Protein-protein interactions within the ensemble, eukaryotic V-ATPase, and its concerted interactions with cellular machineries

Progress in Biophysics and Molecular Biology

Volumn 119, Issue 1, 2015, Pages 84-93

  Balakrishna, Asha Manikkoth ^a   Manimekalai, Malathy Sony Subramanian ^a   Grüber, Gerhard ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Bioenergetics; Coupling; Molecular engine; Saccharomyces cerevisiae; Structural biology; V ATPase; Vacuolar ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PROTEIN BINDING; PROTEIN SUBUNIT; PROTON;

AMINO ACID SEQUENCE; ANIMAL; BIOCATALYSIS; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; EUKARYOTE; HUMAN; METABOLISM; PROTEIN SUBUNIT;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; BIOCATALYSIS; EUKARYOTA; HUMANS; PROTEIN BINDING; PROTEIN SUBUNITS; PROTONS;

EID: 84940900166     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2015.05.003     Document Type: Review

References (65)

1. 0-type ATPase. J. Biol. Chem. 1996, 271:13888-13891.
2. 1-ATPase based on asymmetric crystal structures. Nature 2013, 493:703-707.
3. Armbrüster A., Svergun D.I., Coskun Ü., Juliano S., Bailer S.M., Grüber G. Structural analysis of the stalk subunit Vma5p of the Yeast V-ATPase in solution. FEBS Lett. 2004, 570:119-125.
4. Armbrüster A., Hohn C., Hermesdorf A., Schumacher K., Börsch M., Grüber G. Evidence for major structural changes in subunit C of the vacuolar ATPase due to nucleotide binding. FEBS Lett. 2005, 579:1961-1967.
5. Balakrishna A.M., Basak S., Manimekalai M.S.S., Grüber G. Crystal structure of subunits D and F in complex give insight into energy transmission of the eukaryotic V-ATPase from Saccharomyces cerevisiae. J. Biol. Chem. 2015, 290:3183-3196.
6. Basak S., Lim J., Manimekalai M.S., Balakrishna A.M., Grüber G. Crystal and NMR Structures Give Insights into the role and dynamics of subunit F of the eukaryotic V-ATPase from Saccharomyces cerevisiae. J. Biol. Chem. 2013, 288:11930-11939.
7. +-releasing channel. J. Cell. Biol. 2003, 162:211-222.
8. Benlekbir S., Bueler S.A., Rubinstein J.L. Structure of the vacuolar-type ATPase from Saccharomyces cerevisiae at 11-Å resolution. Nat. Struct. Mol. Biol. 2012, 19:1356-1362.
9. +-ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol. 2006, 209:577-5894.
10. Biasini M., Bienert S., Waterhouse A., Arnold K., Studer G., Schmidt T., Kiefer F., Cassarino T.G., Bertoni M., Bordoli L., Schwede T. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 2014, 42:W252-W258.
11. Breton S., Brown D. Regulation of luminal acidification by the V-ATPAse. Physiology 2013, 28:318-329.
12. Cherfils J., Ménétrey J., Mathieu M., Bras G.L., Robineau S., Béraud-Dufour S., Antonny B., Chardin P. Structure of the Sec7 domain of the Arf exchange factor ARNO. Nature 1998, 392:101-105.
13. Cotter K., Capecci J., Sennoune S., Huss M., Maier M., Martinez-Zaguilan R., Forgac M. Activity of plasma membrane V-ATPases is critical for the invasion of MDA-MB231 breast cancer cells. J. Biol. Chem. 2015, 290:3680-3692.
14. D'Souza-Schorey C., Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell. Biol. 2006, 7:347-358.
15. de Vries S.J., van Dijk M., Bonvin A.M.J.J. The HADDOCK web server for data-driven biomolecular docking. Nat. Prot. 2010, 5:883-897.
16. Diepholz M., Venzke D., Prinz S., Batisse C., Florchinger B., Rössle M., Svergun D.I., Böttcher B., Fethiere J. A different conformation for EGC-stator subcomplex in solution and in the assembled yeast V-ATPase: possible implications for regulatory disassembly. Structure 2008, 16:1789-1798.
17. Dip P.V., Saw W.G., Rössle M., Marshansky V., Grüber G. Solution structure of subunit a, a104-363, of the Saccharomyces cerevisiae V-ATPase and the importance of its C-terminus in structure formation. J. Bioenergy Biomembr. 2012, 44:341-350.
18. Dip P.V., Kamariah N., Manimekalai M.S.S., Nartey W., Balakrishna A.M., Eisenhaber F., Eisenhaber B., Grüber G. Structure, mechanism and ensemble formation of the Alkylhydroperoxide reductase subunits AhpC and AhpF from Escherichia coli. Acta Cryst. D. 2014, 70:2848-2862.
19. Efeyan A., Zoncu R., Sabatini D.M. Amino acids and mTORC1: from lysosomes to disease. Trends Mol. Med. 2012, 18:524-533.
20. Flannery A.R., Graham L.A., Stevens T.H. Topological characterization of the c, c', and c″ subunits of the vacuolar ATPase from the Saccharomyces cerevisiae. J. Biol. Chem. 2004, 279:39856-39862.
21. Forgac M. Vacuolar ATPases: rotatory proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell. Biol. 2007, 11:917-929.
22. Frattini A., Orchard P.J., Sobacchi C., Giliani S., Abinun M., Mattsson J.P., Keeling D.J., Andersson A.K., Wallbrandt P., Zecca L., Notarangelo L.D., Vezzoni P., Villa A. Defects in TCIRG1 subunit of the vacuolar proton pump are responsible for a subset of human autosomal recessive osteopetrosis. Nat. Gen. 2000, 25:343-346.
23. Glatter O., Kratky O. Small-angle X-ray Scattering 1982, Academic Press, London, UK.
24. Graham L.A., Flannery A.R., Stevens T.H. Structure and assembly of the yeast V-ATPase. J. Bioenergy Biomembr. 2003, 35:301-312.
25. 0). BioEssays 2008, 30:1-14.
26. Guinier A., Fournet G. Small-angle Scattering of X-rays 1955, Wiley, New York.
27. Hilario E., Gogarten J.P. The prokaryote-to-eucaryote transition reflected in the evolution of the V/F/A-ATPase catalytic and proteolipid subunits. J. Mol. Evol. 1998, 46:703-715.
28. +-ATPase contains a filamentous actin binding site. J. Biol. Chem. 2000, 275:32331-32337.
29. Hong-Hermesdorf A., Brux A., Grüber A., Grüber G., Schumacher K. A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Lett. 2006, 580:932-939.
30. Hosokawa H., Dip P.V., Merkulova M., Bakulina A., Zhuang Z., Khatri A., Jian X., Keating S.M., Bueler S.A., Rubinstein J.L., Randazzo P.A., Ausiello D.A., Grüber G., Marshansky V. The N-terminus of a-subunit isoforms is involved in signaling between V-ATPase and cytohesin-2. J. Biol. Chem. 2013, 288:896-5913.
31. Hurtado-Lorenzo A., Skinner M., El Annan J., Futai M., Sun-Wada G.H., Bourgoin S., Casanova J., Wildeman A., Bechoua S., Ausiello D.A., Brown D., Marshansky V. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat. Cell. Biol. 2006, 6:124-136.
32. Iwata M., Imamura H., Stambouli E., Ikeda C., Tamakoshi M., Nagata K., Makyio H., Hankamer B., Barber J., Yoshida M., Yokoyama K., Iwata S. Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuole-type ATPase. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:59-64.
33. 1 domain by interaction with the rotary subunit F. J. Biol. Chem. 2008, 283:4512-4519.
34. Kane P.M. Disassembly and reassembly of the yeast vacuolar H(+)-ATPase in vivo. J. Biol. Chem. 1995, 270:17025-17032.
35. +-ATPase cause renal tubular acidosis with sensorineural deafness. Nat. Gen. 1999, 21:84-90.
36. Kelley L.A., Stemberg M.J.E. Protein structure prediction on a web: a case study using the Phyre-server. Nat. Protoc. 2009, 4:363-371.
37. Kishikawa J., Ibuki T., Nakamura S., Nakanishi A., Minamino T., Miyata T., Namba K., Konno H., Ueno H., Imada K., Yokoyama K. Common evolutionary origin for the rotor domain of rotary ATPases and flagellar protein export apparatus. PLoS One 2013, 28:e64695.
38. Konarev P.V., Volkov V.V., Sokolova A.V., Koch M.H.J., Svergun D.I. PRIMUS - a windows-PC based system for small-angle scattering data analysis. J. Appl. Crystallogr. 2003, 36:1277-1282.
39. +-ATPase cause infantile malignant oeteopetrosis. Hum. Mol. Gen. 2000, 9:2059-2063.
40. Lee S.H., Rho J., Jeong D., Sul J.Y., Kim T., Kang J.S., Miyamoto T., Suda T., Lee S.K., Pignolo R.J., Koczon-Jaremko B., Lorenzo J., Choi Y. V-ATPase Vo subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat. Med. 2006, 12:1403-1409.
41. Marshansky V., Rubinstein J., Grüber G. Eukaryotic V-ATPase: novel structural findings and functional insights. Biochim. Biophys. Acta-Bioenergetics 2014, 1837:857-879.
42. Merkulova M., Bakulina A., Thaker Y.R., Grüber G., Marshansky V. Specific motifs of the V-ATPase a2-subunit isoform interact with catalytic and regulatory domains of ARNO. Biochim. Biophys. Acta 2010, 1797:1398-1409.
43. 1 motor of the Manduca sexta V-ATPase. J. Mol. Biol. 2014, 426:286-300.
44. Omri D., Felix F., Nathan N. Crystal structure of yeast V-ATPase subunit C reveals its stator function. EMBO Rep. 2004, 5:1148-1152.
45. Oot R.A., Huang L.-S., Berry E.A., Wilkens S. Crystal structure of the yeast vacuolar ATPase Heterotrimeric EGC-head peripheral stalk complex. Structure 2012, 20:1881-1892.
46. Petoukhov M.V., Franke D., Shkumatov A.V., Tria G., Kikhney A.G., Gajda M., Gorba C., Mertens H.D.T., Konarev P.V., Svergun D.I. New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr. 2012, 45:342-350.
47. 1-ATPase determined by three-dimensional electron microscopy of single particles. J. Struct. Biol. 2001, 135:26-37.
48. +-ATPase rotary motor reveals new mechanistic insights. Structure 2015, 23:1-11.
49. O ATPase determined by solution NMR spectroscopy. J. Bioenergy Biomembr. 2011, 43:447-455.
50. Sagermann M., Stevens T.H., Matthews B.W. Crystal structure of the regulatory subunit H of the V-type ATPase of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:7134-7139.
51. +-ATPase-an enzyme for all seasons. Pflügers Arch. Eur. J. Physiol. 2009, 457:581-587.
52. Srinivasan S., Vyas N.K., Baker M.L., Quiocho F.A. Crystal structure of the cytoplasmic N-terminal domain of subunit I, a homolog of subunit a, of V-ATPase. J. Mol. Biol. 2011, 412:14-21.
53. Sumner J.P., Dow J.A., Earley F.G., Klein U., Jager D., Wieczorek H. Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J. Biol. Chem. 1995, 270:5649-5653.
54. Sun-Wada G.H., Toyomura T., Murata Y., Yamamoto A., Futai M., Wada Y. The a3 isoform of V-ATPase regulates insulin secretion from pancreatic β-cells. J. Cell. Sci. 2006, 119:4531-4540.
55. Svergun D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 1992, 25:495-503.
56. Tabke K., Albertmelcher A., Vitavska O., Huss M., Schmitz H.P., Wieczorek H. Reversible disassembly of the yeast V-ATPase revisited under in vivo conditions. Biochem. J. 2014, 462:185-197.
57. Tay M.Y.F., Saw W.G., Zhao Y., Chan W.K.K., Singh D., Chong Y., Forwood J.K., Ooi E.E., Grüber G., Lescar J., Luo D., Vasudevan S.G. The C-terminal 50 amino acid residues of dengue NS3 protein are important for NS3-NS5 interaction and viral replication. J. Biol. Chem. 2014, 290:2379-2394.
58. Tina K.G., Bhadra R., Srinivasan N. PIC: protein interactions calculator. Nucleic Acids Res. 2007, 35:W473-W476.
59. Tovchigrechko A., Vakser I.A. GRAMM-X public web server for protein-protein docking. Nucleic Acids Res. 2006, 34:W310-W314.
60. van Gunsteren W.F., Billeter S.R., Eising A.A., Hünenberger P.H., Krüger P., Mark A.E., Scott W.R.P., Tironi I.G. Biomolecular Simulation: the GROMOS96 Manual and User Guide, Vdf Hochschulverlag AG an der 1996, 1-1042. ETH Zürich, Zürich, Switzerland.
61. Vitavska O., Merzendorfer H., Wieczorek H. The V-ATPase subunit C binds to polymeric F-actin as well as to monomeric G-actin and induces cross-linking of actin filaments. J. Biol. Chem. 2005, 280:1070-1076.
62. Wang S., Tsun Z.Y., Wolfson R.L., Shen K., Wyant G.A., Plovanich M.E., Yuan E.D., Jones T.D., Chantranupong L., Comb W., Wang T., Bar-Peled L., Zoncu R., Straub C., Kim C., Park J., Sabatini B.L., Sabatini D.M. Metabolism. Lysosomal amino acid transporter SLC38A9 signals arginine sufficiency to mTORC1. Science 2015, 347:188-194.
63. Wilkens S., Zhang Z., Zheng Y. A structural model of the vacuolar ATPase from transmission electron microscopy. Micron 2005, 36:109-126.
64. Xu X., You J., Pei F. Silencing of a novel tumor metastasis suppressor gene LASS2/TMSG1 promotes invasion of prostate cancer cell in vitro through increase of vacuolar ATPase activity. J. Cell. Biochem. 2012, 113:2356-2363.
65. Zoncu R., Bar-Peled L., Efeyan A., Wang S., Sancak Y., Sabatini D.M. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science 2011, 334:678-683.