Direct recruitment of H+-ATPase from lysosomes for phagosomal acidification

Journal of Cell Science

Volumn 122, Issue 14, 2009, Pages 2504-2513

  Sun Wada, Ge Hong ^a   Tabata, Hiroyuki ^a   Kawamura, Nobuyuki ^a   Aoyama, Minako ^b   Wada, Yoh ^b  

^a DOSHISHA WOMEN'S COLLEGE OF LIBERAL ARTS   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Acidification; Macrophage; Microtubules; Tubular lysosome; V ATPase

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE A3 SUBUNIT; UNCLASSIFIED DRUG;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENDOSOME; ENZYME LOCALIZATION; ENZYME MODIFICATION; ENZYME SUBUNIT; EXPERIMENTAL MOUSE; GENE LOCUS; IMAGE ANALYSIS; IMAGING; IMMUNOFLUORESCENCE MICROSCOPY; LYSOSOME; MACROPHAGE; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION;

ANIMALS; CELLS, CULTURED; HYDROGEN-ION CONCENTRATION; LYSOSOMES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; PHAGOCYTOSIS; PHAGOSOMES; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; TIME FACTORS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

MUS;

EID: 69649106201     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.050443     Document Type: Article

References (52)

1. Aoyama, M., Agari, K., Sun-Wada, G. H., Futai, M. and Wada, Y. (2005). Simple and straightforward construction of a mouse gene targeting vector using in vitro transposition reactions. N ucleic Acids Res. 33, e52.
2. + ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol. 209, 577-589.
3. Blin-Wakkach, C., Wakkach, A., Sexton, P. M., Rochet, N. and Carle, G. F. (2004). Hematological defects in the oc/oc mouse, a model of infantile malignant osteopetrosis. Leukemia 18, 1505-1511.
4. Blocker, A., Severin, F. F., Burkhardt, J. K., Bingham, J. B., Yu, H., Olivo, J. C., Schroer, T. A., Hyman, A. A. and Griffiths, G. (1997). Molecular requirements for bi-directional movement of phagosomes along microtubules. J. Cell Biol. 137, 113-129.
5. Breton, S. and Brown, D. (2007). New insights into the regulation of V-ATPase-dependent proton secretion. Am. J. Physiol. Renal Physiol. 292, F1-10.
6. Cantalupo, G., Alifano, P., Roberti, V., Bruni, C. B. and Bucci, C. (2001). Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J. 20, 683-693.
7. +-ATPase in the contractile vacuole complex and the endosomal pathway of Dictyostelium cells. J. Cell Sci. 115, 2893-2905.
8. Del Fattore, A., Cappariello, A. and Teti, A. (2007). Genetics, pathogenesis and complications of osteopetrosis. Bone 42, 19-29.
9. Deretic, V., Singh, S., Master, S., Harris, J., Roberts, E., Kyei, G., Davis, A., de Haro, S., Naylor, J., Lee, H. H. et al. (2006). Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell Microbiol. 8, 719-727.
10. Dermine, J. F., Duclos, S., Garin, J., St-Louis, F., Rea, S., Parton, R. G. and Desjardins, M. (2001). Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J. Biol. Chem. 276, 18507-18512.
11. Desjardins, M., Huber, L. A., Parton, R. G. and Griffiths, G. (1994). Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124, 677-688.
12. Dragonetti, A., Baldassarre, M., Castino, R., Demoz, M., Luini, A., Buccione, R. and Isidoro, C. (2000). The lysosomal protease cathepsin D is efficiently sorted to and secreted from regulated secretory compartments in the rat basophilic/mast cell line RBL. J. Cell Sci. 113, 3289-3298.
13. Drecktrah, D., Knodler, L. A., Howe, D. and Steele-Mortimer, O. (2007). Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 8, 212-225.
14. Fratti, R. A., Chua, J., Vergne, I. and Deretic, V. (2003). Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl. Acad. Sci. USA 100, 5437-5442.
15. Haas, A. (2007). The phagosome: compartment with a license to kill. Traffic 8, 311-330.
16. Harrison, R. E., Bucci, C., Vieira, O. V., Schroer, T. A. and Grinstein, S. (2003). Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol. Cell. Biol. 23, 6494-6506.
17. Hogan, B., Beddington, R., Constantini, F. and Lacy, E. (1994). Manipulating Mouse Embryo: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
18. Hurtado-Lorenzo, A., Skinner, M., El Annan, J., Futai, M., Sun-Wada, G. H., Bourgoin, S., Casanova, J., Wildeman, A., Bechoua, S., Ausiello, D. A. et al. (2006). V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat. Cell Biol. 8, 124-136.
19. +-ATPase. J. Exp. Biol. 203, 81-87.
20. Kominami, E., Tsukahara, T., Hara, K. and Katunuma, N. (1988). Biosyntheses and processing of lysosomal cysteine proteinases in rat macrophages. FEBS Lett. 231, 225-228.
21. Lafourcade, C., Sobo, K., Kieffer-Jaquinod, S., Garin, J. and van der Goot, F. G. (2008). Regulation of the V-ATPase along the endocytic pathway occurs through reversible subunit association and membrane localization. PLoS ONE 3, e2758.
22. Lakso, M., Pichel, J. G., Gorman, J. R., Sauer, B., Okamoto, Y., Lee, E., Alt, F. W. and Westphal, H. (1996). Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. USA 93, 5860-5865.
23. Lee, E. C., Yu, D., Martinez de Velasco, J., Tessarollo, L., Swing, D. A., Court, D. L., Jenkins, N. A. and Copeland, N. G. (2001). A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73, 56-65.
24. Li, Y. P., Chen, W., Liang, Y., Li, E. and Stashenko, P. (1999). Atp6i-deficient mice exhibit severe osteopetrosis due to loss of osteoclast-mediated extracellular acidification. Nat. Genet. 23, 447-451.
25. Lukacs, G. L., Chang, X. B., Kartner, N., Rotstein, O. D., Riordan, J. R. and Grinstein, S. (1992). The cystic fibrosis transmembrane regulator is present and functional in endosomes. Role as a determinant of endosomal pH. J. Biol. Chem. 267, 14568-14572.
26. +-ATPase in murine macrophages. J. Biol. Chem. 265, 21099-21107.
27. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. and Roder, J. C. (1993). Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90, 8424-8428.
28. Nakamura, N., Yamamoto, A., Wada, Y. and Futai, M. (2000). Syntaxin 7 mediates endocytic trafficking to late endosomes. J. Biol. Chem. 275, 6523-6529.
29. Nakamura, N., Sun-Wada, G. H., Yamamoto, A., Wada, Y. and Futai, M. (2001). Association of mouse sorting nexin 1 with early endosomes. [i J. Biochem. 130, 765-771.
30. +-ATPase subunit a. J. Biol. Chem. 276, 40050-40054.
31. Perin, M., Fried, V., Stone, D., Xie, X. and Sudhof, T. (1991). Structure of the 116-kDa polypeptide of the clathrin-coated vesicle/ synaptic vesicle proton pump. J. Biol. Chem. 266, 3877-3881.
32. Rodriguez, C. I., Buchholz, F., Galloway, J., Sequerra, R., Kasper, J., Ayala, R., Stewart, A. F. and Dymecki, S. M. (2000). High-efficiency deleter mice show that FLPe is an alternative to Cre- loxP. Nat. Genet. 25, 139-140.
33. Scimeca, J. C., Franchi, A., Trojani, C., Parrinello, H., Grosgeorge, J., Robert, C., Jaillon, O., Poirier, C., Gaudray, P. and Carle, G. F. (2000). The gene encoding the mouse homologue of the human osteoclast-specific 116-kDa V-ATPase subunit bears a deletion in osteosclerotic (oc/oc) mutants. Bone 26, 207-213.
34. Sprenger, R. R., Fontijn, R. D., van Marle, J., Pannekoek, H. and Horrevoets, A. J. (2006). Spatial segregation of transport and signalling functions between human endothelial caveolae and lipid raft proteomes. Biochem. J. 400, 401-410.
35. Steinberg, B. E., Touret, N., Vargas-Caballero, M. and Grinstein, S. (2007). In situ measurement of the electrical potential across the phagosomal membrane using FRET and its contribution to the proton-motive force. Proc. Natl. Acad. Sci. USA 104, 9523-9528.
36. Sturgill-Koszycki, S., Schlesinger, P. H., Chakraborty, P., Haddix, P. L., Collins, H. L., Fok, A. K., Allen, R. D., Gluck, S. L., Heuser, J. and Russell, D. G. (1994). Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681.
37. Sun-Wada, G. H., Murata, Y., Namba, M., Yamamoto, A., Wada, Y. and Futai, M. (2003). Mouse proton pump ATPase C subunit isoforms (C2-a and C2-b) specifically expressed in kidney and lung. J. Biol. Chem. 278, 44843-44851.
38. Sun-Wada, G. H., Toyomura, T., Murata, Y., Yamamoto, A., Futai, M. and Wada, Y. (2006). The a3 isoform of V-ATPase regulates insulin secretion from pancreatic β-cells. J. Cell Sci. 119, 4531-4540.
39. Sun-Wada, G. H., Tabata, H., Kawamura, N., Futai, M. and Wada, Y. (2007). Differential expression of a subunit isoforms of the vacuolar-type proton pump ATPase in mouse endocrine tissues. Cell Tissue Res. 329, 239-248.
40. +-ATPase with the a3 isoform is the proton pump on premature melanosomes. Cell Tissue Res. 332, 447-460.
41. +-ATPase. Preferential expression of the a3 isoform during osteoclast differentiation. J. Biol. Chem. 275, 8760-8765.
42. +-ATPase with the a3 isoform during osteoclast differentiation. J. Biol. Chem. 278, 22023-22030.
43. Tsang, A. W., Oestergaard, K., Myers, J. T. and Swanson, J. A. (2000). Altered membrane trafficking in activated bone marrow-derived macrophages. J. Leukoc. Biol. 68, 487-494.
44. Utku, N., Heinemann, T., Tullius, S. G., Bulwin, G. C., Beinke, S., Blumberg, R. S., Beato, F., Randall, J., Kojima, R., Busconi, L. et al. (1998). Prevention of acute allograft rejection by antibody targeting of TIRC7, a novel T cell membrane protein. Immunity 9, 509-518.
45. Utku, N., Boerner, A., Tomschegg, A., Bennai-Sanfourche, F., Bulwin, G. C., Heinemann, T., Loehler, J., Blumberg, R. S. and Volk, H. D. (2004). TIRC7 deficiency causes in vitro and in vivo augmentation of T and B cell activation and cytokine response. J. Immunol. 173, 2342-2352.
46. Vieira, O. V., Botelho, R. J. and Grinstein, S. (2002). Phagosome maturation: aging gracefully. Biochem. J. 366, 689-704.
47. Vyas, J. M., Kim, Y. M., Artavanis-Tsakonas, K., Love, J. C., Van der Veen, A. G. and Ploegh, H. L. (2007). Tubulation of class II MHC compartments is microtubule dependent and involves multiple endolysosomal membrane proteins in primary dendritic cells. J. Immunol. 178, 7199-7210.
48. Wada, Y., Kitamoto, K., Kanbe, T., Tanaka, K. and Anraku, Y. (1990). The SLP1 gene of Saccharomyces cerevisiae is essential for vacuolar morphogenesis and function. Mol. Cell. Biol. 10, 2214-2223.
49. Wilson, C. J. and Vellodi, A. (2000). Autosomal recessive osteopetrosis: diagnosis, management, and outcome. Arch. Dis. Child 83, 449-452.
50. Yates, R. M., Hermetter, A. and Russell, D. G. (2005). The kinetics of phagosome maturation as a function of phagosome/lysosome fusion and acquisition of hydrolytic activity. Traffic 6, 413-420.
51. Yates, R. M., Hermetter, A., Taylor, G. A. and Russell, D. G. (2007). Macrophage activation downregulates the degradative capacity of the phagosome. Traffic 8, 241-250.
52. Yeyeodu, S., Ahn, K., Madden, V., Chapman, R., Song, L. and Erickson, A. H. (2000). Procathepsin L self-association as a mechanism for selective secretion. Traffic 1, 724-737.