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Protons and how they are transported by proton pumps

  • Ion Channels, Receptors and Transporters
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Abstract

The very high mobility of protons in aqueous solutions demands special features of membrane proton transporters to sustain efficient yet regulated proton transport across biological membranes. By the use of the chemical energy of ATP, plasma-membrane-embedded ATPases extrude protons from cells of plants and fungi to generate electrochemical proton gradients. The recently published crystal structure of a plasma membrane H+-ATPase contributes to our knowledge about the mechanism of these essential enzymes. Taking the biochemical and structural data together, we are now able to describe the basic molecular components that allow the plasma membrane proton H+-ATPase to carry out proton transport against large membrane potentials. When divergent proton pumps such as the plasma membrane H+-ATPase, bacteriorhodopsin, and FOF1 ATP synthase are compared, unifying mechanistic premises for biological proton pumps emerge. Most notably, the minimal pumping apparatus of all pumps consists of a central proton acceptor/donor, a positively charged residue to control pK a changes of the proton acceptor/donor, and bound water molecules to facilitate rapid proton transport along proton wires.

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References

  1. Auer M, Scarborough GA Kühlbrandt W (1998) Three-dimensional map of the plasma membrane H+-ATPase in the open conformation. Nature 392:840–843

    Article  PubMed  CAS  Google Scholar 

  2. Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101

    Article  PubMed  CAS  Google Scholar 

  3. Brandsburg-Zabary S, Fried O, Marantz Y, Nachliel E, Gutman M (2000) Biophysical aspects of intra-protein proton transfer. Biochim Biophys Acta 1458:120–134

    Article  PubMed  CAS  Google Scholar 

  4. Briskin DP, Hanson JB (1992) How does the plant plasma membrane H+-ATPase pump protons? J Exp Bot 43:269–289

    Article  CAS  Google Scholar 

  5. Buch-Pedersen MJ, Palmgren MG (2003) Conserved Asp684 in transmembrane segment M6 of the plant plasma membrane P-type proton pump AHA2 is a molecular determinant of proton translocation. J Biol Chem 278:17845–17851

    Article  PubMed  CAS  Google Scholar 

  6. Buch-Pedersen MJ, Venema K, Serrano R, Palmgren MG (2000) Abolishment of proton pumping and accumulation in the E1P conformational state of a plant plasma membrane H+-ATPase by substitution of a conserved aspartyl residue in transmembrane segment 6. J Biol Chem 275:39167–39173

    Article  PubMed  CAS  Google Scholar 

  7. Capaldi RA, Aggeler R (2002) Mechanism of the F1FO-type ATP synthase, a biological rotary motor. Trends Biochem Sci 27:154–160

    Article  PubMed  CAS  Google Scholar 

  8. Copeland RA, Chan SI (1989) Proton translocation in proteins. Annu Rev Phys Chem 40:671–98

    Article  PubMed  CAS  Google Scholar 

  9. DeCoursey TE, Cherny VV (2000) Common themes and problems of bioenergetics and voltage-gated proton channels. Biochim Biophys Acta 1458:104–119

    Article  PubMed  CAS  Google Scholar 

  10. Eigen M (1964) Proton transfer acid–base catalysis and enzymatic hydrolysis. Angew Chem Int Ed 3:1–19

    Article  Google Scholar 

  11. Elston T, Wang H, Oster G (1998) Energy transduction in ATP synthase. Nature 391:510–513

    Article  PubMed  CAS  Google Scholar 

  12. Fillingame RH, Angevine CM, Dmitriev OY (2003) Mechanics of coupling proton movements to c-ring rotation in ATP synthase. FEBS Lett 555:29–34

    Article  PubMed  CAS  Google Scholar 

  13. Garczarek F, Brown LS, Lanyi JK, Gerwert K (2005) Proton binding within a membrane protein by a protonated water cluster. Proc Natl Acad Sci USA 102:3633–3638

    Article  PubMed  CAS  Google Scholar 

  14. Gouaux E, Mackinnon R (2005) Principles of selective ion transport in channels and pumps. Science 310:1461–1465

    Article  PubMed  CAS  Google Scholar 

  15. Grigorieff N, Ceska TA, Downing KH, Baldwin JM, Henderson R (1998) Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol 259:393–421

    Article  Google Scholar 

  16. Heberle J (2000) Proton transfer reactions across bacteriorhodopsin and along the membrane. Biochim Biophys Acta 1458:135–147

    Article  PubMed  CAS  Google Scholar 

  17. Lanyi JK (2004) Bacteriorhodopsin. Annu Rev Physiol 66:665–688

    Article  CAS  Google Scholar 

  18. Mathias G, Marx D (2007) Structures and spectral signatures of protonated water networks in bacteriorhodopsin. Proc Natl Acad Sci USA 104:6980–6985

    Article  PubMed  CAS  Google Scholar 

  19. Morth JP, Pedersen BP, Toustrup-Jensen MS, Sørensen TL, Petersen J, Andersen JP, Vilsen B, Nissen P (2007) Crystal structure of the sodium–potassium pump. Nature 450:1043–1049

    Article  PubMed  CAS  Google Scholar 

  20. Neutze R, Pebay-Peyroula E, Edman K, Royant A, Navarro J, Landau EM (2002) Bacteriorhodopsin: a high-resolution structural view of vectorial proton transport. Biochim Biophys Acta 1565:144–167

    Article  PubMed  CAS  Google Scholar 

  21. Olesen C, Picard M, Winther AM, Gyrup C, Morth JP, Oxvig C, Møller JV, Nissen P (2007) The structural basis of calcium transport by the calcium pump. Nature 450:1036–1042

    Article  PubMed  CAS  Google Scholar 

  22. Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845

    Article  PubMed  CAS  Google Scholar 

  23. Pardo JM, Serrano R (1989) Structure of a plasma membrane H+-ATPase gene from the plant Arabidopsis thaliana. J Biol Chem 264:8557–8562

    PubMed  CAS  Google Scholar 

  24. Pedersen PL, Carafoli E (1987) Ion motive ATPases. 1. Ubuiquity properties and significance to cell-function. Trends Biochem Sci 12:146–150

    Article  CAS  Google Scholar 

  25. Pedersen BP, Buch-Pedersen MJ, Morth JP, Palmgren MG, Nissen P (2007) Crystal structure of the plasma membrane proton pump. Nature 450:1111–1114

    Article  PubMed  CAS  Google Scholar 

  26. Pomes R, Roux B (2002) Molecular mechanism of H+ conduction in the single-file water chain of the gramicidin channel. Biophys J 82:2304–2316

    Article  PubMed  CAS  Google Scholar 

  27. Serrano R, Kielland-Brandt MC, Fink GR (1986) Yeast plasma-membrane ATPase is essential for growth and has homology with (Na+/K+), K+- and Ca2+-ATPases. Nature 319:689–693

    Article  PubMed  CAS  Google Scholar 

  28. Sørensen TL, Møller JV, Nissen P (2004) Phosphoryl transfer and calcium ion occlusion in the calcium pump. Science 304:1672–1675

    Article  PubMed  CAS  Google Scholar 

  29. Toyoshima C, Nakasako M, Nomura H, Ogawa H (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 26 Å resolution. Nature 405:647–655

    Article  PubMed  CAS  Google Scholar 

  30. Toyoshima C, Nomura H, Tsuda T (2004) Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues. Nature 432:361–368

    Article  PubMed  CAS  Google Scholar 

  31. Zundel G (2000) Hydrogen bonds with large proton polarizability and proton transfer processes in electrochemistry and biology. Adv Chem Phys 111:1–218

    Article  CAS  Google Scholar 

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Acknowledgments

M.J.B-P. is supported by a post-doctoral fellowship from the Carlsberg Foundation, B.P.P. by a Ph.D. fellowship from the Graduate School of Science at the University of Aarhus, and P.N. by a Hallas-Møller stipend from the Novo Nordisk Foundation.

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Correspondence to M. G. Palmgren.

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Buch-Pedersen, M.J., Pedersen, B.P., Veierskov, B. et al. Protons and how they are transported by proton pumps. Pflugers Arch - Eur J Physiol 457, 573–579 (2009). https://doi.org/10.1007/s00424-008-0503-8

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  • DOI: https://doi.org/10.1007/s00424-008-0503-8

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