Login Register Cart 0
Generic placeholder image

Current Topics in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Sperm Quality in Mouse After Exposure to Low Doses of TCDD

Author(s): Heba Yehia Anwar Elsayed, Esvieta Tenorio Borroto*, Alberto Barbabosa Pliego, Jorge Acosta Dibarrat, Fabiola Rivera Ramirez, Juan Carlos Vázquez Chagoyán, Nazario Pescador Salas and Hector Diaz-Albiter*

Volume 19, Issue 11, 2019

Page: [931 - 943] Pages: 13

DOI: 10.2174/1568026619666190520090132

Price: $65

Abstract

Background: In the last decade, the harmful use of dioxin has been demonstrated in human health and in the whole environment. It is well known among scientists that 2, 3, 7, 8-tetrachloro dibenzo-p-dioxin (TCDD) is an environmental pollutant that causes endocrine disruption, which causes male reproductive toxicity.

Objective: The objective of the present study was to evaluate the toxicity effect of low doses of TCDD in male CD1 mice.

Materials and Methods: Three concentrations of TCDD (0.375, 0.75, 1.5 mg / kg) were analyzed and the effects on spermatozoa were evaluated 10 days after oral administration of the product. As bioindicators of TCDD toxicity, an exhaustive analysis of several spermatic parameters including motility, vitality, count, morphology and viability, flow cytometry was used to determine the affected sperm population by cytotoxicity and apoptosis. In addition, a morphometric analysis of testicles was performed.

Results: The results show that the body weight of the treated animals was reduced in medium and high doses (0.75, 1.5 mg / kg) with respect to the control groups. In the groups treated with TCDD, the abnormal head of the sperm increased by 52.5% more than the control group. Significant differences in apoptosis were observed between the negative control and vehicle control, including the median dose (0.75 mg / kg).

Conclusion: It is concluded that at these low doses there was an impact on the quality of the mouse sperm, adding an effect on apoptosis and cytotoxicity of sperm exposed to these doses of TCDD.

Keywords: TCDD, Mice, Sperm parameters, Endocrine disruptor, Flow cytometry, Morphometry assay.

« Previous Next »
Graphical Abstract

[1]
Chang, G.R. Persistent organochlorine pesticides in aquatic environments and fishes in Taiwan and their risk assessment. Environ. Sci. Pollut. Res. Int., 2018, 25(8), 7699-7708. [http://dx.doi.org/10.1007/s11356-017-1110-z]. [PMID: 29288298].
[2]
Tairova, Z.; Strand, J.; Bossi, R.; Larsen, M.M.; Förlin, L.; Bignert, A.; Hedman, J.; Gercken, J.; Lang, T.; Fricke, N.F.; Asmund, G.; Long, M.; Bonefeld-Jørgensen, E.C. Persistent organic pollutants and related biological responses measured in coastal fish using chemical and biological screening methods. J. Toxicol. Environ. Health A, 2017, 80(16-18), 862-880. [http://dx.doi.org/10.1080/15287394.2017.1372870]. [PMID: 28910589].
[3]
Alsharif, N.Z.; Hassoun, E.A. Protective effects of vitamin A and vitamin E succinate against 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced body wasting, hepatomegaly, thymic atrophy, production of reactive oxygen species and DNA damage in C57BL/6J mice. Basic Clin. Pharmacol. Toxicol., 2004, 95(3), 131-138. [http://dx.doi.org/10.1111/j.1742-7843.2004.950305.x]. [PMID: 15447737].
[4]
Hassoun, E.A.; Vodhanel, J.; Holden, B.; Abushaban, A. The effects of ellagic acid and vitamin E succinate on antioxidant enzymes activities and glutathione levels in different brain regions of rats after subchronic exposure to TCDD. J. Toxicol. Environ. Health A, 2006, 69(5), 381-393. [http://dx.doi.org/10.1080/15287390500246431]. [PMID: 16455616].
[5]
Latchoumycandane, C.; Chitra, K.C.; Mathur, P.P. 2,3,7,8-tetrachlorodibenzo- p-dioxin (TCDD) induces oxidative stress in the epididymis and epididymal sperm of adult rats. Arch. Toxicol., 2003, 77(5), 280-284. [http://dx.doi.org/10.1007/s00204-003-0439-x]. [PMID: 12734642].
[6]
Huang, C.; Xu, X.; Wang, D.; Ma, M.; Rao, K.; Wang, Z. The aryl hydrocarbon receptor (AhR) activity and DNA-damaging effects of chlorinated polycyclic aromatic hydrocarbons (Cl-PAHs). Chemosphere, 2018, 211, 640-647. [http://dx.doi.org/10.1016/j.chemosphere.2018.07.087]. [PMID: 30098559].
[7]
Man, Y.B.; Chow, K.L.; Kang, Y.; Wong, M.H. Mutagenicity and genotoxicity of Hong Kong soils contaminated by polycyclic aromatic hydrocarbons and dioxins/furans. Mutat. Res., 2013, 752(1-2), 47-56. [http://dx.doi.org/10.1016/j.mrgentox.2013.01.004]. [PMID: 23391780].
[8]
Chen, H.M.; Lee, Y.H.; Chen, R.J.; Chiu, H.W.; Wang, B.J.; Wang, Y.J. The immunotoxic effects of dual exposure to PCP and TCDD. Chem. Biol. Interact., 2013, 206(2), 166-174. [http://dx.doi.org/10.1016/j.cbi.2013.09.005]. [PMID: 24051191].
[9]
Kajta, M.; Wójtowicz, A.K. Impact of endocrine-disrupting chemicals on neural development and the onset of neurological disorders. Pharmacol. Rep., 2013, 65(6), 1632-1639. [http://dx.doi.org/10.1016/S1734-1140(13)71524-X]. [PMID: 24553011].
[10]
Schug, T.T.; Blawas, A.M.; Gray, K.; Heindel, J.J.; Lawler, C.P. Elucidating the links between endocrine disruptors and neurodevelopment. Endocrinology, 2015, 156(6), 1941-1951. [http://dx.doi.org/10.1210/en.2014-1734]. [PMID: 25714811].
[11]
Cheshenko, K.; Pakdel, F.; Segner, H.; Kah, O.; Eggen, R.I. Interference of endocrine disrupting chemicals with aromatase CYP19 expression or activity, and consequences for reproduction of teleost fish. Gen. Comp. Endocrinol., 2008, 155(1), 31-62. [http://dx.doi.org/10.1016/j.ygcen.2007.03.005]. [PMID: 17459383].
[12]
Magre, S.; Rebourcet, D.; Ishaq, M.; Wargnier, R.; Debard, C.; Meugnier, E.; Vidal, H.; Cohen-Tannoudji, J.; Le Magueresse-Battistoni, B. Gender differences in transcriptional signature of developing rat testes and ovaries following embryonic exposure to 2,3,7,8-TCDD. PLoS One, 2012, 7(7)e40306 [http://dx.doi.org/10.1371/journal.pone.0040306]. [PMID: 22808131].
[13]
Gao, Z.; Bu, Y.; Zhang, G.; Liu, X.; Wang, X.; Ding, S.; Wang, E.; Shi, R.; Li, Q.; Fu, J.; Yu, Z. Effect of TCDD on the fate of epithelial cells isolated from human fetal palatal shelves (hFPECs). Toxicol. Appl. Pharmacol., 2016, 305, 186-193. [http://dx.doi.org/10.1016/j.taap.2016.06.016]. [PMID: 27312872].
[14]
Enan, E.; El-Sabeawy, F.; Overstreet, J.; Matsumura, F.; Lasley, B. Mechanisms of gender-specific TCDD-induced toxicity in guinea pig adipose tissue. Reprod. Toxicol., 1998, 12(3), 357-369. [http://dx.doi.org/10.1016/S0890-6238(98)00017-3]. [PMID: 9628558].
[15]
Androutsopoulos, V.P.; Tsatsakis, A.M.; Spandidos, D.A. Cytochrome P450 CYP1A1: Wider roles in cancer progression and prevention. BMC Cancer, 2009, 9, 187. [http://dx.doi.org/10.1186/1471-2407-9-187]. [PMID: 19531241].
[16]
Rifkind, A.B. CYP1A in TCDD toxicity and in physiology-with particular reference to CYP dependent arachidonic acid metabolism and other endogenous substrates. Drug Metab. Rev., 2006, 38(1-2), 291-335. [http://dx.doi.org/10.1080/03602530600570107]. [PMID: 16684662].
[17]
Porterfield, W.; Tahmassebi, D.C. Synthesis of a fluorescent 2‘3’-dideoxycytosine analog, tCdd. Bioorg. Med. Chem. Lett., 2009, 19(1), 111-113. [http://dx.doi.org/10.1016/j.bmcl.2008.11.015]. [PMID: 19026534].
[18]
Sengupta, P.; Banerjee, R. Environmental toxins: alarming impacts of pesticides on male fertility. Hum. Exp. Toxicol., 2014, 33(10), 1017-1039. [http://dx.doi.org/10.1177/0960327113515504]. [PMID: 24347299].
[19]
Mehrpour, O.; Karrari, P.; Zamani, N.; Tsatsakis, A.M.; Abdollahi, M. Occupational exposure to pesticides and consequences on male semen and fertility: a review. Toxicol. Lett., 2014, 230(2), 146-156. [http://dx.doi.org/10.1016/j.toxlet.2014.01.029]. [PMID: 24487096].
[20]
Zhu, Y.; Huang, B.; Li, Q.X.; Wang, J. Organochlorine pesticides in follicular fluid of women undergoing assisted reproductive technologies from central China. Environ. Pollut., 2015, 207, 266-272. [http://dx.doi.org/10.1016/j.envpol.2015.09.030]. [PMID: 26412266].
[21]
Gray, L.E.; Ostby, J.; Furr, J.; Wolf, C.J.; Lambright, C.; Parks, L.; Veeramachaneni, D.N.; Wilson, V.; Price, M.; Hotchkiss, A.; Orlando, E.; Guillette, L. Effects of environmental antiandrogens on reproductive development in experimental animals. Hum. Reprod. Update, 2001, 7(3), 248-264. [http://dx.doi.org/10.1093/humupd/7.3.248]. [PMID: 11392371].
[22]
Hwang, S.Y.; Kim, W.J.; Wee, J.J.; Choi, J.S.; Kim, S.K. Panax ginseng improves survival and sperm quality in guinea pigs exposed to 2,3,7,8-tetrachlorodibenzo- p-dioxin. BJU Int., 2004, 94(4), 663-668. [http://dx.doi.org/10.1111/j.1464-410X.2004.05019.x]. [PMID: 15329132].
[23]
Beytur, A.; Ciftci, O.; Aydin, M.; Cakir, O.; Timurkaan, N.; Yılmaz, F. Protocatechuic acid prevents reproductive damage caused by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in male rats. Andrologia, 2012, 44(Suppl. 1), 454-461. [http://dx.doi.org/10.1111/j.1439-0272.2011.01204.x]. [PMID: 21806661].
[24]
Simanainen, U.; Adamsson, A.; Tuomisto, J.T.; Miettinen, H.M.; Toppari, J.; Tuomisto, J.; Viluksela, M. Adult 2,3,7,8-tetrachloro-dibenzo-p-dioxin (TCDD) exposure and effects on male reproductive organs in three differentially TCDD-susceptible rat lines. Toxicol. Sci., 2004, 81(2), 401-407. [http://dx.doi.org/10.1093/toxsci/kfh212]. [PMID: 15240895].
[25]
Altintas, R.; Ciftci, O.; Aydin, M.; Akpolat, N.; Oguz, F.; Beytur, A. Quercetin prevents docetaxel-induced testicular damage in rats. Andrologia, 2015, 47(3), 248-256. [http://dx.doi.org/10.1111/and.12253]. [PMID: 24601972].
[26]
Yin, H.P.; Xu, J.P.; Zhou, X.Q.; Wang, Y. Effects of vitamin E on reproductive hormones and testis structure in chronic dioxin-treated mice. Toxicol. Ind. Health, 2012, 28(2), 152-161. [http://dx.doi.org/10.1177/0748233711408381]. [PMID: 21632572].
[27]
Sanabria, M.; Cucielo, M.S.; Guerra, M.T.; Dos Santos Borges, C.; Banzato, T.P.; Perobelli, J.E.; Leite, G.A.; Anselmo-Franci, J.A.; De Grava Kempinas, W. Sperm quality and fertility in rats after prenatal exposure to low doses of TCDD: A three-generation study. Reprod. Toxicol., 2016, 65, 29-38. [http://dx.doi.org/10.1016/j.reprotox.2016.06.019]. [PMID: 27352640].
[28]
Mor, F.; Ozmen, O. Acute endosulfan poisoning in cattle. Vet. Hum. Toxicol., 2003, 45(6), 323-324. [PMID: 14640487].
[29]
Al-Maghrebi, M.; Kehinde, E.O.; Anim, J.T. Survivin downregulation is associated with vasectomy-induced spermatogenic damage and apoptosis. Med. Princ. Pract., 2011, 20(5), 449-454. [http://dx.doi.org/10.1159/000324551]. [PMID: 21757935].
[30]
McKinlay, R.; Plant, J.A.; Bell, J.N.; Voulvoulis, N. Endocrine disrupting pesticides: Implications for risk assessment. Environ. Int., 2008, 34(2), 168-183. [http://dx.doi.org/10.1016/j.envint.2007.07.013]. [PMID: 17881056].
[31]
Torres-Dosal, A.; Pérez-Maldonado, I.N.; Jasso-Pineda, Y.; Martínez Salinas, R.I.; Alegría-Torres, J.A.; Díaz-Barriga, F. Indoor air pollution in a Mexican indigenous community: evaluation of risk reduction program using biomarkers of exposure and effect. Sci. Total Environ., 2008, 390(2-3), 362-368. [http://dx.doi.org/10.1016/j.scitotenv.2007.10.039]. [PMID: 18036639].
[32]
García-Nieto, E.; Nichkova, M.; Yáñez, L.; Costilla-Salazar, R.; Torres-Dosal, A.; Gee, S.J.; Hammock, B.D.; Juárez-Santacruz, L.; Díaz-Barriga, F. Assessment of dioxin-like soil contamination in Mexico by enzyme-linked immunosorbent assay. Arch. Environ. Contam. Toxicol., 2010, 58(4), 918-926. [http://dx.doi.org/10.1007/s00244-009-9422-8]. [PMID: 20091164].
[33]
Kasai, A.; Hiramatsu, N.; Hayakawa, K.; Yao, J.; Maeda, S.; Kitamura, M. High levels of dioxin-like potential in cigarette smoke evidenced by in vitro and in vivo biosensing. Cancer Res., 2006, 66(14), 7143-7150. [http://dx.doi.org/10.1158/0008-5472.CAN-05-4541]. [PMID: 16849560].
[34]
Zhang, L.; Wu, R.; Dingle, R.W.; Gairola, C.G.; Valentino, J.; Swanson, H.I. Cigarette smoke condensate and dioxin suppress culture shock induced senescence in normal human oral keratinocytes. Oral Oncol., 2007, 43(7), 693-700. [http://dx.doi.org/10.1016/j.oraloncology.2006.08.008]. [PMID: 17070097].
[35]
Sarill, M.; Zago, M.; Sheridan, J.A.; Nair, P.; Matthews, J.; Gomez, A.; Roussel, L.; Rousseau, S.; Hamid, Q.; Eidelman, D.H.; Baglole, C.J. The aryl hydrocarbon receptor suppresses cigarette-smoke-induced oxidative stress in association with dioxin response element (DRE)-independent regulation of sulfiredoxin 1. Free Radic. Biol. Med., 2015, 89, 342-357. [http://dx.doi.org/10.1016/j.freeradbiomed.2015.08.007]. [PMID: 26408075].
[36]
Carbone, L.; Austin, J. Pain and laboratory animals: publication practices for better data reproducibility and better animal welfare. PLoS One, 2016, 11(5)e0155001 [http://dx.doi.org/10.1371/journal.pone.0155001]. [PMID: 27171143].
[37]
Hawkins, P.; Morton, D.B.; Burman, O.; Dennison, N.; Honess, P.; Jennings, M.; Lane, S.; Middleton, V.; Roughan, J.V.; Wells, S.; Westwood, K. A guide to defining and implementing protocols for the welfare assessment of laboratory animals: Eleventh report of the BVAAWF/FRAME/RSPCA/UFAW joint working group on refinement. Lab. Anim., 2011, 45(1), 1-13. [http://dx.doi.org/10.1258/la.2010.010031]. [PMID: 21123303].
[38]
Björndahl, L.; Söderlund, I.; Kvist, U. Evaluation of the one-step eosin-nigrosin staining technique for human sperm vitality assessment. Hum. Reprod., 2003, 18(4), 813-816. [http://dx.doi.org/10.1093/humrep/deg199]. [PMID: 12660276].
[39]
Wyrobek, A.J.; Bruce, W.R. Chemical induction of sperm abnormalities in mice. Proc. Natl. Acad. Sci. USA, 1975, 72(11), 4425-4429. [http://dx.doi.org/10.1073/pnas.72.11.4425]. [PMID: 1060122].
[40]
Chapin, R.E.; Filler, R.S.; Gulati, D.; Heindel, J.J.; Katz, D.F.; Mebus, C.A.; Obasaju, F.; Perreault, S.D.; Russell, S.R.; Schrader, S. Methods for assessing rat sperm motility. Reprod. Toxicol., 1992, 6(3), 267-273. [http://dx.doi.org/10.1016/0890-6238(92)90183-T]. [PMID: 1591485].
[41]
Rehman, S.; Usman, Z.; Rehman, S.; AlDraihem, M.; Rehman, N.; Rehman, I.; Ahmad, G. Endocrine disrupting chemicals and impact on male reproductive health. Transl. Androl. Urol., 2018, 7(3), 490-503. [http://dx.doi.org/10.21037/tau.2018.05.17]. [PMID: 30050807].
[42]
Tavares, R.S.; Escada-Rebelo, S.; Correia, M.; Mota, P.C.; Ramalho-Santos, J. The non-genomic effects of endocrine-disrupting chemicals on mammalian sperm. Reproduction, 2016, 151(1), R1-R13. [http://dx.doi.org/10.1530/REP-15-0355]. [PMID: 26585413].
[43]
Rather, I.A.; Koh, W.Y.; Paek, W.K.; Lim, J. The sources of chemical contaminants in food and their health implications. Front. Pharmacol., 2017, 8, 830. [http://dx.doi.org/10.3389/fphar.2017.00830]. [PMID: 29204118].
[44]
Fisher, M.T.; Nagarkatti, M.; Nagarkatti, P.S. Aryl hydrocarbon receptor-dependent induction of loss of mitochondrial membrane potential in epididydimal spermatozoa by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol. Lett., 2005, 157(2), 99-107. [http://dx.doi.org/10.1016/j.toxlet.2005.01.008]. [PMID: 15836997].
[45]
Bell, S.C. MQ, F.; A, F.; P. M., F.; Jiang, T. L. G.; MacNicoll, A.; Miller, B. G.; Rose, M.; Tran, L.; White, S. Toxicity of 2,3,7,8-Tetrachlorodibenzo-p-dioxin in the developing male wistar(Han) Rat. II: Chronic dosing causes developmental delay. Toxicol. Sci., 2007, 99(1), 224. [DOI: 10.1093/toxsci/kfm141]. [PMID: 17545211].
[46]
Foster, W.G.; Maharaj-Briceño, S.; Cyr, D.G. Dioxin-induced changes in epididymal sperm count and spermatogenesis. Cien. Saude Colet., 2011, 16(6), 2893-2905. [http://dx.doi.org/10.1590/S1413-81232011000600027]. [PMID: 21709986].
[47]
Mably, T.A.; Moore, R.W.; Peterson, R.E. In utero and lactational exposure of male rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin. 1. Effects on androgenic status. Toxicol. Appl. Pharmacol., 1992, 114(1), 97-107. [http://dx.doi.org/10.1016/0041-008X(92)90101-W]. [PMID: 1585378].
[48]
Ateşşahin, A.; Türk, G.; Yilmaz, S.; Sönmez, M.; Sakin, F.; Ceribasi, A.O. Modulatory effects of lycopene and ellagic acid on reproductive dysfunction induced by polychlorinated biphenyl (Aroclor 1254) in male rats. Basic Clin. Pharmacol. Toxicol., 2010, 106(6), 479-489. [http://dx.doi.org/10.1111/j.1742-7843.2009.00529.x]. [PMID: 20074268].
[49]
Sönmez, M.; Türk, G.; Çeribaşı, A.O.; Sakin, F.; Ateşşahin, A. Attenuating effect of lycopene and ellagic acid on 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced spermiotoxicity and testicular apoptosis. Drug Chem. Toxicol., 2011, 34(4), 347-356. [http://dx.doi.org/10.3109/01480545.2011.557382]. [PMID: 21714773].
[50]
Cheng, J.M.; Tang, J.X.; Li, J.; Wang, Y.Q.; Wang, X.X.; Zhang, Y.; Chen, S.R.; Liu, Y.X. Role of WNT signaling in epididymal sperm maturation. J. Assist. Reprod. Genet., 2018, 35(2), 229-236. [http://dx.doi.org/10.1007/s10815-017-1066-4]. [PMID: 29152689].
[51]
Roy, D.; Dey, S.; Majumder, G.C.; Bhattacharyya, D. Role of epididymal anti sticking factor in sperm capacitation. Biochem. Biophys. Res. Commun., 2015, 463(4), 948-953. [http://dx.doi.org/10.1016/j.bbrc.2015.06.040]. [PMID: 26100206].
[52]
Ana Paula Binato de Souza, Â.M.S-L. Franciele Lucca, Ivan Cunha Bustamante-Filho1, The epididymis and its role on sperm quality and male fertility. Anim. Reprod., 2017, 14, 1234-1244. [http://dx.doi.org/10.21451/1984-3143-AR955].
[53]
Denison, M.S.; Nagy, S.R. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol., 2003, 43, 309-334. [http://dx.doi.org/10.1146/annurev.pharmtox.43.100901.135828]. [PMID: 12540743].
[54]
Zoeller, R.T.; Brown, T.R.; Doan, L.L.; Gore, A.C.; Skakkebaek, N.E.; Soto, A.M.; Woodruff, T.J.; Vom Saal, F.S. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology, 2012, 153(9), 4097-4110. [http://dx.doi.org/10.1210/en.2012-1422]. [PMID: 22733974].
[55]
Diamanti-Kandarakis, E.; Bourguignon, J.P.; Giudice, L.C.; Hauser, R.; Prins, G.S.; Soto, A.M.; Zoeller, R.T.; Gore, A.C. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr. Rev., 2009, 30(4), 293-342. [http://dx.doi.org/10.1210/er.2009-0002]. [PMID: 19502515].
[56]
Aneck-Hahn, N.H.; Van Zijl, M.C.; Swart, P.; Truebody, B.; Genthe, B.; Charmier, J.; Jager, C. Estrogenic activity, selected plasticizers and potential health risks associated with bottled water in South Africa. J. Water Health, 2018, 16(2), 253-262. [http://dx.doi.org/10.2166/wh.2018.043]. [PMID: 29676761].
[57]
Liu, J.; Hernández, S.E.; Swift, S.; Singhal, N. Estrogenic activity of cylindrospermopsin and anatoxin-a and their oxidative products by FeIII-B*/H2O2. Water Res., 2018, 132, 309-319. [http://dx.doi.org/10.1016/j.watres.2018.01.018]. [PMID: 29339303].
[58]
Liu, Y.Y.; Lin, Y.S.; Yen, C.H.; Miaw, C.L.; Chen, T.C.; Wu, M.C.; Hsieh, C.Y. Identification, contribution, and estrogenic activity of potential EDCs in a river receiving concentrated livestock effluent in Southern Taiwan. Sci. Total Environ., 2018, 636, 464-476. [http://dx.doi.org/10.1016/j.scitotenv.2018.04.031]. [PMID: 29709864].
[59]
Lin, T.M.; Ko, K.; Moore, R.W.; Buchanan, D.L.; Cooke, P.S.; Peterson, R.E. Role of the aryl hydrocarbon receptor in the development of control and 2,3,7,8-tetrachlorodibenzo-p-dioxin-exposed male mice. J. Toxicol. Environ. Health A, 2001, 64(4), 327-342. [http://dx.doi.org/10.1080/152873901316981312]. [PMID: 11693491].
[60]
Bruner-Tran, K.L.; Ding, T.; Yeoman, K.B.; Archibong, A.; Arosh, J.A.; Osteen, K.G. Developmental exposure of mice to dioxin promotes transgenerational testicular inflammation and an increased risk of preterm birth in unexposed mating partners. PLoS One, 2014, 9(8)e105084 [http://dx.doi.org/10.1371/journal.pone.0105084]. [PMID: 25127480].
[61]
Bruner-Tran, K.L.; Duleba, A.J.; Taylor, H.S.; Osteen, K.G. Developmental toxicant exposure is associated with transgenerational adenomyosis in a murine model. Biol. Reprod., 2016, 95(4), 73. [http://dx.doi.org/10.1095/biolreprod.116.138370]. [PMID: 27535957].
[62]
Agarwal, A.; Virk, G.; Ong, C.; du Plessis, S.S. Effect of oxidative stress on male reproduction. World J. Mens Health, 2014, 32(1), 1-17. [http://dx.doi.org/10.5534/wjmh.2014.32.1.1]. [PMID: 24872947].
[63]
Agarwal, A.; Allamaneni, S.S. Free radicals and male reproduction. J. Indian Med. Assoc., 2011, 109(3), 184-187. [PMID: 22010591].
[64]
Gillan, L.; Evans, G.; Maxwell, W.M. Flow cytometric evaluation of sperm parameters in relation to fertility potential. Theriogenology, 2005, 63(2), 445-457. [http://dx.doi.org/10.1016/j.theriogenology.2004.09.024]. [PMID: 15626410].
[65]
Ayhan, D.H.; Tamer, Y.T.; Akbar, M.; Bailey, S.M.; Wong, M.; Daly, S.M.; Greenberg, D.E.; Toprak, E. Sequence-specific targeting of bacterial resistance genes increases antibiotic efficacy. PLoS Biol., 2016, 14(9)e1002552 [http://dx.doi.org/10.1371/journal.pbio.1002552]. [PMID: 27631336].
[66]
Hossain, M.S.; Johannisson, A.; Wallgren, M.; Nagy, S.; Siqueira, A.P.; Rodriguez-Martinez, H. Flow cytometry for the assessment of animal sperm integrity and functionality: state of the art. Asian J. Androl., 2011, 13(3), 406-419. [http://dx.doi.org/10.1038/aja.2011.15]. [PMID: 21478895].
[67]
Barrier Battut, I.; Kempfer, A.; Becker, J.; Lebailly, L.; Camugli, S.; Chevrier, L. Development of a new fertility prediction model for stallion semen, including flow cytometry. Theriogenology, 2016, 86(4), 1111-1131. [http://dx.doi.org/10.1016/j.theriogenology.2016.04.001]. [PMID: 27207472].
[68]
Gaysinskaya, V.; Soh, I.Y.; van der Heijden, G.W.; Bortvin, A. Optimized flow cytometry isolation of murine spermatocytes. Cytometry A, 2014, 85(6), 556-565. [http://dx.doi.org/10.1002/cyto.a.22463]. [PMID: 24664803].
[69]
Gaysinskaya, V.; Bortvin, A. Flow cytometry of murine spermatocytes. Curr Protoc Cytom, 2015, 72(7), 44-1-24.
[http://dx.doi.org/10.1002/0471142956.cy0744s72]
[70]
Zembruski, N.C.; Stache, V.; Haefeli, W.E.; Weiss, J. 7-Aminoactinomycin D for apoptosis staining in flow cytometry. Anal. Biochem., 2012, 429(1), 79-81. [http://dx.doi.org/10.1016/j.ab.2012.07.005]. [PMID: 22796502].
[71]
Wlodkowic, D.; Telford, W.; Skommer, J.; Darzynkiewicz, Z. Apoptosis and beyond: Cytometry in studies of programmed cell death. Methods Cell Biol., 2011, 103, 55-98. [http://dx.doi.org/10.1016/B978-0-12-385493-3.00004-8]. [PMID: 21722800].
[72]
Tapia, J.A.; Macias-Garcia, B.; Miro-Moran, A.; Ortega-Ferrusola, C.; Salido, G.M.; Peña, F.J.; Aparicio, I.M. The membrane of the mammalian spermatozoa: much more than an inert envelope. Reprod. Domest. Anim., 2012, 47(Suppl. 3), 65-75. [http://dx.doi.org/10.1111/j.1439-0531.2012.02046.x]. [PMID: 22681300].
[73]
Shaha, C.; Tripathi, R.; Mishra, D.P. Male germ cell apoptosis: Regulation and biology. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2010, 365(1546), 1501-1515. [http://dx.doi.org/10.1098/rstb.2009.0124]. [PMID: 20403866].
[74]
Chen, S.C.; Liao, T.L.; Wei, Y.H.; Tzeng, C.R.; Kao, S.H. Endocrine disruptor, dioxin (TCDD)-induced mitochondrial dysfunction and apoptosis in human trophoblast-like JAR cells. Mol. Hum. Reprod., 2010, 16(5), 361-372. [http://dx.doi.org/10.1093/molehr/gaq004]. [PMID: 20083559].
[75]
Cheng, C.Y.; Mruk, D.D. The biology of spermatogenesis: The past, present and future. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2010, 365(1546), 1459-1463. [http://dx.doi.org/10.1098/rstb.2010.0024]. [PMID: 20403863].
[76]
Henriksén, K.; Hakovirta, H.; Parvinen, M. Testosterone inhibits and induces apoptosis in rat seminiferous tubules in a stage-specific manner: in situ quantification in squash preparations after administration of ethane dimethane sulfonate. Endocrinology, 1995, 136(8), 3285-3291. [http://dx.doi.org/10.1210/endo.136.8.7628362]. [PMID: 7628362].
[77]
Kheradmand, A.; Dezfoulian, O.; Alirezaei, M.; Rasoulian, B. Ghrelin modulates testicular germ cells apoptosis and proliferation in adult normal rats. Biochem. Biophys. Res. Commun., 2012, 419(2), 299-304. [http://dx.doi.org/10.1016/j.bbrc.2012.02.014]. [PMID: 22360851].
[78]
Kimura, M.; Itoh, N.; Takagi, S.; Sasao, T.; Takahashi, A.; Masumori, N.; Tsukamoto, T. Balance of apoptosis and proliferation of germ cells related to spermatogenesis in aged men. J. Androl., 2003, 24(2), 185-191. [http://dx.doi.org/10.1002/j.1939-4640.2003.tb02661.x]. [PMID: 12634304].
[79]
Sidorkiewicz, I.; Zaręba, K.; Wołczyński, S.; Czerniecki, J. Endocrine-disrupting chemicals-Mechanisms of action on male reproductive system. Toxicol. Ind. Health, 2017, 33(7), 601-609. [http://dx.doi.org/10.1177/0748233717695160]. [PMID: 28464759].
[80]
Toppari, J.; Rodprasert, W.; Koskenniemi, J.J. Exposure variation and endocrine disruption of the male reproductive system. Horm. Res. Paediatr., 2016, 86(4), 247-252. [http://dx.doi.org/10.1159/000446436]. [PMID: 27255653].
[81]
Spanò, M.; Toft, G.; Hagmar, L.; Eleuteri, P.; Rescia, M.; Rignell-Hydbom, A.; Tyrkiel, E.; Zvyezday, V.; Bonde, J.P. Exposure to PCB and p, p′-DDE in European and Inuit populations: Impact on human sperm chromatin integrity. Hum. Reprod., 2005, 20(12), 3488-3499. [http://dx.doi.org/10.1093/humrep/dei297]. [PMID: 16223788].
[82]
Mehraein, F.; Negahdar, F. Morphometric evaluation of seminiferous tubules in aged mice testes after melatonin administration. Cell J., 2011, 13(1), 1-4. [PMID: 23671820].
[83]
Figueiredo, A.F.; França, L.R.; Hess, R.A.; Costa, G.M. Sertoli cells are capable of proliferation into adulthood in the transition region between the seminiferous tubules and the rete testis in Wistar rats. Cell Cycle, 2016, 15(18), 2486-2496. [http://dx.doi.org/10.1080/15384101.2016.1207835]. [PMID: 27420022].
[84]
Dhanabalan, S.; Jubendradass, R.; Latha, P.; Mathur, P.P. Effect of restraint stress on 2,3,7,8 tetrachloro dibenzo-p-dioxin induced testicular and epididymal toxicity in rats. Hum. Exp. Toxicol., 2011, 30(7), 567-578. [http://dx.doi.org/10.1177/0960327110376548]. [PMID: 20610472].
[85]
Goyal, H.O.; Hutto, V.; Maloney, M.A. Effects of androgen deprivation in the goat epididymis. Acta Anat. (Basel), 1994, 150(2), 127-135. [http://dx.doi.org/10.1159/000147611]. [PMID: 7976193].
[86]
McLachlan, J.A. Environmental signaling: from environmental estrogens to endocrine-disrupting chemicals and beyond. Andrology, 2016, 4(4), 684-694. [http://dx.doi.org/10.1111/andr.12206]. [PMID: 27230799].
[87]
Sanchez de Badajoz, E.; Lage-Sánchez, J.M.; Sánchez-Gallegos, P. Endocrine disruptors and prostate cancer. Arch. Esp. Urol., 2017, 70(3), 331-335. [PMID: 28422034].
[88]
Mortazavi, M.; Salehi, I.; Alizadeh, Z.; Vahabian, M.; Roushandeh, A.M. Protective effects of antioxidants on sperm parameters and seminiferous tubules epithelium in high fat-fed Rats. J. Reprod. Infertil., 2014, 15(1), 22-28. [PMID: 24696792]

Rights & Permissions Print Cite
Article Metrics
35
8
2
3
World Chagas Disease
© 2024 Bentham Science Publishers | Privacy Policy