Squeezing at entrance of proton transport pathway in proton-translocating pyrophosphatase upon substrate binding

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 19312-19320

  Huang, Yun Tzu ^a   Liu, Tseng Huang ^a   Lin, Shih Ming ^a   Chen, Yen Wei ^a   Pan, Yih Jiuan ^a   Lee, Ching Hung ^a   Sun, Yuh Ju ^a   Tseng, Fan Gang ^b   Pan, Rong Long ^a  

^a Institute of Bioinformatics and Structural Biology   (Taiwan)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM TETANI; CONFORMATIONAL CHANGE; CONSERVED POLAR RESIDUES; PROTON TRANSLOCATION; PROTON-TRANSPORT PATHWAYS; SINGLE-MOLECULE FRETS; TRANS-MEMBRANE DOMAINS; TRANSPORT PATHWAYS;

ACTIVATION ANALYSIS; CLOSTRIDIUM; MOLECULES;

PROTONS;

ALANINE; ARGININE; ASPARAGINE; CYSTEINE; GLYCINE; IMIDODIPHOSPHATE; INORGANIC PYROPHOSPHATASE; LYSINE; PROTON TRANSLOCATING PYROPHOSPHATASE; PYROPHOSPHORIC ACID DERIVATIVE; SERINE; UNCLASSIFIED DRUG; VALINE;

ARTICLE; CELL ORGANELLE; CLOSTRIDIUM TETANI; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME SUBSTRATE COMPLEX; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIGAND BINDING; MUTATION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTON TRANSPORT;

CLOSTRIDIUM TETANI PROTON-TRANSLOCATING PYROPHOSPHATASE; FLUORESCENCE RESONANCE ENERGY TRANSFER (FRET); MEMBRANE ENZYMES; MEMBRANE PROTEINS; PROTON PUMPS; PROTON TRANSPORT;

CLOSTRIDIUM TETANI; FLUORESCENCE RESONANCE ENERGY TRANSFER; INORGANIC PYROPHOSPHATASE; ION TRANSPORT; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTONS;

EID: 84880061092     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.469353     Document Type: Article

References (32)

1. Schumacher, K. (2006) Endomembrane proton pumps. Connecting membrane and vesicle transport. Curr. Opin. Plant Biol. 9, 595-600
2. Li, J., Yang, H., Peer, W. A., Richter, G., Blakeslee, J., Bandyopadhyay, A., Titapiwantakun, B., Undurraga, S., Khodakovskaya, M., Richards, E. L., Krizek, B., Murphy, A. S., Gilroy, S., and Gaxiola, R. (2005) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310, 121-125
3. Gaxiola R. A., Palmgren, M. G., and Schumacher, K. (2007) Plant proton pumps. FEBS Lett. 581, 2204-2214
4. Maeshima, M. (2001) Tonoplast transporters. Organization and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 469-497
5. Rea, P. A., Kim, Y., Sarafian, V., Poole, R. J., Davies, J. M., and Sanders, D. (1992) Vacuolar H+-translocating pyrophosphatase. A new category of ion translocase. Trends Biochem. Sci. 17, 348-353
6. Drozdowicz, Y. M., and Rea, P. A. (2001) Vacuolar H+ pyrophosphatase. From the evolutionary backwaters into the mainstream. Trends Plant Sci. 6, 206-211
7. Ginsburg, H. (2002) Abundant proton pumping in Plasmodium falciparum, but why? Trends Parasitol. 18, 483-486
8. Baltscheffsky, M. (1967) Inorganic pyrophosphate and ATP as energy donors in chromatophores from Rhodospirillum rubrum. Nature 216, 241-243
9. Maeshima, M. (2000) Vacuolar H+-pyrophosphatase. Biochim. Biophys. Acta 1465, 37-51
10. Belogurov, G. A., and Lahti, R. (2002) A lysine substitute for K+. A460K mutation eliminates K+ dependence in H+-pyrophosphatase of Carboxydothermus hydrogenoformans. J. Biol. Chem. 277, 49651-49654
11. Nakanishi, Y., Saijo, T., Wada, Y., and Maeshima, M. (2001) Mutagenic analysis of functional residues in putative substrate-binding site and acidic domains of vacuolar H+-pyrophosphatase. J. Biol. Chem. 276, 7654-7660
12. Sato, M. H., Kasahara, M., Ishii, N., Homareda, H., Matsui, H., and Yoshida, M. (1994) Purified vacuolar inorganic pyrophosphatase consisting of a 75-kDa polypeptide can pump H+ into reconstituted proteoliposomes. J. Biol. Chem. 269, 6725-6728
13. Tzeng, C. M., Yang, C. Y., Yang, S. J., Jiang, S. S., Kuo, S. Y., Hung, S. H., Ma, J. T., and Pan, R. L. (1996) Subunit structure of vacuolar proton pyrophosphatase as determined by radiation inactivation. Biochem. J. 316, 143-147
14. Lin, S. M., Tsai, J. Y., Hsiao, C. D., Huang, Y. T., Chiu, C. L., Liu, M. H., Tung, J. Y., Liu, T. H., Pan, R. L., and Sun, Y. J. (2012) Crystal structure of a membrane-embedded H+-translocating pyrophosphatase. Nature 484, 399-403
15. Lee, C. H., Pan, Y. J., Huang, Y. T., Liu, T. H., Hsu, S. H., Lee, C. H., Chen, Y. W., Lin, S. M., Huang, L. K., and Pan, R. L. (2011) Identification of essential lysines involved in substrate binding of vacuolar H+-pyrophosphatase. J. Biol. Chem. 286, 11970-11976
16. Hirono, M., Nakanishi, Y., and Maeshima, M. (2007) Essential amino acid residues in the central transmembrane domains and loops for energy coupling of Streptomyces coelicolor A3(2)H+-pyrophosphatase. Biochim. Biophys. Acta 1767, 930-939
17. Huang, Y. T., Liu, T. H., Chen, Y. W., Lee, C. H., Chen, H. H., Huang, T. W., Hsu, S. H., Lin S. M., Pan, Y. J., Lee, C. H., Hsu, I. C., Tseng, F. G., Fu, C. C., and Pan, R. L. (2010) Distance variations between active sites of H+-pyrophosphatase determined by fluorescence resonance energy transfer. J. Biol. Chem. 285, 23655-23664
18. Pan, Y. J., Lee, C. H., Hsu, S. H., Huang, Y. T., Lee, C. H., Liu, T. H., Chen, Y. W., Lin, S. M., and Pan, R. L. (2011) The transmembrane domain 6 of vacuolar H+-pyrophosphatase mediates protein targeting and proton transport. Biochim. Biophys. Acta 1807, 59-67
19. Van, R. C., Pan, Y. J., Hsu, S. H., Huang, Y. T., Hsiao, Y. Y., and Pan, R. L. (2005) Role of transmembrane segment 5 of the plant vacuolar H+-pyrophosphatase. Biochim. Biophys. Acta 1709, 84-94
20. Hsiao, Y. Y., Pan, Y. J., Hsu, S. H., Huang, Y. T., Liu, T. H., Lee, C. H., Lee, C. H., Liu, P. F., Chang, W. C., Wang, Y. K., Chien, L. F., and Pan, R. L. (2007) Functional roles of arginine residues in mung bean vacuolar H+- pyrophosphatase. Biochim. Biophys. Acta 1767, 965-973
21. Zhen, R. G., Kim, E. J., and Rea P. A. (1997) Acidic residues necessary for pyrophosphate-energized pumping and inhibition of the vacuolar H+- pyrophosphatase by N,N'-dicyclohexylcarbodiimide. J. Biol. Chem. 272, 22340-22348
22. Schultz, A., and Baltscheffsky, M. (2003) Properties of mutated Rhodospirillum rubrum H+-pyrophosphatase expressed in Escherichia coli. Biochim. Biophys. Acta 1607, 141-151
23. Kirsch, R. D., and Joly, E. (1998) An improved PCR-mutagenesis strategy for two-site mutagenesis or sequence swapping between related genes. Nucleic Acids Res. 26, 1848-1850
24. Nomura, S. M., Kondoh, S., Asayama, W., Asada, A., Nishikawa, S., and Akiyoshi, K. (2008) Direct preparation of giant proteo-liposomes by in vitro membrane protein synthesis. J. Biotechnol. 133, 190-195
25. Granier, S., Kim, S., Shafer, A. M., Ratnala, V. R., Fung, J. J., Zare, R. N., and Kobilka, B. (2007) Structure and conformational changes in the C-terminal domain of the β2-adrenoceptor. Insights from fluorescence resonance energy transfer studies. J. Biol. Chem. 282, 13895-13905
26. Lee, N. K., Kapanidis, A. N., Wang, Y., Michalet, X., Mukhopadhyay, J., Ebright, R. H., and Weiss, S. (2005) Accurate FRET measurements within single diffusing biomolecules using alternating-laser excitation. Biophys. J. 88, 2939-2953
27. Förster, T. (1948) Zwischenmolekulare energiewanderung und fluoreszenz. Annalen der Physik. 2, 55-75
28. Lidke, K. A., Rieger, B., Lidke, D. S., and Jovin, T. M. (2005) The role of photon statistics in fluorescence anisotropy imaging. IEEE Trans. Image Process. 14, 1237-1245
29. Ishii, Y., Yoshida, T., Funatsu, T., Wazawa, T., and Yanagida, T. (1999) Fluorescence resonance energy transfer between single fluorophores attached to a coiled-coil protein in aqueous solution. Chem. Phys. 247, 163-173
30. Greenleaf, W. J., Woodside, M. T., and Block, S. M. (2007) High-resolution, single-molecule measurements of biomolecular motion. Annu. Rev. Biophys. Biomol. Struct. 36, 171-190
31. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISSMODEL Workspace. A web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201
32. Kiefer, F., Arnold, K., Künzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL repository and associated resources. Nucleic Acids Res. 37, 387-392