Munc13-4 is an effector of Rab27a and controls secretion of lysosomes in hematopoietic cells

Molecular Biology of the Cell

Volumn 16, Issue 2, 2005, Pages 731-741

  Neeft, Maaike ^a   Wieffer, Marnix ^a   De Jong, Arjan S ^a   Negroiu, Gabriela ^b   Metz, Corina H G ^a   Van Loon, Alexander ^a   Griffith, Janice ^a   Krijgsveld, Jeroen ^c   Wulffraat, Nico ^a   Koch, Henriette ^d   Heck, Albert J R ^c   Brose, Nils ^d   Kleijmeer, Monique ^a   Van Der Sluijs, Peter ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b INSTITUTE OF BIOCHEMISTRY OF THE ROMANIAN ACADEMY   (Romania)

^c UTRECHT UNIVERSITY   (Netherlands)

^d MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN MUNC13 4; RAB27A PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUSION; CELL MEMBRANE; CELL SECRETION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DEGRANULATION; EXOCYTOSIS; GENE MUTATION; GRISCELLI SYNDROME; HEMATOPOIETIC CELL; HEMOPHAGOCYTIC LYMPHOHISTIOCYTOSIS; HUMAN; HUMAN CELL; LYSOSOME; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RAT; SEQUENCE HOMOLOGY;

EID: 19944430653     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-10-0923     Document Type: Article

References (50)

1. Amraoui, A. E., Schonn, J. S., Andermann, P. K., Blanchard, S., Desnos, C., Henry, J. P., Wulfrum, U., Darchen, F., and Petit, C. (2002). MyRIP, a novel rab effector, enables myosin VIIa recruitment to retinal melanosomes. EMBO Rep. 3, 463-470.
2. Ashery, U., Varoqueaux, F., Voets, T., Betz, A., Betz, A., Thakur, P., Koch, H., Neher, E., Brose, N., and Rettig, J. (2000). Munc13-1 acts as a priming factor for large dense core vesicles in bovine chromaffin cells. EMBO J. 19, 3586-3596.
3. Bahadoran, E. K., Aberdam, E., Mantoux, F., Busca, R., Bille, K., Yalman, N., de Saint-Basili, G., Casaroli-Marano, R., Ortonne, J. P., and Ballotti, R. (2001). Rab27a: a key to melanosome transport in human melanocytes. J. Cell Biol. 102, 843-850.
4. Betz, A., Thakur, P., Junge, H. J., Ashery, U., Rhee, J. S., Scheuss, V., Rosenmund, C., Rettig, J., and Brose, N. (2001). Functional interaction of the active zone proteins Munc 13-1 and RIM1 in synaptic vesicle priming. Neuron 30, 183-196.
5. Blank, U., and Rivera, J. (2004). The ins and outs of IgE-dependent mast-cell exocytosis. Trends Immunol. 25, 266-273.
6. Blott E. J., and Griffiths, G. M. (2002). Secretory lysosomes. Nat. Rev. Mol. Cell. Biol. 3, 122-131.
7. Bonifacino, J. S., Perez, P., Klausner, R. D., and Sandoval, I. V. (1986). Study of the transit of an integral membrane protein from secretory granules through the plasma membrane of secreting basophilic leukemia cells using a specific mAb. J. Cell Biol. 102, 516-522.
8. Bonifacino, J. S., Yuan, L., and Sandoval, I. S. (1999). Internalization and recycling to serotonin-containing granules of the 80k integral membrane protein exposed on the surface of secreting rat basophilic leukemia cells. J. Cell Sci. 92, 701-712.
9. Brose, N., Rosenmund, C., and Rettig, J. (2000). Regulation of transmitter release by Unc-13 and its homologues. Curr. Opin. Neurobiol. 10, 303-311.
10. Chen, D., Lemons, P., Schraw, T., and Whiteheart, S. W. (2000). Molecular mechanisms of platelet exocytosis: role of SNAP-23 and syntaxin 2 and 4 in lysosome release. Blood 96, 1782-1788.
11. Christoforidis, S., McBride, H., Burgoyne, R. D., and Zerial, M. (1999). The rab5 effector EEA1 is a core component of endosome docking. Nature 397, 621-625.
12. Deneka, M., Neeft, M., Popa, I., van Oort, M., Sprong, H., Oorschot, V., Klumperman, J., Schu, P., and van der Sluijs, P. (2003a). rabaptin-5α/ rabaptin-4 serves as a linker between rab4 and γ1-adaptin in membrane recycling from endosomes. EMBO J. 22, 2645-2657.
13. Deneka, M., Neeft, M., and van der Sluijs, P. (2003b). Rab GTPase switch in membrane dynamics. CRC Rev. Biochem. Mol. Biol. 38, 121-142.
14. Desnos, C., et al. (2003). Rab27a and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J. Cell Biol. 163, 559-570.
15. Feldmann, J., 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.
16. Fouraux, M., Deneka, M., Ivan, V., van der Heijden, A., Raymackers, J., van Suylekom, D., van Venrooij, W. J., van der Sluijs, P., and Pruijn, G.J.M. (2003). rabip4′ is an effector of rab5 and rab4 and regulates transport through early endosomes. Mol. Biol. Cell 15, 611-624.
17. Fukuda, M., Kanno, E., and Yamamoto, A. (2004). Rabphilin and Noc2 are recruited to dense core vesicles through specific interaction with rab27a in PC12 cells. J. Biol. Chem. 279, 13065-13075.
18. Goishi, K., Mizuno, K., Nakanashi, H., and Sasaki, T. (2004). Involvement of rab27 in antigen induced histamine release from rat basophilic leukemia 2H3 cells. Biochem. Biophys. Res. Comm. 324, 294-301.
19. Kauppi M., Simonsen, A., Bremnes, B., Vieira, A., Callaghan, J., Stenmark, H., and Olkkonen, V. M. (2002). The small GTPase rab22 interacts with EEA1 and controls endosomal trafficking. J. Cell Sci. 115, 899-911.
20. Kleijmeer, M., et al. (2001). Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J. Cell Biol. 155, 53-64.
21. Koch, H., Hofmann, K., and Brose, N. (2000). Definition of Munc13-homology domains and characterization of a novel ubiquitously expressed Munc13 isoform. Biochem. J. 349, 247-253.
22. Kuroda, T. S., Fukuda, M., Ariga, H., and Mikoshiba, K. (2002). The Slp homology domain of synaptotagmin-like proteins 1-4 and slac2 functions as a novel rab27a binding domain. J. Biol. Chem. 277, 9212-9218.
23. Martion-Verdeaux, S., Ponmbo, I., Iannascoli, B., Roa, M., Varin-Blank, N., Rivera, J., and Blank, U. (2002). Evidence for a role of Munc18-2 and microtubules in mast cell granule exocytosis. J. Cell Sci. 116, 325-334.
24. Menasche, G., Feldmann, J., Houdusse, A., Deaymard, C., Fischer, A., Goud, B., and de Saint Basile, G. (2002). Biochemical and functional characterization of rab27a mutations occurring in Griscelli syndrome patients. Blood 101, 2736-2742.
25. Menasche, G., Ho, C. H., Sanal, O., Feldmann, J., Tezcan, I., Ersoy, F., Houdusse, A., Fischer, A., and de Saint Basile, G. (2003). Griscelli syndrome restricted to hypopigmentation results from a melanophilin defect (GS3) or a MYO5A F-exon deletion (GS1). J. Clin. Invest. 112, 450-456.
26. Menasche, H., Pastural, E., Feldmann, J., Certain, S., Ersoy, F., Dupuis, S., Wulffraat, N., Bianchi, D., Fischer, A., Le Deist, F., and de Saint Basile, G. (2000). Mutations in rab27a cause Griscelli's syndrome associated with haemophagocytic syndrome. Nat. Genet. 25, 173-176.
27. Merithew, E., Hatherly, S., Dumas, J. J., Lawe, D. C., Heller-Harrison, R., and Lambright, D. G. (2001). Structural plasticity of an invariant hydrophobic triad in the switch regions of rab GTPases is a determinant of effector recognition. J. Biol. Chem. 276, 13982-13988.
28. Metcalfe, D. D., Baram, D., and Mekori, Y. A. (1997). Mast cells. Physiol. Rev. 77, 1033-1079.
29. Ostermeier, C., and Brunger, A. T. (1999). Structural basis of rab effector specificity: crystal structure of the small G protein rab3A complexed with the effector domain of rabphilin-3A. Cell 96, 363-374.
30. Pagan, J. K., Wylie, F. G., Joseph, S., Widberg, C., Bryant, N. J., James, D. E., and Stow, J. L. (2003). The t-SNARE syntaxin 4 is regulated during macrophage activation to function in membrane traffic and cytokine secretion. Curr. Biol. 13, 156-160.
31. Pastural, E., Barrat, F., R., D.-L., Certain, S., Sanal, O., Jabado, N., Seger, R., Griscelli, C., Fischer, A., and de Saint Basile, G. (1997). Griscelli disease maps to chromosome 15q21 and is associated with mutations in the myosin-Va gene. Nat. Genet. 16, 289-292.
32. Paumet, F., le Mao, J., Martin, S., Galli, T., David, B., Blank, U., and Roa, M. (2000). Soluble NSF attachment protein receptors (SNAREs) in RBL-2H3 mast cells: functional role of syntaxin 4 in exocytosis and identification of a vesicle-associated membrane protein 8-containing secretory compartment. J. Immunol. 164, 5850-5857.
33. Pereira-Leal, J. B., and Seabra, M. C. (2000). The mammalian rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for fundamental specificity in the ras superfamily. J. Mol. Biol. 301, 1077-1087.
34. Pfeffer, S. (2003). Membrane domains in the secretory and endocytic pathways. Cell 112, 507-517.
35. Puri, N., Kruhlak, M. J., Whiteheart, S. W., and Roche, P. A. (2003). Mast cell degranulation requires NEM-sensitive factor mediated SNARE disassembly. J. Immunol. 171, 5345-5352.
36. Raposo, G., Kleijmeer, M., Posthuma, G., Slot, J. W., and Geuze, H. J. (1997). Immunogold labeling of ultrathin cryosections: application in immunology. In: Weir's Handbook of Experimental Immunology, ed. L. A. Herzenberg, D. M. Weir, and C. Blackwell, Malden, MA: Blackwell Malden, chapter 208, 1-11.
37. Rhee, J. S., et al. (2002). Bovine serum albumin-phorbol ester and diacylglycerol induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108, 121-133.
38. Richmond, J. E., Weimer, R. M., and Jorgensen, E. M. (2001). An open form of syntaxin bypasses the requirement for Unc-13 in vesicle priming. Nature 412, 338-340.
39. Rizo, J., and Sudhof, T. C. (2002). SNAREs an Munc18 in synaptic vesicle fusion. Nat. Rev. Neurosci. 3, 641-653.
40. Rosenmund, C., Sigler, A., Augustin, I., Reim, K., Brose, N., and Rhee, J. S. (2002). Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33, 411-424.
41. Sanal, O., Ersoy, F., Tezcan, I., Metin, A., Yel, L., Menasche, G., Gurgey, A., Berkel, I., and de Saint Basile, G. (2002). Griscelli disease: genotype-phenotype correlation in an array of clinical heterogeneity. J. Clin. Immunol. 22, 237-243.
42. Schlüter, O., Khvotchev, M., Jahn, R., and Südhof, T. C. (2002). Localization versus function of rab3 proteins. J. Biol. Chem. 277, 40919-40929.
43. Schlüter, O. M., Schmitz, F., HJahn, R., Rosenmund, C., and Südhof, T. C. (2004). A complete genetical analysis of neuronal rab3 function. J. Neurosci. 24, 6629-6637.
44. Seabra, M. S., Ho, Y. K., and Anant, J. S. (1995). Deficient geranylgeranylation of ram/rab27 in choroideremia. J. Biol. Chem. 270, 24420-24427.
45. Shirakawa, R., Higashi, T., Tabuchi, A., Yoshioka, A., Nishioka, H., Fukuda, M., Kita, T., and Horiuchi, H. (2004). Munc13-4 is a GTP-rab27 binding protein regulating dense core granule secretion in platelets. J. Biol. Chem. 279, 10730-10737.
46. Tolmachova, T., Anders, R., Stinchcombe, J., Bossi, G., Griffiths, G. M., Huxley, C., and Seabra, M. (2004). A general role for rab27a in secretory cells. Mol. Biol. Cell 15, 332-344.
47. Winzler, C., Rovere, P., Rescigno, M., Granucci, F., Penna, G., Adorini, L., Zimmermann, V. S., Davoust, J., and Ricciardi-Castagnoli, P. (1997). Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J. Exp. Med. 185, 317-328.
48. Wu, X. S., Rao, K., Zhang, H., Sellers, J. R., Matesic, L. E., Copeland, N. G., Jenkins, N. A., and Hammer III, J. A. (2002). Identification of an organelle receptor for myosin Va. Nat. Cell Biol. 4, 1-8.
49. Yamamoto, K., et al. (2004). Identification of novel MUNC13-4 mutations in familial haemophagocytic lymphohistiocytosis and functional analysis of Munc13-4-deficient cytotoxic T lymphocytes. J. Med. Genet. 41, 763-767.
50. Yatsuda, A. P., Krijgsveld, J., Cornelissen, A. W., Heck, A. J., and de Vries, E. (2003). Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. J. Biol. Chem. 278, 16941-16951.