Dynamin-related protein-1 controls fusion pore dynamics during platelet granule exocytosis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 3, 2013, Pages 481-488

  Koseoglu, Secil ^a,b   Dilks, James R ^a   Peters, Christian G ^a   Fitch Tewfik, Jennifer L ^a   Fadel, Nathalie A ^a   Jasuja, Reema ^a   Italiano, Joseph E ^c,d   Haynes, Christy L ^b   Flaumenhaft, Robert ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b University of Minnesota   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

dynamin related protein 1; exocytosis; fusion pore; platelets; thrombosis

Indexed keywords

DYNAMIN; DYNAMIN II; DYNAMIN RELATED PROTEIN 1; PADGEM PROTEIN; SEROTONIN; UNCLASSIFIED DRUG;

AMPEROMETRY; ANIMAL CELL; ARTERIOLE; ARTICLE; BLOOD CLOTTING; CELL GRANULE; CHANNEL GATING; CONTROLLED STUDY; EXOCYTOSIS; HUMAN; HUMAN CELL; MEGAKARYOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SEROTONIN RELEASE; THROMBOCYTE ACTIVATION; THROMBOCYTE FUNCTION;

ANIMALS; ARTERIOLES; BLOOD PLATELETS; DISEASE MODELS, ANIMAL; DYNAMINS; EXOCYTOSIS; FIBRINOLYTIC AGENTS; GTP PHOSPHOHYDROLASES; HUMANS; LASERS; MEMBRANE FUSION; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIAL PROTEINS; P-SELECTIN; QUINAZOLINONES; RABBITS; SECRETORY VESICLES; SEROTONIN; THROMBOSIS; TIME FACTORS; VASCULAR SYSTEM INJURIES;

EID: 84874384926     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.255737     Document Type: Article

References (44)

1. Blair P, Flaumenhaft R. Platelet alpha-granules: basic biology and clinical correlates. Blood Rev. 2009;23:177-189.
2. Ge S, Wittenberg NJ, Haynes CL. Quantitative and real-time detection of secretion of chemical messengers from individual platelets. Biochemistry. 2008;47:7020-7024.
3. Ge S, Woo E, White JG, Haynes CL. Electrochemical measurement of endogenous serotonin release from human blood platelets. Anal Chem. 2011;83:2598-2604.
4. Ge S, White JG, Haynes CL. Quantal release of serotonin from platelets. Anal Chem. 2009;81:2935-2943.
5. Ge S, White JG, Haynes CL. Critical role of membrane cholesterol in exocytosis revealed by single platelet study. ACS Chem Biol. 2010;5:819-828.
6. Ge S, White JG, Haynes CL. Cytoskeletal F-actin, not the circumferential coil of microtubules, regulates platelet dense-body granule secretion. Platelets. 2012;23:259-263.
7. Praefcke GJ, McMahon HT. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol. 2004;5:133-147.
8. 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. 1991;88:10754-10758.
9. Graham GJ, Ren Q, Dilks JR, Blair P, Whiteheart SW, Flaumenhaft R. Endobrevin/VAMP-8-dependent dense granule release mediates thrombus formation in vivo. Blood. 2009;114:1083-1090.
10. Jasuja R, Passam FH, Kennedy DR, Kim SH, van Hessem L, Lin L, Bowley SR, Joshi SS, Dilks JR, Furie B, Furie BC, Flaumenhaft R. Protein disulfide isomerase inhibitors constitute a new class of antithrombotic agents. J Clin Invest. 2012;122:2104-2113.
11. Reems JA, Wang W, Tsubata K, Abdurrahman N, Sundell B, Tijssen MR, van der Schoot E, Di Summa F, Patel-Hett S, Italiano J Jr, Gilligan DM. Dynamin 3 participates in the growth and development of megakaryocytes. Exp Hematol. 2008;36:1714-1727.
12. Wang W, Gilligan DM, Sun S, Wu X, Reems JA. Distinct functional effects for dynamin 3 during megakaryocytopoiesis. Stem Cells Dev. 2011;20:2139-2151.
13. Verma DP, Hong Z. The ins and outs in membrane dynamics: tubulation and vesiculation. Trends Plant Sci. 2005;10:159-165.
14. Ramachandran R. Vesicle scission: dynamin. Semin Cell Dev Biol. 2011;22:10-17.
15. Graham ME, O'Callaghan DW, McMahon HT, Burgoyne RD. Dynamindependent and dynamin-independent processes contribute to the regulation of single vesicle release kinetics and quantal size. Proc Natl Acad Sci USA. 2002;99:7124-7129.
16. Tsuboi T, McMahon HT, Rutter GA. Mechanisms of dense core vesicle recapture following "kiss and run" ("cavicapture") exocytosis in insulinsecreting cells. J Biol Chem. 2004;279:47115-47124.
17. Fulop T, Doreian B, Smith C. Dynamin I plays dual roles in the activitydependent shift in exocytic mode in mouse adrenal chromaffin cells. Arch Biochem Biophys. 2008;477:146-154.
18. González-Jamett AM, Báez-Matus X, Hevia MA, Guerra MJ, Olivares MJ, Martínez AD, Neely A, Cárdenas AM. The association of dynamin with synaptophysin regulates quantal size and duration of exocytotic events in chromaffin cells. J Neurosci. 2010;30:10683-10691.
19. 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. 2011;22:1907-1918.
20. Anantharam A, Onoa B, Edwards RH, Holz RW, Axelrod D. Localized topological changes of the plasma membrane upon exocytosis visualized by polarized TIRFM. J Cell Biol. 2010;188:415-428.
21. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell. 2006;10:839-850.
22. Quan A, McGeachie AB, Keating DJ, van Dam EM, Rusak J, Chau N, Malladi CS, Chen C, McCluskey A, Cousin MA, Robinson PJ. Myristyl trimethyl ammonium bromide and octadecyl trimethyl ammonium bromide are surface-active small molecule dynamin inhibitors that block endocytosis mediated by dynamin I or dynamin II. Mol Pharmacol. 2007;72:1425-1439.
23. Smirnova E, Shurland DL, Ryazantsev SN, van der Bliek AM. A human dynamin-related protein controls the distribution of mitochondria. J Cell Biol. 1998;143:351-358.
24. Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. ER tubules mark sites of mitochondrial division. Science. 2011;334:358-362.
25. Montessuit S, Somasekharan SP, Terrones O, Lucken-Ardjomande S, Herzig S, Schwarzenbacher R, Manstein DJ, Bossy-Wetzel E, Basañez G, Meda P, Martinou JC. Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization. Cell. 2010;142:889-901.
26. Chang CR, Blackstone C. Dynamic regulation of mitochondrial fission through modification of the dynamin-related protein Drp1. Ann N Y Acad Sci. 2010;1201:34-39.
27. Santel A, Frank S. Shaping mitochondria: the complex posttranslational regulation of the mitochondrial fission protein DRP1. IUBMB Life. 2008;60:448-455.
28. Zhao J, Liu T, Jin S, Wang X, Qu M, Uhlén P, Tomilin N, Shupliakov O, Lendahl U, Nistér M. Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 2011;30:2762-2778.
29. Zhang B, Alysandratos KD, Angelidou A, Asadi S, Sismanopoulos N, Delivanis DA, Weng Z, Miniati A, Vasiadi M, Katsarou-Katsari A, Miao B, Leeman SE, Kalogeromitros D, Theoharides TC. Human mast cell degranulation and preformed TNF secretion require mitochondrial translocation to exocytosis sites: relevance to atopic dermatitis. J Allergy Clin Immunol. 2011;127:1522-1531.e8.
30. Cassidy-Stone A, Chipuk JE, Ingerman E, Song C, Yoo C, Kuwana T, Kurth MJ, Shaw JT, Hinshaw JE, Green DR, Nunnari J. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bakdependent mitochondrial outer membrane permeabilization. Dev Cell. 2008;14:193-204.
31. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y, Bellen HJ. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron. 2005;47: 365-378.
32. Carneiro L, Allard C, Guissard C, Fioramonti X, Tourrel-Cuzin C, Bailbé D, Barreau C, Offer G, Nédelec E, Salin B, Rigoulet M, Belenguer P, Pénicaud L, Leloup C. Importance of mitochondrial dynamin-related protein 1 in hypothalamic glucose sensitivity in rats. Antioxid Redox Signal. 2012;17:433-444.
33. Ong SB, Subrayan S, Lim SY, Yellon DM, Davidson SM, Hausenloy DJ. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation. 2010;121:2012-2022.
34. Brooks C, Wei Q, Cho SG, Dong Z. Regulation of mitochondrial dynamics in acute kidney injury in cell culture and rodent models. J Clin Invest. 2009;119:1275-1285.
35. Park SW, Kim KY, Lindsey JD, Dai Y, Heo H, Nguyen DH, Ellisman MH, Weinreb RN, Ju WK. A selective inhibitor of drp1, mdivi-1, increases retinal ganglion cell survival in acute ischemic mouse retina. Invest Ophthalmol Vis Sci. 2011;52:2837-2843.
36. Vandendries ER, Hamilton JR, Coughlin SR, Furie B, Furie BC. Par4 is required for platelet thrombus propagation but not fibrin generation in a mouse model of thrombosis. Proc Natl Acad Sci USA. 2007;104:288-292.
37. VerPlank L, Dockendorff C, Negri J, Perez JR, Dilks J, MacPherson L, Palmer M, Flaumenhaft R, Schreiber SL. Chemical genetic analysis of platelet granule secretion-probe 2: probe reports from the NIH molecular libraries program. 2011. http://www.ncbi.nlm.nih.gov/books/NBK47352/. Accessed January 9, 2013.
38. Cui M, Tang X, Christian WV, Yoon Y, Tieu K. Perturbations in mitochondrial dynamics induced by human mutant PINK1 can be rescued by the mitochondrial division inhibitor mdivi-1. J Biol Chem. 2010;285:11740-11752.
39. Lackner LL, Nunnari J. Small molecule inhibitors of mitochondrial division: tools that translate basic biological research into medicine. Chem Biol. 2010;17:578-583.
40. Wiederkehr A, Wollheim CB. Mitochondrial signals drive insulin secretion in the pancreatic β-cell. Mol Cell Endocrinol. 2012;353:128-137.
41. Keating DJ. Mitochondrial dysfunction, oxidative stress, regulation of exocytosis and their relevance to neurodegenerative diseases. J Neurochem. 2008;104:298-305.
42. Ye Y, Perez-Polo JR, Birnbaum Y. Protecting against ischemia-reperfusion injury: antiplatelet drugs, statins, and their potential interactions. Ann N Y Acad Sci. 2010;1207:76-82.
43. Hu H, Batteux F, Chéreau C, Kavian N, Marut W, Gobeaux C, Borderie D, Dinh-Xuan AT, Weill B, Nicco C. Clopidogrel protects from cell apoptosis and oxidative damage in a mouse model of renal ischaemiareperfusion injury. J Pathol. 2011;225:265-275.
44. Iwama D, Miyamoto K, Miyahara S, Tamura H, Tsujikawa A, Yamashiro K, Kiryu J, Yoshimura N. Neuroprotective effect of cilostazol against retinal ischemic damage via inhibition of leukocyte-endothelial cell interactions. J Thromb Haemost. 2007;5:818-825.