A complete genetic analysis of neuronal Rab3 function

Journal of Neuroscience

Volumn 24, Issue 29, 2004, Pages 6629-6637

  Schlüter, Oliver M ^a,b,c,f   Schmitz, Frank ^d   Jahn, Reinhard ^c   Rosenmund, Christian ^c,g   Südhof, Thomas C ^a,e  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d SAARLAND UNIVERSITY   (Germany)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f STANFORD UNIVERSITY   (United States)

^g BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

GTP binding proteins; Membrane fusion; Neurotransmitter release; RIM; Synaptic transmission; Synaptic vesicles

Indexed keywords

COMPLEMENTARY DNA; GUANINE NUCLEOTIDE BINDING PROTEIN; RAB PROTEIN;

ANIMAL CELL; ARTICLE; EMBRYO; KNOCKOUT MOUSE; MEMBRANE FUSION; MOLECULAR CLONING; MOUSE; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN CHEMISTRY; CELLS, CULTURED; EXCITATORY POSTSYNAPTIC POTENTIALS; GENES, LETHAL; MICE; MICE, KNOCKOUT; NEURONS; NEUROTRANSMITTER AGENTS; PATCH-CLAMP TECHNIQUES; PROTEIN ISOFORMS; RAB3 GTP-BINDING PROTEINS; RESPIRATORY INSUFFICIENCY; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 2942737775     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1610-04.2004     Document Type: Article

References (41)

1. Al-Zoubi AM, Efimova EV, Kaithamana S, Martinez O, El-Idrissi Mel-A, Dogan RE, Prabhakar BS (2001) Contrasting effects of IG20 and its splice isoforms, MADD and DENN-SV, on tumor necrosis factor alpha-induced apoptosis and activation of caspase-8 and -3. J Biol Chem 276:47202-47211.
2. Baldini T, Hohl H, Lin Y, Lodish HF (1992) Cloning of a Rab3 isotype predominantly expressed in adipocytes. Proc Natl Acad Sci USA 89:5049-5052.
3. Bekkers JM, Stevens CF (1991) Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci USA 88:7834-7836.
4. Calakos N, Schoch S, Südhof TC, Malenka RC (2004) Multiple roles for the active zone protein RIM1α in late stages of neurotransmitter release. Neuron 42:889-896.
5. Castillo PE, Janz R, Südhof TC, Tzounopoulos T, Malenka RC, Nicoll RA (1997) The synaptic vesicle protein Rab3 is essential for mossy fiber long term potentiation in the hippocampus. Nature 388:590-593.
6. Chow VT, Lee SS (1996) DENN, a novel human gene differentially expressed in normal and neoplastic cells. DNA Seq 6:263-273.
7. Chung SH, Joberty G, Gelino EA, Macara IG, Holz RW (1999) Comparison of the effects on secretion in chromaffin and PC12 cells of Rab3 family members and mutants. Evidence that inhibitory effects are independent of direct interaction with Rabphilin. J Biol Chem 274:18113-18120.
8. Daly C, Ziff EB (1997) Post-transcriptional regulation of synaptic vesicle protein expression and the developmental control of synaptic vesicle formation. J Neurosci 17:2365-2375.
9. Darchen F, Goud B (2000) Multiple aspects of Rab protein action in the secretory pathway: focus on Rab3 and Rab6. Biochimie 82:375-384.
10. Deneka M, Neeft M, van der Sluijs P (2003) Regulation of membrane transport by rab GTPases. Crit Rev Biochem Mol Biol 38:121-142.
11. Fernandez-Chacon R, Südhof TC (2000) Novel SCAMPs lacking NPF repeats: ubiquitous and synaptic vesicle-specific forms implicate SCAMPs in multiple membrane-trafficking functions. J Neurosci 20:7941-7950.
12. 2+-regulator of release probability. Nature 410:41-49.
13. Fischer von Mollard G, Südhof TC, Jahn RA (1991) A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature 349:79-81.
14. Fischer von Mollard G, Stahl B, Khoklatchev A, Südhof TC, Jahn R (1994) Rab3C is a synaptic vesicle protein that dissociates from synaptic vesicles after stimulation of exocytosis. J Biol Chem 269:10971-10974.
15. Francis SC, Sunshine C, Kirk KL (2002) Coordinate regulation of catecholamine uptake by rab3 and phosphoinositide 3-kinase. J Biol Chem 277:7816-7823.
16. Geppert M, Bolshakov VY, Siegelbaum SA, Takei K, De Camilli P, Hammer RE, Südhof TC (1994) The role of Rab3A in neurotransmitter release. Nature 369:493-497.
17. Geppert M, Goda Y, Stevens CF, Südhof TC (1997) Rab3A regulates a late step in synaptic vesicle fusion. Nature 387:810-814.
18. Hammer III JA, Wu XS (2002) Rabs grab motors: defining the connections between Rab GTPases and motor proteins. Curr Opin Cell Biol 14:69-75.
19. Hessler NA, Shirke AM, Malinow R (1993) The probability of transmitter release at a mammalian central synapse. Nature 366:569-572.
20. 2+/phospholipid-binding protein, depends on rab3A/3C. Neuron 13:885-898.
21. Matsui Y, Kikuchi A, Kondo J, Hishida T, Teranishi Y, Takai Y (1988) Nucleotide and deduced amino acid sequences of a GTP-binding protein family with molecular weights of 25,000 from bovine brain. J Biol Chem 263:11071-11074.
22. Michaut M, Tomes CN, De Blas G, Yunes R, Mayorga LS (2000) Calcium-triggered acrosomal exocytosis in human spermatozoa requires the coordinated activation of Rab3A and N-ethylmaleimide-sensitive factor. Proc Natl Acad Sci USA 97:9996-10001.
23. Pyott SJ, Rosenmund C (2002) The effects of temperature on vesicular supply and release in autaptic cultures of hippocampal neurons. J Physiol (Lond) 539:523-535.
24. Riedel D, Antonin W, Fernandez-Chacon R, Alvarez de Toledo G, Jo T, Geppert M, Valentijn JA, Valentijn K, Jamieson JD, Südhof TC, Jahn R (2002) Rab3D is not essential for exocrine exocytosis. Mol Cell Biol 22:6487-6497.
25. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Südhof TC (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375:488-493.
26. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207.
27. Rosenmund C, Clements JD, Westbrook GL (1993) Nonuniform probability of glutamate release at a hippocampal synapse. Science 262:754-757.
28. Sambrook J, Russell DW (2001) Molecular cloning, a laboratory manual, Ed 3. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
29. Schlüter OM, Schnell E, Verhage M, Tzounopoulos T, Nicoll RA, Janz R, Malenka RC, Geppert M, Südhof TC (1999) Rabphilin knock-out mice reveal that rabphilin is not required for rab3 function in regulating neurotransmitter release. J Neurosci 19:5834-5846.
30. Schlüter OM, Khvotchev M, Jahn R, Südhof TC (2002) Localization versus function of Rab3 proteins: evidence for a common regulatory role in controlling fusion. J Biol Chem 277:40919-40929.
31. Schlüter OM, Fornai F, Alessandri MG, Takamori S, Geppert M, Jahn R, Südhof TC (2003) Role of α-synuclein in MPTP-induced Parkinsonism in mice. Neuroscience 118:985-1002.
32. Schoch S, Castillo PE, Jo T, Mukherjee K, Geppert M, Wang Y, Schmitz F, Malenka RC, Südhof TC (2002) RIM1α forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415:321-326.
33. Seabra MC, Mules EH, Hume AN (2002) Rab GTPases, intracellular traffic and disease. Trends Mol Med 8:23-30.
34. Südhof TC (1990) The structure of the human synapsin I gene and protein. J Biol Chem 265:7849-7852.
35. Touchot N, Chardin P, Tavitian A (1987) Four additional members of the ras gene superfamily isolated by an oligonucleotide strategy: molecular cloning of YPT-related cDNAs from a rat brain library. Proc Natl Acad Sci USA 84:8210-8214.
36. Tuvim MJ, Adachi R, Hoffenberg S, Dickey BF (2001) Traffic control: Rab GTPases and the regulation of interorganellar transport. News Physiol Sci 16:56-61.
37. van IJzendoorn SC, Tuvim MJ, Weimbs T, Dickey BF, Mostov KE (2002) Direct interaction between Rab3b and the polymeric immunoglobulin receptor controls ligand-stimulated transcytosis in epithelial cells. Dev Cell 2:219-228.
38. Wang Y, Okamoto M, Schmitz F, Hofmann K, Südhof TC 1997) Rim is a putative Rab3 effector in regulating synaptic vesicle fusion. Nature 338:593-598.
39. Yamaguchi K, Tanaka M, Mizoguchi A, Hirata Y, Ishizaki H, Kaneko K, Miyoshi J, Takai Y (2002) A GDP/GTP exchange protein for the Rab3 small G protein family up-regulates a postdocking step of synaptic exocytosis in central synapses. Proc Natl Acad Sci USA 99:14536-14541.
40. Zahraoui A, Touchot N, Chardin P, Tavitian A (1989) The human Rab genes encode a family of GTP-binding proteins related to yeast YPT1 and SEC4 products involved in secretion. J Biol Chem 264:12394-12401.
41. Zhang Y, Zhou L, Miller CA (1998) A splicing variant of a death domain protein that is regulated by a mitogen-activated kinase is a substrate for c-Jun N-terminal kinase in the human central nervous system. Proc Natl Acad Sci USA 95:2586-2591.