全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2013 

Flexibility within the Rotor and Stators of the Vacuolar H+-ATPase

DOI: 10.1371/journal.pone.0082207

Full-Text   Cite this paper   Add to My Lib

Abstract:

The V-ATPase is a membrane-bound protein complex which pumps protons across the membrane to generate a large proton motive force through the coupling of an ATP-driven 3-stroke rotary motor (V1) to a multistroke proton pump (Vo). This is done with near 100% efficiency, which is achieved in part by flexibility within the central rotor axle and stator connections, allowing the system to flex to minimise the free energy loss of conformational changes during catalysis. We have used electron microscopy to reveal distinctive bending along the V-ATPase complex, leading to angular displacement of the V1 domain relative to the Vo domain to a maximum of ~30°. This has been complemented by elastic network normal mode analysis that shows both flexing and twisting with the compliance being located in the rotor axle, stator filaments, or both. This study provides direct evidence of flexibility within the V-ATPase and by implication in related rotary ATPases, a feature predicted to be important for regulation and their high energetic efficiencies.

References

[1]  Muench SP, Trinick J, Harrison MA (2011) Structural divergence of the rotary ATPases. Q Rev Biophys 44: 311-356. doi:10.1017/S0033583510000338. PubMed: 21426606.
[2]  Nishi T, Forgac M (2002) The vacuolar (H+)-ATPases--nature's most versatile proton pumps. Nat Rev Mol Cell Biol 3: 94-103. doi:10.1038/nrm729. PubMed: 11836511.
[3]  Yoshida M, Muneyuki E, Hisabori T (2001) ATP synthase- a marvellous rotary engine of the cell. NatRevMolCell Biol 2: 669-677.
[4]  Imamura H, Nakano M, Noji H, Muneyuki E, Ohkuma S et al. (2003) Evidence for rotation of V1-ATPase. Proc Natl Acad Sci U S A 100: 2312-2315. doi:10.1073/pnas.0436796100. PubMed: 12598655.
[5]  Noji H, Yasuda R, Yoshida M, Kinosita K Jr. (1997) Direct observation of the rotation of F1-ATPase. Nature 386: 299-302. doi:10.1038/386299a0. PubMed: 9069291.
[6]  Boyer PD (1997) The ATP synthase- a splendid molecular machine. Annu_Rev_Biochem 66: 717-749.
[7]  Sambongi Y, Iko Y, Tanabe M, Omote H, Iwamoto-Kihara A et al. (1999) Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. Science 286: 1722-1724. doi:10.1126/science.286.5445.1722. PubMed: 10576736.
[8]  Yokoyama K, Nakano M, Imamura H, Yoshida M, Tamakoshi M (2003) Rotation of the proteolipid ring in the V-ATPase. J Biol Chem 278: 24255-24258. doi:10.1074/jbc.M303104200. PubMed: 12707282.
[9]  Grabe M, Wang H, Oster G (2000) The mechanochemistry of V-ATPase proton pumps. Biophys J 78: 2798-2813. doi:10.1016/S0006-3495(00)76823-8. PubMed: 10827963.
[10]  Hutcheon ML, Duncan TM, Ngai H, Cross RL (2001) Energy-driven subunit rotation at the interface between subunit a and the c oligomer in the F(O) sector of Escherichia coli ATP synthase. Proc Natl Acad Sci U S A 98: 8519-8524. doi:10.1073/pnas.151236798. PubMed: 11438702.
[11]  Zhang Z, Zheng Y, Mazon H, Milgrom E, Kitagawa N et al. (2008) Structure of the yeast vacuolar ATPase. J Biol Chem 283: 35983-35995. PubMed: 18955482.
[12]  Muench SP, Huss M, Song CF, Phillips C, Wieczorek H et al. (2009) Cryo-electron microscopy of the vacuolar ATPase motor reveals its mechanical and regulatory complexity. J Mol Biol 386: 989-999. doi:10.1016/j.jmb.2009.01.014. PubMed: 19244615.
[13]  Benlekbir S, Bueler SA, Rubinstein JL (2012) Structure of the vacuolar-type ATPase from Saccharomyces cerevisiae at 11-A resolution. Nature Structural and Molecular Biology 19: 1356-1362. doi:10.1038/nsmb.2422.
[14]  Rubinstein JL, Walker JE, Henderson R (2003) Structure of the mitochondrial ATP synthase by electron cryomicroscopy. EMBO J 22: 6182-6192. doi:10.1093/emboj/cdg608. PubMed: 14633978.
[15]  Lau WC, Rubinstein JL (2010) Structure of intact Thermus thermophilus V-ATPase by cryo-EM reveals organization of the membrane-bound V(O) motor. Proc Natl Acad Sci U S A 107: 1367-1372. doi:10.1073/pnas.0911085107. PubMed: 20080582.
[16]  Vonck J, Pisa KY, Morgner N, Brutschy B, Müller V (2009) Three-dimensional structure of A1A0ATP synthase from the hyperthermophilic archeon Pyrococcus furiosus by electron microscopy. Biol_Chem 284: 10110-10119.
[17]  Murata T, Yamato I, Kakinuma Y, Leslie AGW, Walker JE (2005) Structure of the rotor of the V-type Na+-ATPase from Enterococcus hirae. Science 308: 654-659. doi:10.1126/science.1110064. PubMed: 15802565.
[18]  Vollmar M, Schlieper D, Winn M, Buchner C, Groth G (2009) Structure of the c(14) Rotor Ring of the Proton Translocating Chloroplast ATP Synthase. Biol_Chem 284: 18228-18235.
[19]  Meier T, Polzer P, Diederichs K, Welte W, Dimroth P (2005) Structure of the Rotor Ring of F-Type Na+-ATPase from Ilyobacter tartaricus. Science 308: 659-662. doi:10.1126/science.1111199. PubMed: 15860619.
[20]  Pogoryelov D, Yu J, Meier T, Vonck J, Dimroth P et al. (2005) The c15 ring of the Spirulina platensis F-ATP synthase: F1/F0 symmetry mismatch is not obligatory. EMBO Rep 6: 1040-1044. doi:10.1038/sj.embor.7400517. PubMed: 16170308.
[21]  Mitome N, Suzuki T, Hayashi S, Yoshida M (2004) Thermophilic ATP synthase has a decamer c-ring: indication of noninteger 10:3 H+/ATP ratio and permissive elastic coupling. Proc Natl Acad Sci U S A 101: 12159-12164. doi:10.1073/pnas.0403545101. PubMed: 15302927.
[22]  Pogoryelov D, Reichen C, Klyszejko AL, Brunisholz R, Muller DJ et al. (2007) The oligomeric state of c rings from cyanobacterial F-ATP synthases varies from 13 to 15. J Bacteriol 189: 5895-5902. doi:10.1128/JB.00581-07. PubMed: 17545285.
[23]  Grabe M, Wang H, Oster G (2000) The mechanochemistry of V-ATPase proton pumps. Biophys J 78: 2798-3813. PubMed: 10827963.
[24]  Uchihashi T, Iino R, Ando T, Noji H (2011) High-speed atomic force microscopy reveals rotary catalysis of rotorless F(1)-ATPase. Science 333: 755-758. doi:10.1126/science.1205510. PubMed: 21817054.
[25]  Abrahams JP, Leslie AG, Lutter R, Walker JE (1994) Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370: 621-628. doi:10.1038/370621a0. PubMed: 8065448.
[26]  Giraud MF, Paumard P, Sanchez C, Brethes D, Velours J et al. (2012) Rotor architecture in the yeast and bovine F1-c-ring complexes of F-ATP synthase. J Struct Biol 177: 490-497.
[27]  Stock D, Leslie AG, Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286: 1700-1705. doi:10.1126/science.286.5445.1700. PubMed: 10576729.
[28]  Bernal RA, Stock D (2004) Three-dimensional structure of the intact Thermus thermophilus H+-ATPase/synthase by electron microscopy. Structure 12: 1789-1798. doi:10.1016/j.str.2004.07.017. PubMed: 15458628.
[29]  B?ttcher B, Bertsche I, Reuter R, Gr?ber P (2000) Direct visualisation of conformational changes in EF(0)F(1) by electron microscopy. J Mol Biol 296: 449-457. doi:10.1006/jmbi.1999.3435. PubMed: 10669600.
[30]  Matthies D, Haberstock S, Joos F, D?tsch V, Vonck J et al. (2011) Cell-free expression and assembly of ATP synthase. J Mol Biol 413: 593-603. doi:10.1016/j.jmb.2011.08.055. PubMed: 21925509.
[31]  Stewart AG, Lee LK, Donohoe M, Chaston JJ, Stock D (2012) The dynamic stator stalk of rotary ATPases. Nat Commun 3: 687. doi:10.1038/ncomms1693. PubMed: 22353718.
[32]  Sumner JP, Dow JA, Earley FG, Klein U, J?ger D et al. (1995) Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J Biol Chem 270: 5649-5653. doi:10.1074/jbc.270.10.5649. PubMed: 7890686.
[33]  Parra KJ, Kane PM (1998) Reversible association between the V1 and V0 domains of yeast vacuolar H+-ATPase is an unconventional glucose-induced effect. Mol Cell Biol 18: 7064-7074. PubMed: 9819393.
[34]  Voss M, Vitavska O, Walz B, Wieczorek H, Baumann O (2007) Stimulus-induced Phosphorylation of Vacuolar H+-ATPase by Protein Kinase A. J Biol Chem 282: 33735-33742. doi:10.1074/jbc.M703368200. PubMed: 17872947.
[35]  Hong-Hermesdorf A, Brüx A, Grüber A, Grüber G, Schumacher K (2006) A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Lett 580: 932-939. doi:10.1016/j.febslet.2006.01.018. PubMed: 16427632.
[36]  Bond A, Forgac M (2008) The Ras/cAMP/protein kinase A pathway regulates glucose-dependent assembly of the vacuolar (H+)-ATPase in yeast. J Biol Chem 283: 36513-36521. doi:10.1074/jbc.M805232200. PubMed: 18936098.
[37]  Muench SP, Scheres SH, Huss M, Phillips C, Vitavska O et al. (2013) Subunit positioning and stator filament stiffness in regulation and power transmission in the V1 motor of the Manduca sexta V-ATPase. J Mol Biol Epub ahead of print. PubMed: 24075871.
[38]  Tani K, Arthur CP, Tamakoshi M, Yokoyama K, Mitsuoka K et al. (2013) Visualization of two distinct states of disassembly in the bacterial V-ATPase from Thermus thermophilus. Microscopy (Oxf) 62: 467-474. doi:10.1093/jmicro/dft020. PubMed: 23572213.
[39]  Uchida E, Ohsumi Y, Anraku Y (1985) Purification and properties of H+-translocating, Mg2+-adenosine triphosphatase from vacuolar membranes of Saccharomyces cerevisiae. J Biol Chem 260: 1090-1095. PubMed: 2857169.
[40]  Harrison M, Powell B, Finbow ME, Findlay JB (2000) Identification of lipid-accessible sites on the nephrops 16-kDa proteolipid incorporated into a hybrid vacuolar H(+)-ATPase: site-directed labeling with N-(1-Pyrenyl)cyclohexylcarbodiimide and fluorescence quenching analysis. Biochemistry 39: 7531-7537. doi:10.1021/bi000159o. PubMed: 10858302.
[41]  Schweikl H, Klein U, Schindlbeck M, Wieczorek H (1989) A vacuolar-type ATPase, partially purified from potassium transporting plasma membranes of tobacco hornworm midgut. J Biol Chem 264: 11136-11142. PubMed: 2525554.
[42]  Huss M, Ingenhorst G, K?nig S, Gassel M, Dr?se S et al. (2002) Concanamycin A, the specific inhibitor of V-ATPases, binds to the V(o) subunit c. J Biol Chem 277: 40544-40548. doi:10.1074/jbc.M207345200. PubMed: 12186879.
[43]  Walker M, Knight P, Trinick J (1985) Negative staining of myosin molecules. J Mol Biol 184: 535-542. doi:10.1016/0022-2836(85)90300-6. PubMed: 2413217.
[44]  Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97. doi:10.1006/jsbi.1999.4174. PubMed: 10600563.
[45]  Frank J, Radermacher M, Penczek P, Zhu J, Li Y et al. (1996) SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116: 190-199. doi:10.1006/jsbi.1996.0030. PubMed: 8742743.
[46]  van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116: 17-24. doi:10.1006/jsbi.1996.0004. PubMed: 8742718.
[47]  Burgess SA, Walker ML, Thirumurugan K, Trinick J, Knight PJ (2004) Use of negative stain and single-particle image processing to explore dynamic properties of flexible macromolecules. J Struct Biol 147: 247-258. doi:10.1016/j.jsb.2004.04.004. PubMed: 15450294.
[48]  Tang G, Peng L, Baldwin PR, Mann DS, Jiang W et al. (2007) EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol 157: 38-46. doi:10.1016/j.jsb.2006.05.009. PubMed: 16859925.
[49]  Wriggers W, Milligan RA, Schulten K, McCammon JA (1998) Self-organizing neural networks bridge the biomolecular resolution gap. J Mol Biol 284: 1247-1254. doi:10.1006/jmbi.1998.2232. PubMed: 9878345.
[50]  Birmanns S, Rusu M, Wriggers W (2011) Using Sculptor and Situs for simultaneous assembly of atomic components into low-resolution shapes. J Struct Biol 173: 428-435. doi:10.1016/j.jsb.2010.11.002. PubMed: 21078392.
[51]  Stember JN, Wriggers W (2009) Bend-twist-stretch model for coarse elastic network simulation of biomolecular motion. J Chem Phys 131: 074112. doi:10.1063/1.3167410. PubMed: 19708737.
[52]  Chacón P, Tama F, Wriggers W (2003) Mega-Dalton biomolecular motion captured from electron microscopy reconstructions. J Mol Biol 326: 485-492. doi:10.1016/S0022-2836(02)01426-2. PubMed: 12559916.
[53]  Tama F, Wriggers W, Brooks CL 3rd (2002) Exploring global distortions of biological macromolecules and assemblies from low-resolution structural information and elastic network theory. J Mol Biol 321: 297-305. doi:10.1016/S0022-2836(02)00627-7. PubMed: 12144786.
[54]  Brink J, Ludtke SJ, Kong Y, Wakil SJ, Ma J et al. (2004) Experimental verification of conformational variation of human fatty acid synthase as predicted by normal mode analysis. Structure 12: 185-191. doi:10.1016/j.str.2004.01.015. PubMed: 14962379.
[55]  Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM et al. (2004) UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612. doi:10.1002/jcc.20084. PubMed: 15264254.
[56]  Kinosita K Jr., Yasuda R, Noji H, Adachi K (2000) A rotary molecular motor that can work at near 100% efficiency. Philos Trans R Soc Lond B Biol Sci 355: 473-489. doi:10.1098/rstb.2000.0589. PubMed: 10836501.
[57]  W?chter A, Bi Y, Dunn SD, Cain BD, Sielaff H et al. (2011) Two rotary motors in F-ATP synthase are elastically coupled by a flexible rotor and a stiff stator stalk. Proc Natl Acad Sci U S A 108: 3924-3929. doi:10.1073/pnas.1011581108. PubMed: 21368147.
[58]  Sielaff H, Rennekamp H, W?chter A, Xie H, Hilbers F et al. (2008) Domain compliance and elastic power transmission in rotary F(O)F(1)-ATPase. Proc Natl Acad Sci U S A 105: 17760-17765. doi:10.1073/pnas.0807683105. PubMed: 19001275.
[59]  Sugawa M, Okada KA, Masaike T, Nishizaka T (2011) A change in the radius of rotation of F1-ATPase indicates a tilting motion of the central shaft. Biophys J 101: 2201-2206. doi:10.1016/j.bpj.2011.09.016. PubMed: 22067159.
[60]  Rees DM, Leslie AG, Walker JE (2009) The structure of the membrane extrinsic region of bovine ATP synthase. Proc Natl Acad Sci U S A 106: 21597-21601. doi:10.1073/pnas.0910365106. PubMed: 19995987.
[61]  Imamura H, Takeda M, Funamoto S, Shimabukuro K, Yoshida M et al. (2005) Rotation scheme of V1-motor is different from that of F1-motor. Proc Natl Acad Sci U S A 102: 17929-17933. doi:10.1073/pnas.0507764102. PubMed: 16330761.
[62]  Dickson VK, Silvester JA, Fearnley IM, Leslie AG, Walker JE (2006) On the structure of the stator of the mitochondrial ATP synthase. EMBO J 25: 2911-2918. doi:10.1038/sj.emboj.7601177. PubMed: 16791136.
[63]  Diepholz M, B?rsch M, B?ttcher B (2008) Structural organization of the V-ATPase and its implications for regulatory assembly and disassembly. Biochem Soc Trans 36: 1027-1031. doi:10.1042/BST0361027. PubMed: 18793183.
[64]  Lee LK, Stewart AG, Donohoe M, Bernal RA, Stock D (2010) The structure of the peripheral stalk of Thermus thermophilus H+-ATPase/synthase. Nat Struct Mol Biol 17: 373-378. doi:10.1038/nsmb.1761. PubMed: 20173764.
[65]  Diepholz M, Venzke D, Prinz S, Batisse C, Fl?rchinger B et al. (2008) A different conformation for EGC stator subcomplex in solution and in the assembled yeast V-ATPase: possible implications for regulatory disassembly. Structure 16: 1789-1798. doi:10.1016/j.str.2008.09.010. PubMed: 19081055.
[66]  Norgett EE, Borthwick KJ, Al-Lamki RS, Su Y, Smith AN et al. (2007) V1 and V0 domains of the human H+-ATPase are linked by an interaction between the G and a subunits. J Biol Chem 282: 14421-14427. doi:10.1074/jbc.M701226200. PubMed: 17360703.
[67]  Gibbons C, Montgomery MG, Leslie AG, Walker JE (2000) The structure of the central stalk in bovine F(1)-ATPase at 2.4 A resolution. Nat Struct Biol 7: 1055-1061. doi:10.1038/80981. PubMed: 11062563.
[68]  Numoto N, Hasegawa Y, Takeda K, Miki K (2009) Inter-subunit interaction and quaternary rearrangement defined by the central stalk of prokaryotic V1-ATPase. EMBO Rep 10: 1228-1234. doi:10.1038/embor.2009.202. PubMed: 19779483.
[69]  Bahar I, Lezon TR, Yang LW, Eyal E (2010) Global dynamics of proteins: bridging between structure and function. Annu Rev Biophys 39: 23-42. doi:10.1146/annurev.biophys.093008.131258. PubMed: 20192781.
[70]  Huss M, Wieczorek H (2007) Influence of ATP and ADP on dissociation of the V-ATPase into its V(1) and V(O) complexes. FEBS Lett 581: 5566-5572. doi:10.1016/j.febslet.2007.11.004. PubMed: 17997985.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133