#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#