SRGAP2 and Its Human-Specific Paralog Co-Regulate the Development of Excitatory and Inhibitory Synapses

Neuron

Volumn 91, Issue 2, 2016, Pages 356-369

  Fossati, Matteo ^a   Pizzarelli, Rocco ^a   Schmidt, Ewoud R ^b   Kupferman, Justine V ^b   Stroebel, David ^a   Polleux, Franck ^b   Charrier, Cécile ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; AMPA RECEPTOR; ENZYME ACTIVATOR; GEPHYRIN; PROTEIN HOMER; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SLIT ROBO RHO GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 2; UNCLASSIFIED DRUG; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; SRGAP2 PROTEIN, HUMAN;

ADULT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME REGULATION; EXCITATORY SYNAPSE; GENE DUPLICATION; IN VIVO STUDY; INHIBITORY SYNAPSE; MOLECULAR MECHANICS; MOUSE; NERVE CELL; NEWBORN; NONHUMAN; PARALOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; SYNAPSE; SYNAPTIC DENSITY; SYNAPTOGENESIS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; HUMAN; METABOLISM; NERVE CELL INHIBITION; NERVOUS SYSTEM DEVELOPMENT; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PROCEDURES; SYNAPTIC TRANSMISSION;

EXCITATORY POSTSYNAPTIC POTENTIALS; GTPASE-ACTIVATING PROTEINS; HUMANS; NEURAL INHIBITION; NEUROGENESIS; PATCH-CLAMP TECHNIQUES; RECEPTORS, GABA-A; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84978473802     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.06.013     Document Type: Article

References (62)

1. Alvarez, V.A., Sabatini, B.L., Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 30 (2007), 79–97.
2. Araya, R., Vogels, T.P., Yuste, R., Activity-dependent dendritic spine neck changes are correlated with synaptic strength. Proc. Natl. Acad. Sci. USA 111 (2014), E2895–E2904.
3. Bayés, A., Collins, M.O., Croning, M.D., van de Lagemaat, L.N., Choudhary, J.S., Grant, S.G., Comparative study of human and mouse postsynaptic proteomes finds high compositional conservation and abundance differences for key synaptic proteins. PLoS ONE, 7, 2012, e46683.
4. Benavides-Piccione, R., Ballesteros-Yáñez, I., DeFelipe, J., Yuste, R., Cortical area and species differences in dendritic spine morphology. J. Neurocytol. 31 (2002), 337–346.
5. Benson, D.L., Cohen, P.A., Activity-independent segregation of excitatory and inhibitory synaptic terminals in cultured hippocampal neurons. J. Neurosci. 16 (1996), 6424–6432.
6. Bockaert, J., Perroy, J., Bécamel, C., Marin, P., Fagni, L., GPCR interacting proteins (GIPs) in the nervous system: Roles in physiology and pathologies. Annu. Rev. Pharmacol. Toxicol. 50 (2010), 89–109.
7. Cahill, M.E., Xie, Z., Day, M., Photowala, H., Barbolina, M.V., Miller, C.A., Weiss, C., Radulovic, J., Sweatt, J.D., Disterhoft, J.F., et al. Kalirin regulates cortical spine morphogenesis and disease-related behavioral phenotypes. Proc. Natl. Acad. Sci. USA 106 (2009), 13058–13063.
8. Cerri, C., Fabbri, A., Vannini, E., Spolidoro, M., Costa, M., Maffei, L., Fiorentini, C., Caleo, M., Activation of Rho GTPases triggers structural remodeling and functional plasticity in the adult rat visual cortex. J. Neurosci. 31 (2011), 15163–15172.
9. Charrier, C., Joshi, K., Coutinho-Budd, J., Kim, J.E., Lambert, N., de Marchena, J., Jin, W.L., Vanderhaeghen, P., Ghosh, A., Sassa, T., Polleux, F., Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation. Cell 149 (2012), 923–935.
10. Chen, J.L., Villa, K.L., Cha, J.W., So, P.T., Kubota, Y., Nedivi, E., Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 74 (2012), 361–373.
11. Chiu, C.Q., Lur, G., Morse, T.M., Carnevale, N.T., Ellis-Davies, G.C., Higley, M.J., Compartmentalization of GABAergic inhibition by dendritic spines. Science 340 (2013), 759–762.
12. Choquet, D., Triller, A., The dynamic synapse. Neuron 80 (2013), 691–703.
13. Clement, J.P., Aceti, M., Creson, T.K., Ozkan, E.D., Shi, Y., Reish, N.J., Almonte, A.G., Miller, B.H., Wiltgen, B.J., Miller, C.A., et al. Pathogenic SYNGAP1 mutations impair cognitive development by disrupting maturation of dendritic spine synapses. Cell 151 (2012), 709–723.
14. Courchesne, E., Pierce, K., Schumann, C.M., Redcay, E., Buckwalter, J.A., Kennedy, D.P., Morgan, J., Mapping early brain development in autism. Neuron 56 (2007), 399–413.
15. Cui-Wang, T., Hanus, C., Cui, T., Helton, T., Bourne, J., Watson, D., Harris, K.M., Ehlers, M.D., Local zones of endoplasmic reticulum complexity confine cargo in neuronal dendrites. Cell 148 (2012), 309–321.
16. Defelipe, J., The evolution of the brain, the human nature of cortical circuits, and intellectual creativity. Front. Neuroanat., 5, 2011, 29.
17. Dennis, M.Y., Nuttle, X., Sudmant, P.H., Antonacci, F., Graves, T.A., Nefedov, M., Rosenfeld, J.A., Sajjadian, S., Malig, M., Kotkiewicz, H., et al. Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 149 (2012), 912–922.
18. Elston, G.N., Benavides-Piccione, R., DeFelipe, J., The pyramidal cell in cognition: a comparative study in human and monkey. J. Neurosci., 21, 2001, RC163.
19. Fritschy, J.M., Harvey, R.J., Schwarz, G., Gephyrin: where do we stand, where do we go?. Trends Neurosci. 31 (2008), 257–264.
20. Geschwind, D.H., Rakic, P., Cortical evolution: judge the brain by its cover. Neuron 80 (2013), 633–647.
21. Gross, G.G., Junge, J.A., Mora, R.J., Kwon, H.B., Olson, C.A., Takahashi, T.T., Liman, E.R., Ellis-Davies, G.C., McGee, A.W., Sabatini, B.L., et al. Recombinant probes for visualizing endogenous synaptic proteins in living neurons. Neuron 78 (2013), 971–985.
22. Guerrier, S., Coutinho-Budd, J., Sassa, T., Gresset, A., Jordan, N.V., Chen, K., Jin, W.L., Frost, A., Polleux, F., The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138 (2009), 990–1004.
23. Harris, K.M., Stevens, J.K., Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9 (1989), 2982–2997.
24. Hayashi, M.K., Tang, C., Verpelli, C., Narayanan, R., Stearns, M.H., Xu, R.M., Li, H., Sala, C., Hayashi, Y., The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 137 (2009), 159–171.
25. Higley, M.J., Sabatini, B.L., Calcium signaling in dendrites and spines: practical and functional considerations. Neuron 59 (2008), 902–913.
26. Huttenlocher, P.R., Dabholkar, A.S., Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol. 387 (1997), 167–178.
27. Jensen, K.P., Covault, J., Human miR-1271 is a miR-96 paralog with distinct non-conserved brain expression pattern. Nucleic Acids Res. 39 (2011), 701–711.
28. Knott, G.W., Quairiaux, C., Genoud, C., Welker, E., Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34 (2002), 265–273.
29. Krumm, N., O'Roak, B.J., Shendure, J., Eichler, E.E., A de novo convergence of autism genetics and molecular neuroscience. Trends Neurosci. 37 (2014), 95–105.
30. Kubota, Y., Hatada, S., Kondo, S., Karube, F., Kawaguchi, Y., Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocortical afferents. J. Neurosci. 27 (2007), 1139–1150.
31. Lu, W., Shi, Y., Jackson, A.C., Bjorgan, K., During, M.J., Sprengel, R., Seeburg, P.H., Nicoll, R.A., Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62 (2009), 254–268.
32. Luo, L., Hensch, T.K., Ackerman, L., Barbel, S., Jan, L.Y., Jan, Y.N., Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature 379 (1996), 837–840.
33. McAllister, A.K., Dynamic aspects of CNS synapse formation. Annu. Rev. Neurosci. 30 (2007), 425–450.
34. Miesenböck, G., De Angelis, D.A., Rothman, J.E., Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394 (1998), 192–195.
35. Nelson, S.B., Valakh, V., Excitatory/Inhibitory Balance and Circuit Homeostasis in Autism Spectrum Disorders. Neuron 87 (2015), 684–698.
36. Okabe, S., Molecular anatomy of the postsynaptic density. Mol. Cell. Neurosci. 34 (2007), 503–518.
37. Okada, H., Uezu, A., Mason, F.M., Soderblom, E.J., Moseley, M.A. 3rd, Soderling, S.H., SH3 domain-based phototrapping in living cells reveals Rho family GAP signaling complexes. Sci. Signal., 4, 2011, rs13.
38. Parikshak, N.N., Luo, R., Zhang, A., Won, H., Lowe, J.K., Chandran, V., Horvath, S., Geschwind, D.H., Integrative functional genomic analyses implicate specific molecular pathways and circuits in autism. Cell 155 (2013), 1008–1021.
39. Pérez-Otaño, I., Luján, R., Tavalin, S.J., Plomann, M., Modregger, J., Liu, X.B., Jones, E.G., Heinemann, S.F., Lo, D.C., Ehlers, M.D., Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1. Nat. Neurosci. 9 (2006), 611–621.
40. Petanjek, Z., Judaš, M., Šimic, G., Rasin, M.R., Uylings, H.B., Rakic, P., Kostovic, I., Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc. Natl. Acad. Sci. USA 108 (2011), 13281–13286.
41. Pinto, D., Pagnamenta, A.T., Klei, L., Anney, R., Merico, D., Regan, R., Conroy, J., Magalhaes, T.R., Correia, C., Abrahams, B.S., et al. Functional impact of global rare copy number variation in autism spectrum disorders. Nature 466 (2010), 368–372.
42. Ramocki, M.B., Zoghbi, H.Y., Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 455 (2008), 912–918.
43. Rao, Y., Ma, Q., Vahedi-Faridi, A., Sundborger, A., Pechstein, A., Puchkov, D., Luo, L., Shupliakov, O., Saenger, W., Haucke, V., Molecular basis for SH3 domain regulation of F-BAR-mediated membrane deformation. Proc. Natl. Acad. Sci. USA 107 (2010), 8213–8218.
44. Shanks, N.F., Savas, J.N., Maruo, T., Cais, O., Hirao, A., Oe, S., Ghosh, A., Noda, Y., Greger, I.H., Yates, J.R. 3rd, Nakagawa, T., Differences in AMPA and kainate receptor interactomes facilitate identification of AMPA receptor auxiliary subunit GSG1L. Cell Rep. 1 (2012), 590–598.
45. Shen, K., Scheiffele, P., Genetics and cell biology of building specific synaptic connectivity. Annu. Rev. Neurosci. 33 (2010), 473–507.
46. Sheng, M., Hoogenraad, C.C., The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu. Rev. Biochem. 76 (2007), 823–847.
47. Soto, F., Bleckert, A., Lewis, R., Kang, Y., Kerschensteiner, D., Craig, A.M., Wong, R.O., Coordinated increase in inhibitory and excitatory synapses onto retinal ganglion cells during development. Neural Dev., 6, 2011, 31.
48. Spruston, N., Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 9 (2008), 206–221.
49. Spruston, N., Johnston, D., Out of control in the dendrites. Nat. Neurosci. 11 (2008), 733–734.
50. Sudmant, P.H., Kitzman, J.O., Antonacci, F., Alkan, C., Malig, M., Tsalenko, A., Sampas, N., Bruhn, L., Shendure, J., Eichler, E.E., 1000 Genomes Project. Diversity of human copy number variation and multicopy genes. Science 330 (2010), 641–646.
51. Ting, J.T., Peça, J., Feng, G., Functional consequences of mutations in postsynaptic scaffolding proteins and relevance to psychiatric disorders. Annu. Rev. Neurosci. 35 (2012), 49–71.
52. Tretter, V., Mukherjee, J., Maric, H.M., Schindelin, H., Sieghart, W., Moss, S.J., Gephyrin, the enigmatic organizer at GABAergic synapses. Front. Cell. Neurosci., 6, 2012, 23.
53. Tu, J.C., Xiao, B., Yuan, J.P., Lanahan, A.A., Leoffert, K., Li, M., Linden, D.J., Worley, P.F., Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21 (1998), 717–726.
54. Tu, J.C., Xiao, B., Naisbitt, S., Yuan, J.P., Petralia, R.S., Brakeman, P., Doan, A., Aakalu, V.K., Lanahan, A.A., Sheng, M., Worley, P.F., Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23 (1999), 583–592.
55. van Versendaal, D., Rajendran, R., Saiepour, M.H., Klooster, J., Smit-Rigter, L., Sommeijer, J.P., De Zeeuw, C.I., Hofer, S.B., Heimel, J.A., Levelt, C.N., Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron 74 (2012), 374–383.
56. Varki, A., Geschwind, D.H., Eichler, E.E., Explaining human uniqueness: genome interactions with environment, behaviour and culture. Nat. Rev. Genet. 9 (2008), 749–763.
57. Williams, S.R., Mitchell, S.J., Direct measurement of somatic voltage clamp errors in central neurons. Nat. Neurosci. 11 (2008), 790–798.
58. Yizhar, O., Fenno, L.E., Prigge, M., Schneider, F., Davidson, T.J., O'Shea, D.J., Sohal, V.S., Goshen, I., Finkelstein, J., Paz, J.T., et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477 (2011), 171–178.
59. Yuste, R., Dendritic spines and distributed circuits. Neuron 71 (2011), 772–781.
60. Yuste, R., Electrical compartmentalization in dendritic spines. Annu. Rev. Neurosci. 36 (2013), 429–449.
61. Zhao, X., Shoji, S., Lau, P., Balanced GABAergic and glutamatergic synapse development in hippocampal neurons. Biochem. Biophys. Res. Commun. 330 (2005), 1110–1115.
62. Zoghbi, H.Y., Bear, M.F., Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb. Perspect. Biol., 4, 2012, 10.1101/cshperspect.a009886.