Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2022-0131
Animal Reproduction (AR)
THEMATIC SECTION: IX INTERNATIONAL SYMPOSIUM ON ANIMAL BIOLOGY OF REPRODUCTION (ISABR 2022)

The sperm mitochondria: clues and challenges

Diego Bucci; Marcella Spinaci; Ivan Cunha Bustamante-Filho; Salvatore Nesci

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Abstract

Sperm cells rely on different substrates to fulfil thei energy demand for different functions and diverse moments of their life. Species specific mechanism involve both energy substrate transport and their utilization: hexose transporters, a protein family of facilitative passive transporters of glucose and other hexose, have been identified in spermatozoa of different species and, within the species, their localization has been identified and, in some cases, linked to specific glycilitic enzyme presence. The catabolism of hexose sources for energy purposes has been studied in various species, and recent advances has been made in the knowledge of metabolic strategies of sperm cells. In particular, the importance of aerobic metabolism has been defined and described in horse, boar and even mouse spermatozoa; bull sperm cells demonstrate to have a good adaptability and capacity to switch between glycolysis and oxidative phosphorylation; finally, dog sperm cells have been demonstrated to have a great plasticity in energy metabolism management, being also able to activate the anabolic pathway of glycogen syntesis.

In conclusion, the study of energy management and mitochondrial function in spermatozoa of different specie furnishes important base knowledge to define new media for preservation as well as newbases for reproductive biotechnologies.

Keywords

sperm metabolism, bioenergetics, hexose uptake

References

Albarracín JL, Fernández-Novell JM, Ballester J, Rauch MC, Quintero-Moreno A, Peña A, Mogas T, Rigau T, Yañez A, Guinovart JJ, Slebe JC, Concha II, Rodríguez-Gil JE. Gluconeogenesis-linked glycogen metabolism is important in the achievement of in vitro capacitation of dog spermatozoa in a medium without glucose. Biol Reprod. 2004;71(5):1437-45. http://dx.doi.org/10.1095/biolreprod.104.029041. PMid:15215203.

Algieri C, Blanco-Prieto O, Llavanera M, Yeste M, Spinaci M, Mari G, Bucci D, Nesci S. Effects of cryopreservation on the mitochondrial bioenergetics of bovine sperm. Reprod Domest Anim. 2022. http://dx.doi.org/10.1111/rda.14261. PMid:36107136.

Angulo C, Rauch MC, Droppelmann A, Reyes AM, Slebe JC, Delgado-López F, Guaiquil VH, Vera JC, Concha II. Hexose transporter expression and function in mammalian spermatozoa: cellular localization and transport of hexoses and vitamin C. J Cell Biochem. 1998;71(2):189-203. http://dx.doi.org/10.1002/(SICI)1097-4644(19981101)71:2<189::AID-JCB5>3.0.CO;2-R. PMid:9779818.

Ballester J, Fernández-Novell JM, Rutllant J, García-Rocha M, Jesús Palomo M, Mogas T, Peña A, Rigau T, Guinovart JJ, Rodríguez-Gil JE. Evidence for a functional glycogen metabolism in mature mammalian spermatozoa. Mol Reprod Dev. 2000;56(2):207-19. http://dx.doi.org/10.1002/(SICI)1098-2795(200006)56:2<207::AID-MRD12>3.0.CO;2-4. PMid:10813853.

Boguenet M, Bouet PE, Spiers A, Reynier P, May-Panloup P. Mitochondria: their role in spermatozoa and in male infertility. Hum Reprod Update. 2021;27(4):697-719. http://dx.doi.org/10.1093/humupd/dmab001. PMid:33555313.

Brooks D, Mann T. Pyruvate metabolism in boar spermatozoa. J Reprod Fertil. 1973;34(1):105-19. http://dx.doi.org/10.1530/jrf.0.0340105. PMid:4719804.

Brooks DE, Mann T. Relation between the oxidation state of nicotinamide-adenine dinucleotide and the metabolism of spermatozoa. Biochem J. 1972;129(5):1023-34. http://dx.doi.org/10.1042/bj1291023. PMid:4144231.

Bucci D, Isani G, Spinaci M, Tamanini C, Mari G, Zambelli D, Galeati G. Comparative immunolocalization of GLUTs 1, 2, 3 and 5 in boar, stallion and dog spermatozoa. Reprod Domest Anim. 2010a;45(2):315-22. http://dx.doi.org/10.1111/j.1439-0531.2008.01307.x. PMid:19055550.

Bucci D, Rodríguez-Gil JE, Vallorani C, Spinaci M, Galeati G, Tamanini C. GLUTs and mammalian sperm metabolism. J Androl. 2011;32(4):348-55. http://dx.doi.org/10.2164/jandrol.110.011197. PMid:21088231.

Bucci D, Spinaci M, Vallorani C, Contri A, Carluccio A, Isani G, Tamanini C, Galeati G. Detection and localization of GLUTs 1, 2, 3 and 5 in donkey spermatozoa. Reprod Domest Anim. 2010b;45(5):e217-20. http://dx.doi.org/10.1111/j.1439-0531.2009.01544.x. PMid:19930135.

Bulkeley EA, Foutouhi A, Wigney K, Santistevan AC, Collins C, McNabb B, Meyers S. Effects from disruption of mitochondrial electron transport chain function on bull sperm motility. Theriogenology. 2021;176:63-72. http://dx.doi.org/10.1016/j.theriogenology.2021.09.015. PMid:34571399.

Chatterjee S, de Lamirande E, Gagnon C. Cryopreservation alters membrane sulfhydryl status of bull spermatozoa: protection by oxidized glutathione. Mol Reprod Dev. 2001;60(4):498-506. http://dx.doi.org/10.1002/mrd.1115. PMid:11746961.

Contri A, Valorz C, Faustini M, Wegher L, Carluccio A. Effect of semen preparation on casa motility results in cryopreserved bull spermatozoa. Theriogenology. 2010;74(3):424-35. http://dx.doi.org/10.1016/j.theriogenology.2010.02.025. PMid:20451996.

Darr CR, Cortopassi GA, Datta S, Varner DD, Meyers SA. Mitochondrial oxygen consumption is a unique indicator of stallion spermatozoal health and varies with cryopreservation media. Theriogenology. 2016a;86(5):1382-92. http://dx.doi.org/10.1016/j.theriogenology.2016.04.082. PMid:27242178.

Darr CR, Varner DD, Teague S, Cortopassi GA, Datta S, Meyers SA. Lactate and pyruvate are major sources of energy for stallion sperm with dose effects on mitochondrial function, motility, and ROS production. Biol Reprod. 2016b;95(2):34-34. http://dx.doi.org/10.1095/biolreprod.116.140707. PMid:27335066.

Davila MP, Muñoz PM, Bolaños JMG, Stout T A E, Gadella BM, Tapia JA, Silva CB, Ferrusola CO, Peña FJ. Mitochondrial ATP is required for the maintenance of membrane integrity in stallion spermatozoa, whereas motility requires both glycolysis and oxidative phosphorylation. Reproduction. 2016;152(6):683-94. http://dx.doi.org/10.1530/REP-16-0409. PMid:27798283.

Davila MP, Muñoz PM, Tapia JA, Ferrusola CO, Silva CCB, Peña FJ. 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. 2015;10(9):e0138777. http://dx.doi.org/10.1371/journal.pone.0138777. PMid:26407142.

Felix MR, Turner RM, Dobbie T, Hinrichs K. Successful in vitro fertilization in the horse: production of blastocysts and birth of foals after prolonged sperm incubation for capacitation. Biol Reprod. 2022;107(6):1551-64. http://dx.doi.org/10.1093/biolre/ioac172. PMid:36106756.

Fernández-Novell JM, Ballester J, Medrano A, Otaegui PJ, Rigau T, Guinovart JJ, Rodríguez-Gil JE. The presence of a high-Km hexokinase activity in dog, but not in boar, sperm. FEBS Lett. 2004;570(1-3):211-6. http://dx.doi.org/10.1016/j.febslet.2004.06.015. PMid:15251466.

Ford WCL. Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round? Hum Reprod Update. 2006;12(3):269-74. http://dx.doi.org/10.1093/humupd/dmi053. PMid:16407453.

Foutouhi A, Meyers S. Comparative oxidative metabolism in mammalian sperm. Anim Reprod Sci. 2022;247:107095. http://dx.doi.org/10.1016/j.anireprosci.2022.107095. PMid:36272255.

Giaretta E, Mislei B, Martínez-Pastor F, Nesci S, Spinaci M, Galeati G, Nerozzi C, Mari G, Tamanini C, Bucci D. Use of specific mitochondrial complex inhibitors to investigate mitochondrial involvement on horse sperm motility and ROS production. Res Vet Sci. 2022;147:12-9. http://dx.doi.org/10.1016/j.rvsc.2022.03.017. PMid:35397468.

Gibb Z, Aitken RJ. The impact of sperm metabolism during in vitro storage : the stallion as a model. BioMed Res Int. 2016;2016:9380609. http://dx.doi.org/10.1155/2016/9380609. PMid:26881234.

Gibb Z, Lambourne SR, Aitken RJ. The paradoxical relationship between stallion fertility and oxidative stress. Biol Reprod. 2014;91(3):77. http://dx.doi.org/10.1095/biolreprod.114.118539. PMid:25078685.

Gibb Z, Lambourne SR, Quadrelli J, Smith ND, Aitken RJ. L-carnitine and pyruvate are prosurvival factors during the storage of stallion spermatozoa at room temperature. Biol Reprod. 2015;93(4):104. http://dx.doi.org/10.1095/biolreprod.115.131326. PMid:26316064.

González-Fernández L, Ortega-Ferrusola C, Macias-Garcia B, Salido GM, Peña FJ, Tapia J. Identification of protein tyrosine phosphatases and dual-specificity phosphatases in mammalian spermatozoa and their role in sperm motility and protein tyrosine phosphorylation. Biol Reprod. 2009;80(6):1239-52. http://dx.doi.org/10.1095/biolreprod.108.073486. PMid:19211810.

Hutson SM, van Dop C, Lardy HA. Mitochondrial metabolism of pyruvate in bovine spermatozoa. J Biol Chem. 1977;252(4):1309-15. http://dx.doi.org/10.1016/S0021-9258(17)40656-9. PMid:838719.

Johnson L, Weitze KF, Fiser P, Maxwell WM. Storage of boar semen. Anim Reprod Sci. 2000;62(1-3):143-72. http://dx.doi.org/10.1016/S0378-4320(00)00157-3. PMid:10924823.

Krisfalusi M, Miki K, Magyar PL, O’Brien DA. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol Reprod. 2006;75(2):270-8. http://dx.doi.org/10.1095/biolreprod.105.049684. PMid:16687649.

Marin S, Chiang K, Bassilian S, Lee W-NP, Boros LG, Fernández-Novell JM, Centelles JJ, Medrano A, Rodriguez-Gil JE, Cascante M. Metabolic strategy of boar spermatozoa revealed by a metabolomic characterization. FEBS Lett. 2003;554(3):342-6. http://dx.doi.org/10.1016/S0014-5793(03)01185-2. PMid:14623091.

Medrano A, Peña A, Rigau T, Rodrìguez-Gil JE. Variations in the proportion of glycolytic/non-glycolytic energy substrates modulate sperm membrane integrity and function in diluted boar samples stored at 15-17 degrees C. Reprod Domest Anim. 2005;40:448-53. http://dx.doi.org/10.1111/j.1439-0531.2005.00599.x

Medrano A, Fernández-Novell JM, Ramió L, Alvarez J, Goldberg E, Montserrat Rivera M, Guinovart JJ, Rigau T, Rodríguez-Gil JE. Utilization of citrate and lactate through a lactate dehydrogenase and ATP-regulated pathway in boar spermatozoa. Mol Reprod Dev. 2006a;73(3):369-78. http://dx.doi.org/10.1002/mrd.20414. PMid:16362974.

Medrano A, García-Gil N, Ramió L, Montserrat Rivera M, Fernández-Novell JM, Ramírez A, Peña A, Dolors Briz M, Pinart E, Concha II, Bonet S, Rigau T, Rodríguez-Gil JE. Hexose-specificity of hexokinase and ADP-dependence of pyruvate kinase play important roles in the control of monosaccharide utilization in freshly diluted boar spermatozoa. Mol Reprod Dev. 2006b;73(9):1179-94. http://dx.doi.org/10.1002/mrd.20480. PMid:16804879.

Meyers S, Bulkeley E, Foutouhi A. Sperm mitochondrial regulation in motility and fertility in horses. Reprod Domest Anim. 2019;54:22-8. http://dx.doi.org/10.1111/rda.13461.

Moraes CR, Meyers S. The sperm mitochondrion: organelle of many functions. Anim Reprod Sci. 2018;194:71-80. http://dx.doi.org/10.1016/j.anireprosci.2018.03.024. PMid:29605167.

Moraes CR, Moraes LE, Blawut B, Benej M, Papandreou I, Denko NC, Coutinho da Silva M. Effect of glucose concentration and cryopreservation on mitochondrial functions of bull spermatozoa and relationship with sire conception rate. Anim Reprod Sci. 2021;230:106779. http://dx.doi.org/10.1016/j.anireprosci.2021.106779. PMid:34048998.

Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod. 2004;71(2):540-7. http://dx.doi.org/10.1095/biolreprod.103.026054. PMid:15084484.

Nesci S, Spinaci M, Galeati G, Nerozzi C, Pagliarani A, Algieri C, Tamanini C, Bucci D. Sperm function and mitochondrial activity: an insight on boar sperm metabolism. Theriogenology. 2020;144:82-8. http://dx.doi.org/10.1016/j.theriogenology.2020.01.004. PMid:31927418.

Ortiz-Rodriguez JM, Nerozzi C, Bucci D, Mislei B, Mari G, Tamanini C, Peña FJ, Spinaci M, Galeati G. The inhibition of spermatic cystine/glutamate antiporter xCT (SLC7A11) influences the ability of cryopreserved stallion sperm to bind to heterologous zonae pellucidae. Theriogenology. 2021;167:24-31. http://dx.doi.org/10.1016/j.theriogenology.2021.03.002. PMid:33743505.

Peña FJ, Ortiz-Rodríguez JM, Gaitskell-Phillips GL, Gil MC, Ortega-Ferrusola C, Martín-Cano FE. An integrated overview on the regulation of sperm metabolism (glycolysis-Krebs cycle-oxidative phosphorylation). Anim Reprod Sci. 2022;246:106805. http://dx.doi.org/10.1016/j.anireprosci.2021.106805. PMid:34275685.

Peña FJ, Plaza Davila M, Ball B, Squires EL, Martin Muñoz P, Ortega Ferrusola C, Balao da Silva C. The impact of reproductive technologies on stallion mitochondrial function. Reprod Domest Anim. 2015;50(4):529-37. http://dx.doi.org/10.1111/rda.12551. PMid:26031351.

Plaza Dávila M, Bucci D, Galeati G, Peña F, Mari G, Giaretta E, Tamanini C, Spinaci M. Epigallocatechin-3-Gallate (EGCG) reduces rotenone effect on stallion sperm-zona pellucida heterologous binding. Reprod Domest Anim. 2015;50(6):1011-6. http://dx.doi.org/10.1111/rda.12628. PMid:26482419.

Rigau T, Farré M, Ballester J, Mogas T, Peña A, Rodríguez-Gil JE. Effects of glucose and fructose on motility patterns of dog spermatozoa from fresh ejaculates. Theriogenology. 2001;56(5):601-15. http://dx.doi.org/10.1016/S0093-691X(01)00609-4. PMid:11665883.

Rigau T, Rivera M, Palomo MJ, Fernández-Novell JM, Mogas T, Ballester J, Peña A, Otaegui PJ, Guinovart JJ, Rodríguez-Gil JE. Differential effects of glucose and fructose on hexose metabolism in dog spermatozoa. Reproduction. 2002;123(4):579-91. http://dx.doi.org/10.1530/rep.0.1230579. PMid:11914120.

Rizkallah N, Chambers CG, de Graaf SP, Rickard JP. Factors affecting the survival of ram spermatozoa during liquid storage and options for improvement. Animals. 2022;12(3):244. http://dx.doi.org/10.3390/ani12030244. PMid:35158568.

Rodriguez-Gil J. Mammalian sperm energy resources management and survival during conservation in refrigeration. Reprod Domest Anim. 2006;41(Suppl. 2):11-20. http://dx.doi.org/10.1111/j.1439-0531.2006.00765.x. PMid:16984465.

Rodríguez-Gil JE, Bonet S. Current knowledge on boar sperm metabolism: comparison with other mammalian species. Theriogenology. 2016;85(1):4-11. http://dx.doi.org/10.1016/j.theriogenology.2015.05.005. PMid:26094247.

Storey BT. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol. 2008;52(5-6):427-37. http://dx.doi.org/10.1387/ijdb.072522bs. PMid:18649255.

Sung TK, Moley KH. The expression of GLUT8, GLUT9a, and GLUT9b in the mouse testis and sperm. Reprod Sci. 2007;14(5):445-55. http://dx.doi.org/10.1177/1933719107306226. PMid:17913964.

Swegen A, Lambourne SR, Aitken RJ, Gibb Z. Rosiglitazone improves stallion sperm motility, ATP content, and mitochondrial function. Biol Reprod. 2016;95(5):107. http://dx.doi.org/10.1095/biolreprod.116.142687. PMid:27683266.

Thys M, Vandaele L, Morrell JM, Mestach J, van Soom A, Hoogewijs M, Rodriguez-Martinez H. In vitro fertilizing capacity of frozen-thawed bull spermatozoa selected by single-layer (glycidoxypropyltrimethoxysilane) silane-coated silica colloidal centrifugation. Reprod Domest Anim. 2009;44(3):390-4. http://dx.doi.org/10.1111/j.1439-0531.2008.01081.x. PMid:18992094.

Tourmente M, Sansegundo E, Rial E, Roldan ERS. Capacitation promotes a shift in energy metabolism in murine sperm. Front Cell Dev Biol. 2022;10:950979. http://dx.doi.org/10.3389/fcell.2022.950979. PMid:36081906.

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(33):20613-26. http://dx.doi.org/10.1074/jbc.M115.664813. PMid:26048989.

Varner DD, Gibb Z, Aitken RJ. Stallion fertility: a focus on the spermatozoon. Equine Vet J. 2015;47(1):16-24. http://dx.doi.org/10.1111/evj.12308. PMid:24943233.

Vishwanath R, Shannon P. Storage of bovine semen in liquid and frozen state. Anim Reprod Sci. 2000;62(1-3):23-53. http://dx.doi.org/10.1016/S0378-4320(00)00153-6. PMid:10924819.
 


Submitted date:
12/20/2022

Accepted date:
01/24/2023

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