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Effect of in vitro exposure to lead chloride on semen quality and sperm DNA fragmentation

Published online by Cambridge University Press:  13 February 2014

M. Gomes
Affiliation:
Department of Biology & CICECO, University of Aveiro, Campus Universitário de Santiago, 3810–193, Aveiro, Portugal.
A. Gonçalves
Affiliation:
Centre for Reproductive Genetics Prof. Alberto Barros, Av. do Bessa, 240, 1º Dto. Frente, 4100–009 Porto, Portugal.
E. Rocha
Affiliation:
Department of Microscopy, Laboratory of Histology and Embryology, Institute of Biomedical Sciences Abel Salazar, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, E1, P2, R06, Porto, Portugal.
R. Sá
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar, UMIB, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, E1,P2,R07, Porto, Portugal.
A. Alves
Affiliation:
Department of Microscopy, Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar, UMIB, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, E1,P2,R07, Porto, Portugal.
J. Silva
Affiliation:
Centre for Reproductive Genetics Prof. Alberto Barros, Av. do Bessa, 240, 1º Dto. Frente, 4100–009 Porto, Portugal.
A. Barros
Affiliation:
Centre for Reproductive Genetics Prof. Alberto Barros, Av. do Bessa, 240, 1º Dto. Frente, 4100–009 Porto, Portugal. Department of Genetics, Faculty of Medicine, University of Porto, Alameda Prof. Hernâni Monteiro, 4200–319 Porto, Portugal.
M.L. Pereira
Affiliation:
Department of Biology & CICECO, University of Aveiro, Campus Universitário de Santiago, 3810–193, Aveiro, Portugal.
M. Sousa*
Affiliation:
Department of Microscopy, Laboratory of Cell Biology (Director), Building 1, Floor 2, Room 07, Institute of Biomedical Sciences Abel Salazar (ICBAS), UMIB, University of Porto, Rua Jorge Viterbo Ferreira.
*
All correspondence to: Mário Sousa. Department of Microscopy, Laboratory of Cell Biology (Director), Building 1, Floor 2, Room 07, Institute of Biomedical Sciences Abel Salazar (ICBAS), UMIB, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050–313 Porto, Portugal Tel: + 351 220 428 000 (Faculty); + 351 220 428 246 (Office). Fax: +351–22 042 80 90 e-mail: msousa@icbas.up.pt

Summary

Exposure to lead may cause changes in the male reproductive system. We evaluated the effect of lead chloride (PbCl2) in vitro on semen quality from 31 individuals. Samples were incubated at room temperature for two exposure times (4 h and 8 h) and with two concentrations of PbCl2 (15 μg/ml or 30 μg/ml). Results showed that PbCl2 significantly inhibited rapid progressive motility and caused an increase in the percentage of tail anomalies in both times and concentrations assessed, as well as a decrease in vitality in the group exposed to 30 μg/ml PbCl2. A significant increase in immotile sperm was also observed between the group control and the groups submitted to lead. Total motility and DNA fragmentation also showed a significant decrease and increase, respectively, after 4 h of incubation in the group exposed to 30 μg/ml and in both groups after 8 h of incubation. In conclusion, PbCl2 affected sperm parameters and DNA integrity, which are essential for male fertility.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

Agency for Toxic Substances and Disease Registry (2007). Toxicological Profile for Lead. US Department of Health and Human Services. Division of Toxicology and Environmental Medicine/Applied Toxicology Branch, Atlanta, Georgia, USA.Google Scholar
Aitken, R.J. & Krausz, C. (2001). Oxidative stress, DNA damage and the Y chromosome. Reproduction 122, 497506.CrossRefGoogle ScholarPubMed
Aitken, R.J. & Bennetts, L. (2006). Reactive oxygen species: friend or foe. In The Sperm Cell. Production, Maturation, Fertilization, Regeneration (eds. De Jonge, C.J. & Barratt, C.L.R.), pp. 170–93. Cambridge, New York: Cambridge University Press.CrossRefGoogle Scholar
Amaral, A., Castillo, J., Estanyol, J.M., Ballescà, J.L., Ramalho-Santos, J. & Oliva, R. (2013). Human sperm tail proteome suggests new endogenous metabolic pathways. Mol. Cell. Proteomics 12, 330–42.CrossRefGoogle ScholarPubMed
Auger, J., Eustache, F., Andersen, A.G., Irvine, D.S., Jørgensen, N., Skakkebæk, N.E., Suominen, J., Toppari, J., Vierula, M. & Jouannet, P. (2001). Sperm morphological defects related to environment, lifestyle and medical history of 1001 male partners of pregnant women from four European cities. Hum. Reprod. 16, 2710–7.Google Scholar
Bejarano, I., Espino, J., Paredes, S.D., Ortiz, A., Lozano, G., Pariente, J.A. & Rodriguez, A.B. (2012). Apoptosis, ROS and calcium signaling in human spermatozoa: relationship to infertility. In Male Infertility (ed. Bashamboo, A.), pp. 5176. Croatia: INTECH.Google Scholar
Benoff, S., Jacob, A. & Hurley, I.R. (2000a). Male infertility and environmental exposure to lead and cadmium. Hum. Reprod. Update 6, 107–21.Google Scholar
Benoff, S., Cooper, G.W., Centola, G.M., Jacob, A., Hershlag, A. & Hurley, I.R. (2000b). Metal ions and human sperm mannose receptors. Andrologia 32 (4–5), 317–29.CrossRefGoogle ScholarPubMed
Benoff, S., Centola, G.M., Millan, C., Napolitano, B., Marmar, J.L. & Hurley, I.R. (2003). Increased seminal plasma lead levels adversely affect the fertility potential of sperm in IVF. Hum. Reprod. 18, 374–83.Google Scholar
Cocuzza, M., Sikka, S.C., Athayde, K.S. & Agarwal, A. (2007). Clinical relevance of oxidative stress and sperm chromatin damage in male infertility: an evidence based analysis. Int. Braz. J. Urol. 33, 603–21.Google Scholar
de Lamirande, E. & Gagnon, C. (1992). Reactive oxygen species and human spermatozoa. I. Effects on the motility of intact spermatozoa and on sperm axonemes. J. Androl. 13, 368–78.Google Scholar
De Rosa, M., Zarrilli, S., Paesano, L., Carbone, U., Boggia, B., Petretta, M., Maisto, A., Cimmino, F., Puca, G., Colao, A. & Lombardi, G. (2003). Traffic pollutants affect fertility in men. Hum. Reprod. 8, 1055–61.CrossRefGoogle Scholar
Delbès, G., Hales, B.F. & Robaire, B. (2010). Toxicants and human sperm chromatin integrity. Mol. Hum. Reprod. 16, 1422.CrossRefGoogle ScholarPubMed
Fisher-Fischbein, J., Fischbein, A., Melnick, H.D. & Bardin, C.W. (1987). Correlation between biochemical indicators of lead exposure and semen quality in a lead-poisoned firearms instructor. JAMA 257, 803–5.CrossRefGoogle Scholar
Gagnon, C. & de Lamirande, E. (2006). Controls of sperm motility. In The Sperm Cell. Production, Maturation, Fertilization, Regeneration (eds. De Jonge, C.J. & Barratt, C.L.R.), pp. 108–33. Cambridge, New York: Cambridge University Press.Google Scholar
Gavrieli, Y., Sherman, Y. & Ben-Sasson, S.A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493501.Google Scholar
Ghaffari, M.A. & Motlagh, B. (2011). In vitro effect of lead, silver, tin, mercury, indium and bismuth on human sperm creatine kinase activity: a presumable mechanism for men infertility. Iran. Biomed. J. 15 (1–2), 3843.Google ScholarPubMed
González-Marín, C., Gosálvez, J. & Roy, R. (2012). Types, causes, detection and repair of DNA fragmentation in animal and human sperm cells. Int. J. Mol. Sci. 13 (11), 14026–52.CrossRefGoogle ScholarPubMed
Griveau, J.F. & Le Lannou, D. (1997). Reactive oxygen species and human spermatozoa: physiology and pathology. Int. J. Androl. 20, 61–9.Google Scholar
Hammoud, A., Carrell, D.T., Gibson, M., Sanderson, M., Parker-Jones, K. & Peterson, C.M. (2010). Decreased sperm motility is associated with air pollution in Salt Lake City. Fertil. Steril. 93, 1875–9.CrossRefGoogle ScholarPubMed
Hernández-Ochoa, I., García-Vargas, G., López-Carrillo, L., Rubio-Andrade, M., Morán-Martínez, J., Cebrián, M.E. & Quintanilla-Vega, B. (2005). Low lead environmental exposure alters semen quality and sperm chromatin condensation in northern Mexico. Reprod. Toxicol. 20, 221–8.Google Scholar
Hess, R.A. & De Franca, L.R. (2008). Spermatogenesis and cycle of the seminiferous epithelium. In Molecular Mechanisms in Spermatogenesis (ed. Cheng, C.Y.), pp. 115. New York: Springer.Google Scholar
Hsu, P.-C, Chang, Ho-Y., Guo, Y.L., Liu, Y.-C. & Shih, T.-S. (2009). Effect of smoking on blood lead levels in workers and role of reactive oxygen species in lead-induced sperm chromatin DNA damage. Fertil. Steril. 91, 1096–103.Google Scholar
Huang, Y.-L, Tseng, W.-C. & Lin, Te-H. (2001). In vitro effects of metal ions (Fe2+, Mn2+, Pb2+) on sperm motility and lipid peroxidation in human semen. J. Toxicol. Environ. Health. Part A. 62, 259–67.Google Scholar
Kanwar, U., Chadha, S., Batla, A., Sanyal, S.N. & Sandhu, R. (1988). Effect of selected metal ions on the motility and carbohydrate metabolism of ejaculated human spermatozoa. Indian J. Physiol. Pharmacol. 32, 195201.Google Scholar
Kasperczyk, S., Birkner, E., Kasperczyk, A. & Zalejska-Fiolka, J. (2004). Activity of superoxide dismutase and catalase in people protractedly exposed to lead compounds. Ann. Agric. Environ. Med. 11, 291–6.Google Scholar
Kasperczyk, A., Kasperczyk, S., Horak, S., Ostałowska, A., Grucka-Mamczar, E., Romuk, E., Olejek, A. & Birkner, E. (2008). Assessment of semen function and lipid peroxidation among lead exposed men. Toxicol. Appl. Pharmacol. 228, 378–84.Google Scholar
Levin, S.M. & Goldberg, M. (2000). Clinical evaluation and management of lead-exposed construction workers. Am. J. Ind. Med. 37, 2343.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Li, P., Zhong, Y., Jiang, X., Wang, C., Zuo, Z. & Sha, A. (2012). Seminal plasma metals concentration with respect to semen quality. Biol. Trace Elem. Res. 148, 16.CrossRefGoogle ScholarPubMed
Liu, W., Kato, M., Akhand, A.A., Hayakawa, A., Suzuki, H., Miyata, T., Kurokawa, K., Hotta, Y., Ishikawa, N. & Nakashima, I. (2000). 4-Hydroxynonenal induces a cellular redox status-related activation of the caspase cascade for apoptotic cell death. J. Cell Sci. 113 (Pt4), 635–41.Google Scholar
Maneesh, M. & Jayalekshmi, H. (2006). Role of reactive oxygen species and antioxidants on pathophysiology of male reproduction. Indian J. Clin. Biochem. 21, 80–9.Google Scholar
Mendiola, J., Torres-Cantero, A.M., Moreno-Grau, J.M., Ten, J., Roca, M., Moreno-Grau, S. & Bernabeu, R. (2008). Exposure to environmental toxins in males seeking infertility treatment: a case-controlled study. Reprod. Biomed. Online 16, 842–50.Google Scholar
Naha, N. & Chowdhury, A.R. (2006). Inorganic lead exposure in battery and paint factory: effect on human sperm structure and functional activity. J. UOEH 28, 157–71.Google Scholar
Naha, N., Bhar, R.B., Mukherjee, A. & Chowdhury, A.R. (2005). Structural alteration of spermatozoa in the persons employed in lead acid battery factory. Indian J. Physiol. Pharmacol. 49, 153–62.Google Scholar
Nascimento, J.M., Shi, L.Z., Tam, J., Chandsawangbhuwana, C., Durrant, B., Botvinick, E.L. & Berns, M.W. (2008). Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J. Cell. Physiol. 217, 745–51.Google Scholar
Olsen, A., Lindeman, B., Wiger, R., Duale, N. & Brunborg, G. (2005). How do male germ cells handle DNA damage? Toxicol. Appl. Pharmacol. 207(Suppl. 2), 521–31.Google Scholar
Pant, N., Upadhyay, G., Pandey, S., Mathur, N., Saxena, D.K. & Srivastava, S.P. (2003). Lead and cadmium concentration in the seminal plasma of men in the general population: correlation with sperm quality. Reprod. Toxicol. 17, 447–50.Google Scholar
Patrick, L. (2006). Lead Toxicity Part II: The role of free radical damage and the use of antioxidants in the pathology and treatment of lead toxicity. Altern. Med. Rev. 11, 114–27.Google ScholarPubMed
Quintanilla-Vega, B., Hoover, D.J., Bal, W., Silbergeld, E.K., Waalkes, M.P. & Anderson, L.D. (2000a). Lead interaction with human protamine (HP2) as a mechanism of male reproductive toxicity. Chem. Res. Toxicol. 13, 594600.Google Scholar
Quintanilla-Vega, B., Hoover, D.J., Bal, W., Silbergeld, E.K., Waalkes, M.P. & Anderson, L.D. (2000b) Lead Effects on protamine–DNA binding. Am. J. Ind. Med. 38, 324–9.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Ramalho-Santos, J., Amaral, A., Sousa, A.P., Rodrigues, A.S., Martins, L., Baptista, M., Mota, P.C., Tavares, R., Amaral, S. & Gamboa, S. (2007). Probing the structure and function of mammalian sperm using optical and fluorescence microscopy. In Modern Research and Educational Topics in Microscopy, vol. 1 (eds. Mendez-Vilas, A. & Diaz, J.), pp. 394402. Badajoz, Spain: Formatex.Google Scholar
Sakkas, D. & Alvarez, J.G. (2010). Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil. Steril. 93, 1027–36.CrossRefGoogle ScholarPubMed
Sallmén, M. (2001). Exposure to lead and male fertility. Int. J. Occup. Med. Environ. Health. 14, 219–22.Google Scholar
Sergerie, M., Laforest, G., Boulanger, K., Bissonnette, F. & Bleau, G. (2005a). Longitudinal study of sperm DNA fragmentation as measured by terminal uridine nick end-labelling assay. Hum. Reprod. 20, 1921–7.Google Scholar
Sergerie, M., Laforest, G., Bujan, L., Bissonnette, F. & Bleau, G. (2005b). Sperm DNA fragmentation: threshold value in male fertility. Hum. Reprod. 20, 3446–51.Google Scholar
Telisman, S., Cvitkovic, P., Jurasovic, J., Pizent, A., Gavella, M. & Rocic, B. (2000). Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environ. Health Perspect. 108, 4553.Google Scholar
Telisman, S., Colak, B., Pizenta, A., Jurasovic, J. & Cvitkovic, P. (2007). Reproductive toxicity of low-level lead exposure in men. Environ. Res. 105, 256–66.CrossRefGoogle ScholarPubMed
TNO Strategy, Technology and Policy (2005). Risks to Health and the Environment Related to the Use of Lead in Products. The Netherlands: TNO.Google Scholar
United Nations Environment Programme (2003). Technical Guidelines for the Environmentally Sound Management of Waste Lead-Acid Batteries. Basel, Switzerland: UNEP.Google Scholar
World Health Organization, (1980). Recommended Health-Based Limits in Occupational Exposure to Heavy Metals. Geneva, Switzerland: WHO Press.Google Scholar
World Health Organization, (2010). Semen analysis. In Laboratory Manual for the Examination and Processing of Human Semen, 5th edn, pp. 7114. Geneva, Switzerland: WHO Press.Google Scholar
Xu, De-X., Shen, H.-M., Zhu, Qi-X., Chua, L., Wang, Qu-N., Chia, S.-E. & Ong, C.-N. (2003). The associations among semen quality, oxidative DNA damage in human spermatozoa and concentrations of cadmium, lead and selenium in seminal plasma. Mutat. Res. 534 (1–2), 155–63.Google Scholar
Ye, X.-B., Fu, H., Zhu, J.-L., Ni, W.-M., Lu, Y.-W., Kuang, X.-Ya., Yang, S.-L. & Shu, B.-X. (1999). A study on oxidative stress in lead-exposed workers. J. Toxicol. Environ. Health 57, 161–72.Google Scholar
Yeung, C.H., Tüttelmann, F., Bergmann, M., Nordhoff, V., Vorona, E. & Cooper, T.G. (2009). Coiled sperm from infertile patients: characteristics, associated factors and biological implication. Hum. Reprod. 24, 1288–95.Google Scholar