The active zone protein family ELKS supports Ca2+ influx at nerve terminals of inhibitory hippocampal neurons

Journal of Neuroscience

Volumn 34, Issue 37, 2014, Pages 12289-12303

  Liu, Changliang ^a   Bickford, Lydia S ^a   Held, Richard G ^a   Nyitrai, Hajnalka ^a   Südhof, Thomas C ^a,b   Kaeser, Pascal S ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Active zone; Calcium; ELKS; Knock out; Priming

Indexed keywords

BOMBESIN; CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; CHLOROQUINE; COMPOUND 48-80; FLUORESCEIN ISOTHIOCYANATE; GASTRIN RELEASING PEPTIDE; GASTRIN RELEASING PEPTIDE RECEPTOR; GLUTAMATE DECARBOXYLASE 67; GREEN FLUORESCENT PROTEIN; HISTAMINE; IODINE 125; MONOCLONAL ANTIBODY; NEUROKININ 1 RECEPTOR; NEUROMEDIN B; NEUROMEDIN B RECEPTOR; POLYCLONAL ANTIBODY; PROTEIN KINASE C GAMMA; RADIOLIGAND; RESINIFERATOXIN; SAPORIN; SEROTONIN; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; VESICULAR GLUTAMATE TRANSPORTER 2; CALCIUM; CARRIER PROTEIN; NERVE PROTEIN; RAB6IP2 PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL BEHAVIORAL TEST; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; KNOCKOUT MOUSE; MALE; MOUSE; MRNA EXPRESSION ASSAY; NERVE CELL INHIBITION; NEUROTRANSMISSION; NONHUMAN; PROTEIN EXPRESSION; PRURITUS; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR BINDING; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCRATCHING; SENSORY NERVE CELL; SPINAL CORD DORSAL HORN; THALAMUS MEDIALIS CENTRALIS NUCLEUS; TRIGEMINAL NUCLEUS; WESTERN BLOTTING; ACTION POTENTIAL; ANIMAL; CALCIUM SIGNALING; FEMALE; HIPPOCAMPUS; METABOLISM; NERVE CELL; PHYSIOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM SIGNALING; CARRIER PROTEINS; FEMALE; HIPPOCAMPUS; MALE; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURAL INHIBITION; NEURONS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84907013298     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0999-14.2014     Document Type: Article

References (67)

1. Ariel P, Ryan TA (2012) New insights into molecular players involved in neurotransmitter release. Physiology 27:15-24. CrossRef Medline
2. Augustin I, Rosenmund C, Südhof TC, Brose N (1999) Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400: 457-461. CrossRef Medline
3. Billings SE, Clarke GL, Nishimune H (2012) ELKS1 and Ca(2+) channel subunit beta4 interact and colocalize at cerebellar synapses. Neuroreport 23:49 -54. CrossRef Medline
4. 2+ channelopathy. Neuron 43:387- 400. CrossRef Medline
5. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J (2005) International Union of Pharmacology: XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev 57:411- 425. CrossRef Medline
6. Couteaux R, Pécot-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. Medline
7. Dai Y, Taru H, Deken SL, Grill B, Ackley B, Nonet ML, Jin Y (2006) SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS. Nat Neurosci 9:1479 -1487. CrossRef Medline
8. Davydova D, Marini C, King C, Klueva J, Bischof F, Romorini S, Montenegro- Venegas C, Heine M, Schneider R, Schröder MS, Altrock WD, Henneberger C, Rusakov DA, Gundelfinger ED, Fejtova A (2014) Bassoon specifically controls presynaptic P/Q-type Ca(2+) channels via RIMbinding protein. Neuron 82:181-194. CrossRef Medline
9. Deguchi-Tawarada M, Inoue E, Takao-Rikitsu E, Inoue M, Ohtsuka T, Takai Y (2004) CAST2: identification and characterization of a protein structurally related to the presynaptic cytomatrix protein CAST. Genes Cells 9:15-23. CrossRef Medline
10. Deken SL, Vincent R, Hadwiger G, Liu Q, Wang ZW, Nonet ML (2005) Redundant localization mechanisms of RIM and ELKS in Caenorhabditis elegans. J Neurosci 25:5975-5983. CrossRef Medline
11. Deng L, Kaeser PS, Xu W, Südhof TC (2011) RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of Munc13. Neuron 69:317-331. CrossRef Medline
12. Dodge FA Jr, Rahamimoff R (1967) On the relationship between calcium concentration and the amplitude of the end-plate potential. J Physiol 189:90P-92P. Medline
13. Dolphin AC (2003) Beta subunits of voltage-gated calcium channels. J Bioenerg Biomembr 35:599-620. CrossRef Medline
14. Ducut Sigala JL, Bottero V, Young DB, Shevchenko A, Mercurio F, Verma IM (2004) Activation of transcription factor NF-kappaB requires ELKS, an IkappaB kinase regulatory subunit. Science 304:1963-1967. CrossRef Medline
15. Dymecki SM (1996) Flp recombinase promotes site-specific DNA recombination in embryonic stem cells and transgenic mice. Proc Natl Acad Sci U S A 93:6191- 6196. CrossRef Medline
16. Fernández-Chacón R, Königstorfer A, Gerber SH, Garcia J, Matos MF, Stevens CF, Brose N, Rizo J, Rosenmund C, Südhof TC (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature 410: 41-49. CrossRef Medline
17. Fouquet W, Owald D, Wichmann C, Mertel S, Depner H, Dyba M, Hallermann S, Kittel RJ, Eimer S, Sigrist SJ (2009) Maturation of active zone assembly by Drosophila Bruchpilot. J Cell Biol 186:129 -145. Medline
18. Frank T, Rutherford MA, Strenzke N, Neef A, Pangršiè T, Khimich D, Fejtova A, Gundelfinger ED, Liberman MC, Harke B, Bryan KE, Lee A, Egner A, Riedel D, Moser T (2010) Bassoon and the synaptic ribbon organize Ca(2)+ channels and vesicles to add release sites and promote refilling. Neuron 68:724 -738. CrossRef Medline
19. Gracheva EO, Hadwiger G, Nonet ML, Richmond JE (2008) Direct interactions between C. elegans RAB-3 and Rim provide a mechanism to target vesicles to the presynaptic density. Neurosci Lett 444:137-142. CrossRef Medline
20. Grigoriev I, Splinter D, Keijzer N, Wulf PS, Demmers J, Ohtsuka T, Modesti M, Maly IV, Grosveld F, Hoogenraad CC, Akhmanova A (2007) Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell 13:305- 314. CrossRef Medline
21. Grigoriev I, Yu KL, Martinez-Sanchez E, Serra-Marques A, Smal I, Meijering E, Demmers J, Peränen J, Pasterkamp RJ, van der Sluijs P, Hoogenraad CC, Akhmanova A (2011) Rab6, Rab8, and MICAL3 cooperate in controlling docking and fusion of exocytotic carriers. Curr Biol 21:967-974. CrossRef Medline
22. Gundelfinger ED, Fejtova A (2012) Molecular organization and plasticity of the cytomatrix at the active zone. Curr Opin Neurobiol 22:423- 430. CrossRef Medline
23. Hallermann S, Heckmann M, Kittel RJ (2010a) Mechanisms of short-term plasticity at neuromuscular active zones of Drosophila. HFSP J 4:72- 84. CrossRef Medline
24. Hallermann S, Kittel RJ, Wichmann C, Weyhersmüller A, Fouquet W, Mertel S, Owald D, Eimer S, Depner H, Schwärzel M, Sigrist SJ, Heckmann M (2010b) Naked dense bodies provoke depression. J Neurosci 30:14340- 14345. CrossRef Medline
25. Han Y, Kaeser PS, Südhof TC, Schneggenburger R (2011) RIM determines Ca(2+) channel density and vesicle docking at the presynaptic active zone. Neuron 69:304 -316. CrossRef Medline
26. Harlow ML, Ress D, Stoschek A, Marshall RM, McMahan UJ (2001) The architecture of active zone material at the frog's neuromuscular junction. Nature 409:479-484. CrossRef Medline
27. Hibino H, Pironkova R, Onwumere O, Vologodskaia M, Hudspeth AJ, Lesage F (2002) RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca(2+) channels. Neuron 34:411- 423. CrossRef Medline
28. Ho A, Morishita W, Atasoy D, Liu X, Tabuchi K, Hammer RE, Malenka RC, Südhof TC (2006) Genetic analysis of Mint/X11 proteins: essential presynaptic functions of a neuronal adaptor protein family. J Neurosci 26: 13089-13101. CrossRef Medline
29. Hosaka M, Südhof TC (1999) Homo- and heterodimerization of synapsins. J Biol Chem 274:16747-16753. CrossRef Medline
30. Juranek J, Mukherjee K, Rickmann M, Martens H, Calka J, Südhof TC, Jahn R (2006) Differential expression of active zone proteins in neuromuscular junctions suggests functional diversification. Eur J Neurosci 24:3043- 3052. CrossRef Medline
31. Kaeser PS (2011) Pushing synaptic vesicles over the RIM. Cell Logist 1:106- 110. CrossRef Medline
32. Kaeser PS, Regehr WG (2014) Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. Annu Rev Physiol 76:333-363. CrossRef Medline
33. Kaeser PS, Kwon HB, Chiu CQ, Deng L, Castillo PE, Südhof TC (2008) RIM1alpha and RIM1beta are synthesized from distinct promoters of the RIM1 gene to mediate differential but overlapping synaptic functions. J Neurosci 28:13435-13447. CrossRef Medline
34. Kaeser PS, Deng L, Chávez AE, Liu X, Castillo PE, Südhof TC (2009) ELKS2alpha/CAST deletion selectively increases neurotransmitter release at inhibitory synapses. Neuron 64:227-239. CrossRef Medline
35. 2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144:282-295. CrossRef Medline
36. Kaeser PS, Deng L, Fan M, Südhof TC (2012) RIM genes differentially contribute to organizing presynaptic release sites. Proc Natl Acad Sci U S A 109:11830 -11835. CrossRef Medline
37. Kaufman DL, Houser CR, Tobin AJ (1991) Two forms of the gammaaminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J Neurochem 56:720 -723. CrossRef Medline
38. 2+ channel clustering, and vesicle release. Science 312:1051-1054. CrossRef Medline
39. 2+ channels. Nat Neurosci 10:691-701. CrossRef Medline
40. Kiyonaka S, Nakajima H, Takada Y, Hida Y, Yoshioka T, Hagiwara A, Kitajima I, Mori Y, Ohtsuka T (2012) Physical and functional interaction of the active zone protein CAST/ERC2 and the beta-subunit of the voltagedependent Ca(2+) channel. J Biochem 152:149 -159. CrossRef Medline
41. 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. CrossRef Medline
42. Lau CG, Murthy VN (2012) Activity-dependent regulation of inhibition via GAD67. J Neurosci 32:8521- 8531. CrossRef Medline
43. Lazarevic V, Schöne C, Heine M, Gundelfinger ED, Fejtova A (2011) Extensive remodeling of the presynaptic cytomatrix upon homeostatic adaptation to network activity silencing. J Neurosci 31:10189 -10200. CrossRef Medline
44. Liu KS, Siebert M, Mertel S, Knoche E, Wegener S, Wichmann C, Matkovic T, Muhammad K, Depner H, Mettke C, Bückers J, Hell SW,Müller M, Davis GW, Schmitz D, Sigrist SJ (2011) RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science 334: 1565-1569. CrossRef Medline
45. Matkovic T, Siebert M, Knoche E, Depner H, Mertel S, Owald D, Schmidt M, Thomas U, Sickmann A, Kamin D, Hell SW, Bürger J, Hollmann C, Mielke T, Wichmann C, Sigrist SJ (2013) The Bruchpilot cytomatrix determines the size of the readily releasable pool of synaptic vesicles. J Cell Biol 202:667- 683. CrossRef Medline
46. Maximov A, Pang ZP, Tervo DG, Südhof TC (2007) Monitoring synaptic transmission in primary neuronal cultures using local extracellular stimulation. J Neurosci Methods 161:75- 87. CrossRef Medline
47. Monier S, Jollivet F, Janoueix-Lerosey I, Johannes L, Goud B (2002) Characterization of novel Rab6-interacting proteins involved in endosome-to- TGN transport. Traffic 3:289 -297. CrossRef Medline
48. Mozhayeva MG, Sara Y, Liu X, Kavalali ET (2002) Development of vesicle pools during maturation of hippocampal synapses. J Neurosci 22:654- 665. Medline
49. Mukherjee K, Yang X, Gerber SH, Kwon HB, Ho A, Castillo PE, Liu X, Südhof TC (2010) Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proc Natl Acad Sci U S A 107:6504-6509. CrossRef Medline
50. Müller M, Liu KS, Sigrist SJ, Davis GW (2012) RIM controls homeostatic plasticity through modulation of the readily-releasable vesicle pool. J Neurosci 32:16574 -16585. CrossRef Medline
51. Nakata T, Kitamura Y, Shimizu K, Tanaka S, Fujimori M, Yokoyama S, Ito K, EmiM (1999) Fusion of a novel gene, ELKS, to RET due to translocation t(10;12)(q11;p13) in a papillary thyroid carcinoma. Genes Chromosomes Cancer 25:97-103. CrossRef Medline
52. Nishimune H, Numata T, Chen J, Aoki Y, Wang Y, Starr MP, Mori Y, Stanford JA (2012) Active zone protein Bassoon co-localizes with presynaptic calcium channel, modifies channel function, and recovers from aging related loss by exercise. PLoS One 7:e38029. CrossRef Medline
53. O'Gorman S, Dagenais NA, Qian M, Marchuk Y (1997) Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc Natl Acad Sci U S A 94:14602-14607. CrossRef Medline
54. Ohtsuka T, Takao-Rikitsu E, Inoue E, Inoue M, Takeuchi M, Matsubara K, Deguchi-Tawarada M, Satoh K, Morimoto K, Nakanishi H, Takai Y (2002) Cast: a novel protein of the cytomatrix at the active zone of synapses that forms a ternary complex with RIM1 and munc13-1. J Cell Biol 158:577-590. CrossRef Medline
55. Rosahl TW, Geppert M, Spillane D, Herz J, Hammer RE, Malenka RC, Südhof TC (1993) Short-term synaptic plasticity is altered in mice lacking synapsin I. Cell 75:661- 670. CrossRef Medline
56. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207. CrossRef Medline
57. Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, Rhee JS (2002) Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33:411- 424. CrossRef Medline
58. Schoch S, Castillo PE, Jo T, Mukherjee K, Geppert M, Wang Y, Schmitz F, Malenka RC, Südhof TC (2002) RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415:321- 326. CrossRef Medline
59. Schoch S, Mittelstaedt T, Kaeser PS, Padgett D, Feldmann N, Chevaleyre V, Castillo PE, Hammer RE, Han W, Schmitz F, Lin W, Südhof TC (2006) Redundant functions of RIM1alpha and RIM2alpha in Ca(2+)-triggered neurotransmitter release. EMBO J 25:5852-5863. CrossRef Medline
60. 2+. J Gen Physiol 122:265-276. CrossRef Medline
61. Südhof TC (2012) The presynaptic active zone. Neuron 75:11-25. CrossRef Medline
62. 2+-sensor model for neurotransmitter release in a central synapse. Nature 450:676-682. CrossRef Medline
63. tom Dieck S, Specht D, Strenzke N, Hida Y, Krishnamoorthy V, Schmidt KF, Inoue E, Ishizaki H, Tanaka-Okamoto M, Miyoshi J, Hagiwara A, Brandstätter JH, Löwel S, Gollisch T, Ohtsuka T, Moser T (2012) Deletion of the presynaptic scaffold CAST reduces active zone size in rod photoreceptors and impairs visual processing. J Neurosci 32:12192-12203. CrossRef Medline
64. Verhage M, Maia AS, Plomp JJ, Brussaard AB, Heeroma JH, Vermeer H, Toonen RF, Hammer RE, van den Berg TK, Missler M, Geuze HJ, Südhof TC (2000) Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287:864-869. CrossRef Medline
65. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Dürrbeck H, Buchner S, Dabauvalle MC, Schmidt M, Qin G, Wichmann C, Kittel R, Sigrist SJ, Buchner E (2006) Bruchpilot, a protein with homology to ELKS/ CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49:833- 844. CrossRef Medline
66. Wang Y, Liu X, Biederer T, Südhof TC (2002) A family of RIM-binding proteins regulated by alternative splicing: implications for the genesis of synaptic active zones. Proc Natl Acad Sci U S A 99:14464 -14469. CrossRef Medline
67. Weimer RM, Gracheva EO, Meyrignac O, Miller KG, Richmond JE, Bessereau JL (2006) UNC-13 and UNC-10/rim localize synaptic vesicles to specific membrane domains. J Neurosci 26:8040-8047. CrossRef Medline