYSTROPHY; RETARDATION;

AGRIN; ANIMALS; DYSTROGLYCANS; FEMALE; GABAERGIC NEURONS; GLYCOSYLATION; HIPPOCAMPUS; HOMEOSTASIS; HUMANS; MALE; MICE; MICE, INBRED MDX; MUSCULAR DYSTROPHY, ANIMAL; MUTATION; N-ACETYLGLUCOSAMINYLTRANSFERASES; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RNA INTERFERENCE; RNA, SMALL INTERFERING; SYNAPSES;

EID: 84899875212     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321774111     Document Type: Article

References (45)

1. Hendriksen JG, Vles JS (2008) Neuropsychiatric disorders in males with D uchenne muscular dystrophy: Frequency rate of attention-deficit hyperactivity disorder (ADHD), autism spectrum disorder, and obsessive-compulsive disorder. J Child Neurol 23(5):477-481.
2. Pane M, et al. (20 13) Duchenne muscular dystrophy and epilepsy. Neuromuscul Disord 23(4):313-315.
3. Mehler MF (2000) Brain dystrophin, neurogenetics and mental retardation. Brain Res Brain Res Rev 32(1):277-307.
4. Godfrey C, Foley AR, Clement E, Muntoni F (2011) Dystroglycanopathies: Coming into focus. Curr Opin Genet Dev 21(3):278-285.
5. Waite A, Brown S C, Blake DJ (2012) The dystrophin-glycoprotein complex in brain development and disease. Trends Neurosci 35(8):487-496.
6. Gee SH, Montanaro F, Lindenbaum MH, Carbonetto S (1994) Dystroglycan-alpha, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77(5):675-686.
7. Wr ight KM, et al. (2012) Dystroglycan organizes axon guidance cue localization and axonal pathfinding. Neuron 76(5):931-944.
8. Sato S, et al. (2008) Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat Neurosci 11(8):923-931.
9. Sugita S, et al. (2001) A stoichiometric complex of neurexins and dystroglycan in brain. J Cell Biol 154(2):435-445.
10. Peng HB, Xie H, Rossi SG, Rotundo RL (1999) Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J Cell Biol 145(4):91 1-921.
11. Yoshida-Moriguchi T, et al. (2010) O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science 327(5961):88-92.
12. Moore CJ, Hewitt J E (2009) Dystroglycan glycosylation and muscular dystrophy. Glycoconj J 26(3):349-357.
13. Smalheiser NR, Schwartz NB (1987) Cranin: A laminin-binding protein of cell membranes. Proc Natl Acad Sci USA 84(18):6457-6461.
14. Moore SA, et al. (2002) Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418(6896):422-425.
15. Jacobson C, Cô téPD, Rossi SG, Rotundo RL, Carbonetto S (2001) The dystroglycan complex is necessary for stabilization of acetylcholine receptor clusters at neuromuscular junctions and formation of the synapti c basement membrane. J Cell Biol 152(3):435-450.
16. Knuesel I, et al. (1999) Short communication: Altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice). Eur J Neurosci 11(12):4457-4462.
17. Lévi S, et al. (2002) Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci 22(11):4274-4285.
18. Sekiguchi M, et al. (2009) A deficit of brain dystrophin impairs specific amygdala GABAergic transmission and enhances defensive behaviour in mice. Brain 132(Pt 1): 124-135.
19. Vaillend C, et al. (2010) Rescue of a dystrophin-like protein by exon skipping in vivo restores GABAA-receptor clustering in the hippocampus of the mdx mouse. Mol Ther 18(9):1683-1688.
20. Kueh SL, Head SI, Morley JW (2008) GABA(A) receptor expression and inhibitory postsynaptic currents in cerebellar Purkinje cells in dystrophin-deficient mdx mice. Clin Exp Pharmacol Physiol 35(2):2 07-210.
21. Turrigiano G (2012 Homeostatic synaptic plasticity: Local and global mechanisms for stabilizing neuronal function Cold Spring Harb Perspect Biol 4 1 a005736
22. Rannal s MD, Kapur J (2011) Homeostatic strengthening of inhibitory synapses is mediated by the accumulation of GABA(A) receptors. J Neurosci 31(48):17701-17712.
23. Peng YR, et al. (2010) Postsynapti c spiking homeostatically induces cell-autonomous regulation of inhibitory inputs via retrograde signaling. J Neurosci 30(48):16220-16231.
24. Ervasti JM, Campbell KP (1993) A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122(4):809-823.
25. Ibraghimov-Beskrovnaya O, et al. (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355(6362):696-702.
26. Grewal PK, Holzfeind PJ, Bittner RE, Hewitt JE (2001) Mutant glycosyltransferase and altered glycosylatio n of alpha-dystroglycan in the myodystrophy mouse. Nat Genet 28(2):151-154.
27. Adams ME, Anderson KN, Froehner SC (2010) The alpha-syntrophin PH and PDZ domains scaffold acetylcholine receptors, ut rophin, and neuronal nitric oxide synthase at the neuromuscular junction. J Neurosci 30(33):11004-11010.
28. Marty S, WehrléR, Fritschy JM, Sotelo C (2004) Quantitative effects produced by modifications of neuronal activity on the size of GABAA receptor clusters in hippocampal slice cultures. Eur J Neurosci 20(2):427-440.
29. Costa-Mattioli M, Sossin WS, Klann E, Sonenberg N (2009) Translational control of long-lasting synaptic plasticity and memory. Neuron 61(1):10-26.
30. Goddeeris MM, et al. (2013) LARGE glycans on dystroglycan function as a tunable matrix scaffold to prevent dystrophy. Nature 503(7474):136-140.
31. Inamori K, et al. (2012) Dystroglycan function requires xylosyl-and glucuronyltransferase activities of LARGE. Science 335(6064):93-96.
32. Barresi R, et al. (2004) LARGE can functionally bypass alpha-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat Med 10(7):696-703.
33. CôtéPD, Moukhles H, Lindenbaum M, Carbonetto S (1999) Chimaeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneural synapses. Nat Genet 23(3):338-342.
34. Kummer TT, Misgeld T, Sanes JR (2006) Assembly of the postsynaptic membrane at the neuromuscular junction: Paradigm lost. Curr Opin Neurobiol 16(1):74-82.
35. Matsumoto-Miyai K, et al. (2009) Coincident pre-and postsynaptic activation induces dendritic filopodia via neurotrypsin-dependent agrin cleavage. Cell 136(6):1161-1171.
36. Ferreira A (1999) Abnormal sy napse formation in agrin-depleted hippocampal neurons. J Cell Sci 112(Pt 24):4729-4738.
37. Sumita K, et al. (2007) Synaptic scaffolding molecule (S-SCAM) membrane-associated guanylate kinase with inverted or ganization (MAGI)-2 is associated with cell adhesion molecules at inhibitory synapses in rat hippocampal neurons. J Neurochem100(1):154-166.
38. Gingras J, Rassadi S, Cooper E, Ferns M (2007) Synaptic transmission is impaired at neuronal autonomic synapses in agrin-null mice. Dev Neurobiol 67(5):521-534.
39. Daniels MP (2012) The role of agrin in synaptic development, plasticity and signaling in the central nervous system. Neurochem Int 61(6):848-853.
40. Montanaro F, et al. (1998) Laminin and alpha-dystroglycan mediate acetylcholine receptor aggregation via a MuSK-independent pathway. J Neurosci 18(4):1250-1260.
41. De Sarro G, et al. (2004) Seizure susceptibility to various convulsant stimuli in dystrophin-deficient mdx mice. Neurosci Res 50(1):37-44.
42. Yizhar O et al. (2011 Neocortical excitation/inhibition balance in information processing and social dysfunction Nature 477 7363 171-178
43. Vitureira N, Goda Y (2013) Cel l biology in neuroscience: The interplay between Hebbian and homeostatic synaptic plasticity. J Cell Biol 203(2):175-186.
44. Seeburg DP, Sheng M (2008) Activity-induced Polo-like kinase is required for homeostatic plasticity of hippocampal neurons during epileptiform activity. J Neurosci 28(26):6583-6591.
45. Dallérac G, et al. (2011) Rescue of a dystrophin-like protein by exon skipping normalizes synaptic plasticity in the hippocampus of the mdx mouse. Neurobiol Dis 43(3): 635-641.