Planarian MBD2/3 is required for adult stem cell pluripotency independently of DNA methylation

Developmental Biology

Volumn 384, Issue 1, 2013, Pages 141-153

  Jaber Hijazi, Farah ^a   Lo, Priscilla J K P ^b   Mihaylova, Yuliana ^a   Foster, Jeremy M ^c   Benner, Jack S ^c   Tejada Romero, Belen ^a   Chen, Chen ^b   Malla, Sunir ^b   Solana, Jordi ^b   Ruzov, Alexey ^b   Aziz Aboobaker, A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c NEW ENGLAND BIOLABS   (United States)

Author keywords

Differentiation; Methyl binding domain; Pluripotency; Regeneration

Indexed keywords

5 METHYLCYTOSINE; DNA METHYLTRANSFERASE; METHYL CPG BINDING DOMAIN 3; METHYL CPG BINDING PROTEIN; METHYL CPG BINDING PROTEIN 2; SMED PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BILATERIA; CELL DIFFERENTIATION; CELL PLURIPOTENCY; CELL PROLIFERATION; CELLULAR PARAMETERS; CONTROLLED STUDY; DNA METHYLATION; GENE FUNCTION; GENOME; MBD2 GENE; MBD3 GENE; METHYLATION; MITOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; TISSUE REGENERATION; TURBELLARIA;

ANIMALIA; BILATERIA; PLANARIA;

EID: 84886949339     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.09.020     Document Type: Article

References (65)

1. Aboobaker A.A. Planarian stem cells: a simple paradigm for regeneration. Trends in Cell Biology 2011, 21:304-311.
2. Aboobaker A.A., Kao D. A lack of commitment for over 500 million years: conserved animal stem cell pluripotency. EMBO Journal 2012, 31:2747-2749.
3. Aguilera C., Nakagawa K., Sancho R., Chakraborty A., Hendrich B., Behrens A. c-Jun N-terminal phosphorylation antagonises recruitment of the Mbd3/NuRD repressor complex. Nature 2011, 469:231-235.
4. Ahringer J. NuRD and SIN3 histone deacetylase complexes in development. Trends in Genetics 2000, 16:351-356.
5. Albalat R. Evolution of DNA-methylation machinery: DNA methyltransferases and methyl-DNA binding proteins in the amphioxus Branchiostoma floridae. Development Genes and Evolution 2008, 218:691-701.
6. Almeida R.D., Sottile V., Loose M., De Sousa P.A., Johnson A.D., Ruzov A. Semi-quantitative immunohistochemical detection of 5-hydroxymethyl-cytosine reveals conservation of its tissue distribution between amphibians and mammals. Epigenetics 2012, 7:137-140.
7. Blythe M.J., Kao D., Malla S., Rowsell J., Wilson R., Evans D., Jowett J., Hall A., Lemay V., Lam S., Aboobaker A.A. A dual platform approach to transcript discovery for the planarian Schmidtea mediterranea to establish RNAseq for stem cell and regeneration biology. PLoS One 2010, 5:e15617.
8. Bonuccelli L., Rossi L., Lena A., Scarcelli V., Rainaldi G., Evangelista M., Iacopetti P., Gremigni V., Salvetti A. An RbAp48-like gene regulates adult stem cells in planarians. Journal of Cell Science 2010, 123:690-698.
9. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., Guenther M.G., Kumar R.M., Murray H.L., Jenner R.G., Gifford D.K., Melton D.A., Jaenisch R., Young R.A. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956.
10. Cardona A., Fernandez J., Solana J., Romero R. An in situ hybridization protocol for planarian embryos: monitoring myosin heavy chain gene expression. Development Genes and Evolution 2005, 215:482-488.
11. Cebria F., Newmark P.A. Planarian homologs of netrin and netrin receptor are required for proper regeneration of the central nervous system and the maintenance of nervous system architecture. Development 2005, 132:3691-3703.
12. Cebria F., Newmark P.A. Morphogenesis defects are associated with abnormal nervous system regeneration following roboA RNAi in planarians. Development 2007, 134:833-837.
13. Denslow S.A., Wade P.A. The human Mi-2/NuRD complex and gene regulation. Oncogene 2007, 26:5433-5438.
14. Eisenhoffer G.T., Kang H., Sanchez Alvarado A. Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 2008, 3:327-339.
15. Feldman N., Gerson A., Fang J., Li E., Zhang Y., Shinkai Y., Cedar H., Bergman Y. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nature Cell Biology 2006, 8:188-194.
16. Felix D.A., Aboobaker A.A. The TALE class homeobox gene Smed-prep defines the anterior compartment for head regeneration. PLoS Genetics 2010, 6:e1000915.
17. Geyer K.K., Rodriguez Lopez C.M., Chalmers I.W., Munshi S.E., Truscott M., Heald J., Wilkinson M.J., Hoffmann K.F. Cytosine methylation regulates oviposition in the pathogenic blood fluke Schistosoma mansoni. Nature Communications 2011, 2:424.
18. Geyer K.K., Chalmers I.W., Mackintosh N., Hirst J.E., Geoghegan R., Badets M., Brophy P.M., Brehm K., Hoffmann K.F. Cytosine methylation is a conserved epigenetic feature found throughout the phylum Platyhelminthes. BMC Genomics 2013, 14:462. 10.1186/1471-2164-14-462.
19. Gonzalez-Estevez C., Arseni V., Thambyrajah R.S., Felix D.A., Aboobaker A.A. Diverse miRNA spatial expression patterns suggest important roles in homeostasis and regeneration in planarians. International Journal of Developmental Biology 2009, 53:493-505.
20. Guo T., Peters A.H., Newmark P.A. A Bruno-like gene is required for stem cell maintenance in planarians. Developmental Cell 2006, 11:159-169.
21. Gurley K.A., Rink J.C., Sanchez Alvarado A. Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 2008, 319:323-327.
22. Gutierrez A., Sommer R.J. Evolution of dnmt-2 and mbd-2-like genes in the free-living nematodes Pristionchus pacificus, Caenorhabditis elegans and Caenorhabditis briggsae. Nucleic Acids Research 2004, 32:6388-6396.
23. Gutierrez A., Sommer R.J. Functional diversification of the nematode mbd2/3 gene between Pristionchus pacificus and Caenorhabditis elegans. BMC Genetics 2007, 8:57.
24. Hendrich B., Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Molecular and Cellular Biology 1998, 18:6538-6547.
25. Hubert A., Henderson J.M., Ross K.G., Cowles M.W., Torres J., Zayas R.M. Epigenetic regulation of planarian stem cells by the SET1/MLL family of histone methyltransferases. Epigenetics 2013, 8:79-91.
26. Iglesias M., Gomez-Skarmeta J.L., Salo E., Adell T. Silencing of Smed-betacatenin1 generates radial-like hypercephalized planarians. Development 2008, 135:1215-1221.
27. Inoue T., Kumamoto H., Okamoto K., Umesono Y., Sakai M., Sanchez Alvarado A., Agata K. Morphological and functional recovery of the planarian photosensing system during head regeneration. Zoological Science 2004, 21:275-283.
28. Inoue T., Kumamoto H., Okamoto K., Umesono Y., Sakai M., Sanchez Alvarado A., Agata K. Morphological and functional recovery of the planarian photosensing system during head regeneration. Zoological Science 2004, 21:275-283.
29. Iwano H., Nakamura M., Tajima S. Xenopus MBD3 plays a crucial role in an early stage of development. Developmental Biology 2004, 268:416-428.
30. Jaenisch R., Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics 2003, 33(Suppl):245-254.
31. Kaji K., Caballero I.M., MacLeod R., Nichols J., Wilson V.A., Hendrich B. The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nature Cell Biology 2006, 8:285-292.
32. Kaji K., Nichols J., Hendrich B. Mbd3, a component of the NuRD co-repressor complex, is required for development of pluripotent cells. Development 2007, 134:1123-1132.
33. Kehle J., Beuchle D., Treuheit S., Christen B., Kennison J.A., Bienz M., Muller J. dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 1998, 282:1897-1900.
34. Kunert N., Wagner E., Murawska M., Klinker H., Kremmer E., Brehm A. dMec: a novel Mi-2 chromatin remodelling complex involved in transcriptional repression. EMBO Journal 2009, 28:533-544.
35. Labbe R.M., Irimia M., Currie K.W., Lin A., Zhu S.J., Brown D.D., Ross E.J., Voisin V., Bader G.D., Blencowe B.J., Pearson B.J. A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells 2012, 30:1734-1745.
36. Lindsay S., Bird A.P. Use of restriction enzymes to detect potential gene sequences in mammalian DNA. Nature 1987, 327:336-338.
37. Marhold J., Brehm A., Kramer K. The Drosophila methyl-DNA binding protein MBD2/3 interacts with the NuRD complex via p55 and MI-2. BMC Molecular Biology 2004, 5:20.
38. Marhold J., Kramer K., Kremmer E., Lyko F. The Drosophila MBD2/3 protein mediates interactions between the MI-2 chromatin complex and CpT/A-methylated DNA. Development 2004, 131:6033-6039.
39. Matsumoto M., Toraya T. cDNA cloning, expression, and characterization of methyl-CpG-binding domain type 2/3 proteins from starfish and sea urchin. Gene 2008, 420:125-134.
40. McClelland M., Nelson M., Raschke E. Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nucleic Acids Research 1994, 22:3640-3659.
41. McDonel P., Costello I., Hendrich B. Keeping things quiet: roles of NuRD and Sin3 co-repressor complexes during mammalian development. International Journal of Biochemistry and Cell Biology 2009, 41:108-116.
42. Meissner A., Mikkelsen T.S., Gu H., Wernig M., Hanna J., Sivachenko A., Zhang X., Bernstein B.E., Nusbaum C., Jaffe D.B., Gnirke A., Jaenisch R., Lander E.S. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008, 454:766-770.
43. Mohn F., Weber M., Rebhan M., Roloff T.C., Richter J., Stadler M.B., Bibel M., Schubeler D. Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Molecular Cells 2008, 30:755-766.
44. Ogas J., Kaufmann S., Henderson J., Somerville C. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:13839-13844.
45. Ohki I., Shimotake N., Fujita N., Jee J., Ikegami T., Nakao M., Shirakawa M. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 2001, 105:487-497.
46. Önal P., Grun D., Adamidi C., Rybak A., Solana J., Mastrobuoni G., Wang Y., Rahn H.P., Chen W., Kempa S., Ziebold U., Rajewsky N. Gene expression of pluripotency determinants is conserved between mammalian and planarian stem cells. EMBO Journal 2012, 31:2755-2769.
47. Panne D., Raleigh E.A., Bickle T.A. The McrBC endonuclease translocates DNA in a reaction dependent on GTP hydrolysis. Journal of Molecular Biology 1999, 290:49-60.
48. Raddatz G., Guzzardo P.M., Olova N., Fantappie M.R., Rampp M., Schaefer M., Reik W., Hannon G.J., Lyko F. Dnmt2-dependent methylomes lack defined DNA methylation patterns. Proceedings of the National Academy of Sciences of the United States of America 2013, 110:8627-8631.
49. Reddien P.W., Oviedo N.J., Jennings J.R., Jenkin J.C., Sanchez Alvarado A. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 2005, 310:1327-1330.
50. Reynolds N., Salmon-Divon M., Dvinge H., Hynes-Allen A., Balasooriya G., Leaford D., Behrens A., Bertone P., Hendrich B. NuRD-mediated deacetylation of H3K27 facilitates recruitment of polycomb repressive complex 2 to direct gene repression. EMBO Journal 2012, 31:593-605.
51. Rink J.C., Vu H.T., Sanchez Alvarado A. The maintenance and regeneration of the planarian excretory system are regulated by EGFR signaling. Development 2011, 138:3769-3780.
52. Robb S.M., Ross E., Sanchez Alvarado A. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Research 2008, 36:D599-606.
53. Ruzov A., Tsenkina Y., Serio A., Dudnakova T., Fletcher J., Bai Y., Chebotareva T., Pells S., Hannoun Z., Sullivan G., Chandran S., Hay D.C., Bradley M., Wilmut I., De Sousa P. Lineage-specific distribution of high levels of genomic 5-hydroxymethylcytosine in mammalian development. Cell Research 2011, 21:1332-1342.
54. Scimone M.L., Meisel J., Reddien P.W. The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development 2010, 137:1231-1241.
55. Solana J. Closing the circle of germline and stem cells: the primordial stem cell hypothesis. EvoDevo 2013, 4:2.
56. Solana J., Kao D., Mihaylova Y., Jaber-Hijazi F., Malla S., Wilson R., Aboobaker A. Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNAseq, RNA interference and irradiation approach. Genome Biology 2012, 13:R19.
57. Tweedie S., Ng H.H., Barlow A.L., Turner B.M., Hendrich B., Bird A. Vestiges of a DNA methylation system in Drosophila melanogaster?. Nature Genetics 1999, 23:389-390.
58. Verreault A., Kaufman P.D., Kobayashi R., Stillman B. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 1996, 87:95-104.
59. von Zelewsky T., Palladino F., Brunschwig K., Tobler H., Hajnal A., Muller F. The C. elegans Mi-2 chromatin-remodelling proteins function in vulval cell fate determination. Development 2000, 127:5277-5284.
60. Wagner D.E., Ho J.J., Reddien P.W. Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell 2012, 10:299-311.
61. Wagner D.E., Wang I.E., Reddien P.W. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 2011, 332:811-816.
62. Wang Y., Zayas R.M., Guo T., Newmark P.A. nanos function is essential for development and regeneration of planarian germ cells. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:5901-5906.
63. Xue Y., Wong J., Moreno G.T., Young M.K., Cote J., Wang W. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Molecular Cells 1998, 2:851-861.
64. Zeng A., Li Y.Q., Wang C., Han X.S., Li G., Wang J.Y., Li D.S., Qin Y.W., Shi Y., Brewer G., Jing Q. Heterochromatin protein 1 promotes self-renewal and triggers regenerative proliferation in adult stem cells. Journal of Cell Biology 2013, 201:409-425.
65. Zhang Y., Ng H.H., Erdjument-Bromage H., Tempst P., Bird A., Reinberg D. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Development 1999, 13:1924-1935.