Role of aspartate 132 at the orifice of a proton pathway in cytochrome c oxidase

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

Volumn 110, Issue 22, 2013, Pages 8912-8917

  Johansson, Ann Louise ^a   Högbom, Martin ^a   Carlsson, Jens ^a   Gennis, Robert B ^b   Brzezinski, Peter ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Cytochrome aa3; Electron transfer; Metalloprotein; Respiration; Transporter

Indexed keywords

ASPARAGINE; ASPARTIC ACID; CYTOCHROME C OXIDASE; THREONINE; ZINC;

ARTICLE; BINDING SITE; CONTROLLED STUDY; NONHUMAN; PH; PRIORITY JOURNAL; PROTON TRANSPORT;

CYTOCHROME AA3; ELECTRON TRANSFER; METALLOPROTEIN; RESPIRATION; TRANSPORTER;

ABSORPTION; ASPARTIC ACID; CRYSTALLOGRAPHY, X-RAY; ELECTRON TRANSPORT COMPLEX IV; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PROTON PUMPS; PROTON-MOTIVE FORCE; RHODOBACTER SPHAEROIDES; ZINC;

EID: 84878440015     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1303954110     Document Type: Article

References (61)

1. Decoursey TE (2003) Voltage-gated proton channels and other proton transfer pathways. Physiol Rev 83(2):475-579.
2. Wraight CA (2006) Chance and design-proton transfer in water, channels and bioenergetic proteins. Biochim Biophys Acta Bioenerg 1757(8):886-912.
3. Sacks V, et al. (1998) The dynamic feature of the proton collecting antenna of a protein surface. Biochim Biophys Acta Bioenerg 1365(1-2):232-240.
4. Ädelroth P, Brzezinski P (2004) Surface-mediated proton-transfer reactions in membrane-bound proteins. Biochim Biophys Acta 1655(1-3):102-115.
5. Musset B, et al. (2011) Aspartate 112 is the selectivity filter of the human voltagegated proton channel. Nature 480(7376):273-277.
6. Svensson-Ek M, et al. (2002) The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J Mol Biol 321(2): 329-339.
7. Qin L, Hiser C, Mulichak A, Garavito RM, Ferguson-Miller S (2006) Identification of conserved lipid/detergent-binding sites in a high-resolution structure of the membrane protein cytochrome c oxidase. Proc Natl Acad Sci USA 103(44):16117-16122.
8. Fetter JR, et al. (1995) Possible proton relay pathways in cytochrome c oxidase. Proc Natl Acad Sci USA 92(5):1604-1608.
9. Konstantinov AA, Siletsky S, Mitchell D, Kaulen A, Gennis RB (1997) The roles of the two proton input channels in cytochrome c oxidase from Rhodobacter sphaeroides probed by the effects of site-directed mutations on time-resolved electrogenic intraprotein proton transfer. Proc Natl Acad Sci USA 94(17):9085-9090.
10. Brzezinski P, Ädelroth P (1998) Pathways of proton transfer in cytochrome c oxidase. J Bioenerg Biomembr 30(1):99-107.
11. Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376(6542):660-669.
12. Kaila VRI, Verkhovsky MI, Wikström M (2010) Proton-coupled electron transfer in cytochrome oxidase. Chem Rev 110(12):7062-7081.
13. Song Y, Michonova-Alexova E, Gunner MR (2006) Calculated proton uptake on anaerobic reduction of cytochrome C oxidase: Is the reaction electroneutral? Biochemistry 45(26):7959-7975.
14. Olkhova E, Helms V, Michel H (2005) Titration behavior of residues at the entrance of the D-pathway of cytochrome c oxidase from paracoccus denitrificans investigated by continuum electrostatic calculations. Biophys J 89(4):2324-2331.
15. Fetter J, et al. (1996) Fatty acids stimulate activity and restore respiratory control in a proton channel mutant of cytochrome c oxidase. FEBS Lett 393(2-3):155-160.
16. Smirnova IA, Ädelroth P, Gennis RB, Brzezinski P (1999) Aspartate-132 in cytochrome c oxidase from Rhodobacter sphaeroides is involved in a two-step proton transfer during oxo-ferryl formation. Biochemistry 38(21):6826-6833.
17. Gorbikova EA, Belevich NP, Wikström M, Verkhovsky MI (2007) Time-resolved ATRFTIR spectroscopy of the oxygen reaction in the D124N mutant of cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 46(45):13141-13148.
18. Brändén G, Pawate AS, Gennis RB, Brzezinski P (2006) Controlled uncoupling and recoupling of proton pumping in cytochrome c oxidase. Proc Natl Acad Sci USA 103(2):317-322.
19. Varanasi L, Hosler J (2011) Alternative initial proton acceptors for the D pathway of Rhodobacter sphaeroides cytochrome c oxidase. Biochemistry 50(14):2820-2828.
20. Zhu J, Han H, Pawate A, Gennis RB (2010) Decoupling mutations in the D-channel of the aa(3)-type cytochrome c oxidase from Rhodobacter sphaeroides suggest that a continuous hydrogen-bonded chain of waters is essential for proton pumping. Biochemistry 49(21):4476-4482.
21. Belevich I, Verkhovsky MI (2008) Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid Redox Signal 10(1):1-29.
22. Karpefors M, Ädelroth P, Aagaard A, Smirnova IA, Brzezinski P (1999) The deuterium isotope effect as a tool to investigate enzyme catalysis: Proton-transfer control mechanisms in cytochrome c oxidase. Isr J Chem 39(3-4):427-437.
23. Karpefors M, Ädelroth P, Brzezinski P (2000) Localized control of proton transfer through the D-pathway in cytochrome c oxidase: Application of the proton-inventory technique. Biochemistry 39(23):6850-6856.
24. Namslauer A, Brzezinski P (2004) Structural elements involved in electron-coupled proton transfer in cytochrome c oxidase. FEBS Lett 567(1):103-110.
25. Ädelroth P, Ek M, Brzezinski P (1998) Factors determining electron-transfer rates in cytochrome c oxidase: Investigation of the oxygen reaction in the R. sphaeroides enzyme. Biochim Biophys Acta 1367(1-3):107-117.
26. Namslauer A, Aagaard A, Katsonouri A, Brzezinski P (2003) Intramolecular protontransfer reactions in a membrane-bound proton pump: The effect of pH on the peroxy to ferryl transition in cytochrome c oxidase. Biochemistry 42(6):1488-1498.
27. KarpeforsM, Ädelroth P, Zhen Y, Ferguson-Miller S, Brzezinski P (1998) Proton uptake controls electron transfer in cytochrome c oxidase. Proc Natl Acad Sci USA 95(23): 13606-13611.
28. Aagaard A, Brzezinski P (2001) Zinc ions inhibit oxidation of cytochrome c oxidase by oxygen. FEBS Lett 494(3):157-160.
29. Aagaard A, Namslauer A, Brzezinski P (2002) Inhibition of proton transfer in cytochrome c oxidase by zinc ions: Delayed proton uptake during oxygen reduction. Biochim Biophys Acta 1555(1-3):133-139.
30. Faxén K, Salomonsson L, Ädelroth P, Brzezinski P (2006) Inhibition of proton pumping by zinc ions during specific reaction steps in cytochrome c oxidase. Biochim Biophys Acta 1757(5-6):388-394.
31. Kannt A, Ostermann T, Müller H, Ruitenberg M (2001) Zn(2+) binding to the cytoplasmic side of Paracoccus denitrificans cytochrome c oxidase selectively uncouples electron transfer and proton translocation. FEBS Lett 503(2-3):142-146.
32. Vygodina TV, Zakirzianova W, Konstantinov AA (2008) Inhibition of membranebound cytochrome c oxidase by zinc ions: High-affinity Zn2+-binding site at the P-side of the membrane. FEBS Lett 582(30):4158-4162.
33. Kuznetsova SS, Azarkina NV, Vygodina TV, Siletsky SA, Konstantinov AA (2005) Zinc ions as cytochrome C oxidase inhibitors: Two sites of action. Biochemistry (Mosc) 70(2):128-136.
34. Mills DA, Schmidt B, Hiser C, Westley E, Ferguson-Miller S (2002) Membrane potentialcontrolled inhibition of cytochrome c oxidase by zinc. J Biol Chem 277(17): 14894-14901.
35. Qin L, et al. (2007) Crystallographic location and mutational analysis of Zn and Cd inhibitory sites and role of lipidic carboxylates in rescuing proton path mutants in cytochrome c oxidase. Biochemistry 46(21):6239-6248.
36. Muramoto K, et al. (2007) A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase. Proc Natl Acad Sci USA 104(19):7881-7886.
37. Liu J, Qin L, Ferguson-Miller S (2011) Crystallographic and online spectral evidence for role of conformational change and conserved water in cytochrome oxidase proton pump. Proc Natl Acad Sci USA 108(4):1284-1289.
38. Ädelroth P, Hosler J (2006) Surface proton donors for the D-pathway of cytochrome c oxidase in the absence of subunit III. Biochemistry 45(27):8308-8318.
39. García-Horsman JA, Puustinen A, Gennis RB, Wikström M (1995) Proton transfer in cytochrome bo3 ubiquinol oxidase of Escherichia coli: Second-site mutations in subunit I that restore proton pumping in the mutant Asp135->Asn. Biochemistry 34(13):4428-4433.
40. Henry RM, Caplan D, Fadda E, Pomès R (2011) Molecular basis of proton uptake in single and double mutants of cytochrome c oxidase. J Phys Condens Matter 23(23): 234102.
41. Brandsburg-Zabary S, Fried O, Marantz Y, Nachliel E, Gutman M (2000) Biophysical aspects of intra-protein proton transfer. Biochim Biophys Acta Bioenerg 1458(1): 120-134.
42. Xu J, Voth GA (2006) Free energy profiles for H+ conduction in the D-pathway of cytochrome c oxidase: A study of the wild type and N98D mutant enzymes. Biochim Biophys Acta 1757(7):852-859.
43. Henry RM, Yu CH, Rodinger T, Pomès R (2009) Functional hydration and conformational gating of proton uptake in cytochrome c oxidase. J Mol Biol 387(5):1165-1185.
44. Olsson MHM, Siegbahn PEM, Blomberg MRA, Warshel A (2007) Exploring pathways and barriers for coupled ET/PT in cytochrome c oxidase: A general framework for examining energetics and mechanistic alternatives. Biochim Biophys Acta Bioenerg 1767(3):244-260.
45. Olsson MH, Warshel A (2006) Monte Carlo simulations of proton pumps: On the working principles of the biological valve that controls proton pumping in cytochrome c oxidase. Proc Natl Acad Sci USA 103(17):6500-6505.
46. Blomberg MRA, Siegbahn PEM (2012) The mechanism for proton pumping in cytochrome c oxidase from an electrostatic and quantum chemical perspective. Biochim Biophys Acta Bioenerg 1817(4):495-505.
47. Siegbahn PEM, Blomberg MRA (2007) Energy diagrams and mechanism for proton pumping in cytochrome c oxidase. Biochim Biophys Acta Bioenerg 1767(9):1143-1156.
48. Chakrabarty S, Warshel A (2013) Capturing the energetics of water insertion in biological systems: The water flooding approach. Proteins 81(1):93-106.
49. Lepp H, Salomonsson L, Zhu JP, Gennis RB, Brzezinski P (2008) Impaired proton pumping in cytochrome c oxidase upon structural alteration of the D pathway. Biochim Biophys Acta 1777(7-8):897-903.
50. Brzezinski P, Johansson AL (2010) Variable proton-pumping stoichiometry in structural variants of cytochrome c oxidase. Biochim Biophys Acta Bioenerg 1797(6-7): 710-723.
51. Wikström M, Verkhovsky MI (2011) The D-channel of cytochrome oxidase: An alternative view. Biochim Biophys Acta Bioenerg 1807(10):1273-1278.
52. Chakrabarty S, Namslauer I, Brzezinski P, Warshel A (2011) Exploration of the cytochrome c oxidase pathway puzzle and examination of the origin of elusive mutational effects. Biochim Biophys Acta Bioenerg 1807(4):413-426.
53. Popovic DM, Leontyev IV, Beech DG, Stuchebrukhov AA (2010) Similarity of cytochrome c oxidases in different organisms. Proteins 78(12):2691-2698.
54. Mitchell DM, Gennis RB (1995) Rapid purification of wildtype and mutant cytochrome c oxidase from Rhodobacter sphaeroides by Ni(2+)-NTA affinity chromatography. FEBS Lett 368(1):148-150.
55. Zhen Y, et al. (1998) Overexpression and purification of cytochrome coxidase from Rhodobacter sphaeroides. Protein Expr Purif 13:326-336.
56. Brändén M, et al. (2001) On the role of the K-proton transfer pathway in cytochrome c oxidase. Proc Natl Acad Sci USA 98(9):5013-5018.
57. DeLano WL (2002) The PyMOL Molecular Graphics System (DeLano Scientific, Palo Alto, CA).
58. Salomonsson L, Brändén G, Brzezinski P (2008) Deuterium isotope effect of proton pumping in cytochrome c oxidase. Biochim Biophys Acta Bioenerg 1777(4):343-350.
59. Johansson AL, et al. (2013) Proton uptake and pKa changes in the uncoupled Asn139Cys variant of cytochrome c oxidase. Biochemistry 52(5):827-836.
60. Dolinsky TJ, et al. (2007) PDB2PQR: Expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res 35 (Web Server issue, Suppl 2)W522-W525.
61. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc Natl Acad Sci USA 98(18): 10037-10041.