In vivo imaging of intersynaptic vesicle exchange using VGLUT1 Venus knock-in mice

Journal of Neuroscience

Volumn 31, Issue 43, 2011, Pages 15544-15559

  Herzog, Etienne ^a,b,c,d   Nadrigny, Fabien ^a,e,f   Silm, Katlin ^b,c,d   Biesemann, Christoph ^a   Helling, Imke ^g   Bersot, Tiphaine ^b,c,d   Steffens, Heinz ^a,i,j   Schwartzmann, Richard ^d   Valentin Nagerl U ^e,f,g   El Mestikawy, Salah ^b,c,d   Rhee, JeongSeop ^a   Kirchhoff, Frank ^a,h   Brose, Nils ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b INSERM   (France)

^c CNRS   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e UNIVERSITÉ DE BORDEAUX   (France)

^f University of Bordeaux   (France)

^g MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^h SAARLAND UNIVERSITY   (Germany)

ⁱ UNIVERSITY OF GÖTTINGEN   (Germany)

^j MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; CONTROLLED STUDY; HIPPOCAMPUS; IMAGE PROCESSING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUTATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; BACTERIAL PROTEINS; CEREBRAL CORTEX; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GLUTAMIC ACID; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; NEURONS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; PROTEIN TRANSPORT; RNA, MESSENGER; SUBCELLULAR FRACTIONS; SYNAPSES; SYNAPTIC VESICLES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 80054960982     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2073-11.2011     Document Type: Article

References (51)

1. Augustin I, Rosenmund C, Südhof TC, Brose N (1999) Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400:457-461.
2. Balaji J, Ryan TA (2007) Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode. Proc Natl Acad Sci U S A 104:20576-20581.
3. Balschun D, Moechars D, Callaerts-Vegh Z, Vermaercke B, Van Acker N, Andries L, D'Hooge R (2010) Vesicular glutamate transporter VGLUT1 has a role in hippocampal long-term potentiation and spatial reversal learning. Cereb Cortex 20:684-693.
4. Bellocchio EE, Hu H, Pohorille A, Chan J, Pickel VM, Edwards RH (1998) The localization of the brain-specific inorganic phosphate transporter suggests a specific presynaptic role in glutamatergic transmission. J Neurosci 18:8648-8659.
5. Boulland J-L, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau RT Jr, Edwards RH, Storm-Mathisen J, Chaudhry FA (2004) Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J Comp Neurol 480:264-280.
6. Brose N, Huntley GW, Stern-Bach Y, Sharma G, Morrison JH, Heinemann SF (1994) Differential assembly of coexpressed glutamate receptor subunits in neurons of rat cerebral cortex. J Biol Chem 269:16780-16784.
7. Chen X, Barg S, Almers W (2008) Release of the styryl dyes from single synaptic vesicles in hippocampal neurons. J Neurosci 28:1894-1903.
8. Darcy KJ, Staras K, Collinson LM, Goda Y (2006) Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci 9:315-321.
9. De Gois S, Schäfer MK-H, Defamie N, Chen C, Ricci A, Weihe E, Varoqui H, Erickson JD (2005) Homeostatic scaling of vesicular glutamate and GABA transporter expression in rat neocortical circuits. J Neurosci 25:7121-7133.
10. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
11. Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260.
12. Fremeau RT Jr, Voglmaier S, Seal RP, Edwards RH (2004a) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27:98-103.
13. Fremeau RT Jr, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm- Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH (2004b) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304:1815-1819.
14. Gähwiler BH (1981) Organotypic monolayer cultures of nervous tissue. J Neurosci Methods 4:329-342.
15. Galli T, Haucke V (2001) Cycling of synaptic vesicles: how far? How fast! Sci STKE 2001:re1.
16. Giepmans BN, Adams SR, Ellisman MH, Tsien RY (2006) The fluorescent toolbox for assessing protein location and function. Science 312:217-224.
17. Harata N, Ryan TA, Smith SJ, Buchanan J, Tsien RW (2001) Visualizing recycling synaptic vesicles in hippocampal neurons by FM 1-43 photoconversion. Proc Natl Acad Sci U S A 98:12748-12753.
18. Herzog E, Bellenchi GC, Gras C, Bernard V, Ravassard P, Bedet C, Gasnier B, Giros B, El Mestikawy S (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21:RC181.
19. Herzog E, Takamori S, Jahn R, Brose N, Wojcik SM (2006) Synaptic and vesicular co-localization of the glutamate transporters VGLUT1 and VGLUT2 in the mouse hippocampus. J Neurochem 99:1011-1018.
20. Hisano S, Sawada K, Kawano M, Kanemoto M, Xiong G, Mogi K, Sakata- Haga H, Takeda J, Fukui Y, Nogami H (2002) Expression of inorganic phosphate/vesicular glutamate transporters (BNPI/VGLUT1 and DNPI/VGLUT2) in the cerebellum and precerebellar nuclei of the rat. Brain Res Mol Brain Res 107:23-31.
21. Hoopmann P, Punge A, Barysch SV, Westphal V, Bückers J, Opazo F, Bethani I, Lauterbach MA, Hell SW, Rizzoli SO (2010) Endosomal sorting of readily releasable synaptic vesicles. Proc Natl Acad Sci U S A 107:19055-19060.
22. Huttner WB, Schiebler W, Greengard P, De Camilli P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96:1374-1388.
23. Jin Y, Garner CC (2008) Molecular mechanisms of presynaptic differentiation. Annu Rev Cell Dev Biol 24:237-262.
24. Jones DH, Matus AI (1974) Isolation of synaptic plasma membrane from brain by combined flotation-sedimentation density gradient centrifugation. Biochim Biophys Acta 356:276-287.
25. Kalla S, Stern M, Basu J, Varoqueaux F, Reim K, Rosenmund C, Ziv NE, Brose N (2006) Molecular dynamics of a presynaptic active zone protein studied in Munc13-1-enhanced yellow fluorescent protein knock-in mutant mice. J Neurosci 26:13054-13066.
26. Kaneko T, Fujiyama F, Hioki H (2002) Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J Comp Neurol 444:39-62.
27. Khvotchev M, Kavalali ET (2008) Pharmacology of neurotransmitter release: measuring exocytosis. Handb Exp Pharmacol 23-43.
28. Kim SH, Ryan TA (2010) CDK5 serves as a major control point in neurotransmitter release. Neuron 67:797-809.
29. Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci U S A 93:5860-5865.
30. McAnaney TB, Zeng W, Doe CFE, Bhanji N, Wakelin S, Pearson DS, Abbyad P, Shi X, Boxer SG, Bagshaw CR (2005) Protonation, photobleaching, and photoactivation of yellow fluorescent protein (YFP 10C): a unifying mechanism. Biochemistry 44:5510-5524.
31. Mimura Y, Mogi K, Kawano M, Fukui Y, Takeda J, Nogami H, Hisano S (2002) Differential expression of two distinct vesicular glutamate transporters in the rat retina. Neuroreport 13:1925-1928.
32. Moechars D, Weston MC, Leo S, Callaerts-Vegh Z, Goris I, Daneels G, Buist A, Cik M, van der Spek P, Kass S, Meert T, D'Hooge R, Rosenmund C, Hampson RM (2006) Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. J Neurosci 26:12055-12066.
33. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87-90.
34. Pologruto TA, Sabatini BL, Svoboda K (2003) ScanImage: flexible software for operating laser scanning microscopes. Biomed Eng Online 2:13.
35. Pyott SJ, Rosenmund C (2002) The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J Physiol 539:523-535.
36. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Südhof TC, Takahashi M, Rosenmund C, Brose N (2002) Beta phorbol ester-and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108:121-133.
37. Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6:57-69.
38. Rizzoli SO, Richards DA, Betz WJ (2003) Monitoring synaptic vesicle recycling in frog motor nerve terminals with FM dyes. J Neurocytol 32:539-549.
39. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207.
40. Sakata-Haga H, Kanemoto M, Maruyama D, Hoshi K, Mogi K, Narita M, Okado N, Ikeda Y, Nogami H, Fukui Y, Kojima I, Takeda J, Hisano S (2001) Differential localization and colocalization of two neuron-types of sodium-dependent inorganic phosphate cotransporters in rat forebrain. Brain Res 902:143-155.
41. Staras K, Branco T, Burden JJ, Pozo K, Darcy K, Marra V, Ratnayaka A, Goda Y (2010) A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron 66:37-44.
42. Takamori S, Rhee JS, Rosenmund C, Jahn R (2000) Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-194.
43. Thomas KR, Capecchi MR (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51:503-512.
44. Tsuriel S, Geva R, Zamorano P, Dresbach T, Boeckers T, Gundelfinger ED, Garner CC, Ziv NE (2006) Local sharing as a predominant determinant of synaptic matrix molecular dynamics. PLoS Biol 4:e271.
45. Varoqui H, Schäfer MKH, Zhu H, Weihe E, Erickson JD (2002) Identification of the differentiation-associated Na+/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22:142-155.
46. Vinatier J, Herzog E, Plamont M-A, Wojcik SM, Schmidt A, Brose N, Daviet L, El Mestikawy S, Giros B (2006) Interaction between the vesicular glutamate transporter type 1 and endophilin A1, a protein essential for endocytosis. J Neurochem 97:1111-1125.
47. Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, Edwards RH (2006) Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51:71-84.
48. Weston MC, Nehring RB, Wojcik SM, Rosenmund C (2011) Interplay between VGLUT isoforms and endophilin A1 regulates neurotransmitter release and short-term plasticity. Neuron 69:1147-1159.
49. Wilson NR, Kang J, Hueske EV, Leung T, Varoqui H, Murnick JG, Erickson JD, Liu G (2005) Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. J Neurosci 25:6221-6234.
50. Wojcik SM, Brose N (2007) Regulation of membrane fusion in synaptic excitation-secretion coupling: speed and accuracy matter. Neuron 55:11-24.
51. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, Takamori S, Brose N, Rosenmund C (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci U S A 101:7158-7163.