Specific gene-regulation networks during the pre-implantation development of the pig embryo as revealed by deep sequencing

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Cao, Suying ^a,b   Han, Jianyong ^a   Wu, Jun ^c   Li, Qiuyan ^a   Liu, Shichao ^d   Zhang, Wei ^a   Pei, Yangli ^a   Ruan, Xiaoan ^e   Liu, Zhonghua ^d   Wang, Xumin ^f   Lim, Bing ^e   Li, Ning ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF AGRICULTURE   (China)

^c Beijing Novogene Bioinformatics Technology   (China)

^d NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^e GENOME INSTITUTE OF SINGAPORE   (Singapore)

^f Chinese Academy of Sciences and China National Center for Bioinformation   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; FATTY ACID; MESSENGER RNA; TRANSCRIPTOME;

ANIMAL; ANIMAL EMBRYO; BLASTOCYST; C57BL MOUSE; CHEMISTRY; CYTOLOGY; ECTODERM; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GENETIC ENGINEERING; GENETIC LINKAGE; GENOME; HIGH THROUGHPUT SEQUENCING; METABOLISM; MOUSE; PLURIPOTENT STEM CELL; SEQUENCE ANALYSIS; SWINE;

ANIMALS; BIOLOGICAL MARKERS; BLASTOCYST; ECTODERM; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FATTY ACIDS; FEMALE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENETIC ENGINEERING; GENETIC LINKAGE; GENOME; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICE; MICE, INBRED C57BL; PLURIPOTENT STEM CELLS; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; SWINE; TRANSCRIPTOME;

EID: 84894030294     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-4     Document Type: Article

References (54)

1. Hubner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, De La Fuente R, Wood J, Strauss JF, Boiani M, Scholer HR. Derivation of oocytes from mouse embryonic stem cells. Science 2003, 300(5623):1251-1256. 10.1126/science.1083452, 12730498.
2. Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 2004, 427(6970):148-154. 10.1038/nature02247, 14668819.
3. Buehr M, Meek S, Blair K, Yang J, Ure J, Silva J, McLay R, Hall J, Ying QL, Smith A. Capture of authentic embryonic stem cells from rat blastocysts. Cell 2008, 135(7):1287-1298. 10.1016/j.cell.2008.12.007, 19109897.
4. Nagy A, Gocza E, Diaz EM, Prideaux VR, Ivanyi E, Markkula M, Rossant J. Embryonic stem cells alone are able to support fetal development in the mouse. Development 1990, 110(3):815-821.
5. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292(5819):154-156. 10.1038/292154a0, 7242681.
6. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282(5391):1145-1147.
7. Hall V. Porcine embryonic stem cells: a possible source for cell replacement therapy. Stem Cell Rev 2008, 4(4):275-282. 10.1007/s12015-008-9040-2, 18770051.
8. Brevini TA, Antonini S, Cillo F, Crestan M, Gandolfi F. Porcine embryonic stem cells: facts, challenges and hopes. Theriogenology 2007, 68(Suppl 1):S206-S213.
9. Ezashi T, Telugu BP, Alexenko AP, Sachdev S, Sinha S, Roberts RM. Derivation of induced pluripotent stem cells from pig somatic cells. Proc Natl Acad Sci USA 2009, 106(27):10993-10998. 10.1073/pnas.0905284106, 2698893, 19541600.
10. Wu Z, Chen J, Ren J, Bao L, Liao J, Cui C, Rao L, Li H, Gu Y, Dai H, et al. Generation of pig induced pluripotent stem cells with a drug-inducible system. J Mol Cell Biol 2009, 1(1):46-54. 10.1093/jmcb/mjp003, 19502222.
11. Esteban MA, Xu J, Yang J, Peng M, Qin D, Li W, Jiang Z, Chen J, Deng K, Zhong M, et al. Generation of induced pluripotent stem cell lines from Tibetan miniature pig. J Biol Chem 2009, 284(26):17634-17640. 10.1074/jbc.M109.008938, 2719402, 19376775.
12. West FD, Uhl EW, Liu Y, Stowe H, Lu Y, Yu P, Gallegos-Cardenas A, Pratt SL, Stice SL. Brief report: chimeric pigs produced from induced pluripotent stem cells demonstrate germline transmission and no evidence of tumor formation in young pigs. Stem Cells 2011, 29(10):1640-1643. 10.1002/stem.713, 22039609.
13. Hall VJ, Christensen J, Gao Y, Schmidt MH, Hyttel P. Porcine pluripotency cell signaling develops from the inner cell mass to the epiblast during early development. Dev Dyn 2009, 238(8):2014-2024. 10.1002/dvdy.22027, 19618464.
14. Xie D, Chen CC, Ptaszek LM, Xiao S, Cao X, Fang F, Ng HH, Lewin HA, Cowan C, Zhong S. Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Res 2010, 20(6):804-815. 10.1101/gr.100594.109, 2877577, 20219939.
15. Duncan FE, Schultz RM. Gene expression profiling of mouse oocytes and preimplantation embryos. Methods Enzymol 2010, 477:457-480.
16. Hamatani T, Carter MG, Sharov AA, Ko MS. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 2004, 6(1):117-131. 10.1016/S1534-5807(03)00373-3, 14723852.
17. Sharov AA, Piao Y, Matoba R, Dudekula DB, Qian Y, VanBuren V, Falco G, Martin PR, Stagg CA, Bassey UC, et al. Transcriptome analysis of mouse stem cells and early embryos. PLoS Biol 2003, 1(3):E74. 300684, 14691545.
18. Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X, Lao K, Surani MA. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell 2010, 6(5):468-478. 10.1016/j.stem.2010.03.015, 2954317, 20452321.
19. Fang H, Yang Y, Li C, Fu S, Yang Z, Jin G, Wang K, Zhang J, Jin Y. Transcriptome analysis of early organogenesis in human embryos. Dev Cell 2010, 19(1):174-184. 10.1016/j.devcel.2010.06.014, 20643359.
20. Tang F, Barbacioru C, Nordman E, Li B, Xu N, Bashkirov VI, Lao K, Surani MA. RNA-Seq analysis to capture the transcriptome landscape of a single cell. Nat Protoc 2010, 5(3):516-535. 10.1038/nprot.2009.236, 3847604, 20203668.
21. Yan L, Yang M, Guo H, Yang L, Wu J, Li R, Liu P, Lian Y, Zheng X, Yan J, et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol 2013, 20(9):1131-1139. 10.1038/nsmb.2660, 23934149.
22. Schier AF. The maternal-zygotic transition: death and birth of RNAs. Science 2007, 316(5823):406-407. 10.1126/science.1140693, 17446392.
23. Wen DC, Yang CX, Cheng Y, Li JS, Liu ZH, Sun QY, Zhang JX, Lei L, Wu YQ, Kou ZH, et al. Comparison of developmental capacity for intra- and interspecies cloned cat (Felis catus) embryos. Mol Reprod Dev 2003, 66(1):38-45. 10.1002/mrd.10333, 12874797.
24. Chung Y, Bishop CE, Treff NR, Walker SJ, Sandler VM, Becker S, Klimanskaya I, Wun WS, Dunn R, Hall RM, et al. Reprogramming of human somatic cells using human and animal oocytes. Cloning Stem Cells 2009, 11(2):213-223. 10.1089/clo.2009.0004, 19186982.
25. Lorthongpanich C, Laowtammathron C, Chan AW, Ketudat-Cairns M, Parnpai R. Development of interspecies cloned monkey embryos reconstructed with bovine enucleated oocytes. J Reprod Dev 2008, 54(5):306-313. 10.1262/jrd.20049, 18591865.
26. Beyhan Z, Iager AE, Cibelli JB. Interspecies nuclear transfer: implications for embryonic stem cell biology. Cell Stem Cell 2007, 1(5):502-512. 10.1016/j.stem.2007.10.009, 18371390.
27. Chen T, Zhang YL, Jiang Y, Liu JH, Schatten H, Chen DY, Sun QY. Interspecies nuclear transfer reveals that demethylation of specific repetitive sequences is determined by recipient ooplasm but not by donor intrinsic property in cloned embryos. Mol Reprod Dev 2006, 73(3):313-317. 10.1002/mrd.20421, 16362970.
28. Braude P, Bolton V, Moore S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 1988, 332(6163):459-461. 10.1038/332459a0, 3352746.
29. Jarrell VL, Day BN, Prather RS. The transition from maternal to zygotic control of development occurs during the 4-cell stage in the domestic pig, Sus scrofa: quantitative and qualitative aspects of protein synthesis. Biol Reprod 1991, 44(1):62-68. 10.1095/biolreprod44.1.62, 2015352.
30. Latham KE. Early and delayed aspects of nuclear reprogramming during cloning. Biol Cell 2005, 97(2):119-132. 10.1042/BC20040068, 15656778.
31. Mann MR, Bartolomei MS. Epigenetic reprogramming in the mammalian embryo: struggle of the clones. Genome Biol 2002, 3(2):REVIEWS1003. 139014, 11864375.
32. Arnold SJ, Robertson EJ. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 2009, 10(2):91-103. 10.1038/nrm2618, 19129791.
33. Zhang JD, Wiemann S. KEGGgraph: a graph approach to KEGG PATHWAY in R and bioconductor. Bioinformatics 2009, 25(11):1470-1471. 10.1093/bioinformatics/btp167, 2682514, 19307239.
34. Terashita Y, Sugimura S, Kudo Y, Amano R, Hiradate Y, Sato E. Improving the quality of miniature pig somatic cell nuclear transfer blastocysts: aggregation of SCNT embryos at the four-cell stage. Reprod Domest Anim 2011, 46(2):189-196. 10.1111/j.1439-0531.2010.01614.x, 20412512.
35. Niemann H, Rath D. Progress in reproductive biotechnology in swine. Theriogenology 2001, 56(8):1291-1304. 10.1016/S0093-691X(01)00630-6, 11758883.
36. Lin J, Shi L, Zhang M, Yang H, Qin Y, Zhang J, Gong D, Zhang X, Li D, Li J. Defects in trophoblast cell lineage account for the impaired in vivo development of cloned embryos generated by somatic nuclear transfer. Cell Stem Cell 2011, 8(4):371-375. 10.1016/j.stem.2011.02.007, 21474101.
37. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006, 38(4):431-440. 10.1038/ng1760, 16518401.
38. Waterman RA, Wall RJ. Lipid interactions with in vitro development of mammalian zygotes. Gamete Res 1988, 21(3):243-254. 10.1002/mrd.1120210306, 3149950.
39. Nonogaki T, Noda Y, Goto Y, Kishi J, Mori T. Developmental blockage of mouse embryos caused by fatty acids. J Assist Reprod Genet 1994, 11(9):482-488. 10.1007/BF02215713, 7633171.
40. McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK. Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil 2000, 118(1):163-170.
41. Loh HH, Law PY. The role of membrane lipids in receptor mechanisms. Annu Rev Pharmacol Toxicol 1980, 20:201-234. 10.1146/annurev.pa.20.040180.001221, 6247958.
42. Watkins EB, Miller CE, Majewski J, Kuhl TL. Membrane texture induced by specific protein binding and receptor clustering: active roles for lipids in cellular function. Proc Natl Acad Sci USA 2011, 108(17):6975-6980. 10.1073/pnas.1014579108, 3084047, 21474780.
43. Harder T. Lipid raft domains and protein networks in T-cell receptor signal transduction. Curr Opin Immunol 2004, 16(3):353-359. 10.1016/j.coi.2004.03.013, 15134785.
44. Bader B, Kuhn K, Owen DJ, Waldmann H, Wittinghofer A, Kuhlmann J. Bioorganic synthesis of lipid-modified proteins for the study of signal transduction. Nature 2000, 403(6766):223-226. 10.1038/35003249, 10646611.
45. Rondeau I, Picard S, Bah TM, Roy L, Godbout R, Rousseau G. Effects of different dietary omega-6/3 polyunsaturated fatty acids ratios on infarct size and the limbic system after myocardial infarction. Can J Physiol Pharmacol 2011, 89(3):169-176. 10.1139/Y11-007, 21423290.
46. Sellmayer A, Danesch U, Weber PC. Effects of different polyunsaturated fatty acids on growth-related early gene expression and cell growth. Lipids 1996, 31(Suppl):S37-S40.
47. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5(7):621-628. 10.1038/nmeth.1226, 18516045.
48. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26(1):139-140. 10.1093/bioinformatics/btp616, 2796818, 19910308.
49. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 2010, 11(3):R25. 10.1186/gb-2010-11-3-r25, 2864565, 20196867.
50. Wang L, Feng Z, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 2010, 26(1):136-138. 10.1093/bioinformatics/btp612, 19855105.
51. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28(5):511-515. 10.1038/nbt.1621, 3146043, 20436464.
52. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E. EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 2009, 19(2):327-335. 2652215, 19029536.
53. Smedley D, Haider S, Ballester B, Holland R, London D, Thorisson G, Kasprzyk A. BioMart biological queries made easy. BMC Genomics 2009, 10(1):22. 10.1186/1471-2164-10-22, 2649164, 19144180.
54. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13(11):2498-2504. 10.1101/gr.1239303, 403769, 14597658.