A unique SNARE machinery for exocytosis of cytotoxic granules and platelets granules

Molecular Membrane Biology

Volumn 32, Issue 4, 2015, Pages 120-126

  Tang, Bor Luen ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cytotoxic granules; familial hemophagocytic lymphohistiocytosis; Munc18b; platelet; syntaxin 11

Indexed keywords

MUNC18 PROTEIN; RAB27A PROTEIN; SYNTAXIN; CARRIER PROTEIN; PROTEIN BINDING; SNARE PROTEIN;

CELL GRANULE; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; EXOCYTOSIS; HEMOPHAGOCYTIC SYNDROME; HUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; THROMBOCYTE; THROMBOCYTE RELEASE REACTION; ANIMAL; GENETICS; IMMUNOLOGY; METABOLISM; NATURAL KILLER CELL;

ANIMALS; BLOOD PLATELETS; CARRIER PROTEINS; CYTOPLASMIC GRANULES; EXOCYTOSIS; HUMANS; KILLER CELLS, NATURAL; LYMPHOHISTIOCYTOSIS, HEMOPHAGOCYTIC; MUNC18 PROTEINS; PROTEIN BINDING; QA-SNARE PROTEINS; SNARE PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84945939738     PISSN: 09687688     EISSN: 14645203     Source Type: Journal    
DOI: 10.3109/09687688.2015.1079934     Document Type: Review

References (89)

1. Al Hawas R, Ren Q, Ye S, Karim ZA, Filipovich AH, Whiteheart SW. 2012. Munc18b/STXBP2 is required for platelet secretion. Blood 120: 2493-2500
2. Arneson LN, Brickshawana A, Segovis CM, Schoon RA, Dick CJ, Leibson PJ. 2007. Cutting edge: syntaxin 11 regulates lymphocytemediated secretion and cytotoxicity. J Immunol 179: 3397-3401
3. Benarroch EE. 2013. Synaptic vesicle exocytosis: molecular mechanisms and clinical implications. Neurology 80: 1981-1988
4. Bennett MK, García-Arrarás JE, Elferink LA, Peterson K, Fleming AM, Hazuka CD, Scheller RH. 1993. The syntaxin family of vesicular transport receptors. Cell 74: 863-873
5. Bock JB, Matern HT, Peden AA, Scheller RH. 2001. A genomic perspective on membrane compartment organization. Nature 409: 839-841
6. Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116: 153-166
7. Booth AEG, Seabra MC, Hume AN. 2012. Rab27a and melanosomes: a model to investigate the membrane targeting of Rabs. Biochem Soc Trans 40: 1383-1388
8. Boswell KL, James DJ, Esquibel JM, Bruinsma S, Shirakawa R, Horiuchi H, Martin TFJ. 2012. Munc13-4 reconstitutes calciumdependent SNARE-mediated membrane fusion. J Cell Biol 197: 301-312
9. Bryceson YT, Rudd E, Zheng C, Edner J, Ma D, Wood SM, et al. 2007. Defective cytotoxic lymphocyte degranulation in syntaxin-11 deficient familial hemophagocytic lymphohistiocytosis 4 (FHL4) patients. Blood 110: 1906-1915
10. Cetica V, Pende D, Griffiths GM, Aricò M. 2010. Molecular basis of familial hemophagocytic lymphohistiocytosis. Haematologica 95: 538-541
11. Chandrakasan S, Filipovich AH. 2013. Hemophagocytic lymphohistiocytosis: advances in pathophysiology, diagnosis, and treatment. J Pediatr 163: 1253-1259
12. Chen D, Bernstein AM, Lemons PP, Whiteheart SW. 2000a. Molecular mechanisms of platelet exocytosis: role of SNAP-23 and syntaxin 2 in dense core granule release. Blood 95: 921-929
13. Chen D, Lemons PP, Schraw T, Whiteheart SW. 2000b. Molecular mechanisms of platelet exocytosis: role of SNAP-23 and syntaxin 2 and 4 in lysosome release. Blood 96: 1782-1788
14. Cheviet S, Bezzi P, Ivarsson R, Renström E, Viertl D, Kasas S, et al. 2006. Tomosyn-1 is involved in a post-docking event required for pancreatic beta-cell exocytosis. J Cell Sci 119: 2912-2920
15. Côte M, Ménager MM, Burgess A, Mahlaoui N, Picard C, Schaffner C, et al. 2009. Munc18-2 deficiency causes familial hemophagocytic lymphohistiocytosis type 5 and impairs cytotoxic granule exocytosis in patient NK cells. J Clin Invest 119: 3765-3773
16. De Saint Basile G, Ménasché G, Fischer A. 2010. Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat Rev Immunol 10: 568-579
17. DOrlando O, Zhao F, Kasper B, Orinska Z, Müller J, Hermans-Borgmeyer I, et al. 2013. Syntaxin 11 is required for NK and CD8+T-cell cytotoxicity and neutrophil degranulation. Eur J Immunol 43: 194-208
18. Fasshauer D, Sutton RB, Brunger AT, Jahn R. 1998. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci USA 95: 15781-15786
19. Feldmann J, Callebaut I, Raposo G, Certain S, Bacq D, Dumont C, et al. 2003. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 115: 461-473
20. Ferro-Novick S, Brose N. 2013. Nobel 2013 Physiology or medicine: traffic control system within cells. Nature 504: 98
21. Fukuda M. 2002. The C2A domain of synaptotagmin-like protein 3 (Slp3) is an atypical calcium-dependent phospholipid-binding machine: comparison with the C2A domain of synaptotagmin I. Biochem J 366: 681-687
22. Gholam C, Grigoriadou S, Gilmour KC, Gaspar HB. 2011. Familial haemophagocytic lymphohistiocytosis: advances in the genetic basis, diagnosis and management. Clin Exp Immunol 163: 271-283
23. Golebiewska EM, Harper MT, Williams CM, Savage JS, Goggs R, Fischer von Mollard G, Poole AW. 2015. Syntaxin 8 regulates platelet dense granule secretion, aggregation, and thrombus stability. J Biol Chem 290: 1536-1545
24. Golebiewska EM, Poole AW. 2015. Platelet secretion: from haemostasis to wound healing and beyond. Blood Rev 29: 153-162
25. Hackmann Y, Graham SC, Ehl S, Höning S, Lehmberg K, Aricò M, et al. 2013. Syntaxin binding mechanism and disease-causing mutations in Munc18-2. Proc Natl Acad Sci USA 110: E4482-4491
26. Haddad EK, Wu X, Hammer JA, Henkart PA. 2001. Defective granule exocytosis in Rab27a-deficient lymphocytes from Ashen mice. J Cell Biol 152: 835-842
27. Halimani M, Pattu V, Marshall MR, Chang HF, Matti U, Jung M, et al. 2014. Syntaxin11 serves as a t-SNARE for the fusion of lytic granules in human cytotoxic T lymphocytes. Eur J Immunol 44: 573-584
28. Hellewell AL, Foresti O, Gover N, Porter MY, Hewitt EW. 2014. Analysis of familial hemophagocytic lymphohistiocytosis type 4 (FHL-4) mutant proteins reveals that S-acylation is required for the function of syntaxin 11 in natural killer cells. PLoS One 9: e98900
29. Hepp R, Puri N, Hohenstein AC, Crawford GL, Whiteheart SW, Roche PA. 2005. Phosphorylation of SNAP-23 regulates exocytosis from mast cells. J Biol Chem 280: 6610-6620
30. Hong W. 2005. Cytotoxic T lymphocyte exocytosis: bring on the SNAREs!. Trends Cell Biol 15: 644-650
31. Houng A, Polgar J, Reed GL. 2003. Munc18-syntaxin complexes and exocytosis in human platelets. J Biol Chem 278: 19627-19633
32. Hume AN, Seabra MC. 2011. Melanosomes on the move: a model to understand organelle dynamics. Biochem Soc Trans 39: 1191-1196
33. Iinuma T, Aoki T, Arasaki K, Hirose H, Yamamoto A, Samata R, et al. 2009. Role of syntaxin 18 in the organization of endoplasmic reticulum subdomains. J Cell Sci 122: 1680-1690
34. Johnson JL, Brzezinska AA, Tolmachova T, Munafo DB, Ellis BA, Seabra MC, et al. 2010. Rab27a and Rab27b regulate neutrophil azurophilic granule exocytosis and NADPH oxidase activity by independent mechanisms. Traffic 11: 533-547
35. Kasai H, Takahashi N, Tokumaru H. 2012. Distinct initial SNARE configurations underlying the diversity of exocytosis. Physiol Rev 92: 1915-1964
36. Kimura T, Kaneko Y, Yamada S, Ishihara H, Senda T, Iwamatsu A, Niki I. 2008. The GDP-dependent Rab27a effector coronin 3 controls endocytosis of secretory membrane in insulin-secreting cell lines. J Cell Sci 121: 3092-3098
37. Kurowska M, Goudin N, Nehme NT, Court M, Garin J, Fischer A, et al. 2012. Terminal transport of lytic granules to the immune synapse is mediated by the kinesin-1/Slp3/Rab27a complex. Blood 119: 3879-3889
38. Lemons PP, Chen D, Bernstein AM, Bennett MK, Whiteheart SW. 1997. Regulated secretion in platelets: identification of elements of the platelet exocytosis machinery. Blood 90: 1490-1500
39. Lemons PP, Chen D, Whiteheart SW. 2000. Molecular mechanisms of platelet exocytosis: requirements for alpha-granule release. Biochem Biophys Res Commun 267: 875-880
40. Low SH, Miura M, Roche PA, Valdez AC, Mostov KE, Weimbs T. 2000. Intracellular redirection of plasma membrane trafficking after loss of epithelial cell polarity. Mol Biol Cell 11: 3045-3060
41. Marshall MR, Pattu V, Halimani M, Maier-Peuschel M, Müller ML, Becherer U, et al. 2015. VAMP8-dependent fusion of recycling endosomes with the plasma membrane facilitates T lymphocyte cytotoxicity. J Cell Biol 210: 135-151
42. Martín-Martín B, Nabokina SM, Blasi J, Lazo PA, Mollinedo F. 2000. Involvement of SNAP-23 and syntaxin 6 in human neutrophil exocytosis. Blood 96: 2574-2583
43. McNew JA, Parlati F, Fukuda R, Johnston RJ, Paz K, Paumet F, et al. 2000. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407: 153-159
44. Mehta RS, Smith RE. 2013. Hemophagocytic lymphohistiocytosis (HLH): a review of literature. Med Oncol 30: 740
45. Mellman I, Emr SD. 2013. A Nobel Prize for membrane traffic: vesicles find their journeys end. J Cell Biol 203: 559-561
46. Ménasché G, Pastural E, Feldmann J, Certain S, Ersoy F, Dupuis S, et al. 2000. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat Genet 25: 173-176
47. Messenger SW, Falkowski MA, Groblewski GE. 2014. Ca2+-regulated secretory granule exocytosis in pancreatic and parotid acinar cells. Cell Calcium 55: 369-375
48. Mizuno K, Tolmachova T, Ushakov DS, Romao M, Abrink M, Ferenczi MA, et al. 2007. Rab27b regulates mast cell granule dynamics and secretion. Traffic 8: 883-892
49. Mollinedo F, Calafat J, Janssen H, Martín-Martín B, Canchado J, Nabokina SM, Gajate C. 2006. Combinatorial SNARE complexes modulate the secretion of cytoplasmic granules in human neutrophils. J Immunol 177: 2831-2841
50. Müller ML, Chiang SCC, Meeths M, Tesi B, Entesarian M, Nilsson D, Wood SM, Nordenskjöld M, Henter JI, Naqvi A, Bryceson YT. 2014. An N-Terminal missense mutation in STX11 causative of FHL4 abrogates syntaxin-11 binding to Munc18-2. Front Immunol 4: 515
51. Naegelen I, Plançon S, Nicot N, Kaoma T, Muller A, Vallar L, Tschirhart EJ, Bréchard S. 2015. An essential role of syntaxin 3 protein for granule exocytosis and secretion of IL-1a, IL-1b, IL-12b, and CCL4 from differentiated HL-60 cells. J Leukoc Biol 97: 557-571
52. Neeft M, Wieffer M, De Jong AS, Negroiu G, Metz CHG, Van Loon A, et al. 2005. Munc13-4 is an effector of rab27a and controls secretion of lysosomes in hematopoietic cells. Mol Biol Cell 16: 731-741
53. Nichols BJ, Pelham HR. 1998. SNAREs and membrane fusion in the Golgi apparatus. Biochim Biophys Acta 1404: 9-31
54. Offenhäuser C, Lei N, Roy S, Collins BM, Stow JL, Murray RZ. 2011. Syntaxin 11 binds Vti1b and regulates late endosome to lysosome fusion in macrophages. Traffic 12: 762-773
55. Pattu V, Qu B, Marshall M, Becherer U, Junker C, Matti U, et al. 2011. Syntaxin7 is required for lytic granule release from cytotoxic T lymphocytes. Traffic 12: 890-901
56. Pattu V, Qu B, Schwarz EC, Strauss B, Weins L, Bhat SS, et al. 2012. SNARE protein expression and localization in human cytotoxic T lymphocytes. Eur J Immunol 42: 470-475
57. Pfeffer SR. 2013. A prize for membrane magic. Cell 155: 1203-1206
58. Polgár J, Chung SH, Reed GL. 2002. Vesicle-associated membrane protein 3 (VAMP-3) and VAMP-8 are present in human platelets and are required for granule secretion. Blood 100: 1081-1083
59. Prekeris R, Klumperman J, Scheller RH. 2000. Syntaxin 11 is an atypical SNARE abundant in the immune system. Eur J Cell Biol 79: 771-780
60. Prekeris R, Yang B, Oorschot V, Klumperman J, Scheller RH. 1999. Differential roles of syntaxin 7 and syntaxin 8 in endosomal trafficking. Mol Biol Cell 10: 3891-3908
61. Reed GL, Houng AK, Fitzgerald ML. 1999. Human platelets contain SNARE proteins and a Sec1p homologue that interacts with syntaxin 4 and is phosphorylated after thrombin activation: implications for platelet secretion. Blood 93: 2617-2626
62. Schraw TD, Lemons PP, Dean WL, Whiteheart SW. 2003. A role for Sec1/Munc18 proteins in platelet exocytosis. Biochem J 374: 207-217
63. Sieni E, Cetica V, Mastrodicasa E, Pende D, Moretta L, Griffiths G, Aricò M. 2012. Familial hemophagocytic lymphohistiocytosis: a model for understanding the human machinery of cellular cytotoxicity. Cell Mol Life Sci 69: 29-40
64. Simonsen A, Bremnes B, Rønning E, Aasland R, Stenmark H. 1998. Syntaxin-16, a putative Golgi t-SNARE. Eur J Cell Biol 75: 223-231
65. Spessott WA, Sanmillan ML, McCormick ME, Patel N, Villanueva J, Zhang K, et al. 2015. Hemophagocytic lymphohistiocytosis caused by dominant-negative mutations in STXBP2 that inhibit SNAREmediated membrane fusion. Blood 125: 1566-1577
66. Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513-525
67. Stepp SE, Dufourcq-Lagelouse R, Le Deist F, Bhawan S, Certain S, Mathew PA, et al. 1999. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science 286: 1957-1959
68. Sudhof TC. 2004. The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547
69. Südhof TC, Rizo J. 2011. Synaptic vesicle exocytosis. Cold Spring Harbor Perspect Biol 3: a005637
70. Südhof TC, Rothman JE. 2009. Membrane fusion: grappling with SNARE and SM proteins. Science 323: 474-477
71. Suh YH, Yoshimoto-Furusawa A, Weih KA, Tessarollo L, Roche KW, Mackem S, Roche PA. 2011. Deletion of SNAP-23 results in preimplantation embryonic lethality in mice. PLoS One 6: e18444
72. Tang BL, Low DY, Hong W. 1998a. Syntaxin 11: a member of the syntaxin family without a carboxyl terminal transmembrane domain. Biochem Biophys Res Commun 245: 627-632
73. Tang BL, Low DY, Lee SS, Tan AE, Hong W. 1998b. Molecular cloning and localization of human syntaxin 16, a member of the syntaxin family of SNARE proteins. Biochem Biophys Res Commun 242: 673-679
74. Teng FY, Wang Y, Tang BL. 2001. The syntaxins. Genome Biol 2: REVIEWS3012
75. Tolmachova T, Abrink M, Futter CE, Authi KS, Seabra MC. 2007. Rab27b regulates number and secretion of platelet dense granules. Proc Natl Acad Sci USA 104: 5872-5877
76. Tomas A, Meda P, Regazzi R, Pessin JE, Halban PA. 2008. Munc 18-1 and granuphilin collaborate during insulin granule exocytosis. Traffic 9: 813-832
77. Valdez AC, Cabaniols JP, Brown MJ, Roche PA. 1999. Syntaxin 11 is associated with SNAP-23 on late endosomes and the trans-Golgi network. J Cell Sci 112(Pt 6): 845-854
78. Voskoboinik I, Whisstock JC, Trapani JA. 2015. Perforin and granzymes: function, dysfunction and human pathology. Nat Rev Immunol 15: 388-400
79. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, et al. 1998. SNAREpins: minimal machinery for membrane fusion. Cell 92: 759-772
80. Williams AL, Bielopolski N, Meroz D, Lam AD, Passmore DR, Ben-Tal N, et al. 2011. Structural and functional analysis of tomosyn identifies domains important in exocytotic regulation. J Biol Chem 286: 14542-14553
81. Xie LX, De la Iglesia-Vicente J, Fang YX, Mollinedo F. 2009. Expression and subcellular localization of syntaxin 11 in human neutrophils. Inflamm Res 58: 407-412
82. Ye S, Huang Y, Joshi S, Zhang J, Yang F, Zhang G, et al. 2014. Platelet secretion and hemostasis require syntaxin-binding protein STXBP5. J Clin Invest 124: 4517-4528
83. Ye S, Karim ZA, Al Hawas R, Pessin JE, Filipovich AH, Whiteheart SW. 2012. Syntaxin-11, but not syntaxin-2 or syntaxin-4, is required for platelet secretion. Blood 120: 2484-2492
84. Yokosuka T, Saito T. 2010. The immunological synapse, TCR microclusters, and T cell activation. Curr Top Microbiol Immunol 340: 81-107
85. Yu H, Rathore SS, Lopez JA, Davis EM, James DE, Martin JL, Shen J. 2013. Comparative studies of Munc18c and Munc18-1 reveal conserved and divergent mechanisms of Sec1/Munc18 proteins. Proc Natl Acad Sci USA 110: E3271-3280
86. Zhang K, Jordan MB, Marsh RA, Johnson JA, Kissell D, Meller J, et al. 2011. Hypomorphic mutations in PRF1, MUNC13-4, and STXBP2 are associated with adult-onset familial HLH. Blood 118: 5794-5798
87. Zhao XW, Gazendam RP, Drewniak A, Van Houdt M, Tool ATJ, Van Hamme JL, et al. 2013. Defects in neutrophil granule mobilization and bactericidal activity in familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) syndrome caused by STXBP2/Munc18-2 mutations. Blood 122: 109-111
88. Zhu Q, Yamakuchi M, Ture S, De la Luz Garcia-Hernandez M, Ko KA, Modjeski KL, et al. 2014. Syntaxin-binding protein STXBP5 inhibits endothelial exocytosis and promotes platelet secretion. J Clin Invest 124: 4503-4516
89. Zur Stadt U, Rohr J, Seifert W, Koch F, Grieve S, Pagel J, et al. 2009. Familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11. Am J Hum Genet 85: 482-492