Expression Levels of Sperm Genes Associated with Energy Production Pathways Regulate Fertility Status of Bulls

Authors

  • Laxman Ramya Reproductive Physiology Laboratory, Animal Physiology Division, ICAR-National Institute of Animal Nutrition and Physiology, Adugodi, Bengaluru-560030, India
  • Divakar Swathi Reproductive Physiology Laboratory, Animal Physiology Division, ICAR-National Institute of Animal Nutrition and Physiology, Adugodi, Bengaluru-560030, India
  • Santhanahalli Siddalingappa Archana Reproductive Physiology Laboratory, Animal Physiology Division, ICAR-National Institute of Animal Nutrition and Physiology, Adugodi, Bengaluru-560030, India
  • Arunachalam Arangasamy Reproductive Physiology Laboratory, Animal Physiology Division, ICAR-National Institute of Animal Nutrition and Physiology, Adugodi, Bengaluru-560030, India
  • B Krishnan Binsila Reproductive Physiology Laboratory, Animal Physiology Division, ICAR-National Institute of Animal Nutrition and Physiology, Adugodi, Bengaluru-560030, India
  • Balaganur Krishnappa Reproductive Physiology Laboratory, Animal Physiology Division, ICAR-National Institute of Animal Nutrition and Physiology, Adugodi, Bengaluru-560030, India
  • Sellappan Selvaraju Reproductive Physiology Laboratory, Animal Physiology Division, ICAR-National Institute of Animal Nutrition and Physiology, Adugodi, Bengaluru-560030, India

DOI:

https://doi.org/10.48165/ijvsbt.20.1.02

Keywords:

Bull fertility, Energy-production, Fertilization, Sperm kinematics, Sperm transcriptome

Abstract

Sperm biomolecules impact the reproductive success of a bull in many ways from fertilization to the health of the offspring. The  energy produced within the sperm enables them to remain motile and allows them to participate in fertilization events. In this study,  we deciphered the genes associated with energy production and their influence on the fertility rate. Post-thaw buffalo semen samples  (n=21) were analysed for sperm kinematics and field fertility for selecting high (n=5) and low (n=5) fertile samples. Sperm total RNAs  were extracted using a double lysis method followed by column-based extraction and sequenced using the Illumina platform. The  expression levels of the genes involved in energy-regulating pathways were analyzed. Among these genes, 14.6% were significantly  (p<0.05) differentially expressed between high and low fertile sperm. The expression levels of up-regulated genes such as JAK3, DDX5,  PRKCZ, CHD4, CHD5, and ADCY3 had a strong positive correlation (r>0.5) with progressive motility and velocities. In these, up-regulated  genes were involved in chemokine signaling (ADCY2 and JAK2, p=0.0001), calcium signaling (AGTR1 and SLC25A4,p=0.0002) and oocyte  meiosis (ADCY2 and ADCY3, p=0.049). The increase in the expression of ATP-producing genes substantiates the improved progressive  motility (64.51±5.79 vs 33.07±3.34 %), curvilinear velocity (70.58±4.32 vs 50.15±4.92 μm/sec), straight-line velocity (39.84±3.16 vs  26.02±2.52 μm/sec) and average path velocity (49.46±3.59 vs 32.99±3.45 μm/sec) in high fertile bulls compared to low fertile bulls. The  study suggests that the expression level of differentially expressed genes associated with energy-regulating pathways influences the  fertilizing ability of sperm. 

Downloads

Download data is not yet available.

References

Breitbart, H., & Etkovitz, N. (2011). Role and regulation of EGFR in actin remodeling in sperm capacitation and the acrosome reaction. Asian Journal of Andrology, 13(1), 106.

Caballero-Campo, P., Buffone, M.G., Benencia, F., Conejo-García, J.R., Rinaudo, P.F., & Gerton, G.L. (2014). A role for the chemokine receptor CCR6 in mammalian sperm motility and chemotaxis. Journal of Cellular Physiology, 229(1) ,68-78.

Casas, I., Sancho, S., Ballester, J., Briz, M., Pinart, E., Bussalleu, E., Yeste, M., Fàbrega, A., Rodríguez-Gil, J.E., & Bonet, S. (2010). The HSP90AA1 sperm content and the prediction of the boar ejaculate freezability. Theriogenology, 74(6), 940-950.

Dcunha, R., Hussein, R.S., Ananda, H., Kumari, S., Adiga, S.K., Kannan, N., Zhao, Y., & Kalthur, G. (2022). Current insights and latest updates in sperm motility and associated applications in assisted reproduction. Reproduction Sciences, 29,7-25.

Finkelstein, M., Etkovitz, N., & Breitbart, H. (2020). Ca2+ signaling in mammalian spermatozoa. Molecular and Cellular Endocrinology, 516, 110953.

Flegel, C., Vogel, F., Hofreuter, A., Schreiner, B.S., Osthold, S., Veitinger, S., Becker, C., Brockmeyer, N.H., Muschol, M., & Gisselmann, G. (2016). Characterization of the olfactory receptors expressed in human spermatozoa. Frontiersin Molecular Biosciences, 2, 73.

Ge, S. X., Jung, D., & Yao, R. (2020). ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics, 36(8), 2628-2629.

Ickowicz, D., Finkelstein, M., & Breitbart, H. (2012). Mechanism of sperm capacitation and the acrosome reaction: Role of protein kinases. Asian Journal of Andrology, 14(6), 816.

Ijiri, T.W., Mahbub Hasan, A.K.M., & Sato, K.I. (2012). Protein-tyrosine kinase signaling in the biological functions associated with sperm. Journal of Signal Transduction, 2012

Itach, S.B.S., Rubinstein, S., & Breitbart, H. (2007). Phospholipase D mediates motility in sperm capacitation. Fertility Sterility, 88, S362.

Jaldety, Y., Glick, Y., Orr-Urtreger, A., Ickowicz, D., Gerber, D., & Breitbart, H. (2012). Sperm epidermal growth factor receptor (EGFR) mediates α7 acetylcholine receptor (AChR) activation to promote fertilization. Journal of Biological Chemistry, 287(26), 22328-22340.

Jodar, M., Selvaraju, S., Sendler, E., Diamond, M.P., Krawetz, S. A., & Reproductive Medicine Network. (2013). The presence, role and clinical use of spermatozoal RNAs. Human Reproduction Update, 19(6), 604-624.

Kowsar, R., Ronasi, S., Sadeghi, N., Sadeghi, K., & Miyamoto, A. (2021). Epidermal growth factor alleviates the negative impact of urea on frozen-thawed bovine sperm, but the subsequent developmental competence is compromised. Scientific Reports, 11(1), 4687.

Kumar, A., Majhi, R.K., Swain, N., Giri, S.C., Kar, S., Samanta, L., & Goswami, C. (2016). TRPV4 is endogenously expressed in vertebrate spermatozoa and regulates intracellular calcium in human sperm. Biochemical and Biophysical Research Communications, 473(4), 781-788.

Lachance, C., & Leclerc, P. (2011). Mediators of the Jak/STAT signaling pathway in human spermatozoa. Biology of Reproduction, 85(6), 1222-1231.

LaLonde, M., Janssens, H., Yun, S., Crosby, J., Redina, O., Olive, V., Altshuller, Y.M., Choi, S.Y., Du, G., Gergen, J.P., & Frohman, M.A. (2006). A role for phospholipase D in Drosophila embryonic cellularization. BMC Developmental Biology, 6(1), 1-13.

Lavanya, M., Archana, S. S., Swathi, D., Ramya, L., Arangasamy, A., Binsila, B., Dhali, A., Krishnaswamy, N., Singh, S.K., Kumar, H., Sivaram, M., & Selvaraju, S. (2021). Sperm preparedness and adaptation to osmotic and pH stressors relate to functional competence of sperm in Bos taurus. Scientific Reports, 11(1), 22563.

Mannucci, A., Argento, F.R., Fini, E., Coccia, M.E., Taddei, N., Becatti, M., & Fiorillo, C. (2022). The impact of oxidative stress in male infertility. Frontiers in Molecular Biosciences, 8, 799294.

Naz, R.K. and Rajesh, P.B. (2004). Role of tyrosine phosphorylation in sperm capacitation/acrosome reaction. Reproductive Biology and Endocrinology, 2(1), 1-12.

Nowicka-Bauer, K., & Szymczak-Cendlak, M. (2021). Structure and function of ion channels regulating sperm motility - An overview. International Journalof Molecular Sciences, 22(6), 3259.

Parthipan, S., Selvaraju, S., Somashekar, L., Kolte, A. P., Arangasamy, A., & Ravindra, J. P. (2015). Spermatozoa input concentrations and RNA isolation methods on RNA yield and quality in bull (Bos taurus). Analytical biochemistry, 482, 32-39.

Parthipan, S., Selvaraju, S., Somashekar, L., Arangasamy, A., Sivaram, M., & Ravindra, J.P. (2017). Spermatozoal transcripts expression levels are predictive of semen quality and conception rate in bulls (Bos taurus). Theriogenology, 98, 41-49.

Ramya, L., Swathi, D., Archana, S.S., Lavanya, M., Parthipan, S., & Selvaraju, S. (2021). Establishment of bioinformatics pipeline for deciphering the biological complexities of fragmented sperm transcriptome. Analytical Biochemistry, 620, 114141.

Sagare-Patil, V., Vernekar, M., Galvankar, M., & Modi, D. (2013). Progesterone utilizes the PI3K-AKT pathway in human spermatozoa to regulate motility and hyperactivation but not acrosome reaction. Molecular and Cellular Endocrinology, 374(1-2), 82-91.

Sansegundo, E., Tourmente, M., & Roldan, E. R. S. (2022). Energy metabolism and hyperactivation of spermatozoa from three mouse species under capacitating conditions. Cells, 11,220.

Selvaraju, S., Parthipan, S., Somashekar, L., Kolte, A.P., Krishnan Binsila, B., Arangasamy, A., & Ravindra, J.P. (2017). Occurrence and functional significance of the transcriptome in bovine (Bos taurus) spermatozoa. Scientific Reports, 7(1), 42392.

Selvaraju, S., Ramya, L., Parthipan, S., Swathi, D., Binsila, B.K., & Kolte, A.P. (2021). Deciphering the complexity of sperm transcriptome reveals genes governing functional membrane and acrosome integrities potentially influence fertility. Cell and Tissue Research, 385, 207-222.

Selvaraju, S., Ramya, L., Swathi, D., Archana, S.S., Lavanya, M., Krishnappa, B., Binsila, B.K., Mahla, A.S., Arangasamy, A., Andonissamy, J., Kumar, P., & Sharma, R.K. (2023). Cryostress

induces fragmentation and alters the abundance of sperm transcripts associated with fertilizing competence and reproductive processes in buffalo. Cell and Tissue Research, 393, 181-199.

Tong, T., Shen, Y., Lee, H.W., Yu, R., & Park, T. (2016). Adenylyl cyclase 3 haploinsufficiency confers susceptibility to diet-induced obesity and insulin resistance in mice. Scientific Reports, 6(1), 34179.

Vohra, V., Chhotaray, S., Gowane, G., Alex, R., Mukherjee, A., Verma, A., & Deb, S. M. (2021). Genome-wide association studies in Indian buffalo revealed genomic regions for lactation and fertility. Frontiers in Genetics, 12, 696109.

Warriach, H.M., McGill, D.M., Bush, R.D., Wynn, P.C., & Chohan, K.R. (2015). Recent developments in buffalo reproduction - A review. Asian Australasian Journal of Animal Sciences, 28(3), 451.

Downloads

Published

2023-12-22

Issue

Vol. 20 No. 1 (2024): The Indian Journal of Veterinary Sciences and Biotechnology (IJVSBT) (Jan-Feb ) 2024

Section

Articles

License

Copyright (c) 2023 Indian Journal of Veterinary Sciences & Biotechnology

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

How to Cite

Ramya, L., Swathi, D., Archana, S.S., Arangasamy, A., Binsila, B.K., Krishnappa, B., & Selvaraju, S. (2023). Expression Levels of Sperm Genes Associated with Energy Production Pathways Regulate Fertility Status of Bulls. Indian Journal of Veterinary Sciences and Biotechnology, 20(1), 7–13. https://doi.org/10.48165/ijvsbt.20.1.02
Crossref
Scopus
Google Scholar
Europe PMC