The motility-based swim-up technique separates bull sperm based on differences in metabolic rates and tail length
Autoři:
Veronika Magdanz aff001; Sergii Boryshpolets aff002; Clara Ridzewski aff001; Barbara Eckel aff001; Klaus Reinhardt aff001
Působiště autorů:
Chair of Applied Zoology, TU Dresden, Zellescher Weg, Dresden, Germany
aff001; University of South Bohemia in České Budějovice, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrosensors Zátiší 728/II, Vodňany, Czech Republic
aff002
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223576
Souhrn
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.
Klíčová slova:
Glycolysis – Oxidative phosphorylation – Sperm – Viscosity – Swimming – Cell metabolism – Cell swimming – Oxygen metabolism
Zdroje
1. 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. doi: 10.1093/humrep/dew066 27060173
2. Evers JL. Female subfertility. Lancet. 2002;360: 151–159. doi: 10.1016/S0140-6736(02)09417-5 12126838
3. 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. doi: 10.1016/s1472-6483(10)61060-7 17509211
4. Organisation WH. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. Cambridge university press; 1999.
5. 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. doi: 10.2164/jandrol.107.003533 18046050
6. 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. doi: 10.1074/jbc.M115.664813 26048989
7. Mukai C, Okuno M. Glycolysis Plays a Major Role for Adenosine Triphosphate Supplementation in Mouse Sperm Flagellar Movement. Biol Reprod. 2004;71: 540–547. doi: 10.1095/biolreprod.103.026054 15084484
8. Storey BT. Mammalian sperm metabolism: Oxygen and sugar, friend and foe. Int J Dev Biol. 2008;52: 427–437. doi: 10.1387/ijdb.072522bs 18649255
9. Krzyzosiak J, Molan P, Vishwanath R. Measurements of bovine sperm velocities under true anaerobic and aerobic conditions. Anim Reprod Sci. 1999;55: 163–173. https://doi.org/10.1016/S0378-4320(99)00016-0 10379669
10. 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. doi: 10.1002/jcp.21549 18683212
11. 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. doi: 10.4103/1008-682X.135123 25475660
12. 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. doi: 10.1098/rsif.2015.0609 26333813
13. Mahadevan MM, Trounson AO. The influence of seminal characteristics on the success rate of human in vitro fertilization. Fertil Steril. 1984;42: 400–405. doi: 10.1016/s0015-0282(16)48080-5 6468675
14. 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. doi: 10.3109/01485018908986770 2757456
15. 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. doi: 10.1371/journal.pone.0012146 20730092
16. 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. doi: 10.1007/s00265-003-0752-7
17. WHO. Examination and processing of human semen [Internet]. World Health Organisation. 2010. http://whqlibdoc.who.int/publications/2010/9789241547789_eng.pdf
18. Yates CA, De Kretser DM. Male-factor infertility and in vitro fertilization. J Vitr Fertil Embryo Transf. 1987;4: 141–147. doi: 10.1007/BF01555460
19. Davies NJ, Cumming DC. Sperm Preparation for Intra-uterine Insemination. J SOGC. 1999;21: 1294–1303. doi: 10.1016/S0849-5831(16)30051-9
20. 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. doi: 10.1111/j.1439-0272.1996.tb02750.x 8659712
21. 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. doi: 10.1093/humrep/15.10.2173 11006194
22. 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. doi: 10.1111/j.1420-9101.2010.01935.x 20487132
23. 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. doi: 10.1002/j.1939-4640.1987.tb03319.x 3624063
24. Rikmenspoel R. Movements and active moments of bull sperm flagella as a function of temperature and viscosity. J Exp Biol. 1984;108: 205–230. 6707571
25. Kirkman-Brown JC, Smith DJ. Sperm motility: is viscosity fundamental to progress? Mol Hum Reprod. 2011;17: 539–544. doi: 10.1093/molehr/gar043 21653751
26. 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. doi: 10.1016/j.theriogenology.2017.01.016 28237329
27. Aitken RJ, Baker MA. Oxidative stress and male reproductive biology. Reprod Fertil Dev. 2004;16: 581–588. doi: 10.10371/RD03089 15367373
28. Orr TJ, Brennan PLR. Sperm storage: Distinguishing selective processes and evaluating criteria. Trends Ecol Evol. 2015;30: 261–272. doi: 10.1016/j.tree.2015.03.006 25843274
29. Wilson-Leedy JG, Ingermann RL. Computer assisted sperm analysis using ImageJ; description of necessary components and use of free software. 2011; 1–7.
30. 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. doi: 10.1111/jai.12070
31. Huijing F, Slater EC. The Use of Oligomycin as an Inhibitor of Oxidative Phosphorylation. J Biochem. 1961;49: 493–501. doi: 10.1093/oxfordjournals.jbchem.a127334 13716716
32. Hyakutake T, Suzuki H, Yamamoto S. Effect of non-Newtonian fluid properties on bovine sperm motility. J Biomech. 2015;48: 2941–2947. doi: 10.1016/j.jbiomech.2015.08.005 26277700
33. Eamer L, Nosrati R, Vollmer M, Zini A, Sinton D. Microfluidic assessment of swimming media for motility-based sperm selection. Biomicrofluidics. 2015;9: 44113. doi: 10.1063/1.4928129 26339314
34. 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: doi: 10.1093/humrep/17.1.143 11756379
35. R version 3.5.2 [Internet]. 2018. Available: https://cran.r-project.org/bin/windows/base/old/3.5.2/
36. 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
37. 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. doi: 10.1080/10556788.2011.597854
38. Skaug H, Fournier D, Nielsen A, Magnusson A, Bolker B. Generalized linear mixed models using AD model builder. R Packag version 07. 2013;7.
39. 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.
40. 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: doi: 10.1038/nprot.2012.048 22576106
41. 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. doi: 10.1073/pnas.0608611104 17244708
42. Hyakutake T, Mori K, Sato K. Effects of surrounding fluid on motility of hyperactivated bovine sperm. J Biomech. 2018;71: 183–189. doi: 10.1016/j.jbiomech.2018.02.009 29459071
43. Dresdner RD, Katz DF. Relationships of Mammalian Sperm Motility and Morphology to Hydrodynamic Aspects of Cell Function1. Biol Reprod. 1981;25: 920–930. doi: 10.1095/biolreprod25.5.920 7326307
44. 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. doi: 10.1155/2017/1682393 28588746
45. Nevo AC, Rikmenspoel R. Diffusion of ATP in sperm flagella. J Theor Biol. 1970;26: 11–18. doi: 10.1016/s0022-5193(70)80027-3 5411106
46. Ford WCL. Glycolysis and sperm motility: Does a spoonful of sugar help the flagellum go round? Hum Reprod Update. 2006;12: 269–274. doi: 10.1093/humupd/dmi053 16407453
47. 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. doi: 10.1016/j.jtbi.2018.02.013 29462624
48. Reinhardt K, Dobler R, Abbott J. An Ecology of Sperm: Sperm Diversification by Natural Selection. Annu Rev Ecol Evol Syst. 2015;46: 435–459. doi: 10.1146/annurev-ecolsys-120213-091611
49. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005;120: 483–495. doi: 10.1016/j.cell.2005.02.001 15734681
50. Tremellen K. Oxidative stress and male infertility—a clinical perspective. 2008;14: 243–258. doi: 10.1093/humupd/dmn004 18281241
51. 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. doi: 10.1111/j.1095-8312.1993.tb00933.x
52. 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. doi: 10.1111/rda.13285 30044013
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Experimentally validated simulation of coronary stents considering different dogboning ratios and asymmetric stent positioning
- Prevalence of pectus excavatum (PE), pectus carinatum (PC), tracheal hypoplasia, thoracic spine deformities and lateral heart displacement in thoracic radiographs of screw-tailed brachycephalic dogs