Munc13-4 Is a Rab11-binding protein that regulates Rab11-positive vesicle trafficking and docking at the plasma membrane

Journal of Biological Chemistry

Volumn 291, Issue 7, 2016, Pages 3423-3438

  Johnson, Jennifer L ^a   He, Jing ^a   Ramadass, Mahalakshmi ^a   Pestonjamasp, Kersi ^b   Kiosses, William B ^c   Zhang, Jinzhong ^a   Catz, Sergio D ^a  

^a Light Microscopy Core Facility   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINS; CELL MEMBRANES; ENERGY TRANSFER; FLUORESCENCE; MOLECULAR BIOLOGY; MOLECULES;

HEMATOPOIETIC CELL; IMMUNOPRECIPITATION ANALYSIS; RECYCLING ENDOSOMES; SINGLE MOLECULE LEVEL; SPATIOTEMPORAL DISTRIBUTIONS; SUPER-RESOLUTION MICROSCOPY; TIME-RESOLVED FLUORESCENCE; VESICLE TRAFFICKING;

MEMBRANES;

BINDING PROTEIN; MUNC13 4 PROTEIN; RAB11 PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; RAB PROTEIN; RECOMBINANT PROTEIN; UNC13D PROTEIN, HUMAN; UNC13D PROTEIN, MOUSE;

ARTICLE; CELL MEMBRANE; CELL MIGRATION; CORRELATIONAL STUDY; ENDOCYTOSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOPRECIPITATION; INFLAMMATION; INVESTIGATIVE PROCEDURES; MEMBRANE VESICLE; MOLECULAR DOCKING; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SPATIOTEMPORAL ANALYSIS; SUPER RESOLUTION MICROSCOPY; TIME RESOLVED FLUORESCENCE RESONANCE ENERGY TRANSFER; UPREGULATION; VESICULAR DYNAMIC ANALYSIS; AMINO ACID SUBSTITUTION; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CHEMISTRY; CYTOLOGY; ENDOSOME; EXOCYTOSIS; GENETICS; GERMFREE ANIMAL; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; POINT MUTATION; SECRETION (PROCESS);

AMINO ACID SUBSTITUTION; ANIMALS; BONE MARROW CELLS; ENDOCYTOSIS; ENDOSOMES; EXOCYTOSIS; HEK293 CELLS; HUMANS; MALE; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; PEPTIDE FRAGMENTS; POINT MUTATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RAB GTP-BINDING PROTEINS; RECOMBINANT PROTEINS; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 84963604496     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.705871     Document Type: Article

References (45)

1. Pfeffer, S. R. (2001) Rab GTPases: specifying and deciphering organelle identity and function. Trends Cell Biol. 11, 487-491.
2. Kelly, E. E., Horgan, C. P., and McCaffrey, M. W. (2012) Rab11 proteins in health and disease. Biochem. Soc. Trans. 40, 1360-1367.
3. Takahashi, S., Kubo, K., Waguri, S., Yabashi, A., Shin, H. W., Katoh, Y., and Nakayama, K. (2012) Rab11 regulates exocytosis of recycling vesicles at the plasma membrane. J. Cell Sci. 125, 4049-4057.
4. Cox, D., Lee, D. J., Dale, B. M., Calafat, J., and Greenberg, S. (2000) A Rab11-containing rapidly recycling compartment in macrophages that promotes phagocytosis. Proc. Natl. Acad. Sci. U.S.A. 97, 680-685.
5. Ramel, D., Wang, X., Laflamme, C., Montell, D. J., and Emery, G. (2013) Rab11 regulates cell-cell communication during collective cell movements. Nat. Cell Biol. 15, 317-324.
6. Horgan, C. P., and McCaffrey, M. W. (2009) The dynamic Rab11-FIPs. Biochem. Soc. Trans. 37, 1032-1036.
7. 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.
8. Boswell, K. L., James, D. J., Esquibel, J. M., Bruinsma, S., Shirakawa, R., Horiuchi, H., and Martin, T. F. (2012) Munc13-4 reconstitutes calciumdependent SNARE-mediated membrane fusion. J. Cell Biol. 197, 301-312.
9. Feldmann, J., Callebaut, I., Raposo, G., Certain, S., Bacq, D., Dumont, C., Lambert, N., Ouachée-Chardin, M., Chedeville, G., Tamary, H., Minard- Colin, V., Vilmer, E., Blanche, S., Le Deist, F., Fischer, A., and de Saint Basile, G. (2003) Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 115, 461-473.
10. Meéager, M. M., Ménasché, G., Romao, M., Knapnougel, P., Ho, C. H., Garfa, M., Raposo, G., Feldmann, J., Fischer, A., and de Saint Basile, G. (2007) Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol. 8, 257-267.
11. Brzezinska, A. A., Johnson, J. L., Munafo, D. B., Crozat, K., Beutler, B., Kiosses, W. B., Ellis, B. A., and Catz, S. D. (2008) The Rab27a Effectors JFC1/Slp1 and Munc13-4 Regulate Exocytosis of Neutrophil Granules. Traffic 9, 2151-2164.
12. Johnson, J. L., Hong, H., Monfregola, J., Kiosses, W. B., and Catz, S. D. (2011) MUNC13-4 restricts motility of RAB27A-expressing vesicles to facilitate lipopolysaccharide-induced priming of exocytosis in neutrophils. J. Biol. Chem. 286, 5647-5656.
13. 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.
14. Neeft, M., Wieffer, M., de Jong, A. S., Negroiu, G., Metz, C. H., van Loon, A., Griffith, J., Krijgsveld, J., Wulffraat, N., Koch, H., Heck, A. J., Brose, N., Kleijmeer, M., and van der Sluijs, P. (2005) Munc13-4 is an effector of rab27a and controls secretion of lysosomes in hematopoietic cells. Mol. Biol. Cell 16, 731-741.
15. Monfregola, J., Johnson, J. L., Meijler, M. M., Napolitano, G., and Catz, S. D. (2012) MUNC13-4 protein regulates the oxidative response and is essential for phagosomal maturation and bacterial killing in neutrophils. J. Biol. Chem. 287, 44603-44618.
16. Wood, S. M., Meeths, M., Chiang, S. C., Bechensteen, A. G., Boelens, J. J., Heilmann, C., Horiuchi, H., Rosthøj, S., Rutynowska, O., Winiarski, J., Stow, J. L., Nordenskjöld, M., Henter, J. I., Ljunggren, H. G., and Bryceson, Y. T. (2009) Different NK cell-activating receptors preferentially recruit Rab27a or Munc13-4 to perforin-containing granules for cytotoxicity. Blood 114, 4117-4127.
17. Lindsay, A. J., and McCaffrey, M. W. (2004) The C2 domains of the class I Rab11 family of interacting proteins target recycling vesicles to the plasma membrane. J. Cell Sci. 117, 4365-4375.
18. Crozat, K., Hoebe, K., Ugolini, S., Hong, N. A., Janssen, E., Rutschmann, S., Mudd, S., Sovath, S., Vivier, E., and Beutler, B. (2007) Jinx, an MCMV susceptibility phenotype caused by disruption of Unc13d: A mouse model of type 3 familial hemophagocytic lymphohistiocytosis. J. Exp. Med. 204, 853-863.
19. Klempner, M. S., Mikkelsen, R. B., Corfman, D. H., and André-Schwartz, J. (1980) Neutrophil plasma membranes. I. High-yield purification of human neutrophil plasma membrane vesicles by nitrogen cavitation and differential centrifugation. J. Cell Biol. 86, 21-28.
20. Johnson, J. L., Pacquelet, S., Lane, W. S., Eam, B., and Catz, S. D. (2005) Akt regulates the subcellular localization of the Rab27a-binding protein JFC1 by phosphorylation. Traffic 6, 667-681.
21. Johnson, J. L., Monfregola, J., Napolitano, G., Kiosses, W. B., and Catz, S. D. (2012) Vesicular trafficking through cortical actin during exocytosis is regulated by the Rab27a effector JFC1/Slp1 and the RhoA-GTPaseactivating protein Gem-interacting protein. Mol. Biol. Cell 23, 1902-1916.
22. Napolitano, G., Johnson, J. L., He, J., Rocca, C. J., Monfregola, J., Pestonjamasp, K., Cherqui, S., and Catz, S. D. (2015) Impairment of chaperonemediated autophagy leads to selective lysosomal degradation defects in the lysosomal storage disease cystinosis. EMBO Mol. Med. 7, 158-174.
23. Rust, M. J., Bates, M., and Zhuang, X. (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nature Methods 3, 793-795.
24. Huang, B., Wang, W., Bates, M., and Zhuang, X. (2008) Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319, 810-813.
25. Xu, K. S., Sang-Hee; Zhuang, Xiaowei (2013) Super-Resolution Imaging Through Stochastic Switching and Localization of Single Molecules: An overview. in Far-field Optical Nanoscopy (Tinnefeld, P., Eggeling, C., and Hell, S. W., eds), pp. 27-64, Springer Berlin Heidelberg.
26. Huang, B., Jones, S. A., Brandenburg, B., and Zhuang, X. (2008) Whole-cell 3D STORM reveals interactions between cellular structures with nanometer- scale resolution. Nature Methods 5, 1047-1052.
27. Markert, M., Andrews, P. C., and Babior, B. M. (1984) Measurement of O2- production by human neutrophils. The preparation and assay of NADPH oxidase-containing particles from human neutrophils. Methods Enzymol. 358-365.
28. Pylypenko, O., Attanda, W., Gauquelin, C., Lahmani, M., Coulibaly, D., Baron, B., Hoos, S., Titus, M. A., England, P., and Houdusse, A. M. (2013) Structural basis of myosin V Rab GTPase-dependent cargo recognition. Proc. Natl. Acad. Sci. U.S.A. 110, 20443-20448.
29. Eathiraj, S., Mishra, A., Prekeris, R., and Lambright, D. G. (2006) Structural basis for Rab11-mediated recruitment of FIP3 to recycling endosomes. J. Mol. Biol. 364, 121-135.
30. Lall, P., Horgan, C. P., Oda, S., Franklin, E., Sultana, A., Hanscom, S. R., McCaffrey, M. W., and Khan, A. R. (2013) Structural and functional analysis of FIP2 binding to the endosome-localised Rab25 GTPase. Biochim. Biophys. Acta 1834, 2679-2690.
31. Catz, S. D. (2013) Regulation of vesicular trafficking and leukocyte function by Rab27 GTPases and their effectors. J. Leukocyte Biol. 94, 613-622.
32. Cockcroft, S. (1991) Relationship between arachidonate release and exocytosis in permeabilized human neutrophils stimulated with formylmethionyl- leucyl-phenylalanine (fMetLeuPhe), guanosine 5-[-thio]triphosphate (GTP[S]) and Ca2. Biochem. J. 275, 127-131.
33. Brown, G. E., Stewart, M. Q., Bissonnette, S. A., Elia, A. E., Wilker, E., and Yaffe, M. B. (2004) Distinct ligand-dependent roles for p38 MAPK in priming and activation of the neutrophil NADPH oxidase. J. Biol. Chem. 279, 27059-27068.
34. Fan, G. H., Lapierre, L. A., Goldenring, J. R., Sai, J., and Richmond, A. (2004) Rab11-family interacting protein 2 and myosin Vb are required for CXCR2 recycling and receptor-mediated chemotaxis. Mol. Biol. Cell 15, 2456-2469.
35. Mudrakola, H. V., Zhang, K., and Cui, B. (2009) Optically resolving individual microtubules in live axons. Structure 17, 1433-1441.
36. Khandelwal, P., Ruiz, W. G., Balestreire-Hawryluk, E., Weisz, O. A., Goldenring, J. R., and Apodaca, G. (2008) Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc. Natl. Acad. Sci. U.S.A. 105, 15773-15778.
37. Li, B. X., Satoh, A. K., and Ready, D. F. (2007) Myosin V, Rab11, and dRip11 direct apical secretion and cellular morphogenesis in developing Drosophila photoreceptors. J. Cell Biol. 177, 659-669.
38. Sugawara, K., Shibasaki, T., Mizoguchi, A., Saito, T., and Seino, S. (2009) Rab11 and its effector Rip11 participate in regulation of insulin granule exocytosis. Genes Cells 14, 445-456.
39. Su, T., Bryant, D. M., Luton, F., Vergés, M., Ulrich, S. M., Hansen, K. C., Datta, A., Eastburn, D. J., Burlingame, A. L., Shokat, K. M., and Mostov, K. E. (2010) A kinase cascade leading to Rab11-FIP5 controls transcytosis of the polymeric immunoglobulin receptor. Nat. Cell Biol. 12, 1143-1153.
40. Ren, Q., Wimmer, C., Chicka, M. C., Ye, S., Ren, Y., Hughson, F. M., and Whiteheart, S. W. (2010) Munc13-4 is a limiting factor in the pathway required for platelet granule release and hemostasis. Blood 116, 869-877.
41. Singh, R. K., Mizuno, K., Wasmeier, C., Wavre-Shapton, S. T., Recchi, C., Catz, S. D., Futter, C., Tolmachova, T., Hume, A. N., and Seabra, M. C. (2013) Distinct and opposing roles for Rab27a/Mlph/MyoVa and Rab27b/Munc13-4 in mast cell secretion. FEBS J. 280, 892-903.
42. Khandelwal, P., Prakasam, H. S., Clayton, D. R., Ruiz, W. G., Gallo, L. I., van Roekel, D., Lukianov, S., Peränen, J., Goldenring, J. R., and Apodaca, G. (2013) A Rab11a-Rab8a-Myo5B network promotes stretch-regulated exocytosis in bladder umbrella cells. Mol. Biol. Cell 24, 1007-1019.
43. Khvotchev, M. V., Ren, M., Takamori, S., Jahn, R., and Südhof, T. C. (2003) Divergent functions of neuronal Rab11b in Ca2-regulated versus constitutive exocytosis. J. Neurosci. 23, 10531-10539.
44. Savina, A., Fader, C. M., Damiani, M. T., and Colombo, M. I. (2005) Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic 6, 131-143.
45. Yu, S., Nie, Y., Knowles, B., Sakamori, R., Stypulkowski, E., Patel, C., Das, S., Douard, V., Ferraris, R. P., Bonder, E. M., Goldenring, J. R., Ip, Y. T., and Gao, N. (2014) TLR sorting by Rab11 endosomes maintains intestinal epithelial-microbial homeostasis. EMBO J. 33, 1882-1895.