Interplay between pro-inflammatory cytokines and brain oxidative stress biomarkers: Evidence of parallels between butyl paraben intoxication and the valproic acid brain physiopathology in autism rat model

Cytokine

Volumn 71, Issue 2, 2015, Pages 173-180

  Hegazy, Hoda G ^a   Ali, Elham H A ^a   Elgoly, Amany H Mahmoud ^b  

^a Ain Shams University   (Egypt)

^b NATIONAL ORGANIZATION FOR DRUG CONTROL AND RESEARCH NODCAR   (Egypt)

Author keywords

Autism animal model; Brain cytokine; Brain oxidative stress; Butyl paraben; Valproic acid

Indexed keywords

3 NITROTYROSINE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; BUTYL PARABEN; GLUTATHIONE; GLUTATHIONE DISULFIDE; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; TYROSINE; VALPROIC ACID; 3-NITROTYROSINE; 4 HYDROXYBENZOIC ACID ESTER; AUTACOID; BIOLOGICAL MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTISM; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FEMALE; MALE; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; RAT; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; BRAIN DISEASE; CHEMICALLY INDUCED; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MITOCHONDRION; PATHOLOGY; PREGNANCY; WISTAR RAT;

ADENOSINE MONOPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; AUTISTIC DISORDER; BIOLOGICAL MARKERS; BRAIN; BRAIN DISEASES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FEMALE; GLUTATHIONE; GLUTATHIONE DISULFIDE; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; MITOCHONDRIA; OXIDATIVE STRESS; PARABENS; PREGNANCY; RATS, WISTAR; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE; VALPROIC ACID;

EID: 84910011523     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2014.10.027     Document Type: Article

References (70)

1. Dalton R., Forman M.A., Boris N.W. Pervasive developmental disorders and childhood psychosis. Nelson textbook of pediatries 2008, vol. 17. WB Saunder, Philadelphia, p. 93-94.
2. Deth R., Muratone C., Benzecry J., Power-Charnitsky V.A., Waly M. How environmental and genetic factors combine to cause autism: a redox/methylation hypothesis. Neurotoxicology 2008, 29:190-201.
3. Chauhan A., Chauhan V., Brown W.T. Autism: oxidative stress, inflammation and immune abnormalities 2009, CRC Press, Taylor and Francis group, Florida.
4. Kern J.K., Jones A.M. Evidence of toxicity, oxidative stress and neuronal insult in autism. J Toxicol Enviro Health B Crit Rev 2006, 9:485-499.
5. Dringen R. Metabolism and functions of glutathione in brain. Prog Neurobiol 2000, 62:649-671.
6. Perry S.W., Norman J.P., Litzburg A., Gelbard H.A. Antioxidants are required during the early critical period, but not later, for neuronal survival. J Neurosci Res 2004, 78:485-492.
7. Circu M.L., Aw T.Y. Glutathione and apoptosis. Free Radic Res 2008, 42:689-706.
8. Ballatori N., Krance S.M., Notenboon S., Shi S., Tieu K., Hammond C.L. Glutathione dysfunction and the etiology and progression of human diseases. Biol Chem 2009, 390:191-214.
9. Franco R., Cidlowski J.A. Apoptosis and glutayhione: beyond an antioxidant. Cell Death Differ 2009, 16:1303-1314.
10. Martin H.L., Teismann P. Glutathione - a review on its role and significance in Parkinson's disease. FASEB J 2009, 23:3263-3272.
11. Ghezzi P. Role of glutathione in immunity and inflammation in the lung. Int Gen Med 2011, 4:105-113.
12. Gargus J.J., Imtiaz F. Mitochondrial energy-deficient endophenotypein autism?. Am J Biochem Biotechnol 2008, 4(2):198-207.
13. Chauchan A., Audhya T., Chauhan V. Brain region-specific glutathione redox imbalance in autism. Neurochem Res 2012, 37:1681-1689.
14. Sweeten T.L., Posey D.J., Shankar S., Mc Dougles C.J. High nitric oxide production in autistic disorder: a possible role for interferon-gamma. Biol Psychiatry 2004, 55(4):434-437.
15. Deverman B.E., Patterson P.H. Cytokines and CNS development. Neuron 2009, 64:61-78.
16. Gruys E., Toussaint M.J., Neiwold T.A., Koopmans S.J. Acute phase reaction and acute phase proteins. J Zhejiang Univ Sci 2005, B6:1045-1056.
17. Cacci E., Claasen J.H., Kokia Z. Microglia-derived tumor necrosis factor alpha exaggerates death of newborn hippocampal progenitor cells in vitro. J Neurosci Res 2005, 80:789-797.
18. Stellwagen D., Malenka R.C. Synaptic scalling mediated by glial TNF-alpha. Nature 2006, 440:1054-1059.
19. Widera D., Mikenberg I., Elvers M., Kaltschmidt C., Kaltschmidt B. Tumor necrosis factor alpha triggers proliferations of adult neural stem cells via KK/Nf Kappa B signaling BMC. Neuroscience 2006, 7:64.
20. Onore C., Careage M., Ashwood M. The role of immune dysfunction in pathophysiology of autism. Brain Behav Immun 2012, 26:383-392.
21. Frederiksen H., Taxvig C., Hass U., Vinggaard A.M., Nellemann C. Higher levels of ethylparabens and butylparaben in rat amniotic fluid than in maternal plasma after subcutaneous administration. Toxicol Sci 2008, 106:376-383.
22. Shiria S., Suzuki Y., Yoshinaga J., Shiraishi H., Mizumoto Y. Urinary excretion of parabens in pregnant Japanese women. Reproduct Toxicol 2013, 35:96-101.
23. Dendrinos G., Hemelt M., Keller A. Prenatal VPA exposure and changes in sensory processing by the superior colliculus. Front Integr Neurosci 2011, 5:68. 10.3389/fnint.2011.00068.
24. Kim K.C., Kim P., Go H.S., Choi C.S., Yang S., Cheong J.H. The critical period of valproate exposure to induce autistic symptoms in Sprague-Dawley rats. Toxicol Lett 2011, 201:137-142.
25. 14C]-methyl-propyl- and butylparaben in rats after oral, topical or subcutaneous administration. Food Chem Toxicol 2012, 50:445-454.
26. Scientific Committees on Consumer Safety (SCCS. E.U.). Opinion on parabens. 14 December 2010. http://ec.europa.eu/health/scientific_committees/consumer_safety/index_en.htm.%202010.
27. Ali E.H.A., Elgoly A.H.M. Combined prenatal and postnatal butyl paraben exposure produces autism-like symptoms in offspring: comparison with valproic acid autistic model. Pharmacol Biochem Behav 2013, 111:102-110.
28. Fukuyama N., Takizawa S., Ishida H., Hoshiai K., Shinohara Y., Nakazawa H. Proxynitrite formation in focal cerebral ischemia-reperfusion on rats occurs predornimantly in the peri-infract region. J Cereb Bloodflow Metab 1998, 18:123-129.
29. Sperlágh B., Kittel A., Laytha A., Vizi E.S. ATP acts as fast neurotransmitter in rat habenula: neurochemical and enzymcytochemical evidence. Neuroscience 1995, 66:915-920.
30. Shigenaga M.K., Lee H.H., Blount B.C., Christen S., Shigeno E.T., Yip H., et al. Inflammation and NOx-induced nitration: assay for 3-nitrotyrosineby HPLC with electrochemical detection. Proc Natl Acad Sci 1997, 94:3211-3216.
31. Rose S., Melnyk S., Trusty T.A., Pavliv O., Seidel L., Li J., et al. Intracellular and extracellular redox status and free radical generation in primary immune cells from children with autism. Autism Res Treat 2012, 2012:1-10.
32. Cecchi C., Latorraca S., Sorbi S., Lantomasi T., Favilli F., Vincenzini M.T., et al. Glutathione level is altered in lymphoblasts from patients with familial Alzheimer"s disease. Neurosci Lett 1999, 275(2):152-154.
33. Bains J.S., Shaw C.A. Neurodegenerative disorders in humans: the role of glutathione in oxidative-mediated neural death. Brain Res Rev 1997, 25:335-358.
34. Cabungcal J.H., Preissmann D., Delseth C., Cuenod M., Do K.Q. Traansitory glutathione deficit during brain development induces cognitive impairment in juvenile and adult rats: relevence to schizophrenia. Neurobiol Dis 2007, 26:634-645.
35. Zimmerman A.K., Loucks F.A., Schroeder E.K., Bouchard R.J., Tylor K.L. Glutathione binding to the Bcl-2 homology-3 domain groove. J Biol Chem 2007, 282:29296-29304.
36. Vaughn A.E., Deshmukh M. Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome C. Nat Cell Biol 2008, 10:1477-1483.
37. Labri A., Kempf J., Pavelec G. Oxidative stress modulation and T Cell activation. Exp Gerontol 2007, 42(9):852-858.
38. Ando T., Mimura K., Johensson C.C. Transduction with the antioxidant enzyme catalase protects human T cells against oxidative stress. J Immunol 2008, 181(12):8382-8390.
39. Villanueva E.B., Little J.P., Lambeau G., Klegeris A. Secreted phospholipase A(2) group IIA is a neurotoxin released by stimulated human glial cells. Mol Cell Neurosci 2012, 49:430-438.
40. Vargas D.L., Nascimbene C., Krishnan C., Zimmerman A.W., Pardo C.A. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 2005, 57:67-81.
41. Pabon M.M., Bachstetter A.D., Hudsaon C.E., Gemma C., Bickford P.C. CX3CLI reduces neurotoxicity and microglial activation in a rat model of Parkinson's disease. J Neuroinflam 2011, 8:9.
42. Oprica M., Hjorth E., Spulber S., Popescu B.O., Ankarcrone M., Winblad B., et al. Studies on brain volume, Alzheimer-related proteins and cytokines in mice with chronic overexpression of IL-1 receptor antagonist. J Cell Mol Med 2007, 11:810-825.
43. Shaftel S.S., Griffin W.S., O'banion M.K. The role of interlukin-1 in neuroinflammation and Alzheimer disease: an evolving Perspective. J Neuroinflam 2008, 5:7.
44. Nolan A.M., Nolan Y.M., O'Keffe G.W. IL-1B inhibits axonal growth of developing sympathetic neurons. Mol Cell Neurosci 2011, 48:142-150.
45. Dunn A.J. Effect of cytokines and infections on brain neurochemistry. Clin Neurosci Res 2006, 6(102):52-68.
46. Parker-Athill E.C., Tan J. Maternal immune activation and autism spectrum disorder:interlukin-6 signaling as a key mechanistic pathway. Neurosignals 2010, 18:113-128.
47. Malik M., Sheikh A.M., Wen G., Spivak W., Brown W.T., Li X. Expression inflammatory cytokines, Bcl2 and Cathepsin D are altered in lymphoblasts of autism subjects. Immunobiology 2011, 216:80-85.
48. Wie H., Chadman K., Mc Closkey D.P., Sheikh A.M., Malik M., Brown W.T., et al. Brain IL-6 elevation causes neuronal circuity imbalances and mediates autism-like behaviors. Biochim Biophys Acta 2012, 1822:831-842.
49. Pickering M., Cumiskey D., O'Connor J.J. Actions of TNF-α on glutaminergic synaptic transmission in the central nervous system. Exp Physiol 2005, 90:663-670.
50. Melnynk S., Fuchs G.J., Schulz E., Lopez M., Kahier S.G., Fassell J.J. Metabolic imbalance associated with methylation dysregulation and oxidative damage in children with autism. J Autism Dev Disord 2012, 42:367-377.
51. Bishop A., Anderson J.E. No signaling in the CNS from the physiological to the pathological. Toxicology 2005, 208:193-205.
52. Samavati L., Lee I., Mathes I., Lottsspeich F., Huttemann M. Tumor necrosis factor alpha inhibits oxidative phosphorylation through tyrosine phosphorylation at subunit 1 of cytochrome c oxidase. J Biol Chem 2008, 383:21134-21144.
53. Suematsu N., Tsutsui H., Wen J., Kang D., Ikeuchi M., Ide T. Oxidative stress mediates tumor necrosis factor alpha induced mitochondrial DNA damage and dysfunction in cardiac myocytes. Circulation 2003, 107:1418-1423.
54. Balanos J.P., Peuchen S., Heales S.J., Land J.M., Clark J.B. Nitric oxide mediated inhibition of the mitochondrial respiratory chain in cultured astrocyte. J Neurochem 1994, 63:910-916.
55. Vali S., Mythri R.B., Jagatha B., Padiadpu J., Ramanujan K.S., Anderson J.K. Integrating glutathione metabolism and mitochondrial dysfunction with implications for Parkinson's disease: a dysfunction model. Neuroscience 2007, 149:917-930.
56. Calabrese V., Lodi R., Tonon C., Agata D.V., Sapienza M., Scapagnini G. Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedreich's ataxia. J Neurol Sci 2005, 233:145-162.
57. Weller R., Yu L., Yu C.A. The effects of nitric oxide on electron transport complexes. Arch Biochem Biophys 1996, 331:9-14.
58. Strobel H.W., Lu A.Y., Heidema J., Coon M.J. Phosphatidylcholine requirement in the enzymatic reduction of hemoprotein P-450 and in fatty acid, hydrocarbon, and drug hydroxylation. J Biol Chem 1970, 245:4851-4854.
59. Coon M.J. Enzyme ingenuity in biological oxidations: a trail leading to cytochrome p450. J Biol Chem 2002, 277:28351-28363.
60. Coon M.J. Cytochrome P450: nature's most versatile biological catalyst. Annu Rev Pharmacol Toxicol 2005, 45:1-25.
61. Strobel H.W., Hodgson A.V., Shen S. NADPH cytochrome P450 reductase and its structural and functional domains. Cytochrome P450-structure, mechanism and biochemistry 1995, Plenum Publishing Corp, New York, pp. 225-244. P.R. Oritz-De Montellano (Ed.).
62. Cui X., Kalsotra A., Robida A.M., Matzilevich D., Moore A.N., Boehme C.L., et al. Expression of cytochromes P450 4F4 and 4F5 in infection and injury models of inflammation. Biochim Biophys Acta 2003, 1619:325-331.
63. Kalsotra A., Strobel H.W. Cytochrome P450 4F subfamily: at the crossroads of eicosanoid and drug metabolism. Pharmacol Therapeu 2006, 112:589-611.
64. Kaptein A., Paillard V., Saunders M. Dominant negative stat3 mutant inhibits interleukin-6-induced Jak-STAT signal transduction. J Biol Chem 1996, 271:5961-5964.
65. Taga T., Kishimoto T. Gp130 and the interleukin-6 family of cytokines. Annu Rev Immunol 1997, 15:797-819.
66. Bambini-Junior V., Rodrigues L., Behr G.A., Moreira J.C., Riesgo R., Gottfried C. Animal model of autism induced by prenatal exposure to valproate: behavioral changes and liver parameters. Brain Res 2011, 1408:8-16. [Epub 2011 June 12]. 10.1016/j.brainres.2011.06.015.
67. Edalatmanesh M.A., Nikfarjam H., Vafaee F., Moghadas M. Increased hippocampal cell density and enhanced spatial memory in the valproic acid rat model of autism. Brain Res 2013, 1526(14):15-25.
68. Huang Y., Hu Z., Liu G., Zhou W., Zhang Y. Cytokines induced by long-term potentiation (LTP) recording: a potential explanation for the lack of correspondence between learning/memory performance and LTP. Neuroscience 2013, 231:432-443.
69. Camara M.L., Corrigan F., Jaehne E.J., Jawahar M.C., Anscomb H., Koerner H., et al. TNF-α and its receptors modulate complex behaviours and neurotrophins in transgenic mice. Psychoneuroendocrinology 2013, doi: pii: S0306-4530(13)00329-6. 10.1016/j.psyneuen.2013.09.010 [Epub ahead of print].
70. Brunssen S.H., Moy S.S., Toews A.D., McPherson C.A., Harry G.J. Interleukin-6 (IL-6) receptor/IL-6 fusion protein (Hyper IL-6) effects on the neonatal mouse brain: possible role for IL-6 trans-signaling in brain development and functional neurobehavioral outcomes. Brain Behav Immun 2013, 27(1):42-53. 10.1016/j.bbi.2012.08.017.