Formaldehyde metabolism and formaldehyde-induced stimulation of lactate production and glutathione export in cultured neurons

Journal of Neurochemistry

Volumn 125, Issue 2, 2013, Pages 260-272

  Tulpule, Ketki ^a   Hohnholt, Michaela C ^a   Dringen, Ralf ^a  

^a UNIVERSITY OF BREMEN   (Germany)

Author keywords

cerebellar granule neurons; formate; GSH; lactate; metabolism

Indexed keywords

FORMALDEHYDE; FORMIC ACID; GLUCOSE; GLUTATHIONE; LACTIC ACID; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1;

ANIMAL CELL; ARTICLE; CELL LEVEL; CELL METABOLISM; CELL VIABILITY; CEREBELLUM; CONTROLLED STUDY; GENE EXPRESSION; GLUTATHIONE METABOLISM; GLYCOLYSIS; GRANULE CELL; NEUROTOXICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; NERVE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WISTAR RAT;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; FORMALDEHYDE; GLUTATHIONE; LACTIC ACID; NEURONS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84876044317     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12170     Document Type: Article

References (83)

1. Airas L., Mikkola J., Vainio J. M., Elovaara I., and, Smith D. J., (2006) Elevated serum soluble vascular adhesion protein-1 (VAP-1) in patients with active relapsing remitting multiple sclerosis. J. Neuroimmunol. 177, 132-135.
2. Anggono V., Cousin M. A., and, Robinson P. J., (2008) Styryl dye-based synaptic vesicle recycling assay in cultured cerebellar granule neurons. Methods Mol. Biol. 457, 333-345.
3. Anthony T. E., and, Heintz N., (2007) The folate metabolic enzyme ALDH1L1 is restricted to the midline of the early CNS, suggesting a role in human neural tube defects. J. Comp. Neurol. 500, 368-383.
4. Berkich D. A., Ola M. S., Cole J., Sweatt A. J., Hutson S. M., and, LaNoue K. F., (2007) Mitochondrial transport proteins of the brain. J. Neurosci. Res. 85, 3367-3377.
5. Bolanos J. P., Almeida A., and, Moncada S., (2010) Glycolysis: A bioenergetic or a survival pathway? Trends Biochem. Sci. 35, 145-149.
6. Cahoy J. D., Emery B., Kaushal A., et al,. (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28, 264-278.
7. Cloos P. A., Christensen J., Agger K., and, Helin K., (2008) Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev. 22, 1115-1140.
8. Cole S. P. C., and, Deeley R. G., (2006) Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol. Sci. 27, 438-446.
9. Correia S. C., Santos R. X., Cardoso S., Carvalho C., Candeias E., Duarte A. I., Placido A. I., Santos M. S., and, Moreira P. I., (2012) Alzheimer disease as a vascular disorder: where do mitochondria fit? Exp. Gerontol. 47, 878-886.
10. Dhareshwar S. S., and, Stella V. J., (2008) Your prodrug releases formaldehyde: should you be concerned? No! J. Pharm. Sci. 97, 4184-4193.
11. Dringen R., and, Hamprecht B., (1997) Involvement of glutathione peroxidase and catalase in the disposal of exogenous hydrogen peroxide by cultured astroglial cells. Brain Res. 759, 67-75.
12. Dringen R., Kussmaul L., and, Hamprecht B., (1998) Detoxification of exogenous hydrogen peroxide and organic hydroperoxides by cultured astroglial cells assessed by microtiter plate assay. Brain Res. Brain Res. Protoc. 2, 223-228.
13. Ferrer I., Lizcano J. M., Hernandez M., and, Unzeta M., (2002) Overexpression of semicarbazide sensitive amine oxidase in the cerebral blood vessels in patients with Alzheimer's disease and cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Neurosci. Lett. 321, 21-24.
14. Friedenson B., (2011) A common environmental carcinogen unduly affects carriers of cancer mutations: carriers of genetic mutations in a specific protective response are more susceptible to an environmental carcinogen. Med. Hypotheses 77, 791-797.
15. Galter D., Carmine A., Buervenich S., Duester G., and, Olson L., (2003) Distribution of class I, III and IV alcohol dehydrogenase mRNAs in the adult rat, mouse and human brain. Eur. J. Biochem. 270, 1316-1326.
16. de Groot A. C., Flyvholm M. A., Lensen G., Menne T., and, Coenraads P. J., (2009) Formaldehyde-releasers: relationship to formaldehyde contact allergy. Contact allergy to formaldehyde and inventory of formaldehyde-releasers. Contact dermatitis 61, 63-85.
17. Gurel A., Coskun O., Armutcu F., Kanter M., and, Ozen O. A., (2005) Vitamin E against oxidative damage caused by formaldehyde in frontal cortex and hippocampus: biochemical and histological studies. J. Chem. Neuroanat. 29, 173-178.
18. Gutterer J. M., Dringen R., Hirrlinger J., and, Hamprecht B., (1999) Purification of glutathione reductase from bovine brain, generalization of an antiserum, and immunocytochemical localization of the enzyme in neural cells. J. Neurochem. 73, 1422-1430.
19. Haider L., Fischer M. T., Frischer J. M., Bauer J., Höftberger R,., Botond G,., Esterbauer H,., Binder C. J., Witztum J. L., and, Lassmann H,. (2011) Oxidative damage in multiple sclerosis lesions. Brain 134, 1914-1924.
20. Halim N. D., McFate T., Mohyeldin A., et al,. (2010) Phosphorylation status of pyruvate dehydrogenase distinguishes metabolic phenotypes of cultured rat brain astrocytes and neurons. Glia 58, 1168-1176.
21. Hamprecht B., and, Löffler F., (1985) Primary glial cultures as a model for studying hormone action. Methods Enzymol. 109, 341-345.
22. Heck H. D., and, Casanova M., (2004) The implausibility of leukemia induction by formaldehyde: a critical review of the biological evidence on distant-site toxicity. Regul. Toxicol. Pharm. 40, 92-106.
23. Hirrlinger J., and, Dringen R., (2005) Multidrug resistance protein 1-mediated export of glutathione and glutathione disulfide from brain astrocytes. Methods Enzymol. 400, 395-409.
24. Hirrlinger J., Schulz J. B., and, Dringen R., (2002) Glutathione release from cultured brain cells: multidrug resistance protein 1 mediates the release of GSH from rat astroglial cells. J. Neurosci. Res. 69, 318-326.
25. Hou H., and, Yu H., (2010) Structural insights into histone lysine demethylation. Curr. Opin. Struct. Biol. 20, 739-748.
26. Itoh Y., Esaki T., Shimoji K., Cook M., Law M. J., Kaufman E., and, Sokoloff L., (2003) Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose utilization by brain in vivo. Proc. Natl Acad. Sci. USA 100, 4879-4884.
27. Kapur B. M., Vandenbroucke A. C., Adamchik Y., Lehotay D. C., and, Carlen P. L., (2007) Formic acid, a novel metabolite of chronic ethanol abuse, causes neurotoxicity, which is prevented by folic acid. Alcohol. Clin. Exp. Res. 31, 2114-2120.
28. Keppler D., (2011) Multidrug resistance proteins (MRPs, ABCCs): importance for pathophysiology and drug therapy. Handb. Exp. Pharmacol. 201, 299-323.
29. Khokhlov A. P., Zavalishin I. A., Savchenko I. N., and, Dziuba A. N., (1989) Disorders of formaldehyde metabolism and its metabolic precursors in patients with multiple sclerosis. Zh. Nevropatol. Psikhiatr. Im. S. S. Korsakova 89, 45-48.
30. Krieter P. A., Ziegler D. M., Hill K. E., and, Burk R. F., (1985) Studies on the biliary efflux of GSH from rat liver due to the metabolism of aminopyrine. Biochem. Pharmacol. 34, 955-960.
31. Krupenko S. A., (2009) FDH: an aldehyde dehydrogenase fusion enzyme in folate metabolism. Chem. Biol. Interact. 178, 84-93.
32. Krupenko N. I., Dubard M. E., Strickland K. C., Moxley K. M., Oleinik N. V., and, Krupenko S. A., (2010) ALDH1L2 is the mitochondrial homolog of 10-formyltetrahydrofolate dehydrogenase. J. Biol. Chem. 285, 23056-23063.
33. Lee E. S., Chen H. T., Hardman C., Simm A., and, Charlton C., (2008) Excessive S-adenosyl-L-methionine-dependent methylation increases levels of methanol, formaldehyde and formic acid in rat brain striatal homogenates: possible role in S-adenosyl-L-methionine-induced Parkinson's disease-like disorders. Life Sci. 83, 821-827.
34. Lee M., Cho T., Jantaratnotai N., Wang Y. T., McGeer E., and, McGeer P. L., (2010) Depletion of GSH in glial cells induces neurotoxicity: relevance to aging and degenerative neurological diseases. FASEB J. 24, 2533-2545.
35. Leuner K., Muller W. E., and, Reichert A. S., (2012) From mitochondrial dysfunction to amyloid beta formation: novel insights into the pathogenesis of Alzheimer's disease. Mol. Neurobiol. 46, 186-193.
36. Lewerenz J., Dargusch R., and, Maher P., (2010) Lactacidosis modulates glutathione metabolism and oxidative glutamate toxicity. J. Neurochem. 113, 502-514.
37. Liddell J. R., Zwingmann C., Schmidt M. M., Thiessen A., Leibfritz D., Robinson S. R., and, Dringen R., (2009) Sustained hydrogen peroxide stress decreases lactate production by cultured astrocytes. J. Neurosci. Res. 87, 2696-2708.
38. Lowry O. H., Rosebrough N. J., Farr A. L., and, Randall R. J., (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
39. Lu K., Ye W., Zhou L., Collins L. B., Chen X., Gold A., Ball L. M., and, Swenberg J. A., (2010) Structural characterization of formaldehyde-induced cross-links between amino acids and deoxynucleosides and their oligomers. J. Am. Chem. Soc. 132, 3388-3399.
40. MacAllister S. L., Choi J., Dedina L., and, O'Brien P. J., (2011) Metabolic mechanisms of methanol/formaldehyde in isolated rat hepatocytes: carbonyl-metabolizing enzymes versus oxidative stress. Chem. Biol. Interact. 191, 308-314.
41. del Mar Hernandez M., Esteban M., Szabo P., Boada M., and, Unzeta M., (2005) Human plasma semicarbazide sensitive amine oxidase (SSAO), beta-amyloid protein and aging. Neurosci. Lett. 384, 183-187.
42. Martinez S. E., Vaglenova J., Sabria J., Martinez M. C., Farres J., and, Pares X., (2001) Distribution of alcohol dehydrogenase mRNA in the rat central nervous system- consequences for brain ethanol and retinoid metabolism. Eur. J. Biochem. 268, 5045-5056.
43. Mason M. J., Mattsson K., Pasternack M., Voipio J., and, Kaila K., (1990) Postsynaptic fall in intracellular pH and increase in surface pH caused by efflux of formate and acetate anions through GABA-gated channels in crayfish muscle-fibers. Neuroscience 34, 359-368.
44. Miao J., and, He R., (2012) Chronic formaldehyde-mediated impairments and age-related dementia, in Neurodegeneration (, Martin L. M., and, Loh S. H. Y., eds), pp 59-76. InTech, New York, USA.
45. Minich T., Riemer J., Schulz J. B., Wielinga P., Wijnholds J., and, Dringen R., (2006) The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J. Neurochem. 97, 373-384.
46. Moschen I., Broer A., Galic S., Lang F., and, Broer S., (2012) Significance of short chain fatty acid transport by members of the monocarboxylate transporter family (MCT). Neurochem. Res. 37, 2562-2568.
47. Neves A., Costalat R., and, Pellerin L., (2012) Determinants of brain cell metabolic phenotypes and energy substrate utilization unraveled with a modeling approach. PLoS Comput. Biol. 8, e1002686.
48. Nicholls P., (1975) Formate as an inhibitor of cytochrome c oxidase. Biochem. Biophys. Res. Commun. 67, 610-616.
49. Ospina M., Costin A., Barry A. K., and, Vesper H. W., (2011) Characterization of N-terminal formaldehyde adducts to hemoglobin. Rapid Commun. Mass Spectrom. 25, 1043-1050.
50. O'Sullivan J., Unzeta M., Healy J., O'Sullivan M. I., Davey G., and, Tipton K. F., (2004) Semicarbazide-sensitive amine oxidases: enzymes with quite a lot to do. Neurotoxicology 25, 303-315.
51. Prasannan P., Pike S., Peng K., Shane B., and, Appling D. R., (2003) Human mitochondrial C1-tetrahydrofolate synthase: gene structure, tissue distribution of the mRNA, and immunolocalization in chinese hamster ovary calls. J. Biol. Chem. 278, 43178-43187.
52. Regan R. F., and, Guo Y., (1999a) Extracellular reduced glutathione increases neuronal vulnerability to combined chemical hypoxia and glucose deprivation. Brain Res. 817, 145-150.
53. Regan R. F., and, Guo Y. P., (1999b) Potentiation of excitotoxic injury by high concentrations of extracellular reduced glutathione. Neuroscience 91, 463-470.
54. Rose C. F., (2010) Increase brain lactate in hepatic encephalopathy: cause or consequence? Neurochem. Int. 57, 389-394.
55. Scheiber I. F., and, Dringen R., (2011) Copper accelerates glycolytic flux in cultured astrocytes. Neurochem. Res. 36, 894-903.
56. Scheiber I. F., Schmidt M. M., and, Dringen R., (2010) Zinc prevents the copper-induced damage of cultured astrocytes. Neurochem. Int. 57, 314-322.
57. Schmidt M. M., and, Dringen R., (2009) Differential effects of iodoacetamide and iodoacetate on glycolysis and glutathione metabolism of cultured astrocytes. Front. Neuroenergetics 1, 1-10.
58. Sellinger O. Z., Kramer C. M., Conger A., and, Duboff G. S., (1988) The carboxylmethylation of cerebral membrane-bound proteins increases with age. Mech. Ageing Dev. 43, 161-173.
59. Skrzydlewska E., (2003) Toxicological and metabolic consequences of methanol poisoning. Toxicol. Mech. Methods 13, 277-293.
60. Sohal R. S., and, Orr W. C., (2012) The redox stress hypothesis of aging. Free Radic. Biol. Med. 52, 539-555.
61. Soler-Lopez M., Badiola N., Zanzoni A., and, Aloy P., (2012) Towards Alzheimer's root cause: ECSIT as an integrating hub between oxidative stress, inflammation and mitochondrial dysfunction. Hypothetical role of the adapter protein ESCIT in familial and sporadic Alzheimer's disease pathogenesis. BioEssays 34, 532-541.
62. Song M. S., Baker G. B., Dursun S. M., and, Todd K. G., (2010) The antidepressant phenelzine protects neurons and astrocytes against formaldehyde-induced toxicity. J. Neurochem. 114, 1405-1413.
63. Songur A., Sarsilmaz M., Ozen O. A., Sahin S., Koken R., Zararsiz I., and, And Ilhan N., (2008) The effects of inhaled formaldehyde on oxidant and antioxidant systems of rat cerebellum during the postnatal development process. Toxicol. Mech. Methods 18, 569-574.
64. Songur A., Ozen O. A., and, Sarsilmaz M., (2010) The toxic effects of formaldehyde on the nervous system. Rev. Environ. Contam. Toxicol. 203, 105-118.
65. Staab C. A., Alander J., Morgenstern R., Grafstrom R. C., and, Hoog J. O., (2009) The janus face of alcohol dehydrogenase 3. Chem. Biol. Interact. 178, 29-35.
66. Su Y. A., Zhang Q., Su D. M., and, Tang M. X., (2011) Rat mitochondrion-neuron focused microarray (rMNChip) and bioinformatics tools for rapid identification of differential pathways in brain tissues. Int. J. Biol. Sci. 7, 308-322.
67. Thompson C. M., Ceder R., and, Grafstrom R. C., (2010) Formaldehyde dehydrogenase: beyond phase I metabolism. Toxicol. Lett. 193, 1-3.
68. Tong Z., Zhang J., Luo W., et al,. (2011) Urine formaldehyde level is inversely correlated to mini mental state examination scores in senile dementia. Neurobiol. Aging 32, 31-41.
69. Tong Z., Han C., Luo W., Wang X., Li H., Luo H., Zhou J., Qi J., and, He R., (2012) Accumulated hippocampal formaldehyde induces age-dependent memory decline, Age (Dordr) (in press).
70. Tulpule K., and, Dringen R., (2011) Formaldehyde stimulates Mrp1-mediated glutathione deprivation of cultured astrocytes. J. Neurochem. 116, 626-635.
71. Tulpule K., and, Dringen R., (2012) Formate generated by cellular oxidation of formaldehyde accelerates the glycolytic flux in cultured astrocytes. Glia 60, 582-593.
72. Tulpule K., Robinson S. R., Bishop G. M., and, Dringen R., (2010) Uptake of ferrous iron by cultured rat astrocytes. J. Neurosci. Res. 88, 563-571.
73. Tulpule K., Schmidt M. M., Boecker K., Goldbaum O., Richter-Landsberg C., and, Dringen R., (2012) Formaldehyde induces rapid glutathione export from viable oligodendroglial OLN-93 cells. Neurochem. Int. 61, 1302-1313.
74. Unzeta M., Sole M., Boada M., and, Hernandez M., (2007) Semicarbazide-sensitive amine oxidase (SSAO) and its possible contribution to vascular damage in Alzheimer's disease. J. Neural Transm. 114, 857-862.
75. Uotila L., (1981) Thioesters of glutathione. Methods Enzymol. 77, 424-430.
76. Waak J., and, Dringen R., (2006) Formation and rapid export of the monochlorobimane-glutathione conjugate in cultured rat astrocytes. Neurochem. Res. 31, 1409-1416.
77. Wallace K. B., Eells J. T., Madeira V. M., Cortopassi G., and, Jones D. P., (1997) Mitochondria-mediated cell injury. Symposium overview. Fund. Appl. Toxicol. 38, 23-37.
78. Walz W., and, Mukerji S., (1988) Lactate release from cultured astrocytes and neurons: a comparison. Glia 1, 366-370.
79. Yao H., and, Haddad G. G., (2004) Calcium and pH homeostasis in neurons during hypoxia and ischemia. Cell Calcium 36, 247-255.
80. Zararsiz I., Kus I., Akpolat N., Songur A., Ogeturk M., and, Sarsilmaz M., (2006) Protective effects of omega-3 essential fatty acids against formaldehyde-induced neuronal damage in prefrontal cortex of rats. Cell Biochem. Funct. 24, 237-244.
81. Zararsiz I., Kus I., Ogeturk M., Akpolat N., Kose E., Meydan S., and, Sarsilmaz M., (2007) Melatonin prevents formaldehyde-induced neurotoxicity in prefrontal cortex of rats: An immunohistochemical and biochemical study. Cell Biochem. Funct. 25, 413-418.
82. Zararsiz I., Meydan S., Sarsilmaz M., Songur A., Ozen O. A., and, Sogut S., (2011) Protective effects of omega-3 essential fatty acids against formaldehyde-induced cerebellar damage in rats. Toxicol. Ind. Health 27, 489-495.
83. Zwingmann C., and, Leibfritz D., (2003) Regulation of glial metabolism studied by 13C-NMR. NMR Biomed. 16, 370-399.