Tomosyn-2 is required for normal motor performance in mice and sustains neurotransmission at motor endplates

Brain Structure and Function

Volumn 220, Issue 4, 2015, Pages 1971-1982

  Geerts, Cornelia J ^a   Plomp, Jaap J ^b   Koopmans, Bastijn ^c   Loos, Maarten ^c   van der Pijl, Elizabeth M ^b   van der Valk, Martin A ^d   Verhage, Matthijs ^a,e   Groffen, Alexander J A ^a,e  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Sylics (Synaptologics BV)   (Netherlands)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

^e VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Neuromuscular junction; Release willingness; Short term plasticity; STXBP5L; Synaptic transmission; Tomosyn 2

Indexed keywords

ACETYLCHOLINE; CHOLINERGIC RECEPTOR; SNARE PROTEIN; SYNAPSIN; TOMOSYN 2; UNCLASSIFIED DRUG; STXBP5L PROTEIN, MOUSE; SYNAPTOBREVIN;

ACETYLCHOLINE RELEASE; ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DIAPHRAGM MUSCLE; EMBRYO; EMBRYONIC STEM CELL; ENDPLATE POTENTIAL; FEMALE; GENOTYPE; GRANULE CELL; GRIP STRENGTH; HEMIDIAPHRAGM; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; LEARNING; LOXP SITE; MALE; MINIATURE ENDPLATE POTENTIAL; MOTONEURON; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NERVE FIBER GROWTH; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSORY GATING; STARTLE REFLEX; SYNAPTIC TRANSMISSION; ANIMAL; ANIMAL EMBRYO; BIOPHYSICS; C57BL MOUSE; CYTOLOGY; DEFICIENCY; DIAPHRAGM; ELECTROSTIMULATION; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOTOR ACTIVITY; NERVE ENDING; NONPARAMETRIC TEST; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; SYNAPTIC POTENTIAL;

MAMMALIA; MUS;

ANIMALS; BIOPHYSICS; DIAPHRAGM; ELECTRIC STIMULATION; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; MOTOR ENDPLATE; NEUROMUSCULAR JUNCTION; PATCH-CLAMP TECHNIQUES; PSYCHOMOTOR PERFORMANCE; R-SNARE PROTEINS; RECEPTORS, CHOLINERGIC; STATISTICS, NONPARAMETRIC; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION;

EID: 84933177884     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0766-0     Document Type: Article

References (37)

1. Baba T, Sakisaka T, Mochida S, Takai Y (2005) PKA-catalyzed phosphorylation of tomosyn and its implication in Ca2+-dependent exocytosis of neurotransmitter. J Cell Biol 170(7):1113–1125
2. Barak B, Williams A, Bielopolski N, Gottfried I, Okun E, Brown MA, Matti U, Rettig J, Stuenkel EL, Ashery U (2010) Tomosyn expression pattern in the mouse hippocampus suggests both presynaptic and postsynaptic functions. Front Neuroanat 4:149
3. Bhatnagar S, Oler AT, Rabaglia ME, Stapleton DS, Schueler KL, Truchan NA, Worzella SL, Stoehr JP, Clee SM, Yandell BS, Keller MP, Thurmond DC, Attie AD (2011) Positional cloning of a type 2 diabetes quantitative trait locus; tomosyn-2, a negative regulator of insulin secretion. PLoS Genet 7(10):e1002323
4. Chen K, Richlitzki A, Featherstone DE, Schwarzel M, Richmond JE (2011) Tomosyn-dependent regulation of synaptic transmission is required for a late phase of associative odor memory. Proc Natl Acad Sci USA 108(45):18482–18487
5. Cheviet S, Bezzi P, Ivarsson R, Renstrom E, Viertl D, Kasas S, Catsicas S, Regazzi R (2006) Tomosyn-1 is involved in a post-docking event required for pancreatic beta-cell exocytosis. J Cell Sci 119(Pt 14):2912–2920
6. Eken T (1998) Spontaneous electromyographic activity in adult rat soleus muscle. J Neurophysiol 80(1):365–376
7. Fujita Y, Shirataki H, Sakisaka T, Asakura T, Ohya T, Kotani H, Yokoyama S, Nishioka H, Matsuura Y, Mizoguchi A, Scheller RH, Takai Y (1998) Tomosyn: a syntaxin-1-binding protein that forms a novel complex in the neurotransmitter release process. Neuron 20(5):905–915
8. Gladycheva SE, Lam AD, Liu J, D’Andrea-Merrins M, Yizhar O, Lentz SI, Ashery U, Ernst SA, Stuenkel EL (2007) Receptor-mediated regulation of tomosyn-syntaxin 1A interactions in bovine adrenal chromaffin cells. J Biol Chem 282(31):22887–22899
9. Gracheva EO, Burdina AO, Holgado AM, Berthelot-Grosjean M, Ackley BD, Hadwiger G, Nonet ML, Weimer RM, Richmond JE (2006) Tomosyn inhibits synaptic vesicle priming in Caenorhabditis elegans. PLoS Biol 4(8):e261
10. Groffen AJ, Jacobsen L, Schut D, Verhage M (2005) Two distinct genes drive expression of seven tomosyn isoforms in the mammalian brain, sharing a conserved structure with a unique variable domain. J Neurochem 92(3):554–568
11. Hatsuzawa K, Lang T, Fasshauer D, Bruns D, Jahn R (2003) The R-SNARE motif of tomosyn forms SNARE core complexes with syntaxin 1 and SNAP-25 and down-regulates exocytosis. J Biol Chem 278(33):31159–31166
12. Jahn R, Fasshauer D (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490(7419):201–207
13. Klooster R, Plomp JJ, Huijbers MG, Niks EH, Straasheijm KR, Detmers FJ, Hermans PW, Sleijpen K, Verrips A, Losen M, Martinez-Martinez P, De Baets MH, van der Maarel SM, Verschuuren JJ (2012) Muscle-specific kinase myasthenia gravis IgG4 autoantibodies cause severe neuromuscular junction dysfunction in mice. Brain 135(Pt 4):1081–1101
14. Kraut R, Menon K, Zinn K (2001) A gain-of-function screen for genes controlling motor axon guidance and synaptogenesis in Drosophila. Curr Biol 11(6):417–430
15. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445(7124):168–176
16. Lou X, Scheuss V, Schneggenburger R (2005) Allosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion. Nature 435(7041):497–501
17. Magleby KL, Stevens CF (1972) A quantitative description of end-plate currents. J Physiol 223(1):173–197
18. McEwen JM, Madison JM, Dybbs M, Kaplan JM (2006) Antagonistic regulation of synaptic vesicle priming by tomosyn and UNC-13. Neuron 51(3):303–315
19. McLachlan EM, Martin AR (1981) Non-linear summation of end-plate potentials in the frog and mouse. J Physiol 311:307–324
20. Mistry R, Dennis S, Frerking M, Mellor JR (2011) Dentate gyrus granule cell firing patterns can induce mossy fiber long-term potentiation in vitro. Hippocampus 21(11):1157–1168
21. Mohrmann R, de Wit H, Verhage M, Neher E, Sorensen JB (2010) Fast vesicle fusion in living cells requires at least three SNARE complexes. Science 330(6003):502–505
22. Pobbati AV, Razeto A, Boddener M, Becker S, Fasshauer D (2004) Structural basis for the inhibitory role of tomosyn in exocytosis. J Biol Chem 279(45):47192–47200
23. Pobbati AV, Stein A, Fasshauer D (2006) N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science 313(5787):673–676
24. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16(6):1197–1207
25. Sakisaka T, Baba T, Tanaka S, Izumi G, Yasumi M, Takai Y (2004) Regulation of SNAREs by tomosyn and ROCK: implication in extension and retraction of neurites. J Cell Biol 166(1):17–25
26. Sakisaka T, Yamamoto Y, Mochida S, Nakamura M, Nishikawa K, Ishizaki H, Okamoto-Tanaka M, Miyoshi J, Fujiyoshi Y, Manabe T, Takai Y (2008) Dual inhibition of SNARE complex formation by tomosyn ensures controlled neurotransmitter release. J Cell Biol 183(2):323–337
27. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23(2):399–409
28. Segal MM, Furshpan EJ (1990) Epileptiform activity in microcultures containing small numbers of hippocampal neurons. J Neurophysiol 64(5):1390–1399
29. 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(6700):347–353
30. Swerdlow NR, Braff DL, Geyer MA (2000) Animal models of deficient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. Behav Pharmacol 11(3–4):185–204
31. Williams AL, Bielopolski N, Meroz D, Lam AD, Passmore DR, Ben-Tal N, Ernst SA, Ashery U, Stuenkel EL (2011) Structural and functional analysis of tomosyn identifies domains important in exocytotic regulation. J Biol Chem 286(16):14542–14553
32. Wood SJ, Slater CR (2001) Safety factor at the neuromuscular junction. Prog Neurobiol 64(4):393–429
33. Yamamoto Y, Fujikura K, Sakaue M, Okimura K, Kobayashi Y, Nakamura T, Sakisaka T (2010a) The tail domain of tomosyn controls membrane fusion through tomosyn displacement by VAMP2. Biochem Biophys Res Commun 399(1):24–30
34. Yamamoto Y, Mochida S, Miyazaki N, Kawai K, Fujikura K, Kurooka T, Iwasaki K, Sakisaka T (2010b) Tomosyn inhibits synaptotagmin-1-mediated step of Ca2+-dependent neurotransmitter release through its N-terminal WD40 repeats. J Biol Chem 285(52):40943–40955
35. Yizhar O, Matti U, Melamed R, Hagalili Y, Bruns D, Rettig J, Ashery U (2004) Tomosyn inhibits priming of large dense-core vesicles in a calcium-dependent manner. Proc Natl Acad Sci USA 101(8):2578–2583
36. Zhang W, Lilja L, Mandic SA, Gromada J, Smidt K, Janson J, Takai Y, Bark C, Berggren PO, Meister B (2006) Tomosyn is expressed in beta-cells and negatively regulates insulin exocytosis. Diabetes 55(3):574–581
37. Zurita E, Chagoyen M, Cantero M, Alonso R, Gonzalez-Neira A, Lopez-Jimenez A, Lopez-Moreno JA, Landel CP, Benitez J, Pazos F, Montoliu L (2011) Genetic polymorphisms among C57BL/6 mouse inbred strains. Transgenic Res 20(3):481–489