A newly identified isoform of Slp2a associates with Rab27a in cytotoxic T cells and participates to cytotoxic granule secretion

Blood

Volumn 112, Issue 13, 2008, Pages 5052-5062

  Ménasché, Gaël ^a,b   Ménager, Mickaël M ^a,b   Lefebvre, Juliette M ^a,b   Deutsch, Einat ^a,b   Athman, Rafika ^a,b   Lambert, Nathalie ^c   Mahlaoui, Nizar ^c   Court, Magali ^a,d,e   Garin, Jérôme ^a,d,e   Fischer, Alain ^a,b,c   De Saint Basile, Geneviève ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d CEA GRENOBLE   (France)

^e UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RAB27A PROTEIN; SLP2A; SYNAPTOTAGMIN; UNCLASSIFIED DRUG; ISOPROTEIN; MEMBRANE PROTEIN; RAB PROTEIN; RAB27A PROTEIN, HUMAN; SYTL2 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CELL GRANULE; CELL MATURATION; CELL SECRETION; CYTOTOXIC T LYMPHOCYTE; EXOCYTOSIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INFECTION CONTROL; MASS SPECTROMETRY; NATURAL KILLER CELL; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SYNAPTIC MEMBRANE; TARGET CELL; IMMUNOLOGICAL SYNAPSE; IMMUNOLOGY; METABOLISM; PROTEIN TRANSPORT; SECRETION; SECRETORY VESICLE;

EXOCYTOSIS; IMMUNOLOGICAL SYNAPSES; MEMBRANE PROTEINS; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SECRETORY VESICLES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 58149388232     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-02-141069     Document Type: Article

References (51)

1. Voskoboinik I, Smyth MJ, Trapani JA. Perforin-mediated target-cell death and immune ho-meostasis. Nat Rev Immunol. 2006;6:940-952.
2. Russell JH, Ley TJ. Lymphocyte-mediated cyto-toxicity. Annu Rev Immunol. 2002;20:323-370.
3. Shresta S, Pham CT, Thomas DA, Graubert TA, Ley TJ. How do cytotoxic lymphocytes kill their targets? Curr Opin Immunol. 1998;10:581-587.
4. Stinchcombe JC, Bossi G, Booth S, Griffiths GM. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity. 2001;15:751-761.
5. Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM. Centrosome polarization delivers secretory granules to the immunological synapse. Nature. 2006;443:462-465.
6. Kuhn JR, Poenie M. Dynamic polarization of the microtubule cytoskeleton during CTL-mediated killing. Immunity. 2002;16:111-121.
7. Ménager MM, Menasche G, Romao M, et al. Secretory cytotoxic granule maturation and exocyto-sis require the effector protein hMunc13-4. Nat Immunol. 2007;8:257-267.
8. de Saint Basile G, Fischer A. The role of cytotox-icity in lymphocyte homeostasis. Curr Opin Immunol. 2001;13:549-554.
9. Ménasché G, Feldmann J, Fischer A, de Saint Basile G. Primary hemophagocytic syndromes point to a direct link between lymphocyte cytotox-icity and homeostasis. Immunol Rev. 2005;203: 165-179.
10. Ménasché G, Pastural E, Feldmann J, et al. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat Genet. 2000;25:173-176.
11. Wilson SM, Yip R, Swing DA, et al. A mutation in Rab27a causes the vesicle transport defects observed in ashen mice. Proc Natl Acad Sci U SA. 2000;97:7933-7938.
12. Martinez O, Goud B. Rab proteins. Biochim Bio-phys Acta. 1998;1404:101-112.
13. Takai Y, Sasaki T, Matozaki T. Small GTP-binding proteins. Physiol Rev. 2001;81:153-208.
14. Haddad EK, Wu X, Hammer JAIII, Henkart PA. Defective granule exocytosis in Rab27a-deficient lymphocytes from Ashen mice. J Cell Biol. 2001;152:835-842.
15. Stinchcombe JC, Barral DC, Mules EH, et al. Rab27a is required for regulated secretion in cy-totoxic T lymphocytes. J Cell Biol. 2001;152:825-834.
16. Feldmann J, Callebaut I, Raposo G, et al. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophago-cytic lymphohistiocytosis (FHL3). Cell. 2003;115: 461-473.
17. Crozat K, Hoebe K, Ugolini S, et al. Jinx, an MCMV susceptibility phenotype caused by disruption of Unc13d: a mouse model of type 3 familial hemophagocytic lymphohistiocytosis. J Exp Med. 2007;204:853-863.
18. Shirakawa R, Higashi T, Tabuchi A, et al. Munc13-4 is a GTP-Rab27-binding protein regulating dense core granule secretion in platelets. J Biol Chem. 2004;279:10730-10737.
19. Basu J, Shen N, Dulubova I, et al. A minimal domain responsible for Munc13 activity. Nat Struct Mol Biol. 2005;12:1017-1018.
20. Kuroda TS, Fukuda M, Ariga H, Mikoshiba K. The Slp homology domain of synaptotagmin-like proteins 1-4 and Slac2 functions as a novel Rab27A binding domain. J Biol Chem. 2002;277:9212-9218.
21. Fukuda M, Saegusa C, Mikoshiba K. Novel splicing isoforms of synaptotagmin-like proteins 2 and 3: identification of the Slp homology domain. Biochem Biophys Res Commun. 2001;283:513-519.
22. Wang J, Takeuchi T, Yokota H, Izumi T. Novel rab-philin-3-like protein associates with insulin-containing granules in pancreatic beta cells. J Biol Chem. 1999;274:28542-28548.
23. McAdara Berkowitz JK, Catz SD, Johnson JL, Ruedi JM, Thon V, Babior BM. JFC1, a novel tandem C2 domain-containing protein associated with the leukocyte NADPH oxidase. J Biol Chem. 2001;276:18855-18862.
24. Cheviet S, Coppola T, Haynes LP, Burgoyne RD, Regazzi R. The Rab-binding protein Noc2 is associated with insulin-containing secretory granules and is essential for pancreatic betacell exocytosis. Mol Endocrinol. 2004;18:117-126.
25. Fukuda M, Kanno E, Yamamoto A. Rabphilin and Noc2 are recruited to dense-core vesicles through specific interaction with Rab27A in PC12 cells. J Biol Chem. 2004;279:13065-13075.
26. Yi Z, Yokota H, Torii S, et al. The Rab27a/ granuphilin complex regulates the exocytosis of insulin-containing dense-core granules. Mol Cell Biol. 2002;22:1858-1867.
27. Torii S, Zhao S, Yi Z, Takeuchi T, Izumi T. Granuphilin modulates the exocytosis of secretory granules through interaction with syntaxin 1a. Mol Cell Biol. 2002;22:5518-5526.
28. Waselle L, CoppolaT, Fukuda M, et al. Involvement of the Rab27 binding protein Slac2c/MyRIP in insulin exocytosis. Mol Biol Cell. 2003;14:4103-4113.
29. Desnos C, Schonn JS, Huet S, et al. Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J Cell Biol. 2003;163:559-570.
30. Wu XS, Rao K, Zhang H, et al. Identification of an organelle receptor for myosin-Va. Nat Cell Biol. 2002;4:271-278.
31. Matesic LE, Yip R, Reuss AE, et al. Mutations in Mlph, encoding a member of the Rab effector family, cause the melanosome transport defects observed in leaden mice. Proc Natl Acad Sci USA. 2001;98:10238-10243.
32. KurodaTS, Fukuda M. Rab27A-binding protein Slp2-a is required for peripheral melanosome distribution and elongated cell shape in melanocytes. Nat Cell Biol. 2004;6:1195-1203.
33. SaegusaC, TanakaT, Tani S, ItoharaS, MikoshibaK, Fukuda M. Decreased basal mucus secretion by Slp2-a-deficient gastric surface mucous cells. Genes Cells. 2006;11:623-631.
34. Yu M, Kasai K, NagashimaK, et al. Exophilin4/ Slp2-a targets glucagon granules to the plasma membrane through unique Ca2+-inhibitory phospholipid-binding activity of the C2A domain. Mol Biol Cell. 2007;18:688-696.
35. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, Seraphin B. Ageneric protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol. 1999;17: 1030-1032.
36. Puig O, Caspary F, Rigaut G, et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods. 2001;24:218-229.
37. Menasche G, Feldmann J, Houdusse A, et al. Biochemical and functional characterization of Rab27a mutations occurring in Griscelli syndrome patients. Blood. 2003;101:2736-2742.
38. Wellcome Trust Sanger. Ensembl. http://www.ensembl.org. Accessed March 2005.
39. National Center for Biotechnology Information. GenBank. http://www.ncbi.nlm.nih.gov/Genbank. Accessed July 2007.
40. Ferro M, Seigneurin-Berny D, Rolland N, et al. Organic solvent extraction as a versatile procedure to identify hydrophobic chloroplast membrane proteins. Electrophoresis. 2000;21:3517-3526.
41. European Bioinformatics Institute. UniProtKB/ Swiss-Prot. http://www.ebi.ac.uk/swissprot. Accessed June 2003.
42. European Bioinformatics Institute. TrEMBL. http://www.ebi.ac.uk/trembl. Accessed June 2003.
43. Manders EM, Hoebe R, Strackee J, Vossepoel AM, Aten JA. Largest contour segmentation: a tool for the localization of spots in confocal images. Cytometry. 1996;23:15-21.
44. Fukuda M, Itoh T. Slac2-a/melanophilin contains multiple PEST-like sequences that are highly sensitive to proteolysis. J Biol Chem. 2004;279: 22314-22321.
45. Holt O, Kanno E, Bossi G, et al. Slp1 and Slp2-a localize to the plasma membrane of CTL and contribute to secretion from the immunological synapse. Traffic. 2008;9:446-457.
46. El-AmraouiA, Schonn JS, Kussel-Andermann P, et al. MyRIP, a novel Rab effector, enables myosin VIIa recruitment to retinal melanosomes. EMBO Rep. 2002;3:463-470.
47. Izumi T, Gomi H, Kasai K, Mizutani S, Torii S. The roles of Rab27 and its effectors in the regulated secretory pathways. Cell Struct Funct. 2003;28: 465-474.
48. Tsuboi T, Fukuda M. The Slp4-a linker domain controls exocytosis through interaction with Munc18-1.syntaxin-1a complex. Mol Biol Cell. 2006;17:2101-2112.
49. Gomi H, Mizutani S, Kasai K, Itohara S, Izumi T. Granuphilin molecularly docks insulin granules to the fusion machinery. J Cell Biol. 2005;171:99-109.
50. Tsuboi T, Fukuda M. The C2B domain of rabphi-lin directly interacts with SNAP-25 and regulates the docking step of dense core vesicle exocytosis in PC12 cells. J Biol Chem. 2005;280:39253-39259.
51. Tang F, Kauffman EJ, Novak JL, Nau JJ, Catlett NL, Weisman LS. Regulated degradation of a class V myosin receptor directs movement of the yeast vacuole. Nature. 2003;422: 87-92.