Skip to main content
SpringerLink
Log in
Book cover

Organellar Proton-ATPases pp 1–27Cite as

Molecular and Cellular Biology of F- and V-ATPases

  • Chapter

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

Abstract

There are two mechanistically distinct ATP-dependent proton pumps. One belongs to the family of P-ATPases that operates with a phosphoenzyme intermediate, and the second belongs to the families of F- and V-ATPases that operate without an apparent phospho-enzyme intermediate.1, 2 The P-type proton pumps are integral membrane proteins, having similar structure and mechanism of action to those of Na+/K+-ATPases and Ca++-ATPases. The function of this proton pump is primarily in the plasma membrane of plant and fungal cells and in specialized mammalian cells such as parietal cells in the stomach.3 F- and V-ATPases are more universal proton pumps and at least one of them is present in every living cell.4 They share a common structure and mechanism of action and have a common evolutionary ancestry. In eukaryotic cells F-ATPases are confined to the semiautonomous organelles, chloroplasts and mitochondria that contain their own genes encoding some of the F-ATPase subunits.5 F-ATPase is also vital for every known eubacterium acting in photosynthetic or respiratory ATP-formation and/or in generating protonmotive force (pmf) by the reaction of ATP-dependent proton pumping.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Pedersen PL, Carafoli E. Ion motive ATPases. II. Energy coupling and work output. Trends Biochem Sci 1987; 12:186–189.

    Article  CAS  Google Scholar 

  2. Nelson N, Taiz L. The evolution of H+-ATPases. Trends Biochem Sci 1989; 14:113–116.

    Article  PubMed  CAS  Google Scholar 

  3. Sachs G, Besancon M, Shin JM, et al. Structural aspects of the gastric H, K-ATPase. J Bioenerg Biomembr 1992; 301-308.

    Google Scholar 

  4. Nelson N. Evolution of organellar proton-ATPases. Biochim Biophys Acta 1992; 1100:109–124.

    Article  PubMed  CAS  Google Scholar 

  5. Nelson N. Structural conservation and functional diversity of V-ATPases. Bioenerg Biomembr 1992; 24:407–414.

    Article  CAS  Google Scholar 

  6. Nelson N. Structure, molecular genetics and evolution of vacuolar H+-ATPases. J Bioenerg Biomembr 1989; 21:553–571.

    Article  PubMed  CAS  Google Scholar 

  7. Mellman I, Fuchs R, Helenius A. Acidification of the endocytic and exocytic pathways. Annu Rev Biochem 1986; 55:663–700.

    Article  PubMed  CAS  Google Scholar 

  8. Abrahams JP, Lutter R, Todd RJ, et al. Inherent asymmetry of the structure of F1-ATPase from bovine heart mitochondria at 6.5 Å resolution. EMBO J 1993; 12:1775–1780.

    PubMed  CAS  Google Scholar 

  9. Nelson N. Organellar proton-ATPases. Curr Opin Cell Biol 1992; 4:654–660.

    Article  PubMed  CAS  Google Scholar 

  10. Futai M, Noumi T, Maeda M. ATP synthase (H+-ATPase): Results by combined biochemical and molecular biological approaches. Annu Rev Biochem 1989; 58:111–136.

    Article  PubMed  CAS  Google Scholar 

  11. Bowman BJ, Dschida WJ, Harris T, et al. The vacuolar ATPase of Neurospora crassa contains an F1-like structure. J Biol Chem 1989; 264:15606–15612.

    PubMed  CAS  Google Scholar 

  12. Taiz SL, Taiz L. Ultrastructural comparison of the vacuolar and mitochondrial H+-ATPases of Daucus carota. Bot Acta 1991; 104:85–168.

    Google Scholar 

  13. Moriyama Y, Nelson N. Cold inactivation of vacuolar H+-ATPases. J Biol Chem 1989; 264:3577–3582.

    PubMed  CAS  Google Scholar 

  14. Moriyama Y, Nelson N. Lysosomal H+-translocating ATPase has a similar subunit structure to chromaffin grauune H+-ATPase complex. Biochim Biophys Acta 1989; 980:241–247.

    Article  PubMed  CAS  Google Scholar 

  15. Moriyama Y, Nelson N. H+-translocating ATPase in Golgi apparatus: Characterization as vacuolar H+-ATPase and its subunit structures. J Biol Chem 1989; 264:18445–18450.

    PubMed  CAS  Google Scholar 

  16. Schäfer G, Meyering-Vos M. The plasma membrane ATPase of archaebacteria: A chimeric energy converter. In: Scarpa A, Carafoli E, Papa S. eds. Ion-Motive ATPases: Structure, Function, and Regulation (Vol. 671). New York: The New York Academy of Sciences, 1992:293–309.

    Google Scholar 

  17. Moriyama Y, Nelson N. Nucleotide binding sites and chemical modification of the chromaffin granule proton ATPase. J Biol Chem 1987; 262:14723–14729.

    PubMed  CAS  Google Scholar 

  18. Bowman EJ, Tenney K, Bowman BJ. Isolation of genes encoding the Neurospora vacuolar ATPase. J Biol Chem 1988; 263:13994–14001.

    PubMed  CAS  Google Scholar 

  19. Zimniak L, Dittrich P, Gogarten JP, et al. The cDNA sequence of the 69 kDa subunit of the carrot vacuolar H+-ATPase. J Biol Chem 1988; 263:9102–9112.

    PubMed  CAS  Google Scholar 

  20. Feng Y, Forgac M. Cysteine 254 of the 73-kDa A subunit is responsible for inhibition of the coated vesicle (H+)-ATPase upon modification by sulfhydryl reagents. J Biol Chem 1992; 267:5817–5822.

    PubMed  CAS  Google Scholar 

  21. Manolson MF, Rea PA, Poole RJ. Identification of 3-O-(4-benzoyl) benzoyladenosine 5-triphosphate-and N,N’-dicyclohexylcarbodiimide-binding subunits of a higher plant proton-translocating tonoplast. J Biol Chem 1985; 260:12273–12279.

    PubMed  CAS  Google Scholar 

  22. Bowman BJ, Allen R, Wechser MA, et al. Isolation of genes encoding the Neurospora vacuolar ATPase. J Biol Chem 1988; 263:14002–14007.

    PubMed  CAS  Google Scholar 

  23. Beltrán C, Kopecky J, Pan Y-CE, et al. Cloning and mutational analysis of the gene encoding subunit C of yeast V-ATPase. J Biol Chem 1992; 267:774–779.

    PubMed  Google Scholar 

  24. Hirsch S, Strauss A, Masood K, et al. Isolation and sequence of a cDNA clone encoding the 31-kDa subunit of bovine kidney vacuolar H+-ATPase. Proc Natl Acad Sci USA 1988; 85:3004–3008.

    Article  PubMed  CAS  Google Scholar 

  25. Gluck SL, Nelson RD, Lee BS, et al. Biochemistry of the renal V-ATPase. J Exp Biol 1992; 172:219–229.

    PubMed  CAS  Google Scholar 

  26. Foury F. The 31-kDa polypeptide is an essential subunit of the vacuolar ATPase in Saccharomyces cerevisiae. J Biol Chem 1990; 265:18554–18560.

    PubMed  CAS  Google Scholar 

  27. Graf R, Lepier A, Harvey WR, et al. A novel 14-kDa V-ATPase subunit in the tobacco hornworm midgut. J Biol Chem 1994 (In press).

    Google Scholar 

  28. Nelson H, Mandiyan S, Nelson N. The Sacchoromyus ceranisiae VMA7 gene encodes a 14-kDa subunit of the vacuolar H+-/ATPase catalytic sector. J Biol Chem 1994 (in press).

    Google Scholar 

  29. Fillingame RH. H+ transport and coupling by the F0 sector of the ATP synthase: insights into the molecular mechanism of function. J Bioenerg Biomembr 1992; 24:485–491.

    Article  PubMed  CAS  Google Scholar 

  30. Girvin ME, Gillingame RH. Helical structure and folding of subunit c of F1F0 ATP synthase: H NMR resonance assignments and NOE analysis. Biochemistry 1993; 32:12167–12177.

    Article  PubMed  CAS  Google Scholar 

  31. Mandel M, Moriyama Y, Hulmes JD, et al. Cloning of cDNA sequence encoding the 16-kDa proteolipid of chromaffin granules implies gene duplication in the evolution of H+-ATPases. Proc Natl Acad Sci USA 1988; 85:5521–5524.

    Article  PubMed  CAS  Google Scholar 

  32. Arai H, Berne M, Forgac M. Inhibition of the coated vesicle proton pump and labeling of a 17,000-dalton polypeptide by N,N’-dicyclohexyl-carbodiimide. J Biol Chem 1987; 262:11006–11011.

    PubMed  CAS  Google Scholar 

  33. Sze H, Ward JM, Lai S, et al. Vacuolar-type H+-translocating ATPases in plant endomembranes: subunit organization and multigene families. J Exp Eiol 1992; 172:123–135.

    CAS  Google Scholar 

  34. Nelson H, Nelson N. The progenitor of ATP synthases was closely related to the current vacuolar H+-ATPase. FEBS Lett 1989; 247:147–153.

    Article  PubMed  CAS  Google Scholar 

  35. Nelson H, Nelson N. Disruption of genes encoding subunits of yeast vacuolar H+-ATPase causes conditional lethality. Proc Natl Acad Sci USA 1990; 87:3503–3507.

    Article  PubMed  CAS  Google Scholar 

  36. Schneider E, Altendorf K. Bacterial adenosine 5-triphosphate synthase (F1 Fo): purification and reconstitution of Fo complexes and biochemical and functional characterization of their subunits. Microbiol Rev 1987; 51:477–497.

    PubMed  CAS  Google Scholar 

  37. Perin MS, Fried VA, Stone DK, et al. Structure of the 116-kDa polypeptide of the clathrin-coated vesicle/synaptic vesicle proton pump. J Biol Chem 1991; 266:3877–3881.

    PubMed  CAS  Google Scholar 

  38. Wang S-Y, Moriyama Y, Mandel M, et al. Cloning of cDNA encoding a 32-kDa protein: an accessory polypeptide of the H+-ATPase from chromaffin granules. J Biol Chem 1989; 263:17638–17642.

    Google Scholar 

  39. Bauerle C, Ho MN, Lindorfer MA, et al. The Saccharomyces cerevisiae VMA6 gene encodes the 36-kDa subunit of the vacuolar H+-ATPase membrane sector. J Biol Chem 1993; 268:12749–12757.

    PubMed  CAS  Google Scholar 

  40. Supek F, Supekova L, Mandiyan S, et al. A novel accessory subunit for vacuolar H+-ATPase from chromaffin granules. J Biol Chem 1994 (in press).

    Google Scholar 

  41. Manolson MF, Ouellette BFF, Filion M, et al. cDNA sequence and homologies of the “57-kDa” nucleotide-binding subunit of the vacuolar ATPase from Arabidopsis. J Biol Chem 1988; 263:17987–17994.

    PubMed  CAS  Google Scholar 

  42. Gogarten JP, Kibak H, Dittrich P, et al. Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc Natl Acad Sci USA 1989; 86:6661–6665.

    Article  PubMed  CAS  Google Scholar 

  43. Denda K, Konishi J, Oshima T, et al. The membrane-associated ATPase from Sulfolobus acidocaldarius is distantly related to F1-ATPase as assessed from the primary structure of its a-subunit. J Biol Chem 1988; 263:6012–6015.

    PubMed  CAS  Google Scholar 

  44. Shih C-K, Wagner R, Feinstein S, et al. A dominant trifluoperazine resistance gene from Saccharomyces cerevisiae has homology with F0F1 ATP synthase and confers calcium-sensitive growth. Mol Cell Biol 1988; 8:3094–3103.

    PubMed  CAS  Google Scholar 

  45. Hirata R, Ohsumi Y, Nakano A, et al. Molecular structure of a gene, VMA1 encoding the catalytic subunit of H+-translocating adenosine triphosphatase from vacuolar membranes of Saccharomyces cerevisiae. J Biol Chem 1990; 265:6726–6733.

    PubMed  CAS  Google Scholar 

  46. Kane PM, Yamashiro CT, Wolczyk DF, et al. Protein splicing converts the yeast TFP1 gene product to the 69-kD subunit of the vacuolar H+-adenosine triphosphatase. Science 1990; 250:651–657.

    Article  PubMed  CAS  Google Scholar 

  47. Penefsky HS, Cross RL. Structure and mechanism of F0F1-type ATP synthases and ATPases. In: Meister A. ed. Advances in Enzymology and Related Areas of Molecular Biology, Vol. 64. New York: John Wiley & Sons, Inc., 1991:173–214.

    Google Scholar 

  48. Manolson MF, Rea PA, Poole RJ. Identification of 3-O-(4-benzoyl) benzoyladenosine 5-triphosphate-and N,N’-dicyclohexylcarbodiimide-binding subunits of a higher plant H+-translocating tonoplast ATPase. J Biol Chem 1985; 260:12273–12279.

    PubMed  CAS  Google Scholar 

  49. Walker JE, Fearnley IM, Gay NJ, et al. Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. J Mol Biol 1985; 184:677–701.

    Article  PubMed  CAS  Google Scholar 

  50. Puopolo K, Kumamoto C, Adachi I, et al. Differential expression of the “B” subunit of the vacuolar H+-ATPase in bovine tissues. J Biol Chem 1992; 267:3696–3706.

    PubMed  CAS  Google Scholar 

  51. Nelson H, Mandiyan S, Noumi T, et al. Molecular cloning of cDNA encoding the C subunit of H+-ATPase from bovine chromaffin granules. J Biol Chem 1990; 265:20390–20393.

    PubMed  CAS  Google Scholar 

  52. Denda K, Konishi J, Hajiro K, et al. Structure of an ATPase operon of an acidothermophilic archaebacterium, Sulfolobus acidocaldarius. J Biol Chem 1990; 265:21509–21513.

    PubMed  CAS  Google Scholar 

  53. Ho MN, Hill KJ, Lindorfer MA, et al. Isolation of vacuolar membrane H+-ATPase-deficient yeast mutants; the VMA5 and VMA4 genes are essential for assembly and activity of the vacuolar H+-ATPase. J Biol Chem 1993; 268:221–227.

    PubMed  CAS  Google Scholar 

  54. Noumi T, Beltrán C, Nelson H, et al. Mutational analysis of yeast vacuolar H+-ATPase. Proc Natl Acad Sci USA 1991; 88:1938–1942.

    Article  PubMed  CAS  Google Scholar 

  55. Supek F, Supekova L, Beltrán C, et al. Structure, function, and mutational analysis of V-ATPases. Ann NY Acad Sci 1992; 671:284–292.

    Article  PubMed  CAS  Google Scholar 

  56. Manolson MF, Proteau D, Preston RA, et al. The VPH1 gene encodes a 95-kDa integral membrane polypeptide required for in vivo assembly and activity of the yeast vacuolar H+-ATPase. J Biol Chem 1992; 267: 14294–14303.

    PubMed  CAS  Google Scholar 

  57. Umemoto N, Ohya Y, Anraku Y. MA11, a novel gene that encodes a putative proteolipid, is indispensable for expression of yeast vacuolar membrane H+-ATPase activity. J Biol Chem 1991; 266:24526–24532.

    PubMed  CAS  Google Scholar 

  58. Stevens TH. The structure and function of the fungal V-ATPase. J Exp Biol 1992; 172:47–55.

    PubMed  CAS  Google Scholar 

  59. Gluck SL. The structure and biochemistry of the vacuolar H+ ATPase in proximal and distal urinary acidification. J Bioenerg Biomembr 1992; 24:351–359.

    Article  PubMed  CAS  Google Scholar 

  60. Cross RL, Taiz L. Gene duplication as a means for altering H+/ATP ratios during the evolution of F0F1 ATPases and synthases. FEBS Lett 1990; 259:227–229.

    Article  PubMed  CAS  Google Scholar 

  61. Beltrán C, Nelson N. The membrane sector of vacuolar H+-ATPase by itself is impermeable to protons. Acta Physiol Scand 1992; 146:41–47.

    Article  Google Scholar 

  62. Njus D, Knoth J, Zallakian M. Proton-linked transport in chromaffin granules. Curr Topics Biognergetics 1981; 11:107–147.

    CAS  Google Scholar 

  63. Tabb JS, Kish PE, Van Dyke R, et al. Glutamate transport into synaptic vesicles. J Biol Chem 1992; 267:15412–15418.

    PubMed  CAS  Google Scholar 

  64. Moriyama Y, Nelson N. The purified ATPase from chromaffin granule membranes is an anion-dependent proton pump. J Biol Chem 1987; 262:9175–9180.

    PubMed  CAS  Google Scholar 

  65. Nelson N. Structure and pharmacology of the proton-ATPases. Trends Pharmac Sci 1991; 12:71–75.

    Article  CAS  Google Scholar 

  66. Kanner BI. Ion-coupled neurotransmitter transport. Curr Opin Cell Biol 1989; 1:735–738.

    Article  PubMed  CAS  Google Scholar 

  67. Liu Y, Peter D, Roghani A, et al. A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter. Cell 1992; 70:539–551.

    Article  PubMed  CAS  Google Scholar 

  68. Cidon S, Sihra T. Characterization of a H+ATPase in rat brain synaptic vesicles. Coupling to L-glutamate transport. J Biol Chem 1989; 264:8281–8288.

    PubMed  CAS  Google Scholar 

  69. Moriyama Y, Maeda M, Futai M. Energy coupling of L-glutamate transport and vacuolar H+-ATPase in brain synaptic vesicles. J Biochem 1990; 108:689–693.

    PubMed  CAS  Google Scholar 

  70. Liu Q-R, Mandiyan S, Nelson H, et al. A family of genes encoding neurotransmitter transporters. Proc Natl Acad Sci USA 1992; 89:6639–6643.

    Article  PubMed  CAS  Google Scholar 

  71. Liu Q-R, López-Corcuera B, Mandiyan S, et al. Molecular characterization of four pharmacologically distinct γ-aminobutyric acid transporters in mouse brain. J Biol Chem 1993; 268:2106–2112.

    PubMed  CAS  Google Scholar 

  72. Ohkuma S, Moriyama Y, Takano T. Identification and characterization of a proton pump on lysosomes by fluorescein isothiocyanate dextran fluorescence. Proc Natl Acad Sci USA 1982; 79:2758–2762.

    Article  PubMed  CAS  Google Scholar 

  73. Schneider DL. ATP-dependent acidification of intact and disrupted lysosomes. Evidence for an ATP-driven proton pump. J Biol Chem 1981; 256:3858–3864.

    PubMed  CAS  Google Scholar 

  74. Reeves JP, Reames T. ATP stimulates amino acid accumulation by lysosomes incubated with amino acid methyl esters. J Biol Chem 1981; 256:6047–6053.

    PubMed  CAS  Google Scholar 

  75. Klionsky DJ, Herman PK, Emr SD. The fungal vacuole: composition, function, and biogenesis. Microbiol Rev 1990; 54:266–292.

    PubMed  CAS  Google Scholar 

  76. Taiz L. The plant vacuole. J Exp Biol 1992; 172:113–122.

    PubMed  CAS  Google Scholar 

  77. Sarafian V, Kim Y, Poole RJ, et al. Molecular cloning and sequence of cDNA encoding the pyrophosphate-energized vacuolar membrane proton pump of Arabidopsis thaliana. Proc Natl Acad Sci USA 1992; 89:1775–1779.

    Article  PubMed  CAS  Google Scholar 

  78. Anraku Y, Hirata R, Wada Y, et al. Molecular genetics of the yeast vacuolar H+-ATPase. J Exp Biol 1992; 172:67–81.

    PubMed  CAS  Google Scholar 

  79. Ohya Y, Umemoto N, Tanida I, et al. Calcium-sensitive cls mutants of Saccharmoyces cerevisiae showing a pet-phenotype are ascribable to defects of vacuolar membrane H+-ATPase activity. J Biol Chem 1991; 266: 13971–13977.

    PubMed  CAS  Google Scholar 

  80. Chanson A, Taiz L. Evidence for an ATP-dependent proton pump on the Golgi of corn coleoptiles. Plant Physiol 1985; 78:232–240.

    Article  PubMed  CAS  Google Scholar 

  81. Young GP-H, Qiao J-Z, Al-Awqati Q. Purification and reconstitution of the proton-translocating ATPase of Golgi-enriched membranes. Proc Natl Acad Sci USA 1988; 85:9590–9594.

    Article  PubMed  CAS  Google Scholar 

  82. Klionsky DJ, Nelson H, Nelson N. Compartment acidification is required for efficient sorting of proteins to the vacuole in Saccharomyces cerevisiae.

    Google Scholar 

  83. Yaver DS, Nelson H, Nelson N, et al. Vacuolar ATPase mutants accumulate precursor proteins in a pre-vacuolar compartment. J Biol Chem 1993; 268:10564–10572.

    PubMed  CAS  Google Scholar 

  84. Gogarten JP, Fichmann J, Braun Y, et al. The use of antisense mRNA to inhibit the tonoplast H+-ATPase in carrot. The Plant Cell 1992; 4:851–864.

    PubMed  CAS  Google Scholar 

  85. Kelly RB. Pathways of protein secretion in eukaryotes. Science 1985; 230:25–32.

    Article  PubMed  CAS  Google Scholar 

  86. Finbow ME. Structure of a 16 kDa integral membrane protein that has identity to the putative proton channel of the vacuolar H+-ATPase. Protein Engineering 1991; 5:7–15.

    Google Scholar 

  87. Birman S., Meunier F-M, Lesbats B, et al. A 15 kDa proteolipid found in mediatophore preparations from Torpedo electric organ presents high sequence homology with the bovine chromaffin granule protonophore. FEBS Lett 1990; 261:303–306.

    Article  PubMed  CAS  Google Scholar 

  88. Hanada H, Hasebe M, Moriyama Y, et al. Molecular cloning of cDNA encoding the 16 kDa subunit of vacuolar H+-ATPase from mouse cerebellum. Biochem. Biophys, Res. Commun. 1991; 176:1062–1076.

    Article  CAS  Google Scholar 

  89. Meagher L, McLean P, Finbow ME. Sequence of a cDNA from Drosophila coding for the 16 kD proteolipid component of the vacuolar H+-ATPase. Nucleic Acids Res. 1990; 18:6712.

    Article  PubMed  CAS  Google Scholar 

  90. Lai S, Watson, JC, Hansen JN. Molecular cloning and sequencing of cDNAs encoding the proteolipid subunit of the vacuolar H+-ATPase from a higher plant. J. Biol. Chem. 1991; 266:16078–16084.

    PubMed  CAS  Google Scholar 

  91. Nelson H, Mandiyan S, Nelson N. A bovine cDNA and a yeast gene-VMAS encoding subunit D of the vacuolar H+-ATPase 1994 (submitted).

    Google Scholar 

Download references

Authors
  1. Nathan Nelson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 1995 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Nelson, N. (1995). Molecular and Cellular Biology of F- and V-ATPases. In: Organellar Proton-ATPases. Molecular Biology Intelligence Unit. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-22265-2_1

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-22265-2_1

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-22267-6

  • Online ISBN: 978-3-662-22265-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation