Animal Reproduction (AR)
https://www.animal-reproduction.org/article/doi/10.1590/1984-3143-AR2022-0048
Animal Reproduction (AR)
ORIGINAL ARTICLE

Impact of quercetin, carnosine, and ozone in the cryopreservation on Nellore (Bos indicus) semen

Willian Vaniel Alves dos Reis; Raiza Rocha Pereira; Mozarth Vieira Junior; Cibele Cristina Tavares da Cunha; Bianca Rodrigues Acácio; Gustavo Guerino Macedo; Eliane Vianna da Costa-e-Silva; Breno Fernandes Barreto Sampaio

Downloads: 0
Views: 314

Abstract

The objective of this study was to reduce the effects of cryoinjury caused in bovine semen by cryopreservation. Ejaculates were collected from Nellore bulls and subjected to freezing in C (control), ozone (15, 30, and 60 µg mL-1 of ozone), quercetin (25, 50, and 100 µg mL-1 of quercetin), and carnosine groups (100, 200, and 300 ng mL-1 of carnosine). Samples were evaluated post-thaw (M0) and post-rapid thermoresistance test (M30) for sperm kinetics (total motility, progressive motility, curvilinear speed, linearity and amplitude of lateral head displacement) and cell structure viability (plasma membrane integrity, acrosomal integrity, mitochondrial potential, membrane fluidity, and lipid peroxidation). There were no differences (P > 0.05) between the control, quercetin, and carnosine-treated groups for the parameters evaluated at M0 and M30. In turn, supplementation with ozone resulted in lower values for sperm kinetics (P < 0.05) and lower mitochondrial potential at M30 (P < 0.05). Quercetin and carnosine at the concentrations used did not promote significant gains in frozen semen, nor did they demonstrate cytotoxicity. We expected to obtain positive results with the use of ozone. Nonetheless, the addition was harmful to the parameters of sperm kinetics, and its effect was not observed as a possible pro-antioxidant. We believe that the fact that the gas did not harm the sperm structure opens avenues for tests with lower dosages, since, by reducing its concentration, we could minimize the damage to sperm kinetics.

Keywords

lipid peroxidation, reactive oxygen species, spermatozoa

References

Abud COG, Abud LJ, Oliveira JC No, Dode MAN, Sereno JRB, Martins CF. Comparação entre os sistemas automatizado e convencional de criopreservação de sêmen bovino. Cienc Anim Bras. 2014;15(1):32-7. http://dx.doi.org/10.5216/cab.v15i1.12233.

Agrillo A, Petrucci MT, Tedaldi M, Mustazza MC, Marino SMF, Gallucci C, Iannetti G. New therapeutic protocol in the treatment of avascular necrosis of the jaws. J Craniofac Surg. 2006;17(6):1080-3. http://dx.doi.org/10.1097/01.scs.0000249350.59096.d0. PMid:17119409.

Ahmed H, Jahan S, Salman MM, Ullah F. Stimulating effects of Quercetin (QUE) in tris citric acid extender on post thaw quality and in vivo fertility of buffalo (Bubalus bubalis) bull spermatozoa. Theriogenology. 2019;134:18-23. http://dx.doi.org/10.1016/j.theriogenology.2019.05.012. PMid:31112913.

Aitken RJ, Smith TB, Jobling MS, Baker MA, Iuliis GN. Oxidative stress and male reproductive health. Asian J Androl. 2014;16(1):31-8. http://dx.doi.org/10.4103/1008-682X.122203. PMid:24369131.

Alves GES, Abreu JMG, Ribeiro JD Fo, Muzzi LAL, Oliveira HP, Tannus RJ, Buchanan T. Efeitos do ozônio nas lesões de reperfusão do jejuno em eqüinos. Arq Bras Med Vet Zootec. 2004;56(4):433-7. http://dx.doi.org/10.1590/S0102-09352004000400002.

Andrade ER, Seneda MM, Alfieri AA. Consequências da produção das espécies reativas de oxigênio na reprodução e principais mecanismos antioxidantes. Rev Bras Reprod Anim. 2010;34:79-85.

Avdatek F, Yeni D, İnanç ME, Çil B, Tuncer BP, Türkmen R, Taşdemir U. Supplementation of quercetin for advanced DNA integrity in bull semen cryopreservation. Andrologia. 2018;50(4):e12975. http://dx.doi.org/10.1111/and.12975. PMid:29411886.

Barbosa KBF, Costa NMB, Alfenas RCG, Paula SO, Minim VPR, Bressan J. Estresse oxidativo: conceito, implicações e fatores modulatórios. Rev Nutr. 2010;23(4):629-43. http://dx.doi.org/10.1590/S1415-52732010000400013.

Behling EB, Sendão MC, Francescato HDC, Antunes LMG, Bianchi M LP. Flavonóide quercetina: aspectos gerais e ações biológicas. Aliment Nutr. 2004;15:285-92.

Beorlegui N, Cetica P, Trinchero G, Córdoba M, Beconi M. Comparative study of functional and biochemical parameters in frozen bovine sperm. Andrologia. 1997;29(1):37-42. http://dx.doi.org/10.1111/j.1439-0272.1997.tb03146.x. PMid:9049010.

Bollwein H, Bittner L. Impacts of oxidative stress on bovine sperm function and subsequent in vitro embryo development. Anim Reprod. 2018;15(Suppl 1):703-10. http://dx.doi.org/10.21451/1984-3143-AR2018-0041. PMid:36249836.

Camargo LS, Freitas-Dell’Aqua CP, Schmith RA, Guasti PN, Volpato M, Souza FFD. New multicolor protocol to assessment dog spermatozoa by flow cytometer. Anim Reprod. 2017;14:311.

Carneiro JAM, Canisso IF, Bandeira RS, Scheeren VFC, Freitas-Dell’Aqua CP, Alvarenga MA, Papa FO, Dell’Aqua JA Jr. Effects of coenzyme Q10 on semen cryopreservation of stallions classified as having good or bad semen freezing ability. Anim Reprod Sci. 2018;192:107-18. http://dx.doi.org/10.1016/j.anireprosci.2018.02.020. PMid:29502896.

CBRA. Manual para exame andrológico e avaliação de sêmen animal. 3rd ed. Belo Horizonte: Colégio Brasileiro de Reprodução Animal; 2013.

Chacur MGM, Dias HS, Papa FO, Louvison BA, Calesco MM, Papa PM. Efeito de meios diluentes na viabilidade de sêmen congelado bovino. Vet Zootec. 2012;19:346-55.

Drozak J, Veiga-da-Cunha M, Vertommen D, Stroobant V, Van Schaftingen E. Molecular identification of carnosine synthase as ATP-grasp domain-containing protein 1 (ATPGD1). J Biol Chem. 2010;285(13):9346-56. http://dx.doi.org/10.1074/jbc.M109.095505. PMid:20097752.

Dufresne J, Cyr DG. Regulation of the pannexin-1 promoter in the rat epididymis. Biol Reprod. 2014;91(6):143. http://dx.doi.org/10.1095/biolreprod.114.122168. PMid:25376229.

Duque CJE, Rojano BA, Restrepo BG. Criotolerancia de semen equino congelado con aditivos en el diluyente. Rev Investig Vet Peru. 2017;28(1):120-9. http://dx.doi.org/10.15381/rivep.v28i1.12944.

Freitas-Dell’Aqua CP, Guasti PN, Monteiro GA, Maziero RRD, Dell’Aqua JJA, Papa FO. Flow cytometric analysis of fertile and subfertile frozen stallion spermatozoa. Anim Reprod. 2012;9:941.

Gibb Z, Butler TJ, Morris LHA, Maxwell WMC, Grupen CG. Quercetin improves the postthaw characteristics of cryopreserved sex-sorted and nonsorted stallion sperm. Theriogenology. 2013;79(6):1001-9. http://dx.doi.org/10.1016/j.theriogenology.2012.06.032. PMid:23453253.

Guasti P, Freitas-Dell’Aqua CP, Maziero RRD, Hartwig F, Monteiro GA, Lisboa FP. Validation of flow cytometry for assessment of membrane lipid peroxidation of equine spermatozoa. Anim Reprod. 2012;9:929.

Harrison RAP, Ashworth PJC, Miller NGA. Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev. 1996;45(3):378-91. http://dx.doi.org/10.1002/(SICI)1098-2795(199611)45:3<378::AID-MRD16>3.0.CO;2-V. PMid:8916050.

Hipkiss AR, Gaunitz F. Inhibition of tumour cell growth by carnosine: some possible mechanisms. Amino Acids. 2014;46(2):327-37. http://dx.doi.org/10.1007/s00726-013-1627-5. PMid:24292217.

Hipkiss AR, Worthington VC, Himsworth DT, Herwig W. Protective effects of carnosine against protein modification mediated by malondialdehyde and hypochlorite. Biochim Biophys Acta. 1998;1380(1):46-54. http://dx.doi.org/10.1016/S0304-4165(97)00123-2. PMid:9545530.

Hossain MS, Johannisson A, Wallgren M, Nagy S, Siqueira AP, Rodriguez-Martinez H. Flow cytometry for the assessment of animal sperm integrity and functionality: state of the art. Asian J Androl. 2011;13(3):406-19. http://dx.doi.org/10.1038/aja.2011.15. PMid:21478895.

Leite PA, Schreder GG, Almeida CLR, Zúccari CESN, Costa-e-Silva EV. Criopreservação do sêmen bovino. J Health Sci. 2011;13:279-86.

Losano JDA, Angrimani DSR, Redondo RF, Brito MM, Rui BR, Kawai GKV, Silva BCS, Mendes CM, Assumpção MEOD, Nichi M. Deleterious effect of high carnosine concentrations in extenders during sperm cryopreservation in dogs. J Vet Androl. 2017;2(2):60-7.

Maia M, Bicudo S. Radicais livres, antioxidantes e função espermática em mamíferos: uma revisão. Rev Bras Reprod Anim. 2009;33:183-93.

McNiven MA, Richardson GF. Effect of quercetin on capacitation status and lipid peroxidation of stallion spermatozoa. Cell Preserv Technol. 2006;4(3):169-77. http://dx.doi.org/10.1089/cpt.2006.4.169.

Meamar M, Zribi N, Cambi M, Tamburrino L, Marchiani S, Filimberti E, Fino MG, Biggeri A, Menezo Y, Forti G, Baldi E, Muratori M. Sperm DNA fragmentation induced by cryopreservation: new insights and effect of a natural extract from Opuntia ficus-indica. Fertil Steril. 2012;98(2):326-33. http://dx.doi.org/10.1016/j.fertnstert.2012.05.001. PMid:22633258.

Merhi Z, Bazzi A, Moseley-LaRue R, Moseley AR, Smith AH, Zhang J, Ruggiero M. Ozone therapy: overview of its potential utility in male reproduction. Am J Immunol. 2018;14(1):15-25. http://dx.doi.org/10.3844/ajisp.2018.15.25.

Mortimer D. Sperm preparation methods. J Androl. 2000;21(3):357-66. PMid:10819443.

Nassar A, Mahony M, Blackmore P, Morshedi M, Ozgur K, Oehninger S. Increase of intracellular calcium is not a cause of pentoxifylline- induced hyperactivated motility or acrosome reaction in human sperm. Fertil Steril. 1998;69(4):748-54. http://dx.doi.org/10.1016/S0015-0282(98)00013-2. PMid:9548168.

Neild DM, Brouwers JFHM, Colenbrander B, Agüero A, Gadella BM. Lipid peroxide formation in relation to membrane stability of fresh and frozen thawed stallion spermatozoa. Mol Reprod Dev. 2005;72(2):230-8. http://dx.doi.org/10.1002/mrd.20322. PMid:15948163.

Parrish JJ, Susko-Parrish J, Winer MA, First NL. Capacitation of bovine sperm by heparin. Biol Reprod. 1988;38(5):1171-80. http://dx.doi.org/10.1095/biolreprod38.5.1171. PMid:3408784.

Patel HA, Siddiquee GM, Chaudhari DV, Suthar VS. Effect of different antioxidant additives in semen diluent on cryopreservability (-196°C) of buffalo semen. Vet World. 2016;9(3):299-303. http://dx.doi.org/10.14202/vetworld.2016.299-303. PMid:27057115.

Rocha CC, Kawai GKV, Losano JDA, Angrimani DSR, Rui BR, Bicudo LC, Silva BCS, Alonso MA, Mendes CM, Assumpção MEOD, Pereira RJG, Barnabe VH, Nichi M. Carnosine as malondialdehyde scavenger in stallion seminal plasma and its role in sperm function and oxidative status. Theriogenology. 2018;119:10-7. http://dx.doi.org/10.1016/j.theriogenology.2018.06.016. PMid:29960162.

Ruiz-Pesini E, Diez C, Lapeña AC, Pérez-Martos A, Montoya J, Alvarez E, Arenas J, López-Pérez MJ. Correlation of sperm motility with mitochondrial enzymatic activities. Clin Chem. 1998;44(8):1616-20. http://dx.doi.org/10.1093/clinchem/44.8.1616. PMid:9702947.

Santos DS, Rodrigues MMF. Atividades farmacológicas dos flavonoides: um estudo de revisão. Estaç Cient. 2017;7(3):29. http://dx.doi.org/10.18468/estcien.2017v7n3.p29-35.

Seifi-Jamadi A, Kohram H, Shahneh AZ, Ansari M, Macías-García B. Quercetin ameliorate motility in frozen-thawed turkmen stallions sperm. J Equine Vet Sci. 2016;45:73-7. http://dx.doi.org/10.1016/j.jevs.2016.06.078.

Silva ECB, Arruda LCP, Silva SV, Souza HM, Guerra MMP. High resveratrol or quercetin concentrations reduce the oscillation index of frozen goat semen. Arq Bras Med Vet Zootec. 2016;68(5):1237-43. http://dx.doi.org/10.1590/1678-4162-8670.

Silva ECB, Cajueiro JFP, Silva SV, Soares PC, Guerra MMP. Effect of antioxidants resveratrol and quercetin on in vitro evaluation of frozen ram sperm. Theriogenology. 2012;77(8):1722-6. http://dx.doi.org/10.1016/j.theriogenology.2011.11.023. PMid:22289215.

Sunnen GV. Ozone in medicine: overview and future directions. J Adv Med. 1988;1:159-74.

Timm M, Saaby L, Moesby L, Hansen EW. Considerations regarding use of solvents in in vitro cell based assays. Cytotechnology. 2013;65(5):887-94. http://dx.doi.org/10.1007/s10616-012-9530-6. PMid:23328992.

Tironi SMT, Martinez AC, Seixas FAV, Stefanello TF, Nakamura CV, Moraes GV. Effects of treatment with quercetin on the quality of cryopreserved bovine semen. Acta Sci Vet. 2019;47(1):1-7. http://dx.doi.org/10.22456/1679-9216.90279.

Tvrdá E, Lukáč N, Schneidgenová M, Lukáčová J, Szabó C, Goc Z, Greń A, Massányi P. Impact of seminal chemical elements on the oxidative balance in bovine seminal plasma and spermatozoa. J Vet Med. 2013;2013:125096. http://dx.doi.org/10.1155/2013/125096. PMid:26464901.

Verstegen J, Iguer-Ouada M, Onclin K. Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology. 2002;57(1):149-79. http://dx.doi.org/10.1016/S0093-691X(01)00664-1. PMid:11775967.

Vianna FP, Papa FO, Zahn FS, Melo CM, Dell’Aqua JA Jr. Thermoresistance sperm tests are not predictive of potential fertility for cryopreserved bull semen. Anim Reprod Sci. 2009;113(1-4):279-82. http://dx.doi.org/10.1016/j.anireprosci.2008.06.009. PMid:18707830.

Winn E, Whitaker BD. Quercetin supplementation during boar semen thawing and incubation improves sperm characteristics. J Anim Sci. 2018;96(Suppl 2):261-2. http://dx.doi.org/10.1093/jas/sky073.486.

Zribi N, Chakroun NF, Abdallah FB, Elleuch H, Sellami A, Gargouri J, Rebai T, Fakhfakh F, Keskes LA. Effect of freezing-thawing process and quercetin on human sperm survival and DNA integrity. Cryobiology. 2012;65(3):326-31. http://dx.doi.org/10.1016/j.cryobiol.2012.09.003. PMid:23010483.
 


Submitted date:
03/02/2022

Accepted date:
02/23/2023

64241ffea953956b3601e863 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections