Potential effect of smoking on semen quality through DNA damage and the downregulation of Chk1 in sperm

Cui,Xiangrong; Jing,Xuan; Wu,Xueqing; Wang,Zhenqiang; Li,Qiang

doi:10.3892/mmr.2016.5318

Potential effect of smoking on semen quality through DNA damage and the downregulation of Chk1 in sperm

Authors:
- Xiangrong Cui
- Xuan Jing
- Xueqing Wu
- Zhenqiang Wang
- Qiang Li
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Affiliations: Reproductive Medicine Center, Children's Hospital of Shanxi and Women Health Center of Shanxi, Taiyuan, Shanxi 030000, P.R. China, Clinical Laboratory, Shanxi Province People's Hospital, Taiyuan, Shanxi 030000, P.R. China
Published online on: May 20, 2016 https://doi.org/10.3892/mmr.2016.5318
Pages: 753-761
Copyright: © Cui et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Previous studies have found that smoking is associated with decreased male fertility via altering the quality of semen. However, the mechanism by which cigarette smoking affects semen quality remains to be fully elucidated. Heavy smoking-induced DNA damage has been reported to correlate with abnormal spermatozoa and male infertility. It has been reported that, in response to DNA damage, activation of the checkpoint kinase 1 (Chk1) facilitates S and G2 checkpoint arrest. The aim of the present study was to investigate the expression levels of Chk1 in sperm cells of smoking and non‑smoking men, and to further examine the correlation between DNA fragmentation rates and the expression levels of Chk1 with smoking. The present study was performed on a cohort of 841 smoking men and 287 non‑smoking men. In the investigation, sperm concentration, motility, viability, seminal plasma zinc concentration, acrosin activity and sperm DNA fragmentation were examined. The gene and protein expression levels of Chk1 were detected using reverse transcription-quantitative polymerase chain reaction and western blot analyses, respectively. It was observed that the progressive motility of the sperm was significantly decreased in the moderate and heavy smoking groups, whereas no significant changes were observed in the mild smoking group. The sperm in the medium‑term smoking group had significantly decreased progressive motility, and the semen concentration, sperm count and progressive motility vitality were markedly decreased in the long‑term smoking group. Compared with the non‑smoking group, the abnormal head rates in the heavy smoking group and long‑term smoking group were significantly increased. The sperm viability and seminal plasma zinc concentration were markedly increased in the smoking group. Increased DNA fragmentation rates were found in the smoking group. The expression of Chk1 was significantly decreased in the smoking group, compared with the non‑smoking group. Progressive motility and sperm concentration showed a nonlinear association with the relative mRNA expression of Chk1. However, an inverse association was found between DNA fragmentation rates and the progressive motility and sperm concentration. These data suggested that the decrease of semen quality caused by cigarette smoking was not only correlated with sperm DNA fragmentation rates, but was also correlated with a decline in the expressive level of Chk1. The expression of Chk1 was associated with DNA damage and apoptosis, the reduction of which may lead to decreased sperm repair and increased sperm apoptosis, with a subsequent effect on semen quality.

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1	Jo J, Lee SH, Lee JM and Jerng UM: Semen quality improvement in a man with idiopathic infertility treated with traditional Korean medicine: A case report. Explore (NY). 11:320–323. 2015. View Article : Google Scholar
2	Agarwal A, Mulgund A, Hamada A and Chyatte MR: A unique view on male infertility around the globe. Reprod Biol Endocrinol. 13:372015. View Article : Google Scholar : PubMed/NCBI
3	Gilany K, Minai-Tehrani A, Savadi-Shiraz E, Rezadoost H and Lakpour N: Exploring the human seminal plasma proteome: An unexplored gold mine of biomarker for male infertility and male reproduction disorder. J Reprod Infertil. 16:61–71. 2015.PubMed/NCBI
4	Samplaski MK, Dimitromanolakis A, Lo KC, Grober ED, Mullen B, Garbens A and Jarvi KA: The relationship between sperm viability and DNA fragmentation rates. Reprod Biol Endocrinol. 13:422015. View Article : Google Scholar : PubMed/NCBI
5	Abdul-Ghani R, Qazzaz M, Dabdoub N, Muhammad R and Abdul-Ghani AS: Studies on cigarette smoke induced oxidative DNA damage and reduced spermatogenesis in rats. J Environ Biol. 35:943–947. 2014.PubMed/NCBI
6	Hamad MF, Shelko N, Kartarius S, Montenarh M and Hammadeh ME: Impact of cigarette smoking on histone (H2B) to protamine ratio in human spermatozoa and its relation to sperm parameters. Andrology. 2:666–677. 2014. View Article : Google Scholar : PubMed/NCBI
7	Ahmadnia H, Ghanbari M, Moradi MR and Khaje-Dalouee M: Effect of cigarette smoke on spermatogenesis in rats. Urol J. 4:159–163. 2007.PubMed/NCBI
8	Shukla KK, Mahdi AA and Rajender S: Apoptosis, spermatogenesis and male infertility. Front Biosci (Elite Ed). 4:746–754. 2012. View Article : Google Scholar
9	Sun QY, Breitbart H and Schatten H: Role of the MAPK cascade in mammalian germ cells. Reprod Fertil Dev. 11:443–450. 1999. View Article : Google Scholar
10	Tian M, Bao H, Martin FL, Zhang J, Liu L, Huang Q and Shen H: Association of DNA methylation and mitochondrial DNA copy number with human semen quality. Biol Reprod. 91:1012014. View Article : Google Scholar : PubMed/NCBI
11	Albiges L, Goubar A, Scott V, Vicier C, Lefèbvre C, Alsafadi S, Commo F, Saghatchian M, Lazar V, Dessen P, et al: Chk1 as a new therapeutic target in triple-negative breast cancer. Breast. 23:250–258. 2014. View Article : Google Scholar : PubMed/NCBI
12	Al-Kaabi MM, Alshareeda AT, Jerjees DA, Muftah AA, Green AR, Alsubhi NH, Nolan CC, Chan S, Cornford E, Madhusudan S, et al: Checkpoint kinase1 (CHK1) is an important biomarker in breast cancer having a role in chemotherapy response. Br J Cancer. 112:901–911. 2015. View Article : Google Scholar : PubMed/NCBI
13	Ma YC, Su N, Shi XJ, Zhao W, Ke Y, Zi X, Zhao NM, Qin YH, Zhao HW and Liu HM: Jaridonin-induced G2/M phase arrest in human esophageal cancer cells is caused by reactive oxygen species-dependent Cdc2-tyr15 phosphorylation via ATM-Chk1/2-Cdc25C pathway. Toxicol Appl Pharmacol. 282:227–236. 2015. View Article : Google Scholar
14	Zuazua-Villar P, Rodriguez R, Gagou ME, Eyers PA and Meuth M: DNA replication stress in CHK1-depleted tumour cells triggers premature (S-phase) mitosis through inappropriate activation of Aurora kinase B. Cell Death Dis. 5:e12532014. View Article : Google Scholar : PubMed/NCBI
15	Sepaniak S, Forges T, Fontaine B, Gerard H, Foliguet B, Guillet-May F, Zaccabri A and Monnier-Barbarino P: Negative impact of cigarette smoking on male fertility: From spermatozoa to the offspring. J Gynecol Obstet Biol Reprod (Paris). 33:384–390. 2004.In French. View Article : Google Scholar
16	Silver EW, Eskenazi B, Evenson DP, Block G, Young S and Wyrobek AJ: Effect of antioxidant intake on sperm chromatin stability in healthy nonsmoking men. J Androl. 26:550–556. 2005. View Article : Google Scholar : PubMed/NCBI
17	Ozkosem B, Feinstein SI, Fisher AB and O'Flaherty C: Advancing age increases sperm chromatin damage and impairs fertility in peroxiredoxin 6 null mice. Redox Biol. 5:15–23. 2015. View Article : Google Scholar : PubMed/NCBI
18	Pasqualotto FF, Sobreiro BP, Hallak J, Pasqualotto EB and Lucon AM: Cigarette smoking is related to a decrease in semen volume in a population of fertile men. BJU Int. 97:324–326. 2006. View Article : Google Scholar : PubMed/NCBI
19	Zhou YL, Chen K, Yu BL and Gao XC: Cigarette smoking decreases sperm nucleoprotein transition in infertile males. Zhonghua Nan Ke Xue. 19:794–797. 2013.In Chinese.
20	Trummer H, Habermann H, Haas J and Pummer K: The impact of cigarette smoking on human semen parameters and hormones. Hum Reprod. 17:1554–1559. 2002. View Article : Google Scholar : PubMed/NCBI
21	Lu JC, Huang YF and Lü NQ: WHO laboratory manual for the examination and processing of human serum: Its applicability to andrology laboratories in China. Zhonghua Nan Ke Xue. 16:867–871. 2010.
22	Sobinoff AP, Sutherland JM, Beckett EL, Stanger SJ, Johnson R, Jarnicki AG, McCluskey A, St John JC, Hansbro PM and McLaughlin EA: Damaging legacy: Maternal cigarette smoking has long-term consequences for male offspring fertility. Hum Reprod. 29:2719–2735. 2014. View Article : Google Scholar : PubMed/NCBI
23	Davar R, Sekhavat L and Naserzadeh N: Semen parameters of non-infertile smoker and non-smoker men. J Med Life. 5:465–468. 2012.
24	Fariello RM, Pariz JR, Spaine DM, Gozzo FC, Pilau EJ, Fraietta R, Bertolla RP, Andreoni C and Cedenho AP: Effect of smoking on the functional aspects of sperm and seminal plasma protein profiles in patients with varicocele. Hum Reprod. 27:3140–3149. 2012. View Article : Google Scholar : PubMed/NCBI
25	Dai JB, Wang ZX and Qiao ZD: The hazardous effects of tobacco smoking on male fertility. Asian J Androl. 17:954–960. 2015. View Article : Google Scholar : PubMed/NCBI
26	La Maestra S, De Flora S and Micale RT: Effect of cigarette smoke on DNA damage, oxidative stress, and morphological alterations in mouse testis and spermatozoa. Int J Hyg Environ Health. 218:117–122. 2015. View Article : Google Scholar
27	Bryant C, Rawlinson R and Massey AJ: Chk1 inhibition as a novel therapeutic strategy for treating triple-negative breast and ovarian cancers. BMC Cancer. 14:5702014. View Article : Google Scholar : PubMed/NCBI
28	Bryant C, Scriven K and Massey AJ: Inhibition of the checkpoint kinase Chk1 induces DNA damage and cell death in human Leukemia and Lymphoma cells. Mol Cancer. 13:1472014. View Article : Google Scholar : PubMed/NCBI
29	Han X, Aslanian A, Fu K, Tsuji T and Zhang Y: The interaction between checkpoint kinase 1 (Chk1) and the minichromosome maintenance (MCM) complex is required for DNA damage-induced Chk1 phosphorylation. J Biol Chem. 289:24716–24723. 2014. View Article : Google Scholar : PubMed/NCBI
30	González Besteiro MA and Gottifredi V: The fork and the kinase: A DNA replication tale from a CHK1 perspective. Mutat Res Rev Mutat Res. 763:168–180. 2015. View Article : Google Scholar : PubMed/NCBI
31	Goto H, Kasahara K and Inagaki M: Novel insights into Chk1 regulation by phosphorylation. Cell Struct Funct. 40:43–50. 2015. View Article : Google Scholar : PubMed/NCBI
32	Grabocka E, Commisso C and Bar-Sagi D: Molecular pathways: Targeting the dependence of mutant RAS cancers on the DNA damage response. Clin Cancer Res. 21:1243–1247. 2015. View Article : Google Scholar :