Antioxidant protective effect of honey in cigarette smoke-induced testicular damage in rats

International Journal of Molecular Sciences

Volumn 12, Issue 9, 2011, Pages 5508-5521

  Mohamed, Mahaneem ^a   Sulaiman, Siti Amrah ^a   Jaafar, Hasnan ^a   Salam, Kuttulebbai Nainamohamed ^a  

^a SCHOOL OF MEDICAL SCIENCES   (Malaysia)

Author keywords

Cigarette smoke; Histology; Honey; Oxidative stress; Testis

Indexed keywords

ANTIOXIDANT; CATALASE; CIGARETTE SMOKE; GLUTATHIONE PEROXIDASE; HONEY EXTRACT; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; PROTECTIVE AGENT; SMOKE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL COUNT; CELL LOSS; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; GERM CELL; HISTOPATHOLOGY; HONEY; LEYDIG CELL; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; RAT; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE EPITHELIUM; TESTIS INJURY; TREATMENT DURATION; ANIMAL; CHEMISTRY; DRUG EFFECTS; METABOLISM; PATHOLOGY; SMOKE; SPRAGUE DAWLEY RAT; TESTIS; TOBACCO;

RATTUS;

ANIMALS; ANTIOXIDANTS; CATALASE; GLUTATHIONE PEROXIDASE; HONEY; LEYDIG CELLS; LIPID PEROXIDATION; MALE; PROTECTIVE AGENTS; RATS, SPRAGUE-DAWLEY; SEMINIFEROUS TUBULES; SMOKE; SUPEROXIDE DISMUTASE; TESTIS; THIOBARBITURIC ACID REACTIVE SUBSTANCES; TOBACCO; TOBACCO PRODUCTS;

EID: 80053192291     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms12095508     Document Type: Article

References (47)

1. Richthoff, J.; Elzanaty, S.; Rylander, L.; Hagmar, L.; Giwercman, A. Association between tobacco exposure and reproductive parameters in adolescent males. Int. J. Androl. 2008, 31, 31-39.
2. Gaur, D.S.; Talekar, M.; Pathak, V.P. Effect of cigarette smoking on semen quality of infertile men. Singapore Med. J. 2007, 48, 119-123.
3. Evans, H.J.; Fletcher, J.; Torrance, M.; Hargreave, T.B. Sperm abnormalities and cigarette smoking. Lancet 1981, 1, 627-629.
4. Potts, R.J.; Newbury, C.J.; Smith, G.; Notarianni, L.J.; Jefferies, T.M. Sperm chromatin damage associated with male smoking. Mutat. Res. 1999, 423, 103-111.
5. Sepaniak, S.; Forges, T.; Gerard, H.; Foliguet, B.; Bene, M.C.; Monnier-Barbarino, P. The influence of cigarette smoking on human sperm quality and DNA fragmentation. Toxicology 2006, 223, 54-60.
6. Yardimci, S.; Atan, A.; Delibasi, T.; Sunguroglu, K.; Guven, M.C. Long-term effects of cigarettesmoke exposure on plasma testosterone, luteinizing hormone and follicle-stimulating hormone levels in male rats. Br. J. Urol. 1997, 79, 66-69.
7. Rajpurkar, A.; Li, H.; Dhabuwala, C.B. Morphometric analysis of rat testis following chronic exposure to cigarette smoke. J. Environ. Pathol. Toxicol. Oncol. 2000, 19, 363-368.
8. Ahmadnia, H.; Ghanbari, M.; Moradi, M.R.; Khaje-Dalouee, M. Effect of cigarette smoke on spermatogenesis in rats. Urol. J. 2007, 4, 159-163.
9. Rajpurkar, A.; Dhabuwala, C.B.; Jiang, Y.; Li, H. Chronic cigarette smoking induces an oxidantantioxidant imbalance in the testis. J. Environ. Pathol. Toxicol. Oncol. 2000, 19, 369-373.
10. Kücük, M.; Kolayli, S.; Karaoǧlu, S.; Ulusoy, E.; Baltaci, C.; Candan, F. Biological activities and chemical composition of three honeys of different types from Anatolia. Food Chem. 2007, 100, 526-534.
11. Gheldof, N.; Wang, X.H.; Engeseth, N.J. Identification and quantification of antioxidant components of honeys from various floral sources. J. Agric. Food Chem. 2002, 50, 5870-5877.
12. Mato, I.; Huidobro, J.F.; Simal-Lozano, J.; Sancho, M.T. Significance of nonaromatic organic acids in honey. J. Food Prot. 2003, 66, 2371-2376.
13. Al-Waili, N.S. Effects of daily consumption of honey solution on hematological indices and blood levels of minerals and enzymes in normal individuals. J. Med. Food 2003, 6, 135-140.
14. Yao, L.; Jiang, Y.; D'Arcy, B.; Singanusong, R.; Datta, N.; Caffin, N.; Raymont, K. Quantitative high-performance liquid chromatography analyses of flavonoids in Australian Eucalyptus honeys. J. Agric. Food Chem. 2004, 52, 210-214.
15. Michalkiewicz, A.; Biesaga, M.; Pyrzynska, K. Solid-phase extraction procedure for determination of phenolic acids and some flavonols in honey. J. Chromatogr. A 2008, 1187, 18-24.
16. Tan, H.T.; Rahman, R.A.; Gan, S.H.; Halim, A.S.; Hassan, S.A.; Sulaiman, S.A.; Kirnpal-Kaur, B. The antibacterial properties of Malaysian tualang honey against wound and enteric microorganisms in comparison to manuka honey. BMC Complement. Altern. Med. 2009, 9, 34.
17. Molan, P.C. The Antibacterial Activity of Honey. 1. The Nature of the Antibacterial Activity. Bee World 1992, 73, 5-28.
18. Prakash, A.; Medhi, B.; Avti, P.K.; Saikia, U.N.; Pandhi, P.; Khanduja, K.L. Effect of different doses of Manuka honey in experimentally induced inflammatory bowel disease in rats. Phytother. Res. 2008, 22, 1511-1519.
19. Bilsel, Y.; Bugra, D.; Yamaner, S.; Bulut, T.; Cevikbas, U.; Turkoglu, U. Could honey have a place in colitis therapy? Effects of honey, prednisolone, and disulfiram on inflammation, nitric oxide, and free radical formation. Dig. Surg. 2002, 19, 306-312.
20. Berretta, G.; Granata, P.; Ferrero, M.; Orioli, M.; Facino, R.M. Standardization of antioxidant properties of honey by combination of spectrophotometric/fluorometric assays and chemometrics. Anal. Chim. Acta 2005, 533, 185-191.
21. Perez, E.; Rodriguez-Malaver, A.J.; Vit, P. Antioxidant capacity of Venezuelan honey in wistar rat homogenates. J. Med. Food 2006, 9, 510-516.
22. Mohamed, M.; Sirajudeen, K.N.S.; Swamy, M.; Yaacob, N.S.; Sulaiman, S.A. Studies on the antioxidant properties of tualang honey of Malaysia. Afr. J. Trad. CAM 2010, 7, 59-63.
23. Mahaneem, M.; Sulaiman, S.A.; Jaafar, H.; Sirajudeen, K.N.S. Effect of honey on testicular functions in rats exposed to cigarette smoke. J. ApiProd. ApiMed. Sci. 2011, 3, 12-17.
24. Ozyurt, H.; Pekmez, H.; Parlaktas, B.S.; Kus, I.; Ozyurt, B.; Sarsilmaz, M. Oxidative stress in testicular tissues of rats exposed to cigarette smoke and protective effects of caffeic acid phenethyl ester. Asian J. Androl. 2006, 8, 189-193.
25. Church, D.F.; Pryor, W.A. Free-radical chemistry of cigarette smoke and its toxicological implications. Environ. Health Perspect. 1985, 64, 111-126.
26. Bartalis, J.; Zhao, Y.L.; Flora, J.W.; Paine, J.B.; Wooten, J.B. Carbon-centered radicals in cigarette smoke: acyl and alkylaminocarbonyl radicals. Anal. Chem. 2009, 81, 631-641.
27. Alvarez, J.G.; Storey, B.T. Differential incorporation of fatty acids into and peroxidative loss of fatty acids from phospholipids of human spermatozoa. Mol. Reprod. Dev. 1995, 42, 334-346.
28. Smith, C.; Marks, A.D.; Liebermann, M.L. Oxygen Toxicity and Free Radical Injury. In Mark's Basic Medical Biochemistry: A Clinical Approach, 2nd ed.; Lippincott Williams & Wilkins: Baltimore, MD, USA, 2005; pp. 439-457.
29. Somogyi, A.; Rosta, K.; Pusztai, P.; Tulassay, Z.; Nagy, G. Antioxidant measurements. Physiol. Meas. 2007, 28, R41-R55.
30. Kohen, R.; Nyska, A. Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol. Pathol. 2002, 30, 620-650.
31. Tian, L.; Shi, M.M.; Forman, H.J. Increased transcription of the regulatory subunit of gammaglutamylcysteine synthetase in rat lung epithelial L2 cells exposed to oxidative stress or glutathione depletion. Arch. Biochem. Biophys. 1997, 342, 126-133.
32. Lu, S.C. Regulation of glutathione synthesis. Mol. Aspects Med. 2009, 30, 42-59.
33. Moskaug, J.O.; Carlsen, H.; Myhrstad, M.C.; Blomhoff, R. Polyphenols and glutathione synthesis regulation. Am. J. Clin. Nutr. 2005, 81, 277S-283S.
34. Beretta, G.; Orioli, M.; Facino, R.M. Antioxidant and radical scavenging activity of honey in endothelial cell cultures. Planta Med. 2007, 73, 1182-1189.
35. Cesar-Neto, J.B.; Duarte, P.M.; Sallum, E.A.; Barbieri, D.; Moreno, H., Jr.; Nociti, F.H., Jr. A comparative study on the effect of nicotine administration and cigarette smoke inhalation on bone healing around titanium implants. J. Periodontol. 2003, 74, 1454-1459.
36. Faqi, A.S.; Johnson, W.D.; Morrissey, R.L.; McCormick, D.L. Reproductive toxicity assessment of chronic dietary exposure to soy isoflavones in male rats. Reprod. Toxicol. 2004, 18, 605-611.
37. D'Souza, U.J. Effect of tamoxifen on spermatogenesis and tubular morphology in rats. Asian J. Androl. 2004, 6, 223-226.
38. Watanabe, N.; Kamei, S.; Ohkubo, A.; Yamanaka, M.; Ohsawa, S.; Makino, K.; Tokuda, K. Urinary protein as measured with a pyrogallol red-molybdate complex, manually and in a Hitachi 726 automated analyzer. Clin. Chem. 1986, 32, 1551-1554.
39. Ohkawa, H.; Ohishi, N.; Yagi, K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95, 351-358.
40. Koracevic, D.; Koracevic, G.; Djordjevic, V.; Andrejevic, S.; Cosic, V. Method for the measurement of antioxidant activity in human fluids. J. Clin. Pathol. 2001, 54, 356-361.
41. Goth, L. A simple method for determination of serum catalase activity and revision of reference range. Clin. Chim. Acta 1991, 196, 143-151.
42. Luchese, C.; Pinton, S.; Nogueira, C.W. Brain and lungs of rats are differently affected by cigarette smoke exposure: antioxidant effect of an organoselenium compound. Pharmacol. Res. 2009, 59, 194-201.
43. Habig, W.H.; Pabst, M.J.; Jakoby, W.B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974, 249, 7130-7139.
44. Beretta, G.; Granata, P.; Ferrero, M.; Orioli, M.; Facino, R.M. Standardization of antioxidant properties of honey by combination of spectrophotometric/fluorometric assays and chemometrics. Anal. Chim. Acta 2005, 533, 185-191.
45. Benzie, I.F.; Strain, J.J. Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol. 1999, 299, 15-27.
46. Chen, L.; Mehta, A.; Berenbaum, M.; Zangerl, A.R.; Engeseth, N.J. Honeys from different floral sources as inhibitors of enzymatic browning in fruit and vegetable homogenates. J. Agric. Food Chem. 2000, 48, 4997-5000.
47. Aljadi, A.M.; Kamaruddin, M.Y. Evaluation of the phenolic contents and antioxidant capacities of two Malaysian floral honeys. Food Chem. 2004, 85, 513-518.