Silymarin protects from varicocele-induced damages in testis and improves sperm quality: evidence for E2f1 involvement

References

• Angeli, J.P., Barcelos, G.R., Serpeloni, J.M., Barbosa, F., Nersesyan, A. and Mantovani, M.S. (2010) Evaluation of the genotoxic and anti-genotoxic activities of silybin in human hepatoma cells (HepG2). Mutagenesis 25:223–229.
   PubMed Web of Science ®Google Scholar
• Angelis, E., Zhao, P., Zhang, R., Goldhaber, J.I. and MacLellan, W.R. (2011) The role of E2F-1 and downstream target genes in mediating ischemia/reperfusion injury in vivo. J Mol Cell Cardiol 51:919–926.
   PubMed Web of Science ®Google Scholar
• Chomczynski, P. and Sacchi, N. (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1:581–585.
   PubMed Web of Science ®Google Scholar
• El-Darwish, K.S., Parvinen, M. and Toppari, J. (2006) Differential expression of members of the E2F family of transcription factors in rodent testes. Reprod Biol Endocrinol 2006: 4:63. doi:10.1186/1477-7827-4-63.
   PubMed Web of Science ®Google Scholar
• El-Shitany, N.A., El-Haggar, S. and El-Desoky, K. (2008) Silymarin prevents adriamycin-induced cardiotoxicity and nephrotoxicity in rats. Food Chem Toxicol 46:2422–2428.
   PubMed Web of Science ®Google Scholar
• Evers, J.L. and Collins, J.A. (2008) Surgery or embolisation for varicocele in sub-fertile men. Cochrane Database Syst Rev: 3:CD000479.
   Google Scholar
• French, D.B., Desai, N.R. and Agarwal, A. (2008) Varicocele repair: Does it still have a role in infertility treatment? Curr Opin Obstet Gynecol 20:269–274.
   Google Scholar
• Gat, Y., Zukerman, Z., Chakraborty, J. and Gornish, M. (2005) Varicocele, hypoxia and male infertility. Fluid Mechanics analysis of the impaired testicular venous drainage system. Human Reprod 20:2614–2619.
   PubMed Web of Science ®Google Scholar
• Griveau, J.F. and Le Lannou, D. (1997) Reactive oxygen species and human spermatozoa. Int J Androl 20:61–69.
   PubMedGoogle Scholar
• Hallstrom, T.C. and Nevins, J.R. (2003) Specificity in the activation and control of transcription factor E2F-dependent apoptosis. Proc Natl Acad Sci USA 100:10848–10853.
   PubMed Web of Science ®Google Scholar
• Hauck, L., Hansmann, G., Dietz, R. and von Harsdorf, R. (2002) Inhibition of hypoxia-induced apoptosis by modulation of retinoblastoma protein-dependent signaling in cardiomyocytes. Circ Res 91:782–789.
   PubMed Web of Science ®Google Scholar
• Hendin, B.N., Kolettis, P.N., Sharma, R.K. and Thomas, A. (1999) Varicocele is associated with elevated spermatozoal reactive oxygen species production and diminished seminal plasma antioxidant capacity. J Urol 161:1831–1834.
   PubMed Web of Science ®Google Scholar
• Hu, M. and Dillared, C.J. (1994) Plasma SH and GSH measurement. Methods Enzymol 233: 385–387.
   PubMed Web of Science ®Google Scholar
• Hurtado de Catalfo, G.E. Ranieri-Casilla, A. and Marra, F.A. (2007) Oxidative stress biomarkers and hormonal profile in human patients undergoing varicocelectomy. Int J Androl 30:519–530.
   PubMedGoogle Scholar
• Kessopoulou, E., Tomlinson, M.J., Banat, C.L.R. and Cooke, I.D. (1992) Origin of reactive oxygen species in human semen: spermatozoa or leukocytes? J Reprod Fertil 94:463–470.
   Google Scholar
• Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275.
   PubMed Web of Science ®Google Scholar
• Malekinejad, H., Janbaz-Acyabar, H., Razi, M. and Varasteh, S. (2012a) Preventive and protective effects of Silymarin on Doxorubicin-induced testicular damages correlate with changes in c-myc gene expression. Phytomedicine 19:1077–1084.
   PubMed Web of Science ®Google Scholar
• Malekinejad, H., Taheri-brujerdi, M., Janbaz-Acyabar, H. and Amniattalab, A. (2012b) Silymarin regulates the HIF-1α and iNOS expression in the Brain and Gills of the hypoxic reoxygenated rainbow trout (Oncorhynchus mykis). Aquatic Biology 15:261–273.
   Google Scholar
• Mata-Santos, H,A., Lino, F.G., Rocha, C.C., Paiva, C.N., Castelo Branco, M.T. and Pyrrho Ados, S. (2010) Silymarin treatment reduces granuloma and hepatic fibrosis in experimental schistosomiasis. Parasitol Res 107:1429–1434.
   PubMed Web of Science ®Google Scholar
• Moskowtsev, S.I., Lecker, I., Mullen, J.B., Jarvi, K., Willis, J., White, J. and Lo, K.C. (2009) Cause-specific treatment in patients with high sperm DNA damage resulted in significant DNA improvement. Syst Biol Reprod Med 55:109–115.
   PubMed Web of Science ®Google Scholar
• Mostafa, T., Anis, T.H., El-Nashar, A., Imam, H. and Osman, I.A. (2001) Varicocelectomy reduces reactive oxygen species levels and increases antioxidant activity of seminal plasma from infertile men with varicocele. Int J Androl 24:261–265.
   PubMedGoogle Scholar
• Naughton, C.K., Nangia, A.K. and Agarwal, A. (2001) Pathophysiology of varicoceles in male infertility. Hum Reprod Update 7:473–481.
   PubMed Web of Science ®Google Scholar
• Nencini, C., Giorgi, G. and Micheli, L. (2007) Protective effect of silymarin on oxidative stress in rat brain. Phytomedicine 14:129–135.
   PubMed Web of Science ®Google Scholar
• Niehaus, W.G. and Samuelsson, J.R.B. (1968) Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation. Eur J Biochem 6:126–130.
   PubMedGoogle Scholar
• Ozokutan, B.H., Kucukaydin, M., Muhtaroglu, S. and Tekin, Y. (2000) The role of nitricoxide in testicular ischemia-reperfusion injury. J Pediatr Surg 35:101–103.
   PubMed Web of Science ®Google Scholar
• Padron, O.F. Brackett, N.L. and Sharma, R.K. (1997) Seminal reactive oxygen species, sperm motility and morphology in men with spinal cord injury. Fertil Steril 67:1115–1120.
   PubMed Web of Science ®Google Scholar
• Pant, N. and Srivastava, S.P. (2003) Testicular and spermatotoxic effect of quinaphos in rats. J Appl Toxicol 23:271–274.
   PubMed Web of Science ®Google Scholar
• Rašković, A., Stilinović, N., Kolarović, J., Vasović, V., Vukmirović, S. and Mikov, M. (2011) The Protective Effects of silymarin against Doxorubicin-Induced Cardiotoxicity and Hepatotoxicity in Rats. Molecules 16:8601–8613.
   PubMed Web of Science ®Google Scholar
• Pasqualotto, F., Lucon, A.M., Hallak. J., GoÂes, P.M. Saldanha, L.B. and Arap, S. (2003) Induction of spermatogenesis in azoospermic men after varicocele repair, Human Reprod 18:108–112.
   Google Scholar
• Razi, M., Sadrkhanlou, R.A., Malekinejad, H. and Sarrafzadeh, F. (2010) Testicular biohistochemical alterations following experimental varicocele in rats. Iran J Reprod Med 10:209–218.
   Google Scholar
• Razi, M., Sadrkhanlou, R.A., Malekinejad, H. and Sarafzadeh, A. (2011) The Varicocele time-dependently affects the DNA integrity of sperm cells: evidence for lower in vitro fertilization rate in varicocele-positive rats. Inter J Fertil Steril 5:174–185.
   PubMed Web of Science ®Google Scholar
• Romeo, C., Ientile, R., Impellizzeri, P., Turiaco, N., Impala, P., Cifala, S. (2003) Preliminary report on nitric oxide-mediated oxidative damage in adolescent varicocele. Hum Reprod 18:26–29.
   PubMed Web of Science ®Google Scholar
• Saalu, L.C., Oguntola, J.A., Babalola, O.S. and Oyewopo, A.O. (2009) Reversal of experimental varicocele-induced testicular toxicity by L-ascorbate in rats. Afric J Biotech 8:965–970.
   Google Scholar
• Saleh, R.A., Agarwal, A., Sharma, R.K., Said, M., Sikka, S.C. and Thomas, AJ. (2003) Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertil Steril 80:1431–1436.
   PubMed Web of Science ®Google Scholar
• Shibata, M., Hariya, T., Hatao, M., Ashikaga, T. and Ichikawa, H. (1999) Quantitative polymerase chain reaction using an external control mRNA for determination of gene expression in a heterogeneous cell population. Toxicol Sci 49:290–296.
   PubMed Web of Science ®Google Scholar
• Shiraishi, K. and Naito, K. (2007) Effects of 4-hydroxy-2-nonenal, a marker of oxidative stress, on spermatogenesis and expression of pp53 protein in male infertility. J Urol 178:1012–1017.
   PubMed Web of Science ®Google Scholar
• Smith, R., Kaune, H. and Parodi, D. (2003) Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod 21:986–993.
   Google Scholar
• Sofikitis, N. and Miyagawa, I. (1992) Experimental models for the study of varicocele: A selected review. Jpn J Fertil Steril 38:168–177.
   Google Scholar
• Suziki, N. and Sofikitis, N. (1999) Protective effects of antioxidants on testicular fractions of varicocelized rats. Yonago Acta Med 42:87–94.
   Google Scholar
• Tejada, R.I., Mitchel, J.C. and Norman, A. (1984) A test for the practical evaluation of male infertility by acridine orange (AO) fluorescence. Fertil Steril 42:87–91.
   PubMed Web of Science ®Google Scholar
• Terquem, A. and Dadoune, J.P. (1983) Aniline blue staining of human spermatozoa chromatin evaluation of nuclear maturation. In The Sperm Cell. ed. Andre, J., Martinus Nijhoff Publishers, London, UK, 249–252.
   Google Scholar
• Turkyilmaz, Z., Gulen, S., Sonmez, K., Karahulut, R., Diucer, S., Can Basaklar, A. (2004) Increased nitric oxide is accompanied by lipid oxidation in adolescent varicocele. Int J Androl 27:183–187.
   PubMedGoogle Scholar
• WHO (1999) WHO laboratory manual for the examination of human semen and sperm cervical mucus interaction. Cambridge University Press, Cambridge, UK.
   Google Scholar
• Wong, J.W., Yao, G., Nevins, J.R. and You, L. (2011) Viral-Mediated Noisy Gene Expression Reveals Biphasic E2f1 Response to MYC. Molecular Cell 41:275–285.
   PubMed Web of Science ®Google Scholar
• Zhang, X.P., Liu, F. and Wang, W. (2010) Coordination between Cell Cycle Progression and Cell Fate Decision by the p53 and E2F1 Pathways in Response to DNA Damage. J Biol Chem 285:31571–31580.
   PubMed Web of Science ®Google Scholar