DNA methylation profiles provide a viable index for porcine pluripotent stem cells

Genesis

Volumn 51, Issue 11, 2013, Pages 763-776

  Arai, Yoshikazu ^a   Ohgane, Jun ^a   Fujishiro, Shuh Hei ^b   Nakano, Kazuaki ^a   Matsunari, Hitomi ^a   Watanabe, Masahito ^a   Umeyama, Kazuhiro ^a   Azuma, Dai ^a   Uchida, Naomi ^a   Sakamoto, Nozomu ^a   Makino, Tomohiro ^a   Yagi, Shintaro ^c   Shiota, Kunio ^c   Hanazono, Yutaka ^b,d   Nagashima, Hiroshi ^a  

^a MEIJI UNIVERSITY   (Japan)

^b JICHI MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Epigenetics; Induced pluripotent stem cells; Translational research

Indexed keywords

DNA; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BLASTOCYST; CELL LINE; CELLULAR PARAMETERS; CONTROLLED STUDY; CULTURE MEDIUM; DNA METHYLATION; EMBRYO; GENE; GENETIC SELECTION; INNER CELL MASS; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SWINE;

SUIDAE; SUS;

EPIGENETICS; INDUCED PLURIPOTENT STEM CELLS; TRANSLATIONAL RESEARCH;

ANIMALS; BLASTOCYST INNER CELL MASS; CELL LINE; CHIMERA; DNA METHYLATION; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; GENE EXPRESSION; GENES; GENETIC LOCI; INDUCED PLURIPOTENT STEM CELLS; MICE; SWINE; SWINE, MINIATURE; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84888127352     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22423     Document Type: Article

References (50)

1. Aoi T, Yae K, Nakagawa M, Ichisaka T, Okita K, Takahashi K, Chiba T, Yamanaka S. 2008. Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 321:699-702.
2. Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, Vallier L. 2007. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448:191-195.
3. Buehr M, Meek S, Blair K, Yang J, Ure J, Silva J, McLay R, Hall J, Ying QL, Smith A. 2008. Capture of authentic embryonic stem cells from rat blastocysts. Cell 135:1287-1298.
4. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, Loh YH, Yeo HC, Yeo ZX, Narang V, Govindarajan KR, Leong B, Shahab A, Ruan Y, Bourque G, Sung WK, Clarke ND, Wei CL, Ng HH. 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133:1106-1117.
5. Ebert AD, Yu J, Rose FF Jr, Mattis VB, Lorson CL, Thomson JA, Svendsen CN. 2009. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457:277-280.
6. Ezashi T, Telugu BP, Alexenko AP, Sachdev S, Sinha S, Roberts RM. 2009. Derivation of induced pluripotent stem cells from pig somatic cells. Proc Natl Acad Sci USA 106:10993-10998.
7. Fujishiro SH, Nakano K, Mizukami Y, Azami T, Arai Y, Matsunari H, Ishino R, Nishimura T, Watanabe M, Abe T, Furukawa Y, Umeyama K, Yamanaka S, Ema M, Nagashima H, Hanazono Y. 2013. Generation of naive-like porcine-induced pluripotent stem cells capable of contributing to embryonic and fetal development. Stem Cells Dev 22:473-482.
8. Golob JL, Paige SL, Muskheli V, Pabon L, Murry CE. 2008. Chromatin remodeling during mouse and human embryonic stem cell differentiation. Dev Dyn 237:1389-1398.
9. Hanna J, Markoulaki S, Mitalipova M, Cheng AW, Cassady JP, Staerk J, Carey BW, Lengner CJ, Foreman R, Love J, Gao Q, Kim J, Jaenisch R. 2009. Metastable pluripotent states in NOD-mouse-derived ESCs. Cell Stem Cell 4:513-524.
10. Hattori N, Nishino K, Ko YG, Hattori N, Ohgane J, Tanaka S, Shiota K. 2004. Epigenetic control of mouse Oct-4 gene expression in embryonic stem cells and trophoblast stem cells. J Biol Chem 279:17063-17069.
11. Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. 2011. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146:519-532.
12. Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. 2012. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 338:971-975.
13. Ikegami K, Ohgane J, Tanaka S, Yagi S, Shiota K. 2009. Interplay between DNA methylation, histone modification and chromatin remodeling in stem cells and during development. Int J Dev Biol 53:203-214.
14. Imaizumi Y, Okada Y, Akamatsu W, Koike M, Kuzumaki N, Hayakawa H, Nihira T, Kobayashi T, Ohyama M, Sato S, Takanashi M, Funayama M, Hirayama A, Soga T, Hishiki T, Suematsu M, Yagi T, Ito D, Kosakai A, Hayashi K, Shouji M, Nakanishi A, Suzuki N, Mizuno Y, Mizushima N, Amagai M, Uchiyama Y, Mochizuki H, Hattori N, Okano H. 2012. Mitochondrial dysfunction associated with increased oxidative stress and alpha-synuclein accumulation in PARK2 iPSC-derived neurons and postmortem brain tissue. Mol Brain 5:35.
15. Imamura M, Miura K, Iwabuchi K, Ichisaka T, Nakagawa M, Lee J, Kanatsu-Shinohara M, Shinohara T, Yamanaka S. 2006. Transcriptional repression and DNA hypermethylation of a small set of ES cell marker genes in male germline stem cells. BMC Dev Biol 6:34.
16. Inoue H, Yamanaka S. 2011. The use of induced pluripotent stem cells in drug development. Clin Pharmacol Ther 89:655-661.
17. Kobayashi T, Yamaguchi T, Hamanaka S, Kato-Itoh M, Yamazaki Y, Ibata M, Sato H, Lee YS, Usui J, Knisely AS, Hirabayashi M, Nakauchi H. 2010. Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell 142:787-799.
18. Li P, Tong C, Mehrian-Shai R, Jia L, Wu N, Yan Y, Maxson RE, Schulze EN, Song H, Hsieh CL, Pera MF, Ying QL. 2008. Germline competent embryonic stem cells derived from rat blastocysts. Cell 135:1299-1310.
19. Lieb JD, Beck S, Bulyk ML, Farnham P, Hattori N, Henikoff S, Liu XS, Okumura K, Shiota K, Ushijima T, Greally JM. 2006. Applying whole-genome studies of epigenetic regulation to study human disease. Cytogenet Genome Res 114:1-15.
20. Lunney JK. 2007. Advances in swine biomedical model genomics. Int J Biol Sci 3:179-184.
21. Matsunari H, Onodera M, Tada N, Mochizuki H, Karasawa S, Haruyama E, Nakayama N, Saito H, Ueno S, Kurome M, Miyawaki A, Nagashima H. 2008. Transgenic-cloned pigs systemically expressing red fluorescent protein, Kusabira-Orange. Cloning Stem Cells 10:313-323.
22. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, Gnirke A, Jaenisch R, Lander ES. 2008. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454:766-770.
23. Montserrat N, Bahima EG, Batlle L, Häfner S, Rodrigues AM, González F, Izpisúa Belmonte JC. 2011. Generation of pig iPS cells: A model for cell therapy. J Cardiovasc Transl Res 4:121-130.
24. Nagashima H, Giannakis C, Ashman RJ, Nottle MB. 2004. Sex differentiation and germ cell production in chimeric pigs produced by inner cell mass injection into blastocysts. Biol Reprod 70:702-707.
25. Nagy A, Rossant J. 1993. Production of completely ES cell-derived fetuses. In: Joyner AL, editor. Gene targeting: a practical approch. UK: IRL Press. p 147-179.
26. Niwa H, Miyazaki J, Smith AG. 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24:372-376.
27. Okita K, Ichisaka T, Yamanaka S. 2007. Generation of germline-competent induced pluripotent stem cells. Nature 448:313-317.
28. Okita K, Yamanaka S. 2011. Induced pluripotent stem cells: opportunities and challenges. Philos Trans R Soc Lond B Biol Sci 366:2198-2207.
29. Petters RM. 1994. Transgenic livestock as genetic models of human disease. Reprod Fertil Dev 6:643-645.
30. Prather RS, Hawley RJ, Carter DB, Lai L, Greenstein JL. 2003. Transgenic swine for biomedicine and agriculture. Theriogenology 59:115-123.
31. Rodríguez A, Allegrucci C, Alberio R. 2012. Modulation of pluripotency in the porcine embryo and iPS cells. PLoS One 7:e49079.
32. Sakaki-Yumoto M, Kobayashi C, Sato A, Fujimura S, Matsumoto Y, Takasato M, Kodama T, Aburatani H, Asashima M, Yoshida N, Nishinakamura R. 2006. The murine homolog of SALL4, a causative gene in Okihiro syndrome, is essential for embryonic stem cell proliferation, and cooperates with Sall1 in anorectal, heart, brain and kidney development. Development 133:3005-3013.
33. Sakamoto H, Suzuki M, Abe T, Hosoyama T, Himeno E, Tanaka S, Greally JM, Hattori N, Yagi S, Shiota K. 2007. Cell type-specific methylation profiles occurring disproportionately in CpG-less regions that delineate developmental similarity. Genes Cells 10:1123-1132.
34. Sato S, Yagi S, Arai Y, Hirabayashi K, Hattori N, Iwatani M, Okita K, Ohgane J, Tanaka S, Wakayama T, Yamanaka S, Shiota K. 2010. Genome-wide DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) residing in mouse pluripotent stem cells. Genes Cells 15:607-618.
35. Shiota K. 2004. DNA methylation profiles of CpG islands for cellular differentiation and development in mammals. Cytogenet Genome Res 105:325-334.
36. Shiota K, Kogo Y, Ohgane J, Imamura T, Urano A, Nishino K, Tanaka S, Hattori N. 2002. Epigenetic marks by DNA methylation specific to stem, germ and somatic cells in mice. Genes Cells 7:961-969.
37. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872.
38. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676.
39. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, McKay RD. 2007. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448:196-199.
40. Tsubooka N, Ichisaka T, Okita K, Takahashi K, Nakagawa M, Yamanaka S. 2009. Roles of Sall4 in the generation of pluripotent stem cells from blastocysts and fibroblasts. Genes Cells 14:683-694.
41. Usui J, Kobayashi T, Yamaguchi T, Knisely AS, Nishinakamura R, Nakauchi H. 2012. Generation of kidney from pluripotent stem cells via blastocyst complementation. Am J Pathol 180:2417-2426.
42. van der Spoel TI, Jansen of Lorkeers SJ, Agostoni P, van Belle E, Gyöngyösi M, Sluijter JP, Cramer MJ, Doevendans PA, Chamuleau SA. 2011. Human relevance of pre-clinical studies in stem cell therapy: systematic review and meta-analysis of large animal models of ischaemic heart disease. Cardiovasc Res 91:649-658.
43. West FD, Terlouw SL, Kwon DJ, Mumaw JL, Dhara SK, Hasneen K, Dobrinsky JR, Stice SL. 2010. Porcine induced pluripotent stem cells produce chimeric offspring. Stem Cells Dev 8:1211-1220.
44. West FD, Uhl EW, Liu Y, Stowe H, Lu Y, Yu P, Gallegos-Cardenas A, Pratt SL, Stice SL. 2011. Chimeric pigs produced from induced pluripotent stem cells demonstrate germline transmission and no evidence of tumor formation in young pigs. Stem Cells 10:1640-1643.
45. Wu Z, Chen J, Ren J, Bao L, Liao J, Cui C, Rao L, Li H, Gu Y, Dai H, Zhu H, Teng X, Cheng L, Xiao L. 2009. Generation of pig induced pluripotent stem cells with a drug-inducible system. J Mol Cell Biol 1:46-54.
46. Xu J, Pope SD, Jazirehi AR, Attema JL, Papathanasiou P, Watts JA, Zaret KS, Weissman IL, Smale ST. 2007. Pioneer factor interactions and unmethylated CpG dinucleotides mark silent tissue-specific enhancers in embryonic stem cells. Proc Natl Acad Sci USA 104:12377-12382.
47. Yagi S, Hirabayashi K, Sato S, Li W, Takahashi Y, Hirakawa T, Wu G, Hattori N, Hattori N, Ohgane J, Tanaka S, Liu XS, Shiota K. 2008. DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) in mouse promoter regions demonstrating tissue-specific gene expression. Genome Res 18:1969-1978.
48. Xiong Z, Laird PW. 1997. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res 25:2532-2534.
49. Zhao MT, Prather RS. 2011. The multi-potentiality of skin-derived stem cells in pigs. Theriogenology 75:1372-1380.
50. Zhou L, Wang W, Liu Y, Fernandez de Castro J, Ezashi T, Telugu BP, Roberts RM, Kaplan HJ, Dean DC. 2011. Differentiation of induced pluripotent stem cells of swine into rod photoreceptors and their integration into the retina. Stem Cells 29:972-980.