Stemness is only a state of the cell

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 73, Issue , 2008, Pages 227-234

  Kagalwala, M N ^a,c   Singh, S K ^a   Majumder, S ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 21; REPRESSOR ELEMENT 1 SILENCING TRANSCRIPTION; REPRESSOR PROTEIN; UNCLASSIFIED DRUG; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR REST; RE1 SILENCING TRANSCRIPTION FACTOR; RE1-SILENCING TRANSCRIPTION FACTOR;

BLASTOCYST; CELL MATURATION; CELL RENEWAL; CONFERENCE PAPER; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; EPIGENETICS; GENE TARGETING; HUMAN; MEDULLOBLASTOMA; MUSCLE DEVELOPMENT; MYOBLAST; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; STEM CELL; CELL DIFFERENTIATION; DNA MODIFICATION; MOUSE EMBRYONIC STEM CELL; NUCLEAR REPROGRAMMING; STEM CELL SELF-RENEWAL; ANIMAL; BIOLOGICAL MODEL; CELL PROLIFERATION; CEREBELLUM TUMOR; CYTOLOGY; GENE EXPRESSION; GENETICS; INNER CELL MASS; NERVE CELL; PATHOLOGY; PHYSIOLOGY; PLURIPOTENT STEM CELL; REVIEW;

ANIMALS; BLASTOCYST INNER CELL MASS; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLAR NEOPLASMS; EMBRYONIC STEM CELLS; GENE EXPRESSION; HUMANS; MEDULLOBLASTOMA; MODELS, BIOLOGICAL; MYOBLASTS; NEURONS; PLURIPOTENT STEM CELLS; REPRESSOR PROTEINS; STEM CELLS;

EID: 68549085527     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2008.73.042     Document Type: Conference Paper

References (82)

1. Andres, M.E., Burger, C., Peral-Rubio, M.J., Battaglioli, E., Anderson, M.E., Grimes, J., Dallman, J., Ballas, N., and Mandel, G. 1999. CoREST:A functional corepressor required for regulation of neural-specific gene expression. Proc. Natl. Acad. Sci. 96: 9873-9878.
2. Avilion, A.A., Nicolis, S.K., Pevny, L.H., Perez, L., Vivian, N., and Lovell-Badge, R. 2003. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17: 126-140.
3. Ballas, N. and Mandel, G. 2005. The many faces of REST oversee epigenetic programming of neuronal genes. Curr. Opin. Neurobiol. 15: 500-506.
4. Ballas, N., Grunseich, C., Lu, D.D., Speh, J.C., and Mandel, G. 2005. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121: 645-657.
5. Ballas, N., Battaglioli, E., Atouf, F., Andres, M.E., Chenoweth, J., Anderson, M.E., Burger, C., Moniwa, M., Davie, J.R., Bowers, W.J., et al. 2001. Regulation of neuronal traits by a novel transcriptional complex. Neuron 31: 353-365.
6. Bingham, A.J., Ooi, L., Kozera, L., White, E., and Wood, I.C. 2007. The repressor element 1-silencing transcription factor regulates heart-specific gene expression using multiple chromatin-modifying complexes. Mol. Cell. Biol. 27: 4082-4092.
7. 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., et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
8. Bruce, A.W., Donaldson, I.J., Wood, I.C., Yerbury, S.A., Sadowski, M.I., Chapman, M., Gottgens, B., and Buckley, N.J. 2004. Genome-wide analysis of repressor element 1 silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) target genes. Proc. Natl. Acad. Sci. 101: 10458-10463.
9. Calderone, A., Jover, T., Noh, K.M., Tanaka, H.,Yokota, H., Lin, Y., Grooms, S.Y., Regis, R., Bennett, M.V., and Zukin, R.S. 2003. Ischemic insults derepress the gene silencer REST in neurons destined to die. J. Neurosci. 23: 2112-2121.
10. Canzonetta, C., Mulligan, C., Deutsch, S., Ruf, S., O'Doherty, A., Lyle, R., Borel, C., Lin-Marq, N., Delom, F., Groet, J., et al. 2008. DYRK1A-dosage imbalance perturbs NRSF/REST levels, deregulating pluripotency and embryonic stem cell fate in Down syndrome. Am. J. Hum. Genet. 83: 388-400.
11. Cao, X., Yeo, G., Muotri, A.R., Kuwabara, T., and Gage, F.H. 2006. Noncoding RNAs in the mammalian central nervous system. Annu. Rev. Neurosci. 29: 77-103.
12. Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S., and Smith, A. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113: 643-655.
13. Chen, Z.F., Paquette, A.J., and Anderson, D.J. 1998. NRSF/REST is required in vivo for repression of multiple neuronal target genes during embryogenesis. Nat. Genet. 20: 136-142.
14. Cheong, A., Bingham, A.J., Li, J., Kumar, B., Sukumar, P., Munsch, C., Buckley, N.J., Neylon, C.B., Porter, K.E., Beech, D.J., andWood, I.C. 2005. Downregulated REST transcription factor is a switch enabling critical potassium channel expression and cell proliferation. Mol. Cell 20: 45-52.
15. Chong, J.A.,Tapia-Ramirez, J., Kim, S.,Toledo-Aral, J.J., Zheng, Y., Boutros, M.C., Altshuller, Y.M., Frohman, M.A., Kraner, S.D., and Mandel, G. 1995. REST:A mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80: 949-957.
16. Conaco, C., Otto, S., Han, J.J., and Mandel, G. 2006. Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl. Acad. Sci. 103: 2422-2427.
17. Coulson, J.M. 2005. Transcriptional regulation: Cancer, neurons and the REST. Curr. Biol. 15: R665-R668.
18. Davis, A.C.,Wims, M., Spotts, G.D., Hann, S.R., and Bradley, A. 1993. A null c-myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes Dev. 7: 671-682.
19. Dellovade, T., Romer, J.T., Curran, T., and Rubin, L.L. 2006. The hedgehog pathway and neurological disorders. Annu. Rev. Neurosci. 29: 539-563.
20. Ding, N., Zhou, H., Esteve, P.O., Chin, H.G., Kim, S., Xu, X., Joseph, S.M., Friez, M.J., Schwartz, C.E., Pradhan, S., and Boyer, T.G. 2008. Mediator links epigenetic silencing of neuronal gene expression with x-linked mental retardation. Mol. Cell 31: 347-359.
21. Eberhart, C.G. and Burger, P.C. 2003. Anaplasia and grading in medulloblastomas. Brain Pathol. 13: 376-385.
22. Fogarty, M.P., Kessler, J.D., and Wechsler-Reya, R.J. 2005. Morphing into cancer: The role of developmental signaling pathways in brain tumor formation. J. Neurobiol. 64: 458-475.
23. Formisano, L., Noh, K.M., Miyawaki, T., Mashiko, T., Bennett, M.V., and Zukin, R.S. 2007. Ischemic insults promote epigenetic reprogramming of μ opioid receptor expression in hippocampal neurons. Proc. Natl. Acad. Sci. 104: 4170-4175.
24. Fuller, G.N., Su, X., Price, R.E., Cohen, Z.R., Lang, F.F., Sawaya, R., and Majumder, S. 2005. Many human medulloblastoma tumors overexpress repressor element-1 silencing transcription (REST)/neuron-restrictive silencer factor, which can be functionally countered by REST-VP16. Mol. Cancer Ther. 4: 343-349.
25. Gilbertson, R.J. 2004. Medulloblastoma: Signalling a change in treatment. Lancet Oncol. 5: 209-218.
26. Griffith, E.C., Cowan, C.W., and Greenberg, M.E. 2001. REST acts through multiple deacetylase complexes. Neuron 31: 339-340.
27. Guardavaccaro, D., Frescas, D., Dorrello, N.V., Peschiaroli, A., Multani,A.S.,Cardozo,T., Lasorella,A., Iavarone,A.,Chang, S., Hernando, E., and Pagano, M. 2008. Control of chromosome stability by the β-TrCP-REST-Mad2 axis. Nature 452: 365-369.
28. Higashino, K., Narita,T.,Taga,T., Ohta, S., andTakeuchi,Y. 2003. Malignant rhabdoid tumor shows a unique neural differentiation as distinct from neuroblastoma. Cancer Sci. 94: 37-42.
29. Houbaviy, H.B., Murray, M.F., and Sharp, P.A. 2003. Embryonic stem cell-specific microRNAs. Dev. Cell 5: 351-358.
30. Hsieh, J. and Gage, F.H. 2005. Chromatin remodeling in neural development and plasticity. Curr.Opin. Cell. Biol. 17: 664-671.
31. Immaneni, A., Lawinger, P., Zhao, Z., Lu, W., Rastelli, L., Morris, J.H., and Majumder, S. 2000. REST-VP16 activates multiple neuronal differentiation genes in human NT2 cells. Nucleic Acids Res. 28: 3403-3410.
32. Jaenisch, R. andYoung, R. 2008. Stemcells, themolecular circuitry of pluripotency and nuclear reprogramming. Cell 132: 567-582.
33. Jepsen, K., Hermanson, O., Onami, T.M., Gleiberman, A.S., Lunyak, V., McEvilly, R.J., Kurokawa, R., Kumar, V., Liu, F., Seto, E., et al. 2000. Combinatorial roles of the nuclear receptor corepressor in transcription and development. Cell 102: 753-763.
34. Johnson, D.S., Mortazavi, A., Myers, R.M., and Wold, B. 2007. Genome-wide mapping of in vivo protein-DNA interactions. Science 316: 1497-1502.
35. Johnson, R., Teh, C.H., Kunarso, G.,Wong, K.Y., Srinivasan, G., Cooper, M.L., Volta, M., Chan, S.S., Lipovich, L., Pollard, S.M., et al. 2008. REST regulates distinct transcriptional networks in embryonic and neural stem cells. PLoS Biol. 6: e256.
36. Kenney, A.M., Widlund, H.R., and Rowitch, D.H. 2004. Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 131: 217-228.
37. Kim, C.S., Hwang, C.K., Choi, H.S., Song, K.Y., Law, P.Y.,Wei, L.N., and Loh, H.H. 2004. Neuron-restrictive silencer factor (NRSF) functions as a repressor in neuronal cells to regulate the μ opioid receptor gene. J. Biol. Chem. 279: 46464-46473.
38. Kim, J., Chu, J., Shen, X., Wang, J., and Orkin, S.H. 2008. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132: 1049-1061.
39. Knoepfler, P.S. andKenney,A.M. 2006.Neural precursor cycling at sonic speed: N-Myc pedals, GSK-3 brakes. Cell Cycle 5: 47-52.
40. Koenigsberger, C., Chicca II, J.J., Amoureux, M.C., Edelman, G.M., and Jones, F.S. 2000. Differential regulation by multiple promoters of the gene encoding the neuron-restrictive silencer factor. Proc. Natl. Acad. Sci. 97: 2291-2296.
41. Kuwabara, T., Hsieh, J., Nakashima, K., Taira, K., and Gage, F.H. 2004. A small modulatory dsRNA specifies the fate of adult neural stem cells. Cell 116: 779-793.
42. Kuwahara, K., Saito, Y., Takano, M., Arai, Y., Yasuno, S., Nakagawa,Y., Takahashi, N., Adachi,Y., Takemura, G., Horie, M., et al. 2003. NRSF regulates the fetal cardiac gene program andmaintains normal cardiac structure and function. EMBO J. 22: 6310-6321.
43. Lawinger, P.,Venugopal, R., Guo, Z.S., Immaneni, A., Sengupta, D., Lu, W., Rastelli, L., Marin Dias Carneiro, A., Levin, V., Fuller, G.N., et al. 2000. The neuronal repressor REST/NRSF is an essential regulator in medulloblastoma cells. Nat. Med. 6: 826-831.
44. Lemonde, S., Rogaeva, A., and Albert, P.R. 2004. Cell type-dependent recruitment of trichostatinA-sensitive repression of the human 5-HT1A receptor gene. J. Neurochem. 88: 857-868.
45. Lengner, C.J.,Welstead, G.G., and Jaenisch, R. 2008.The pluripotency regulator Oct4: A role in somatic stem cells? Cell Cycle 7: 725-728.
46. Li, M., Sendtner, M., and Smith, A. 1995. Essential function of LIF receptor in motor neurons. Nature 378: 724-727.
47. Lie, D.C., Colamarino, S.A., Song, H.J., Desire, L., Mira, H., Consiglio, A., Lein, E.S., Jessberger, S., Lansford, H., Dearie, A.R., and Gage, F.H. 2005. Wnt signalling regulates adult hippocampal neurogenesis. Nature 437: 1370-1375.
48. Lunyak, V.V. and Rosenfeld, M.G. 2005. No rest for REST: REST/NRSF regulation of neurogenesis. Cell 121: 499-501.
49. Lunyak, V.V., Burgess, R., Prefontaine, G.G., Nelson, C., Sze, S.H., Chenoweth, J., Schwartz, P., Pevzner, P.A., Glass, C., Mandel, G., and Rosenfeld, M.G. 2002. Corepressor-dependent silencing of chromosomal regions encoding neuronal genes. Science 298: 1747-1752.
50. Majumder, S. 2006. REST in good times and bad: Roles in tumor suppressor and oncogenic activities. Cell Cycle 5: 1929-1935.
51. McMahon, A.P. 2000. More surprises in the Hedgehog signaling pathway. Cell 100: 185-188.
52. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M., and Yamanaka, S. 2003. The homeoprotein Nanog is required for maintenance of pluripotency inmouse epiblast and ES cells. Cell 113: 631-642.
53. Nichols, J., Chambers, I., Taga, T., and Smith, A. 2001. Physiological rationale for responsiveness of mouse embryonic stem cells to gp130 cytokines. Development 128: 2333-2339.
54. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Scholer, H., and Smith, A. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4.Cell 95: 379-391.
55. Nishihara, S., Tsuda, L., and Ogura, T. 2003. The canonical Wnt pathway directly regulates NRSF/REST expression in chick spinal cord. Biochem. Biophys. Res. Commun. 311: 55-63.
56. Nishimura, E., Sasaki, K., Maruyama, K., Tsukada, T., and Yamaguchi, K. 1996. Decrease in neuron-restrictive silencer factor (NRSF) mRNA levels during differentiation of cultured neuroblastoma cells. Neurosci. Lett. 211: 101-104.
57. Otto, S.J., McCorkle, S.R., Hover, J., Conaco, C., Han, J.J., Impey, S., Yochum, G.S., Dunn, J.J., Goodman, R.H., and Mandel, G. 2007. A new binding motif for the transcriptional repressor REST uncovers large gene networks devoted to neuronal functions. J. Neurosci. 27: 6729-6739.
58. Pan, G. and Thomson, J.A. 2007. Nanog and transcriptional networks in embryonic stemcell pluripotency. Cell Res. 17: 42-49.
59. Paquette, A.J., Perez, S.E., and Anderson, D.J. 2000. Constitutive expression of the neuron-restrictive silencer factor (NRSF)/REST in differentiating neurons disrupts neuronal gene expression and causes axon pathfinding errors in vivo. Proc. Natl. Acad. Sci. 97: 12318-12323.
60. Raffel, C. 2004. Medulloblastoma: Molecular genetics and animal models. Neoplasia 6: 310-322.
61. Romer, J. and Curran, T. 2005. Targeting medulloblastoma: Small-molecule inhibitors of the Sonic Hedgehog pathway as potential cancer therapeutics. Cancer Res. 65: 4975-4978.
62. Rutka, J.T., Kuo, J.S., Carter, M., Ray, A., Ueda, S., and Mainprize, T.G. 2004. Advances in the treatment of pediatric brain tumors. Expert Rev. Neurother. 4: 879-893.
63. Schoenherr, C.J. and Anderson, D.J. 1995. The neuron-restrictive silencer factor (NRSF): A coordinate repressor of multiple neuron-specific genes. Science 267: 1360-1363.
64. Shimojo, M. and Hersh, L.B. 2004. Regulation of the cholinergic gene locus by the repressor element-1 silencing transcription factor/neuron restrictive silencer factor (REST/NRSF). Life Sci. 74: 2213-2225.
65. Shimojo, M., Paquette, A.J., Anderson, D.J., and Hersh, L.B. 1999. Protein kinaseA regulates cholinergic gene expression in PC12 cells: REST4 silences the silencing activity of neuronrestrictive silencer factor/REST. Mol. Cell. Biol. 19: 6788-6795.
66. Singh, S.K., Kagalwala, M.N., Parker-Thornburg, J., Adams, H., and Majumder, S. 2008. REST maintains self-renewal and pluripotency of embryonic stem cells. Nature 453: 223-227.
67. Stewart, C.L., Kaspar, P., Brunet, L.J., Bhatt, H., Gadi, I., Kontgen, F., and Abbondanzo, S.J. 1992. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359: 76-79.
68. Su, X., Kameoka, S., Lentz, S., andMajumder, S. 2004.Activation of REST/NRSF target genes in neural stem cells is sufficient to cause neuronal differentiation. Mol. Cell. Biol. 24: 8018-8025.
69. Su, X., Gopalakrishnan, V., Stearns, D., Aldape, K., Lang, F.F., Fuller, G., Snyder, E., Eberhart, C.G., and Majumder, S. 2006. Abnormal expression of REST/NRSF and Myc in neural stem/progenitor cells causes cerebellar tumors by blocking neuronal differentiation. Mol. Cell. Biol. 26: 1666-1678.
70. Sun, Y.M., Cooper, M., Finch, S., Lin, H.H., Chen, Z.F., Williams, B.P., and Buckley, N.J. 2008. Rest-mediated regulation of extracellular matrix is crucial for neural development. PLoS ONE 3: e3656.
71. Tahiliani, M., Mei, P., Fang, R., Leonor, T., Rutenberg, M., Shimizu, F., Li, J., Rao, A., and Shi, Y. 2007. The histone H3K4 demethylase SMCX links REST target genes to X-linked mental retardation. Nature 447: 601-605.
72. Takeda, K., Noguchi, K., Shi, W., Tanaka, T., Matsumoto, M., Yoshida, N., Kishimoto, T., and Akira, S. 1997. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc. Natl. Acad. Sci. 94: 3801-3804.
73. Watanabe, Y., Kameoka, S., Gopalakrishnan, V., Aldape, K.D., Pan, Z.Z., Lang, F.F., and Majumder, S. 2004. Conversion of myoblasts to physiologically active neuronal phenotype. Genes Dev. 18: 889-900.
74. Weissman, A.M. 2008. How much REST is enough? Cancer Cell 13: 381-383.
75. Westbrook, T.F., Martin, E.S., Schlabach, M.R., Leng,Y., Liang, A.C., Feng, B., Zhao, J.J., Roberts, T.M., Mandel, G., Hannon, G.J., et al. 2005. A genetic screen for candidate tumor suppressors identifies REST. Cell 121: 837-848.
76. Westbrook, T.F., Hu, G., Ang, X.L., Mulligan, P., Pavlova, N.N., Liang, A., Leng, Y., Maehr, R., Shi, Y., Harper, J.W., and Elledge, S.J. 2008. SCFβ-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 452: 370-374.
77. Willert, J., Epping, M., Pollack, J.R., Brown, P.O., and Nusse, R. 2002. A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Dev. Biol. 2: 8.
78. Wu, J. and Xie X. 2006. Comparative sequence analysis reveals an intricate network among REST, CREB and miRNA in mediating neuronal gene expression. Genome Biol. 7: R85.
79. Yamanaka, S. 2008. Induction of pluripotent stem cells from mouse fibroblasts by four transcription factors. Cell Prolif. (suppl. 1) 41: 51-56.
80. Yu, J. and Thomson, J.A. 2008. Pluripotent stem cell lines. Genes Dev. 22: 1987-1997.
81. Zuccato, C., Tartari, M., Crotti, A., Goffredo, D., Valenza, M., Conti, L., Cataudella, T., Leavitt, B.R., Hayden, M.R., Timmusk, T., et al. 2003. Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat. Genet. 35: 76-83.
82. Zuccato, C., Belyaev, N., Conforti, P., Ooi, L., Tartari, M., Papadimou, E., MacDonald, M., Fossale, E., Zeitlin, S., Buckley, N., and Cattaneo, E. 2007.Widespread disruption of repressor element-1 silencing transcription factor/neuron-restrictive silencer factor occupancy at its target genes in Huntington's disease. J. Neurosci. 27: 6972-6983.