Heterochromatin protein 1 promotes self-renewal and triggers regenerative proliferation in adult stem cells

Journal of Cell Biology

Volumn 201, Issue 3, 2013, Pages 409-425

  Zeng, An ^a   Li, Yong Qin ^a   Wang, Chen ^a   Han, Xiao Shuai ^a   Li, Ge ^a,e   Wang, Jian Yong ^a   Li, Dang Sheng ^c   Qin, Yong Wen ^b   Shi, Yufang ^a   Brewer, Gary ^a,d   Jing, Qing ^a,b  

^a SHANGHAI UNIVERSITY OF MEDICINE AND HEALTH SCIENCES   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c Chinese Academy of Sciences   (China)

^d RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROCHROMATIN PROTEIN 1; MINICHROMOSOME MAINTENANCE PROTEIN 5;

ADULT STEM CELL; ARTICLE; BLASTEMA; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CELL RENEWAL; EPIGENETICS; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; TURBELLARIA;

ADULT STEM CELLS; ANIMALS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; CHROMOSOMAL PROTEINS, NON-HISTONE; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HELMINTH PROTEINS; HUMANS; MICE; NIH 3T3 CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; PLANARIANS; PROTEIN TRANSPORT; REGENERATION; RNA INTERFERENCE; TRANSCRIPTOME;

TURBELLARIA;

EID: 84878662838     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201207172     Document Type: Article

References (75)

1. Agata, K. 2003. Regeneration and gene regulation in planarians. Curr. Opin. Genet. Dev., 13:492-496. http://dx.doi.org/10.1016/j.gde.2003.08.009
2. Azuara, V., P. Perry, S. Sauer, M. Spivakov, H.F. Jørgensen, R.M. John, M. Gouti, M. Casanova, G. Warnes, M. Merkenschlager, and A.G. Fisher. 2006. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol., 8:532-538. http://dx.doi.org/10.1038/ncb1403
3. Bannister, A.J., P. Zegerman, J.F. Partridge, E.A. Miska, J.O. Thomas, R.C. Allshire, and T. Kouzarides. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature., 410:120-124. http://dx.doi.org/10.1038/35065138
4. Barrero, M.J., and J.C. Izpisua Belmonte. 2011. Regenerating the epigenome. EMBO Rep., 12:208-215. http://dx.doi.org/10.1038/embor.2011.10
5. Bernstein, B.E., T.S. Mikkelsen, X. Xie, M. Kamal, D.J. Huebert, J. Cuff, B. Fry, A. Meissner, M. Wernig, K. Plath, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell., 125:315-326. http://dx.doi.org/10.1016/j.cell.2006.02.041
6. Bonuccelli, L., L. Rossi, A. Lena, V. Scarcelli, G. Rainaldi, M. Evangelista, P. Iacopetti, V. Gremigni, and A. Salvetti. 2010. An RbAp48-like gene regulates adult stem cells in planarians. J. Cell Sci., 123:690-698. http://dx.doi.org/10.1242/jcs.053900
7. Cammas, F., M. Herzog, T. Lerouge, P. Chambon, and R. Losson. 2004. Association of the transcriptional corepressor TIF1beta with heterochromatin protein 1 (HP1): an essential role for progression through differentiation. Genes Dev., 18:2147-2160. http://dx.doi.org/10.1101/gad.302904
8. Cebriá, F., and P.A. Newmark. 2005. 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., 132:3691-3703. http://dx.doi.org/10.1242/dev.01941
9. Collins, J.J., III, X. Hou, E.V. Romanova, B.G. Lambrus, C.M. Miller, A. Saberi, J.V. Sweedler, and P.A. Newmark. 2010. Genome-wide analyses reveal a role for peptide hormones in planarian germline development. PLoS Biol., 8:e1000509. http://dx.doi.org/10.1371/journal.pbio.1000509
10. Core, L.J., and J.T. Lis. 2008. Transcription regulation through promoterproximal pausing of RNA polymerase II. Science., 319:1791-1792. http://dx.doi.org/10.1126/science.1150843
11. Craig, J.M. 2005. Heterochromatin-many flavours, common themes. Bioessays., 27:17-28. http://dx.doi.org/10.1002/bies.20145
12. Cui, K., C. Zang, T.Y. Roh, D.E. Schones, R.W. Childs, W. Peng, and K. Zhao. 2009. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell., 4:80-93. http://dx.doi.org/10.1016/j.stem.2008.11.011
13. De Lucia, F., J.Q. Ni, C. Vaillant, and F.L. Sun. 2005. HP1 modulates the transcription of cell-cycle regulators in Drosophila melanogaster. Nucleic Acids Res., 33:2852-2858. http://dx.doi.org/10.1093/nar/gki584
14. Dovey, O.M., C.T. Foster, and S.M. Cowley. 2010. Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation. Proc. Natl. Acad. Sci. USA., 107:8242-8247. http://dx.doi.org/10.1073/pnas.1000478107
15. Eisenhoffer, G.T., H. Kang, and A. Sánchez Alvarado. 2008. Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell., 3:327-339. http://dx.doi.org/10.1016/j.stem.2008.07.002
16. Eissenberg, J.C., and S.C. Elgin. 2000. The HP1 protein family: getting a grip on chromatin. Curr. Opin. Genet. Dev., 10:204-210. http://dx.doi.org/10.1016/S0959-437X(00)00058-7
17. Eissenberg, J.C., T.C. James, D.M. Foster-Hartnett, T. Hartnett, V. Ngan, and S.C. Elgin. 1990. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA., 87:9923-9927. http://dx.doi.org/10.1073/pnas.87.24.9923
18. Fanti, L., and S. Pimpinelli. 2008. HP1: a functionally multifaceted protein. Curr. Opin. Genet. Dev., 18:169-174. http://dx.doi.org/10.1016/j.gde.2008.01.009
19. Fazzio, T.G., J.T. Huff, and B. Panning. 2008. An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell., 134:162-174. http://dx.doi.org/10.1016/j.cell.2008.05.031
20. Garcia, H., D. Fleyshman, K. Kolesnikova, A. Safina, M. Commane, G. Paszkiewicz, A. Omelian, C. Morrison, and K. Gurova. 2011. Expression of FACT in mammalian tissues suggests its role in maintaining of undifferentiated state of cells. Oncotarget., 2:783-796.
21. Gaspar-Maia, A., A. Alajem, E. Meshorer, and M. Ramalho-Santos. 2011. Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol., 12:36-47. http://dx.doi.org/10.1038/nrm3036
22. Grewal, S.I., and S. Jia. 2007. Heterochromatin revisited. Nat. Rev. Genet., 8:35-46. http://dx.doi.org/10.1038/nrg2008
23. Guo, T., A.H. Peters, and P.A. Newmark. 2006. A Bruno-like gene is required for stem cell maintenance in planarians. Dev. Cell., 11:159-169. http://dx.doi.org/10.1016/j.devcel.2006.06.004
24. Hayashi, T., M. Asami, S. Higuchi, N. Shibata, and K. Agata. 2006. Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev. Growth Differ., 48:371-380. http://dx.doi.org/10.1111/j.1440-169X.2006.00876.x
25. Ho, L., J.L. Ronan, J. Wu, B.T. Staahl, L. Chen, A. Kuo, J. Lessard, A.I. Nesvizhskii, J. Ranish, and G.R. Crabtree. 2009. An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc. Natl. Acad. Sci. USA., 106:5181-5186. http://dx.doi.org/10.1073/pnas.0812889106
26. Houlard, M., S. Berlivet, A.V. Probst, J.P. Quivy, P. Héry, G. Almouzni, and M. Gérard. 2006. CAF-1 is essential for heterochromatin organization in pluripotent embryonic cells. PLoS Genet., 2:e181. http://dx.doi.org/10.1371/journal.pgen.0020181
27. Kaji, K., I.M. Caballero, R. MacLeod, J. Nichols, V.A. Wilson, and B. Hendrich. 2006. The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat. Cell Biol., 8:285-292. http://dx.doi.org/10.1038/ncb1372
28. Kwon, S.H., L. Florens, S.K. Swanson, M.P. Washburn, S.M. Abmayr, and J.L. Workman. 2010. Heterochromatin protein 1 (HP1) connects the FACT histone chaperone complex to the phosphorylated CTD of RNA polymerase II. Genes Dev., 24:2133-2145. http://dx.doi.org/10.1101/gad.1959110
29. Labbé, R.M., M. Irimia, K.W. Currie, A. Lin, S.J. Zhu, D.D. Brown, E.J. Ross, V. Voisin, G.D. Bader, B.J. Blencowe, and B.J. Pearson. 2012. A comparative transcriptomic analysis reveals conserved features of stem cell pluripotency in planarians and mammals. Stem Cells., 30:1734-1745. http://dx.doi.org/10.1002/stem.1144
30. Lachner, M., D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature., 410:116-120. http://dx.doi.org/10.1038/35065132
31. Lee, T.I., S.E. Johnstone, and R.A. Young. 2006. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc., 1:729-748. http://dx.doi.org/10.1038/nprot.2006.98
32. Li, B.Z., Z. Huang, Q.Y. Cui, X.H. Song, L. Du, A. Jeltsch, P. Chen, G. Li, E. Li, and G.L. Xu. 2011a. Histone tails regulate DNA methylation by allosterically activating de novo methyltransferase. Cell Res., 21:1172-1181. http://dx.doi.org/10.1038/cr.2011.92
33. Li, L., and H. Clevers. 2010. Coexistence of quiescent and active adult stem cells in mammals. Science., 327:542-545. http://dx.doi.org/10.1126/science.1180794
34. Li, Y., D.A. Kirschmann, and L.L. Wallrath. 2002. Does heterochromatin protein 1 always follow code. Proc. Natl. Acad. Sci. USA., 99(Suppl. 4):16462-16469. http://dx.doi.org/10.1073/pnas.162371699
35. Li, Y.Q., A. Zeng, X.S. Han, C. Wang, G. Li, Z.C. Zhang, J.Y. Wang, Y.W. Qin, and Q. Jing. 2011b. Argonaute-2 regulates the proliferation of adult stem cells in planarian. Cell Res., 21:1750-1754. http://dx.doi.org/10.1038/cr.2011.151
36. Maison, C., and G. Almouzni. 2004. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol., 5:296-304. http://dx.doi.org/10.1038/nrm1355
37. Mikkelsen, T.S., M. Ku, D.B. Jaffe, B. Issac, E. Lieberman, G. Giannoukos, P. Alvarez, W. Brockman, T.K. Kim, R.P. Koche, et al. 2007. Genomewide maps of chromatin state in pluripotent and lineage-committed cells. Nature., 448:553-560. http://dx.doi.org/10.1038/nature06008
38. Newmark, P.A., and A. Sánchez Alvarado. 2000. Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev. Biol., 220:142-153. http://dx.doi.org/10.1006/dbio.2000.9645
39. Newmark, P.A., and A. Sánchez Alvarado. 2002. Not your father's planarian: a classic model enters the era of functional genomics. Nat. Rev. Genet., 3:210-219. http://dx.doi.org/10.1038/nrg759
40. Newmark, P.A., P.W. Reddien, F. Cebriá, and A. Sánchez Alvarado. 2003. Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proc. Natl. Acad. Sci. USA., 100(Suppl. 1):11861-11865. http://dx.doi.org/10.1073/pnas.1834205100
41. Nielsen, A.L., J.A. Ortiz, J. You, M. Oulad-Abdelghani, R. Khechumian, A. Gansmuller, P. Chambon, and R. Losson. 1999. Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TIF1 family. EMBO J., 18:6385-6395. http://dx.doi.org/10.1093/emboj/18.22.6385
42. Onal, P., D. Grün, C. Adamidi, A. Rybak, J. Solana, G. Mastrobuoni, Y. Wang, H.P. Rahn, W. Chen, S. Kempa, et al. 2012. Gene expression of pluripotency determinants is conserved between mammalian and planarian stem cells. EMBO J., 31:2755-2769. http://dx.doi.org/10.1038/emboj.2012.110
43. Orkin, S.H., and K. Hochedlinger. 2011. Chromatin connections to pluripotency and cellular reprogramming. Cell., 145:835-850. http://dx.doi.org/10.1016/j.cell.2011.05.019
44. Orphanides, G., G. LeRoy, C.H. Chang, D.S. Luse, and D. Reinberg. 1998. FACT, a factor that facilitates transcript elongation through nucleosomes. Cell., 92:105-116. http://dx.doi.org/10.1016/S0092-8674(00)80903-4
45. Panteleeva, I., S. Boutillier, V. See, D.G. Spiller, C. Rouaux, G. Almouzni, D. Bailly, C. Maison, H.C. Lai, J.P. Loeffler, and A.L. Boutillier. 2007. HP1alpha guides neuronal fate by timing E2F-targeted genes silencing during terminal differentiation. EMBO J., 26:3616-3628. http://dx.doi.org/10.1038/sj.emboj.7601789
46. Pearson, B.J., G.T. Eisenhoffer, K.A. Gurley, J.C. Rink, D.E. Miller, and A. Sánchez Alvarado. 2009. Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev. Dyn., 238:443-450. http://dx.doi.org/10.1002/dvdy.21849
47. Peiris, T.H., F. Weckerle, E. Ozamoto, D. Ramirez, D. Davidian, M.E. García-Ojeda, and N.J. Oviedo. 2012. TOR signaling regulates planarian stem cells and controls localized and organismal growth. J. Cell Sci., 125:1657-1665. http://dx.doi.org/10.1242/jcs.104711
48. Pellettieri, J., P. Fitzgerald, S. Watanabe, J. Mancuso, D.R. Green, and A. Sánchez Alvarado. 2010. Cell death and tissue remodeling in planarian regeneration. Dev. Biol., 338:76-85. http://dx.doi.org/10.1016/j.ydbio.2009.09.015
49. Piacentini, L., L. Fanti, M. Berloco, B. Perrini, and S. Pimpinelli. 2003. Heterochromatin protein 1 (HP1) is associated with induced gene expression in Drosophila euchromatin. J. Cell Biol., 161:707-714. http://dx.doi.org/10.1083/jcb.200303012
50. Reddien, P.W., and A. Sánchez Alvarado. 2004. Fundamentals of planarian regeneration. Annu. Rev. Cell Dev. Biol., 20:725-757. http://dx.doi.org/10.1146/annurev.cellbio.20.010403.095114
51. Reddien, P.W., A.L. Bermange, K.J. Murfitt, J.R. Jennings, and A. Sánchez Alvarado. 2005a. Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev. Cell., 8:635-649. http://dx.doi.org/10.1016/j.devcel.2005.02.014
52. Reddien, P.W., N.J. Oviedo, J.R. Jennings, J.C. Jenkin, and A. Sánchez Alvarado. 2005b. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science., 310:1327-1330. http://dx.doi.org/10.1126/science.1116110
53. Reddien, P.W., P.A. Newmark, and A. Sánchez Alvarado. 2008. Gene nomenclature guidelines for the planarian Schmidtea mediterranea. Dev. Dyn., 237:3099-3101. http://dx.doi.org/10.1002/dvdy.21623
54. Ritou, E., M. Bai, and S.D. Georgatos. 2007. Variant-specific patterns and humoral regulation of HP1 proteins in human cells and tissues. J. Cell Sci., 120: 3425-3435. http://dx.doi.org/10.1242/jcs.012955
55. Robb, S.M., E. Ross, and A. Sánchez Alvarado. 2008. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res., 36(Suppl. 1):D599-D606. http://dx.doi.org/10.1093/nar/gkm684
56. Rossi, L., A. Salvetti, F.M. Marincola, A. Lena, P. Deri, L. Mannini, R. Batistoni, E. Wang, and V. Gremigni. 2007. Deciphering the molecular machinery of stem cells: a look at the neoblast gene expression profile. Genome Biol., 8:R62. http://dx.doi.org/10.1186/gb-2007-8-4-r62
57. Rouhana, L., N. Shibata, O. Nishimura, and K. Agata. 2010. Different requirements for conserved post-transcriptional regulators in planarian regeneration and stem cell maintenance. Dev. Biol., 341:429-443. http://dx.doi.org/10.1016/j.ydbio.2010.02.037
58. Ryu, S., J. Holzschuh, S. Erhardt, A.K. Ettl, and W. Driever. 2005. Depletion of minichromosome maintenance protein 5 in the zebrafish retina causes cell-cycle defect and apoptosis. Proc. Natl. Acad. Sci. USA., 102:18467-18472. http://dx.doi.org/10.1073/pnas.0506187102
59. Saldanha, A.J. 2004. Java Treeview-extensible visualization of microarray data. Bioinformatics., 20:3246-3248. http://dx.doi.org/10.1093/bioinformatics/bth349
60. Saló, E., and J. Baguñá. 1984. 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., 83:63-80.
61. Salvetti, A., L. Rossi, P. Deri, and R. Batistoni. 2000. An MCM2-related gene is expressed in proliferating cells of intact and regenerating planarians. Dev. Dyn., 218:603-614. http://dx.doi.org/10.1002/1097-0177(2000)9999:9999::AID-DVDY10163.0.CO;2-C
62. Salvetti, A., L. Rossi, A. Lena, R. Batistoni, P. Deri, G. Rainaldi, M.T. Locci, M. Evangelista, and V. Gremigni. 2005. DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development., 132:1863-1874. http://dx.doi.org/10.1242/dev.01785
63. Sánchez Alvarado, A. 2006. Planarian regeneration: its end is its beginning. Cell., 124:241-245. http://dx.doi.org/10.1016/j.cell.2006.01.012
64. Scimone, M.L., J. Meisel, and P.W. Reddien. 2010. The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development., 137:1231-1241. http://dx.doi.org/10.1242/dev.042051
65. Solana, J., D. Kao, Y. Mihaylova, F. Jaber-Hijazi, S. Malla, R. Wilson, and A. Aboobaker. 2012. Defining the molecular profile of planarian pluripotent stem cells using a combinatorial RNAseq, RNA interference and irradiation approach. Genome Biol., 13:R19. http://dx.doi.org/10.1186/gb-2012-13-3-r19
66. Tu, K.C., B.J. Pearson, and A. Sánchez Alvarado. 2012. TORC1 is required to balance cell proliferation and cell death in planarians. Dev. Biol., 365:458-469. http://dx.doi.org/10.1016/j.ydbio.2012.03.010
67. Vermaak, D., and H.S. Malik. 2009. Multiple roles for heterochromatin protein 1 genes in Drosophila. Annu. Rev. Genet., 43:467-492. http://dx.doi.org/10.1146/annurev-genet-102108-134802
68. Wagner, D.E., I.E. Wang, and P.W. Reddien. 2011. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science., 332:811-816. http://dx.doi.org/10.1126/science.1203983
69. Wagner, D.E., J.J. Ho, and P.W. Reddien. 2012. Genetic regulators of a pluripotent adult stem cell system in planarians identified by RNAi and clonal analysis. Cell Stem Cell., 10:299-311. http://dx.doi.org/10.1016/j.stem.2012.01.016
70. Wang, Y., R.M. Zayas, T. Guo, and P.A. Newmark. 2007. nanos function is essential for development and regeneration of planarian germ cells. Proc. Natl. Acad. Sci. USA., 104:5901-5906. http://dx.doi.org/10.1073/pnas.0609708104
71. Wang, Y., J.M. Stary, J.E. Wilhelm, and P.A. Newmark. 2010. A functional genomic screen in planarians identifies novel regulators of germ cell development. Genes Dev., 24:2081-2092. http://dx.doi.org/10.1101/gad.1951010
72. Weissman, I.L. 2000. Stem cells: units of development, units of regeneration, and units in evolution. Cell., 100:157-168. http://dx.doi.org/10.1016/S0092-8674(00)81692-X
73. Wenemoser, D., and P.W. Reddien. 2010. Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. Dev. Biol., 344:979-991. http://dx.doi.org/10.1016/j.ydbio.2010.06.017
74. Wenemoser, D., S.W. Lapan, A.W. Wilkinson, G.W. Bell, and P.W. Reddien. 2012. A molecular wound response program associated with regeneration initiation in planarians. Genes Dev., 26:988-1002. http://dx.doi.org/10.1101/gad.187377.112
75. Zayas, R.M., A. Hernández, B. Habermann, Y. Wang, J.M. Stary, and P.A. Newmark. 2005. The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: analysis of ESTs from the hermaphroditic strain. Proc. Natl. Acad. Sci. USA., 102:18491-18496. http://dx.doi.org/10.1073/pnas.0509507102