Heterocyclic analogues of squamocin as inhibitors of mitochondrial complex I. On the role of the terminal lactone of annonaceous acetogenins

Biochemistry

Volumn 45, Issue 8, 2006, Pages 2721-2728

  Duval, Romain A ^a   Lewin, Guy ^a   Peris, Eva ^b   Chahboune, Nadia ^b   Garofano, Aurelio ^c   Dröse, Stefan ^c   Cortes, Diego ^b   Brandt, Ulrich ^c   Hocquemiller, Reynald ^a  

^a UNIVERSITÉ PARIS SUD   (France)

^b UNIVERSITY OF VALENCIA   (Spain)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CATALYSIS; CRYSTAL STRUCTURE; ESTERS; KETONES;

HETEROAROMATIC; MITOCHONDRIAL COMPLEX I; SQUAMOCIN; UBIQUINONE-BINDING SITE;

ENZYME INHIBITION;

1 GERANYL 2 METHYLBENZIMIDAZOLE; 37 METHOXYQUINOXALINONE; 39 PYRIDOPYRAZINONE; ACETOGENIN; ANTHRAQUINOBENZOPIPERAZINONE; BENZIMIDAZOLE; BENZOXAZINONE DERIVATIVE; BULLATACIN; BUTENOLIDE; IMIDAZOLE; LACTONE; MYXOTHIAZOL; QUINOLONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; SQUAMOCIN; TRIAZINE; UBIQUINONE; UNCLASSIFIED DRUG;

ALLOSTERISM; ANNONA; ARTICLE; BIOLOGICAL ACTIVITY; CYTOTOXICITY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME INHIBITION; INSECTICIDAL ACTIVITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARASITISM; POLYMERIZATION; PRIORITY JOURNAL;

ANNONA; ELECTRON TRANSPORT COMPLEX I; ENZYME INHIBITORS; ESTERS; FATTY ALCOHOLS; FURANS; LACTONES; MITOCHONDRIA, HEART; NADH, NADPH OXIDOREDUCTASES; OXIDATION-REDUCTION; RUTHENIUM; SEEDS; SUBSTRATE SPECIFICITY;

ANNONA;

EID: 33644507467     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051261u     Document Type: Article

References (60)

1. Alali, F. Q., Liu, X.-X., McLaughlin, J. L. (1999) Annonaceous acetogenins: Recent progress, J. Nat. Prod. 62, 504-540.
2. Londershausen, M., Leicht, W., Lieb, F., Moeschler, H., Weiss, H. (1991) Molecular mode of action of annonins, Pestic. Sci 33, 427-438.
3. Ahammadsahib, K. I., Hollingworth, R. M., McGovren, J. P., Hui, Y.-H., McLaughlin, J. L. (1993) Mode of action of bullatacin: A potent antitumor and pesticidal annonaceous acetogenin, Life Sci. 53, 1113-1120.
4. Chih, H.-W., Chiu, H.-F., Tang, K.-S., Chang, F.-R., Wu, Y.-C. (2001) Bullatacin, a potent antitumor annonaceous acetogenin, inhibits proliferation of human hepatocarcinoma cell line 2.2.15 by apoptosis induction, Life Sci. 69, 1321-1331.
5. Takada, M., Kuwabara, K., Nakato, H., Tanaka, A., Iwamura, H., Miyoshi, H. (2000) Definition of crucial structural factors of acetogenins, potent inhibitors of mitochondrial Complex I, Biochim. Biophys. Acta 1460, 302-310.
6. Tormo, J. R., Estornell, E., Gallardo, T., González, M. C., Cavé, A., Granell, S., Cortes, D., Zafra-Polo M. C. (2001) γ-lactone-functionalized antitumoral acetogenins are the most potent inhibitors of mitochondrial Complex I, Bioorg. Med. Chem. Lett. 11, 681-684.
7. Arndt, S., Emde, U., Bäurle, S., Friedrich, T., Grubert, L., Koert, U. (2001) Quinone-annonaceous acetogenins: Synthesis and Complex I inhibition studies of a new class of natural product hybrids, Chem. Eur. J. 7, 993-1005.
8. Hoppen, S., Emde, U., Friedrich, T., Grubert, L., Koert, U. (2000) Natural product hybrids: Design, synthesis and biological evaluation of quinone-annonaceous acetogenins, Angew. Chem., Int. Ed. 39, 2099-2102.
9. Hamada, T., Ichimaru, N., Abe, M., Fujita, D., Kenmochi, A., Nishioka, T., Zwicker, K., Brandt, U., Miyoshi, H. (2004) Synthesis and inhibitory action of novel acetogenin mimics with bovine heart mitochondrial complex I, Biochemistry 43, 3651-3658.
10. Degli Esposti, M., Ghelli, A., Ratta, M., Cortes, D., Estornell, E. (1994) Natural substances (acetogenins) from the family Annonaceae are powerful inhibitors of mitochondrial NADH dehydrogenase (Complex I), Biochem. J. 301, 161-167.
11. Estornell, E., Tormo, J. R., Cortes, D. (1997) Cherimolin-1, new selective inhibitor of the first energy-coupling site of the NADH: ubiquinone oxidoreductase (complex I), Biochem. Biophys. Res. Commun. 240, 234-238.
12. Tormo, J. R., González, M. C., Cortes, D., Estornell, E. (1999) Kinetic characterization of mitochondrial complex I inhibitors using annonaceous acetogenins, Arch. Biochem. Biophys. 369, 119-126.
13. Duval, R., Lewin, G., Hocquemiller, R. (2003) Semisynthesis of heterocyclic analogues of squamocin, a cytotoxic annonaceous acetogenin, by an unusual oxidative decarboxylation reaction, Bioorg. Med. Chem. 16, 3439-3446.
14. Tam, V. T., Hieu, B. C, Chappe, B. (1993) Squamocin and rolliniastatin-1 from the seeds of Annona reticulata, Planta Med. 59, 576.
15. Kuwano, E., Sato, N., Eto, M. (1982) Insecticidal benzimidazoles with a terpenoid moiety, Agric. Biol. Chem. 46, 6, 1715-1716.
16. Gallardo, T., Zafra-Polo, M. C., Tormo, J. R., González, M. C., Franck, X., Estornell, E., Cortes, D. (2000) Semisynthesis of antitumoral acetogenins: SAR of functionalized alkyl-chain bis-tetrahydrofuranic acetogenins, specific inhibitors of mitochondrial Complex I, J. Med. Chem. 43, 4793-4800.
17. Oettmeier, W., Masson, K., Soll, M., Reil, E. (1994) Acridones and quinolones as inhibitors of ubiquinone functions in the mitochondrial respiratory chain, Biochem. Soc. Trans. 7 22, 213-216.
18. Lümmen, P. (1998) Complex I inhibitors as insecticides and acaricides, Biochim. Biophys. Acta 1364, 287-296.
19. Nakagawa, Y., Kuwano, E., Eto, M., Fujita, T. (1985) Effects of insect-growth-regulatory benzimidazole derivates on cultured integument of the rice stem borer and mitochondria from rat liver, Agric. Biol. Chem. 49, 3569-3578.
20. Hollingworth, R. M., Ahammadsahib, K. I., Gadelhac, G., McLaughlin, J. L. (1994) New inhibitors of Complex I of the mitochondrial electron transport chain with activity as pesticides, Biochem. Soc. Trans. 7 22, 230-233.
21. Degli Esposti, M. (1998) Inhibitors of NADH-ubiquinone reductase: An overview, Biochim. Biophys. Acta 1364, 222-235.
22. Yoshida, S., Nagao, A., Watanabe, N., Takahashi, N. (1980) Structure-activity relationship in piericidins inhibitors on the electron transport system in mitochondria, Agric. Biol. Chem. 44, 2921-2924.
23. Chung, K. H., Cho, K. Y., Asami, Y., Takahashi, N., Yoshida, S. (1989) New 4-hydroxypyridine and 4-hydroxyquinoline derivatives as inhibitors of NADH-ubiquinone reductase in the respiratory chain, Z. Naturforsch. 44C, 609-616.
24. Okada, I., Okui, S., Takahashi, Y., Fukuchi, T. (1991) Synthesis and acaricidal activity of pyrazole-5-carboxamide derivatives, Nihon Noyaku Gakkaishi (J. Pestic. Sci.) 16, 623-629.
25. Motoba, K., Susuki, T., Uchida, M. (1992) Effect of a new acaricide, fenpyroxymate, on energy metabolism and mitochondrial morphology in adult female Tetranychus urticae (two-spotted spider mite), Pestic. Biochem. Physiol. 43, 37-44.
26. Hollingworth, R. M., Ahammadsahib, K. I. (1995) Inhibitors of respiratory complex I: Mechanisms, pesticidal actions and toxicology, Rev. Pestic. Toxicol. 3, 277-302.
27. Labib, G.H., Rahman, M. A., El-Kilany, Y., El-Massry, A. I., El-Ahry, E. S. H. (1988) Synthesis of γ-butyrolactones, quinoxalines, and azauracils from 4-aryl-2-oxobutanoic acid derivatives, Bull. Chem. Soc. Jpn. 61, 12, 4427-4430.
28. Friedrich, T., Van Heek, P., Leif, H., Ohnishi, T., Forche, E., Kunze, B., Jansen, R., Trowitzsch-Kienast, W., Höfle, G., Reichenbach, H., Weiss, H. (1994) Two binding sites of inhibitors in NADH:ubiquinone oxidoreductase (complex I). Relationship of one site with the ubiquinone binding site of bacterial glucose: ubiquinone oxidoreductase, Eur. J. Biochem. 219, 691-698.
29. Friedrich, T., Ohnishi, T., Forche, E., Kunze, B., Jansen, R., Trowitzsch-Kienast, W., Höfle, G., Reichenbach, H., Weiss, H. (1994) Two binding sites for naturally occurring inhibitors in mitochondrial and bacterial NADH:ubiquinone oxidoreductase (complex I), Biochem. Soc. Trans. 22, 7, 226-230.
30. Inter allia: Kawabata, K., Takehana, K., Ikeyama, M., Harada, T. (Nihon Nohyaku Co., Ltd., Japan) (1975) 2-substituted 4,5-dicyanoimidazoles as acaricides, herbicides, and insecticides, Jpn. Kokai Tokkyo Koho (patent number JP 50125031).
31. Okun, J. G., Lümmen, P., Brandt, U. (1999) Three classes of inhibitors share a common binding domain in mitochondrial Complex I (NADH:ubiquinone oxidoreductase), J. Biol. Chem. 274, 5, 2625-2630.
32. Tormo, J. R., Gallardo, T., González, M. C., Bermejo, A., Cabedo, N., Andreu, I., Estornell, E. (1999) Annonaceous acetogenins as inhibitors of mitochondrial Complex I, Curr. Top. Phytochem. 2, 69-90.
33. 3H-labeled rotenone analogue, Biochem. Soc. Trans. 7 22, 247-251.
34. Degli Esposti, M., Ghelli, A., Crimi, M. (1993) Complex I and Complex III of mitochondria have common inhibitors acting as ubiquinone antagonists, Biochem. Biophys. Res. Comm. 190, 3, 1090-1096.
35. Degli Esposti, M., Crimi, M., Ghelli, A. (1994) Natural variation in the potency and binding sites of mitochondrial quinone-like inhibitors, Biochem. Soc. Trans. 7, 209-213.
36. Degli Esposti, M., Ghelli, A. (1994) The mechanism of proton and electron transport in mitochondrial complex I, Biochim. Biophys. Acta 1187, 116-120.
37. Degli Esposti, M., Ngo, A., McMullen, G., Ghelli, A., Sparla, F., Benelli, B., Ratta, M., Linnane, A. W. (1996) The specificity of mitochondrial Complex I for ubiquinones, Biochem. J. 313, 327-334.
38. Miyoshi, H. (1998) Structure-activity relationships of some Complex I inhibitors, Biochim. Biophys. Acta 1364, 236-244.
39. Lindell, S. D., Ort, O., Lümmen, P., Klein, R. (2004) The design and synthesis of novel inhibitors of NADH:ubiquinone oxidoreductase, Bioorg. Med. Chem. Lett. 14, 511-514.
40. Yabunaka, H., Abe, M., Kenmochi, A., Hamada, T., Nishioka, T., Miyoshi, H. (2003) Synthesis and inhibitory activity of ubiquinone-acetogenin hybrid inhibitor with bovine mitochondrial complex I, Bioorg. Med. Chem. Lett. 13, 2385-2388.
41. Fato, R., Estornell, E., Di Bernardo, S., Palotti, F., Parenti, Castelli, G., Lenaz, G. (1996) Steady-state kinetics of the reduction of coenzyme Q analogues by complex I (NADH:ubiquinone oxidoreductase) in bovine heart mitochondria and submitochondrial particles, Biochemistry 35, 2705-2716.
42. Gutman, M., Coles, C. J., Singer, T. P., Casida, J. E. (1971) On the functional organization of the respiratory chain at the dehydrogenase-coenzyme Q junction, Biochemistry 10 11, 2036-2043.
43. Vinogradov, A. D., Sled, V. D., Burbaev, D. S., Grivennikova, V. G., Moroz, I. A., Ohnishi, T. (1995) Energy-dependent complex I-associated ubisemiquinones in submitochondrial particles, FEBS Lett. 370, 83-87.
44. Ohnishi, T. (1998) Iron-sulfur clusters/semiquinones in complex I, Biochim. Biophys. Acta 1364, 186-206.
45. Lancaster, C. R. D., Michel, H. (1997) The coupling of light-induced electron transfer and proton uptake as derived from crystal structures of reaction centres from Rhodopseudomonas viridis modified at the binding site of the secondary quinone QB, Structure 5, 1339-1359.
46. Crofts, A. R., Barquera, B., Gennis, R. B., Kuras, R., Guergova-Kuras, M., Berry, E. A. (1999) Mechanism of ubiquinol oxidation by the bc(1) Complex: Different domains for the quinol binding pocket and their role in the mechanism and binding of the inhibitors, Biochemistry 38, 48, 15807-15826.
47. Gutman, M., Singer, T. P., Beinert, H., Casida, J. E. (1970) Reaction sites of rotenone, piericidin A and amytal in relation to the non-heme iron complex of NADH dehydrogenase, Proc. Natl. Acad. Sci. U.S.A. 65, 3, 763-770.
48. +) and of the respiratory chain inhibitor piericidin A are the same, Biochem. J. 15, 273, 481-484.
49. Degli Esposti, M., Ghelli, A. (1999) Ubiquinone and inhibitor sites in complex I: One, two or three? Biochem. Soc. Trans. 27, 4, 606-609.
50. Duval, R. A., Poupon, E., Brandt, U., Hocquemiller, R. (2005) Remarkable substituent effect: Beta-aminosquamocin, a potent dual inhibitor of mitochondrial complexes I and III, Biochim. Blophys. Acta 1709, 191-194.
51. Tormo, J. R., Gallardo, T., Peris, E., Bermejo, A., Cabedo, N., Estornell, E., Zafra-Polo, M. C., Cortes, D. (2003) Inhibitory effects on mitochondrial complex I of semisynthetic monotetrahydrofuran acetogenin derivatives, Bioorg. Med. Chem. Lett. 13, 4101-4105.
52. Cortes, D., Myint, S. H., Harmange, J.-C., Sahpaz, S., Figadère, B. (1992) Catalytic hydrogenation of Annonaceous acetogenins, Tetrahedron Lett. 33, 5225-5226.
53. Ichimaru, N., Murai, M., Abe, M., Hamada, T., Yamada, Y., Makino, S., Nishioka, T., Makabe, H., Makino, A., Kobayashi, T., Miyoshi, H. (2005) Synthesis and inhibition mechanism of Δlac-acetogenins, a novel type of inhibitor of bovine heart mitochondrial Complex I, Biochemistry 44, 2, 816-825.
54. Tormo, J. R., Gallardo, T., Aragón, R., Cortes, D., Estornell E. (1999) Specific interactions of monotetrahydrofuranic annonaceous acetogenins as inhibitors of mitochondrial Complex I, Chem.-Biol. Interact. 122, 171-183.
55. Darrouzet, E., Dupuis, A. (1997) Genetic evidence for the existence of two quinone related inhibitor binding sites in NADH-CoQ reductase, Biochim. Biophys. Acta 1319, 1-4.
56. Darrouzet, E., Issrate, J.-P., Lunardi, J., Dupuis, A. (1998) The 49 kDa subunit of NADH-ubiquinone oxidoreductase (Complex I) is involved in the binding of piericidin and rotenone, two quinone-related inhibitors, FEBS Lett. 431, 34-38.
57. +) and its analogues with the rotenone/piericidin binding site of NADH dehydrogenase, J. Neurochem. 56, 4, 1184-1190.
58. 3H]dihydrorotenone binding to NADH:ubiquinone reductase (Complex I) of the electron transport chain: An autoradiographic study, J. Neurosci. 16, 12, 3807-3816.
59. Schuler, F., Casida, J. E. (2001) Functional coupling of PSST and ND1 subunits in NADH:ubiquinone oxidoreductase established by photoaffinity labeling, Biochim. Biophys. Acta 1506, 79-87.
60. Gluck, M. R., Krueger, M. J., Ramsay, R. R., Sablin, S. O., Singer, T. P., Nicklas, W. J. (1994) Characterization of the inhibitory mechanism of 1-methyl-4-phenylpyridinium and 4-phenylpyridine analogues in inner membrane preparations, J. Biol. Chem. 269, 3167-3174.