Redox-induced activation of the proton pump in the respiratory complex i

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 37, 2015, Pages 11571-11576

  Sharma, Vivek ^a   Belevich, Galina ^b   Gamiz Hernandez, Ana P ^c   Róg, Tomasz ^a   Vattulainen, Ilpo ^a,d   Verkhovskaya, Marina L ^b   Wikström, Mårten ^b   Hummer, Gerhard ^e   Kaila, Ville R I ^c  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^e MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

Cell respiration; Electron transfer; Molecular dynamics simulations; NADH quinone oxidoreductase; QM MM simulations

Indexed keywords

ANTIPORTER; ASPARAGINE; BACTERIAL PROTEIN; HISTIDINE; HYDROQUINONE DERIVATIVE; MEMBRANE PROTEIN; NQO4 PROTEIN; PROTON; PROTON PUMP; QUINOL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TYROSINE; UNCLASSIFIED DRUG; LIPID BILAYER; PHOTOSYNTHESIS; PROTEIN BINDING;

ARTICLE; ATOM; CONFORMATIONAL TRANSITION; DISSOCIATION; ELECTRON TRANSPORT; ENZYME ACTIVITY; LARGE SCALE PRODUCTION; MITOCHONDRIAL RESPIRATION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SUBUNIT; PROTON TRANSPORT; QUANTUM MECHANICS; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY; THERMUS THERMOPHILUS; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; LIPID BILAYER; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; TEMPERATURE; X RAY;

ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX I; ESCHERICHIA COLI; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTON PUMPS; STATIC ELECTRICITY; TEMPERATURE; THERMUS THERMOPHILUS; X-RAYS;

EID: 84941671298     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1503761112     Document Type: Article

References (55)

1. Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75:69-92.
2. Verkhovskaya M, Bloch DA (2013) Energy-converting respiratory Complex I: On the way to the molecular mechanism of the proton pump. Int J Biochem Cell Biol 45(2): 491-511.
3. 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.
4. Mimaki M, Wang X, McKenzie M, Thorburn DR, Ryan MT (2012) Understanding mi-tochondrial complex I assembly in health and disease. Biochim Biophys Acta 1817(6): 851-862.
5. Verkhovskaya ML, Belevich N, Euro L, Wikström M, Verkhovsky MI (2008) Real-time electron transfer in respiratory complex I. Proc Natl Acad Sci USA 105(10):3763-3767.
6. Brandt U (2011) A two-state stabilization-change mechanism for proton-pumping complex I. Biochim Biophys Acta 1807(10):1364-1369.
7. Euro L, Belevich G, Verkhovsky MI, Wikström M, Verkhovskaya M (2008) Conserved lysine residues of the membrane subunit NuoM are involved in energy conversion by the proton-pumping NADH:ubiquinone oxidoreductase (Complex I). Biochim Biophys Acta 1777(9):1166-1172.
8. Wikström M, Hummer G (2012) Stoichiometry of proton translocation by respiratory complex I and its mechanistic implications. Proc Natl Acad Sci USA 109(12):4431-4436.
9. Baradaran R, Berrisford JM, Minhas GS, Sazanov LA (2013) Crystal structure of the entire respiratory complex I. Nature 494(7438):443-448.
10. de Vries S, Dörner K, Strampraad MJF, Friedrich T (2015) Electron tunneling rates in respiratory complex I are tuned for efficient energy conversion. Angew Chem Int Ed Engl 54(9):2844-2848.
11. Wikström M (1984) Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett 169(2):300-304.
12. Berrisford JM, Sazanov LA (2009) Structural basis for the mechanism of respiratory complex I. J Biol Chem 284(43):29773-29783.
13. Ohnishi ST, Salerno JC, Ohnishi T (2010) Possible roles of two quinone molecules in direct and indirect proton pumps of bovine heart NADH-quinone oxidoreductase (complex I). Biochim Biophys Acta 1797(12):1891-1893.
14. Pohl T, et al. (2008) Nucleotide-induced conformational changes in the Escherichia coli NADH:ubiquinone oxidoreductase (complex I). Biochem Soc Trans 36(Pt 5): 971-975.
15. Kaila VRI, Wikström M, Hummer G (2014) Electrostatics, hydration, and proton transfer dynamics in the membrane domain of respiratory complex I. Proc Natl Acad Sci USA 111(19):6988-6993.
16. Sazanov LA, Baradaran R, Efremov RG, Berrisford JM, Minhas G (2013) A long road towards the structure of respiratory complex I, a giant molecular proton pump. Biochem Soc Trans 41(5):1265-1271.
17. Zickermann V, et al. (2015) Structural biology. Mechanistic insight from the crystal structure of mitochondrial complex I. Science 347(6217):44-49.
18. Moser CC, Farid TA, Chobot SE, Dutton PL (2006) Electron tunneling chains of mitochondria. Biochim Biophys Acta 1757(9-10):1096-1109.
19. Tocilescu MA, Fendel U, Zwicker K, Kerscher S, Brandt U (2007) Exploring the ubi-quinone binding cavity of respiratory complex I. J Biol Chem 282(40):29514-29520.
20. Efremov RG, Sazanov LA (2012) The coupling mechanism of respiratory complex I-a structural and evolutionary perspective. Biochim Biophys Acta 1817(10):1785-1795.
21. Verkhovsky M, Bloch DA, Verkhovskaya M (2012) Tightly-bound ubiquinone in the Escherichia coli respiratory complex I. Biochim Biophys Acta 1817(9):1550-1556.
22. Verkhovskaya M, Wikström M (2014) Oxidoreduction properties of bound ubiqui-none in Complex I from Escherichia coli. Biochim Biophys Acta 1837(2):246-250.
23. Masuya T, Murai M, Ifuku K, Morisaka H, Miyoshi H (2014) Site-specific chemical labeling of mitochondrial respiratory complex I through ligand-directed tosylate chemistry. Biochemistry 53(14):2307-2317.
24. Verkhovskaya M, Knuuti J, Wikström M (2011) Role of Ca(2+) in structure and function of Complex I from Escherichia coli. Biochim Biophys Acta 1807(1):36-41.
25. Sinha PK, et al. (2015) Conserved amino acid residues of the NuoD segment important for structure and function of Escherichia coli NDH-1 (complex I). Biochemistry 54(3): 753-764.
26. Belevich G, Euro L, Wikström M, Verkhovskaya M (2007) Role of the conserved argi-nine 274 and histidine 224 and 228 residues in the NuoCD subunit of complex I from Escherichia coli. Biochemistry 46(2):526-533.
27. Grgic L, Zwicker K, Kashani-Poor N, Kerscher S, Brandt U (2004) Functional significance of conserved histidines and arginines in the 49-kDa subunit of mitochondrial complex I. J Biol Chem 279(20):21193-21199.
28. Kaila VRI, Verkhovsky MI, Hummer G, Wikström M (2008) Glutamic acid 242 is a valve in the proton pump of cytochrome c oxidase. Proc Natl Acad Sci USA 105(17):6255-6259.
29. Kaila VRI, Verkhovsky MI, Hummer G, Wikström M (2009) Mechanism and energetics by which glutamic acid 242 prevents leaks in cytochrome c oxidase. Biochim Biophys Acta 1787(10):1205-1214.
30. Sinha PK, et al. (2009) Critical roles of subunit NuoH (ND1) in the assembly of peripheral subunits with the membrane domain of Escherichia coli NDH-1. J Biol Chem 284(15):9814-9823.
31. Kurki S, Zickermann V, Kervinen M, Hassinen I, Finel M (2000) Mutagenesis of three conserved Glu residues in a bacterial homologue of the ND1 subunit of complex I affects ubiquinone reduction kinetics but not inhibition by dicyclohexylcarbodiimide. Biochemistry 39(44):13496-13502.
32. Valentino ML, et al. (2004) The ND1 gene of complex I is a mutational hot spot for Leber's hereditary optic neuropathy. Ann Neurol 56(5):631-641.
33. Kaila VRI, Verkhovsky MI, Wikström M (2010) Proton-coupled electron transfer in cytochrome oxidase. Chem Rev 110(12):7062-7081.
34. Wikström M, Sharma V, Kaila VRI, Hosler JP, Hummer G (2015) New perspectives on proton pumping in cellular respiration. Chem Rev 115(5):2196-2221.
35. Smart OS, Neduvelil JG, Wang X, Wallace BA, Sansom MSP (1996) HOLE: A program for the analysis of the pore dimensions of ion channel structural models. J Mol Graph 14(6):354-360, 376.
36. Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234(3):779-815.
37. MacKerell AD, Jr, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102(18):3586-3616.
38. Klauda JB, et al. (2010) Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types. J Phys Chem B 114(23):7830-7843.
39. Ahlrichs R, Bär M, Häser M, Horn H, Kölmel C (1989) Electronic structure calculations on workstation computers: The program system turbomole. Chem Phys Lett 162(3):165-169.
40. 1 complex predicted by atomistic molecular dynamics simulations. Biochim Biophys Acta 1827(6):761-768.
41. Chang CH, Kim K (2009) Density functional theory calculation of bonding and charge parameters for molecular dynamics studies on [FeFe] hydrogenases. J Chem Theory Comput 5(4):1137-1145.
42. Freddolino PL, Dittrich M, Schulten K (2006) Dynamic switching mechanisms in LOV1 and LOV2 domains of plant phototropins. Biophys J 91(10):3630-3639.
43. Vagedes P, Rabenstein B, Åqvist J, Marelius J, Knapp EW (2000) The deacylation step of acetylcholinestrase: Computer simulation studies. J Am Chem Soc 122(49):12254-12262.
44. Phillips JC, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26(16):1781-1802.
45. Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. J Mol Graph 14(1):33-38.
46. Kieseritzky G, Knapp EW (2008) Optimizing pKa computation in proteins with pH adapted conformations. Proteins 71(3):1335-1348.
47. Kieseritzky G, Knapp EW (2008) Improved pK(a) prediction: Combining empirical and semimicroscopic methods. J Comput Chem 29(15):2575-2581.
48. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nano-systems: Application to microtubules and the ribosome. Proc Natl Acad Sci USA 98(18): 10037-10041.
49. Rabenstein B, Knapp EW (2001) Calculated pH-dependent population and protonation of carbon-monoxy-myoglobin conformers. Biophys J 80(3):1141-1150.
50. Becke AD (1993) Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 98(7):5648-5652.
51. Lee C, Yang W, Parr RG (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B Condens Matter 37(2): 785-789.
52. Weigend F, Ahlrichs R (2005) Balanced basis sets of split valence, triple zeta valence and quadruple zeta valence quality for H to Rn: Design and assessment of accuracy. Phys Chem Chem Phys 7(18):3297-3305.
53. Shao Y, et al. (2006) Advances in methods and algorithms in a modern quantum chemistry program package. Phys Chem Chem Phys 8(27):3172-3191.
54. Woodcock HL, 3rd, et al. (2007) Interfacing Q-Chem and CHARMM to perform QM/MM reaction path calculations. J Comput Chem 28(9):1485-1502.
55. Brooks BR, et al. (2009) CHARMM: The biomolecular simulation program. J Comput Chem 30(10):1545-1614.