Dominant negative SNARE peptides stabilize the fusion pore in a narrow, release-unproductive state

Cellular and Molecular Life Sciences

Volumn 73, Issue 19, 2016, Pages 3719-3731

  Guček, Alenka ^a   Jorgačevski, Jernej ^a,b   Singh, Priyanka ^a   Geisler, Claudia ^c   Lisjak, Marjeta ^a   Vardjan, Nina ^a,b   Kreft, Marko ^a,b,d   Egner, Alexander ^c   Zorec, Robert ^a,b  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b Celica Biomedical Sciences Center   (Slovenia)

^c LASER LABORATORIUM GÖTTINGEN E V   (Germany)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Astrocytes; Capacitance measurements; Fusion pore; Gliotransmitters; Regulated exocytosis; STED microscopy

Indexed keywords

ADENOSINE TRIPHOSPHATE; BOTULINUM NEUROTOXIN D; BOTULINUM TOXIN; BOTULINUM TOXIN E; SNARE PROTEIN; UNCLASSIFIED DRUG; PEPTIDE;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL EXPANSION; CELL FUSION; CELL POPULATION; CELL VACUOLE; CONTROLLED STUDY; EXOCYTOSIS; FEMALE; MICROSCOPY; NEWBORN; NONHUMAN; PHASE TRANSITION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STABILITY; RAT; SENSITIVITY ANALYSIS; STRUCTURED ILLUMINATION MICROSCOPY; SUPERRESOLUTION STIMULATED EMISSION DEPLETION MICROSCOPY; SYNAPSE VESICLE; ANIMAL; BIOLOGICAL MODEL; DRUG EFFECTS; EXOSOME; MEMBRANE FUSION; METABOLISM; TIME FACTOR; WISTAR RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; ASTROCYTES; EXOCYTOSIS; EXTRACELLULAR VESICLES; FEMALE; MEMBRANE FUSION; MICROSCOPY; MODELS, BIOLOGICAL; PEPTIDES; RATS, WISTAR; SNARE PROTEINS; TIME FACTORS;

EID: 84964033687     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-016-2213-2     Document Type: Article

References (59)

1. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22(5):208–215. pii:S0166-2236(98)01349-6
2. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247(4941):470–473
3. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte–neuron signalling. Nature 369(6483):744–747
4. Kreft M, Stenovec M, Rupnik M, Grilc S, Krzan M, Potokar M, Pangrsic T, Haydon PG, Zorec R (2004) Properties of Ca(2+)-dependent exocytosis in cultured astrocytes. Glia 46(4):437–445
5. Krzan M, Stenovec M, Kreft M, Pangrsic T, Grilc S, Haydon PG, Zorec R (2003) Calcium-dependent exocytosis of atrial natriuretic peptide from astrocytes. J Neurosci 23(5):1580–1583
6. Zhang Q, Pangrsic T, Kreft M, Krzan M, Li N, Sul JY, Halassa M, Van Bockstaele E, Zorec R, Haydon PG (2004) Fusion-related release of glutamate from astrocytes. J Biol Chem 279(13):12724–12733
7. Ben Achour S, Pascual O (2012) Astrocyte–neuron communication: functional consequences. Neurochem Res. doi:10.1007/s11064-012-0807-0
8. Gundersen V, Storm-Mathisen J, Bergersen LH (2015) Neuroglial transmission. Physiol Rev 95(3):695–726. doi:10.1152/physrev.00024.2014
9. Guček A, Vardjan N, Zorec R (2012) Exocytosis in astrocytes: transmitter release and membrane signal regulation. Neurochem Res. doi:10.1007/s11064-012-0773-6
10. Vardjan N, Parpura V, Zorec R (2015) Loose excitation-secretion coupling in astrocytes. Glia. doi:10.1002/glia.22920
11. Wilhelm A, Volknandt W, Langer D, Nolte C, Kettenmann H, Zimmermann H (2004) Localization of SNARE proteins and secretory organelle proteins in astrocytes in vitro and in situ. Neurosci Res 48(3):249–257. doi:10.1016/j.neures.2003.11.002
12. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7(6):613–620
13. Verderio C, Cagnoli C, Bergami M, Francolini M, Schenk U, Colombo A, Riganti L, Frassoni C, Zuccaro E, Danglot L, Wilhelm C, Galli T, Canossa M, Matteoli M (2012) TI-VAMP/VAMP7 is the SNARE of secretory lysosomes contributing to ATP secretion from astrocytes. Biol Cell 104(4):213–228. doi:10.1111/boc.201100070
14. Schubert V, Bouvier D, Volterra A (2011) SNARE protein expression in synaptic terminals and astrocytes in the adult hippocampus: a comparative analysis. Glia 59(10):1472–1488. doi:10.1002/glia.21190
15. Pascual O (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113–116
16. Halassa MM (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61:213–219
17. Bergersen LH, Morland C, Ormel L, Rinholm JE, Larsson M, Wold JF, Røe AT, Stranna A, Santello M, Bouvier D, Ottersen OP, Volterra A, Gundersen V (2011) Immunogold detection of l-glutamate and d-serine in small synaptic-like microvesicles in adult hippocampal astrocytes. Cereb Cortex. doi:10.1093/cercor/bhr254
18. Crippa D, Schenk U, Francolini M, Rosa P, Verderio C, Zonta M, Pozzan T, Matteoli M, Carmignoto G (2006) Synaptobrevin2-expressing vesicles in rat astrocytes: insights into molecular characterization, dynamics and exocytosis. J Physiol 570(Pt 3):567–582
19. Martineau M, Shi T, Puyal J, Knolhoff AM, Dulong J, Gasnier B, Klingauf J, Sweedler JV, Jahn R, Mothet JP (2013) Storage and uptake of d-serine into astrocytic synaptic-like vesicles specify gliotransmission. J Neurosci 33(8):3413–3423. doi:10.1523/JNEUROSCI.3497-12.2013
20. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278(2):1354–1362
21. Pangrsic T, Potokar M, Stenovec M, Kreft M, Fabbretti E, Nistri A, Pryazhnikov E, Khiroug L, Giniatullin R, Zorec R (2007) Exocytotic release of ATP from cultured astrocytes. J Biol Chem 282(39):28749–28758
22. Zhang Z, Chen G, Zhou W, Song A, Xu T, Luo Q, Wang W, Gu XS, Duan S (2007) Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol 9(8):945–953
23. Bergami M, Santi S, Formaggio E, Cagnoli C, Verderio C, Blum R, Berninger B, Matteoli M, Canossa M (2008) Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J Cell Biol 183(2):213–221
24. Potokar M, Stenovec M, Kreft M, Kreft ME, Zorec R (2008) Stimulation inhibits the mobility of recycling peptidergic vesicles in astrocytes. Glia 56(2):135–144
25. Malarkey EB, Parpura V (2011) Temporal characteristics of vesicular fusion in astrocytes: examination of synaptobrevin 2-laden vesicles at single vesicle resolution. J Physiol 589(Pt 17):4271–4300
26. Bowser DN, Khakh BS (2007) Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc Natl Acad Sci USA 104(10):4212–4217
27. Chen X, Wang L, Zhou Y, Zheng LH, Zhou Z (2005) “Kiss-and-run” glutamate secretion in cultured and freshly isolated rat hippocampal astrocytes. J Neurosci 25(40):9236–9243
28. Hell SW, Wichmann J (1994) Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett 19(11):780–782
29. Gustafsson MG (2000) Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198(Pt 2):82–87
30. Neher E, Marty A (1982) Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci USA 79(21):6712–6716
31. Flašker A, Jorgačevski J, Calejo AI, Kreft M, Zorec R (2013) Vesicle size determines unitary exocytic properties and their sensitivity to sphingosine. Mol Cell Endocrinol. doi:10.1016/j.mce.2013.06.012
32. Singh P, Jorgačevski J, Kreft M, Grubišić V, Stout RF, Potokar M, Parpura V, Zorec R (2014) Single-vesicle architecture of synaptobrevin2 in astrocytes. Nat Commun 5:3780. doi:10.1038/ncomms4780
33. Bückers J, Wildanger D, Vicidomini G, Kastrup L, Hell SW (2011) Simultaneous multi-lifetime multi-color STED imaging for colocalization analyses. Opt Express 19(4):3130–3143
34. Rituper B, Guček A, Jorgačevski J, Flašker A, Kreft M, Zorec R (2013) High-resolution membrane capacitance measurements for the study of exocytosis and endocytosis. Nat Protoc 8(6):1169–1183. doi:10.1038/nprot.2013.069
35. Lollike K, Borregaard N, Lindau M (1995) The exocytotic fusion pore of small granules has a conductance similar to an ion channel. J Cell Biol 129(1):99–104
36. Spruce AE, Breckenridge LJ, Lee AK, Almers W (1990) Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron 4(5):643–654. pii:0896-6273(90)90192-I
37. Gentet LJ, Stuart GJ, Clements JD (2000) Direct measurement of specific membrane capacitance in neurons. Biophys J 79(1):314–320. doi:10.1016/S0006-3495(00)76293-X
38. Abbe E (1873) Beiträgezurtheorie des mikroskops und der mikroskopischenwahrnehmung. Archiv für mikroskopische Anatomie 9:413–418
39. Hell SW (2007) Far-field optical nanoscopy. Science 316(5828):1153–1158. doi:10.1126/science.1137395
40. Potokar M, Stenovec M, Gabrijel M, Li L, Kreft M, Grilc S, Pekny M, Zorec R (2010) Intermediate filaments attenuate stimulation-dependent mobility of endosomes/lysosomes in astrocytes. Glia 58(10):1208–1219. doi:10.1002/glia.21000
41. Alvarez de Toledo G, Fernández-Chacón R, Fernández JM (1993) Release of secretory products during transient vesicle fusion. Nature 363(6429):554–558. doi:10.1038/363554a0
42. Jahn R, Scheller RH (2006) SNAREs—engines for membrane fusion. Nat Rev Mol Cell Biol 7(9):631–643. doi:10.1038/nrm2002
43. Ormel L, Stensrud MJ, Bergersen LH, Gundersen V (2012) VGLUT1 is localized in astrocytic processes in several brain regions. Glia 60(2):229–238. doi:10.1002/glia.21258
44. Ban N, Escobar C, Garcia R, Hasel K, Day J, Greenwood A, McPherson A (1994) Crystal structure of an idiotype-anti-idiotype Fab complex. Proc Natl Acad Sci USA 91(5):1604–1608
45. Jorgacevski J, Fosnaric M, Vardjan N, Stenovec M, Potokar M, Kreft M, Kralj-Iglic V, Iglic A, Zorec R (2010) Fusion pore stability of peptidergic vesicles. Mol Membr Biol 27(2–3):65–80. doi:10.3109/09687681003597104
46. Elhamdani A, Azizi F, Artalejo CR (2006) Double patch clamp reveals that transient fusion (kiss-and-run) is a major mechanism of secretion in calf adrenal chromaffin cells: high calcium shifts the mechanism from kiss-and-run to complete fusion. J Neurosci 26(11):3030–3036. doi:10.1523/JNEUROSCI.5275-05.2006
47. He L, Wu LG (2007) The debate on the kiss-and-run fusion at synapses. Trends Neurosci 30(9):447–455. doi:10.1016/j.tins.2007.06.012
48. Verkhratsky A, Matteoli M, Parpura V, Mothet JP, Zorec R (2016) Astrocytes as secretory cells of the central nervous system: idiosyncrasies of vesicular secretion. EMBO J 35(3):239–257. doi:10.15252/embj.201592705
49. Stenovec M, Kreft M, Poberaj I, Betz WJ, Zorec R (2004) Slow spontaneous secretion from single large dense-core vesicles monitored in neuroendocrine cells. FASEB J 18(11):1270–1272
50. Sloan SA, Barres BA (2014) Looks can be deceiving: reconsidering the evidence for gliotransmission. Neuron 84(6):1112–1115. doi:10.1016/j.neuron.2014.12.003
51. Jorgacevski J, Potokar M, Grilc S, Kreft M, Liu W, Barclay JW, Bückers J, Medda R, Hell SW, Parpura V, Burgoyne RD, Zorec R (2011) Munc18-1 tuning of vesicle merger and fusion pore properties. J Neurosci 31(24):9055–9066. doi:10.1523/JNEUROSCI.0185-11.2011
52. Fellin T, Halassa MM, Terunuma M, Succol F, Takano H, Frank M, Moss SJ, Haydon PG (2009) Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc Natl Acad Sci USA 106(35):15037–15042. doi:10.1073/pnas.0906419106
53. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310(5745):113–116. doi:10.1126/science.1116916
54. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY, Abel T, Haydon PG, Frank MG (2009) Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61(2):213–219. doi:10.1016/j.neuron.2008.11.024
55. Jahn HM, Scheller A, Kirchhoff F (2015) Genetic control of astrocyte function in neural circuits. Front Cell Neurosci 9:310. doi:10.3389/fncel.2015.00310
56. Fujita T, Chen MJ, Li B, Smith NA, Peng W, Sun W, Toner MJ, Kress BT, Wang L, Benraiss A, Takano T, Wang S, Nedergaard M (2014) Neuronal transgene expression in dominant-negative SNARE mice. J Neurosci 34(50):16594–16604. doi:10.1523/JNEUROSCI.2585-14.2014
57. Lee HS, Ghetti A, Pinto-Duarte A, Wang X, Dziewczapolski G, Galimi F, Huitron-Resendiz S, Piña-Crespo JC, Roberts AJ, Verma IM, Sejnowski TJ, Heinemann SF (2014) Astrocytes contribute to gamma oscillations and recognition memory. Proc Natl Acad Sci USA 111(32):E3343–E3352. doi:10.1073/pnas.1410893111
58. Vaidyanathan VV, Yoshino K, Jahnz M, Dörries C, Bade S, Nauenburg S, Niemann H, Binz T (1999) Proteolysis of SNAP-25 isoforms by botulinum neurotoxin types A, C, and E: domains and amino acid residues controlling the formation of enzyme-substrate complexes and cleavage. J Neurochem 72(1):327–337
59. Popoff MR, Poulain B (2010) Bacterial toxins and the nervous system: neurotoxins and multipotential toxins interacting with neuronal cells. Toxins (Basel) 2(4):683–737. doi:10.3390/toxins2040683