Abstract
The interaction of the nucleotide-binding subunit B with subunit F is essential in coupling of ion pumping and ATP synthesis in A1AO ATP synthases. Here we provide structural and thermodynamic insights on the nucleotide binding to the surface of subunits B and F of Methanosarcina mazei Gö1 A1AO ATP synthase, which initiated migration to its final binding pocket via two transitional intermediates on the surface of subunit B. NMR- and fluorescence spectroscopy as well as ITC data combined with molecular dynamics simulations of the nucleotide bound subunit B and nucleotide bound B-F complex in explicit solvent, suggests that subunit F is critical for the migration to and eventual occupancy of the final binding site by the nucleotide of subunit B. Rotation of the C-terminus and conformational changes in subunit B are initiated upon binding with subunit F causing a perturbation that leads to the migration of ATP from the transition site 1 through an intermediate transition site 2 to the final binding site 3. This mechanism is elucidated on the basis of change in binding affinity for the nucleotide at the specific sites on subunit B upon complexation with subunit F. The change in enthalpy is further explained based on the fluctuating local environment around the binding sites.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Brooks B, Karplus M (1983) Proc Natl Acad Sci U S A 80:6571–6575
Brooks BR, Brooks CL 3rd, Mackerell AD Jr, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S, Caflisch A, Caves L, Cui Q, Dinner AR, Feig M, Fischer S, Gao J, Hodoscek M, Im W, Kuczera K, Lazaridis T, Ma J, Ovchinnikov V, Paci E, Pastor RW, Post CB, Pu JZ, Schaefer M, Tidor B, Venable RM, Woodcock HL, Wu X, Yang W, York DM, Karplus M (2009) J Comput Chem 30:1545–1614
Butterfield SM, Waters ML (2003) J Am Chem Soc 125:9580–9581
Chang CE, Chen W, Gilson MK (2005) J Chem Theor Comput 1:1017–1028
Darden T, York D, Pedersen L (1993) J Chem Phys 98:10089–10093
DeLano WL (2002) The PyMOL molecular graphics system DeLano Scientific. Palo Alto, California
Dougherty DA (1996) Science 271:163–168
Dougherty DA (2007) J Nutr 137:1504–1508
Feller SE, Zhang YH, Pastor RW, Brooks BR (1995) J Chem Phys 103:4613–4621
Gallivan JP, Dougherty DA (1999) Proc Natl Acad Sci U S A 96:9459–9464
Gayen S, Vivekanandan S, Biuković G, Grüber G, Yoon HS (2007) Biochemistry 46:11684–11694
Grüber G, Marshansky V (2008) Bioessays 30:1096–1109
Grüber G, Svergun DI, Coskun U, Lemker T, Koch MH, Schägger H, Müller V (2001) Biochemistry 40:1890–1896
Hunke C, Chen WJ, Schäfer HJ, Grüber G (2007) Protein Expr Purif 53:378–383
Im W, Lee MS, Brooks CL 3rd (2003) J Comput Chem 24:1691–1702
Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) J Chem Phys 79:926–935
Kneller DG, Goddard TD (1997) SPARKY, 3.105 ed. University of California, San Francisco
Kollman PA, Massova I, Reyes C, Kuhn B, Huo S, Chong L, Lee M, Lee T, Duan Y, Wang W, Donini O, Cieplak P, Srinivasan J, Case DA, Cheatham TE 3rd (2000) Acc Chem Res 33:889–897
Kumar A, Manimekalai MS, Grüber G (2008) Acta Crystallogr D: Biol Crystallogr D64:1110–1115
Kumar A, Manimekalai MS, Balakrishna AM, Hunke C, Weigelt S, Sewald N, Grüber G (2009) Proteins 75:807–819
Levitt M, Sander C, Stern PS (1985) J Mol Biol 181:423–447
Lolkema JS, Chaban Y, Boekema EJ (2003) J Bioenerg Biomembr 35:323–335
Mackerell AD Jr (2004) J Comput Chem 25:1584–1604
Mackerell AD Jr, Nilsson L (2008) Curr Opin Struct Biol 18:194–199
MacKerell AD Jr, Banavali N, Foloppe N (2000) Biopolymers 56:257–265
Manimekalai MS, Kumar A, Balakrishna AM, Grüber G (2009) J Struct Biol 166:38–45
Martyna GJ, Tobias DJ, Klein ML (1994) J Chem Phys 101:4177–4189
Müller V, Grüber G (2003) Cell Mol Life Sci 60:474–494
Numoto N, Kita A, Miki K (2004) Acta Crystallogr D60:810–815
Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K (2005) J Comput Chem 26:1781–1802
Raghunathan D, Gayen S, Grüber G, Verma CS (2010) Biochemistry 49:4181–4190
R Development Core Team (2008) R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0
Schäfer G, Engelhard M, Müller V (1999) Microbiol Mol Biol Rev 63:570–620
Schäfer I, Rössle M, Biuković G, Müller V, Grüber G (2006a) J Bioenerg Biomembr 38:83–92
Schäfer IB, Bailer SM, Düser MG, Börsch M, Bernal RA, Stock D, Grüber G (2006b) J Mol Biol 358:725–740
Seeber M, Cecchini M, Rao F, Settanni G, Caflisch A (2007) Bioinformatics 23:2625–2627
Sharp KA, Nicholls A, Fine RF, Honig B (1991) Science 252:106–109
Sitkoff D, Sharp KA, Honig B (1994) Biophys Chem 51:397–403
Srinivasan J, Miller J, Kollman PA, Case DA (1998) J Biomol Struct Dyn 16:671–682
Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) EMBO J 1:945–951
Weber J, Senior AE (2003) FEBS Lett 545:61–70
Willis BTM, Pryor AW (1975) Thermal vibrations in crystallography. Cambridge University Press
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 1.34 mb)
Rights and permissions
About this article
Cite this article
Raghunathan, D., Gayen, S., Kumar, A. et al. Subunit F modulates ATP binding and migration in the nucleotide-binding subunit B of the A1AO ATP synthase of Methanosarcina mazei Gö1. J Bioenerg Biomembr 44, 213–224 (2012). https://doi.org/10.1007/s10863-012-9410-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10863-012-9410-y