Top

Journal of Assisted Reproduction and Genetics

Published in:

01-06-2017 | Gamete Biology

Sodium-Hydrogen-Exchanger expression in human sperm and its relationship with semen parameters

Authors: Zhe Zhang, Yuzhuo Yang, Han Wu, Hongliang Zhang, Haitao Zhang, Jiaming Mao, Defeng Liu, Lianming Zhao, Haocheng Lin, Wenhao Tang, Kai Hong, Hui Jiang

Published in: Journal of Assisted Reproduction and Genetics | Issue 6/2017

Abstract

Purpose

Sperm-specific sodium-hydrogen exchanger (sNHE) is essential to maintain sperm normal function in mice; however, its role in human sperm has not been clarified to date. The aim of this study is to investigate the expression pattern of sNHE in human spermatozoa and its relationship with sperm functional parameters.

Method

Semen samples from 68 asthenozoospermic and 61 normozoospermic men were analyzed for sperm concentration, motility, and acrosome reaction, and high motile spermatozoa were collected by swim-up method. The expression of sNHE in spermatozoa was detected by Western blot and immunofluorescence staining. The relationship between sNHE expression and sperm parameters was assessed.

Results

We identified sNHE is mainly localized to the principal piece of the human sperm tail. The expression of sNHE was positively correlated with sperm concentration, total number, and progressive motility. Moreover, sNHE expression was upregulated in swim-up sperm and associated with most of sperm motility parameters including straight line velocity and curvilinear velocity. Our results also showed that sNHE expression is decreased in sperm from patients with asthenozoospermia compared with that from normal controls. However, no correlation was found between sNHE expression and acrosome reaction in spermatozoa.

Conclusions

The expression pattern of sNHE suggested that this protein may be involved in the regulation of sperm motility, and aberration of its expression in sperm may contribute to the pathogenesis of asthenozoospermia.

Skakkebaek NE, Jorgensen N, Main KM, Rajpert-De Meyts E, Leffers H, Andersson AM, et al. Is human fecundity declining? Int J Androl. 2006;29(1):2–11. doi:10.1111/j.1365-2605.2005.00573.x.CrossRefPubMed

Diagnostic evaluation of the infertile male: a committee opinion. Fertil Steril. 2015;103(3):e18–25. doi:10.1016/j.fertnstert.2014.12.103.

Yoshida M, Kawano N, Yoshida K. Control of sperm motility and fertility: diverse factors and common mechanisms. Cellular and molecular life sciences: CMLS. 2008;65(21):3446–57. doi:10.1007/s00018-008-8230-z.CrossRefPubMed

Bajpai M, Doncel GF. Involvement of tyrosine kinase and cAMP-dependent kinase cross-talk in the regulation of human sperm motility. Reproduction (Cambridge, England). 2003;126(2):183–95.CrossRef

Singh AP, Rajender S. CatSper channel, sperm function and male fertility. Reprod BioMed Online. 2015;30(1):28–38. doi:10.1016/j.rbmo.2014.09.014.CrossRefPubMed

Skalhegg BS, Huang Y, Su T, Idzerda RL, McKnight GS, Burton KA. Mutation of the Calpha subunit of PKA leads to growth retardation and sperm dysfunction. Molecular endocrinology (Baltimore, Md). 2002;16(3):630–9. doi:10.1210/mend.16.3.0793.

Liu SW, Li Y, Zou LL, Guan YT, Peng S, Zheng LX, et al. Chloride channels are involved in sperm motility and are downregulated in spermatozoa from patients with asthenozoospermia. Asian journal of andrology. 2016; doi:10.4103/1008-682x.181816.

Liu B, Wang P, Wang Z, Jia Y, Niu X, Wang W, et al. Analysis and difference of voltage-dependent anion channel mRNA in ejaculated spermatozoa from normozoospermic fertile donors and infertile patients with idiopathic asthenozoospermia. J Assist Reprod Genet. 2010a;27(12):719–24. doi:10.1007/s10815-010-9466-8.CrossRefPubMedPubMedCentral

Donowitz M, Ming Tse C, Fuster D. SLC9/NHE gene family, a plasma membrane and organellar family of Na+/H+ exchangers. Mol Asp Med. 2013;34(2–3):236–51. doi:10.1016/j.mam.2012.05.001.CrossRef

10.

Fuster DG, Alexander RT. Traditional and emerging roles for the SLC9 Na+/H+ exchangers. Pflugers Archiv: European journal of physiology. 2014;466(1):61–76. doi:10.1007/s00424-013-1408-8.CrossRefPubMed

11.

Xu H, Chen H, Li J, Zhao Y, Ghishan FK. Disruption of NHE8 expression impairs Leydig cell function in the testes. American journal of physiology Cell physiology. 2015;308(4):C330–8. doi:10.1152/ajpcell.00289.2014.CrossRefPubMed

12.

Woo AL, James PF, Lingrel JB. Roles of the Na, K-ATPase alpha 4 isoform and the Na+/H+ exchanger in sperm motility. Mol Reprod Dev. 2002;62(3):348–56. doi:10.1002/mrd.90002.CrossRefPubMed

13.

Wang D, King SM, Quill TA, Doolittle LK, Garbers DL. A new sperm-specific Na+/H+ exchanger required for sperm motility and fertility. Nat Cell Biol. 2003;5(12):1117–22. doi:10.1038/ncb1072.CrossRefPubMed

14.

Bell SM, Schreiner CM, Schultheis PJ, Miller ML, Evans RL, Vorhees CV, et al. Targeted disruption of the murine Nhe1 locus induces ataxia, growth retardation, and seizures. Am J Phys. 1999;276(4 Pt 1):C788–95.

15.

Liu T, Huang JC, Zuo WL, Lu CL, Chen M, Zhang XS, et al. A novel testis-specific Na+/H+ exchanger is involved in sperm motility and fertility. Frontiers in bioscience (Elite edition). 2010b;2:566–81.CrossRef

16.

Mortimer ST, Swan MA, Mortimer D. Effect of seminal plasma on capacitation and hyperactivation in human spermatozoa. Human reproduction (Oxford, England). 1998;13(8):2139–46.CrossRef

17.

Hamamah S, Gatti JL. Role of the ionic environment and internal pH on sperm activity. Human reproduction (Oxford, England). 1998;13(Suppl 4):20–30.CrossRef

18.

Darszon A, Trevino CL, Wood C, Galindo B, Rodriguez-Miranda E, Acevedo JJ, et al. Ion channels in sperm motility and capacitation. Society of Reproduction and Fertility supplement. 2007;65:229–44.PubMed

19.

Wang D, Hu J, Bobulescu IA, Quill TA, McLeroy P, Moe OW, et al. A sperm-specific Na+/H+ exchanger (sNHE) is critical for expression and in vivo bicarbonate regulation of the soluble adenylyl cyclase (sAC). Proc Natl Acad Sci U S A. 2007;104(22):9325–30. doi:10.1073/pnas.0611296104.CrossRefPubMedPubMedCentral

20.

Tamburrino L, Marchiani S, Vicini E, Muciaccia B, Cambi M, Pellegrini S, et al. Quantification of CatSper1 expression in human spermatozoa and relation to functional parameters. Human reproduction (Oxford, England). 2015;30(7):1532–44. doi:10.1093/humrep/dev 103. CrossRef

21.

Soda T, Miyagawa Y, Ueda N, Takezawa K, Okuda H, Fukuhara S, et al. Systematic characterization of human testis-specific actin capping protein β3 as a possible biomarker for male infertility. Hum Reprod (Oxford, England). 2017 Jan 18; doi:10.1093/humrep/dew 353.

22.

Shi Y, Yuan H, Kim D, Chanana V, Baba A, Matsuda T, et al. Stimulation of Na+/H+ exchanger isoform 1 promotes microglial migration. PLoS One. 2013;8(8):e74201. doi:10.1371/journal.pone.0074201.CrossRefPubMedPubMedCentral

23.

Huetsch JC, Jiang H, Larrain C, Shimoda LA. The Na+/H+ exchanger contributes to increased smooth muscle proliferation and migration in a rat model of pulmonary arterial hypertension. Physiological reports. 2016;4:5. doi:10.14814/phy2.12729.CrossRef

24.

Van den Bergh M, Emiliani S, Biramane J, Vannin AS, Englert Y. A first prospective study of the individual straight line velocity of the spermatozoon and its influences on the fertilization rate after intracytoplasmic sperm injection. Human reproduction (Oxford, England). 1998;13(11):3103–7.CrossRef

25.

Florman HM, Jungnickel MK, Sutton KA. Shedding light on sperm pHertility. Cell. 2010;140(3):310–2. doi:10.1016/j.cell.2010.01.035.CrossRefPubMed

26.

Nishigaki T, Jose O, Gonzalez-Cota AL, Romero F, Trevino CL, Darszon A. Intracellular pH in sperm physiology. Biochem Biophys Res Commun. 2014;450(3):1149–58. doi:10.1016/j.bbrc.2014.05.100.CrossRefPubMedPubMedCentral

27.

Suarez SS. Control of hyperactivation in sperm. Hum Reprod Update. 2008;14(6):647–57. doi:10.1093/humupd/dmn029.CrossRefPubMed

28.

Wiser A, Sachar S, Ghetler Y, Shulman A, Breitbart H. Assessment of sperm hyperactivated motility and acrosome reaction can discriminate the use of spermatozoa for conventional in vitro fertilisation or intracytoplasmic sperm injection: preliminary results. Andrologia. 2014;46(3):313–5. doi:10.1111/and.12068.CrossRefPubMed

29.

Stival C, Puga Molina Ldel C, Paudel B, Buffone MG, Visconti PE, Krapf D. Sperm capacitation and acrosome reaction in mammalian sperm. Adv Anat Embryol Cell Biol. 2016;220:93–106. doi:10.1007/978-3-319-30567-7_5.CrossRefPubMed

30.

Garcia MA, Meizel S. Regulation of intracellular pH in capacitated human spermatozoa by a Na+/H+ exchanger. Mol Reprod Dev. 1999;52(2):189–95. doi:10.1002/(sici)1098-2795(199902)52:2<189::aid-mrd10>3.0.co;2-d.CrossRefPubMed

31.

Tomlinson M, Lewis S, Morroll D. Sperm quality and its relationship to natural and assisted conception: British fertility society guidelines for practice. Human fertility (Cambridge, England). 2013;16(3):175–93. doi:10.3109/14647273.2013.807522.CrossRef

32.

Verheyen G, Tournaye H, Staessen C, De Vos A, Vandervorst M, Van Steirteghem A. Controlled comparison of conventional in-vitro fertilization and intracytoplasmic sperm injection in patients with asthenozoospermia. Human reproduction (Oxford, England). 1999;14(9):2313–9.CrossRef

33.

Ben-Chetrit A, Senoz S, Greenblatt EM, Casper RF. In vitro fertilization outcome in the presence of severe male factor infertility. Fertil Steril. 1995;63(5):1032–7.CrossRefPubMed

34.

Liu T, Huang JC, Lu CL, Yang JL, Hu ZY, Gao F, et al. Immunization with a DNA vaccine of testis-specific sodium-hydrogen exchanger by oral feeding or nasal instillation reduces fertility in female mice. Fertil Steril. 2010c;93(5):1556–66. doi:10.1016/j.fertnstert.2009.03.056.CrossRefPubMed

35.

Peralta-Arias RD, Vívenes CY, Camejo MI, Piñero S, Proverbio T, Martínez E, et al. ATPases, ion exchangers and human sperm motility. Reproduction. 2015;149(5):475–84. doi:10.1530/REP-14-0471.CrossRefPubMed

Title: Sodium-Hydrogen-Exchanger expression in human sperm and its relationship with semen parameters
Authors: Zhe Zhang
Yuzhuo Yang
Han Wu
Hongliang Zhang
Haitao Zhang
Jiaming Mao
Defeng Liu
Lianming Zhao
Haocheng Lin
Wenhao Tang
Kai Hong
Hui Jiang
Publication date: 01-06-2017
Publisher: Springer US
Published in: Journal of Assisted Reproduction and Genetics / Issue 6/2017
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI: https://doi.org/10.1007/s10815-017-0898-2

At a glance: The STEP trials

Springer Medicine

Sodium-Hydrogen-Exchanger expression in human sperm and its relationship with semen parameters

Abstract

Purpose

Method

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Method

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 6/2017

Follicular ADAMTS-1 and aggrecan levels in polycystic ovary syndrome

Elective single blastocyst transfer in advanced maternal age

Re-analysis of aneuploidy blastocysts with an inner cell mass and different regional trophectoderm cells

Free radical and superoxide reactivity detection in semen quality assessment: past, present, and future

Elevated progesterone and its impact on birth weight after fresh embryo transfers

The cumulative dose of gonadotropins used for controlled ovarian stimulation does not influence the odds of embryonic aneuploidy in patients with normal ovarian response