Food deprivation and social inequality may lead to oxidative damage: a study on the preventive role of melatonin in the male rat reproductive system
Shiva Nasiraei-Moghadam A E , Kazem Parivar A , Abolhasan Ahmadiani B , Mansoureh Movahhedin C and Mohammad-Reza Vaez Mahdavi DA Department of Biology, Faculty of Basic Sciences, Islamic Azad University, Science and Research Branch, Tehran, Iran.
B Neuroscience Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
C Department of Anatomy, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran.
D Department of Physiology, Faculty of Medicine, Shahed Medical University, Tehran, Iran.
E Corresponding author. Email: shiva_nasiraei@yahoo.com
Reproduction, Fertility and Development 28(8) 1232-1239 https://doi.org/10.1071/RD14432
Submitted: 6 September 2014 Accepted: 13 December 2014 Published: 16 February 2015
Abstract
Spermatogenic cells are susceptible to oxidative stress and apoptosis. Food deprivation (FD) has been reported as a stressor that could increase reactive oxygen species. In the present study, FD-induced oxidative stress and apoptosis, as well as the protective effects of melatonin, were evaluated in the testes. Wistar rats in the control group were fed a standard diet, whereas a sham group was administered saline as the melatonin vehicle. A third group received daily injections of melatonin (5 mg kg–1 bodyweight). These rats were further divided into four groups of rats that were either subjected to FD, FD + isolation, FD + melatonin injection and FD + melatonin injection + isolation. Testicular tissues were evaluated for malondialdehyde (MDA) and reduced glutathione (GSH) concentrations, as well as and DNA damage. FD increased MDA and reduced GSH concentrations, whereas melatonin treatment improved these parameters. Immunohistochemistry for capsase-3 and terminal deoxyribonucleotidyl transferase-mediated dUTP–digoxigenin nick end-labelling revealed that the number of apoptotic cells was increased in rats subjected to FD alone. Melatonin treatment offset the number of apoptotic cells following FD. The results provide evidence that FD can increase oxidative stress, leading to activation of apoptosis, and that melatonin has the ability to protect the testes against oxidative damage induced by FD.
Additional keywords: apoptosis, testis.
References
Adams, J. G. J., Dhar, A., Shukla, S. D., and Silver, D. (1995). Effect of pentoxifylline on tissue injury and platelet-activating factor production during ischemia–reperfusion injury. J. Vasc. Surg. 21, 742–749.| Effect of pentoxifylline on tissue injury and platelet-activating factor production during ischemia–reperfusion injury.Crossref | GoogleScholarGoogle Scholar |
Agarwal, A., Prabakaran, S., and Allamaneni, S. (2006). Relationship between oxidative stress, varicocele and infertility: a meta-analysis. Reprod. Biomed. Online 12, 630–633.
| Relationship between oxidative stress, varicocele and infertility: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xltleitrk%3D&md5=09b7390804c01c1f996a50c6ad82f0cdCAS | 16790111PubMed |
Al-Majed, A. A. (2011). Probucol attenuates oxidative stress, energy starvation, and nitric acid production following transient forebrain ischemia in the rat hippocampus. Oxid. Med. Cell. Longev. 2011, 471590.
| 21904644PubMed |
Benoff, S. H., Millan, C., Hurley, I. R., Napolitano, B., and Marmar, J. L. (2004). Bilateral increased apoptosis and bilateral accumulation of cadmium in infertile men with left varicocele. Hum. Reprod. 19, 616–627.
| Bilateral increased apoptosis and bilateral accumulation of cadmium in infertile men with left varicocele.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFSqt7w%3D&md5=8d9c9b9702049776fbdb1128b034cc2bCAS | 14998961PubMed |
Bhardwaj, S. K., Sharma, M. L., Gulati, G., Chhabra, A., Kaushik, R., Sharma, P., and Kaur, G. (1998). Effect of starvation and insulin-induced hypoglycemia on oxidative stress scavenger system and electron transport chain complexes from rat brain, liver, and kidney. Mol. Chem. Neuropathol. 34, 157–168.
| Effect of starvation and insulin-induced hypoglycemia on oxidative stress scavenger system and electron transport chain complexes from rat brain, liver, and kidney.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFygu7c%3D&md5=a0b51e5384c299ff40aad91d056c9a27CAS | 10327415PubMed |
Blokhina, O., Virolainen, E., and Fagerstedt, K. V. (2003). Anti oxidant, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. 91, 179–194.
| Anti oxidant, oxidative damage and oxygen deprivation stress: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitVCksbw%3D&md5=9cea26d880900305c076371cf8f78601CAS | 12509339PubMed |
Buege, J. A., and Aust, S. D. (1978). Microsomal lipid peroxidation. Methods Enzymol. 52, 302–310.
| 1:CAS:528:DyaE1MXltVajsw%3D%3D&md5=c165458c6b2f6561c0e05868b480435fCAS | 672633PubMed |
Cagnacci, A., and Volpe, A. (1996). Influence of melatonin and photoperiod on animal and human reproduction. J. Endocrinol. Invest. 19, 382–411.
| Influence of melatonin and photoperiod on animal and human reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xltlyqtb8%3D&md5=1c1dc68f4848273f27e452ab89ad9b38CAS | 8844459PubMed |
Carrell, D. T., and Peterson, C. M. (2010). ‘Reproductive Endocrinology and Infertility.’ (Springer Science+Business Media: New York.)
Clutton, S. (1997). The importance of oxidative stress in apoptosis. Br. Med. Bull. 53, 662–668.
| The importance of oxidative stress in apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsF2nt7g%3D&md5=2ffad8507d48b740691c4a3d676e8418CAS | 9374044PubMed |
Domenicali, M., Caraceni, P., Vendemiale, G., Grattagliano, I., Nardo, B., Dall’Agata, M., Santoni, B., Trevisani, F., Cavallari, A., Altomare, E., and Bernardi, M. (2001). Food deprivation exacerbates mitochondrial oxidative stress in rat liver exposed to ischemia-reperfusion injury. J. Nutr. 131, 105–110.
| 1:CAS:528:DC%2BD3MXotVKksg%3D%3D&md5=cc4c4e584f72dfb3d163de5976973094CAS | 11208945PubMed |
El-Sokkary, G. H., Abdel-Rahman, G. H., and Kamel, E. S. (2005). Melatonin protects against lead-induced hepatic and renal toxicity in male rats. Toxicology 213, 25–33.
| Melatonin protects against lead-induced hepatic and renal toxicity in male rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsVWgtrc%3D&md5=4cbdd16fdbc51d57dc9ea0d2fc6e290fCAS | 15964675PubMed |
Ferlini, C., Scambia, G., Marone, M., Distefano, M., Gaggini, C., Ferrandina, G., Fattorossi, A., Isola, G., Benedetti Panici, P., and Mancuso, S. (1999). Tamoxifen induces oxidative stress and apoptosis in oestrogen receptor-negative human cancer cell lines. Br. J. Cancer 79, 257–263.
| Tamoxifen induces oxidative stress and apoptosis in oestrogen receptor-negative human cancer cell lines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFegsg%3D%3D&md5=28c8fddfda12d3c3bb47d332cf317f25CAS | 9888466PubMed |
Fraga, C. G., Motchnik, P. A., Shigenaga, M. K., Helbock, H. J., Jacob, R. A., and Ames, B. N. (1991). Ascorbic acid protects against endogenous oxidative DNA damage in human sperm. Proc. Natl Acad. Sci. USA 88, 11 003–11 006.
| Ascorbic acid protects against endogenous oxidative DNA damage in human sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlsl2lug%3D%3D&md5=8d80819742fd876b41744528132b293bCAS |
Grosshans, K., and Calvin, H. I. (1985). Estimation of glutathione in purified populations of mouse testis germ cells. Biol. Reprod. 33, 1197–1205.
| Estimation of glutathione in purified populations of mouse testis germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XkvFaruw%3D%3D&md5=465e108a9e00a247d86b2b261fadc525CAS | 4074809PubMed |
Hardeland, R., Reiter, R. J., Poeggeler, B., and Tan, D. X. (1993). The significance of the metabolism of the neurohormone melatonin: antioxidative protection and formation of bioactive substances. Neurosci. Biobehav. Rev. 17, 347–357.
| The significance of the metabolism of the neurohormone melatonin: antioxidative protection and formation of bioactive substances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXht1Cqur0%3D&md5=2c6a4568360f13cdfb1cc0b7c181d27cCAS | 8272286PubMed |
Heidary, F., and Gharebaghi, R. (2012). Ideas to assist the underprivileged dispossessed individuals. Med. Hypothesis Discov. Innov. Ophthalmol. 1, 43–44.
| 24600620PubMed |
Heidary, R., Heidary, F., Vaez Mahdavi, M. R., Rahimi, A., and Gharebaghi, R. (2012). Potential negative impacts of social inequality on visual health: the possible pathophysiology mechanisms. Med. Hypothesis Discov. Innov. Ophthalmol. 1, 42.
| 24600619PubMed |
Heidary, F., Rahimi, A., and Gharebaghi, R. (2013). Poverty as a risk factor in human cancers. Iran J. Public Health 42, 341–343.
| 23641414PubMed |
Lepage, G., Munoz, G., Champagne, J., and Roy, C. C. (1991). Preparative steps for the accurate measurement of malondialdehyde by high-performance liquid chromatography. Anal. Biochem. 197, 277–283.
| Preparative steps for the accurate measurement of malondialdehyde by high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmt1Ons7c%3D&md5=5cbc324eed34623951ce2ece1dd3811bCAS | 1785679PubMed |
Mojarab, S. H., Vaez Mahdavi, M. R., Roghani, M., Safarpour, A. L., Tiraihi, T., Faghihzadeh, S., Azathy, M. H., and Nasabi, N. A. (2010). Effect of food inequality and unstable social status on myocardial cells of male rabbits. World Appl. Sci. J. 8, 680–686.
Moradi, F., Vaez-Mahdavi, M. R., Ahmadiani, A., Roghani, M., Altiraihi, T., and Mojarab, S. (2012). Can social instability, food deprivation and food inequality accelerate neuronal aging? Basic Clin. Neurosci. 3, 38–48.
Morales, A. E., Pe’rez-Jime’neza, A., Hidalgoa, M. C., Abella’nb, E., and Cardenetea, G. (2004). Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 139, 153–161.
| 15556078PubMed |
Narayana, K., D’Souza, U. J., and Rao, K. P. (2002). Effect of ribavirin on epididymal spermcount in rat. Indian J. Physiol. Pharmacol. 46, 97–101.
| 1:CAS:528:DC%2BD38XhsVensL0%3D&md5=7a1bb6029247f3a45234fa4794400edfCAS | 12024964PubMed |
Nasiraei-Moghadam, S., Parivar, K., Ahmadiani, A., Movahhedin, M., and Reza Vaez Mahdavi, M. (2014). Protective effect of melatonin against inequality-induced damages on testicular tissue and sperm parameters. Int. J. Fertil. Steril. 7, 313–322.
| 24520501PubMed |
Nasri, S., Roghani, M., Baluchnejad-mojarad, T., Rabani, T., and Balvardi, M. (2011). Vascular mechanisms of cyanidin-3-glucoside response in streptozotocin-diabetic rats. Pathophysiology 18, 273–278.
| Vascular mechanisms of cyanidin-3-glucoside response in streptozotocin-diabetic rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFyns78%3D&md5=b6e7100b952ac36ce38a7b91f0fc5a06CAS | 21546226PubMed |
Okutan, H., Savas, C., and Delibas, N. (2004). The antioxidant effect of melatonin in lung injury after aortic occlusion–reperfusion. Interact. Cardiovasc. Thorac. Surg. 3, 519–522.
| The antioxidant effect of melatonin in lung injury after aortic occlusion–reperfusion.Crossref | GoogleScholarGoogle Scholar | 17670300PubMed |
Pascual, P., Pedrajas, J. R., Toribio, F., López-Barea, J., and Peinado, J. (2003). Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem. Biol. Interact. 145, 191–199.
| Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXis12jtL0%3D&md5=89eb4bbf44a168ec15291bfb0dd3a69cCAS | 12686495PubMed |
Pieri, C., Marra, M., Moroni, F., Recchioni, R., and Marcheselli, F. (1994). Melatonin: a peroxyl radical scavenger more effective than vitamin E. Life Sci. 55, PL271–PL276.
| Melatonin: a peroxyl radical scavenger more effective than vitamin E.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1amu7c%3D&md5=20d29f1f93c9ee11f4e0e3abea54ee96CAS | 7934611PubMed |
Rao, A. V., and Shaha, C. (2000). Role of glutathione S-transferases in oxidative stress-induced male germ cell apoptosis. Free Radic. Biol. Med. 29, 1015–1027.
| Role of glutathione S-transferases in oxidative stress-induced male germ cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVCrurc%3D&md5=7fe8c2b8d77f8d460e6d4c8e2f1f416cCAS | 11084290PubMed |
Reiter, R., Tang, L., Garcia, J. J., and Munoz-Hoyos, A. (1997). Pharmacological actions of melatonin in oxygen radical pathophysiology. Life Sci. 60, 2255–2271.
| Pharmacological actions of melatonin in oxygen radical pathophysiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsFOisrk%3D&md5=1de5ab27d1134ab1b018ac0eee08e20eCAS | 9194681PubMed |
Reiter, R. J., Tan, D. X., Manchester, L. C., and Qi, W. (2001). Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochem. Biophys. 34, 237–256.
| Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1alsro%3D&md5=686a3380a8b726fbcc73a42c2bfdf6e8CAS | 11898866PubMed |
Reiter, R. J., Tan, D. X., and Allegra, M. (2002). Melatonin: reducing molecular pathology and dysfunction due to free radicals and associated reactants. Neuroendocrinol. Lett. 23, 3–8.
| 1:CAS:528:DC%2BD38Xkt1Snurs%3D&md5=eb526be1bdb61fa0bd5ec7717b32ed7bCAS | 12019343PubMed |
Roghani, M., and Baluchnejadmojarad, T. (2010). Mechanisms underlying vascular effect of chronic resveratrol in streptozotocin-diabetic rats. Phytother. Res. 24, S148–S154.
| Mechanisms underlying vascular effect of chronic resveratrol in streptozotocin-diabetic rats.Crossref | GoogleScholarGoogle Scholar | 20013818PubMed |
Santos, R. X., Cardoso, S., Silva, S., Correia, S., Carvalho, C., Crisóstomo, J., Rodrigues, L., Amaral, C., Louro, T., Matafome, P., Santos, M. S., Proenc, T. A., Duarte, A. I., Seic, R., and Moreira, P. I. (2009). Food Deprivation Promotes Oxidative Imbalance in Rat Brain. J. Food Sci. 74, H8–H14.
| Food Deprivation Promotes Oxidative Imbalance in Rat Brain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Ojsbc%3D&md5=0ab6ce7678895afdd46930f1eab10dfbCAS | 19200099PubMed |
Sarvari, A., Naderi, M. M., Heidari, M., Zarnani, A. H., Jeddi-Tehrani, M., Sadeghi, M. R., and Akhondi, M. M. (2010). Effect of environmental risk factors on human fertility. J. Reprod. Infertil. 11, 211–225.
Sucu, N., Unlu, A., Tamer, L., Aytacoglu, B., Coskun, B., Bilgin, R., Ercan, B., Gul, A., Dikmengil, M., and Atik, U. (2002). Effects of trimetazidine on tissue damage in kidney after hindlimb ischemia-reperfusion. Pharmacol. Res. 46, 345–349.
| Effects of trimetazidine on tissue damage in kidney after hindlimb ischemia-reperfusion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38rgtVKqtQ%3D%3D&md5=566bb69898aef6a45befe7a8b7ae9b66CAS | 12361697PubMed |
Troyer-Caudle, J. (1993). Reperfusion injury. J. Vasc. Nurs. 11, 76–79.
| 1:STN:280:DyaK2c7hsVCiuw%3D%3D&md5=78ed4431885f2620831156241c86be17CAS | 8286274PubMed |
Wakatsuki, A., Okatani, Y., Izumiya, C., and Ikenoue, N. (1999). Melatonin protects against ischemia and reperfusion-induced oxidative lipid and DNA damage in fetal rat brain. J. Pineal Res. 26, 147–152.
| Melatonin protects against ischemia and reperfusion-induced oxidative lipid and DNA damage in fetal rat brain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisF2iurY%3D&md5=735fe48beb5b0edd908a5c810327f908CAS | 10231727PubMed |
Yang, Y., Cheng, J. Z., Singhal, S. S., Saini, M., Pandya, U., Awasthi, S., and Awasthi, Y. C. (2001). Role of glutathione S-transferases in protection against lipid peroxidation. Overexpression of hGSTA2–2 in K562 cells protects against hydrogen peroxide-induced apoptosis and inhibits JNK and caspase 3 activation. J. Biol. Chem. 276, 19 220–19 230.
| Role of glutathione S-transferases in protection against lipid peroxidation. Overexpression of hGSTA2–2 in K562 cells protects against hydrogen peroxide-induced apoptosis and inhibits JNK and caspase 3 activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt12rsL8%3D&md5=8dda5027549e19a852501088c4da9407CAS |
Yu, Z. H., Chow, P. H., and Pang, S. F. (1994). Identification and characterization of 2[125I]-iodomelatonin binding sites in the rat epididymis. J. Pineal Res. 17, 195–201.
| Identification and characterization of 2[125I]-iodomelatonin binding sites in the rat epididymis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtVyhsbg%3D&md5=6d12360dfee0f24918082aa10ac31808CAS | 7722869PubMed |