Skip to main content
SpringerLink
Log in
Book cover

Trends in Stem Cell Biology and Technology pp 83–100Cite as

Pluripotent Stem Cell Epigenetics During Development and Cancer

  • Chapter
  • First Online:

  • 865 Accesses

Abstract

Studies on biological development and cancer have pointed out the importance of specific epigenetic environments to maintain the equilibrium between repressed and activated genes. It has been possible to establish that this kind of environment induces chromatin structure modification and heritable changes in gene functions without altering primary DNA sequencing. We show here recent results of our laboratory on the expression of two imprinted genes, U2af1-rs1 and H19, in normal and pluripotent male germinal cells and in embryonic stem cell after induction of differentiation and apoptosis by retinoic acid treatments. These experimental observations can shed new light for a better understanding of testis embryonal carcinoma biology.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Esteller M, Herman JG. Cancer as an epigenetic disease: DNA methylation and chromatin alterations in human tumours. J Pathol 2002;196:1–7.

    Article  PubMed  CAS  Google Scholar 

  2. Fulka H, St John JC, Fulka J, Hozak P. Chromatin in early mammalian embryos: achieving the pluripotent state. Differentiation 2008;76:3–14.

    Article  PubMed  CAS  Google Scholar 

  3. Kiefer JC. Epigenetics in development. Dev Dyn 2007;236:1144–56.

    Article  PubMed  CAS  Google Scholar 

  4. Murrell A. Genomic imprinting and cancer: from primordial germ cells to somatic cells. Sci World J 2006;6:1888–910.

    Google Scholar 

  5. Rizzino A. Embryonic stem cells provide a powerful and versatile model system. Vitam Horm 2002;64:1–42.

    Article  PubMed  Google Scholar 

  6. Spivakov M, Fisher AG. Epigenetic signatures of stem-cell identity. Nat Rev Genet 2007;8:263–71.

    Article  PubMed  CAS  Google Scholar 

  7. Szutorisz H, Dillon N. The epigenetic basis for embryonic stem cell pluripotency. Bioessays 2005;27:1286–93.

    Article  PubMed  CAS  Google Scholar 

  8. Boyano MD, Andollo N, Zalduendo MM, Arechaga J. Imprinting in mammalian gametes is gene specific and do not occur at a single stage of differentiation. Int J Dev Biol 2008;52(8):1105–11.

    Article  PubMed  CAS  Google Scholar 

  9. Andollo N, Boyano MD, Andrade R, Arechaga JM. Epigenetic regulation of the imprinted U2af1-rs1 gene during retinoic acid-induced differentiation of embryonic stem cells. Dev Growth Differ 2006;48:349–60.

    Article  PubMed  CAS  Google Scholar 

  10. Andollo N, Boyano MD, Andrade R, et al. Structural and functional preservation of specific sequences of DNA and mRNA in apoptotic bodies from ES cells. Apoptosis 2005;10:417–28.

    Article  PubMed  CAS  Google Scholar 

  11. Harrison NJ, Baker D, Andrews PW. Culture adaptation of embryonic stem cells echoes germ cell malignancy. Int J Androl 2007;30:275–81.

    Article  PubMed  Google Scholar 

  12. Diez-Torre A, Silvan U, De Wever O, Bruyneel E, Mareel M, Arechaga J. Germinal tumor invasion and the role of the testicular stroma. Int J Dev Biol 2004;48:545–57.

    Article  PubMed  CAS  Google Scholar 

  13. Ferguson-Smith AC, Surani MA. Imprinting and the epigenetic asymmetry between parental genomes. Science 2001;293:1086–9.

    Article  PubMed  CAS  Google Scholar 

  14. da Rocha ST, Ferguson-Smith AC. Genomic imprinting. Curr Biol 2004;14:646–9.

    Article  Google Scholar 

  15. Feil R, Handel MA, Allen ND, Reik W. Chromatin structure and imprinting: developmental control of DNase-I sensitivity in the mouse insulin-like growth factor 2 gene. Dev Genet 1995;17:240–52.

    Article  PubMed  CAS  Google Scholar 

  16. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33 Supp 1: 245–54.

    Article  PubMed  CAS  Google Scholar 

  17. Durcova-Hills G, Burgoyne P, McLaren A. Analysis of sex differences in EGC imprinting. Dev Biol 2004;268:105–10.

    Article  PubMed  CAS  Google Scholar 

  18. Delaval K, Feil R. Epigenetic regulation of mammalian genomic imprinting. Curr Opin Genet Dev 2004;14:188–95.

    Article  PubMed  CAS  Google Scholar 

  19. Gregory RI, O’Neill LP, Randall TE, et al. Inhibition of histone deacetylases alters allelic chromatin conformation at the imprinted U2af1-rs1 locus in mouse embryonic stem cells. J Biol Chem 2002;277:11728–34.

    Article  PubMed  CAS  Google Scholar 

  20. Drewell RA, Goddard CJ, Thomas JO, Surani MA. Methylation-dependent silencing at the H19 imprinting control region by MeCP2. Nucleic Acids Res 2002;30:1139–44.

    Article  PubMed  CAS  Google Scholar 

  21. Hatada I, Sugama T, Mukai T. A new imprinted gene cloned by a methylation-sensitive genome scanning method. Nucleic Acids Res 1993;21:5577–82.

    Article  PubMed  CAS  Google Scholar 

  22. Hayashizaki Y, Shibata H, Hirotsune S, et al. Identification of an imprinted U2af binding protein related sequence on mouse chromosome 11 using the RLGS method. Nat Genet 1994;6:33–40.

    Article  PubMed  CAS  Google Scholar 

  23. Brannan CI, Dees EC, Ingram RS, Tilghman SM. The product of the H19 gene may function as an RNA. Mol Cell Biol 1990;10:28–36.

    PubMed  CAS  Google Scholar 

  24. Bartolomei MS, Tilghman SM. Genomic imprinting in mammals. Annu Rev Genet 1997;31:493–525.

    Article  PubMed  CAS  Google Scholar 

  25. El-Maarri O, Buiting K, Peery EG, et al. Maternal methylation imprints on human chromosome 15 are established during or after fertilization. Nat Genet 2001;27:341–4.

    Article  PubMed  CAS  Google Scholar 

  26. Reik W, Walter J. Evolution of imprinting mechanisms: the battle of the sexes begins in the zygote. Nat Genet 2001;27:255–6.

    Article  PubMed  CAS  Google Scholar 

  27. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. Demethylation of the zygotic paternal genome. Nature 2000;403:501–2.

    Article  PubMed  CAS  Google Scholar 

  28. Oswald J, Engemann S, Lane N, et al. Active demethylation of the paternal genome in the mouse zygote. Curr Biol 2000;10:475–8.

    Article  PubMed  CAS  Google Scholar 

  29. Santos F, Hendrich B, Reik W, Dean W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002;241:172–82.

    Article  PubMed  CAS  Google Scholar 

  30. Ueda T, Abe K, Miura A, et al. The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells 2000;5:649–59.

    Article  PubMed  CAS  Google Scholar 

  31. Davis TL, Yang GJ, McCarrey JR, Bartolomei MS. The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet 2000;9:2885–94.

    Article  PubMed  CAS  Google Scholar 

  32. Feil R, Khosla S. Genomic imprinting in mammals: an interplay between chromatin and DNA methylation? Trends Genet 1999;15:431–5.

    Article  PubMed  CAS  Google Scholar 

  33. Hark AT, Tilghman SM. Chromatin conformation of the H19 epigenetic mark. Hum Mol Genet 1998;7:1979–85.

    Article  PubMed  CAS  Google Scholar 

  34. Khosla S, Aitchison A, Gregory R, Allen ND, Feil R. Parental allele-specific chromatin configuration in a boundary-imprinting-control element upstream of the mouse H19 gene. Mol Cell Biol 1999;19:2556–66.

    PubMed  CAS  Google Scholar 

  35. Hajkova P, Erhardt S, Lane N et al. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 2002;117:15–23.

    Article  PubMed  CAS  Google Scholar 

  36. Li JY, Lees-Murdock DJ, Xu GL, Walsh CP. Timing of establishment of paternal methylation imprints in the mouse. Genomics 2004;84:952–60.

    Article  PubMed  CAS  Google Scholar 

  37. Trasler JM. Gamete imprinting: setting epigenetic patterns for the next generation. Reprod Fertil Dev 2006;18:63–9.

    Article  PubMed  Google Scholar 

  38. Mummery CL, Feyen A, Freund E, Shen S. Characteristics of embryonic stem cell differentiation: a comparison with two embryonal carcinoma cell lines. Cell Differ Dev 1990;30:195–206.

    Article  PubMed  CAS  Google Scholar 

  39. Rohwedel J, Guan K, Wobus AM. Induction of cellular differentiation by retinoic acid in vitro. Cells Tissues Organs 1999;165:190–202.

    Article  PubMed  CAS  Google Scholar 

  40. Razin A, Kantor B. DNA methylation in epigenetic control of gene expression. Prog Mol Subcell Biol 2005;38:151–67.

    Article  PubMed  CAS  Google Scholar 

  41. Cerny J, Quesenberry PJ. Chromatin remodeling and stem cell theory of relativity. J Cell Physiol 2004;201:1–16.

    Article  PubMed  CAS  Google Scholar 

  42. Bird A. The essentials of DNA methylation. Cell 1992;70:5–8.

    Article  PubMed  CAS  Google Scholar 

  43. Razin A, Cedar H. DNA methylation and genomic imprinting. Cell 1994;77:473–6.

    Article  PubMed  CAS  Google Scholar 

  44. Tilghman SM. The sins of the fathers and mothers: genomic imprinting in mammalian development. Cell 1999;96:185–93.

    Article  PubMed  CAS  Google Scholar 

  45. Feil R, Boyano MD, Allen ND, Kelsey G. Parental chromosome-specific chromatin conformation in the imprinted U2af1-rs1 gene in the mouse. J Biol Chem 1997;272:20893–900.

    Article  PubMed  CAS  Google Scholar 

  46. Nabetani A, Hatada I, Morisaki H, Oshimura M, Mukai T. Mouse U2af1-rs1 is a neomorphic imprinted gene. Mol Cell Biol 1997;17:789–98.

    PubMed  CAS  Google Scholar 

  47. Feil R, Walter J, Allen ND, Reik W. Developmental control of allelic methylation in the imprinted mouse Igf2 and H19 genes. Development 1994;120:2933–43.

    PubMed  CAS  Google Scholar 

  48. Vizirianakis IS, Pappas IS, Gougoumas D, Tsiftsoglou AS. Expression of ribosomal protein S5 cloned gene during differentiation and apoptosis in murine erythroleukemia (MEL) cells. Oncol Res 1999;11:409–19.

    PubMed  CAS  Google Scholar 

  49. Warnecke PM, Clark SJ. DNA methylation profile of the mouse skeletal alpha-actin promoter during development and differentiation. Mol Cell Biol 1999;19:164–72.

    PubMed  CAS  Google Scholar 

  50. Kaneko KJ, Rein T, Guo ZS, Latham K, DePamphilis ML. DNA methylation may restrict but does not determine differential gene expression at the Sgy/Tead2 locus during mouse development. Mol Cell Biol 2004;24:1968–82.

    Article  PubMed  CAS  Google Scholar 

  51. Cho KS, Elizondo LI, Boerkoel CF. Advances in chromatin remodeling and human disease. Curr Opin Genet Dev 2004;14:308–15.

    Article  PubMed  CAS  Google Scholar 

  52. Lee JH, Hart SR, Skalnik DG. Histone deacetylase activity is required for embryonic stem cell differentiation. Genesis 2004;38:32–8.

    Article  PubMed  CAS  Google Scholar 

  53. El Kharroubi A, Piras G, Stewart CL. DNA demethylation reactivates a subset of imprinted genes in uniparental mouse embryonic fibroblasts. J Biol Chem 2001;276:8674–80.

    Article  PubMed  CAS  Google Scholar 

  54. Hattori N, Abe T, Suzuki M et al. Preference of DNA methyltransferases for CpG islands in mouse embryonic stem cells. Genome Res 2004;14:1733–40.

    Article  PubMed  CAS  Google Scholar 

  55. Liu L, Saldanha SN, Pate MS, Andrews LG, Tollefsbol TO. Epigenetic regulation of human telomerase reverse transcriptase promoter activity during cellular differentiation. Genes Chromosomes Cancer 2004;41:26–37.

    Article  PubMed  CAS  Google Scholar 

  56. Rugg-Gunn PJ, Ferguson-Smith AC, Pedersen RA. Human embryonic stem cells as a model for studying epigenetic regulation during early development. Cell Cycle 2005;4:1323–6.

    Article  PubMed  CAS  Google Scholar 

  57. Szutorisz H, Canzonetta C, Georgiou A, Chow CM, Tora L, Dillon N. Formation of an active tissue-specific chromatin domain initiated by epigenetic marking at the embryonic stem cell stage. Mol Cell Biol 2005;25:1804–20.

    Article  PubMed  CAS  Google Scholar 

  58. Jones PA. Cancer Death and methylation. Nature 2001;409:141, 143–4.

    Article  Google Scholar 

  59. Atencia R, Garcia-Sanz M, Unda F, Arechaga J. Apoptosis during retinoic acid-induced differentiation of F9 embryonal carcinoma cells. Exp Cell Res 1994;214:663–7.

    Article  PubMed  CAS  Google Scholar 

  60. Asumendi A, Andollo N, Boyano MD, et al. The role of cleavage of cell structures during apoptosis. Cell Mol Biol (Noisy-le-grand) 2000;46:1–11.

    CAS  Google Scholar 

  61. Saitoh F, Hiraishi K, Adachi M, Hozumi M. Induction by 5-aza-2′-deoxycytidine, an inhibitor of DNA methylation, of Le(y) antigen, apoptosis and differentiation in human lung cancer cells. Anticancer Res 1995;15:2137–43.

    PubMed  CAS  Google Scholar 

  62. Jackson-Grusby L, Beard C, Possemato R, et al. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet 2001;27:31–9.

    Article  PubMed  CAS  Google Scholar 

  63. Stancheva I, Hensey C, Meehan RR. Loss of the maintenance methyltransferase, xDnmt1, induces apoptosis in Xenopus embryos. EMBO J 2001;20:1963–73.

    Article  PubMed  CAS  Google Scholar 

  64. Jablonka E, Goitein R, Marcus M, Cedar H. DNA hypomethylation causes an increase in DNase-I sensitivity and an advance in the time of replication of the entire inactive X chromosome. Chromosoma 1985;93:152–6.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Spanish Ministry of Education and Science grant (BFU 2007–66610/BFI), University of the Basque Country Research Group grant (GIU08/04) to J.A. and Jesús de Gangoiti Barrera Foundation fellowship to N.A.

Author information

Authors and Affiliations

  1. Laboratory of Developmental Biology and Cancer, Department of Cell Biology and Histology, Faculty of Medicine and Odontology, University of the Basque Country, 48940, Leioa, Vizcaya, Spain

    Noelia Andollo, M. Dolores Boyano, M. del Mar Zalduendo & Juan Aréchaga

Authors
  1. Noelia Andollo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Dolores Boyano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. del Mar Zalduendo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan Aréchaga
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan Aréchaga .

Editor information

Editors and Affiliations

    Rights and permissions

    Reprints and permissions

    Copyright information

    © 2009 Humana Press, a part of Springer Science+Business Media, LLC

    About this chapter

    Cite this chapter

    Andollo, N., Boyano, M.D., del Mar Zalduendo, M., Aréchaga, J. (2009). Pluripotent Stem Cell Epigenetics During Development and Cancer. In: Baharvand, H. (eds) Trends in Stem Cell Biology and Technology. Humana Press. https://doi.org/10.1007/978-1-60327-905-5_6

    Download citation

    Publish with us

    Policies and ethics

    Search

    Navigation