The secreted protein C1QL1 and its receptor BAI3 control the synaptic connectivity of excitatory inputs converging on cerebellar purkinje cells

Cell Reports

Volumn 10, Issue 5, 2015, Pages 820-832

  Sigoillot, SéverineM ^a   Iyer, Keerthana ^a   Binda, Francesca ^b   González Calvo, Inés ^a,b   Talleur, Maëva ^a   Vodjdani, Guilan ^c   Isope, Philippe ^b   Selimi, Fekrije ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN ANGIOGENESIS INHIBITOR 3 PROTEIN; C1QL1 PROTEIN; COMPLEMENT COMPONENT C1Q; G PROTEIN COUPLED RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; INNERVATION; INTRACELLULAR SIGNALING; MOUSE; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PURKINJE CELL; SENSORY NERVE; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; TARGET CELL;

EID: 84923351709     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.01.034     Document Type: Article

References (39)

1. Ango F., di Cristo G., Higashiyama H., Bennett V., Wu P., Huang Z.J. Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 2004, 119:257-272.
2. Ango F., Wu C., Van der Want J.J., Wu P., Schachner M., Huang Z.J. Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites. PLoS Biol. 2008, 6:e103.
3. Avci H.X., Lebrun C., Wehrlé R., Doulazmi M., Chatonnet F., Morel M.-P., Ema M., Vodjdani G., Sotelo C., Flamant F., Dusart I. Thyroid hormone triggers the developmental loss of axonal regenerative capacity via thyroid hormone receptor α1 and krüppel-like factor 9 in Purkinje cells. Proc. Natl. Acad. Sci. USA 2012, 109:14206-14211.
4. Bolliger M.F., Martinelli D.C., Südhof T.C. The cell-adhesion G protein-coupled receptor BAI3 is a high-affinity receptor for C1q-like proteins. Proc. Natl. Acad. Sci. USA 2011, 108:2534-2539.
5. Cesa R., Strata P. Axonal competition in the synaptic wiring of the cerebellar cortex during development and in the mature cerebellum. Neuroscience 2009, 162:624-632.
6. Cesa R., Premoselli F., Renna A., Ethell I.M., Pasquale E.B., Strata P. Eph receptors are involved in the activity-dependent synaptic wiring in the mouse cerebellar cortex. PLoS ONE 2011, 6:e19160.
7. Collins M.O., Husi H., Yu L., Brandon J.M., Anderson C.N.G., Blackstock W.P., Choudhary J.S., Grant S.G.N. Molecular characterization and comparison of the components and multiprotein complexes in the postsynaptic proteome. J.Neurochem. 2006, 97(1):16-23.
8. DeRosse P., Lencz T., Burdick K.E., Siris S.G., Kane J.M., Malhotra A.K. The genetics of symptom-based phenotypes: toward a molecular classification of schizophrenia. Schizophr. Bull. 2008, 34:1047-1053.
9. Duman J.G., Tzeng C.P., Tu Y.-K., Munjal T., Schwechter B., Ho T.S.-Y., Tolias K.F. The adhesion-GPCR BAI1 regulates synaptogenesis by controlling the recruitment of the Par3/Tiam1 polarity complex to synaptic sites. J.Neurosci. 2013, 33:6964-6978.
10. Hashimoto K., Ichikawa R., Kitamura K., Watanabe M., Kano M. Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 2009, 63:106-118.
11. Hirai H., Pang Z., Bao D., Miyazaki T., Li L., Miura E., Parris J., Rong Y., Watanabe M., Yuzaki M., Morgan J.I. Cbln1 is essential for synaptic integrity and plasticity in the cerebellum. Nat. Neurosci. 2005, 8:1534-1541.
12. Iijima T., Miura E., Watanabe M., Yuzaki M. Distinct expression of C1q-like family mRNAs in mouse brain and biochemical characterization of their encoded proteins. Eur. J. Neurosci. 2010, 31:1606-1615.
13. Ito-Ishida A., Miyazaki T., Miura E., Matsuda K., Watanabe M., Yuzaki M., Okabe S. Presynaptically released Cbln1 induces dynamic axonal structural changes by interacting with GluD2 during cerebellar synapse formation. Neuron 2012, 76:549-564.
14. Lanoue V., Usardi A., Sigoillot S.M., Talleur M., Iyer K., Mariani J., Isope P., Vodjdani G., Heintz N., Selimi F. The adhesion-GPCR BAI3, a gene linked to psychiatric disorders, regulates dendrite morphogenesis in neurons. Mol. Psychiatry 2013, 18:943-950.
15. Liao H.-M., Chao Y.-L., Huang A.-L., Cheng M.-C., Chen Y.-J., Lee K.-F., Fang J.-S., Hsu C.-H., Chen C.-H. Identification and characterization of three inherited genomic copy number variations associated with familial schizophrenia. Schizophr. Res. 2012, 139:229-236.
16. Luo L. Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu. Rev. Cell Dev. Biol. 2002, 18:601-635.
17. Matsuda K., Miura E., Miyazaki T., Kakegawa W., Emi K., Narumi S., Fukazawa Y., Ito-Ishida A., Kondo T., Shigemoto R., et al. Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer. Science 2010, 328:363-368.
18. O'Rourke N.A., Weiler N.C., Micheva K.D., Smith S.J. Deep molecular diversity of mammalian synapses: why it matters and how to measure it. Nat. Rev. Neurosci. 2012, 13:365-379.
19. Okajima D., Kudo G., Yokota H. Antidepressant-like behavior inbrain-specific angiogenesis inhibitor 2-deficient mice. J.Physiol. Sci. 2011, 61:47-54.
20. Park D., Tosello-Trampont A.-C., Elliott M.R., Lu M., Haney L.B., Ma Z., Klibanov A.L., Mandell J.W., Ravichandran K.S. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 2007, 450:430-434.
21. Pinan-Lucarré B., Tu H., Pierron M., Cruceyra P.I., Zhan H., Stigloher C., Richmond J.E., Bessereau J.-L. C. elegans Punctin specifies cholinergic versus GABAergic identity of postsynaptic domains. Nature 2014, 511:466-470.
22. Rodriguez A., Ehlenberger D.B., Dickstein D.L., Hof P.R., Wearne S.L. Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS ONE 2008, 3:e1997.
23. Rossi F., Strata P. Reciprocal trophic interactions in the adult climbing fibre-Purkinje cell system. Prog. Neurobiol. 1995, 47:341-369.
24. Salinas P.C. Wnt signaling in the vertebrate central nervous system: from axon guidance to synaptic function. Cold Spring Harb. Perspect. Biol. 2012, 4:a008003.
25. Sanes J.R., Yamagata M. Many paths to synaptic specificity. Annu. Rev. Cell Dev. Biol. 2009, 25:161-195.
26. Selimi F., Cristea I.M., Heller E., Chait B.T., Heintz N. Proteomic studies of a single CNS synapse type: the parallel fiber/purkinje cell synapse. PLoS Biol. 2009, 7:e83.
27. Shen K., Scheiffele P. Genetics and cell biology of building specific synaptic connectivity. Annu. Rev. Neurosci. 2010, 33:473-507.
28. Sia G.-M., Béïque J.-C., Rumbaugh G., Cho R., Worley P.F., Huganir R.L. Interaction of the N-terminal domain of the AMPA receptor GluR4 subunit with the neuronal pentraxin NP1 mediates GluR4 synaptic recruitment. Neuron 2007, 55:87-102.
29. Sotelo C. Cerebellar synaptogenesis: what we can learn from mutant mice. J.Exp. Biol. 1990, 153:225-249.
30. Sperry R.W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 1963, 50:703-710.
31. Stevens B., Allen N.J., Vazquez L.E., Howell G.R., Christopherson K.S., Nouri N., Micheva K.D., Mehalow A.K., Huberman A.D., Stafford B., et al. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131:1164-1178.
32. Südhof T.C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 2008, 455:903-911.
33. Uemura T., Kakizawa S., Yamasaki M., Sakimura K., Watanabe M., Iino M., Mishina M. Regulation of long-term depression and climbing fiber territory by glutamate receptor delta2 at parallel fiber synapses through its C-terminal domain in cerebellar Purkinje cells. J.Neurosci. 2007, 27:12096-12108.
34. Uemura T., Lee S.-J., Yasumura M., Takeuchi T., Yoshida T., Ra M., Taguchi R., Sakimura K., Mishina M. Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 2010, 141:1068-1079.
35. Williams M.E., Wilke S.A., Daggett A., Davis E., Otto S., Ravi D., Ripley B., Bushong E.A., Ellisman M.H., Klein G., Ghosh A. Cadherin-9 regulates synapse-specific differentiation in the developing hippocampus. Neuron 2011, 71:640-655.
36. Yamagata M., Sanes J.R. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 2008, 451:465-469.
37. Yuste R., Bonhoeffer T. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat. Rev. Neurosci. 2004, 5:24-34.
38. Yuzaki M. Cbln1 and its family proteins in synapse formation and maintenance. Curr. Opin. Neurobiol. 2011, 21:215-220.
39. Yuzaki M. The ins and outs of GluD2-why and how Purkinje cells use the special glutamate receptor. Cerebellum 2012, 11:438-439.