The effects of alpha-lipoic acid on breast of female albino rats exposed to malathion: Histopathological and immunohistochemical study

Pathology Research and Practice

Volumn 211, Issue 6, 2015, Pages 462-469

  Omran, Ola M ^a,b,c   Omer, Osama H ^a  

^a QASSIM UNIVERSITY   (Saudi Arabia)

^b Assiut University   (Egypt)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Breast carcinoma; Malathion; Rats; Lipoic acid

Indexed keywords

CYCLINE; MALATHION; PROTEIN BAX; PROTEIN P53; THIOCTIC ACID; ANTIOXIDANT; INSECTICIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD SAMPLING; BREAST CANCER; CANCER INCIDENCE; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; EXPOSURE; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; METABOLIC PARAMETERS; NONHUMAN; PROTECTION; PROTEIN EXPRESSION; RAT; STRESS; WISTAR RAT; ANIMAL; BREAST; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; METABOLISM; OXIDATIVE STRESS; PROCEDURES;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; BREAST; CELL PROLIFERATION; FEMALE; IMMUNOHISTOCHEMISTRY; INSECTICIDES; MALATHION; OXIDATIVE STRESS; RATS, WISTAR; THIOCTIC ACID;

EID: 84928762467     PISSN: 03440338     EISSN: 16180631     Source Type: Journal    
DOI: 10.1016/j.prp.2015.02.006     Document Type: Article

References (72)

1. Perera F.P. Environment and cancer: who are susceptible?. Science 1997, 278(5340):1068-1073.
2. Cabello G., Valenzuela M., Vilaxa A., Durán V., Rudolph I., Hrepic N., Calaf G. A rat mammary tumor model induced by the organophosphorous pesticides parathion and malathion, possibly through acetylcholinesterase inhibition. Environ. Health Perspect. 2001, 109(5):471-479.
3. Knower K.C., To S.Q., Leung Y.K., Ho S.M., Clyne C.D. Endocrine disruption of the epigenome: a breast cancer link. Endocr. Relat. Cancer. 2014, 21(2):T33-T55.
4. Falck F., Ricci A.J., Wolf M.S., Godbold J., Deckers P. Pesticides and polychlorinated biphenyl residues in human breast lipids and their relation to breast cancer. Arch. Environ. Health 1992, 47(2):143-146.
5. Wolf M.S., Toniolo P.G., Lee E.W., Rivera M., Dubin N. Blood levels of organochlorine residues and risk of breast cancer. J. Natl. Cancer Inst. 1993, 85(8):648-652.
6. Ware G.W. The Pesticide Book 2000, 52-67. Thompson Publications, Fresno, CA. 5th ed.
7. Fahmy G.H. Malathion toxicity effect on some metabolic activities in Oreochromis niloticus, the Tilapia fish. Int. J. Biosci. Biochem. Bioinform. 2012, 2(1):52-55.
8. Al-Qurainy F., Abdel-Megeed A. Phytoremediation and detoxification of two organophosphorous pesticides residues in Riyadh area. World Appl. Sci. J. 2009, 6(7):987-998.
9. Brenner L. Malathion fact sheet. J. Pestic. Reform 1992, 12:1-17.
10. Taylor P. Anticholinesterase agents. The Pharmacological Basis of Therapeutics 1990, 131-147. Pergamon Press Inc., New York. Goodman, A. Gilman, T.W. Rall, A.S. Nies, P. Taylor (Eds.).
11. Klaasen C. Nonmetallic environmental toxicants: air pollutants, solvents and vapors, and pesticides. The Pharmacological Basis of Therapeutics 1990, 1615-1635. Pergamon Press Inc., New York. Goodman, A. Gilman, T.W. Rall, A.S. Nies, P. Taylor (Eds.).
12. Calaf G.M., Echiburu-Chau C., Roy D. Organophosphorous pesticides and estrogen induce transformation of breast cells affecting p53 and c-Ha-ras genes. Int. J. Oncol. 2009, 35(5):1061-1068.
13. Calaf G.M., Echiburú-Chau C. Synergistic effect of malathion and estrogen on mammary gland carcinogenesis. Oncol. Rep. 2012, 28(2):640-646.
14. Kjeldsen L.S., Ghisari M., Bonefeld-Jørgensen E.C. Currently used pesticides and their mixtures affect the function of sex hormone receptors and aromatase enzyme activity. Toxicol. Appl. Pharmacol. 2013, 272(2):453-464.
15. Akhgari M., Abdollahi M., Kebryaeezadeh A., Hosseini R., Sazevari O. Biochemical evidence for free radical-induced lipid peroxidation as a mechanism for subchronic toxicity of malathion in blood and liver of rats. Hum. Exp. Toxicol. 2003, 22(4):205-211.
16. Dare B.J., Oyeniyi F., Olaniyan O.T. Role of antioxidant in testicular integrity. Annu. Res. Rev. Biol. 2014, 4(7):998-1023.
17. Chiumiento L., Bruschi F. Enzymatic antioxidant systems in helminth parasites. Parasitol. Res. 2009, 105(3):593-603.
18. Dal-Pizzol F., Klamt F., Frota M.L., Andrades M.E., Caregnato F.F., Vianna M.M., Schröder N., Quevedo J., Izquierdo I., Archer T., Moreira J.C. Neonatal iron exposure induces oxidative stress in adult Wistar rat. Brain Res. Dev. Brain Res. 2001, 130(1):109-114.
19. Subash S., Subramanian P. Morin a flavonoid exerts antioxidant potential in chronic hyperammonemic rats: a biochemical and histopathological study. Mol. Cell Biochem. 2009, 327(1-2):153-161.
20. D'souza A., Kurien B.T., Rodgers R., Shenoi J., Kurono S., Matsumoto H., Hensley K., Nath S.K., Scofield R.H. Detection of catalase as a major protein target of the lipid peroxidation product 4-HNE and the lack of its genetic association as a risk factor in SLE. BMC Med. Genet. 2008, 7(9):62.
21. Aebi H. Catalase in vitro. Methods Enzymol. 1984, 105:121-126.
22. Ayene I.S., Biaglow J.E., Kachur A.V., Stamato T.D., Koch C.J. Mutation in G6PD gene leads to loss of cellular control of protein glutathionylation: mechanism and implication. J. Cell Biochem. 2008, 103(1):123-135.
23. Goldhirsch A., Wood W.C., Senn H.-J., Glick G.H., Gelbe R.D. Fifth International Conference on Adjuvant Therapy of Breast Cancer, St Gallen, March 1995. International Consensus Panel on the Treatment of Primary Breast Cancer. Eur. J. Cancer 1995, 31A(11):1754-1759.
24. Wang J., Song Y., Xu S., Zhang Q., Li Y., Tang D., Jin S. Down-regulation of ICBP90 contributes to doxorubicin resistance. Eur. J. Pharmacol. 2011, 656(1-3):33-38.
25. Henderson J.W., Donatelle R.J. Complementary and alternative medicine use by women after completion of allopathic treatment for breast cancer. Altern. Ther. Health Med. 2004, 10(1):52-57.
26. McLay J.S., Stewart D., George J., Rore C., Heys S.D. Complementary and alternative medicines use by Scottish women with breast cancer. What, why and the potential for drug interactions?. Eur. J. Clin. Pharmacol. 2012, 68(5):811-819.
27. Tan A.C., Konczak I., Sze D.M., Ramzan I. Molecular pathways for cancer chemoprevention by dietary phytochemicals. Nutr. Cancer 2011, 63(4):495-505.
28. Singh M., Singh P., Shukla Y. New strategies in cancer chemoprevention by phytochemicals. Front. Biosci. (Elite Ed.) 2012, 4:426-452.
29. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39(1):44-84.
30. Kataoka H. Chromatographic analysis of lipoic acid and related compounds. J. Chromatogr. B: Biomed. Sci. Appl. 1998, 717(1-2):247-262.
31. Lachman J., Hamouz K., Orsak M., Pivec V. Potato tubers as a significant source of antioxidants in human nutrition. Rostl. Vyroba 2000, 46(5):231-236.
32. Packer L., Tritschler H.J., Wessel K. Neuroprotection by the metabolic antioxidant alpha-lipoic acid. Free Radic. Biol. Med. 1997, 22(1-2):359-378.
33. Hagen T.M., Ingersoll R.T., Lykkesfeldt J., Liu J., Wehr C.M., Vinarsky V., Bartholomew J.C., Ames A.B. (R)-Alpha-lipoic acid-supplemented old rats have improved mitochondrial function, decreased oxidative damage, and increased metabolic rate. FASEB J. 1999, 13(2):411-418.
34. Packer L., Kraemer K., Rimbach G. Molecular aspects of lipoic acid in the prevention of diabetes complications. Nutrition 2001, 17(10):888-895.
35. Yilmaz O., Ozkan Y., Yildirim M., Oztürk A.I., Erşan Y. Effects of alpha lipoic acid, ascorbic acid-6-palmitate, and fish oil on the glutathione, malonaldehyde, and fatty acids levels in erythrocytes of streptozotocin induced diabetic male rats. J. Cell Biochem. 2002, 86(3):530-539.
36. Wollin S.D., Jones P.J. Alpha-lipoic acid and cardiovascular disease. J. Nutr. 2003, 133(11):3327-3330.
37. Matsugo S., Yan L.J., Konishi T., Youn H.D., Lodge J.K., Ulrich H., Packer L. The lipoic acid analogue 1,2-diselenolane-3-pentanoic acid protects human low density lipoprotein against oxidative modification mediated by copper ion. Biochem. Biophys. Res. Commun. 1997, 240(3):819-824.
38. Arivazhagan P., Thilakavathy T., Ramanathan K., Kumaran S., Panneerselvam C. Effect of dl-alpha-lipoic acid on the status of lipid peroxidation and protein oxidation in various brain regions of aged rats. J. Nutr. Biochem. 2002, (10):619-624.
39. Russo J., Russo I.H. Mammary tumorigenesis. Prog. Exp. Tumor Res. 1991, 33:175-191.
40. Russo J., Russo I.H. Influence of differentiation and cell kinetics on the susceptibility of the rat mammary gland to carcinogenesis. Cancer Res. 1980, 40(8 Pt 1):2677-2687.
41. Russo J., Tay L.K., Russo I.H. Differentiation of the mammary gland and susceptibility to carcinogenesis. Breast Cancer Res. Treat. 1982, 2(1):5-73.
42. Russo J., Russo I.H. The etiopathogenesis of breast cancer prevention. Cancer Lett. 1995, 90(1):81-89.
43. Kanthan R., Fried I., Rueckl T., Senger J.L., Kanthan S.C. Expression of cell cycle proteins in male breast carcinoma. World J. Surg. Oncol. 2010, 8:10.
44. Arriazu R., Pozuelo J.M., Henriques-Gil N., Perucho T., Martín R., Rodríguez R., Santamaría L. Immunohistochemical study of cell proliferation: Bcl-2, p53, and caspase-3 expression on preneoplastic changes induced by cadmium and zinc chloride in the ventral rat prostate. J. Histochem. Cytochem. 2006, 54(9):981-990.
45. Dong H.Y., Wang Z.F. Antitumor effects of artesunate on human breast carcinoma MCF-7 cells and IGF-IR expression in nude mice xenografts. Chin. J. Cancer Res. 2014, 26(2):200-207.
46. Bonner M.R., Coble J., Blair A., Beane Freeman L.E., Hoppin J.A., Sandler D.P., Alavanja M.C. Malathion exposure and the incidence of cancer in the agricultural health study. Am. J. Epidemiol. 2007, 166(9):1023-1034.
47. Blair A., Dosemeci M., Heineman E.F. Cancer and other causes of death among male and female farmers from twenty-three states. Am. J. Ind. Med. 1993, 23(5):729-742.
48. Zahm S.H., Ward M.H., Blair A. Pesticides and cancer. Occup. Med. 1997, 12(2):269-289.
49. Koutros S., Beane Freeman L.E., Lubin J.H., Heltshe S.L., Andreotti G., Barry K.H., DellaValle C.T., Hoppin J.A., Sandler D.P., Lynch C.F., Blair A., Alavanja M.C. Risk of total and aggressive prostate cancer and pesticide use in the agricultural health study. Am. J. Epidemiol. 2013, 177(1):59-74.
50. Błasiak J., Jałoszynski P., Trzeciak A., Szyfter K. In vitro studies on the genotoxicity of the organophosphorus insecticide malathion and its two analogues. Mutat. Res. 1999, 445(2):275-283.
51. Uzun F.G., Kalender S., Durak D., Demir F., Kalender Y. Malathion-induced testicular toxicity in male rats and the protective effect of vitamins C and E. Food Chem. Toxicol. 2009, 47(8):1903-1908.
52. Choudhary N., Goyal R., Joshi S.C. Effect of malathion on reproductive system of male rats. J. Environ. Biol. 2008, 29(2):259-262.
53. 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(3):221-226.
54. Moore P.D., Patlolla A.K., Tchounwou P.B. Cytogenetic evaluation of malathion-induced toxicity in Sprague-Dawley rats. Mutat. Res. 2011, 725(1-2):78-82.
55. Zhang X., Wallace A.D., Du P., Kibbe W.A., Jafari N., Xie H., Lin S., Baccarelli A., Soares M.B., Hou L. DNA methylation alterations in response to pesticide exposure in vitro. Environ. Mol. Mutagen. 2012, 53(7):542-549.
56. Kirkin V., Joos S., Zornig M. The role of Bcl-2 family members in tumorigenesis. Biochim. Biophys. Acta 2004, 1644(2-3):229-249.
57. Feuerecker B., Pirsig S., Seidl C., Aichler M., Feuchtinger A., Bruchelt G., Senekowitsch-Schmidtke R. Lipoic acid inhibits cell proliferation of tumor cells in vitro and in vivo. Cancer Biol. Ther. 2012, 13(14):1425-1435.
58. Lee H.S., Na M.H., Kim W.K. Alpha-lipoic acid reduces matrix metalloproteinase activity in MDA-MB-231 human breast cancer cells. Nutr. Res. 2010, 30(6):403-409.
59. Dozio E., Ruscica M., Passafaro L., Dogliotti G., Steffani L., Marthyn P., Pagani A., Demartini G., Esposti D., Fraschini F., Magni P. The natural antioxidant alpha-lipoic acid induces p27(Kip1)-dependent cell cycle arrest and apoptosis in MCF-7 human breast cancer cells. Eur. J. Pharmacol. 2010, 641(1):29-34.
60. Karami-Mohajeri S., Hadian M.R., Fouladdel S., Azizi E., Ghahramani M.H., Hosseini R., Abdollahi M. Mechanisms of muscular electrophysiological and mitochondrial dysfunction following exposure to malathion, an organophosphorus pesticide. Hum. Exp. Toxicol. 2014, 33(3):251-263.
61. Cabello G., Juarranz A., Botella L.M., Calaf G.M. Organophosphorous pesticides in breast cancer progression. J. Submicrosc. Cytol. Pathol. 2003, 35(1):1-9.
62. Hollstein M., Sidransky D., Vogelstein B., Harris C.C. Mutations in human cancers. Science 1991, 253(5015):49-53.
63. Yan W., Zhang Y., Zhang J., Liu S., Cho S.J., Chen X. Mutant p53 protein is targeted by arsenic for degradation and plays a role in arsenic-mediated growth suppression. J. Biol. Chem. 2011, 286(20):17478-17486.
64. Simbula G., Columbano A., Ledda-Columbano G.M., Sanna L., Deidda M., Diana A., Pibiri M. Increased ROS generation and p53 activation in alpha-lipoic acid-induced apoptosis of hepatoma cells. Apoptosis 2007, 12(1):113-123.
65. Selmi S., El-Fazaa S., Gharbi N. Oxidative stress and alteration of biochemical markers in liver and kidney by malathion in rat pups. Toxicol. Ind. Health 2013, 1-7.
66. El-Gamal D.M., Fathy H.M., Ghandour N.M., Elbaz M.A. A comparative histological and biochemical study on the use of vitamins C, E and alpha-lipoic acid either separately or in combination on acute hepatic toxicity with malathion. Egypt. J. Histol. 2009, 32(1):192-206.
67. Reyes J.G., Rodríguez G.G., Osuna M.C., Jaward F.M. Bioaccumulation and evidence of hormonal disruptions in tilapia fish (Oreochromis spp.) exposed to sub-lethal concentrations of pesticides in Sinaloa, Mexico. Int. J. Biochem. Res. Rev. 2014, 4(4):333-343.
68. Prakash N., Venkatesh N. Human chorionic gonadotrophin (HCG) protects malathion induced PLA leutenizing hormone and testosterone changes in rats. Ind. J. Pharmacol. 1996, 28:257-260.
69. Burtis C.A., Ashwood E.R., Bruns D.E. Tietz Fundamentals of Clinical Chemistry 2008, St Louis, MO, Saunders. 6th ed.
70. Al-Attar A.M. Physiological and histopathological investigations on the effects of alpha-lipoic acid in rats exposed to malathion. J. Biomed. Biotechnol. 2010, 2010:1-8.
71. Russo J. Significance of rat mammary tumors for human risk assessment. Toxicol. Pathol. 2014, 153:3-1601. (review).
72. Chawla A., Alatrash G., Wu Y., Mittendorf E.A. Immune aspects of the breast tumor microenvironment. Breast Cancer Manag. 2013, 2(3):231-244.