Roles of semiquinone species in proton pumping mechanism by complex I

Journal of Bioenergetics and Biomembranes

Volumn 46, Issue 4, 2014, Pages 269-277

  Nakamaru Ogiso, Eiko ^a   Narayanan, Madhavan ^a   Sakyiama, Joseph A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Complex I; Energy coupling; EPR; Flavin; Iron sulfur clusters; NADH dehydrogenase; Proton pumping; Reactive oxygen species; Semiquinone

Indexed keywords

GRAMICIDIN D; PROTEOLIPOSOME; PROTON; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SEMIQUINONE; ANTIINFECTIVE AGENT; ESCHERICHIA COLI PROTEIN; GAMMA BUTYROLACTONE; GRAMICIDIN; NUOL PROTEIN, E COLI; NUOM PROTEIN, E COLI; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SQUAMOTACIN; SUCCINATE DEHYDROGENASE (UBIQUINONE);

BINDING SITE; CONFORMATION; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENERGY TRANSFER; ESCHERICHIA COLI; MAGNETISM; NONHUMAN; PH; PHYSICAL CHEMISTRY; PROTON MOTIVE FORCE; PROTON TRANSPORT; SHORT SURVEY; STOICHIOMETRY; ANALOGS AND DERIVATIVES; CHEMISTRY; DRUG EFFECTS; ELECTRON SPIN RESONANCE; ENZYMOLOGY; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION;

4-BUTYROLACTONE; ANTI-BACTERIAL AGENTS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GRAMICIDIN; NADH DEHYDROGENASE; OXIDATION-REDUCTION;

EID: 84906331120     PISSN: 0145479X     EISSN: 15736881     Source Type: Journal    
DOI: 10.1007/s10863-014-9557-9     Document Type: Short Survey

References (53)

1. Bales BL, Peric M, Lamy-Freund MT (1998) Contributions to the Gaussian line broadening of the proxyl spin probe EPR spectrum due to magnetic-field modulation and unresolved proton hyperfine structure. J Magn Reson 132:279-286 (Pubitemid 128450728)
2. Baradaran R, Berrisford JM, Minhas GS, Sazanov LA (2013) Crystal structure of the entire respiratory complex I. Nature 494:443-448
3. Baranova EA, Holt PJ, Sazanov LA (2007a) Projection structure of the membrane domain of Escherichia coli respiratory complex I at 8 A resolution. J Mol Biol 366:140-154 (Pubitemid 46123333)
4. Baranova EA, Morgan DJ, Sazanov LA (2007b) Single particle analysis confirms distal location of subunits NuoL and NuoMin Escherichia coli complex I. J Struct Biol 159:238-242 (Pubitemid 47096869)
5. Berrisford JM, Thompson CJ, Sazanov LA (2008) Chemical and NADH-induced, ROS-dependent, cross-linking between subunits of complex I from Escherichia coli and Thermus thermophilus. Biochemistry 47:10262-10270
6. Bogachev AV, Murtazina RA, Skulachev VP (1996) H+/e- stoichiometry for NADH dehydrogenase I and dimethyl sulfoxide reductase in anaerobically grown Escherichia coli cells. J Bacteriol 178:6233-6237 (Pubitemid 26365704)
7. Bongaerts J, Zoske S, Weidner U, Unden G (1995) Transcriptional regulation of the proton translocating NADH dehydrogenase genes (nuoA-N) of Escherichia coli by electron acceptors, electron donors and gene regulators. Mol Microbiol 16:521-534
8. Bowyer JR, Ohnishi T (1985) In: Coenxyme Q, Lenaz G (eds) EPR spedtrostudy in the study of ubisemiquinones in redox chains. Wiley, New York, pp 409-432
9. Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75:69-92
10. Brandt U, Kerscher S, Drose S, Zwicker K, Zickermann V (2003) Proton pumping by NADH:ubiquinone oxidoreductase. A redox driven conformational change mechanism? FEBS Lett 545:9-17 (Pubitemid 36629630)
11. Chevallet M, Dupuis A, Lunardi J, van Belzen R, Albracht SP, Issartel JP (1997) The NuoI subunit of the Rhodobacter capsulatus respiratory Complex I (equivalent to the bovine TYKY subunit) is required for proper assembly of the membraneous and peripheral domains of the enzyme. Eur J Biochem FEBS 250:451-458 (Pubitemid 28012688)
12. De Jong AM, Albracht SP (1994) Ubisemiquinones as obligatory intermediates in the electron transfer from NADH to ubiquinone. Eur J Biochem FEBS 222:975-982 (Pubitemid 24212313)
13. Degli Esposti M (1998) Inhibitors of NADH-ubiquinone reductase: an overview. Biochim Biophys Acta 1364:222-235
14. Fato R, Bergamini C, Bortolus M, Maniero AL, Leoni S, Ohnishi T, Lenaz G (2008) Differential effects of mitochondrial Complex I inhibitors on production of reactive oxygen species. Biochim Biophys Acta 1787:384-392
15. Fendel U, Tocilescu MA, Kerscher S, Brandt U (2008) Exploring the inhibitor binding pocket of respiratory complex I. Biochim Biophys Acta 1777:660-665
16. Friedrich T (2001) Complex I: a chimaera of a redox and conformationdriven proton pump? J Bioenerg Biomembr 33:169-177
17. Galkin AS, Grivennikova VG, Vinogradov AD (1999) ->H+/2e- stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles. FEBS Lett 451:157-161 (Pubitemid 29231941)
18. Galkin A, Drose S, Brandt U (2006) The proton pumping stoichiometry of purified mitochondrial complex I reconstituted into proteoliposomes. Biochim Biophys Acta 1757:1575-1581 (Pubitemid 44841960)
19. Hales BJ, Case EE (1981) Immobilized radicals IV. Biological semiquinone anions and neutral semiquinones. Biochim Biophys Acta 637:291-302
20. Hirst J (2013) Mitochondrial complex I. Annu Rev Biochem 82:551-575
21. Ingledew WJ, Ohnishi T, Salerno JC (1995) Studies on a stabilisation of ubisemiquinone by Escherichia coli quinol oxidase, cytochrome bo. Eur J Biochem FEBS 227:903-908
22. Kotlyar AB, Sled VD, Burbaev DS, Moroz IA, Vinogradov AD (1990) Coupling site I and the rotenone-sensitive ubisemiquinone in tightly coupled submitochondrial particles. FEBS Lett 264:17-20 (Pubitemid 20139794)
23. Magnitsky S, Toulokhonova L, Yano T, Sled VD, Hagerhall C, Grivennikova VG, Burbaev DS, Vinogradov AD, Ohnishi T (2002) EPR characterization of ubisemiquinones and iron-sulfur cluster N2, central components of the energy coupling in the NADH-ubiquinone oxidoreductase (complex I) in situ. J Bioenerg Biomembr 34:193-208 (Pubitemid 34847802)
24. Mathiesen C, Hagerhall C (2002) Transmembrane topology of the NuoL, M and N subunits of NADH:quinone oxidoreductase and their homologues among membrane-bound hydrogenases and bona fide antiporters. Biochim Biophys Acta 1556:121-132 (Pubitemid 35379670)
25. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144-148
26. Mitchell P (1979) Keilin's respiratory chain concept and its chemiosmotic consequences. Science 206:1148-1159
27. Moser CC, Farid TA, Chobot SE, Dutton PL (2006) Electron tunneling chains of mitochondria. Biochim Biophys Acta 1757:1096-1109 (Pubitemid 44472548)
28. Murai M, Sekiguchi K, Nishioka T, Miyoshi H (2009) Characterization of the inhibitor binding site in mitochondrial NADH-ubiquinone oxidoreductase by photoaffinity labeling using a quinazoline-type inhibitor. Biochemistry 48:688-698
29. Nakamaru-Ogiso E, Kao MC, Chen H, Sinha SC, Yagi T, Ohnishi T (2010) The membrane subunit NuoL(ND5) is involved in the indirect proton pumping mechanism of Escherichia coli complex I. J Biol Chem 285:39070-39078
30. Nakashima Y, Shinzawa-Itoh K, Watanabe K, Naoki K, Hano N, Yoshikawa S (2002) The second coenzyme Q1 binding site of bovine heart NADH: coenzyme Q oxidoreductase. J Bioenerg Biomembr 34:89-94 (Pubitemid 34477971)
31. Narayanan M, Gabrieli DJ, Leung SA, Elguindy MM, Glaser CA, Saju N, Sinha SC, Nakamaru-Ogiso E (2013) Semiquinone and cluster N6 signals in His-tagged proton-translocating NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli. J Biol Chem288:14310-14319
32. Ohnishi T, Salerno JC (2005) Conformation-driven and semiquinone-gated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett 579:4555-4561 (Pubitemid 41218626)
33. Ohnishi T, Sled VD, Yano T, Yagi T, Burbaev DS, Vinogradov AD (1998) Structure-function studies of iron-sulfur clusters and semiquinones in the NADH-Q oxidoreductase segment of the respiratory chain. Biochim Biophys Acta 1365:301-308 (Pubitemid 29359272)
34. Ohnishi T, Johnson JE Jr, Yano T, Lobrutto R, Widger WR (2005) Thermodynamic and EPR studies of slowly relaxing ubisemiquinone species in the isolated bovine heart complex I. FEBS Lett 579:500-506 (Pubitemid 40092434)
35. Ohnishi ST, Shinzawa-Itoh K, Ohta K, Yoshikawa S, Ohnishi T (2010) New insights into the superoxide generation sites in bovine heart NADH-ubiquinone oxidoreductase (Complex I): the significance of protein-associated ubiquinone and the dynamic shifting of generation sites between semiflavin and semiquinone radicals. Biochim Biophys Acta 1797:1901-1909
36. Ripple MO, Kim N, Springett R (2013) Mammalian complex I pumps 4 protons per 2 electrons at high and physiological proton motive force in living cells. J Biol Chem 288:5374-5380
37. Robertson DE, Prince RC, Bowyer JR, Matsuura K, Dutton PL, Ohnishi T (1984) Thermodynamic properties of the semiquinone and its binding site in the ubiquinol-cytochrome c (c2) oxidoreductase of respiratory and photosynthetic systems. J Biol Chem 259:1758-1763 (Pubitemid 14146563)
38. Sazanov LA (2007) Respiratory complex I: mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. Biochemistry 46:2275-2288
39. Sazanov LA, Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430-1436 (Pubitemid 43376691)
40. Sazanov LA, Peak-Chew SY, Fearnley IM, Walker JE (2000) Resolution of the membrane domain of bovine complex I into subcomplexes: implications for the structural organization of the enzyme. Biochemistry 39:7229-7235 (Pubitemid 30413113)
41. Sinha PK, Torres-Bacete J, Nakamaru-Ogiso E, Castro-Guerrero N, Matsuno-Yagi A, Yagi T (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 284:9814-9823
42. Suzuki H, King TE (1983) Evidence of an ubisemiquinone radical(s) from the NADH-ubiquinone reductase of the mitochondrial respiratory chain. J Biol Chem 258:352-358
43. Tocilescu MA, Fendel U, Zwicker K, Kerscher S, Brandt U (2007) Exploring the ubiquinone binding cavity of respiratory complex I. J Biol Chem 282:29514-29520 (Pubitemid 350043352)
44. Tocilescu MA, Fendel U, Zwicker K, Drose S, Kerscher S, Brandt U (2010) The role of a conserved tyrosine in the 49-kDa subunit of complex I for ubiquinone binding and reduction. Biochim Biophys Acta 1797:625-632
45. van Belzen R, Kotlyar AB, Moon N, Dunham WR, Albracht SP (1997) The iron-sulfur clusters 2 and ubisemiquinone radicals of NADH: ubiquinone oxidoreductase are involved in energy coupling in submitochondrial particles. Biochemistry 36:886-893 (Pubitemid 27110970)
46. Vinogradov AD, Sled VD, Burbaev DS, Grivennikova VG, Moroz IA, Ohnishi T (1995) Energy-dependent Complex I-associated ubisemiquinones in submitochondrial particles. FEBS Lett 370:83-87
47. Wikstrom M (1984) Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett 169:300-304
48. Wraight CA (2004) Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides. Front Biosci J Virtual Libr 9:309-337
49. Yagi T, Matsuno-Yagi A (2003) The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 42:2266-2274 (Pubitemid 36255200)
50. Yagi T, Yano T, Di Bernardo S, Matsuno-Yagi A (1998) Procaryotic complex I (NDH-1), an overview. Biochim Biophys Acta 1364:125-133
51. Yano T, Dunham WR, Ohnishi T (2005) Characterization of the delta muH+-sensitive ubisemiquinone species (SQ(Nf)) and the interaction with cluster N2: new insight into the energy-coupled electron transfer in complex I. Biochemistry 44:1744-1754 (Pubitemid 40204415)
52. Yip CY, Harbour ME, Jayawardena K, Fearnley IM, Sazanov LA (2011) Evolution of respiratory complex I: "supernumerary" subunits are present in the alpha-proteobacterial enzyme. J Biol Chem 286:5023-5033
53. Yuasa J, Yamada S, Fukuzumi S (2008) One-step versus stepwise mechanism in protonated amino acid-promoted electron-transfer reduction of a quinone by electron donors and two-electron reduction by a dihydronicotinamide adenine dinucleotide analogue. Interplay between electron transfer and hydrogen bonding. J Am Chem Soc 130:5808-5820 (Pubitemid 351600514)