Hepatic response to aluminum toxicity: Dyslipidemia and liver diseases

Experimental Cell Research

Volumn 317, Issue 16, 2011, Pages 2231-2238

  Mailloux, Ryan J ^a,b   Lemire, Joseph ^a   Appanna, Vasu D ^a  

^a LAURENTIAN UNIVERSITY   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Aluminum toxicity; Dyslipidemia; Hepatic metabolism; Liver diseases; Obesity

Indexed keywords

2 OXOGLUTARIC ACID; ADENOSINE TRIPHOSPHATE; ALUMINUM; CARNITINE; HYPOXIA INDUCIBLE FACTOR 1; REACTIVE OXYGEN METABOLITE; TRICARBOXYLIC ACID;

AEROBIC METABOLISM; ALUMINUM OVERLOAD; BRAIN DISEASE; CALCIUM HOMEOSTASIS; CELL CULTURE; CELL STRAIN HEPG2; CITRIC ACID CYCLE; DIALYSIS ENCEPHALOPATHY; DYSLIPIDEMIA; FATTY ACID OXIDATION; GLYCOLYSIS; HEPATOBLASTOMA; HOMEOSTASIS; LIPID MEMBRANE; LIPID STORAGE; LIPOGENESIS; LIVER DISEASE; MITOCHONDRIAL RESPIRATION; OSTEOMALACIA; OXIDATION REDUCTION REACTION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW;

EID: 80051794514     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.07.009     Document Type: Review

References (70)

1. Neal A.P., Guilarte T.R. Molecular neurobiology of lead (Pb(2+)): effects on synaptic function. Mol. Neurobiol. 2010, 42:151-160.
2. Waalkes M.P., Rehm S. Cadmium and prostate cancer. J. Toxicol. Environ. Health 1994, 43:251-269.
3. Lisiewicz J. Immunotoxic and hematotoxic effects of occupational exposures. Folia Med. Cracov. 1993, 34:29-47.
4. Desvergne B., Feige J.N., Casals-Casas C. PPAR-mediated activity of phthalates: a link to the obesity epidemic?. Mol. Cell. Endocrinol. 2009, 304:43-48.
5. Latini G., Marcovecchio M.L., Del Vecchio A., Gallo F., Bertino E., Chiarelli F. Influence of environment on insulin sensitivity. Environ. Int. 2009, 35:987-993.
6. Paolo Zatta T.K., Suwalsky Mario, Berthon Guy Aluminum(III) as a promoter of cellular oxidation. Coord. Chem. Rev. 2002, 228:271-284.
7. 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, 20:627-638.
8. Becaria A., Campbell A., Bondy S.C. Aluminum as a toxicant. Toxicol. Ind. Health 2002, 18:309-320.
9. Exley C. The pro-oxidant activity of aluminum. Free Radic. Biol. Med. 2004, 36:380-387.
10. Peto M.V. Aluminium and iron in humans: bioaccumulation, pathology, and removal. Rejuvenation Res. 2010, 13:589-598.
11. Jeffery E.H., Abreo K., Burgess E., Cannata J., Greger J.L. Systemic aluminum toxicity: effects on bone, hematopoietic tissue, and kidney. J. Toxicol. Environ. Health 1996, 48:649-665.
12. Jaffe J.A., Liftman C., Glickman J.D. Frequency of elevated serum aluminum levels in adult dialysis patients. Am. J. Kidney Dis. 2005, 46:316-319.
13. Exley C. Aluminium and iron, but neither copper nor zinc, are key to the precipitation of beta-sheets of Abeta_{42} in senile plaque cores in Alzheimer's disease. J. Alzheimers Dis. 2006, 10:173-177.
14. Kumar V., Bal A., Gill K.D. Aluminium-induced oxidative DNA damage recognition and cell-cycle disruption in different regions of rat brain. Toxicology 2009, 264:137-144.
15. Banasik A., Lankoff A., Piskulak A., Adamowska K., Lisowska H., Wojcik A. Aluminum-induced micronuclei and apoptosis in human peripheral-blood lymphocytes treated during different phases of the cell cycle. Environ. Toxicol. 2005, 20:402-406.
16. Lemire J., Mailloux R., Puiseux-Dao S., Appanna V.D. Aluminum-induced defective mitochondrial metabolism perturbs cytoskeletal dynamics in human astrocytoma cells. J. Neurosci. Res. 2009, 87:1474-1483.
17. Arroyo-Serralta G.A., Ku-Gonzalez A., Hernandez-Sotomayor S.M., Zuniga Aguilar J.J. Exposure to toxic concentrations of aluminum activates a MAPK-like protein in cell suspension cultures of Coffea arabica. Plant Physiol. Biochem. 2005, 43:27-35.
18. Drago D., Cavaliere A., Mascetra N., Ciavardelli D., di Ilio C., Zatta P., Sensi S.L. Aluminum modulates effects of beta amyloid(1-42) on neuronal calcium homeostasis and mitochondria functioning and is altered in a triple transgenic mouse model of Alzheimer's disease. Rejuvenation Res. 2008, 11:861-871.
19. Hellstrom H.O., Michaelsson K., Mallmin H., Mjoberg B. The aluminium content of bone, and mortality risk. Age Ageing 2008, 37:217-220.
20. Exley C. Aluminum and Alzheimer's disease. J. Alzheimers Dis. 2001, 3:551-552.
21. Xu Z.X., Fox L., Melethil S., Winberg L., Badr M. Mechanism of aluminum-induced inhibition of hepatic glycolysis: inactivation of phosphofructokinase. J. Pharmacol. Exp. Ther. 1990, 254:301-305.
22. Beardmore J., Rugg G., Exley C. A systems biology approach to the blood-aluminium problem: the application and testing of a computational model. J. Inorg. Biochem. 2007, 101:1187-1191.
23. Beardmore J., Exley C. Towards a model of non-equilibrium binding of metal ions in biological systems. J. Inorg. Biochem. 2009, 103:205-209.
24. Mailloux R.J., Appanna V.D. Aluminum toxicity triggers the nuclear translocation of HIF-1alpha and promotes anaerobiosis in hepatocytes. Toxicol. In Vitro 2007, 21:16-24.
25. Mailloux R.J., Puiseux-Dao S., Appanna V.D. Alpha-ketoglutarate abrogates the nuclear localization of HIF-1alpha in aluminum-exposed hepatocytes. Biochimie 2009, 91:408-415.
26. Mailloux R.J., Hamel R., Appanna V.D. Aluminum toxicity elicits a dysfunctional TCA cycle and succinate accumulation in hepatocytes. J. Biochem. Mol. Toxicol. 2006, 20:198-208.
27. Levi S., Rovida E. The role of iron in mitochondrial function. Biochim. Biophys. Acta 2009, 1790:629-636.
28. Janero D.R., Hreniuk D., Sharif H.M. Hydrogen peroxide-induced oxidative stress to the mammalian heart-muscle cell (cardiomyocyte): lethal peroxidative membrane injury. J. Cell. Physiol. 1991, 149:347-364.
29. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
30. Mailloux R.J., Lemire J., Appanna V.D. Metabolic networks to combat oxidative stress in Pseudomonas fluorescens. Antonie Van Leeuwenhoek 2011, 99:433-442.
31. +/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid. Redox Signal. 2008, 10:179-206.
32. Middaugh J., Hamel R., Jean-Baptiste G., Beriault R., Chenier D., Appanna V.D. 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, 280:3159-3165.
33. Chen H., Davidson T., Singleton S., Garrick M.D., Costa M. Nickel decreases cellular iron level and converts cytosolic aconitase to iron-regulatory protein 1 in A549 cells. Toxicol. Appl. Pharmacol. 2005, 206:275-287.
34. Costello L.C., Franklin R.B. Aconitase activity, citrate oxidation, and zinc inhibition in rat ventral prostate. Enzyme 1981, 26:281-287.
35. 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, 267:3049-3055.
36. Wlodek D., Gonzales M. Decreased energy levels can cause and sustain obesity. J. Theor. Biol. 2003, 225:33-44.
37. Selak M.A., Armour S.M., MacKenzie E.D., Boulahbel H., Watson D.G., Mansfield K.D., Pan Y., Simon M.C., Thompson C.B., Gottlieb E. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 2005, 7:77-85.
38. MacKenzie E.D., Selak M.A., Tennant D.A., Payne L.J., Crosby S., Frederiksen C.M., Watson D.G., Gottlieb E. Cell-permeating alpha-ketoglutarate derivatives alleviate pseudohypoxia in succinate dehydrogenase-deficient cells. Mol. Cell. Biol. 2007, 27:3282-3289.
39. Perez-Carreras M., Del Hoyo P., Martin M.A., Rubio J.C., Martin A., Castellano G., Colina F., Arenas J., Solis-Herruzo J.A. Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology 2003, 38:999-1007.
40. Holloway G.P., Perry C.G., Thrush A.B., Heigenhauser G.J., Dyck D.J., Bonen A., Spriet L.L. PGC-1alpha's relationship with skeletal muscle palmitate oxidation is not present with obesity despite maintained PGC-1alpha and PGC-1beta protein. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E1060-E1069.
41. Mailloux R.J., Beriault R., Lemire J., Singh R., Chenier D.R., Hamel R.D., Appanna V.D. The tricarboxylic acid cycle, an ancient metabolic network with a novel twist. PLoS One 2007, 2:e690.
42. Applegate M.A., Humphries K.M., Szweda L.I. Reversible inhibition of alpha-ketoglutarate dehydrogenase by hydrogen peroxide: glutathionylation and protection of lipoic acid. Biochemistry 2008, 47:473-478.
43. Tretter L., Adam-Vizi V. Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:2335-2345.
44. Fedotcheva N.I., Sokolov A.P., Kondrashova M.N. Nonezymatic formation of succinate in mitochondria under oxidative stress. Free Radic. Biol. Med. 2006, 41:56-64.
45. Tiziani S., Lodi A., Khanim F.L., Viant M.R., Bunce C.M., Gunther U.L. Metabolomic profiling of drug responses in acute myeloid leukaemia cell lines. PLoS One 2009, 4:e4251.
46. Tretter L., Adam-Vizi V. Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase. J. Neurosci. 2004, 24:7771-7778.
47. Harten S.K., Ashcroft M., Maxwell P.H. Prolyl hydroxylase domain inhibitors: a route to HIF activation and neuroprotection. Antioxid. Redox Signal. 2010, 12:459-480.
48. Kaelin W.G., Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 2008, 30:393-402.
49. Semenza G.L. Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Semin. Cancer Biol. 2009, 19:12-16.
50. Bell E.L., Klimova T.A., Eisenbart J., Moraes C.T., Murphy M.P., Budinger G.R., Chandel N.S. The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J. Cell Biol. 2007, 177:1029-1036.
51. Cioffi C.L., Liu X.Q., Kosinski P.A., Garay M., Bowen B.R. Differential regulation of HIF-1 alpha prolyl-4-hydroxylase genes by hypoxia in human cardiovascular cells. Biochem. Biophys. Res. Commun. 2003, 303:947-953.
52. Davidson T.L., Chen H., Di Toro D.M., D'Angelo G., Costa M. Soluble nickel inhibits HIF-prolyl-hydroxylases creating persistent hypoxic signaling in A549 cells. Mol. Carcinog. 2006, 45:479-489.
53. Martin F., Linden T., Katschinski D.M., Oehme F., Flamme I., Mukhopadhyay C.K., Eckhardt K., Troger J., Barth S., Camenisch G., Wenger R.H. Copper-dependent activation of hypoxia-inducible factor (HIF)-1: implications for ceruloplasmin regulation. Blood 2005, 105:4613-4619.
54. Birchall J.D., Espie A.W. Biological implications of the interaction (via silanol groups) of silicon with metal ions. Ciba Found. Symp. 1986, 121:140-159.
55. Exley C., Price N.C., Birchall J.D. Aluminum inhibition of hexokinase activity in vitro: a study in biological availability. J. Inorg. Biochem. 1994, 54:297-304.
56. Exley C., Birchall J.D. The cellular toxicity of aluminium. J. Theor. Biol. 1992, 159:83-98.
57. Pollak N., Dolle C., Ziegler M. The power to reduce: pyridine nucleotides - small molecules with a multitude of functions. Biochem. J. 2007, 402:205-218.
58. Mailloux R.J., Singh R., Appanna V.D. In-gel activity staining of oxidized nicotinamide adenine dinucleotide kinase by blue native polyacrylamide gel electrophoresis. Anal. Biochem. 2006, 359:210-215.
59. Bournat J.C., Brown C.W. Mitochondrial dysfunction in obesity. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 17:446-452.
60. Johannsen D.L., Ravussin E. The role of mitochondria in health and disease. Curr. Opin. Pharmacol. 2009, 9:780-786.
61. Grun F. Obesogens. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 17:453-459.
62. Serviddio G., Bellanti F., Vendemiale G., Altomare E. Mitochondrial dysfunction in nonalcoholic steatohepatitis. Expert Rev. Gastroenterol. Hepatol. 2011, 5:233-244.
63. Lemire J., Mailloux R., Darwich R., Auger C., Appanna V.D. The disruption of l-carnitine metabolism by aluminum toxicity and oxidative stress promotes dyslipidemia in human astrocytic and hepatic cells. Toxicol. Lett. 2011, 203:219-226.
64. Vaz F.M., Wanders R.J. Carnitine biosynthesis in mammals. Biochem. J. 2002, 361:417-429.
65. Infante J.P., Huszagh V.A. Secondary carnitine deficiency and impaired docosahexaenoic (22:6n-3) acid synthesis: a common denominator in the pathophysiology of diseases of oxidative phosphorylation and beta-oxidation. FEBS Lett. 2000, 468:1-5.
66. Boudin G., Mikol J., Guillard A., Engel A.G. Fatal systemic carnitine deficiency with lipid storage in skeletal muscle, heart, liver and kidney. J. Neurol. Sci. 1976, 30:313-325.
67. Pessayre D., Mansouri A., Berson A., Fromenty B. Mitochondrial involvement in drug-induced liver injury. Handb. Exp. Pharmacol. 2010, 311-365.
68. Serviddio G., Bellanti F., Sastre J., Vendemiale G., Altomare E. Targeting mitochondria: a new promising approach for the treatment of liver diseases. Curr. Med. Chem. 2010, 17:2325-2337.
69. Lowell B.B., Shulman G.I. Mitochondrial dysfunction and type 2 diabetes. Science 2005, 307:384-387.
70. Mantena S.K., King A.L., Andringa K.K., Eccleston H.B., Bailey S.M. Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol- and obesity-induced fatty liver diseases. Free Radic. Biol. Med. 2008, 44:1259-1272.