Skip to main content

Epigenetics and Regeneration

  • Chapter
  • First Online:
New Perspectives in Regeneration

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 367))

Abstract

During newt lens regeneration a unique transdifferentiation event occurs. In this process, dorsal iris pigmented epithelial cells transdifferentiate into lens cells. This system should provide a new insight into cellular plasticity in basic and applied research. Recently, a series of approaches to study epigenetic reprogramming during transdifferentiation have been performed. In this review, we introduce the regulation of dynamic regulation of core-histone modifications and the emergence of an oocyte-type linker histone during transdifferentiation. Finally, we show supporting evidence that there are common strategies of reprogramming between newt somatic cell in transdifferentiation and oocytes after somatic cell nuclear transfer.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
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

Institutional subscriptions

References

  • Abe S, Eguchi G (1977) An analysis of differentiative capacity of pigmented epithelial cells of adult newt iris in clonal cell culture. Dev Growth Differ 19:309–317

    Article  Google Scholar 

  • Agata K, Kobayashi H, Itoh Y, Mochii M, Sawada K, Eguchi G (1993) Genetic characterization of the multipotent dedifferentiated state of pigmented epithelial cells in vitro. Development 118:1025–1030

    CAS  PubMed  Google Scholar 

  • Anderson RM, Bosch JA, Goll MG, Hesselson D, Dong PD, Shin D, Chi NC, Shin CH, Schlegel A, Halpern M, Stainier DY (2009) Loss of Dnmt1 catalytic activity reveals multiple roles for DNA methylation during pancreas development and regeneration. Dev Biol 334:213–223

    Article  CAS  PubMed  Google Scholar 

  • Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8:532–538

    Article  CAS  PubMed  Google Scholar 

  • Baddoo M, Hill K, Wilkinson R, Gaupp D, Hughes C, Kopen GC, Phinney DG (2003) Characterization of mesenchymal stem cells isolated from murine bone marrow by negative selection. J Cell Biochem 89:1235–1249

    Article  CAS  PubMed  Google Scholar 

  • Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837

    Article  CAS  PubMed  Google Scholar 

  • Becker M, Becker A, Miyara F, Han Z, Kihara M, Brown DT, Hager GL, Latham K, Adashi EY, Misteli T (2005) Differential in vivo binding dynamics of somatic and oocyte-specific linker histones in oocytes and during ES cell nuclear transfer. Mol Biol Cell 16:3887–3895

    Article  CAS  PubMed  Google Scholar 

  • Beekman C, Nichane M, De Clercq S, Maetens M, Floss T, Wurst W, Bellefroid E, Marine JC (2006) Evolutionarily conserved role of nucleostemin: controlling proliferation of stem/progenitor cells during early vertebrate development. Mol Cell Biol 26:9291–9301

    Article  CAS  PubMed  Google Scholar 

  • Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326

    Article  CAS  PubMed  Google Scholar 

  • Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20:1123–1136

    Article  CAS  PubMed  Google Scholar 

  • Cho H, Wolffe AP (1994) Xenopus laevis B4, an intron-containing oocyte-specific linker histone-encoding gene. Gene 143:233–238

    Article  CAS  PubMed  Google Scholar 

  • Coulombre AJ (1965) The eye. In: DeHaan RL, Ursprung H (ed) Organogenesis. New Yolk: Holt, Rinehart and Winston, pp 219–251

    Google Scholar 

  • Cowan CA, Atienza J, Melton DA, Eggan K (2005) Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 309:1369–1373

    Article  CAS  PubMed  Google Scholar 

  • Dai MS, Sun XX, Lu H (2008) Aberrant expression of nucleostemin activates p53 and induces cell cycle arrest via inhibition of MDM2. Mol Cell Biol 28:4365–4376

    Article  CAS  PubMed  Google Scholar 

  • Eguchi G (1980) Lens regeneration: transdifferentiation of tissue cells. Iwanami shoten, Tokyo

    Google Scholar 

  • Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156

    Article  CAS  PubMed  Google Scholar 

  • Fischle W, Wang Y, Allis CD (2003) Histone and chromatin cross-talk. Curr Opin Cell Biol 15:172–183

    Article  CAS  PubMed  Google Scholar 

  • Gao S, Chung YG, Parseghian MH, King GJ, Adashi EY, Latham KE (2004) Rapid H1 linker histone transitions following fertilization or somatic cell nuclear transfer: evidence for a uniform developmental program in mice. Dev Biol 266:62–75

    Article  CAS  PubMed  Google Scholar 

  • Grant PA, Eberharter A, John S, Cook RG, Turner BM, Workman JL (1999) Expanded lysine acetylation specificity of Gcn5 in native complexes. J Biol Chem 274:5895–5900

    Article  CAS  PubMed  Google Scholar 

  • Grogg MW, Call MK, Okamoto M, Vergara MN, Del Rio-Tsonis K, Tsonis PA (2005) BMP inhibition-driven regulation of six-3 underlies induction of newt lens regeneration. Nature 438:858–862

    Article  CAS  PubMed  Google Scholar 

  • Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77–88

    Article  CAS  PubMed  Google Scholar 

  • Gurdon JB, Elsdale TR, Fischberg M (1958) Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182:64–65

    Article  CAS  PubMed  Google Scholar 

  • Hayashi T, Mizuno N, Takada R, Takada S, Kondoh H (2006) Determinative role of Wnt signals in dorsal iris-derived lens regeneration in newt eye. Mech Dev 123:793–800

    Article  CAS  PubMed  Google Scholar 

  • Hayashi T, Mizuno N, Ueda Y, Okamoto M, Kondoh H (2004) FGF2 triggers iris-derived lens regeneration in newt eye. Mech Dev 121:519–526

    Article  CAS  PubMed  Google Scholar 

  • Jopling C, Sleep E, Raya M, Marti M, Raya A, Izpisua Belmonte JC (2010) Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464:606–609

    Article  CAS  PubMed  Google Scholar 

  • Jullien J, Astrand C, Halley-Stott RP, Garrett N, Gurdon JB (2010) Characterization of somatic cell nuclear reprogramming by oocytes in which a linker histone is required for pluripotency gene reactivation. Proc Natl Acad Sci U S A 107:5483–5488

    Article  CAS  PubMed  Google Scholar 

  • Kornberg RD (1974) Chromatin structure: a repeating unit of histones and DNA. Science 184:868–871

    Article  CAS  PubMed  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705

    Article  CAS  PubMed  Google Scholar 

  • Krogan NJ, Kim M, Tong A, Golshani A, Cagney G, Canadien V, Richards DP, Beattie BK, Emili A, Boone C, Shilatifard A, Buratowski S, Greenblatt J (2003) Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol Cell Biol 23:4207–4218

    Article  CAS  PubMed  Google Scholar 

  • Kuo MH, Brownell JE, Sobel RE, Ranalli TA, Cook RG, Edmondson DG, Roth SY, Allis CD (1996) Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature 383:269–272

    Article  CAS  PubMed  Google Scholar 

  • Lachner M, O’Sullivan RJ, Jenuwein T (2003) An epigenetic road map for histone lysine methylation. J Cell Sci 116:2117–2124

    Article  CAS  PubMed  Google Scholar 

  • Li J, Moazed D, Gygi SP (2002) Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J Biol Chem 277:49383–49388

    Article  CAS  PubMed  Google Scholar 

  • Maki N, Suetsugu-Maki R, Sano S, Nakamura K, Nishimura O, Tarui H, Del Rio-Tsonis K, Ohsumi K, Agata K, Tsonis PA (2010a) Oocyte-type linker histone B4 is required for transdifferentiation of somatic cells in vivo. FASEB J 24:3462–3467

    Article  CAS  PubMed  Google Scholar 

  • Maki N, Suetsugu-Maki R, Tarui H, Agata K, Del Rio-Tsonis K, Tsonis PA (2009) Expression of stem cell pluripotency factors during regeneration in newts. Dev Dyn 238:1613–1616

    Article  CAS  PubMed  Google Scholar 

  • Maki N, Takechi K, Sano S, Tarui H, Sasai Y, Agata K (2007) Rapid accumulation of nucleostemin in nucleolus during newt regeneration. Dev Dyn 236:941–950

    Article  CAS  PubMed  Google Scholar 

  • Maki N, Tsonis PA, Agata K (2010b) Changes in global histone modifications during dedifferentiation in newt lens regeneration. Mol Vis 16:1893–1897

    CAS  PubMed  Google Scholar 

  • Mandl B, Brandt WF, Superti-Furga G, Graninger PG, Birnstiel ML, Busslinger M (1997) The five cleavage-stage (CS) histones of the sea urchin are encoded by a maternally expressed family of replacement histone genes: functional equivalence of the CS H1 and frog H1 M (B4) proteins. Mol Cell Biol 17:1189–1200

    CAS  PubMed  Google Scholar 

  • Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. In: Proceedings of the national academy of sciences of the United States of America, vol 78. pp 7634–7638

    Google Scholar 

  • McGraw S, Vigneault C, Tremblay K, Sirard MA (2006) Characterization of linker histone H1FOO during bovine in vitro embryo development. Mol Reprod Dev 73:692–699

    Article  CAS  PubMed  Google Scholar 

  • Mendenhall EM, Bernstein BE (2008) Chromatin state maps: new technologies, new insights. Curr Opin Genet Dev 18:109–115

    Article  CAS  PubMed  Google Scholar 

  • Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O’Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560

    Article  CAS  PubMed  Google Scholar 

  • Nikpour P, Mowla SJ, Jafarnejad SM, Fischer U, Schulz WA (2009) Differential effects of Nucleostemin suppression on cell cycle arrest and apoptosis in the bladder cancer cell lines 5637 and SW1710. Cell Prolif 42:762–769

    Article  CAS  PubMed  Google Scholar 

  • Nishioka K, Chuikov S, Sarma K, Erdjument-Bromage H, Allis CD, Tempst P, Reinberg D (2002) Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes Dev 16:479–489

    Article  CAS  PubMed  Google Scholar 

  • Ohmura M, Naka K, Hoshii T, Muraguchi T, Shugo H, Tamase A, Uema N, Ooshio T, Arai F, Takubo K, Nagamatsu G, Hamaguchi I, Takagi M, Ishihara M, Sakurada K, Miyaji H, Suda T, Hirao A (2008) Identification of stem cells during prepubertal spermatogenesis via monitoring of nucleostemin promoter activity. Stem cells 26:3237–3246

    Article  CAS  PubMed  Google Scholar 

  • Ohsumi K, Katagiri C (1991) Occurrence of H1 subtypes specific to pronuclei and cleavage-stage cell nuclei of anuran amphibians. Dev Biol 147:110–120

    Article  CAS  PubMed  Google Scholar 

  • Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448:313–317

    Article  CAS  PubMed  Google Scholar 

  • Pan G, Tian S, Nie J, Yang C, Ruotti V, Wei H, Jonsdottir GA, Stewart R, Thomson JA (2007) Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1:299–312

    Article  CAS  PubMed  Google Scholar 

  • Peters AH, Kubicek S, Mechtler K, O’Sullivan RJ, Derijck AA, Perez-Burgos L, Kohlmaier A, Opravil S, Tachibana M, Shinkai Y, Martens JH, Jenuwein T (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12:1577–1589

    Article  CAS  PubMed  Google Scholar 

  • Rice JC, Briggs SD, Ueberheide B, Barber CM, Shabanowitz J, Hunt DF, Shinkai Y, Allis CD (2003) Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 12:1591–1598

    Article  CAS  PubMed  Google Scholar 

  • Romanova L, Grand A, Zhang L, Rayner S, Katoku-Kikyo N, Kellner S, Kikyo N (2009) Critical role of nucleostemin in pre-rRNA processing. J Biol Chem 284:4968–4977

    Article  CAS  PubMed  Google Scholar 

  • Rundlett SE, Carmen AA, Kobayashi R, Bavykin S, Turner BM, Grunstein M (1996) HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc Natl Acad Sci USA 93:14503–14508

    Article  CAS  PubMed  Google Scholar 

  • Ruthenburg AJ, Li H, Patel DJ, Allis CD (2007) Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8:983–994

    Article  CAS  PubMed  Google Scholar 

  • Sadler KC, Krahn KN, Gaur NA, Ukomadu C (2007) Liver growth in the embryo and during liver regeneration in zebrafish requires the cell cycle regulator, uhrf1. In: Proceedings of the national academy of sciences of the United States of America, vol 104. pp 1570–1575

    Google Scholar 

  • Saeki H, Ohsumi K, Aihara H, Ito T, Hirose S, Ura K, Kaneda Y (2005) Linker histone variants control chromatin dynamics during early embryogenesis. Proc Natl Acad Sci USA 102:5697–5702

    Article  CAS  PubMed  Google Scholar 

  • Schaft D, Roguev A, Kotovic KM, Shevchenko A, Sarov M, Neugebauer KM, Stewart AF (2003) The histone 3 lysine 36 methyltransferase, SET2, is involved in transcriptional elongation. Nucleic Acids Res 31:2475–2482

    Article  CAS  PubMed  Google Scholar 

  • Schiltz RL, Mizzen CA, Vassilev A, Cook RG, Allis CD, Nakatani Y (1999) Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J Biol Chem 274:1189–1192

    Article  CAS  PubMed  Google Scholar 

  • Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T (2004) A silencing pathway to induce H3–K9 and H4–K20 trimethylation at constitutive heterochromatin. Genes Dev 18:1251–1262

    Article  CAS  PubMed  Google Scholar 

  • Shahbazian MD, Grunstein M (2007) Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76:75–100

    Article  CAS  PubMed  Google Scholar 

  • Spencer TE, Jenster G, Burcin MM, Allis CD, Zhou J, Mizzen CA, McKenna NJ, Onate SA, Tsai SY, Tsai MJ, O’Malley BW (1997) Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 389:194–198

    Article  CAS  PubMed  Google Scholar 

  • Stewart S, Tsun ZY, Belmote JC (2009) A histone demethylase is necessary for regeneration in zebrafish. Proc Natl Acad Sci U S A 106:19889–19894

    Google Scholar 

  • Tada M, Takahama Y, Abe K, Nakatsuji N, Tada T (2001) Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Curr Biol: CB 11:1553–1558

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    Article  CAS  PubMed  Google Scholar 

  • Tanaka M, Hennebold JD, Macfarlane J, Adashi EY (2001) A mammalian oocyte-specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1 M histone of the frog. Development 128:655–664

    CAS  PubMed  Google Scholar 

  • Tanaka Y, Kato S, Tanaka M, Kuji N, Yoshimura Y (2003) Structure and expression of the human oocyte-specific histone H1 gene elucidated by direct RT-nested PCR of a single oocyte. Biochem Biophys Res Commun 304:351–357

    Article  CAS  PubMed  Google Scholar 

  • Teranishi T, Tanaka M, Kimoto S, Ono Y, Miyakoshi K, Kono T, Yoshimura Y (2004) Rapid replacement of somatic linker histones with the oocyte-specific linker histone H1foo in nuclear transfer. Dev Biol 266:76–86

    Article  CAS  PubMed  Google Scholar 

  • Tsai RY, McKay RD (2002) A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes Dev 16:2991–3003

    Article  CAS  PubMed  Google Scholar 

  • Wakayama T, Perry AC, Zuccotti M, Johnson KR, Yanagimachi R (1998) Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394:369–374

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Cao R, Xia L, Erdjument-Bromage H, Borchers C, Tempst P, Zhang Y (2001) Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol Cell 8:1207–1217

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40:897–903

    Article  CAS  PubMed  Google Scholar 

  • Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448:318–324

    Article  CAS  PubMed  Google Scholar 

  • Wibrand K, Olsen LC (2002) Linker histone H1 M transcripts mark the developing germ line in zebrafish. Mech Dev 117:249–252

    Article  CAS  PubMed  Google Scholar 

  • Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385:810–813

    Article  CAS  PubMed  Google Scholar 

  • Yakushiji N, Suzuki M, Satoh A, Sagai T, Shiroishi T, Kobayashi H, Sasaki H, Ide H, Tamura K (2007) Correlation between Shh expression and DNA methylation status of the limb-specific Shh enhancer region during limb regeneration in amphibians. Dev Biol 312:171–182

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920

    Article  CAS  PubMed  Google Scholar 

  • Zhao XD, Han X, Chew JL, Liu J, Chiu KP, Choo A, Orlov YL, Sung WK, Shahab A, Kuznetsov VA, Bourque G, Oh S, Ruan Y, Ng HH, Wei CL (2007) Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1:286–298

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Kiyoe Ura for critical reading and suggestions, and Rinako Maki for making illustrations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nobuyasu Maki .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Maki, N., Kimura, H. (2012). Epigenetics and Regeneration. In: Heber-Katz, E., Stocum, D. (eds) New Perspectives in Regeneration. Current Topics in Microbiology and Immunology, vol 367. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2012_293

Download citation

Publish with us

Policies and ethics