Dynamics of the Equine Placental DNA Methylome and Transcriptome from Mid- to Late Gestation.
Abstract: The placenta is a temporary organ that is essential for the survival of the fetus, with a lifelong effect on the health of both the offspring and the dam. The functions of the placenta are controlled by its dynamic gene expression during gestation. In this study, we aimed to investigate the equine placental DNA methylome as one of the fundamental mechanisms that controls the gene expression dynamic. Chorioallantois samples from four (4M), six (6M), and ten (10M) months of gestation were used to map the methylation pattern of the placenta. Globally, methylation levels increased toward the end of gestation. We identified 921 differentially methylated regions (DMRs) between 4M and 6M, 1225 DMRs between 4M and 10M, and 1026 DMRs between 6M and 10M. A total of 817 genes carried DMRs comparing 4M and 6M, 978 comparing 4M and 10M, and 804 comparing 6M and 10M. We compared the transcriptomes between the samples and found 1381 differentially expressed genes (DEGs) when comparing 4M and 6M, 1428 DEGs between 4M and 10M, and 741 DEGs between 6M and 10M. Finally, we overlapped the DEGs and genes carrying DMRs (DMRs-DEGs). Genes exhibiting (a) higher expression, low methylation and (b) low expression, high methylation at different time points were identified. The majority of these DMRs-DEGs were located in introns (48.4%), promoters (25.8%), and exons (17.7%) and were involved in changes in the extracellular matrix; regulation of epithelial cell migration; vascularization; and regulation of minerals, glucose, and metabolites, among other factors. Overall, this is the first report highlighting the dynamics in the equine placenta methylome during normal pregnancy. The findings presented serve as a foundation for future studies on the impact of abnormal methylation on the outcomes of equine pregnancies.
Publication Date: 2023-04-11 PubMed ID: 37108254PubMed Central: PMC10139181DOI: 10.3390/ijms24087084Google 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.
- 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 study explores the changes in DNA methylation and gene expression in horse placentas during various stages of gestation. Increased methylation levels were observed as gestation progressed and these changes were linked to crucial biological functions such as cell migration, vascularization, and metabolic regulation.
Research Objectives and Methods
- The researchers aimed to understand the patterns of DNA methylation, a mechanism that influences gene expression, in the placenta of horses (equine) during various stages of gestation. This was carried out with the intended purpose of learning how these fundamental controls affect the behavior of genes over the pregnancy duration.
- They examined placental samples from the fourth (4M), sixth (6M), and tenth (10M) month of gestation to determine the methylation pattern in the placenta. They also compared the transcriptomes (set of all RNA molecules) between these samples to identify differentially expressed genes (DEGs).
Key Findings
- The overall methylation levels in the placenta increased towards the end of gestation. During this process, they identified numerous differentially methylated regions (DMRs), with a significant number of genes carrying these DMRs in the different gestational stages compared.
- By investigating the transcriptomes, they uncovered a significant number of DEGs between the compared gestational stages. The DEGs were then compared with the genes carrying DMRs to identify genes with both changing methylation and gene expression levels over time.
- It was observed that genes with higher expression had lower methylation and those with lower expression had higher methylation at different stages of pregnancy.
- The majority of the identified genes that carry both DMRs and DEGs (DMRs-DEGs) were found within introns (within genes), promoters (start of genes), and exons (coding regions of genes). These genes were linked to crucial biological functions and changes throughout gestation, including regulation of cell migration, vascularization, and metabolic processes among others.
Significance of the Study
- This investigation is the first of its kind to outline the dynamics of DNA methylation in the horse placenta during a normal pregnancy. It helps understand how methylation changes are potentially crucial to the health and survival of the fetus as well as the mother.
- The study establishes a foundation for future research by providing a basis for exploration into understanding how abnormal methylation could impact horse pregnancies. This research could be instrumental in providing insights into maintaining the health of pregnant horses and their offspring.
Cite This Article
APA
Orellana-Guerrero D, Uribe-Salazar JM, El-Sheikh Ali H, Scoggin KE, Ball B, Daels P, Finno CJ, Dini P.
(2023).
Dynamics of the Equine Placental DNA Methylome and Transcriptome from Mid- to Late Gestation.
Int J Mol Sci, 24(8), 7084.
https://doi.org/10.3390/ijms24087084 Publication
Researcher Affiliations
- Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA.
- Genome Center, University of California, Davis, CA 95616, USA.
- Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY 40546, USA.
- College of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt.
- Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY 40546, USA.
- Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY 40546, USA.
- Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium.
- Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA.
- Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA.
MeSH Terms
- Pregnancy
- Animals
- Female
- Horses / genetics
- Placenta / metabolism
- DNA Methylation
- Transcriptome
- Epigenome
- Fetus / metabolism
- Epigenesis, Genetic
Grant Funding
- CEH / Center for Equine Health
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 90 references
- Rossant J, Cross JC. Placental development: lessons from mouse mutants.. Nat Rev Genet 2001 Jul;2(7):538-48.
- Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta.. Dev Biol 2002 Oct 15;250(2):358-73.
- Hemberger M, Hanna CW, Dean W. Mechanisms of early placental development in mouse and humans.. Nat Rev Genet 2020 Jan;21(1):27-43.
- Koukoura O, Sifakis S, Spandidos DA. DNA methylation in the human placenta and fetal growth (review).. Mol Med Rep 2012 Apr;5(4):883-9.
- Novakovic B, Yuen RK, Gordon L, Penaherrera MS, Sharkey A, Moffett A, Craig JM, Robinson WP, Saffery R. Evidence for widespread changes in promoter methylation profile in human placenta in response to increasing gestational age and environmental/stochastic factors.. BMC Genomics 2011 Oct 28;12:529.
- Gheorghe CP, Goyal R, Mittal A, Longo LD. Gene expression in the placenta: maternal stress and epigenetic responses.. Int J Dev Biol 2010;54(2-3):507-23.
- Ng HK, Novakovic B, Hiendleder S, Craig JM, Roberts CT, Saffery R. Distinct patterns of gene-specific methylation in mammalian placentas: implications for placental evolution and function.. Placenta 2010 Apr;31(4):259-68.
- Turner. Some General Observations on the Placenta, with especial reference to the Theory of Evolution.. J Anat Physiol 1876 Oct;11(Pt 1):33-53.
- Dini P, Kalbfleisch T, Uribe-Salazar JM, Carossino M, Ali HE, Loux SC, Esteller-Vico A, Norris JK, Anand L, Scoggin KE, Rodriguez Lopez CM, Breen J, Bailey E, Daels P, Ball BA. Parental bias in expression and interaction of genes in the equine placenta.. Proc Natl Acad Sci U S A 2021 Apr 20;118(16).
- Carter AM, Enders AC. The evolution of epitheliochorial placentation.. Annu Rev Anim Biosci 2013 Jan;1:443-67.
- Dini P, Norris J, Ali HE, Loux SC, Carossino M, Esteller-Vico A, Bailey E, Kalbfleisch T, Daels P, Ball BA. Landscape of Overlapping Gene Expression in the Equine Placenta.. Genes (Basel) 2019 Jul 2;10(7).
- Loux SC, Dini P, El-Sheikh Ali H, Kalbfleisch T, Ball BA. Characterization of the placental transcriptome through mid to late gestation in the mare.. PLoS One 2019;14(11):e0224497.
- Carter AM, Enders AC. Comparative aspects of trophoblast development and placentation.. Reprod Biol Endocrinol 2004 Jul 5;2:46.
- Proudhon C, Bourc'his D. Identification and resolution of artifacts in the interpretation of imprinted gene expression.. Brief Funct Genomics 2010 Dec;9(5-6):374-84.
- Ginther O. Reproductive Biology of the Mare. Equiservices; Cross Plains, WI, USA: 1992.
- Allen W, Stewart F. Equine Reproduction. Wiley-Blackwell; Hoboken, NJ, USA: 1993.
- Conley AJ. Review of the reproductive endocrinology of the pregnant and parturient mare.. Theriogenology 2016 Jul 1;86(1):355-65.
- Holtan DW, Squires EL, Lapin DR, Ginther OJ. Effect of ovariectomy on pregnancy in mares.. J Reprod Fertil Suppl 1979;(27):457-63.
- Loux SC, Conley AJ, Scoggin KE, El-Sheikh Ali H, Dini P, Ball BA. New insights in equine steroidogenesis: an in-depth look at steroid signaling in the placenta.. Reproduction 2020 Jul;160(1):65-82.
- Dini P, Daels P, Loux SC, Esteller-Vico A, Carossino M, Scoggin KE, Ball BA. Kinetics of the chromosome 14 microRNA cluster ortholog and its potential role during placental development in the pregnant mare.. BMC Genomics 2018 Dec 20;19(1):954.
- El-Sheikh Ali H, Legacki EL, Scoggin KE, Loux SC, Dini P, Esteller-Vico A, Conley AJ, Stanley SD, Ball BA. Steroid synthesis and metabolism in the equine placenta during placentitis.. Reproduction 2020 Mar;159(3):289-302.
- Dini P, El-Sheikh Ali H, Carossino M, C Loux S, Esteller-Vico A, E Scoggin K, Daels P, A Ball B. Expression Profile of the Chromosome 14 MicroRNA Cluster (C14MC) Ortholog in Equine Maternal Circulation throughout Pregnancy and Its Potential Implications.. Int J Mol Sci 2019 Dec 13;20(24).
- Siegfried Z, Simon I. DNA methylation and gene expression.. Wiley Interdiscip Rev Syst Biol Med 2010 May-Jun;2(3):362-371.
- Robertson KD. DNA methylation and human disease.. Nat Rev Genet 2005 Aug;6(8):597-610.
- Grigoriu A, Ferreira JC, Choufani S, Baczyk D, Kingdom J, Weksberg R. Cell specific patterns of methylation in the human placenta.. Epigenetics 2011 Mar;6(3):368-79.
- Lee JR, Hong CP, Moon JW, Jung YD, Kim DS, Kim TH, Gim JA, Bae JH, Choi Y, Eo J, Kwon YJ, Song S, Ko J, Yang YM, Lee HK, Park KD, Ahn K, Do KT, Ha HS, Han K, Yi JM, Cha HJ, Cho BW, Bhak J, Kim HS. Genome-wide analysis of DNA methylation patterns in horse.. BMC Genomics 2014 Jul 15;15(1):598.
- Robinson WP, Price EM. The human placental methylome.. Cold Spring Harb Perspect Med 2015 Feb 26;5(5):a023044.
- Bianco-Miotto T, Mayne BT, Buckberry S, Breen J, Rodriguez Lopez CM, Roberts CT. Recent progress towards understanding the role of DNA methylation in human placental development.. Reproduction 2016 Jul;152(1):R23-30.
- Phillips T. The role of methylation in gene expression. Nat. Educ. 2008;1:116.
- Schroeder DI, Blair JD, Lott P, Yu HO, Hong D, Crary F, Ashwood P, Walker C, Korf I, Robinson WP, LaSalle JM. The human placenta methylome.. Proc Natl Acad Sci U S A 2013 Apr 9;110(15):6037-42.
- Greenberg MVC, Bourc'his D. The diverse roles of DNA methylation in mammalian development and disease.. Nat Rev Mol Cell Biol 2019 Oct;20(10):590-607.
- Novakovic B, Saffery R. DNA methylation profiling highlights the unique nature of the human placental epigenome.. Epigenomics 2010 Oct;2(5):627-38.
- Vlahos A, Mansell T, Saffery R, Novakovic B. Human placental methylome in the interplay of adverse placental health, environmental exposure, and pregnancy outcome.. PLoS Genet 2019 Aug;15(8):e1008236.
- Neidhart M. DNA Methylation and Complex Human Disease. Academic Press; Cambridge, MA, USA: 2015.
- Gamage TKJB, Schierding W, Hurley D, Tsai P, Ludgate JL, Bhoothpur C, Chamley LW, Weeks RJ, Macaulay EC, James JL. The role of DNA methylation in human trophoblast differentiation.. Epigenetics 2018;13(12):1154-1173.
- Falick Michaeli T, Spiro A, Sabag O, Karavani G, Yagel S, Eventov-Friedman S, Cedar H, Bergman Y, Gielchinsky Y. Determining gestational age using genome methylation profile: A novel approach for fetal medicine.. Prenat Diagn 2019 Oct;39(11):1005-1010.
- Pelizzola M, Ecker JR. The DNA methylome.. FEBS Lett 2011 Jul 7;585(13):1994-2000.
- Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR. Human DNA methylomes at base resolution show widespread epigenomic differences.. Nature 2009 Nov 19;462(7271):315-22.
- Maltepe E, Fisher SJ. Placenta: the forgotten organ.. Annu Rev Cell Dev Biol 2015;31:523-52.
- Steinhart Z, Angers S. Wnt signaling in development and tissue homeostasis.. Development 2018 Jun 8;145(11).
- Winn VD, Haimov-Kochman R, Paquet AC, Yang YJ, Madhusudhan MS, Gormley M, Feng KT, Bernlohr DA, McDonagh S, Pereira L, Sali A, Fisher SJ. Gene expression profiling of the human maternal-fetal interface reveals dramatic changes between midgestation and term.. Endocrinology 2007 Mar;148(3):1059-79.
- Mikheev AM, Nabekura T, Kaddoumi A, Bammler TK, Govindarajan R, Hebert MF, Unadkat JD. Profiling gene expression in human placentae of different gestational ages: an OPRU Network and UW SCOR Study.. Reprod Sci 2008 Nov;15(9):866-77.
- Zhou X, Xu Y, Ren S, Liu D, Yang N, Han Q, Kong S, Wang H, Deng W, Qi H, Lu J. Single-cell RNA-seq revealed diverse cell types in the mouse placenta at mid-gestation.. Exp Cell Res 2021 Aug 15;405(2):112715.
- Monkley SJ, Delaney SJ, Pennisi DJ, Christiansen JH, Wainwright BJ. Targeted disruption of the Wnt2 gene results in placentation defects.. Development 1996 Nov;122(11):3343-53.
- Parr BA, Cornish VA, Cybulsky MI, McMahon AP. Wnt7b regulates placental development in mice.. Dev Biol 2001 Sep 15;237(2):324-32.
- Andersson L, Archibald AL, Bottema CD, Brauning R, Burgess SC, Burt DW, Casas E, Cheng HH, Clarke L, Couldrey C, Dalrymple BP, Elsik CG, Foissac S, Giuffra E, Groenen MA, Hayes BJ, Huang LS, Khatib H, Kijas JW, Kim H, Lunney JK, McCarthy FM, McEwan JC, Moore S, Nanduri B, Notredame C, Palti Y, Plastow GS, Reecy JM, Rohrer GA, Sarropoulou E, Schmidt CJ, Silverstein J, Tellam RL, Tixier-Boichard M, Tosser-Klopp G, Tuggle CK, Vilkki J, White SN, Zhao S, Zhou H. Coordinated international action to accelerate genome-to-phenome with FAANG, the Functional Annotation of Animal Genomes project.. Genome Biol 2015 Mar 25;16(1):57.
- Nelissen EC, van Montfoort AP, Dumoulin JC, Evers JL. Epigenetics and the placenta.. Hum Reprod Update 2011 May-Jun;17(3):397-417.
- Serman L, Dodig D. Impact of DNA methylation on trophoblast function.. Clin Epigenetics 2011 Nov 1;3(1):7.
- Schuster J, Uzun A, Stablia J, Schorl C, Mori M, Padbury JF. Effect of prematurity on genome wide methylation in the placenta.. BMC Med Genet 2019 Jun 28;20(1):116.
- Dhar GA, Saha S, Mitra P, Nag Chaudhuri R. DNA methylation and regulation of gene expression: Guardian of our health.. Nucleus (Calcutta) 2021;64(3):259-270.
- Maunakea AK, Chepelev I, Cui K, Zhao K. Intragenic DNA methylation modulates alternative splicing by recruiting MeCP2 to promote exon recognition.. Cell Res 2013 Nov;23(11):1256-69.
- Suzuki S, Shaw G, Renfree MB. Identification of a novel antisense noncoding RNA, ALID, transcribed from the putative imprinting control region of marsupial IGF2R.. Epigenetics Chromatin 2018 Sep 29;11(1):55.
- Makaroun SP, Himes KP. Differential Methylation of Syncytin-1 and 2 Distinguishes Fetal Growth Restriction from Physiologic Small for Gestational Age.. AJP Rep 2018 Jan;8(1):e18-e24.
- Gao Y, He Z, Wang Z, Luo Y, Sun H, Zhou Y, Huang L, Li M, Fang Q, Jiang S. Increased expression and altered methylation of HERVWE1 in the human placentas of smaller fetuses from monozygotic, dichorionic, discordant twins.. PLoS One 2012;7(3):e33503.
- Ruebner M, Strissel PL, Langbein M, Fahlbusch F, Wachter DL, Faschingbauer F, Beckmann MW, Strick R. Impaired cell fusion and differentiation in placentae from patients with intrauterine growth restriction correlate with reduced levels of HERV envelope genes.. J Mol Med (Berl) 2010 Nov;88(11):1143-56.
- Langbein M, Strick R, Strissel PL, Vogt N, Parsch H, Beckmann MW, Schild RL. Impaired cytotrophoblast cell-cell fusion is associated with reduced Syncytin and increased apoptosis in patients with placental dysfunction.. Mol Reprod Dev 2008 Jan;75(1):175-83.
- Kudaka W, Oda T, Jinno Y, Yoshimi N, Aoki Y. Cellular localization of placenta-specific human endogenous retrovirus (HERV) transcripts and their possible implication in pregnancy-induced hypertension.. Placenta 2008 Mar;29(3):282-9.
- Ruebner M, Strissel PL, Ekici AB, Stiegler E, Dammer U, Goecke TW, Faschingbauer F, Fahlbusch FB, Beckmann MW, Strick R. Reduced syncytin-1 expression levels in placental syndromes correlates with epigenetic hypermethylation of the ERVW-1 promoter region.. PLoS One 2013;8(2):e56145.
- Yu Y, He JH, Hu LL, Jiang LL, Fang L, Yao GD, Wang SJ, Yang Q, Guo Y, Liu L, Shang T, Sato Y, Kawamura K, Hsueh AJ, Sun YP. Placensin is a glucogenic hormone secreted by human placenta.. EMBO Rep 2020 Jun 4;21(6):e49530.
- Fowden AL, Comline RS, Silver M. Insulin secretion and carbohydrate metabolism during pregnancy in the mare.. Equine Vet J 1984 Jul;16(4):239-46.
- George LA, Staniar WB, Cubitt TA, Treiber KH, Harris PA, Geor RJ. Evaluation of the effects of pregnancy on insulin sensitivity, insulin secretion, and glucose dynamics in Thoroughbred mares.. Am J Vet Res 2011 May;72(5):666-74.
- Poulet M, Sirois J, Boyé K, Uetani N, Hardy S, Daubon T, Dubrac A, Tremblay ML, Bikfalvi A. PRL-2 phosphatase is required for vascular morphogenesis and angiogenic signaling.. Commun Biol 2020 Oct 23;3(1):603.
- Li L, Shi H, Zhang M, Guo X, Tong F, Zhang W, Zhou J, Wang H, Yang S. Upregulation of metastasis-associated PRL-3 initiates chordoma in zebrafish.. Int J Oncol 2016 Apr;48(4):1541-52.
- Guo K, Li J, Wang H, Osato M, Tang JP, Quah SY, Gan BQ, Zeng Q. PRL-3 initiates tumor angiogenesis by recruiting endothelial cells in vitro and in vivo.. Cancer Res 2006 Oct 1;66(19):9625-35.
- Zimmerman MW, McQueeney KE, Isenberg JS, Pitt BR, Wasserloos KA, Homanics GE, Lazo JS. Protein-tyrosine phosphatase 4A3 (PTP4A3) promotes vascular endothelial growth factor signaling and enables endothelial cell motility.. J Biol Chem 2014 Feb 28;289(9):5904-13.
- St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, Montgomery E, Lal A, Riggins GJ, Lengauer C, Vogelstein B, Kinzler KW. Genes expressed in human tumor endothelium.. Science 2000 Aug 18;289(5482):1197-202.
- Bardelli A, Saha S, Sager JA, Romans KE, Xin B, Markowitz SD, Lengauer C, Velculescu VE, Kinzler KW, Vogelstein B. PRL-3 expression in metastatic cancers.. Clin Cancer Res 2003 Nov 15;9(15):5607-15.
- Haneda S, Dini P, Esteller-Vico A, Scoggin KE, Squires EL, Troedsson MH, Daels P, Nambo Y, Ball BA. Estrogens Regulate Placental Angiogenesis in Horses.. Int J Mol Sci 2021 Nov 9;22(22).
- Dini P, Carossino M, Balasuriya UBR, El-Sheikh Ali H, Loux SC, Esteller-Vico A, Scoggin KE, Loynachan AT, Kalbfleisch T, De Spiegelaere W, Daels P, Ball BA. Paternally expressed retrotransposon Gag-like 1 gene, RTL1, is one of the crucial elements for placental angiogenesis in horses†.. Biol Reprod 2021 Jun 4;104(6):1386-1399.
- Dini P, Carossino M, Loynachan AT, El-Sheikh Ali H, Wolfsdorf KE, Scoggin KE, Daels P, Ball BA. Equine hydrallantois is associated with impaired angiogenesis in the placenta.. Placenta 2020 Apr;93:101-112.
- Tunster SJ, Creeth HDJ, John RM. The imprinted Phlda2 gene modulates a major endocrine compartment of the placenta to regulate placental demands for maternal resources.. Dev Biol 2016 Jan 1;409(1):251-260.
- Frank D, Mendelsohn CL, Ciccone E, Svensson K, Ohlsson R, Tycko B. A novel pleckstrin homology-related gene family defined by Ipl/Tssc3, TDAG51, and Tih1: tissue-specific expression, chromosomal location, and parental imprinting.. Mamm Genome 1999 Dec;10(12):1150-9.
- Dunwoodie SL, Beddington RS. The expression of the imprinted gene Ipl is restricted to extra-embryonic tissues and embryonic lateral mesoderm during early mouse development.. Int J Dev Biol 2002;46(4):459-66.
- Takao T, Asanoma K, Tsunematsu R, Kato K, Wake N. The maternally expressed gene Tssc3 regulates the expression of MASH2 transcription factor in mouse trophoblast stem cells through the AKT-Sp1 signaling pathway.. J Biol Chem 2012 Dec 14;287(51):42685-94.
- Tunster SJ, Tycko B, John RM. The imprinted Phlda2 gene regulates extraembryonic energy stores.. Mol Cell Biol 2010 Jan;30(1):295-306.
- Salas M, John R, Saxena A, Barton S, Frank D, Fitzpatrick G, Higgins MJ, Tycko B. Placental growth retardation due to loss of imprinting of Phlda2.. Mech Dev 2004 Oct;121(10):1199-210.
- Janssen AB, Tunster SJ, Heazell AE, John RM. Placental PHLDA2 expression is increased in cases of fetal growth restriction following reduced fetal movements.. BMC Med Genet 2016 Mar 5;17:17.
- Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications.. Bioinformatics 2011 Jun 1;27(11):1571-2.
- Andrews S. FastQC: A Quality Control Tool for High throughput Sequence Data. Babraham Bioinformatics, Babraham Institute; Cambridge, UK: 2010.
- Gifford CA, Ziller MJ, Gu H, Trapnell C, Donaghey J, Tsankov A, Shalek AK, Kelley DR, Shishkin AA, Issner R, Zhang X, Coyne M, Fostel JL, Holmes L, Meldrim J, Guttman M, Epstein C, Park H, Kohlbacher O, Rinn J, Gnirke A, Lander ES, Bernstein BE, Meissner A. Transcriptional and epigenetic dynamics during specification of human embryonic stem cells.. Cell 2013 May 23;153(5):1149-63.
- Habibi E, Brinkman AB, Arand J, Kroeze LI, Kerstens HH, Matarese F, Lepikhov K, Gut M, Brun-Heath I, Hubner NC, Benedetti R, Altucci L, Jansen JH, Walter J, Gut IG, Marks H, Stunnenberg HG. Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells.. Cell Stem Cell 2013 Sep 5;13(3):360-9.
- Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling.. Nat Protoc 2011 Apr;6(4):468-81.
- Gim JA, Hong CP, Kim DS, Moon JW, Choi Y, Eo J, Kwon YJ, Lee JR, Jung YD, Bae JH, Choi BH, Ko J, Song S, Ahn K, Ha HS, Yang YM, Lee HK, Park KD, Do KT, Han K, Yi JM, Cha HJ, Ayarpadikannan S, Cho BW, Bhak J, Kim HS. Genome-wide analysis of DNA methylation before-and after exercise in the thoroughbred horse with MeDIP-Seq.. Mol Cells 2015 Mar;38(3):210-20.
- Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes.. Nucleic Acids Res 2000 Jan 1;28(1):27-30.
- Kanehisa M. Toward understanding the origin and evolution of cellular organisms.. Protein Sci 2019 Nov;28(11):1947-1951.
- Kanehisa M, Furumichi M, Sato Y, Ishiguro-Watanabe M, Tanabe M. KEGG: integrating viruses and cellular organisms.. Nucleic Acids Res 2021 Jan 8;49(D1):D545-D551.
- Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, Narechania A. PANTHER: a library of protein families and subfamilies indexed by function.. Genome Res 2003 Sep;13(9):2129-41.
- Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data.. Bioinformatics 2014 Aug 1;30(15):2114-20.
- Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression.. Nat Methods 2017 Apr;14(4):417-419.
- 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.
Citations
This article has been cited 1 times.- Semik-Gurgul E, Pawlina-Tyszko K, Gurgul A, Szmatoła T, Rybińska J, Ząbek T. In search of epigenetic hallmarks of different tissues: an integrative omics study of horse liver, lung, and heart. Mamm Genome 2024 Dec;35(4):600-620.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists