Dynamic function of the spacer region of acetogenins in the inhibition of bovine mitochondrial NADH-ubiquinone oxidoreductase (complex I)

Biochemistry

Volumn 47, Issue 23, 2008, Pages 6260-6266

  Abe, Masato ^a   Kubo, Akina ^a   Yamamoto, Shuhei ^a   Hatoh, Yoshinori ^a   Murai, Masatoshi ^a   Hattori, Yasunao ^b   Makabe, Hidefumi ^b   Nishioka, Takaaki ^a   Miyoshi, Hideto ^a  

^a KYOTO UNIVERSITY   (Japan)

^b SHINSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM; BINDING ENERGY; BINDING SITES; BIOCHEMISTRY; CARBON; DYNAMICS; ENZYMES; FOOD ADDITIVES; MECHANICS;

ACETOGENINS; ACTION MECHANISMS; BOVINE HEART; CARBON ATOMS; DYNAMIC FUNCTIONS; INHIBITOR BINDING; LACTONE RINGS; MITOCHONDRIAL COMPLEX; MITOCHONDRIAL NADH; OXIDOREDUCTASE; UBIQUINONE (UQ);

ENZYME INHIBITION;

ACETOGENIN; CARBENE; GAMMA LACTONE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ARTICLE; BINDING AFFINITY; COW; ENZYME ACTIVITY; HYDROPHOBICITY; MOLECULAR DYNAMICS; PHOTOREACTIVITY; PRIORITY JOURNAL; PROTEIN FUNCTION; THERMODYNAMICS; ULTRAVIOLET IRRADIATION;

ACETOGENINS; ANIMALS; CATTLE; ELECTRON TRANSPORT COMPLEX I; ENZYME INHIBITORS; ISOMERISM; KINETICS; MITOCHONDRIA, HEART; MODELS, MOLECULAR; MULTIENZYME COMPLEXES; NADH, NADPH OXIDOREDUCTASES; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; SUBMITOCHONDRIAL PARTICLES;

BOVINAE; TOXOPHORA;

EID: 44949164731     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800506s     Document Type: Article

References (31)

1. Zeng, L., Ye, Q., Oberlies, N. H., Shi, G., Gu, Z. M., He, K., and McLaughlin, J. L. (1996) Recent advances in annonaceous acetogenins. Nat. Prod. Rep. 13, 275-306.
2. Alali, F. Q., Liu, X. X., and McLaughlin, J. L. (1999) Annonaceous acetogenins: Recent progress. J. Nat. Prod. 62, 504-540.
3. Bermejo, A., Figadere, B., Zafra-Polo, M.-C., Barrachina, I., Estornell, E., and Cortes, D. (2005) Acetogenins from Annonaceae: Recent progress in isolation, synthesis and mechanisms of action. Nat. Prod. Rep. 22, 269-303.
4. Lannuzel, A., Michel, P. P., Höglinger, G. U., Champy, P., Jousset, A., Medja, F., Lombes, A., Darios, F., Gleye, C., Laurens, A., Hocquemiller, R., Hirsch, E. C., and Ruberg, M. (2003) The mitochondrial complex I inhibitor annonacin is toxic to mesencephalic dopaminergic neurons by impairment of energy metabolism. Neuroscience 121, 287-296.
5. Escobar-Khondiker, M., Höllerhage, M., Muriel, M. P., Champy, P., Bach, A., Depienne, C., Respondek, G., Yamada, E., Lannuzel, A., Yagi, T., Hirsch, E. C., Oertel, W. H., Jacob, R., Michel, P. P., Ruberg, M., and Höglinger, G. U. (2007) Annonacin, a natural mitochondrial complex I inhibitor, causes tau pathology in cultured neurons. J. Neurosci. 27, 7827-7837.
6. Degli Esposti, M., Ghelli, A., Ratta, M., Cortes, D., and Estornell, E. (1994) Natural substances (acetogenins) from the family Annonaceae are powerful inhibitors of mitochondrial NADH dehydrogenase (complex I). Biochem. J. 301, 161-167.
7. Friedrich, T., Van Heek, P., Leif, H., Ohnishi, T., Forche, E., Kunze, B., Jansen, R., Trowitzsch-Kienast, W., Höfle, G., Reichenbach, H., and Weiss, H. (1994) Two binding sites of inhibitors in NADH: ubiquinone oxidoreductase (complex I). Eur. J. Biochem. 219, 691-698.
8. Okun, J. G., Lümmen, P., and Brandt, U. (1999) Three classes of inhibitor share a common binding domain in mitochondrial complex I (NADH-ubiquinone oxidoreductase). J. Biol. Chem. 274, 2625-2630.
9. Miyoshi, H. (2001) Probing the ubiquinone reduction site in bovine mitochondrial complex I using a series of synthetic ubiquinones and inhibitors. J. Bioenerg. Biomembr. 33, 223-231.
10. Murai, M., Ishihara, A., Nishioka, T., Yagi, T., and Miyoshi, H. (2007) The ND1 subunit constructs the inhibitor binding domain in bovine heart mitochondrial complex I. Biochemistry 46, 6409-6416.
11. Yagi, T., and Matsuno-Yagi, A. (2003) The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: The secret unlocked. Biochemistry 42, 2266-2274.
12. Takada, M., Kuwabara, K., Nakato, H., Tanaka, A., Iwamura, H., and Miyoshi, H. (2000) Definition of crucial structural factors of acetogenins, potent inhibitors of mitochondrial complex I. Biochim. Biophys. Acta 1460, 302-310.
13. Hoppen, S., Emde, U., Friedrich, T., Grubert, L., and Koert, U. (2000) Natural-product hybrid: Design, synthesis, and biological evaluation of quinone-annonaceous acetogenins. Angew. Chem., Int. Ed. 39, 2099-2102.
14. Torm, J. R., Estornell, E., Gallardo, T., Gonzalez, M. C., Cave, A., Cranell, S., Cortes, D., and Zafra-Polo, M. C. (2001) γ-Lactone- functionalized antitumal acetogenins are the most potent inhibitors of mitochondrial complex I. Bioorg. Med. Chem. Lett. 11, 681-684.
15. Torm, J. R., Gallardo, T., Peris, E., Bermejo, A., Cabedo, N., Estornell, E., Zafra-Polo, M. C., and Cortes, D. (2003) Inhibitory effects on mitochondrial complex I of semisynthetic monotetrahydrofuran acetogenin derivatives. Bioorg. Med. Chem. Lett. 13, 4101-4105.
16. Yabunaka, H., Abe, M., Kenmochi, A., Hamada, T., Nishioka, T., and Miyoshi, H. (2003) Synthesis and Inhibitory Activity of Ubiquinone-Acetogenin Hybrid Inhibitor with Bovine Mitochondrial Complex I. Bioorg. Med. Chem. Lett. 13, 2385-2388.
17. Miyoshi, H., Ohshima, M., Shimada, H., Akagi, T., Iwamura, H., and McLaughlin, J. L. (1998) Essential structural factors of Annonaceous acetogenins as potent inhibitors of mitochondrial complex I. Biochim. Biophys. Acta 1365, 443-452.
18. Makabe, H., Miyawaki, A., Takahashi, R., Hattori, Y., Konno, H., Abe, M., and Miyoshi, H. (2004) Synthesis of two possible diastereomers of reticulatain-1. Tetrahedron Lett. 45, 973-977.
19. Makabe, H., Hattori, Y., Kimura, Y., Konno, H., Abe, M., Miyoshi, H., Tanaka, A., and Oritani, T. (2004) Total synthesis of cis-solamin and its inhibitory action with bovine heart mitochondrial complex I. Tetrahedron 60, 10651-10657.
20. Abe, M., Kenmochi, A., Ichimaru, N., Hamada, T., Nishioka, T., and Miyoshi, H. (2004) Essential structural features of acetogenins: Role of hydroxy groups adjacent to the bis-THF rings. Bioorg. Med. Chem. Lett. 14, 779-782.
21. Motoyama, T., Yabunaka, H., and Miyoshi, H. (2002) Essential structural factors of acetogenins, potent inhibitors of mitochondrial complex I. Bioorg. Med. Chem. Lett. 12, 2089-2092.
22. Tormo, J. R., Gallardo, T., Aragon, R., Cortes, D., and Estornell, E. (1999) Specific interactions of mono-tetrahydrofuranic annonaceous acetogenins as inhibitors of mitochondrial complex I. Chem.-Biol. Interact. 122, 171-183.
23. Kuwabara, K., Takada, M., Iwata, J., Tatsumoto, K., Sakamoto, K., Iwamura, H., and Miyoshi, H. (2000) Design syntheses and mitochondrial complex I inhibitory activity of novel acetogenin mimics. Eur. J. Biochem. 267, 2538-2546.
24. Hamada, T., Ichimaru, N., Abe, M., Fujita, D., Kenmochi, A., Nishioka, T., Zwicker, K., Brandt, U., and Miyoshi, H. (2004) Synthesis and inhibitory action of novel acetogenin mimics with bovine heart mitochondrial complex I. Biochemistry 43, 3651-3658.
25. Abe, M., Murai, M., Ichimaru, N., Kenmochi, A., Yoshida, T., Kubo, A., Kimura, Y., Moroda, A., Makabe, H., Nishioka, T., and Miyoshi, H. (2005) Dynamic function of the alkyl spacer of acetogenins in their inhibitory action with mitochondrial complex I (NADH-ubiquinone oxidoreductase). Biochemistry 44, 14898-14906.
26. Matsuno-Yagi, A., and Hatefi, Y. (1985) Studies on the mechanism of oxidative phosphorylation. J. Biol. Chem. 260, 14424-14427.
27. Ichimaru, N., Murai, M., Abe, M., Hamada, T., Yamada, Y., Makino, S., Nishioka, T., Makabe, H., Makino, A., Kobayashi, T., and Miyoshi, H. (2005) Synthesis and inhibition mechanism of Δlac-acetogenins: A novel type of inhibitor of bovine heart mitochondrial complex I. Biochemistry 44, 816-825.
28. Fujita, D., Murai, M., Nishioka, T., and Miyoshi, H. (2006) Light control of mitochondrial complex I activity by a photoresponsive inhibitor. Biochemistry 45, 6581-6586.
29. Yang, L., Takisawa, N., Hayashita, T., and Shirahama, K. (1995) Colloid chemical characterization of the photosurfactant 4-ethylazobenzene 4′-(oxyethyl)trimethylammonium bromide. J. Phys. Chem. 99, 8799-8803.
30. Henzl, J., Mehlhorn, M., Grawronski, H., Rieder, K. H., and Morgenstern, K. (2006) Reversible cis-trans isomerization of a single azobenzene molecule. Angew. Chem., Int. Ed. 45, 603-606.
31. Fujita, D., Ichimaru, N., Abe, M., Murai, M., Hamada, T., Nishioka, T., and Miyoshi, H. (2005) Synthesis of non-THF analogs of acetogenin toward simplified mimics. Tetrahedron Lett. 46, 5775-5779.