Effects of anthocyanin extracted from black soybean seed coat on spermatogenesis in a rat varicocele-induced model
Hoon Jang A , Su Jin Kim A , Seung Mo Yuk A , Dong Seok Han A , U.-Syn Ha A , Sung Hoo Hong A , Ji Yeol Lee A , Tae Kon Hwang A , Seong Yeon Hwang B and Sae Woong Kim A C
+ Author Affiliations
- Author Affiliations
A The Department of Urology, The Catholic University of Korea College of Medicine, Seoul 137-701, Korea.
B Korea Bio Medical Science Institute, Sinhan Building, Nonhyun-dong 80-1, Kangnam-gu, Seoul 135-010, Korea.
C Corresponding author. Email: ksw1227@catholic.ac.kr
Reproduction, Fertility and Development 24(5) 649-655 https://doi.org/10.1071/RD11174
Submitted: 10 July 2011 Accepted: 19 October 2011 Published: 28 November 2011
Abstract
Varicocele is the most common cause of primary male infertility and is associated with oxidative stress. The aim of the present study was to investigate the effects of anthocyanin on a rat model of varicocele. Twenty-four male rats were divided into four experimental groups: a normal control group, a varicocele-induced control group and two varicocele-induced groups treated with either 40 or 80 mg kg–1, p.o., anthocyanin for 4 weeks. Varicocele was induced by the partial obstruction of the left renal vein. After 8 weeks, the testes and epididymides from rats in all groups were removed, weighed and subjected to histological examination and semen analysis. Apoptosis in the testes was determined by terminal deoxyribonucleotidyl transferase-mediated dUTP–digoxigenin nick end-labelling (TUNEL) and oxidative stress was assessed by measuring 8-hydroxy-2′-deoxyguanosine (8-OHdG) levels. Although no significant differences in sperm counts were observed among the groups, anthocyanin treatment of the varicocele-induced groups resulted in significantly increased testes weight, sperm motility and spermatogenic cell density (P < 0.05). Anthocyanin treatment also significantly decreased apoptotic body count and 8-OHdG concentrations (P < 0.05). We suggest that the antioxidant effect of anthocyanin prevented the damage caused by varicocele-induced reactive oxygen species.
Additional keywords: apoptosis, fertility, spermatozoa, testis.
References
Agarwal, A., and Allamaneni, S. S. (2005). Sperm DNA damage assessment: a test whose time has come. Fertil. Steril. 84, 850–853.| Sperm DNA damage assessment: a test whose time has come.Crossref | GoogleScholarGoogle Scholar | 16213833PubMed |
Agarwal, A., and Said, T. M. (2005). Oxidative stress, DNA damage and apoptosis in male infertility: a clinical approach. BJU Int. 95, 503–507.
| Oxidative stress, DNA damage and apoptosis in male infertility: a clinical approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis1Kgsrs%3D&md5=f9d49eef718b1ab6d4a39007b2358305CAS | 15705068PubMed |
Aitken, R. J., and Clarkson, J. S. (1987). Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J. Reprod. Fertil. 81, 459–469.
| Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXltlyjsw%3D%3D&md5=29b9a6ba3cc6ba15caac4ccdb2afb2f0CAS | 2828610PubMed |
Aitken, R. J., Buckingham, D., West, K., Wu, F. C., Zikopoulos, K., and Richardson, D. W. (1992). Differential contribution of leucocytes and spermatozoa to the generation of reactive oxygen species in the ejaculates of oligozoospermic patients and fertile donors. J. Reprod. Fertil. 94, 451–462.
| Differential contribution of leucocytes and spermatozoa to the generation of reactive oxygen species in the ejaculates of oligozoospermic patients and fertile donors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktVGnuro%3D&md5=0338d71a72cedb878de49ce3110377eaCAS | 1317451PubMed |
Atessahin, A., Karahan, I., Turk, G., Gur, S., Yilmaz, S., and Ceribasi, A. O. (2006a). Protective role of lycopene on cisplatin-induced changes in sperm characteristics, testicular damage and oxidative stress in rats. Reprod. Toxicol. 21, 42–47.
| Protective role of lycopene on cisplatin-induced changes in sperm characteristics, testicular damage and oxidative stress in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvFOqug%3D%3D&md5=f2f566e7a14f34028bd8aa71bed9dc01CAS | 15979841PubMed |
Atessahin, A., Turk, G., Karahan, I., Yilmaz, S., Ceribasi, A. O., and Bulmus, O. (2006b). Lycopene prevents adriamycin-induced testicular toxicity in rats. Fertil. Steril. 85, 1216–1222.
| Lycopene prevents adriamycin-induced testicular toxicity in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFWjsr4%3D&md5=506b8c7939221980660d2d856f686b75CAS | 16616095PubMed |
Cam, K., Simsek, F., Yuksel, M., Turkeri, L., Haklar, G., Yalcin, S., and Akdas, A. (2004). The role of reactive oxygen species and apoptosis in the pathogenesis of varicocele in a rat model and effeiciency of vitamin E treatment. Int. J. Androl. 27, 228–233.
| The role of reactive oxygen species and apoptosis in the pathogenesis of varicocele in a rat model and effeiciency of vitamin E treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXns1GmsLY%3D&md5=44e991acc74da0af7933876d59dc695cCAS | 15271202PubMed |
Cayan, S., Akbay, E., Bozlu, M., Doruk, E., Acar, D., and Ulusoy, E. (2002). The effect of varicocele repair on testicular volume in children and adolescents with varicocele. J. Urol. 168, 731–734.
| The effect of varicocele repair on testicular volume in children and adolescents with varicocele.Crossref | GoogleScholarGoogle Scholar | 12131361PubMed |
Colagar, A. H., and Marzony, E. T. (2009). Ascorbic acid in human seminal plasma: determination and its relationship to sperm quality. J. Clin. Biochem. Nutr. 45, 144–149.
| Ascorbic acid in human seminal plasma: determination and its relationship to sperm quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlWrsbvP&md5=fc4417c50b9af0bd9f73262411f3b988CAS | 19794921PubMed |
de Lamirande, E., Jiang, H., Zini, A., Kodama, H., and Gagnon, C. (1997). Reactive oxygen species and sperm physiology. Rev. Reprod. 2, 48–54.
| Reactive oxygen species and sperm physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Kmsrk%3D&md5=1c78ee2f6e68c2c8da6435cb44a452deCAS | 9414465PubMed |
Fujisawa, M., Hiramine, C., Tanaka, H., Okada, H., Arakawa, S., and Kamidono, S. (1999). Decrease in apoptosis of germ cells in the testes of infertile men with varicocele. World J. Urol. 17, 296–300.
| Decrease in apoptosis of germ cells in the testes of infertile men with varicocele.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FhvF2gtA%3D%3D&md5=b5eaf0aa881b2df31f703393404c98efCAS | 10552147PubMed |
Goldstein, M. (1998). Surgical management of male infertility and other scrotal disorders. In ‘Campbell’s Urology’. 7th edn. (Eds P. C. Walsh, A. B. Retick, A. W. Wein and E. Vaugh.) pp. 1343–1344. (Lippincott Williams and Wilkins: Philadelphia.)
Gorelick, J. I., and Goldstein, M. (1993). Loss of fertility in men with varicocele. Fertil. Steril. 59, 613–616.
| 1:STN:280:DyaK3s3gvFCitA%3D%3D&md5=2b01a0bddc510f25c9eacfc25e771ccfCAS | 8458466PubMed |
Gürdal, M., Kireççi, S., Huri, E., Karaman, I., and Türkeri, L. (2008). Correlation between duration of varicocele and apoptosis in testicular tissue in an experimental model. Urology 72, 933–936.
| Correlation between duration of varicocele and apoptosis in testicular tissue in an experimental model.Crossref | GoogleScholarGoogle Scholar | 18387659PubMed |
Hagood, P. G., Mehan, D. J., Worischeck, J. H., Andrus, C. H., and Parra, R. O. (1992). Laparoscopic varicocelectomy: preliminary report of a new technique. J. Urol. 147, 73–76.
| 1:STN:280:DyaK387gs1CgsA%3D%3D&md5=e1fc476fd29f0d5153dc0a4fffd651bdCAS | 1530871PubMed |
Hendin, B. N., Kolettis, P. N., Sharma, R. K., Thomas, A. J.,, and Agarwal, A. (1999). Varicocele is associated with elevated spermatozoal reactive oxygen species production and diminished seminal plasma antioxidant capacity. J. Urol. 161, 1831–1834.
| Varicocele is associated with elevated spermatozoal reactive oxygen species production and diminished seminal plasma antioxidant capacity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3msVymsw%3D%3D&md5=13ea1737db5a66a236b1663dfbff2c68CAS | 10332447PubMed |
Henkel, R. (2005). The impact of oxidants on sperm function. Andrologia 37, 205–206.
| The impact of oxidants on sperm function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFygt7k%3D&md5=07d93b319ebdb9716ef11070fecb785aCAS | 16336248PubMed |
Ibrahim, S. F., Osman, K., Das, S., Othman, A. M., Majid, N. A., and Rahman, M. P. (2008). A study of the antioxidant effect of alpha lipoic acids on sperm quality. Clinics 63, 545–550.
| A study of the antioxidant effect of alpha lipoic acids on sperm quality.Crossref | GoogleScholarGoogle Scholar | 18719769PubMed |
Jang, H., Ha, U. S., Kim, S. J., Yoon, B. I., Han, D. S., Yuk, S. M., and Kim, S. W. (2010). Anthocyanin extracted from black soybean reduces prostate weight and promotes apoptosis in the prostatic hyperplasia-induced rat model. J. Agric. Food Chem. 58, 12 686–12 691.
| Anthocyanin extracted from black soybean reduces prostate weight and promotes apoptosis in the prostatic hyperplasia-induced rat model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsV2gtrnK&md5=2e9c35295f66b3a5e9623690a3ba970eCAS |
Jarow, J. P., Assimos, D. G., and Pittaway, D. E. (1993). Effectiveness of laparoscopic varicocelectomy. Urology 42, 544–547.
| Effectiveness of laparoscopic varicocelectomy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2FlsVynsw%3D%3D&md5=202b0582a6656981860be16c43725176CAS | 8236598PubMed |
Ko, K. W., Chae, J. Y., Kim, S. W., Moon, D. G., Kim, J. J., Yoon, D. K., and Park, J. Y. (2010). The effect of the partial obstruction site of the renal vein on testis and kidney in rats: is the traditional animal model suitable for varicocele research? Korean J. Urol. 51, 565–571.
| The effect of the partial obstruction site of the renal vein on testis and kidney in rats: is the traditional animal model suitable for varicocele research?Crossref | GoogleScholarGoogle Scholar | 20733964PubMed |
Lyon, R. P., Marshall, S., and Scott, M. P. (1982). Varicocele in childhood and adolescence: implication in adulthood infertility? Urology 19, 641–644.
| Varicocele in childhood and adolescence: implication in adulthood infertility?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL383isFWnsA%3D%3D&md5=b29fcad29e9790c5addb4b03b3636489CAS | 7090115PubMed |
Naughton, C. K., Nangia, A. K., and Agarwal, A. (2001). Pathophysiology of varicoceles in male infertility. Hum. Reprod. Update 7, 473–481.
| Pathophysiology of varicoceles in male infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrgvVSlsw%3D%3D&md5=ebb903aa7171dcf9057ae9f226553921CAS | 11556494PubMed |
Ralph, D. J., Timoney, A. G., Parker, C., and Pryor, J. P. (1993). Laparoscopic varicocele ligation. Br. J. Urol. 72, 230–233.
| 1:STN:280:DyaK2c%2FgsFGntw%3D%3D&md5=f50aeaa0916943c9f684ad438e61f685CAS | 8402029PubMed |
Rosenblat, M., Hayek, T., and Aviram, M. (2006). Anti-oxidative effects of pomegranate juice (PJ) consumption by diabetic patients on serum and on macrophages. Atherosclerosis 187, 363–371.
| Anti-oxidative effects of pomegranate juice (PJ) consumption by diabetic patients on serum and on macrophages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xms1agsLY%3D&md5=12dc0bc0b1e018805a050db1e753d93fCAS | 16226266PubMed |
Saleh, R. A., Agarwal, A., Sharma, R. K., Said, T. M., Sikka, S. C., and Thomas, A. J., (2003). Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertil. Steril. 80, 1431–1436.
| Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele.Crossref | GoogleScholarGoogle Scholar | 14667879PubMed |
Saypol, D. C., Howards, S. S., Turner, T. T., and Miller, E. D., (1981). Influence of surgically induced varicocele on testicular blood flow, temperature, and histology in adult rats and dogs. J. Clin. Invest. 68, 39–45.
| Influence of surgically induced varicocele on testicular blood flow, temperature, and histology in adult rats and dogs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M3ktVWisQ%3D%3D&md5=7d2e9849c852d50b82c0b91edc4a0d02CAS | 7251866PubMed |
Sharma, R. K., and Agarwal, A. (1996). Role of reactive oxygen species in male infertility. Urology 48, 835–850.
| Role of reactive oxygen species in male infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s7ivFWhtw%3D%3D&md5=a607a0524bbee21375680226c553478cCAS | 8973665PubMed |
Shih, P. H., Yeh, C. T., and Yen, G. C. (2005). Effects of anthocyanidin on the inhibition of proliferation and induction of apoptosis in human gastric adenocarcinoma cells. Food Chem. Toxicol. 43, 1557–1566.
| Effects of anthocyanidin on the inhibition of proliferation and induction of apoptosis in human gastric adenocarcinoma cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmt1ehsrk%3D&md5=321bde907adf40d0e2fc63c7577a21e0CAS | 15964118PubMed |
Sonmez, M., Turk, G., and Yuce, A. (2005). The effect of ascorbic acid supplementation on sperm quality, lipid peroxidation and testosterone levels of male Wistar rats. Theriogenology 63, 2063–2072.
| The effect of ascorbic acid supplementation on sperm quality, lipid peroxidation and testosterone levels of male Wistar rats.Crossref | GoogleScholarGoogle Scholar | 15823361PubMed |
Sonmez, M., Yuce, A., and Turk, G. (2007). The protective effects of melatonin and Vitamin E on antioxidant enzyme activities and epididymal sperm characteristics of homocysteine treated male rats. Reprod. Toxicol. 23, 226–231.
| The protective effects of melatonin and Vitamin E on antioxidant enzyme activities and epididymal sperm characteristics of homocysteine treated male rats.Crossref | GoogleScholarGoogle Scholar | 17178211PubMed |
Sumner, M. D., Elliott-Eller, M., Weidner, G., Daubenmier, J. J., Chew, M. H., Marlin, R., Raisin, C. J., and Ornish, D. (2005). Effects of pomegranate juice consumption on myocardial perfusion in patients with coronary heart disease. Am. J. Cardiol. 96, 810–814.
| Effects of pomegranate juice consumption on myocardial perfusion in patients with coronary heart disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWnsbnP&md5=2ca1ca4774619b12632a4d75f3d6980bCAS | 16169367PubMed |
Turek, P., and Lipshultz, L. (1995). The varicocele controversies: II. Diagnosis and management. AUA Update Series 14, 114–119.
Turk, G., Atessahin, A., Sonmez, M., Yuce, A., and Ceribasi, A. O. (2007). Lycopene protects against cyclosporine A-induced testicular toxicity in rats. Theriogenology 67, 778–785.
| Lycopene protects against cyclosporine A-induced testicular toxicity in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlCksLc%3D&md5=2017321f4b83199669017e9da509d49fCAS | 17123593PubMed |
Turk, G., Sonmez, M., Aydin, M., Yuce, A., Gur, G., Yuksel, M., Aksu, E. H., and Aksoy, H. (2008). Effects of pomegranate juice consumption on sperm quality, spermatogenic cell density, antioxidant activity and testosterone level in male rats. Clin. Nutr. 27, 289–296.
| Effects of pomegranate juice consumption on sperm quality, spermatogenic cell density, antioxidant activity and testosterone level in male rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksVansbc%3D&md5=8a3150d1fc5a1f861958f6bf19276a45CAS | 18222572PubMed |
Wang, S. Y., and Jiao, H. (2000). Scavenging capacity of berry crops on superoxide radicals, hydrogen peroxide, hydroxyl radicals, and singlet oxygen. J. Agric. Food Chem. 48, 5677–5684.
| Scavenging capacity of berry crops on superoxide radicals, hydrogen peroxide, hydroxyl radicals, and singlet oxygen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsVamsrw%3D&md5=646d19e7894129676cf84366e334dd25CAS | 11087538PubMed |
