Evaluation of carp sperm respiration: fluorometry with optochemical oxygen sensor versus polarography
Jazyk angličtina Země Nizozemsko Médium print-electronic
Typ dokumentu časopisecké články
PubMed
39630387
PubMed Central
PMC11618158
DOI
10.1007/s10695-024-01418-2
PII: 10.1007/s10695-024-01418-2
Knihovny.cz E-zdroje
- Klíčová slova
- Clark-type electrode, Common carp, Optochemical oxygen sensor, Oxygen consumption rate, Sperm motility, Spermatozoa,
- MeSH
- buněčné dýchání fyziologie MeSH
- fluorometrie * metody veterinární přístrojové vybavení MeSH
- kapři * fyziologie metabolismus MeSH
- kyslík metabolismus MeSH
- motilita spermií fyziologie MeSH
- polarografie * metody přístrojové vybavení veterinární MeSH
- spermie * fyziologie MeSH
- spotřeba kyslíku * fyziologie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- kyslík MeSH
The primary function of spermatozoa is to fertilize the oocyte, which depends on their motility and is directly associated with their metabolic state. The oxygen consumption rate (OCR) of spermatozoa reflects the respiratory capacity of sperm mitochondria under various physiological conditions and is an essential marker of sperm quality. We determined the OCR of common carp (Cyprinus carpio) sperm using two respirometry methods: the conventionally used polarographic method with a Clark-type electrode and fluorometric assay with an Oxo Dish optochemical oxygen sensor. The latter was used for the first time to evaluate spermatozoa oxygen consumption in various metabolic states (under different treatments) at different dilution rates. These two methods were compared using Bland-Altman analysis, and the applicability of the optochemical oxygen sensor for evaluating carp sperm oxygen consumption was discussed. Sperm motility and progressive velocity parameters were also assessed to evaluate the effect of sperm respiration under different metabolic states and dilution rates and preincubation period on the physiological status of spermatozoa. The comparison of these respirometry methods clearly shows that while the polarographic method allows immediate measurement of oxygen levels after adding a sperm sample, the optochemical oxygen sensor has a priority in the amount of data obtained due to simultaneous measurements of several samples (e.g., different males, different fish species, repetitions of the same sample or various experimental conditions), even at a later time after adding sperm to the measuring chamber. However, the compared methods are complementary, and the proposed methodology can be applied to other fish species.
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Alavi SMH, Cosson J, Karami M, Mojazi Amiri B, Akhoundzadeh MA (2004) Spermatozoa motility in the Persian sturgeon, Acipenser persicus: effects of pH, dilution rate, ions and osmolality. Reproduction 128(6):819–828. 10.1530/rep.1.00244 PubMed
Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1(8476):307–310. 10.1016/S0140-6736(86)90837-8 PubMed
Bland JM, Altman DG (2003) Applying the right statistics: analyses of measurement studies. Ultrasound Obstet Gynecol 22(1):85–93. 10.1002/uog.122 PubMed
Boryshpolets S, Dzyuba B, Drokin S (2009a) Pre-spawning water temperature affects sperm respiration and reactivation parameters in male carps. Fish Physiol Biochem 35(4):661–668. 10.1007/s10695-008-9292-4 PubMed
Boryshpolets S, Dzyuba B, Rodina M, Li P, Hulak M, Gela D, Linhart O (2009b) Freeze-thawing as the factor of spontaneous activation of spermatozoa motility in common carp (Cyprinus carpio L.). Cryobiology 59(3): 291–296. 10.1016/j.cryobiol.2009.08.005 PubMed
Cejko BI, Żarski D, Sarosiek B, Dryl K, Palińska-Żarska K, Skorupa W, Kowalski RK (2022) Application of artificial seminal plasma to short-term storage of a large volume of common carp (Cyprinus carpio) sperm for two weeks under controlled conditions. Aquaculture 546:737385. 10.1016/j.aquaculture.2021.737385
Chang SC, Stetter JR, Cha CS (1993) Amperometric gas sensors. Talanta 40(4):461–477. 10.1016/0039-9140(93)80002-9 PubMed
Cosson J (2019) Fish sperm physiology: structure, factors regulating motility, and motility evaluation. In: Bozkurt Y (ed) Biological research in aquatic science. Intech Open. 10.5772/intechopen.85139
Darr CR, Cortopassi GA, Datta S, Varner DD, Meyers SA (2016) Mitochondrial oxygen consumption is a unique indicator of stallion spermatozoal health and varies with cryopreservation media. Theriogenology 86(5):1382–1392. 10.1016/j.theriogenology.2016.04.082 PubMed
Darr CR, Moraes LE, Scanlan TN, Baumber-Skaife J, Loomis PR, Cortopassi GA, Meyers SA (2017) Sperm mitochondrial function is affected by stallion age and predicts post-thaw motility. J Equine Vet 50:52–61. 10.1016/j.jevs.2016.10.015
Dietrich MA, Nynca J, Ciereszko A (2019) Proteomic and metabolomic insights into the functions of the male reproductive system in fishes. Theriogenology 132:182–200. 10.1016/j.theriogenology.2019.04.018 PubMed
Dzyuba B, Bondarenko O, Fedorov P, Gazo I, Prokopchuk G, Cosson J (2017) Energetics of fish spermatozoa: the proven and the possible. Aquaculture 472:60–72. 10.1016/j.aquaculture.2016.05.038
Dzyuba V, Dzyuba B, Cosson J, Rodina M (2016) Enzyme activity in energy supply of spermatozoon motility in two taxonomically distant fish species (sterlet Acipenser ruthenus, Acipenseriformes and common carp Cyprinus carpio, Cypriniformes). Theriogenology 85(4):567–574. 10.1016/j.theriogenology.2015.09.040 PubMed
Figueroa E, Valdebenito I, Zepeda AB, Figueroa CA, Dumorné K, Castillo RL, Farias JG (2017) Effects of cryopreservation on mitochondria of fish spermatozoa. Rev Aquac 9(1):76–87. 10.1111/raq.12105
Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14(1):44–47. 10.1016/j.cub.2003.12.028 PubMed
Gouspillou G, Rouland R, Calmettes G, Deschodt-Arsac V, Franconi JM, Bourdel-Marchasson I, Diolez P (2011) Accurate determination of the oxidative phosphorylation affinity for ADP in isolated mitochondria. PLoS ONE 6(6):e20709. 10.1371/journal.pone.0020709 PubMed PMC
Gronczewska J, Niedźwiecka N, Grzyb K, Skorkowski EF (2019) Bioenergetics of fish spermatozoa with focus on some herring (Clupea harengus) enzymes. Fish Physiol Biochem 45(5):1615–1625. 10.1007/s10695-019-00650-5 PubMed PMC
Henning H, Petrunkina AM, Harrison RAP, Waberski D (2014) Cluster analysis reveals a binary effect of storage on boar sperm motility function. Reprod Fertil Dev 26:623–632. 10.1071/RD13113 PubMed
Hollenbeck PJ, Bray D, Adams RJ (1985) Effects of the uncoupling agents FCCP and CCCP on the saltatory movements of cytoplasmic organelles. Cell Biol Int Rep 9(2):193–199. 10.1016/0309-1651(85)90094-3 PubMed
Ingermann RL (2008) Energy metabolism and respiration in fish spermatozoa. In: Alavi SMH, Cosson JJ, Coward K, Rafiee G (eds) Fish spermatology. Alpha Science International Ltd., Oxford, pp 241–266
Ingermann RL, Robinson ML, Cloud JG (2003) Respiration of steelhead trout sperm: sensitivity to pH and carbon dioxide. J Fish Biol 62(1):13–23. 10.1046/j.1095-8649.2003.00003.x
Liljedal S, Rudolfsen G, Folstad I (2008) Factors predicting male fertilization success in an external fertilizer. Behav Ecol Sociobiol 62:1805–1811. 10.1007/s00265-008-0609-1
Magari RT (2004) Bias estimation in method comparison studies. J Biopharm Stat 14(4):881–892. 10.1081/bip-200035450 PubMed
Mansour N, Lahnsteiner F, Berger B (2003) Metabolism of intratesticular spermatozoa of a tropical teleost fish (Clarias gariepinus). Comp Biochem Physiol b: Biochem Mol Biol 135(2):285–296. 10.1016/S1096-4959(03)00083-6 PubMed
McDonald JH (2014) Handbook of biological statistics (third ed.). Sparky House Publishing. Baltimore, Maryland, U.S.A.
Mendizabal-Ruiz G, Chavez-Badiola A, Aguilar Figueroa I, Martinez Nuño V, Flores-Saiffe Farias A, Valencia-Murilloa R, Drakeley A, Garcia-Sandoval JP, Cohen J (2022) Computer software (SiD) assisted real-time single sperm selection associated with fertilization and blastocyst formation. Reprod Biomed Online 45(4):703–711. 10.1016/j.rbmo.2022.03.036 PubMed
Moraes CR, Meyers S (2018) The sperm mitochondrion: organelle of many functions. Anim Reprod Sci 194:71–80. 10.1016/j.anireprosci.2018.03.024 PubMed
Nůsková H, Vrbacký M, Drahota Z, Houštěk J (2010) Cyanide inhibition and pyruvate-induced recovery of cytochrome c oxidase. J Bioenerg Biomembr 42(5):395–403. 10.1007/s10863-010-9307-6 PubMed
Pacelli C, Latorre D, Cocco T, Capuano F, Kukat C, Seibel P, Villani G (2011) Tight control of mitochondrial membrane potential by cytochrome c oxidase. Mitochondrion 11(2):334–341. 10.1016/j.mito.2010.12.004 PubMed
Park SM, Ho S, Aruliah S, Weber MF, Ward CA, Venter RD, Srinivasan S (1986) Electrochemical reduction of oxygen at platinum electrodes in KOH solutions - temperature and concentration effects. J Electrochem Soc 133(8):1641–1649. 10.1149/1.2108982
Perchec G, Jeulin C, Cosson J, André F, Billard R (1995) Relationship between sperm ATP content and motility of carp spermatozoa. J Cell Sci 108(2):747–753. 10.1242/jcs.108.2.747 PubMed
Plaza Davila M, Martin Muñoz P, Tapia JA, Ortega Ferrusola C, Balao da Silva CC, Peña FJ (2015) Inhibition of mitochondrial complex I leads to decreased motility and membrane integrity related to increased hydrogen peroxide and reduced ATP production, while the inhibition of glycolysis has less impact on sperm motility. PLoS ONE 10(9):e0138777–e0138777. 10.1371/journal.pone.0138777 PubMed PMC
Potter AE, White CR, Marshall DJ (2024) Per capita sperm metabolism is density-dependent. J Exp Biol jeb.246674. 10.1242/jeb.246674 PubMed PMC
Pum J (2019) Chapter six - a practical guide to validation and verification of analytical methods in the clinical laboratory. In: Makowski GS (ed) Advances in clinical chemistry. Elsevier. pp. 215–281. 10.1016/bs.acc.2019.01.006 PubMed
Purchase CF, Earle PT (2012) Modifications to the IMAGEJ computer assisted sperm analysis plugin greatly improve efficiency and fundamentally alter the scope of attainable data. J Appl Ichthyol 28:1013–1016. 10.1111/jai.12070
Rahi D, Dzyuba B, Policar T, Malinovskyi O, Rodina M, Dzyuba V (2021) Bioenergetic pathways in the sperm of an under-ice spawning fish, burbot (Lota lota): the role of mitochondrial respiration in a varying thermal environment. Biology (Basel) 10(8). 10.3390/biology10080739 PubMed PMC
Rahi D, Dzyuba B, Xin M, Cheng Y, Dzyuba V (2020) Energy pathways associated with sustained spermatozoon motility in the endangered Siberian sturgeon Acipenser baerii. J Fish Biol 97(2):435–443. 10.1111/jfb.14382 PubMed
Schuh RA, Clerc P, Hwang H, Mehrabian Z, Bittman K, Chen H, Polster BM (2011) Adaptation of microplate-based respirometry for hippocampal slices and analysis of respiratory capacity. J Neurosci Res 89(12):1979–1988. 10.1002/jnr.22650 PubMed PMC
Tremoen NH, Gaustad AH, Andersen-Ranberg I, van Son M, Zeremichael TT, Frydenlund K, Grindflek E, Våge DI, Myromslien FD (2018) Relationship between sperm motility characteristics and ATP concentrations, and association with fertility in two different pig breeds. Anim Reprod Sci 193:226–234. 10.1016/j.anireprosci.2018.04.075 PubMed
Van Bergen NJ, Blake RE, Crowston JG, Trounce IA (2014) Oxidative phosphorylation measurement in cell lines and tissues. Mitochondrion 15:24–33. 10.1016/j.mito.2014.03.003 PubMed
Wang X-d, Wolfbeis OS (2014) Optical methods for sensing and imaging oxygen: materials, spectroscopies and applications. Chem Soc Rev 43(10):3666–3761. 10.1039/C4CS00039K PubMed
Wilson DF, Erecińska M, Drown C, Silver IA (1979) The oxygen dependence of cellular energy metabolism. Arch Biochem Biophys 195(2):485–493. 10.1016/0003-9861(79)90375-8 PubMed
Wilson-Leedy JG, Ingermann RL (2007) Development of a novel CASA system based on open source software for characterization of zebrafish sperm motility parameters. Theriogenology 67(3):661–672. 10.1016/j.theriogenology.2006.10.003 PubMed
Zhang J, Chen S, Li Y, Xiao W, An W (2021) Alleviation of CCCP-induced mitochondrial injury by augmenter of liver regeneration via the PINK1/Parkin pathway-dependent mitophagy. Exp Cell Res 409(1):112866. 10.1016/j.yexcr.2021.112866 PubMed
Zhang T, Anderson AB (2007) Oxygen reduction on platinum electrodes in base: theoretical study. Electrochim Acta 53(2):982–989. 10.1016/j.electacta.2007.08.014