The effects and mechanisms of mitochondrial nutrient α-lipoic acid on improving age-associated mitochondrial and cognitive dysfunction: An overview

Neurochemical Research

Volumn 33, Issue 1, 2008, Pages 194-203

  Liu, Jiankang ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alpha lipoic acid; Cognitive function; Mitochondrial dysfunction; Oxidative damage

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; CARNITINE; CHOLINE; GLUTAMIC ACID; LEVACECARNINE; MENADIONE; MITOCHONDRIAL ENZYME; NICOTINAMIDE; NICOTINIC ACID; OXIDIZING AGENT; RIBOFLAVIN; THIAMINE; THIOCTIC ACID; UBIDECARENONE;

ALZHEIMER DISEASE; BRAIN DISEASE; CELL FUNCTION; CELL STRUCTURE; CLINICAL FEATURE; COGNITIVE DEFECT; DEGENERATIVE DISEASE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; DRUG SCREENING; ENCEPHALOMYOPATHY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; MEMORY; MICHAELIS CONSTANT; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MYOPATHY; MORTALITY; MUSCLE WEAKNESS; NONHUMAN; NUTRIENT; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; TREATMENT OUTCOME;

AGING; ANIMALS; COGNITION DISORDERS; HUMANS; MITOCHONDRIA; THIOCTIC ACID;

EID: 36949012725     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-007-9403-0     Document Type: Review

References (100)

1. Ames BN (2003) Delaying the mitochondrial decay of aging-a metabolic tune-up. Alzheimer Dis Assoc Disord 17(Suppl 2):S54-S57
2. Ames BN, Shigenaga MK, Hagen TM (1995) Mitochondrial decay in aging. Biochim Biophys Acta 1271:165-170
3. Ames BN, Shigenaga MK, Hagen TM (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 90:7915-7922
4. Shigenaga MK, Hagen TM, Ames BN (1994) Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci USA 91:10771-10778
5. Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547-581
6. Harman D (2002) Increasing healthy life span. The New York Academy of Sciences, New York
7. Roubertoux PL, Sluyter F, Carlier M, Marcet B, Maarouf-Veray F, Cherif C, Marican C, Arrechi P, Godin F, Jamon M et al (2003) Mitochondrial DNA modifies cognition in interaction with the nuclear genome and age in mice. Nat Genet 35:65-69
8. Tritschler HJ, Packer L, Medori R (1994) Oxidative stress and mitochondrial dysfunction in neurodegeneration. Biochem Mol Biol Int 34:169-181
9. Beal MF (1992) Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann Neurol 31:119-130
10. Liu J, Mori A (1999) Stress, aging, and brain oxidative damage. Neurochem Res 24:1479-1497
11. Albers DS, Beal MF (2000) Mitochondrial dysfunction and oxidative stress in aging and neurodegenerative disease. J Neural Transm Suppl 59:133-154
12. Aliev G, Smith MA, Seyidov D, Neal ML, Lamb BT, Nunomura A, Gasimov EK, Vinters HV, Perry G, LaManna JC et al (2002) The role of oxidative stress in the pathophysiology of cerebrovascular lesions in Alzheimer's disease. Brain Pathol 12:21-35
13. Rao AV, Balachandran B (2002) Role of oxidative stress and antioxidants in neurodegenerative diseases. Nutr Neurosci 5:291-309
14. Perry G, Nunomura A, Friedlich AL, Boswell MV et al (2000) Factors controlling oxidative damage in Alzheimer disease: metals and mitochondria. In: Yoshikawa T, Toyokuni S, Yamamato Y, Naito Y (eds) Free radicals in chemistry, biology and medicine. OICA International, London, pp 417-423
15. Beal MF (2003) Bioenergetic approaches for neuroprotection in Parkinson's disease. Ann Neurol 53(Suppl 3):S39-S47; discussion S47-S-38
16. Butterfield D, Castegna A, Pocernich C, Drake J, Scapagnini G, Calabrese V (2002) Nutritional approaches to combat oxidative stress in Alzheimer's disease. J Nutr Biochem 13:444
17. Butterfield DA, Castegna A, Drake J, Scapagnini G, Calabrese V (2002) Vitamin E and neurodegenerative disorders associated with oxidative stress. Nutr Neurosci 5:229-239
18. Marriage B, Clandinin MT, Glerum DM (2003) Nutritional cofactor treatment in mitochondrial disorders. J Am Diet Assoc 103:1029-1038
19. McDaniel MA, Maier SF, Einstein GO (2003) "Brain-specific" nutrients: a memory cure? Nutrition 19:957-975
20. Baker SK, Tarnopolsky MA (2003) Targeting cellular energy production in neurological disorders. Expert Opin Investig Drugs 12:1655-1679
21. Black MM (2003) Micronutrient deficiencies and cognitive functioning. J Nutr 133:3927S-3931S
22. Price MC (2002) Longevity Report 91: the role of enzymic cofactors in aging. Available at: http://www.quantium.cwe.net/lr91.htm#_Toc22709815
23. Moini H, Packer L, Saris NE (2002) Antioxidant and prooxidant activities of alpha-lipoic acid and dihydrolipoic acid. Toxicol Appl Pharmacol 182:84-90
24. Packer L, Roy S, Sen CK (1997) Alpha-lipoic acid: a metabolic antioxidant and potential redox modulator of transcription. Adv Pharmacol 38:79-101
25. Packer L, Tritschler HJ, Wessel K (1997) Neuroprotection by the metabolic antioxidant α-lipoic acid. Free Radic Biol Med 22:359-378
26. Packer L, Witt EH, Tritschler HJ (1995) Alpha-lipoic acid as a biological antioxidant. Free Radic Biol Med 19:227-250
27. Bustamante J, Lodge JK, Marcocci L, Tritschler HJ, Packer L, Rihn BH (1998) Alpha-lipoic acid in liver metabolism and disease. Free Radic Biol Med 24:1023-1039
28. Fuchs J, Packer L, Zimmer G (1997) Lipoic acid in health and disease. Marcel Dekker Inc, New York
29. Sen CK, Roy S, Khanna S, Packer L (1999) Determination of oxidized and reduced lipoic acid using high- performance liquid chromatography and coulometric detection. Methods Enzymol 299:239-246
30. Ou P, Tritschler HJ, Wolff SP (1995) Thioctic (lipoic) acid: a therapeutic metal-chelating antioxidant? Biochem Pharmacol 50:123-126
31. Hagen TM, Ingersoll RT, Lykkesfeldt J, Liu J, Wehr CM, Vinarsky V, Bartholomew JC, Ames AB (1999) (R)-alpha-lipoic acid-supplemented old rats have improved mitochondrial function, decreased oxidative damage, and increased metabolic rate. FASEB J 13:411-418
32. Hagen TM, Vinarsky V, Wehr CM, Ames BN (2000) (R)-alpha-lipoic acid reverses the age-associated increase in susceptibility of hepatocytes to tert-butylhydroperoxide both in vitro and in vivo. Antioxid Redox Signal 2:473-483
33. Suh JH, Shigeno ET, Morrow JD, Cox B, Rocha AE, Frei B, Hagen TM (2001) Oxidative stress in the aging rat heart is reversed by dietary supplementation with (R)-(alpha)-lipoic acid. FASEB J 15:700-706
34. Harman D (1972) The biologic clock: the mitochondria? J Am Geriatr Soc 20:145-147
35. Hagen TM, Ingersoll RT, Wehr CM, Lykkesfeldt J, Vinarsky V, Bartholomew JC, Song MH, Ames BN (1998) Acetyl-l-carnitine fed to old rats partially restores mitochondrial function and ambulatory activity. Proc Natl Acad Sci USA 95:9562-9566
36. Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273:59-63
37. Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222-230
38. Stadtman ER, Levine RL (2000) Protein oxidation. Ann N Y Acad Sci 899:191-208
39. Chen JJ, Yu BP (1994) Alterations in mitochondrial membrane fluidity by lipid peroxidation products. Free Radic Biol Med 17:411-418
40. Choi JH, Yu BP (1995) Brain synaptosomal aging: free radicals and membrane fluidity. Free Radic Biol Med 18:133-139
41. Paradies G, Ruggiero FM, Petrosillo G, Gadaleta MN, Quagliariello E (1994) Effect of aging and acetyl-l-carnitine on the activity of cytochrome oxidase and adenine nucleotide translocase in rat heart mitochondria. FEBS Lett 350:213-215
42. Stoll S, Hartmann H, Cohen SA, Muller WE (1993) The potent free radical scavenger alpha-lipoic acid improves memory in aged mice: putative relationship to NMDA receptor deficits. Pharmacol Biochem Behav 46:799-805
43. Farr SA, Poon HF, Dogrukol-Ak D, Drake J, Banks WA, Eyerman E, Butterfield DA, Morley JE (2003) The antioxidants alpha-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice. J Neurochem 84:1173-1183
44. Poon HF, Farr SA, Thongboonkerd V, Lynn BC, Banks WA, Morley JE, Klein JB, Butterfield DA (2005) Proteomic analysis of specific brain proteins in aged SAMP8 mice treated with alpha-lipoic acid: implications for aging and age-related neurodegenerative disorders. Neurochem Int 46:159-168
45. Poon HF, Frasier M, Shreve N, Calabrese V, Wolozin B, Butterfield DA (2005) Mitochondrial associated metabolic proteins are selectively oxidized in A30P alpha-synuclein transgenic mice-a model of familial Parkinson's disease. Neurobiol Dis 18:492-498
46. Cui X, Zuo P, Zhang Q, Li X, Hu Y, Long J, Packer L, Liu J (2006) Chronic systemic d-galactose exposure induces memory loss, neurodegeneration, and oxidative damage in mice: protective effects of R-alpha-lipoic acid. J Neurosci Res 83:1584-1590
47. Quinn JF, Bussiere JR, Hammond RS, Montine TJ, Henson E, Jones RE, Stackman RW Jr (2007) Chronic dietary alpha-lipoic acid reduces deficits in hippocampal memory of aged Tg2576 mice. Neurobiol Aging 28:213-225
48. Manda K, Ueno M, Moritake T, Anzai K (2007) Radiation-induced cognitive dysfunction and cerebellar oxidative stress in mice: protective effect of alpha-lipoic acid. Behav Brain Res 177:7-14
49. Evans JL, Goldfine ID (2000) Alpha-lipoic acid: a multifunctional antioxidant that improves insulin sensitivity in patients with type 2 diabetes. Diabetes Technol Ther 2:401-413
50. Ziegler D, Gries FA (1997) Alpha-lipoic acid in the treatment of diabetic peripheral and cardiac autonomic neuropathy. Diabetes 46(Suppl 2):S62-S66
51. Sharma M, Gupta YK (2003) Effect of alpha lipoic acid on intracerebroventricular streptozotocin model of cognitive impairment in rats. Eur Neuropsychopharmacol 13:241-247
52. Schreibelt G, Musters RJ, Reijerkerk A, de Groot LR, van der Pol SM, Hendrikx EM, Dopp ED, Dijkstra CD, Drukarch B, de Vries HE (2006) Lipoic acid affects cellular migration into the central nervous system and stabilizes blood-brain barrier integrity. J Immunol 177:2630-2637
53. Holmguist L, Stuchbury G, Berbaum K, Muscat S, Young S, Hager K, Engel J, Munch G (2007) Lipoic acid as a novel treatment for Alzheimer's disease and related dementias. Pharmacol Ther113:154-164
54. Arivazhagan P, Ayusawa D, Panneerselvam C (2006) Protective efficacy of alpha-lipoic acid on acetylcholinesterase activity in aged rat brain regions. Rejuvenation Res 9:198-201
55. Arivazhagan P, Panneerselvam C (2004) Alpha-lipoic acid increases Na + K + ATPase activity and reduces lipofuscin accumulation in discrete brain regions of aged rats. Ann N Y Acad Sci 1019:350-354
56. Zhang L, Xing GQ, Barker JL, Chang Y, Maric D, Ma W, Li BS, Rubinow DR (2001) Alpha-lipoic acid protects rat cortical neurons against cell death induced by amyloid and hydrogen peroxide through the Akt signalling pathway. Neurosci Lett 312:125-128
57. Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634
58. Choi DW (1992) Excitotoxic cell death. J Neurobiol 23:1261-1276
59. Dumuis A, Sebben M, Haynes L, Pin JP, Bockaert J (1988) NMDA receptors activate the arachidonic acid cascade system in striatal neurons. Nature 336:68-70
60. Lafon CM, Pietri S, Culcasi M, Bockaert J (1993) NMDA-dependent superoxide production and neurotoxicity. Nature 364:535-537
61. Henneberry RC, Novelli A, Cox JA, Lysko PG (1989) Neurotoxicity at the N-methyl-d-aspartate receptor in energy-compromised neurons. An hypothesis for cell death in aging and disease. Ann N Y Acad Sci 568:225-233
62. Morimoto BH, Koshland DE Jr (1990) Excitatory amino acid uptake and N-methyl-d-aspartate-mediated secretion in a neural cell line. Proc Natl Acad Sci USA 87:3518-3521
63. Liu J, Atamna H, Kuratsune H, Ames BN (2002) Delaying brain mitochondrial decay and aging with mitochondrial antioxidants and metabolites. Ann N Y Acad Sci 959:133-166
64. Tirosh O, Sen CK, Roy S, Packer L (2000) Cellular and mitochondrial changes in glutamate-induced HT4 neuronal cell death. Neuroscience 97:531-541
65. Wolz P, Krieglstein J (1996) Neuroprotective effects of alpha-lipoic acid and its enantiomers demonstrated in rodent models of focal cerebral ischemia. Neuropharmacology 35:369-375
66. Marangon K, Devaraj S, Tirosh O, Packer L, Jialal I (1999) Comparison of the effect of alpha-lipoic acid and alpha-tocopherol supplementation on measures of oxidative stress. Free Radic Biol Med 27:1114-1121
67. Aksenova MV, Aksenov MY, Carney JM, Butterfield DA (1998) Protein oxidation and enzyme activity decline in old brown Norway rats are reduced by dietary restriction. Mech Ageing Dev 100:157-168
68. Suh JH, Moreau R, Heath SH, Hagen TM (2005) Dietary supplementation with (R)-alpha-lipoic acid reverses the age-related accumulation of iron and depletion of antioxidants in the rat cerebral cortex. Redox Rep 10:52-60
69. Gao X, Dinkova-Kostova AT, Talalay P (2001) Powerful and prolonged protection of human retinal pigment epithelial cells, keratinocytes, and mouse leukemia cells against oxidative damage: the indirect antioxidant effects of sulforaphane. Proc Natl Acad Sci USA 98:15221-15226
70. Satoh T, Okamoto SI, Cui J, Watanabe Y, Furuta K, Suzuki M, Tohyama K, Lipton SA (2006) Activation of the Keap1/Nrf2 pathway for neuroprotection by electrophilic [correction of electrophillic] phase II inducers. Proc Natl Acad Sci USA 103:768-773
71. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, Kensler TW (2001) Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA 98:3410-3415
72. Smith AR, Shenvi SV, Widlansky M, Suh JH, Hagen TM (2004) Lipoic acid as a potential therapy for chronic diseases associated with oxidative stress. Curr Med Chem 11:1135-1146
73. Reznick RM, Shulman GI (2006) The role of AMP-activated protein kinase in mitochondrial biogenesis. J Physiol 574:33-39
74. Hardie DG (2004) AMP-activated protein kinase: a key system mediating metabolic responses to exercise. Med Sci Sports Exerc 36:28-34
75. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, Sciorati C, Bracale R, Valerio A, Francolini M, Moncada S et al (2003) Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299:896-899
76. Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, Bassel-Duby R, Williams RS (2002) Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296:349-352
77. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC et al (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115-124
78. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, Handschin C, Zheng K, Lin J, Yang W et al (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397-408
79. Cui L, Jeong H, Borovecki F, Parkhurst CN, Tanese N, Krainc D (2006) Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127:59-69
80. Prasad KN, Cole WC, Prasad KC (2002) Risk factors for Alzheimer's disease: role of multiple antioxidants, non-steroidal anti-inflammatory and cholinergic agents alone or in combination in prevention and treatment. J Am Coll Nutr 21:506-522
81. Hongu N, Sachan DS (2000) Caffeine, carnitine and choline supplementation of rats decreases body fat and serum leptin concentration as does exercise. J Nutr 130:152-157
82. Gonzalez-Perez O, Gonzalez-Castaneda RE, Huerta M, Luquin S, Gomez-Pinedo U, Sanchez-Almaraz E, Navarro-Ruiz A, Garcia-Estrada J (2002). Beneficial effects of alpha-lipoic acid plus vitamin E on neurological deficit, reactive gliosis and neuronal remodeling in the penumbra of the ischemic rat brain. Neurosci Lett 321:100-104
83. Hagen TM, Liu J, Lykkesfeldt J, Wehr CM, Ingersoll RT, Vinarsky V, Bartholomew JC, Ames BN (2002) Feeding acetyl-l-carnitine and lipoic acid to old rats significantly improves metabolic function while decreasing oxidative stress. Proc Natl Acad Sci USA 99:1870-1875
84. Liu J, Head E, Gharib AM, Yuan W, Ingersoll RT, Hagen TM, Cotman CW, Ames BN (2002) Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: Partial reversal by feeding acetyl-l-carnitine and/or R-alpha-lipoic acid. Proc Natl Acad Sci USA 99:2356-2361
85. Liu J, Killilea DW, Ames BN (2002) Age-associated mitochondrial oxidative decay: improvement of carnitine acetyltransferase substrate-binding affinity and activity in brain by feeding old rats acetyl-l-carnitine and/or R-alpha-lipoic acid. Proc Natl Acad Sci USA 99:1876-1881
86. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60
87. Gharib A, Derby S, Roberts S (2001) Timing and the control of variation. J Exp Psychol Anim Behav Process 27:165-178
88. Muthuswamy AD, Vedagiri K, Ganesan M, Chinnakannu P (2006) Oxidative stress-mediated macromolecular damage and dwindle in antioxidant status in aged rat brain regions: role of l-carnitine and dl-alpha-lipoic acid. Clin Chim Acta 368:84-92
89. Abdul HM, Butterfield DA (2007) Involvement of PI3K/PKG/ERK1/2 signaling pathways in cortical neurons to trigger protection by cotreatment of acetyl-l-carnitine and alpha-lipoic acid against HNE-mediated oxidative stress and neurotoxicity: implications for Alzheimer's disease. Free Radic Biol Med 42:371-384
90. Kozlov AV, Gille L, Staniek K, Nohl H (1999) Dihydrolipoic acid maintains ubiquinone in the antioxidant active form by two-electron reduction of ubiquinone and one-electron reduction of ubisemiquinone. Arch Biochem Biophys 363:148-154
91. Milgram NW, Head E, Zicker SC, Ikeda-Douglas CJ, Murphey H, Muggenburg B, Siwak C, Tapp D, Cotman CW (2005) Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: a two-year longitudinal study. Neurobiol Aging 26:77-90
92. Opii WO, Joshi G, Head E, Milgram NW, Muggenburg BA, Klein JB, Pierce WM, Cotman CW, Butterfield DA (2006) 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. Neurobiol Aging, doi: 10.1016/j.neurobiolaging.2006.09.012
93. Kayali R, Cakatay U, Akcay T, Altug T (2006) Effect of alpha-lipoic acid supplementation on markers of protein oxidation in post-mitotic tissues of ageing rat. Cell Biochem Funct 24:79-85
94. Tirosh O, Sen CK, Roy S, Kobayashi MS, Packer L (1999) Neuroprotective effects of alpha-lipoic acid and its positively charged amide analogue. Free Radic Biol Med 26:1418-1426
95. Korotchkina LG, Yang H, Tirosh O, Packer L, Patel MS (2001) Protection by thiols of the mitochondrial complexes from 4-hydroxy-2-nonenal. Free Radic Biol Med 30:992-999
96. Guo Q, Tirosh O, Packer L (2001) Inhibitory effect of alpha-lipoic acid and its positively charged amide analogue on nitric oxide production in RAW 264.7 macrophages. Biochem Pharmacol 61:547-554
97. Venkatachalam SR, Salaskar A, Chattopadhyay A, Barik A, Mishra B, Gangabhagirathi R, Priyadarsini KI (2006) Synthesis, pulse radiolysis, and in vitro radioprotection studies of melatoninolipoamide, a novel conjugate of melatonin and alpha-lipoic acid. Bioorg Med Chem 14:6414-6419
98. Dixit V, Van den Bossche J, Sherman DM, Thompson DH, Andres RP (2006) Synthesis and grafting of thioctic acid-PEG-folate conjugates onto Au nanoparticles for selective targeting of folate receptor-positive tumor cells. Bioconjug Chem 17:603-609
99. Di Stefano A, Sozio P, Cocco A, Iannitelli A, Santucci E, Costa M, Pecci L, Nasuti C, Cantalamessa F, Pinnen F (2006) l-dopa- and dopamine-(R)-alpha- lipoic acid conjugates as multifunctional codrugs with antioxidant properties. J Med Chem 49:1486-1493
100. Biessels GJ, Smale S, Duis SE, Kamal A, Gispen WH (2001) The effect of gamma-linolenic acid-alpha-lipoic acid on functional deficits in the peripheral and central nervous system of streptozotocin-diabetic rats. J Neurol Sci 182:99-106