The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea

M. Lucila Scimone; Joshua Meisel; Peter W. Reddien

doi:10.1242/dev.042051

journal article Apr 15, 2010

The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea

M. Lucila Scimone Joshua Meisel Peter W. Reddien

Development Vol. 137 No. 8 pp. 1231-1241 · The Company of Biologists

View at Publisher Save 10.1242/dev.042051

Abstract

Freshwater planarians are able to regenerate any missing part of their body and have extensive tissue turnover because of the action of dividing cells called neoblasts. Neoblasts provide an excellent system for in vivo study of adult stem cell biology. We identified the Smed-CHD4 gene, which is predicted to encode a chromatin-remodeling protein similar to CHD4/Mi-2 proteins, as required for planarian regeneration and tissue homeostasis. Following inhibition of Smed-CHD4 with RNA interference (RNAi), neoblast numbers were initially normal, despite an inability of the animals to regenerate. However, the proliferative response of neoblasts to amputation or growth stimulation in Smed-CHD4(RNAi) animals was diminished. Smed-CHD4(RNAi) animals displayed a dramatic reduction in the numbers of certain neoblast progeny cells. Smed-CHD4 was required for the formation of these neoblast progeny cells. Together, these results indicate that Smed-CHD4 is required for neoblasts to produce progeny cells committed to differentiation in order to control tissue turnover and regeneration and suggest a crucial role for CHD4 proteins in stem cell differentiation.

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References

50

[1]

NuRD and SIN3

Julie Ahringer

Trends in Genetics 2000 10.1016/s0168-9525(00)02066-7

[2]

Baguñà "Mitosis in the intact and regenerating planarian Dugesia mediterranea n.sp. I. Mitotic studies during growth, feeding and starvation" J. Exp. Zool. (1976) 10.1002/jez.1401950106

[3]

Bardeen "The inhibitive action of the Roentgen rays on regeneration in planarians" J. Exp. Zool. (1904) 10.1002/jez.1400010107

[4]

Becker "ATP-dependent nucleosome remodeling" Annu. Rev. Biochem. (2002) 10.1146/annurev.biochem.71.110601.135400

[5]

Bibikova "Unraveling epigenetic regulation in embryonic stem cells" Cell Stem Cell (2008) 10.1016/j.stem.2008.01.005

[6]

Bonifer "How transcription factors program chromatin-lessons from studies of the regulation of myeloid-specific genes" Semin. Immunol. (2008) 10.1016/j.smim.2008.05.001

[7]

Boyer "Polycomb complexes repress developmental regulators in murine embryonic stem cells" Nature (2006) 10.1038/nature04733

[8]

Denslow "The human Mi-2/NuRD complex and gene regulation" Oncogene (2007) 10.1038/sj.onc.1210611

[9]

Dubois "Contribution á l ’ètude de la migration des cellules de règènèration chez les Planaires dulcicoles" Bull. Biol. Fr. Belg. (1949)

[10]

Eisenhoffer "Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea" Cell Stem Cell (2008) 10.1016/j.stem.2008.07.002

[11]

Ezhkova "Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells" Cell (2009) 10.1016/j.cell.2008.12.043

[12]

Fuchs "More than one way to skin" Genes Dev. (2008) 10.1101/gad.1645908

[13]

Georgopoulos "Haematopoietic cell-fate decisions, chromatin regulation and ikaros" Nat. Rev. Immunol. (2002) 10.1038/nri747

[14]

Guo "A Bruno-like gene is required for stem cell maintenance in planarians" Dev. Cell (2006) 10.1016/j.devcel.2006.06.004

[15]

Isolation of planarian X‐ray‐sensitive stem cells by fluorescence‐activated cell sorting

Tetsutaro Hayashi, Maki Asami, Sayaka Higuchi et al.

Development, Growth & Differentiation 2006 10.1111/j.1440-169x.2006.00876.x

[16]

Kaji "The NuRD component Mbd3 is required for pluripotency of embryonic stem cells" Nat. Cell Biol. (2006) 10.1038/ncb1372

[17]

Kaji "Mbd3, a component of the NuRD co-repressor complex, is required for development of pluripotent cells" Development (2007) 10.1242/dev.02802

[18]

Kehle "dMi-2, a hunchback-interacting protein that functions in polycomb repression" Science (1998) 10.1126/science.282.5395.1897

[19]

Kim "Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes" Immunity (1999) 10.1016/s1074-7613(00)80034-5

[20]

Kingston "ATP-dependent remodeling and acetylation as regulators of chromatin fluidity" Genes Dev. (1999) 10.1101/gad.13.18.2339

[21]

Chromatin Modifications and Their Function

Tony Kouzarides

Cell 2007 10.1016/j.cell.2007.02.005

[22]

Lee "Control of developmental regulators by Polycomb in human embryonic stem cells" Cell (2006) 10.1016/j.cell.2006.02.043

[23]

Le Grand "Skeletal muscle satellite cells and adult myogenesis" Curr. Opin. Cell Biol. (2007) 10.1016/j.ceb.2007.09.012

[24]

The Role of Chromatin during Transcription

Bing Li, Michael Carey, Jerry L. Workman

Cell 2007 10.1016/j.cell.2007.01.015

[25]

Lunyak "Epigenetic regulation of stem cell fate" Hum. Mol. Genet. (2008) 10.1093/hmg/ddn149

[26]

Narlikar "Cooperation between complexes that regulate chromatin structure and transcription" Cell (2002) 10.1016/s0092-8674(02)00654-2

[27]

Newmark "Bromodeoxyuridine specifically labels the regenerative stem cells of planarians" Dev. Biol. (2000) 10.1006/dbio.2000.9645

[28]

Newmark "Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians" Proc. Natl. Acad. Sci. USA (2003) 10.1073/pnas.1834205100

[29]

Ng "Histone deacetylases: silencers for hire" Trends Biochem. Sci. (2000) 10.1016/s0968-0004(00)01551-6

[30]

Ogas "Cellular differentiation regulated by Gibberellin in the Arabidopsis thaliana pickle mutant" Science (1997) 10.1126/science.277.5322.91

[31]

Ogas "PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis" Proc. Natl. Acad. Sci. USA (1999) 10.1073/pnas.96.24.13839

[32]

Hematopoiesis: An Evolving Paradigm for Stem Cell Biology

Stuart H. Orkin, Leonard I. Zon

Cell 2008 10.1016/j.cell.2008.01.025

[33]

Pearson "A planarian p53 homolog regulates proliferation and self-renewal in adult stem cell lineages" Development (2010) 10.1242/dev.044297

[34]

Formaldehyde‐based whole‐mount in situ hybridization method for planarians

Bret J. Pearson, George T. Eisenhoffer, Kyle A. Gurley et al.

Developmental Dynamics 2009 10.1002/dvdy.21849

[35]

Reddien "Fundamentals of planarian regeneration" Annu. Rev. Cell Dev. Biol. (2004) 10.1146/annurev.cellbio.20.010403.095114

[36]

Reddien "Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria" Dev. Cell (2005) 10.1016/j.devcel.2005.02.014

[37]

Reddien "SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells for regeneration and homeostasis" Science (2005) 10.1126/science.1116110

[38]

Saló "Regeneration and pattern formation in planarians. I. The pattern of mitosis in anterior and posterior regeneration in Dugesia (G) tigrina, and a new proposal for blastema formation" J. Embryol. Exp. Morphol. (1984)

[39]

Sánchez Alvarado "The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration" Development (2002) 10.1242/dev.00167

[40]

Seelig "Two forms of the major antigenic protein of the dermatomyositis-specific Mi-2 autoantigen" Arthritis Rheum. (1996) 10.1002/art.1780391029

[41]

Shimono "Mi-2 beta associates with BRG1 and RET finger protein at the distinct regions with transcriptional activating and repressing abilities" J. Biol. Chem. (2003) 10.1074/jbc.m309198200

[42]

Tong "Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex" Nature (1998) 10.1038/27699

[43]

Unhavaithaya "MEP-1 and a homolog of the NURD complex component Mi-2 act together to maintain germline-soma distinctions in C. elegans" Cell (2002) 10.1016/s0092-8674(02)01202-3

[44]

von Zelewsky "The C. elegans Mi-2 chromatin-remodelling proteins function in vulval cell fate determination" Development (2000) 10.1242/dev.127.24.5277

[45]

Wade "A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase" Curr. Biol. (1998) 10.1016/s0960-9822(98)70328-8

[46]

Wagers "Plasticity of adult stem cells" Cell (2004) 10.1016/s0092-8674(04)00208-9

[47]

Weissman "Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations" Annu. Rev. Cell Dev. Biol. (2001) 10.1146/annurev.cellbio.17.1.387

[48]

Williams "The chromatin remodeler Mi-2beta is required for CD4 expression and T cell development" Immunity (2004) 10.1016/j.immuni.2004.05.005

[49]

Yoshida "The role of the chromatin remodeler Mi-2beta in hematopoietic stem cell self-renewal and multilineage differentiation" Genes Dev. (2008) 10.1101/gad.1642808

[50]

Zhang "The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities" Cell (1998) 10.1016/s0092-8674(00)81758-4

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Details

Published: Apr 15, 2010
Vol/Issue: 137(8)
Pages: 1231-1241

Authors

M

M. Lucila Scimone

Howard Hughes Medical Institute, Whitehead Institute, 9 Cambridge Center, Cambridge, MA 02142, USA.

J

Joshua Meisel

Howard Hughes Medical Institute, Whitehead Institute, 9 Cambridge Center, Cambridge, MA 02142, USA.

P

Peter W. Reddien

Howard Hughes Medical Institute, Whitehead Institute, 9 Cambridge Center, Cambridge, MA 02142, USA.; Department of Biology, Massachusetts Institute of Technology, 9 Cambridge Center, Cambridge, MA 02142, USA.

Cite This Article

M. Lucila Scimone, Joshua Meisel, Peter W. Reddien (2010). The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development, 137(8), 1231-1241. https://doi.org/10.1242/dev.042051

The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea

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