Enantioselective oxidation of trans-4-hydroxy-2-nonenal is aldehyde dehydrogenase isozyme and Mg2+ dependent

Chemical Research in Toxicology

Volumn 20, Issue 6, 2007, Pages 887-895

  Brichac, Jiri ^a,d   Kwok, Ki Ho ^c   Honzatko, Ales ^a   Wang, Rongying ^b   Lu, Xiaoning ^b   Weiner, Henry ^c   Picklo Sr , Matthew J ^a  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

^b UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c PURDUE UNIVERSITY   (United States)

^d CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYNONENAL; ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE 5A; ALDEHYDE DEHYDROGENASE ISOENZYME 2; CYSTEINE; ISOENZYME; MAGNESIUM; TRANS 4 HYDROXY 2 NONENOIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN MITOCHONDRION; CHEMICAL REACTION; CONTROLLED STUDY; ENANTIOMER; ENANTIOSELECTIVITY; MITOCHONDRION; NONHUMAN; OXIDATION; RAT;

ACETALDEHYDE; ALDEHYDE DEHYDROGENASE; ALDEHYDES; ANIMALS; CATALYSIS; CATIONS, DIVALENT; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GAMMA-AMINOBUTYRIC ACID; ISOENZYMES; KINETICS; MAGNESIUM; MODELS, MOLECULAR; NAD; OXIDATION-REDUCTION; PROTEIN CONFORMATION; RATS; RATS, SPRAGUE-DAWLEY; STEREOISOMERISM;

RATTUS;

EID: 34447118905     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx7000509     Document Type: Article

References (57)

1. Esterbauer, H., Schaur, R. J., and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biol. Med. 11, 81-128.
2. Uchida, K. (2003) 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog. Lipid Res. 42, 318-343.
3. Picklo, M. J., Montine, T. J., Amarnath, V., and Neely, M. D. (2002) Carbonyl toxicology and Alzheimer's disease. Toxicol. Appl. Pharmacol. 184, 187-197.
4. McKracken, E., Graham, D. I., Nilsen, M., Stewart, J., Nicoll, J. A., and Horsburgh, K. (2001) 4-Hydroxynonenal immunoreactivity is increased in human hippocampus after global ischemia. Brain Pathol. 11, 414-421.
5. Montine, K. S., Olson, S. J., Amarnath, V., Whetsell, W. O., Jr., Graham, D. G., and Montine, T. J. (1997) Immunohistochemical detection of 4-hydroxy-2-nonenal adducts in Alzheimer's disease is associated with inheritance of APOE4. Am. J. Pathol. 150, 437-443.
6. Sayre, L. M., Zelasko, D. A., Harris, P. L., Perry, G., Salomon, R. G., and Smith, M. A. (1997) 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J. Neurochem. 68, 2092-2097.
7. Yoritaka, A., Hattori, N., Uchida, K., Tanaka, M., Stadtman, E. R., and Mizuno, Y. (1996) Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc. Natl. Acad. Sci. U.S.A. 93, 2696-2701.
8. Sayre, L. M., Arora, P. K., Iyer, R. S., and Salomon, R. G. (1993) Pyrrole formation from 4-hydroxynonenal and primary amines. Chem. Res. Toxicol. 6, 19-22.
9. Amarnath, V., Valentine, W. M., Montine, T. J., Patterson, W. H., Amarnath, K., Bassett, C. N., and Graham, D. G. (1998) Reactions of 4-hydroxy-2(E)-nonenal and related aldehydes with proteins studied by carbon-13 nuclear magnetic resonance spectroscopy. Chem. Res. Toxicol. 11, 317-328.
10. Nadkarni, D. V., and Sayre, L. M. (1995) Structural definition of early lysine and histidine adduction chemistry of 4-hydroxynonenal. Chem. Res. Toxicol. 8, 284-291.
11. Petersen, D. R., and Doorn, J. A. (2004) Reactions of 4-hydroxynonenal with proteins and cellular targets, Free Radical Biol. Med. 37, 937-945.
12. Alary, J., Gueraud, F., and Cravedi, J. P. (2003) Fate of 4-hydroxynonenal in vivo: disposition and metabolic pathways. Mol. Aspects Med. 24, 177-187.
13. Kubatova, A., Murphy, T. C., Combs, C., and Picklo, M. J., Sr. (2006) Astrocytic Biotransformation of trans-4-Hydroxy-2-nonenal Is Dose-Dependent. Chem. Res. Toxicol. 19, 844-851.
14. Srivastava, S., Chandra, A., Wang, L. F., Seifert, W. E., Jr., DaGue, B. B., Ansari, N. H., Srivastava, S. K., and Bhatnagar, A. (1998) Metabolism of the lipid peroxidation product, 4-hydroxy-trans-2-nonenal, in isolated perfused rat heart. J. Biol. Chem. 273, 10893-10900.
15. Mitchell, D., and Petersen, D. (1987) The oxidation of a,b,unsaturated aldehydic products in lipid peroxidation by rat liver aldehyde dehydrogenases. Toxicol. Appl. Pharmacol. 87, 403-410.
16. Murphy, T. C., Amarnath, V., Gibson, K. M., and Picklo, M. J., Sr. (2003) Oxidation of 4-hydroxy-2-nonenal by succinic semialdehyde dehydrogenase (ALDH5A). J. Neurochem. 86, 298-305.
17. Chambliss, K. L., and Gibson, K. M. (1992) Succinic semialdehyde dehydrogenase from mammalian brain: subunit analysis using polyclonal antiserum. Int. J. Biochem. 24, 1493-1499.
18. +-dependent succinic semialdehyde dehydrogenase. Arch. Biochem. Biophys. 266, 386-396.
19. Kang, T. C., Park, S. K., Hwang, I. K., An, S. J., Choi, S. Y., Cho, S. W., and Won, M. H. (2002) Spatial and temporal alterations in the GABA shunt in the gerbil hippocampus following transient ischemia. Brain Res. 944, 10-18.
20. Picklo, M. J., Olson, S. J., Markesbery, W. R., and Montine, T. J. (2001) Expression and activities of aldo-keto oxidoreductases in Alzheimer disease. J. Neuropathol. Exp. Neurol. 60, 686-695.
21. Hashimoto, M., Sibata. T., Wasada, H., Toyokuni, S., and Uchida, K. (2003) Structural basis of protein-bound endogenous aldehydes. Chemical and immunochemical characterizations of configurational isomers of a 4-hydroxy-2-nonenal-histidine adduct. J. Biol. Chem. 278, 5044-5051.
22. Honzatko, A., Brichac, J., Murphy, T. C., Reberg, A., Kubatova, A., Smoliakova, I. P., and Picklo, M. J., Sr. (2005) Enantioselective metabolism of trans-4-hydroxy-2-nonenal by brain mitochondria. Free Radical Biol. Med. 39, 913-924.
23. Hiratsuka, A., Hirose, K., Saito, H., and Watabe, T. (2000) 4-Hydroxy-2(E)-nonenal enantiomers: (S)-selective inactivation of glyceraldehyde-3-phosphate dehydrogenase and detoxification by rat glutathione S-transferase A4-4. Biochem. J. 349, 729-735.
24. Tatton, W. G., Chalmers-Redman, R., Brown, D. and Tatton, N. (2003) Apoptosis in Parkinson's disease: signals for neuronal degradation. Ann. Neurol. 53 (Suppl. 3), S61-70, discussion S70-62.
25. Wang, Q., Woltjer, R. L., Cimino, P. J., Pan, C., Montine, K. S., Zhang, J., and Montine, T. J. (2005) Proteomic analysis of neurofibrillary tangles in Alzheimer disease identifies GAPDH as a detergent-insoluble paired helical filament tau binding protein. FASEB J. 19, 869-871.
26. Hiratsuka, A., Tobita, K., Saito, H., Sakamoto, Y., Nakano, H., Ogura, K., Nishiyama, T., and Watabe, T. (2001) (S)-preferential detoxification of 4-hydroxy-2(E)-nonenal enantiomers by hepatic glutathione S-transferase isoforms in guinea-pigs and rats. Biochem. J. 355, 237-244.
27. Chandra, A., and Srivastava, S. K. (1997) A synthesis of 4-hydroxy-2-trans-nonenal and 4-(3H) 4-hydroxy-2-trans-nonenal. Lipids 32, 779-782.
28. Alary, J., Bravais, F., Cravedi, J. P., Debrauwer, L., Rao, D., and Bories, G. (1995) Mercapturic acid conjugates as urinary end metabolites of the lipid peroxidation product 4-hydroxy-2-nonenal in the rat. Chem. Res. Toxicol. 8, 34-39.
29. Murphy, T. C., Amarnath, V., and Picklo, M. J., Sr. (2003) Mitochondrial oxidation of 4-hydroxy-2-nonenal in rat cerebral cortex. J. Neurochem. 84, 1313-1321.
30. Nguyen, E., and Picklo, M. J. (2003) Inhibition of succinic semialdehyde dehydrogenase activity by alkenal products of lipid peroxidation. Biochim. Biophys. Acta 1637, 107-112.
31. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
32. Leiphon, L. J., and Picklo, M. J. S. Inhibition of aldehyde detoxification in CNS mitochondria by fungicides. Neurotoxicology (in press).
33. Combet, C., Jambon, M., Deleage, G., and Geourjon, C. (2002) Geno3D: automatic comparative molecular modelling of protein. Bioinformatics 18, 213-214.
34. Schuttelkopf, A. W., and van Aalten, D. M. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr., D: Biol. Crystallogr. 60, 1355-1363.
35. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.
36. Yang, S. K., Bao, Z., and Shou, M. (1996) Stereoselective nucleophilic substitution of oxazepam and racemization in acidic methanol and ethanol. Chirality 8, 214-223.
37. Aso, Y., Yoshioka, S., and Takeda, Y. (1990) Epimerization and racemization of some chiral drugs in the presence of human serum albumin. Chem. Pharm. Bull. (Tokyo) 38, 180-184.
38. Gineyts, E., Cloos, P. A., Borel, O., Grimaud, L., Delmas, P. D., and Garnero, P. (2000) Racemization and isomerization of type I collagen C-telopeptides in human bone and soft tissues: assessment of tissue turnover. Biochem. J. 345 (Part 3), 481-485.
39. Stadtman, E. R. (1988) Protein modification in aging, J. Gerontol. 43, B112-120.
40. Schneider, C., Tallman, K. A., Porter, N. A., and Brash, A. R. (2001) Two distinct pathways of formation of 4-hydroxynonenal. Mechanisms of nonenzymatic transformation of the 9- and 13-hydroperoxides of linoleic acid to 4-hydroxyalkenals. J. Biol. Chem. 276, 20831-20838.
41. Schneider, C., Porter, N. A., and Brash, A. R. (2004) Autoxidative transformation of chiral omega6 hydroxy linoleic and arachidonic acids to chiral 4-hydroxy-2E-nonenal. Chem. Res. Toxicol. 17, 937-941.
42. Doorn, J. A., Hurley, T. D., and Petersen, D. R. (2006) Inhibition of human mitochondrial aldehyde dehydrogenase by 4-hydroxynon-2-enal and 4-oxonon-2-enal. Chem. Res. Toxicol. 19, 102-110.
43. 2+ ions on the individual kinetic steps of human cytosolic and mitochondrial aldehyde dehydrogenases. Biochemistry 44, 8022-8029.
44. 2+ on sheep liver cytoplasmic aldehyde dehydrogenase. Biochem. J. 205, 443-448.
45. Larson, H. N., Weiner, H., and Hurley, T. D. (2005) Disruption of the coenzyme binding site and dimer interface revealed in the crystal structure of mitochondrial aldehyde dehydrogenase "Asian" variant. J. Biol. Chem. 280, 30550-30556.
46. Moore, S. A., Baker, H. M., Blythe, T. J., Kitson, K. E., Kitson, T. M., and Baker, E. N. (1998) Sheep liver cytosolic aldehyde dehydrogenase: the structure reveals the basis for the retinal specificity of class 1 aldehyde dehydrogenases. Structure 6, 1541-1551.
47. Steinmetz, C. G., Xie, P., Weiner, H., and Hurley, T. D. (1997) Structure of mitochondrial aldehyde dehydrogenase: the genetic component of ethanol aversion. Structure 5, 701-711.
48. Liu, Z. J., Hempel, J., Sun, J., Rose, J., Hsiao, D., Chang, W. R., Chung, Y. J., Kuo, I., Lindahl, R., and Wang, B. C. (1997) Crystal structure of a class 3 aldehyde dehydrogenase at 2.6 Å resolution. Adv. Exp. Med. Biol. 414, 1-7.
49. Esterbauer, H., Schaur, R., and Zollner, H. (1991) Chemistry and Biochemistry of 4-hydroxynonenal, malondialdehyde, and related aldehydes. Free Radical Biol. Med. 11, 81-128.
50. Burgi, H. B., and Dunitz, J. D. (1983) From crystal statics to chemical dynamics. Acc. Chem. Res. 16, 153-161.
51. Johansson, K., El-Ahmad, M., Ramaswamy, S., Hjelmqvist, L., Jornvall, H., and Eklund, H. (1998) Structure of betaine aldehyde dehydrogenase at 2.1 Å resolution. Protein Sci. 7, 2106-2117.
52. Lamb, A. L., and Newcomer, M. E. (1999) The structure of retinal dehydrogenase type II at 2.7 Å resolution: implications for retinal specificity. Biochemistry 38, 6003-6011.
53. Corkey, B. E., Duszynski, J., Rich, T. L., Matschinsky, B., and Williamson, J. R. (1986) Regulation of free and bound magnesium in rat hepatocytes and isolated mitochondria. J. Biol. Chem. 261, 2567-2574.
54. 2+ transport. J. Biol. Chem. 261, 16478-16483.
55. Pappa, A., Estey, T., Manzer, R., Brown, D., and Vasiliou, V. (2003) Human aldehyde dehydrogenase 3A1 (ALDH3A1): biochemical characterization and immunohistochemical localization in the cornea. Biochem. J. 376, 615-623.
56. Farres, J., Wang, T. T., Cunningham, S. J., and Weiner, H. (1995) Investigation of the active site cysteine residue of rat liver mitochondrial aldehyde dehydrogenase by site-directed mutagenesis. Biochemistry 34, 2592-2598.
57. Sheikh, S., Ni, L., Hurley, T. D., and Weiner, H. (1997) The potential roles of the conserved amino acids in human liver mitochondrial aldehyde dehydrogenase. J. Biol. Chem. 272, 18817-18822.