Neuronal Ig/Caspr Recognition Promotes the Formation of Axoaxonic Synapses in Mouse Spinal Cord

Neuron

Volumn 81, Issue 1, 2014, Pages 120-129

  Ashrafi, Soha ^a,b   Betley, J Nicholas ^c   Comer, JohnD ^a,b,d   Brenner Morton, Susan ^c   Bar, Vered ^e   Shimoda, Yasushi ^f   Watanabe, Kazutada ^f,g   Peles, Elior ^e   Jessell, ThomasM ^c   Kaltschmidt, JuliaA ^a,b  

^a Weill Cornell Medical Center   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d The Weizmann Institute of Science ^*

^e WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^f NAGAOKA UNIVERSITY OF TECHNOLOGY   (Japan)

^g NAGAOKA NATIONAL COLLEGE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CONTACTIN; CONTACTIN 5; CONTACTIN ASSOCIATED PROTEIN 4; IMMUNOGLOBULIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CASPR4 GENE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; GABAERGIC SYSTEM; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE LOCATION; INTERNEURON; MOLECULAR RECOGNITION; MOUSE; NB2 GENE; NERVE CELL NETWORK; NERVE FIBER; NONHUMAN; PRESYNAPTIC INHIBITION; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SENSORY NERVE; SENSORY NERVE CELL; SENSORY NERVE CONDUCTION; SPINAL CORD; SYNAPTIC TRANSMISSION; SYNAPTOSOME;

ANIMALS; ANIMALS, NEWBORN; AXONS; CELL ADHESION MOLECULES; CELL ADHESION MOLECULES, NEURONAL; COMPUTATIONAL BIOLOGY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; MUTATION; PARVALBUMINS; PRESYNAPTIC TERMINALS; SENSORY RECEPTOR CELLS; SPINAL CORD; SYNAPSES; TRANSCRIPTION FACTORS;

EID: 84891809781     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.10.060     Document Type: Article

References (49)

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. Arber S., Han B., Mendelsohn M., Smith M., Jessell T.M., Sockanathan S. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 1999, 23:659-674.
3. Arber S., Ladle D.R., Lin J.H., Frank E., Jessell T.M. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 2000, 101:485-498.
4. Ashrafi S., Lalancette-Hebert M., Friese A., Sigrist M., Arber S., Shneider N.A., Kaltschmidt J.A. Wnt7A identifies embryonic gamma-motor neurons and reveals early postnatal dependence of gamma-motor neurons on a muscle spindle-derived signal. J.Neurosci. 2012, 32:8725-8731.
5. Betley J.N., Wright C.V., Kawaguchi Y., Erdélyi F., Szabó G., Jessell T.M., Kaltschmidt J.A. Stringent specificity in the construction of a GABAergic presynaptic inhibitory circuit. Cell 2009, 139:161-174.
6. Buffelli M., Burgess R.W., Feng G., Lobe C.G., Lichtman J.W., Sanes J.R. Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 2003, 424:430-434.
7. Dahme M., Bartsch U., Martini R., Anliker B., Schachner M., Mantei N. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat. Genet. 1997, 17:346-349.
8. Feinberg K., Eshed-Eisenbach Y., Frechter S., Amor V., Salomon D., Sabanay H., Dupree J.L., Grumet M., Brophy P.J., Shrager P., Peles E. A glial signal consisting of gliomedin and NrCAM clusters axonal Na+ channels during the formation of nodes of Ranvier. Neuron 2010, 65:490-502.
9. Fritschy J.M., Weinmann O., Wenzel A., Benke D. Synapse-specificlocalization of NMDA and GABA(A) receptor subunits revealed by antigen-retrieval immunohistochemistry. J.Comp. Neurol. 1998, 390:194-210.
10. Furley A.J., Morton S.B., Manalo D., Karagogeos D., Dodd J., Jessell T.M. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 1990, 61:157-170.
11. Gennarini G., Cibelli G., Rougon G., Mattei M.G., Goridis C. The mouse neuronal cell surface protein F3: a phosphatidylinositol-anchored member of the immunoglobulin superfamily related to chicken contactin. J.Cell Biol. 1989, 109:775-788.
12. Glasgow S.M., Henke R.M., Macdonald R.J., Wright C.V., Johnson J.E. Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn. Development 2005, 132:5461-5469.
13. Gollan L., Salomon D., Salzer J.L., Peles E. Caspr regulates the processing of contactin and inhibits its binding to neurofascin. J.Cell Biol. 2003, 163:1213-1218.
14. Gray G.E., Sanes J.R. Migratory paths and phenotypic choices of clonally related cells in the avian optic tectum. Neuron 1991, 6:211-225.
15. Hippenmeyer S., Vrieseling E., Sigrist M., Portmann T., Laengle C., Ladle D.R., Arber S. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 2005, 3:e159.
16. Hughes D.I., Mackie M., Nagy G.G., Riddell J.S., Maxwell D.J., Szabó G., Erdélyi F., Veress G., Szucs P., Antal M., Todd A.J. P boutons in lamina IX of the rodent spinal cord express high levels of glutamic acid decarboxylase-65 and originate from cells in deep medial dorsal horn. Proc. Natl. Acad. Sci. USA 2005, 102:9038-9043.
17. Hume R.I., Purves D. Geometry of neonatal neurones and the regulation of synapse elimination. Nature 1981, 293:469-471.
18. Kawaguchi Y., Cooper B., Gannon M., Ray M., MacDonald R.J., Wright C.V. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat. Genet. 2002, 32:128-134.
19. Kwon H.B., Kozorovitskiy Y., Oh W.J., Peixoto R.T., Akhtar N., Saulnier J.L., Gu C., Sabatini B.L. Neuroligin-1-dependent competition regulates cortical synaptogenesis and synapse number. Nat. Neurosci. 2012, 15:1667-1674.
20. Li H., Takeda Y., Niki H., Ogawa J., Kobayashi S., Kai N., Akasaka K., Asano M., Sudo K., Iwakura Y., Watanabe K. Aberrant responses to acoustic stimuli in mice deficient for neural recognition molecule NB-2. Eur. J. Neurosci. 2003, 17:929-936.
21. Lin Y., Bloodgood B.L., Hauser J.L., Lapan A.D., Koon A.C., Kim T.K., Hu L.S., Malik A.N., Greenberg M.E. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 2008, 455:1198-1204.
22. Madisen L., Zwingman T.A., Sunkin S.M., Oh S.W., Zariwala H.A., Gu H., Ng L.L., Palmiter R.D., Hawrylycz M.J., Jones A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 2010, 13:133-140.
23. Montag-Sallaz M., Schachner M., Montag D. Misguided axonal projections, neural cell adhesion molecule 180 mRNA upregulation, and altered behavior in mice deficient for the close homolog of L1. Mol. Cell. Biol. 2002, 22:7967-7981.
24. Ogawa J., Kaneko H., Masuda T., Nagata S., Hosoya H., Watanabe K. Novel neural adhesion molecules in the Contactin/F3 subgroup of the immunoglobulin superfamily: isolation and characterization of cDNAs from rat brain. Neurosci. Lett. 1996, 218:173-176.
25. Peles E., Nativ M., Lustig M., Grumet M., Schilling J., Martinez R., Plowman G.D., Schlessinger J. Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions. EMBO J. 1997, 16:978-988.
26. Phillips G.R., Huang J.K., Wang Y., Tanaka H., Shapiro L., Zhang W., Shan W.S., Arndt K., Frank M., Gordon R.E., et al. The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 2001, 32:63-77.
27. Poliak S., Peles E. The local differentiation of myelinated axons at nodes of Ranvier. Nat. Rev. Neurosci. 2003, 4:968-980.
28. Poliak S., Gollan L., Martinez R., Custer A., Einheber S., Salzer J.L., Trimmer J.S., Shrager P., Peles E. Caspr2, a new member of the neurexin superfamily, is localized at the juxtaparanodes of myelinated axons and associates with K+ channels. Neuron 1999, 24:1037-1047.
29. Poliak S., Salomon D., Elhanany H., Sabanay H., Kiernan B., Pevny L., Stewart C.L., Xu X., Chiu S.Y., Shrager P., et al. Juxtaparanodal clustering of Shaker-like K+ channels in myelinated axons depends on Caspr2 and TAG-1. J.Cell Biol. 2003, 162:1149-1160.
30. Price S.R., De Marco Garcia N.V., Ranscht B., Jessell T.M. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 2002, 109:205-216.
31. Prince J.E.A., Brignal A.C., Cutforth T., Shen K., Cloutier J.F. Kirrel3 is required for the coalescence of vomeronasal sensory neuron. Development 2013, 140:2398-2408.
32. Quevedo J., Eguibar J.R., Lomeli J., Rudomin P. Patterns of connectivity of spinal interneurons with single muscle afferents. Exp. Brain Res. 1997, 115:387-402.
33. Rudomin P. In search of lost presynaptic inhibition. Exp. Brain Res. 2009, 196:139-151.
34. Rudomin P., Schmidt R.F. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp. Brain Res. 1999, 129:1-37.
35. Sakurai T., Lustig M., Babiarz J., Furley A.J., Tait S., Brophy P.J., Brown S.A., Brown L.Y., Mason C.A., Grumet M. Overlapping functions of the cell adhesion molecules Nr-CAM and L1 in cerebellar granule cell development. J.Cell Biol. 2001, 154:1259-1273.
36. Sherman D.L., Tait S., Melrose S., Johnson R., Zonta B., Court F.A., Macklin W.B., Meek S., Smith A.J., Cottrell D.F., Brophy P.J. Neurofascins are required to establish axonal domains for saltatory conduction. Neuron 2005, 48:737-742.
37. Shimoda Y., Watanabe K. Contactins: emerging key roles in the development and function of the nervous system. Cell Adhes. Migr. 2009, 3:64-70.
38. Shimoda Y., Koseki F., Itoh M., Toyoshima M., Watanabe K. A cis-complex of NB-2/contactin-5 with amyloid precursor-like protein 1 is localized on the presynaptic membrane. Neurosci. Lett. 2012, 510:148-153.
39. Spiegel I., Salomon D., Erne B., Schaeren-Wiemers N., Peles E. Caspr3 and caspr4, two novel members of the Caspr family are expressed in the nervous system and interact with PDZ domains. Mol. Cell. Neurosci. 2002, 20:283-297.
40. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
41. Stepanyants A., Tamás G., Chklovskii D.B. Class-specific features of neuronal wiring. Neuron 2004, 43:251-259.
42. Tian N., Petersen C., Kash S., Baekkeskov S., Copenhagen D., Nicoll R. The role of the synthetic enzyme GAD65 in the control of neuronal gamma-aminobutyric acid release. Proc. Natl. Acad. Sci. USA 1999, 96:12911-12916.
43. Toyoshima M., Sakurai K., Shimazaki K., Takeda Y., Shimoda Y., Watanabe K. Deficiency of neural recognition molecule NB-2 affects the development of glutamatergic auditory pathways from the ventral cochlear nucleus to the superior olivary complex in mouse. Dev. Biol. 2009, 336:192-200.
44. Traka M., Goutebroze L., Denisenko N., Bessa M., Nifli A., Havaki S., Iwakura Y., Fukamauchi F., Watanabe K., Soliven B., et al. Association of TAG-1 with Caspr2 is essential for the molecular organization of juxtaparanodal regions of myelinated fibers. J.Cell Biol. 2003, 162:1161-1172.
45. Walmsley B., Wieniawa-Narkiewicz E., Nicol M.J. Ultrastructural evidence related to presynaptic inhibition of primary muscle afferents in Clarke's column of the cat. J.Neurosci. 1987, 7:236-243.
46. Williams M.E., de Wit J., Ghosh A. Molecular mechanisms of synaptic specificity in developing neural circuits. Neuron 2010, 68:9-18.
47. Yamagata M., Sanes J.R. Expanding the Ig superfamily code for laminar specificity in retina: expression and role of contactins. J.Neurosci. 2012, 32:14402-14414.
48. Yoshihara Y., Kawasaki M., Tani A., Tamada A., Nagata S., Kagamiyama H., Mori K. BIG-1: a new TAG-1/F3-related member of the immunoglobulin superfamily with neurite outgrowth-promoting activity. Neuron 1994, 13:415-426.
49. Yoshihara Y., Kawasaki M., Tamada A., Nagata S., Kagamiyama H., Mori K. Overlapping and differential expression of BIG-2, BIG-1, TAG-1, and F3: four members of an axon-associated cell adhesion molecule subgroup of the immunoglobulin superfamily. J.Neurobiol. 1995, 28:51-69.