The interaction between seminal plasma, sperm, and endometrium in inter- and intra-species breeding in equids

in Reproduction
Authors:
Giorgia Podico Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois Urbana-Champaign, Urbana, Illinois, USA

Search for other papers by Giorgia Podico in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0001-8046-6254
,
João H Bittar Department of Large Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, Florida, USA

Search for other papers by João H Bittar in
Current site
Google Scholar
PubMed Close
,
Shavahn C Loux Maxwell H. Gluck Equine Research Center, University of Kentucky, Lexington, Kentucky, USA

Search for other papers by Shavahn C Loux in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0001-5193-6675
,
Fabiana F Souza Department of Veterinary Surgery and Reproduction, Sao Paulo State University, Botucatu, São Paulo, Brazil

Search for other papers by Fabiana F Souza in
Current site
Google Scholar
PubMed Close
, and
Igor F Canisso Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois Urbana-Champaign, Urbana, Illinois, USA

Search for other papers by Igor F Canisso in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0003-3799-6641

Correspondence should be addressed to I F Canisso; Email: canisso@illinois.edu
DOI:
https://doi.org/10.1530/REP-23-0472
Volume/Issue:
Volume 167: Issue 6
Article ID:
e230472
Article Type:
Research Article
Online Publication Date:
07 May 2024
Copyright:
© the author(s) 2024
Restricted access
Rent on DeepDyve

Sign up for journal news

In brief

In some instances, extra-species breeding in equids is more successful than intraspecies breeding; however, little is known about the immunomodulatory effect of donkey semen and seminal plasma on the mare’s endometrium. This study compared the mare uterine inflammatory response during extra- and intraspecies breeding.

Abstract

Anecdotal experience suggests horse mares have less post-breeding inflammation and better fertility when bred with donkeys. This study aimed to compare the post-breeding inflammatory response of mares exposed to donkey and horse semen and seminal plasma and evaluate the proteome and metabolome of donkey and horse sperm and seminal plasma. Uterine edema, intrauterine fluid accumulation, polymorphonuclear neutrophils on cytology, and concentrations of progesterone, and pro- and anti-inflammatory cytokines (IL1A, IL1B, IL4, IL6, CXCL8, IL10) were assessed pre- and post infusion of semen and seminal plasma (donkey and horse). The metabolome and proteome were analyzed by LC-MS/MS. Mare cycles bred with horse semen had a greater progesterone concentration than those bred with donkey semen at 8 days post ovulation (P = 0.046). At 6 h post infusion, the inflammatory response due to the donkey semen tended to be lower (P = 0.074). Donkey seminal plasma had anti-inflammatory properties compared to horse semen and seminal plasma, as determined by fewer neutrophils on uterine cytology (P < 0.05). Horse semen resulted in greater concentrations of IL6 and lesser concentrations of IL1B (P < 0.05). PGE1, PGE3, and lactoferrin concentrations were significantly more abundant in donkey sperm and seminal plasma. Prostaglandins play an important role in immunomodulation and might contribute to the response triggered in interspecies breeding. In conclusion, breeding horse mares with donkey semen induces similar post-breeding endometritis as observed with horse semen. Donkey seminal plasma results in a lower post-infusion inflammatory response compared to other combinations in the immediate post-breeding.

Reproduction is committed to supporting researchers in demonstrating the impact of their articles published in the journal.

The two types of article metrics we measure are (i) more traditional full-text views and pdf downloads, and (ii) Altmetric data, which shows the wider impact of articles in a range of non-traditional sources, such as social media.

More information is on the Reasons to publish page.

Sept 2018 onwards Past Year Past 30 Days
Full Text Views 142 98 5
PDF Downloads 190 125 6

 

  • Collapse
  • Expand
Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Allen WR & & Short RV 1997 Interspecific and extraspecific pregnancies in equids: anything goes. Journal of Heredity 88 384–392. (https://doi.org/10.1093/oxfordjournals.jhered.a023123)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Allen WR, Kydd J, Boyle MS & & Antczak DF 1985 Between-species transfer of horse and donkey embryos: a valuable research tool. Equine Veterinary Journal 17 53–62. (https://doi.org/10.1111/j.2042-3306.1985.tb04594.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Allen WR, Skidmore JA, Stewart F & & Antczak DF 1993 Effects of fetal genotype and uterine environment on placental development in equids. Journal of Reproduction and Fertility 98 55–60. (https://doi.org/10.1530/jrf.0.0980055)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Antczak DF, Davies CJ, Kydd J & & Allen WR 1985 Immunological aspects of pregnancy in mules. Equine Veterinary Journal 17 68–72. (https://doi.org/10.1111/j.2042-3306.1985.tb04596.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Boakari YL, Alonso MA, Riccio AV & & Fernandes CB 2019 Are mule pregnancies really longer than equine pregnancies? Comparison between mule and equine pregnancies. Reproduction in Domestic Animals 54 823–827. (https://doi.org/10.1111/rda.13423)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Boeta M & & Zarco L 2005 Progesterone and equine chorionic gonadotropin concentrations around the time of pregnancy loss in mares impregnated by donkeys or stallions. Journal of Equine Veterinary Science 25 531–538. (https://doi.org/10.1016/j.jevs.2005.10.007)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Boeta M & & Zarco L 2010 Endocrine alterations around the time of abortion in mares impregnated with donkey or horse semen. Animal Reproduction Science 121 124–130. (https://doi.org/10.1016/j.anireprosci.2010.05.015)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Canisso IF 2010 Donkey breeding behavior with an emphasis on the Pêga breed. In Veterinary Care of Donkeys. eds Matthews NS. United States: International Veterinary Information Service.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Canisso IF, Davies Morel MCGD & & McDonnell S 2009 Strategies for the management of donkey jacks in intensive breeding systems. Equine Veterinary Education 21 652–659. (https://doi.org/10.2746/095777309X479058)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Canisso IF, Carvalho GR, Davies Morel MC, Guimaraes JD & & McDonnell SM 2010 Sexual behavior and ejaculate characteristics in Pega donkeys (Equus asinus) mounting estrous horse mares (Equus caballus). Theriogenology 73 56–63. (https://doi.org/10.1016/j.theriogenology.2009.07.026)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Canisso IF, Carvalho GR, Davis Morel MD, Ker PG, Rodrigues AL, Silva EC & & Coutinho da Silva MA 2011 Seminal parameters and field fertility of cryopreserved donkey jack semen after insemination of horse mares. Equine Veterinary Journal 43 179–183. (https://doi.org/10.1111/j.2042-3306.2010.00130.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Canisso IF, Stewart J & & Coutinho Da Silva MA 2016 Endometritis: managing persistent post-breeding endometritis. Veterinary Clinic of North America: Equine Practice 32 465–480. (https://doi.org/10.1016/j.cveq.2016.08.004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Canisso IF, Panzani D, Mirό J & & Ellerbrock RE 2019 Key aspects of donkey and mule reproduction. Veterinary Clinics of North America. Equine Practice 35 607–642. (https://doi.org/10.1016/j.cveq.2019.08.014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Canisso IF, Segabinazzi LGTM & & Fedorka CE 2020 Persistent breeding-induced endometritis in mares—A multifaceted challenge: from clinical aspects to immunopathogenesis and pathobiology. International Journal of Molecular Sciences 21 1432. (https://doi.org/10.3390/ijms21041432)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Carluccio A, Bucci R, Fusi J, Robbe D & & Veronesi MC 2020 Effect of age and of reproductive status on reproductive indices in horse mares carrying mule pregnancies. Heliyon 6 e05175. (https://doi.org/10.1016/j.heliyon.2020.e05175)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chaleckis R, Meister I, Zhang P & & Wheelock CE 2019 Challenges, progress and promises of metabolite annotation for LC–MS-based metabolomics. Current Opinion in Biotechnology 55 44–50. (https://doi.org/10.1016/j.copbio.2018.07.010)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cui J, Shan K, Yang Q, Qi Y, Qu H, Li J, Wang R, Jia L, Chen W, Feng N, et al.2021 Prostaglandin E3 attenuates macrophage-associated inflammation and prostate tumour growth by modulating polarization. Journal of Cellular and Molecular Medicine 25 5586–5601. (https://doi.org/10.1111/jcmm.16570)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • De Oliveira JV, Oliveira PV, Melo e Oña CM, Guasti PN, Monteiro GA, Sancler da Silva YF, Sancler Da Silva Y, Alvarenga MA, Dell’Aqua Junior JA, Papa FO, et al.2016 Strategies to improve the fertility of fresh and frozen donkey semen. Theriogenology 85 1267–1273. (https://doi.org/10.1016/j.theriogenology.2015.12.010)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Desta TT, Teklemariam H & & Mulugeta T 2022 The insights of smallholder farmers on special attributes of the genetically robust mule. Biodiversitas Journal of Biological Diversity 23 100663. (https://doi.org/10.13057/biodiv/d230732)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Elolimy A, Alharthi A, Zeineldin M, Parys C, Helmbrecht A & & Loor JJ 2019 Supply of methionine during late-pregnancy alters fecal microbiota and metabolome in neonatal dairy calves without changes in daily feed intake. Frontiers in Microbiology 10 2159. (https://doi.org/10.3389/fmicb.2019.02159)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fedorka CE, Scoggin KE, Boakari YL, Hoppe NE, Squires EL, Ball BA & & Troedsson MHT 2018 The anti-inflammatory effect of exogenous lactoferrin on breeding-induced endometritis when administered post-breeding in susceptible mares. Theriogenology 114 63–69. (https://doi.org/10.1016/j.theriogenology.2018.03.017)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fitzpatrick RJ 1957 Uterine response to adrenaline in intact cows and sheep. Journal of Comparative Pathology 67 223–238. (https://doi.org/10.1016/s0368-1742(5780022-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Fumuso EA, Aguilar J, Giguére S, Rivulgo M, Wade J & & Rogan D 2007 Immune parameters in mares resistant and susceptible to persistent post-breeding endometritis: effects of immunomodulation. Veterinary Immunology and Immunopathology 118 30–39. (https://doi.org/10.1016/j.vetimm.2007.04.009)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gobato MLM, Segabinazzi LGTM, Scheeren VFC, Bandeira RS, Freitas-Dell'Aqua CP, Dell'Aqua JA Jr & & Papa FO 2022 Ability of donkey sperm to tolerate cooling: effect of extender base and removal of seminal plasma on sperm parameters and fertility rates in mares. Frontiers in Veterinary Science 9 1011899. (https://doi.org/10.3389/fvets.2022.1011899)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Griffin RA, Swegen A, Baker M, Aitjen RJ, Skerrett-Byrne DA, Rodriguez AS, Martin-Cano FE, Nixon B, Pena FJ, Delehedde M, et al.2020 Mass spectrometry reveals distinct proteomic profiles in high -and low-quality stallion spermatozoa. Reproduction 160 695–707. (https://doi.org/10.1530/REP-20-0284)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Griffin RA, Swegen A, Baker MA, Ogle RA, Smith N, Aitken RJ, Skerrett-Byrne DA, Fair S & & Gibb Z 2022 Proteomic analysis of spermatozoa reveals caseins play a pivotal role in preventing short-term periods of subfertility in stallions. Biology of Reproduction 106 741–755. (https://doi.org/10.1093/biolre/ioab225)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hays RL, Van Demark NL & & Ormiston EE 1958 Effect of oxytocin and epinephrine on the conception rate of cows. Journal of Dairy Science 41 1376–1379. (https://doi.org/10.3168/jds.S0022-0302(5891101-9)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Inagaki M, Kikuchi M, Orino K, Ohnami Y & & Watanabe K 2002 Purification and quantification of lactoferrin in equine seminal plasma. Journal of Veterinary Medical Science 64 75–77. (https://doi.org/10.1292/jvms.64.75)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Juyena NS & & Stelletta C 2012 Seminal plasma: an essential attribute to spermatozoa. Journal of Andrology 33 536–551. (https://doi.org/10.2164/jandrol.110.012583)

  • Kolm G, Knapp E, Wagner R & & Klein D 2007 Lactoferrin, a glycoprotein with immunomodulatory and mast cell stabilising properties, in skin of horses suffering from Culicoides hypersensitivity. Research in Veterinary Science 83 165–170. (https://doi.org/10.1016/j.rvsc.2006.11.007)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kotilainen T, Huhtinen MKT & & Katila T 1994 Sperm-induced leukocytosis in the equine uterus. Theriogenology 41 629–636. (https://doi.org/10.1016/0093-691x(9490173-g)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Li W, Fu K, Lv X, Wang Y, Wang J, Li H, Tian W & & Cao R 2015 Lactoferrin suppresses lipopolysaccharide-induced endometritis in mice via down-regulation of the NF-κB pathway. International Immunopharmacology 28 695–699. (https://doi.org/10.1016/j.intimp.2015.07.040)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lodi L, Henry M & & Paranhos Da Costa M 1995 Behavior of donkey jacks (Equus asinus) breeding horse mares (Equus caballus) at pasture. Biology of Reproduction 1 591–598. (https://doi.org/10.1093/biolreprod/52.monograph_series1.591)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Luo B, Liang H, Zhang S, Qin X, Liu X, Liu W, Zeng F, Wu Y & & Yang X 2015 Novel lactoferrin-conjugated amphiphilic poly (aminoethyl ethylene phosphate)/poly(L-lactide) copolymer nanobubbles for tumor-targeting ultrasonic imaging. International Journal of Nanomedicine 10 5805–5817. (https://doi.org/10.2147/IJN.S83582)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Magalhaes HBM, Canuto LEF, Zhao F, Li M, Li X, Ji C & & Canisso IF 2021 Daily sperm output, spermatogenic efficiency, and sexual behavior of Dezhou donkey jacks mounting jennies in estrus. Journal of Equine Veterinary Science 101 103420. (https://doi.org/10.1016/j.jevs.2021.103420)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Martinez-Colόn GJ & & Moore BB 2018 Prostaglandin E2 as a regulator of immunity to pathogens. Pharmacology and Therapeutics 185 135–146. (https://doi.org/10.1016/j.pharmthera.2017.12.008)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mirό J, Vilés K, García W, Jordana J & & Yeste M 2013 Effect of donkey seminal plasma on sperm movement and sperm–polymorphonuclear neutrophils attachment in vitro. Animal Reproduction Science 140 164–172. (https://doi.org/10.1016/j.anireprosci.2013.06.007)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mirό J, Catalán J, Marín H, Yánez-Ortiz I & & Yeste M 2021 Specific seminal plasma fractions are responsible for the modulation of sperm–PMN binding in the donkey. Animals 11 1388. (https://doi.org/10.3390/ani11051388)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Oliveira RR, Rates DM, Pugliesi G, Ker PG, Arruda RP, Moraes EA & & Carvalho GR 2014 Use of cholesterol-loaded cyclodextrin in donkey semen cryopreservation improves sperm viability but results in low fertility in mares. Reproduction in Domestic Animals 49 845–850. (https://doi.org/10.1111/rda.12379)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Paolucci M, Palombia C, Syllaa L, Stradaioli G & & Monaci M 2012 Ultrasonographic features of the mule embryo, fetus and fetal-placental unit. Theriogenology 77 240–252. (https://doi.org/10.1016/j.theriogenology.2011.07.030)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Podico G & & Canisso IF 2024 Mule embryos share identical morphological features to horse embryos. Theriogenology 216 196–202. (https://doi.org/10.1016/j.theriogenology.2023.11.026)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rota A, Panzani D, Sabatini C & & Camillo F 2012 Donkey jack (Equus asinus) semen cryopreservation: studies of seminal parameters, post breeding inflammatory response, and fertility in donkey jennies. Theriogenology 78 1846–1854. (https://doi.org/10.1016/j.theriogenology.2012.07.015)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sabatini C, Mari G, Mislei B, Love C, Panzani D, Camillo F & & Rota A 2014 Effect of post-thaw addition of seminal plasma on motility, viability and chromatin integrity of cryopreserved donkey jack (Equus asinus) spermatozoa. Reproduction in Domestic Animals 49 989–994. (https://doi.org/10.1111/rda.12419)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Scher JU & & Pillinger MH 2009 The anti-inflammatory effects of prostaglandins. Journal of Investigative Medicine 57 703–708. (https://doi.org/10.2310/JIM.0b013e31819aaa76)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Segabinazzi LGTM, Scheeren VFDC, Freitas-Dell’Aqua CP, Papa FO, Alvarenga MA, Dell’Aqua JA & & Canisso IF 2021 Cholesterol-loaded cyclodextrin addition to skim milk-based extender enhances donkey semen cooling and fertility in horse mares. Journal of Equine Veterinary Science 105 103719. (https://doi.org/10.1016/j.jevs.2021.103719)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Skogstrand K 2012 Multiplex assays of inflammatory markers, a description of methods and discussion of precautions – our experience through the last ten years. Methods 56 204–212. (https://doi.org/10.1016/j.ymeth.2011.09.025)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Troedsson MH, Loset K, Alghamdi AM, Dahms B & & Crabo BG 2001 Interaction between equine semen and the endometrium: the inflammatory response to semen. Animal Reproduction Science 68 273–278. (https://doi.org/10.1016/s0378-4320(0100164-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Troedsson MH, Desvousges A, Alghamdi AS, Dahms B, Dowa CA, Hayna J, Valesco R, Collahan PT, Macpherson ML, Pozor M, et al.2005 Components in seminal plasma regulating sperm transport and elimination. Animal Reproduction Science 89 171–186. (https://doi.org/10.1016/j.anireprosci.2005.07.005)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vidament M, Vincent P, Martin FX, Magistrini M & & Blescois E 2009 Differences in ability of jennies and mares to conceive with cooled and frozen semen containing glycerol or not. Animal Reproduction Science 112 22–35. (https://doi.org/10.1016/j.anireprosci.2008.03.016)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vilés K, Rabanal R, Rodriguéz-Prado M & & Mirό J 2013 Influence of seminal plasma on leucocyte migration and amount of COX-2 protein in the jenny endometrium after insemination with frozen–thawed semen. Animal Reproduction Science 143 57–63. (https://doi.org/10.1016/j.anireprosci.2013.11.002)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Xia J, Psychogios N, Young N & & Wishart DS 2009 MetaboAnalyst: a web server for metabolomics data analysis and interpretation. Nucleic Acids Research 37 W652–W660. (https://doi.org/10.1093/nar/gkp356)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zerbe H, Schuberth HJ, Engelke F, Frank J, Klug E & & Leibold W 2003 Development and comparison of in vivo and in vitro models for endometritis in cows and mares. Theriogenology 60 209–223. (https://doi.org/10.1016/s0093-691x(0201376-6)

    • PubMed
    • Search Google Scholar
    • Export Citation