Global Methylation and Protamine Deficiency in Ram Spermatozoa Correlate with Sperm Production and Quality but Are Not Influenced by Melatonin or Season

Overview

Journal Animals (Basel)

Date 2020 Dec 9

PMID 33291841

Citations 2

Authors

Kelsey R Pool

Jessica P Rickard

Simon P de Graaf

Affiliations

Soon will be listed here.

Abstract

This study assessed whether the seasonal effects of melatonin that upregulate ram reproductive function alter sperm global methylation or protamine deficiency and whether these parameters corresponded to ram endocrinology, semen production and quality. Ejaculates were assessed from rams that received melatonin implants ( = 9) or no implants ( = 9) during the non-breeding season. Ejaculates ( = 2/ram/week) were collected prior to implantation (week 0), 1, 6 and 12 weeks post implantation and during the following breeding season (week 30). Flow cytometry was used to assess the sperm global methylation and protamine deficiency in each ejaculate, which had known values for sperm concentration, motility, morphology, DNA fragmentation, seminal plasma levels of melatonin, anti-Mullerian hormone and inhibin A. Serum levels of testosterone and melatonin were also evaluated. Though there was no effect of melatonin or season, sperm protamine deficiency was negatively correlated with sperm production and seminal plasma levels of anti-Mullerian hormone and positively correlated with sperm DNA fragmentation and morphology. Global methylation of spermatozoa was positively correlated with sperm DNA fragmentation, morphology and serum testosterone and negatively correlated with sperm motility. These moderate associations with sperm production and quality suggest that sperm protamine deficiency and global methylation are indicative of ram testicular function.

Citing Articles

Ancestral lineages of dietary exposure to an endocrine disrupting chemical drive distinct forms of transgenerational subfertility in an insect model.

Pool K, Gajanayakage R, Connolly C, Blache D Sci Rep. 2024; 14(1):18153.

PMID: 39103404 PMC: 11300584. DOI: 10.1038/s41598-024-67921-x.

The potential of sperm bovine protamine as a protein marker of semen production and quality at the National Artificial Insemination Center of Indonesia.

Pardede B, Maulana T, Kaiin E, Agil M, Karja N, Sumantri C Vet World. 2021; 14(9):2473-2481.

PMID: 34840468 PMC: 8613797. DOI: 10.14202/vetworld.2021.2473-2481.

References

Lolis D, Georgiou I, Syrrou M, Zikopoulos K, Konstantelli M, Messinis I . Chromomycin A3-staining as an indicator of protamine deficiency and fertilization. Int J Androl. 1996; 19(1):23-7. DOI: 10.1111/j.1365-2605.1996.tb00429.x. View

Fortes M, Satake N, Corbet D, Corbet N, Burns B, Moore S . Sperm protamine deficiency correlates with sperm DNA damage in Bos indicus bulls. Andrology. 2014; 2(3):370-8. DOI: 10.1111/j.2047-2927.2014.00196.x. View

Rosa H, Juniper D, Bryant M . Effects of recent sexual experience and melatonin treatment of rams on plasma testosterone concentration, sexual behaviour and ability to induce ovulation in seasonally anoestrous ewes. J Reprod Fertil. 2000; 120(1):169-76. View

Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E . Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature. 2004; 429(6994):900-3. DOI: 10.1038/nature02633. View

Khadivi F, Razavi S, Hashemi F . Protective effects of zinc on rat sperm chromatin integrity involvement: DNA methylation, DNA fragmentation, ubiquitination and protamination after bleomycin etoposide and cis-platin treatment. Theriogenology. 2019; 142:177-183. DOI: 10.1016/j.theriogenology.2019.09.039. View

Legendre A, Elmhiri G, Gloaguen C, Magneron V, Kereselidze D, Saci N . Multigenerational exposure to uranium changes morphometric parameters and global DNA methylation in rat sperm. C R Biol. 2019; 342(5-6):175-185. DOI: 10.1016/j.crvi.2019.07.002. View

Lewis J, Song Y, de Jong M, Bagha S, Ausio J . A walk though vertebrate and invertebrate protamines. Chromosoma. 2003; 111(8):473-82. DOI: 10.1007/s00412-002-0226-0. View

Radford E, Ito M, Shi H, Corish J, Yamazawa K, Isganaitis E . In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science. 2014; 345(6198):1255903. PMC: 4404520. DOI: 10.1126/science.1255903. View

Piscopo M, Trifuoggi M, Notariale R, Labar S, Troisi J, Giarra A . Protamine-like proteins' analysis as an emerging biotechnique for cadmium impact assessment on male mollusk Mytilus galloprovincialis (Lamarck 1819). Acta Biochim Pol. 2018; 65(2):259-267. DOI: 10.18388/abp.2017_2533. View

10.

Rahiminia T, Yazd E, Fesahat F, Moein M, Mirjalili A, Talebi A . Sperm chromatin and DNA integrity, methyltransferase mRNA levels, and global DNA methylation in oligoasthenoteratozoospermia. Clin Exp Reprod Med. 2018; 45(1):17-24. PMC: 5897243. DOI: 10.5653/cerm.2018.45.1.17. View

11.

Pool K, Rickard J, Pini T, de Graaf S . Exogenous melatonin advances the ram breeding season and increases testicular function. Sci Rep. 2020; 10(1):9711. PMC: 7297710. DOI: 10.1038/s41598-020-66594-6. View

12.

Nery S, Vieira M, Dela Cruz C, Lobach V, Del Puerto H, Torres P . Seminal plasma concentrations of Anti-Müllerian hormone and inhibin B predict motile sperm recovery from cryopreserved semen in asthenozoospermic men: a prospective cohort study. Andrology. 2014; 2(6):918-23. DOI: 10.1111/andr.278. View

13.

Pierik F, Vreeburg J, Stijnen T, de Jong F, WEBER R . Serum inhibin B as a marker of spermatogenesis. J Clin Endocrinol Metab. 1998; 83(9):3110-4. DOI: 10.1210/jcem.83.9.5121. View

14.

La Marca A, Sighinolfi G, Radi D, Argento C, Baraldi E, Artenisio A . Anti-Mullerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update. 2009; 16(2):113-30. DOI: 10.1093/humupd/dmp036. View

15.

Benchaib M, Ajina M, Lornage J, Niveleau A, Durand P, Guerin J . Quantitation by image analysis of global DNA methylation in human spermatozoa and its prognostic value in in vitro fertilization: a preliminary study. Fertil Steril. 2003; 80(4):947-53. DOI: 10.1016/s0015-0282(03)01151-8. View

16.

Rekik M, Taboubi R, Ben Salem I, Fehri Y, Sakly C, Lassoued N . Melatonin administration enhances the reproductive capacity of young rams under a southern Mediterranean environment. Anim Sci J. 2015; 86(7):666-72. DOI: 10.1111/asj.12350. View

17.

Verma A, Rajput S, De S, Kumar R, Chakravarty A, Datta T . Genome-wide profiling of sperm DNA methylation in relation to buffalo (Bubalus bubalis) bull fertility. Theriogenology. 2014; 82(5):750-9.e1. DOI: 10.1016/j.theriogenology.2014.06.012. View

18.

Cho C, Willis W, Goulding E, Choi Y, Hecht N, Eddy E . Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat Genet. 2001; 28(1):82-6. DOI: 10.1038/ng0501-82. View

19.

Barranco I, Fernandez-Fuertes B, Padilla L, Delgado-Bermudez A, Tvarijonaviciute A, Yeste M . Seminal Plasma Anti-Müllerian Hormone: A Potential AI-Boar Fertility Biomarker?. Biology (Basel). 2020; 9(4). PMC: 7236007. DOI: 10.3390/biology9040078. View

20.

Snyder P . Effects of age on testicular function and consequences of testosterone treatment. J Clin Endocrinol Metab. 2001; 86(6):2369-72. DOI: 10.1210/jcem.86.6.7602. View