medigraphic.com
ISSN 2395-8723 (Electronic)
ISSN 1405-888X (Print)
TIP Revista Especializada en Ciencias Químico-Biológicas

2017, Number 2

<< Back Next >>

TIP Rev Esp Cienc Quim Biol 2017; 20 (2)

Topology and function of the membrane-embedded proteins of the mitochondrial F1FO-ATP synthase

Sánchez-Vásquez L, González-Halphen D

Language: Spanish
References: 45
Page: 29-47
PDF size: 2137.24 Kb.


ABSTRACT

The F1FO-ATP synthase is a complex widely distributed in energy-transducing membranes. All ATPases, including the mitochondrial, chloroplastic and bacterial, share structural and functional similarities. However, there are differences in their composition that depend on the species, being more complex in organisms such as Saccharomyces cerevisiae or Bos taurus. This is why, a better understanding of the F1FO-ATP synthase structure will contribute to a greater knowledge at a molecular level, both of the function, and the regulation of this enzymatic complex. At present, very little is known about the structural organization of the subunits from the FO domain. Considering the former, this paper presents information concerning the intrinsic membrane proteins from the most researched F1FO-ATP synthases to date, as well as some other membrane subunits present in less studied organisms.


REFERENCES

  1. Abrahams, J.P., Leslie, A.G., Lutter, R. & Walker, J.E. (1994). Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature, 370(6491), 621-628. DOI: 10.1038/370621a0.

  2. Allegretti, M., Klusch, N., Mills, D.J., Vonck, J., Kühlbrandt, W. & Davies, K.M. (2015). Horizontal membrane-intrinsic α-helices in the stator a-subunit of an F-type ATP synthase. Nature, 521(7551), 237-240. DOI: 10.1038/nature14185.

  3. Altendorf, K., Stalz, W., Greie, J. & Deckers-Hebestreit, G. (2000). Structure and function of the F(O) complex of the ATP synthase from Escherichia coli. J. Exp. Biol., 203(Pt 1), 19-28.

  4. Amutha, B., Gordon, D.M., Gu, Y. & Pain, D. (2004). A novel role of Mgm1p, a dynamin-related GTPase, in ATP synthase assembly and cristae formation/maintenance. Biochem. J., 381(Pt 1), 19-23. DOI: 10.1042/BJ20040566.

  5. Aris, J.P., Klionsky, D.J. & Simoni, R.D. (1985). The FO subunits of the Escherichia coli F1FO-ATP synthase are sufficient to form a functional proton pore. J. Biol. Chem., 260(20), 11207-11215.

  6. Arnold, I., Pfeiffer, K., Neupert, W., Stuart, R.A. & Schägger, H. (1998). Yeast mitochondrial F1FO-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J., 17(24), 7170-7178. DOI: 10.1093/emboj/17.24.7170.

  7. Arselin, G., Giraud, M.F., Dautant, A., Vaillier, J., Brèthes, D., Coulary- Salin, B., Schaeffer, J. & Velours, J. (2003). The GxxxG motif of the transmembrane domain of subunit e is involved in the dimerization/oligomerization of the yeast ATP synthase complex in the mitochondrial membrane. Eur. J. Biochem., 270(8), 1875- 1884. DOI: 10.1046/j.1432-1033.2003.03557.x.

  8. Arselin, G., Vaillier, J., Graves, P.V. & Velours, J. (1996). ATP synthase of yeast mitochondria. Isolation of the subunit h and disruption of the ATP14 gene. J. Biol. Chem., 271(34), 20284-20290. DOI: 10.1074/jbc.271.34.20284.

  9. Arselin, G., Vaillier, J., Salin, B., Schaeffer, J., Giraud, M.F., Dautant, A., Brèthes, D. & Velours, J. (2004). The modulation in subunits e and g amounts of yeast ATP synthase modifies mitochondrial cristae morphology. J. Biol. Chem., 279(39), 40392-40399. DOI: 10.1074/jbc.M404316200.

  10. Balabaskaran Nina, P., Dudkina, N.V., Kane, L.A., van Eyk, J.E., Boekema, E.J., Mather, M.W. & Vaidya, A.B. (2010). Highly divergent mitochondrial ATP synthase complexes in Tetrahymena thermophila. PLoS Biol., 8(7), e1000418. DOI: 10.1371/journal. pbio.1000418.

  11. Brunner, S., Everard-Gigot, V. & Stuart, R.A. (2002). Su e of the yeast F1FO-ATP synthase forms homodimers. J. Biol. Chem., 277(50), 48484-48489. DOI: 10.1074/jbc.M209382200.

  12. Bustos, D.M. & Velours, J. (2005). The modification of the conserved GXXXG motif of the membrane-spanning segment of subunit g destabilizes the supramolecular species of yeast ATP synthase. J. Biol. Chem., 280(32), 29004-29010. DOI: 10.1074/jbc. M502140200.

  13. Cano-Estrada, A & González-Halphen, D. (2011). F1FO-ATP sintasa y sus diferencias estructurales. REB, 30(3), 98-108.

  14. Cingolani, G. & Duncan, T.M. (2011). Structure of the ATP synthase catalytic complex (F1) from Escherichia coli in an auto inhibited conformation. Nat. Struct. Mol. Biol., 18(6), 701-707. DOI: 10.1038/nsmb.2058.

  15. Claggett, S.B., Grabar, T.B., Dunn, S.D. & Cain, B.D. (2007). Functional incorporation of chimeric b subunits into F1Fo ATP synthase. J. Bacteriol., 189(15), 5463-5471. DOI: 10.1128/JB.00191-07.

  16. Collinson, I.R., Runswick, M.J., Buchanan, S.K., Fearnley, I.M., Skehel, J.M., van Raaij, M.J., Griffiths, D.E. & Walker, J.E. (1994). FO membrane domain of ATP synthase from bovine heart mitochondria: purification, subunit composition, and reconstitution with F1-ATPase. Biochemistry, 33(25), 7971-7978. DOI: 10.1021/ bi00191a026.

  17. Couoh-Cardel, S.J., Uribe-Carvajal, S., Wilkens, S. & García-Trejo, J.J. (2010). Structure of dimeric F1FO-ATP synthase. J. Biol. Chem., 285(47), 36447-36455. DOI: 10.1074/jbc.M110.144907.

  18. Deckers-Hebestreit, G. & Altendorf, K. (1992). The FO complex of the proton-translocating F-type ATPase of Escherichia coli. J. Exp. Biol., 172, 451-459.

  19. Deckers-Hebestreit, G. & Altendorf, K. (1996). The F0F1-type ATP synthases of bacteria: structure and function of the F0 complex. Annu. Rev. Microbiol., 50, 791-824. DOI: 10.1146/annurev. micro.50.1.791.

  20. Devenish, R.J., Papakonstantinou, T., Galanis, M., Law, R.H., Linnane, A.W. & Nagley, P. (1992). Structure/function analysis of yeast mitochondrial ATP synthase subunit 8. Ann. NY Acad. Sci., 671, 403-414. DOI: 10.1111/j.1749-6632.1992.tb43814.x.

  21. Dickson, V.K., Silvester, J.A., Fearnley, I.M., Leslie, A.G. & Walker, J.E. (2006). On the structure of the stator of the mitochondrial ATP synthase. EMBO J., 25, 2911–2918. DOI: 10.1038/ sj.emboj.7601177.

  22. Dmitriev, O., Jones, P.C., Jiang, W. & Fillingame, R.H. (1999). Structure of the membrane domain of subunit b of the Escherichia coli FOF1 ATP synthase. J. Biol. Chem., 274(22), 15598-15604. DOI: 10.1074/jbc.274.22.15598.

  23. Domínguez-Ramírez, L. & Tuena de Gómez-Poyou, M. (2003). Virtudes y pecados de una enzima: La FOF1 ATP sintasa. Mensaje Bioquímico, Depto. de Bioq., Fac. de Medicina, UNAM, 27, 25-44. P.V. & Velours, J. (2000). Environmental study of subunit i, a F(O) component of the yeast ATP synthase. Biochemistry, 39(14), 4199-4205. DOI: 10.1021/bi992438l.

  24. Rees, D.M., Leslie, A.G. & Walker, J.E. (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.

  25. Roudeau, S., Spannagel, C., Vaillier, J., Arselin, G., Graves, P.V. & Velours, J. (1999). Subunit f of the yeast mitochondrial ATP synthase: topological and functional studies. J. Bioenerg. Biomembr., 31(2), 85-94. DOI: 10.1023/A:1005407525915.

  26. Roy, A., Hutcheon, M.L., Duncan, T.M. & Cingolani, G. (2012). Improved crystallization of Escherichiacoli ATP synthase catalytic complex (F1) by introducing a phosphomimetic mutation in subunit ε. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun., 68(Pt 10), 1229–1233. DOI: 10.1107/s1744309112036718.

  27. Saddar, S. & Stuart, R.A. (2005). The yeast F(1)F(0)-ATP synthase: analysis of the molecular organization of subunit g and the importance of a conserved GXXXG motif. J. Biol. Chem., 280(26), 24435-24442. DOI: 10.1074/jbc.M502804200.

  28. Shirakihara, Y., Shiratori, A., Tanikawa, H., Nakasako, M., Yoshida, M. & Suzuki, T. (2015). Structure of a thermophilic F1-ATPase inhibited by an ε-subunit: deeper insight into the ε-inhibition mechanism. FEBS J, 282(15), 2895–2913. DOI: 10.1111/ febs.13329.

  29. Soubannier, V., Rusconi, F., Vaillier, J., Arselin, G., Chaignepain, S., Graves, P.V., Schmitter, J.M., Zhang, J.L., Mueller, D. & Velours, J. (1999). The second stalk of the yeast ATP synthase complex: identification of subunits showing cross-links with known positions of subunit 4 (subunit b). Biochemistry, 38(45), 15017-15024. DOI: 10.1021/bi9916067.

  30. Soubannier, V., Vaillier, J., Paumard, P., Coulary, B., Schaeffer, J. & Velours, J. (2002). In the absence of the first membrane-spanning segment of subunit 4(b), the yeast ATP synthase is functional but does not dimerize or oligomerize. J. Biol. Chem., 277(12), 10739-10745. DOI: 10.1074/jbc.M111882200.

  31. Spannagel, C., Vaillier, J., Arselin, G., Graves, P.V. & Velours, J. (1997). The subunit f of mitochondrial yeast ATP-synthase: characterization of the protein and disruption of the structural gene ATP17. Eur. J. Biochem., 247(3), 1111-1117. DOI: 10.1111/j.1432- 1033.1997.01111.x.

  32. Stewart, A.G., Sobti, M., Harvey, R.P. & Stock, D. (2013). Rotatory ATPases: Models, machine elements and technical specifications. BioArchitecture, 3(1), 2-12. DOI: 10.4161/bioa.23301.

  33. Stock, D., Leslie, A.G. & Walker, J.E. (1999). Molecular architecture of the rotary motor in ATP synthase. Science, 286, 1700–1705. DOI: 10.1126/science.286.5445.1700.

  34. Stocker, A., Keis, S., Vonck, J., Cook, G.M. & Dimroth, P. (2007). The structural basis for unidirectional rotation of thermo alkaliphilic F1-ATPase. Structure, 15(8), 904–914. DOI: 10.1016/j. str.2007.06.009.

  35. Vázquez-Acevedo, M., Cardol, P., Cano-Estrada, A., Lapaille, M., Remacle, C. & González-Halphen, D. (2006). The mitochondrial ATP synthase of chlorophycean algae contains eight subunits of unknown origin involved in the formation of an atypical stator-stalk and in the dimerization of the complex. J. Bioenerg. Biomembr., 38(5-6), 271-282. DOI: 10.1007/s10863-006- 9046-x.

  36. Vázquez-Acevedo, M., Vega-de Luna, F., Sánchez-Vásquez, L., Colina-Tenorio, L., Remacle, C., Cardol, P., Miranda-Astudillo, H. & González-Halphen, D. (2016). Dissecting the peripheral stalk of the mitochondrial ATP synthase of chlorophycean algae. Biochim. Biophys. Acta, pii: S0005-2728(16), 30022-30026. DOI: 10.1016/j.bbabio.2016.02.003.

  37. Velours, J., Paumard, P., Soubannier, V., Spannagel, C., Vaillier, J., Arselin, G. & Graves, P.V. (2000). Organisation of the yeast ATP synthase F(0): a study based on cysteine mutants, thiol modification and cross-linking reagents. Biochim. Biophys. Acta, 1458(2-3), 443-456. DOI: 10.1016/S0005-2728(00)00093-1.

  38. Vik, S.B. & Ishmukhametov, R.R. (2005). Structure and function of subunit a of the ATP synthase of Escherichia coli. J. Bioenerg. Biomembr., 37(6), 445-449. DOI: 10.1007/s10863-005-9488-6.

  39. Wagner, K., Perschil, I., Fichter, C.D. & van der Laan, M. (2010). Stepwise assembly of dimeric F(1)F(o)-ATP synthase in mitochondria involves the small F(o)-subunits k and i. Mol. Biol. Cell., 21(9), 1494-1504. DOI: 10.1091/mbc.E09-12-1023.

  40. Walker, J.E. (2013). The ATP synthase: the understood, the uncertain and the unknown. Biochem. Soc. Trans., 41, 1-16. DOI: 10.1042/ bst20110773.

  41. Welch, A.K., Claggett, S.B. & Cain, B.D. (2008). The b (arg36) contributes to efficient coupling in F(1)F(o) ATP synthase in Escherichia coli. J. Bioenerg. Biomembr., 40(1), 1-8. DOI: 10.1007/s10863-008-9124-3.

  42. Wittig, I. & Schägger, H. (2008). Structural organization of mitochondrial ATP synthase. Biochim. Biophys. Acta, 1777(7-8), 592-598. DOI: 10.1016/j.bbabio.2008.04.027.

  43. Yoshida, M., Muneyuki, E. & Hisabori, T. (2001). ATP synthase-a marvellous rotary engine of the cell. Nat. Rev. Mol. Cell. Biol., 2(9), 669-677. DOI: 10.1038/35089509.

  44. Zhou, A., Rohou, A., Scheo, D.G., Bason, J.V., Montgomery, M.G., Walker, J.E., Grigorieff, N. & Rubinstein, J.L. (2015). Structure and conformational states of the bovine mitochondrial ATP synthase by cryo-EM. eLife, 4, e10180. DOI: 10.7554/eLife.10180.

  45. Zíková, A., Schnaufer, A., Dalley, R.A., Panigrahi, A.K. & Stuart, K.D. (2009). The F(o)F(1)-ATP synthase complex contains novel subunits and is essential for procyclic Trypanosoma brucei. PLoSPathog., 5(5), e1000436. DOI: 10.1371/journal. ppat.1000436.




2020     |     www.medigraphic.com