Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2020

Open Access 01-12-2020 | Infertility | Research

Cigarette smoking is associated with high level of ferroptosis in seminal plasma and affects semen quality

Authors: Zhanhui Ou, Qirong Wen, Yu Deng, Yang Yu, Zhiheng Chen, Ling Sun

Published in: Reproductive Biology and Endocrinology | Issue 1/2020

Login to get access

Abstract

Purpose

The effects of cigarette smoking on male semen quality are controversial, and the molecular mechanisms underlying how cigarette smoking affects semen quality are not clear yet.

Methods

In this study, semen samples from 70 heavy smokers and 75 non-smokers receiving infertility treatment were included. Basic semen parameters in non-smokers and heavy smokers were evaluated. Levels of glutathione (GSH), lipid reactive oxygen species (ROS), iron and GSH-dependent peroxidase 4 (GPX4) protein level were observed in human seminal plasma and in GC-2Spd cells exposed to cigarette smoke condensate (CSC).

Results

Heavy smokers had significantly higher abnormalities (sperm viability and sperm progressive motility) than non-smoking counterparts. Comparing non-smokers group, GSH level was reduced in the group of heavy smokers (P < 0.05). However, the level of lipid ROS and iron were significantly increased (P < 0.05). Besides, GSH level was reduced following treatment with CSC for 24 h, while lipid ROS and iron levels were increased (P < 0.05). However, the levels were reduced after being co-cultured with Ferrostatin-1 (Fer-1) (P < 0.05). The level of GPX4 protein was reduced after being treated with CSC in 24 h, and increased after being co-cultured with Fer-1(P < 0.05).

Conclusion

Cigarette smoking is associated with high level of ferroptosis in seminal plasma and affect semen quality.
Literature
1.
Bashamboo A, Ferraz-de-Souza B, Lourenço D, Lin L, Sebire NJ, Montjean D, Bignon-Topalovic J, Mandelbaum J, Siffroi J, Christin-Maitre S, Radhakrishna U, Rouba H, Ravel C, Seeler J, Achermann JC, McElreavey K. Human male infertility associated with mutations in NR5A1 encoding steroidogenic factor 1. Am J Hum Genet. 2010;87:505–12.PubMedPubMedCentralCrossRef
2.
Auger J, Kunstmann JM, Czyglik F, Jouannet P. Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med. 1995;332:281–5.PubMedCrossRef
3.
de Kretser DM. Male infertility. Lancet (London, England). 1997;349:787–90.CrossRef
4.
5.
Anifandis G, Bounartzi T, Messini CI, Dafopoulos K, Sotiriou S, Messinis IE. The impact of cigarette smoking and alcohol consumption on sperm parameters and sperm DNA fragmentation (SDF) measured by Halosperm. Arch Gynecol Obstet. 2014;290(4):777–82.PubMedCrossRef
6.
Yu B, Qi Y, Liu D, Gao X, Chen H, Bai C, Huang Z. Cigarette smoking is associated with abnormal histone-to-protamine transition in human sperm. Fertil Steril. 2014;101:51–7.PubMedCrossRef
7.
Trummer H, Habermann H, Haas J, Pummer K. The impact of cigarette smoking on human semen parameters and hormones. Hum Reprod. 2002;17:1554–9.PubMedCrossRef
8.
Li Y, Lin H, Ma M, Li L, Cai M, Zhou N, Han X, Bao H, Huang L, Zhu C, Li C, Yang H, Rao Z, Xiang Y, Cui Z, Ao L, Zhou Z, Xiong H, Cao J. Semen quality of 1346 healthy men, results from the Chongqing area of southwest China. Hum Reprod. 2009;24:459–69.PubMedCrossRef
9.
Aryanpur M, Tarahomi M, Sharifi H, Heydari G, Hessami Z, Akhoundi M, Masjedi MR. Comparison of spermatozoa quality in male smokers and nonsmokers of Iranian infertile couples. Int J Fertil Steril. 2011;5:152–7.PubMedPubMedCentral
10.
Al-Matubsi HY, Kanaan RA, Hamdan F, Salim M, Oriquat GA, Al Hanbali OA. Smoking practices in Jordanian people and their impact on semen quality and hormonal levels among adult men. Cent Eur J Public Health. 2011;19:54–9.PubMedCrossRef
11.
Li Y, Lin H, Li Y, Cao J. Association between socio-psycho-behavioral factors and male semen quality: systematic review and meta-analyses. Fertil Steril. 2011;95:116–23.PubMedCrossRef
12.
Martini AC, Molina RI, Estofán D, Senestrari D, Fiol De Cuneo M, Ruiz RD. Effects of alcohol and cigarette consumption on human seminal quality. Fertil Steril. 2004;82:374–7.PubMedCrossRef
13.
Sergerie M, Ouhilal S, Bissonnette F, Brodeur J, Bleau G. Lack of association between smoking and DNA fragmentation in the spermatozoa of normal men. Hum Reprod. 2000;15:1314–21.PubMedCrossRef
14.
Pryor WA, Stone K, Zang LY, Bermúdez E. Fractionation of aqueous cigarette tar extracts: fractions that contain the tar radical cause DNA damage. Chem Res Toxicol. 1998;11:441–8.PubMedCrossRef
15.
Zang LY, Stone K, Pryor WA. Detection of free radicals in aqueous extracts of cigarette tar by electron spin resonance. Free Radic Biol Med. 1995;19:161–7.PubMedCrossRef
16.
Yu B, Chen J, Liu D, Zhou H, Xiao W, Xia X, Huang Z. Cigarette smoking is associated with human semen quality in synergy with functional NRF2 polymorphisms. Biol Reprod. 2013;89:5.PubMedCrossRef
17.
Ramlau-Hansen CH, Thulstrup AM, Aggerholm AS, Jensen MS, Toft G, Bonde JP. Is smoking a risk factor for decreased semen quality? A cross-sectional analysis. Hum Reprod. 2007;22:188–96.CrossRefPubMed
18.
Künzle R, Mueller MD, Hänggi W, Birkhäuser MH, Drescher H, Bersinger NA. Semen quality of male smokers and nonsmokers in infertile couples. Fertil Steril. 2003;79:287–91.PubMedCrossRef
19.
Vine MF, Margolin BH, Morrison HI, Hulka BS. Cigarette smoking and sperm density: a meta-analysis. Fertil Steril. 1994;61:35–43.PubMedCrossRef
20.
Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, Morrison BR, Stockwell BR. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149:1060–72.PubMedPubMedCentralCrossRef
21.
Yang WS, Stockwell BR. Ferroptosis: death by lipid peroxidation. Trends Cell Biol. 2016;26:165–76.PubMedCrossRef
22.
23.
Hayano M, Yang WS, Corn CK, Pagano NC, Stockwell BR. Loss of cysteinyl-tRNA synthetase (CARS) induces the transsulfuration pathway and inhibits ferroptosis induced by cystine deprivation. Cell Death Differ. 2016;23:270–8.PubMedCrossRef
24.
Yang WS, Stockwell BR. Synthetic lethal screening identifies compounds activating iron-dependent, nonapoptotic cell death in oncogenic-RAS-harboring cancer cells. Chem Biol. 2008;15:234–45.PubMedPubMedCentralCrossRef
25.
Wang H, An P, Xie E, Wu Q, Fang X, Gao H, Zhang Z, Li Y, Wang X, Zhang J, Li G, Yang L, Liu W, Min J, Wang F. Characterization of ferroptosis in murine models of hemochromatosis. Hepatology. 2017;66:449–65.PubMedCrossRef
26.
Guiney SJ, Adlard PA, Bush AI, Finkelstein DI, Ayton S. Ferroptosis and cell death mechanisms in Parkinson's disease. Neurochem Int. 2017;104:34–48.PubMedCrossRef
27.
Sun X, Ou Z, Chen R, Niu X, Chen D, Kang R, Tang D. Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology. 2016;63:173–84.PubMedCrossRef
28.
Bromfield EG, Walters JLH, Cafe SL, Bernstein IR, Stanger SJ, Anderson AL, Aitken RJ, McLaughlin EA, Dun MD, Gadella BM, Nixon B. Differential cell death decisions in the testis: evidence for an exclusive window of ferroptosis in round spermatids. Mol Hum Reprod. 2019;25:241–56.PubMedCrossRef
29.
World Health Organization. WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva: World Health Organization press; 2010.
30.
Ou Z, Chen Y, Niu X, He W, Song B, Fan D, Sun X. High-mobility group box 1 regulates cytoprotective autophagy in a mouse spermatocyte cell line (GC-2spd) exposed to cadmium. Ir J Med Sci. 2017;186:1041–50.PubMedCrossRef
31.
Liu F, Killian JK, Yang M, Walker RL, Hong JA, Zhang M, Davis S, Zhang Y, Hussain M, Xi S, Rao M, Meltzer PA, Schrump DS. Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene. 2010;29:3650–64.PubMedPubMedCentralCrossRef
32.
Sun X, Ou Z, Xie M, Kang R, Fan Y, Niu X, Wang H, Cao L, Tang D. HSPB1 as a novel regulator of ferroptotic cancer cell death. Oncogene. 2015;34:5617–25.PubMedPubMedCentralCrossRef
33.
34.
Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108.PubMedCrossRef
35.
Taha EA, Ez-Aldin AM, Sayed SK, Ghandour NM, Mostafa T. Effect of smoking on sperm vitality, DNA integrity, seminal oxidative stress, zinc in fertile men. Urology. 2012;80:822–5.PubMedCrossRef
36.
Calogero A, Polosa R, Perdichizzi A, Guarino F, La Vignera S, Scarfia A, Fratantonio E, Condorelli R, Bonanno O, Barone N, Burrello N, D'Agata R, Vicari E. Cigarette smoke extract immobilizes human spermatozoa and induces sperm apoptosis. Reprod BioMed Online. 2009;19:564–71.PubMedCrossRef
37.
Li L, Hao Y, Zhao Y, Wang H, Zhao X, Jiang Y, Gao F. Ferroptosis is associated with oxygen-glucose deprivation/reoxygenation-induced Sertoli cell death. Int J Mol Med. 2018;41:3051–62.PubMed
38.
El-Seweidy MM, Hashem RM, Abo-El-matty DM, Mohamed RH. Frequent inadequate supply of micronutrients in fast food induces oxidative stress and inflammation in testicular tissues of weanling rats. J Pharm Pharmacol. 2008;60:1237–42.PubMedCrossRef
39.
Sundarraj K, Manickam V, Raghunath A, Periyasamy M, Viswanathan MP, Perumal E. Repeated exposure to iron oxide nanoparticles causes testicular toxicity in mice. Environ Toxicol. 2017;32:594–608.PubMedCrossRef
40.
Martin-Sanchez D, Ruiz-Andres O, Poveda J, Carrasco S, Cannata-Ortiz P, Sanchez-Niño MD, Ruiz Ortega M, Egido J, Linkermann A, Ortiz A, Sanz AB. Ferroptosis, but not Necroptosis, is important in nephrotoxic folic acid-induced AKI. J Am Soc Nephrol. 2017;28:218–29.PubMedCrossRef
41.
Metadata
Title
Cigarette smoking is associated with high level of ferroptosis in seminal plasma and affects semen quality
Authors
Zhanhui Ou
Qirong Wen
Yu Deng
Yang Yu
Zhiheng Chen
Ling Sun
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2020
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-020-00615-x

Other articles of this Issue 1/2020

Reproductive Biology and Endocrinology 1/2020 Go to the issue

Review

Review of psychological stress on oocyte and early embryonic development in female mice

Research

Effectiveness and safety of follitropin alfa (Ovaleap®) for ovarian stimulation using a GnRH antagonist protocol in real-world clinical practice: a multicenter, prospective, open, non-interventional assisted reproductive technology study

Research

Establishment of a WHO Reference Reagent for anti-Mullerian hormone

Research

Reduced frequency and functional defects of CD4+CD25highCD127low/− regulatory T cells in patients with unexplained recurrent spontaneous abortion

Research

The effectiveness of different down-regulating protocols on in vitro fertilization-embryo transfer in endometriosis: a meta-analysis

Research

Evaluation of treatment of previous cesarean scar pregnancy with methotrexate: a systematic review and meta-analysis