How aluminum, an intracellular ROS generator promotes hepatic and neurological diseases: The metabolic tale

Cell Biology and Toxicology

Volumn 29, Issue 2, 2013, Pages 75-84

  Han, Sungwon ^a   Lemire, Joseph ^b   Appanna, Varun P ^a   Auger, Christopher ^a   Castonguay, Zachary ^a   Appanna, Vasu D ^a  

^a LAURENTIAN UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

ketoacids; Aluminum toxicity; Dyslipidemia; Mitochondrial dysfunction; Neurological and hepatic diseases; Reactive oxygen species

Indexed keywords

2 OXOACID; ADENOSINE TRIPHOSPHATE; ALUMINUM; CARNITINE; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; SUCCINIC ACID;

ASTROCYTE; BIOSYNTHESIS; CELL METABOLISM; DISEASE ASSOCIATION; DRUG MECHANISM; ENERGY METABOLISM; ENVIRONMENTAL EXPOSURE; HUMAN; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIVER CELL; LIVER DISEASE; MITOCHONDRIAL RESPIRATION; MOLECULAR PATHOLOGY; NEUROLOGIC DISEASE; NONHUMAN; OSTEOMALACIA; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ALUMINUM; ASTROCYTES; DRUG-INDUCED LIVER INJURY; DYSLIPIDEMIAS; ENVIRONMENTAL EXPOSURE; HEPATOCYTES; HUMANS; LIPID METABOLISM; LIPOGENESIS; LIVER DISEASES; MITOCHONDRIA; MITOCHONDRIAL DISEASES; NERVOUS SYSTEM DISEASES; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84879463709     PISSN: 07422091     EISSN: 15736822     Source Type: Journal    
DOI: 10.1007/s10565-013-9239-0     Document Type: Review

References (85)

1. Adibhatla RM, Hatcher JF. Altered lipid metabolism in brain injury and disorders lipids in health and disease. In: Quinn PJ, Wang X, editors. Springer, Dordrecht; 2008.
2. Barnard CG, McBride DI, Firth HM, Herbison GP. Assessing individual employee risk factors for occupational asthma in primary aluminium smelting. Occup Environ Med. 2004;61:604-8. (Pubitemid 38869593)
3. Becaria A, Lahiri DK, Bondy SC, Chen D, Hamadeh A, Li H, et al. Aluminum and copper in drinking water enhance inflammatory or oxidative events specifically in the brain. J Neuroimmunol. 2006;176:16-23. (Pubitemid 44080334)
4. Bhasin P, Singla N, Dhawan DK. Protective role of zinc during aluminum-induced hepatotoxicity. Environ Toxicol. 2012. doi: 10.1002/tox.21760.
5. Bignucolo A, Lemire J, Auger C, Castonguay Z, Appanna V, Appanna VD. The molecular connection between aluminum toxicity, anemia, inflammation and obesity: therapeutic cues. In: Silverberg DD, editor. Anemia: InTech; 2012.
6. Bosetti F, Solaini G, Tendi EA, Chikhale EG, Chandrasekaran K, Rapoport SI. Mitochondrial cytochrome c oxidase subunit III is selectively down-regulated by aluminum exposure in PC12S cells. Neuroreport. 2001;12:721-4. (Pubitemid 32222705)
7. Buchman AL, Iyer K, Fryer J. Parenteral nutrition-associated liver disease and the role for isolated intestine and intestine/liver transplantation. Hepatology. 2006;43:9-19. (Pubitemid 43733585)
8. Candan N, Tuzmen N. Very rapid quantification of malondialdehyde (MDA) in rat brain exposed to lead, aluminium and phenolic antioxidants by high-performance liquid chromatography-fluorescence detection. Neurotoxicology. 2008;29:708-13.
9. Christen Y. Oxidative stress and Alzheimer disease. Am J Clin Nutr. 2000;71:621s-9s. (Pubitemid 30061247)
10. Cuajungco MP, Faget KY, Huang X, Tanzi RE, Bush AI. Metal chelation as a potential therapy for Alzheimer's disease. Ann N Y Acad Sci. 2000;920:292-304. (Pubitemid 32056584)
11. De Marchi U, Mancon M, Battaglia V, Ceccon S, Cardellini P, Toninello A. Influence of reactive oxygen species production by monoamine oxidase activity on aluminum-induced mitochondrial permeability transition. Cell Mol Life Sci. 2004;61:2664-71. (Pubitemid 39586526)
12. Exley C. A biogeochemical cycle for aluminium? J Inorg Biochem. 2003;97:1-7. (Pubitemid 37152405)
13. Exley C. Darwin, natural selection and the biological essentiality of aluminium and silicon. Trends Biochem Sci. 2009;34:589-93.
14. Ferreira PC, Piai KdA, Takayanagui AMM, Segura-Muñoz SI. Aluminum as a risk factor for Alzheimer's disease. Rev Lat Am Enfermagem. 2008;16:151-7.
15. Ferretti G, Marchionni C, Bacchetti T, Galeazzi T, Dousset N. Effect of aluminium on lipid peroxidation of human high density lipoproteins. Free Radic Res. 2003;37:515-21. (Pubitemid 36410892)
16. Flaten TP. Aluminium as a risk factor in Alzheimer's disease, with emphasis on drinking water. Brain Res Bull. 2001;55:187-96. (Pubitemid 32722158)
17. Ganz T. Hepcidin and iron regulation, 10 years later. Blood. 2011;117:4425-33.
18. Gao X, Wu J, Dong Z, Hua C, Hu H, Mei C. A low-protein diet supplemented with ketoacids plays a more protective role against oxidative stress of rat kidney tissue with 5/6 nephrectomy than a low-protein alone. Br J Nutr. 2009;103:608-16.
19. Gómez M, Esparza JL, Cabré M, García T, Domingo JL. Aluminum exposure through the diet: metal levels in Amyloid βPP transgenic mice, a model for Alzheimer's disease. Toxicology. 2008;249:214-9.
20. González M, Bernal C, Mahieu S, Carrillo M. The interactions between the chronic exposure to aluminum and liver regeneration on bile flow and organic anion transport in rats. Biol Trace Elem Res. 2009;127:164-76.
21. Gorell JM, Peterson EL, Rybicki BA, Johnson CC. Multiple risk factors for Parkinson's disease. J Neurol Sci. 2004;217:169-74. (Pubitemid 38056551)
22. Guo C-H, Hsu G-SW, Chuang C-J, Chen P-C. Aluminum accumulation induced testicular oxidative stress and altered selenium metabolism in mice. Environ Toxicol Pharmacol. 2009;27:176-81.
23. Gura KM. Aluminum contamination in products used in parenteral nutrition: has anything changed? Nutrition. 2010;26:585-94.
24. Harris WR, Berthon G, Day JP, Exley C, Pender T, William F, et al. Speciation of aluminium in biological systems. J Toxicol Environ Health. 1996;48:543-68. (Pubitemid 26285831)
25. Hegde KR, Kovtun S, Varma SD. Induction of ultraviolet cataract in vitro: prevention by pyruvate. J Ocul Pharmacol Ther. 2007;23:492-502. (Pubitemid 350202481)
26. Hung Y, Bush A, Cherny R. Copper in the brain and Alzheimer's disease. J Biol Inorg Chem. 2010;15:61-76.
27. Jeffery EH, Abreo K, Burgess E, Cannata J, Greger JL. Systemic aluminum toxicity: effects on bone, hematopoietic tissue and kidney. J Toxicol Environ Health. 1996;48:649-66. (Pubitemid 26285837)
28. Kaizer RR, Corrêa MC, Spanevello RM, Morsch VM, Mazzanti CM, Gonçalves JF, et al. Acetylcholinesterase activation and enhanced lipid peroxidation after long-term exposure to low levels of aluminum on different mouse brain regions. J Inorg Biochem. 2005;99:1865-70. (Pubitemid 41253775)
29. Kaneko N, Yasui H, Takada J, Suzuki K, Sakurai H. Orally administrated aluminum-maltolate complex enhances oxidative stress in the organs of mice. J Inorg Biochem. 2004;98:2022-31. (Pubitemid 39488134)
30. Kaneko N, Sugioka T, Sakurai H. Aluminum compounds enhance lipid peroxidation in liposomes: Insight into cellular damage caused by oxidative stress. J Inorg Biochem. 2007;101:967-75. (Pubitemid 46770853)
31. Kaur A, Joshi K, Minz RW, Gill KD. Neurofilament phosphorylation and disruption: a possible mechanism of chronic aluminium toxicity in Wistar rats. Toxicology. 2006;219:1-10. (Pubitemid 43120701)
32. Kawahara M, Kato-Negishi M. Link between aluminum and the pathogenesis of Alzheimer's disease: the integration of the aluminum and Amyloid cascade hypothesis. Int J Alzheimer's Dis. 2011; 276393.
33. Kjellman UW, Björk K, Ekroth R, Karlsson H, Jagenburg R, Nilsson FN, et al. Addition of α-ketoglutarate to blood cardioplegia improves cardioprotection. Ann Thorac Surg. 1997;63:1625-33. (Pubitemid 27321526)
34. Klein GL. Aluminum: new recognition of an old problem. Curr Opin Pharmacol. 2005;5:637-40. (Pubitemid 41614465)
35. Krewski D, Yokel RA, Nieboer E, Borchelt D, Cohen J, Harry J, et al. Human health risk assessment for aluminium, aluminium oxide, and aluminium hydroxide. J Toxicol Environ Health B. 2007;10:1-269.
36. Kumar V, Bal A, Gill KD. Impairment of mitochondrial energy metabolism in different regions of rat brain following chronic exposure to aluminium. Brain Res. 2008;1232:94-103.
37. Kumar V, Bal A, Gill KD. Susceptibility of mitochondrial superoxide dismutase to aluminium induced oxidative damage. Toxicology. 2009;255:117-23.
38. Lemire J. A global metabolic perspective on aluminum toxicity in human astrocytes: Implications for neurological disorders. Ph.D, Laurentian University; 2011.
39. Lemire J, Mailloux R, Puiseux-Dao S, Appanna VD. Aluminum-induced defective mitochondrial metabolism perturbs cytoskeletal dynamics in human astrocytoma cells. J Neurosci Res. 2009;87:1474-83.
40. Lemire J, Mailloux R, Darwich R, Auger C, Appanna VD. The disruption of l-carnitine metabolism by aluminum toxicity and oxidative stress promotes dyslipidemia in human astrocytic and hepatic cells. Toxicol Lett. 2011;203:219-26.
41. Li J, Bosch-Marce M, Nanayakkara A, Savransky V, Fried SK, Semenza GL, et al. Altered metabolic responses to intermittent hypoxia in mice with partial deficiency of hypoxia-inducible factor-1α. Physiol Genomics. 2006;25:450-7. (Pubitemid 43764766)
42. Li X, Han Y, Guan Y, Zhang L, Bai C & Li Y. Aluminum induces osteoblast apoptosis through the oxidative stress-mediated jnk signaling pathway. Biol Trace Elem Res. 2012; 1-7.
43. Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR. Copper, iron and zinc in Alzheimer's disease senile plaques. J Neurol Sci. 1998;158:47-52. (Pubitemid 28277534)
44. Lukiw WJ, Pogue AI. Induction of specific micro RNA (miRNA) species by ROS-generating metal sulfates in primary human brain cells. J Inorg Biochem. 2007;101:1265-9. (Pubitemid 47313522)
45. Lukiw WJ, Percy ME, Kruck TP. Nanomolar aluminum induces pro-inflammatory and pro-apoptotic gene expression in human brain cells in primary culture. J Inorg Biochem. 2005;99:1895-8. (Pubitemid 41253779)
46. Mailloux RJ, Appanna VD. Aluminum toxicity triggers the nuclear translocation of HIF-1α and promotes anaerobiosis in hepatocytes. Toxicol In Vitro. 2007;21:16-24. (Pubitemid 44855508)
47. Mailloux RJ, Hamel R, Appanna VD. Aluminum toxicity elicits a dysfunctional TCA cycle and succinate accumulation in hepatocytes. J Biochem Mol Toxicol. 2006;20:198-208. (Pubitemid 44384710)
48. Mailloux R, Lemire J, Appanna V. Aluminum-induced mitochondrial dysfunction leads to lipid accumulation in human hepatocytes: a link to obesity. Cell Physiol Biochem. 2007;20:627-38. (Pubitemid 47340623)
49. Mailloux RJ, Puiseux-Dao S, Appanna VD. α-ketoglutarate abrogates the nuclear localization of HIF-1α in aluminum-exposed hepatocytes. Biochimie. 2009;91:408-15.
50. Mailloux RJ, Lemire J, Appanna VD. Hepatic response to aluminum toxicity: dyslipidemia and liver diseases. Exp Cell Res. 2011;317:2231-8.
51. Mallet RT, Sun J, Knott EM, Sharma AB, Olivencia-Yurvati AH. Metabolic cardioprotection by pyruvate: recent progress. Exp Biol Med. 2005;230:435-43. (Pubitemid 40923420)
52. Middaugh J, Hamel R, Jean-Baptiste G, Beriault R, Chenier D, Appanna VD. Aluminum triggers decreased aconitase activity via Fe-S cluster disruption and the overexpression of isocitrate dehydrogenase and isocitrate lyase: a metabolic network mediating cellular survival. J Biol Chem. 2005;280:3159-65. (Pubitemid 40223777)
53. Moulin JJ, Clavel T, Buclez B, Laffitte-Rigaud G. A mortality study among workers in a French aluminium reduction plant. Int Arch Occup Environ Health. 2000;73:323-30. (Pubitemid 30487384)
54. Nakamura H, Rose P, Blumer J, Reed M. Acute encephalopathy due to aluminum toxicity successfully treated by combined intravenous deferoxamine and hemodialysis. J Clin Pharmacol. 2000;40:296-300.
55. Nayak P. Aluminum: impacts and disease. Environ Res. 2002;89:101-15. (Pubitemid 34680879)
56. Nayak P, Sharma SB, Chowdary NV. Augmentation of aluminum-induced oxidative stress in rat cerebrum by presence of pro-oxidant (graded doses of ethanol) exposure. Neurochem Res. 2010;35:1681-90.
57. Nehru B, Anand P. Oxidative damage following chronic aluminium exposure in adult and pup rat brains. J Trace Elem Med Biol. 2005;19:203-8. (Pubitemid 41606717)
58. Nehru B, Bhalla P. Reversal of an aluminium induced alteration in redox status in different regions of rat brain by administration of centrophenoxine. Mol Cell Biochem. 2006;290:185-91. (Pubitemid 44473250)
59. Ohyashiki T, Satoh E, Okada M, Takadera T, Sahara M. Nerve growth factor protects against aluminum-mediated cell death. Toxicology. 2002;176:195-207. (Pubitemid 34686960)
60. Peto MV. Aluminum and iron in humans: bioaccumulation, pathology and removal. Rejuvenation Res. 2010;13:589-98.
61. Petzold GC, Murthy VN. Role of astrocytes in neurovascular coupling. Neuron. 2011;71:782-97.
62. Praticò D, Uryu K, Sung S, Tang S, Trojanowski J. Q. & Lee V. M.-Y. Aluminum modulates brain amyloidosis through oxidative stress in APP transgenic mice. The FASEB Journal. 2002. 16, 1138-1140
63. Priest ND. The biological behaviour and bioavailability of aluminium in man, with special reference to studies employing aluminium-26 as a tracer: review and study update. J Environ Monit. 2004;6:375-403. (Pubitemid 38716532)
64. Reichenbach A, Wolburg H. Structural association of astrocytes with neurons and vasculature: defining territorial boundaries astrocytes in (patho)physiology of the nervous system. In: Haydon PG, Parpura V, editors. New York: Springer; 2009.
65. Richards SA, Muter J, Ritchie P, Lattanzi G, Hutchison CJ. The accumulation of un-repairable DNA damage in laminopathy progeria fibroblasts is caused by ROS generation and is prevented by treatment with N-acetyl cysteine. Hum Mol Genet. 2011;20:3997-4004.
66. Romundstad P, Haldorsen T, Andersen A. Lung and bladder cancer among workers in a Norwegian aluminium reduction plant. Occup Environ Med. 2000;57:495-9. (Pubitemid 30410713)
67. Rondeau V, Commenges D, Jacqmin-Gadda H, Dartigues J-F. Relation between aluminum concentrations in drinking water and Alzheimer's disease: an 8-year follow-up study. Am J Epidemiol. 2000;152:59-66. (Pubitemid 30637398)
68. Rondeau V, Jacqmin-Gadda H, Commenges D, Helmer C, Dartigues J-F. Aluminum and silica in drinking water and the risk of alzheimer's disease or cognitive decline: findings from 15-year follow-up of the PAQUID Cohort. Am J Epidemiol. 2009;169:489-96.
69. Rosenlöf K, Fyhrquist F, Tenhunen R. Erythropoietin, aluminium, and anaemia in patients on haemodialysis. Lancet. 1990;335:247-9. (Pubitemid 20047711)
70. Rouault TA, Tong W-H. Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat Rev Mol Cell Biol. 2005;6:345-51. (Pubitemid 40516901)
71. Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield KD, et al. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase. Cancer Cell. 2005;7:77-85. (Pubitemid 40126384)
72. Silva VlS, Miguel Cordeiro J, Matos MJ, Oliveira CR, Gonçalves PP. Aluminum accumulation and membrane fluidity alteration in synaptosomes isolated from rat brain cortex following aluminum ingestion: effect of cholesterol. Neurosci Res. 2002;44:181-93. (Pubitemid 38365960)
73. Soni MG, White SM, Flamm WG, Burdock GA. Safety evaluation of dietary aluminum. Regul Toxicol Pharmacol. 2001;33:66-79. (Pubitemid 32242948)
74. Sood P, Nahar U, Nehru B. Curcumin attenuates aluminum-induced oxidative stress and mitochondrial dysfunction in rat brain. Neurotox Res. 2011;20:351-61.
75. Taylor JM, Main BS, Crack PJ. Neuroinflammation and oxidative stress: co-conspirators in the pathology of Parkinson's disease. Neurochem Int. 2013. doi: 10.1016/j.neuint.2012.12.016.
76. Tomljenovic L. Aluminum and Alzheimer's disease: after a century of controversy, is there a plausible link? J Alzheimers Dis. 2011;23:567-98.
77. Vaz FM, Wanders RJA. Carnitine biosynthesis in mammals. Biochem J. 2002;361:417-29. (Pubitemid 34177810)
78. Wang XF, Cynader MS. Pyruvate released by astrocytes protects neurons from copper-catalyzed cysteine neurotoxicity. J Neurosci. 2001;21:3322-31. (Pubitemid 32422797)
79. Ward RJ, Zhang Y, Crichton RR. Aluminium toxicity and iron homeostasis. J Inorg Biochem. 2001;87:9-14. (Pubitemid 33049895)
80. Wu Z, Du Y, Xue H, Wu Y, Zhou B. Aluminum induces neurodegeneration and its toxicity arises from increased iron accumulation and reactive oxygen species (ROS) production. Neurobiol Aging. 2012;33:199. e1-199.e12.
81. Yokel RA, Hicks CL, Florence RL. Aluminum bioavailability from basic sodium aluminum phosphate, an approved food additive emulsifying agent, incorporated in cheese. Food Chem Toxicol. 2008;46:2261-6.
82. Yousef MI, Salama AF. Propolis protection from reproductive toxicity caused by aluminium chloride in male rats. Food Chem Toxicol. 2009;47:1168-75.
83. Yuan CY, Lee YJ, Hsu GS. Aluminum overload increases oxidative stress in four functional brain areas of neonatal rats. J Biomed Sci. 2012;19:51.
84. Zatta P, Lain E, Cagnolini C. Effects of aluminum on activity of Krebs cycle enzymes and glutamate dehydrogenase in rat brain homogenate. Eur J Biochem. 2000;267:3049-55. (Pubitemid 30321353)
85. Zhang X, Banerjee A, Banks WA, Ercal N. N-Acetylcysteine amide protects against methamphetamine-induced oxidative stress and neurotoxicity in immortalized human brain endothelial cells. Brain Res. 2009;1275:87-95.