Neuroligin 1 regulates spines and synaptic plasticity via LIMK1/cofilin-mediated actin reorganization

Journal of Cell Biology

Volumn 212, Issue 4, 2016, Pages 449-463

  Liu, An ^a   Zhou, Zikai ^a   Dang, Rui ^a   Zhu, Yuehua ^a   Qi, Junxia ^a   He, Guiqin ^b,c   Leung, Celeste ^a   Pak, Daniel ^d   Jia, Zhengping ^b,c   Xie, Wei ^a  

^a SOUTHEAST UNIVERSITY   (China)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COFILIN; LIM KINASE 1; NEUROLIGIN 1; ACTIN DEPOLYMERIZING FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; LIM KINASE; LIMK1 PROTEIN, MOUSE; LIMK2 PROTEIN, MOUSE; NERVE CELL ADHESION MOLECULE; PROTEIN BINDING; RAP1 PROTEIN; SIPA1L1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HEK293 CELL LINE; HUMAN; HUMAN CELL; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SPINAL NERVE; ACTIN FILAMENT; ANIMAL; BRAIN CORTEX; CYTOLOGY; DEFICIENCY; DENDRITIC SPINE; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; GENOTYPE; HIPPOCAMPUS; IN VITRO STUDY; KNOCKOUT MOUSE; METABOLISM; PHENOTYPE; PHOSPHORYLATION; PROTEIN DOMAIN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SYNAPSE; TIME FACTOR;

ACTIN CYTOSKELETON; ACTIN DEPOLYMERIZING FACTORS; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CEREBRAL CORTEX; DENDRITIC SPINES; GENOTYPE; GTPASE-ACTIVATING PROTEINS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; IN VITRO TECHNIQUES; LIM KINASES; MICE, KNOCKOUT; NEURONAL PLASTICITY; PHENOTYPE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RAP1 GTP-BINDING PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SYNAPSES; TIME FACTORS; TRANSFECTION;

EID: 84959566066     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201509023     Document Type: Article

References (64)

1. Aizawa, H., S. Wakatsuki, A. Ishii, K. Moriyama, Y. Sasaki, K. Ohashi, Y. Sekine-Aizawa, A. Sehara-Fujisawa, K. Mizuno, Y. Goshima, and I. Yahara. 2001. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat. Neurosci. 4:367-373. http://dx.doi.org/10.1038/86011
2. Asrar, S., and Z. Jia. 2013. Molecular mechanisms coordinating functional and morphological plasticity at the synapse: role of GluA2/N-cadherin interaction-mediated actin signaling in mGluR-dependent LTD. Cell. Signal. 25:397-402. http://dx.doi.org/10.1016/j.cellsig.2012.11.007
3. Baksh, M.M., C. Dean, S. Pautot, S. DeMaria, E. Isacoff, and J.T. Groves. 2005. Neuronal activation by GPI-linked neuroligin-1 displayed in synthetic lipid bilayer membranes. Langmuir. 21:10693-10698. http://dx.doi.org/10.1021/la051243d
4. Bamburg, J.R. 1999. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15:185-230. http://dx.doi.org/10.1146/annurev.cellbio.15.1.185
5. Baudouin, S.J., J. Gaudias, S. Gerharz, L. Hatstatt, K. Zhou, P. Punnakkal, K.F. Tanaka, W. Spooren, R. Hen, C.I. De Zeeuw, et al. 2012. Shared synaptic pathophysiology in syndromic and nonsyndromic rodent models of autism. Science. 338:128-132. http://dx.doi.org/10.1126/science.1224159
6. Becker-Hapak, M., S.S. McAllister, and S.F. Dowdy. 2001. TAT-mediated protein transduction into mammalian cells. Methods. 24:247-256. http://dx.doi.org/10.1006/meth.2001.1186
7. Bernard, O. 2007. Lim kinases, regulators of actin dynamics. Int. J. Biochem. Cell Biol. 39:1071-1076. http://dx.doi.org/10.1016/j.biocel.2006.11.011
8. Bernstein, B.W., and J.R. Bamburg. 2010. ADF/cofilin: a functional node in cell biology. Trends Cell Biol. 20:187-195. http://dx.doi.org/10.1016/j.tcb.2010.01.001
9. Blundell, J., C.A. Blaiss, M.R. Etherton, F. Espinosa, K. Tabuchi, C. Walz, M.F. Bolliger, T.C. Südhof, and C.M. Powell. 2010. Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior. J. Neurosci. 30:2115-2129. http://dx.doi.org/10.1523/JNEUROSCI.4517-09.2010
10. Bosch, M., J. Castro, T. Saneyoshi, H. Matsuno, M. Sur, and Y. Hayashi. 2014. Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron. 82:444-459. http://dx.doi.org/10.1016/j.neuron.2014.03.021
11. Boucard, A.A., A.A. Chubykin, D. Comoletti, P. Taylor, and T.C. Südhof. 2005. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to α- and β-neurexins. Neuron. 48:229-236. http://dx.doi.org/10.1016/j.neuron.2005.08.026
12. Chen, B., K. Brinkmann, Z. Chen, C.W. Pak, Y. Liao, S. Shi, L. Henry, N.V. Grishin, S. Bogdan, and M.K. Rosen. 2014. The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell. 156:195-207. http://dx.doi.org/10.1016/j.cell.2013.11.048
13. Chih, B., S.K. Afridi, L. Clark, and P. Scheiffele. 2004. Disorder-associated mutations lead to functional inactivation of neuroligins. Hum. Mol. Genet. 13:1471-1477. http://dx.doi.org/10.1093/hmg/ddh158
14. Chubykin, A.A., D. Atasoy, M.R. Etherton, N. Brose, E.T. Kavalali, J.R. Gibson, and T.C. Südhof. 2007. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron. 54:919-931. http://dx.doi.org/10.1016/j.neuron.2007.05.029
15. Cingolani, L.A., and Y. Goda. 2008. Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 9:344-356. http://dx.doi.org/10.1038/nrn2373
16. Cline, H. 2005. Synaptogenesis: a balancing act between excitation and inhibition. Curr. Biol. 15:R203-R205. http://dx.doi.org/10.1016/j.cub.2005.03.010
17. Conroy, W.G., Q. Nai, B. Ross, G. Naughton, and D.K. Berg. 2007. Postsynaptic neuroligin enhances presynaptic inputs at neuronal nicotinic synapses. Dev. Biol. 307:79-91. http://dx.doi.org/10.1016/j.ydbio.2007.04.017
18. Dean, C., and T. Dresbach. 2006. Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function. Trends Neurosci. 29:21-29. http://dx.doi.org/10.1016/j.tins.2005.11.003
19. Dean, C., F.G. Scholl, J. Choih, S. DeMaria, J. Berger, E. Isacoff, and P. Scheiffele. 2003. Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6:708-716. http://dx.doi.org/10.1038/nn1074
20. Dong, N., J. Qi, and G. Chen. 2007. Molecular reconstitution of functional GABAergic synapses with expression of neuroligin-2 and GABAA receptors. Mol. Cell. Neurosci. 35:14-23. http://dx.doi.org/10.1016/j.mcn.2007.01.013
21. Feng, G., R.H. Mellor, M. Bernstein, C. Keller-Peck, Q.T. Nguyen, M. Wallace, J.M. Nerbonne, J.W. Lichtman, and J.R. Sanes. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron. 28:41-51. http://dx.doi.org/10.1016/S0896-6273(00)00084-2
22. Freeman, S.A., V. Lei, M. Dang-Lawson, K. Mizuno, C.D. Roskelley, and M.R. Gold. 2011. Cofilin-mediated F-actin severing is regulated by the Rap GTPase and controls the cytoskeletal dynamics that drive lymphocyte spreading and BCR microcluster formation. J. Immunol. 187:5887-5900. http://dx.doi.org/10.4049/jimmunol.1102233
23. Futai, K., M.J. Kim, T. Hashikawa, P. Scheiffele, M. Sheng, and Y. Hayashi. 2007. Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nat. Neurosci. 10:186-195. http://dx.doi.org/10.1038/nn1837
24. Gottmann, K. 2008. Transsynaptic modulation of the synaptic vesicle cycle by cell-adhesion molecules. J. Neurosci. Res. 86:223-232. http://dx.doi.org/10.1002/jnr.21484
25. Govek, E.E., S.E. Newey, and L. Van Aelst. 2005. The role of the Rho GTPases in neuronal development. Genes Dev. 19:1-49. http://dx.doi.org/10.1101/gad.1256405
26. Graf, E.R., X. Zhang, S.X. Jin, M.W. Linhoff, and A.M. Craig. 2004. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell. 119:1013-1026. http://dx.doi.org/10.1016/j.cell.2004.11.035
27. Gu, J., C.W. Lee, Y. Fan, D. Komlos, X. Tang, C. Sun, K. Yu, H.C. Hartzell, G. Chen, J.R. Bamburg, and J.Q. Zheng. 2010. ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat. Neurosci. 13:1208-1215. http://dx.doi.org/10.1038/nn.2634
28. Hoe, H.S., J.Y. Lee, and D.T. Pak. 2009. Combinatorial morphogenesis of dendritic spines and filopodia by SPAR and alpha-actinin2. Biochem. Biophys. Res. Commun. 384:55-60. http://dx.doi.org/10.1016/j.bbrc.2009.04.069
29. Huang, Z.H., Y. Wang, Z.D. Su, J.G. Geng, Y.Z. Chen, X.B. Yuan, and C. He. 2011. Slit-2 repels the migration of olfactory ensheathing cells by triggering Ca2+-dependent cofilin activation and RhoA inhibition. J. Cell Sci. 124:186-197. http://dx.doi.org/10.1242/jcs.071357
30. Irie, M., Y. Hata, M. Takeuchi, K. Ichtchenko, A. Toyoda, K. Hirao, Y. Takai, T.W. Rosahl, and T.C. Südhof. 1997. Binding of neuroligins to PSD-95. Science. 277:1511-1515. http://dx.doi.org/10.1126/science.277.5331.1511
31. Jedlicka, P., M. Vnencak, D.D. Krueger, T. Jungenitz, N. Brose, and S.W. Schwarzacher. 2015. Neuroligin-1 regulates excitatory synaptic transmission, LTP and EPSP-spike coupling in the dentate gyrus in vivo. Brain Struct. Funct. 220:47-58. http://dx.doi.org/10.1007/s00429-013-0636-1
32. Jia, Z., Z. Todorovski, Y. Meng, S. Asrar, and L.Y. Wang. 2009. LIMK-1 and actin regulation of spine and synaptic function. In The New Encyclopedia of Neurosciences. L.R. Squire, editor. Academic Press, Oxford, England, UK. 467-472.
33. Jung, S.Y., J. Kim, O.B. Kwon, J.H. Jung, K. An, A.Y. Jeong, C.J. Lee, Y.B. Choi, C.H. Bailey, E.R. Kandel, and J.H. Kim. 2010. Input-specific synaptic plasticity in the amygdala is regulated by neuroligin-1 via postsynaptic NMDA receptors. Proc. Natl. Acad. Sci. USA. 107:4710-4715. http://dx.doi.org/10.1073/pnas.1001084107
34. Kattenstroth, G., E. Tantalaki, T.C. Südhof, K. Gottmann, and M. Missler. 2004. Postsynaptic N-methyl-D-aspartate receptor function requires α-neurexins. Proc. Natl. Acad. Sci. USA. 101:2607-2612. http://dx.doi.org/10.1073/pnas.0308626100
35. Kemp, N., and Z.I. Bashir. 1999. Induction of LTD in the adult hippocampus by the synaptic activation of AMPA/kainate and metabotropic glutamate receptors. Neuropharmacology. 38:495-504. http://dx.doi.org/10.1016/S0028-3908(98)00222-6
36. Kemp, N., J. McQueen, S. Faulkes, and Z.I. Bashir. 2000. Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol. Eur. J. Neurosci. 12:360-366. http://dx.doi.org/10.1046/j.1460-9568.2000.00903.x
37. Kim, J., S.Y. Jung, Y.K. Lee, S. Park, J.S. Choi, C.J. Lee, H.S. Kim, Y.B. Choi, P. Scheiffele, C.H. Bailey, et al. 2008. Neuroligin-1 is required for normal expression of LTP and associative fear memory in the amygdala of adult animals. Proc. Natl. Acad. Sci. USA. 105:9087-9092. http://dx.doi.org/10.1073/pnas.0803448105
38. Knaus, U.G., A. Bamberg, and G.M. Bokoch. 2007. Rac and Rap GTPase activation assays. Methods Mol. Biol. 412:59-67. http://dx.doi.org/10.1007/978-1-59745-467-4 _5
39. Ko, J., C. Zhang, D. Arac, A.A. Boucard, A.T. Brunger, and T.C. Südhof. 2009. Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation. EMBO J. 28:3244-3255. http://dx.doi.org/10.1038/emboj.2009.249
40. Kwon, H.B., Y. Kozorovitskiy, W.J. Oh, R.T. Peixoto, N. Akhtar, J.L. Saulnier, C. Gu, and B.L. Sabatini. 2012. Neuroligin-1-dependent competition regulates cortical synaptogenesis and synapse number. Nat. Neurosci. 15:1667-1674. http://dx.doi.org/10.1038/nn.3256
41. LaVallie, E.R., E.A. DiBlasio, S. Kovacic, K.L. Grant, P.F. Schendel, and J.M. McCoy. 1993. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnology (N. Y.). 11:187-193. http://dx.doi.org/10.1038/nbt0293-187
42. Meng, Y., Y. Zhang, V. Tregoubov, C. Janus, L. Cruz, M. Jackson, W.Y. Lu, J.F. MacDonald, J.Y. Wang, D.L. Falls, and Z. Jia. 2002. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron. 35:121-133. http://dx.doi.org/10.1016/S0896-6273(02)00758-4
43. Meng, Y., Y. Zhang, and Z. Jia. 2003. Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron. 39:163-176. http://dx.doi.org/10.1016/S0896-6273(03)00368-4
44. Meng, Y., H. Takahashi, J. Meng, Y. Zhang, G. Lu, S. Asrar, T. Nakamura, and Z. Jia. 2004. Regulation of ADF/cofilin phosphorylation and synaptic function by LIM-kinase. Neuropharmacology. 47:746-754. http://dx.doi.org/10.1016/j.neuropharm.2004.06.030
45. Meyer, G., F. Varoqueaux, A. Neeb, M. Oschlies, and N. Brose. 2004. The complexity of PDZ domain-mediated interactions at glutamatergic synapses: a case study on neuroligin. Neuropharmacology. 47:724-733. http://dx.doi.org/10.1016/j.neuropharm.2004.06.023
46. Nam, C.I., and L. Chen. 2005. Postsynaptic assembly induced by neurexinneuroligin interaction and neurotransmitter. Proc. Natl. Acad. Sci. USA. 102:6137-6142. http://dx.doi.org/10.1073/pnas.0502038102
47. Pak, D.T., S. Yang, S. Rudolph-Correia, E. Kim, and M. Sheng. 2001. Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron. 31:289-303. http://dx.doi.org/10.1016/S0896-6273(01)00355-5
48. Palsson, E.M., M. Popoff, M. Thelestam, and L.A. O'Neill. 2000. Divergent roles for Ras and Rap in the activation of p38 mitogen-activated protein kinase by interleukin-1. J. Biol. Chem. 275:7818-7825. http://dx.doi.org/10.1074/jbc.275.11.7818
49. Peixoto, R.T., P.A. Kunz, H. Kwon, A.M. Mabb, B.L. Sabatini, B.D. Philpot, and M.D. Ehlers. 2012. Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron. 76:396-409. http://dx.doi.org/10.1016/j.neuron.2012.07.006
50. Rust, M.B. 2015. ADF/cofilin: a crucial regulator of synapse physiology and behavior. Cell. Mol. Life Sci. 72:3521-3529. http://dx.doi.org/10.1007/s00018-015-1941-z
51. Rust, M.B., C.B. Gurniak, M. Renner, H. Vara, L. Morando, A. Görlich, M. Sassoè-Pognetto, M.A. Banchaabouchi, M. Giustetto, A. Triller, et al. 2010. Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics. EMBO J. 29:1889-1902. http://dx.doi.org/10.1038/emboj.2010.72
52. Scheiffele, P., J. Fan, J. Choih, R. Fetter, and T. Serafini. 2000. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell. 101:657-669. http://dx.doi.org/10.1016/S0092-8674(00)80877-6
53. Shipman, S.L., and R.A. Nicoll. 2012. A subtype-specific function for the extracellular domain of neuroligin 1 in hippocampal LTP. Neuron. 76:309-316. http://dx.doi.org/10.1016/j.neuron.2012.07.024
54. Suzuki, K., Y. Hayashi, S. Nakahara, H. Kumazaki, J. Prox, K. Horiuchi, M. Zeng, S. Tanimura, Y. Nishiyama, S. Osawa, et al. 2012. Activitydependent proteolytic cleavage of neuroligin-1. Neuron. 76:410-422. http://dx.doi.org/10.1016/j.neuron.2012.10.003
55. Tabuchi, K., J. Blundell, M.R. Etherton, R.E. Hammer, X. Liu, C.M. Powell, and T.C. Südhof. 2007. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science. 318:71-76. http://dx.doi.org/10.1126/science.1146221
56. Takahashi, H., U. Koshimizu, J. Miyazaki, and T. Nakamura. 2002. Impaired spermatogenic ability of testicular germ cells in mice deficient in the LIM-kinase 2 gene. Dev. Biol. 241:259-272. http://dx.doi.org/10.1006/dbio.2001.0512
57. Varoqueaux, F., G. Aramuni, R.L. Rawson, R. Mohrmann, M. Missler, K. Gottmann, W. Zhang, T.C. Südhof, and N. Brose. 2006. Neuroligins determine synapse maturation and function. Neuron. 51:741-754. http://dx.doi.org/10.1016/j.neuron.2006.09.003
58. Wang, Y., Q. Dong, X.F. Xu, X. Feng, J. Xin, D.D. Wang, H. Yu, T. Tian, and Z.Y. Chen. 2013. Phosphorylation of cofilin regulates extinction of conditioned aversive memory via AMPAR trafficking. J. Neurosci. 33:6423-6433. http://dx.doi.org/10.1523/JNEUROSCI.5107-12.2013
59. Woolfrey, K.M., D.P. Srivastava, H. Photowala, M. Yamashita, M.V. Barbolina, M.E. Cahill, Z. Xie, K.A. Jones, L.A. Quilliam, M. Prakriya, and P. Penzes. 2009. Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat. Neurosci. 12:1275-1284. http://dx.doi.org/10.1038/nn.2386
60. Xie, Z., R.L. Huganir, and P. Penzes. 2005. Activity-dependent dendritic spine structural plasticity is regulated by small GTPase Rap1 and its target AF-6. Neuron. 48:605-618. http://dx.doi.org/10.1016/j.neuron.2005.09.027
61. Xu, J., N. Xiao, and J. Xia. 2010. Thrombospondin 1 accelerates synaptogenesis in hippocampal neurons through neuroligin 1. Nat. Neurosci. 13:22-24. http://dx.doi.org/10.1038/nn.2459
62. Zhou, Z., J. Hu, M. Passafaro, W. Xie, and Z. Jia. 2011. GluA2 (GluR2) regulates metabotropic glutamate receptor-dependent long-term depression through N-cadherin-dependent and cofilin-mediated actin reorganization. J. Neurosci. 31:819-833. http://dx.doi.org/10.1523/JNEUROSCI.3869-10.2011
63. Zhu, J.J., Y. Qin, M. Zhao, L. Van Aelst, and R. Malinow. 2002. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell. 110:443-455. http://dx.doi.org/10.1016/S0092-8674(02)00897-8
64. Zhu, Y., D. Pak, Y. Qin, S.G. McCormack, M.J. Kim, J.P. Baumgart, V. Velamoor, Y.P. Auberson, P. Osten, L. van Aelst, et al. 2005. Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron. 46:905-916. http://dx.doi.org/10.1016/j.neuron.2005.04.037