Ca2+ triggers a novel clathrin-independent but actin-dependent fast endocytosis in pancreatic beta cells

Traffic

Volumn 9, Issue 6, 2008, Pages 910-923

  He, Zixuan ^a   Fan, Junmei ^b   Kang, Lijun ^b   Lu, Jingze ^a   Xue, Yanhong ^a   Xu, Pingyong ^a   Xu, Tao ^a,b   Chen, Liangyi ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Actin, Ca2+ i; Clathrin independent endocytosis

Indexed keywords

ACTIN; CALCIUM ION; CLATHRIN; DEXTRAN; DYNAMIN; GUANOSINE TRIPHOSPHATE; CALCIUM; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; SECRETORY VESICLE; ANIMAL; BAGG ALBINO MOUSE; ELECTRIC CAPACITANCE; ELECTROPHYSIOLOGY; GENETIC TRANSFECTION; INSULINOMA; METABOLISM; PATCH CLAMP; PATHOLOGY; PHYSIOLOGY; RNA INTERFERENCE; TUMOR CELL LINE;

ACTINS; ANIMALS; CALCIUM; CELL LINE, TUMOR; CLATHRIN; ELECTRIC CAPACITANCE; ELECTROPHYSIOLOGY; ENDOCYTOSIS; INSULIN-SECRETING CELLS; INSULINOMA; MALE; MICE; MICE, INBRED BALB C; MICROSCOPY, FLUORESCENCE; PATCH-CLAMP TECHNIQUES; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 43049172403     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00730.x     Document Type: Article

References (58)

1. Harata NC, Aravanis AM, Tsien RW. Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. J Neurochem 2006;97:1546-1570.
2. Royle SJ, Lagnado L. Endocytosis at the synaptic terminal. J Physiol 2003;553:345-355.
3. Artalejo CR, Elhamdani A, Palfrey HC. Sustained stimulation shifts the mechanism of endocytosis from dynamin-1-dependent rapid endocytosis to clathrin- and dynamin-2-mediated slow endocytosis in chromaffin cells. Proc Natl Acad Sci U S A 2002;99:6358-6363.
4. Jockusch WJ, Praefcke GJ, McMahon HT, Lagnado L. Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 2005;46:869-878.
5. Macdonald PE, Braun M, Galvanovskis J, Rorsman P. Release of small transmitters through kiss-and-run fusion pores in rat pancreatic beta cells. Cell Metab 2006;4:283-290.
6. He L, Wu XS, Mohan R, Wu LG. Two modes of fusion pore opening revealed by cell-attached recordings at a synapse. Nature 2006;444:102-105.
7. Holt M, Cooke A, Wu MM, Lagnado L. Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. J Neurosci 2003;23:1329-1339.
8. Paillart C, Li J, Matthews G, Sterling P. Endocytosis and vesicle recycling at a ribbon synapse. J Neurosci 2003;23:4092-4099.
9. von Gersdorff H, Matthews G. Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 1994;370:652-655.
10. Rouze NC, Schwartz EA. Continuous and transient vesicle cycling at a ribbon synapse. J Neurosci 1998;18:8614-8624.
11. Wu LG, Betz WJ. Nerve activity but not intracellular calcium determines the time course of endocytosis at the frog neuromuscular junction. Neuron 1996;17:769-779.
12. Neves G, Gomis A, Lagnado L. Calcium influx selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. Proc Natl Acad Sci U S A 2001;98:15282-15287.
13. Wu W, Xu J, Wu XS, Wu LG. Activity-dependent acceleration of endocytosis at a central synapse. J Neurosci 2005;25:11676-11683.
14. Beutner D, Voets T, Neher E, Moser T. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 2001;29:681-690.
15. Klingauf J, Kavalali ET, Tsien RW. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 1998;394:581-585.
16. Sankaranarayanan S, Ryan TA. Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat Neurosci 2001;4:129-136.
17. Ales E, Tabares L, Poyato JM, Valero V, Lindau M, Alvarez de Toledo G. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat Cell Biol 1999;1:40-44.
18. Lindau M, Neher E. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch 1988;411:137-146.
19. Kanno T, Ma X, Barg S, Eliasson L, Galvanovskis J, Gopel S, Larsson M, Renstrom E, Rorsman P. Large dense-core vesicle exocytosis in pancreatic beta-cells monitored by capacitance measurements. Methods 2004;33:302-311.
20. Rorsman P, Eliasson L, Renstrom E, Gromada J, Barg S, Gopel S. The cell physiology of biphasic insulin secretion. News Physiol Sci 2000;15:72-77.
21. Eliasson L, Proks P, Ammala C, Ashcroft FM, Bokvist K, Renstrom E, Rorsman P, Smith PA. Endocytosis of secretory granules in mouse pancreatic beta-cells evoked by transient elevation of cytosolic calcium. J Physiol 1996;493:755-767.
22. Gromada J, Bokvist K, Ding WG, Barg S, Buschard K, Renstrom E, Rorsman P. Adrenaline stimulates glucagon secretion in pancreatic A-cells by increasing the Ca2+ current and the number of granules close to the L-type Ca2+ channels. J Gen Physiol 1997;110:217-228.
23. James Keener JS. Mathematical Physiology. New York: Springer-Verlag; 1998.
24. Engisch KL, Nowycky MC. Compensatory and excess retrieval: Two types of endocytosis following single step depolarizations in bovine adrenal chromaffin cells. J Physiol 1998;506:591-608.
25. Marks B, McMahon HT. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr Biol 1998;8:740-749.
26. Lee AK, Tse A. Endocytosis in identified rat corticotrophs. J Physiol 2001;533:389-405.
27. Morgan JR, Prasad K, Jin S, Augustine GJ, Lafer EM. Eps15 homology domain-NPF motif interactions regulate clathrin coat assembly during synaptic vesicle recycling. J Biol Chem 2003;278:33583-33592.
28. Benmerah A, Poupon V, Cerf-Bensussan N, Dautry-Varsat A. Mapping of Eps15 domains involved in its targeting to clathrin-coated pits. J Biol Chem 2000;275:3288-3295.
29. Cao H, Garcia F, McNiven MA. Differential distribution of dynamin isoforms in mammalian cells. Mol Biol Cell 1998;9: 2595-2609.
30. Hinshaw JE. Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol 2000;16:483-519.
31. Merrifield CJ, Perrais D, Zenisek D. Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 2005;121:593-606.
32. Yamashita T, Hige T, Takahashi T. Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 2005;307:124-127.
33. Artalejo CR, Henley JR, McNiven MA, Palfrey HC. Rapid endocytosis coupled to exocytosis in adrenal chromaffin cells involves Ca2+ GTP, and dynamin but not clathrin. Proc Natl Acad Sci U S A 1995;92:8328-8332.
34. MacDonald PE, Obermuller S, Vikman J, Galvanovskis J, Rorsman P, Eliasson L. Regulated exocytosis and kiss-and-run of synaptic-like microvesicles in INS-1 and primary rat beta-cells. Diabetes 2005;54:736-743.
35. Braun M, Wendt A, Birnir B, Broman J, Eliasson L, Galvanovskis J, Gromada J, Mulder H, Rorsman P. Regulated exocytosis of GABA-containing synaptic-like microvesicles in pancreatic beta-cells. J Gen Physiol 2004;123:191-204.
36. Heuser JE, Reese TS. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 1973;57:315-344.
37. 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 2006;9:752-760.
38. Elhamdani A, Azizi F, Solomaha E, Palfrey HC, Artalejo CR. Two mechanistically distinct forms of endocytosis in adrenal chromaffin cells: Differential effects of SH3 domains and amphiphysin antagonism. FEBS Lett 2006;580:3263-3269.
39. 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 U S A 2002;99:7124-7129.
40. Tsuboi T, McMahon HT, Rutter GA. Mechanisms of dense core vesicle recapture following "kiss and run"("cavicapture") exocytosis in insulin-secreting cells. J Biol Chem 2004;279:47115-47124.
41. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 2004;118:591-605.
42. Heuser JE, Kirschner MW. Filament organization revealed in platinum replicas of freeze-dried cytoskeletons. J Cell Biol 1980;86:212-234.
43. Thomas P, Lee AK, Wong JG, Almers W. A triggered mechanism retrieves membrane in seconds after Ca(2+)-stimulated exocytosis in single pituitary cells. J Cell Biol 1994; 124: 667-675.
44. Heinemann C, Chow RH, Neher E, Zucker RS. Kinetics of the secretory response in bovine chromaffin cells following flash photolysis of caged Ca2+. Biophys J 1994;67:2546-2557.
45. Smith C, Neher E. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J Cell Biol 1997;139:885-894.
46. Hsu SF, Jackson MB. Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. J Physiol 1996;494:539-553.
47. Takahashi N, Kadowaki T, Yazaki Y, Miyashita Y, Kasai H. Multiple exocytotic pathways in pancreatic beta cells. J Cell Biol 1997;138:55-64.
48. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003;422:37-44.
49. Sauvonnet N, Dujeancourt A, Dautry-Varsat A. Cortactin and dynamin are required for the clathrin-independent endocytosis of gammac cytokine receptor. J Cell Biol 2005;168:155-163.
50. Pelkmans L, Puntener D, Helenius A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 2002;296:535-539.
51. Kaksonen M, Toret CP, Drubin DG. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 2005;123:305-320.
52. Yarar D, Waterman-Storer CM, Schmid SL. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 2005;16:964-975.
53. Logiudice L, Matthews G. Endocytosis at ribbon synapses. Traffic 2007;9:1123-1128.
54. Sudhof TC. The synaptic vesicle cycle. Annu Rev Neurosci 2004; 27: 509-547.
55. Wu LG. Kinetic regulation of vesicle endocytosis at synapses. Trends Neurosci 2004; 27: 548-554.
56. Artalejo CR, Elhamdani A, Palfrey HC. Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells. Neuron 1996; 16: 195-205.
57. Duman JG, Chen L, Palmer AE, Hille B. Contributions of intracellular compartments to calcium dynamics: Implicating an acidic store. Traffic 2006; 7: 859-872.
58. Yang X, Xu P, Xiao Y, Xiong X, Xu T. Domain requirement for the membrane trafficking and targeting of syntaxin 1A. J Biol Chem 2006; 281: 15457-15463.