Neuronal dystroglycan is necessary for formation and maintenance of functional CCK-positive basket cell terminals on pyramidal cells

Journal of Neuroscience

Volumn 36, Issue 40, 2016, Pages 10296-10313

  Früh, Simon ^a   Romanos, Jennifer ^a   Panzanelli, Patrizia ^b   Bürgisser, Daniela ^c   Tyagarajan, Shiva K ^a   Campbell, Kevin P ^d   Santello, Mirko ^a   Fritschy, Jean Marc ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF TURIN   (Italy)

^c ETH ZURICH   (Switzerland)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

Cholecystokinin; Dystroglycanopathy; Dystrophin glycoprotein complex; GABA; Interneurons; Perisomatic

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CARBACHOL; CHOLECYSTOKININ; DYSTROGLYCAN; NEUREXIN; SYNAPTOTAGMIN II; 4 AMINOBUTYRIC ACID; MUSCARINIC AGENT; NERVE CELL ADHESION MOLECULE; NRXN1 PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BASKET CELL; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; FEMALE; GENOTYPE; GRANULE CELL; HIPPOCAMPAL CA1 REGION; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MUSCULAR DYSTROPHY; NEOCORTEX; NERVE ENDING; NONHUMAN; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; STEREOLOGY; SYNAPSE; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CHOLINERGIC SYSTEM; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE TARGETING; GENETICS; INTERNEURON; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; CARBACHOL; CHOLECYSTOKININ; DYSTROGLYCANS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GAMMA-AMINOBUTYRIC ACID; GENE KNOCK-IN TECHNIQUES; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCARINIC AGONISTS; NEURAL CELL ADHESION MOLECULES; PARASYMPATHETIC NERVOUS SYSTEM; PRESYNAPTIC TERMINALS; PYRAMIDAL CELLS;

EID: 84990852269     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1823-16.2016     Document Type: Article

References (35)

1. Bartos M, Elgueta C (2012) Functional characteristics of parvalbumin-and cholecystokinin-expressing basket cells. J Physiol 590: 669-681. CrossRef Medline
2. Brünig I, Suter A, Knuesel I, Lüscher B, Fritschy JM (2002) GABAergic terminals are required for postsynaptic clustering of dystrophin but not of GABA(A) receptors and gephyrin. J Neurosci 22: 4805-4813. Medline
3. Dinçer P, Balci B, Yuva Y, Talim B, Brockington M, Dinçel D, Torelli S, Brown S, Kale G, Haliloglu G, Gerçeker FO, Atalay RC, Yakicier C, Longman C, Muntoni F, Topaloglu H (2003) A novel form of recessive limb girdle muscular dystrophy with mental retardation and abnormal expression of alpha-dystroglycan. Neuromuscul Disord 13: 771-778. CrossRef Medline
4. Fishell G, Rudy B (2011) Mechanisms of inhibition within the telencephalon:"where the wild things are." Annu Rev Neurosci 34: 535-567. CrossRef Medline
5. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56: 33-42. CrossRef Medline
6. Fritschy JM, Mohler H (1995) GABAA-receptor heterogeneity in the adult rat brain: Differential regional and cellular distribution of seven major subunits. J Comp Neurol 359: 154-194. CrossRef Medline
7. Fuccillo MV, Földy C, Gökce Ö, Rothwell PE, Sun GL, Malenka RC, Südhof TC (2015) Single-cell mRNA profiling reveals cell-type-specific expression of neurexin isoforms. Neuron 87: 326-340. CrossRef Medline
8. Fukaya M, Kamata A, Hara Y, Tamaki H, Katsumata O, Ito N, Takeda S, Hata Y, Suzuki T, Watanabe M, Harvey RJ, Sakagami H (2011) SynArfGEF is a guanine nucleotide exchange factor for Arf6 and localizes preferentially at post-synaptic specializations of inhibitory synapses. J Neurochem 116: 1122-1137. CrossRef Medline
9. Godfrey C, Clement E, Mein R, Brockington M, Smith J, Talim B, Straub V, Robb S, Quinlivan R, Feng L, Jimenez-Mallebrera C, Mercuri E, Manzur AY, Kinali M, Torelli S, Brown SC, Sewry CA, Bushby K, Topaloglu H, North K, et al. (2007) Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan. Brain 130: 2725-2735. CrossRef Medline
10. Goebbels S, Bormuth I, Bode U, Hermanson O, Schwab MH, Nave KA (2006) Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 44: 611-621. CrossRef Medline
11. Hara Y, Balci-Hayta B, Yoshida-Moriguchi T, Kanagawa M, Beltrán-Valero de Bernabé D, Gündeşli H, Willer T, Satz JS, Crawford RW, Burden SJ, Kunz S, Oldstone MB, Accardi A, Talim B, Muntoni F, Topaloğlu H, Dinçer P, Campbell KP (2011) A dystroglycan mutation associated with limb-girdle muscular dystrophy. N Engl J Med 364: 939-946. CrossRef Medline
12. Kaczmarek L, Lapinska-Dzwonek J, Szymczak S (2002) Matrix metalloproteinases in the adult brain physiology: A link between c-Fos, AP-1 and remodeling of neuronal connections? EMBO J 21: 6643-6648. CrossRef Medline
13. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science 321: 53-57. CrossRef Medline
14. Knuesel I, Mastrocola M, Zuellig RA, Bornhauser B, Schaub MC, Fritschy JM (1999) Short communication: Altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice). Eur J Neurosci 11: 4457-4462. CrossRef Medline
15. Krasowska E, Zablocki K, Górecki DC, Swinny JD (2014) Aberrant location of inhibitory synaptic marker proteins in the hippocampus of dystrophindeficient mice: Implications for cognitive impairment in Duchenne muscular dystrophy. PLoS One 9: e108364. CrossRef Medline
16. Lévi S, Grady RM, Henry MD, Campbell KP, Sanes JR, Craig AM (2002) Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci 22: 4274-4285. Medline
17. Lidov HG, Byers TJ, Watkins SC, Kunkel LM (1990) Localization of dystrophin to postsynaptic regions of central nervous system cortical neurons. Nature 348: 725-728. CrossRef Medline
18. McNally EM, Pytel P (2007) Muscle diseases: The muscular dystrophies. Annu Rev Pathol 2: 87-109. CrossRef Medline
19. Michaluk P, Kolodziej L, Mioduszewska B, Wilczynski GM, Dzwonek J, Jaworski J, Gorecki DC, Ottersen OP, Kaczmarek L (2007) Betadystroglycan as a target for MMP-9, in response to enhanced neuronal activity. J Biol Chem 282: 16036-16041. CrossRef Medline
20. Nagode DA, Tang AH, Yang K, Alger BE (2014) Optogenetic identification of an intrinsic cholinergically driven inhibitory oscillator sensitive to cannabinoids and opioids in hippocampal CA1. J Physiol 592: 103-123. CrossRef Medline
21. Notter T, Panzanelli P, Pfister S, Mircsof D, Fritschy JM (2014) A protocol for concurrent high-quality immunohistochemical and biochemical analyses in adult mouse central nervous system. Eur J Neurosci 39: 165-175. CrossRef Medline
22. Nyíri G, Freund TF, Somogyi P (2001) Input-dependent synaptic targeting of alpha(2)-subunit-containing GABA(A) receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci 13: 428-442. CrossRef Medline
23. Panzanelli P, Gunn BG, Schlatter MC, Benke D, Tyagarajan SK, Scheiffele P, Belelli D, Lambert JJ, Rudolph U, Fritschy JM (2011) Distinct mechanisms regulate GABAA receptor and gephyrin clustering at perisomatic and axo-axonic synapses on CA1 pyramidal cells. J Physiol 589: 4959-4980. CrossRef Medline
24. Poulopoulos A, Aramuni G, Meyer G, Soykan T, Hoon M, Papadopoulos T, Zhang M, Paarmann I, Fuchs C, Harvey K, Jedlicka P, Schwarzacher SW, Betz H, Harvey RJ, Brose N, Zhang W, Varoqueaux F (2009) Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63: 628-642. CrossRef Medline
25. Reissner C, Stahn J, Breuer D, Klose M, Pohlentz G, Mormann M, Missler M (2014) Dystroglycan binding to alpha-neurexin competes with neurexophilin-1 and neuroligin in the brain. J Biol Chem 289: 27585-27603. CrossRef Medline
26. Satz JS, Ostendorf AP, Hou S, Turner A, Kusano H, Lee JC, Turk R, Nguyen H, Ross-Barta SE, Westra S, Hoshi T, Moore SA, Campbell KP (2010) Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J Neurosci 30: 14560-14572. CrossRef Medline
27. Schäfer MK, Varoqui H, Defamie N, Weihe E, Erickson JD (2002) Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J Biol Chem 277: 50734-50748. CrossRef Medline
28. Sugita S, Saito F, Tang J, Satz J, Campbell K, Südhof TC (2001) A stoichiometric complex of neurexins and dystroglycan in brain. J Cell Biol 154: 435-445. CrossRef Medline
29. Sumita K, Sato Y, Iida J, Kawata A, Hamano M, Hirabayashi S, Ohno K, Peles E, Hata Y (2007) Synaptic scaffolding molecule (S-SCAM) membraneassociated guanylate kinase with inverted organization (MAGI)-2 is associated with cell adhesion molecules at inhibitory synapses in rat hippocampal neurons. J Neurochem 100: 154-166. CrossRef Medline
30. Tyagarajan SK, Fritschy JM (2014) Gephyrin: A master regulator of neuronal function? Nat Rev Neurosci 15: 141-156. CrossRef Medline
31. Vaillend C, Perronnet C, Ros C, Gruszczynski C, Goyenvalle A, Laroche S, Danos O, Garcia L, Peltekian E (2010) Rescue of a dystrophin-like protein by exon skipping in vivo restores GABAA-receptor clustering in the hippocampus of themdx mouse. Mol Ther 18: 1683-1688. CrossRef Medline
32. Waite A, Brown SC, Blake DJ (2012) The dystrophin-glycoprotein complex in brain development and disease. Trends Neurosci 35: 487-496. CrossRef Medline
33. Wright KM, Lyon KA, Leung H, Leahy DJ, Ma L, Ginty DD (2012) Dystroglycan organizes axon guidance cue localization and axonal pathfinding. Neuron 76: 931-944. CrossRef Medline
34. Wyeth MS, Zhang N, Mody I, Houser CR (2010) Selective reduction of cholecystokinin-positive basket cell innervation in a model of temporal lobe epilepsy. J Neurosci 30: 8993-9006. CrossRef Medline
35. Yamada H, Saito F, Fukuta-Ohi H, Zhong D, Hase A, Arai K, Okuyama A, Maekawa R, Shimizu T, Matsumura K (2001) Processing of betadystroglycan by matrix metalloproteinase disrupts the link between the extracellular matrix and cell membrane via the dystroglycan complex. Hum Mol Genet 10: 1563-1569. CrossRef Medline