GFP Reconstitution Across Synaptic Partners (GRASP) Defines Cell Contacts and Synapses in Living Nervous Systems

Neuron

Volumn 57, Issue 3, 2008, Pages 353-363

  Feinberg, Evan H ^a   VanHoven, Miri K ^b   Bendesky, Andres ^a   Wang, George ^b   Fetter, Richard D ^c   Shen, Kang ^b   Bargmann, Cornelia I ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

CELLBIO; MOLNEURO

Indexed keywords

CARRIER PROTEIN; MEMBRANE PROTEIN; PROTEIN GRASP; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CONTACT; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DENSE BODY; ELECTRON MICROSCOPY; FLUORESCENCE ANALYSIS; MEMBRANE RECONSTITUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPSE; SYNAPTIC MEMBRANE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; CELLS, CULTURED; GREEN FLUORESCENT PROTEINS; MICROSCOPY, ELECTRON; MODELS, BIOLOGICAL; MUTATION; NERVOUS SYSTEM; NEURONS; SYNAPSES;

EID: 38749109672     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.11.030     Document Type: Article

References (48)

1. Ackley B.D., Harrington R.J., Hudson M.L., Williams L., Kenyon C.J., Chisholm A.D., and Jin Y. The two isoforms of the Caenorhabditis elegans leukocyte-common antigen related receptor tyrosine phosphatase PTP-3 function independently in axon guidance and synapse formation. J. Neurosci. 25 (2005) 7517-7528
2. Ahmari S.E., and Smith S.J. Knowing a nascent synapse when you see it. Neuron 34 (2002) 333-336
3. Armstrong J.D., Kaiser K., Müller A., Fischbach K.F., Merchant N., and Strausfeld N.J. Flybrain, an on-line atlas and database of the Drosophila nervous system. Neuron 15 (1995) 17-20
4. Binzegger T., Douglas R.J., and Martin K.A. A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24 (2004) 8441-8453
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77 (1974) 71-94
6. Briggman K.L., and Denk W. Towards neural circuit reconstruction with volume electron microscopy techniques. Curr. Opin. Neurobiol. 16 (2006) 562-570
7. Cabantous S., Terwilliger T.C., and Waldo G.S. Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat. Biotechnol. 23 (2005) 102-107
8. Cabot J.B., Mennone A., Bogan N., Carroll J., Evinger C., and Erichsen J.T. Retrograde, trans-synaptic and transneuronal transport of fragment C of tetanus toxin by sympathetic preganglionic neurons. Neuroscience 40 (1991) 805-823
9. Card J.P., Rinaman L., Schwaber J.S., Miselis R.R., Whealy M.E., Robbins A.K., and Enquist L.W. Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J. Neurosci. 10 (1990) 1974-1994
10. Christensen M., Estevez A., Yin X., Fox R., Morrison R., McDonnell M., Gleason C., Miller III D.M., and Strange K. A primary culture system for functional analysis of C. elegans neurons and muscle cells. Neuron 33 (2002) 503-514
11. Colon-Ramos D.A., Margeta M.A., and Shen K. Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans. Science 318 (2007) 103-106
12. Combes D., Fedon Y., Toutant J.P., and Arpagaus M. Multiple ace genes encoding acetylcholinesterases of Caenorhabditis elegans have distinct tissue expression. Eur. J. Neurosci. 18 (2003) 497-512
13. Craig A.M., and Kang Y. Neurexin-neuroligin signaling in synapse development. Curr. Opin. Neurobiol. 17 (2007) 43-52
14. Dunah A.W., Hueske E., Wyszynski M., Hoogenraad C.C., Jaworski J., Pak D.T., Simonetta A., Liu G., and Sheng M. LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat. Neurosci. 8 (2005) 458-467
15. Ghosh I., Hamilton A.D., and Regan L. Antiparallel leucine zipper-directed protein reassembly: application to the green fluorescent protein. J. Am. Chem. Soc. 122 (2000) 5658-5659
16. Katz L.C., and Dalva M.B. Scanning laser photostimulation: a new approach for analyzing brain circuits. J. Neurosci. Methods 54 (1994) 205-218
17. Kaufmann N., DeProto J., Ranjan R., Wan H., and Van Vactor D. Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34 (2002) 27-38
18. Kerppola T.K. Visualization of molecular interactions by fluorescence complementation. Nat. Rev. Mol. Cell Biol. 7 (2006) 449-456
19. Klassen M.P., and Shen K. A Wnt signaling pathway inhibits synapse formation in C. elegans. Cell 130 (2007) 704-716
20. 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 445 (2007) 168-176
21. Lickteig K.M., Duerr J.S., Frisby D.L., Hall D.H., Rand J.B., and Miller III D.M. Regulation of neurotransmitter vesicles by the homeodomain protein UNC-4 and its transcriptional corepressor UNC-37/groucho in Caenorhabditis elegans cholinergic motor neurons. J. Neurosci. 21 (2001) 2001-2014
22. Maskos U., Kissa K., St Cloment C., and Brulet P. Retrograde trans-synaptic transfer of green fluorescent protein allows the genetic mapping of neuronal circuits in transgenic mice. Proc. Natl. Acad. Sci. USA 99 (2002) 10120-10125
23. Mello C., and Fire A. DNA transformation. Methods Cell Biol. 48 (1995) 451-482
24. Miller D.M., Shen M.M., Shamu C.E., Burglin T.R., Ruvkun G., Dubois M.L., Ghee M., and Wilson L. C. elegans unc-4 gene encodes a homeodomain that determines the pattern of synaptic input to specific motor neurons. Nature 355 (1992) 841-845
25. Nonet M.L. Visualization of synaptic specializations in live C. elegans with synaptic vesicle protein-GFP fusions. J. Neurosci. Methods 89 (1999) 33-40
26. Patel M.R., Lerhman E.K., Poon V., Crump J.G., Zhen M., Bargmann C.I., and Shen K. Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat. Neurosci. 9 (2006) 1488-1499
27. Pedelacq J.D., Cabantous S., Tran T., Terwilliger T.C., and Waldo G.S. Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol. 24 (2006) 79-88
28. Peschanski M., and Ralston III H.J. Light and electron microscopic evidence of transneuronal labeling with WGA-HRP to trace somatosensory pathways to the thalamus. J. Comp. Neurol. 236 (1985) 29-41
29. Pflugrad A., Meir J.Y., Barnes T.M., and Miller III D.M. The Groucho-like transcription factor UNC-37 functions with the neural specificity gene unc-4 to govern motor neuron identity in C. elegans. Development 124 (1997) 1699-1709
30. Reid R.C., and Alonso J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378 (1995) 281-284
31. Richardson S.M., Wheelan S.J., Yarrington R.M., and Boeke J.D. GeneDesign: rapid, automated design of multikilobase synthetic genes. Genome Res. 16 (2006) 550-556
32. Rogers C., Reale V., Kim K., Chatwin H., Li C., Evans P., and de Bono M. Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat. Neurosci. 6 (2003) 1178-1185
33. Ryu S.E., Kwong P.D., Truneh A., Porter T.G., Arthos J., Rosenberg M., Dai X., Xuong N.H., Axel R., Sweet R.W., and Hendrickson W.A. Crystal structure of an HIV-binding recombinant fragment of human CD4. Nature 348 (1990) 419-426
34. Schwab M.E., and Thoenen H. Electron microscopic evidence for a transsynaptic migration of tetanus toxin in spinal cord motoneurons: an autoradiographic and morphometric study. Brain Res. 105 (1976) 213-227
35. Shen K. Molecular mechanisms of target specificity during synapse formation. Curr. Opin. Neurobiol. 14 (2004) 83-88
36. Shen K., and Bargmann C.I. The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans. Cell 112 (2003) 619-630
37. Shen K., Fetter R.D., and Bargmann C.I. Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell 116 (2004) 869-881
38. Spieth J., Brooke G., Kuersten S., Lea K., and Blumenthal T. Operons in C. elegans: polycistronic mRNA precursors are processed by trans-splicing of SL2 to downstream coding regions. Cell 73 (1993) 521-532
39. Vaney D.I., and Taylor W.R. Direction selectivity in the retina. Curr. Opin. Neurobiol. 12 (2002) 405-410
40. Varoqueaux F., Aramuni G., Rawson R.L., Mohrmann R., Missler M., Gottmann K., Zhang W., Sudhof T.C., and Brose N. Neuroligins determine synapse maturation and function. Neuron 51 (2006) 741-754
41. Vogel B.E., and Hedgecock E.M. Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions. Development 128 (2001) 883-894
42. Wassle H., and Boycott B.B. Functional architecture of the mammalian retina. Physiol. Rev. 71 (1991) 447-480
43. White J.G., Southgate E., Thomson J.N., and Brenner S. The structure of the ventral nerve cord of Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 275 (1976) 327-348
44. White J.G., Southgate E., Thomson J.N., and Brenner S. The structure of the nervous system of Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314 (1986) 1-340
45. White J.G., Southgate E., and Thomson J.N. Mutations in the Caenorhabditis elegans unc-4 gene alter the synaptic input to ventral cord motor neurons. Nature 355 (1992) 838-841
46. Wickersham I.R., Lyon D.C., Barnard R.J., Mori T., Finke S., Conzelmann K.K., Young J.A., and Callaway E.M. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53 (2007) 639-647
47. Yoshihara Y., Mizuno T., Nakahira M., Kawasaki M., Watanabe Y., Kagamiyama H., Jishage K., Ueda O., Suzuki H., Tabuchi K., et al. A genetic approach to visualization of multisynaptic neural pathways using plant lectin transgene. Neuron 22 (1999) 33-41
48. Zhang S., Ma C., and Chalfie M. Combinatorial marking of cells and organelles with reconstituted fluorescent proteins. Cell 119 (2004) 137-144