Detection of Plasma Membrane Alpha Enolase (ENO1) and Its Relationship with Sperm Quality of Bali Cattle
Abstract
Bali cattle are the indigenous cattle well known attributed to their high fertility. Various proteomes in sperm are substances that can determine sperm quality and fertility. One of which is alpha enolase (ENO1). This study aims to assess the presence of ENO1 in the plasma membrane of sperm and its relationship with the semen quality of Bali cattle. The study used 30 ejaculates from 5 bulls for sperm quality assessment and detection of ENO1. Sperm quality is indicated by total motility, progressive motility, kinematics motility, viability, plasma membrane integrity, and ENO1 quantity. Sperm motility and kinematics motility were measured using CASA, while viability was assessed by eosin-nigrosine differential staining. The HOS test was used to determine plasma membrane integrity, and ENO1 quantity was measured by the ELISA method. Data were analyzed using ANOVA (randomized group design), linear regression, Pearson’s correction, and the t-Student test. The results showed that ENO1 was detected in the plasma membrane at 1.27 ng/106 sperms. The amount of alpha-enolase in the plasma membrane of Bali cattle sperm is affected by sperm concentration (p<0.01) and not involved in sperm motility. There was no correlation between plasma membrane ENO1 quantity and semen quality. The results of this experiment indicated that alpha-enolase in the plasma membrane of Bali cattle sperm is affected by sperm concentration but not related to sperm quality.
References
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Byrne, K., T. Leahy, R. McCulloch, L. Michelle. M. L. Colgrave, & M. K. Holland. 2012. Comprehensive mapping of the bull sperm surface proteome. Proteomics 12:3559–3579. https://doi.org/10.1002/pmic.201200133
Capello, M., S. Ferri-Borgogno, C. Riganti, M. S. Chattaragada, M. Principe, & C. Roux. 2016. Targeting the Warburg effect in cancer cells through ENO1 knockdown rescues oxidative phosphorylation and induces growth arrest. Oncotarget 7:5598–5612. https://doi.org/10.18632/oncotarget.6798
D’Amours, O., G. Frenette, M. Fortier, P. Leclerc, & R. Sullivan. 2010. Proteomic comparison of detergent- extracted sperm proteins from bulls with different fertility indexes. Reproduction 139:545–556. https://doi.org/10.1530/REP-09-0375
Dcunha, R., R. S. Hussein, H. Ananda, S. Kumari, S. K. Adiga, N. Kannan, Y. Zhao, & G. Kalthur. 2022. Current insights and latest updates in sperm motility and associated applications in assisted reproduction. Reprod. Sci. 29:7-25. https://doi.org/10.1007/s43032-020-00408-y
Diaz-Ramos, A., A. Roig-Borelllas, A. Garcia-Melero, & R. Lopez-Alemany. 2012. α-Enolase, a multifunctional protein: Its role on pathophysiological situations. J. Biomed. Biotechnol. 2012:156795. https://doi.org/10.1155/2012/156795
Didiasova, M., L. Scahefer, & M. Wygrecka. 2019. When place matters: Shuttling of enolase-1 across cellular compartments. Cell Dev. Biol. 7:61. https://doi.org/10.3389/fcell.2019.00061
Dixit, S., V. Pandey, D. K. Swain, R. Nigam, A. Sharma, D. Sharma, A. Saxena, & P. Singh. 2016. Seminal plasma and sperm membrane proteins of buffalo and cattle bulls: A comparative study. Buffalo Bulletin 35:437-443.
du Plessis, S. S., A. Agarwal, G. Mohanty, & M. Van der Linde. 2014. Oxidative phosphorylation versus glycolysis: what fuel do sperm use? Asian J. Androl. 17:230-235. https://doi.org/10.4103/1008-682X.135123
Fair, S. & P. Lonergan. 2018. Understanding the causes of variation in reproductive wastage among bulls. A review. Animal 12:s53-s62. https://doi.org/10.1017/S1751731118000964
Gallagher, M. T., G. Cupples, E. H. Ooi, J. C. Kirkman-Brown, & D. J. Smith. 2019. Rapid sperm capture: high-throughput flagellar waveform analysis. Hum. Reprod. 34:1173–1185. https://doi.org/10.1101/551267
Gaviraghi, A., F. Deriu, A. Soggiu, A. Galli, C. Bonacina, L. Bonizzi, & P. Roncada. 2010. Proteomics to investigate fertility in bull. Vet. Res. Commun. 34:33-36. https://doi.org/10.1007/s11259-010-9387-0
Gitlits, V. M., B. H. Toh, K. L. Loveland, & J. W. Sentry. 2000. The glycolytic enzyme enolase is present in sperm tail and displays nucleotide-dependent association with microtubules. Eur. J. Cell Biol. 79:104-111. https://doi.org/10.1078/S0171-9335(04)70012-6
Harayama, H., K. Minami, K. Kishida, & T. Noda. 2017. Protein biomarkers for male artificial insemination subfertility in bovine spermatozoa. Reprod. Med. Biol. 16:89-98. https://doi.org/10.1002/rmb2.12021
He, Y., H. Li, J. He, & X. Zhao. 2014. Heavy ion radiation can promote greater motility and enolase protein expression in ram sperm in in vitro liquid storage. Anim. Reprod. Sci. 148:260-266. https://doi.org/10.1016/j.anireprosci.2014.06.019
Hezavehei, M., M. Sharafi, H. M. Kouchesfahani, R. Henkel, A. Agarwal, & V. Esmaeili. 2018. Sperm cryopreservation: A review on current molecular cryobiology and advanced approaches. Reprod. Biomed. Online 37:327-339. https://doi.org/10.1016/j.rbmo.2018.05.012
Ji, H., J. Wang, J. Guo, Y. Li, S. Lian, W. Guo, H. Yang, F. Kong, L. Zhen, L. Guo, & Y. Liu. 2016. Progress in the biological function of alpha-enolase. Animal Nutrition 2:12-17. https://doi.org/10.1016/j.aninu.2016.02.005
Jiang, X. P., S. Q. Wang, W. Wang, Y. Xu, Z. Xu, J. Y. Tang, H. Y. Sun, Z. J. Wang, & W. Zhang. 2015. Enolase1 (ENO1) and glucose-6-phosphate isomerase (GPI) are good markers to predict human sperm freezability. Cryobiology 71:141-145. https://doi.org/10.1016/j.cryobiol.2015.04.006
Juliana, A., M. Hartono, & S. Suharyati. 2015. Repeat breeder pada sapi Bali di Kabupaten Pringsewu. Jurnal Ilmiah Peternakan Terpadu 3:42-47.
Kastelic, J. P. & J. Thundathil. 2008. Breeding soundness evaluation and semen analysis for predicting bull fertility. Reprod. Domest. Anim. 43:368–373. https://doi.org/10.1111/j.1439-0531.2008.01186.x
Kasvandik, S., G. Sillaste, A. Velhut-Meikas, A. V. Mikelsaar, T. Hallap, P. Padrik, T. Tenson, U. Jaakma, S. Koks, & A. Salumets. 2015. Bovine sperm plasma membrane proteomics through biotinylation and subcellular enrichment. Proteomics 15:1906-1920. ttps://doi.org/10.1002/pmic.201400297
Keller, A., J. Peltzer, G. Carpentier, I. Horvath, J. Olah, & A. Duchesnay. 2007. Interactions of enolase isoforms with tubulin and microtubules during myogenesis. Biochim. Biophys. Acta 1770:919–926. https://doi.org/10.1016/j.bbagen.2007.01.015
Kim, J. W. & C. V. Dang. 2005. Multifaceted roles of glycolytic enzymes. Trends Biochem. Sci. 30:142-150. https://doi.org/10.1016/j.tibs.2005.01.005
Kwon, W. S., J. S. Ryu, J. W. Park, I. C. Kim, J. Kim , M. S. Rahman, S. J. Yoon, Y. J. Park, Y. A. You, & M. G. Pang. 2012. Correlation of motion kinematics of spermatozoaand litter size in porcine. Reproductive Developmental Biology 36:189-192.
Lavanya, M., S. S. Archana, D. Swathi, L. Ramya, A. Arangasamy, B. Binsila, A. Dhali, N. Krishnaswamy, S. K. Singh, H. Kumar, M. Sivaram, & S. Selvaraju. 2021. Sperm preparedness and adaptation to osmotic and pH stressors relate to functional competence of sperm in Bos taurus. Scientific Reports 11:22563. https://doi.org/10.1038/s41598-021-01928-6
Liu, Z., A. Zhang, L. Zheng, A. F. Johnathan, J. Zhang, & G. Zhang. 2018. The biological significance and regulatory mechanism of c-Myc binding protein 1 (MBP-1). Int. J. Mol. Sci. 19:3868-3879. https://doi.org/10.3390/ijms19123868
Mortimer, D., C. L. R. Barratt, L. Bjorndahl, C. de Jager, A. M. Jequer, & C. H. Muller. 2013. What should it take to describe a substance or product as ‘sperm-safe’. Hum. Reprod. Update. 19:i1-i45. https://doi.org/10.1093/humupd/dmt008
Nagy, A., T. Polichronopoulos, A. Gaspardy, L. Solti, & S. Cseh. 2015. Correlation between bull fertility and sperm cell velocity parameters generated by computer-assisted semen analysis. Acta. Vet. Hung. 63:370-381. https://doi.org/10.1556/004.2015.035
Pancholi, V. & V. A. Fischetti. 1998. α-Enolase, a novel strong plasmin (ogen) binding protein of the surface of pathogenic streptococci. J. Biol. Chem. 273:14503-14515. https://doi.org/10.1074/jbc.273.23.14503
Park, Y. J., A. E. S. Mohamed, S. A. Oh, S. J. Yoon, W. S. Kwon, H. R. Kim, M. S. Lee, K. Lee, & M. G. Pang. 2012. Sperm penetration assay as an indicator of bull fertility. J. Reprod. Dev. 58:461-466. https://doi.org/10.1262/jrd.11-067H
Park, Y. J., B. M. Lee, W. K. Pang, D. Y. Ryu, M. S. Rahman, & M. G. Pang. 2022. Low sperm motility is determined by abnormal protein modification during epididymal maturation. World J. Mens Health 40:626-535. https://doi.org/10.5534/wjmh.210180
Pathak, P. K., A. J. Dhami, & D. V. Chaudhari. 2019. Correlations of motion characteristics and kinematic tttributes of fresh and frozen-thawed sperm of gir bulls. Indian Journal Veterinary Sciences Biotechnology 15:9-13. https://doi.org/10.21887/ijvsbt.15.1.2
Pérez-Patiño, C., I. Parrilla, J. Li, I. Barranco, E. A. Martínez, H. Rodriguez-Martínez, & J. Roca. 2019. The proteome of pig sperm is remodeled during ejaculation. Mol. Cell. Proteomics. 18:41-50. https://doi.org/10.1074/mcp.RA118.000840
Petit, F. M., C. Serres, F. Bourgeon, C. Pineau, & J. Auer. 2013. Identification of sperm head proteins involved in zona pellucida binding. Hum. Reprod. 28:852-65. https://doi.org/10.1093/humrep/des452
Prastowo, S., P. Dharmawan, T. Nugroho, A. Bachtiar, Lutojo, & A. Pramono. 2018. Kualitas semen segar sapi Bali (Bos javanicus) pada kelompok umur yang berbeda. Jurnal Ilmu Ternak Universitas Padjadjaran 18:1-7. https://doi.org/10.24198/jit.v18i1.17684
Purwantara, B., R. R. Noor, G. Anderson, & H. Rodriguez-Martinez. 2012. Banteng and Bali cattle in Indonesia: Status and forecasts. Reprod. Domest. Anim. 47:2–6. https://doi.org/10.1111/j.1439-0531.2011.01956.x
Rahman, M. S., J. S. Lee, W. S. Kwon, & M. G. Pang. 2013. Sperm proteomics: Road to male fertility and contraception. Int. J. Endocrinol. https://doi.org/10.1155/2013/360986
Ramu, S. & R. S. Jayendran. 2012. The hypo-osmotic swelling test for evaluation of sperm membrane integrity. Methods Mol. Biol. 927:21-25. https://doi.org/10.1007/978-1-62703-038-0_3
Reis, L. S. L. S., A. A. Ramos, A. S. Camargos, & E. Oba. 2016. Integrity of the plasma membrane, the acrosomal membrane, and the mitochondrial membrane potential of sperm in Nelore bulls from puberty to sexual maturity. Arq. Bras. Med. Vet. Zootec. 68:620-628. https://doi.org/10.1590/1678-4162-8748
Soler, C., A. Valverde, & D. Bompart. 2017. New methods of semen analysis by CASA. Agric. Biol. 52:232–241.
Tripathi, D., N. C. Sharma, S. K. Singh, & L. K. Gupta. 1999. Identification of bovine sperm specific polypeptides reactive with antisperm antibodies. Indian J. Exp. Biol. 37:655-661.
Turner, R. M. 2006. Moving to the beat: A review of mammalian sperm motility regulation. Reprod. Fertil. Dev. 18:25–38. https://doi.org/10.1071/RD05120
Yulnawati, Y., M. C. Abraham, D. Laskowski, A. Johannisson, & J. M. Morrell. 2014. Changes in bull sperm kinematics after single layer centrifugation. Reprod. Domest. Anim . 49:954-956. https://doi.org/10.1111/rda.12412
Zoca, S. M., E. J. Northrop-Albrecht, J. A. Walker, R. A. Cushman, & G. A. Perry. 2022. Proteomic analyses identify differences between bovine epididymal and ejaculated sperm that contribute to longevity. Theriogenology 184:51-60. https://doi.org/10.1016/j.theriogenology.2022.02.021
Agarwal, A., R. P. Bertolla, & L. Samanta. 2016a. Sperm proteomics: Potential impact on male infertility treatment. Expert. Rev. Proteomics 13:285-296. https://doi.org/10.1586/14789450.2016.1151357
Byrne, K., T. Leahy, R. McCulloch, L. Michelle. M. L. Colgrave, & M. K. Holland. 2012. Comprehensive mapping of the bull sperm surface proteome. Proteomics 12:3559–3579. https://doi.org/10.1002/pmic.201200133
Capello, M., S. Ferri-Borgogno, C. Riganti, M. S. Chattaragada, M. Principe, & C. Roux. 2016. Targeting the Warburg effect in cancer cells through ENO1 knockdown rescues oxidative phosphorylation and induces growth arrest. Oncotarget 7:5598–5612. https://doi.org/10.18632/oncotarget.6798
D’Amours, O., G. Frenette, M. Fortier, P. Leclerc, & R. Sullivan. 2010. Proteomic comparison of detergent- extracted sperm proteins from bulls with different fertility indexes. Reproduction 139:545–556. https://doi.org/10.1530/REP-09-0375
Dcunha, R., R. S. Hussein, H. Ananda, S. Kumari, S. K. Adiga, N. Kannan, Y. Zhao, & G. Kalthur. 2022. Current insights and latest updates in sperm motility and associated applications in assisted reproduction. Reprod. Sci. 29:7-25. https://doi.org/10.1007/s43032-020-00408-y
Diaz-Ramos, A., A. Roig-Borelllas, A. Garcia-Melero, & R. Lopez-Alemany. 2012. α-Enolase, a multifunctional protein: Its role on pathophysiological situations. J. Biomed. Biotechnol. 2012:156795. https://doi.org/10.1155/2012/156795
Didiasova, M., L. Scahefer, & M. Wygrecka. 2019. When place matters: Shuttling of enolase-1 across cellular compartments. Cell Dev. Biol. 7:61. https://doi.org/10.3389/fcell.2019.00061
Dixit, S., V. Pandey, D. K. Swain, R. Nigam, A. Sharma, D. Sharma, A. Saxena, & P. Singh. 2016. Seminal plasma and sperm membrane proteins of buffalo and cattle bulls: A comparative study. Buffalo Bulletin 35:437-443.
du Plessis, S. S., A. Agarwal, G. Mohanty, & M. Van der Linde. 2014. Oxidative phosphorylation versus glycolysis: what fuel do sperm use? Asian J. Androl. 17:230-235. https://doi.org/10.4103/1008-682X.135123
Fair, S. & P. Lonergan. 2018. Understanding the causes of variation in reproductive wastage among bulls. A review. Animal 12:s53-s62. https://doi.org/10.1017/S1751731118000964
Gallagher, M. T., G. Cupples, E. H. Ooi, J. C. Kirkman-Brown, & D. J. Smith. 2019. Rapid sperm capture: high-throughput flagellar waveform analysis. Hum. Reprod. 34:1173–1185. https://doi.org/10.1101/551267
Gaviraghi, A., F. Deriu, A. Soggiu, A. Galli, C. Bonacina, L. Bonizzi, & P. Roncada. 2010. Proteomics to investigate fertility in bull. Vet. Res. Commun. 34:33-36. https://doi.org/10.1007/s11259-010-9387-0
Gitlits, V. M., B. H. Toh, K. L. Loveland, & J. W. Sentry. 2000. The glycolytic enzyme enolase is present in sperm tail and displays nucleotide-dependent association with microtubules. Eur. J. Cell Biol. 79:104-111. https://doi.org/10.1078/S0171-9335(04)70012-6
Harayama, H., K. Minami, K. Kishida, & T. Noda. 2017. Protein biomarkers for male artificial insemination subfertility in bovine spermatozoa. Reprod. Med. Biol. 16:89-98. https://doi.org/10.1002/rmb2.12021
He, Y., H. Li, J. He, & X. Zhao. 2014. Heavy ion radiation can promote greater motility and enolase protein expression in ram sperm in in vitro liquid storage. Anim. Reprod. Sci. 148:260-266. https://doi.org/10.1016/j.anireprosci.2014.06.019
Hezavehei, M., M. Sharafi, H. M. Kouchesfahani, R. Henkel, A. Agarwal, & V. Esmaeili. 2018. Sperm cryopreservation: A review on current molecular cryobiology and advanced approaches. Reprod. Biomed. Online 37:327-339. https://doi.org/10.1016/j.rbmo.2018.05.012
Ji, H., J. Wang, J. Guo, Y. Li, S. Lian, W. Guo, H. Yang, F. Kong, L. Zhen, L. Guo, & Y. Liu. 2016. Progress in the biological function of alpha-enolase. Animal Nutrition 2:12-17. https://doi.org/10.1016/j.aninu.2016.02.005
Jiang, X. P., S. Q. Wang, W. Wang, Y. Xu, Z. Xu, J. Y. Tang, H. Y. Sun, Z. J. Wang, & W. Zhang. 2015. Enolase1 (ENO1) and glucose-6-phosphate isomerase (GPI) are good markers to predict human sperm freezability. Cryobiology 71:141-145. https://doi.org/10.1016/j.cryobiol.2015.04.006
Juliana, A., M. Hartono, & S. Suharyati. 2015. Repeat breeder pada sapi Bali di Kabupaten Pringsewu. Jurnal Ilmiah Peternakan Terpadu 3:42-47.
Kastelic, J. P. & J. Thundathil. 2008. Breeding soundness evaluation and semen analysis for predicting bull fertility. Reprod. Domest. Anim. 43:368–373. https://doi.org/10.1111/j.1439-0531.2008.01186.x
Kasvandik, S., G. Sillaste, A. Velhut-Meikas, A. V. Mikelsaar, T. Hallap, P. Padrik, T. Tenson, U. Jaakma, S. Koks, & A. Salumets. 2015. Bovine sperm plasma membrane proteomics through biotinylation and subcellular enrichment. Proteomics 15:1906-1920. ttps://doi.org/10.1002/pmic.201400297
Keller, A., J. Peltzer, G. Carpentier, I. Horvath, J. Olah, & A. Duchesnay. 2007. Interactions of enolase isoforms with tubulin and microtubules during myogenesis. Biochim. Biophys. Acta 1770:919–926. https://doi.org/10.1016/j.bbagen.2007.01.015
Kim, J. W. & C. V. Dang. 2005. Multifaceted roles of glycolytic enzymes. Trends Biochem. Sci. 30:142-150. https://doi.org/10.1016/j.tibs.2005.01.005
Kwon, W. S., J. S. Ryu, J. W. Park, I. C. Kim, J. Kim , M. S. Rahman, S. J. Yoon, Y. J. Park, Y. A. You, & M. G. Pang. 2012. Correlation of motion kinematics of spermatozoaand litter size in porcine. Reproductive Developmental Biology 36:189-192.
Lavanya, M., S. S. Archana, D. Swathi, L. Ramya, A. Arangasamy, B. Binsila, A. Dhali, N. Krishnaswamy, S. K. Singh, H. Kumar, M. Sivaram, & S. Selvaraju. 2021. Sperm preparedness and adaptation to osmotic and pH stressors relate to functional competence of sperm in Bos taurus. Scientific Reports 11:22563. https://doi.org/10.1038/s41598-021-01928-6
Liu, Z., A. Zhang, L. Zheng, A. F. Johnathan, J. Zhang, & G. Zhang. 2018. The biological significance and regulatory mechanism of c-Myc binding protein 1 (MBP-1). Int. J. Mol. Sci. 19:3868-3879. https://doi.org/10.3390/ijms19123868
Mortimer, D., C. L. R. Barratt, L. Bjorndahl, C. de Jager, A. M. Jequer, & C. H. Muller. 2013. What should it take to describe a substance or product as ‘sperm-safe’. Hum. Reprod. Update. 19:i1-i45. https://doi.org/10.1093/humupd/dmt008
Nagy, A., T. Polichronopoulos, A. Gaspardy, L. Solti, & S. Cseh. 2015. Correlation between bull fertility and sperm cell velocity parameters generated by computer-assisted semen analysis. Acta. Vet. Hung. 63:370-381. https://doi.org/10.1556/004.2015.035
Pancholi, V. & V. A. Fischetti. 1998. α-Enolase, a novel strong plasmin (ogen) binding protein of the surface of pathogenic streptococci. J. Biol. Chem. 273:14503-14515. https://doi.org/10.1074/jbc.273.23.14503
Park, Y. J., A. E. S. Mohamed, S. A. Oh, S. J. Yoon, W. S. Kwon, H. R. Kim, M. S. Lee, K. Lee, & M. G. Pang. 2012. Sperm penetration assay as an indicator of bull fertility. J. Reprod. Dev. 58:461-466. https://doi.org/10.1262/jrd.11-067H
Park, Y. J., B. M. Lee, W. K. Pang, D. Y. Ryu, M. S. Rahman, & M. G. Pang. 2022. Low sperm motility is determined by abnormal protein modification during epididymal maturation. World J. Mens Health 40:626-535. https://doi.org/10.5534/wjmh.210180
Pathak, P. K., A. J. Dhami, & D. V. Chaudhari. 2019. Correlations of motion characteristics and kinematic tttributes of fresh and frozen-thawed sperm of gir bulls. Indian Journal Veterinary Sciences Biotechnology 15:9-13. https://doi.org/10.21887/ijvsbt.15.1.2
Pérez-Patiño, C., I. Parrilla, J. Li, I. Barranco, E. A. Martínez, H. Rodriguez-Martínez, & J. Roca. 2019. The proteome of pig sperm is remodeled during ejaculation. Mol. Cell. Proteomics. 18:41-50. https://doi.org/10.1074/mcp.RA118.000840
Petit, F. M., C. Serres, F. Bourgeon, C. Pineau, & J. Auer. 2013. Identification of sperm head proteins involved in zona pellucida binding. Hum. Reprod. 28:852-65. https://doi.org/10.1093/humrep/des452
Prastowo, S., P. Dharmawan, T. Nugroho, A. Bachtiar, Lutojo, & A. Pramono. 2018. Kualitas semen segar sapi Bali (Bos javanicus) pada kelompok umur yang berbeda. Jurnal Ilmu Ternak Universitas Padjadjaran 18:1-7. https://doi.org/10.24198/jit.v18i1.17684
Purwantara, B., R. R. Noor, G. Anderson, & H. Rodriguez-Martinez. 2012. Banteng and Bali cattle in Indonesia: Status and forecasts. Reprod. Domest. Anim. 47:2–6. https://doi.org/10.1111/j.1439-0531.2011.01956.x
Rahman, M. S., J. S. Lee, W. S. Kwon, & M. G. Pang. 2013. Sperm proteomics: Road to male fertility and contraception. Int. J. Endocrinol. https://doi.org/10.1155/2013/360986
Ramu, S. & R. S. Jayendran. 2012. The hypo-osmotic swelling test for evaluation of sperm membrane integrity. Methods Mol. Biol. 927:21-25. https://doi.org/10.1007/978-1-62703-038-0_3
Reis, L. S. L. S., A. A. Ramos, A. S. Camargos, & E. Oba. 2016. Integrity of the plasma membrane, the acrosomal membrane, and the mitochondrial membrane potential of sperm in Nelore bulls from puberty to sexual maturity. Arq. Bras. Med. Vet. Zootec. 68:620-628. https://doi.org/10.1590/1678-4162-8748
Soler, C., A. Valverde, & D. Bompart. 2017. New methods of semen analysis by CASA. Agric. Biol. 52:232–241.
Tripathi, D., N. C. Sharma, S. K. Singh, & L. K. Gupta. 1999. Identification of bovine sperm specific polypeptides reactive with antisperm antibodies. Indian J. Exp. Biol. 37:655-661.
Turner, R. M. 2006. Moving to the beat: A review of mammalian sperm motility regulation. Reprod. Fertil. Dev. 18:25–38. https://doi.org/10.1071/RD05120
Yulnawati, Y., M. C. Abraham, D. Laskowski, A. Johannisson, & J. M. Morrell. 2014. Changes in bull sperm kinematics after single layer centrifugation. Reprod. Domest. Anim . 49:954-956. https://doi.org/10.1111/rda.12412
Zoca, S. M., E. J. Northrop-Albrecht, J. A. Walker, R. A. Cushman, & G. A. Perry. 2022. Proteomic analyses identify differences between bovine epididymal and ejaculated sperm that contribute to longevity. Theriogenology 184:51-60. https://doi.org/10.1016/j.theriogenology.2022.02.021
Authors
SumarsonoT., SupriatnaI., SetiadiM. A., AgilM., & PurwantaraB. (2023). Detection of Plasma Membrane Alpha Enolase (ENO1) and Its Relationship with Sperm Quality of Bali Cattle. Tropical Animal Science Journal, 46(1), 36-42. https://doi.org/10.5398/tasj.2023.46.1.36
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