Methylation profile of bovine Oct4 gene coding region in relation to three germ layers

doi:10.1016/S2095-3119(15)61100-5

Journal of Integrative Agriculture ›› 2016, Vol. 15 ›› Issue (3): 618-628.DOI: 10.1016/S2095-3119(15)61100-5

Methylation profile of bovine Oct4 gene coding region in relation to three germ layers

ZHOU Xin-yu, LIU Liang-liang, JIA Wen-chao, PAN Chuan-ying

1、College of Life Sciences, Northwest A&F University, Yangling 712100, P.R.China
2、School of Computer Science & Engineering, Jiangsu University of Science and Technology, Zhenjiang 212003, P.R.China
3、College of Animal Science and Technology, Northwest A&F University/Shaanxi Key Laboratory of Molecular Biology for
Agriculture, Yangling 712100, P.R.China

收稿日期:2015-02-11 出版日期:2016-03-07 发布日期:2016-03-09
通讯作者: PAN Chuan-ying, Tel: +86-29-87092102, Fax: +86-29-87092164,E-mail: panyu1980@126.com
作者简介:ZHOU Xin-yu, E-mail: zhouxinyu0531@163.com; LIU Liangliang,E-mail: lingyun79626@126.com;* These authors contributed equally to this study.
基金资助:
This work was supported by the Natural Science Foundation of Shaanxi Province, China (2014JQ3104), the National Natural Science Foundation of China (31000655) and China Postdoctoral Science Foundation funded project (2014M560809).

Methylation profile of bovine Oct4 gene coding region in relation to three germ layers

ZHOU Xin-yu, LIU Liang-liang, JIA Wen-chao, PAN Chuan-ying

1、College of Life Sciences, Northwest A&F University, Yangling 712100, P.R.China
2、School of Computer Science & Engineering, Jiangsu University of Science and Technology, Zhenjiang 212003, P.R.China
3、College of Animal Science and Technology, Northwest A&F University/Shaanxi Key Laboratory of Molecular Biology for
Agriculture, Yangling 712100, P.R.China

Received:2015-02-11 Online:2016-03-07 Published:2016-03-09
Contact: PAN Chuan-ying, Tel: +86-29-87092102, Fax: +86-29-87092164,E-mail: panyu1980@126.com
About author:ZHOU Xin-yu, E-mail: zhouxinyu0531@163.com; LIU Liangliang,E-mail: lingyun79626@126.com;* These authors contributed equally to this study.
Supported by:
This work was supported by the Natural Science Foundation of Shaanxi Province, China (2014JQ3104), the National Natural Science Foundation of China (31000655) and China Postdoctoral Science Foundation funded project (2014M560809).

摘要/Abstract

摘要： Previous studies have shown that octamer-binding transcription factor 4 (Oct4) plays a significant role in early embryonic development of mammalian animals, and different Oct4 expression levels induce multi-lineage differentiation which are regulated by DNA methylation. To explore the relationship between the methylation pattern of Oct4 gene exon 1 and embryonic development, in this work, five different tissues (heart, liver, lung, cerebrum and cerebellum) from three germ layers were chosen from low age (50–60 d) and advanced age (60–70 d) of fetal cattle and the differences between tissues or ages were analyzed, respectively. The result showed that the DNA methylation level of Oct4 gene exon 1 was significant different (P<0.01) between any two of three germ layers in low age (<60 d), but kept steady of advanced age (P>0.05) (>60 d), suggesting that 60-d post coital was an important boundary for embryonic development. In addition, in ectoderm (cerebrum and cerebellum), there was no significant methylation difference of Oct4 gene exon 1 between low age and advanced age (P>0.05), but the result of endoderm (liver and lung) and mesoderm (heart) were on the contrary (P<0.01), which indicated the development of ectoderm was earlier than endoderm and mesoderm. The methylation differences from the 3rd, 5th and 9th CpG-dinucleotide loci of Oct4 gene exon 1 were significantly different between each two of three germ layers (P<0.05), indicating that these three loci may have important influence on bovine embryonic development. This study showed that bovine germ layers differentiation was significantly related to the DNA methylation status of Oct4 gene exon 1. This work firstly identified the DNA methylation profile of bovine Oct4 gene exon 1 and its association with germ layers development in fetus and adult of cattle. Moreover, the work also provided epigenetic information for further studying bovine embryonic development and cellular reprogramming.

关键词: bovine , DNA methylation , octamer-binding transcription factor 4 (Oct4) , exon , germ layer

Abstract: Previous studies have shown that octamer-binding transcription factor 4 (Oct4) plays a significant role in early embryonic development of mammalian animals, and different Oct4 expression levels induce multi-lineage differentiation which are regulated by DNA methylation. To explore the relationship between the methylation pattern of Oct4 gene exon 1 and embryonic development, in this work, five different tissues (heart, liver, lung, cerebrum and cerebellum) from three germ layers were chosen from low age (50–60 d) and advanced age (60–70 d) of fetal cattle and the differences between tissues or ages were analyzed, respectively. The result showed that the DNA methylation level of Oct4 gene exon 1 was significant different (P<0.01) between any two of three germ layers in low age (<60 d), but kept steady of advanced age (P>0.05) (>60 d), suggesting that 60-d post coital was an important boundary for embryonic development. In addition, in ectoderm (cerebrum and cerebellum), there was no significant methylation difference of Oct4 gene exon 1 between low age and advanced age (P>0.05), but the result of endoderm (liver and lung) and mesoderm (heart) were on the contrary (P<0.01), which indicated the development of ectoderm was earlier than endoderm and mesoderm. The methylation differences from the 3rd, 5th and 9th CpG-dinucleotide loci of Oct4 gene exon 1 were significantly different between each two of three germ layers (P<0.05), indicating that these three loci may have important influence on bovine embryonic development. This study showed that bovine germ layers differentiation was significantly related to the DNA methylation status of Oct4 gene exon 1. This work firstly identified the DNA methylation profile of bovine Oct4 gene exon 1 and its association with germ layers development in fetus and adult of cattle. Moreover, the work also provided epigenetic information for further studying bovine embryonic development and cellular reprogramming.

Key words: bovine , DNA methylation , octamer-binding transcription factor 4 (Oct4) , exon , germ layer

ZHOU Xin-yu, LIU Liang-liang, JIA Wen-chao, PAN Chuan-ying. Methylation profile of bovine Oct4 gene coding region in relation to three germ layers[J]. Journal of Integrative Agriculture, 2016, 15(3): 618-628.

参考文献

ZHOU Xin-yu, E-mail: zhouxinyu0531@163.com; LIU Liangliang,E-mail: lingyun79626@126.com; Al-Khtib M, Blachère T, Guérin J F, Lefèvre A. 2012. Methylationprofile of the promoters of Nanog and Oct4 in ICSI humanembryos. Human Reproduction, 27, 2948-2954

Basu A, Dasari V, Mishra R K, Khosla S. 2014. The CpGisland encompassing the promoter and first exon of humanDNMT3L gene is a PcG/TrX response element (PRE).PLOS ONE, 9, e93561.

Beltrami A P, Cesselli D, Bergamin N, Marcon P, Rigo S,Puppato E, D’Aurizio F, Verardo R, Piazza S, PignatelliA, Poz A, Baccarani U, Damiani D, Fanin R, Mariuzzi L,Finato N, Masolini P, Burelli S, Belluzzi O, Schneider C,et al. 2007. Multipotent cells can be generated in vitro fromseveral adult human organs (heart, liver, and bone marrow).Blood, 110, 3438-3446

Brenet F, Moh M, Funk P, Feierstein E, Viale A J, Socci N D,Scandura J M. 2011. DNA methylation of the first exon istightly linked to transcriptional silencing. PLoS ONE, 6,e14524.

Buganim Y, Faddah D A, Cheng A W, Itskovich E, MarkoulakiS, Ganz K, Klemm S L, van Oudenaarden A, JaenischR. 2012. Single-cell expression analyses during cellularreprogramming reveal an early stochastic and a latehierarchic phase. Cell, 150, 1209-1222

Chaumeil J, Skok J A. 2012. The role of CTCF in regulatingV(D)J recombination. Current Opinion in Immunology, 24,153-159

Choy M K, Movassagh M, Goh H G, Bennett M R, Down TA, Foo R S. 2010. Genome-wide conserved consensustranscription factor binding motifs are hyper-methylated.BMC Genomics, 11, 519.

Corry G N, Tanasijevic B, Barry E R, Krueger W, RasmussenT P. 2009. Rasmussen epigenetic regulatory mechanismsduring pre-implantation development. Birth DefectsResearch (Part C: Embryo Today: Reviews), 87, 297-313

Davis S F, Hood J, Thomas A, Bunnell B A. 2006. Isolationof adult rhesus neural stem and progenitor cells anddifferentiation into immature oligodendrocytes. Stem Cellsand Development, 15, 191-199

Van Dyck F, Declercq J, Braem C V, Van de Ven W J. 2007.PLAG1, the prototype of the PLAG gene family: Versatilityin tumour development. International Journal of Oncology,30, 765-774

Goissis M D, Cibelli J B. 2014. Functional characterizationof SOX2 in bovine preimplantation embryos. Biology ofReproduction, 90, 30.

Harvey E B. 1959. Aging and foetal development. In: Cole HH, Eupps P T, eds., Reproduction in Domestic Animals.Academic Press, New York, America. pp. 461-466

Hawkins K, Joy S, McKay T. 2014. Cell signalling pathwaysunderlying induced pluripotent stem cell reprogramming.World Journal of Stem Cells, 6, 620-628

Hernández-Negrete I, Sala-Newby G B, Perl A, Kunkel GR, Newby A C, Bond M. 2011. Adhesion-dependentSkp2 transcription requires selenocysteine tRNA genetranscription-activating factor (STAF). The BiochemicalJournal, 436, 133-143

Herreros-Villanueva M, Bujanda L, Billadeau D D, Zhang J S.2014. Embryonic stem cell factors and pancreatic cancer.World Journal of Gastroenterology, 20, 2247-2255

Hilger-Eversheim K, Moser M, Schorle H, Buettner R. 2000.Regulatory roles of AP-2 transcription factors in vertebratedevelopment, apoptosis and cell-cycle control. Gene, 260,1-12

Hou P, Li Y, Zhang X, Liu C, Guan J, Li H, Zhao T, Ye J, YangW, Liu K, Ge J, Xu J, Zhang Q, Zhao Y, Deng H. 2013.Pluripotent stem cells induced from mouse somatic cellsby small-molecule compounds. Science, 341, 651-654

Illingworth R S, Bird A P. 2009. CpG islands - ’a rough guide’.FEBS Letters, 583, 1713-1720

Jerabek S, Merino F, Schöler H R, Cojocaru V. 2014. OCT4:Dynamic DNA binding pioneers stem cell pluripotency.Biochimica et Biophysica Acta, 1839, 138-154

Kelly V P, Suzuki T, Nakajima O, Arai T, Tamai Y, TakahashiS, Nishimura S, Yamamoto M. 2005. The distal sequenceelement of the selenocysteine tRNA gene is a tissuedependentenhancer essential for mouse embryogenesis.Molecular and Cellular Biology, 25, 3658-3669

Kim J, Chu J, Shen X, Wang J, Orkin S H. 2008. An extendedtranscriptional network for pluripotency of embryonic stemcells. Cell, 132, 1049-1061

Kumar D, Talluri T R, Anand T, Kues W A 2015. Inducedpluripotent stem cells: Mechanisms, achievements andperspectives in farm animals. World Journal of Stem Cells,7, 315-328

Li J Y, Pu M T, Hirasawa R, Li B Z, Huang Y N, Zeng R, JingN H, Chen T, Li E, Sasaki H, Xu G L. 2007. Synergisticfunction of DNA methyltransferases Dnmt3a and Dnmt3b inthe methylation of Oct4 and Nanog. Molecular and CellularBiology, 27, 8748-8759

Li L C, Dahiya R. 2002. MethPrimer: designing primers formethylation PCRs. Bioinformatics, 18, 1427-1431

Ling T Y, Kuo M D, Li C L, Yu A L, Huang Y H, Wu T J, LinY C, Chen S H, Yu J. 2006. Identification of pulmonaryOct-4+ stem/progenitor cells and demonstration of theirsusceptibility to SARS coronavirus (SARS-CoV) infectionin vitro. Proceedings of the National Academy of Sciencesof the United States America, 103, 9530-9535

Liu K, Song Y, Yu H, Zhao T. 2014. Understanding theroadmaps to induced pluripotency. Cell Death & Disease,5, e1232.

Loh Y H, Wu Q, Chew J L, Vega V B, Zhang W, Chen X,Bourque G, George J, Leong B, Liu J, Wong K Y, Sung K W,Lee C W, Zhao X D, Chiu K P, Lipovich L, Kuznetsov V A,Robson P, Stanton L W, Wei C L, et al. The Oct4 and Nanogtranscription network regulates pluripotency in mouseembryonic stem cells. Nature Genetics, 38, 431-440

Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R,Takahashi K, Okochi H, Okuda A, Matoba R, Sharov A A,Ko M S, Niwa H. 2007. Pluripotency governed by Sox2 viaregulation of Oct3/4 expression in mouse embryonic stemcells. Nature Cell Biology, 9, 625-635

Moser M, Imhof A, Pscherer A, Bauer R, Amselgruber W,Sinowatz F, Hofstädter F, Schüle R, Buettner R

1995.Cloning and characterization of a second AP-2 transcriptionfactor: AP-2 beta. Development, 121, 2779-2788

Nei M, Li W H. 1979. Mathematical model for studying geneticvariation in terms of restriction endonucleases. Proceedingsof the National Academy of Sciences of the United Statesof America, 76, 5269-5273

Okuda T, Tagawa K, Qi M L, Hoshio M, Ueda H, Kawano H,Kanazawa I, Muramatsu M, Okazawa H. 2004. Oct-3/4repression accelerates differentiation of neural progenitorcells in vitro and in vivo. Brain Research. Molecular BrainResearch, 132, 18-30

Palmieri S L, Peter W, Hess H, Schöler H R. 1994. Oct-4transcription factor is differentially expressed in the mouseembryo during establishment of the first two extraembryoniccell lineages involved in implantation. DevelopmentalBiology, 166, 259-267

Pan C, Jia W, Wu X, Zhao H, Liu S, Lei C, Lan X, Chen H.2013. DNA methylation profile of DNA methyltransferase3b (Dnmt3b) gene and its influence on growth traits in goat.The Journal of Animal and Plant Sciences, 23, 380-387

Park I H, Zhao R, West J A, Yabuuchi A, Huo H, Ince T A, LerouP H, Lensch M W, Daley G Q. 2008. Reprogramming ofhuman somatic cells to pluripotency with defined factors.Nature, 451, 141-146

Qin C H, Chu Q, Chu G Y, Zhang Y, Zhang Q, Zhang S L, SunD X. 2014. Mapping QTLs affecting economic traits on BTA3in Chinese holstein with microsatellite markers. Journal ofIntegrative Agriculture, 13, 1999-2004

Robertson K D, Wolffe A P. 2000. DNA methylation in healthand disease. Nature Reviews Genetics, 1, 11-19

Rosner M H, Vigano M A, Ozato K, Timmons P M, Poirier F,Rigby P W, Staudt L M. 1990. A POU-domain transcriptionfactor in early stem cells and germ cells of the mammalianembryo. Nature, 345, 686-692

Sagrinati C, Netti G S, Mazzinghi B, Lazzeri E, Liotta F, FrosaliF, Ronconi E, Meini C, Gacci M, Squecco R, Carini M,Gesualdo L, Francini F, Maggi E, Annunziato F, LasagniL, Serio M, Romagnani S, Romagnani P. 2006. Isolationand characterization of multipotent progenitor cells fromthe Bowman’s capsule of adult human kidneys. Journal ofAmerican Society of Nephrology, 17, 2443-2456

Santos F, Hendrich B, Reik W, Dean W. 2002. Dynamicreprogramming of DNA methylation in the early mouseembryo. Developmental Biology, 241, 172-182

Takahashi K, Yamanaka S. 2006. Induction of pluripotent stemcells from mouse embryonic and adult fibroblast culturesby defined factors. Cell, 126, 663-676

Thomas T, Nowka K, Lan L, Derwahl M. 2006. Expression ofendoderm stem cell markers: evidence for the presenceof adult stem cells in human thyroid glands. Thyroid, 16,537-544

Wang H, Maurano M T, Qu H, Varley K E, Gertz J, Pauli F, LeeK, Canfield T, Weaver M, Sandstrom R, Thurman R E, KaulR, Myers R M, Stamatoyannopoulos J A. 2012. Widespreadplasticity in CTCF occupancy linked to DNA methylation.Genome Research, 22, 1680-1688

Wei Z, Yang Y, Zhang P, Andrianakos R, Hasegawa K, Lyu J,Chen X, Bai G, Liu C, Pera M, Lu W. 2009. Klf4 interactsdirectly with Oct4 and Sox2 to promote reprogramming.Stem Cells, 27, 2969-2978

Werling U, Schorle H. 2002. Transcription factor gene AP-2γessential for early murine development. Molecular andCellular Biology, 22, 3149-3156

West-Mays J A, Coyle B M, Piatigorsky J, Papagiotas S, LibbyD. 2002. Ectopic expression of AP-2α transcription factorin the lens disrupts fiber cell differentiation. DevelopmentalBiology, 245, 13-27

Winters L M, Green W W, Comstock R E. 1942. Prenataldevelopment of the bovine. University of Minnesota,Agricultural Experiment Station, 151, 1-50

Wu G, Schöler H R 2014. Role of Oct4 in the early embryodevelopment. Cell Regeneration (London, England), 3, 7.

Xu W H, Li Z C, Ouyang Z P, Yu B, Shi J S, Liu D W, Wu Z F.2015. RNA-Seq transcriptome analysis of porcine clonedand in vitro fertilized blastocysts. Journal of IntegrativeAgriculture, 14, 926-938

Yamazaki Y, Fujita T C, Low E W, Alarcón V B, YanagimachiR, Marikawa Y. 2006. Gradual DNA demethylation ofthe Oct4 promoter in cloned mouse embryos. MolecularReproduction and Development, 73, 180-188

Yeom Y I, Fuhrmann G, Ovitt C E, Brehm A, Ohbo K, Gross M,Hubner K, Scholer H R. 1996. Germline regulatory elementof Oct-4 specific for the totipotent cycle of embryonal cells.Development, 122, 881-894

Yu J, Vodyanik M A, Smuga-Otto K, Antosiewicz-Bourget J,Frane J L, Tian S, Nie J, Jonsdottir G A, Ruotti V, StewartR, Slukvin I I, Thomson J A. 2007. Induced pluripotent stemcell lines derived from human somatic cells. Science, 318,1917-1920

Zhang H J, Siu M K, Wong E S, Wong K Y, Li A S, Chan KY, Ngan H Y, Cheung A N. 2008. Oct4 is epigeneticallyregulated by methylation in normal placenta and gestationaltrophoblastic disease. Placenta, 29, 549-554

[1]	ZHANG Yong-qiang, LIU Hai-sheng, WU Xiao-dong, WANG Xiao-zhen, LI Jin-ming, ZHAO Yonggang, Lü Yan, REN Wei-jie, GE Sheng-qiang, WANG Zhi-liang. A novel real-time RT-PCR with TaqMan-MGB probes and its application in detecting BVDV infections in dairy farms[J]. Journal of Integrative Agriculture, 2015, 14(8): 1637-1643.
[2]	Jianhong E Mu, Bruce A McCarl, Amy Hagerman, David Bessler. Impacts of bovine spongiform encephalopathy and avian influenza on U.S. meat demand[J]. Journal of Integrative Agriculture, 2015, 14(6): 1130-1141.
[3]	WEI Fang, HU Jie, CUI Ming-zhu, ZHANG Yan-hui, LI Yun-ling , TIAN Bao-ming. Global Analysis of Cytosine Methylation and Proteome Under Cold Treatment in Brassica napus[J]. Journal of Integrative Agriculture, 2014, 13(10): 2170-2176.
[4]	JIA Li-jun, ZHANG Shou-fa, CAO Shi-nuo, QIAN Nian-chao, YU Long-zheng , XUAN Xue-nan. The Finding and Phylogenetic Evolution Analysis of Bovine Piroplasms in the Ras?n Area of North Korea[J]. Journal of Integrative Agriculture, 2013, 12(10): 1847-1854.
[5]	LI Shan-shan, WEI Hong-yang, BU Deng-pan, ZHANG Le-ying, ZHOU Ling-yun . Identification of Bovine Casein Phosphorylation Using Titanium Dioxide Enrichment in Combination with Nano Electrospray Ionization Tandem Mass Spectrometry[J]. Journal of Integrative Agriculture, 2012, 12(3): 439-445.
[6]	TONG Jin-jin, LI Ye, LIU Rong, GAO Xue-jun , LI Qing-zhang. Effect of Semen vaccariae and Taraxacumogono on CellAdhesion of Bovine Mammary Epithelial Cells[J]. Journal of Integrative Agriculture, 2012, 12(12): 2043-2050.
[7]	LI Ming-gui, LIU Zhen-shan, PAN Zeng-xiang, LUO Hua, XIE Zhuang,LI Qi-fa. The mRNA Expression and Methylation Status in Imprinting Control Region of H19 Gene Between Cattle-Yak and Their Parents[J]. Journal of Integrative Agriculture, 2012, 12(10): 1691-1699.
[8]	SUNDong-bo, WURui, HEXian-jing, WANGShuang, LINYun-cheng, HANXu, WANGYue-qiang, GUOTing-ting, WUGuo-jun , YANGKe-li. Development of a Multiplex PCR for Diagnosis of Staphylococcus aureus, Escherichia coli and Bacillus cereus from Cows with Endometritis[J]. Journal of Integrative Agriculture, 2011, 10(10): 1624-1629.

Methylation profile of bovine Oct4 gene coding region in relation to three germ layers

Methylation profile of bovine Oct4 gene coding region in relation to three germ layers

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 8

编辑推荐

Metrics