Synapse maturation by activity-dependent ectodomain shedding of SIRPα

Nature Neuroscience

Volumn 16, Issue 10, 2013, Pages 1417-1425

  Toth, Anna B ^a   Terauchi, Akiko ^a   Zhang, Lily Y ^a   Johnson Venkatesh, Erin M ^a   Larsen, David J ^a   Sutton, Michael A ^a   Umemori, Hisashi ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CD47 ANTIGEN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 22; MATRIX METALLOPROTEINASE; PRESYNAPTIC RECEPTOR; REGULATOR PROTEIN; SIGNAL REGULATORY PROTEIN ALPHA; TETRODOTOXIN; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ARTICLE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SYNAPSE; SYNAPTOSOME;

ANIMALS; CELLS, CULTURED; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN CULTURE TECHNIQUES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, IMMUNOLOGIC; SYNAPSES;

EID: 84884859099     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3516     Document Type: Article

References (49)

1. Lipska, B.K., Halim, N.D., Segal, P.N. &Weinberger, D.R. Effects of reversible inactivation of the neonatal ventral hippocampus on behavior in the adult rat. J. Neurosci. 22, 2835-2842 (2002). (Pubitemid 37465832)
2. Pfeiffer, B.E. et al. Fragile X mental retardation protein is required for synapse elimination by the activity-dependent transcription factor MEF2. Neuron 66, 191-197 (2010).
3. Kasai, H., Fukuda, M., Watanabe, S., Hayashi-Takagi, A. &Noguchi, J. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 33, 121-129 (2010).
4. Sanes, J.R. &Lichtman, J.W. Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 22, 389-442 (1999). (Pubitemid 29144893)
5. Waites, C.L., Craig, A.M. &Garner, C.C. Mechanisms of vertebrate synaptogenesis. Annu. Rev. Neurosci. 28, 251-274 (2005). (Pubitemid 41098906)
6. Fox, M.A. &Umemori, H. Seeking long-term relationship: axon and target communicate to organize presynaptic differentiation. J. Neurochem. 97, 1215-1231 (2006). (Pubitemid 43725563)
7. Dalva, M.B., McClelland, A.C. &Kayser, M.S. Cell adhesion molecules: signaling functions at the synapse. Nat. Rev. Neurosci. 8, 206-220 (2007). (Pubitemid 46294663)
8. Goda, Y. &Davis, G.W. Mechanisms of synapse assembly and disassembly. Neuron 40, 243-264 (2003). (Pubitemid 37244095)
9. Tessier, C.R. &Broadie, K. Activity-dependent modulation of neural circuit synaptic connectivity. Front. Mol. Neurosci. 2, 8 (2009).
10. Kano, M. &Hashimoto, K. Synapse elimination in the central nervous system. Curr. Opin. Neurobiol. 19, 154-161 (2009).
11. Zhang, L.I. &Poo, M. Electrical activity and development of neural circuits. Nat. Neurosci. 4, 1207-1214 (2001). (Pubitemid 33733110)
12. Bleckert, A. &Wong, R.O. Identifying roles for neurotransmission in circuit assembly: insights gained from multiple model systems and experimental approaches. Bioessays 33, 61-72 (2011).
13. Kay, L., Humphreys, L., Eickholt, B.J. &Burrone, J. Neuronal activity drives matching of pre-and postsynaptic function during synapse maturation. Nat. Neurosci. 14, 688-690 (2011).
14. Flavell, S.W. &Greenberg, M.E. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu. Rev. Neurosci. 31, 563-590 (2008).
15. Umemori, H., Linhoff, M.W., Onitz, D.M. &Sanes, J.R. FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118, 257-270 (2004). (Pubitemid 38962580)
16. Umemori, H. &Sanes, J.R. Signal regulatory proteins (SIRPs) are secreted presynaptic organizing molecules. J. Biol. Chem. 283, 34053-34061 (2008).
17. Terauchi, A. et al. Distinct FGFs promote differentiation of excitatory and inhibitory synapses. Nature 465, 783-787 (2010).
18. van Beek, E.M., Cochrane, F., Barclay, A.N. &van den Berg, T.K. Signal regulatory proteins in the immune system. J. Immunol. 175, 7781-7787 (2005). (Pubitemid 41798335)
19. Barclay, A.N. &Brown, M.H. The SIRP family of receptors and immune regulation. Nat. Rev. Immunol. 6, 457-464 (2006).
20. Matozaki, T., Murata, Y., Okazawa, H. &Ohnishi, H. Functions and molecular mechanisms of the CD47-SIRP signaling pathway. Trends Cell Biol. 19, 72-80 (2009).
21. Danglot, L., Triller, A. &Marty, S. The development of hippocampal interneurons in rodents. Hippocampus 16, 1032-1060 (2006). (Pubitemid 46062830)
22. Steward, O. &Falk, P.M. Selective localization of polyribosomes beneath developing synapses: a quantitative analysis of the relationships between polyribosomes and developing synapses in the hippocampus and dentate gyrus. J. Comp. Neurol. 314, 545-557 (1991).
23. Bouvier, D. et al. Pre-synaptic and post-synaptic localization of EphA4 and EphB2 in adult mouse forebrain. J. Neurochem. 106, 682-695 (2008).
24. Biederer, T. &Scheiffele, P. Mixed-culture assays for analyzing neuronal synapse formation. Nat. Protoc. 2, 670-676 (2007). (Pubitemid 47040028)
25. Guo, C., Yang, W. &Lobe, C.G. A Cre recombinase transgene with mosaic, widespread tamoxifen-inducible action. Genesis 32, 8-18 (2002). (Pubitemid 34117127)
26. Yasuda, M. et al. Multiple forms of activity-dependent competition refine hippocampal circuits in vivo. Neuron 70, 1128-1142 (2011).
27. Wayman, G.A., Lee, Y.S., Tokumitsu, H., Silva, A.J. &Soderling, T.R. Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59, 914-931 (2008).
28. Ethell, I.M. &Ethell, D.W. Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets. J. Neurosci. Res. 85, 2813-2823 (2007). (Pubitemid 47523564)
29. Lindberg, F.P. et al. Decreased resistance to bacterial infection and granulocyte defects in IAP-deficient mice. Science 274, 795-798 (1996). (Pubitemid 26398263)
30. Chang, H.P., Lindberg, F.P., Wang, H.L., Huang, A.M. &Lee, E.H. Impaired memory retention and decreased long-term potentiation in integrin-associated protein-deficient mice. Learn. Mem. 6, 448-457 (1999). (Pubitemid 29503841)
31. Shen, K. &Cowan, C.W. Guidance molecules in synapse formation and plasticity. Cold Spring Harb. Perspect. Biol. 2, a001842 (2010).
32. Williams, M.E., de Wit, J. &Ghosh, A. Molecular mechanisms of synaptic specificity in developing neural circuits. Neuron 68, 9-18 (2010).
33. Siddiqui, T.J. &Craig, A.M. Synaptic organizing complexes. Curr. Opin. Neurobiol. 21, 132-143 (2011).
34. Wang, X.X. &Pfenninger, K.H. Functional analysis of SIRP in the growth cone. J. Cell Sci. 119, 172-183 (2006). (Pubitemid 43169310)
35. Ohnishi, H. et al. Stress-evoked tyrosine phosphorylation of signal regulatory protein regulates behavioral immobility in the forced swim test. J. Neurosci. 30, 10472-10483 (2010).
36. Hatherley, D. et al. Paired receptor specificity explained by structures of signal regulatory proteins alone and complexed with CD47. Mol. Cell 31, 266-277 (2008). (Pubitemid 352001399)
37. Hatherley, D., Graham, S.C., Harlos, K., Stuart, D.I. &Barclay, A.N. Structure of signal-regulatory protein : a link to antigen receptor evolution. J. Biol. Chem. 284, 26613-26619 (2009).
38. Edwards, D.R., Handsley, M.M. &Pennington, C.J. The ADAM metalloproteinases. Mol. Aspects Med. 29, 258-289 (2008).
39. Reiss, K. &Saftig, P. The "a disintegrin and metalloprotease" (ADAM) family of sheddases: physiological and cellular functions. Semin. Cell Dev. Biol. 20, 126-137 (2009).
40. Bai, G. &Pfaff, S.L. Protease regulation: the yin and yang of neural development and disease. Neuron 72, 9-21 (2011).
41. Peixoto, R.T. et al. Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 76, 396-409 (2012).
42. Suzuki, K. et al. Activity-dependent proteolytic cleavage of neuroligin-1. Neuron 76, 410-422 (2012).
43. Schaeren-Wiemers, N. &Gerfin-Moser, A. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100, 431-440 (1993). (Pubitemid 24049312)
44. Uesaka, T. et al. Conditional ablation of GFR1 in postmigratory enteric neurons triggers unconventional neuronal death in the colon and causes a Hirschsprung's disease phenotype. Development 134, 2171-2181 (2007). (Pubitemid 46979803)
45. Woodhams, P.L., Webb, M., Atkinson, D.J. &Seeley, P.J. A monoclonal antibody, Py, distinguishes different classes of hippocampal neurons. J. Neurosci. 9, 2170-2181 (1989). (Pubitemid 19157002)
46. Oldenborg, P.A. et al. Role of CD47 as a marker of self on red blood cells. Science 288, 2051-2054 (2000).
47. Ohnishi, H. et al. Ectodomain shedding of SHPS-1 and its role in regulation of cell migration. J. Biol. Chem. 279, 27878-27887 (2004). (Pubitemid 38900056)
48. Hahn, C.G. et al. The post-synaptic density of human postmortem brain tissues: an experimental study paradigm for neuropsychiatric illnesses. PLoS ONE 4, e5251 (2009).
49. Fox, M.A. &Sanes, J.R. Synaptotagmin I and II are present in distinct subsets of central synapses. J. Comp. Neurol. 503, 280-296 (2007). (Pubitemid 47091707)