Oxidative modification of lipoic acid by HNE in alzheimer disease brain

Redox Biology

Volumn 1, Issue 1, 2013, Pages 80-85

  Hardas, Sarita S ^a,b   Sultana, Rukhsana ^a,b   Clark, Amy M ^a   Beckett, Tina L ^b   Szweda, Luke I ^c   Paul Murphy, M ^b   Butterfield, D Allan ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

4 hydroxy 2 trans nonenal (HNE); Alzheimer disease; Lipid peroxidation; Lipoamide dehydrogenase; Lipoic acid

Indexed keywords

2 OXOGLUTARIC ACID; 4 HYDROXYNONENAL; DIHYDROLIPOAMIDE DEHYDROGENASE; PYRUVATE DEHYDROGENASE; THIOCTIC ACID; 4-HYDROXY-2-NONENAL; ALDEHYDE;

ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN FUNCTION; CELL ENERGY; CONTROLLED STUDY; COVALENT BOND; ENZYME ACTIVITY; GLUCOSE METABOLISM; HUMAN; HUMAN TISSUE; IN VITRO STUDY; LIPID PEROXIDATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN MODIFICATION; SENILE PLAQUE; ANIMAL; BRAIN; C57BL MOUSE; CASE CONTROL STUDY; MALE; METABOLISM; MOUSE;

MUS;

ALDEHYDES; ALZHEIMER DISEASE; ANIMALS; BRAIN; CASE-CONTROL STUDIES; DIHYDROLIPOAMIDE DEHYDROGENASE; HUMANS; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; THIOCTIC ACID;

EID: 84878786543     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2013.01.002     Document Type: Article

References (72)

1. Duyckaerts, C.; Delatour, B.; Potier, M. C. Classification and basic pathology of Alzheimer disease. Acta Neuropathology 118(1):5-36; 2009.
2. Grundke-Iqbal I.; Iqbal, K.; Quinlan, M.; Tung, Y. C.; Zaidi, M. S.; Wisniewski, H. M. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. Journal of Biological Chemistry 261(13):6084-6089; 1986.
3. Markesbery, W. R. Oxidative stress hypothesis in Alzheimer's disease. Free Radical Biology and Medicine 23(1):134-147; 1997.
4. Butterfield, D. A.; Drake, J.; Pocernich, C.; Castegna, A. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends in Molecular Medicine 7(12):548-554; 2001.
5. Butterfield, D. A.; Castegna, A.; Lauderback, C. M.; Drake, J. Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death. Neurobiology of Aging 23(5):655-664; 2002.
6. Mark, R. J.; Lovell, M. A.; Markesbery, W. R.; Uchida, K.; Mattson, M. P. A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide. Journal of Neurochemistry 68(1):255-264; 1997.
7. Mattson, M. P. Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiological Reviews 77(4):1081-1132; 1997.
8. Lauderback, C. M.; Hackett, J. M.; Huang, F. F.; Keller, J. N.; Szweda, L. I.; Markesbery, W. R., et al. The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of a beta 1-42. Journal of Neurochemistry 78(2):413-416; 2001.
9. Higdon, A. N.; Landar, A.; Barnes, S.; Darley-Usmar, V. M. The electrophile responsive proteome: integrating proteomics and lipidomics with cellular function. Antioxidants and Redox Signaling 17(11):1580-1589; 2012.
10. Mello, C. F.; Sultana, R.; Piroddi, M.; Cai, J.; Pierce, W. M.; Klein, J. B., et al. Acrolein induces selective protein carbonylation in synaptosomes. Neu-roscience 147(3):674-679; 2007.
11. Norton, N. D.; Mamiya, B. M.; Kehrer, J. P. Relationships between cell density, glutathione and proliferation of A549 human lung adenocarcinoma cells treated with acrolein. Toxicology 122(1-2):111-122; 1997.
12. Pocernich, C. B.; Butterfield, D. A. Acrolein inhibits NADH-linked mitochon-drial enzyme activity: implications for Alzheimer's disease. Neurotoxicity Research 5(7):515-519; 2003.
13. Yang, X.; Wu, X.; Choi, Y. E.; Kern, J. C.; Kehrer, J. P. Effect of acrolein and glutathione depleting agents on thioredoxin. Toxicology 204(2-3):209-218; 2004.
14. Keller, J. N.; Schmitt, F. A.; Scheff, S. W.; Ding, Q.; Chen, Q.; Butterfield, D. A., et al. Evidence of increased oxidative damage in subjects with mild cognitive impairment. Neurology 64(7):1152-1156; 2005.
15. Yao, Y.; Clark, C. M.; Trojanowski, J. Q.; Lee, V. M.; Pratico, D. Elevation of 12/15 lipoxygenase products in AD and mild cognitive impairment. Annals of Neurology 58(4):623-626; 2005.
16. Lovell, M. A.; Ehmann, W. D.; Mattson, M. P.; Markesbery, W. R. Elevated 4-hydroxynonenal in ventricular fluid in Alzheimer's disease. Neurobiology of Aging 18(5):457-461; 1997.
17. Markesbery, W. R.; Lovell, M. A. Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiology of Aging 19(1):33-36; 1998.
18. Butterfield, D. A.; Stadtman, E. R. Protein Oxidation Processes in Aging Brain. In: Paula, S. T., Bittar, E. E., editors. Advances in Cell Aging and Gerontology. Elsevier; 1997. p. 161-191.
19. Hensley, K.; Hall, N.; Subramaniam, R.; Cole, P.; Harris, M.; Aksenov, M., et al. Brain regional correspondence between Alzheimers-disease histopathology and biomarkers of protein oxidation. Journal of Neurochemistry 65(5):2146-2156; 1995.
20. Sultana, R.; Piroddi, M.; Galli, F.; Butterfield, D. A. Protein levels and activity of some antioxidant enzymes in hippocampus of subjects with amnestic mild cognitive impairment. Neurochemical Research 33(12):2540-2546; 2008.
21. Guidi, I.; Galimberti, D.; Lonati, S.; Novembrino, C.; Bamonti, F.; Tiriticco, M., et al. Oxidative imbalance in patients with mild cognitive impairment and Alzheimer's disease. Neurobiology of Aging 27(2):262-269; 2006.
22. Butterfield, D. A.; Poon St. H. F.; Clair, D.; Keller, J. N.; Pierce, W. M.; Klein, J. B., et al. Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer's disease. Neurobiology of Disease 22(2):223-232; 2006.
23. Kagan, V. E.; Shvedova, A.; Serbinova, E.; Khan, S.; Swanson, C.; Powell, R., et al. Dihydrolipoic acid-a universal antioxidant both in the membrane and in the aqueous phase: reduction of peroxyl, ascorbyl and chromanoxyl radicals. Biochemical Pharmacology 44(8):1637-1649; 1992.
24. Biewenga, G. P.; Dorstijn, M. A.; Verhagen, J. V.; GRMM, Haenen; Bast, A. Reduction of lipoic acid by lipoamide dehydrogenase. Biochemical Pharmacology 51(3):233-238; 1996.
25. Butterfield, D. A. Beta-Amyloid-associated free radical oxidative stress and neurotoxicity: implications for Alzheimer's disease. Chemical Research in Toxicology 10(5):495-506; 1997.
26. Sultana, R.; Mecocci, P.; Mangialasche, F.; Cecchetti, R.; Baglioni, M.; Butter-field, D. A. Increased protein and lipid oxidative damage in mitochondria isolated from lymphocytes from patients with Alzheimer's disease: insights into the role of oxidative stress in Alzheimer's disease and initial investigations into a potential biomarker for this dementing disorder. Journal of Alzheimer's Disease 24(1):77-84; 2011.
27. Carbone, D. L.; Doorn, J. A.; Kiebler, Z.; Petersen, D. R. Cysteine modification by lipid peroxidation products inhibits protein disulfide isomerase. Chemical Research in Toxicology 18(8):1324-1331; 2005.
28. Niki, E. Lipid peroxidation: physiological levels and dual biological effects. Free Radical Biology and Medicine 47(5):469-484; 2009.
29. Carini, M.; Aldini, G.; Facino, R. M. Mass spectrometry for detection of 4-hydroxy-trans-2-nonenal (HNE) adducts with peptides and proteins. Mass Spectrometry Reviews 23(4):281-305; 2004.
30. Poli, G.; Dianzani, M. U.; Cheeseman, K. H.; Slater, T. F.; Lang, J.; Esterbauer, H. Separation and characterization of the aldehydic products of lipid peroxida-tion stimulated by carbon tetrachloride or ADP-iron in isolated rat hepato-cytes and rat liver microsomal suspensions. Biochemical Journal 227(2): 629-638; 1985.
31. Poli, G.; Schaur, J. R. 4-hydroxynonenal in the pathomechanisms of oxidative stress. IUBMB Life 50(4/5):315-321; 2000.
32. Subramaniam, R.; Roediger, F.; Jordan, B.; Mattson, M. P.; Keller, J. N.; Waeg, G., et al. The lipid peroxidation product, 4-hydroxy-2-trans-nonenal, alters the conformation of cortical synaptosomal membrane proteins. Journal of Neurochemistry 69(3):1161-1169; 1997.
33. Beal, M. F. Aging, energy, and oxidative stress in neurodegenerative diseases. Annals of Neurology 38(3):357-366; 1995.
34. Humphries, K. M.; Szweda, L. I. Selective inactivation of a-ketoglutarate dehydrogenase and pyruvate dehydrogenase: reaction of lipoic acid with 4-hydroxy-2-nonenal. Biochemistry 37(45):15835-15841; 1998.
35. Meier-Ruge, W.; Bertoni-Freddari, C.; Iwangoff, P. Changes in brain glucose metabolism as a key to the pathogenesis of Alzheimer's disease. Gerontology 40(5):246-252; 1994.
36. Klivenyi, P.; Starkov, A. A.; Calingasan, N. Y.; Gardian, G.; Browne, S. E.; Yang, L., et al. Mice deficient in dihydrolipoamide dehydrogenase show increased vulnerability to MPTP, malonate and 3-nitropropionic acid neurotoxicity. Journal of Neurochemistry 88(6):1352-1360; 2004.
37. Hoyer, S. Glucose metabolism and insulin receptor signal transduction in Alzheimer disease. European Journal of Pharmacology 490(1-3):115-125; 2004.
38. Manczak, M.; Park, B. S.; Jung, Y.; Reddy, P. H. Differential expression of oxidative phosphorylation genes in patients with Alzheimer's disease: implications for early mitochondrial dysfunction and oxidative damage. NeuroMolecular Medicine 5(2):147-162; 2004.
39. Wang, X.; Su, B.; Siedlak, S. L.; Moreira, P. I.; Fujioka, H.; Wang, Y., et al. Amyloid-beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proceedings of the National Academy of Sciences USA 105(49):19318-19323; 2008.
40. Aleardi, A. M.; Benard, G.; Augereau, O.; Malgat, M.; Talbot, J. C.; Mazat, J. P., et al. Gradual alteration of mitochondrial structure and function by beta-amyloids: importance of membrane viscosity changes, energy deprivation, reactive oxygen species production, and cytochrome c release. Journal of Bioenergetics and Biomembranes 37(4):207-225; 2005.
41. Perez-Gracia, E.; Torrejon-Escribano, B.; Ferrer, I. Dystrophic neurites of senile plaques in Alzheimer's disease are deficient in cytochrome c oxidase. Acta Neuropathology 116(3):261-268; 2008.
42. Kim, S. H.; Vlkolinsky, R.; Cairns, N.; Fountoulakis, M.; Lubec, G. The reduction of NADH ubiquinone oxidoreductase 24- and 75-kDa subunits in brains of patients with Down syndrome and Alzheimer's disease. Life Science 68(24):2741-2750; 2001.
43. Sultana, R.; Butterfield, D. A. Oxidatively modified, mitochondria-relevant brain proteins in subjects with Alzheimer disease and mild cognitive impairment. Journal of Bioenergetics and Biomembranes 41(5):441-446; 2009.
44. Mosconi, L. Brain glucose metabolism in the early and specific diagnosis of Alzheimer's disease. FDG-PET studies in MCI and AD. European Journal of Nuclear Medicine and Molecular Imaging 32(4):486-510; 2005.
45. Rapoport, S. I.; Hatanpaa, K.; Brady, D. R.; Chandrasekaran, K. Brain energy metabolism, cognitive function and down-regulated oxidative phosphoryla-tion in Alzheimer disease. Neurodegeneration 5(4):473-476; 1996.
46. Atamna, H.; Frey 2nd W. H. Mechanisms of mitochondrial dysfunction and energy deficiency in Alzheimer's disease. Mitochondrion 7(5):297-310; 2007.
47. Mosconi, L.; Pupi, A.; De Leon, M. J. Brain glucose hypometabolism and oxidative stress in preclinical Alzheimer's disease. Annals of the New York Academy of Sciences 1147:180-195; 2008.
48. Butterfield, D. A.; Perluigi, M.; Reed, T.; Muharib, T.; Hughes, C. P.; Robinson, R. A., et al. Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications. Antioxidants and Redox Signaling 17(11): 1610-1655; 2012.
49. Yao, J.; Irwin, R. W.; Zhao, L.; Nilsen, J.; Hamilton, R. T.; Brinton, R. D. Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proceedings of the National Academy of Sciences USA 106(34):14670-14675; 2009.
50. Korotchkina, L. G.; Yang, H. -S.; Tirosh, O.; Packer, L.; Patel, M. S. Protection by thiols of the mitochondrial complexes from 4-hydroxy-2-nonenal. Free Radical Biology and Medicine 30(9):992-999; 2001.
51. Lindsay, J. G. Targeting of 2-oxo acid dehydrogenase complexes to the mitochondriona. Annals of the New York Academy of Sciences 573(1): 254-266; 1989.
52. Hunter, A.; Lindsay, J. G. Immunological and biosynthetic studies on the mammalian 2-oxoglutarate dehydrogenase multienzyme complex. European Journal of Biochemistry 155(1):103-109; 1986.
53. Mastrogiacomo, F.; Lindsay, J. G.; Bettendorff, L.; Rice, J.; Kish, S. J. Brain protein and a-ketoglutarate dehydrogenase complex activity in Alzheimer's disease. Annals of Neurology 39(5):592-598; 1996.
54. Gibson, G. E.; Park, L. C. H.; Sheu, K. -F. R.; Blass, J. P.; Calingasan, N. Y. The a-ketoglutarate dehydrogenase complex in neurodegeneration. Neurochem-istry International 36(2):97-112; 2000.
55. Sheu, K. -F. R.; Cooper, A. J. L.; Koike, K.; Koike, M.; Lindsay, J. G.; Blass, J. P. Abnormality of the a-ketoglutarate dehydrogenase complex in fibroblasts from familial Alzheimer's disease. Annals of Neurology 35(3):312-318; 1994.
56. Brown, A. M.; Gordon, D.; Lee, H.; Caudy, M.; Hardy, J.; Haroutunian, V., et al. Association of the dihydrolipoamide dehydrogenase gene with Alzheimer's disease in an Ashkenazi Jewish population. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics 131B(1):60-66; 2004.
57. Fu, W.; Luo, H.; Parthasarathy, S.; Mattson, M. P. Catecholamines potentiate amyloid beta-peptide neurotoxicity: involvement of oxidative stress, mitochon-drial dysfunction, and perturbed calcium homeostasis. Neurobiology of Disease 5(4):229-243; 1998.
58. Gibson, G. E.; Zhang, H.; Xu, H.; Park, L. C. H.; Jeitner, T. M. Oxidative stress increases internal calcium stores and reduces a key mitochondrial enzyme. Biochimica Biophysica Acta 1586(2):177-189; 2002.
59. Smith, M. A.; Rottkamp, C. A.; Nunomura, A.; Raina, A. K.; Perry, G. Oxidative stress in Alzheimer's disease. Biochimica Biophysica Acta 1502(1):139-144; 2000.
60. Opii, W. O.; Joshi, G.; Head, E.; Milgram, N. W.; Muggenburg, B. A.; Klein, J. B., et al. Proteomic identification of brain proteins in the canine model of human aging following a long-term treatment with antioxidants and a program of behavioral enrichment: relevance to Alzheimer's disease. Neuro-biology of Aging 29(1):51-70; 2008.
61. Mancuso, C.; Bates, T. E.; Butterfield, D. A.; Calafato, S.; Cornelius, C.; Lorenzo, A. D., et al. Natural antioxidants in Alzheimer's disease. Expert Opinion on Orphan Drugs 16(12):1921-1931; 2007.
62. Yatin, S. M.; Varadarajan, S.; Butterfield, D. A. Vitamin E prevents Alzheimer's amyloid b-peptide (1-42)-induced neuronal protein oxidation and reactive oxygen species production. Journal of Alzheimer's Disease 2(2):123-131; 2000.
63. Behl, C; Moosmann, B. Antioxidant neuroprotection in Alzheimer's disease as preventive and therapeutic approach. Free Radical Biology and Medicine 33(2): 182-191; 2002.
64. Pratico, D. Evidence of oxidative stress in Alzheimer's disease brain and antioxidant therapy. Annalsof the New York Academy of Sciences 1147(l):70-78; 2008.
65. Pitchumoni, S. S.; Doraiswamy, P. M. Current status of antioxidant therapy for Alzheimer's Disease. Journal of the American Geriatrics Society 46(12): 1566-1572;1998.
66. Moreira, P. I.; Harris, P. L. R.; Zhu, X.; Santos, M. S.; Oliveira, C. R.; Smith, M. A., et al. Lipoic acid and N-acetyl cysteine decrease mitochondrial-related oxidative stress in Alzheimer disease patient fibroblasts. Journal of Alzheimer Disease 12(2):195-206; 2007.
67. Hafiz, M. A.; Butterfield, D. A. Involvement of PI3K/PKG/ERK1/2 signaling pathways in cortical neurons to trigger protection by cotreatment of acetyl-L- carnitine and a-lipoic acid against HNE-mediated oxidative stress and neurotoxicity: Implications for Alzheimer's disease. Free Radical Biology and Medicine 42(3):371-384; 2007.
68. Zhu, X.; Lee, H-g; Perry, G.; Smith, M. A. Alzheimer disease, the two-hit hypothesis: an update. Biochimica Biophysica Acta 1772(4):494-502; 2007.
69. Reddy, V. P.; Zhu, X.; Perry, G.; Smith, M. A. Oxidative stress in diabetes and Alzheimer's disease. Journal of Alzheimer Disease 16(4):763-774; 2009.
70. Nagy, Z. The last neuronal division: a unifying hypothesis for the pathogen- esis of Alzheimer's disease. Journal of Cellular and Molecular Medicine 9(3): 531-541; 2005.
71. Zhu, X.; Castellani, R. J.; Takeda, A.; Nunomura, A.; Atwood, C. S.; Perry, G., et al. Differential activation of neuronal ERK, JNK/SAPK and p38 in Alzheimer disease: the 'two hit' hypothesis. Mechanisms of Ageing and Development 123(l):39-46; 2001.
72. Zhu, X.; Raina, A. K.; Perry, G.; Smith, M. A. Alzheimer's disease: the two-hit hypothesis. Lancet Neurology 3(4):219-226; 2004.