High-throughput genetic screen for synaptogenic factors: Identification of lrp6 as critical for excitatory synapse development

Cell Reports

Volumn 5, Issue 5, 2013, Pages 1330-1341

  Sharma, Kamal ^a   Choi, Se Young ^b   Zhang, Yong ^a   Nieland, Thomas J F ^c   Long, Shunyou ^a   Li, Min ^a   Huganir, Richard L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BK 21 Plus   (South Korea)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; REGULATOR PROTEIN; SHORT HAIRPIN RNA; SYNAPTOGENIC FACTOR; UNCLASSIFIED DRUG; WNT LIGAND RECEPTOR COMPLEX; WNT PROTEIN; WNT8A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOMATION; CONTROLLED STUDY; EMBRYO; EXCITATORY SYNAPSE; GENE SILENCING; HIGH THROUGHPUT SCREENING; IN VIVO STUDY; MAMMAL; MOUSE; NERVE CELL; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SYNAPSE; SYNAPTOGENESIS;

INVERTEBRATA; MAMMALIA;

ANIMALS; CLONING, MOLECULAR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HEK293 CELLS; HIGH-THROUGHPUT SCREENING ASSAYS; HIPPOCAMPUS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MICE; NEURONS; OPTICAL IMAGING; PROTEIN BINDING; RATS; RNA, SMALL INTERFERING; SYNAPSES; SYNAPTIC POTENTIALS;

EID: 84890229121     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.11.008     Document Type: Article

References (54)

1. Aberle H., Haghighi A.P., Fetter R.D., McCabe B.D., Magalhães T.R., Goodman C.S. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 2002, 33:545-558.
2. Allen N.J., Bennett M.L., Foo L.C., Wang G.X., Chakraborty C., Smith S.J., Barres B.A. Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 2012, 486:410-414.
3. Brewer G.J., Cotman C.W. Survival and growth of hippocampal neurons in defined medium at low density: advantages of a sandwich culture technique or low oxygen. Brain Res. 1989, 494:65-74.
4. Chen J., Park C.S., Tang S.J. Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J.Biol. Chem. 2006, 281:11910-11916.
5. Chih B., Engelman H., Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 2005, 307:1324-1328.
6. Christopherson K.S., Ullian E.M., Stokes C.C., Mullowney C.E., Hell J.W., Agah A., Lawler J., Mosher D.F., Bornstein P., Barres B.A. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005, 120:421-433.
7. Chung N., Zhang X.D., Kreamer A., Locco L., Kuan P.F., Bartz S., Linsley P.S., Ferrer M., Strulovici B. Median absolute deviation to improve hit selection for genome-scale RNAi screens. J.Biomol. Screen. 2008, 13:149-158.
8. Ciani L., Salinas P.C. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat. Rev. Neurosci. 2005, 6:351-362.
9. 2+/Calmodulin-dependent protein kinase II. Proc. Natl. Acad. Sci. USA 2011, 108:10732-10737.
10. Dalva M.B., Takasu M.A., Lin M.Z., Shamah S.M., Hu L., Gale N.W., Greenberg M.E. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 2000, 103:945-956.
11. Davidson G., Shen J., Huang Y.L., Su Y., Karaulanov E., Bartscherer K., Hassler C., Stannek P., Boutros M., Niehrs C. Cell cycle control of wnt receptor activation. Dev. Cell 2009, 17:788-799.
12. Featherstone D.E., Rushton E.M., Hilderbrand-Chae M., Phillips A.M., Jackson F.R., Broadie K. Presynaptic glutamic acid decarboxylase is required for induction of the postsynaptic receptor field at a glutamatergic synapse. Neuron 2000, 27:71-84.
13. Garner C.C., Nash J., Huganir R.L. PDZ domains in synapse assembly and signalling. Trends Cell Biol. 2000, 10:274-280.
14. Gogolla N., Galimberti I., Deguchi Y., Caroni P. Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron 2009, 62:510-525.
15. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 2004, 119:1013-1026.
16. Hering H., Sheng M. Direct interaction of Frizzled-1, -2, -4, and -7 with PDZ domains of PSD-95. FEBS Lett. 2002, 521:185-189.
17. Itasaki N., Jones C.M., Mercurio S., Rowe A., Domingos P.M., Smith J.C., Krumlauf R. Wise, a context-dependent activator and inhibitor of Wnt signalling. Development 2003, 130:4295-4305.
18. Jain S., Heutink P. From single genes to gene networks: high-throughput-high-content screening for neurological disease. Neuron 2010, 68:207-217.
19. Knott G.W., Holtmaat A., Wilbrecht L., Welker E., Svoboda K. Spine growth precedes synapse formation in the adult neocortex invivo. Nat. Neurosci. 2006, 9:1117-1124.
20. Koles K., Budnik V. Wnt signaling in neuromuscular junction development. Cold Spring Harb. Perspect. Biol. 2012, 4:a008045.
21. König R., Chiang C.Y., Tu B.P., Yan S.F., DeJesus P.D., Romero A., Bergauer T., Orth A., Krueger U., Zhou Y., Chanda S.K. A probability-based approach for the analysis of large-scale RNAi screens. Nat. Methods 2007, 4:847-849.
22. Korkut C., Budnik V. WNTs tune up the neuromuscular junction. Nat. Rev. Neurosci. 2009, 10:627-634.
23. Kurusu M., Cording A., Taniguchi M., Menon K., Suzuki E., Zinn K. A screen of cell-surface molecules identifies leucine-rich repeat proteins as key mediators of synaptic target selection. Neuron 2008, 59:972-985.
24. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
25. Linhoff M.W., Laurén J., Cassidy R.M., Dobie F.A., Takahashi H., Nygaard H.B., Airaksinen M.S., Strittmatter S.M., Craig A.M. An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 2009, 61:734-749.
26. McAllister A.K. Dynamic aspects of CNS synapse formation. Annu. Rev. Neurosci. 2007, 30:425-450.
27. Melom J.E., Littleton J.T. Synapse development in health and disease. Curr. Opin. Genet. Dev. 2011, 21:256-261.
28. Miech C., Pauer H.U., He X., Schwarz T.L. Presynaptic local signaling by a canonical wingless pathway regulates development of the Drosophila neuromuscular junction. J.Neurosc. 2008, 28:10875-10884.
29. Mitchell K.J. The genetics of neurodevelopmental disease. Curr. Opin. Neurobiol. 2011, 21:197-203.
30. Najdi R., Proffitt K., Sprowl S., Kaur S., Yu J., Covey T.M., Virshup D.M., Waterman M.L. A uniform human Wnt expression library reveals a shared secretory pathway and unique signaling activities. Differentiation 2012, 84:203-213.
31. Nitkin R.M., Smith M.A., Magill C., Fallon J.R., Yao Y.M., Wallace B.G., McMahan U.J. Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J.Cell Biol. 1987, 105:2471-2478.
32. Okabe S. Molecular dynamics of the excitatory synapse. Adv. Exp. Med. Biol. 2012, 970:131-152.
33. O'Rourke N.A., Weiler N.C., Micheva K.D., Smith S.J. Deep molecular diversity of mammalian synapses: why it matters and how to measure it. Nat. Rev. Neurosci. 2012, 13:365-379.
34. Packard M., Koo E.S., Gorczyca M., Sharpe J., Cumberledge S., Budnik V. The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 2002, 111:319-330.
35. Paradis S., Harrar D.B., Lin Y., Koon A.C., Hauser J.L., Griffith E.C., Zhu L., Brass L.F., Chen C., Greenberg M.E. An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 2007, 53:217-232.
36. Park M., Watanabe S., Poon V.Y., Ou C.Y., Jorgensen E.M., Shen K. CYY-1/cyclin Y and CDK-5 differentially regulate synapse elimination and formation for rewiring neural circuits. Neuron 2011, 70:742-757.
37. Peng H.B., Baker L.P., Chen Q. Induction of synaptic development in cultured muscle cells by basic fibroblast growth factor. Neuron 1991, 6:237-246.
38. Penzes P., Beeser A., Chernoff J., Schiller M.R., Eipper B.A., Mains R.E., Huganir R.L. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 2003, 37:263-274.
39. Pinson K.I., Brennan J., Monkley S., Avery B.J., Skarnes W.C. An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 2000, 407:535-538.
40. Schaefer A.M., Hadwiger G.D., Nonet M.L. rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 2000, 26:345-356.
41. Scheiffele P., Fan J., Choih J., Fetter R., Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 2000, 101:657-669.
42. Shen K., Scheiffele P. Genetics and cell biology of building specific synaptic connectivity. Annu. Rev. Neurosci. 2010, 33:473-507.
43. Sheng M., McFadden G., Greenberg M.E. Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 1990, 4:571-582.
44. Siddiqui T.J., Craig A.M. Synaptic organizing complexes. Curr. Opin. Neurobiol. 2011, 21:132-143.
45. Tabata H., Nakajima K. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 2001, 103:865-872.
46. Takahashi H., Arstikaitis P., Prasad T., Bartlett T.E., Wang Y.T., Murphy T.H., Craig A.M. Postsynaptic TrkC and presynaptic PTPσ function as a bidirectional excitatory synaptic organizing complex. Neuron 2011, 69:287-303.
47. Tamai K., Semenov M., Kato Y., Spokony R., Liu C., Katsuyama Y., Hess F., Saint-Jeannet J.P., He X. LDL-receptor-related proteins in Wnt signal transduction. Nature 2000, 407:530-535.
48. Tamai K., Zeng X., Liu C., Zhang X., Harada Y., Chang Z., He X. A mechanism for Wnt coreceptor activation. Mol. Cell 2004, 13:149-156.
49. van Amerongen R., Mikels A., Nusse R. Alternative wnt signaling is initiated by distinct receptors. Sci. Signal. 2008, 1:re9.
50. Varela-Nallar L., Alfaro I.E., Serrano F.G., Parodi J., Inestrosa N.C. Wingless-type family member 5A (Wnt-5a) stimulates synaptic differentiation and function of glutamatergic synapses. Proc. Natl. Acad. Sci. USA 2010, 107:21164-21169.
51. Wayman G.A., Impey S., Marks D., Saneyoshi T., Grant W.F., Derkach V., Soderling T.R. Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 2006, 50:897-909.
52. Wehrli M., Dougan S.T., Caldwell K., O'Keefe L., Schwartz S., Vaizel-Ohayon D., Schejter E., Tomlinson A., DiNardo S. arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 2000, 407:527-530.
53. Williams M.E., de Wit J., Ghosh A. Molecular mechanisms of synaptic specificity in developing neural circuits. Neuron 2010, 68:9-18.
54. Zhang J.H., Chung T.D., Oldenburg K.R. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J.Biomol. Screen. 1999, 4:67-73.