Amelioration of sperm count and sperm quality by lycopene supplementation in irradiated mice
Małgorzata M. Dobrzyńska
A B and Aneta Gajowik A
+ Author Affiliations
- Author Affiliations
A National Institute of Public Health – National Institute of Hygiene, Department of Radiation Hygiene and Radiobiology, 24 Chocimska Street, 00-791 Warsaw, Poland.
B Corresponding author. Email: mdobrzynska@pzh.gov.pl
Reproduction, Fertility and Development 32(12) 1040-1047 https://doi.org/10.1071/RD19433
Submitted: 25 November 2019 Accepted: 12 March 2020 Published: 31 July 2020
Abstract
Male mice were exposed to lycopene (LYC; 0.15 and 0.30 mg kg−1) and irradiation (0.5, 1 Gy) alone or in combination (0.5 Gy + 0.15 mg kg−1 LYC; 0.5 Gy + 0.30 mg kg−1 LYC; 1 Gy + 0.15 mg kg−1 LYC; 1 Gy + 0.30 mg kg−1 LYC) for 2 weeks. LYC administration in the drinking water was started 24 h or on Day 8 after the first irradiation dose or equivalent time point for groups treated with LYC alone. Sperm count, motility, morphology and DNA damage were determined at the end of the 2-week treatment period. Irradiation deteriorated sperm count and quality. Supplementation with LYC from 24 h significantly increased the sperm count compared with irradiation alone. In almost all combined treatment groups, the percentage of abnormal spermatozoa was significantly decreased compared with that after irradiation alone. In some cases, combined treatment reduced levels of DNA damage in gametes. Both doses of LYC administered from Day 8 significantly reduced the percentage of morphologically abnormal spermatozoa compared with that seen after 1 Gy irradiation and reduced DNA damage in all combined treatment groups. In conclusion, LYC supplementation after irradiation can ameliorate the harmful effects of irradiation on gametes. Mitigation of radiation-induced damage in germ cells following LYC administration may be useful for radiological accidents and to protect non-treated tissues in patients with cancer undergoing radiotherapy.
Additional keywords: germ cells, irradiation, mitigation.
References
Agarwal, A., Saleh, R. A., and Bedaiwy, M. A. (2003). Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil. Steril. 79, 829–843.| Role of reactive oxygen species in the pathophysiology of human reproduction.Crossref | GoogleScholarGoogle Scholar | 12749418PubMed |
Agarwal, A., Hamada, A., and Esteves, S. C. (2012). Insight into oxidative stress in varicocele-associated male infertility: part 1. Nat. Rev. Urol. 9, 678–690.
| Insight into oxidative stress in varicocele-associated male infertility: part 1.Crossref | GoogleScholarGoogle Scholar | 23165403PubMed |
Aitken, R. J., Irvine, D. S., and Wu, F. C. (1991). Prospective analysis of sperm–oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am. J. Obstet. Gynecol. 164, 542–551.
| Prospective analysis of sperm–oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility.Crossref | GoogleScholarGoogle Scholar | 1992700PubMed |
Aly, H. A., El-Beshbishy, H. A., and Banjar, Z. M. (2012). Mitochondrial dysfunction induced impairment of spermatogenesis in LPS-treated rats: modulatory role of lycopene. Eur. J. Pharmacol. 677, 31–38.
| Mitochondrial dysfunction induced impairment of spermatogenesis in LPS-treated rats: modulatory role of lycopene.Crossref | GoogleScholarGoogle Scholar | 22222822PubMed |
Andic, F., Garipagaoglu, M., Yurdakonar, E., Tuncel, N., and Kucuk, O. (2009). Lycopene in the prevention of gastrointestinal toxicity of radiotherapy. Nutr. Cancer 61, 784–788.
| Lycopene in the prevention of gastrointestinal toxicity of radiotherapy.Crossref | GoogleScholarGoogle Scholar | 20155616PubMed |
Ateşşahin, A., Karahan, İ., Türk, G., Gür, S., Yilmaz, S., and Çeribaşi, 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 | 15979841PubMed |
Ateşşahin, A., Türk, G., Karahan, İ., Yilmaz, S., Çeribaşi, A. O., and Bulmuş, Ö. (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 | 16616095PubMed |
Boeira, S. P., Funck, V. R., Borges Filho, C., Del’Fabbro, L., de Gomes, M. G., Donato, F., Royes, L. F., Oliveira, M. S., Jesse, C. R., and Furian, A. F. (2015). Lycopene protects against acute zearalenone-induced oxidative, endocrine, inflammatory and reproductive damages in male mice. Chem. Biol. Interact. 230, 50–57.
| Lycopene protects against acute zearalenone-induced oxidative, endocrine, inflammatory and reproductive damages in male mice.Crossref | GoogleScholarGoogle Scholar | 25682699PubMed |
Böhm, V., Frohlich, K., and Bitsch, R. (2003). Rosehip – a ‘new’ source of lycopene? Mol. Aspects Med. 24, 385–389.
| Rosehip – a ‘new’ source of lycopene?Crossref | GoogleScholarGoogle Scholar | 14585309PubMed |
Bonde, J. P. (2010). Male reproductive organs are at risk from environmental hazards. Asian J. Androl. 12, 152–156.
| Male reproductive organs are at risk from environmental hazards.Crossref | GoogleScholarGoogle Scholar | 19966832PubMed |
Bonde, J. P., and Giwercman, A. (1995). Occupational hazard to male fecundity. Reprod. Med. Rev. 4, 59–73.
| Occupational hazard to male fecundity.Crossref | GoogleScholarGoogle Scholar |
Cavusoglu, K., and Yalcin, E. (2009). Radioprotective effect of lycopene on chromosomal aberrations (CAs) induced by gamma radiation in human lymphocytes. J. Environ. Biol. 30, 113–117.
| 20112872PubMed |
Çeribaşi, A. O., Türk, G., Sönmez, M., Sakin, F., and Ateşşahin, A. (2010). Toxic effect of cyclophosphamide on sperm morphology, testicular histology and blood oxidant–antioxidant balance, and protective roles of lycopene and ellagic acid. Basic Clin. Pharmacol. Toxicol. 107, 730–736.
| Toxic effect of cyclophosphamide on sperm morphology, testicular histology and blood oxidant–antioxidant balance, and protective roles of lycopene and ellagic acid.Crossref | GoogleScholarGoogle Scholar | 20353483PubMed |
Chauhan, K., Sharma, S., Agarwal, N., and Chauhan, B. (2011). Lycopene of tomato fame: its role in health and disease. Int. J. Pharm. Sci. Rev. Res. 10, 99–115.
Choi, S. K., and Seo, J. S. (2013). Lycopene supplementation suppresses oxidative stress induced by a high fat diet in gerbils. Nutr. Res. Pract. 7, 26–33.
| Lycopene supplementation suppresses oxidative stress induced by a high fat diet in gerbils.Crossref | GoogleScholarGoogle Scholar | 23423845PubMed |
Citrin, D., Cotrim, A. P., Hyodo, F., Baum, B. J., Krishna, M. C., and Mitchell, J. B. (2010). Radioprotectors and mitigators of radiation-induced normal tissue injury. Oncologist 15, 360–371.
| Radioprotectors and mitigators of radiation-induced normal tissue injury.Crossref | GoogleScholarGoogle Scholar | 20413641PubMed |
Dobrzyńska, M. M. (2003). The changes in the quantity and quality of semen following subchronic exposure of mice to irradiation. In ‘Human Monitoring for Genetic Effects’. (Eds A. Cebulska-Wasilewska, W. W. Au, and R. J. Sram.) pp. 309–317. (IOS Press: Amsterdam.)
Dobrzyńska, M. M. (2005). The effects in mice of combined treatments to X-rays and antineoplastic drugs in the comet assay. Toxicology 207, 331–338.
| The effects in mice of combined treatments to X-rays and antineoplastic drugs in the comet assay.Crossref | GoogleScholarGoogle Scholar | 15596263PubMed |
Dobrzyńska, M. M., and Czajka, U. (2005). Male-mediated developmental toxicity after 8 weeks’ exposure to low doses of X-rays. Int. J. Radiat. Biol. 81, 793–799.
| Male-mediated developmental toxicity after 8 weeks’ exposure to low doses of X-rays.Crossref | GoogleScholarGoogle Scholar | 16484148PubMed |
Dobrzyńska, M. M., Jankowska-Steifer, E. A., Tyrkiel, E. J., Gajowik, A., Radzikowska, J., and Pachocki, K. A. (2014). Comparison of the effects of bisphenol A alone and in a combination with X-irradiation on sperm count and quality in male adult and pubescent mice. Environ. Toxicol. 29, 1301–1313.
| 23619965PubMed |
Dobrzyńska, M. M., Gajowik, A., and Radzikowska, J. (2019). The effect of lycopene supplementation on radiation-induced micronuclei in mice reticulocytes in vivo. Radiat. Environ. Biophys. 58, 425–432.
| The effect of lycopene supplementation on radiation-induced micronuclei in mice reticulocytes in vivo.Crossref | GoogleScholarGoogle Scholar | 31123854PubMed |
Durairajanayagam, D., Agarwal, A., Ong, C., and Prashast, P. (2014). Lycopene and male infertility. Asian J. Androl. 16, 420–425.
| Lycopene and male infertility.Crossref | GoogleScholarGoogle Scholar | 24675655PubMed |
Erenpreisa, J., Erenpreis, J., Freivalds, T., Slaidina, M., Krampe, R., Butikova, J., Ivanov, A., and Pjanova, D. (2003). Toluidine blue test for sperm DNA integrity and elaboration of image cytometry algorithm. Cytometry A 52A, 19–27.
| Toluidine blue test for sperm DNA integrity and elaboration of image cytometry algorithm.Crossref | GoogleScholarGoogle Scholar |
Forman, H. J., and Torres, M. (2002). Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am. J. Respir. Crit. Care Med. 166, S4–S8.
| Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling.Crossref | GoogleScholarGoogle Scholar | 12471082PubMed |
Fukunaga, H., Butterworth, K. T., Yokoya, A., Ogawa, T., and Prise, K. M. (2017). Low-dose radiation-induced risk in spermatogenesis. Int. J. Radiat. Biol. 93, 1291–1298.
| Low-dose radiation-induced risk in spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 28764606PubMed |
Gajowik, A., and Dobrzyńska, M. M. (2014). Lycopene – antioxidant with radioprotective and anticancer properties. A review. Rocz. Panstw. Zakl. Hig. 65, 263–271.
| 25526570PubMed |
Gerster, H. (1997). The potential role of lycopene for human health. J. Am. Coll. Nutr. 16, 109–126.
| The potential role of lycopene for human health.Crossref | GoogleScholarGoogle Scholar | 9100211PubMed |
Gharagozloo, P., and Aitken, R. J. (2011). The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum. Reprod. 26, 1628–1640.
| The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy.Crossref | GoogleScholarGoogle Scholar | 21546386PubMed |
Goyal, A., Chopra, M., Lwaleed, B. A., Birch, B., and Cooper, A. J. (2007). The effects of dietary lycopene supplementation on human seminal plasma. BJU Int. 99, 1456–1460.
| The effects of dietary lycopene supplementation on human seminal plasma.Crossref | GoogleScholarGoogle Scholar | 17484766PubMed |
Gupta, N. P., and Kumar, R. (2002). Lycopene therapy in idiopathic male infertility – a preliminary report. Int. Urol. Nephrol. 34, 369–372.
| Lycopene therapy in idiopathic male infertility – a preliminary report.Crossref | GoogleScholarGoogle Scholar | 12899230PubMed |
Hamada, A. J., Montgomery, B., and Agarwal, A. (2012). Male infertility: a critical review of pharmacologic management. Expert Opin. Pharmacother. 13, 2511–2531.
| Male infertility: a critical review of pharmacologic management.Crossref | GoogleScholarGoogle Scholar | 23121497PubMed |
Harrison, A., and Moore, P. C. (1980). Reduction in sperm count and increase in abnormal sperm in the mouse following X-radiation or injection of 22Na. Health Phys. 39, 219–224.
| Reduction in sperm count and increase in abnormal sperm in the mouse following X-radiation or injection of 22Na.Crossref | GoogleScholarGoogle Scholar | 7429832PubMed |
Hekimoglu, A., Kurcer, Z., Aral, F., Baba, F., Sahna, E., and Atessahin, A. (2009). Lycopene, an antioxidant carotenoid, attenuates testicular injury caused by ischemia/reperfusion in rats. Tohoku J. Exp. Med. 218, 141–147.
| Lycopene, an antioxidant carotenoid, attenuates testicular injury caused by ischemia/reperfusion in rats.Crossref | GoogleScholarGoogle Scholar | 19478470PubMed |
International Commission on Radiological Protection (ICRP) (2007). ICRP publication 103. The 2007 recommendations of the International Commission on Radiological Protection. Ann. ICRP 37, 1–332.
| 18762065PubMed |
Końca, K., Lankoff, A., Banasik, A., Lisowska, H., Kuszewski, T., Góźdź, S., Koza, Z., and Wojcik, A. (2003). A cross-platform public domain PC image-analysis program for comet assay. Mutat. Res. 534, 15–20.
| A cross-platform public domain PC image-analysis program for comet assay.Crossref | GoogleScholarGoogle Scholar | 12504751PubMed |
Krishnamoorthy, G., Selvakumar, K., Elumalai, P., Venkataraman, P., and Arunakaran, J. (2011). Protective role of lycopene on polychlorinated biphenyls (Aroclor 1254)-induced adult rat Sertoli cell dysfunction by increased oxidative stress and endocrine disruption. Biomed. Prev. Nutr. 1, 116–125.
| Protective role of lycopene on polychlorinated biphenyls (Aroclor 1254)-induced adult rat Sertoli cell dysfunction by increased oxidative stress and endocrine disruption.Crossref | GoogleScholarGoogle Scholar |
Kumar, D., Salian, S. R., Kalthur, G., Uppangala, S., Kumari, S., Challapalli, S., Chandraguthi, S. G., Krishnamurthy, H., Jain, N., Kumar, P., and Adiga, S. K. (2013). Semen abnormalities, sperm DNA and global hypermethylation in health workers occupationally exposed to ionizing radiation. PLOS One 8, e69927.
| 24367621PubMed |
Lee, J., Richburg, J. H., Younskin, S. C., and Boekelheide, K. (1997). The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138, 2081–2088.
| The Fas system is a key regulator of germ cell apoptosis in the testis.Crossref | GoogleScholarGoogle Scholar | 9112408PubMed |
Little, J. B. (2000). Radiation carcinogenesis. Carcinogenesis 21, 397–404.
| Radiation carcinogenesis.Crossref | GoogleScholarGoogle Scholar | 10688860PubMed |
Liu, G., Gong, P., Zhao, H., Wang, Z., Gong, S., and Cai, L. (2006). Effect of low-level radiation on the death of male germ cells. Radiat. Res. 165, 379–389.
| Effect of low-level radiation on the death of male germ cells.Crossref | GoogleScholarGoogle Scholar | 16579650PubMed |
Mangiagalli, M. G., Martino, P. A., Smajlovic, T., Guidobono Cavalchini, L., and Marelli, S. P. (2010). Effect of lycopene on semen quality, fertility and native immunity of broiler breeder. Br. Poult. Sci. 51, 152–157.
| Effect of lycopene on semen quality, fertility and native immunity of broiler breeder.Crossref | GoogleScholarGoogle Scholar | 20390581PubMed |
Mangiagalli, M. G., Cesari, V., Cerolini, S., Luzi, F., and Toschi, L. (2012). Effect of lycopene supplementation on semen quality and reproductive performance in rabbit. World Rabbit Sci. 20, 141–148.
| Effect of lycopene supplementation on semen quality and reproductive performance in rabbit.Crossref | GoogleScholarGoogle Scholar |
Mayne, S. T. (1996). Beta-carotene, carotenoids, and disease prevention in humans. FASEB J. 10, 690–701.
| Beta-carotene, carotenoids, and disease prevention in humans.Crossref | GoogleScholarGoogle Scholar | 8635686PubMed |
Meistrich, M. L. (2013). Effects of chemotherapy and radiotherapy on spermatogenesis in humans. Fertil. Steril. 100, 1180–1186.
| Effects of chemotherapy and radiotherapy on spermatogenesis in humans.Crossref | GoogleScholarGoogle Scholar | 24012199PubMed |
Meistrich, M. L., Hunter, N. R., Suzuki, N., Trostle, P. K., and Withers, H. R. (1978). Gradual regeneration of mouse testicular stem cells after exposure to ionizing radiation. Radiat. Res. 74, 349–362.
| Gradual regeneration of mouse testicular stem cells after exposure to ionizing radiation.Crossref | GoogleScholarGoogle Scholar | 149333PubMed |
Meydan, D., Gursel, B., Bilgici, B., Can, B., and Ozbek, N. (2011). Protective effect of lycopene against radiation-induced hepatic toxicity in rats. J. Int. Med. Res. 39, 1239–1252.
| Protective effect of lycopene against radiation-induced hepatic toxicity in rats.Crossref | GoogleScholarGoogle Scholar | 21986126PubMed |
Mohanty, N. K., Kumar, S., Jha, A. K., and Arora, R. P. (2001). Management of idiopathic oligoasthenospermia with lycopene. Indian J. Urol. 18, 57–61.
Mortimer, D., Barratt, C. L. R., Bjorndahl, L., de Jager, C., Jequier, A. M., and Muller, C. H. (2013). What should it take to describe a substance or product as ‘sperm-safe’. Hum. Reprod. Update 19, i1–i45.
| What should it take to describe a substance or product as ‘sperm-safe’.Crossref | GoogleScholarGoogle Scholar | 23552271PubMed |
Oborna, I., Malickova, K., Fingerova, H., Brezinova, J., Horka, P., Novotny, J., Bryndova, H., Filipcikova, R., and Svobodova, M. (2011). A randomized controlled trial of lycopene treatment on soluble receptor for advanced glycation end products in seminal and blood plasma of normospermic men. Am. J. Reprod. Immunol. 66, 179–184.
| A randomized controlled trial of lycopene treatment on soluble receptor for advanced glycation end products in seminal and blood plasma of normospermic men.Crossref | GoogleScholarGoogle Scholar | 21276122PubMed |
Palan, P., and Naz, R. (1996). Changes in various antioxidant levels in human seminal plasma related to immunoinfertility. Arch. Androl. 36, 139–143.
| Changes in various antioxidant levels in human seminal plasma related to immunoinfertility.Crossref | GoogleScholarGoogle Scholar | 8907675PubMed |
Palozza, P., Parrone, N., Catalano, A., and Simone, R. (2010). Tomato lycopene and inflammatory cascade: basic interactions and clinical implications. Curr. Med. Chem. 17, 2547–2563.
| Tomato lycopene and inflammatory cascade: basic interactions and clinical implications.Crossref | GoogleScholarGoogle Scholar | 20491642PubMed |
Palozza, P., Catalano, A., Simone, R., and Cittadini, A. (2012). Lycopene as a guardian of redox signalling. Acta Biochim. Pol. 59, 21–25.
| Lycopene as a guardian of redox signalling.Crossref | GoogleScholarGoogle Scholar | 22428131PubMed |
Rao, A. V., and Agarwal, S. (1999). Role of lycopene as antioxidant carotenoid in the prevention of chronic diseases: a review. Nutr. Res. 19, 305–323.
| Role of lycopene as antioxidant carotenoid in the prevention of chronic diseases: a review.Crossref | GoogleScholarGoogle Scholar |
Rao, A. V., and Agarwal, S. (2000). Role of antioxidant lycopene in cancer and heart disease. J. Am. Coll. Nutr. 19, 563–569.
| Role of antioxidant lycopene in cancer and heart disease.Crossref | GoogleScholarGoogle Scholar | 11022869PubMed |
Rao, A. V., and Rao, L. G. (2007). Carotenoids and human health. Pharmacol. Res. 55, 207–216.
| Carotenoids and human health.Crossref | GoogleScholarGoogle Scholar | 17349800PubMed |
Rao, A. V., Ray, M. R., and Rao, L. G. (2006). Lycopene. Adv. Food Nutr. Res. 51, 99–164.
| Lycopene.Crossref | GoogleScholarGoogle Scholar | 17011475PubMed |
Rato, L., Alves, M. G., Socorro, S., Duarte, A. I., Cavaco, J. E., and Oliveira, P. F. (2012). Metabolic regulation is important for spermatogenesis. Nat. Rev. Urol. 9, 330–338.
| Metabolic regulation is important for spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 22549313PubMed |
Rosato, M. P., Centoducati, G., Santacroce, M. P., and Iaffaldano, N. (2012). Effects of lycopene on in vitro quality and lipid peroxidation in refrigerated and cryopreserved turkey spermatozoa. Br. Poult. Sci. 53, 545–552.
| Effects of lycopene on in vitro quality and lipid peroxidation in refrigerated and cryopreserved turkey spermatozoa.Crossref | GoogleScholarGoogle Scholar | 23130590PubMed |
Saada, H. N., and Azab, K. S. (2001). Role of lycopene in recovery of radiation induced injury to mammalian cellular organelles. Pharmazie 56, 239–241.
Saada, H. N., Rezk, R. G., and Eltahawy, N. A. (2010). Lycopene protects the structure of the small intestine against gamma-radiation-induced oxidative stress. Phytother. Res. 24, S204–S208.
| Lycopene protects the structure of the small intestine against gamma-radiation-induced oxidative stress.Crossref | GoogleScholarGoogle Scholar | 20041432PubMed |
Sabeti, P., Pourmasumi, S., Rahiminia, T., Akyash, F., and Talebi, A. R. (2016). Etiologies of sperm oxidative stress. Int. J. Reprod. Biomed. (Yazd) 14, 231–240.
| Etiologies of sperm oxidative stress.Crossref | GoogleScholarGoogle Scholar |
Said, T. M., Paasch, U., Glander, H., and Agarwal, A. (2004). Role of caspases in male infertility. Hum. Reprod. Update 10, 39–51.
| Role of caspases in male infertility.Crossref | GoogleScholarGoogle Scholar | 15005463PubMed |
Salem, E. A., Salem, N. A., Maarouf, A. M., Serefoglu, E. C., and Hellstrom, W. J. (2012). Selenium and lycopene attenuate cisplatin-induced testicular toxicity associated with oxidative stress in Wistar rats. Urology 79, 1184.e1–1184.e6.
| Selenium and lycopene attenuate cisplatin-induced testicular toxicity associated with oxidative stress in Wistar rats.Crossref | GoogleScholarGoogle Scholar |
Searle, A. G., and Beechey, C. V. (1974). Sperm count, egg-fertilization and dominant lethality after X-irradiation of mice. Mutat. Res. 22, 63–72.
| Sperm count, egg-fertilization and dominant lethality after X-irradiation of mice.Crossref | GoogleScholarGoogle Scholar | 4842084PubMed |
Sharma, A. (2017). Male infertility; evidences, risk factors, causes, diagnosis and management in human. Ann. Clin. Lab. Res. 5, 188.
| Male infertility; evidences, risk factors, causes, diagnosis and management in human.Crossref | GoogleScholarGoogle Scholar |
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 | 8973665PubMed |
Sheiner, E. K., Sheiner, E., Hammel, R. D., Potashnik, G., and Carel, R. (2003). Effect of occupational exposures on male fertility: literature review. Ind. Health 41, 55–62.
| Effect of occupational exposures on male fertility: literature review.Crossref | GoogleScholarGoogle Scholar | 12725464PubMed |
Srinivasan, M., Sudheer, A. R., Pillai, K. R., Kumar, P. R., Suhakaran, P. R., and Menon, V. P. (2007). Lycopene as a natural protector against γ-radiation induced DNA damage, lipid peroxidation and antioxidant status in primary culture of isolated rat hepatocytes in vitro. Biochim. Biophys. Acta 1770, 659–665.
| Lycopene as a natural protector against γ-radiation induced DNA damage, lipid peroxidation and antioxidant status in primary culture of isolated rat hepatocytes in vitro.Crossref | GoogleScholarGoogle Scholar | 17189673PubMed |
Srinivasan, M., Devipriya, N., Kalpana, K. B., and Menon, V. P. (2009). Lycopene: an antioxidant and radioprotector against γ-radiation-induced cellular damages in cultured human lymphocytes. Toxicology 262, 43–49.
| Lycopene: an antioxidant and radioprotector against γ-radiation-induced cellular damages in cultured human lymphocytes.Crossref | GoogleScholarGoogle Scholar | 19450652PubMed |
Trejo-Solís, C., Pedraza-Chaverrí, J., Torres-Ramos, M., Jiménez-Farfán, D., Cruz Salgado, A., Serrano-García, N., Osorio-Riso, L., and Sotelo, J. (2013). Multiple molecular and cellucular mechanisms action of lycopene in cancer inhibition. Evid. Based Complement. Alternat. Med. 2013, 705121.
| Multiple molecular and cellucular mechanisms action of lycopene in cancer inhibition.Crossref | GoogleScholarGoogle Scholar | 23983787PubMed |
Tremellen, K. (2008). Oxidative stress and male infertility – a clinical perspective. Hum. Reprod. Update 14, 243–258.
| Oxidative stress and male infertility – a clinical perspective.Crossref | GoogleScholarGoogle Scholar | 18281241PubMed |
Türk, G., Ateşşahin, A., Sönmez, M., Yüce, A., and Çeribaşi, 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 | 17123593PubMed |
Tvrdá, E., Kováčik, A., Tušimová, E., Paál, D., Mackovich, A., Alimov, J., and Lukác, M. (2016). Antioxidant efficiency of lycopene on oxidative stress-induced damage in bovine spermatozoa. J. Anim. Sci. Biotechnol. 7, 50.
| Antioxidant efficiency of lycopene on oxidative stress-induced damage in bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 27602206PubMed |
Working, P. K., Bus, J. S., and Hamm, T. E. (1985). Reproductive effects of inhaled methyl chloride in the male Fisher 344 rat. II. Spermatogonial toxicity and sperm quality. Toxicol. Appl. Pharmacol. 77, 144–157.
| Reproductive effects of inhaled methyl chloride in the male Fisher 344 rat. II. Spermatogonial toxicity and sperm quality.Crossref | GoogleScholarGoogle Scholar | 3966237PubMed |
Wyrobek, A. J., and Bruce, W. R. (1975). Chemical induction of sperm abnormalities in mice. Proc. Natl Acad. Sci. USA 72, 4425–4429.
| Chemical induction of sperm abnormalities in mice.Crossref | GoogleScholarGoogle Scholar | 1060122PubMed |
Yamamoto, Y., Aizawa, K., Mieno, M., Karamatsu, M., Hirano, Y., Furui, K., Miyashita, T., Yamazaki, K., Inakuma, T., Sato, I., Suganuma, H., and Iwamato, T. (2017). The effects of tomato juice on male infertility. Asia Pac. J. Clin. Nutr. 26, 65–71.
| 28049263PubMed |
Zhou, D. D., Hao, J. L., Guo, K. M., Lu, C. W., and Liu, X. D. (2016). Sperm quality and DNA damage in men from Jilin Province, China, who are occupationally exposed to ionizing radiation. Genet. Mol. Res. 15, gmr8078.
| Sperm quality and DNA damage in men from Jilin Province, China, who are occupationally exposed to ionizing radiation.Crossref | GoogleScholarGoogle Scholar | 27706730PubMed |
Zini, A., San Gabriel, M., and Libman, J. (2010). Lycopene supplementation in vitro can protect human sperm deoxyribonucleic acid from oxidative damage. Fertil. Steril. 94, 1033–1036.
| Lycopene supplementation in vitro can protect human sperm deoxyribonucleic acid from oxidative damage.Crossref | GoogleScholarGoogle Scholar | 19439288PubMed |
