Syndapin 3 modulates fusion pore expansion in mouse neuroendocrine chromaffin cells

American Journal of Physiology - Cell Physiology

Volumn 306, Issue 9, 2014, Pages

  Samasilp, Prattana ^a   Lopin, Kyle ^b   Chan, Shyue An ^a   Ramachandran, Rajesh ^a   Smith, Corey ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Catecholamine; Chromaffin cells; Fusion pore; Neuroendocrine; Syndapin

Indexed keywords

DYNAMIN; DYNAMIN I; MESSENGER RNA; SYNDAPIN 3; UNCLASSIFIED DRUG;

ADRENAL MEDULLA; ANIMAL CELL; ARTICLE; CATECHOLAMINE RELEASE; CELL EXPANSION; CELL MEMBRANE; CELL STIMULATION; CELLULAR DISTRIBUTION; CHROMAFFIN CELL; ENDOCYTOSIS; EXOCYTOSIS; HORMONE RELEASE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; INTERNALIZATION; MOUSE; NERVE CELL MEMBRANE; NEUROSECRETORY CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SECRETORY GRANULE; STRESS; SYMPATHETIC TONE; SYNAPSE VESICLE; WESTERN BLOTTING;

CATECHOLAMINE; CHROMAFFIN CELLS; FUSION PORE; NEUROENDOCRINE; SYNDAPIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADRENAL MEDULLA; ANIMALS; CARRIER PROTEINS; CATECHOLAMINES; CELLS, CULTURED; CHROMAFFIN CELLS; DYNAMIN I; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KINETICS; MEMBRANE FUSION; MICE; MICE, INBRED C57BL; MUTATION; NEUROPEPTIDES; PHOSPHOPROTEINS; POROSITY; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEINS; RATS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; TRANSFECTION;

EID: 84900532154     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00291.2013     Document Type: Article

References (68)

1. Albillos A, Dernick G, Horstmann H, Almers W, Alvarez de Toledo G, Lindau M. The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389: 509-512, 1997.
2. Amatore C, Arbault S, Bonifas I, Guille M, Lemaitre F, Verchier Y. Relationship between amperometric pre-spike feet and secretion granule composition in chromaffin cells: an overview. Biophys Chem 129: 181-189, 2007.
3. Anantharam A, Bittner MA, Aikman RL, Stuenkel EL, Schmid SL, Axelrod D, Holz RW. A new role for the dynamin GTPase in the regulation of fusion pore expansion. Mol Biol Cell 22: 1907-1918, 2011.
4. Anggono V, Smillie KJ, Graham ME, Valova VA, Cousin MA, Robinson PJ. Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nat Neurosci 9: 752-760, 2006.
5. Angleson JK, Cochilla AJ, Kilic G, Nussinovitch I, Betz WJ. Regulation of dense core release from neuroendocrine cells revealed by imaging single exocytotic events. Nat Neurosci 2: 440-446, 1999.
6. Artalejo CR, Lemmon MA, Schlessinger J, Palfrey HC. Specific role for the pH domain of dynamin-1 in the regulation of rapid endocytosis in adrenal chromaffin cells. EMBO J 16: 1565-1574, 1997.
7. Barclay JW, Aldea M, Craig TJ, Morgan A, Burgoyne RD. Regulation of the fusion pore conductance during exocytosis by cyclin-dependent kinase 5. J Biol Chem 279: 41495-41503, 2004.
8. Brittain JM, Piekarz AD, Wang Y, Kondo T, Cummins TR, Khanna R. An atypical role for collapsin response mediator protein 2 (CRMP-2) in neurotransmitter release via interaction with presynaptic voltage-gated calcium channels. J Biol Chem 284: 31375-31390, 2009.
9. Brown M, Adyshev D, Bindokas V, Moitra J, Garcia JG, Dudek SM. Quantitative distribution and colocalization of non-muscle myosin light chain kinase isoforms and cortactin in human lung endothelium. Microvasc Res 80: 75-88, 2010.
10. 2+ current rundown. Pflügers Arch 430: 213-219, 1995.
11. V2.2) calcium channel interacting protein. Channels (Austin) 1: 11-20, 2007.
12. Chan SA, Chow R, Smith C. Calcium dependence of action potentialinduced endocytosis in chromaffin cells. Pflügers Arch 445: 540-546, 2003.
13. Chan SA, Smith C. Low frequency stimulation of mouse adrenal slices reveals a clathrin-independent, protein kinase C-mediated endocytic mechanism. J Physiol 553: 707-717, 2003.
14. Chan SA, Smith C. Physiological stimuli evoke two forms of endocytosis in bovine chromaffin cells. J Physiol 537: 871-885, 2001.
15. Chow RH, von Ruden L, Neher E. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356: 60-63, 1992.
16. Clayton EL, Anggono V, Smillie KJ, Chau N, Robinson PJ, Cousin MA. The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles. J Neurosci 29: 7706-7717, 2009.
17. Cuajungco MP, Grimm C, Oshima K, D'Hoedt D, Nilius B, Mensenkamp AR, Bindels RJ, Plomann M, Heller S. PACSINs bind to the TRPV4 cation channel. PACSIN 3 modulates the subcellular localization of TRPV4. J Biol Chem 281: 18753-18762, 2006.
18. D'Hoedt D, Owsianik G, Prenen J, Cuajungco MP, Grimm C, Heller S, Voets T, Nilius B. Stimulus-specific modulation of the cation channel TRPV4 by PACSIN 3. J Biol Chem 283: 6272-6280, 2008.
19. Da Costa SR, Sou E, Xie J, Yarber FA, Okamoto CT, Pidgeon M, Kessels MM, Mircheff AK, Schechter JE, Qualmann B, Hamm-Alvarez SF. Impairing actin filament or syndapin functions promotes accumulation of clathrin-coated vesicles at the apical plasma membrane of acinar epithelial cells. Mol Biol Cell 14: 4397-4413, 2003.
20. Dharmalingam E, Haeckel A, Pinyol R, Schwintzer L, Koch D, Kessels MM, Qualmann B. F-BAR proteins of the syndapin family shape the plasma membrane and are crucial for neuromorphogenesis. J Neurosci 29: 13315-13327, 2009.
21. Doreian BW, Fulop TG, Smith CB. Myosin II activation and actin reorganization regulate the mode of quantal exocytosis in mouse adrenal chromaffin cells. J Neurosci 28: 4470-4478, 2008.
22. Elhamdani A, Palfrey HC, Artalejo CR. Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells. Neuron 31: 819-830, 2001.
23. Engisch KL, Nowycky MC. Compensatory and excess retrieval: two types of endocytosis following single step depolarizations in bovine adrenal chromaffin cells. J Physiol 506: 591-608, 1998.
24. Fang Q, Berberian K, Gong LW, Hafez I, Sorensen JB, Lindau M. The role of the C terminus of the SNARE protein SNAP-25 in fusion pore opening and a model for fusion pore mechanics. Proc Natl Acad Sci USA 105: 15388-15392, 2008.
25. Ferguson SM, De Camilli P. Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol 13: 75-88, 2012.
26. Fulop T, Doreian B, Smith C. Dynamin I plays dual roles in the activity-dependent shift in exocytic mode in mouse adrenal chromaffin cells. Arch Biochem Biophys 477: 146-154, 2008.
27. Fulop T, Radabaugh S, Smith C. Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J Neurosci 25: 7324-7332, 2005.
28. Fulop T, Smith C. Matching native electrical stimulation by graded chemical stimulation in isolated mouse adrenal chromaffin cells. J Neurosci Methods 166: 195-202, 2007.
29. Fulop T, Smith C. Physiological stimulation regulates the exocytic mode through calcium activation of protein kinase C in mouse chromaffin cells. Biochem J 399: 111-119, 2006.
30. Goh SL, Wang Q, Byrnes LJ, Sondermann H. Versatile membrane deformation potential of activated pacsin. PLos One 7: e51628, 2012.
31. Gomez JF, Brioso MA, Machado JD, Sanchez JL, Borges R. New approaches for analysis of amperometrical recordings. Ann NY Acad Sci 971: 647-654, 2002.
32. Gonzalez-Jamett AM, Momboisse F, Guerra MJ, Ory S, Baez-Matus X, Barraza N, Calco V, Houy S, Couve E, Neely A, Martinez AD, Gasman S, Cardenas AM. Dynamin-2 regulates fusion pore expansion and quantal release through a mechanism that involves actin dynamics in neuroendocrine chromaffin cells. PLos One 8: e70638, 2013.
33. Graham ME, O'Callaghan DW, McMahon HT, Burgoyne RD. Dynamin-dependent and dynamin-independent processes contribute to the regulation of single vesicle release kinetics and quantal size. Proc Natl Acad Sci USA 99: 7124-7129, 2002.
34. Hansen CG, Howard G, Nichols BJ. Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis. J Cell Sci 124: 2777-2785, 2011.
35. Kessels MM, Dong J, Leibig W, Westermann P, Qualmann B. Complexes of syndapin II with dynamin II promote vesicle formation at the trans-Golgi network. J Cell Sci 119: 1504-1516, 2006.
36. Kessels MM, Qualmann B. Syndapin oligomers interconnect the machineries for endocytic vesicle formation and actin polymerization. J Biol Chem 281: 13285-13299, 2006.
37. Kessels MM, Qualmann B. The syndapin protein family: linking membrane trafficking with the cytoskeleton. J Cell Sci 117: 3077-3086, 2004.
38. Kessels MM, Qualmann B. Syndapins integrate N-WASP in receptormediated endocytosis. EMBO J 21: 6083-6094, 2002.
39. Khanna R, Li Q, Stanley EF. "Fractional recovery" analysis of a presynaptic synaptotagmin 1-anchored endocytic protein complex. PLos One 1: e67, 2006.
40. Klyachko VA, Jackson MB. Capacitance steps and fusion pores of small and large dense-core vesicles in nerve terminals. Nature 418: 89-92, 2002.
41. Koch D, Spiwoks-Becker I, Sabanov V, Sinning A, Dugladze T, Stellmacher A, Ahuja R, Grimm J, Schuler S, Muller A, Angenstein F, Ahmed T, Diesler A, Moser M, Tom Dieck S, Spessert R, Boeckers TM, Fassler R, Hubner CA, Balschun D, Gloveli T, Kessels MM, Qualmann B. Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin I. EMBO J 30: 4955-4969, 2011.
42. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, Stanley EF. A syntaxin 1, Gα°, and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 24: 4070-4081, 2004.
43. Lou X, Fan F, Messa M, Raimondi A, Wu Y, Looger LL, Ferguson SM, De Camilli P. Reduced release probability prevents vesicle depletion and transmission failure at dynamin mutant synapses. Proc Natl Acad Sci USA 109: E515-E523, 2012.
44. Matthies HJ, Han Q, Shields A, Wright J, Moore JL, Winder DG, Galli A, Blakely RD. Subcellular localization of the antidepressantsensitive norepinephrine transporter. BMC Neurosci 10: 65, 2009.
45. Modregger J, Ritter B, Witter B, Paulsson M, Plomann M. All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J Cell Sci 113: 4511-4521, 2000.
46. Mosharov EV, Sulzer D. Analysis of exocytotic events recorded by amperometry. Nat Methods 2: 651-658, 2005.
47. Neco P, Fernandez-Peruchena C, Navas S, Gutierrez LM, de Toledo GA, Ales E. Myosin II contributes to fusion pore expansion during exocytosis. J Biol Chem 283: 10949-10957, 2008.
48. Ngatchou AN, Kisler K, Fang Q, Walter AM, Zhao Y, Bruns D, Sorensen JB, Lindau M. Role of the synaptobrevin C terminus in fusion pore formation. Proc Natl Acad Sci USA 107: 18463-18468, 2010.
49. Perez-Alvarez A, Hernandez-Vivanco A, Albillos A. Past, present and future of human chromaffin cells: role in physiology and therapeutics. Cell Mol Neurobiol 30: 1407-1415, 2010.
50. Perrais D, Kleppe IC, Taraska JW, Almers W. Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells. J Physiol 560: 413-428, 2004.
51. Plomann M, Lange R, Vopper G, Cremer H, Heinlein UA, Scheff S, Baldwin SA, Leitges M, Cramer M, Paulsson M, Barthels D. PACSIN, a brain protein that is upregulated upon differentiation into neuronal cells. Eur J Biochem 256: 201-211, 1998.
52. Qualmann B, Kelly RB. Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J Cell Biol 148: 1047-1062, 2000.
53. Qualmann B, Roos J, DiGregorio PJ, Kelly RB. Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol Biol Cell 10: 501-513, 1999.
54. Quan A, Robinson PJ. Syndapin, a membrane remodelling and endocytic F-BAR protein. FEBS J 280: 5198-5212, 2013.
55. Quan A, Robinson PJ. Repurposing molecular mechanisms of transmitter release: a new job for syndapin at the fusion pore. Focus on "Syndapin 3 modulates fusion pore expansion in mouse neuroendocrine chromaffin cells. " Am J Physiol Cell Physiol (March 19). doi:10.1152/ ajpcell.00079.2014.
56. Ritter B, Modregger J, Paulsson M, Plomann M. PACSIN 2, a novel member of the PACSIN family of cytoplasmic adapter proteins. FEBS Lett 454: 356-362, 1999.
57. Roach W, Plomann M. PACSIN3 overexpression increases adipocyte glucose transport through GLUT1. Biochem Biophys Res Commun 355: 745-750, 2007.
58. Samasilp P, Chan SA, Smith C. Activity-dependent fusion pore expansion regulated by a calcineurin-dependent dynamin-syndapin pathway in mouse adrenal chromaffin cells. J Neurosci 32: 10438-10447, 2012.
59. Senju Y, Itoh Y, Takano K, Hamada S, Suetsugu S. Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. J Cell Sci 124: 2032-2040, 2011.
60. Smith C, Neher E. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J Cell Biol 139: 885-894, 1997.
61. Sumoy L, Pluvinet R, Andreu N, Estivill X, Escarceller M. PACSIN 3 is a novel SH3 domain cytoplasmic adapter protein of the pacsin-syndapin-FAP52 gene family. Gene 262: 199-205, 2001.
62. Tavare JM, Fletcher LM, Welsh GI. Using green fluorescent protein to study intracellular signalling. J Endocrinol 170: 297-306, 2001.
63. Trouillon R, Ewing AG. Amperometric measurements at cells support a role for dynamin in the dilation of the fusion pore during exocytosis. Chemphyschem 14: 2295-2301, 2011.
64. 2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: fusion pore opening and fusion pore dilation. J Physiol 570: 295-307, 2006.
65. Wang CT, Lu JC, Bai J, Chang PY, Martin TF, Chapman ER, Jackson MB. Different domains of synaptotagmin control the choice between kiss-and-run and full fusion. Nature 424: 943-947, 2003.
66. Wiederhold K, Kloepper TH, Walter AM, Stein A, Kienle N, Sorensen JB, Fasshauer D. A coiled coil trigger site is essential for rapid binding of synaptobrevin to the SNARE acceptor complex. J Biol Chem 285: 21549-21559, 2010.
67. Wightman RM, Jankowski JA, Kennedy RT, Kawagoe KT, Schroeder TJ, Leszczyszyn DJ, Near JA, Diliberto EJ Jr, Viveros OH. Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc Natl Acad Sci USA 88: 10754-10758, 1991.
68. Zhang Z, Hui E, Chapman ER, Jackson MB. Regulation of exocytosis and fusion pores by synaptotagmin-effector interactions. Mol Biol Cell 21: 2821-2831, 2010.