Munc13-4 Is Essential for Cytolytic Granules Fusion and Is Mutated in a Form of Familial Hemophagocytic Lymphohistiocytosis (FHL3)

Cell

Volumn 115, Issue 4, 2003, Pages 461-473

  Feldmann, Jérôme ^a   Callebaut, Isabelle ^b   Raposo, Graça ^c   Certain, Stéphanie ^a   Bacq, Delphine ^d   Dumont, Cécile ^a   Lambert, Nathalie ^a   Ouachée Chardin, Marie ^a   Chedeville, Gaëlle ^a   Tamary, Hannah ^e   Minard Colin, Véronique ^a   Vilmer, Etienne ^f   Blanche, Stéphane ^a   Le Deist, Françoise ^a   Fischer, Alain ^a   De Saint Basile, Geneviève ^a  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b UNIVERSITÉ PIERRE ET MARIE CURIE   (France)

^c CNRS   (France)

^d CENTRE NATIONAL DE GÉNOTYPAGE   (France)

^e Pediatric Hematology Oncology   (Israel)

^f HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MUNC13 4 PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME 17Q; CLINICAL ARTICLE; CYTOLYSIS; EXOCYTOSIS; FAMILIAL DISEASE; FEMALE; GENE LOCUS; GENE MAPPING; HEMOPHAGOCYTIC LYMPHOHISTIOCYTOSIS; HISTIOCYTOSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MEMBRANE BINDING; MEMBRANE FUSION; POLARIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFICIENCY;

EID: 10744224641     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(03)00855-9     Document Type: Article

References (50)

1. Ashery U., Varoqueaux F., Voets T., Betz A., Thakur P., Koch H., Neher E., Brose N., Rettig J. Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. EMBO J. 19:2000;3586-3596.
2. Augustin I., Betz A., Herrmann C., Jo T., Brose N. Differential expression of two novel Munc13 proteins in rat brain. Biochem. J. 337:1999;363-371. a.
3. Augustin I., Rosenmund C., Sudhof T.C., Brose N. Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature. 400:1999;457-461. b.
4. Baetz K., Isaaz S., Griffiths G.M. Loss of cytotoxic T lymphocyte function in Chediak-Higashi syndrome arise from a secretory defect that prevents lytic granule exocytosis. J. Immunol. 154:1995;6122-6131.
5. Betz A., Okamoto M., Benseler F., Brose N. Direct interaction of the rat unc-13 homologue Munc13-1 with the N terminus of syntaxin. J. Biol. Chem. 272:1997;2520-2526.
6. Betz A., Ashery U., Rickmann M., Augustin I., Neher E., Sudhof T.C., Rettig J., Brose N. Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron. 21:1998;123-136.
7. Betz A., Thakur P., Junge H.J., Ashery U., Rhee J.S., Scheuss V., Rosenmund C., Rettig J., Brose N. Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron. 30:2001;183-196.
8. Brose N., Hofmann K., Hata Y., Sudhof T.C. Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J. Biol. Chem. 270:1995;25273-25280.
9. Brose N., Rosenmund C., Rettig J. Regulation of transmitter release by Unc-13 and its homologues. Curr. Opin. Neurobiol. 10:2000;303-311.
10. Callebaut I., Labesse G., Durand P., Poupon A., Canard L., Chomilier J., Henrissat B., Mornon J.P. Deciphering protein sequence information through hydrophobic cluster analysis (HCA). current status and perspectives Cell. Mol. Life Sci. 53:1997;621-645.
11. Cottingham R.W. Jr., Idury R.M., Schaffer A.A. Faster sequential genetic linkage computations. Am. J. Hum. Genet. 53:1993;252-263.
12. de Saint Basile G., Fischer A. The role of cytotoxicity in lymphocyte homeostasis. Curr. Opin. Immunol. 13:2001;549-554.
13. Dufourcq-Lagelouse R., Jabado N., Le Deist F., Stephan J.L., Souillet G., Bruin M., Vilmer E., Schneider M., Janka G., Fischer A., de Saint Basile G. Linkage of familial hemophagocytic lymphohistiocytosis to 10q21-22 and evidence for heterogeneity. Am. J. Hum. Genet. 64:1999;172-179.
14. Dulubova I., Sugita S., Hill S., Hosaka M., Fernandez I., Sudhof T.C., Rizo J. A conformational switch in syntaxin during exocytosis. role of munc18 EMBO J. 18:1999;4372-4382.
15. Fernandez I., Arac D., Ubach J., Gerber S.H., Shin O., Gao Y., Anderson R.G., Sudhof T.C., Rizo J. Three-dimensional structure of the synaptotagmin 1 C2B-domain. synaptotagmin 1 as a phospholipid binding machine Neuron. 32:2001;1057-1069.
16. Fortier A.H., Nacy C.A., Sitkovsky M.V. Similar molecular requirements for antigen receptor-triggered secretion of interferon and granule enzymes by cytolytic T lymphocytes. Cell. Immunol. 124:1989;64-76.
17. Griffiths G.M., Isaaz S. Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose-6-phosphate receptor. J. Cell Biol. 120:1993;885-896.
18. Haddad E.K., Wu X., Hammer J.A., Henkart P.A. Defective granule exocytosis in rab27a-deficient lymphocytes from ashen mice. J. Cell Biol. 152:2001;835-842.
19. Hu C., Ahmed M., Melia T.J., Sollner T.H., Mayer T., Rothman J.E. Fusion of cells by flipped SNAREs. Science. 300:2003;1745-1749.
20. Jahn R., Sudhof T.C. Membrane fusion and exocytosis. Annu. Rev. Biochem. 68:1999;863-911.
21. Jahn R., Lang T., Sudhof T.C. Membrane fusion. Cell. 112:2003;519-533.
22. Jones D.T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292:1999;195-202.
23. Koch H., Hofmann K., Brose N. Definition of Munc13-homology-domains and characterization of a novel ubiquitously expressed Munc13 isoform. Biochem. J. 349:2000;247-253.
24. Kupfer A., Singer S.J. Cell biology of cytotoxic and helper T cell functions. immunofluorescence microscopic studies of single cells and cell couples Annu. Rev. Immunol. 7:1989;309-337.
25. Kupfer H., Monks C.R., Kupfer A. Small splenic B cells that bind to antigen-specific T helper (Th) cells and face the site of cytokine production in the Th cells selectively proliferate. immunofluorescence microscopic studies of Th-B antigen-presenting cell interactions J. Exp. Med. 179:1994;1507-1515.
26. Lin R.C., Scheller R.H. Mechanisms of synaptic vesicle exocytosis. Annu. Rev. Cell Dev. Biol. 16:2000;19-49.
27. Ménasché G., Pastural E., Feldmann J., Certain S., Ersoy F., Dupuis S., Wulffraat N., Bianci D., Fischer A., Le Deist F., de Saint Basile G. Mutations in RAB27A cause Griscelli syndrome associated with hemophagocytic syndrome. Nat. Genet. 25:2000;173-176.
28. Nagle D.L., Karim A.M., Woolf E.A., Holmgren L., Bork P., Misumi D.J., McGrail S.H., Dussault B.J., Perou C.M., Boissy R.E.et al. Identification and mutation analysis of the complete gene for Chediak-Higashi syndrome. Nat. Genet. 14:1996;307-311.
29. Nalefski E.A., Falke J.J. The C2 domain calcium-binding motif. structural and functional diversity Protein Sci. 5:1996;2375-2390.
30. Ohadi M., Lalloz M.R., Sham P., Zhao J., Dearlove A.M., Shiach C., Kinsey S., Rhodes M., Layton D.M. Localization of a gene for familial hemophagocytic lymphohistiocytosis at chromosome 9q21.3-22 by homozygosity mapping. Am. J. Hum. Genet. 64:1999;165-171.
31. Orita S., Naito A., Sakaguchi G., Maeda M., Igarashi H., Sasaki T., Takai Y. Physical and functional interactions of Doc2 and Munc13 in Ca2+-dependent exocytotic machinery. J. Biol. Chem. 272:1997;16081-16084.
32. Perisic O., Fong S., Lynch D.E., Bycroft M., Williams R.L. Crystal structure of a calcium-phospholipid binding domain from cytosolic phospholipase A2. J. Biol. Chem. 273:1998;1596-1604.
33. Peters P.J., Geuze H.J., Van der Donk H.A., Slot J.W., Griffith J.M., Stam N.J., Clevers H.C., Borst J. Molecules relevant for T cell-target cell interaction are present in cytolytic granules of human T lymphocytes. Eur. J. Immunol. 19:1989;1469-1475.
34. Richmond J.E., Weimer R.M., Jorgensen E.M. An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming. Nature. 412:2001;338-341.
35. Rizo J., Sudhof T.C. C2-domains, structure and function of a universal Ca2+-binding domain. J. Biol. Chem. 273:1998;15879-15882.
36. Rizo J., Sudhof T.C. Snares and Munc18 in synaptic vesicle fusion. Nat. Rev. Neurosci. 3:2002;641-653.
37. Rothstein T.L., Mage M., Jones G., McHugh L.L. Cytotoxic T lymphocyte sequential killing of immobilized allogeneic tumor target cells measured by time-lapse microcinematography. J. Immunol. 121:1978;1652-1656.
38. Russell J.H., Ley T.J. Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20:2002;323-370.
39. Sali A., Potterton L., Yuan F., van Vlijmen H., Karplus M. Evaluation of comparative protein modeling by MODELLER. Proteins. 23:1995;318-326.
40. Sassa T., Harada S., Ogawa H., Rand J.B., Maruyama I.N., Hosono R. Regulation of the UNC-18-Caenorhabditis elegans syntaxin complex by UNC-13. J. Neurosci. 19:1999;4772-4777.
41. Shiratsuchi T., Oda K., Nishimori H., Suzuki M., Takahashi E., Tokino T., Nakamura Y. Cloning and characterization of BAP3 (BAI-associated protein 3), a C2 domain-containing protein that interacts with BAI1. Biochem. Biophys. Res. Commun. 251:1998;158-165.
42. Shresta S., Pham C.T., Thomas D.A., Graubert T.A., Ley T.J. How do cytotoxic lymphocytes kill their targets? Curr. Opin. Immunol. 10:1998;581-587.
43. Stepp S., Dufourcq-Lagelouse R., Le Deist F., Bhawan S., Certain S., Mathew P., Henter J., Bennett M., Fischer A., de Saint Basile G., Kumar V. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science. 286:1999;1957-1959.
44. Stinchcombe J.C., Barral D.C., Mules E.H., Booth S., Hume A.N., Machesky L.M., Seabra M.C., Griffiths G.M. Rab27a is required for regulated secretion in cytotoxic t lymphocytes. J. Cell Biol. 152:2001;825-834. a.
45. Stinchcombe J.C., Bossi G., Booth S., Griffiths G.M. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity. 15:2001;751-761. b.
46. Sutton R.B., Ernst J.A., Brunger A.T. Crystal structure of the cytosolic C2A-C2B domains of synaptotagmin III. Implications for Ca(+2)-independent snare complex interaction. J. Cell Biol. 147:1999;589-598.
47. Ubach J., Garcia J., Nittler M.P., Sudhof T.C., Rizo J. Structure of the Janus-faced C2B domain of rabphilin. Nat. Cell Biol. 1:1999;106-112.
48. Vyas Y.M., Maniar H., Dupont B. Visualization of signaling pathways and cortical cytoskeleton in cytolytic and noncytolytic natural killer cell immune synapses. Immunol. Rev. 189:2002;161-178.
49. Weber T., Zemelman B.V., McNew J.A., Westermann B., Gmachl M., Parlati F., Sollner T.H., Rothman J.E. SNAREpins. minimal machinery for membrane fusion Cell. 92:1998;759-772.
50. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2:2001;107-117.