272
Views
13
CrossRef citations to date
0
Altmetric
Original Articles

In Utero Exposure to Environmentally Relevant Concentrations of PCB 153 and PCB 118 Disrupts Fetal Testis Development in Sheep

, , , , , & show all

REFERENCES

  • Acaro, K. F., Yi, L., Seegal, R. F., Vakharia, D. D., Yang, Y., Spink, D. C., Brosch, K., and Gierthy, J. F. 1999. 2,2′,6,6’-Tetrachlorobiphenyl is estrogenic in vitro and in vivo. J. Cell. Biochem. 72: 94–102.
  • Aire, T.A., and Ozegbe, P.C. 2008. Immunohistochemistry of the cytoskeleton in the excurrent ducts of the testis in birds of the Galloanserae monophyly. Cell Tissue Res. 333: 311–321.
  • Anjum, S., Rahman, S., Kaur, M., Ahmad, F., Rashid, H., Ansari, R.A., and Raisuddin, S. 2011. Melatonin ameliorates bisphenol A-induced biochemical toxicity in testicular mitochondria of mouse. Food Chain Toxicol. 49: 2849–2854.
  • Aumüller, G., Schulze, C., and Viebahn, C. 1992. Intermediate filaments in Sertoli cells. Microsc. Res. Tech. 20: 50–72.
  • Aumüller, G., Steinbrück, M., Krause, W., and Wagner, H. J. 1988. Distribution of vimentin-type intermediate filaments in Sertoli cells of the human testis, normal and pathologic. Anat. Embryol. (Berl.) 178: 129–136.
  • Bellingham, M., McKinnell, C., Fowler, P. A., Amezaga, M. R., Zhang, Z., Rhind, S. M., Cotinot, C., Mandon-Pepin, B., Evans, N. P., and Sharpe, R. M. 2012. Foetal and post-natal exposure of sheep to sewage sludge chemicals disrupts sperm production in adulthood in a subset of animals. Int. J. Androl 35: 317–329.
  • Berg, V., Lyche, J. L., Gutleb, A. C., Lie, E., Skaare, J. U., Aleksandersen, M., and Ropstad, E. 2010. Distribution of PCB 118 and PCB 153 and hydroxylated PCB metabolites (OH-CBs) in maternal, fetal and lamb tissue of sheep exposed during gestation and lactation. Chemosphere 80: 1144–1150.
  • Bernhoft, A., Wiig, O., and Skaare, J. U. 1997. Organochlorines in polar bears (Ursus maritimus) at Svalbard. Environ. Pollut. 95: 159–175.
  • Brouwer, A., Longnecker, M. P., Birnbaum, L. S., Cogliano, J., Kostyniak, P., Moore, J., Schantz, S., and Winneke, G. 1999. Characterization of potential endocrine-related health effects at low-dose levels of exposure to PCBs. Environ. Health Perspect. 107: 639–649.
  • Cao, W., Huang, P., Zhang, L., Wu, H. Z., Zhang, J., and Shi, F. X. 2009. Acute heat stress increases HSP70 expression in the testis, epididymis and vas deferens of adult mice. Zhonghua Nan Ke Xue. 15: 200–206.
  • Cerna, M., Maly, M., Grabic, R., Batariova, A., Smid, J., and Benes, B. 2008. Serum concentrations of indicator PCB congeners in the Czech adult population. Chemosphere 72:1124–1131.
  • Connor, K., Ramamoorthy, K., Moore, M., Mustain, M., Chen, I., Safe, S., Zacharewski, T., Gillesby, B., Joyeux, A., and Balaguer, P. 1997. Hydroxylated polychlorinated biphenyls (PCBs) as estrogens and antiestrogens: Structure–activity relationships. Toxicol. Appl. Pharmacol. 145: 111–123.
  • EFSA CONTAM. 2005. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to the presence of non dioxin-like polychlorinated biphenyls (PCB) in feed and food. EFSA J. 284: 1–137.
  • Facemire, C. F., Gross, T. S., and Guilette, L. J., Jr.1995. Reproductive impairment in the Florida panther: Nature or nurture? Environ. Health. Perspect. 103: 79–86.
  • Fowler, P. A., Abramovich, D. R., Haites, N. E., Cash, P., Groome, N. P., Al-Qahtani, A., Murray, T. J., and Lea, R. G. 2007a. Human fetal testis Leydig cell disruption by exposure to the pesticide dieldrin at low concentrations. Hum. Reprod. 22: 2919–2927.
  • Fowler, P. A., Dorà, N. J., McFerran, H., Amezaga, M. R., Miller, D. W., Lea, R. G., Cash, P., McNeilly, A. S., Evans, N. P., Cotinot, C., Sharpe, R. M., and Rhind, S. M. 2008. In utero exposure to low doses of pollutants disrupts fetal ovarian development in sheep. Mol. Hum. Reprod. 14: 269–280.
  • Fowler, P. A., Flannigan, S., Mathers, A., Gillanders, K., Lea, R. G., Wood, M. J., Maheshwari, A., Bhattacharya, S., Collie-Duguid, E. S. R., Baker, P. J., Monteiro, A., and O’Shaughnessy, P. J. 2009. Gene expression analysis of human fetal ovarian primordial follicle formation. J. Clin. Endocrinol. Metab. 94: 1427–1435.
  • Fowler, P. A., Tattum, J., Bhattacharya, S., Klonisch, T., Hombach-Klonisch, S., Gazvani, R., Lea, R. G., Miller, I., Simpson, W. G., and Cash, P. 2007b. An investigation of the effects of endometriosis on the proteome of human eutopic endometrium: A heterogeneous tissue with a complex disease. Proteomics 7: 130–142.
  • Furukawa, K., and Hotta, Y. 1993. cDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO J. 12: 97–106.
  • Guillette, L. J., Jr, Woodward, A. R., Crain, D. A., Pickford, D. B., Rooney, A. A., and Percival, H. F. 1999a. Plasma steroid concentrations and male phallus size in juvenile alligators from seven Florida lakes. Gen. Comp. Endocrinol. 116: 356–372.
  • Guillette, L. J., Jr., Brock, J. W., Rooney, A. A., and Woodward, A. R. 1999b. Serum concentrations of various environmental contaminants and their relationship to sex steroid concentrations and phallus size in juvenile American alligators. Arch. Environ. Contam. Toxicol. 36: 447–455.
  • Gupta, S. C., Siddique, H. R., Mathur, N., Mishra, R. K., Mitra, K., Saxena, D. K., and Chowdhuri, D. K. 2007. Adverse effect of organophosphate compounds, dichlorvos and chlorpyrifos in the reproductive tissues of transgenic Drosophila melanogaster: 70kDa heat shock proteins as a marker of cellular damage. Toxicology 238: 1–14.
  • Gutleb, A. C., Arvidsson, D., Orberg, J., Larsson, S., Skaare, J. U., Aleksandersen, M., Ropstad, E., and Lind, P. M. 2010. Effects on bone tissue in ewes (Ovies aries) and their foetuses exposed to PCB 118 and PCB 153. Toxicol. Lett. 192:126–133.
  • Gutleb, A. C., Lilienthal, H., Erhard, H. W., Zimmer, K. E., Skaare, J. U., and Ropstad, E. 2011. Effects of pre- and postnatal polychlorinated biphenyl exposure on emotional reactivity observed in lambs before weaning. Ecotoxicol. Environ. Safety 74: 1396–1401.
  • Halliwell, B., and Gutteridge, J. M. 1984. Free radicals, lipid peroxidation and cell damage. Lancet 2: 1095.
  • Hany, J., Lilienthal, H., Sarasin, A., Roth-Härer, A., Fastabend, A., Dunemann, L., Lichtensteiger, W., and Winneke, G. 1999. Developmental exposure of rats to a reconstituted PCB mixture or aroclor 1254: Effects on organ weights, aromatase activity, sex hormone levels, and sweet preference behaviour. Toxicol. Appl. Pharmacol. 158: 231–243.
  • He, D., Zhang, D., Wei, G., Lin, T., and Li, X. 2007. Cytoskeleton vimentin disruption of mouse sertoli cells injured by nitrogen mustard in vitro. J. Androl. 28: 389–396.
  • He, X. Y., Merz, G., Mehta, P., Schulz, H., and Yang, S. 1999. Human brain short chain L-3-hydroxyacyl coenzyme A dehydrogenase is a single-domain multifuctional enzyme. J. Biol. Chem. 274: 15014–15019.
  • He, X. Y., Merz, G., Yang, Y. Z., Pullakart, R., Mehta, P., Schulz, H., and Yang, S. Y. 2000. Function of human brain short chain L-3-hydroxyacyl coenzyme A dehydrogenase in androgen metabolism. Biochim. Biophys. Acta 1484: 267–277.
  • Henny, C. J., Grove, J. A., and Hedstrom, O. R. 1996. A field evaluation of mink and otter on the lower Columbia River and the influence of environmental contaminants. Final report. Forest and Rangeland Ecosystem Science Center (U.S.). Northwest Research Station. Lower Columbia River Bi-State Water-Quality Program.
  • Hestermann, E. V., Stegeman, J. J., and Hahn, M. E. 2000. Relative contributions of affinity and intrinsic efficacy to aryl hydrocarbon receptor ligand potency. Toxicol. Appl. Pharmacol. 168: 160–172.
  • Henriksen, E. O., Gabrielsen, G. W., Trudeau, S., Wolkers, J., Sagerup, K., and Skaare, J. U. 2000. Organochlorines and possible biochemical effects in glaucous gulls (Larus hyperboreus) from Bjørnøya, the Barents Sea. Arch. Environ. Contam. Toxicol. 38: 234–243.
  • Hurst, S., Howes, E. A., Coadwell, J., and Jones, R. 1998. Expression of a testis-specific putative actin-capping protein associated with the developing acrosome during rat spermiogenesis. Mol. Reprod. Dev. 49: 81–91.
  • Ihara, M., Kinoshita, A., Yamada, S., Tanaka, H., Tanigaki, A., Kitano, A., Goto, M., Okubo, K., Nishiyama, H., Ogawa, O., and Takahashi, C. 2005. Cortical organization by the septin cytoskeleton is essential for structural and mechanical integrity of mammalian spermatozoa. Dev. Cell. 8: 343–352.
  • Ishii, T., and Yanagawa, T. 2007. Stress-induced peroxiredoxins. Subcell. Biochem. 44: 375–384.
  • Johansen, H. R., Becher, G., Polder, A., and Skaare, J. U. 1994. Congener-specific determination of polychlorinated biphenyls and organochlorine pesticides in human milk from Norwegian mothers living in Oslo. J. Toxicol. Environ. Health 42: 157–171.
  • Jørgensen, N., Joensen, U. N., Jensen, T. K., Jensen, M. B., Almstrup, K., Olesen, I. A., Juul, A., Toppari, J., and Skakkebæk, N. 2012. Human semen quality in the new millenium: A prospective cross-sectional population-based study of 4867 men. Br. Med. J. 2: 1–13.
  • Kester, M. H., Bulduk, S., Tibboel, D., Meinl, W., Glatt, H., Falany, C. N., Coughtrie, M. W., Bergman, A., Safe, S. H., Kuiper, G. G., Schuur, A. G., Brouwer, A., and Visser, T. J. 2000. Potent inhibition of estrogen sulfotransferase by hydroxylated PCB metabolites: A novel pathway explaining the strogenic activity of PCBs. Endocrinology 141: 1897–900.
  • Kharat, I., and Saatcioglu, F. 1996. Antiestrogenic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin are mediated by direct transcriptional interference with the ligand estrogen receptor. Cross-talk between aryl hydrocarbon-and estrogen-mediated signalling. J. Biol. Chem. 271: 10533–10537.
  • Kierzenbaum, A. L., Rivkin, E., and Tres, L. L. 2007. Molecular biology of sperm head shaping. Soc. Reprod. Fertil. Suppl. 65: 33–43.
  • Kim, I. S. 2001. Effects of exposure of lactating female rats to polychlorinated biphenyls (PCBs) on testis weight, sperm production and Sertoli cell numbers in the adult male offspring. J. Vet. Med. Sci. 63: 5–9.
  • Kiviranta, H., Tuomisto, J. T., Tuomisto, J., Tukiainen, E., and Vartiainen, T. 2005. Polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in the general population in Finland. Chemosphere 60:854–869.
  • Klonisch, T., Fowler, P. A., and Hombach-Klonisch, S. 2004. Molecular and genetic regulation of testis descent and external genitalia development. Dev. Biol. 270: 1–18.
  • Kodavanti, P. R. 2006. Neurotoxicity of persistent organic pollutants: Possible mode(s) of action and further considerations. Dose Response 3: 273–305.
  • Kraugerud, M., Aleksandersen, M., Nyengaard, J.R., Østby, G., Gutleb, A., Dahl, E., Berg, V., Farstad, W., Schweder, T., Skaare, J. U., and Ropstad, E. 2012. In utero and lactational exposure to PCB 118 and PCB 153 alter ovarian follicular dynamics and GnRH-induced luteinizing hormone secretion in female lambs. Environ. Toxicol. 27: 623–634.
  • Kruse, R., Eigelshoven, S., Kaiser, A., Ruzicka, T., and Neumann, N. J. 2009. Cytokeratin 18 expression in immature Sertoli cells: Co-localization with interstitial lymphocytic infiltrates. Folia Histochem. Cytobiol. 47: 127–130.
  • Kvalem, H. E., Knutsen, H. K., Thomsen, C., Haugen, M., Stigum, H., Brantsæter, A. L., Frøshaug, M., Lohmann, N., Päpke, O., Becher, G., Alexander, J., and Meltzer, H. M. 2009. Role of dietary patterns for dioxin and PCB exposure. Mol. Nutr. Food Res. 53: 1438–1451.
  • Langer, P. 2008. Persistent organochlorinated pollutants (PCB, DDE, HCB, dioxins, furans) and the thyroid-review. Endocr. Regul. 42: 79–104.
  • Lans, M. C., Klasson-Wehler, E., Willemsen, M., Meussen, E., Safe, S., and Brouwer, A. 1993. Structure-dependant, competitive interaction of hydroxyl-polychlorobiphenyls, -dibenzo-p-dioxins and -dibenzofurans with human transthyretin. Chem. Biol. Interact. 88: 7–21.
  • Lee, K., Park, J. S., Kim, Y., Lee, Y. S., Hwang, T. S., Kim, D. J., Park, E. M., and Park, Y. M. 2002. Differential expression of Prx I and II in mouse testis and their up-regulation by radiation. Biochem. Biophys. Res. Commun. 296: 337–342.
  • Li, E., Guo, Y., Ning, Q., Zhang, S., and Li, D. 2011. Research for the effect of octylphenol on spermatogenesis and proteomic analysis in octylphenol-treated mice testes. Cell Biol. Int. 35: 305–309.
  • Lhuillier, P., Rode, B., Escalier, D., Lorès, P., Dirami, T., Bienvenu, T., Gacon, G., Dulioust, E., and Touré, A. 2009. Absence of annulus in human asthenoospermia: Case report. Hum. Reprod. 24: 1296–1303.
  • Luo, J., Rodriguez-Sosa, J.R., Tang, L., Bondareva, A., Megee, S., and Dobrinski, I. 2010. Expression pattern of acetylated alpha-tubulin in porcine spermatogonia. Mol. Reprod. Dev. 77: 348–352.
  • Lyche, J. L., Skaare, J. U., Larsen, H. J., and Ropstad, E. 2004. Levels of PCB 126 and PCB 153 in plasma and tissues in goats exposed during gestation and lactation. Chemosphere 55: 621–629.
  • Lyche, J. L., Larsen, H. J. S., Skaare, J. U., Tverdal, A., Johansen, G. M., and Ropstad, E. 2006. Perinatal exposure to low doses of PCB 135 and PCB 126 affects maternal and neonatal immunity in goat kids. J. Toxicol. Environ. Health A 69: 139–158.
  • McGuinness, M. P., and Orth, J. M. 1992. Gonocytes of male rats resume migratory activity postnatally. Eur. J. Cell Biol. 59: 196–210.
  • Murugesan, P., Balaganesh, M., Balasubramanian, K., and Arunakaran, J. 2007. Effects of polychlorinated biphenyl (Aroclor 1254) on steroidogenesis and antioxidant system in cultured adult rat Leydig cells. J. Endocrinol. 192: 325–338.
  • Murugesan, P., Muthusamy, T., Balasubramanian, K., and Arunakaran, J. 2008. Polychlorinated biphenyl (Aroclor 1254) inhibits testosterone biosynthesis and antioxidant enzymes in cultured rat Leydig cells. Reprod. Toxicol. 25: 447–454.
  • Onorato, T. M., Brown, P. W., and Morris, P. L. 2008. Mono-(2-ethylhexyl phthalate increases spermatocyte mitochondrial peroxiredoxin 3 and cyclooxygenase 2. J. Androl. 29: 293–303.
  • Osanai, M., Chiba, H., Kojima, T., Fujibe, M., Kuwahara, K., Kimura, H., Satoh, M., and Sawada, N. 2002. Hepatocyte nuclear factor (HNF)-4alpha induces expression of endothelial Fas ligand (FasL) to prevent cancer cell transmigration: A novel defense mechanism of endothelium against cancer metastasis. Jpn. J. Cancer Res. 93: 532–541.
  • Oskam, I. C., Lyche, J. L., Krogenæs, A., Thomassen, R., Skaare, J. U., Wiger, R., Dahl, E., Sweeney, T., Stien, A., and Ropstad, E. 2005. Effects of long-term maternal exposure to low doses of PCB 126 and PCB 153 on the reproductive system and related hormones of young, male goats. Reproduction 130: 731–742.
  • Oskam, I. C., Ropstad, E., Dahl, E., Lie, E., Derocher, A. E., Wiig, O., Larsen, S., Wiger, R., and Skaare, J. U. 2003. Organochlorines affect the major androgenic hormone, testosterone, in male polar bears (Ursus maritimus) at Svalbard. J. Toxicol. Environ. Health A 66: 2119–2139.
  • Peltola, V., Mäntylä, E., Huhtaniemi, I., and Ahotupa, M. 1994. Lipid peroxidation and antioxidant enzyme activities in the rat testis after cigarette smoke inhalation or administration of polychlorinated biphenyls or polychlorinated naphthalenes. J. Androl. 15: 353–361.
  • Peterson, E. A., Kalikin, L. M., Steels, J. D., Estey, M. P., Trimble, W. S., and Petty, E. M. 2007. Characterization of a SEPT9 interacting protein, SEPT14, a novel testis-specific septin. Mammal Genome 18: 796–807.
  • Pucciarelli, S., Parker, S. K., Detrich, H. W. 3rd, and Melki, R. 2006. Characterization of the cytoplasmic chaperonin containing TCP-1 from the Antarctic fish Notothenia coriiceps. Extremophiles 10: 537–549.
  • Rivkin, E., Eddy, E. M., Willis, W. D., Goulding, E. H., Suganuma, R., Yanagimachi, R., and Kierszenbaum, A. L. 2005. Sperm tail abnormalities in mutant mice with neo® gene insertion into an intron of the keratin 9 gene. Mol. Reprod. Dev. 72: 259–271.
  • Ropstad, E., Oskam, I. C., Lyche, J. L., Larsen, H. J., Lie, E., Haave, M., Dahl. E., Wiger, R., and Skaare, J. U. 2006. Endocrine disruption induced by organochlorines (OCs): Field studies and experimental models. J. Toxicol. Environ. Health A 69: 53–76.
  • Saradha, B., Vaithinathan, S., and Mathur, P. P. 2008. Lindane alters the levels of HSP70 and clusterin in adult rat testis. Toxicology 243: 116–123.
  • Schütz, W., Alsheimer, M., Ollinger, R., and Benavente, R. 2005. Nuclear envelope remodelling during mouse spermiogenesis: Postmeiotic expression and redistribution of germline lamin B3. Exp. Cell. Res. 307: 285–291.
  • Selim, M. E., el Rashed, H. A., Aleisa, N. A., and Daghestani, M. H. 2012. The protection role of heat shock protein 70 (HSP-70) in the testes of cadmium-exposed rats. Bioinformation 8: 58–64.
  • Selvakumar, E., Prahalathan, C., Mythili, Y., and Varalakhmi, P. 2005. Beneficial effects of DL-alpha-lipoic acid on cyclophosphamide-induced oxidative stress in mitochondrial fractions of rat testis. Chem. Biol. Interact. 152: 59–66.
  • Sharpe, R. M., and Skakkebæk, N. E. 1993. Are oestrogens involved in falling sperm counts and male reproductive tract? Lancet 341: 1392–1396.
  • Shen, H., Han, J., Tie, X., Xu, W., Ren, Y., and Ye, C. 2009. Polychlorinated dibenzo-p-dioxins/furans and polychlorinated biphenyls in human adipose tissue from Zhejiang Province, China. Chemosphere 74: 384–388.
  • Sjaastad, Ø., Hove, K., and Sand, O. 2003. The endocrine system. In Physiology of domestic animals, 190–233. Oslo, Norway: Scandinavian Veterinary Press.
  • Skakkebæk, N. E., Rajpert-De Meyts, E., and Main, K. M. 2001.Testicular dysgenesis syndrome: An increasingly common development disorder with environmental aspects. Hum. Reprod. 16: 972–978.
  • Smith, A., and Benavente, R. 1992. Identification of a short nuclear lamin protein selectively expressed during meiotic stages of rat spermatogenesis. Differentiation 52: 55–60.
  • Steels, J. D., Estey, M. P., Froese, C. D., Reynaud, D., Pace-Asciak, C., and Trimble, W. S. 2007. Sept12 is a component of the mammalian sperm tail annulus. Cell Motil. Cytoskeleton 64: 794–807.
  • Storelli, M. M., Scarano, C., Spanu, C., De Santis, E. P. L., Busco, V. P., Storelli, A, Marcotrigiano, G. O. 2012. Levels and congener profiles of polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs) and polychlorinated biphenyls (PCBs) in sheep milk from an industrialised area of Sardinia, Italy. Food Chem. Toxicol. 50: 1413–1417.
  • Tay, T. W., Andriana, B. B., Ishii, M., Tsunekawa, N., Kanai, Y., and Kurohmaru, M. 2007. Disappearance of vimentin in Sertoli cells: A mono (2-ethylhexyl) phthalate effect. Int. J. Toxicol. 26: 289–295.
  • Tokuhiro, K., Miyagawa, Y., and Tanaka, H. 2008. Characterizing mouse male germ cell-specific actin capping protein α3 (CPα3): Dynamic patterns of expression in testicular and epididymal sperm. Asian J. Androl. 10: 711–718.
  • Toppari, J., Larsen, J.C., Christiansen, P., Giwercman, A., Grandjean, P., Guilette, L. J., Jégou, B., Jensen, T. K., Jouannet, P., Keiding, N., Leffers, H., McLachlan, J. A., Meyer, O., Müller, J., Rajpert-De Meyts, E., Scheike, T., Sharpe, R., Sumpter, J., and Skakkebæk, N. E. 1996. Male reproductive health and environmental xenoestrogens. Environ. Health Perspect. 104: 741–803.
  • Van den Berg, M., Birnbaum, L., Bosveld, A. T., Brunström, B., Cook, P., Feeley, M., Giesy, J. P., Hanberg, A., Hasegawa, R., Kennedy, S. W., Kubiak, T., Larsen, J. C., van Leeuwen, F. X., Liem, A. K., Nolt, C., Peterson, R. E., Poellinger, L., Safe, S., Schrenk, D., Tillitt, D., Tysklind, M., Younes, M., Waern, F., and Zacharewski, T. 1998. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ. Health Perspect. 106: 775–792.
  • Van den Berg, M., Birnbaum, L. S., Dension, M., De Vito, M., Farland, W., Feeley, M., Fiedler, H., Hakansson, H., Hanberg, A., Haws, L., Rose, M., Safe, S., Schrenk, D., Tohyama, C., Tritscher, A., Tuomisto, J., Tysklind, M., Walker, N., and Peterson, R. E. 2006. The 2005 World Health Organization re-evaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol. Sci. 93: 223–241.
  • Vester, B., Smith, A., Krohne, G., and Benavente, R. 1993. Presence of a nuclear lamina in pachytene spermatocytes of the rat. J. Cell. Sci. 104: 557–563.
  • Vogl, A. W., Vaid, K. S., and Guttman, J. A. 2008. The Sertoli cell cytoskeleton. Adv. Exp. Med. Biol. 636: 186–211.
  • von Bülow, M., Rackwitz, H. R., Zimbelmann, R., and Franke, W. W. 1997. CP beta3, a novel isoform of an actin-binding protein, is a component of the cytoskeletal calyx of the mammalian sperm head. Exp. Cell. Res. 25: 216–224.
  • Wakayama, T., Nakata, H., Kurobo, M., Sai, Y., and Iseki, S. 2009. Expression, localization, and binding activity of the Ezrin/Radixin/Moesin proteins in the mouse testis. J. Histochem. Cytochem. 57: 351–362.
  • Wisdom, R., Johnson, R. S., and Moore, C. 1999. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J. 18: 188–197.
  • Wolfahrt-Veje, C., Main, K. M., and Skakkebaek, N. E. 2009. Testicular dysgenesis syndrome: Foetal origin of adult reproductive problems. Clin. Endocrinol. (Oxford) 71: 459–465.
  • Wu, J., Wang, F., Gong, Y., Li, D., Sha, J., Huang, X., and Han, X. 2009. Proteomic analysis of changes induced by nonylphenol in Sprague-Dawley rat. Chem. Res. Toxicol. 22: 668–675.
  • Zamoner, A., Barreto, K. P., Filho, D. W., Sell, F., Woehl, V. M., Guma, F. C., Pessoa-Pureur, R., and Silva, F. R. 2008. Propylthiouracil-induced congenital hypothyroidism upregulates vimetin phosphorylation and depletes antioxidant defences in immature rat testis. J. Mol. Endocrinol. 40: 125–135.
  • Zamoner, A., Barreto, K. P., Filho, D. W., Sell, F., Woehl, V. M., Guma, F. C., Silva, F. R., and Pessoa-Pureur, R. 2007. Hyperthyroidism in rthe developing rat testis is associated with oxidative stress and hyperphosphorylated vimetin accumulation. Mol. Cell. Endocrinol. 267: 116–126.
  • Zhang, W., Shen, H., Ma, L., Shen, B., Xu, Z., and Wang, X. 2007. Differential expression of peroxiredoxin 6 in fetal testis following in utero exposure to di(nbutyl) phthalate. Toxicology 240: 86–95.
  • Zhong, L., and Belote, J. M. 2007. The testis-specific proteasome subunit Prosα6T of D. melanogaster is required for individualization and nuclear maturation during spermatogenesis. Development 134: 3517–3525.
  • Zhu, Y. F., Cui, Y. G., Guo, X. J., Wang, L., Bi, Y., Hu, Y.Q., Zhao, X., Liu, Q., Huo, R., Lin, M., Zhou, Z. M., and Sha, J. H. 2006. Proteomic analysis of effect of hyperthermia on spermatogenesis in adult male mice. J. Proteome Res. 5: 2217–2225.
  • Zimmer, K. E., Kraugerud, M., Aleksandersen, M., Gutleb, A.C., Østby, G. C., Dahl, E., Berg, V., Skaare, J. U., Olsaker, I., and Ropstad, E. 2011. Fetal adrenal development: Comparing effects of combined exposures to PCB 118 and PCB 153 in a sheep model. Environ. Toxicol. 28: 166–177.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.