The reproductive toxicology of male SD rats after PM2.5 exposure mediated by the stimulation of endoplasmic reticulum stress

Chemosphere

Volumn 189, Issue , 2017, Pages 547-555

  Liu, Xiaona ^a   Jin, Xiaoting ^a,b   Su, Ruijun ^a   Li, Zhuoyu ^a  

^a SHANXI UNIVERSITY   (China)

^b RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

Author keywords

Apoptosis; Endoplasmic reticulum (ER) stress; Epididymis; PM2.5; Reproductive toxicity; Testis

Indexed keywords

CELL DEATH; RATS; TISSUE;

ENDOPLASMIC RETICULUM STRESS; EPIDIDYMIS; PM2.5; REPRODUCTIVE TOXICITIES; TESTIS;

TOXICITY;

BIOLOGICAL MARKER; CASPASE 12; EOSIN; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEMATOXYLIN; X BOX BINDING PROTEIN 1; HEAT SHOCK PROTEIN; MOLECULAR CHAPERONE GRP78;

APOPTOSIS; BIOMARKER; DOSE-RESPONSE RELATIONSHIP; GENE EXPRESSION; GERM CELL; INJURY; MALE; MOLECULAR ANALYSIS; PARTICULATE MATTER; PERFORMANCE ASSESSMENT; RODENT; SPERM; TOXICITY; TOXICOLOGY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; EPIDIDYMIS; EXPOSURE; GERM CELL; HISTOPATHOLOGY; MALE; NONHUMAN; PARTICULATE MATTER; PROTEIN EXPRESSION; RAT; REPRODUCTIVE TOXICITY; SEMEN ANALYSIS; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERM QUALITY; SPERMATOCYTE; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; SPRAGUE DAWLEY RAT; STAINING; SUMMER; TESTIS INJURY; TESTIS TISSUE; TISSUE INJURY; UPREGULATION; WESTERN BLOTTING; WINTER; AIR POLLUTANT; ANIMAL; DRUG EFFECTS; REPRODUCTION; SEASON; SPERMATOZOON; TESTIS DISEASE; TOXICITY; TUNEL ASSAY;

ANIMALIA; RATTUS;

AIR POLLUTANTS; ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM STRESS; EPIDIDYMIS; GERM CELLS; HEAT-SHOCK PROTEINS; IN SITU NICK-END LABELING; MALE; PARTICULATE MATTER; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCTION; SEASONS; SEMEN ANALYSIS; SPERMATOZOA; TESTICULAR DISEASES;

EID: 85029913755     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2017.09.082     Document Type: Article

References (42)

1. Chen, Q., Hong, X., Song, Y., Sun, Q., Wang, J., Effects of diesel exhaust particles on the quality of mouse sperm. Chin. J. Androl. 23 (2009), 22–25.
2. Cui, J., Zhang, Z., Xia, N., Ping, F., Geng, H., Pollution characteristics of heavy metals in PM2.5 during four seasons in Taiyuan City. Acta Sci. Circumstantiae 36 (2016), 1566–1572.
3. Deng, Z., Chen, F., Zhang, M., Lan, L., Qiao, Z., Cui, Y., An, J., Wang, N., Fan, Z., Zhao, X., Li, X., Association between air pollution and sperm quality: a systematic review and meta -analysis. Environ. Pollut. 208:Pt B (2016), 663–669.
4. Domke, L.M., Rickelt, S., Dörflinger, Y., Kuhn, C., Winter-Simanowski, S., Zimbelmann, R., Rosin-Arbesfeld, R., Heid, H., Franke, W.W., The cell–cell junctions of mammalian testes: I. The adhering junctions of the seminiferous epithelium represent special differentiation structures. Cell. Tissue. Res. 357 (2014), 645–665.
5. Dickhout, J.G., Carlisle, R.E., Austin, R.C., Interrelationship between cardiac hypertrophy, heart failure, and chronic kidney disease: endoplasmic reticulum stress as a mediator of pathogenesis. Circ. Res. 108 (2011), 629–642.
6. Diane, R.F., Constantinos, K., The PERK/elF2α/ATF4 module of the UPR in hypoxia resistance and tumor growth. Cancer. Biol. Ther. 5 (2006), 723–728.
7. El, F.A., Ghorbel, F., Smaoui, M., Makni-Ayadi, F., Kammoun, A., Effects of automobile lead on the general growth and sexual activity of the rat. Gynecol. Obstet. Fertil. 28 (2000), 51–59.
8. Ema, M., Naya, M., Horimoto, M., Kato, H., Developmental toxicity of diesel exhaust: a review of studies in experimental animals. Reprod. Toxicol. 42 (2013), 1–17.
9. Guven, A., Kayikci, A., Cam, K., Arbak, P., Balbay, O., Cam, M., Alterations in semen parameters of toll collectors working at motorways: does diesel exposure induce detrimental effects on semen?. Andrologia 40 (2008), 346–351.
10. Glembotski, C.C., The role of th e unfolded protein response in the heart. J. Mol. Cell. Cardiol. 44 (2008), 453–459.
11. Han, D., Lerner, A.G., Walle, L.V., Upton, J.P., Xu, W., Hagen, A., Backes, B.J., Oakes, S.A., Papa, F.R., IRE1 alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138 (2009), 562–575.
12. Hammoud, A., Carrell, D.T., Gibson, M., Sanderson, M., Parker-Jones, K., Peterson, C.M., Decreased sperm motility is associated with air pollution in Salt Lake City. Fertil. Steril. 93 (2010), 1875–1879.
13. Jeong, S.C., Cho, Y., Song, M.-K., Lee, E., Ryu, J.C., Epidermal growth factor receptor (EGFR)-MAPK-nuclear factor(NF)-κB-IL8: a possible mechanism of particulate matter(PM) 2.5-induced lung toxicity. Environ. Toxicol. 32 (2017), 1628–1636.
14. Jin, X., Su, R., Li, R., Song, L., Chen, M., Cheng, L., Li, Z., Amelioration of particulate matter-induced oxidative damage by vitamin c and quercetin in human bronchial epithelial cells. Chemosphere 144 (2016), 459–466.
15. Jiang, X.H., Bukhari, I., Zheng, W., Yin, S., Wang, Z., Cooke, H.J., Shi, Q.H., Blood–testis barrier and spermatogenesis: lessons from genetically-modified mice. Asian. J. Androl. 16 (2014), 572–580.
16. Kohno, K., How transmembrane proteins sense endoplasmic reticulum stress. Antioxid. Redox. Signal 9 (2007), 2295–2303.
17. Kuo, F., Clodfelter, D.K., Priest, T.R., Kau, D.L.K., Synthesis of a carbon- 14 labeled 1-(indole-6-carbonyl-D-phenylglycinyl)-4-(1-methylpiperidin-4-YL) piperazine-[carbonyl -14C], LY517717-14C, a factor Xa inhibitor. J. Label. Compd. Radiopharm. 47 (2004), 599–608.
18. Li, R., Kou, X., Xie, L., Cheng, F., Geng, H., Effects of ambient PM2.5 on pathological injury, inflammation, oxidative stress, metabolic enzyme activity, and expression of c-fos and c-jun in lungs of rats. Environ. Sci. Pollut. Res. Int. 22 (2015), 20167–20176.
19. Lin, J.H., Li, H., Yasumura, D., Cohen, H.R., Zhang, C., Panning, B., Shokat, K.M., Lavail, M.M., Walter, P., IRE1 signaling affects cell fate during the unfolded protein response. Science 318 (2007), 944–999.
20. Li, R.J., Kou, X.J., Geng, H., Dong, C., Cai, Z.W., Pollution characteristics of ambient PM2.5-bound PAHs and NPAHs in a typical winter time period in Taiyuan. Chin. Chem. Lett. 25 (2014), 663–666.
21. Li, R.J., Geng, H., Cai, Z.W., Song, Z.P., Xu, L.M., Chen, J., Chen, M.H., Winter pollution characteristics of polycyclic aromatic hydrocarbons, nitro polycyclic aromatic hydrocarbons (PAHs), SO42- and NO3- in PM2.5 in Taiyuan. Res. Appl. Build. Mater. 12 (2014), 12–15.
22. Liu, S., Peng, L., Wen, Y.P., Bai, H.L., Liu, F.X., Shi, M.X., Li, L.J., Pollution characteristics of organic and elemental carbon in PM2.5 in Taiyuan. Huan. Jing. Ke. Xue 36 (2015), 396–401.
23. Mendiola, J., Jørgensen, N., Andersson, A.M., Stahlhut, R.W., Liu, F., Swan, S.H., Reproductive parameters in young men living in rochester, New York. Fertil. Steril. 101 (2014), 1064–1071.
24. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J., Yankner, B.A., Yuan, J., Caspase -12 mediates ER-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403 (2000), 98–103.
25. Oyadomari, S., Mori, M., Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell. death. Differ. 11 (2004), 381–389.
26. Pires, A., de Melo, E.N., Mauad, T., Nascimento Saldiva, P.H., de Siqueira Bueno, H.M., Pre- and postnatal exposure to ambient levels of urban particulate matter (PM(2.5)) affects mice spermatogenesis. Inhal. Toxicol. 23 (2011), 237–245.
27. Parhizkar, S., Yusoff, M.J., Dollah, M.A., Effect of phaleria macrocarpa on sperm characteristics in adult rats. Adv. Pharm. Bull. 3 (2013), 345–352.
28. Reichardt, T., Call to boost research on particulates. Nature 392 (1998), 642–643.
29. Rasheva, V.I., Domingos, P.M., Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 4 (2009), 996–1007.
30. Radwan, M., Jurewicz, J., Polanska, K., Sobala, W., Radwan, P., Bochenek, M., Hanke, W., Exposure to ambient air pollution-does it affect semen quality and the level of reproductive hormones?. Ann. Hum. Biol. 43 (2016), 50–56.
31. Ron, D., Walter, P., Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell. Biol. 8 (2017), 519–529.
32. Rao, R.V., Peel, A., Logvinova, A., del Rio, G., Hermel, E., Yokota, T., Goldsmith, P.C., Ellerby, L.M., Ellerby, H.M., Bredesen, D.E., Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS. Lett. 514 (2002), 122–128.
33. Rathje, T.A., Johnson, R.K., Lunstra, D.D., Sperm production in boars after nine generations of selection for increased weight of testis. J. Anim. Sci. 73 (1995), 2177–2185.
34. Selevan, S.G., Borkovec, L., Slott, V.L., Zudova, Z., Rubes, J., Evenson, D.P., Perreault, S.D., Semen quality and reproductive health of young Czech men exposed to seasonal air pollution. Environ. Health. Perspect. 108 (2000), 887–894.
35. Tanaka, T., Asai, M., Yanagita, Y., Nishinakagawa, T., Miyamoto, N., Kotaki, K., Yano, Y., Kozu, R., Honda, S., Senjyu, H., Longitudinal study of respiratory function and symptoms in a non-smoking group of long-term officially-acknowledged victims of pollution-related illness. BMC. Public. Health 13 (2013), 1–10.
36. Viskum, S., Rabjerg, L., Jørgensen, P.J., Grandjean, P., Improvement in semen quality associated with decreasing occupational lead exposure. Am. J. Ind. Med. 35 (1999), 257–263.
37. Wek, R.C., Cavener, D.R., Translational control and the unfolded protein response. Antioxid. Redox. Signal 9 (2007), 2357–2371.
38. Wu, L., Jin, L., Shi, T., Zhang, B., Zhou, Y., Zhou, T., Bao, W., Xiang, H., Zuo, Y., Li, G.L., Wang, C., Duan, Y.G., Peng, Z., Huang, X.J., Zhang, H., Xi, T., Li, Y.G., Pan, X.Y., Xia, Y., Gong, X., Chen, W.H., Liu, Y.W., Association between ambient particulate matter exposure and semen quality in wuhan, China. Environ. Int. 98 (2017), 219–228.
39. Watanabe, N., Oonuki, Y., Inhalation of diesel engine exhaust affects spermatogenesis in growing male rats. Environ. Health Perspect. 107 (1999), 539–544.
40. Yuan, X.L., Bai, R.L., Liu, S.S., Zhang, J.H., Progress on opening and closing of the blood-testis barrier (BTB). Prog. Veterinary. Med. 12 (2006), 31–34.
41. Zhou, N., Cui, Z., Yang, S., Han, X., Chen, G., Zhou, Z., Zhai, C., Ma, M., Li, L., Cai, M., Li, Y., Ao, L., Shu, W., Liu, J., Cao, J., Air pollution and decreased semen quality: a comparative study of Chongqing urban and rural areas. Environ. Pollut. 187 (2014), 145–152.
42. Zhang, K., Kaufman, R.J., The unfolded protien response: a stress signaling pathway critical for health and disease. Neurology 66:2 Suppl. 1 (2006), S102–S109.