Modulatory effect of l-glutamine on 2,3,7,8 tetrachlorodibenzo-p-dioxin- induced liver injury in rats

Toxicology and Industrial Health

Volumn 28, Issue 7, 2012, Pages 663-672

  Türkez, Hasan ^a   Geyikoǧlu, Fatime ^a   Yousef, Mokhtar I ^b  

^a ATATÜRK UNIVERSITY   (Turkey)

^b ALEXANDRIA UNIVERSITY   (Egypt)

Author keywords

antioxidant enzymes; histopathology; l glutamine; liver; micronucleus assay; rat; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; CATALASE; GLUTAMINE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; LIVER CELL; LIVER INJURY; MALE; NONHUMAN; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; CATALASE; DRUG-INDUCED LIVER INJURY; GLUTAMINE; HISTOCYTOCHEMISTRY; LIVER; MALE; MICRONUCLEUS TESTS; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE; TETRACHLORODIBENZODIOXIN;

ANIMALIA; RATTUS;

EID: 84864133893     PISSN: 07482337     EISSN: 14770393     Source Type: Journal    
DOI: 10.1177/0748233711420474     Document Type: Article

References (93)

1. Aebi H Methods in Enzymology. Academic Press. Packer L, ed. 1984: 1-126.
2. Akerboom TPM, Sies H. Assay of glutathione, glutathione disulfide and glutathione mixed disulfides in biological samples. Methods in Enzymology. 1981 ; 77: 373-382
3. Austgen TR, Chen MK, Flynn TC, Souba WW. The effects of endotoxin on the splanchnic metabolism of glutamine and related substrates. The Journal of Trauma. 1991 ; 31 (6). 742-751
4. Babu R, Eaton S, Drake DP, Spitz L, Pierro A. Glutamine and glutathione counteract the inhibitory effects of mediators of sepsis in neonatal hepatocytes. Journal of Pediatric Surgery. 2001 ; 36 (2). 282-286
5. Bergamini E, Bombara M, Del Roso A, Gori Z, Masiello P, Masini M, et al. The regulation of liver protein degradation by aminoacids in vivo. Effects of glutamine and leucine. Archives of Physiology and Biochemistry. 1995 ; 103 (4). 512-515
6. Berk L, James J, Schwartz A, Hug E, Mahadevan A, Samuels M, et al. A randomized, double-blind, placebo-controlled trial of a beta-hydroxyl beta-methyl butyrate, glutamine, and arginine mixture for the treatment of cancer cachexia (RTOG0122). Supportive Care in Cancer. 2008 ; 16 (10). 1179-1188
7. Bock KW. Aryl hydrocarbon or dioxin receptor: biologic and toxic responses. Reviews of Physiology, Biochemistry, and Pharmacology. 1994 ; 125: 1-42
8. Bort JA, Stern B, Borth N. CHO-K1 host cells adapted to growth in glutamine-free medium by FACS-assisted evolution. Biotechnology Journal. 2010 ; 5 (10). 1090-1097
9. Boutros PC, Yan R, Moffat ID, Pohjanvirta R, Okey AB. Transcriptomic responses to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in liver: comparison of rat and mouse. BMC Genomics. 2008 ; 9: 419
10. Boverhof DR, Burgoon LD, Tashiro C, Sharratt B, Chittim B, Harkema JR, et al. Comparative toxicogenomic analysis of the hepatotoxic effects of TCDD in Sprague Dawley rats and C57BL/6 mice. Toxicological Sciences. 2006 ;: 398-416
11. Cano KE, Li YJ, Chen Y. NMR metabolomic profiling reveals new roles of sumoylation in DNA damage response. Journal of Proteome Research. 2010 ; 9 (10). 5382-5388
12. Castroe Silva O, Franco CFF, Souza MEJ, Picinato MAN, Zucoloto S, Ceneviva R. Alterações hepáticas e níveis séricos de aminotransferases 24 horas após ligadura do ducto hepático em ratos. Acta Cirurgica Brasileira. 1991 ; 6: 159-161
13. Chopra M, Gährs M, Haben M, Michels C, Schrenk D. Inhibition of apoptosis by 2,3,7,8-tetrachlorodibenzo-p-dioxin depends on protein biosynthesis. Cell Biology and Toxicology. 2010 ; 26 (4). 391-401
14. Ciftci O, Ozdemir I, Tanyildizi S, Yildiz S, Oguzturk H. Antioxidative effects of curcumin, {beta}-myrcene and 1,8-cineole against 2,3,7,8- tetrachlorodibenzo-p-dioxin-induced oxidative stress in rats liver. Toxicology and Industrial Health. 2011 ; 27 (5). 447-453
15. Clark RH, Feleke G, Din M, Yasmin T, Singh G, Khan FA, et al. Nutritional treatment for acquired immunodeficiency virus-associated wasting using beta-hydroxy beta-methylbutyrate, glutamine, and arginine: a randomized, double-blind, placebo-controlled study. Journal of Parenteral and Enteral Nutrition. 2000 ; 24 (3). 133-139
16. Colombo SL, Palacios-Callender M, Frakich N, De Leon J, Schmitt CA, Boorn L, et al. Anaphase-promoting complex/cyclosome-Cdh1 coordinates glycolysis and glutaminolysis with transition to S phase in human T lymphocytes. The Proceedings of the National Academy of Sciences of the United States of America. 2010 ; 107 (44). 18868-18873
17. Czepiel J, Biesiada G, Gajda M, Szczepański W, Szypuła K, Dabrowski Z, et al. The effect of TCDD dioxin on the rat liver in biochemical and histological assessment. Folia Biologica (Kraków. 2010 ; 58 ((1-2)). 85-90
18. Darmaun D. Role of glutamine depletion in severe illness. Diabetes, Nutrition & Metabolism. 2000 ; 13 (1). 25-30
19. Fenoglio I, Corazzari I, Francia C, Bodoardo S, Fubini B. The oxidation of glutathione by cobalt/tungsten carbide contributes to hard metal-induced oxidative stress. Free Radical Research. 2008 ; 42 (8). 437-745
20. Forgacs AL, Burgoon LD, Lynn SG, LaPres JJ, Zacharewski T. Effects of TCDD on the expression of nuclear encoded mitochondrial genes. Toxicology and Applied Pharmacology. 2010 ; 246 (1-2). 58-65
21. Gan LQ, Fu YX, Liu X, Qiu L, Wu SD, Tian XF, et al. Transforming growth factor-beta3 expression up-regulates on cleft palates induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in mice. Toxicology and Industrial Health. 2009 ; 25 (7). 473-478
22. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, et al. c-Myc suppression of miR-23 enhances mitochondrial glutaminase and glutamine metabolism. Nature. 2009 ; 458 (7239). 762-765
23. Gonzales S, Polizio AH, Erario MA, Tomaro ML. Glutamine is highly effective in preventing in vivo cobalt-induced oxidative stress in rat liver. World Journal of Gastroenterology. 2005 ; 11 (23). 3533-3538
24. Grassman JA, Masten NA, Walker NJ, Lucier GW. Animal models of human response to dioxins. Environmental Health Perspectives. 1998 ; 106 (suppl 2). 761-775
25. Halder AK, Adhikary N, Maity MK, Jha T. Synthesis, pharmacological activity and comparative QSAR modeling of 1,5-N,N'-substituted-2-(substituted naphthalenesulphonyl) glutamamides as possible anticancer agents. European Journal of Medicinal Chemistry. 2010 ; 45 (5). 1760-1771
26. Halliwell B, Gutteridge JMC. Role of free radicals and catalytic metal ions in human disease: an overview. Methods in Enzymology. 1990 ; 186: 1-85
27. Hassoun EA, Li F, Abushaban A, Stohs SJ. The relative abilities of TCDD and its congeners to induce oxidative stress in the hepatic and brain tissues of rats after subchronic exposure. Toxicology. 2000 ; 145 (2-3). 103-113
28. Hassoun EA, Li F, Abushaban A, Stohs SJ. Production of superoxide anion, lipid peroxidation and DNA damage in the hepatic and brain tissues of rats after subchronic exposure to mixtures of TCDD and its congeners. Journal of Applied Toxicology. 2001 ; 21 (3). 211-219
29. Hong RW, Rounds JD, Helton WS, Robinson MK, Wilmore DW. Glutamine preserves liver glutathione after lethal hepatic injury. Annals of Surgery. 1992 ; 215 (2). 114-119
30. Huff J, Lucier G, Tritscher A. Carcinogenicity of TCDD: experimental, mechanistic, and epidemiologic evidence. Review of Pharmacology and Toxicology. 1994 ; 34: 343-372
31. Hung YC, Huang GS, Sava VM, Blagodarsky VA, Hong MY. Protective effects of tea melanin against 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity: antioxidant activity and aryl hydrocarbon receptor suppressive effect. Biological & Pharmaceutical Bulletin. 2006 ; 29 (11). 2284-2291
32. IARC monographs on the evaluation of carcinogenic risk of chemicals to humans. Lyon, France: International Agency for Research on Cancer ; 1997: 666.
33. Jain SK, Pemberton PW, Smith A, McMahon RF, Burrows PC, Aboutwerat A, et al. Oxidative stress in chronic hepatitis C: not just a feature of late stage disease. Journal of Hepatology. 2002 ; 36 (6). 805-811
34. Jia CJ, Dai CL, Zhang X, Cui K, Xu F, Xu YQ. Alanyl-glutamine dipeptide inhibits hepatic ischemia-reperfusion injury in rats. World Journal of Gastroenterology. 2006 ; 12 (9). 1373-1378
35. Jin MH, Hong CH, Lee HY, Kang HJ, Han SW. Enhanced TGF-α1 is involved in 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) induced oxidative stress in C57BL/6 mouse testis. Toxicology Letters. 2008 ; (3). 178 202-209
36. Kaufmann Y, Spring P, Klimberg VSY. Oral glutamine prevents DMBA-induced mammary carcinogenesis via upregulation of glutathione production. Journal of Nutrition. 2008 ; 24 (5). 462-469
37. Kawada H, Kojima M, Kimura T, Natori S, Sasaki K, Sasaki H. Effect of 5-S-GAD on UV-B-induced cataracts in rats. Japanese Journal of Ophthalmology. 2009 ; 53 (5). 531-535
38. Kidd PM. Glutathione: systemic protectant against oxidative and free radical damage. Alternative Medicine Review. 1997 ; 1: 155-176
39. Komano T, Egashira Y, Sanada H. GLN and L-Ser suppress the D-galactosamine-induced IL-18 expression and hepatitis. Biochemical and Biophysical Research Communications. 2008 ; 372 (4). 688-690
40. Kopec AK, Lyle DB, Daher IA, Bryan DM, Colleen T, Potter D, et al. PCB153-elicited hepatic responses in the immature, ovariectomized C57BL/6 mice: comparative toxicogenomic effects of dioxin and non-dioxin-like ligands. Toxicology and Applied Pharmacology. 2010 ; 243 (3). 359-371
41. Koyama K, Ito K, Ouchi K, Sato T. Mitochondrial function of rat liver in biliary obstruction. Tohoku Journal of Experimental Medicine. 1980 ; 131 (1). 59-69
42. Kuhls DA, Rathmacher JA, Musngi MD, Frisch DA, Nielson J, Barber A, et al. Betahydroxy-beta-methylbutyrate supplementation in critically ill trauma patients. The Journal of Trauma. 2007 ; 62 (1). 125-132
43. Kulkarni PS, Crespo JG, Afonso CA. Dioxins sources and current remediation technologies-a review. Environment International. 2008 ; 34 (1). 139-153
44. Kumar HS, Anandan R. Biochemical studies on the cardioprotective effect of glutamine on tissue antioxidant defense system in isoprenaline-induced myocardial infarction in rats. Journal of Clinical Biochemistry & Nutrition. 2007 ; 40 (1). 49-55
45. Lacey JM, Wilmore DW. Is glutamine a conditionally essential amino acid?. Nutrition Reviews. 1990 ; 48 (8). 297-309
46. Lawrence RA, Burk RF. Glutathione peroxidase activity in selenium-deficient rat liver. Biochemical and Biophysical Research Communications. 1976 ; 71 (4). 952-958
47. Lee DH, Jacobs DR. Jr,. Is serum gamma-glutamyltransferase a marker of exposure to various environmental pollutants?. Free Radical Research. 2009 ; 43 (6). 533-537
48. Lee JH, Wada T, Febbraio M, He J, Matsubara T, Lee MJ, et al. A novel role for the dioxin receptor in fatty acid metabolism and hepatic steatosis. Gastroenterology. 2010 ; 139 (2). 653-663
49. Lee YS, Jin DQ, Park SH, Han SY, Kim HS, Jeong TC, et al. 2,3,7,8-tetrachlorobenzo-p-dioxin inhibits proliferation of SK-N-SH human neuronal cells through decreased production of reactive oxygen species. Free Radical Research. 2002 ; 36 (12). 1283-1289
50. Li CH, Shi B, He W, Meng T. Is it possible to antagonize 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced cleft palate by prenatal administration of folic acid?. An experimental study. Toxicology and Industrial Health. 2010 ; 26 (5). 281-286
51. Lin MT, Kung SP, Yeh SL, Lin C, Lin TH, Chen KH, et al. The effect of glutamine-supplemented total parenteral nutrition on nitrogen economy depends on severity of diseases in surgical patients. Clinical Nutrition. 2002 ; 21 (3). 213-218
52. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with Folin phenol reagent. The Journal of Biological Chemistry. 1951 ; 193 (1). 265-275
53. Marcora S, Lemmey A, Maddison P. Dietary treatment of rheumatoid cachexia with beta-hydroxy-beta-methylbutyrate,glutamine and arginine: a randomized controlled trial. Clinical Nutrition. 2005 ; 24 (3). 442-454
54. Margaritis VG, Filos KS, Michalaki MA, Scopa CD, Spiliopoulou I, Nikolopoulou VN, et al. Effect of oral glutamine administration on bacterial translocation, endotoxemia, liver and ileal morphology, and apoptosis in rats with obstructive jaundice. World Journal of Surgery. 2005 ; 29 (10). 1329-1334
55. Mates JM, Pérez-Gómez C, Núñez de Castro I, Asenjo M, Márquez J. Glutamine and its relationship with intracellular redox status, oxidative stress and cell proliferation/death. The International Journal of Biochemistry. 2002 ; 34 (5). 439-458
56. May PE, Barber A, D'Olimpio JT, Hourihane A, Abumrad NN. Reversal of cancer-related wasting using oral supplementation with a combination of [beta]-hydroxy-[beta]-methylbutyrate, arginine, and glutamine. The American Journal of Surgery. 2002 ; 183 (4). 471-479
57. Misra HP, Fridovich K. The generation of superoxide radical during the autooxidation of hemoglobin. The Journal of Biological Chemistry. 1972 ; 247 (21). 6960-6962
58. Moffat ID, Boutros PC, Chen H, Okey AB, Pohjanvirta R. Aryl hydrocarbon receptor (AHR)-regulated transcriptomic changes in rats sensitive or resistant to major dioxin toxicities. BMC Genomics. 2010 ; 11: 263
59. Müller T, Topp T, Weismüller K, Kwapisz M, Engel J. The influence of upstream IL-2-330 (T/G) and TNF-α-308 (A/G) polymorphisms on glutamine-supplemented cytokine release. Scandinavian Journal of Immunology. 2010 ; 72 (4). 365-371
60. Nader MA, el-Agamy DS, Suddek GM. Protective effects of propolis and thymoquinone on development of atherosclerosis in cholesterol-fed rabbits. Archives of Pharmacal Research. 2010 ; 33 (4). 637-643
61. Nakamura M, Saito H, Ikeda M, Hokari R, Kato N, Hibi T, et al. An antioxidant resveratrol significantly enhanced replication of hepatitis C virus. World Journal of Gastroenterology. 2010 ; 16 (2). 184-192
62. Guide for the Care and Use of Laboratory Animals. 1996 ;:
63. Nelson DL, Cox MM Lehninger Principles of Biochemistry. New York, NY: Freeman ; 2008:
64. Neu JJ, DeMarco V, Li N. Glutamine: clinical applications and mechanisms of action. Current Opinion in Clinical Nutrition & Metabolic Care. 2002 ; 5 (1). 69-75
65. N'Jai A, Boverhof DR, Dere E, Burgoon LD, Tan YS, Rowlands JC, et al. Comparative temporal toxicogenomic analysis of TCDD- and TCDF-mediated hepatic effects in immature female C57BL/6 mice. Toxicological Science. 2008 ; 103 (2). 285-297
66. Palmer TEA, Griffiths RD, Jones C. Effect of parenteral L-glutamine on muscle in the very severely ill. Nutrition. 1996 ; 12 (5). 316-320
67. Park SH, Lee HW, Cao W. Screening of nitrosative stress resistance genes in Coxiella burnetii: involvement of nucleotide excision repair. Microbial Pathogenesis. 2010 ; 49 (6). 323-329
68. Pereira MB, Freitas RL, Assis MA, Silva RF, Fonteles MM, Freitas RM, et al. Study pharmacologic of the GABAergic and glutamatergic drugs on seizures and status epilepticus induced by pilocarpine in adult Wistar rats. Letters. 2007 ; 419 (3). 253-257
69. Ralpha DM, Robinsona SR, Campbella MS, Bishop GM. Histidine, cystine, glutamine, and threonine collectively protect astrocytes from the toxicity of zinc. Free Radical Biology & Medicine. 2010 ; 49 (4). 649-657
70. Reyes-Hernánde OD, Mejía-García A, Sánchez-Ocampo EM, Cabañas-Cortés MA, Ramírez P, Chávez-González L, et al. Ube2l3 gene expression is modulated by activation of the aryl hydrocarbon receptor: implications for p53 ubiquitination. Biochemical Pharmacology. 2010 ; 80 (6). 932-940
71. Rohde T, MacLean DA, Klarlund Pedersen B. Glutamine, lymphocyte proliferation and cytokine production. Scandinavian Journal of Immunology. 1996 ; 44 (6). 648-650
72. Roth E, Oehler R, Manhart N, Exner R, Wessner B, Strasser E, et al. Regulative potential of glutamine-relation to glutathione metabolism. Nutrition. 2002 ; 18 (3). 217-221
73. Sakamoto MK, Mima S, Tanimura T. A morphological study of liver lesions in Xenopus larvae exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) with special reference to apoptosis of hepatocytes. Journal of Environmental Pathology, Toxicology and Oncology. 1995 ; 14 (2). 69-82
74. Schauer RJ, Kalmuk S, Gerbes AL, Leiderer R, Meissner H, Schildberg FW, et al. Intravenous administration of glutathione protects parenchymal and non-parenchymal liver cells against reperfusion injury following rat liver transplantation. World Journal of Gastroenterology. 2004 ; 10 (6). 864-870
75. Scrogi K. Levels and congener distributions of PCDDs. PCDFs and dioxin-like PCBs in environmental and human samples: a review. Environmental Chemistry Letters. 2008 ;: 1-28
76. Shertzer HG. Protective effects of the antioxidant 4b,5,9b,10- tetrahydroindeno[1,2-b]indole against TCDD toxicity in C57BL/6J mice. International Journal of Toxicology. 2010 ; 29 (1). 40-48
77. Skrzydlewska E, Farbiszewski R. Decreased antioxidant defense mechanisms in rat liver after methanol intoxication. Free Radical Research. 1997 ; 27 (4). 369-375
78. Slezak BP, Hatch GE, DeVito MJ, Diliberto JJ, Slade R, Crissman K, et al. Oxidative stress in female B6C3F1 mice following acute and subchronic exposure to 2,3,7,8-tetrachlorodibenzo-pdioxin (TCDD). Toxicological Science. 2000 ; 54 (2). 390-398
79. Suzuki H, Takasawa H, Kobayashi K, Terashima Y, Shimada Y, Ogawa I, et al. Evaluation of a liver micronucleus assay with 12 chemicals using young rats (II): a study by the collaborative study group for the micronucleus test/Japanese environmental mutagen society-mammalian mutagenicity study group. Mutagenesis. 2009 ; 24 (1). 9-16
80. Svegliati Baroni G, D'Ambrosio L, Ferretti G, Casini A, Di Sario A, Salzano R, et al. Fibrogenic effect of oxidative stress on rat hepatic stellate cells. Hepatology. 1998 ; 27 (3). 720-726
81. Szijarto A. Methods of increasing ischemic tolerance in liver surgery. Magyar Sebeszet. 2008 ; 61 (3). 128-135
82. Thebault S, Deniel N, Galland A, Lecleire S, Charlionet R, Coëffier M, et al. Proteomics human duodenal proteome modulations by glutamine and antioxidants. Proteomics. Clinical Applications. 2010 ; 4 (3). 325-336
83. Todorova VK, Kaufmann Y, Hennings L, Klimberg VS. Oral glutamine protects against acute doxorubicin-induced cardiotoxicity of tumor-bearing rats. Journal of Nutrition. 2010 ; 140 (1). 44-48
84. Tung-Kwang L, O'Brien KF, Wang W, Johnke RM, Sheng C, Benhabib SM, et al. Radioprotective effect of American ginseng on human lymphocytes at 90 minutes post-irradiation: a study of 40 cases. Journal of Alternative and Complementary Medicine. 2010 ; 16 (5). 561-567
85. Twaroski LW, O'Brien ML, Robertson LW. Effects of selected polychlorinated biphenyl (PCB) congeners on hepatic glutathione, glutathione-related enzymes and selenium status: implications for oxidative stress. Biochemical Pharmacology. 2001 ; 62 (3). 273-278
86. Urbina JJO, Jorquera F, Culebras J, Villares C, González-Gallego J, Tuñón MJ. Influencia de la formulación de la glutamina en sus efectos sobre los sistemas antioxidantes y de destoxificación hepática en la rata. Nutrición Hospitalaria. 2004 ; 19 (2). 73-82
87. Wang HX, Ma XC, Deng QL, Li D. Cytotoxicity of flutamide and 2-hydroxyflutamide and their effects on CYP1A2 mRNA in primary rat hepatocytes. Acta Pharmacologica Sinica. 2002 ; 23 (6). 562-566
88. Xia JZ, Wu ZH. Metabolism of glutamine-dipeptide supplemented TPN decreasing injuries of liver and intestine in intraperitoneal chemotherapy rats. Parenteral and Enteral Nutrition. 1997 ; 4: 78-82
89. Xu JP, Yin YP, Zhou XQ. Effect of vitamin E on reproductive function in the mice treated with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicology and Industrial Health. 2008 ; 24 (9). 595-601
90. Yang H, Ierapetritou MG, Roth CM. Effects of amino acid transport limitations on cultured hepatocytes. Biophysical Chemistry. 2010 ; 152 (1-3). 89-98
91. Yang RR. The effect of glutamine on cholestasis caused by total parenteral nutrition. Zhonghua Wai Ke Za Zhi. 1993 ; 31 (2). 94-96
92. Yilmaz S, Aksoy H, Unal F, Celik M, Yüzbaşioǧlu D. Genotoxic action of fungicide Conan 5FL (hexaconazole) on mammalian cells in vivo and in vitro. Genetika. 2008 ; 44 (3). 323-328
93. Yin HP, Xu JP, Zhou XQ, Wang Y. Effects of Vitamin E on reproductive hormones and testis structure in chronic dioxin-treated mice. Toxicology and Industrial Health. 2011 ;: