Low Sperm Motility Is Determined by Abnormal Protein Modification During Epididymal Maturation

Overview

Journal World J Mens Health

Date 2022 Mar 11

PMID 35274503

Authors

Yoo-Jin Park

Byeong-Mu Lee

Won-Ki Pang

Do-Yeal Ryu

Md Saidur Rahman

Myung-Geol Pang

Affiliations

Soon will be listed here.

Abstract

Purpose: During epididymal sperm maturation, spermatozoa acquire progressive motility through dynamic protein modifications. However, the relationship between sequential protein modifications during epididymal sperm maturation and sperm motility and fertility has not yet been investigated. This study investigated whether sequential changes in fertility-related protein expression including that of enolase 1 (ENO1), ubiquinol-cytochrome c reductase core protein 1 and 2 (UQCRC1 and UQCRC2), and voltage-dependent anion channel 2 (VDAC2) in spermatozoa during epididymal maturation are related to bovine sperm motility. Moreover, we found that mitochondrial metabolism is closely related to fertility-related proteins. Therefore, we investigated how the sequential modification of mitochondrial proteins during epididymal maturation regulates sperm motility.

Materials And Methods: To determine the differential protein expression in caput and cauda epididymal spermatozoa from low and high motility bulls, western blot analysis was performed. Moreover, signaling pathways were identified to understand the mechanisms of regulation of sperm motility through the differential protein expression associated with fertility-related proteins.

Results: We found that ENO1 was substantially higher in the caput spermatozoa from low motility bulls than the caput and cauda spermatozoa from high motility bulls. However, ENO1 expression in low motility bull spermatozoa was downregulated to a level comparable to that in the high motility bull spermatozoa during epididymal maturation. Moreover, there was a lack of modification of mitochondrial proteins, including glutathione peroxidase 4 and NADH:Ubiquinone Oxidoreductase Core Subunit S8, in low motility bull spermatozoa during epididymal maturation, whereas active changes were detected in high motility bull spermatozoa.

Conclusions: Irregular modifications of mitochondrial proteins during epididymal sperm maturation may increase excessive ROS production and premature activation of spermatozoa during epididymal maturation. Consequently, spermatozoa may lose their motility by the earlier consumption of their energy source and may be damaged by ROS during epididymal maturation, resulting in a decline in sperm motility and bull fertility.

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References

Suryawanshi A, Khan S, Gajbhiye R, Gurav M, Khole V . Differential proteomics leads to identification of domain-specific epididymal sperm proteins. J Androl. 2010; 32(3):240-59. DOI: 10.2164/jandrol.110.010967. View

Lord T, Nixon B . Metabolic Changes Accompanying Spermatogonial Stem Cell Differentiation. Dev Cell. 2020; 52(4):399-411. DOI: 10.1016/j.devcel.2020.01.014. View

Park Y, Battistone M, Kim B, Breton S . Relative contribution of clear cells and principal cells to luminal pH in the mouse epididymis. Biol Reprod. 2017; 96(2):366-375. PMC: 6213081. DOI: 10.1095/biolreprod.116.144857. View

Sohni A, Tan K, Song H, Burow D, de Rooij D, Laurent L . The Neonatal and Adult Human Testis Defined at the Single-Cell Level. Cell Rep. 2019; 26(6):1501-1517.e4. PMC: 6402825. DOI: 10.1016/j.celrep.2019.01.045. View

Ford W . Regulation of sperm function by reactive oxygen species. Hum Reprod Update. 2004; 10(5):387-99. DOI: 10.1093/humupd/dmh034. View

Reimand J, Isserlin R, Voisin V, Kucera M, Tannus-Lopes C, Rostamianfar A . Pathway enrichment analysis and visualization of omics data using g:Profiler, GSEA, Cytoscape and EnrichmentMap. Nat Protoc. 2019; 14(2):482-517. PMC: 6607905. DOI: 10.1038/s41596-018-0103-9. View

Dacheux J, Dacheux F . New insights into epididymal function in relation to sperm maturation. Reproduction. 2013; 147(2):R27-42. DOI: 10.1530/REP-13-0420. View

Cornwall G . New insights into epididymal biology and function. Hum Reprod Update. 2009; 15(2):213-27. PMC: 2639084. DOI: 10.1093/humupd/dmn055. View

Park Y, Kwon W, Oh S, Pang M . Fertility-related proteomic profiling bull spermatozoa separated by percoll. J Proteome Res. 2012; 11(8):4162-8. DOI: 10.1021/pr300248s. View

10.

Kwon W, Oh S, Kim Y, Rahman M, Park Y, Pang M . Proteomic approaches for profiling negative fertility markers in inferior boar spermatozoa. Sci Rep. 2015; 5:13821. PMC: 4562270. DOI: 10.1038/srep13821. View

11.

Xu X, Duan S, Yi F, Ocampo A, Liu G, Izpisua Belmonte J . Mitochondrial regulation in pluripotent stem cells. Cell Metab. 2013; 18(3):325-32. DOI: 10.1016/j.cmet.2013.06.005. View

12.

Breton S, Ruan Y, Park Y, Kim B . Regulation of epithelial function, differentiation, and remodeling in the epididymis. Asian J Androl. 2015; 18(1):3-9. PMC: 4736353. DOI: 10.4103/1008-682X.165946. View

13.

Wang C, Swerdloff R . Limitations of semen analysis as a test of male fertility and anticipated needs from newer tests. Fertil Steril. 2014; 102(6):1502-7. PMC: 4254491. DOI: 10.1016/j.fertnstert.2014.10.021. View

14.

Ijiri T, Vadnais M, Huang A, Lin A, Levin L, Buck J . Thiol changes during epididymal maturation: a link to flagellar angulation in mouse spermatozoa?. Andrology. 2013; 2(1):65-75. PMC: 4253137. DOI: 10.1111/j.2047-2927.2013.00147.x. View

15.

O Meara C, Hanrahan J, Prathalingam N, Owen J, Donovan A, Fair S . Relationship between in vitro sperm functional tests and in vivo fertility of rams following cervical artificial insemination of ewes with frozen-thawed semen. Theriogenology. 2008; 69(4):513-22. DOI: 10.1016/j.theriogenology.2007.12.003. View

16.

Foresta C, Flohe L, Garolla A, Roveri A, Ursini F, Maiorino M . Male fertility is linked to the selenoprotein phospholipid hydroperoxide glutathione peroxidase. Biol Reprod. 2002; 67(3):967-71. DOI: 10.1095/biolreprod.102.003822. View

17.

Park Y, Pang M . Mitochondrial Functionality in Male Fertility: From Spermatogenesis to Fertilization. Antioxidants (Basel). 2021; 10(1). PMC: 7826524. DOI: 10.3390/antiox10010098. View

18.

Kang S, Pang W, Ryu D, Song W, Rahman M, Park Y . Porcine seminal protein-I and II mRNA expression in boar spermatozoa is significantly correlated with fertility. Theriogenology. 2019; 138:31-38. DOI: 10.1016/j.theriogenology.2019.06.043. View

19.

Gervasi M, Visconti P . Molecular changes and signaling events occurring in spermatozoa during epididymal maturation. Andrology. 2017; 5(2):204-218. PMC: 5354101. DOI: 10.1111/andr.12320. View

20.

Skerget S, Rosenow M, Petritis K, Karr T . Sperm Proteome Maturation in the Mouse Epididymis. PLoS One. 2015; 10(11):e0140650. PMC: 4640836. DOI: 10.1371/journal.pone.0140650. View