Structure-function relationships in membrane segment 6 of the yeast plasma membrane Pma1 H+-ATPase

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 7, 2011, Pages 1781-1789

  Miranda, Manuel ^a   Pardo, Juan Pablo ^b   Petrov, Valery V ^c  

^a UNIVERSITY OF TEXAS AT EL PASO   (United States)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c SKRYABIN INSTITUTE OF BIOCHEMISTRY AND PHYSIOLOGY OF MICROORGANISMS   (Russian Federation)

Author keywords

H+ ATPase; Ion pump; P2 ATPases; Plasma membrane ATPase; PMA1; Transmembrane segment 6

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE MAGNESIUM; FUNGAL ENZYME; FUNGAL PROTEIN; ORTHOVANADIC ACID; PROTON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE MEMBRANE SEGMENT 6; UNCLASSIFIED DRUG;

ALKALINITY; ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; CELL MEMBRANE; CELL PH; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STRUCTURE; ENZYME SYNTHESIS; FUNGAL GENE; FUNGUS GROWTH; IC 50; NONHUMAN; PMA1 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTON TRANSPORT; REACTION OPTIMIZATION; RESIDUE ANALYSIS; SECRETORY VESICLE; SITE DIRECTED MUTAGENESIS; STOICHIOMETRY; STRUCTURE ACTIVITY RELATION; WILD TYPE; YEAST CELL;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; HYDROLYSIS; KINETICS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTON-TRANSLOCATING ATPASES; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP;

MAMMALIA;

EID: 79955789016     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.11.034     Document Type: Article

References (59)

1. S. Lutsenko, and J.H. Kaplan Organization of P-type ATPases: significance of structural diversity Biochemistry 34 1995 15607 15613
2. J.V. Moller, B. Juul, and M. le Maire Structural organization, ion transport, and energy transduction of P-type ATPases Biochim. Biophys. Acta 1286 1996 1 51 (Pubitemid 26188366)
3. K.B. Axelsen, and M.G. Palmgren Evolution of substrate specificities in the P-type ATPase superfamily J. Mol. Evol. 46 1998 84 101 (Pubitemid 28047242)
4. R. Serrano, M.C. Kielland-Brandt, and G.R. Fink Yeast plasma membrane ATPase is essential for growth and has homology with (Na+ + K+), K+- and Ca2+-ATPases Nature 319 1986 689 693 (Pubitemid 16119457)
5. C. Toyoshima, M. Nakasako, H. Nomura, and H. Ogawa Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution Nature 405 2000 647 655 (Pubitemid 30428644)
6. C. Toyoshima, and H. Nomura Structural changes in the calcium pump accompanying the dissociation of calcium Nature 418 2002 605 611
7. J.P. Morth, B.P. Pedersen, M.S. Toustrup-Jensen, T.L. Sorensen, J. Petersen, J.P. Andersen, B. Vilsen, and P. Nissen Crystal structure of the sodium-potassium pump Nature 450 2007 1043 1049 (Pubitemid 350273618)
8. H. Ogawa, T. Shinoda, F. Cornelius, and C. Toyoshima Crystal structure of the sodium-potassium pump (Na+, K+-ATPase) with bound potassium and ouabain Proc. Natl Acad. Sci. USA 106 2009 13742 13747
9. T. Shinoda, H. Ogawa, F. Cornelius, and C. Toyoshima Crystal structure of the sodium-potassium pump at 2.4 A resolution Nature 459 2009 446 450
10. B.P. Pedersen, M.J. Buch-Pedersen, J.P. Morth, M.G. Palmgren, and P. Nissen Crystal structure of the plasma membrane proton pump Nature 450 2007 1111 1114 (Pubitemid 350273616)
11. M. Auer, G.A. Scarborough, and W. Kuhlbrandt Three-dimensional map of the plasma membrane H+-ATPase in the open conformation Nature 392 1998 840 843 (Pubitemid 28225328)
12. J.P. Andersen, and B. Vilsen Amino acids Asn796 and Thr799 of the Ca(2+)-ATPase of sarcoplasmic reticulum bind Ca2+ at different sites J. Biol. Chem. 269 1994 15931 15936
13. Z. Zhang, D. Lewis, C. Strock, G. Inesi, M. Nakasako, H. Nomura, and C. Toyoshima Detailed characterization of the cooperative mechanism of Ca(2+) binding and catalytic activation in the Ca(2+) transport (SERCA) ATPase Biochemistry 39 2000 8758 8767 (Pubitemid 30602785)
14. W.J. Rice, and D.H. MacLennan Scanning mutagenesis reveals a similar pattern of mutation sensitivity in transmembrane sequences M4, M5, and M6, but not in M8, of the Ca2+-ATPase of sarcoplasmic reticulum SERCA1a J. Biol. Chem. 271 1996 31412 31419 (Pubitemid 26408594)
15. T.A. Kuntzweiler, J.M. Arguello, and J.B. Lingrel Asp804 and Asp808 in the transmembrane domain of the Na, K-ATPase alpha subunit are cation coordinating residues J. Biol. Chem. 271 1996 29682 29687 (Pubitemid 26389593)
16. D.S. Perlin, M.J. San Francisco, C.W. Slayman, and B.P. Rosen H+/ATP stoichiometry of proton pumps from Neurospora crassa and Escherichia coli Arch. Biochem. Biophys. 248 1986 53 61 (Pubitemid 16045584)
17. D.P. Briskin, S. Basu, and S.M. Assmann Characterization of the red beet plasma membrane H+-ATPase reconstituted in a planar bilayer system Plant Physiol. 108 1995 393 398
18. D. Gradmann, U.P. Hansen, W.S. Long, C.L. Slayman, and J. Warncke Current-voltage relationships for the plasma membrane and its principal electrogenic pump in Neurospora crassa. I. Steady-state conditions J. Membr. Biol. 39 1978 333 367 (Pubitemid 8301416)
19. H.J. Apell How do P-type ATPases transport ions? Bioelectrochemistry 63 2004 149 156
20. E.A. Jewell-Motz, and J.B. Lingrel Site-directed mutagenesis of the sodium-potassium-ATPase: consequences of substitutions of negatively-charged amino acids localized in the transmembrane domains Biochemistry 32 1993 13523 13530 (Pubitemid 24020227)
21. J.M. Nielsen, P.A. Pedersen, S.J.D. Karlish, and P.L. Jorgensen Importance of intramembrane carboxylic acids for occlusion of K+ ions at equilibrium in renal Na, K-ATPase† Biochemistry 37 1998 1961 1968 (Pubitemid 28099820)
22. B. Vilsen, and J.P. Andersen Mutation to the glutamate in the fourth membrane segment of Na+, K+-ATPase and Ca2+-ATPase affects cation binding from both sides of the membrane and destabilizes the occluded enzyme forms† Biochemistry 37 1998 10961 10971 (Pubitemid 28368920)
23. V.V. Petrov, K.P. Padmanabha, R.K. Nakamoto, K.E. Allen, and C.W. Slayman Functional role of charged residues in the transmembrane segments of the yeast plasma membrane H+-ATPase J. Biol. Chem. 275 2000 15709 15716 (Pubitemid 30366868)
24. G. Guerra, V.V. Petrov, K.E. Allen, M. Miranda, J.P. Pardo, and C.W. Slayman Role of transmembrane segment M8 in the biogenesis and function of yeast plasma-membrane H(+)-ATPase Biochim. Biophys. Acta 1768 2007 2383 2392 (Pubitemid 47532021)
25. A. Cid, R. Perona, and R. Serrano Replacement of the promoter of the yeast plasma membrane ATPase gene by a galactose-dependent promoter and its physiological consequences Curr. Genet. 12 1987 105 110
26. R.K. Nakamoto, R. Rao, and C.W. Slayman Expression of the yeast plasma membrane [H+]ATPase in secretory vesicles. A new strategy for directed mutagenesis J. Biol. Chem. 266 1991 7940 7949 (Pubitemid 21906456)
27. P. Novick, C. Field, and R. Schekman Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway Cell 21 1980 205 215 (Pubitemid 10040069)
28. G. Sarkar, and S.S. Sommer The "megaprimer" method of site-directed mutagenesis Biotechniques 8 1990 404 407
29. G. Wang, M.J. Tamas, M.J. Hall, A. Pascual-Ahuir, and D.S. Perlin Probing conserved regions of the cytoplasmic LOOP1 segment linking transmembrane segments 2 and 3 of the Saccharomyces cerevisiae plasma membrane H+-ATPase J. Biol. Chem. 271 1996 25438 25445 (Pubitemid 26337917)
30. A. Ambesi, K.E. Allen, and C.W. Slayman Isolation of transport-competent secretory vesicles from Saccharomyces cerevisiae Anal. Biochem. 251 1997 127 129 (Pubitemid 27352158)
31. D. Perlin, S. Harris, D. Seto-Young, and J. Haber Defective H(+)-ATPase of hygromycin B-resistant pma1 mutants from Saccharomyces cerevisiae J. Biol. Chem. 264 1989 21857 21864 (Pubitemid 20028759)
32. V.V. Petrov, and C.W. Slayman Site-directed mutagenesis of the yeast PMA1 H(+)-ATPase. Structural and functional role of cysteine residues J. Biol. Chem. 270 1995 28535 28540
33. K.M. Hager, S.M. Mandala, J.W. Davenport, D.W. Speicher, E.J. Benz Jr., and C.W. Slayman Amino acid sequence of the plasma membrane ATPase of Neurospora crassa: deduction from genomic and cDNA sequences Proc. Natl Acad. Sci. USA 83 1986 7693 7697 (Pubitemid 17183913)
34. C.H. Fiske, and Y. Subbarow The colorimetric determination of phosphorus J. Biol. Chem. 66 1925 375 400
35. A. Fabiato, and F. Fabiato Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells J. Physiol. Paris 75 1979 463 505 (Pubitemid 10241310)
36. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
37. A. Bensadoun, and D. Weinstein Assay of proteins in the presence of interfering materials Anal. Biochem. 70 1976 241 250
38. K. Arnold, L. Bordoli, J. Kopp, and T. Schwede The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling Bioinformatics 22 2006 195 201 (Pubitemid 43205406)
39. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22 1994 4673 4680 (Pubitemid 24354800)
40. R.A. Laskowski, M.W. Macarthur, D.S. Moss, and J.M. Thornton Procheck-a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291
41. R.W. Hooft, G. Vriend, C. Sander, and E.E. Abola Errors in protein structures Nature 381 1996 272
42. C. Colovos, and T.O. Yeates Verification of protein structures: patterns of nonbonded atomic interactions Protein Sci. 2 1993 1511 1519 (Pubitemid 23262844)
43. J. Pontius, J. Richelle, and S.J. Wodak Deviations from standard atomic volumes as a quality measure for protein crystal structures J. Mol. Biol. 264 1996 121 136 (Pubitemid 26399998)
44. M.J. Sippl Recognition of errors in three-dimensional structures of proteins Proteins 17 1993 355 362 (Pubitemid 23358545)
45. M. Gerstein A resolution-sensitive procedure for comparing protein surfaces and its application to the comparison of antigen-combining sites Acta Crystallogr. A 48 1992 271 276
46. S.S. Gupta, N.D. DeWitt, K.E. Allen, and C.W. Slayman Evidence for a salt bridge between transmembrane segments 5 and 6 of the yeast plasma-membrane H+-ATPase J. Biol. Chem. 273 1998 34328 34334 (Pubitemid 29008910)
47. A. Ambesi, M. Miranda, K.E. Allen, and C.W. Slayman Stalk segment 4 of the yeast plasma membrane H+-ATPase. Mutational evidence for a role in the E1-E2 conformational change J. Biol. Chem. 275 2000 20545 20550 (Pubitemid 30457637)
48. M.B. Dutra, A. Ambesi, and C.W. Slayman Structure-function relationships in membrane segment 5 of the yeast Pma1 H+-ATPase J. Biol. Chem. 273 1998 17411 17417 (Pubitemid 28355069)
49. L. Segall, S.E. Daly, and R. Blostein Mechanistic basis for kinetic differences between the rat α1, α2, and α3 isoforms of the Na, K-ATPase J. Biol. Chem. 276 2001 31535 31541
50. S.E. Daly, L.K. Lane, and R. Blostein Functional consequences of amino-terminal diversity of the catalytic subunit of the Na, K-ATPase J. Biol. Chem. 269 1994 23944 23948 (Pubitemid 24300921)
51. K.P. Padmanabha, J.P. Pardo, V.V. Petrov, S. Sen Gupta, and C.W. Slayman Functional role of aspartyl and glutamyl residues in the membrane segments of the yeast PMA1 ATPase: interaction with DCCD Folia Microbiol. (Praha) 42 1997 245 249 (Pubitemid 127445244)
52. M.J. Buch-Pedersen, K. Venema, R. Serrano, and M.G. Palmgren 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 2000 39167 39173 (Pubitemid 32058933)
53. M.J. Buch-Pedersen, and M.G. Palmgren 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 2003 17845 17851 (Pubitemid 36799389)
54. D. Mandal, T.B. Woolf, and R. Rao Manganese selectivity of pmr1, the yeast secretory pathway ion pump, is defined by residue gln783 in transmembrane segment 6. Residue Asp778 is essential for cation transport J. Biol. Chem. 275 2000 23933 23938 (Pubitemid 30624682)
55. V. Leone, A. Krah, and J.D. Faraldo-Gomez On the question of hydronium binding to ATP-synthase membrane rotors Biophys. J. 99 2010 L53 55
56. S.J. Hersey, and G. Sachs Gastric acid secretion Physiol. Rev. 75 1995 155 189
57. M. Morii, M. Yamauchi, T. Ichikawa, T. Fujii, Y. Takahashi, S. Asano, N. Takeguchi, and H. Sakai Involvement of the H3O+-Lys-164 -Gln-161-Glu-345 charge transfer pathway in proton transport of gastric H+, K+-ATPase J. Biol. Chem. 283 2008 16876 16884
58. J. Warncke, and C.L. Slayman Metabolic modulation of stoichiometry in a proton pump Biochim. Biophys. Acta 591 1980 224 233
59. W. L. DeLano, The PYMOL molecular graphics system., http://www.pymol.org (2002).