Association of inflammatory response and oxidative injury in the pathogenesis of liver steatosis and insulin resistance following subchronic exposure to malathion in rats

Environmental Toxicology and Pharmacology

Volumn 38, Issue 2, 2014, Pages 542-553

  Lasram, Mohamed Montassar ^a   Dhouib, Ines Bini ^a,c   Bouzid, Kahna ^b   Lamine, Aicha Jrad ^a   Annabi, Alya ^a   Belhadjhmida, Nadia ^c   Ahmed, Malika Ben ^c   Fazaa, Saloua El ^a   Abdelmoula, Jaouida ^b   Gharbi, Najoua ^a  

^a FACULTÉ DES SCIENCES DE TUNIS   (Tunisia)

^b CHARLES NICOLLE HOSPITAL   (Tunisia)

^c PASTEUR INSTITUTE OF TUNIS   (Tunisia)

Author keywords

Hepatosteatosis; Inflammation; Insulin resistance; Malathion; Oxidative stress

Indexed keywords

ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; CATALASE; CHOLINESTERASE; GAMMA INTERFERON; GLUCOSE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; GLYCOGEN; GLYCOSYLATED HEMOGLOBIN; INSULIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LACTATE DEHYDROGENASE; MALATHION; MALONALDEHYDE; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; BIOLOGICAL MARKER; CD3 ANTIGEN; CD4 ANTIGEN; CYTOKINE; LIPID; GLUCOSE BLOOD LEVEL; PESTICIDE;

ADULT; ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; CD3+ T LYMPHOCYTE; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; FATTY LIVER; GLUCOSE BLOOD LEVEL; HEMOGLOBIN DETERMINATION; HOMEOSTASIS MODEL ASSESSMENT FOR INSULIN RESISTANCE; INFLAMMATION; INSULIN RESISTANCE; INSULINEMIA; LIPID PEROXIDATION; LIVER TOXICITY; LIVER WEIGHT; MALE; METABOLIC PARAMETERS; NEUTROPHIL COUNT; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; BODY WEIGHT; PATHOPHYSIOLOGY; PLASMA; ANIMAL; BLOOD; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION REGULATION; IMMUNOLOGY; MAXIMUM TOLERATED DOSE; METABOLISM; PATHOLOGY; TOXIC HEPATITIS; WISTAR RAT;

ANIMALS; BIOLOGICAL MARKERS; BLOOD GLUCOSE; CYTOKINES; DRUG-INDUCED LIVER INJURY; FATTY LIVER; GENE EXPRESSION REGULATION; INFLAMMATION; INSULIN RESISTANCE; LIPID PEROXIDATION; MALATHION; MALE; MAXIMUM TOLERATED DOSE; OXIDATIVE STRESS; PESTICIDES; RATS; RATS, WISTAR;

EID: 84907971862     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2014.08.007     Document Type: Article

References (74)

1. Abdollahi M., Donyavi M., Pournourmohammadi S., Saadat M. Hyperglycemia associated with increased hepatic glycogen phosphorylase and phosphoenolpyruvate carboxykinase in rats following subchronic exposure to malathion. Comp. Biochem. Physiol. Part C 2004, 137:343-347.
2. Aboul-Soud M.A.M., Al-Othman A.M., El-Desoky G.E., Al-Othman Z.A., Yusuf K., Ahmad J., Al-Khedhairy A.A. Hepatoprotective effects of Vitamin E/Selenium against malathion-induced injuries on the antioxidant status and apoptosis-related gene expresison in rats. J. Toxicol. Sci. 2011, 36:285-296.
3. Abuharfeil N.M., Salim M., Von Kleist S. Augmentation of natural killer cell activity in vivo against tumour cells by some wild plants from Jordan. Phytother. Res. 2001, 15:109-113.
4. Aguirre V., Uchida T., Yenush L., Davis R., White M.F. The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J. Biol. Chem. 2000, 275:9047-9054.
5. Al-Othman M.A., Al-Othman Z.A., El-Desoky G.E., Yusuf K., Aboul-Soud M.A. Ameliorative effect of α-tocopherol and selenium on effects of Malathion on plasmatic biochemical indices and lesions in the liver of rats. Curr. Pharm. Anal. 2012, 8:214-218.
6. Alp H., Aytekin I., Hatipoglu N.K., Alp A., Ogun M. Effects of sulforophane and curcumin on oxidative stress created by acute malathion toxicity in rats. Eur. Rev. Med. Pharmacol. Sci. 2012, 16(3):144-148.
7. Andrés D., Sánchez-Reus I., Bautista M., Cascales M. Depletion of Kupffer cell function by gadolinium chloride attenuates thioacetamide-induced hepatotoxicity. Expression of metallothionein and HSP70. Biochem. Pharmacol. 2003, 66:917-926.
8. Araki E., Murakami T., Shirotani T., Kanai F., Shinohara Y., Shimada F., Mori M., Shichiri M., Ebina Y. A cluster of four Sp1 binding sites required for efficient expression of the human insulin receptor gene. J. Biol. Chem. 1991, 266(6):3944-3948.
9. Arkan M.C., Hevener A.L., Greten F.R., Maeda S., Li Z.W., Long J.M., Wynshaw-Boris A., Poli G., Olefsky J., Karin M. IKK-beta links inflammation to obesity-induced insulin resistance. Nat. Med. 2005, 11:191-198.
10. Ayud S., Verma J., Das N. Effect of endosulfan and malathion on lipid peroxidation, nitrite and TNF-α release by rat peritoneal macrophages. Int. Immunopharmacol. 2003, 3:1819-1828.
11. Banks C.N., Lein P.J. A review of experimental evidence linking neurotoxic organophosphorus compounds and inflammation. Neurotoxicology 2012, 33:575-584.
12. Bonaventura J., Schroeder W.A., Fang S. Human erythrocyte catalase: an improved method of isolation and a reevaluation of reported properties. Arch. Biochem. Biophys. 1972, 150:606-617.
13. Brown K.E., Brunt E.M., Heinecke J.W. Immunohistochemical detection of myeloperoxidase and its oxidation products in Kupffer cells of human liver. Am. J. Pathol. 2001, 159:2081-2088.
14. Cai D., Yuan M., Frantz D.F., Melendez P.A., Hansen L., Lee J., Shoelson S.E. Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NFkappaB. Nat. Med. 2005, 11:183-190.
15. Chapman S., Kadar T., Gilat E. Seizure duration following sarin exposure affects neuroinflammatory markers in the rat brain. Neurotoxicology 2006, 27:277-283.
16. Collino M., Aragno M., Castiglia S., Miglio G., Tomasinelli C., Boccuzzi G., Thiemermann C., Fantozzi R. Pioglitazone improves lipid and insulin levels in overweight rats on a high cholesterol and fructose diet by decreasing hepatic inflammation. Br. J. Pharmacol. 2010, 160:1892-1902.
17. Corsini E., Liesivuori J., Vergieva T., Van Loveren H., Colosio C. Br. J. Pharmacol. 2008, 27:671-680.
18. Dandona P., Ghanim H., Chaudhuri A., Dhindsa S., Kim S.S. Macronutrient intake induces oxidative and inflammatory stress: potential relevance to atherosclerosis and insulin resistance. Exp. Mol. Med. 2010, 42:245-253.
19. Donath M.Y., Shoelson S.E. Type 2 diabetes as an inflammatory disease. Nat. Rev. Immunol. 2011, 11:98-107.
20. Ellman G.L., Countney D.K., Andres V., Featheretone R.H. A new and colorimetric determination of acetylcholine esterase activity. Biochem. Pharmacol. 1961, 7:88-95.
21. Erqou S., Lee C.T.C., Suffoletto Echouffo-Tcheugui M.J.B., de Boer R.A., van Melle J.P., Adler A.I. Association between glycated haemoglobin and the risk of congestive heart failure in diabetes mellitus: systematic review and meta-analysis. Eur. J. Heart Fail. 2013, 15(2):185-193.
22. Fujii H., Kawada N. Inflammation and fibrogenesis in steatohepatitis. J. Gastroenterol. 2012, 47:215-225.
23. Gao Z., Zhang X., Zuberi A., Hwang D., Quon M.J., Lefevre M., Ye J. Inhibition of insulin sensitivity by free fatty acids requires activation of multiple serine kinases in 3T3-L1 adipocytes. Mol. Endocrinol. 2004, 18:2024-2034.
24. Ghosh R., Mitchell D. Effect of oxidative DNA damage in promoter elements on transcription factor binding. Nucleic Acids Res. 1999, 27(15):3213-3218.
25. Gokcimen A., Gulle K., Demirin H., Bayram D., Kocak A., Altuntas I. Effects of diazinon at different doses on rat liver and pancreas tissues. Pestic. Biochem. Phys. 2007, 87:103-108.
26. Good C., Kramer H., Somogyi M. The determination of glycogen. J. Biol. Chem. 1933, 100:485-491.
27. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980, 106:207-212.
28. Habig W.H., Pabst M.J., Jacoby W.B. Glutathione-Stransferase: the first step in mercapturic acid formation. J. Biol. Chem. 1974, 249:7130-7139.
29. Hariri A.T., Moallem S.A., Mahmoudi M., Memar B., Hosseinzadeh H. Sub-acute effects of diazinon on biochemical indices and specific biomarkers in rats: protective effects of crocin and safranal. Food Chem. Toxicol. 2010, 48(10):2803-2808.
30. Hazarika A., Sarkar S.N., Hajare S., Katarina M., Malik J.K. Infvuence of malathion pretreatment on the toxicity of anilofos in male rats: a biochemical interaction study. Toxicology 2003, 185:1-8.
31. Neal R.A. A comparison of the in vitro metabolism of parathion in the lung and liver of the rabbit. Toxicol. Appl. Phamacol. 1972, 23:123-130.
32. Horiguchi K., Kikuchi M., Kusumoto K., Fujiwara K., Kouki T., Kawanishi K., Yashiro T. Living-cell imaging of transgenic rat anterior pituitary cells in primary culture reveals novel characteristics of folliculo-stellate cells. J. Endocrinol. 2010, 204:115-123.
33. Ihle J.N., Kerr I.M. Jaks and Stats in signaling by the cytokine receptor superfamily. Trends Genet. 1995, 11:69-74.
34. IPCS IPCS, International Programme on Chemical Safety. The WHO Recommended Classification of Pesticides by Hazard and Guidelines to Classification 1996-1997 1996, Organisation Mondiale de la santé, Genève, WHO/PCS/96.3.
35. Jager J., Gremeaux T., Cormont M., Le Marchand-Brustel Y., Tanti J.F. Interleukin-1beta-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology 2007, 148:241-251.
36. Kalender S., Uzun F.G., Durak D., Demir F., Kalender Y. Malathion induced hepatotoxicty in rats: the effects of vitamins C and E. Food Chem. Toxicol. 2010, 48:633-638.
37. Koretzky G.A. Multiple roles of CD4 and CD8 in T cell activation. J. Immunol. 2010, 185:2643-2644.
38. Kraegen E.W., Clark P.W., Jenkins A.B., Daley E.A., Chisholm D.J., Storlien L.H. Development of muscle insulin resistance after liver insulin resistance in high-fat-fed rats. Diabetes 1991, 40:1397-1403.
39. Kubosaki A., Aihara M., Park B.J., Sugiura Y., Shibutani M., Hirose M., Suzuki Y., Takatori K., Sugita-Konishi Y. Immunotoxicity of nivalenol after subchronic dietary exposure to rats. Food Chem. Toxicol. 2008, 46:253-258.
40. Lasram M.M., Annabi A.B., Elj N., Selmi S., Kamoun A., El-Fazaa S., Gharbi N. Metabolic disorders of acute exposure to malathion in adult Wistar rats. J. Hazard. Mater. 2009, 163:1052-1055.
41. Lasram M.M., Annabi A.B., Rezg R., Elj N., Slimen S., Kamoun A., El-Fazza S., Gharbi N. Effect of short-time malathion administration on glucose homeostasis in Wistar rat. Pestic. Biochem. Physiol. 2008, 92:114-119.
42. Lassiter T.L., Ryde I.T., Mackillop E.A., Brown K.K., Levin E.D., Seidler F.J., Slotkin T.A. Exposure of neonatal rats to parathion elicits sex-selective reprogramming of metabolism and alters the response to a high-fat diet in adulthood. Environ. Health Perspect. 2008, 116:1456-1462.
43. Lawrence R.A., Burk R.F. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 1976, 71:952-958.
44. Lott J.A., Turner K. Evaluation of Trinder's glucose oxidase method for measuring glucose in serum and urine. Clin. Chem. 1975, 21:1754-1760.
45. Luster M.I., Simeonova P.P., Gallucci R.M., Matheson J.M., Yucesoy B. Immunotoxicology: role of inflammation in chemical-induced hepatotoxicity. Int. J. Immunopharmacol. 2000, 22:1143-1147.
46. Martin D.N., Mikhail I.S., Landgren O. Autoimmunity and hematologic malignancies: associations and mechanisms. Leuk. Lymphoma 2009, 50:541-550.
47. Matthews D.R., Hosker J.P., Rudenski A.S., Naylor B.A., Treacher D.F., Turner R.C. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985, 28:412-419.
48. Misra H.P., Fridovich I. The role of superoxide anion in the autooxidation of epinephrine and simple assay for superoxide dismutase. J. Biol. Chem. 1972, 247:3170-3175.
49. Montgomery M.P., Kamel F., Saldana T.M., Alavanja M.C., Sandler D.P. Incident diabetes and pesticide exposure among licensed pesticide applicators Agricultural Health Study, 1993-2003. Am. J. Epidemiol. 2008, 167:1235-1246.
50. Moore P.D., Yedjou C.G., Tchounwou P.B. Malathion-induced oxidative stress cytotoxicity and genotoxicity in human liver carcinoma (HepG2) cells. Environ. Toxicol. 2010, 25:221-226.
51. Mostafalou S., Eghbal M.A., Nili-Ahmadabadi A., Baeeri M., Abdollahi M. Biochemical evidence on the potential role of organophosphates in hepatic glucose metabolism toward insulin resistance through inflammatory signaling and free radical pathways. Toxicol. Ind. Health 2012, 28(9):840-851.
52. Mullane K.M., Kraemer R., Smith B. Myeloperoxidase activity as a quantitative assessment of neutrophil infiltration into ischemic myocardium. J. Pharmacol. Methods 1985, 14(3):157-167.
53. Nain S., Bour A., Chalmers C., Smits J.E. Immunotoxicity and disease resistance in Japanese quail (Coturnix coturnix japonica) exposed to malathion. Ecotoxicology 2011, 20:892-900.
54. Nili-Ahmadabadi A., Pourkhalili N., Fouladdel S., Pakzad M., Mostafalou S., Hassani S., Baeeri M., Azizi E., Ostad S.N., Hosseini R., Sharifzadeh M., Abdollahi M. On the biochemical and molecular mechanisms by which malathion induces dysfunction in pancreatic islets in vivo and in vitro. Pestic. Biochem. Physiol. 2013, 106:51-60.
55. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
56. Pineda B., Estrada-Parra S., Pedraza-Medina B., Rodriguez-Ropon A., Pérez R., Arrieta O. Interstitial transfer factor as adjuvant immunotherapy for experimental glioma. J. Exp. Clin. Cancer Res. 2005, 24:575-583.
57. Pournourmohammadi S., Farzami B., Ostad S.N., Azizi E., Abdollahi M. E-ects of malathion subchronic exposure on rat skeletal muscle glucose metabolism. Environ. Toxicol. Pharmacol. 2005, 19:191-196.
58. Pournourmohammadi S., Ostad S.N., Azizi E., Ghahremani M.H., Farzami B., Bagher Larijani M.B., Abdollahi M. Induction of insulin resistance by malathion: evidence for disrupted islets cells metabolism and mitochondrial dysfunction. Pestic. Biochem. Physiol. 2007, 88:346-352.
59. Raafat N., Abass M.A., Salem H.M. Malathion exposure and insulin resistance among a group of farmers in Al-Sharkia governorate. Clin. Biochem. 2012, 45:1591-1595.
60. Rahimi R., Abdollahi M. A review on the mechanisms involved in hyperglycemia induced by organophosphorus pesticides. Pestic. Biochem. Physiol. 2007, 88:115-121.
61. Rains J.L., Jain S.K. Oxidative stress, insulin signaling, and diabetes. Free Radic. Biol. Med. 2011, 50(5):567-575.
62. Ramon O., Wong H.K., Joyeux M., Riondel J., Halimi S., Ravanat J.L., Favier A., Cadet J., Faure P. 2'-Deoxyguanosine oxidation is associated with decrease in the DNA-binding activity of the transcription factor sp1 in liver and kidney from diabetic and insulinresistant rats. Free Radic. Biol. Med. 2001, 30(1):107-118.
63. Ranjbar A., Ghahremani M.H., Sharifzadeh M., Golestani A., Ghazi-Khansari M., Baeeri M., Abdollahi M. Protection by pentoxifylline of malathion-induced toxic stress and mitochondrial damage in rat brain. Hum. Exp. Toxicol. 2010, 29(10):851-864.
64. Rezg R., Mornagui B., El-Arbi M., Kamoun A., El-Fazaa S., Gharbi N. Effect of subchronic exposure to malathion on glycogen phosphorylase and hexokinase activities in rat liver using native PAGE. Toxicology 2006, 223(1-2):9-14.
65. Rezg R., Mornagui B., Benahmed M., Gharsalla Chouchane S., Belhajhmida N., Abdeladhim M., Kamoun A., El-Fazaa S., Gharbi N. Malathion exposure modulates hypothalamic gene expression and induces dyslipedemia in Wistar rats. Food Chem. Toxicol. 2010, 48(6):1473-1477.
66. Rieusset J., Bouzakri K., Chevillotte E., Ricard N., Jacquet D., Bastard J.P., Laville M., Vidal H. Suppressor of cytokine signaling 3 expression and insulin resistance in skeletal muscle of obese and type 2 diabetic patients. Diabetes 2004, 53:2232-2241.
67. Rodríguez-Cabezas M.E., Camuesco D., Arribas B., Garrido-Mesa N., Comalada M., Bailón E., Cueto-Sola M., Utrilla P., Guerra-Hernández E., Pérez-Roca C., Gálvez J., Zarzuelo A. The combination of fructooligosaccharides and resistant starch shows prebiotic additive effects in rats. Clin. Nutr. 2010, 29:832-839.
68. Saafi E.B., Louedi M., Elfeki A., Zakhama A., Najjar M.F., Hammami M., Achour L. Protective effect of date palm fruit extract (Phoenix dactylifera L) on dimethoate induced-oxidative stress in rat liver. Exp. Toxicol. Pathol. 2011, 63:433-441.
69. Sabio G., Cavanagh-Kyros J., Ko H.J., Jung D.Y., Gray S., Jun J.Y., Barrett T., Kim J.K., Davis R.J. Role of muscle JNK1 in obesity-induced insulin resistance. Mol. Cell. Biol. 2010, 30:106-115.
70. Sabio G., Cavanagh-Kyros J., Ko H.J., Jung D.Y., Gray S., Jun J.Y., Barrett T., Mora A., Kim J.K., Davis R.J. Prevention of steatosis by hepatic JNK1. Cell Metab. 2009, 10:491-498.
71. Vosough-Ghanbari S., Sayyar P., Pournourmohammadi S., Aliahmadi S., Ostad N.S., Abdollahi M. Stimulation of insulin and glucagon synthesis in rat Langerhans islets by malathion in vitro Evidence for mitochondrial interaction and involvement of subcellular noncholinergic mechanisms. Pestic. Biochem. Physiol. 2007, 89:130-136.
72. Yang M.C., McLean A.J., Rivory L.P., Le Couteur D.G. Hepatic disposition of neurotoxins and pesticides. Pharmacol. Toxicol. 2000, 87:286-291.
73. Yurumez Y., Cemek M., Yavuz Y., Birdane Y., Buyukokuroglu M.E. Beneficial effect of N-acetylcysteine against organophosphate toxicity in mice. Biol. Pharm. Bull. 2007, 30:490-494.
74. Zou C.H., Shao J.H. Role of adipocytokines in obesity-associated insulin resistance. J. Nutr. Biochem. 2008, 19:277-286.