The disruption of l-carnitine metabolism by aluminum toxicity and oxidative stress promotes dyslipidemia in human astrocytic and hepatic cells

Toxicology Letters

Volumn 203, Issue 3, 2011, Pages 219-226

  Lemire, Joseph ^a   Mailloux, Ryan ^a   Darwich, Rami ^a   Auger, Christopher ^a   Appanna, Vasu D ^a  

^a LAURENTIAN UNIVERSITY   (Canada)

Author keywords

Aluminum toxicity; Carnitine biosynthesis; Dyslipidemia; Neurological disorders; Obesity

Indexed keywords

2 OXOGLUTARIC ACID; ALUMINUM; CARNITINE; GAMMA BUTYROBETAINE DIOXYGENASE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE;

ALUMINUM OVERLOAD; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DYSLIPIDEMIA; FATTY ACID OXIDATION; HUMAN; HUMAN CELL; LIPID STORAGE; LIVER CELL; MAMMAL; OXIDATIVE STRESS; PRIORITY JOURNAL;

ALUMINUM; ASTROCYTES; CARNITINE; CELL LINE, TUMOR; DYSLIPIDEMIAS; GAMMA-BUTYROBETAINE DIOXYGENASE; HEP G2 CELLS; HEPATOCYTES; HUMANS; HYDROGEN PEROXIDE; KETOGLUTARIC ACIDS; LIPID METABOLISM; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

MAMMALIA;

EID: 79955949682     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2011.03.019     Document Type: Article

References (48)

1. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat.. Neurosci. 2000, 3:1301-1306.
2. Bhatnagar A. Environmental cardiology: studying mechanistic links between pollution and heart disease. Circ. Res. 2006, 99:692-705.
3. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
4. Briggs D. Environmental pollution and the global burden of disease. Br. Med. Bull. 2003, 68:1-24.
5. Chenier D., Beriault R., Mailloux R., Baquie M., Abramia G., Lemire J., Appanna V. Involvement of fumarase C and NADH oxidase in metabolic adaptation of Pseudomonas fluorescens cells evoked by aluminum and gallium toxicity. Appl. Environ. Microbiol. 2008, 74:3977-3984.
6. Chern M.K., Pietruszko R. Evidence for mitochondrial localization of betaine aldehyde dehydrogenase in rat liver: purification, characterization, and comparison with human cytoplasmic E3 isozyme. Biochem. Cell Biol. 1999, 77:179-187.
7. Donato M.T., Hallifax D., Picazo L., Castell J.V., Houston J.B., Gomez-Lechon M.J., Lahoz A. Metabolite formation kinetics and intrinsic clearance of phenacetin, tolbutamide, alprazolam, and midazolam in adenoviral cytochrome P450-transfected HepG2 cells and comparison with hepatocytes and in vivo. Drug Metab. Dispos. 2010, 38:1449-1455.
8. 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.
9. Foster P.M. Disruption of reproductive development in male rat offspring following in utero exposure to phthalate esters. Int. J. Androl. 2006, 29:140-147. discussion 181-145.
10. Fujita M., Nakanishi T., Shibue Y., Kobayashi D., Moseley R.H., Shirasaka Y., Tamai I. Hepatic uptake of gamma-butyrobetaine, a precursor of carnitine biosynthesis, in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 297:G681-686.
11. Galy B., Ferring-Appel D., Sauer S.W., Kaden S., Lyoumi S., Puy H., Kolker S., Grone H.J., Hentze M.W. Iron regulatory proteins secure mitochondrial iron sufficiency and function. Cell Metab. 2010, 12:194-201.
12. Goya L., Martin M.A., Ramos S, Mateos R, Bravo L A cell culture model for the assessment of the chemopreventive potential of dietary compounds. Curr. Nutr. Food Sci. 2009, 5:56-64.
13. Guilarte T.R. Manganese and Parkinson's disease: a critical review and new findings. Environ. Health Perspect. 2010, 118:1071-1080.
14. Gulcin I. Antioxidant and antiradical activities of l-carnitine. Life Sci. 2006, 78:803-811.
15. Ji Q., Shi X., Lin R., Mao Y., Zhai X., Lin Q., Zhang J. Participation of lipid transport and fatty acid metabolism in valproate sodium-induced hepatotoxicity in HepG2 cells. Toxicol. In Vitro 2010, 24:1086-1091.
16. Kaizer R.R., Correa M.C., Gris L.R., da Rosa C.S., Bohrer D., Morsch V.M., Schetinger M.R. Effect of long-term exposure to aluminum on the acetylcholinesterase activity in the central nervous system and erythrocytes. Neurochem. Res. 2008, 33:2294-2301.
17. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
18. Lemire J., Mailloux R.J., Appanna V.D. Mitochondrial lactate dehydrogenase is involved in oxidative-energy metabolism in human astrocytoma cells (CCF-STTG1). PLoS ONE 2008, 3:e1550.
19. 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.
20. Lill R., Kispal G. Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem. Sci. 2000, 25:352-356.
21. Lindstedt S., Nordin I. Multiple forms of gamma-butyrobetaine hydroxylase (EC 1.14.11.1). Biochem. J. 1984, 223:119-127.
22. Liu X., Liu M., Zhang J., Bai X., Ramos F., Van Remmen H., Richardson A., Liu F.Y., Dong L.Q., Liu F. Downregulation of Grb2 contributes to the insulin-sensitizing effect of calorie restriction. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E1067-1075.
23. Liu S., Li S., Du Y. Polychlorinated biphenyls (PCBs) enhance metastatic properties of breast cancer cells by activating Rho-associated kinase (ROCK). PLoS One 2010, 5:e11272.
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., 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.
26. 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.
27. 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.
28. 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.
29. Mailloux R.J., Singh R., Brewer G., Auger C., Lemire J., Appanna V.D. Alpha-ketoglutarate dehydrogenase and glutamate dehydrogenase work in tandem to modulate the antioxidant alpha-ketoglutarate during oxidative stress in Pseudomonas fluorescens. J. Bacteriol. 2009, 191:3804-3810.
30. Mallet R.T., Squires J.E., Bhatia S., Sun J. Pyruvate restores contractile function and antioxidant defenses of hydrogen peroxide-challenged myocardium. J. Mol. Cell Cardiol. 2002, 34:1173-1184.
31. May J.M., Qu Z.C., Whitesell R.R. Ascorbate is the major electron donor for a transmembrane oxidoreductase of human erythrocytes. Biochim. Biophys. Acta 1995, 1238:127-136.
32. Mentz S., de Lacalle S., Baerga-Ortiz A., Knauer M.F., Knauer D.J., Komives E.A. Mechanism of thrombin clearance by human astrocytoma cells. J. Neurochem. 1999, 72:980-987.
33. 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.
34. Minkler P.E., Stoll M.S., Ingalls S.T., Yang S., Kerner J., Hoppel C.L. Quantification of carnitine and acylcarnitines in biological matrices by HPLC electrospray ionization-mass spectrometry. Clin. Chem. 2008, 54:1451-1462.
35. Muniyappa R. Oral carnitine therapy and insulin resistance. Hypertension 2010, 55:e13.
36. Peschechera A., Scalibastri M., Russo F., Giarrizzo M.G., Carminati P., Giannessi F., Arduini A., Ricciolini R. Carnitine depletion in rat pups from mothers given mildronate: a model of carnitine deficiency in late fetal and neonatal life. Life Sci. 2005, 77:3078-3091.
37. Rosenlund M., Berglind N., Pershagen G., Hallqvist J., Jonson T., Bellander T. Long-term exposure to urban air pollution and myocardial infarction. Epidemiology 2006, 17:383-390.
38. Schagger H., von Jagow G. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 1991, 199:223-231.
39. Schotz M.C., Garfinkel A.S., Huebotter R.J., Stewart J.E. A rapid assay for lipoprotein lipase. J. Lipid Res. 1970, 11:68-69.
40. 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.
41. Sherer T.B., Betarbet R., Greenamyre J.T. Environment, mitochondria, and Parkinson's disease. Neuroscientist 2002, 8:192-197.
42. Simonovic A.D., Gaddameedhi S., Anderson M.D. In-gel precipitation of enzymatically released phosphate. Anal. Biochem. 2004, 334:312-317.
43. Swan S.H. Environmental phthalate exposure in relation to reproductive outcomes and other health endpoints in humans. Environ. Res. 2008, 108:177-184.
44. 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.
45. Vaz F.M., Wanders R.J. Carnitine biosynthesis in mammals. Biochem. J. 2002, 361:417-429.
46. Vaz F.M., van Gool S., Ofman R., Wanders R.J., Ijlst L. Carnitine biosynthesis. Purification of gamma-butyrobetaine hydroxylase from rat liver. Adv. Exp. Med. Biol. 1999, 466:117-124.
47. Vaz F.M., Ofman R., Westinga K., Back J.W., Wanders R.J. Molecular and Biochemical Characterization of Rat epsilon-N-Trimethyllysine Hydroxylase, the First Enzyme of Carnitine Biosynthesis. J. Biol. Chem. 2001, 276:33512-33517.
48. 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.