An update in the structure, function, and regulation of V-ATPases: The role of the C subunit;Uma atualização na estrutura, função e regulação das V-ATPases: O papel das subunidades C

Brazilian Journal of Biology

Volumn 72, Issue 1, 2012, Pages 189-198

  Perez Sayans M ^a   Suarez Penaranda J M ^b   Barros Angueira, F ^b   Diz, P G ^c   Gandara Rey J M ^d   Garcia Garcia A ^d  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b Instituto de Salud Carlos III   (Spain)

^c HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

^d Complejo Hospitalario Universitario de Santiago ^*  (Spain)

Author keywords

ATP6V1C1,V1 domain; C subunit; Proton transport; V ATPases; V0 domain

Indexed keywords

EUKARYOTA;

EID: 84859055472     PISSN: 15196984     EISSN: 16784375     Source Type: Journal    
DOI: 10.1590/S1519-69842012000100023     Document Type: Article

References (67)

1. ARMBRUSTER, A., HOHN, C., HERMESDORF, A., SCHUMACHER, K., BORSCH, M. and GRUBER, G., 2005. Evidence for major structural changes in subunit C of the vacuolar ATPase due to nucleotide binding. FEBS Letters, vol. 579, no. 9, p. 1961-1967. PMid:15792803. http://dx.doi.org/10.1016/j.febslet.2005.02.042
2. ARMBRUSTER, A., SVERGUN, DI., COSKUN, U., JULIANO, S., BAILER, SM. and GRUBER, G., 2004. Structural analysis of the stalk subunit Vma5p of the yeast V-ATPase in solution. FEBS Letters, vol. 570, no. 1-3, p. 119-125. PMid:15251451. http://dx.doi.org/10.1016/j.febslet.2004.06.029
3. BAARS, TL., PETRI, S., PETERS, C. and MAYER, A., 2007. Role of the V-ATPase in regulation of the vacuolar fission fusion equilibrium. Molecular Biology of the Cell, vol. 18, no. 10, p. 3873-3882. PMid:17652457. PMCid:1995711. http://dx.doi.org/10.1091/mbc.E07-03-0205
4. BOYER, PD., 1993. The binding change mechanism for ATP synthase--some probabilities and possibilities. Biochimica et Biophysica Acta, vol. 1140, no. 3, p. 215-250. http://dx.doi.org/10.1016/0005-2728(93)90063-L
5. BRETON, S. and BROWN, D., 2007. New insights into the regulation of V-ATPase-dependent proton secretion. American Journal of Physiology-Renal Physiology, vol. 292, no. 1, p. F1-10. PMid:17032935. http://dx.doi.org/10.1152/ajprenal.00340.2006
6. CHABAN, YL., JULIANO, S., BOEKEMA, EJ. and GRUBER, G., 2005. Interaction between subunit C (Vma5p) of the yeast vacuolar ATPase and the stalk of the C-depleted V(1) ATPase from Manduca sexta midgut. Biochimica et Biophysica Acta, vol. 1708, no. 2, p. 196-200.
7. CIPRIANO, DJ., WANG, Y., BOND, S., HINTON, A., JEFFERIES, KC, QI, J. and FORGAC, M., 2008. Structure and regulation of the vacuolar ATPases. Biochimica et Biophysica Acta (BBA)-Bioenergetics, vol. 1777, no. 7-8, p. 599-604.
8. CURTIS, KK. and KANE, PM., 2002. Novel Vacuolar H+-ATPase Complexes Resulting from Overproduction of Vma5p and Vma13p. Journal of Biological Chemistry, vol. 277, no. 4, p. 2716-2724. PMid:11717306. http://dx.doi.org/10.1074/jbc.M107777200
9. DOMÍNGUEZ, L. and TUENA, M., 2005. ATP sintasa: un complejo proteico con gran versatilidad estructural y funcional. Tip Revista Especializada en Ciencias Químico-Biológicas, vol. 8, no. 1, p. 18-27.
10. DRORY, O. and NELSON, N. 2006. The emerging structure of vacuolar ATPases. Physiology, vol. 21, p. 317-325. PMid:16990452. http://dx.doi.org/10.1152/physiol.00017.2006
11. DRORY, O., FROLOW, F. and NELSON, N., 2004. Crystal structure of yeast V-ATPase subunit C reveals its stator function. EMBO reports, vol. 5, no. 12, p. 1148-1152. PMid:15540116. PMCid:1299189. http://dx.doi.org/10.1038/sj.embor.7400294
12. FINBOW, ME. and HARRISON, MA., 1997. The vacuolar H+-ATPase: a universal proton pump of eukaryotes. Biochemical Journal, vol. 324, pt. 3, p. 697-712.
13. FORGAC, M., 1998. Structure, function and regulation of the vacuolar (H+)-ATPases. FEBS Letters, vol. 440, no. 3, p. 258-263. http://dx.doi.org/10.1016/S0014-5793(98)01425-2
14. FORGAC, M., 2007. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nature Reviews Molecular Cell Biology, vol. 8, no. 11, p. 917-929. PMid:17912264. http://dx.doi.org/10.1038/nrm2272
15. GRUBER, G., 2005. Structural features and nucleotide-binding capability of the C subunit are integral to the regulation of the eukaryotic V1Vo ATPases. Biochemical Society Transactions, vol. 33, pt. 4, p. 883-885. PMid:16042619.
16. HARVEY, WR. and WIECZOREK, H., 1997. Animal plasma membrane energization by chemiosmotic H+ V-ATPases. Journal of Experimental Biology, vol. 200, pt. 2, p. 203-216. PMid:9050228.
17. HARVEY, WR., 1992. Physiology of V-ATPases. Journal of Experimental Biology, vol. 172, p. 1-17.
18. INOUE, T. and FORGAC, M., 2005. 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. Journal of Biological Chemistry, vol. 280, no. 30, p. 27896-27903. PMid:15951435. http://dx.doi.org/10.1074/jbc.M504890200
19. INOUE, T., WANG, Y., JEFFERIES, K., QI, J., HINTON, A. and FORGAC, M., 2005. Structure and regulation of the V-ATPases. Journal of Bioenergetics and Biomembranes, vol. 37, no. 6, p. 393-398. PMid:16691471. http://dx.doi.org/10.1007/s10863-005-9478-8
20. JEFFERIES, KC. and FORGAC, M., 2008. Subunit H of the Vacuolar (H+) ATPase Inhibits ATP Hydrolysis by the Free V1 Domain by Interaction with the Rotary Subunit F. Journal of Biological Chemistry, no. 8, p. 4512-4519. PMid:18156183. PMCid:2408380.
21. JONES, RP., DUROSE, LJ., FINDLAY, JB. and HARRISON, MA., 2005. Defined sites of interaction between subunits E (Vma4p), C (Vma5p), and G (Vma10p) within the stator structure of the vacuolar H+-ATPase. Biochemistry, vol. 44, no. 10, p. 3933-3941.
22. KANE, PM., 1999. Introduction: V-ATPases 1992-1998. Journal of Bioenergetics and Biomembranes, vol. 31, no. 1, p. 3-5. PMid:10340843. http://dx.doi.org/10.1023/A:1001884227654
23. KAWASAKI-NISHI, S., NISHI, T. and FORGAC, M., 2003. Proton translocation driven by ATP hydrolysis in V-ATPases. FEBS Letters, vol. 545, no. 1, p. 76-85. http://dx.doi.org/10.1016/S0014-5793(03)00396-X
24. KEENAN, CK. and KANE, PM., 2002. Novel Vacuolar H+-ATPase Complexes Resulting from Overproduction of Vma5p and Vma13p J. Biol. Chem., 2002, 277, 4, 2716-2724
25. KURASHIMA, K., NUMATA, M., YACHIE, A., SAI, Y., ISHIZAKA, N., FUJIMURA, M., MATSUDA, T. and OHKUMA, S.1996. The role of vacuolar H(+)-ATPase in the control of intragranular pH and exocytosis in eosinophils. Laboratory Investigation, vol. 75, no. 5, p. 689-698. PMid:8941214.
26. MARSHANSKY, V. and FUTAI, M., 2008. The V-type H+-ATPase in vesicular trafficking: targeting, regulation and function. Current Opinion in Cell Biology, vol. 20, no. 4, p. 415-26.
27. MARTÍNEZ-MUNOZ, GA. and KANE, P., 2008. Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast. Journal of Biological Chemistry, vol. 283, no. 29, p. 20309-20319. PMid:18502746. PMCid:2459297. http://dx.doi.org/10.1074/jbc.M710470200
28. MARTÍNEZ-ZAGUILAN, R., LYNCH, RM., MARTINEZ, GM. and GILLIES, RJ., 1993. Vacuolar-type H(+)-ATPases are functionally expressed in plasma membranes of human tumor cells. American Journal of Physiology-Cell Physiology, vol. 265, no. 4, p. C1015-1029.
29. MIURA, GI., FROELICK, GJ., MARSH, DJ., STARK, KL. and PALMITER, RD., 2003. The d Subunit of the Vacuolar ATPase (Atp6d) is Essential for Embryonic Development. Transgenic research, vol. 12, no. 1.
30. MORIYAMA, Y. and NELSON, N., 1989. H+-translocating ATPase in Golgi apparatus. Characterization as vacuolar H+-ATPase and its subunit structures. Journal of Biological Chemistry, vol. 264, no. 31, p. 18445-18450.
31. MULLER, O., NEUMANN, H., BAYER, MJ. and MAYER, A., 2003. Role of the Vtc proteins in V-ATPase stability and membrane trafficking. Journal of Cell Science, vol. 116, no. 6, p. 1107-1115. PMid:12584253. http://dx.doi.org/10.1242/jcs.00328
32. NANDA, A., BRUMELL, JH., NORDSTROM, T., KJELDSEN, L., SENGELOV, H., BORREGAARD, N., ROTSTEIN, OD. and GRINSTEIN, S., 1996. Activation of Proton Pumping in Human Neutrophils Occurs by Exocytosis of Vesicles Bearing Vacuolar-type H+-ATPases. Journal of Biological Chemistry, vol. 271, no. 27, p. 15963-15970. PMid:8663143. http://dx.doi.org/10.1074/jbc.271.27.15963
33. NELSON, H. and NELSON, N., 1989. The progenitor of ATP synthases was closely related to the current vacuolar H+-ATPase. FEBS Letters, vol. 247, no. 1, p. 147-153. http://dx.doi.org/10.1016/0014-5793(89)81259-1
34. NELSON, N. and HARVEY, WR., 1999. Vacuolar and Plasma Membrane Proton-Adenosinetriphosphatases. Physiological Reviews, vol. 79, no. 2, p. 361-385. PMid:10221984.
35. NELSON, N., 1992. Evolution of organellar proton-ATPases. Biochimica et Biophysica Acta, vol. 1100, no. 2, p. 109-124. http://dx.doi.org/10.1016/0005-2728(92)90072-A
36. NELSON, N., PERZOV, N., COHEN, A., HAGAI, K., PADLER, V. and NELSON, H., 2000. The cellular biology of proton-motive force generation by V-ATPases. Journal of Experimental Biology, vol. 203, pt. 1, p. 89-95.
37. NISHI, T. and FORGAC, M., 2002. The vacuolar (H+)-ATPases--nature's most versatile proton pumps. Nature Reviews Molecular Cell Biology, vol. 3, no. 2, p. 94-103. PMid:11836511. http://dx.doi.org/10.1038/nrm729
38. OTERO-REY, EM., SOMOZA-MARTIN, M., BARROS-ANGUEIRA, F. and GARCIA-GARCIA, A., 2008. Intracellular pH regulation in oral squamous cell carcinoma is mediated by increased V-ATPase activity via over-expression of the ATP6V1C1 gene. Oral Oncology, vol. 44, no.2, p. 193-199. PMid:17467328. http://dx.doi.org/10.1016/j.oraloncology.2007.02.011
39. PENG, S., STONE, D. and XIE, X., 1993. Reconstitution of recombinant 40-kDa subunit of the clathrin-coated vesicle H(+)-ATPase. Journal of Biological Chemistry, vol. 268, no. 31, p. 23519-23523. PMid:8226880.
40. PEREZ-SAYANS, M., GARCIA-GARCIA, A., REBOIRAS-LOPEZ, MD. and GANDARA-VILA, P., 2009a. Role of V-ATPases in solid tumors: Importance of the subunit C (Review). International Journal of Oncology, vol. 34, no. 6, p. 1513-1520. http://dx.doi.org/10.3892/ijo_00000280
41. PÉREZ-SAYÁNS, M., REBOIRAS-LÓPEZ, MD., SOMOZA-MARTÍN, JM., BARROS-ANGUEIRA, F., GAYOSO-DIZ, P., GÁNDARA-REY, JM. and GARCÍA-GARCÍA, A., 2010. Measurement of ATP6V1C1 expression in brush cytology samples as a diagnostic and prognostic marker in oral squamous cell carcinoma. Cancer Biology & Therapy, vol. 9, no. 12, p. 1-8.
42. PEREZ-SAYANS, M., SOMOZA-MARTIN, JM., BARROS-ANGUEIRA, F., REY, JM. and GARCIA-GARCIA, A., 2009b. V-ATPase inhibitors and implication in cancer treatment. Cancer Treatment Reviews, vol. 35, no. 8, p. 707-13. PMid:19758758. http://dx.doi.org/10.1016/j.ctrv.2009.08.003
43. PHILIPPE, JM., DUBOIS, JM., ROUZAIRE-DUBOIS, B., CARTRON, PF., VALLETTE, F. and MOREL, N., 2002. Functional expression of V-ATPases in the plasma membrane of glial cells. Glia, vol. 37, no. 4, p. 365-373. PMid:11870875. http://dx.doi.org/10.1002/glia.10041
44. PIETREMENT, C., SUN-WADA, GH., SILVA, ND., MCKEE, M., MARSHANSKY, V. and BROWN, D., FUTAI M. and BRETON, S., 2006. Distinct expression patterns of different subunit isoforms of the V-ATPase in the rat epididymis. Biology of Reproduction, vol. 74, no. 1, p. 185-194. PMid:16192400. http://dx.doi.org/10.1095/biolreprod.105.043752
45. PUOPOLO, K., SCZEKAN, M., MAGNER, R. and FORGAC, M., 1992. The 40-kDa subunit enhances but is not required for activity of the coated vesicle proton pump. Journal of Biological Chemistry, vol. 267, no. 8, p. 5171-5176. PMid:1531980.
46. QI, J. and WANG, Y., FORGAC, M., 2007. The vacuolar (H+)-ATPase: subunit arrangement and in vivo regulation. Journal of Bioenergetics and Biomembranes, vol. 39, no. 5-6, p. 423-426. PMid:18040762. http://dx.doi.org/10.1007/s10863-007-9116-8
47. SAROUSSI, S. and NELSON, N. 2008. Vacuolar H(+)-ATPase-an enzyme for all seasons. Pflugers Archiv, vol. 457, no. 3, p. 581-587. PMid:18853182. http://dx.doi.org/10.1007/s00424-008-0458-9
48. SCHOONDERWOERT, VTG., HOLTHUIS, JCM., TANAKA, S., TOOZE, SA. and MARTENS, GJM., 2000. Inhibition of the vacuolar H+-ATPase perturbs the transport, sorting, processing and release of regulated secretory proteins. European Journal of Biochemistry, vol. 267, no. 17, p. 5646-5654.
49. SMARDON, AM. and KANE, PM., 2007. RAVE is essential for the efficient assembly of the C subunit with the vacuolar H(+)-ATPase. Journal of Biological Chemistry, vol. 282, no. 36, p. 26185-26194. PMid:17623654. http://dx.doi.org/10.1074/jbc.M703627200
50. SMITH, AN., BORTHWICK, KJ. and KARET, FE., 2002. Molecular cloning and characterization of novel tissue-specific isoforms of the human vacuolar H(+)-ATPase C, G and d subunits, and their evaluation in autosomal recessive distal renal tubular acidosis. Gene, vol. 297, no. 1-2, p. 169-177. http://dx.doi.org/10.1016/S0378-1119(02)00884-3
51. SMITH, AN., JOURET, F., BORD, S., BORTHWICK, KJ., AL-LAMKI, RS., WAGNER, CA., IRELAND, DC., CORMIER-DAIRE, V., FRATTINI, A., VILLA, A., KORNAK, U., DEVUYST, O. and KARET, FE., 2005. Vacuolar H+-ATPase d2 subunit: molecular characterization, developmental regulation, and localization to specialized proton pumps in kidney and bone. Journal of the American Society of Nephrology, vol. 16, no. 5, p. 1245-1256. PMid:15800125. http://dx.doi.org/10.1681/ASN.2004090761
52. SMITH, AN., LOVERING, RC., FUTAI, M., TAKEDA, J., BROWN, D. and KARET, FE., 2003. Revised Nomenclature for Mammlian Vacuolar-Type H+-ATPase Subunit Genes. Molecular Cell, vol. 12, p. 801-803. http://dx.doi.org/10.1016/S1097-2765(03)00397-6
53. STEVENS, TH. and FORGAC, M., 1997. Structure, function and regulation of the vacuolar (H+)-ATPase. Annual Review of Cell and Developmental Biology, vol. 13, p. 779-808. PMid:9442887. http://dx.doi.org/10.1146/annurev.cellbio.13.1.779
54. SUN-WADA, G., WADA, Y. and FUTAI, M., 2004. Diverse and essential roles of mammalian vacuolar-type proton pump ATPase: toward the physiological understanding of inside acidic compartments. Biochimica et Biophysica Acta (BBA)-Bioenergetics, vol. 1658, no. 1-2, p. 106-114.
55. SUN-WADA, GH., WADA, Y. and FUTAI, M., 2003a. Vacuolar H+ pumping ATPases in luminal acidic organelles and extracellular compartments: common rotational mechanism and diverse physiological roles. Journal of Bioenergetics and Biomembranes, vol. 35, no. 4, p. 347-358. PMid:14635780. http://dx.doi.org/10.1023/A:1025780932403
56. SUN-WADA, GH., YOSHIMIZU, T., IMAI-SENGA, Y., WADA, Y. and FUTAI, M., 2003b. Diversity of mouse proton-translocating ATPase: presence of multiple isoforms of the C, d and G subunits. Gene, vol. 302, no. 1-2, p. 147-153. http://dx.doi.org/10.1016/S0378-1119(02)01099-5
57. SVERGUN, DI., KONRAD, S., HUSS, M., KOCH, MH., WIECZOREK, H., ALTENDORF, K., VOLKOV, VV. and GRÜBER, G., 1998. Quaternary structure of V1 and F1 ATPase: significance of structural homologies and diversities. Biochemistry, vol. 37, no. 51, p. 17659-17663.
58. TORIGOE, T., IZUMI, H., ISE, T., MURAKAMI, T., URAMOTO, H., ISHIGUCHI, H., YOSHIDA, Y., TANABE, M., NOMOTO, M. and KOHNO, K., 2002. Vacuolar H(+)-ATPase: functional mechanisms and potential as a target for cancer chemotherapy. Anticancer Drugs, vol. 13, no. 3, p. 237-243. PMid:11984067. http://dx.doi.org/10.1097/00001813-200203000-00005
59. Van HILLE, B., VANEK, M., RICHENER, H., GREEN, JR. and BILBE, G., 1993. Cloning and tissue distribution of subunits C, D, and E of the human vacuolar H(+)-ATPase. Biochemical and Biophysical Research Communications, vol. 30;197, no. 1, p. 15-21.
60. VITAVSKA, O., WIECZOREK, H. and MERZENDORFER, H., 2003. A Novel Role for Subunit C in Mediating Binding of the H+-V-ATPase to the Actin Cytoskeleton. Journal of Biological Chemistry, vol. 278, no. 20, p. 18499-18505. PMid:12606563. http://dx.doi.org/10.1074/jbc.M212844200
61. VOSS, M., VITAVSKA, O., WALZ, B., WIECZOREK, H. and BAUMANN, O., 2007. Stimulus-induced phosphorylation of vacuolar H(+)-ATPase by protein kinase A. Journal of Biological Chemistry, vol. 282, no. 46, p. 33735-33742. PMid:17872947. http://dx.doi.org/10.1074/jbc.M703368200
62. WADA, Y., SUN-WADA, GH., TABATA, H. and KAWAMURA, N., 2008. Vacuolar-type proton ATPase as regulator of membrane dynamics in multicellular organisms. Journal of Bioenergetics and Biomembranes, vol. 40, no. 1, p. 53-57. PMid:18214654. http://dx.doi.org/10.1007/s10863-008-9128-z
63. WIECZOREK, H, BROWN, D., GRINSTEIN, S., EHRENFELD, J. and HARVEY, WR., 1999. Animal plasma membrane energization by proton-motive V-ATPases. Bioessays, vol. 21, no. 8, p. 637-648. http://dx.doi.org/10.1002/(SICI)1521-1878(199908)21:8%3C637::AID-BIES3%3 E3.0.CO;2-W
64. WILKENS, S., ZHANG, Z. and ZHENG, Y., 2005. A structural model of the vacuolar ATPase from transmission electron microscopy. Micron, vol. 36, no. 2, p. 109-126. PMid:15629643. http://dx.doi.org/10.1016/j.micron.2004.10.002
65. XU, T., VASILYEVA, E. and FORGAC, M., 1999. Subunit interactions in the clathrin-coated vesicle vacuolar (H(+)-ATPase complex. Journal of Biological Chemistry, vol. 274, no. 41, p. 28909-28915. PMid:10506135. http://dx.doi.org/10.1074/jbc.274.41.28909
66. ZHANG, J., MYERS, M. and FORGAC, M., 1992. Characterization of the V0 domain of the coated vesicle (H+)-ATPase. Journal of Biological Chemistry, vol. 267, no. 14, p. 9773-9778. PMid:1533640.
67. ZHANG, Z., INOUE, T., FORGAC, M. and WILKENS, S., 2006. Localization of subunit C (Vma5p) in the yeast vacuolar ATPase by immuno electron microscopy. FEBS Letters, vol. 580, no. 8, p. 2006-2010. PMid:16546180. http://dx.doi.org/10.1016/j.febslet.2006.03.001