Release mode of large and small dense-core vesicles specified by different synaptotagmin isoforms in PC12 cells

Molecular Biology of the Cell

Volumn 22, Issue 13, 2011, Pages 2324-2336

  Zhang, Zhen ^a,c   Wu, Yao ^a,b   Wang, Zhao ^a,b   Dunning, F Mark ^a,b   Rehfuss, Jonathan ^a,b   Ramanan, Deepshika ^a,b   Chapman, Edwin R ^a,b   Jackson, Meyer B ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; LIPOSOME; SYNAPTOTAGMIN; SYNAPTOTAGMIN IV; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; EXOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SECRETORY VESICLE; SYNAPSE VESICLE;

ANIMALS; CALCIUM; EXOCYTOSIS; MEMBRANE FUSION; NERVE TISSUE PROTEINS; PC12 CELLS; PROTEIN ISOFORMS; RATS; SECRETORY VESICLES; SENSITIVITY AND SPECIFICITY; SYNAPTOTAGMIN I; SYNAPTOTAGMINS;

EID: 79959896913     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-02-0159     Document Type: Article

References (72)

1. Ahras M, Otto GP, Tooze SA (2006). Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells. J Cell Biol 173, 241-251.
2. Alvarez de Toledo G, Fernandez-Chacon R, Fernandez JM (1993). Release of secretory products during transient vesicle fusion. Nature 363, 554-558. (Pubitemid 23186644)
3. Ariga T, Macala LJ, Saito M, Margolis RK, Greene LA, Margolis RU, Yu RK (1988). Lipid composition of PC12 pheochromocytoma cells: characterization of globoside as a major neutral glycolipid. Biochemistry 27, 52-58. (Pubitemid 18036284)
4. Atluri PP, Ryan TA (2006). The kinetics of synaptic vesicle reacidification at hippocampal nerve terminals. J Neurosci 26, 2313-2320. (Pubitemid 44699040)
5. Augustine GJ (2001). How does calcium trigger neurotransmitter release? Curr Opin Neurobiol 11, 320-326.
6. Bean AJ, Zhang X, Hokfelt T (1994). Peptide secretion: what do we know? FASEB J 8, 630-638.
7. Bhalla A, Chicka MC, Chapman ER (2008). Analysis of the synaptotagmin family during reconstituted membrane fusion. Uncovering a class of inhibitory isoforms. J Biol Chem 283, 21799-21807.
8. 2+ concentration to SNARE-mediated membrane fusion. Mol Biol Cell 16, 4755-4764.
9. Bolte S, Cordelieres FP (2006). A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224, 213-232. (Pubitemid 46010930)
10. 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, 4212-4217. (Pubitemid 47181604)
11. Chapman ER (2008). How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77, 615-641.
12. Childs GV, Unabia G, Tibolt R, Lloyd JM (1987). Cytological factors that support nonparallel secretion of luteinizing hormone and follicle-stimulating hormone during the estrous cycle. Endocrinology 121, 1801-1813. (Pubitemid 18012786)
13. Craxton M (2007). Evolutionary genomics of plant genes encoding N-terminal-TM-C2 domain proteins and the similar FAM62 genes and synaptotagmin genes of metazoans. BMC Genomics 8, 259.
14. 2+ binding to synaptotagmin 4. Nat Struct Mol Biol 11, 844-849.
15. Dean C, Liu H, Dunning FM, Chang PY, Jackson MB, Chapman ER (2009). Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release. Nat Neurosci 12, 767-776.
16. Denovan-Wright EM, Newton RA, Armstrong JN, Babity JM, Robertson HA (1998). Acute administration of cocaine, but not amphetamine, increases the level of synaptotagmin IV mRNA in the dorsal striatum of rat. Brain Res Mol Brain Res 55, 350-354. (Pubitemid 28248054)
17. Ferguson GD, Thomas DM, Elferink LA, Herschman HR (1999). Synthesis degradation, and subcellular localization of synaptotagmin IV, a neuronal immediate early gene product. J Neurochem 72, 1821-1831. (Pubitemid 29185984)
18. Fisher JM, Sossin W, Newcomb R, Scheller RH (1988). Multiple neuropeptides derived from a common precursor are differentially packaged and transported. Cell 54, 813-822.
19. 2+-dependent exocytosis in PC12 cells. J Biol Chem 279, 52677-52684.
20. 2+-dependent secretion in PC12 cells. J Biol Chem 277, 4601-4604.
21. Fukuda M, Mikoshiba K (2000). Distinct self-oligomerization activities of synaptotagmin familyUnique calcium-dependent oligomerization properties of synaptotagmin VII. J Biol Chem 275, 28180-28185.
22. Fulop T, Radabaugh S, Smith C (2005). Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J Neurosci 25, 7324-7332. (Pubitemid 41129804)
23. 2+-triggered fusion in vitro: critical residues revealed by scanning alanine mutagenesis. J Biol Chem 283, 31763-31775.
24. Gandhi SP, Stevens CF (2003). Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607-613.
25. Glombik MM, Gerdes HH (2000). Signal-mediated sorting of neuropeptides and prohormones: secretory granule biogenesis revisited. Biochimie 82, 315-326. (Pubitemid 30391910)
26. Gong LW, Hafez I, Alvarez de Toledo G, Lindau M (2003). Secretory vesicles membrane area is regulated in tandem with quantal size in chromaffin cells. J Neurosci 23, 7917-7921. (Pubitemid 37052360)
27. Guan JS et al. (2005). Interaction with vesicle luminal protachykinin regulates surface expression of delta-opioid receptors and opioid analgesia. Cell 122, 619-631.
28. Hokfelt T, Broberger C, Xu ZQ, Sergeyev V, Ubink R, Diez M (2000). Neuropeptides - an overview. Neuropharmacology 39, 1337-1356. (Pubitemid 30249197)
29. Hokfelt T, Zhang X, Wiesenfeld-Hallin Z (1994). Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17, 22-30. (Pubitemid 24024322)
30. Holroyd P, Lang T, Wenzel D, De Camilli P, Jahn R (2002). Imaging direct, dynamin-dependent recapture of fusing secretory granules on plasma membrane lawns from PC12 cells. Proc Natl Acad Sci USA 99, 16806-16811. (Pubitemid 36034054)
31. Hui E, Bai J, Wang P, Sugimori M, Llinas RR, Chapman ER (2005). Three distinct kinetic groupings of the synaptotagmin family: candidate sensors for rapid and delayed exocytosis. Proc Natl Acad Sci USA 102, 5210-5214.
32. Ibata K, Fukuda M, Hamada T, Kabayama H, Mikoshiba K (2000). Synaptotagmin IV is present at the Golgi and distal parts of neurites. J Neurochem 74, 518-526. (Pubitemid 30053723)
33. Kim T, Gondre-Lewis MC, Arnaoutova I, Loh YP (2006). Dense-core secretory granule biogenesis. Physiology (Bethesda) 21, 124-133. (Pubitemid 43752508)
34. 2+ sensor for neurotransmitter release. Trends Neurosci 26, 413-422.
35. MacDonald PE, Braun M, Galvanovskis J, Rorsman P (2006). Release of small transmitters through kiss-and-run fusion pores in rat pancreatic beta cells. Cell Metab 4, 283-290. (Pubitemid 44430913)
36. Marqueze B, Berton F, Seagar M (2000). Synaptotagmins in membrane traffic: which vesicles do the tagmins tag? Biochimie 82, 409-420.
37. Martinez I, Chakrabarti S, Hellevik T, Morehead J, Fowler K, Andrews NW (2000). Synaptotagmin VII regulates Ca(2+)-dependent exocytosis of lysosomes in fibroblasts. J Cell Biol 148, 1141-1149.
38. McNeilly AS, Crawford JL, Taragnat C, Nicol L, McNeilly JR (2003). The differential secretion of FSH and LH: regulation through genes, feedback and packaging. Reprod Suppl 61, 463-476.
39. Michael DJ, Geng X, Cawley NX, Loh YP, Rhodes CJ, Drain P, Chow RH (2004). Fluorescent cargo proteins in pancreatic beta-cells: design determines secretion kinetics at exocytosis. Biophys J 87, L03-05.
40. Miesenbock G, De Angelis DA, Rothman JE (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195. (Pubitemid 28325974)
41. Opazo F, Punge A, Buckers J, Hoopmann P, Kastrup L, Hell SW, Rizzoli SO (2010). Limited intermixing of synaptic vesicle components upon vesicle recycling. Traffic 11, 800-812.
42. Peng W, Premkumar A, Mossner R, Fukuda M, Lesch KP, Simantov R (2002). Synaptotagmin I and IV are differentially regulated in the brain by the recreational drug 3,4-methylenedioxymethamphetamine (MDMA). Brain Res Mol Brain Res 108, 94-101. (Pubitemid 35447967)
43. Perello M, Stuart R, Nillni EA (2008). Prothyrotropin-releasing hormone targets its processing products to different vesicles of the secretory pathway. J Biol Chem 283, 19936-19947.
44. Poopatanapong A, Teramitsu I, Byun JS, Vician LJ, Herschman HR, White SA (2006). Singing, but not seizure, induces synaptotagmin IV in zebra finch song circuit nuclei. J Neurobiol 66, 1613-1629. (Pubitemid 46005371)
45. Salio C, Lossi L, Ferrini F, Merighi A (2006). Neuropeptides as synaptic transmitters. Cell Tissue Res 326, 583-598. (Pubitemid 44444794)
46. Shin OH, Rhee JS, Tang J, Sugita S, Rosenmund C, Sudhof TC (2003). Sr2+ binding to the Ca2+ binding site of the synaptotagmin 1 C2B domain triggers fast exocytosis without stimulating SNARE interactions. Neuron 37, 99-108. (Pubitemid 36106437)
47. Sossin WS, Fisher JM, Scheller RH (1990). Sorting within the regulated secretory pathway occurs in the trans-Golgi network. J Cell Biol 110, 1-12.
48. Sossin WS, Scheller RH (1991). Biosynthesis and sorting of neuropeptides. Curr Opin Neurobiol 1, 79-83.
49. Sudhof TC (2002). Synaptotagmins: why so many? J Biol Chem 277, 7629-7632.
50. Taraska JW, Almers W (2004). Bilayers merge even when exocytosis is transient. Proc Natl Acad Sci USA 101, 8780-8785. (Pubitemid 38745848)
51. Tsuboi T, Rutter GA (2003). Multiple forms of "kiss-and-run" exocytosis revealed by evanescent wave microscopy. Curr Biol 13, 563-567.
52. Tucker WC, Edwardson JM, Bai J, Kim HJ, Martin TF, Chapman ER (2003). Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells. J Cell Biol 162, 199-209. (Pubitemid 36928834)
53. Tucker WC, Weber T, Chapman ER (2004). Reconstitution of Ca2+-regulated membrane fusion by synaptotagmin and SNAREs. Science 304, 435-438. (Pubitemid 38495938)
54. Verhage M, McMahon HT, Ghijsen WE, Boomsma F, Scholten G, Wiegant VM, Nicholls DG (1991). Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron 6, 517-524.
55. Vician L, Lim IK, Ferguson G, Tocco G, Baudry M, Herschman HR (1995). Synaptotagmin IV is an immediate early gene induced by depolarization in PC12 cells and in brain. Proc Natl Acad Sci USA 92, 2164-2168.
56. 2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: fusion pore opening and fusion pore dilation. J Physiol 570, 295-307.
57. Wang CT, Grishanin R, Earles CA, Chang PY, Martin TF, Chapman ER, Jackson MB (2001). Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294, 1111-1115. (Pubitemid 33041868)
58. Wang CT, Lu JC, Bai J, Chang PY, Martin TF, Chapman ER, Jackson MB (2003). Different domains of synaptotagmin control the choice between kiss-and-run and full fusion. Nature 424, 943-947. (Pubitemid 37051685)
59. Wang P, Chicka MC, Bhalla A, Richards DA, Chapman ER (2005). Synaptotagmin VII is targeted to secretory organelles in PC12 cells, where it functions as a high-affinity calcium sensor. Mol Cell Biol 25, 8693-8702. (Pubitemid 41369187)
60. Whim MD (2006). Near simultaneous release of classical and peptide cotransmitters from chromaffin cells. J Neurosci 26, 6637-6642.
61. Willig KI, Rizzoli SO, Westphal V, Jahn R, Hell SW (2006). STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440, 935-939.
62. Winkler H, Apps DK, Fischer-Colbrie R (1986). The molecular function of adrenal chromaffin granules: established facts and unresolved topics. Neuroscience 18, 261-290. (Pubitemid 16065454)
63. 2+-triggered exocytosis. Neuron 34, 599-611.
64. Zhang Z, Bhalla A, Dean C, Chapman ER, Jackson MB (2009a). Synaptotagmin IV: a multifunctional regulator of peptidergic nerve terminals. Nat Neurosci 12, 163-171.
65. 2+-triggered exocytosis and fusion pores in PC12 cells. Mol Biol Cell 20, 5086-5095.
66. Zhang Z, Hui E, Chapman ER, Jackson MB (2010a). Regulation of exocytosis and fusion pores by synaptotagmin-effector interactions. Mol Biol Cell 21, 2821-2831.
67. 2+-triggered exocytosis from PC12 cells. J Gen Physiol 131, 117-124.
68. Zhang Z, Jackson MB (2010). Membrane bending energy and fusion pore kinetics in Ca(2+)-triggered exocytosis. Biophys J 98, 2524-2534.
69. Zhang Z, Zhang Z, Jackson MB (2010b). Synaptotagmin IV modulation of vesicle size and fusion pores in PC12 cells. Biophys J 98, 968-978.
70. Zhou Z, Misler S (1995). Action potential-induced quantal secretion of catecholamines from rat adrenal chromaffin cells. J Biol Chem 270, 3498-3505.
71. Zhou Z, Misler S, Chow RH (1996). Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys J 70, 1543-1552. (Pubitemid 26073067)
72. Zhu D, Zhou W, Liang T, Yang F, Zhang RY, Wu ZX, Xu T (2007). Synaptotagmin I and IX function redundantly in controlling fusion pore of large dense core vesicles. Biochem Biophys Res Commun 361, 922-927. (Pubitemid 47263456)