FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Reprod Domest Anim / Specific microRNAs in stallion spermatozoa are potential bio...
Reproduction in domestic animals = Zuchthygiene2024; 59(7); e14674; doi: 10.1111/rda.14674

Specific microRNAs in stallion spermatozoa are potential biomarkers of high functionality.

Abstract: Males of some species, from horses to humans, require medical help for subfertility problems. There is an urgent need for novel molecular assays that reflect spermatozoal function. In the last 25 years, studies examined RNAs in spermatozoa as a window into gene expression during their development and, more recently, for their functions in early embryo development. In clinics, more dense spermatozoa are isolated by density gradient centrifugation before use in artificial insemination to increase pregnancy rates. The objectives of the current study were to discover and quantify the microRNAs in stallion spermatozoa and identify those with differential expression levels in more dense versus less dense spermatozoa. First, spermatozoa from seven stallions were separated into more dense and less dense populations by density gradient centrifugation. Next, small RNAs were sequenced from each of the 14 RNA samples. We identified 287 different mature microRNAs within the 11,824,720 total mature miRNA reads from stallion spermatozoa. The most prevalent was miR-10a/b-5p. The less dense spermatozoa had fewer mature microRNAs and more microRNA precursor sequences than more dense spermatozoa, perhaps indicating that less dense spermatozoa are less mature. Two of the most prevalent microRNAs in more dense stallion spermatozoa were predicted to target mRNAs that encode proteins that accelerate mRNA decay. Nine microRNAs were more highly expressed in more dense spermatozoa. Three of those microRNAs were predicted to target mRNAs that encode proteins involved in protein decay. Both mRNA and protein decay are very active in late spermiogenesis but not in mature spermatozoa. The identified microRNAs may be part of the mechanism to shut down those processes. The microRNAs with greater expression in more dense spermatozoa may be useful biomarkers for spermatozoa with greater functional capabilities.
© 2024 Wiley‐VCH GmbH. Published by John Wiley & Sons Ltd.
Get Full Text
Publication Date: 2024-07-15 PubMed ID: 39005151DOI: 10.1111/rda.14674Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article addresses the relationship between microRNAs in stallion spermatozoa and fertility, suggesting that specific microRNAs could be used as biomarkers for sperm functionality.

Objective and Methodology

  • The study aims to examine the microRNAs in stallion spermatozoa and evaluate if their expression levels can be indicative of sperm functionality. This investigation was sparked due to the need for more sophisticated molecular assays to address subfertility issues in males of several species, including humans.
  • The researchers isolated spermatozoa from seven stallions and separated them into more dense and less dense populations through density gradient centrifugation. This method is commonly used in clinics to isolate denser spermatozoa, which have been correlated with higher success rates in artificial insemination.
  • The small RNAs from each of these samples were sequenced, yielding a total of 287 different mature microRNAs from 11,824,720 total mature miRNA reads.

Findings

  • The most prevalent microRNA found was miR-10a/b-5p. It was observed that less dense spermatozoa contained fewer mature microRNAs and more microRNA precursor sequences, suggesting that these spermatozoa might be less mature than the denser ones.
  • Two of the most prevalent microRNAs in denser spermatozoa were predicted to target mRNAs encoding proteins involved in accelerating mRNA decay, a process very active in late spermiogenesis but absent in mature spermatozoa.
  • Nine microRNAs were more highly expressed in denser spermatozoa, out of which three were expected to target mRNAs encoding proteins involved in protein decay. This observation led to the suggestion that these microRNAs might be part of the mechanism that ceases these processes.

Implications

  • The microRNAs that are more prevalent in denser spermatozoa might be instrumental in defining sperm functionality, thereby serving as potential biomarkers. Their higher expression in denser spermatozoa indicates a plausible correlation with greater functional capabilities of these spermatozoa.
  • This investigation provides significant insights that could enable the development of more advanced molecular assays for assessing fertility in males. The identified microRNA biomarkers could be supportive tools for fertility clinics to improve the success rate of procedures like artificial insemination.

Cite This Article

APA
Ing NH, Konganti K, Ghaffar N, Johnson CD, Forrest DW, Love CC, Varner DD. (2024). Specific microRNAs in stallion spermatozoa are potential biomarkers of high functionality. Reprod Domest Anim, 59(7), e14674. https://doi.org/10.1111/rda.14674

Publication

Reproduction in domestic animals = Zuchthygiene
ISSN: 1439-0531
NlmUniqueID: 9015668
Country: Germany
Language: English
Volume: 59
Issue: 7
Pages: e14674

Researcher Affiliations

Ing, Nancy H
  • Department of Animal Science, Texas A&M University, College Station, Texas, USA.
Konganti, Kranti
  • Texas A&M Institute for Genome Sciences and Society, Texas A&M University, College Station, Texas, USA.
Ghaffar, Noushin
  • Texas A&M Institute for Genome Sciences and Society, Texas A&M University, College Station, Texas, USA.
Johnson, Charles D
  • AgriLife Genomics and Bioinformatics, Texas A&M University, College Station, Texas, USA.
Forrest, David W
  • Department of Animal Science, Texas A&M University, College Station, Texas, USA.
Love, Charles C
  • Large Animal Clinical Sciences, Texas A&M University, College Station, Texas, USA.
Varner, Dickson D
  • Large Animal Clinical Sciences, Texas A&M University, College Station, Texas, USA.

MeSH Terms

  • Horses
  • Male
  • Animals
  • Spermatozoa / physiology
  • Spermatozoa / metabolism
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Biomarkers / metabolism

References

This article includes 47 references
  1. Abu‐Halima M, Hammadeh M, Schmitt J, Leidinger P, Keller A, Meese E, Backes C. Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertility and Sterility 99(5), 1249–1255.
    doi: 10.1016/j.fertnstert.2012.11.054google scholar: lookup
  2. Aken BL, Ayling S, Barrell D, Clarke L, Curwen V, Fairley S, Fernandez Banet J, Billis K, García Girón C, Hourlier T, Howe K, Kähäri A, Kokocinski F, Martin FJ, Murphy DN, Nag R, Ruffier M, Schuster M, Tang YA, Searle SMJ. The Ensembl gene annotation system. Database 2016, baw093.
    doi: 10.1093/database/baw093google scholar: lookup
  3. Bartel DP. Metazoan microRNAs. Cell 8(173), 20–51.
    doi: 10.1016/j.cell.2018.03.006google scholar: lookup
  4. Bissonnette N, Levesque‐Sergerie JP, Thibault C, Boissonneault G. Spermatozoal transcriptome profiling for bull sperm motility: A potential tool to evaluate semen quality. Reproduction 138(1), 65–80.
    doi: 10.1530/rep‐08‐0503google scholar: lookup
  5. Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30(15), 2114–2120.
    doi: 10.1093/bioinformatics/btu170google scholar: lookup
  6. Capra E, Turri F, Lazzari B, Cremonesi P, Gliozzi TM, Fojadelli I, Stella A, Pizzi F. Small RNA sequencing of cryopreserved semen from single bulls revealed altered miRNAs and piRNAs between high‐ and low‐motile sperm populations. BMC Genomics 18, 14.
    doi: 10.1186/s12864‐016‐3394‐7google scholar: lookup
  7. Chen Q. Sperm RNA‐mediated epigenetic inheritance in mammals: Challenges and opportunities. Reproduction, Fertility and Development 35(1–2), 118–124.
    doi: 10.1071/rd22218google scholar: lookup
  8. Colleoni SC, Lagutina I, Lazzari G, Rodriguez‐Martinez H, Galli C, Morrell JM. New methods for selecting stallion spermatozoa for assisted reproduction. Journal of Equine Veterinary Science 31, 536–541.
    doi: 10.1016/j.jevs.2011.03.009google scholar: lookup
  9. Cui L, Fang L, Zhuang L, Lin CP, Ye Y. Sperm‐borne microRNA‐34c regulates maternal mRNA degradation and preimplantation embryonic development in mice. Reproductive Biology and Endocrinology 21, 40.
    doi: 10.1186/s12958‐023‐01089‐3google scholar: lookup
  10. Curry W, Safranski TJ, Pratt SL. Differential expression of porcine sperm microRNAs and their association with sperm morphology and motility. Theriogenology 76, 1532–1539.
    doi: 10.1016/j.theriogenology.2011.06.025google scholar: lookup
  11. Das PJ, McCarthy F, Vishnoi M, Paria N, Gresham C, Li G, Kachroo P, Sudderth AE, Teague S, Love CC, Varner DD, Chowdhary BP, Raudsepp T. Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA‐seq. PLoS One 8, e56535.
    doi: 10.1371/journal.pone.0056535google scholar: lookup
  12. Dickson DA, Paulus JK, Mensah V, Lem J, Saavedra‐Rodriguez L, Gentry A, Pagidas K, Feig LA. Reduced levels of miRNAs 449 and 34 in sperm of mice and men exposed to early life stress. Translational Psychiatry 8, 101.
    doi: 10.1038/s41398‐018‐0146‐2google scholar: lookup
  13. Dlamini NH, Nguyen T, Gad A, Tesfaye D, Liao SF, Willard ST, Ryan PL, Feugang JM. Characterization of extracellular vesicle‐coupled miRNA profiles in seminal plasma of boars with divergent semen quality status. International Journal of Molecular Sciences 24, 3194.
    doi: 10.3390/ijms24043194google scholar: lookup
  14. Fagerlind M, Stalhammar H, Olsson B, Klinga‐Levan K. Expression of miRNAs in bull spermatozoa correlates with fertility rates. Reproduction in Domestic Animals 50, 587–594.
    doi: 10.1111/rda.12531google scholar: lookup
  15. Gilbert I, Bissonnette N, Boissonneault G, Vallee M, Robert C. A molecular analysis of the population of mRNA in bovine spermatozoa. Reproduction 133, 1073–1086.
    doi: 10.1530/rep‐06‐0292google scholar: lookup
  16. Godia M, Estill M, Castello A, Belasch S, Rodriguez‐Gil JE, Krawetz SA, Sanchez A, Clop A. A RNA‐Seq analysis to describe the boar sperm transcriptome and its seasonal changes. Frontiers in Genetics 10, 299.
    doi: 10.3389/fgebe.2019.00299google scholar: lookup
  17. Ha M, Kim N. Regulation of microRNA biogenesis. Nature Reviews 15, 509524.
    doi: 10.1038/nrm3838google scholar: lookup
  18. Hamatani T. Human spermatozoal RNAs. Fertility and Sterility 97(2), 275–281.
    doi: 10.1016/j.fertnstert.2011.12.035google scholar: lookup
  19. Hamilton M, Russell S, Menezes K, Moskovtsev SI, Librach C. Assessing spermatozoal small ribonucleic acids and their relationship to blastocyst development in idiopathic infertility males. Scientific Reports 12, 20010.
    doi: 10.1038/s41598‐022‐24568‐wgoogle scholar: lookup
  20. Hua M, Liu W, Chen Y, Zhang F, Xu B, Liu S, Chen G, Shi H, Wu L. Identification of small non‐coding RNAs as sperm quality biomarkers for in vitro fertilization. Cell Discovery 5, 20.
    doi: 10.1038/s41421‐019‐0087‐9google scholar: lookup
  21. Ing NH, Forrest DW, Love CC, Varner DD. Dense spermatozoa in stallion ejaculates contain lower concentrations of mRNAs encoding the sperm‐specific calcium channel 1, ornithine decarboxylase antizyme 3, aromatase, and estrogen receptor alpha than less dense spermatozoa. Theriogenology 82, 347–353.
    doi: 10.1016/j.theriogenology.2014.04.016google scholar: lookup
  22. Ing NH, Konganti K, Ghaffari N, Johnson CD, Forrest D, Love CC, Varner DD. Identification and quantification of coding and long non‐coding RNAs in stallion spermatozoa separated by density. Andrology 8, 1409–1418.
    doi: 10.1111/andr.12791google scholar: lookup
  23. Jaglan K, Dhaka SS, Magotra A, Patil CS. Exploring microRNA biogenesis, applications and bioinformatics in livestock: A comprehensive review. Reproduction in Domestic Animals 59, e14529.
    doi: 10.1111/rda.14529google scholar: lookup
  24. Johnson GD, Sendler E, Lalancette C, Hauser R, Diamond MP, Krawetz SA. Cleavage of rRNA ensures translational cessation in sperm at fertilization. Molecular Human Reproduction 17(12), 721–726.
    doi: 10.1093/molehr/gar054google scholar: lookup
  25. Joshi M, Andrabi SW, Yadav RK, Sankhwar SN, Gupta G, Rajender S. Qualitative and quantitative assessment of sperm miRNAs identifies has‐miR‐9‐3p, has‐miR‐30b‐5p and has‐miR‐122‐5p a potential biomarkers of male inferetility and sperm quality. Reproductive Biology and Endocrinology 20, 122.
    doi: 10.1186/s12958‐022‐00990‐7google scholar: lookup
  26. Joshi M, Sethi S, Mehta P, Kumari A, Rajender S. Small RNAs, spermatogenesis, and male infertility: A decade of retrospect. Reproductive Biology and Endocrinology 21, 106.
    doi: 10.1186/s12958‐023‐01155‐wgoogle scholar: lookup
  27. Kataruka S, Kinterova V, Horvat F, Kulmann MIR, Kanka J, Svoboda P. Physiologically relevant miRNAs in mammalian oocytes are rare and highly abundant. EMBO Reports 23(6), e53514.
    doi: 10.15252/embr.202153514google scholar: lookup
  28. Kotaja N. MicroRNAs and spermatogenesis. Fertilty and Sterility 101, 1552–1562.
    doi: 10.1016/j.fertnstert.2014.04.025google scholar: lookup
  29. Krawetz SA, Kruger A, Lalancette C, Tagett R, Anton E, Draghici S, Diamond MP. A survey of small RNAs in human sperm. Human Reproduction 26(12), 3401–3412.
    doi: 10.1093/humrep/der329google scholar: lookup
  30. Linschooten JO, Van Schooten FJ, Baumgartner A, Cemeli E, Van Delft J, Anderson D, Godschalk RW. Use of spermatozoal mRNA profiles to study gene‐environment interactions in human germ cells. Mutation Research 667(1–2), 70–76.
    doi: 10.1016/j.mrfmmm.2008.12.014google scholar: lookup
  31. Love MI, Hubr W, Anders S. Moderated estimation of fold change and dispersion for RNA‐Seq data with DESeq2. Genome Biology 15, 550.
    doi: 10.1186/s13059‐014‐0550‐8google scholar: lookup
  32. Miller D. Sperm RNA as a mediator of genomic plasticity. Advances in Biology 2014, 179701.
    doi: 10.1155/2014/179701google scholar: lookup
  33. Morgan M, Kumar L, Li Y, Baptissart M. Post‐transcriptional regulation in spermatogenesis: All RNA pathways lead to healthy sperm. Cellular and Molecular Life Sciences 78, 8049–8071.
    doi: 10.1007/s00018‐021‐04012‐4google scholar: lookup
  34. Nixon B, Stanger SJ, Mihalas BP, Reilly JN, Anderson AL, Tyagi S, Holt JE, McLaughlin EA. The microRNA signature of mouse spermatozoa is substantially modified during epididymal maturation. Biology of Reproduction 93(4), 1–20.
    doi: 10.1095/biolreprod.115.132209google scholar: lookup
  35. Ostermeier GC, Dix DJ, Miller D, Khatri P, Krawetz SA. Spermatozoal RNA profiles of normal fertile men. Lancet 360(9335), 772–777.
    doi: 10.1016/s0140‐6736(02)09899‐9google scholar: lookup
  36. Palovita P, Hyden‐Granskog C, Yohannes DA, Paluoja P, Kere J, Tapanainen JS, Krjutskov K, Tuuri T, Vosa U, Vuoristo S. Small RNA expression and miRNA modification dynamics in human oocytes and early embryos. Genome Research 31, 1474–1485.
    doi: 10.1101/gr.268193.120google scholar: lookup
  37. Royo H, Seitz H, Ellnati E, Peters AHFM, Stadler MB, Turner JMA. Silencing of X‐linked microRNAs by meiotic sex chromosome inactivation. PLoS Genetics 11, e1005461.
    doi: 10.1371/journal.pgen.1005461google scholar: lookup
  38. Russell SJ, Stalker L, LaMarre J. PIWIs, piRNAs and retrotransposons: Complex battles during reprogramming in gametes and early embryos. Reproduction in Domestic Animals 52(Suppl 4), 28–38.
    doi: 10.1111/rda.13053google scholar: lookup
  39. Sellem E, Marthey S, Jouneau L, Bonnet A, Perrier J‐P, Fritz S, Le Danvic C, Boussaha M, Kiefer H, Jammes H, Schibler L. A comprehensive overview of bull sperm‐borne small non‐coding RNAs and their diversity across breeds. Epigenetics & Chromatin 13, 19.
    doi: 10.1186/s13072‐020‐00340‐0google scholar: lookup
  40. Uhen M, Fagerberg L, Hallstrom BM. Tissue‐based map of the human proteome. Science 347(6220), 1260419.
    doi: 10.1126/science.1260419google scholar: lookup
  41. Varner DD, Love CC, Brinsko SP, Blanchard TL, Hartman TJ, Bliss SB, Carroll BS, Eslick MC. Semen processing for the subfertile stallion. Journal of Equine Veterinary Science 28(11), 677–685.
    doi: 10.1016/j.jevs.2008.10.012google scholar: lookup
  42. Werry N, Russell SJ, Gillis DJ, Miller S, Kickey K, Larmer S, Lohuis M, Librach C. Characteristics of miRNAs present in bovine sperm and associations with differences in fertility. Frontiers in Endocrinology 13, 874371.
    doi: 10.3389/fendo.2022.874371google scholar: lookup
  43. Xiong Y, Yu C, Zhang Q. Ubiquitin‐proteasome system‐regulated protein degradation in spermatogenesis. Cells 11, 1058.
    doi: 10.3390/cells11061058google scholar: lookup
  44. Yang C, Zeng QX, Liu JC, Yeung WSB, Zhang JV, Duan YG. Role of small RNAs harbored by sperm in embryonic development and offspring phenotype. Andrology 11, 770–782.
    doi: 10.1111/andr.13347google scholar: lookup
  45. Yuan S, Schuster A, Tang C, Yu T, Ortogero N, Bao J, Zheng H, Yan W. Sperm‐borne miRNAs and endo‐siRNAs are important for fertilization and preimplantation embryonic development. Development 143, 635–647.
    doi: 10.1242/dev.131755google scholar: lookup
  46. Yuan S, Tang C, Zhang Y, Wu J, Bao J, Zheng H, Xu C, Yan W. Mir‐34b/c and mir‐449a/b/c are required for spermatogenesis but not for the first cleavage division in mice. Biology Open 4, 212–223.
    doi: 10.1242/bio.201410959google scholar: lookup
  47. Zhang Y, Shi J, Rassoulzadegan M, Tuorto F, Chen Q. Sperm RNA code programmes the metabolic health of offspring. Nature Reviews 15, 489–498.
    doi: 10.1038/s41574‐019‐0226‐2google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.