Splicing-Dependent Trans-synaptic SALM3-LAR-RPTP Interactions Regulate Excitatory Synapse Development and Locomotion

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2015 Sep 1

PMID 26321637

Citations 42

Authors

Yan Li

Peng Zhang

Tae-Yong Choi

Sook Kyung Park

Hanwool Park

Eun-Jae Lee

Dongsoo Lee

Junyeop Daniel Roh

Won Mah

Ryunhee Kim

Yangsik Kim

Harah Kwon

Yong Chul Bae

Se-Young Choi

Ann Marie Craig

Eunjoon Kim

Affiliations

Soon will be listed here.

Abstract

Synaptic adhesion molecules regulate diverse aspects of synapse development and plasticity. SALM3 is a PSD-95-interacting synaptic adhesion molecule known to induce presynaptic differentiation in contacting axons, but little is known about its presynaptic receptors and in vivo functions. Here, we identify an interaction between SALM3 and LAR family receptor protein tyrosine phosphatases (LAR-RPTPs) that requires the mini-exon B splice insert in LAR-RPTPs. In addition, SALM3-dependent presynaptic differentiation requires all three types of LAR-RPTPs. SALM3 mutant (Salm3(-/-)) mice display markedly reduced excitatory synapse number but normal synaptic plasticity in the hippocampal CA1 region. Salm3(-/-) mice exhibit hypoactivity in both novel and familiar environments but perform normally in learning and memory tests administered. These results suggest that SALM3 regulates excitatory synapse development and locomotion behavior.

Citing Articles

Activity-dependent diffusion trapping of AMPA receptors as a key step for expression of early LTP.

Nowacka A, Getz A, Bessa-Neto D, Choquet D Philos Trans R Soc Lond B Biol Sci. 2024; 379(1906):20230220.

PMID: 38853553 PMC: 11343219. DOI: 10.1098/rstb.2023.0220.

Alternative splicing controls teneurin-3 compact dimer formation for neuronal recognition.

Gogou C, Beugelink J, Frias C, Kresik L, Jaroszynska N, Drescher U Nat Commun. 2024; 15(1):3648.

PMID: 38684645 PMC: 11058771. DOI: 10.1038/s41467-024-47763-x.

Specification of neural circuit architecture shaped by context-dependent patterned LAR-RPTP microexons.

Han K, Yoon T, Kim J, Lee J, Lee J, Jang G Nat Commun. 2024; 15(1):1624.

PMID: 38388459 PMC: 10883964. DOI: 10.1038/s41467-024-45695-0.

POU2F1/DNMT3a Pathway Participates in Neuropathic Pain by Hypermethylation-Mediated LRFN4 Downregulation Following Oxaliplatin Treatment.

Gu Y, Wang J, Lu W, Cheng Y, Tao R, Zhang S Neurochem Res. 2023; 48(12):3652-3664.

PMID: 37592110 DOI: 10.1007/s11064-023-04011-w.

Combinatorial expression of neurexins and LAR-type phosphotyrosine phosphatase receptors instructs assembly of a cerebellar circuit.

Sclip A, Sudhof T Nat Commun. 2023; 14(1):4976.

PMID: 37591863 PMC: 10435579. DOI: 10.1038/s41467-023-40526-0.

References

Shmelkov S, Hormigo A, Jing D, Proenca C, Bath K, Milde T . Slitrk5 deficiency impairs corticostriatal circuitry and leads to obsessive-compulsive-like behaviors in mice. Nat Med. 2010; 16(5):598-602, 1p following 602. PMC: 2907076. DOI: 10.1038/nm.2125. View

Ennaceur A, Delacour J . A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res. 1988; 31(1):47-59. DOI: 10.1016/0166-4328(88)90157-x. View

Malhotra D, McCarthy S, Michaelson J, Vacic V, Burdick K, Yoon S . High frequencies of de novo CNVs in bipolar disorder and schizophrenia. Neuron. 2011; 72(6):951-63. PMC: 3921625. DOI: 10.1016/j.neuron.2011.11.007. View

Phillips R, LeDoux J . Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci. 1992; 106(2):274-85. DOI: 10.1037//0735-7044.106.2.274. View

Yamagata M, Sanes J, Weiner J . Synaptic adhesion molecules. Curr Opin Cell Biol. 2003; 15(5):621-32. DOI: 10.1016/s0955-0674(03)00107-8. View

Kim J, Jung S, Lee Y, Park S, Choi J, Lee C . Neuroligin-1 is required for normal expression of LTP and associative fear memory in the amygdala of adult animals. Proc Natl Acad Sci U S A. 2008; 105(26):9087-92. PMC: 2449369. DOI: 10.1073/pnas.0803448105. View

Shen K, Scheiffele P . Genetics and cell biology of building specific synaptic connectivity. Annu Rev Neurosci. 2010; 33:473-507. PMC: 3082953. DOI: 10.1146/annurev.neuro.051508.135302. View

Tessarollo L, Tsoulfas P, Donovan M, Palko M, Hempstead B, Parada L . Targeted deletion of all isoforms of the trkC gene suggests the use of alternate receptors by its ligand neurotrophin-3 in neuronal development and implicates trkC in normal cardiogenesis. Proc Natl Acad Sci U S A. 1998; 94(26):14776-81. PMC: 25113. DOI: 10.1073/pnas.94.26.14776. View

Deacon R, Rawlins J . T-maze alternation in the rodent. Nat Protoc. 2007; 1(1):7-12. DOI: 10.1038/nprot.2006.2. View

10.

Siddiqui T, Craig A . Synaptic organizing complexes. Curr Opin Neurobiol. 2010; 21(1):132-43. PMC: 3016466. DOI: 10.1016/j.conb.2010.08.016. View

11.

Houbaert X, Zhang C, Gambino F, Lepleux M, Deshors M, Normand E . Target-specific vulnerability of excitatory synapses leads to deficits in associative memory in a model of intellectual disorder. J Neurosci. 2013; 33(34):13805-19. PMC: 6618660. DOI: 10.1523/JNEUROSCI.1457-13.2013. View

12.

Han S, Nam J, Li Y, Kim S, Cho S, Cho Y . Regulation of dendritic spines, spatial memory, and embryonic development by the TANC family of PSD-95-interacting proteins. J Neurosci. 2010; 30(45):15102-12. PMC: 6633848. DOI: 10.1523/JNEUROSCI.3128-10.2010. View

13.

de Wit J, Ghosh A . Control of neural circuit formation by leucine-rich repeat proteins. Trends Neurosci. 2014; 37(10):539-50. PMC: 4189993. DOI: 10.1016/j.tins.2014.07.004. View

14.

Jung S, Kim J, Kwon O, Jung J, An K, Jeong A . Input-specific synaptic plasticity in the amygdala is regulated by neuroligin-1 via postsynaptic NMDA receptors. Proc Natl Acad Sci U S A. 2010; 107(10):4710-5. PMC: 2842073. DOI: 10.1073/pnas.1001084107. View

15.

Ko J, Kim S, Chung H, Kim K, Han K, Kim H . SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses. Neuron. 2006; 50(2):233-45. DOI: 10.1016/j.neuron.2006.04.005. View

16.

Xu B, Woodroffe A, Rodriguez-Murillo L, Roos J, van Rensburg E, Abecasis G . Elucidating the genetic architecture of familial schizophrenia using rare copy number variant and linkage scans. Proc Natl Acad Sci U S A. 2009; 106(39):16746-51. PMC: 2757863. DOI: 10.1073/pnas.0908584106. View

17.

Johnson K, Van Vactor D . Receptor protein tyrosine phosphatases in nervous system development. Physiol Rev. 2002; 83(1):1-24. DOI: 10.1152/physrev.00016.2002. View

18.

. Biological insights from 108 schizophrenia-associated genetic loci. Nature. 2014; 511(7510):421-7. PMC: 4112379. DOI: 10.1038/nature13595. View

19.

Morimura N, Inoue T, Katayama K, Aruga J . Comparative analysis of structure, expression and PSD95-binding capacity of Lrfn, a novel family of neuronal transmembrane proteins. Gene. 2006; 380(2):72-83. DOI: 10.1016/j.gene.2006.05.014. View

20.

Morris R . Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984; 11(1):47-60. DOI: 10.1016/0165-0270(84)90007-4. View