Sertoli cell is a potential target for perfluorooctane sulfonate-induced reproductive dysfunction in male mice

Toxicological Sciences

Volumn 135, Issue 1, 2013, Pages 229-240

  Qiu, Lianglin ^a,b,c   Zhang, Xuhui ^a,c   Zhang, Xiaoming ^a,c   Zhang, Yudong ^a,c   Gu, Jun ^a,c   Chen, Minjian ^a,c   Zhang, Zhan ^a,c   Wang, Xinru ^a,c   Wang, Shou Lin ^a,c  

^a NANJING MEDICAL UNIVERSITY   (China)

^b NANTONG UNIVERSITY   (China)

^c Nanjing Medical University   (China)

Author keywords

Blood testis barrier; Male reproductive dysfunction; Mapk signal pathway; Perfluorooctane sulfonate; Sertoli cells

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CLAUDIN 11; CONNEXIN 43; MITOGEN ACTIVATED PROTEIN KINASE; OCCLUDIN; PERFLUOROOCTANESULFONIC ACID; PROTEIN ZO1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD TESTIS BARRIER; CELL MEMBRANE PERMEABILITY; CELL ULTRASTRUCTURE; CELL VACUOLE; CONTROLLED STUDY; CYTOTOXICITY; ELECTRIC RESISTANCE; MALE; MALE GENITAL SYSTEM DISEASE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REPRODUCTIVE TOXICITY; SEMINIFEROUS TUBULE; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATOZOON COUNT;

BLOOD-TESTIS BARRIER; MALE REPRODUCTIVE DYSFUNCTION; MAPK SIGNAL PATHWAY.; PERFLUOROOCTANE SULFONATE; SERTOLI CELLS;

ALKANESULFONIC ACIDS; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUOROCARBONS; MALE; MICE; MICE, INBRED ICR; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SERTOLI CELLS; SPERMATOGENESIS; TESTIS; TIGHT JUNCTION PROTEINS;

EID: 84883176629     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft129     Document Type: Article

References (36)

1. Bao, L. J., Maruya, K. A., Snyder, S. A., and Zeng, E. Y. (2012). China's water pollution by persistent organic pollutants. Environ. Pollut. 163, 100-108.
2. Cheng, C. Y., Wong, E. W., Lie, P. P., Li, M. W., Su, L., Siu, E. R., Yan, H. H., Mannu, J., Mathur, P. P., Bonanomi, M., et al. (2011). Environmental toxicants and male reproductive function. Spermatogenesis 1, 2-13.
3. Eid, N., Ito, Y., and Otsuki, Y. (2012). Enhanced mitophagy in Sertoli cells of ethanol-treated rats: Morphological evidence and clinical relevance. J. Mol. Histol. 43, 71-80.
4. Fiorini, C., Tilloy-Ellul, A., Chevalier, S., Charuel, C., and Pointis, G. (2004). Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod. Toxicol. 18, 413-421.
5. Jensen, A. A., and Leffers, H. (2008). Emerging endocrine disrupters: Perfluoroalkylated substances. Int. J. Androl. 31, 161-169.
6. Joensen, U. N., Bossi, R., Leffers, H., Jensen, A. A., Skakkebaek, N. E., and Jørgensen, N. (2009). Do perfluoroalkyl compounds impair human semen quality? Environ. Health Perspect. 117, 923-927.
7. Johnson, L., Thompson, D. L., Jr, and Varner, D. D. (2008). Role of Sertoli cell number and function on regulation of spermatogenesis. Anim. Reprod. Sci. 105, 23-51.
8. La Rocca, C., Alessi, E., Bergamasco, B., Caserta, D., Ciardo, F., Fanello, E., Focardi, S., Guerranti, C., Stecca, L., Moscarini, M., et al. (2012). Exposure and effective dose biomarkers for perfluorooctane sulfonic acid (PFOS) and perfluorooctanoic acid (PFOA) in infertile subjects: Preliminary results of the PREVIENI project. Int. J. Hyg. Environ. Health 215, 206-211.
9. Li, M. W., Mruk, D. D., Lee, W. M., and Cheng, C. Y. (2009). Disruption of the blood-testis barrier integrity by bisphenol A in vitro: Is this a suitable model for studying blood-testis barrier dynamics? Int. J. Biochem. Cell Biol. 41, 2302-2314.
10. Lim, T. C., Wang, B., Huang, J., Deng, S., and Yu, G. (2011). Emission inventory for PFOS in China: Review of past methodologies and suggestions. ScientificWorldJournal 11, 1963-1980.
11. Lui, W. Y., Lee, W. M., and Cheng, C. Y. (2003a). Transforming growth factor beta3 regulates the dynamics of Sertoli cell tight junctions via the p38 mitogen-activated protein kinase pathway. Biol. Reprod. 68, 1597-1612.
12. Lui, W. Y., Wong, C. H., Mruk, D. D., and Cheng, C. Y. (2003b). TGF-beta3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: An in vivo study. Endocrinology 144, 1139-1142.
13. Morrow, C. M., Tyagi, G., Simon, L., Carnes, K., Murphy, K. M., Cooke, P. S., Hofmann, M. C., and Hess, R. A. (2009). Claudin 5 expression in mouse seminiferous epithelium is dependent upon the transcription factor ets variant 5 and contributes to blood-testis barrier function. Biol. Reprod. 81, 871-879.
14. Mruk, D. D., and Cheng, C. Y. (2011). An in vitro system to study Sertoli cell blood-testis barrier dynamics. Methods Mol. Biol. 763, 237-252.
15. Nah, W. H., Lee, J. E., Park, H. J., Park, N. C., and Gye, M. C. (2011). Claudin-11 expression increased in spermatogenic defect in human testes. Fertil. Steril. 95, 385-388.
16. OECD (2002). Hazard Assessment of Perfluorooctane Sulfonate (PFOS) and Its Salts. Available at: http://www.oecd.org/dataoecd/23/18/2382880.pdf. Accessed November 21, 2002.
17. Pointis, G., Gilleron, J., Carette, D., and Segretain, D. (2011). Testicular connexin 43, a precocious molecular target for the effect of environmental toxicants on male fertility. Spermatogenesis 1, 303-317.
18. Rajendar, B., Bharavi, K., Rao, G. S., Kishore, P. V., Kumar, P. R., Kumar, C. S., and Patel, T. P. (2011). Protective effect of an aphrodisiac herb Tribulus terrestris Linn on cadmium-induced testicular damage. Indian J. Pharmacol. 43, 568-573.
19. Rosen, M. B., Schmid, J. E., Das, K. P., Wood, C. R., Zehr, R. D., and Lau, C. (2009). Gene expression profiling in the liver and lung of perfluorooctane sulfonate-exposed mouse fetuses: Comparison to changes induced by exposure to perfluorooctanoic acid. Reprod. Toxicol. 27, 278-288.
20. Siu, E. R., Mruk, D. D., Porto, C. S., and Cheng, C. Y. (2009). Cadmiuminduced testicular injury. Toxicol. Appl. Pharmacol. 238, 240-249.
21. Su, L., Cheng, C. Y., and Mruk, D. D. (2010). Adjudin-mediated Sertoli-germ cell junction disassembly affects Sertoli cell barrier function in vitro and in vivo. Int. J. Biochem. Cell Biol. 42, 1864-1875.
22. Su, L., Mruk, D. D., Lui, W. Y., Lee, W. M., and Cheng, C. Y. (2011). P-glycoprotein regulates blood-testis barrier dynamics via its effects on the occludin/zonula occludens 1 (ZO-1) protein complex mediated by focal adhesion kinase (FAK). Proc. Natl. Acad. Sci. U. S. A. 108, 19623-19628.
23. Thibodeaux, J. R., Hanson, R. G., Rogers, J. M., Grey, B. E., Barbee, B. D., Richards, J. H., Butenhoff, J. L., Stevenson, L. A., and Lau, C. (2003). Exposure to perfluorooctane sulfonate during pregnancy in rat and mouse. I: Maternal and prenatal evaluations. Toxicol. Sci. 74, 369-381.
24. Toft, G., Jönsson, B. A., Lindh, C. H., Giwercman, A., Spano, M., Heederik, D., Lenters, V., Vermeulen, R., Rylander, L., Pedersen, H. S., et al. (2012). Exposure to perfluorinated compounds and human semen quality in Arctic and European populations. Hum. Reprod. 27, 2532-2540.
25. Wan, H. T., Zhao, Y. G., Wong, M. H., Lee, K. F., Yeung, W. S., Giesy, J. P., and Wong, C. K. (2011). Testicular signaling is the potential target of perfluorooctanesulfonate- mediated subfertility in male mice. Biol. Reprod. 84, 1016-1023.
26. Wang, D., Kamijima, M., Okamura, A., Ito, Y., Yanagiba, Y., Jia, X. F., Naito, H., Ueyama, J., and Nakajima, T. (2012). Evidence for diazinon-mediated inhibition of cis-permethrin metabolism and its effects on reproductive toxicity in adult male mice. Reprod. Toxicol. 34, 489-497.
27. Wang, Y., Fu, J., Wang, T., Liang, Y., Pan, Y., Cai, Y., and Jiang, G. (2010). Distribution of perfluorooctane sulfonate and other perfluorochemicals in the ambient environment around a manufacturing facility in China. Environ. Sci. Technol. 44, 8062-8067.
28. Wang, X., Li, B., Zhao, W. D., Liu, Y. J., Shang, D. S., Fang, W. G., and Chen, Y. H. (2011). Perfluorooctane sulfonate triggers tight junction "opening" in brain endothelial cells via phosphatidylinositol 3-kinase. Biochem. Biophys. Res. Commun. 410, 258-263.
29. Wong, C. H., Mruk, D. D., Siu, M. K., and Cheng, C. Y. (2005). Blood-testis barrier dynamics are regulated by {alpha}2-macroglobulin via the c-Jun N-terminal protein kinase pathway. Endocrinology 146, 1893-1908.
30. Wong, E. W., and Cheng, C. Y. (2011). Impacts of environmental toxicants on male reproductive dysfunction. Trends Pharmacol. Sci. 32, 290-299.
31. Xiao, X., Mruk, D. D., Lee, W. M., and Cheng, C. Y. (2011). c-Yes regulates cell adhesion at the blood-testis barrier and the apical ectoplasmic specialization in the seminiferous epithelium of rat testes. Int. J. Biochem. Cell Biol. 43, 651-665.
32. Yeung, L. W., So, M. K., Jiang, G., Taniyasu, S., Yamashita, N., Song, M., Wu, Y., Li, J., Giesy, J. P., Guruge, K. S., et al. (2006). Perfluorooctanesulfonate and related fluorochemicals in human blood samples from China. Environ. Sci. Technol. 40, 715-720.
33. Yao, P. L., Lin, Y. C., and Richburg, J. H. (2010). Mono-(2-ethylhexyl) phthalate-induced disruption of junctional complexes in the seminiferous epithelium of the rodent testis is mediated by MMP2. Biol. Reprod. 82, 516-527.
34. Zhang, J., Liang, J., Zhu, H., Li, C., and Wu, Q. (2011). PFOS and PCB 153 have direct adverse effects on neonatal testis modeled using a coculture of primary gonocyte and sertoli cells. Environ. Toxicol. 28, 322-331.
35. Zhang, L., Liu, J., Hu, J., Liu, C., Guo, W., Wang, Q., and Wang, H. (2012). The inventory of sources, environmental releases and risk assessment for perfluorooctane sulfonate in China. Environ. Pollut. 165, 193-198.
36. Zhang, T., Wu, Q., Sun, H. W., Zhang, X. Z., Yun, S. H., and Kannan, K.Perfluorinated compounds in whole blood samples from infants, children, and adults in China. Environ. Sci. Technol. 44, 4341-4347.