Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis

Cell Stem Cell

Volumn 10, Issue 3, 2012, Pages 299-311

  Wagner, Daniel E ^a   Ho, Jaclyn J ^a   Reddien, Peter W ^a  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIP29 PROTEIN; EED 1 PROTEIN; EZH PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR; KHD 1 PROTEIN; PROTEIN; PROTEIN C JUN; SOXP 1 PROTEIN; TRANSCRIPTION FACTOR SOX; UNCLASSIFIED DRUG; VASA 1 PROTEIN; ZFP 1 PROTEIN; ZINC FINGER PROTEIN; ZMYM 1 PROTEIN;

ADULT STEM CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TURBELLARIA;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CLONE CELLS; GENE EXPRESSION PROFILING; MICROARRAY ANALYSIS; PLANARIANS; PLURIPOTENT STEM CELLS; RNA INTERFERENCE;

ANIMALIA; PLANARIA; TURBELLARIA;

EID: 84857856280     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.01.016     Document Type: Article

References (62)

1. A.A. Avilion, S.K. Nicolis, L.H. Pevny, L. Perez, N. Vivian, and R. Lovell-Badge Multipotent cell lineages in early mouse development depend on SOX2 function Genes Dev. 17 2003 126 140 (Pubitemid 36062514)
2. C. Bardeen, and F. Baetjer The inhibitive action of the Roentgen rays on regeneration in planarians J. Exp. Zool. 1 1904 191 195
3. L.A. Boyer, T.I. Lee, M.F. Cole, S.E. Johnstone, S.S. Levine, J.P. Zucker, M.G. Guenther, R.M. Kumar, H.L. Murray, and R.G. Jenner Core transcriptional regulatory circuitry in human embryonic stem cells Cell 122 2005 947 956 (Pubitemid 41345211)
4. L.A. Boyer, K. Plath, J. Zeitlinger, T. Brambrink, L.A. Medeiros, T.I. Lee, S.S. Levine, M. Wernig, A. Tajonar, and M.K. Ray Polycomb complexes repress developmental regulators in murine embryonic stem cells Nature 441 2006 349 353 (Pubitemid 44050199)
5. S.J. Chamberlain, D. Yee, and T. Magnuson Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency Stem Cells 26 2008 1496 1505
6. R.E. Denell Homoeosis in Drosophila. II. A genetic analysis of polycomb Genetics 90 1978 277 289 (Pubitemid 9049482)
7. F. Dubois Contribution á l 'tude de la migration des cellules de rgnration chez les Planaires dulcicoles Bull. Biol. Fr. Belg. 83 1949 213 283
8. G.T. Eisenhoffer, H. Kang, and A. Sánchez Alvarado Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea Cell Stem Cell 3 2008 327 339
9. E. Ezhkova, W.-H. Lien, N. Stokes, H.A. Pasolli, J.M. Silva, and E. Fuchs EZH1 and EZH2 cogovern histone H3K27 trimethylation and are essential for hair follicle homeostasis and wound repair Genes Dev. 25 2011 485 498
10. Y. Fong, L. Bender, W. Wang, and S. Strome Regulation of the different chromatin states of autosomes and X chromosomes in the germ line of C. elegans Science 296 2002 2235 2238 (Pubitemid 34680311)
11. C. Garvin, R. Holdeman, and S. Strome The phenotype of mes-2, mes-3, mes-4 and mes-6, maternal-effect genes required for survival of the germline in Caenorhabditis elegans, is sensitive to chromosome dosage Genetics 148 1998 167 185 (Pubitemid 28063485)
12. T. Guo, A.H.F.M. Peters, and P.A. Newmark A Bruno-like gene is required for stem cell maintenance in planarians Dev. Cell 11 2006 159 169 (Pubitemid 44138497)
13. T. Hayashi, M. Asami, S. Higuchi, N. Shibata, and K. Agata Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting Dev. Growth Differ. 48 2006 371 380 (Pubitemid 44035795)
14. T. Hayashi, N. Shibata, R. Okumura, T. Kudome, O. Nishimura, H. Tarui, and K. Agata Single-cell gene profiling of planarian stem cells using fluorescent activated cell sorting and its "index sorting" function for stem cell research Dev. Growth Differ. 52 2010 131 144
15. S. Higuchi, T. Hayashi, I. Hori, N. Shibata, H. Sakamoto, and K. Agata Characterization and categorization of fluorescence activated cell sorted planarian stem cells by ultrastructural analysis Dev. Growth Differ. 49 2007 571 581 (Pubitemid 47283727)
16. A. Janic, L. Mendizabal, S. Llamazares, D. Rossell, and C. Gonzalez Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila Science 330 2010 1824 1827
17. A.H. Juan, A. Derfoul, X. Feng, J.G. Ryall, S. Dell'Orso, A. Pasut, H. Zare, J.M. Simone, M.A. Rudnicki, and V. Sartorelli Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells Genes Dev. 25 2011 789 794
18. C.E. Juliano, S.Z. Swartz, and G.M. Wessel A conserved germline multipotency program Development 137 2010 4113 4126
19. S.W. Lapan, and P.W. Reddien dlx and sp6-9 control optic cup regeneration in a prototypic eye PLoS Genet. 7 2011 e1002226
20. P.F. Lasko, and M. Ashburner The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A Nature 335 1988 611 617
21. T.I. Lee, R.G. Jenner, L.A. Boyer, M.G. Guenther, S.S. Levine, R.M. Kumar, B. Chevalier, S.E. Johnstone, M.F. Cole, and K.I. Isono Control of developmental regulators by Polycomb in human embryonic stem cells Cell 125 2006 301 313 (Pubitemid 44313811)
22. K. Mochizuki, C. Nishimiya-Fujisawa, and T. Fujisawa Universal occurrence of the vasa-related genes among metazoans and their germline expression in Hydra Dev. Genes Evol. 211 2001 299 308 (Pubitemid 32821516)
23. P.A. Newmark, and A. Sánchez Alvarado Bromodeoxyuridine specifically labels the regenerative stem cells of planarians Dev. Biol. 220 2000 142 153 (Pubitemid 30228143)
24. K. Nishioka, J.C. Rice, K. Sarma, H. Erdjument-Bromage, J. Werner, Y. Wang, S. Chuikov, P. Valenzuela, P. Tempst, and R. Steward PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin Mol. Cell 9 2002 1201 1213 (Pubitemid 34722300)
25. H. Oda, I. Okamoto, N. Murphy, J. Chu, S.M. Price, M.M. Shen, M.E. Torres-Padilla, E. Heard, and D. Reinberg Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development Mol. Cell. Biol. 29 2009 2278 2295
26. K. Ogawa, C. Kobayashi, T. Hayashi, H. Orii, K. Watanabe, and K. Agata Planarian fibroblast growth factor receptor homologs expressed in stem cells and cephalic ganglions Dev. Growth Differ. 44 2002 191 204 (Pubitemid 34639365)
27. M. Osawa, K.i. Hanada, H. Hamada, and H. Nakauchi Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell Science 273 1996 242 245 (Pubitemid 26285891)
28. D. Palakodeti, M. Smielewska, Y.-C. Lu, G.W. Yeo, and B.R. Graveley The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians RNA 14 2008 1174 1186 (Pubitemid 351717497)
29. B.J. Pearson, and A. Sánchez Alvarado A planarian p53 homolog regulates proliferation and self-renewal in adult stem cell lineages Development 137 2010 213 221
30. B.J. Pearson, G.T. Eisenhoffer, K.A. Gurley, J.C. Rink, D.E. Miller, and A. Sánchez Alvarado Formaldehyde-based whole-mount in situ hybridization method for planarians Dev. Dyn. 238 2009 443 450
31. P.W. Reddien, and A. Sánchez Alvarado Fundamentals of planarian regeneration Annu. Rev. Cell Dev. Biol. 20 2004 725 757 (Pubitemid 39488656)
32. P.W. Reddien, A.L. Bermange, K.J. Murfitt, J.R. Jennings, and A. Sánchez Alvarado Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria Dev. Cell 8 2005 635 649 (Pubitemid 40585288)
33. P.W. Reddien, N.J. Oviedo, J.R. Jennings, J.C. Jenkin, and A. Sánchez Alvarado SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells Science 310 2005 1327 1330 (Pubitemid 41698864)
34. L. Ringrose, and R. Paro Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins Annu. Rev. Genet. 38 2004 413 443 (Pubitemid 40013734)
35. S.M.C. Robb, E. Ross, and A. Sánchez Alvarado SmedGD: the Schmidtea mediterranea genome database Nucleic Acids Res. 36 Database issue 2008 D599 D606
36. C. Rongo, and R. Lehmann Regulated synthesis, transport and assembly of the Drosophila germ plasm Trends Genet. 12 1996 102 109 (Pubitemid 26094855)
37. L. Rossi, A. Salvetti, F.M. Marincola, A. Lena, P. Deri, L. Mannini, R. Batistoni, E. Wang, and V. Gremigni Deciphering the molecular machinery of stem cells: a look at the neoblast gene expression profile Genome Biol. 8 2007 R62
38. L. Rouhana, N. Shibata, O. Nishimura, and K. Agata Different requirements for conserved post-transcriptional regulators in planarian regeneration and stem cell maintenance Dev. Biol. 341 2010 429 443
39. A. Salvetti, L. Rossi, A. Lena, R. Batistoni, P. Deri, G. Rainaldi, M.T. Locci, M. Evangelista, and V. Gremigni DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance Development 132 2005 1863 1874 (Pubitemid 40691776)
40. A. Salvetti, L. Rossi, L. Bonuccelli, A. Lena, C. Pugliesi, G. Rainaldi, M. Evangelista, and V. Gremigni Adult stem cell plasticity: neoblast repopulation in non-lethally irradiated planarians Dev. Biol. 328 2009 305 314
41. A. Sánchez Alvarado, and P.A. Newmark Double-stranded RNA specifically disrupts gene expression during planarian regeneration Proc. Natl. Acad. Sci. USA 96 1999 5049 5054 (Pubitemid 29214533)
42. A. Sánchez Alvarado, P.A. Newmark, S.M. Robb, and R. Juste The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration Development 129 2002 5659 5665 (Pubitemid 36054610)
43. M.L. Scimone, J. Meisel, and P.W. Reddien The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea Development 137 2010 1231 1241
44. M.L. Scimone, M. Srivastava, G.W. Bell, and P.W. Reddien A regulatory program for excretory system regeneration in planarians Development 138 2011 4387 4398
45. G. Seydoux, and R.E. Braun Pathway to totipotency: lessons from germ cells Cell 127 2006 891 904 (Pubitemid 44792258)
46. N. Shibata, Y. Umesono, H. Orii, T. Sakurai, K. Watanabe, and K. Agata Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians Dev. Biol. 206 1999 73 87 (Pubitemid 29069875)
47. N. Shibata, L. Rouhana, and K. Agata Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians Dev. Growth Differ. 52 2010 27 41
48. A.J.G. Simpson, O.L. Caballero, A. Jungbluth, Y.-T. Chen, and L.J. Old Cancer/testis antigens, gametogenesis and cancer Nat. Rev. Cancer 5 2005 615 625 (Pubitemid 41081387)
49. A.H. Sinclair, P. Berta, M.S. Palmer, J.R. Hawkins, B.L. Griffiths, M.J. Smith, J.W. Foster, A.M. Frischauf, R. Lovell-Badge, and P.N. Goodfellow A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif Nature 346 1990 240 244
50. J. Solana, P. Lasko, and R. Romero Spoltud-1 is a chromatoid body component required for planarian long-term stem cell self-renewal Dev. Biol. 328 2009 410 421
51. G.J. Spangrude, S. Heimfeld, and I.L. Weissman Purification and characterization of mouse hematopoietic stem cells Science 241 1988 58 62
52. S. Styhler, A. Nakamura, A. Swan, B. Suter, and P. Lasko vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development Development 125 1998 1569 1578 (Pubitemid 28256725)
53. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. USA 102 2005 15545 15550 (Pubitemid 41528093)
54. T. Sugiura, K. Sakurai, and Y. Nagano Intracellular characterization of DDX39, a novel growth-associated RNA helicase Exp. Cell Res. 313 2007 782 790 (Pubitemid 46198822)
55. J.E. Till, and E.A. McCulloch A direct measurement of the radiation sensitivity of normal mouse bone marrow cells Radiat. Res. 14 1961 213 222
56. P. Tomancak, A. Guichet, P. Zavorszky, and A. Ephrussi Oocyte polarity depends on regulation of gurken by Vasa Development 125 1998 1723 1732 (Pubitemid 28256740)
57. R. Valverde, L. Edwards, and L. Regan Structure and function of KH domains FEBS J. 275 2008 2712 2726 (Pubitemid 351678660)
58. D.E. Wagner, I.E. Wang, and P.W. Reddien Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration Science 332 2011 811 816
59. L. Wang, J. Xu, L. Zeng, X. Ye, Q. Wu, J. Dai, C. Ji, S. Gu, C. Zhao, Y. Xie, and Y. Mao Cloning and characterization of a novel human STAR domain containing cDNA KHDRBS2 Mol. Biol. Rep. 29 2002 369 375 (Pubitemid 36035327)
60. T. Yamazaki, N. Fujiwara, H. Yukinaga, M. Ebisuya, T. Shiki, T. Kurihara, N. Kioka, T. Kambe, M. Nagao, E. Nishida, and S. Masuda The closely related RNA helicases, UAP56 and URH49, preferentially form distinct mRNA export machineries and coordinately regulate mitotic progression Mol. Biol. Cell 21 2010 2953 2965
61. R.A. Young Control of the embryonic stem cell state Cell 144 2011 940 954
62. R.M. Zayas, A. Hernández, B. Habermann, Y. Wang, J.M. Stary, and P.A. Newmark The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: analysis of ESTs from the hermaphroditic strain Proc. Natl. Acad. Sci. USA 102 2005 18491 18496 (Pubitemid 43011253)