FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Int J Mol Sci / Transcriptomics Reveal Molecular Differences in Equine Oocyt...
International journal of molecular sciences2023; 24(8); 6915; doi: 10.3390/ijms24086915

Transcriptomics Reveal Molecular Differences in Equine Oocytes Vitrified before and after In Vitro Maturation.

Abstract: In the last decade, in vitro embryo production in horses has become an established clinical practice, but blastocyst rates from vitrified equine oocytes remain low. Cryopreservation impairs the oocyte developmental potential, which may be reflected in the messenger RNA (mRNA) profile. Therefore, this study aimed to compare the transcriptome profiles of metaphase II equine oocytes vitrified before and after in vitro maturation. To do so, three groups were analyzed with RNA sequencing: (1) fresh in vitro matured oocytes as a control (FR), (2) oocytes vitrified after in vitro maturation (VMAT), and (3) oocytes vitrified immature, warmed, and in vitro matured (VIM). In comparison with fresh oocytes, VIM resulted in 46 differentially expressed (DE) genes (14 upregulated and 32 downregulated), while VMAT showed 36 DE genes (18 in each category). A comparison of VIM vs. VMAT resulted in 44 DE genes (20 upregulated and 24 downregulated). Pathway analyses highlighted cytoskeleton, spindle formation, and calcium and cation ion transport and homeostasis as the main affected pathways in vitrified oocytes. The vitrification of in vitro matured oocytes presented subtle advantages in terms of the mRNA profile over the vitrification of immature oocytes. Therefore, this study provides a new perspective for understanding the impact of vitrification on equine oocytes and can be the basis for further improvements in the efficiency of equine oocyte vitrification.
Get Full Text
Publication Date: 2023-04-07 PubMed ID: 37108081PubMed Central: PMC10138936DOI: 10.3390/ijms24086915Google 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.

This research focuses on studying the differences at molecular level in horse eggs (oocytes) vitrified (freezing process) before and after lab-based maturation. The goal is to increase understanding of the impact of cryopreservation on these oocytes, with a view to improving horse embryo production in vitro.

Overview of the Study

  • The research is conducted in the context of in vitro embryo production in horses, a widely accepted clinical practice. The main challenge faced in this practice is the low blastocyst rates from vitrified equine oocytes. Cryopreservation, or the freezing process, seems to affect the developmental potential of the oocytes, and this effect can be seen in the messenger RNA (mRNA) profile of the oocytes.
  • The researchers, therefore, aimed to compare the mRNA profiles or transcriptomes of mature equine oocytes that were vitrified either before or after in vitro maturation. They analyzed three groups of oocytes with RNA sequencing: fresh in vitro matured oocytes as a control, oocytes vitrified after maturation, and oocytes which were vitrified while immature, then warmed and matured in vitro.

Findings of the Study

  • The researchers found differences in gene expression between the vitrified groups and the fresh group. Comparing vitrified immature oocytes (VIM) with fresh oocytes, they identified 46 differentially expressed (DE) genes, of which 14 were upregulated (increased in expression) and 32 were downregulated (decreased in expression).
  • In contrast, 36 DE genes were found when comparing oocytes vitrified after maturation (VMAT) with fresh oocytes, with 18 each in the upregulated and downregulated categories.
  • Comparing VIM with VMAT resulted in 44 DE genes, with 20 upregulated and 24 downregulated. Therefore, there were molecular differences in oocytes vitrified before and after in vitro.
  • The researchers conducted pathway analyses, looking at activities or functions that involved more than one gene. They found that the main pathways affected in vitrified oocytes were cytoskeleton, spindle formation, and calcium and cation ion transport and homeostasis. This tells us about the potential effects of vitrification on oocyte functions.
  • Overall, they found that vitrifying oocytes after in vitro maturation had some minor advantages over vitrifying them while still immature, when looking at the mRNA profiles. However, both methods did result in significant transcriptional changes.

Impact of the Study

  • This research has added a new perspective to our understanding of the impact of vitrification on equine oocytes. It has provided valuable insights for improving the efficiency of equine oocyte vitrification, thereby potentially increasing the success rates of in vitro horse embryo production.

Cite This Article

APA
Angel-Velez D, Meese T, Hedia M, Fernandez-Montoro A, De Coster T, Pascottini OB, Van Nieuwerburgh F, Govaere J, Van Soom A, Pavani K, Smits K. (2023). Transcriptomics Reveal Molecular Differences in Equine Oocytes Vitrified before and after In Vitro Maturation. Int J Mol Sci, 24(8), 6915. https://doi.org/10.3390/ijms24086915

Publication

International journal of molecular sciences
ISSN: 1422-0067
NlmUniqueID: 101092791
Country: Switzerland
Language: English
Volume: 24
Issue: 8
PII: 6915

Researcher Affiliations

Angel-Velez, Daniel
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.
  • Research Group in Animal Sciences-INCA-CES, Universidad CES, Medellin 050021, Colombia.
Meese, Tim
  • Laboratory for Pharmaceutical Biotechnology, Faculty of Pharmaceutical Science, Ghent University, 9000 Ghent, Belgium.
Hedia, Mohamed
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.
  • Department of Theriogenology, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt.
Fernandez-Montoro, Andrea
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.
De Coster, Tine
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.
Pascottini, Osvaldo Bogado
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.
Van Nieuwerburgh, Filip
  • Laboratory for Pharmaceutical Biotechnology, Faculty of Pharmaceutical Science, Ghent University, 9000 Ghent, Belgium.
Govaere, Jan
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.
Van Soom, Ann
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.
Pavani, Krishna
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.
  • Department for Reproductive Medicine, Ghent University Hospital, Corneel Heymanslaan 10, 9000 Gent, Belgium.
Smits, Katrien
  • Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium.

MeSH Terms

  • Horses / genetics
  • Animals
  • In Vitro Oocyte Maturation Techniques / methods
  • Transcriptome
  • Oocytes / metabolism
  • Cryopreservation / veterinary
  • Cryopreservation / methods
  • Vitrification

Grant Funding

  • 2018000504 (GOA030-18 BOF / Bijzonder Onderzoeksfonds GOA (Geconcerteerde onderzoeksacties)
  • 860960 / European Union's Horizon 2020 research and innovation program under the Marie Sku0142odow-ska-Curie
  • 1139820N, 1228821N, and 12Y5220N / Research Foundation Flanders
  • NA / COLFUTURO and and the Ministerio de Ciencia Tecnologu00eda Innovaciu00f3n

Conflict of Interest Statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

This article includes 105 references
  1. De Coster T, Velez DA, Van Soom A, Woelders H, Smits K. Cryopreservation of equine oocytes: looking into the crystal ball.. Reprod Fertil Dev 2020 Mar;32(5):453-467.
    doi: 10.1071/RD19229pubmed: 32172776google scholar: lookup
  2. Maclellan LJ, Carnevale EM, Coutinho da Silva MA, Scoggin CF, Bruemmer JE, Squires EL. Pregnancies from vitrified equine oocytes collected from super-stimulated and non-stimulated mares.. Theriogenology 2002 Sep;58(5):911-9.
    doi: 10.1016/S0093-691X(02)00920-2pubmed: 12212891google scholar: lookup
  3. Ortiz-Escribano N, Bogado Pascottini O, Woelders H, Vandenberghe L, De Schauwer C, Govaere J, Van den Abbeel E, Vullers T, Ververs C, Roels K, Van De Velde M, Van Soom A, Smits K. An improved vitrification protocol for equine immature oocytes, resulting in a first live foal.. Equine Vet J 2018 May;50(3):391-397.
    doi: 10.1111/evj.12747pubmed: 28833413google scholar: lookup
  4. Tharasanit T, Colenbrander B, Stout TA. Effect of maturation stage at cryopreservation on post-thaw cytoskeleton quality and fertilizability of equine oocytes.. Mol Reprod Dev 2006 May;73(5):627-37.
    doi: 10.1002/mrd.20432pubmed: 16477611google scholar: lookup
  5. Canesin HS, Brom-de-Luna JG, Choi YH, Pereira AM, Macedo GG, Hinrichs K. Vitrification of germinal-vesicle stage equine oocytes: Effect of cryoprotectant exposure time on in-vitro embryo production.. Cryobiology 2018 Apr;81:185-191.
    doi: 10.1016/j.cryobiol.2018.01.001pubmed: 29305835google scholar: lookup
  6. Angel D, Canesin HS, Brom-de-Luna JG, Morado S, Dalvit G, Gomez D, Posada N, Pascottini OB, Urrego R, Hinrichs K, Velez IC. Embryo development after vitrification of immature and in vitro-matured equine oocytes.. Cryobiology 2020 Feb 1;92:251-254.
    doi: 10.1016/j.cryobiol.2020.01.014pubmed: 31962104google scholar: lookup
  7. Angel-Velez D, De Coster T, Azari-Dolatabad N, Fernandez-Montoro A, Benedetti C, Bogado Pascottini O, Woelders H, Van Soom A, Smits K. New Alternative Mixtures of Cryoprotectants for Equine Immature Oocyte Vitrification.. Animals (Basel) 2021 Oct 28;11(11).
    doi: 10.3390/ani11113077pmc: PMC8614364pubmed: 34827809google scholar: lookup
  8. Clérico G, Taminelli G, Veronesi JC, Polola J, Pagura N, Pinto C, Sansinena M. Mitochondrial function, blastocyst development and live foals born after ICSI of immature vitrified/warmed equine oocytes matured with or without melatonin.. Theriogenology 2021 Jan 15;160:40-49.
    doi: 10.1016/j.theriogenology.2020.10.036pubmed: 33171351google scholar: lookup
  9. Edgar DH, Gook DA. A critical appraisal of cryopreservation (slow cooling versus vitrification) of human oocytes and embryos.. Hum Reprod Update 2012 Sep-Oct;18(5):536-54.
    doi: 10.1093/humupd/dms016pubmed: 22537859google scholar: lookup
  10. Kuwayama M, Vajta G, Kato O, Leibo SP. Highly efficient vitrification method for cryopreservation of human oocytes.. Reprod Biomed Online 2005 Sep;11(3):300-8.
    doi: 10.1016/S1472-6483(10)60837-1pubmed: 16176668google scholar: lookup
  11. Papis K, Shimizu M, Saha S, Izaike Y, Modliński JA. Effects of Vitrification of Partially Denuded Bovine Immature Oocytes.. Anim. Sci. Pap. Rep. 2013;31:14.
  12. Somfai T, Nakai M, Tanihara F, Noguchi J, Kaneko H, Kashiwazaki N, Egerszegi I, Nagai T, Kikuchi K. Comparison of ethylene glycol and propylene glycol for the vitrification of immature porcine oocytes.. J Reprod Dev 2013;59(4):378-84.
    doi: 10.1262/jrd.2013-015pmc: PMC3944359pubmed: 23666455google scholar: lookup
  13. Wu G, Jia B, Quan G, Xiang D, Zhang B, Shao Q, Hong Q. Vitrification of porcine immature oocytes: Association of equilibration manners with warming procedures, and permeating cryoprotectants effects under two temperatures.. Cryobiology 2017 Apr;75:21-27.
    doi: 10.1016/j.cryobiol.2017.03.001pubmed: 28283337google scholar: lookup
  14. Van Blerkom J, Davis PW. Cytogenetic, cellular, and developmental consequences of cryopreservation of immature and mature mouse and human oocytes.. Microsc Res Tech 1994 Feb 1;27(2):165-93.
    doi: 10.1002/jemt.1070270209pubmed: 8123908google scholar: lookup
  15. Gasparrini B, Attanasio L, De Rosa A, Monaco E, Di Palo R, Campanile G. Cryopreservation of in vitro matured buffalo (Bubalus bubalis) oocytes by minimum volumes vitrification methods.. Anim Reprod Sci 2007 Apr;98(3-4):335-42.
    doi: 10.1016/j.anireprosci.2006.04.046pubmed: 16698202google scholar: lookup
  16. Sripunya N, Somfai T, Inaba Y, Nagai T, Imai K, Parnpai R. A comparison of cryotop and solid surface vitrification methods for the cryopreservation of in vitro matured bovine oocytes.. J Reprod Dev 2010 Feb;56(1):176-81.
    doi: 10.1262/jrd.09-108Hpubmed: 19815985google scholar: lookup
  17. Liu Y, Du Y, Lin L, Li J, Kragh PM, Kuwayama M, Bolund L, Yang H, Vajta G. Comparison of efficiency of open pulled straw (OPS) and Cryotop vitrification for cryopreservation of in vitro matured pig oocytes.. Cryo Letters 2008 Jul-Aug;29(4):315-20.
    pubmed: 19137194
  18. Song WY, Peng ZF, Chen XM, Jin HX, Yao GD, Shi SL, Yang HY, Zhang XY, Sun YP. Effects of Vitrification on Outcomes of In Vivo-Mature, In Vitro-Mature and Immature Human Oocytes.. Cell Physiol Biochem 2016;38(5):2053-62.
    doi: 10.1159/000445564pubmed: 27165189google scholar: lookup
  19. Sprícigo JF, Morais K, Ferreira AR, Machado GM, Gomes AC, Rumpf R, Franco MM, Dode MA. Vitrification of bovine oocytes at different meiotic stages using the Cryotop method: assessment of morphological, molecular and functional patterns.. Cryobiology 2014 Oct;69(2):256-65.
    doi: 10.1016/j.cryobiol.2014.07.015pubmed: 25106744google scholar: lookup
  20. Chaves DF, Corbin E, Almiñana C, Locatelli Y, Souza-Fabjan JM, Bhat MH, Freitas VJ, Mermillod P, Sou-za-Fabjan JMG, Freitas VJF. Vitrification of Immature and in Vitro Matured Bovine Cumulus-Oocyte Complexes: Effects on Oocyte Structure and Embryo Development.. Livest. Sci. 2017;199:50–56.
    doi: 10.1016/j.livsci.2017.02.022google scholar: lookup
  21. Mogas T. Update on the vitrification of bovine oocytes and invitro-produced embryos.. Reprod Fertil Dev 2018 Jan;31(1):105-117.
    doi: 10.1071/RD18345pubmed: 32188546google scholar: lookup
  22. Zhou XL, Al Naib A, Sun DW, Lonergan P. Bovine oocyte vitrification using the Cryotop method: effect of cumulus cells and vitrification protocol on survival and subsequent development.. Cryobiology 2010 Aug;61(1):66-72.
    doi: 10.1016/j.cryobiol.2010.05.002pubmed: 20510225google scholar: lookup
  23. Díez C, Muñoz M, Caamaño JN, Gómez E. Cryopreservation of the bovine oocyte: current status and perspectives.. Reprod Domest Anim 2012 Jun;47 Suppl 3:76-83.
    doi: 10.1111/j.1439-0531.2012.02029.xpubmed: 22681301google scholar: lookup
  24. Ishii T, Tomita K, Sakakibara H, Ohkura S. Embryogenesis of vitrified mature bovine oocytes is improved in the presence of multi-layered cumulus cells.. J Reprod Dev 2018 Feb 27;64(1):95-99.
    doi: 10.1262/jrd.2017-095pmc: PMC5830364pubmed: 29057767google scholar: lookup
  25. Dujíčková L, Makarevich AV, Olexiková L, Kubovičová E, Strejček F. Methodological approaches for vitrification of bovine oocytes.. Zygote 2021 Feb;29(1):1-11.
    doi: 10.1017/S0967199420000465pubmed: 32885775google scholar: lookup
  26. Rojas C, Palomo MJ, Albarracín JL, Mogas T. Vitrification of immature and in vitro matured pig oocytes: study of distribution of chromosomes, microtubules, and actin microfilaments.. Cryobiology 2004 Dec;49(3):211-20.
    doi: 10.1016/j.cryobiol.2004.07.002pubmed: 15615607google scholar: lookup
  27. Purohit GN, Meena H, Solanki K. Effects of Vitrification on Immature and in vitro Matured, Denuded and Cumulus Compact Goat Oocytes and Their Subsequent Fertilization.. J Reprod Infertil 2012 Jan;13(1):53-9.
    pmc: PMC3719371pubmed: 23926524
  28. Maclellan LJ, Stokes JE, Preis KA, Mccue PM, Carnevale EM. Vitrification, Warming, ICSI and Transfer of Equine Oocytes Matured in Vivo.. Anim. Reprod. Sci. 2010;121:260–261.
    doi: 10.1016/j.anireprosci.2010.04.157google scholar: lookup
  29. Roser JF, Meyers-Brown G. Superovulation in the Mare: A Work in Progress.. J. Equine Veter Sci. 2012;32:376–386.
    doi: 10.1016/j.jevs.2012.05.055google scholar: lookup
  30. Tharasanit T, Colleoni S, Galli C, Colenbrander B, Stout TA. Protective effects of the cumulus-corona radiata complex during vitrification of horse oocytes.. Reproduction 2009 Mar;137(3):391-401.
    doi: 10.1530/REP-08-0333pubmed: 19073713google scholar: lookup
  31. Agnieszka N, Joanna K, Wojciech W, Adam O. In vitro maturation of equine oocytes followed by two vitrification protocols and subjected to either intracytoplasmic sperm injection (ICSI) or parthenogenic activation.. Theriogenology 2021 Mar 1;162:42-48.
    doi: 10.1016/j.theriogenology.2020.12.022pubmed: 33444915google scholar: lookup
  32. Ducheyne K, Rizzo M, Beitsma M, Deelen C, Daels P, Stout T, De Ruijter-Villani M. Vitrifying Equine Oocytes at the Germinal Vesicle Stage Disturbs Spindle Morphology and Chromosome Alignment.. J. Equine Veter Sci. 2018;66:178.
    doi: 10.1016/j.jevs.2018.05.070google scholar: lookup
  33. Dalcin L, Silva RC, Paulini F, Silva BD, Neves JP, Lucci CM. Cytoskeleton structure, pattern of mitochondrial activity and ultrastructure of frozen or vitrified sheep embryos.. Cryobiology 2013 Oct;67(2):137-45.
    doi: 10.1016/j.cryobiol.2013.05.012pubmed: 23770514google scholar: lookup
  34. Fu XW, Shi WQ, Zhang QJ, Zhao XM, Yan CL, Hou YP, Zhou GB, Fan ZQ, Suo L, Wusiman A, Wang YP, Zhu SE. Positive effects of Taxol pretreatment on morphology, distribution and ultrastructure of mitochondria and lipid droplets in vitrification of in vitro matured porcine oocytes.. Anim Reprod Sci 2009 Oct;115(1-4):158-68.
    doi: 10.1016/j.anireprosci.2008.12.002pubmed: 19131190google scholar: lookup
  35. Gutnisky C, Morado S, Gadze T, Donato A, Alvarez G, Dalvit G, Cetica P. Morphological, biochemical and functional studies to evaluate bovine oocyte vitrification.. Theriogenology 2020 Feb;143:18-26.
    doi: 10.1016/j.theriogenology.2019.11.037pubmed: 31830686google scholar: lookup
  36. Berthelot-Ricou A, Perrin J, di Giorgio C, de Meo M, Botta A, Courbiere B. Assessment of 1,2-propanediol (PrOH) genotoxicity on mouse oocytes by comet assay.. Fertil Steril 2011 Oct;96(4):1002-7.
    doi: 10.1016/j.fertnstert.2011.07.1106pubmed: 21890131google scholar: lookup
  37. Ishida GM, Saito H, Ohta N, Takahashi T, Ito MM, Saito T, Nakahara K, Hiroi M. The optimal equilibration time for mouse embryos frozen by vitrification with trehalose.. Hum Reprod 1997 Jun;12(6):1259-62.
    doi: 10.1093/humrep/12.6.1259pubmed: 9222013google scholar: lookup
  38. Sterzik K, Rosenbusch B, Grab D, Wahl A, Beier HM, Lauritzen C. Numerical chromosome anomalies after fertilization of freeze-thawed mouse oocytes.. Arch Gynecol Obstet 1992;251(3):133-8.
    doi: 10.1007/BF02718375pubmed: 1605678google scholar: lookup
  39. Tamura AN, Huang TT, Marikawa Y. Impact of vitrification on the meiotic spindle and components of the microtubule-organizing center in mouse mature oocytes.. Biol Reprod 2013 Nov;89(5):112.
    doi: 10.1095/biolreprod.113.108167pmc: PMC4076379pubmed: 24025740google scholar: lookup
  40. Hinrichs K, Choi YH, Love LB, Varner DD, Love CC, Walckenaer BE. Chromatin configuration within the germinal vesicle of horse oocytes: changes post mortem and relationship to meiotic and developmental competence.. Biol Reprod 2005 May;72(5):1142-50.
    doi: 10.1095/biolreprod.104.036012pubmed: 15647456google scholar: lookup
  41. de Leon PM, Campos VF, Corcini CD, Santos EC, Rambo G, Lucia T Jr, Deschamps JC, Collares T. Cryopreservation of immature equine oocytes, comparing a solid surface vitrification process with open pulled straws and the use of a synthetic ice blocker.. Theriogenology 2012 Jan 1;77(1):21-7.
    doi: 10.1016/j.theriogenology.2011.07.008pubmed: 21835449google scholar: lookup
  42. Canesin HS, Brom-de-Luna JG, Choi YH, Ortiz I, Diaw M, Hinrichs K. Blastocyst development after intracytoplasmic sperm injection of equine oocytes vitrified at the germinal-vesicle stage.. Cryobiology 2017 Apr;75:52-59.
    doi: 10.1016/j.cryobiol.2017.02.004pubmed: 28209499google scholar: lookup
  43. Chen JY, Li XX, Xu YK, Wu H, Zheng JJ, Yu XL. Developmental competence and gene expression of immature oocytes following liquid helium vitrification in bovine.. Cryobiology 2014 Dec;69(3):428-33.
    doi: 10.1016/j.cryobiol.2014.09.380pubmed: 25307439google scholar: lookup
  44. Ebrahimi B, Valojerdi MR, Eftekhari-Yazdi P, Baharvand H, Farrokhi A. IVM and gene expression of sheep cumulus-oocyte complexes following different methods of vitrification.. Reprod Biomed Online 2010 Jan;20(1):26-34.
    doi: 10.1016/j.rbmo.2009.10.020pubmed: 20158984google scholar: lookup
  45. Azari M, Kafi M, Ebrahimi B, Fatehi R, Jamalzadeh M. Oocyte maturation, embryo development and gene expression following two different methods of bovine cumulus-oocyte complexes vitrification.. Vet Res Commun 2017 Mar;41(1):49-56.
    doi: 10.1007/s11259-016-9671-8pubmed: 27943152google scholar: lookup
  46. Turathum B, Saikhun K, Sangsuwan P, Kitiyanant Y. Effects of vitrification on nuclear maturation, ultrastructural changes and gene expression of canine oocytes.. Reprod Biol Endocrinol 2010 Jun 22;8:70.
    doi: 10.1186/1477-7827-8-70pmc: PMC2916914pubmed: 20565987google scholar: lookup
  47. Stigliani S, Moretti S, Anserini P, Casciano I, Venturini PL, Scaruffi P. Storage time does not modify the gene expression profile of cryopreserved human metaphase II oocytes.. Hum Reprod 2015 Nov;30(11):2519-26.
    doi: 10.1093/humrep/dev232pubmed: 26385790google scholar: lookup
  48. Monzo C, Haouzi D, Roman K, Assou S, Dechaud H, Hamamah S. Slow freezing and vitrification differentially modify the gene expression profile of human metaphase II oocytes.. Hum Reprod 2012 Jul;27(7):2160-8.
    doi: 10.1093/humrep/des153pubmed: 22587994google scholar: lookup
  49. Barberet J, Ducreux B, Bruno C, Guilleman M, Simonot R, Lieury N, Guilloteau A, Bourc'his D, Fauque P. Comparison of oocyte vitrification using a semi-automated or a manual closed system in human siblings: survival and transcriptomic analyses.. J Ovarian Res 2022 Dec 5;15(1):128.
    doi: 10.1186/s13048-022-01064-3pmc: PMC9720994pubmed: 36464714google scholar: lookup
  50. Ma Y, Long C, Liu G, Bai H, Ma L, Bai T, Zuo Y, Li S. WGBS combined with RNA-seq analysis revealed that Dnmt1 affects the methylation modification and gene expression changes during mouse oocyte vitrification.. Theriogenology 2022 Jan 1;177:11-21.
    doi: 10.1016/j.theriogenology.2021.09.032pubmed: 34653792google scholar: lookup
  51. Gao L, Jia G, Li A, Ma H, Huang Z, Zhu S, Hou Y, Fu X. RNA-Seq transcriptome profiling of mouse oocytes after in vitro maturation and/or vitrification.. Sci Rep 2017 Oct 16;7(1):13245.
    doi: 10.1038/s41598-017-13381-5pmc: PMC5643491pubmed: 29038524google scholar: lookup
  52. Huang J, Ma Y, Wei S, Pan B, Qi Y, Hou Y, Meng Q, Zhou G, Han H. Dynamic changes in the global transcriptome of bovine germinal vesicle oocytes after vitrification followed by in vitro maturation.. Reprod Fertil Dev 2018 Oct;30(10):1298-1313.
    doi: 10.1071/RD17535pubmed: 29661269google scholar: lookup
  53. Wang N, Li CY, Zhu HB, Hao HS, Wang HY, Yan CL, Zhao SJ, Du WH, Wang D, Liu Y, Pang YW, Zhao XM. Effect of vitrification on the mRNA transcriptome of bovine oocytes.. Reprod Domest Anim 2017 Aug;52(4):531-541.
    doi: 10.1111/rda.12942pubmed: 28295644google scholar: lookup
  54. Zhang F, Zhang ZY, Cai MD, Li XX, Li YH, Lei Y, Yu XL. Effect of vitrification temperature and cryoprotectant concentrations on the mRNA transcriptome of bovine mature oocytes after vitrifying at immature stage.. Theriogenology 2020 May;148:225-235.
    doi: 10.1016/j.theriogenology.2019.11.006pubmed: 31761539google scholar: lookup
  55. Jia BY, Xiang DC, Quan GB, Zhang B, Shao QY, Hong QH, Wu GQ. Transcriptome analysis of porcine immature oocytes and surrounding cumulus cells after vitrification and in vitro maturation.. Theriogenology 2019 Aug;134:90-97.
    doi: 10.1016/j.theriogenology.2019.05.019pubmed: 31158735google scholar: lookup
  56. Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: oocytes carry the conversation.. Science 2002 Jun 21;296(5576):2178-80.
    doi: 10.1126/science.1071965pubmed: 12077402google scholar: lookup
  57. Labrecque R, Sirard MA. The study of mammalian oocyte competence by transcriptome analysis: progress and challenges.. Mol Hum Reprod 2014 Feb;20(2):103-16.
    doi: 10.1093/molehr/gat082pubmed: 24233546google scholar: lookup
  58. Telford NA, Watson AJ, Schultz GA. Transition from maternal to embryonic control in early mammalian development: a comparison of several species.. Mol Reprod Dev 1990 May;26(1):90-100.
    doi: 10.1002/mrd.1080260113pubmed: 2189447google scholar: lookup
  59. Eppig JJ. Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals.. Reprod Fertil Dev 1996;8(4):485-9.
    doi: 10.1071/RD9960485pubmed: 8870074google scholar: lookup
  60. Sirard MA. Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence.. Theriogenology 2001 Apr 1;55(6):1241-54.
    doi: 10.1016/S0093-691X(01)00480-0pubmed: 11327682google scholar: lookup
  61. Bouniol-Baly C, Hamraoui L, Guibert J, Beaujean N, Szöllösi MS, Debey P. Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes.. Biol Reprod 1999 Mar;60(3):580-7.
    doi: 10.1095/biolreprod60.3.580pubmed: 10026102google scholar: lookup
  62. De La Fuente R, Viveiros MM, Burns KH, Adashi EY, Matzuk MM, Eppig JJ. Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function.. Dev Biol 2004 Nov 15;275(2):447-58.
    doi: 10.1016/j.ydbio.2004.08.028pubmed: 15501230google scholar: lookup
  63. Su YQ, Sugiura K, Woo Y, Wigglesworth K, Kamdar S, Affourtit J, Eppig JJ. Selective degradation of transcripts during meiotic maturation of mouse oocytes.. Dev Biol 2007 Feb 1;302(1):104-17.
    doi: 10.1016/j.ydbio.2006.09.008pmc: PMC1847322pubmed: 17022963google scholar: lookup
  64. Sha QQ, Yu JL, Guo JX, Dai XX, Jiang JC, Zhang YL, Yu C, Ji SY, Jiang Y, Zhang SY, Shen L, Ou XH, Fan HY. CNOT6L couples the selective degradation of maternal transcripts to meiotic cell cycle progression in mouse oocyte.. EMBO J 2018 Dec 14;37(24).
    doi: 10.15252/embj.201899333pmc: PMC6293276pubmed: 30478191google scholar: lookup
  65. Takeuchi H, Yamamoto M, Fukui M, Inoue A, Maezawa T, Nishioka M, Kondo E, Ikeda T, Matsumoto K, Miyamoto K. Single-cell profiling of transcriptomic changes during in vitro maturation of human oocytes.. Reprod Med Biol 2022 Jan-Dec;21(1):e12464.
    doi: 10.1002/rmb2.12464pmc: PMC9084694pubmed: 35582522google scholar: lookup
  66. Brevini TA, Lonergan P, Cillo F, Francisci C, Favetta LA, Fair T, Gandolfi F. Evolution of mRNA polyadenylation between oocyte maturation and first embryonic cleavage in cattle and its relation with developmental competence.. Mol Reprod Dev 2002 Dec;63(4):510-7.
    doi: 10.1002/mrd.10191pubmed: 12412054google scholar: lookup
  67. Reyes JM, Chitwood JL, Ross PJ. RNA-Seq profiling of single bovine oocyte transcript abundance and its modulation by cytoplasmic polyadenylation.. Mol Reprod Dev 2015 Feb;82(2):103-14.
    doi: 10.1002/mrd.22445pmc: PMC4651626pubmed: 25560149google scholar: lookup
  68. Ma F, Fuqua BK, Hasin Y, Yukhtman C, Vulpe CD, Lusis AJ, Pellegrini M. A comparison between whole transcript and 3' RNA sequencing methods using Kapa and Lexogen library preparation methods.. BMC Genomics 2019 Jan 7;20(1):9.
    doi: 10.1186/s12864-018-5393-3pmc: PMC6323698pubmed: 30616562google scholar: lookup
  69. Somfai T, Men NT, Noguchi J, Kaneko H, Kashiwazaki N, Kikuchi K. Optimization of cryoprotectant treatment for the vitrification of immature cumulus-enclosed porcine oocytes: comparison of sugars, combinations of permeating cryoprotectants and equilibration regimens.. J Reprod Dev 2015;61(6):571-9.
    doi: 10.1262/jrd.2015-089pmc: PMC4685224pubmed: 26411536google scholar: lookup
  70. Ortiz-Escribano N, Smits K, Piepers S, Van den Abbeel E, Woelders H, Van Soom A. Role of cumulus cells during vitrification and fertilization of mature bovine oocytes: Effects on survival, fertilization, and blastocyst development.. Theriogenology 2016 Jul 15;86(2):635-41.
    doi: 10.1016/j.theriogenology.2016.02.015pubmed: 27056413google scholar: lookup
  71. Shirazi A, Naderi MM, Hassanpour H, Heidari M, Borjian S, Sarvari A, Akhondi MM. The effect of ovine oocyte vitrification on expression of subset of genes involved in epigenetic modifications during oocyte maturation and early embryo development.. Theriogenology 2016 Dec;86(9):2136-2146.
    doi: 10.1016/j.theriogenology.2016.07.005pubmed: 27501872google scholar: lookup
  72. de la Fuente A, Scoggin C, Bradecamp E, Ali H, Troedsson M, Meyers S, Dini P. 146 Transcriptome characterisation of equine oocyte maturation.. Reprod Fertil Dev 2021 Dec;34(2):311.
    doi: 10.1071/RDv34n2Ab146pubmed: 35231353google scholar: lookup
  73. Bachvarova R, De Leon V, Johnson A, Kaplan G, Paynton BV. Changes in total RNA, polyadenylated RNA, and actin mRNA during meiotic maturation of mouse oocytes.. Dev Biol 1985 Apr;108(2):325-31.
    doi: 10.1016/0012-1606(85)90036-3pubmed: 2416609google scholar: lookup
  74. Chamayou S, Bonaventura G, Alecci C, Tibullo D, Di Raimondo F, Guglielmino A, Barcellona ML. Consequences of metaphase II oocyte cryopreservation on mRNA content.. Cryobiology 2011 Apr;62(2):130-4.
    doi: 10.1016/j.cryobiol.2011.01.014pubmed: 21272569google scholar: lookup
  75. Huo Y, Yuan P, Qin Q, Yan Z, Yan L, Liu P, Li R, Yan J, Qiao J. Effects of vitrification and cryostorage duration on single-cell RNA-Seq profiling of vitrified-thawed human metaphase II oocytes.. Front Med 2021 Feb;15(1):144-154.
    doi: 10.1007/s11684-020-0792-7pubmed: 32876878google scholar: lookup
  76. Chang CC, Shapiro DB, Bernal DP, Wright G, Kort HI, Nagy ZP. Human oocyte vitrification: in-vivo and in-vitro maturation outcomes.. Reprod Biomed Online 2008 Nov;17(5):684-8.
    doi: 10.1016/S1472-6483(10)60316-1pubmed: 18983753google scholar: lookup
  77. Inoue J, Gohda J, Akiyama T. Characteristics and biological functions of TRAF6.. Adv Exp Med Biol 2007;597:72-9.
    pubmed: 17633018doi: 10.1007/978-0-387-70630-6_6google scholar: lookup
  78. He L, Wu X, Siegel R, Lipsky PE. TRAF6 regulates cell fate decisions by inducing caspase 8-dependent apoptosis and the activation of NF-kappaB.. J Biol Chem 2006 Apr 21;281(16):11235-49.
    doi: 10.1074/jbc.M508779200pubmed: 16436380google scholar: lookup
  79. Perkins ND. Integrating cell-signalling pathways with NF-kappaB and IKK function.. Nat Rev Mol Cell Biol 2007 Jan;8(1):49-62.
    doi: 10.1038/nrm2083pubmed: 17183360google scholar: lookup
  80. Krishnaswamy JK, Singh A, Gowthaman U, Wu R, Gorrepati P, Sales Nascimento M, Gallman A, Liu D, Rhebergen AM, Calabro S, Xu L, Ranney P, Srivastava A, Ranson M, Gorham JD, McCaw Z, Kleeberger SR, Heinz LX, Müller AC, Bennett KL, Superti-Furga G, Henao-Mejia J, Sutterwala FS, Williams A, Flavell RA, Eisenbarth SC. Coincidental loss of DOCK8 function in NLRP10-deficient and C3H/HeJ mice results in defective dendritic cell migration.. Proc Natl Acad Sci U S A 2015 Mar 10;112(10):3056-61.
    doi: 10.1073/pnas.1501554112pmc: PMC4364188pubmed: 25713392google scholar: lookup
  81. Miyamoto Y, Torii T, Kawahara K, Tanoue A, Yamauchi J. Dock8 interacts with Nck1 in mediating Schwann cell precursor migration.. Biochem Biophys Rep 2016 Jul;6:113-123.
    doi: 10.1016/j.bbrep.2016.03.013pmc: PMC5600352pubmed: 28955869google scholar: lookup
  82. Soma-Nagae T, Nada S, Kitagawa M, Takahashi Y, Mori S, Oneyama C, Okada M. The lysosomal signaling anchor p18/LAMTOR1 controls epidermal development by regulating lysosome-mediated catabolic processes.. J Cell Sci 2013 Aug 15;126(Pt 16):3575-84.
    doi: 10.1242/jcs.121913pubmed: 23781028google scholar: lookup
  83. Gumus E, Sari I, Yilmaz M, Cetin A. Investigation of LAMTOR1 gene and protein expressions in germinal vesicle and metaphase II oocytes and embryos from 1-cell to blastocyst stage in a mouse model.. Gene Expr Patterns 2018 Jun;28:72-76.
    doi: 10.1016/j.gep.2018.03.002pubmed: 29510224google scholar: lookup
  84. Nakaseko Y, Yanagida M. Cell biology. Cytoskeleton in the cell cycle.. Nature 2001 Jul 19;412(6844):291-2.
    doi: 10.1038/35085684pubmed: 11460149google scholar: lookup
  85. Humeau J, Bravo-San Pedro JM, Vitale I, Nuñez L, Villalobos C, Kroemer G, Senovilla L. Calcium signaling and cell cycle: Progression or death.. Cell Calcium 2018 Mar;70:3-15.
    doi: 10.1016/j.ceca.2017.07.006pubmed: 28801101google scholar: lookup
  86. Zhang W, Liu HT. MAPK signal pathways in the regulation of cell proliferation in mammalian cells.. Cell Res 2002 Mar;12(1):9-18.
    doi: 10.1038/sj.cr.7290105pubmed: 11942415google scholar: lookup
  87. Girka E, Gatenby L, Gutierrez EJ, Bondioli KR. The effects of microtubule stabilizing and recovery agents on vitrified bovine oocytes.. Theriogenology 2022 Apr 1;182:9-16.
    doi: 10.1016/j.theriogenology.2022.01.031pubmed: 35123313google scholar: lookup
  88. Pitchayapipatkul J, Somfai T, Matoba S, Parnpai R, Nagai T, Geshi M, Vongpralub T. Microtubule stabilisers docetaxel and paclitaxel reduce spindle damage and maintain the developmental competence of in vitro-mature bovine oocytes during vitrification.. Reprod Fertil Dev 2017 Sep;29(10):2028-2039.
    doi: 10.1071/RD16193pubmed: 28147214google scholar: lookup
  89. Park SE, Chung HM, Cha KY, Hwang WS, Lee ES, Lim JM. Cryopreservation of ICR mouse oocytes: improved post-thawed preimplantation development after vitrification using Taxol, a cytoskeleton stabilizer.. Fertil Steril 2001 Jun;75(6):1177-84.
    doi: 10.1016/S0015-0282(01)01809-Xpubmed: 11384646google scholar: lookup
  90. Succu S, Berlinguer F, Leoni GG, Bebbere D, Satta V, Marco-Jimenez F, Pasciu V, Naitana S. Calcium concentration in vitrification medium affects the developmental competence of in vitro matured ovine oocytes.. Theriogenology 2011 Mar 1;75(4):715-21.
    doi: 10.1016/j.theriogenology.2010.10.012pubmed: 21144566google scholar: lookup
  91. Larman MG, Sheehan CB, Gardner DK. Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes.. Reproduction 2006 Jan;131(1):53-61.
    doi: 10.1530/rep.1.00878pubmed: 16388009google scholar: lookup
  92. Paynton BV, Rempel R, Bachvarova R. Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse.. Dev Biol 1988 Oct;129(2):304-14.
    doi: 10.1016/0012-1606(88)90377-6pubmed: 2458285google scholar: lookup
  93. Lewis N, Hinrichs K, Schnauffer K, Morganti M, Argo CM. Effect of Oocyte Source and Transport Time on Rates of Equine Oocyte Maturation and Cleavage after Fertilization by ICSI, with a Note on the Validation of Equine Embryo Morphological Classification.. Clin. Theriogenol. 2016;8:25–39.
  94. Krueger F.T.G. A Wrapper Tool around Cutadapt and FastQC to Consistently Apply Quality and Adapter Trimming to FastQ Files. 2015. [(accessed on 13 February 2023)]. Available online: https://www.bioinformatics.babraham.ac.uk/projects/trim_galore/
  95. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. STAR: ultrafast universal RNA-seq aligner.. Bioinformatics 2013 Jan 1;29(1):15-21.
    doi: 10.1093/bioinformatics/bts635pmc: PMC3530905pubmed: 23104886google scholar: lookup
  96. Smith T, Heger A, Sudbery I. UMI-tools: modeling sequencing errors in Unique Molecular Identifiers to improve quantification accuracy.. Genome Res 2017 Mar;27(3):491-499.
    doi: 10.1101/gr.209601.116pmc: PMC5340976pubmed: 28100584google scholar: lookup
  97. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome.. BMC Bioinformatics 2011 Aug 4;12:323.
    doi: 10.1186/1471-2105-12-323pmc: PMC3163565pubmed: 21816040google scholar: lookup
  98. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  99. Geistlinger L, Csaba G, Santarelli M, Ramos M, Schiffer L, Turaga N, Law C, Davis S, Carey V, Morgan M, Zimmer R, Waldron L. Toward a gold standard for benchmarking gene set enrichment analysis.. Brief Bioinform 2021 Jan 18;22(1):545-556.
    doi: 10.1093/bib/bbz158pmc: PMC7820859pubmed: 32026945google scholar: lookup
  100. Tarca AL, Draghici S, Bhatti G, Romero R. Down-weighting overlapping genes improves gene set analysis.. BMC Bioinformatics 2012 Jun 19;13:136.
    doi: 10.1186/1471-2105-13-136pmc: PMC3443069pubmed: 22713124google scholar: lookup
  101. Geistlinger L, Csaba G, Zimmer R. Bioconductor's EnrichmentBrowser: seamless navigation through combined results of set- & network-based enrichment analysis.. BMC Bioinformatics 2016 Jan 20;17:45.
    doi: 10.1186/S12859-016-0884-1/FIGURES/6pmc: PMC4721010pubmed: 26791995google scholar: lookup
  102. Gu Z, Hübschmann D. simplifyEnrichment: A Bioconductor Package for Clustering and Visualizing Functional Enrichment Results.. Genomics Proteomics Bioinformatics 2023 Feb;21(1):190-202.
    doi: 10.1016/j.gpb.2022.04.008pmc: PMC10373083pubmed: 35680096google scholar: lookup
  103. Bates D, Mächler M, Bolker BM, Walker SC. Fitting Linear Mixed-Effects Models Using Lme4.. J. Stat. Softw. 2014;67:1–48.
    doi: 10.48550/arxiv.1406.5823google scholar: lookup
  104. Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models.. Biom J 2008 Jun;50(3):346-63.
    doi: 10.1002/bimj.200810425pubmed: 18481363google scholar: lookup
  105. CRAN—Package MultcompView. [(accessed on 8 December 2022)]. Available online: https://cran.r-project.org/web/packages/multcompView/index.html.

Citations

This article has been cited 0 times.
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.