Comparative analysis of single-cell transcriptomics in human and Zebrafish oocytes.

Handan Can, Sree K Chanumolu, Elena Gonzalez-Muñoz, Sukumal Prukudom, Hasan H Otu, Jose B Cibelli
Author Information
  1. Handan Can: Department of Electrical and Computer Engineering, University of Nebraska-Lincoln, Lincoln, NE, 68588, USA.
  2. Sree K Chanumolu: Department of Electrical and Computer Engineering, University of Nebraska-Lincoln, Lincoln, NE, 68588, USA.
  3. Elena Gonzalez-Muñoz: LARCEL, Andalusian Laboratory of Cell Reprogramming (LARCel), Andalusian Center for Nanomedicine and Biotechnology-BIONAND, 29590, Málaga, Spain.
  4. Sukumal Prukudom: Department of Anatomy, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, 10900, Thailand.
  5. Hasan H Otu: Department of Electrical and Computer Engineering, University of Nebraska-Lincoln, Lincoln, NE, 68588, USA. hotu2@unl.edu. ORCID
  6. Jose B Cibelli: Departments of Animal Science and Large Animal Clinical Sciences, Michigan State University, East Lansing, MI, 48824, USA. cibelli@msu.edu.

Abstract

BACKGROUND: Zebrafish is a popular model organism, which is widely used in developmental biology research. Despite its general use, the direct comparison of the zebrafish and human oocyte transcriptomes has not been well studied. It is significant to see if the similarity observed between the two organisms at the gene sequence level is also observed at the expression level in key cell types such as the oocyte.
RESULTS: We performed single-cell RNA-seq of the zebrafish oocyte and compared it with two studies that have performed single-cell RNA-seq of the human oocyte. We carried out a comparative analysis of genes expressed in the oocyte and genes highly expressed in the oocyte across the three studies. Overall, we found high consistency between the human studies and high concordance in expression for the orthologous genes in the two organisms. According to the Ensembl database, about 60% of the human protein coding genes are orthologous to the zebrafish genes. Our results showed that a higher percentage of the genes that are highly expressed in both organisms show orthology compared to the lower expressed genes. Systems biology analysis of the genes highly expressed in the three studies showed significant overlap of the enriched pathways and GO terms. Moreover, orthologous genes that are commonly overexpressed in both organisms were involved in biological mechanisms that are functionally essential to the oocyte.
CONCLUSIONS: Orthologous genes are concurrently highly expressed in the oocytes of the two organisms and these genes belong to similar functional categories. Our results provide evidence that zebrafish could serve as a valid model organism to study the oocyte with direct implications in human.

Keywords

References

  1. Prog Lipid Res. 2016 Apr;62:25-40 [PMID: 26769304]
  2. Toxicology. 2011 Mar 15;281(1-3):25-36 [PMID: 21237239]
  3. Dev Biol. 2015 Feb 15;398(2):177-92 [PMID: 25448697]
  4. Database (Oxford). 2015 Jul 07;2015:bav067 [PMID: 26153137]
  5. Bioinformatics. 2014 Aug 1;30(15):2114-20 [PMID: 24695404]
  6. Nucleic Acids Res. 2012 Jan;40(Database issue):D109-14 [PMID: 22080510]
  7. Dev Dyn. 2014 Jan;243(1):88-98 [PMID: 23913366]
  8. Nat Commun. 2011;2:241 [PMID: 21407207]
  9. Wiley Interdiscip Rev Dev Biol. 2018 May;7(3):e312 [PMID: 29436122]
  10. Proc Natl Acad Sci U S A. 2006 Sep 19;103(38):14027-32 [PMID: 16968779]
  11. Tissue Barriers. 2013 Jul 1;1(3):e25391 [PMID: 24665402]
  12. Nucleic Acids Res. 2019 Jan 8;47(D1):D867-D873 [PMID: 30407545]
  13. Nucleic Acids Res. 2019 Jan 8;47(D1):D745-D751 [PMID: 30407521]
  14. Cancer Metastasis Rev. 2014 Dec;33(4):843-56 [PMID: 25398252]
  15. BMC Bioinformatics. 2019 Aug 15;20(1):424 [PMID: 31416440]
  16. Nat Protoc. 2009;4(1):44-57 [PMID: 19131956]
  17. Nature. 2013 Aug 29;500(7464):593-7 [PMID: 23892778]
  18. Gene Expr Patterns. 2011 Jan-Feb;11(1-2):3-11 [PMID: 20804857]
  19. Methods Cell Biol. 2016;135:245-57 [PMID: 27443929]
  20. Development. 2016 Jan 15;143(2):244-54 [PMID: 26674311]
  21. Methods Mol Biol. 2019;1920:353-375 [PMID: 30737703]
  22. Nat Genet. 2000 May;25(1):25-9 [PMID: 10802651]
  23. Bioinformatics. 2014 Feb 15;30(4):523-30 [PMID: 24336805]
  24. Genes Dev. 2015 Apr 1;29(7):702-17 [PMID: 25805847]
  25. Antioxid Redox Signal. 2019 Feb 1;30(4):542-559 [PMID: 29486586]
  26. Dev Dyn. 1995 Jul;203(3):253-310 [PMID: 8589427]
  27. F1000Res. 2015 Dec 30;4:1521 [PMID: 26925227]
  28. Stem Cells Dev. 2018 Jul 1;27(13):871-887 [PMID: 29737235]
  29. Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50 [PMID: 16199517]
  30. Front Immunol. 2019 Sep 06;10:2100 [PMID: 31555292]
  31. Nat Methods. 2017 Apr;14(4):417-419 [PMID: 28263959]
  32. Zebrafish. 2009 Mar;6(1):97-105 [PMID: 19292671]
  33. Biomed Res Int. 2019 Nov 20;2019:1253710 [PMID: 31828085]
  34. Gen Comp Endocrinol. 2010 Sep 15;168(3):388-400 [PMID: 20553723]
  35. Neurosci Biobehav Rev. 2014 Sep;45:258-61 [PMID: 25003805]
  36. Curr Opin Drug Discov Devel. 2003 Mar;6(2):218-23 [PMID: 12669457]
  37. Nature. 2013 Apr 25;496(7446):498-503 [PMID: 23594743]
  38. Development. 2018 Jan 9;145(1): [PMID: 29180571]
  39. Methods Cell Biol. 2016;135:509-34 [PMID: 27443942]
  40. Mol Cell. 2012 Jun 29;46(6):893-5 [PMID: 22749402]

Grants

  1. N/A/Fundacion Progreso y Salud
  2. R41OD021456/NIH HHS
  3. R21LM012759/U.S. National Library of Medicine
  4. N/A/Michigan AbBioresearch
  5. N/A/Fundacion Publica Andaluza Progreso y Salud
  6. R21 LM012759/NLM NIH HHS
  7. R21OD019915/NIH HHS
  8. MRG5480228/Thailand Research Fund
  9. R01GM125991/NIH HHS
  10. N/A/Ministerio de Economía, Industria y Competitividad, Gobierno de España

MeSH Term

Animals
Humans
Oocytes
RNA-Seq
Single-Cell Analysis
Transcriptome
Zebrafish

Word Cloud

Created with Highcharts 10.0.0genesoocytehumanexpressedorganismszebrafishtwostudieshighlyZebrafishsingle-cellRNA-seqanalysisorthologousmodelorganismbiologydirectsignificantobservedlevelexpressionperformedcomparedthreehighresultsshowedoocytesBACKGROUND:popularwidelyuseddevelopmentalresearchDespitegeneralusecomparisontranscriptomeswellstudiedseesimilaritygenesequencealsokeycelltypesRESULTS:carriedcomparativeacrossOverallfoundconsistencyconcordanceAccordingEnsembldatabase60%proteincodinghigherpercentageshoworthologylowerSystemsoverlapenrichedpathwaysGOtermsMoreovercommonlyoverexpressedinvolvedbiologicalmechanismsfunctionallyessentialCONCLUSIONS:OrthologousconcurrentlybelongsimilarfunctionalcategoriesprovideevidenceservevalidstudyimplicationsComparativetranscriptomicsOocyteOrthologyTranscriptome

Similar Articles

Cited By