UNC-13 and UNC-10/Rim localize synaptic vesicles to specific membrane domains

Journal of Neuroscience

Volumn 26, Issue 31, 2006, Pages 8040-8047

  Weimer, Robby M ^a,d   Gracheva, Elena O ^b   Meyrignac, Olivier ^a   Miller, Kenneth G ^c   Richmond, Janet E ^b   Bessereau, Jean Louis ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^d Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

C. elegans; Electron microscopy; Exocytosis; High pressure freezing; Neuromuscular junction; Postembedding immunogold labeling

Indexed keywords

PRESYNAPTIC RECEPTOR; PROTEIN RIM; PROTEIN UNC 10; PROTEIN UNC 13; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CARRIER PROTEIN; NERVE PROTEIN; UNC 10 PROTEIN, C ELEGANS; UNC-10 PROTEIN, C ELEGANS; UNC13B PROTEIN, HUMAN;

ARTICLE; CAENORHABDITIS ELEGANS; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; EXOCYTOSIS; FREEZING; IMMUNOGOLD STAINING; MORPHOLOGY; MORPHOMETRICS; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN TARGETING; SYNAPSE VESICLE; ANIMAL; CELL CULTURE; METABOLISM; ULTRASTRUCTURE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; CELLS, CULTURED; MEMBRANE MICRODOMAINS; NERVE TISSUE PROTEINS; SYNAPTIC VESICLES;

EID: 33748129499     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2350-06.2006     Document Type: Article

References (58)

1. Andrews-Zwilling YS, Kawabe H, Reim K, Varoqueaux F, Brose N (2006) Binding to RAB3a-interacting-molecule rim regulates the presynaptic recruitment of MUNC13-1 and ubMUNC13-2. J Biol Chem, in press.
2. Aravamudan B, Fergestad T, Davis WS, Rodesch CK, Broadie K (1999) Drosophila UNC-13 is essential for synaptic transmission. Nat Neurosci 2:965-971.
3. Augustin I, Rosenmund C, Sudhof TC, Brose N (1999) Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400:457-461.
4. Bamber BA, Beg AA, Twyman RE, Jorgensen EM (1999) The Caenorhabditis elegans unc-49 locus encodes multiple subunits of a heteromultimeric GABA receptor. J Neurosci 19:5348-5359.
5. Basu J, Shen N, Dulubova I, Lu J, Guan R, Guryev O, Grishin NV, Rosenmund C, Rizo J (2005) A minimal domain responsible for Munc13 activity. Nat Struct Mol Biol 12:1017-1018.
6. Betz A, Thakur P, Junge HJ, Ashery U, Rhee JS, Scheuss V, Rosenmund C, Rettig J, Brose N (2001) Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30:183-196.
7. Bloom O, Evergren E, Tomilin N, Kjaerulff O, Low P, Brodin L, Pieribone VA, Greengard P, Shupliakov O (2003) Colocalization of synapsin and actin during synaptic vesicle recycling. J Cell Biol 161:737-747.
8. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.
9. Broadie K, Prokop A, Bellen HJ, O'Kane CJ, Schulze KL, Sweeney ST (1995) Syntaxin and synaptobrevin function downstream of vesicle docking in Drosophila. Neuron 15:663-673.
10. Brose N, Rosenmund C, Rettig J (2000) Regulation of transmitter release by Unc-13 and its homologues. Curr Opin Neurobiol 10:303-311.
11. Cathala L, Holderith NB, Nusser Z, DiGregorio DA, Cull-Candy SG (2005) Changes in synaptic structure underlie the developmental speeding of AMPA receptor-mediated EPSCs. Nat Neurosci 8:1310-1318.
12. Charlie NK, Thomure AM, Schade MA, Miller KG (2006) The Dunce cAMP phosphodiesterase PDE-4 negatively regulates G{alpha}s-dependent and G{alpha}s-independent cAMP pools in the Caenorhabditis elegans synaptic signaling network. Genetics 173:111-130.
13. Clark SG, Shurland DL, Meyerowitz EM, Bargmann CI, van der Bliek AM (1997) A dynamin GTPase mutation causes a rapid and reversible temperature- inducible locomotion defect in C. elegans. Proc Natl Acad Sci USA 94:10438-10443.
14. Couteaux R, Pecot-Dechavassine M (1970) Synaptic vesicles and pouches at the level of "active zones" of the neuromuscular junction. C R Acad Sci Hebd Seances Acad Sci D 271:2346-2349.
15. Deak F, Schoch S, Liu X, Sudhof TC, Kavalali ET (2004) Synaptobrevin is essential for fast synaptic-vesicle endocytosis. Nat Cell Biol 6:1102-1108.
16. Dulubova I, Sugita S, Hill S, Hosaka M, Fernandez I, Sudhof TC, Rizo J (1999) A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J 18:4372-4382.
17. Dulubova I, Lou X, Lu J, Huryeva I, Alam A, Schneggenburger R, Sudhof TC, Rizo J (2005) A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity? EMBO J 24:2839-2850.
18. Evergren E, Zotova E, Brodin L, Shupliakov O (2006) Differential efficiency of the endocytotic machinery in tonic and phasic synapses. Neuroscience 141:123-131.
19. Fasshauer D (2003) Structural insights into the SNARE mechanism. Biochim Biophys Acta 1641:87-97.
20. Foletti DL, Lin R, Finley MA, Scheller RH (2000) Phosphorylated syntaxin 1 is localized to discrete domains along a subset of axons. J Neurosci 20:4535-4544.
21. Gally C, Bessereau JL (2003) GABA is dispensable for the formation of junctional GABA receptor clusters in Caenorhabditis elegans. J Neurosci 23:2591-2599.
22. Gilkey JC, Staehelin LA (1986) Advances in ultrarapid freezing for the preservation of cellular ultrastructure. J Electron Micros Tech 3:177-210.
23. Hanson PI, Roth R, Morisaki H, Jahn R, Heuser JE (1997) Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 90:523-535.
24. Harris TW, Hartwieg E, Horvitz HR, Jorgensen EM (2000) Mutations in synaptojanin disrupt synaptic vesicle recycling. J Cell Biol 150:589-600.
25. Heuser JE, Reese TS, Dennis MJ, Jan Y, Jan L, Evans L (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol 81:275-300.
26. Hunt JM, Bommert K, Charlton MP, Kistner A, Habermann E, Augustine GJ, Betz H (1994) A post-docking role for synaptobrevin in synaptic vesicle fusion. Neuron 12:1269-1279.
27. Kiss JZ, Giddings TH Jr, Staehelin LA, Sack FD (1990) Comparison of the ultrastructure of conventionally fixed and high pressure frozen/freeze substituted root tips of Nicotiana and Arabidopsis. Protoplasma 157:64-74.
28. Ko J, Na M, Kim S, Lee JR, Kim E (2003) Interaction of the ERC family of RIM-binding proteins with the liprin-alpha family of multidomain proteins. J Biol Chem 278:42377-42385.
29. Koenig JH, Kosaka T, Ikeda K (1989) The relationship between the number of synaptic vesicles and the amount of transmitter released. J Neurosci 9:1937-1942.
30. Kohn RE, Duerr JS, McManus JR, Duke A, Rakow TL, Maruyama H, Moulder G, Maruyama IN, Barstead RJ, Rand JB (2000) Expression of multiple UNC-13 proteins in the C. elegans nervous system. Mol Biol Cell 11:3441-3452.
31. Koushika SP, Richmond JE, Hadwiger G, Weimer RM, Jorgensen EM, Nonet ML (2001) A post-docking role for active zone protein Rim. Nat Neurosci 4:997-1005.
32. Labrousse AM, Shurland DL, van der Bliek AM (1998) Contribution of the GTPase domain to the subcellular localization of dynamin in the nematode Caenorhabditis elegans. Mol Biol Cell 9:3227-3239.
33. Lonart G, Sudhof TC (2000) Assembly of SNARE core complexes prior to neurotransmitter release sets the readily releasable pool of synaptic vesicles. J Biol Chem 275:27703-27707.
34. Madison JM, Nurrish S, Kaplan JM (2005) UNC-13 interaction with syntaxin is required for synaptic transmission. Curr Biol 15:2236-2242.
35. Maruyama IN, Brenner S (1991) A phorbol ester/diacylglycerol-binding protein encoded by the unc-13 gene of Caenorhabditis elegans. Proc Natl Acad Sci USA 88:5729-5733.
36. McMenamin S, Reinsch S, Conway G (2003) Direct comparison of common fixation methods for preservation of microtubules in zebrafish embryos. Biotechniques 34:468-470:472.
37. Morgan JR, Augustine GJ, Lafer EM (2002) Synaptic vesicle endocytosis: the races, places, and molecular faces. Neuromol Med 2:101-114.
38. Nonet ML, Staunton JE, Kilgard MP, Fergestad T, Hartwieg E, Horvitz HR, Jorgensen EM, Meyer BJ (1997) Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J Neurosci 17:8061-8073.
39. Richmond JE, Davis WS, Jorgensen EM (1999) UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat Neurosci 2:959-964.
40. Richmond JE, Weimer RM, Jorgensen EM (2001) An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming. Nature 412:338-341.
41. Rizzoli SO, Betz WJ (2004) The structural organization of the readily releasable pool of synaptic vesicles. Science 303:2037-2039.
42. Rostaing P, Weimer RM, Jorgensen EM, Triller A, Bessereau JL (2004) Preservation of immunoreactivity and fine structure of adult C. elegans tissues using high-pressure freezing. J Histochem Cytochem 52:1-12.
43. Schluter OM, Schmitz F, Jahn R, Rosenmund C, Sudhof TC (2004) A complete genetic analysis of neuronal Rab3 function. J Neurosci 24:6629-6637.
44. Schluter OM, Basu J, Sudhof TC, Rosenmund C (2006) Rab3 superprimes synaptic vesicles for release: implications for short-term synaptic plasticity. J Neurosci 26:1239-1246.
45. Schoch S, Castillo PE, Jo T, Mukherjee K, Geppert M, Wang Y, Schmitz F, Malenka RC, Sudhof TC (2002) RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415:321-326.
46. Shupliakov O, Low P, Grabs D, Gad H, Chen H, David C, Takei K, De Camilli P, Brodin L (1997) Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276:259-263.
47. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318-324.
48. Stevens DR, Wu ZX, Matti U, Junge HJ, Schirra C, Becherer U, Wojcik SM, Brose N, Rettig J (2005) Identification of the minimal protein domain required for priming activity of Munc13-1. Curr Biol 15:2243-2248.
49. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509-547.
50. Sutton RB, Fasshauer D, Jahn R, Brunger AT (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395:347-353.
51. van der Bliek AM, Meyerowitz EM (1991) Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351:411-414.
52. Varoqueaux F, Sigler A, Rhee JS, Brose N, Enk C, Reim K, Rosenmund C (2002) Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc Natl Acad Sci USA 99:9037-9042.
53. Wang Y, Okamoto M, Schmitz F, Hofmann K, Sudhof TC (1997) Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388:593-598.
54. Weimer RM (2006) Preservation of C. elegans tissue via high-pressure freezing and freeze-substitution for ultrastructural analysis and immunocytochemistry. In: C. elegans: methods and applications (Strange K, ed). Totowa, NJ: Humana, in press.
55. Weimer RM, Richmond JE, Davis WS, Hadwiger G, Nonet ML, Jorgensen EM (2003) Defects in synaptic vesicle docking in unc-18 mutants. Nat Neurosci 6:1023-1030.
56. Yeh E, Kawano T, Weimer RM, Bessereau JL, Zhen M (2005) Identification of genes involved in synaptogenesis using a fluorescent active zone marker in Caenorhabditis elegans. J Neurosci 25:3833-3841.
57. Zhai RG, Bellen HJ (2004) The architecture of the active zone in the presynaptic nerve terminal. Physiology (Bethesda) 19:262-270.
58. Zhen M, Jin Y (1999) The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401:371-375.