Amphiphilic amide nitrones: A new class of protective agents acting as modifiers of mitochondrial metabolism

Journal of Medicinal Chemistry

Volumn 53, Issue 13, 2010, Pages 4849-4861

  Durand, Grégory ^a   Poeggeler, Burkhard ^b,c   Ortial, Stéphanie ^a   Polidori, Ange ^a   Villamena, Frederick A ^d   Böker, Jutta ^c   Hardeland, Rüdiger ^c   Pappolla, Miguel A ^e   Pucci, Bernard ^a  

^a UNIVERSITY OF AVIGNON   (France)

^b UNIVERSITY OF LÜBECK   (Germany)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^e MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE NITRONE DERIVATIVE; AMPHOPHILE; ANTIOXIDANT; DOPAMINE; HYDROXYL RADICAL; NITRONE DERIVATIVE; PROTECTIVE AGENT; UNCLASSIFIED DRUG; WATER;

ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CELL CULTURE; CYCLIC POTENTIOMETRY; DRUG ACTIVITY; DRUG SYNTHESIS; IONIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION REDUCTION REACTION; PROTON TRANSPORT; RAT;

ANIMALS; BENZOTHIAZOLES; BRAIN; FREE RADICAL SCAVENGERS; HYDROGEN PEROXIDE; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NITROGEN OXIDES; OPTICAL ROTATION; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SULFONIC ACIDS; SURFACE-ACTIVE AGENTS;

EID: 77954332672     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm100212x     Document Type: Article

References (74)

1. Coulter, C. V.; Kelso, G. F.; Lin, T.-K.; Smith, R. A. J.; Murphy, M. P. Mitochondrially targeted antioxidants and thiol reagents Free Radical Biol. Med. 2000, 28, 1547-1554
2. Muratovska, A.; Lightowlers, R. N.; Taylor, R. W.; Wilce, J. A.; Murphy, M. P. Targeting large molecules to mitochondria Adv. Drug Delivery Rev. 2001, 49, 189-198
3. Murphy, M. P.; Echtay, K. S.; Blaikie, F. H.; Asin-Cayuela, J.; Cocheme, H. M.; Green, K.; Buckingham, J. A.; Taylor, E. R.; Hurrell, F.; Hughes, G.; Miwa, S.; Cooper, C. E.; Svistunenko, D. A.; Smith, R. A. J.; Brand, M. D. Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation: studies using a mitochondria-targeted spin trap derived from α-phenyl- tert -butylnitrone J. Biol. Chem. 2003, 278, 48534-48545
4. Covey, M. V.; Murphy, M. P.; Hobbs, C. E.; Smith, R. A. J.; Oorschot, D. E. Effect of the mitochondrial antioxidant, mito vitamin E, on hypoxic-ischemic striatal injury in neonatal rats: a dose-response and stereological study Exp. Neurol. 2006, 199, 513-519
5. Horton, K. L.; Stewart, K. M.; Fonseca, S. B.; Guo, Q.; Kelley, S. O. Mitochondria-penetrating peptides Chem. Biol. 2008, 15, 375-382
6. Zhao, K.; Luo, G.; Giannelli, S.; Szeto, H. H. Mitochondria-targeted peptide prevents mitochondrial depolarization and apoptosis induced by tert -butyl hydroperoxide in neuronal cell lines Biochem. Pharmacol. 2005, 70, 1796-1806
7. Wipf, P.; Xiao, J.; Jiang, J.; Belikova, N. A.; Tyurin, V. A.; Fink, M. P.; Kagan, V. E. Mitochondrial targeting of selective electron scavengers: synthesis and biological analysis of hemigramicidin-TEMPO conjugates J. Am. Chem. Soc. 2005, 127, 12460-12461
8. El Fangour, S.; Marini, M.; Good, J.; McQuaker, S. J.; Shiels, P. G.; Hartley, R. C. Nitrones for understanding and ameliorating the oxidative stress associated with aging Age 2009, 31, 269-276
9. Ouari, O.; Polidori, A.; Pucci, B.; Tordo, P.; Chalier, F. Synthesis of a glycolipidic amphiphilic nitrone as a new spin trap J. Org. Chem. 1999, 64, 3554-3556
10. Geromel, V.; Kadhom, N.; Cebalos-Picot, I.; Ouari, O.; Polidori, A.; Munnich, A.; Rötig, A.; Rustin, P. Superoxide-induced massive apoptosis in cultured skin fibroblasts harboring the neurogenic ataxia retinitis pigmentosa (NARP) mutation in the ATPase-6 gene of the mitochondrial DNA Hum. Mol. Genet. 2001, 10, 1221-1228
11. Périno, S.; Contino-Pépin, C.; Jasseron, S.; Rapp, M.; Maurizis, J.-C.; Pucci, B. Design, synthesis and preliminary biological evaluations of novel amphiphilic drug carriers Bioorg. Med. Chem. Lett. 2006, 16, 1111-1114
12. Ortial, S.; Durand, G.; Poeggeler, B.; Polidori, A.; Pappolla, M. A.; Boeker, J.; Hardeland, R.; Pucci, B. Fluorinated amphiphilic amino acid derivatives as antioxidant carriers: a new class of protective agents J. Med. Chem. 2006, 49, 2812-2820
13. Durand, G.; Prosak, R. A.; Han, Y.; Ortial, S.; Rockenbauer, A.; Pucci, B.; Villamena, F. A. Spin trapping and cytoprotective properties of fluorinated amphiphilic carrier conjugates of cyclic versus linear nitrones Chem. Res. Toxicol. 2009, 22, 1570-1581
14. Durand, G.; Polidori, A.; Salles, J.-P.; Pucci, B. Synthesis of a new family of glycolipidic nitrones as potential antioxidant drugs for neurodegenerative disorders Bioorg. Med. Chem. Lett. 2003, 13, 859-862
15. Durand, G.; Polidori, A.; Ouari, O.; Tordo, P.; Geromel, V.; Rustin, P.; Pucci, B. Synthesis and preliminary biological evaluations of ionic and nonionic amphiphilic alpha-phenyl- N-tert -butylnitrone derivatives J. Med. Chem. 2003, 46, 5230-5237
16. Durand, G.; Polidori, A.; Salles, J.-P.; Prost, M.; Durand, P.; Pucci, B. Synthesis and antioxidant efficiency of a new amphiphilic spin-trap derived from PBN and lipoic acid Bioorg. Med. Chem. Lett. 2003, 13, 2673-2676
17. Asanuma, T.; Yasui, H.; Inanami, O.; Waki, K.; Takahashi, M.; Iizuka, D.; Uemura, T.; Durand, G.; Polidori, A.; Kon, Y.; Pucci, B.; Kuwabara, M. A new amphiphilic derivative, N -{[4-(lactobionamido)methyl]benzylidene}-1,1-dimethyl- 2-(octylsulfanyl)ethylamine N -oxide, has a protective effect against copper-induced fulminant hepatitis in Long-Evans cinnamon rats at an extremely low concentration compared with its original form alpha-phenyl- N -(tert -butyl) nitrone Chem. Biodiversity 2007, 4, 2253-2267
18. Poeggeler, B.; Durand, G.; Polidori, A.; Pappolla, M. A.; Vega-Naredo, I.; Coto-Montes, A.; Boeker, J.; Hardeland, R.; Pucci, B. Mitochondrial medicine: neuroprotection and life extension by the new amphiphilic nitrone LPBNAH acting as a highly potent antioxidant agent J. Neurochem. 2005, 95, 962-973
19. Tanguy, S.; Durand, G.; Reboul, C.; Polidori, A.; Pucci, B.; Dauzat, M.; Obert, P. Protection against reactive oxygen species injuries in rat isolated perfused hearts: effect of LPBNAH, a new amphiphilic spin-trap derived from PBN Cardiovasc. Drugs Ther. 2006, 20, 147-149
20. Durand, G.; Poeggeler, B.; Boeker, J.; Raynal, S.; Polidori, A.; Pappolla, M. A.; Hardeland, R.; Pucci, B. Fine-tuning the amphiphilicity: a crucial parameter in the design of potent alpha-phenyl- N-tert -butylnitrone analogues J. Med. Chem. 2007, 50, 3976-3979
21. Ouari, O.; Chalier, F.; Bonaly, R.; Pucci, B.; Tordo, P. Synthesis and spin-trapping behavior of glycosylated nitrones J. Chem. Soc., Perkin Trans. 2 1998, 2299-2308
22. Lebaupain, F.; Salvay, A. G.; Olivier, B.; Durand, G.; Fabiano, A. S.; Michel, N.; Popot, J. L.; Ebel, C.; Breyton, C.; Pucci, B. Lactobionamide surfactants with hydrogenated, perfluorinated or hemifluorinated tails: physical-chemical and biochemical characterization Langmuir 2006, 22, 8881-8890
23. Kissa, E. Fluorinated Surfactants: Synthesis, Properties, Applications; Dekker: New York, 1994; Vol. 7, pp 264 - 282.
24. Poeggeler, B.; Thuermann, S.; Dose, A.; Schoenke, M.; Burkhardt, S.; Hardeland, R. Melatonins unique radical scavenging properties-roles of its functional substituents as revealed by a comparison with its structural analogs J. Pineal Res. 2002, 33, 20-30
25. Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay Free Radical Biol. Med. 1999, 26, 1231-1237
26. Durand, G.; Choteau, F.; Pucci, B.; Villamena, F. A. Reactivity of superoxide radical anion and hydroperoxyl radical with α-phenyl- N-tert -butylnitrone (PBN) derivatives J. Phys. Chem. A 2008, 112, 12498-12509
27. McIntire, G. L.; Blount, H. N.; Stronks, H. J.; Shetty, R. V.; Janzen, E. G. Spin trapping in electrochemistry. 2. Aqueous and nonaqueous electrochemical characterizations of spin traps J. Phys. Chem. 1980, 84, 916-921
28. Tuccio, B.; Bianco, P.; Bouteiller, J. C.; Tordo, P. Electrochemical characterisation of [beta]-phosphorylated nitrone spin traps Electrochim. Acta 1999, 44, 4631-4634
29. Gille, L.; Nohl, H. Analyses of the molecular mechanism of adriamycin-induced cardiotoxicity Free Radical Biol. Med. 1997, 23, 775-782
30. Kotamraju, S.; Konorev, E. A.; Joseph, J.; Kalyanaraman, B. Doxorubicin-induced apoptosis in endothelial cells and cardiomyocytes is ameliorated by nitrone spin traps and ebselen. Role of reactive oxygen and nitrogen species J. Biol. Chem. 2000, 275, 33585-33592
31. Radi, R.; Rodriguez, M.; Castro, L.; Telleri, R. Inhibition of mitochondrial electron transport by peroxynitrite Arch. Biochem. Biophys. 1994, 308, 89-95
32. Estévez, A. G.; Radi, R.; Barbeito, L.; Shin, J.; Thompson, J. A.; Beckman, J. S. Peroxynitrite-induced cytotoxicity in PC12 cells: evidence for an apoptotic mechanism differentially modulated by neurotrophic factors J. Neurochem. 1995, 65, 1543-1550
33. Meadow, N. D.; Barrows, C. H. J. Studies on aging in a bdelloid rotifer. I. The effect of various culture systems on longevity and fecundity J. Exp. Zool. 1971, 176, 303-313
34. Meadow, N. D.; Barrows, C. H. J. Studies on aging in a bdelloid rotifer. II. The effects of various environmental conditions and maternal age on longevity and fecundity J. Gerontol. 1971, 26, 302-309
35. Enesco, H. E.; Verdone-Smith, C. α-Tocopherol increases lifespan in the rotifer philodina Exp. Gerontol. 1980, 15, 335-338
36. Sawada, M.; Carlson, J. C. Association between lipid peroxidation and life-modifying factors in rotifers J. Gerontol. 1987, 42, 451-456
37. Sawada, M.; Carlson, J. C. Biochemical changes associated with the mechanism controlling superoxide radical formation in the aging rotifer J. Cell. Biochem. 1990, 44, 153-165
38. Hermes-Lima, M.; Willmore, W. G.; Storey, K. B. Quantification of lipid peroxidation in tissue extracts based on Fe(III) xylenol orange complex formation Free Radical Biol. Med. 1995, 10, 271-280
39. Lyras, L.; Cairns, N. J.; Jenner, A.; Jenner, B.; Halliwell, B. An assessment of oxidative damage to proteins, lipids, and DNA in brain from patients with Alzheimers disease J. Neurochem. 1997, 68, 2061-2069
40. Hensley, K.; Pye, Q. N.; Maidt, M. L.; Stewart, C. A.; Robinson, K. A.; Jaffrey, F.; Floyd, R. A. Interaction of α-phenyl- N-tert -butyl nitrone and alternative electron acceptors with complex 1 indicates a substrate reduction site upstream from the rotenone binding site J. Neurochem. 1998, 71, 2549-2557
41. Genova, M. L.; Pich Merlo, M.; Bernacchia, A.; Bianchi, C.; Biondi, A.; Bovina, C.; Falasca, A. I.; Formiggini, G.; Parenti Castelli, G.; Lenaz, G. The mitochondrial production of reactive oxygen species in relation to aging and pathology Ann. N.Y. Acad. Sci. 2004, 1011, 86-100
42. Genova, M. L.; Ventura, B.; Giuliano, G.; Bovina, C.; Formiggini, G.; Parenti Castelli, G.; Lenaz, G. The site of production of superoxide radical in mitochondrial complex I is not a bound ubisemiquinone but presumably iron-sulfur cluster N2 FEBS Lett. 2001, 505, 364-368
43. Murakami, K.; Kondo, T.; Kawase, M.; Li, Y.; Sato, S.; Chen, S. F.; Chan, P. H. Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency J. Neurosci. 1998, 18, 205-213
44. Scadoto, R. C.; Grotyohann, L. W. Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives Biophys. J. 1999, 76, 469-477
45. Lee, S. J.; Jin, Y.; Yoon, H. Y.; Choi, B.-O.; Kim, H. C.; Oh, Y.-K.; Kim, H.-S.; Kim, W.-C. Ciclopirox protects mitochondria from hydrogen peroxide toxicity Br. J. Pharmacol. 2005, 145, 469-476
46. Ben-Shachar, D.; Zuk, R.; Glinka, Y. Dopamine neurotoxicity: inhibition of mitochondrial respiration J. Neurochem. 1995, 64, 718-723
47. Ben-Shachar, D.; Zuk, R.; Gazawi, H.; Ljubuncic, P. Dopamine toxicity involves mitochondrial complex I inhibition: implications to dopamine-related neuropsychiatric disorders Biochem. Pharmacol. 2004, 67, 1965-1974
48. Brenner-Lavie, H.; Klein, E.; Zuk, R.; Gazawi, H.; Ljubuncic, P.; Ben-Shachar, D. Dopamine modulates mitochondrial function in viable SH-SY5Y cells possibly via its interaction with complex I: relevance to dopamine pathology in schizophrenia Biochim. Biophys. Acta 2008, 1777, 173-185
49. Brenner-Lavie, H.; Klein, E.; Ben-Shachar, D. Mitochondrial complex I as a novel target for intraneuronal DA: modulation of respiration in intacts cells Biochem. Pharmacol. 2009, 78, 85-95
50. Moreno-Sanchez, R.; Hogue, B. A.; Bravo, C.; Newman, A. H.; Basile, A. S.; Chiang, P. K. Inhibition of substrate oxidation in mitochondria by the peripheral-type benzodiazepine receptor ligand AHN 086 Biochem. Pharmacol. 1991, 41, 1479-1484
51. Gutman, M.; Singer, T. P. EPR studies on the iron sulfur centers of DPNH dehydrogenase during redox cycle of the enzyme Biochem. Biophys. Res. Commun. 1973, 44, 1572-1578
52. Lusty, C. J.; Machinist, J. M.; Singer, T. P. Studies on the respiratory chainlinked nicotinamide adenine dinucleotide dehydrogenase. VII. Labile sulfide group in the dehydrogenase and related proteins J. Biol. Chem. 1965, 240, 1804-1810
53. Harmon, H. J.; Crane, F. L. Inhibition of mitochondrial electron transport by hydrophilic metal chelators. Determination of dehydrogenase topography Biochim. Biophys. Acta 1976, 440, 45-48
54. Lenaz, G.; Fato, R.; Genova, M. L.; Bergamini, C.; Bianchi, C.; Biondi, A. Mitochondrial complex I: structural and functional aspects Biochim. Biophys. Acta 2006, 1757, 1406-1420
55. Poeggeler, B.; Reiter, R. J.; Hardeland, R.; Tan, D.-X.; Barlow-Walden, L. R. Melatonin and structurally-related endogenous indoles act as potent electron donors and radical scavengers in vitro Redox Rep. 1996, 2, 179-184
56. Halgren, T. A. Merck molecular force field. I. Basis, form, scope, parametrization and performance of MMF94 J. Comput. Chem. 1996, 17, 490-519
57. MacroModel, version 9.6; Schrödinger, LLC: New York, 2005.
58. Still, W. C.; Tempczyk, A.; Hawlely, R. C.; Hendrickson, T. Semianalytical treatment of solvation for molecular mechanics and dynamics J. Am. Chem. Soc. 1990, 112, 6127-6129
59. Labanowski, J. W.; Andzelm, J. Density Functional Methods in Chemistry; Springer: New York, 1991.
60. Parr, R. G.; Yang, W. Density Functional Theory in Atoms and Molecules; Oxford University Press: New York, 1989.
61. Becke, A. D. Density-functional exchange-energy approximation with correct asymptotic behavior Phys. Rev. A 1988, 38, 3098-3100
62. Becke, A. D. Density-functional thermochemistry. III. The role of exact exchange J. Chem. Phys. 1993, 98, 5648-5652
63. Hehre, W. J.; Radom, L.; Schleyer, P. V.; Pople, J. A. Ab Initio Molecular Orbital Theory; John Wiley & Sons: New York, 1986.
64. Lee, C.; Yang, W.; Parr, R. G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Phys. Rev. B 1988, 37, 785-789
65. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Montgomery, J. A., Jr.; Vreven, T.; Kudin, K. N.; Burant, J. C.; Millam, J. M.; Iyengar, S. S.; Tomasi, J.; Barone, V.; Mennucci, B.; Cossi, M.; Scalmani, G.; Rega, N.; Petersson, G. A.; Nakatsuji, H.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Klene, M.; Li, X.; Knox, J. E.; Hratchian, H. P.; Cross, J. B.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Ayala, P. Y.; Morokuma, K.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Zakrzewski, V. G.; Dapprich, S.; Daniels, A. D.; Strain, M. C.; Farkas, O.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.; Foresman, J. B.; Ortiz, J. V.; Cui, Q.; Baboul, A. G.; Clifford, S.; Cioslowski, J.; Stefanov, B. B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, I.; Martin, R. L.; Fox, D. J.; Keith, T.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara, A.; Challacombe, M.; Gill, P. M. W.; Johnson, B.; Chen, W.; Wong, M. W.; Gonzalez, C.; Pople, J. A. Gaussian 03, revision B.04; Gaussian, Inc.: Pittsburgh PA, 2003.
66. Freed, J. H. Theory of Slow Tumbling ESR Spectra for Nitroxides; Academic: New York, 1976.
67. Cossi, M.; Barone, V. Analytical second derivatives of the free energy in solution by polarizable continuum models J. Chem. Phys. 1998, 109, 6246-6254
68. Cossi, M.; Barone, V.; Cammi, R.; Tomasi, J. Ab initio study of solvated molecules: a new implementation of the polarizable continuum model Chem. Phys. Lett. 1996, 255, 327-335
69. Tedeschi, A. M.; DErrico, G.; Busi, E.; Basosi, R.; Barone, V. Micellar aggregation of sulfonate surfactants studied by electron paramagnetic resonance of a cationic nitroxide: an experimental and computational approach Phys. Chem. Chem. Phys. 2002, 2180-2188
70. Tomasi, J.; Persico, M. Molecular interactions in solution: an overview of methods based on continuous distributions of the solvent Chem. Rev. 1994, 94, 2027-2094
71. Law, A.; Gauthier, S.; Quirion, R. Neuroprotective and neurorescuing effects of isoform-specific nitric oxide synthase inhibitors, nitric oxide scavenger, and antioxidant against beta-amyloid toxicity Br. J. Pharmacol. 2001, 133, 1114-1124
72. Uliasz, T. F.; Hewett, S. J. A microtiter trypan blue absorbance assay for the quantitative determination of excitoxic neuronal injury in cell culture J. Neurosci. Methods 2000, 100, 157-163
73. 2+, nitroxide spin probes, and synaptosomal membrane proteins Life Sci. 1996, 58, 217-228
74. Vrablic, A. S.; Albright, C. D.; Craciunescu, C. N.; Salganik, R. I.; Zeisel, S. H. Altered mitochondrial function and overgeneration of reactive oxygen species precede the induction of apoptosis by 1- O -octadecyl-2-methyl- rac-glycero-3-phosphocholine in p53-defective hepatocytes FASEB J. 2001, 15, 1739-1744