SALM5 trans-synaptically interacts with LAR-RPTPs in a splicing-dependent manner to regulate synapse development

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Choi, Yeonsoo ^a   Nam, Jungyong ^a   Whitcomb, Daniel J ^b   Song, Yoo Sung ^c   Kim, Doyoun ^d   Jeon, Sangmin ^e   Um, Ji Won ^e,f   Lee, Seong Gyu ^a   Woo, Jooyeon ^a   Kwon, Seok Kyu ^a   Li, Yan ^d   Mah, Won ^g   Kim, Ho Min ^a   Ko, Jaewon ^e   Cho, Kwangwook ^b,h   Kim, Eunjoon ^a,d  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c Seoul National University Bundang Hospital   (South Korea)

^d Institute for Basic Science   (South Korea)

^e Yonsei University   (South Korea)

^f Yonsei University College of Medicine   (South Korea)

^g Kyungpook National University   (South Korea)

^h UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE CELL ADHESION MOLECULE; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE; SALM5 PROTEIN, MOUSE;

ALTERNATIVE RNA SPLICING; ANIMAL; AXON; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION;

ALTERNATIVE SPLICING; ANIMALS; AXONS; CELL ADHESION MOLECULES, NEURONAL; MICE; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 2; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84971254351     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep26676     Document Type: Article

References (69)

1. Yuzaki, M. Cbln1 and its family proteins in synapse formation and maintenance. Curr Opin Neurobiol 21, 215-220, doi: 10.1016/j.conb.2011.01.010 (2011).
2. Takahashi, H. & Craig, A. M. Protein tyrosine phosphatases PTPdelta, PTPsigma, and LAR: presynaptic hubs for synapse organization. Trends Neurosci 36, 522-534, doi: 10.1016/j.tins.2013.06.002 (2013).
3. Krueger, D. D., Tuffy, L. P., Papadopoulos, T. & Brose, N. The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses. Curr Opin Neurobiol 22, 412-422, doi: 10.1016/j.conb.2012.02.012 (2012).
4. Um, J. W. & Ko, J. LAR-RPTPs: synaptic adhesion molecules that shape synapse development. Trends Cell Biol 23, 465-475, doi: 10.1016/j.tcb.2013.07.004 (2013).
5. Sudhof, T. C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903-911, doi: 10.1038/nature07456 (2008).
6. Missler, M., Sudhof, T. C. & Biederer, T. Synaptic cell adhesion. Cold Spring Harb Perspect Biol 4, a005694, doi: 10.1101/cshperspect.a005694 (2012).
7. Valnegri, P., Sala, C. & Passafaro, M. Synaptic dysfunction and intellectual disability. Adv Exp Med Biol 970, 433-449, doi: 10.1007/978-3-7091-0932-8-19 (2012).
8. Siddiqui, T. J. & Craig, A. M. Synaptic organizing complexes. Curr Opin Neurobiol 21, 132-143, doi: 10.1016/j.conb.2010.08.016 (2011).
9. De Wit, J. & Ghosh, A. Control of neural circuit formation by leucine-rich repeat proteins. Trends Neurosci 37, 539-550, doi: 10.1016/j.tins.2014.07.004 (2014).
10. Yogev, S. & Shen, K. Cellular and molecular mechanisms of synaptic specificity. Annu Rev Cell Dev Biol 30, 417-437, doi: 10.1146/ annurev-cellbio-100913-012953 (2014).
11. Wright, G. J. & Washbourne, P. Neurexins, neuroligins and LRRTMs: synaptic adhesion getting fishy. J Neurochem 117, 765-778, doi: 10.1111/j.1471-4159.2010.07141.x (2011).
12. Song, Y. S. & Kim, E. Presynaptic proteoglycans: sweet organizers of synapse development. Neuron 79, 609-611, doi: 10.1016/j.neuron.2013.07.048 (2013).
13. Nam, J., Mah, W. & Kim, E. The SALM/Lrfn family of leucine-rich repeat-containing cell adhesion molecules. Semin Cell Dev Biol 22, 492-498, doi: 10.1016/j.semcdb.2011.06.005 (2011).
14. Ko, J. et al. SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses. Neuron 50, 233-245, doi: 10.1016/j.neuron.2006.04.005 (2006).
15. Wang, C. Y. et al. A novel family of adhesion-like molecules that interacts with the NMDA receptor. J Neurosci 26, 2174-2183 (2006).
16. 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 380, 72-83, doi: 10.1016/j.gene.2006.05.014 (2006).
17. Mah, W. et al. Selected SALM (synaptic adhesion-like molecule) family proteins regulate synapse formation. J Neurosci 30, 5559-5568, doi: 10.1523/JNEUROSCI.4839-09.2010 (2010).
18. Seabold, G. K. et al. The SALM family of adhesion-like molecules forms heteromeric and homomeric complexes. J Biol Chem 283, 8395-8405, doi: 10.1074/jbc.M709456200 (2008).
19. De Bruijn, D. R. et al. Severe Progressive Autism Associated with Two de novo Changes: A 2.6-Mb 2q31.1 Deletion and a Balanced t(14;21)(q21.1;p11.2) Translocation with Long-Range Epigenetic Silencing of LRFN5 Expression. Mol Syndromol 1, 46-57, doi: 10.1159/000280290 (2010).
20. Mikhail, F. M. et al. Clinically relevant single gene or intragenic deletions encompassing critical neurodevelopmental genes in patients with developmental delay, mental retardation, and/or autism spectrum disorders. Am J Med Genet A 155A, 2386-2396, doi: 10.1002/ajmg.a.34177 (2011).
21. Hussman, J. P. et al. A noise-reduction GWAS analysis implicates altered regulation of neurite outgrowth and guidance in autism. Mol Autism 2, 1, doi: 10.1186/2040-2392-2-1 (2011).
22. Wang, K. et al. Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature 459, 528-533, doi: 10.1038/ nature07999 (2009).
23. Voineagu, I. & Yoo, H. J. Current progress and challenges in the search for autism biomarkers. Dis Markers 35, 55-65, doi: 10.1155/2013/476276 (2013).
24. Xu, B. et al. Elucidating the genetic architecture of familial schizophrenia using rare copy number variant and linkage scans. Proc Natl Acad Sci USA 106, 16746-16751, doi: 10.1073/pnas.0908584106 (2009).
25. Mitchell, K. J. The genetics of neurodevelopmental disease.Curr Opin Neurobiol, doi: 10.1016/j.conb.2010.08.009 (2010).
26. Johnson, K. G. & Van Vactor, D. Receptor protein tyrosine phosphatases in nervous system development. Physiol Rev 83, 1-24, doi: 10.1152/physrev.00016.2002 (2003).
27. Stryker, E. & Johnson, K. G. LAR, liprin alpha and the regulation of active zone morphogenesis. J Cell Sci 120, 3723-3728, doi: 10.1242/jcs.03491 (2007).
28. Dunah, A. W. et al. LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci 8, 458-467, doi: 10.1038/nn1416 (2005).
29. Hoogenraad, C. C. et al. Liprinalpha1 degradation by calcium/calmodulin-dependent protein kinase II regulates LAR receptor tyrosine phosphatase distribution and dendrite development. Dev Cell 12, 587-602, doi: 10.1016/j.devcel.2007.02.006 (2007).
30. Woo, J. et al. Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nature Neurosci 12, 428-437 (2009).
31. Woo, J., Kwon, S. K. & Kim, E. The NGL family of leucine-rich repeat-containing synaptic adhesion molecules. Mol Cell Neurosci 42, 1-10 (2009).
32. Kwon, S. K., Woo, J., Kim, S. Y., Kim, H. & Kim, E. Trans-synaptic adhesions between netrin-G ligand-3 (NGL-3) and receptor tyrosine phosphatases LAR, protein-tyrosine phosphatase delta (PTPdelta), and PTPsigma via specific domains regulate excitatory synapse formation. J Biol Chem 285, 13966-13978, doi: 10.1074/jbc.M109.061127 (2010).
33. Takahashi, H. et al. Postsynaptic TrkC and presynaptic PTPsigma function as a bidirectional excitatory synaptic organizing complex. Neuron 69, 287-303, doi: 10.1016/j.neuron.2010.12.024 (2011).
34. Valnegri, P. et al. The X-linked intellectual disability protein IL1RAPL1 regulates excitatory synapse formation by binding PTPdelta and RhoGAP2. Hum Mol Genet 20, 4797-4809, doi: 10.1093/hmg/ddr418 (2011).
35. Yoshida, T. et al. IL-1 receptor accessory protein-like 1 associated with mental retardation and autism mediates synapse formation by trans-synaptic interaction with protein tyrosine phosphatase delta. J Neurosci 31, 13485-13499, doi: 10.1523/ JNEUROSCI.2136-11.2011 (2011).
36. Yoshida, T. et al. Interleukin-1 receptor accessory protein organizes neuronal synaptogenesis as a cell adhesion molecule. J Neurosci 32, 2588-2600, doi: 10.1523/JNEUROSCI.4637-11.2012 (2012).
37. Takahashi, H. et al. Selective control of inhibitory synapse development by Slitrk3-PTPdelta trans-synaptic interaction. Nat Neurosci 15, 389-398, S381-382, doi: 10.1038/nn.3040 (2012).
38. Yim, Y. S. et al. Slitrks control excitatory and inhibitory synapse formation with LAR receptor protein tyrosine phosphatases. Proc Natl Acad Sci USA 110, 4057-4062, doi: 10.1073/pnas.1209881110 (2013).
39. Li, Y. et al. Splicing-Dependent Trans-synaptic SALM3-LAR-RPTP Interactions Regulate Excitatory Synapse Development and Locomotion. Cell reports, doi: 10.1016/j.celrep.2015.08.002 (2015).
40. Ko, J. S. et al. PTPsigma functions as a presynaptic receptor for the glypican-4/LRRTM4 complex and is essential for excitatory synaptic transmission. PNAS 112, 1874-1879, doi: 10.1073/pnas.1410138112 (2015).
41. Song, Y. S., Lee, H. J., Prosselkov, P., Itohara, S. & Kim, E. Trans-induced cis interaction in the tripartite NGL-1, netrin-G1 and LAR adhesion complex promotes development of excitatory synapses. J Cell Sci 126, 4926-4938, doi: 10.1242/jcs.129718 (2013).
42. Uetani, N. et al. Impaired learning with enhanced hippocampal long-term potentiation in PTPdelta-deficient mice. EMBO J 19, 2775-2785, doi: 10.1093/emboj/19.12.2775 (2000).
43. Elchebly, M. et al. Neuroendocrine dysplasia in mice lacking protein tyrosine phosphatase sigma. Nat Genet 21, 330-333, doi: 10.1038/6859 (1999).
44. Wallace, M. J. et al. Neuronal defects and posterior pituitary hypoplasia in mice lacking the receptor tyrosine phosphatase PTPsigma. Nat Genet 21, 334-338, doi: 10.1038/6866 (1999).
45. Yeo, T. T. et al. Deficient LAR expression decreases basal forebrain cholinergic neuronal size and hippocampal cholinergic innervation. J Neurosci Res 47, 348-360 (1997).
46. Van Lieshout, E. M., Van der Heijden, I., Hendriks, W. J. & Van der Zee, C. E. A decrease in size and number of basal forebrain cholinergic neurons is paralleled by diminished hippocampal cholinergic innervation in mice lacking leukocyte common antigenrelated protein tyrosine phosphatase activity. Neuroscience 102, 833-841 (2001).
47. Meathrel, K., Adamek, T., Batt, J., Rotin, D. & Doering, L. C. Protein tyrosine phosphatase sigma-deficient mice show aberrant cytoarchitecture and structural abnormalities in the central nervous system. J Neurosci Res 70, 24-35, doi: 10.1002/jnr.10382 (2002).
48. Kolkman, M. J. et al. Mice lacking leukocyte common antigen-related (LAR) protein tyrosine phosphatase domains demonstrate spatial learning impairment in the two-trial water maze and hyperactivity in multiple behavioural tests. Behav Brain Res 154, 171-182, doi: 10.1016/j.bbr.2004.02.006 (2004).
49. Xie, Y. et al. The leukocyte common antigen-related protein tyrosine phosphatase receptor regulates regenerative neurite outgrowth in vivo. J Neurosci 21, 5130-5138 (2001).
50. Van der Zee, C. E. et al. Delayed peripheral nerve regeneration and central nervous system collateral sprouting in leucocyte common antigen-related protein tyrosine phosphatase-deficient mice. Eur J Neurosci 17, 991-1005 (2003).
51. Schormair, B. et al. PTPRD (protein tyrosine phosphatase receptor type delta) is associated with restless legs syndrome. Nature Genet 40, 946-948, doi: 10.1038/ng.190 (2008).
52. Elia, J. et al. Rare structural variants found in attention-deficit hyperactivity disorder are preferentially associated with neurodevelopmental genes. Mol Psychiatry, doi: 10.1038/mp.2010.75 (2010).
53. Pinto, D. et al. Functional impact of global rare copy number variation in autism spectrum disorders. Nature, doi: 10.1038/ nature09146 (2010).
54. Yang, Q. et al. Family-based and population-based association studies validate PTPRD as a risk factor for restless legs syndrome. Mov Disorders 26, 516-519, doi: 10.1002/mds.23459 (2011).
55. Malhotra, D. et al. High Frequencies of De Novo CNVs in Bipolar Disorder and Schizophrenia. Neuron 72, 951-963, doi: 10.1016/j.neuron.2011.11.007 (2011).
56. Um, J. W. et al. Structural basis for LAR-RPTP/Slitrk complex-mediated synaptic adhesion. Nat Commun 5, 5423, doi: 10.1038/ ncomms6423 (2014).
57. Chih, B., Gollan, L. & Scheiffele, P. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51, 171-178, doi: 10.1016/j.neuron.2006.06.005 (2006).
58. Boucard, A. A., Chubykin, A. A., Comoletti, D., Taylor, P. & Sudhof, T. C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha-and beta-neurexins. Neuron 48, 229-236, doi: 10.1016/j.neuron.2005.08.026 (2005).
59. Graf, E. R., Kang, Y., Hauner, A. M. & Craig, A. M. Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J Neurosci 26, 4256-4265 (2006).
60. Ko, J., Fuccillo, M. V., Malenka, R. C. & Sudhof, T. C. LRRTM2 Functions as a Neurexin Ligand in Promoting Excitatory Synapse Formation. Neuron 64, 791-798, doi: 10.1016/j.neuron.2009.12.012 (2009).
61. Siddiqui, T. J., Pancaroglu, R., Kang, Y., Rooyakkers, A. & Craig, A. M. LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development. J Neurosci 30, 7495-7506, doi: 10.1523/JNEUROSCI.0470-10.2010 (2010).
62. Uemura, T. et al. Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 141, 1068-1079, doi: 10.1016/j.cell.2010.04.035 (2010).
63. Comoletti, D. et al. Gene selection, alternative splicing, and post-translational processing regulate neuroligin selectivity for betaneurexins. Biochemistry 45, 12816-12827, doi: 10.1021/bi0614131 (2006).
64. Pulido, R., Serra-Pages, C., Tang, M. & Streuli, M. The LAR/PTP delta/PTP sigma subfamily of transmembrane protein-tyrosinephosphatases: multiple human LAR, PTP delta, and PTP sigma isoforms are expressed in a tissue-specific manner and associate with the LAR-interacting protein LIP.1. PNAS 92, 11686-11690 (1995).
65. Irimia, M. et al. A highly conserved program of neuronal microexons is misregulated in autistic brains. Cell 159, 1511-1523, 66. doi: 10.1016/j.cell.2014.11.035 (2014).
66. Han, W. et al. Shank2 associates with and regulates Na+ /H+ exchanger 3. J Biol Chem 281, 1461-1469, doi: 10.1074/jbc.M509786200 (2006).
67. Kim, H. M. et al. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist eritoran. Cell 130, 906-917, 69. doi: 10.1016/j.cell.2007.08.002 (2007).
68. Biederer, T. & Scheiffele, P. Mixed-culture assays for analyzing neuronal synapse formation. Nature protocols 2, 670-676 (2007).
69. Ko, J., Soler-Llavina, G. J., Fuccillo, M. V., Malenka, R. C. & Sudhof, T. C. Neuroligins/LRRTMs prevent activity-and Ca2+ / calmodulin-dependent synapse elimination in cultured neurons. J Cell Biol 194, 323-334, doi: 10.1083/jcb.201101072 (2011).