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RESEARCH ARTICLE

Effects of capacitating media and incubation time on collared peccary sperm quality, acrosome reaction, and binding ability

Maria Valéria de Oliveira Santos A , Andréia Maria da Silva B , Leonardo Vitorino Costa de Aquino A , Lhara Ricarliany Medeiros de Oliveira A , João Batista Freire de Souza-Junior B , Moacir Franco de Oliveira C , Alexandre Rodrigues Silva A and Alexsandra Fernandes Pereira https://orcid.org/0000-0003-2137-854X A *
+ Author Affiliations
- Author Affiliations

A Laboratory of Animal Biotechnology, Federal Rural University of Semi-Arid, Mossoro, RN, Brazil.

B Laboratory of Animal Germplasm Conservation, Federal Rural University of Semi-Arid, Mossoro, RN, Brazil.

C Laboratory of Applied Animal Morphophysiology, Federal Rural University of Semi-Arid, Mossoro, RN, Brazil.


Handling Editor: Rodolfo Ungerfeld

Animal Production Science 63(17) 1740-1749 https://doi.org/10.1071/AN23225
Submitted: 20 June 2023  Accepted: 9 October 2023  Published: 26 October 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Several assisted reproduction techniques have been proposed for collared peccaries due to the interest in its conservation. However, there is little information about the requirements for sperm capacitation, an initial step in in vitro fertilisation.

Aims

We aimed to determine the optimal conditions for collared peccary sperm capacitation by comparing Tyrode’s albumin lactate pyruvate (TALP) or the same media plus heparin, caffeine, or their combination at different exposure times (1, 3, and 6 h).

Methods

The samples were evaluated for kinetic parameters, membrane functionality and integrity, mitochondrial activity, morphology, DNA integrity, reactive oxygen species (ROS) expression levels, capacitation, and sperm binding ability using swine oocytes.

Key results

Samples incubated with caffeine or heparin had a higher percentage of capacitated spermatozoa. The maximum percentage of capacitation was achieved after 3 h of incubation with either agent. Moreover, spermatozoa subjected to heparin capacitation showed better motility than when subjected to caffeine, and lower ROS expression levels after 1 h. No differences were observed among incubation times for the binding ability.

Conclusions

In summary, collared peccary spermatozoa can be capacitated with caffeine or heparin; however, heparin better maintains sperm motility and ROS expression levels. The co-incubation of gametes in a medium with heparin for 3 h could be efficient for in vitro fertilisation in collared peccaries.

Implications

This result will contribute to the development of assisted reproduction techniques for conservation and productivity of collared peccaries.

Keywords: animal conservation, assisted reproduction, caffeine, capacitation, heparin, semen, spermatozoa, wild ungulates.

References

Abeydeera LR, Day BN (1997) In vitro penetration of pig oocytes in a modified Tris-buffered medium: effect of BSA, caffeine and calcium. Theriogenology 48, 537-544.
| Crossref | Google Scholar | PubMed |

Almiñana C, Gil MA, Cuello C, Parrilla I, Roca J, Vazquez JM, Martinez EA (2008) Effects of ultrashort gamete co-incubation time on porcine in vitro fertilization. Animal Reproduction Science 106, 393-401.
| Crossref | Google Scholar | PubMed |

Awda BJ, Mackenzie-Bell M, Buhr MM (2009) Reactive oxygen species and boar sperm function. Biology of Reproduction 81, 553-561.
| Crossref | Google Scholar | PubMed |

Bodmer RE (1990) Responses of ungulates to seasonal inundations in the Amazon floodplain. Journal of Tropical Ecology 6, 191-201.
| Crossref | Google Scholar |

Castelo TS, Bezerra FSB, Lima GL, Alves HM, Oliveira IRS, Santos EAA, Peixoto GCX, Silva AR (2010) Effect of centrifugation and sugar supplementation on the semen cryopreservation of captive collared peccaries (Tayassu tajacu). Cryobiology 61, 275-279.
| Crossref | Google Scholar | PubMed |

Celeghini ECC, De Arruda RP, De Andrade AFC, Nascimento J, Raphael CF (2007) Practical techniques for bovine sperm simultaneous fluorimetric assessment of plasma, acrosomal and mitochondrial membranes. Reproduction in Domestic Animals 42, 479-488.
| Crossref | Google Scholar | PubMed |

Chen Y, Wang K, Zhang D, Zhao Z, Huang J, Zhou L, Feng M, Shi J, Wei H, Li L, Wu Z, Zhang S (2020) GPx6 is involved in the in vitro induced capacitation and acrosome reaction in porcine sperm. Theriogenology 156, 107-115.
| Crossref | Google Scholar | PubMed |

Dapino DG, Marini PE, Cabada MO (2006) Effect of heparin on in vitro capacitation of boar sperm. Biological Research 39, 631-639.
| Crossref | Google Scholar | PubMed |

Desbiez ALJ, Keuroghlian A, Beisiegel BM, Medici EP, Gatti A, Pontes ARM, Campos CB, Tófoli CF, Júnior EAM, Azevedo FC, Pinho GM (2012) Avaliação do risco de extinção do cateto Pecari tajacu Linnaeus, 1758, no Brasil. Biodiversidade Brasileira 1, 74-83.
| Google Scholar |

Flesch FM, Gadella BM (2000) Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochimica et Biophysica Acta (BBA) – Reviews on Biomembranes 1469, 197-235.
| Crossref | Google Scholar | PubMed |

Florman HM, First NL (1988) The regulation of acrosomal exocytosis. I. Sperm capacitation is required for the induction of acrosome reactions by the bovine zona pellucida in vitro. Developmental Biology 128, 453-463.
| Crossref | Google Scholar | PubMed |

Funahashi H, Nagai T (2001) Regulation of in vitro penetration of frozen–thawed boar spermatozoa by caffeine and adenosine. Molecular Reproduction and Development 58, 424-431.
| Crossref | Google Scholar | PubMed |

Gambini A, De Stéfano A, Jarazo J, Buemo C, Karlanian F, Salamone DF (2016) Embryo aggregation does not improve the development of interspecies somatic cell nuclear transfer embryos in the horse. Theriogenology 86, 1081-1091.
| Crossref | Google Scholar | PubMed |

Gil MA, Almiñana C, Cuello C, Parrilla I, Roca J, Vazquez JM, Martinez EA (2007) Brief coincubation of gametes in porcine in vitro fertilization: role of sperm:oocyte ratio and post-coincubation medium. Theriogenology 67, 620-626.
| Crossref | Google Scholar | PubMed |

Gongora J, Reyna-Hurtado R, Beck H, Taber A, Altrichter M, Keuroghlian A (2011) Pecari tajacu. The IUCN Red List of Threatened Species 2011, Article e.T41777A10562361. Available at https://doi.org/10.2305/IUCN.UK.2011-2.RLTS.T41777A10562361.en

Handrow RR, First NL, Parrish JJ (1989) Calcium requirement and increased association with bovine sperm during capacitation by heparin. Journal of Experimental Zoology 252, 174-182.
| Crossref | Google Scholar | PubMed |

Harrison RAP, Gadella BM (2005) Bicarbonate-induced membrane processing in sperm capacitation. Theriogenology 63, 342-351.
| Crossref | Google Scholar | PubMed |

Kumar P, Mohanty TK, Kumaresan A, Nag P, Saraf KK, Kumar V, Lathika S, Nayak S, Bhakat M (2018) Incubation of spermatozoa with Anandamide prior to cryopreservation reduces cryocapacitation and improves post-thaw sperm quality in the water buffalo (Bubalus bubalis). Animal Reproduction Science 189, 77-83.
| Crossref | Google Scholar | PubMed |

Kwon W-S, Rahman MS, Lee J-S, Kim J, Yoon S-J, Park Y-J, You Y-A, Hwang S, Pang M-G (2014) A comprehensive proteomic approach to identifying capacitation related proteins in boar spermatozoa. BMC Genomics 15, 897.
| Crossref | Google Scholar |

Lee S-H, Kim Y-J, Kang BH, Yun YS, Park C-K (2020) The relationship between acrosome reaction and polyunsaturated fatty acid composition in boar sperm. Reproduction in Domestic Animals 55, 624-631.
| Crossref | Google Scholar | PubMed |

Li Y, Li R-H, Ran M-X, Zhang Y, Liang K, Ren Y-N, He W-C, Zhang M, Zhou G-B, Qazi IH, Zeng C-J (2018) High throughput small RNA and transcriptome sequencing reveal capacitation-related microRNAs and mRNA in boar sperm. BMC Genomics 19, 736.
| Crossref | Google Scholar |

Mann T (1954) ‘The biochemistry of semen.’ p. 1958. (Methuen & Co. Ltd: London, UK)

Martins CF, Dode MN, Bao SN, Rumpf R (2007) The use of the acridine orange test and the TUNEL assay to assess the integrity of freeze-dried bovine spermatozoa DNA. Genetics Molecular Research 6, 94-104.
| Google Scholar |

Moreira SSJ, Silva AM, Praxedes ÉCG, Campos LB, Santos CS, Souza ALP, Pereira AF, Souza-Júnior JBF, Costa LLM, Silva AR (2019) Composition of collared peccary seminal plasma and sperm motility kinetics in semen obtained during dry and rainy periods in a semiarid biome. Animal Reproduction Science 211, 106229.
| Crossref | Google Scholar | PubMed |

Mun S-E, Sim B-W, Yoon S-B, Jeong P-S, Yang H-J, Choi S-A, Park Y-H, Kim Y-H, Kang P, Jeong K-J, Lee Y, Jin YB, Song B-S, Kim J-S, Huh J-W, Lee S-R, Choo Y-K, Kim S-U, Chang K-T (2017) Dual effect of fetal bovine serum on early development depends on stage-specific reactive oxygen species demands in pigs. PLoS ONE 12, e0175427.
| Crossref | Google Scholar | PubMed |

Nagai T, Miura K, Kikuchi K, Okamura N (1993) Effects of caffeine on in-vitro fertilization of pig follicular oocytes. Journal of Reproduction and Development 39, 347-352.
| Crossref | Google Scholar |

Osycka-Salut CE, Martínez-León E, Gervasi MG, Castellano L, Davio C, Chiarante N, Franchi AM, Ribeiro ML, Díaz ES, Perez-Martinez S (2020) Fibronectin induces capacitation-associated events through the endocannabinoid system in bull sperm. Theriogenology 153, 91-101.
| Crossref | Google Scholar | PubMed |

Pang Y-W, Sun Y-Q, Jiang X-L, Huang Z-Q, Zhao S-J, Du W-H, Hao H-S, Zhao X-M, Zhu H-B (2016) Protective effects of melatonin on bovine sperm characteristics and subsequent in vitro embryo development. Molecular Reproduction and Development 83, 993-1002.
| Crossref | Google Scholar | PubMed |

Paramio M-T, Izquierdo D (2016) Recent advances in in vitro embryo production in small ruminants. Theriogenology 86, 152-159.
| Crossref | Google Scholar | PubMed |

Parrish JJ (2014) Bovine in vitro fertilization: in vitro oocyte maturation and sperm capacitation with heparin. Theriogenology 81, 67-73.
| Crossref | Google Scholar | PubMed |

Parrish JJ, Susko-Parrish J, Winer MA, First NL (1988) Capacitation of bovine sperm by heparin. Biology of Reproduction 38, 1171-1180.
| Crossref | Google Scholar | PubMed |

Pipan MZ, Mrkun J, Strajn BJ, Vrtač KP, Kos J, Pišlar A, Zrimšek P (2017) The influence of macro- and microelements in seminal plasma on diluted boar sperm quality. Acta Veterinaria Scandinavica 59, 11.
| Crossref | Google Scholar |

Rath D, Long CR, Dobrinsky JR, Welch GR, Schreier LL, Johnson LA (1999) In vitro production of sexed embryos for gender preselection: high-speed sorting of X-chromosome-bearing sperm to produce pigs after embryo transfer. Journal of Animal Science 77, 3346-3352.
| Crossref | Google Scholar | PubMed |

Rivlin J, Mendel J, Rubinstein S, Etkovitz N, Breitbart H (2004) Role of hydrogen peroxide in sperm capacitation and acrosome reaction. Biology of Reproduction 70, 518-522.
| Crossref | Google Scholar | PubMed |

Robles-Gómez L, González-Brusi L, Sáez-Espinosa P, Huerta-Retamal N, Cots-Rodríguez P, Avilés M, Gómez-Torres MJ (2021) Specific lectin binding sites during in vitro capacitation and acrosome reaction in boar spermatozoa. Italian Journal of Animal Science 20, 372-382.
| Crossref | Google Scholar |

Romar R, Cánovas S, Matás C, Gadea J, Coy P (2019) Pig in vitro fertilization: where are we and where do we go? Theriogenology 137, 113-121.
| Crossref | Google Scholar | PubMed |

Santos EAA, Sousa PC, Peixoto GCX, Simão BR, Oliveira MF, Silva AR (2013) Establishing the hypoosmotic swelling test for sperm analysis in collared peccaries (Pecari tajacu). Arquivo Brasileiro de Medicina Veterinária e Zootecnia 65, 1257-1260.
| Crossref | Google Scholar |

Santos MVdO, Silva AM, Praxedes ÉA, Borges AA, Teles Filho ACdA, Souza-Junior JBF, Bertini LM, Silva AR, Pereira AF (2019) Antioxidant effects of the essential oil of Syzygium aromaticum on bovine epididymal spermatozoa. Andrologia 51, e13448.
| Crossref | Google Scholar | PubMed |

Santos MVO, Silva AR, Pereira AF (2022) Embryo production by in vitro fertilization in wild ungulates: progress and perspectives – a review. Annals of Animal Science 22, 1151-1162.
| Crossref | Google Scholar |

Santos MVO, Silva AM, Aquino LVC, Oliveira LRM, Moreira SSJ, Oliveira MF, Silva AR, Pereira AF (2023) Different methods for seminal plasma removal and sperm selection on the quality and fertility of collared peccary sperm. Animals 13, 1955.
| Crossref | Google Scholar | PubMed |

Sousa PC, Santos EAA, Souza ALP, Lima GL, Barros FFPC, Oliveira MF, Silva AR (2013) Sperm morphological and morphometric evaluation in captive collared peccaries (Pecari tajacu). Pesquisa Veterinária Brasileira 33, 924-930.
| Crossref | Google Scholar |

Souza ALP, Castelo TS, Queiroz JPAF, Barros IO, Paula VV, Oliveira MF, Silva AR (2009) Evaluation of anesthetic protocol for the collection of semen from captive collared peccaries (Tayassu tajacu) by electroejaculation. Animal Reproduction Science 116, 370-375.
| Crossref | Google Scholar | PubMed |

Souza ALP, Lima GL, Peixoto GCX, de Souza Castelo T, Oliveira MGC, de Paula VV, Silva AR (2015) Sperm characteristics following freezing in extenders supplemented with whole egg yolk and different concentrations of low-density lipoproteins in the collared peccary (Pecari tajacu). Reproductive Biology 15, 223-228.
| Crossref | Google Scholar | PubMed |

Souza ALP, Lima GL, Peixoto GCX, Silva AM, Oliveira MF, Silva AR (2016) Use of Aloe vera–based extender for chilling and freezing collared peccary (Pecari tajacu) semen. Theriogenology 85, 1432-1438.
| Crossref | Google Scholar | PubMed |

Vadnais ML, Galantino-Homer HL, Althouse GC (2007) Current concepts of molecular events during bovine and porcine spermatozoa capacitation. Archives of Andrology 53, 109-123.
| Crossref | Google Scholar | PubMed |

Valle Nunes A, Guariento RD, Santos BA, Fischer E (2019) Wild meat sharing among non-indigenous people in the southwestern Amazon. Behavioral Ecology and Sociobiology 73, 26.
| Crossref | Google Scholar |

Visconti PE, Galantino-Homer H, Moore GD, Bailey JL, Ning X, Fornes M, Kopf GS (1998) The molecular basis of sperm capacitation. Journal of Andrology 19, 242-248.
| Crossref | Google Scholar | PubMed |

Wada A, Harayama H (2021) Calmodulin is involved in the occurrence of extracellular Ca2+-dependent full-type hyperactivation in boar ejaculated spermatozoa incubated with cyclic AMP analogs. Animal Science Journal 92, e13552.
| Crossref | Google Scholar | PubMed |

Ward CR, Storey BT (1984) Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay. Developmental Biology 104, 287-296.
| Crossref | Google Scholar | PubMed |

Weng X-G, Cai M-M, Zhang Y-T, Liu Y, Gao Z-L, Song J, Liu Z-H (2018) Effect of Astragalus polysaccharide addition to thawed boar sperm on in vitro fertilization and embryo development. Theriogenology 121, 21-26.
| Crossref | Google Scholar | PubMed |

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 (2015) Intracellular calcium movements of boar spermatozoa during ‘in vitro’ capacitation and subsequent acrosome exocytosis follow a multiple-storage place, extracellular calcium-dependent model. Andrology 3, 729-747.
| Crossref | Google Scholar | PubMed |

Zhang R, Chu M, Chen Y, Yan P (2022) Heparin-induced and caffeine or ouabain supplemented capacitation of frozen-thawed yak (Bos grunniens) spermatozoa. Reproduction in Domestic Animals 57, 587-597.
| Crossref | Google Scholar | PubMed |