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Home / Equine Research Bank / Biology (Basel) / Cryotolerance of Stallion Spermatozoa Relies on Aquaglycerop...
Biology2019; 8(4); 85; doi: 10.3390/biology8040085

Cryotolerance of Stallion Spermatozoa Relies on Aquaglyceroporins rather than Orthodox Aquaporins.

Abstract: Aquaporins (AQPs), a family of ubiquitous water channels divided into orthodox AQPs, aquaglyceroporins (GLPs), and superAQPs, are present in stallion spermatozoa. The aim of this study was to elucidate the functional relevance of each group of AQPs during stallion sperm cryopreservation through the use of three different inhibitors: acetazolamide (AC), phloretin (PHL) and propanediol (PDO). Sperm quality and function parameters were evaluated in the presence or absence of each inhibitor in fresh and frozen-thawed samples. In the presence of AC, different parameters were altered ( < 0.05), but not in a concentration- or time-depending manner. PHL was found to decrease sperm motility, viability, acrosome integrity, and the percentages of spermatozoa with low membrane lipid disorder, high mitochondrial membrane potential (MMP) and high intracellular levels of calcium and superoxides ( < 0.05). Finally, the sperm motility, viability, acrosome integrity, the percentages of spermatozoa with low membrane lipid disorder, high MMP and high intracellular calcium levels were higher ( < 0.05) in PDO treatments than in the control. The sperm response to AC, PHL and PDO indicates that GLPs, rather than orthodox AQPs, play a crucial role during stallion sperm cryopreservation. Furthermore, post-thaw sperm quality was higher in PDO treatments than in the control, suggesting that this molecule is a potential permeable cryoprotectant.
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Publication Date: 2019-11-12 PubMed ID: 31726707PubMed Central: PMC6955868DOI: 10.3390/biology8040085Google Scholar: Lookup
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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.

This research article investigates the role of aquaglyceroporins (GLPs), a kind of water channel found in stallion spermatozoa, during cryopreservation, the process of freezing and preserving. The researchers discovered that GLPs contribute more significantly to the success of this process than orthodox aquaporins.

Overview of Research Methodology

  • The researchers studied the function of different types of aquaporins in stallion sperm during the process of cryopreservation. The types of aquaporins considered include orthodox aquaporins, aquaglyceroporins (GLPs), and super aquaporins.
  • The functionality of the aquaporins was tested through the application of three different inhibitors: acetazolamide (AC), phloretin (PHL), and propanediol (PDO).
  • Parameters of sperm quality and function were evaluated both in the presence and absence of each inhibitor in fresh and frozen-thawed samples.

Main Findings

  • The application of acetazolamide affected several parameters but this did not occur in a consistent concentration- or time-dependent manner.
  • Phloretin was found to reduce sperm motility, viability, acrosome integrity, and the percentages of spermatozoa with low membrane lipid disorder, high mitochondrial membrane potential and high internal levels of calcium and superoxides.
  • Propanediol treatments resulted in improved sperm motility, viability, acrosome integrity, and the percentages of spermatozoa with low membrane lipid disorder, high mitochondrial membrane potential and high intracellular calcium levels compared to the control treatments.

Key Conclusions

  • The reaction of spermatozoa to the three inhibitors indicates that GLPs have a more crucial role in the cryopreservation of stallion sperm than orthodox aquaporins.
  • The quality of post-thaw sperm was better in the propanediol treatments than in the control, hinting that this molecule is a potentially effective cryoprotectant.

Cite This Article

APA
Delgado-Bermúdez A, Noto F, Bonilla-Correal S, Garcia-Bonavila E, Catalán J, Papas M, Bonet S, Miró J, Yeste M. (2019). Cryotolerance of Stallion Spermatozoa Relies on Aquaglyceroporins rather than Orthodox Aquaporins. Biology (Basel), 8(4), 85. https://doi.org/10.3390/biology8040085

Publication

Biology
ISSN: 2079-7737
NlmUniqueID: 101587988
Country: Switzerland
Language: English
Volume: 8
Issue: 4
PII: 85

Researcher Affiliations

Delgado-Bermúdez, Ariadna
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Unit of Cell Biology, Department of Biology, Institute of Food and Agricultural Technology, Faculty of Sciences, University of Girona, 17003 Girona, Spain.
Noto, Federico
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Unit of Cell Biology, Department of Biology, Institute of Food and Agricultural Technology, Faculty of Sciences, University of Girona, 17003 Girona, Spain.
Bonilla-Correal, Sebastián
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, 08193 Bellaterra (Cerdanyola del Vallès), Spain.
Garcia-Bonavila, Estela
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Unit of Cell Biology, Department of Biology, Institute of Food and Agricultural Technology, Faculty of Sciences, University of Girona, 17003 Girona, Spain.
Catalán, Jaime
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, 08193 Bellaterra (Cerdanyola del Vallès), Spain.
Papas, Marion
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, 08193 Bellaterra (Cerdanyola del Vallès), Spain.
Bonet, Sergi
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Unit of Cell Biology, Department of Biology, Institute of Food and Agricultural Technology, Faculty of Sciences, University of Girona, 17003 Girona, Spain.
Miró, Jordi
  • Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, 08193 Bellaterra (Cerdanyola del Vallès), Spain.
Yeste, Marc
  • Biotechnology of Animal and Human Reproduction (TechnoSperm), Unit of Cell Biology, Department of Biology, Institute of Food and Agricultural Technology, Faculty of Sciences, University of Girona, 17003 Girona, Spain.

Grant Funding

  • AGL2017-88329-R / Ministerio de Ciencia, Innovaciu00f3n y Universidades
  • RYC-2014-15581 / Ministerio de Ciencia, Innovaciu00f3n y Universidades
  • PRE2018-083488 / Ministerio de Ciencia, Innovaciu00f3n y Universidades
  • 2017-SGR-1229 / Agu00e8ncia de Gestiu00f3 d'Ajuts Universitaris i de Recerca

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 57 references
  1. Watson H. Biological membranes.. Essays Biochem 2015;59:43-69.
    doi: 10.1042/bse0590043pmc: PMC4626904pubmed: 26504250google scholar: lookup
  2. Yeste M, Morató R, Rodríguez-Gil JE, Bonet S, Prieto-Martínez N. Aquaporins in the male reproductive tract and sperm: Functional implications and cryobiology.. Reprod Domest Anim 2017 Oct;52 Suppl 4:12-27.
    doi: 10.1111/rda.13082pubmed: 29052330google scholar: lookup
  3. Feugang JM, Liao SF, Willard ST, Ryan PL. In-depth proteomic analysis of boar spermatozoa through shotgun and gel-based methods.. BMC Genomics 2018 Jan 18;19(1):62.
    doi: 10.1186/s12864-018-4442-2pmc: PMC5774113pubmed: 29347914google scholar: lookup
  4. Bonilla-Correal S, Noto F, Garcia-Bonavila E, Rodríguez-Gil JE, Yeste M, Miro J. First evidence for the presence of aquaporins in stallion sperm.. Reprod Domest Anim 2017 Oct;52 Suppl 4:61-64.
    doi: 10.1111/rda.13059pubmed: 29052325google scholar: lookup
  5. Prieto-Martínez N, Vilagran I, Morató R, Rodríguez-Gil JE, Yeste M, Bonet S. Aquaporins 7 and 11 in boar spermatozoa: detection, localisation and relationship with sperm quality.. Reprod Fertil Dev 2016 Apr;28(6):663-72.
    doi: 10.1071/RD14237pubmed: 25482725google scholar: lookup
  6. Prieto-Martínez N, Morató R, Vilagran I, Rodríguez-Gil JE, Bonet S, Yeste M. Aquaporins in boar spermatozoa. Part II: detection and localisation of aquaglyceroporin 3.. Reprod Fertil Dev 2017 Apr;29(4):703-711.
    doi: 10.1071/RD15164pubmed: 26677911google scholar: lookup
  7. Chen Q, Peng H, Lei L, Zhang Y, Kuang H, Cao Y, Shi QX, Ma T, Duan E. Aquaporin3 is a sperm water channel essential for postcopulatory sperm osmoadaptation and migration.. Cell Res 2011 Jun;21(6):922-33.
    doi: 10.1038/cr.2010.169pmc: PMC3343308pubmed: 21135872google scholar: lookup
  8. Yeung CH, Callies C, Rojek A, Nielsen S, Cooper TG. Aquaporin isoforms involved in physiological volume regulation of murine spermatozoa.. Biol Reprod 2009 Feb;80(2):350-7.
    doi: 10.1095/biolreprod.108.071928pubmed: 18829704google scholar: lookup
  9. Yeung CH, Cooper TG. Aquaporin AQP11 in the testis: molecular identity and association with the processing of residual cytoplasm of elongated spermatids.. Reproduction 2010 Jan;139(1):209-16.
    doi: 10.1530/REP-09-0298pubmed: 19812234google scholar: lookup
  10. Yeung CH, Callies C, Tüttelmann F, Kliesch S, Cooper TG. Aquaporins in the human testis and spermatozoa - identification, involvement in sperm volume regulation and clinical relevance.. Int J Androl 2010 Aug 1;33(4):629-41.
    doi: 10.1111/j.1365-2605.2009.00998.xpubmed: 19840149google scholar: lookup
  11. Laforenza U, Pellavio G, Marchetti AL, Omes C, Todaro F, Gastaldi G. Aquaporin-Mediated Water and Hydrogen Peroxide Transport Is Involved in Normal Human Spermatozoa Functioning.. Int J Mol Sci 2016 Dec 30;18(1).
    doi: 10.3390/ijms18010066pmc: PMC5297701pubmed: 28042826google scholar: lookup
  12. Prieto-Martínez N, Morató R, Muiño R, Hidalgo CO, Rodríguez-Gil JE, Bonet S, Yeste M. Aquaglyceroporins 3 and 7 in bull spermatozoa: identification, localisation and their relationship with sperm cryotolerance.. Reprod Fertil Dev 2017 Jun;29(6):1249-1259.
    doi: 10.1071/RD16077pubmed: 27221122google scholar: lookup
  13. Morató R, Prieto-Martínez N, Muiño R, Hidalgo CO, Rodríguez-Gil JE, Bonet S, Yeste M. Aquaporin 11 is related to cryotolerance and fertilising ability of frozen-thawed bull spermatozoa.. Reprod Fertil Dev 2018 Jul;30(8):1099-1108.
    doi: 10.1071/RD17340pubmed: 29365310google scholar: lookup
  14. Vicente-Carrillo A, Ekwall H, Álvarez-Rodríguez M, Rodríguez-Martínez H. Membrane Stress During Thawing Elicits Redistribution of Aquaporin 7 But Not of Aquaporin 9 in Boar Spermatozoa.. Reprod Domest Anim 2016 Oct;51(5):665-79.
    doi: 10.1111/rda.12728pubmed: 27405395google scholar: lookup
  15. Huang HF, He RH, Sun CC, Zhang Y, Meng QX, Ma YY. Function of aquaporins in female and male reproductive systems.. Hum Reprod Update 2006 Nov-Dec;12(6):785-95.
    doi: 10.1093/humupd/dml035pubmed: 16840793google scholar: lookup
  16. Peña FJ, García BM, Samper JC, Aparicio IM, Tapia JA, Ferrusola CO. Dissecting the molecular damage to stallion spermatozoa: the way to improve current cryopreservation protocols?. Theriogenology 2011 Oct 15;76(7):1177-86.
    doi: 10.1016/j.theriogenology.2011.06.023pubmed: 21835453google scholar: lookup
  17. Ball BA, Vo AT, Baumber J. Generation of reactive oxygen species by equine spermatozoa.. Am J Vet Res 2001 Apr;62(4):508-15.
    doi: 10.2460/ajvr.2001.62.508pubmed: 11327456google scholar: lookup
  18. Sieme H, Harrison RA, Petrunkina AM. Cryobiological determinants of frozen semen quality, with special reference to stallion.. Anim Reprod Sci 2008 Sep;107(3-4):276-92.
    doi: 10.1016/j.anireprosci.2008.05.001pubmed: 18585878google scholar: lookup
  19. Casas I, Sancho S, Briz M, Pinart E, Bussalleu E, Yeste M, Bonet S. Freezability prediction of boar ejaculates assessed by functional sperm parameters and sperm proteins.. Theriogenology 2009 Oct 15;72(7):930-48.
    doi: 10.1016/j.theriogenology.2009.07.001pubmed: 19651432google scholar: lookup
  20. Yeste M, Estrada E, Casas I, Bonet S, Rodríguez-Gil JE. Good and bad freezability boar ejaculates differ in the integrity of nucleoprotein structure after freeze-thawing but not in ROS levels.. Theriogenology 2013 Apr 1;79(6):929-39.
    doi: 10.1016/j.theriogenology.2013.01.008pubmed: 23398739google scholar: lookup
  21. Yeste M, Estrada E, Pinart E, Bonet S, Miró J, Rodríguez-Gil JE. The improving effect of reduced glutathione on boar sperm cryotolerance is related with the intrinsic ejaculate freezability.. Cryobiology 2014 Apr;68(2):251-61.
    doi: 10.1016/j.cryobiol.2014.02.004pubmed: 24530509google scholar: lookup
  22. Kuisma P, Andersson M, Koskinen E, Katila T. Fertility of frozen-thawed stallion semen cannot be predicted by the currently used laboratory methods.. Acta Vet Scand 2006 Aug 17;48(1):14.
    doi: 10.1186/1751-0147-48-14pmc: PMC1564023pubmed: 16987393google scholar: lookup
  23. Yeste M, Estrada E, Rocha LG, Marín H, Rodríguez-Gil JE, Miró J. Cryotolerance of stallion spermatozoa is related to ROS production and mitochondrial membrane potential rather than to the integrity of sperm nucleus.. Andrology 2015 Mar;3(2):395-407.
    doi: 10.1111/andr.291pubmed: 25294093google scholar: lookup
  24. Katila T. In vitro evaluation of frozen-thawed stallion semen: a review.. Acta Vet Scand 2001;42(2):199-217.
    doi: 10.1186/1751-0147-42-199pmc: PMC2202319pubmed: 11503365google scholar: lookup
  25. Macías García B, Morrell JM, Ortega-Ferrusola C, González-Fernández L, Tapia JA, Rodriguez-Martínez H, Peña FJ. Centrifugation on a single layer of colloid selects improved quality spermatozoa from frozen-thawed stallion semen.. Anim Reprod Sci 2009 Aug;114(1-3):193-202.
    doi: 10.1016/j.anireprosci.2008.08.025pubmed: 18842364google scholar: lookup
  26. Prieto-Martínez N, Mateo E, Puig-Timonet A, Rodríguez-Gil JE, Bonet S, Morató R, Yeste M. Aquaporins 3 and 7 as cryotolerance markers in boar semen.. Reprod. Domest. Anim. 2016;51(Suppl. 2):132.
  27. Delgado-Bermúdez A, Llavanera M, Fernández-Bastit L, Recuero S, Mateo-Otero Y, Bonet S, Barranco I, Fernández-Fuertes B, Yeste M. Aquaglyceroporins but not orthodox aquaporins are involved in the cryotolerance of pig spermatozoa.. J Anim Sci Biotechnol 2019;10:77.
    doi: 10.1186/s40104-019-0388-8pmc: PMC6791021pubmed: 31636902google scholar: lookup
  28. Prieto-Martínez N, Vilagran I, Morató R, Rivera Del Álamo MM, Rodríguez-Gil JE, Bonet S, Yeste M. Relationship of aquaporins 3 (AQP3), 7 (AQP7), and 11 (AQP11) with boar sperm resilience to withstand freeze-thawing procedures.. Andrology 2017 Nov;5(6):1153-1164.
    doi: 10.1111/andr.12410pubmed: 28941027google scholar: lookup
  29. Kenney RM, Bergman RV, Cooper WL, Morse FW. Minimal contamination techniques for breeding mares: Techniques and preliminary findings.. Proc. Am. Assoc. Equine Pract. 1975;21:327–336.
  30. 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.
    doi: 10.1016/j.theriogenology.2009.12.006pubmed: 20171719google scholar: lookup
  31. 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
  32. Nagy S, Jansen J, Topper EK, Gadella BM. A triple-stain flow cytometric method to assess plasma- and acrosome-membrane integrity of cryopreserved bovine sperm immediately after thawing in presence of egg-yolk particles.. Biol Reprod 2003 May;68(5):1828-35.
    doi: 10.1095/biolreprod.102.011445pubmed: 12606354google scholar: lookup
  33. Rathi R, Colenbrander B, Bevers MM, Gadella BM. Evaluation of in vitro capacitation of stallion spermatozoa.. Biol Reprod 2001 Aug;65(2):462-70.
    doi: 10.1095/biolreprod65.2.462pubmed: 11466214google scholar: lookup
  34. Yeste M, Estrada E, Rivera Del Álamo MM, Bonet S, Rigau T, Rodríguez-Gil JE. The increase in phosphorylation levels of serine residues of protein HSP70 during holding time at 17°C is concomitant with a higher cryotolerance of boar spermatozoa.. PLoS One 2014;9(3):e90887.
    doi: 10.1371/journal.pone.0090887pmc: PMC3946327pubmed: 24603527google scholar: lookup
  35. 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
  36. Yeste M, Fernández-Novell JM, Ramió-Lluch L, Estrada E, Rocha LG, Cebrián-Pérez JA, Muiño-Blanco T, Concha II, Ramírez A, Rodríguez-Gil JE. Intracellular calcium movements of boar spermatozoa during 'in vitro' capacitation and subsequent acrosome exocytosis follow a multiple-storage place, extracellular calcium-dependent model.. Andrology 2015 Jul;3(4):729-47.
    doi: 10.1111/andr.12054pubmed: 26097097google scholar: lookup
  37. Harrison RA, Mairet B, Miller NG. Flow cytometric studies of bicarbonate-mediated Ca2+ influx in boar sperm populations.. Mol Reprod Dev 1993 Jun;35(2):197-208.
    doi: 10.1002/mrd.1080350214pubmed: 8391278google scholar: lookup
  38. Kadirvel G, Kumar S, Kumaresan A, Kathiravan P. Capacitation status of fresh and frozen-thawed buffalo spermatozoa in relation to cholesterol level, membrane fluidity and intracellular calcium.. Anim Reprod Sci 2009 Dec;116(3-4):244-53.
    doi: 10.1016/j.anireprosci.2009.02.003pubmed: 19261396google scholar: lookup
  39. Guthrie HD, Welch GR. Determination of intracellular reactive oxygen species and high mitochondrial membrane potential in Percoll-treated viable boar sperm using fluorescence-activated flow cytometry.. J Anim Sci 2006 Aug;84(8):2089-100.
    doi: 10.2527/jas.2005-766pubmed: 16864869google scholar: lookup
  40. Gao J, Wang X, Chang Y, Zhang J, Song Q, Yu H, Li X. Acetazolamide inhibits osmotic water permeability by interaction with aquaporin-1.. Anal Biochem 2006 Mar 15;350(2):165-70.
    doi: 10.1016/j.ab.2006.01.003pubmed: 16480680google scholar: lookup
  41. Tanimura Y, Hiroaki Y, Fujiyoshi Y. Acetazolamide reversibly inhibits water conduction by aquaporin-4.. J Struct Biol 2009 Apr;166(1):16-21.
    doi: 10.1016/j.jsb.2008.11.010pubmed: 19114109google scholar: lookup
  42. Rezk BM, Haenen GR, van der Vijgh WJ, Bast A. The antioxidant activity of phloretin: the disclosure of a new antioxidant pharmacophore in flavonoids.. Biochem Biophys Res Commun 2002 Jul 5;295(1):9-13.
    doi: 10.1016/S0006-291X(02)00618-6pubmed: 12083758google scholar: lookup
  43. Barreca D, Currò M, Bellocco E, Ficarra S, Laganà G, Tellone E, Laura Giunta M, Visalli G, Caccamo D, Galtieri A, Ientile R. Neuroprotective effects of phloretin and its glycosylated derivative on rotenone-induced toxicity in human SH-SY5Y neuronal-like cells.. Biofactors 2017 Jul 8;43(4):549-557.
    doi: 10.1002/biof.1358pubmed: 28401997google scholar: lookup
  44. Przybylo M, Procek J, Hof M, Langner M. The alteration of lipid bilayer dynamics by phloretin and 6-ketocholestanol.. Chem Phys Lipids 2014 Feb;178:38-44.
    doi: 10.1016/j.chemphyslip.2013.11.005pubmed: 24316311google scholar: lookup
  45. Yu L, Rodriguez RA, Chen LL, Chen LY, Perry G, McHardy SF, Yeh CK. 1,3-propanediol binds deep inside the channel to inhibit water permeation through aquaporins.. Protein Sci 2016 Feb;25(2):433-41.
    doi: 10.1002/pro.2832pmc: PMC4815352pubmed: 26481430google scholar: lookup
  46. Yu L, Villarreal OD, Chen LL, Chen LY. 1,3-Propanediol binds inside the water-conducting pore of aquaporin 4: Does this efficacious inhibitor have sufficient potency?. J Syst Integr Neurosci 2016;2(1):91-98.
    doi: 10.15761/JSIN.1000117pmc: PMC4873003pubmed: 27213050google scholar: lookup
  47. Jakobsen E, Lange SC, Andersen JV, Desler C, Kihl HF, Hohnholt MC, Stridh MH, Rasmussen LJ, Waagepetersen HS, Bak LK. The inhibitors of soluble adenylate cyclase 2-OHE, KH7, and bithionol compromise mitochondrial ATP production by distinct mechanisms.. Biochem Pharmacol 2018 Sep;155:92-101.
    doi: 10.1016/j.bcp.2018.06.023pubmed: 29940175google scholar: lookup
  48. Lark DS, Reese LR, Ryan TE, Torres MJ, Smith CD, Lin CT, Neufer PD. Protein Kinase A Governs Oxidative Phosphorylation Kinetics and Oxidant Emitting Potential at Complex I.. Front Physiol 2015;6:332.
    doi: 10.3389/fphys.2015.00332pmc: PMC4646981pubmed: 26635618google scholar: lookup
  49. Nishigaki T, José O, González-Cota AL, Romero F, Treviño CL, Darszon A. Intracellular pH in sperm physiology.. Biochem Biophys Res Commun 2014 Aug 1;450(3):1149-58.
    doi: 10.1016/j.bbrc.2014.05.100pmc: PMC4146485pubmed: 24887564google scholar: lookup
  50. Yeste M. Sperm cryopreservation update: Cryodamage, markers, and factors affecting the sperm freezability in pigs.. Theriogenology 2016 Jan 1;85(1):47-64.
    doi: 10.1016/j.theriogenology.2015.09.047pubmed: 26506124google scholar: lookup
  51. Pohl P, Rokitskaya TI, Pohl EE, Saparov SM. Permeation of phloretin across bilayer lipid membranes monitored by dipole potential and microelectrode measurements.. Biochim Biophys Acta 1997 Jan 31;1323(2):163-72.
    doi: 10.1016/S0005-2736(96)00185-Xpubmed: 9042340google scholar: lookup
  52. Wacker SJ, Aponte-Santamaría C, Kjellbom P, Nielsen S, de Groot BL, Rützler M. The identification of novel, high affinity AQP9 inhibitors in an intracellular binding site.. Mol Membr Biol 2013 May;30(3):246-60.
    doi: 10.3109/09687688.2013.773095pubmed: 23448163google scholar: lookup
  53. Miller EW, Dickinson BC, Chang CJ. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling.. Proc Natl Acad Sci U S A 2010 Sep 7;107(36):15681-6.
    doi: 10.1073/pnas.1005776107pmc: PMC2936599pubmed: 20724658google scholar: lookup
  54. Cooper TG, Barfield JP, Yeung CH. The tonicity of murine epididymal spermatozoa and their permeability towards common cryoprotectants and epididymal osmolytes.. Reproduction 2008 May;135(5):625-33.
    doi: 10.1530/REP-07-0573pubmed: 18304983google scholar: lookup
  55. Widiasih D, Yeung CH, Junaidi A, Cooper TG. Multistep and single-step treatment of human spermatozoa with cryoprotectants.. Fertil Steril 2009 Jul;92(1):382-9.
    doi: 10.1016/j.fertnstert.2008.05.046pubmed: 19409545google scholar: lookup
  56. Lopes CA, Alves AM, Jewgenow K, Báo SN, de Figueiredo JR. Cryopreservation of canine ovarian cortex using DMSO or 1,3-propanediol.. Theriogenology 2016 Sep 15;86(5):1165-74.
    doi: 10.1016/j.theriogenology.2016.04.006pubmed: 27160447google scholar: lookup
  57. Pogozhykh D, Prokopyuk V, Pogozhykh O, Mueller T, Prokopyuk O. Influence of Factors of Cryopreservation and Hypothermic Storage on Survival and Functional Parameters of Multipotent Stromal Cells of Placental Origin.. PLoS One 2015;10(10):e0139834.
    doi: 10.1371/journal.pone.0139834pmc: PMC4592233pubmed: 26431528google scholar: lookup

Citations

This article has been cited 9 times.
  1. Ďuračka M, Benko F, Tvrdá E. Molecular Markers: A New Paradigm in the Prediction of Sperm Freezability. Int J Mol Sci 2023 Feb 8;24(4).
    doi: 10.3390/ijms24043379pubmed: 36834790google scholar: lookup
  2. Delgado-Bermúdez A, Ribas-Maynou J, Yeste M. Relevance of Aquaporins for Gamete Function and Cryopreservation. Animals (Basel) 2022 Feb 24;12(5).
    doi: 10.3390/ani12050573pubmed: 35268142google scholar: lookup
  3. Ribeiro JC, Carrageta DF, Bernardino RL, Alves MG, Oliveira PF. Aquaporins and Animal Gamete Cryopreservation: Advances and Future Challenges. Animals (Basel) 2022 Feb 2;12(3).
    doi: 10.3390/ani12030359pubmed: 35158682google scholar: lookup
  4. Rodriguez RA, Chan R, Liang H, Chen LY. Quantitative study of unsaturated transport of glycerol through aquaglyceroporin that has high affinity for glycerol. RSC Adv 2020;10(56):34203-34214.
    doi: 10.1039/d0ra05262kpubmed: 32944226google scholar: lookup
  5. Chan R, Falato M, Liang H, Chen LY. In silico simulations of erythrocyte aquaporins with quantitative in vitro validation. RSC Adv 2020;10(36):21283-21291.
    doi: 10.1039/d0ra03456hpubmed: 32612811google scholar: lookup
  6. Delgado-Bermúdez A, Llavanera M, Recuero S, Mateo-Otero Y, Bonet S, Barranco I, Fernandez-Fuertes B, Yeste M. Effect of AQP Inhibition on Boar Sperm Cryotolerance Depends on the Intrinsic Freezability of the Ejaculate. Int J Mol Sci 2019 Dec 11;20(24).
    doi: 10.3390/ijms20246255pubmed: 31835821google scholar: lookup
  7. Wang J, Li R, Huang F, Niu P, Zheng Y, Yuan D, Du Y, Li C, Yang M, Suo J, Gao Q. Comparative analysis of AQP7 expression and cryotolerance in X- and Y-chromosome bearing bovine sperm. Front Cell Dev Biol 2025;13:1582961.
    doi: 10.3389/fcell.2025.1582961pubmed: 40454315google scholar: lookup
  8. Casao A, Miguel-Jimenez S, Pérez-Pe R. Sperm Intracellular Calcium Evaluation. Methods Mol Biol 2025;2897:341-352.
    doi: 10.1007/978-1-0716-4406-5_24pubmed: 40202647google scholar: lookup
  9. Suo J, Wang J, Zheng Y, Xiao F, Li R, Huang F, Niu P, Zhu W, Du X, He J, Gao Q, Khan A. Recent advances in cryotolerance biomarkers for semen preservation in frozen form-A systematic review. PLoS One 2024;19(5):e0303567.
    doi: 10.1371/journal.pone.0303567pubmed: 38776323google scholar: lookup
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