The motility-based swim-up technique separates bull sperm based on differences in metabolic rates and tail length
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31600297
PubMed Central
PMC6786571
DOI
10.1371/journal.pone.0223576
PII: PONE-D-19-21814
Knihovny.cz E-zdroje
- MeSH
- adenosintrifosfát biosyntéza MeSH
- bazální metabolismus * MeSH
- bičík spermie metabolismus MeSH
- chov MeSH
- flagella metabolismus MeSH
- kinetika MeSH
- motilita spermií fyziologie MeSH
- oxidativní fosforylace MeSH
- skot MeSH
- spermie metabolismus MeSH
- spotřeba kyslíku MeSH
- viskozita MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- skot MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- adenosintrifosfát MeSH
Swim-up is a sperm purification method that is being used daily in andrology labs around the world as a simple step for in vitro sperm selection. This method accumulates the most motile sperm in the upper fraction and leaves sperm with low or no motility in the lower fraction. However, the underlying reasons are not fully understood. In this article, we compare metabolic rate, motility and sperm tail length of bovine sperm cells of the upper and lower fraction. The metabolic assay platform reveals oxygen consumption rates and extracellular acidification rates simultaneously and thereby delivers the metabolic rates in real time. Our study confirms that the upper fraction of bull sperm has not only improved motility compared to the cells in the lower fraction but also shows higher metabolic rates and longer flagella. This pattern was consistent across media of two different levels of viscosity. We conclude that the motility-based separation of the swim-up technique is also reflected in underlying metabolic differences. Metabolic assays could serve as additional or alternative, label-free method to evaluate sperm quality.
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Somigliana E, Paffoni A, Busnelli A, Filippi F, Pagliardini L, Vigano P, et al. Age-related infertility and unexplained infertility: An intricate clinical dilemma. Hum Reprod. 2016;31: 1390–1396. 10.1093/humrep/dew066 PubMed DOI
Evers JL. Female subfertility. Lancet. 2002;360: 151–159. 10.1016/S0140-6736(02)09417-5 PubMed DOI
Huszar G, Jakab A, Sakkas D, Ozenci CC, Cayli S, Delpiano E, et al. Fertility testing and ICSI sperm selection by hyaluronic acid binding: Clinical and genetic aspects. Reprod Biomed Online. 2007;14: 650–663. 10.1016/s1472-6483(10)61060-7 PubMed DOI
Organisation WH. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. Cambridge university press; 1999.
Garrett LJA, Revell SG, Leese HJ. Adenosine triphosphate production by bovine spermatozoa and its relationship to semen fertilizing ability. J Androl. 2008;29: 449–458. 10.2164/jandrol.107.003533 PubMed DOI
Tourmente M, Villar-Moya P, Rial E, Roldan ERS. Differences in ATP generation via glycolysis and oxidative phosphorylation and relationships with sperm motility in mouse species. J Biol Chem. 2015;290: 20613–20626. 10.1074/jbc.M115.664813 PubMed DOI PMC
Mukai C, Okuno M. Glycolysis Plays a Major Role for Adenosine Triphosphate Supplementation in Mouse Sperm Flagellar Movement. Biol Reprod. 2004;71: 540–547. 10.1095/biolreprod.103.026054 PubMed DOI
Storey BT. Mammalian sperm metabolism: Oxygen and sugar, friend and foe. Int J Dev Biol. 2008;52: 427–437. 10.1387/ijdb.072522bs PubMed DOI
Krzyzosiak J, Molan P, Vishwanath R. Measurements of bovine sperm velocities under true anaerobic and aerobic conditions. Anim Reprod Sci. 1999;55: 163–173. 10.1016/S0378-4320(99)00016-0 PubMed DOI
Nascimento JM, Shi LZ, Tam J, Chandsawangbhuwana C, Durrant B, Botvinick EL, et al. Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J Cell Physiol. 2008;217: 745–751. 10.1002/jcp.21549 PubMed DOI PMC
du Plessis S, Agarwal A, Mohanty G, van der Linde M. Oxidative phosphorylation versus glycolysis: what fuel do spermatozoa use? Asian J Androl. 2015;17: 230 10.4103/1008-682X.135123 PubMed DOI PMC
Reinhardt K, Breunig HG, Uchugonova A, König K. Sperm metabolism is altered during storage by female insects: Evidence from two-photon auto-fluorescence lifetime measurements in bedbugs. J R Soc Interface. 2015;12 10.1098/rsif.2015.0609 PubMed DOI PMC
Mahadevan MM, Trounson AO. The influence of seminal characteristics on the success rate of human in vitro fertilization. Fertil Steril. 1984;42: 400–405. 10.1016/s0015-0282(16)48080-5 PubMed DOI
Bongso TA, Ng SC, Mok H, Lim MN, Teo HL, Wong PC, et al. Effect of sperm motility on human in vitro fertilization. Syst Biol Reprod Med. 1989;22: 185–190. 10.3109/01485018908986770 PubMed DOI
Gasparini C, Simmons LW, Beveridge M, Evans JP. Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri. PLoS One. 2010;5: 1–5. 10.1371/journal.pone.0012146 PubMed DOI PMC
Burness G, Casselman SJ, Schulte-Hostedde AI, Moyes CD, Montgomerie R. Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus). Behav Ecol Sociobiol. 2004;56: 65–70. 10.1007/s00265-003-0752-7 DOI
WHO. Examination and processing of human semen [Internet]. World Health Organisation; 2010. http://whqlibdoc.who.int/publications/2010/9789241547789_eng.pdf
Yates CA, De Kretser DM. Male-factor infertility and in vitro fertilization. J Vitr Fertil Embryo Transf. 1987;4: 141–147. 10.1007/BF01555460 PubMed DOI
Davies NJ, Cumming DC. Sperm Preparation for Intra-uterine Insemination. J SOGC. 1999;21: 1294–1303. 10.1016/S0849-5831(16)30051-9 DOI
Yavetz H, Hauser R, Homonnai ZT, Paz GF, Lessing JB, Amit A, et al. Separation of sperm cells by sedimentation technique is not suitable for in vitro fertilization purposes. Andrologia. 2018;28: 3–6. 10.1111/j.1439-0272.1996.tb02750.x PubMed DOI
Esteves SC, Sharma RK, Thomas AJ, Agarwal A. Improvement in motion characteristics and acrosome status in cryopreserved human spermatozoa by swim-up processing before freezing. Hum Reprod. 2000;15: 2173–2179. 10.1093/humrep/15.10.2173 PubMed DOI
Holt WV., Hernandez M, Warrell L, Satake N. The long and the short of sperm selection in vitro and in vivo: Swim-up techniques select for the longer and faster swimming mammalian sperm. J Evol Biol. 2010;23: 598–608. 10.1111/j.1420-9101.2010.01935.x PubMed DOI
Parrish JJ, Foote RH. Quantification of Bovine Sperm Separation by a Swim‐up Method Relationship to Sperm Motility, Integrity of Acrosomes, Sperm Migration in Polyacrylamide Gel and Fertility. J Androl. 1987;8: 259–266. 10.1002/j.1939-4640.1987.tb03319.x PubMed DOI
Rikmenspoel R. Movements and active moments of bull sperm flagella as a function of temperature and viscosity. J Exp Biol. 1984;108: 205–230. PubMed
Kirkman-Brown JC, Smith DJ. Sperm motility: is viscosity fundamental to progress? Mol Hum Reprod. 2011;17: 539–544. 10.1093/molehr/gar043 PubMed DOI
González-Abreu D, García-Martínez S, Fernández-Espín V, Romar R, Gadea J. Incubation of boar spermatozoa in viscous media by addition of methylcellulose improves sperm quality and penetration rates during in vitro fertilization. Theriogenology. 2017;92: 14–23. 10.1016/j.theriogenology.2017.01.016 PubMed DOI
Aitken RJ, Baker MA. Oxidative stress and male reproductive biology. Reprod Fertil Dev. 2004;16: 581–588. 10.10371/RD03089 PubMed DOI
Orr TJ, Brennan PLR. Sperm storage: Distinguishing selective processes and evaluating criteria. Trends Ecol Evol. 2015;30: 261–272. 10.1016/j.tree.2015.03.006 PubMed DOI
Wilson-Leedy JG, Ingermann RL. Computer assisted sperm analysis using ImageJ; description of necessary components and use of free software. 2011; 1–7.
Purchase CF, Earle PT. Modifications to the imagej computer assisted sperm analysis plugin greatly improve efficiency and fundamentally alter the scope of attainable data. J Appl Ichthyol. 2012;28: 1013–1016. 10.1111/jai.12070 DOI
Huijing F, Slater EC. The Use of Oligomycin as an Inhibitor of Oxidative Phosphorylation. J Biochem. 1961;49: 493–501. 10.1093/oxfordjournals.jbchem.a127334 PubMed DOI
Hyakutake T, Suzuki H, Yamamoto S. Effect of non-Newtonian fluid properties on bovine sperm motility. J Biomech. 2015;48: 2941–2947. 10.1016/j.jbiomech.2015.08.005 PubMed DOI
Eamer L, Nosrati R, Vollmer M, Zini A, Sinton D. Microfluidic assessment of swimming media for motility-based sperm selection. Biomicrofluidics. 2015;9: 44113 10.1063/1.4928129 PubMed DOI PMC
Ivic A, Onyeaka H, Girling A, Brewis IA, Ola B, Hammadieh N, et al. Critical evaluation of methylcellulose as an alternative medium in sperm migration tests. Hum Reprod. 2002;17: 143–149. Available: 10.1093/humrep/17.1.143 PubMed DOI
R version 3.5.2 [Internet]. 2018. Available: https://cran.r-project.org/bin/windows/base/old/3.5.2/
Bates D, Mächler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Software; Vol 1, Issue 1 2015; Available: https://www.jstatsoft.org/v067/i01
Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder MN, et al. AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw. 2012;27: 233–249. 10.1080/10556788.2011.597854 DOI
Skaug H, Fournier D, Nielsen A, Magnusson A, Bolker B. Generalized linear mixed models using AD model builder. R Packag version 07. 2013;7.
Amir D, Schindler H. The effect of high sperm concentrations on the rates of respiration and fructolysis by ram spermatozoa. Reproduction. 1967;13: 93–99. PubMed
Zhang J, Nuebel E, Wisidagama DRR, Setoguchi K, Hong JS, Van Horn CM, et al. Measuring energy metabolism in cultured cells, including human pluripotent stem cells and differentiated cells. Nat Protoc. 2012;7: 10.1038/nprot.2012.048 PubMed DOI PMC
Lai SK, O’Hanlon DE, Harrold S, Man ST, Wang Y-Y, Cone R, et al. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus. Proc Natl Acad Sci U S A. 2007;104: 1482–7. 10.1073/pnas.0608611104 PubMed DOI PMC
Hyakutake T, Mori K, Sato K. Effects of surrounding fluid on motility of hyperactivated bovine sperm. J Biomech. 2018;71: 183–189. 10.1016/j.jbiomech.2018.02.009 PubMed DOI
Dresdner RD, Katz DF. Relationships of Mammalian Sperm Motility and Morphology to Hydrodynamic Aspects of Cell Function1. Biol Reprod. 1981;25: 920–930. 10.1095/biolreprod25.5.920 PubMed DOI
Losano JDA, Padín JF, Méndez-López I, Angrimani DSR, García AG, Barnabe VH, et al. The stimulated glycolytic pathway is able to maintain ATP levels and kinetic patterns of bovine epididymal sperm subjected to mitochondrial uncoupling. Oxid Med Cell Longev. 2017;2017 10.1155/2017/1682393 PubMed DOI PMC
Nevo AC, Rikmenspoel R. Diffusion of ATP in sperm flagella. J Theor Biol. 1970;26: 11–18. 10.1016/s0022-5193(70)80027-3 PubMed DOI
Ford WCL. Glycolysis and sperm motility: Does a spoonful of sugar help the flagellum go round? Hum Reprod Update. 2006;12: 269–274. 10.1093/humupd/dmi053 PubMed DOI
Ishimoto K, Gadêlha H, Gaffney EA, Smith DJ, Kirkman-Brown J. Human sperm swimming in a high viscosity mucus analogue. J Theor Biol. 2018;446: 1–10. 10.1016/j.jtbi.2018.02.013 PubMed DOI
Reinhardt K, Dobler R, Abbott J. An Ecology of Sperm: Sperm Diversification by Natural Selection. Annu Rev Ecol Evol Syst. 2015;46: 435–459. 10.1146/annurev-ecolsys-120213-091611 DOI
Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005;120: 483–495. 10.1016/j.cell.2005.02.001 PubMed DOI
Tremellen K. Oxidative stress and male infertility—a clinical perspective. 2008;14: 243–258. 10.1093/humupd/dmn004 PubMed DOI
Birkhead TR, Moller AP. Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biol J Linn Soc. 1993;50: 295–311. 10.1111/j.1095-8312.1993.tb00933.x DOI
Alm-Kristiansen AH, Standerholen FB, Bai G, Waterhouse KE, Kommisrud E. Relationship between post-thaw adenosine triphosphate content, motility and viability in cryopreserved bovine semen applying two different preservation methods. Reprod Domest Anim. 2018;53: 1448–1455. 10.1111/rda.13285 PubMed DOI
Genetic Association in the Maintenance of the Mitochondrial Microenvironment and Sperm Capacity