Diverse and essential roles of mammalian vacuolar-type proton pump ATPase: Toward the physiological understanding of inside acidic compartments

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1658, Issue 1-2, 2004, Pages 106-114

  Sun Wada, Ge Hong ^a   Wada, Yoh ^a   Futai, Masamitsu ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Endomembrane organelle; Luminal acidification; Subunit isoform; V ATPase; Vesicle transport

Indexed keywords

ADENOSINE TRIPHOSPHATASE;

ACIDIFICATION; ACROSOME; CATALYSIS; CELL FUNCTION; CELL MEMBRANE; CELL ORGANELLE; CELL VACUOLE; CHROMAFFIN GRANULE; COATED VESICLE; ENDOCYTOSIS; ENDOSOME; ENZYME PHOSPHORYLATION; ENZYME RELEASE; ENZYME SUBUNIT; EPITHELIUM CELL; GOLGI COMPLEX; HYDROLYSIS; INTRACELLULAR SPACE; LAMELLAR BODY; LYSOSOME; MALE GENITAL SYSTEM; MAMMAL; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTON TRANSPORT; REVIEW;

ANIMALS; CELL LINE; CELL MEMBRANE; HUMANS; HYDROGEN-ION CONCENTRATION; ORGANELLES; OSTEOCLASTS; PROTEIN TRANSPORT; VACUOLAR PROTON-TRANSLOCATING ATPASES;

MAMMALIA;

EID: 3542998744     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2004.04.013     Document Type: Review

References (94)

1. Mellman I., Fuchs R., Helenius A. Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 55:1986;663-700
2. Futai M., Oka T., Moriyama Y., Wada Y. Diverse roles of single membrane organelles: factors establishing the acid lumenal pH. J. Biochem. 124:1998;259-267
3. Harding C.V., Geuze H.J. Immunogenic peptides bind to Class-II MHC molecules in an early lysosomal compartment. J. Immunol. 151:1993;3988-3998
4. Peters P., et al. Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Biol. 173:1991;1099-1109
5. McNicol A., Israels S.J. Platelet granules:structure, function and implications for haemostasis. Thromb. Res. 95:1999;1-18
6. Baron R., Neff L., Louvard D., Courtoy P.J. Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100 kDa lysosomal membrane protein at the osteoclast ruffled border. J. Cell Biol. 101:1985;2210-2222
7. Katzmann D.J., Odorizzi G., Emr S.D. Receptor downregulation and multivesicular-body sorting. Nat. Rev., Mol. Cell Biol. 3:2002;893-905
8. Tjelle T.E., Brech A., Juvet L.K., Griffiths G., Berg T. Isolation and characterization of early endosomes and terminal lysosomes: their role in protein degradation. J. Cell Sci. 109:1996;2905-2914
9. Hasilik A. The early and late processing of lysosomal enzymes: proteolysis and compartmentation. Experientia. 48:1992;130-151
10. Pisoni R.L., Thoene J.G. The transport systems of mammalian lysosomes. Biochim. Biophys. Acta. 1071:1991;351-373
11. Futai M., Oka T., Sun-Wada G.-H., Moriyama Y., Kanazawa H., Wada Y. Luminal acidification of diverse organelles by V-ATPase in animal cells. J. Exp. Biol. 203:2000;107-116
12. + pumping ATPases in luminal acidic organelles and extracellular compartments:common rotational mechanism and diverse physiological roles. J. Bioenerg. Biomembranes. 35:2003;347-358
13. +-ATPase - nature's most versatile proton pumps. Nat. Rev., Mol. Cell Biol. 3:2002;94-103
14. Nelson N., Harvey W.R. Vacuolar and plasma membrane proton- adenosinetriphosphatases. Physiol. Rev. 79:1999;361-385
15. Futai M., Noumi T., Maeda M. Annu. Rev. Biochem. 58:1989;111
16. Anraku Y. Kornings W.N., Kaback H.R., Lolkema J.S. Handbook of Biological Physics. 1996;99-109 Elsevier, Amsterdam
17. Oka T., Futai M. Requirement of V-ATPase for ovulation and embryogenesis in Caenorhabditis elegans. J. Biol. Chem. 275:2000;29556-29561
18. +-ATPase subunit a. J. Biol. Chem. 276:2001;40050-40054
19. +-ATPase. cell-specific expression during development. J. Biol. Chem. 276:2001;33079-33085
20. Oka T., Yamamoto R., Futai M. Three vha genes encode proteolipids of Caenorhabditis elegans vacuolar-type ATPase. Gene structures and preferential expression in an H-shaped excretory cell and rectal cells. J. Biol. Chem. 272:1997;24387-24392
21. Oka T., Yamamoto R., Futai M. Multiple genes for vacuolar-type ATPase proteolipids in Caenorhabditis elegans. A new gene, vha-3, has a distinct cell-specific distribution. J. Biol. Chem. 273:1998;22570-22576
22. +-ATPase with the a3 isoform during osteoclast dfferentiation. J. Biol Chem. 278:2003;22023-22030
23. +-ATPase. Preferential expression of the a3 isoform during osteoclast differentiation. J. Biol. Chem. 275:2000;8760-8765
24. Nishi T., Forgac M. Molecular cloning and expression of three isoforms of the 100-kDa a subunit of the mouse vacuolar proton-translocating ATPase. J. Biol. Chem. 275:2000;6824-6830
25. Manolson M.F., Proteau D., Jones E.W. Evidence for a conserved 95-120 kDa subunit associated with and essential for activity of V-ATPases. J. Exp. Biol. 172:1992;105-112
26. +-ATPase subunit Vph1p. J. Biol. Chem. 269:1994;14064-14074
27. Kawasaki-Nishi S., Nishi T., Forgac M. Yeast V-ATPase complexes containing different isoforms of the 100-kDa a-subunit differ in coupling efficiency and in vivo dissociation. J. Biol. Chem. 276:2001;17941-17948
28. +-ATPase a-subunit gene. J. Biol. Chem. 276:2001;42382-42388
29. +-ATPase subunit genes. Mol. Cell. 12:2003;801-803
30. Sun-Wada G.-H., Yoshimizu T., Imai-Senga Y., Wada Y., Futai M. Diversity of mouse proton-translocating ATPase: presence of multiple isoforms of the C, d and G subunits. Gene. 302:2003;147-153
31. +-ATPases. FEBS Lett. 440:1998;258-263
32. Hirata T., Wada Y., Futai M. Sodium and sulfate ion transport in yeast vacuoles. J. Biochem. (Tokyo). 131:2002;261-265
33. Forgac M. Structure and properties of the clathrin-coated vesicle and yeast vacuolar V-ATPases. J. Bioenerg. Biomembranes. 31:1999;57-65
34. Noji H., Yasuda R., Yoshida M.C., Kinosita K.J. Direct observation of the rotation of F1-ATPase. Nature. 386:1997;299-302
35. + ATPase: coupling between catalysis, mechanical work, and proton translocation. Biochim. Biophys. Acta. 1458:2000;276-288
36. Wada Y., Sambongi Y., Futai M. Biological nano motor, ATP synthase FoF1: from catalysis to gec10-12 subunit assembly rotation. Biochim. Biophys. Acta. 1459:2000;499-505
37. Hirata T., Iwamoto-Kihara A., Sun-Wada G.H., Okajima T., Wada Y., Futai M. Subunit rotation of vacuolar-type proton pumping ATPase: relative rotation of the G as to c subunit. J. Biol. Chem. 278:2003;23714-23719
38. +)-ATPase complex. J. Biol. Chem. 274:1999;28909-28915
39. +-ATPase and effects of bafilomycin A1. Biochem. Biophys. Res. Commun. 170:1990;873-878
40. Huss M., Ingenhorst G., König S., Gassel M., Dröse S., Zeeck A., Altendorf K., Wieczorek H. Concanamycin A, the specific inhibitor of V-ATPases, binds to the Vo subunit c. J. Biol. Chem. 277:2002;40544-40548
41. Bowman B.J., Bowman E.J. Mutations in subunit c of the vacuolar ATPase confer resistance to bafilomycin and identify a conserved antibiotic binding site. J. Biol. Chem. 277:2002;3965-3972
42. Zhang J., Feng Y., Forgac M. Proton conduction and bafilomycin binding by the V0 domain of the coated vesicle V-ATPase. J. Biol. Chem. 269:1994;23518-23523
43. Sun-Wada G.-H., Murata Y., Yamamoto A., Kanazawa H., Wada Y., Futai M. Acidic endomembrane organelles are required for mouse postimplantation development. Dev. Biol. 228:2000;315-325
44. Marshansky V., Bourgoin S., Londono I., Bendayan M., Vinay P. Identification of ADP-ribosylation factor-6 in brush-border membrane and early endosomes of human kidney proximal tubules. Electrophoresis. 18:1997;538-547
45. +-ATPase and endocytosis in rat kidney cortex. Kidney Int. 53:1998;1713-1726
46. Lloyd S.E., Gunther W., Pearce S.H., Thomson A., Bianchi M.L., Bosio M., Craig I.W., Fisher S.E., Scheinman S.J., Wrong O., Jentsch T.J., Thakker R.V., Steinmeyer K., Schwappach B., Harding B., Bolino A., Devoto M., Goodyer P., Rigden S.P. Characterisation of renal chloride channel, CLCN5, mutations in hypercalciuric nephrolithiasis (kidney stones) disorders: a common molecular basis for three inherited kidney stone diseases. Hum. Mol. Genet. 6:1997;1233-1239
47. Lloyd S.E., Pearce S.H., Fisher S.E., Steinmeyer K., Schwappach B., Scheinman S.J., Harding B., Bolino A., Devoto M., Goodyer P., Rigden S.P., Wrong O., Jentsch T.J., Craig I.W., Thakker R.V. A common molecular basis for three inherited kidney stone diseases. Nature. 379:1996;445-449
48. --channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature. 408:2000;369-373
49. Geyer M., Yu H., Mandic R., Linnemann T., Zheng Y.H., Fackler O.T., Peterlin B.M. Subunit H of the V-ATPase binds to the medium chain of adaptor protein complex 2 and connects Nef to the endocytic machinery. J. Biol. Chem. 277:2002;28521-28529
50. Pearse B.M., Robinson M.S. Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol. 6:1990;151-171
51. Mandic R., Fackler O.T., Geyer M., Linnemann T., Zheng Y.H., Peterlin B.M., Lu X., Yu H., Liu S.H., Brodsky F.M. Negative factor from SIV binds to the catalytic subunit of the V-ATPase to internalize CD4 and to increase viral infectivity: Interactions between HIV1 Nef and vacuolar ATPase facilitate the internalization of CD4. Mol. Biol. Cell. 12:2001;463-473
52. Lu X., Yu H., Liu S.H., Brodsky F.M., Peterlin B.M. Interactions between HIV1 Nef and vacuolar ATPase facilitate the internalization of CD4. Immunity. 8:1998;647-656
53. +-ATPase subunit required for activity but not assembly of the enzyme complex in Saccharomyces cerevisiae. J. Biol. Chem. 268:1993;18286-18292
54. +-ATPase complexes resulting from overproduction of Vma5p and Vma13p. J. Biol. Chem. 277:2002;2124-2716
55. Kane P.M. Biosynthesis and regulation of the yeast vacuolar H+-ATPase. J. Bioenerg. Biomembranes. 31:1999;49-56
56. Maranda B., Brown D., Bourgoin S., Casanova J.E., Vinay P., Ausiello D.A., Marshansky V. Intra-endosomal pH-sensitive recruitment of the Arf-nucleotide exchange factor ARNO and Arf6 from cytoplasm to proximal tubule endosomes. J. Biol. Chem. 276:2001;18540-18550
57. + pump activity. J. Cell Biol. 103:1986;1257-1267
58. Orci L., Ravazzola M., Amherdt M., Madsen O., Perrelet A., Vassalli J.D., Anderson R.G. Conversion of proinsulin to insulin occurs coordinately with acidification of maturing secretory vesicles. J. Cell Biol. 103:1986;2273-2281
59. Urbe S., Dittie A.S., Tooze S.A. pH-dependent processing of secretogranin II by the endopeptidase PC2 in isolated immature secretory granules. Biochem. J. 321:1997;65-74
60. Barg S., Huang P., Eliasson L., Nelson D.J., Obermuller S., Rorsman P., Thevenod F., Renstrom E. Priming of insulin granules for exocytosis by granular Cl-uptake and acidification. J. Cell Sci. 114:2001;2145-2154
61. +-ATPase perturbs the transport, sorting, processing and release of regulated secretory proteins. Eur. J. Biochem. 267:2000;5646-5654
62. Karsenty G. The genetic transformation of bone biology. Gene Dev. 13:1999;3037-3051
63. Roodman G.D. Cell biology of the osteoclasts. Exp. Hematol. 27:1999;1229-1241
64. Vaananen H.K., Zhao H., Mulari M., Halleen J.M. The cell biology of osteoclast function. J. Cell Sci. 113:2000;377-381
65. Blair H.C., Teitelbaum S.M., Ghiselli R., Gluck L.S. Osteoclastic bone resorption by a vacuolar proton pump. Science. 245:1989;855-857
66. Li Y., Chen W., Liang Y., Li E., Stashenko P. Atp6i-deficient mice exhibit severe osteopetrosis due to loss of osteoclast-mediated extracellular acidification. Nat. Genet. 23:1999;447-451
67. +-ATPase in osteoclasts of rat tibiae. Arch. Histol. Cytol. 57:1994;535-539
68. Scimeca J.-C., Franchi A., Trojani C., Parrinello H., Grosgeorge J., Robert C., Jaillon O., Poirier C., Gaudray P., Carle G.F. Bone. 26:2000;207-213
69. Sobacchi C., Frattini A., Orchard P., Porras O., Tezcan I. The mutational spectrum of human malignant autosomal recessive soteopetrosis. Hum. Mol. Genet. 10:2001;1767-1773
70. +-ATPase cause infantile malignant osteopetrosis. Hum. Mol. Genet. 9:2000;2059-2063
71. Takayanagi H., Kim S., Taniguchi T. Signaling crosstalk between RANKL and interferons in osteoclast differentiation. Arthritis Res. 4:2002;S227-S232
72. Huang L., Xu J., Wood D.J., Zheng M.H. Am. J. Pathol. 156:2000;761-767
73. Rajapurohitam V., Chalhoub N., Benachenhou N., Neff L., Baron R., Vacher J. The mouse osteopetrotic grey-lethal mutation induces a defect in osteoclast maturation/function. Bone. 28:2001;513-523
74. Chalhoub N., Benachenhou N., Rajapurohitam V., Pata M., Ferron M., Frattini A., Villa A., Vacher J. Grey-lethal mutation induces severe malignant autosomal recessive osteopetrosis in mouse and human. Nat. Med. 9:2003;399-406
75. Matsumoto M., Sudo T., Saito T., Osada H., Tsujimoto M. Involvement of p38 mitogen-activated protein kinase signaling pathway in osteoclastogenesis mediated by receptor activator of NF-kB ligand (RANKL). J. Biol. Chem. 275:2000;31155-31161
76. Hsu H., Lacey D.L., Dunstan C.R., Solovyev I., Colombero A., Timms E., Tan H.L., Elliott G., Kelley M.J., Sarosi I., Wang L., Xia X.Z., Elliott R., Chiu L., Black T., Scully S., Capparelli C., Morony S., Shimamoto G., Bass M.B., Boyle W.J. Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc. Natl. Acad. Sci. U. S. A. 96:1999;3540-3545
77. +-ATPase and microfilaments during osteoclast activation. J. Biol. Chem. 274:1999;29164-29171
78. Chander A., Fisher A.B. Regulation of lung surfactant secretion. Am. J. Physiol. 258:1990;L241-L253
79. Chander A., Johnson R.G., Reicherter J., Fischer A.B. Lung lammelar bodies maintained an acidic internal pH. J. Biol. Chem. 261:1986;6126-6131
80. 2+ uptake in lung lamellar bodies. J. Membr. Biol. 174:2000;41-51
81. +-ATPase. J. Biol. Chem. 268:1993;221-227
82. +-ATPase in plant growth and development. Genes Dev. 13:1999;3259-3270
83. Huizing M., Anikster Y., Gahl W.A. Hermansky-Pudlak syndrome and related disorders of organelle formation. Traffic. 1:2000;823-835
84. Nakatani Y., Nakamura N., Sano J., Inayama Y., Kawano N., Yamanaka S., Miyagi Y., Nagashima Y., Ohbayashi C., Mizushima M., Manabe T., Kuroda M., Yokoi T., Matsubara O. Interstitial pneumonia in Hermansky-Pudlak syndrome: significance of florid foamy swelling/degeneration (giant lamellar body degeneration) of type-2 pneumocytes. Virchows Arch. 437:2000;304-313
85. Chi E.Y., Lagunoff D. Abnormal mast cell granules in the beige (Chediak-Higashi syndrome) mouse. J. Histochem. Cytochem. 23:1975;117-122
86. Kang-Decker N., Mantchev G.T., Juneja S.C., McNiven M.A., van Deursen J.M. Lack of acrosome formation in Hrb-deficient mice. Science. 294:2001;1531-1533
87. Burgess T.L., Kelly R.B. Constitutive and regulated secretion of proteins. Annu. Rev. Cell Biol. 3:1987;243-293
88. Sun-Wada G.-H., Imai-Senga Y., Yamamoto A., Murata Y., Hirata T., Wada Y., Futai M. A proton pump ATPase with testis-specific E1 subunit isoform required for acrosome acidification. J. Biol. Chem. 277:2002;18098-18105
89. Sinowatz F., Wrobel K.H. Development of the bovine acrosome. An ultrastructural and cytochemical study. Cell Tissue Res. 219:1981;511-524
90. Hermo L., Rambourg A., Clermont Y. Three-dimensional architecture of the cortical region of the Golgi apparatus in rat spermatids. Am. J. Anat. 157:1980;357-373
91. Glassner M., Jones J., Kligman I., Woolkalis M.J., Gerton G.L., Kopf G.S. Immunocytochemical and biochemical characterization of guanine nucleotide-binding regulatory proteins in mammalian spermatozoa. Dev. Biol. 146:1991;438-450
92. Romrell L.J., Bellve A.R., Fawcett D.W. Separation of mouse spermatogenic cells by sedimentation velocity. A morphological characterization. Dev. Biol. 49:1976;119-131
93. +-ATPase E subunit. J. Biol. Chem. 276:2001;46276-46283
94. Lamaze C., Chuang T.H., Terlecky L.J., Bokoch G.M., Schmid S.L. Regulation of receptor-mediated endocytosis by Rho and Rac. Nature. 382:1996;177-179