Recombination homeostasis of meiosis during spermatogenesis under nicotine treatment

Authors

  • Jingli Zhai School of Life Science and Biotechnology, Shanghai Key Laboratory for Reproductive Medicine, Shanghai Jiao Tong University, Shanghai, 200240
  • Qingqing Yuan State Key Laboratory of Oncogenes and Related Genes, Renji-Med X Clinical Stem Cell Research Center, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai
  • Tianqi Yang School of Life Science and Biotechnology, Shanghai Key Laboratory for Reproductive Medicine, Shanghai Jiao Tong University, Shanghai, 200240
  • Xianglong Zhao School of Life Science and Biotechnology, Shanghai Key Laboratory for Reproductive Medicine, Shanghai Jiao Tong University, Shanghai, 200240
  • Meixing Zhang School of Life Science and Biotechnology, Shanghai Key Laboratory for Reproductive Medicine, Shanghai Jiao Tong University, Shanghai, 200240
  • Dong Zhang School of Life Science and Biotechnology, Shanghai Key Laboratory for Reproductive Medicine, Shanghai Jiao Tong University, Shanghai, 200240
  • Wangjie Xu School of Life Science and Biotechnology, Shanghai Key Laboratory for Reproductive Medicine, Shanghai Jiao Tong University, Shanghai, 200240
  • Zhongdong Qiao School of Life Science and Biotechnology, Shanghai Key Laboratory for Reproductive Medicine, Shanghai Jiao Tong University, Shanghai, 200240

Keywords:

recombination, nicotine, meiosis, homeostasis, spermatogenesis

Abstract

Cigarette smoking can affect male fertility via the quality of semen. To explore the effects of nicotine, a major component of cigarettes, on meiotic recombination during spermatogenesis, C57BL/6J male mice were injected with nicotine at a dosage of 0.2 mg/100 g body weight daily for 35 days (nicotine-treated group); mice in the control group were injected with isopycnic normal saline. According to previous expression profiles of mouse sperm, a subset of meiosis-related genes was pooled using bioinformatic analysis. Protein expression was compared between the two groups using by Western blotting and immunohistochemistry. Recombination frequency during the meiosis phase of spermatogenesis was estimated by combined use of chromosome spread and immunofluorescence staining in mouse testes. Data mining analysis indicated that 4 genes that express meiotic topoisomerase-like protein SPO11, MutS protein homolog 4 (MSH4), strand exchange protein RAD51 and MutL protein homologue 1 (MLH1), were associated with the meiosis recombination process. The results of Western blotting and immunohistochemistry further showed that the protein expression of SPO11 (0.73-fold) and MSH4 (0.73-fold) was downregulated in murine testes after nicotine treatment, whereas the protein expression of both RAD51 (2.06-fold) and MLH1 (1.40-fold) was upregulated. Unexpectedly, we did not detect a significant difference in recombination frequency in meiosis during spermatogenesis in the nicotine-treated group as compared to the control. Taken together, these results indicate that nicotine can affect the expression profile of restructuring-related genes, but it does not significantly change the recombination frequency during male meiosis. These findings suggest there is a self-regulating mechanism during meiotic chromosome restructuring in male mice that responds to environmental stress.

https://doi.org/10.2298/ABS170419025Z

Received: April 19, 2017; Revised: May 15, 2017; Accepted: May 18, 2017; Published online: July 26, 2017

How to cite this article: Zhai J, Yuan Q, Yang T, Zhao X, Zhang M, Zhang D, Xu W, Qiao Z. Recombination homeostasis of meiosis during spermatogenesis under nicotine treatment. Arch Biol Sci. 2018;70(1):55-62.

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References

Gu Y, Xu W, Nie D, Zhang D, Dai J, Zhao X, Zhang M, Wang Z, Chen Z, Qiao Z. Nicotine induces Nme2-mediated apoptosis in mouse testes. Biochem Bioph Res Co. 2016;472(4):573-9.

Benowitz N. Nicotine addiction. New Engl J Med. 2010;362(24):2295-303.

Colquhoun D, Shelley C, Hatton C, Unwin N, Sivilotti L. Nicotinic acetylcholine receptors. In: Burger's Medicinal Chemistry and Drug Discovery. John Wiley & Sons; 2003. p. 357-405.

Zhu Z, Xu W, Dai J, Chen X, Zhao X, Fang P, Yang F, Tang M, Wang Z, Wang L, Ma D, Qiao Z. The alteration of protein profile induced by cigarette smoking via oxidative stress in mice epididymis. Int J Biochem Cell Biol. 2013;45(3):571-82.

Belcheva A, Ivanova‐Kicheva M, Tzvetkova P, Marinov M. Effects of cigarette smoking on sperm plasma membrane integrity and DNA fragmentation. Int J Androl. 2004;27(5):296-300.

Condorelli R, La Vignera S, Giacone F, Iacoviello L, Vicari E, Mongioi L, Calogero A. In vitro effects of nicotine on sperm motility and bio-functional flow cytometry sperm parameters. Int J Immunopathol Pharmacol. 2013;26(3):739-46.

Pasqualotto F, Sobreiro B, Hallak J, Pasqualott E, Lucon A. Cigarette smoking is related to a decrease in semen volume in a population of fertile men. BJU Int. 2006;97(2):324-6.

Gu H, Tang M, Fang P, Zhu Z, Xu W, Wang Z, Wang L, Qiao Z. Effects of cigarette smoke on fertility in Male. J Shanghai Jiaotong Univ (Sci). 2012;30(3):1-5.

Chen X, Dai J, Xu W, Wang Z, Qiao Z. Influence of passive smoke on the male mouse fertility. Reprod Contracep. 2014;34(10):805-8.

Nie D, Zhang D, Dai J, Zhang M, Zhao X, Xu W, Chen Z, Wang L, Wang Z, Qiao Z. Nicotine induced murine spermatozoa apoptosis via up-regulation of deubiquitinated RIP1 by Trim27 promoter hypomethylation 1. Biol Reprod. 2015;94(2):31.

Ma S, Arsovska S, Moens P, Nigro M, Chow V. Analysis of early meiotic events and aneuploidy in nonobstructive azoospermic men: a preliminary report. Fertil Steril. 2006;85(3):646-52.

J L , Copenhaver G. Meiotic recombination gets stressed out: CO frequency is plastic under pressure. Curr Opin Plant Biol. 2017;36:95-102.

Abdullah M, Borts R. Meiotic recombination frequencies are affected by nutritional states in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 2001;98(25):14524-9.

Francis K, Lam S, Harrison B, Bey A, Berchowitz L, Copenhaver G. Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc Natl Acad Sci USA. 2007;104(10):3913-8.

Bomblies K, Higgins J, Yant L. Meiosis evolves: adaptation to external and internal environments. New Phytol. 2015;208(2):306-23.

Zinn K, Tunc-Ozdemir M, Harper J. Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot. 2010;61(7):1959-68.

Chan A, Borts R, Hoffmann E. Temperature-dependent modulation of chromosome segregation in msh4 mutants of budding yeast. PLoS One. 2009;4(10):e7284.

Bavarva J, Tae H, Settlage R, Garner H. Characterizing the genetic basis for nicotine induced cancer development: an expression sequencing study. PLoS One. 2013;8(6):e67252.

Matta S, Balfour D, Benowitz N, Boyd R, Buccafusco J, Caggiula A, Craig C, Collins A, Damaj M, Donny E, Gardiner P, Grady S, Heberlein U, Leonard S, Levin E. Guidelines on nicotine dose selection for in vivo research. Psychopharmacol. 2007;190(3):269-319.

Ma H, Niu C, Guo J, Zheng Y. Progress in the genes regulating meiosis during spermatogenesis. J Reprod Med. 2016;25(9):865-9.

Yin Y, Wang P. Screening and verification of proteins that interact with MLH1, the key protein in meiosis recombination, by yeast two hybrid screening. Chinese J Androl. 2016;30(1):16-20.

Cole F, Kauppi L, Lange J, Roig I, Wang R, Keeney S, Jasin M. Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol. 2012;14(4):424-30.

Zhang J, Yan G, Tian M, Yuan D, Xiong J, Miao W. The analysis of gene expression changes in SPO11 deficient cells of Tetrahymena thermophila. Genom Appl Biol. 2016;35(2):350-7.

Zhang J, Tian M, Feng L, Miao W. Meiosis in Tetrahymena thermophila. Chinese J Zool. 2016;51(1):126-36.

Sun F, Trpkov K, Rademaker A, Ko E, Barclay L, Mikhaail-Philip M, Martin R. The effect of cold storage on recombination frequencies in human male testicular cells. Cytogenet Genome Res. 2004;106(1):39-42.

Huang J, Copenhaver G, Ma H, Wang Y. New insights into the role of DNA synthesis in meiotic recombination. Science Bulletin. 2016;61(16):1260-9.

Baudat F, Imai Y, De Massy B. Meiotic recombination in mammals: localization and regulation. Nat Rev Genet. 2013;14(11):794-806.

Rodgers J, Lerin C, Haas W, Gygi S, Spiegelman B, Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1. Nature. 2005;434(7029):113-8.

Skinner M. Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics. 2011;6(7):838-42.

Phillips D, Jenkins G, Macaulay M, Nibau C, Wnetrzak J, Fallding D, Colas L, Oakey H, Waugh R, Ramsay L. The effect of temperature on the male and female recombination landscape of barley. New Phytol. 2015;208(2):421-9.

Loidl J. Effects of elevated temperature on meiotic chromosome synapsis in Allium ursinum. Chromosoma. 1989;97(6):449-58.

Martini E, Diaz R, Hunter N, Keeney S. Crossover homeostasis in yeast meiosis. Cell. 2006;126(2):285-95.

Wang K, Wang C, Liu Q, Liu W, Fu Y. Increasing the genetic recombination frequency by partial loss of function of the synaptonemal complex in rice. Mol Plant. 2015;8(8):1295-8.

Dubin M, Zhang P, Meng D, Remigereau M, Osborne E, Casale F, Drewe P, Kahles A, Jean G, Vilhjalmsson B, Jagoda J, Irez S, Voronin V, Song Q, Long Q, Ratsch G, Stegle O, Clark R, Nordborg M. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. Elife. 2015;4:e05255.

Balasubramanian S, Sureshkumar S, Lempe J, Weigel D. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2006;2(7):e106.

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Published

2018-03-13

How to Cite

1.
Zhai J, Yuan Q, Yang T, Zhao X, Zhang M, Zhang D, Xu W, Qiao Z. Recombination homeostasis of meiosis during spermatogenesis under nicotine treatment. Arch Biol Sci [Internet]. 2018Mar.13 [cited 2024Apr.18];70(1):055-62. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/1700

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Vol. 70 No. 1 (2018)

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