Current topics on inhibitors of respiratory complex i

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1857, Issue 7, 2016, Pages 884-891

  Murai, Masatoshi ^a   Miyoshi, Hideto ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Chemical modifications of protein; Complex I; Inhibitors

Indexed keywords

AMILORIDE DERIVATIVE; BIGUANIDE DERIVATIVE; COMPLEX I INHIBITOR; ENZYME INHIBITOR; UNCLASSIFIED DRUG; PROTEIN BINDING; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ARTICLE; DRUG DESIGN; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; STRUCTURAL MODEL; X RAY CRYSTALLOGRAPHY; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ENZYME ACTIVATION; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

BINDING SITES; DRUG DESIGN; ELECTRON TRANSPORT COMPLEX I; ENZYME ACTIVATION; ENZYME INHIBITORS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84957824612     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2015.11.009     Document Type: Article

References (87)

1. M. Degli Esposti Inhibitors of NADH-ubiquinone reductase: an overview Biochim. Biophys. Acta 1364 1998 222 235
2. R. Baradaran, J.M. Berrisford, G.S. Minhas, and L.A. Sazanov Crystal structure of the entire respiratory complex I Nature 494 2013 443 448
3. V. Zickermann, C. Wirth, H. Nasiri, K. Siegmund, H. Schwalbe, C. Hunte, and U. Brandt Mechanistic insight from the crystal structure of mitochondrial complex I Science 347 2015 44 49
4. J.G. Okun, P. Lümmen, and U. Brandt Three classes of inhibitor share a common binding domain in mitochondrial complex I (NADH-ubiquinone oxidoreductase) J. Biol. Chem. 274 1999 2625 2630
5. U. Fendel, M.A. Tocilescu, S. Kerscher, and U. Brandt Exploring the inhibitor binding pocket of respiratory complex I Biochim. Biophys. Acta 1777 2008 660 665
6. H. Miyoshi Structure-activity relationship of some complex I inhibitors Biochim. Biophys. Acta 1364 1998 236 244
7. H. Miyoshi Probing the ubiquinone reduction site in bovine mitochondrial complex I using a series of synthetic ubiquinones and inhibitors J. Bioenerg. Biomembr. 33 2001 223 231
8. M. Murai, and M. Miyoshi Chemical modifications of respiratory complex I for structural and functional studies J. Bioenerg. Biomembr. 46 2014 313 321
9. J. Hirst Mitochondrial complex I Annu. Rev. Biochem. 82 2013 551 575
10. T.R. Kleyman, and E.J. Cragoe Jr. Amiloride and its analogs as tools in the study of ion transport J. Membr. Biol. 105 1988 1 21
11. + exchanger, NHE: structure, regulation, and cellular actions Annu. Rev. Pharmacol. Toxicol. 42 2002 527 552
12. T. Hunt, H.C. Atherton-Watson, S.P. Collingwood, K.J. Coote, S. Czarnecki, H. Danahay, C. Howsham, P. Hunt, D. Paisley, and A. Young Discovery of a novel chemotype of potent human ENaC blockers using a bioisostere approach. Part 2: α-branched quaternary amines Bioorg. Med. Chem. Lett. 22 2012 2877 2879
13. E. Nakamaru-Ogiso, B.B. Seo, T. Yagi, and A. Matsuno-Yagi Amiloride inhibition of the proton-translocating NADH-quinone oxidoreductase of mammals and bacteria FEBS Lett. 549 2003 43 46
14. S. Stolpe, and T. Friedrich The Escherichia coli NADH-ubiquinone oxidoreductase (complex I) is a primary proton pump but may be capable of secondary sodium antiport J. Biol. Chem. 279 2004 18377 18383
15. C. Mathiesen, and C. Hägerhäll 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 2002 121 132
16. M. Murai, S. Murakami, T. Ito, and H. Miyoshi Amilorides bind to the quinone binding pocket of bovine mitochondrial complex I Biochemistry 54 2015 2739 2746
17. M. Murai, A. Ishihara, T. Nishioka, T. Yagi, and H. Miyoshi The ND1 subunit constructs the inhibitor binding domain in bovine heart mitochondrial complex I Biochemistry 2007 6409 6416
18. M. Murai, K. Sekiguchi, T. Nishioka, and H. Miyoshi Characterization of the inhibitor binding site in mitochondrial NADH-ubiquinone oxidoreductase by photoaffinity labeling using a quinazoline-type inhibitor Biochemistry 48 2009 688 698
19. K. Sekiguchi, M. Murai, and H. Miyoshi Exploring the binding site of acetogenin in the ND1 subunit of bovine mitochondrial complex I Biochim. Biophys. Acta 1787 2009 1106 1111
20. N. Kakutani, M. Murai, N. Sakiyama, and H. Miyoshi Exploring the binding site of Δlac-acetogenin in bovine heart mitochondrial NADH-ubiquinone oxidoreductase Biochemistry 49 2010 4794 4803
21. M. Murai, Y. Mashimo, J. Hirst, and H. Miyoshi Exploring interactions between the 49 kDa and ND1 subunits in mitochondrial NADH-ubiquinone oxidoreductase (complex I) by photoaffinity labeling Biochemistry 50 2011 6901 6908
22. Y. Shiraishi, M. Murai, N. Sakiyama, K. Ifuku, and H. Miyoshi Fenpyroximate binds to the interface between PSST and 49 kDa subunits in mitochondrial NADH-ubiquinone oxidoreductase Biochemistry 51 2012 1953 1963
23. K.R. Vinothkumar, P. Zhu, and J. Hirst Architecture of mammalian respiratory complex I Nature 515 2014 80 84
24. T. Ito, M. Murai, H. Morisaka, and H. Miyoshi Identification of the binding position of amilorides in the quinone binding pocket of mitochondrial complex I Biochemistry 54 2015 3677 3686
25. T. Masuya, M. Murai, K. Ifuku, H. Morisaka, and H. Miyoshi Site-specific chemical labeling of mitochondrial respiratory complex I through ligand-directed tosylate chemistry Biochemistry 53 2014 2307 2317
26. T. Masuya, M. Murai, H. Morisaka, and H. Miyoshi Pinpoint chemical modification of Asp160 in the 49 kDa subunit of bovine mitochondrial complex I via a combination of ligand-directed tosyl chemistry and click chemistry Biochemistry 53 2014 7816 7823
27. A.F.G. Cicerol, E. Tartagni, and S. Ertek Metformin and its clinical use: new insights for an old drug in clinical practice Arch. Med. Sci. 8 2012 907 917
28. I. Pernicova, and M. Korbonits Metformin - mode of action and clinical implications for diabetes and cancer Nat. Rev. Endocrinol. 10 2014 143 156
29. G. Hollunger Guanidines and oxidative phosphorylations Acta Pharmacol. Toxicol. 11 S1 1955 1 84
30. B. Chance, and G. Hollunger Inhibition of electron and energy transfer in mitochondria, II. The site and the mechanism of guanidine action J. Biol. Chem. 238 1963 432 438
31. G. Schäfer Guanidines and biguanides Pharmacol. Ther. 8 1980 275 295
32. J.B. Chappell The effect of alkylguanidines on mitochondrial respiration J. Biol. Chem. 238 1963 410 417
33. G. Schäfer Site-specific uncoupling and inhibition of energy transfer by biguanides Biochim. Biophys. Acta 93 1964 279 283
34. G. Schäfer Site-specific uncoupling and inhibition of oxidative phosphorylation by biguanides. II Biochim. Biophys. Acta 172 1969 334 337
35. F. Davidoff Effects of guanidine derivatives on mitochondrial function. III. The mechanism of phenethylbiguanide accumulation and its relationship to in vitro respiratory inhibition J. Biol. Chem. 238 1971 410 417
36. M.R. Owen, E. Doran, and A.P. Halestrap Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain Biochem. J. 348 2000 607 614
37. M.Y. El-Mir, V. Nogueira, E. Fontaine, N. Avéret, M. Rigoulet, and X. Leverve Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I J. Biol. Chem. 275 2000 223 228
38. H.R. Bridges, A.J.Y. Jones, M.N. Pollak, and J. Hirst Effects of metformin and other biguanides on oxidative phosphorylation in mitochondria Biochem. J. 462 2014 475 487
39. A.B. Kotlyar, and A.D. Vinogradov Slow active/inactive transition of the mitochondrial NADH-ubiquinone reductase Biochim. Biophys. Acta 1019 1990 151 158
40. M. Babot, A. Birch, P. Labarbuta, and A. Galkin Characterisation of the active/de-active transition of mitochondrial complex I Biochim. Biophys. Acta 1837 2014 1083 1092
41. S. Matsuzaki, and K.M. Humphries Selective inhibition of deactivated mitochondrial complex I by biguanides Biochemistry 54 2015 2011 2021
42. E.T. Chouchani, C. Methner, S.M. Nadtochiy, A. Logan, V.R. Pell, S. Ding, A.M. James, H.M. Cochemé, J. Reinhold, K.S. Lilley, L. Partridge, I.M. Fearnley, A.J. Robinson, R.C. Hartley, R.A.J. Smith, T. Krieg, P.S. Brookes, and M.P. Murphy Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I Nat. Med. 19 2013 753 759
43. C. Bardin, E. Nobecourt, E. Larger, F. Chast, J.M. Treluyer, and S. Urien Population pharmacokinetics of metformin in obese and non-obese patients with type 2 diabetes mellitus Eur. J. Clin. Pharmacol. 68 2012 961 968
44. A.T. Nies, H. Koepsell, K. Damme, and M. Schwab Organic cation transporters (OCTs, MATEs), in vitro and in vivo evidence for the importance in drug therapy Handb. Exp. Pharmacol. 201 2011 105 167
45. Y. Shitara, N. Nakamichi, M. Norioka, H. Shima, Y. Kato, and T. Horie Role of organic cation/carnitine transporter 1 in uptake of phenformin and inhibitory effect on complex I respiration in mitochondria Toxicol. Sci. 132 2013 32 42
46. R.A. Miller, and M.J. Birnbaum An energetic tale of AMPK-independent effects of metformin J. Clin. Invest. 120 2010 2267 2270
47. R.A. Miller, Q. Chu, J. Xie, M. Foretz, B. Viollet, and M.J. Birnbaum Biguanides suppress hepatic glucagon signalling by decreasing production of cyclic AMP Nature 494 2013 256 260
48. R.J. Shaw, K.A. Lamia, D. Vasquez, S.H. Koo, N. Bardeesy, R.A. Depinho, M. Montminy, and L.C. Cantley The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin Science 310 2005 1642 1646
49. J.E. Gunton, P.J. Delhanty, S. Takahashi, and R.C. Baxter Metformin rapidly increases insulin receptor activation in human liver and signals preferentially through insulin-receptor substrate-2 J. Clin. Endocrinol. Metab. 88 2003 1323 1332
50. C.A. Collier, C.R. Bruce, A.C. Smith, G. Lopaschuk, and D.J. Dyck Metformin counters the insulin-induced suppression of fatty acid oxidation and stimulation of triacylglycerol storage in rodent skeletal muscle Am. J. Physiol. Endocrinol. Metab. 291 2006 E182 E189
51. J.M. Evans, L.A. Donnelly, A.M. Emslie-Smith, D.R. Alessi, and A.D. Morris Metformin and reduced risk of cancer in diabetic patients Br. Med. J. 330 2005 1304 1305
52. S.E. Weinberg, and N.S. Chandel Targeting mitochondria metabolism for cancer therapy Nat. Chem. Biol. 11 2015 9 15
53. R.J. Dowling, M. Zakikhani, I.G. Fantus, M. Pollak, and N. Sonenberg Metformin inhibits mammalian target of rapamycin-dependent translation initiation in breast cancer cells Cancer Res. 67 2007 10804 10812
54. A. Kalender, A. Selvaraj, S.Y. Kim, P. Gulati, S. Brûlé, B. Viollet, B.E. Kemp, N. Bardeesy, P. Dennis, J.J. Schlager, A.A. Marette, S.C. Kozma, and G. Thomas Metformin, independent of AMPK, inhibits mTORC1 in a rag GTPase-dependent manner Cell Metab. 11 2010 390 401
55. B. Kelly, G.M. Tannahill, M.P. Murphy, and L.A.J. O'Neill Metformin inhibits the production of reactive oxygen species from NADH:ubiquinone oxidoreductase to limit induction of IL-1β, and boosts IL-10 in LPS-activated macrophages J. Biol. Chem. 290 2015 20455 20465
56. J.M. Clark, and I. Yamaguchi Scope and Status of Pesticide Resistance J.M. Clark, I. Yamaguchi, Agrochemical Resistance: Extent, Mechanism, and Detection 2002 American Chemical Society Washington, DC 1 22
57. D. Barnes-Seeman, M. Jain, L. Bell, S. Ferreira, S. Cohen, X.-H. Chen, J. Amin, B. Snodgrass, and P. Hatsis Metabolically stable tert-butyl replacement ACS Med. Chem. Lett. 4 2013 514 516
58. T.C. Sparks, and C.V. DeAmicis Inhibitors of mitochondrial electron transport: acaricides and insecticides W. Krämer, U. Schirmer, Modern Crop Protection Compounds 2007 Wiley-VCH 885 908
59. K. Motoba, H. Nishizawa, T. Suzuki, H. Hamaguchi, and M. Uchida Rapid hydrolysis pathway for a tertiary alcohol ester through intramolecular transesterification in rats Biosci. Biotechnol. Biochem. 56 1992 366 367
60. T.C. Sparks, and C.V. DeAmicis Inhibitors of mitochondrial electron transport: acaricides and insecticides W. Krämer, U. Schirmer, P. Jeschke, M. Witschel, Modern Crop Protection Compounds 2nd edition 2012 Wiley-VCH 1078 1108
61. E. Nakamaru-Ogiso, K. Sakamoto, A. Matsuno-Yagi, H. Miyoshi, and T. Yagi The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovine mitochondrial complex I Biochemistry 42 2003 746 754
62. L.A. Sazanov, and J.E. Walker Cryo-electron crystallography of two sub-complexes of bovine complex I reveals the relationship between the membrane and peripheral arms J. Mol. Biol. 302 2000 455 464
63. F. Schuler, T. Yano, S.D. Bernardo, T. Yagi, V. Yankovskaya, T.P. Singer, and J.E. Casida NADH-quinone oxidoreductase: PSST subunit couples electron transfer from iron-sulfur cluster N2 to quinone Proc. Natl. Acad. Sci. U. S. A. 96 1999 4149 4153
64. T. Akagi, Y. Takahashi, and S. Sasaki Exhaustive conformational searches for superimposition of acaricidal compounds Quant. Struct.-Act. Relat. 15 1996 290 295
65. C. Sakai, E. Tomitsuka, H. Esumi, S. Harada, and K. Kita Mitochondrial fumarate reductase as a target of chemotherapy: from parasites to cancer cells Biochim. Biophys. Acta 1820 2012 643 651
66. K. Kita, K. Shiomi, and S. Omura Advances in drug discovery and biochemical studies Trends Parasitol. 23 2007 223 229
67. S. Omura, H. Miyadera, H. Ui, K. Shiomi, Y. Yamaguchi, R. Masuma, T. Nagamitsu, D. Takano, T. Sunazuka, A. Harder, H. Kölbl, M. Namikoshi, H. Miyoshi, K. Sakamoto, and K. Kita Anthelmintic compound, nafuredin, shows selective inhibition of complex I in helminth mitochondria Proc. Natl. Acad. Sci. U. S. A. 98 2001 60 62
68. K. Shiomi, H. Ui, H. Suzuki, H. Hatano, T. Nagamitsu, D. Takano, H. Miyadera, T. Yamashita, K. Kita, H. Miyoshi, A. Harder, H. Tomoda, and S. Omura A γ-lactone form nafuredin, nafuredin-γ, also inhibits helminth complex I J. Antibiot. 58 2005 50 55
69. M. Ohtawa, M. Matsunaga, K. Fukunaga, R. Shimizu, E. Shimizu, S. Arima, J. Ohmori, K. Kita, K. Shiomi, S. Omura, and T. Nagamitsu Design, synthesis, and biological evaluation of air-stable nafuredin-g analogs as complex I inhibitors Bioorg. Med. Chem. 23 2015 932 943
70. M. Mori, H. Morimoto, Y. Kim, H. Ui, K. Nonaka, R. Masuma, K. Sakamoto, K. Kita, H. Tomoda, K. Shiomi, and S. Omura Ukulactones A and B, new NADH-fumarate reductase inhibitors produced by Penicillium sp. FKI-3389 Tetrahedron 67 2011 6582 6586
71. T. Ino, T. Nishioka, and H. Miyoshi Characterization of inhibitor binding sites of mitochondrial complex I using fluorescent inhibitor Biochim. Biophys. Acta 1605 2003 15 20
72. T. Yamashita, T. Ino, H. Miyoshi, K. Sakamoto, A. Osanai, E. Nakamaru-Ogiso, and K. Kita Rhodoquinone reaction site of mitochondrial complex I in parasitic helminth, Ascaris suum Biochim. Biophys. Acta 1608 2004 97 103
73. J. Matsumoto, K. Sakamoto, N. Shinjyo, Y. Kido, N. Yamamoto, K. Yagi, H. Miyoshi, N. Nonaka, K. Katakura, K. Kita, and Y. Oku Anaerobic NADH-fumarate reductase system is predominant in the respiratory chain of Echinococcus multilocularis, providing a novel target for the chemotherapy of alveolar Echinococcosis Antimicrob. Agents Chemother. 52 2008 164 170
74. M.P. Murphy Mitochondrial thiols in antioxidant protection and redox signaling: distinct roles for glutathionylation and other thiol modifications Antioxid. Redox Signal. 16 2012 476 495
75. S. Dröse, U. Brandt, and I. Wittig Mitochondrial respiratory chain complexes as sources and targets of thiol-based redox-regulation Biochim. Biophys. Acta 1844 2014 1344 1354
76. +-translocating NADH-quinone oxidoreductase probed by zero-length cross-linking Biochemistry 43 2004 3750 3755
77. M. Berrisford, C.J. Thompson, and L.A. Sazanov Chemical and NADH-induced, ROS-dependent, cross-linking between subunits of complex I from Escherichia coli and Thermus thermophilus Biochemistry 47 2008 10262 10270
78. T. Pohl, T. Spatzal, M. Aksoyoglu, A.M. Rostas, H. Lay, U. Glessner, C. Boudon, P. Hellwig, S. Weber, and T. Friedrich Spin labeling of the Escherichia coli NADH ubiquinone oxidoreductase (complex I) Biochim. Biophys. Acta 1797 2010 1894 1900
79. A. Galkin, B. Meyer, I. Wittig, M. Karas, H. Schägger, A. Vinogradov, and U. Brandt Identification of the mitochondrial ND3 subunit as a structural component involved in the active/deactive enzyme transition of respiratory complex I J. Biol. Chem. 283 2008 20907 20913
80. S. Steimle, C. Schnick, E-M. Burger, F. Nuber, D. Krämer, H. Dawitz, S. Brander, B. Matlosz, J. Schäfer, K. Maurer, U. Glessner, T. Friedrich, Cysteine scanning reveals minor local rearrangements of the horizontal helix of respiratory complex I, Mol. Microbiol. (doi: http://dx.doi.org/10.1111/mmi.13112)
81. S. Zhu, and S.B. Vik Constraining the lateral helix of respiratory complex I by cross-linking does not impair enzyme activity or proton translocation J. Biol. Chem. 290 2015 20761 20773
82. R.G. Efremov, R. Baradaran, and L.A. Sazanov The architecture of respiratory complex I Nature 465 2010 441 445
83. S. Tsukiji, M. Miyagawa, Y. Takaoka, T. Tamura, and I. Hamachi Ligand-directed tosyl chemistry for protein labeling in vivo Nat. Chem. Biol. 5 2009 341 343
84. Y. Takaoka, A. Ojida, and I. Hamachi Protein organic chemistry and applications for labeling and engineering in live-cell systems Angew. Chem. Int. Ed. 52 2013 4088 4106
85. Q. Wang, T.R. Chan, R. Hilgraf, V.V. Fokin, K.B. Sharpless, and M.G. Finn Bioconjugation by copper(I)-catalyzed azide-alkyne [3 + 2] cycloaddition J. Am. Chem. Soc. 125 2003 3192 3193
86. S. Nakanishi, M. Abe, S. Yamamoto, M. Murai, and H. Miyoshi Bis-THF motif of acetogenin binds to the third matrix-side loop of ND1 subunit in mitochondrial NADH-ubiquinone oxidoreductase Biochim. Biophys. Acta 1807 2011 1170 1176
87. E. Weerapana, G.M. Simon, and B. Cravatt Disparate proteome reactivity profiles of carbon electrophiles Nat. Chem. Biol. 4 2014 405 407