The Aorta-Gonad-Mesonephros Organ Culture Recapitulates 5hmC Reorganization and Replication-Dependent and Independent Loss of DNA Methylation in the Germline

Stem Cells and Development

Volumn 24, Issue 13, 2015, Pages 1536-1545

  Calvopina, Joseph Hargan ^a   Cook, Helene ^a   Vincent, John J ^a   Nee, Kevin ^a   Clark, Amander T ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; CYTOSINE; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL CELL; AORTA GONAD MESONEPHROS ORGAN CULTURE; ARTICLE; CELL COUNT; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL PROLIFERATION; DEMETHYLATION; DNA METHYLATION; EMBRYO; FEMALE; GENE; GENE LOCUS; GENOME IMPRINTING; GERM LINE; H19 GENE; MALE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; ORGAN CULTURE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; SNRPN GENE; ANIMAL; AORTA; CYTOLOGY; DNA REPLICATION; GERM CELL; GONAD; MESONEPHROS; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY;

MAMMALIA;

5-METHYLCYTOSINE; ANIMALS; AORTA; CELL PROLIFERATION; DNA METHYLATION; DNA REPLICATION; GERM CELLS; GONADS; MESONEPHROS; MICE; ORGAN CULTURE TECHNIQUES;

EID: 84931476499     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0410     Document Type: Article

References (36)

1. Anway MD, AS Cupp, M Uzumcu and MK Skinner. (2005). Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466-1469.
2. Seisenberger S, JR Peat, TA Hore, F Santos, W Dean, W Reik and PTRS B. (2013). Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Philos Trans R Soc Lond B Biol Sci 368:20110330.
3. Skinner MK, CG-BM Haque, E Nilsson, R Bhandari and JR McCarrey. (2013). Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line. PLoS One 8:e66318.
4. De Waal E, Y Yamazaki, P Ingale, M Bartolomei, R Yanagimachi and JR McCarrey. (2012). Primary epimutations introduced during intracytoplasmic sperm injection (ICSI) are corrected by germline-specific epigenetic reprogramming. Proc Natl Acad Sci U S A 109:4163-4168.
5. Seki Y, K Hayashi, K Itoh, M Mizugaki, M Saitou and Y Matsui. (2005). Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol 278:440-458.
6. Hajkova P, S Erhardt, N Lane, T Haaf, O El-Maarri, W Reik, J Walter and MA Surani. (2002). Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 117:15-23.
7. Lane N, W Dean, S Erhardt, P Hajkova, A Surani, J Walter and W Reik. (2003). Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35:88-93.
8. Maatouk DM, LD Kellam, MRW Mann, H Lei, E Li, MS Bartolomei and JL Resnick. (2006). DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages. Development 133:3411-3418.
9. Ng J, V Kumar, M Muratani, P Kraus, J Yeo, L Yaw and K Xue. (2013). In vivo epigenomic profiling of germ cells reveals germ cell molecular signatures. Dev Cell 24:324-333.
10. Seisenberger S, S Andrews, F Krueger, J Arand, J Walter, F Santos, C Popp, B Thienpont, W Dean and W Reik. (2012). The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48:849-862.
11. Mochizuki K, M Tachibana, M Saitou, Y Tokitake and Y Matsui. (2012). Implication of DNA demethylation and bivalent histone modification for selective gene regulation in mouse primordial germ cells. PLoS One 7:e46036.
12. Sachs M, C Onodera, K Blaschke, KT Ebata, JS Song and M Ramalho-Santos. (2013). Bivalent chromatin marks developmental regulatory genes in the mouse embryonic germline in vivo. Cell Rep 3:1777-1784.
13. Hajkova P, SJ Jeffries, C Lee, N Miller, SP Jackson and MA Surani. (2010). Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329:78-82.
14. Yamaguchi S, L Shen, Y Liu, D Sendler and Y Zhang. (2013). Role of Tet1 in erasure of genomic imprinting. Nature 504:460-464.
15. Dawlaty MM, A Breiling, T Le, G Raddatz, MI Barrasa, AW Cheng, Q Gao, BE Powell, Z Li, et al. (2013). Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev Cell 24:310-323.
16. Hackett J a, R Sengupta, JJ Zylicz, K Murakami, C Lee, T a Down and MA Surani. (2013). Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339:448-452.
17. Yamaguchi S, K Hong, R Liu, A Inoue, L Shen, K Zhang and Y Zhang. (2013). Dynamics of 5-methylcytosine and 5-hydroxymethylcytosine during germ cell reprogramming. Cell Res 23:329-339.
18. Yamaguchi S, K Hong, R Liu, L Shen, A Inoue, D Diep, K Zhang and Y Zhang. (2012). Tet1 controls meiosis by regulating meiotic gene expression. Nature 5:1-7.
19. Kagiwada S, K Kurimoto, T Hirota, M Yamaji and M Saitou. (2013). Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. EMBO J 32:340-353.
20. Hashimoto H, Y Liu, AK Upadhyay, Y Chang, SB Howerton, PM Vertino, X Zhang and X Cheng. (2012). Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation. Nucleic Acids Res 40:4841-4849.
21. Cortellino S, J Xu, M Sannai, R Moore, E Caretti, A Cigliano, M Le Coz, K Devarajan, A Wessels, et al. (2011). Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146:67-79.
22. Kawasaki Y, J Lee, A Matsuzawa, T Kohda, T Kaneko- Ishino and F Ishino. (2014). Active DNA demethylation is required for complete imprint erasure in primordial germ cells. Sci Rep 4:3658.
23. Ciccarone F, FG Klinger, A Catizone, R Calabrese, M Zampieri, MG Bacalini, M De Felici and P Caiafa. (2012). Poly(ADP-ribosyl)ation acts in the DNA demethylation of mouse primordial germ cells also with DNA damage-independent roles. PLoS One 7:e46927.
24. Hayashi K, S Ogushi, K Kurimoto, S Shimamoto, H Ohta and M Saitou. (2012). Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 338:971-975.
25. Hayashi K, H Ohta, K Kurimoto, S Aramaki and M Saitou. (2011). Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146:519-532.
26. Vincent JJ, Y Huang, P-Y Chen, S Feng, JH Calvopiña, K Nee, SA Lee, T Le, AJ Yoon, et al. (2013). Stage-specific roles for tet1 and tet2 in DNA demethylation in primordial germ cells. Cell Stem Cell 12:470-478.
27. Lengner CJ, FD Camargo, K Hochedlinger, G Grant, S Zaidi, S Gokhale, HR Scholer and A Tomilin. (2007). Oct4 expression is not required for mouse somatic stem cell self-renewal. Cell Stem Cell 1:403-415.
28. Wakeling SI, DC Miles and PS Western. (2013). Identifying disruptors of male germ cell development by small molecule screening in ex vivo gonad cultures. BMC Res Notes 6:168.
29. El-Maarri O, K Buiting, EG Peery, PM Kroisel, B Balaban, K Wagner, B Urman, J Heyd, C Lich, et al. (2001). Maternal methylation imprints on human chromosome 15 are established during or after fertilization. Nat Genet 27:341-344.
30. Koopman P, A Munsterberg, B Capel, N Vivian and R Lovell-Badge. (1990). Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348:450-452.
31. Sekido R and R Lovell-Badge. (2008). Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453:930-934.
32. McLaren ABM. (1990). Development of mouse germ cells in cultures of fetal gonads. Cell Differ Dev 31:185-195.
33. Munsterberg A and R Lovell-badge. (1991). Expression of the mouse anti-Mullerian hormone gene suggests a role in both male and female sexual differentiation. Development 624:613-624.
34. Moe-Behrens GH, FG Klinger, W Esklid, T Grotmol, TB Haugen and M De Felici. (2003). Akt/PTEN signaling mediates estrogen-dependent proliferation of primordial germ cells in vitro. Mol Endocrinol 17:2630-2638.
35. Netchine I, S Rossignol, S Azzi, F Brioude and Y Le Bouc. (2012). Imprinted anomalies in fetal and childhood growth disorders: the model of Russell-Silver and Beckwith-Wiedemann syndromes. Endocr Dev 23:60-70.
36. Susiarjo M, I Sasson, C Mesaros and MS Bartolomei. (2013). Bisphenol a exposure disrupts genomic imprinting in the mouse. PLoS Genet 9:e1003401.