Specific motifs of the V-ATPase a2-subunit isoform interact with catalytic and regulatory domains of ARNO

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1797, Issue 8, 2010, Pages 1398-1409

  Merkulova, Maria ^a   Bakulina, Anastasia ^b   Thaker, Youg Raj ^c   Grüber, Gerhard ^c,d   Marshansky, Vladimir ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b STATE RESEARCH CENTER OF VIROLOGY AND BIOTECHNOLOGY VECTOR   (Russian Federation)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d BIOINFORMATICS INSTITUTE   (Singapore)

Author keywords

Arf GEF ARNO; BIAcore; NMR; PB domain; Peptide structure; Phosphorylation; Sec7 domain; V type ATPase

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR NUCLEOTIDE SITE OPENER; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG; VACUOLAR TYPE PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE A2;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CATALYSIS; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; ENZYME SUBUNIT; GENE REARRANGEMENT; HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS; SURFACE PLASMON RESONANCE; WILD TYPE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; GTPASE-ACTIVATING PROTEINS; HUMANS; ISOENZYMES; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; STRUCTURAL HOMOLOGY, PROTEIN; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 77953807182     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.02.009     Document Type: Article

References (51)

1. 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, 8:124-136.
2. Marshansky V. The V-ATPase a2-subunit as a putative endosomal pH-sensor. Biochem. Soc. Trans. 2007, 35:1092-1099.
3. Marshansky V., Futai M. The V-type H(+)-ATPase in vesicular trafficking: targeting, regulation and function. Curr. Opin. Cell Biol. 2008, 20:415-426.
4. Zhang Z., Zheng Y., Mazon H., Milgrom E., Kitagawa N., Kish-Trier E., Heck A.J., Kane P.M., Wilkens S. Structure of the yeast vacuolar ATPase. J. Biol. Chem. 2008, 283:35983-35995.
5. 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.
6. Muench S.P., Huss M., Song C.F., Phillips C., Wieczorek H., Trinick J., Harrison M.A. Cryo-electron microscopy of the vacuolar ATPase motor reveals its mechanical and regulatory complexity. J. Mol. Biol. 2009, 386:989-999.
7. Brown D., Marshansky V. Renal V-ATPase: physiology and pathophysiology. Handbook of ATPases. Biochemistry, Cell Biology, Pathophysiology 2004, 413-442. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim. M. Futai, Y. Wada, J.H. Kaplan (Eds.).
8. Wagner C.A., Finberg K.E., Breton S., Marshansky V., Brown D., Geibel J.P. Renal vacuolar H+-ATPase. Physiol. Rev. 2004, 84:1263-1314.
9. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell. Biol. 2007, 8:917-929.
10. Grüber G., Marshansky V. New insights into structure-function relationships between archeal ATP synthase (A1A0) and vacuolar type ATPase (V1V0). Bioessays 2008, 30:1096-1109.
11. Brown D., Breton S., Ausiello D.A., Marshansky V. Sensing, signaling and sorting events in kidney epithelial cell physiology. Traffic 2009, 10:275-284.
12. Blake-Palmer K.G., Karet F.E. Cellular physiology of the renal H+ ATPase. Curr. Opin. Nephrol. Hypertens. 2009, 18:433-438.
13. Wang Y., Toei M., Forgac M. Analysis of the membrane topology of transmembrane segments in the C-terminal hydrophobic domain of the yeast vacuolar ATPase subunit a (Vph1p) by chemical modification. J. Biol. Chem. 2008, 283:20696-20702.
14. Toyomura T., Oka T., Yamaguchi C., Wada Y., Futai M. Three subunit a isoforms of mouse vacuolar H(+)-ATPase. Preferential expression of the a3 isoform during osteoclast differentiation. J. Biol. Chem. 2000, 275:8760-8765.
15. Oka T., Murata Y., Namba M., Yoshimizu T., Toyomura T., Yamamoto A., Sun-Wada G.H., Hamasaki N., Wada Y., Futai M. a4, a unique kidney-specific isoform of mouse vacuolar H+-ATPase subunit a. J. Biol. Chem. 2001, 276:40050-40054.
16. Smith A.N., Skaug J., Choate K.A., Nayir A., Bakkaloglu A., Ozen S., Hulton S.A., Sanjad S.A., Al-Sabban E.A., Lifton R.P., Scherer S.W., Karet F.E. Mutations in ATP6N1B, encoding a new kidney vacuolar proton pump 116-kD subunit, cause recessive distal renal tubular acidosis with preserved hearing. Nat. Genet. 2000, 26:71-75.
17. Smith A.N., Finberg K.E., Wagner C.A., Lifton R.P., Devonald M.A., Su Y., Karet F.E. Molecular cloning and characterization of Atp6n1b: a novel fourth murine vacuolar H+-ATPase a-subunit gene. J. Biol. Chem. 2001, 276:42382-42388.
18. Xu T., Vasilyeva E., Forgac M. Subunit interactions in the clathrin-coated vesicle vacuolar (H(+))-ATPase complex. J. Biol. Chem. 1999, 274:28909-28915.
19. Landolt-Marticorena C., Williams K.M., Correa J., Chen W., Manolson M.F. Evidence that the NH2 terminus of vph1p, an integral subunit of the V0 sector of the yeast V-ATPase, interacts directly with the Vma1p and Vma13p subunits of the V1 sector. J. Biol. Chem. 2000, 275:15449-15457.
20. Inoue T., Forgac M. Cysteine-mediated cross-linking indicates that subunit C of the V-ATPase is in close proximity to subunits E and G of the V1 domain and subunit a of the V0 domain. J. Biol. Chem. 2005, 280:27896-27903.
21. Qi J., Forgac M. Function and subunit interactions of the N-terminal domain of subunit a (Vph1p) of the yeast V-ATPase. J. Biol. Chem. 2008, 283:19274-19282.
22. Norgett E.E., Borthwick K.J., Al-Lamki R.S., Su Y., Smith A.N., Karet F.E. V1 and V0 domains of the human H+-ATPase are linked by an interaction between the G and a subunits. J. Biol. Chem. 2007, 282:14421-14427.
23. Lu M., Holliday L.S., Zhang L., Dunn W.A., Gluck S.L. Interaction between aldolase and vacuolar H+-ATPase: evidence for direct coupling of glycolysis to the ATP-hydrolyzing proton pump. J. Biol. Chem. 2001, 276:30407-30413.
24. Lu M., Sautin Y.Y., Holliday L.S., Gluck S.L. The glycolytic enzyme aldolase mediates assembly, expression, and activity of vacuolar H+-ATPase. J. Biol. Chem. 2004, 279:8732-8739.
25. Sautin Y.Y., Lu M., Gaugler A., Zhang L., Gluck S.L. Phosphatidylinositol 3-kinase-mediated effects of glucose on vacuolar H+-ATPase assembly, translocation, and acidification of intracellular compartments in renal epithelial cells. Mol. Cell. Biol. 2005, 25:575-589.
26. Lu M., Ammar D., Ives H., Albrecht F., Gluck S.L. Physical interaction between aldolase and vacuolar H+-ATPase is essential for the assembly and activity of the proton pump. J. Biol. Chem. 2007, 282:24495-24503.
27. Su Y., Zhou A., Al-Lamki R.S., Karet F.E. The a-subunit of the V-type H+-ATPase interacts with phosphofructokinase-1 in humans. J. Biol. Chem. 2003, 278:20013-20018.
28. Su Y., Blake-Palmer K.G., Sorrell S., Javid B., Bowers K., Zhou A., Chang S.H., Qamar S., Karet F.E. Human H+ATPase a4 subunit mutations causing renal tubular acidosis reveal a role for interaction with phosphofructokinase-1. Am. J. Physiol. Renal Physiol. 2008, 295:F950-F958.
29. Bourne H.R., Sanders D.A., McCormick F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature 1990, 348:125-132.
30. Donaldson J.G., Klausner R.D. ARF: a key regulatory switch in membrane traffic and organelle structure. Curr. Opin. Cell Biol. 1994, 6:527-532.
31. D'Souza-Schorey C., Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell. Biol. 2006, 7:347-358.
32. DiNitto J.P., Delprato A., Gabe Lee M.T., Cronin T.C., Huang S., Guilherme A., Czech M.P., Lambright D.G. Structural basis and mechanism of autoregulation in 3-phosphoinositide-dependent Grp1 family Arf GTPase exchange factors. Mol. Cell 2007, 28:569-583.
33. Casanova J.E. Regulation of Arf activation: the Sec7 family of guanine nucleotide exchange factors. Traffic 2007, 8:1476-1485.
34. Santy L.C., Frank S.R., Hatfield J.C., Casanova J.E. Regulation of ARNO nucleotide exchange by a PH domain electrostatic switch. Curr. Biol. 1999, 9:1173-1176.
35. Marles J.A., Dahesh S., Haynes J., Andrews B.J., Davidson A.R. Protein-protein interaction affinity plays a crucial role in controlling the Sho1p-mediated signal transduction pathway in yeast. Mol. Cell 2004, 14:813-823.
36. Kneller D.G., Goddar T.D. SPARKY 3.105 1997, San Francisco, CA. U. Edit (Ed.).
37. Wüthrich K. NMR of Proteins and Nucleic acids 1986, Wiley, Interscience, New York.
38. Herrmann T., Güntert P., Wüthrich K. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 2002, 319:209-227.
39. Lupas A., Van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science 1991, 252:1162-1164.
40. Jones D.T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 1999, 292:195-202.
41. McGuffin L.J., Bryson K., Jones D.T. The PSIPRED protein structure prediction server. Bioinformatics 2000, 16:404-405.
42. Marti-Renom M.A., Stuart A.C., Fiser A., Sanchez R., Melo F., Sali A. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 2000, 29:291-325.
43. Hiesinger P.R., Fayyazuddin A., Mehta S.Q., Rosenmund T., Schulze K.L., Zhai R.G., Verstreken P., Cao Y., Zhou Y., Kunz J., Bellen H.J. The v-ATPase Vo subunit a1 is required for a late step in synaptic vesicle exocytosis in Drosophila. Cell 2005, 121:607-620.
44. Chardin P., Paris S., Antonny B., Robineau S., Beraud-Dufour S., Jackson C.L., Chabre M. A human exchange factor for ARF contains Sec7- and pleckstrin-homology domains. Nature 1996, 384:481-484.
45. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 1997, 18:2714-2723.
46. Van Der Spoel D., Lindahl E., Hess B., Groenhof G., Mark A.E., Berendsen H.J. GROMACS: fast, flexible, and free. J. Comput. Chem. 2005, 26:1701-1718.
47. Mansour M., Lee S.Y., Pohajdak B. The N-terminal coiled coil domain of the cytohesin/ARNO family of guanine nucleotide exchange factors interacts with the scaffolding protein CASP. J. Biol. Chem. 2002, 277:32302-32309.
48. Chantalat S., Park S.K., Hua Z., Liu K., Gobin R., Peyroche A., Rambourg A., Graham T.R., Jackson C.L. The Arf activator Gea2p and the P-type ATPase Drs2p interact at the Golgi in Saccharomyces cerevisiae. J. Cell Sci. 2004, 117:711-722.
49. Yamamoto M., Unzai S., Saijo S., Ito K., Mizutani K., Suno-Ikeda C., Yabuki-Miyata Y., Terada T., Toyama M., Shirouzu M., Kobayashi T., Kakinuma Y., Yamato I., Yokoyama S., Iwata S., Murata T. Interaction and stoichiometry of the peripheral stalk subunits NtpE and NtpF and the N-terminal hydrophilic domain of NtpI of Enterococcus hirae V-ATPase. J. Biol. Chem. 2008, 283:19422-19431.
50. Thaker Y.R., Hunke C., Yau Y.H., Shochat S.G., Li Y., Grüber G. Association of the eukaryotic V1VO ATPase subunits a with d and d with A. FEBS Lett. 2009, 583:1090-1095.
51. Cherfils J., Menetrey J., Mathieu M., Le Bras G., Robineau S., Beraud-Dufour S., Antonny B., Chardin P. Structure of the Sec7 domain of the Arf exchange factor ARNO. Nature 1998, 392:101-105.