Analyze Diet
Biology2020; 9(9); 254; doi: 10.3390/biology9090254

Red-Light Irradiation of Horse Spermatozoa Increases Mitochondrial Activity and Motility through Changes in the Motile Sperm Subpopulation Structure.

Abstract: Previous studies in other mammalian species have shown that stimulation of semen with red-light increases sperm motility, mitochondrial activity, and fertilizing capacity. This study sought to determine whether red-light stimulation using a light emitting diode (LED) at 620-630 nm affects sperm motility and structure of motile subpopulations, sperm viability, mitochondrial activity, intracellular ATP levels, rate of O consumption and DNA integrity of horse spermatozoa. For this purpose, nine ejaculates were collected from nine different adult stallions. Upon collection, semen was diluted in Kenney extender, analyzed, its concentration was adjusted, and finally it was stimulated with red-light. In all cases, semen was packaged in 0.5-mL transparent straws, which were randomly divided into controls and 19 light-stimulation treatments; 6 consisted of a single exposure to red-light, and the other 13 involved irradiation with intervals of irradiation and darkness (light-dark-light). After irradiation, sperm motility was assessed using a Computerized Semen Analysis System (CASA). Flow cytometry was used to evaluate sperm viability, mitochondrial membrane potential and DNA fragmentation. Intracellular levels of ATP and O consumption rate were also determined. Specific red-light patterns were found to modify kinetics parameters (patterns: 4, 2-2-2, 3-3-3, 4-4-4, 5-1-5, and 5-5-5 min), the structure of motile sperm subpopulations (patterns: 2, 2-2-2, 3-3-3, and 4-1-4 min), mitochondrial membrane potential (patterns: 4, 3-3-3, 4-4-4, 5-1-5, 5-5-5, 15-5-15, and 15-15-15 min), intracellular ATP levels and the rate of O consumption (pattern: 4 min), without affecting sperm viability or DNA integrity. Since the increase in some kinematic parameters was concomitant with that of mitochondrial activity, intracellular ATP levels and O consumption rate, we suggest that the positive effect of light-irradiation on sperm motility is related to its impact upon mitochondrial activity. In conclusion, this study shows that red LED light stimulates motility and mitochondrial activity of horse sperm. Additional research is needed to address the impact of red-light irradiation on fertilizing ability and the mechanisms through which light exerts its effects.
Publication Date: 2020-08-29 PubMed ID: 32872467PubMed Central: PMC7565061DOI: 10.3390/biology9090254Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research tested the effect of red-light stimulation on horse sperm activity, including motility, viability, mitochondrial activity, intracellular ATP levels, DNA integrity, and consumption of Oxygen. The findings suggest that certain patterns of the red-light irradiation enhanced sperm kinetics, altered the structure of motile sperm subpopulations, influenced mitochondrial activity, ATP level, and oxygen consumption rates without affecting sperm viability or integrity.

Research Methodology

  • The semen samples were collected from nine adult stallions and were subjected to red-light stimulation using a LED at a wavelength between 620-630 nm. This was done in the hope that it would affect the sperm’s motility and structure of motile subpopulations, as well as their viability, mitochondrial activity, intracellular ATP levels, oxygen consumption rate, and DNA integrity.
  • The collected and diluted semen was divided into control samples and 19 different light-stimulation treatments. Where six of these treatments were single exposure to red-light and the remaining 13 involved red-light irradiation with varying intervals of light and darkness (e.g., light-dark-light).
  • The sperm motility was assessed using a Computerized Semen Analysis System (CASA). Additionally, methods such as flow cytometry were used to evaluate sperm viability, mitochondrial membrane potential, and DNA fragmentation.
  • ATP levels and Oxygen consumption rates were also tested to evaluate the effects of red light stimulation.

Key Findings

  • Certain red-light patterns were found to enhance the kinetics parameters of the sperm. Most effective patterns included: 4, 2-2-2, 3-3-3, 4-4-4, 5-1-5, and 5-5-5 minutes.
  • Exposure to specific light patterns brought changes to the structure of motile sperm subpopulations. The patterns that induced changes were 2, 2-2-2, 3-3-3, and 4-1-4 minutes.
  • Some red-light patterns boosted mitochondrial membrane potential. These patterns were 4, 3-3-3, 4-4-4, 5-1-5, 5-5-5, 15-5-15, and 15-15-15 minutes.
  • The pattern that increased both the intracellular ATP levels and the oxygen consumption rate was 4 minutes.
  • The application of the red-light did not affect the sperm’s viability or DNA integrity.

Conclusion

From the study results, an increase in kinematic features showed a parallel increase in mitochondrial activity, ATP levels, and Oxygen consumption rate. This parallel increase strongly suggests that the improvement in sperm motility is linked to the positive influence exerted by light-irradiation on the sperm’s mitochondrial activities. The research confidently states that red LED light can stimulate motility and mitochondrial activity of horse sperm. However, more research is required to understand the overall effect of red-light irradiation on the fertilizing ability of the sperm and to gain clarity on the mechanisms behind the lights’ effect.

Cite This Article

APA
Catalán J, Papas M, Gacem S, Mateo-Otero Y, Rodríguez-Gil JE, Miró J, Yeste M. (2020). Red-Light Irradiation of Horse Spermatozoa Increases Mitochondrial Activity and Motility through Changes in the Motile Sperm Subpopulation Structure. Biology (Basel), 9(9), 254. https://doi.org/10.3390/biology9090254

Publication

ISSN: 2079-7737
NlmUniqueID: 101587988
Country: Switzerland
Language: English
Volume: 9
Issue: 9
PII: 254

Researcher Affiliations

Catalán, Jaime
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, ES-08193 Bellaterra (Cerdanyola del Vallès), Spain.
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Institute of Food and Agricultural Technology, University of Girona, ES-17003 Girona, Spain.
  • Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, ES-17003 Girona, Spain.
Papas, Marion
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, ES-08193 Bellaterra (Cerdanyola del Vallès), Spain.
Gacem, Sabrina
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, ES-08193 Bellaterra (Cerdanyola del Vallès), Spain.
Mateo-Otero, Yentel
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Institute of Food and Agricultural Technology, University of Girona, ES-17003 Girona, Spain.
  • Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, ES-17003 Girona, Spain.
Rodríguez-Gil, Joan E
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, ES-08193 Bellaterra (Cerdanyola del Vallès), Spain.
Miró, Jordi
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, ES-08193 Bellaterra (Cerdanyola del Vallès), Spain.
Yeste, Marc
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Institute of Food and Agricultural Technology, University of Girona, ES-17003 Girona, Spain.
  • Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, ES-17003 Girona, Spain.

Grant Funding

  • AGL2017-88329-R / Ministerio de Ciencia e Innovaciu00f3n
  • RYC-2014-15581 / Ministerio de Ciencia e Innovaciu00f3n
  • 2017-SGR-1229 / Agu00e8ncia de Gestiu00f3 d'Ajuts Universitaris i de Recerca
  • 2017/72180128 / Comisiu00f3n Nacional de Investigaciu00f3n Cientu00edfica y Tecnolu00f3gica

Conflict of Interest Statement

J.E.R.-G. and M.Y. are inventors of a patent entitled ‘Method and apparatus for improving the quality of mammalian sperm’ (European Patent Office, no. 16199093.2; EP-3-323-289-A1), which is owned by Instruments Utils de Laboratori Geniul, SL (Barcelona, Spain).

References

This article includes 56 references
  1. Brinsko SP, Varner DD. Artificial insemination and preservation of semen.. Vet Clin North Am Equine Pract 1992 Apr;8(1):205-18.
    doi: 10.1016/S0749-0739(17)30476-5pubmed: 1576550google scholar: lookup
  2. Aurich J.E.. Artificial Insemination in Horses-More than a Century of Practice and Research.. J. Equine Vet. Sci. 2012;32:458–463.
  3. Canisso I.F., Souza F.A., Marlén J., Escobar O., Ribeiro De Carvalho G., Davies Morel M.C., Capistrano Da Silva E., Domingos Guimarães J., Lima A.L.. Freezing of Donkey Semen (Equus Asinus). Rev. Investig. Vet. Perú. 2008;19:113–125.
  4. Losinno L., Aguilar J.. Reproducción y Biotecnologías en la Producción Equina: Curso de Producción Equina I.. 2002 :1–4.
  5. Varner DD. Strategies for Processing Semen from Subfertile Stallions for Cooled Transport.. Vet Clin North Am Equine Pract 2016 Dec;32(3):547-560.
    doi: 10.1016/j.cveq.2016.07.007pubmed: 27726991google scholar: lookup
  6. Loomis PR. Advanced methods for handling and preparation of stallion semen.. Vet Clin North Am Equine Pract 2006 Dec;22(3):663-76.
    doi: 10.1016/j.cveq.2006.07.002pubmed: 17129794google scholar: lookup
  7. Yeste M, Codony F, Estrada E, Lleonart M, Balasch S, Peña A, Bonet S, Rodríguez-Gil JE. Specific LED-based red light photo-stimulation procedures improve overall sperm function and reproductive performance of boar ejaculates.. Sci Rep 2016 Mar 2;6:22569.
    doi: 10.1038/srep22569pmc: PMC4773850pubmed: 26931070google scholar: lookup
  8. Blanco Prieto O, Catalán J, Lleonart M, Bonet S, Yeste M, Rodríguez-Gil JE. Red-light stimulation of boar semen prior to artificial insemination improves field fertility in farms: A worldwide survey.. Reprod Domest Anim 2019 Aug;54(8):1145-1148.
    doi: 10.1111/rda.13470pubmed: 31104351google scholar: lookup
  9. Pezo F, Zambrano F, Uribe P, Ramírez-Reveco A, Romero F, Sanchéz R. LED-based red light photostimulation improves short-term response of cooled boar semen exposed to thermal stress at 37°C.. Andrologia 2019 Jun;51(5):e13237.
    doi: 10.1111/and.13237pubmed: 30656707google scholar: lookup
  10. Cohen N, Lubart R, Rubinstein S, Breitbart H. Light irradiation of mouse spermatozoa: stimulation of in vitro fertilization and calcium signals.. Photochem Photobiol 1998 Sep;68(3):407-13.
  11. Zan-Bar T, Bartoov B, Segal R, Yehuda R, Lavi R, Lubart R, Avtalion RR. Influence of visible light and ultraviolet irradiation on motility and fertility of mammalian and fish sperm.. Photomed Laser Surg 2005 Dec;23(6):549-55.
    doi: 10.1089/pho.2005.23.549pubmed: 16356145google scholar: lookup
  12. Preece D, Chow KW, Gomez-Godinez V, Gustafson K, Esener S, Ravida N, Durrant B, Berns MW. Red light improves spermatozoa motility and does not induce oxidative DNA damage.. Sci Rep 2017 Apr 20;7:46480.
    doi: 10.1038/srep46480pmc: PMC5397839pubmed: 28425485google scholar: lookup
  13. Gabel CP, Carroll J, Harrison K. Sperm motility is enhanced by Low Level Laser and Light Emitting Diode photobiomodulation with a dose-dependent response and differential effects in fresh and frozen samples.. Laser Ther 2018 Jun 30;27(2):131-136.
    doi: 10.5978/islsm.18-OR-13pmc: PMC6062680pubmed: 30087533google scholar: lookup
  14. Yeste M, Castillo-Martín M, Bonet S, Rodríguez-Gil JE. Impact of light irradiation on preservation and function of mammalian spermatozoa.. Anim Reprod Sci 2018 Jul;194:19-32.
  15. Iaffaldano N, Paventi G, Pizzuto R, Passarella S, Cerolini S, Zaniboni L, Marzoni M, Castillo A, Rosato MP. The post-thaw irradiation of avian spermatozoa with He-Ne laser differently affects chicken, pheasant and turkey sperm quality.. Anim Reprod Sci 2013 Nov 30;142(3-4):168-72.
  16. Corral-Baqués MI, Rigau T, Rivera M, Rodríguez JE, Rigau J. Effect of 655-nm diode laser on dog sperm motility.. Lasers Med Sci 2005;20(1):28-34.
    doi: 10.1007/s10103-005-0332-3pubmed: 15838719google scholar: lookup
  17. Corral-Baqués MI, Rivera MM, Rigau T, Rodríguez-Gil JE, Rigau J. The effect of low-level laser irradiation on dog spermatozoa motility is dependent on laser output power.. Lasers Med Sci 2009 Sep;24(5):703-13.
    doi: 10.1007/s10103-008-0606-7pubmed: 18787758google scholar: lookup
  18. Iaffaldano N, Rosato MP, Paventi G, Pizzuto R, Gambacorta M, Manchisi A, Passarella S. The irradiation of rabbit sperm cells with He-Ne laser prevents their in vitro liquid storage dependent damage.. Anim Reprod Sci 2010 May;119(1-2):123-9.
  19. Rodríguez-Gil JE. Photostimulation and thermotaxis of sperm: Overview and practical implications in porcine reproduction.. Theriogenology 2019 Oct 1;137:8-14.
  20. Karu T. Photobiology of low-power laser effects.. Health Phys 1989 May;56(5):691-704.
  21. Gao X, Xing D. Molecular mechanisms of cell proliferation induced by low power laser irradiation.. J Biomed Sci 2009 Jan 12;16(1):4.
    doi: 10.1186/1423-0127-16-4pmc: PMC2644974pubmed: 19272168google scholar: lookup
  22. Kenney M.R.. Minimal contamination techniques for breeding mares: Techniques and priliminary findings.. Proc. Am. Assoc. Equine Pract. 1975:327–336.
  23. Lee JA, Spidlen J, Boyce K, Cai J, Crosbie N, Dalphin M, Furlong J, Gasparetto M, Goldberg M, Goralczyk EM, Hyun B, Jansen K, Kollmann T, Kong M, Leif R, McWeeney S, Moloshok TD, Moore W, Nolan G, Nolan J, Nikolich-Zugich J, Parrish D, Purcell B, Qian Y, Selvaraj B, Smith C, Tchuvatkina O, Wertheimer A, Wilkinson P, Wilson C, Wood J, Zigon R, Scheuermann RH, Brinkman RR. MIFlowCyt: the minimum information about a Flow Cytometry Experiment.. Cytometry A 2008 Oct;73(10):926-30.
    doi: 10.1002/cyto.a.20623pmc: PMC2773297pubmed: 18752282google scholar: lookup
  24. Petrunkina AM, Waberski D, Bollwein H, Sieme H. Identifying non-sperm particles during flow cytometric physiological assessment: a simple approach.. Theriogenology 2010 Apr 15;73(7):995-1000.
  25. Yeste M, Flores E, Estrada E, Bonet S, Rigau T, Rodríguez-Gil JE. Reduced glutathione and procaine hydrochloride protect the nucleoprotein structure of boar spermatozoa during freeze-thawing by stabilising disulfide bonds.. Reprod Fertil Dev 2013;25(7):1036-50.
    doi: 10.1071/RD12230pubmed: 23089308google scholar: lookup
  26. Garner DL, Johnson LA. Viability assessment of mammalian sperm using SYBR-14 and propidium iodide.. Biol Reprod 1995 Aug;53(2):276-84.
    doi: 10.1095/biolreprod53.2.276pubmed: 7492679google scholar: lookup
  27. Ortega-Ferrusola C, Sotillo-Galán Y, Varela-Fernández E, Gallardo-Bolaños JM, Muriel A, González-Fernández L, Tapia JA, Peña FJ. Detection of "apoptosis-like" changes during the cryopreservation process in equine sperm.. J Androl 2008 Mar-Apr;29(2):213-21.
    doi: 10.2164/jandrol.107.003640pubmed: 17978341google scholar: lookup
  28. Evenson DP, Darzynkiewicz Z, Melamed MR. Relation of mammalian sperm chromatin heterogeneity to fertility.. Science 1980 Dec 5;210(4474):1131-3.
    doi: 10.1126/science.7444440pubmed: 7444440google scholar: lookup
  29. Evenson DP. Sperm chromatin structure assay (SCSA®).. Methods Mol Biol 2013;927:147-64.
    doi: 10.1007/978-1-62703-038-0_14pubmed: 22992911google scholar: lookup
  30. Morrell JM, Johannisson A, Dalin AM, Hammar L, Sandebert T, Rodriguez-Martinez H. Sperm morphology and chromatin integrity in Swedish warmblood stallions and their relationship to pregnancy rates.. Acta Vet Scand 2008 Jan 7;50(1):2.
    doi: 10.1186/1751-0147-50-2pmc: PMC2246141pubmed: 18179691google scholar: lookup
  31. Chida J, Yamane K, Takei T, Kido H. An efficient extraction method for quantitation of adenosine triphosphate in mammalian tissues and cells.. Anal Chim Acta 2012 May 21;727:8-12.
    doi: 10.1016/j.aca.2012.03.022pubmed: 22541816google scholar: lookup
  32. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.. Anal Biochem 1976 May 7;72:248-54.
    doi: 10.1016/0003-2697(76)90527-3pubmed: 942051google scholar: lookup
  33. Luna C, Yeste M, Rivera Del Alamo MM, Domingo J, Casao A, Rodriguez-Gil JE, Pérez-Pé R, Cebrián-Pérez JA, Muiño-Blanco T. Effect of seminal plasma proteins on the motile sperm subpopulations in ram ejaculates.. Reprod Fertil Dev 2017 Feb;29(2):394-405.
    doi: 10.1071/RD15231pubmed: 26300553google scholar: lookup
  34. Abdel-Salam Z, Dessouki SH, Abdel-Salam SA, Ibrahim MA, Harith MA. Green laser irradiation effects on buffalo semen.. Theriogenology 2011 Apr 1;75(6):988-94.
  35. Salman Yazdi R, Bakhshi S, Jannat Alipoor F, Akhoond MR, Borhani S, Farrahi F, Lotfi Panah M, Sadighi Gilani MA. Effect of 830-nm diode laser irradiation on human sperm motility.. Lasers Med Sci 2014 Jan;29(1):97-104.
    doi: 10.1007/s10103-013-1276-7pubmed: 23407899google scholar: lookup
  36. Huang YY, Sharma SK, Carroll J, Hamblin MR. Biphasic dose response in low level light therapy - an update.. Dose Response 2011;9(4):602-18.
  37. Ban Frangez H, Frangez I, Verdenik I, Jansa V, Virant Klun I. Photobiomodulation with light-emitting diodes improves sperm motility in men with asthenozoospermia.. Lasers Med Sci 2015 Jan;30(1):235-40.
    doi: 10.1007/s10103-014-1653-xpubmed: 25204851google scholar: lookup
  38. Huang YY, Chen AC, Carroll JD, Hamblin MR. Biphasic dose response in low level light therapy.. Dose Response 2009 Sep 1;7(4):358-83.
  39. Lubart R, Lavi R, Friedmann H, Rochkind S. Photochemistry and photobiology of light absorption by living cells.. Photomed Laser Surg 2006 Apr;24(2):179-85.
    doi: 10.1089/pho.2006.24.179pubmed: 16706696google scholar: lookup
  40. Chow RT, Heller GZ, Barnsley L. The effect of 300 mW, 830 nm laser on chronic neck pain: a double-blind, randomized, placebo-controlled study.. Pain 2006 Sep;124(1-2):201-10.
    doi: 10.1016/j.pain.2006.05.018pubmed: 16806710google scholar: lookup
  41. Firestone RS, Esfandiari N, Moskovtsev SI, Burstein E, Videna GT, Librach C, Bentov Y, Casper RF. The effects of low-level laser light exposure on sperm motion characteristics and DNA damage.. J Androl 2012 May-Jun;33(3):469-73.
    doi: 10.2164/jandrol.111.013458pubmed: 21757512google scholar: lookup
  42. Lenzi A, Claroni F, Gandini L, Lombardo F, Barbieri C, Lino A, Dondero F. Laser radiation and motility patterns of human sperm.. Arch Androl 1989;23(3):229-34.
    doi: 10.3109/01485018908986845pubmed: 2694995google scholar: lookup
  43. Siqueira AF, Maria FS, Mendes CM, Hamilton TR, Dalmazzo A, Dreyer TR, da Silva HM, Nichi M, Milazzotto MP, Visintin JA, Assumpção ME. Effects of photobiomodulation therapy (PBMT) on bovine sperm function.. Lasers Med Sci 2016 Aug;31(6):1245-50.
    doi: 10.1007/s10103-016-1966-zpubmed: 27272676google scholar: lookup
  44. Sato H, Landthaler M, Haina D, Schill WB. The effects of laser light on sperm motility and velocity in vitro.. Andrologia 1984 Jan-Feb;16(1):23-5.
  45. Iaffaldano N, Paventi G, Pizzuto R, Di Iorio M, Bailey JL, Manchisi A, Passarella S. Helium-neon laser irradiation of cryopreserved ram sperm enhances cytochrome c oxidase activity and ATP levels improving semen quality.. Theriogenology 2016 Aug;86(3):778-84.
  46. Quintero-Moreno A, Miró J, Teresa Rigau A, Rodríguez-Gil JE. Identification of sperm subpopulations with specific motility characteristics in stallion ejaculates.. Theriogenology 2003 May;59(9):1973-90.
    doi: 10.1016/S0093-691X(02)01297-9pubmed: 12600734google scholar: lookup
  47. Miró J, Lobo V, Quintero-Moreno A, Medrano A, Peña A, Rigau T. Sperm motility patterns and metabolism in Catalonian donkey semen.. Theriogenology 2005 Apr 1;63(6):1706-16.
  48. Muiño R, Tamargo C, Hidalgo CO, Peña AI. Identification of sperm subpopulations with defined motility characteristics in ejaculates from Holstein bulls: effects of cryopreservation and between-bull variation.. Anim Reprod Sci 2008 Dec;109(1-4):27-39.
  49. Corredor L.H., Rodríguez O.C., Torres A.S., Páez J.D.M., Moreno A.Q.. Effects of cryopreservation on sperm subpopulations in goats.. Rev. Investig. Vet. Peru. 2018;29:882–893.
  50. Dorado J, Molina I, Muñoz-Serrano A, Hidalgo M. Identification of sperm subpopulations with defined motility characteristics in ejaculates from Florida goats.. Theriogenology 2010 Sep 15;74(5):795-804.
  51. Begum R, Powner MB, Hudson N, Hogg C, Jeffery G. Treatment with 670 nm light up regulates cytochrome C oxidase expression and reduces inflammation in an age-related macular degeneration model.. PLoS One 2013;8(2):e57828.
  52. Breitbart H, Levinshal T, Cohen N, Friedmann H, Lubart R. Changes in calcium transport in mammalian sperm mitochondria and plasma membrane irradiated at 633 nm (HeNe laser).. J Photochem Photobiol B 1996 Jul;34(2-3):117-21.
    doi: 10.1016/1011-1344(95)07281-0pubmed: 8810529google scholar: lookup
  53. Moscatelli N, Spagnolo B, Pisanello M, Lemma ED, De Vittorio M, Zara V, Pisanello F, Ferramosca A. Single-cell-based evaluation of sperm progressive motility via fluorescent assessment of mitochondria membrane potential.. Sci Rep 2017 Dec 20;7(1):17931.
    doi: 10.1038/s41598-017-18123-1pmc: PMC5738389pubmed: 29263401google scholar: lookup
  54. Meyers S, Bulkeley E, Foutouhi A. Sperm mitochondrial regulation in motility and fertility in horses.. Reprod Domest Anim 2019 Sep;54 Suppl 3:22-28.
    doi: 10.1111/rda.13461pubmed: 31512320google scholar: lookup
  55. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Walter P.. Molecular Biology of the Cell.. 4th ed. Garland Science; New York, NY, USA: 2002. Energy Conversion: Mitochondria and Chloroplasts; pp. 753–812.
  56. Zorova LD, Popkov VA, Plotnikov EY, Silachev DN, Pevzner IB, Jankauskas SS, Babenko VA, Zorov SD, Balakireva AV, Juhaszova M, Sollott SJ, Zorov DB. Mitochondrial membrane potential.. Anal Biochem 2018 Jul 1;552:50-59.
    doi: 10.1016/j.ab.2017.07.009pmc: PMC5792320pubmed: 28711444google scholar: lookup

Citations

This article has been cited 8 times.
  1. Blanco-Prieto O, Maside C, Àlex Peña, Ibáñez-Príncep J, Bonet S, Yeste M, Rodríguez-Gil JE. The effects of red LED light on pig sperm function rely upon mitochondrial electron chain activity rather than on a PKC-mediated mechanism. Front Cell Dev Biol 2022;10:930855.
    doi: 10.3389/fcell.2022.930855pubmed: 36274839google scholar: lookup
  2. Starovlah IM, Radovic Pletikosic SM, Tomanic TM, Medar MLJ, Kostic TS, Andric SA. Spermatozoal Mitochondrial Dynamics Markers and Other Functionality-Related Signaling Molecules Exert Circadian-like Response to Repeated Stress of Whole Organism. Cells 2022 Mar 15;11(6).
    doi: 10.3390/cells11060993pubmed: 35326444google scholar: lookup
  3. Yánez-Ortiz I, Catalán J, Mateo-Otero Y, Dordas-Perpinyà M, Gacem S, Yeste N, Bassols A, Yeste M, Miró J. Extracellular Reactive Oxygen Species (ROS) Production in Fresh Donkey Sperm Exposed to Reductive Stress, Oxidative Stress and NETosis. Antioxidants (Basel) 2021 Aug 27;10(9).
    doi: 10.3390/antiox10091367pubmed: 34572999google scholar: lookup
  4. Miró J, Catalán J, Marín H, Yánez-Ortiz I, Yeste M. Specific Seminal Plasma Fractions Are Responsible for the Modulation of Sperm-PMN Binding in the Donkey. Animals (Basel) 2021 May 13;11(5).
    doi: 10.3390/ani11051388pubmed: 34068214google scholar: lookup
  5. Catalán J, Yánez-Ortiz I, Gacem S, Papas M, Bonet S, Rodríguez-Gil JE, Yeste M, Miró J. The Effects of Red Light on Mammalian Sperm Rely upon the Color of the Straw and the Medium Used. Animals (Basel) 2021 Jan 8;11(1).
    doi: 10.3390/ani11010122pubmed: 33429933google scholar: lookup
  6. Catalán J, Papas M, Trujillo-Rojas L, Blanco-Prieto O, Bonilla-Correal S, Rodríguez-Gil JE, Miró J, Yeste M. Red LED Light Acts on the Mitochondrial Electron Chain of Donkey Sperm and Its Effects Depend on the Time of Exposure to Light. Front Cell Dev Biol 2020;8:588621.
    doi: 10.3389/fcell.2020.588621pubmed: 33365309google scholar: lookup
  7. Blanco-Prieto O, Maside C, Gruzmacher A, Ortiz M, Ratto M, Urra FJ, Vera T, Strobel P, Catalán J, Mislei B, Bucci D, Yeste M, Rodríguez-Gil JE, Ramírez-Reveco A. Red LED Light Irradiation Increases the Resistance Against Environmental Stress of Frozen Bovine Sperm Thawed in Suboptimal Conditions. Animals (Basel) 2025 Nov 20;15(22).
    doi: 10.3390/ani15223353pubmed: 41302061google scholar: lookup
  8. Dordas-Perpinyà M, Yánez-Ortiz I, Sergeant N, Mevel V, Catalán J, Bruyas JF, Miró J, Briand-Amirat L. ProAKAP4 as Indicator of Long-Lasting Motility Marker in Post-Thaw Conditions in Stallions. Animals (Basel) 2024 Apr 23;14(9).
    doi: 10.3390/ani14091264pubmed: 38731267google scholar: lookup