Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells

Cell

Volumn 157, Issue 3, 2014, Pages 580-594

  Suvà, Mario L ^a,b,c   Rheinbay, Esther ^a,b,c   Gillespie, Shawn M ^a,b,c   Patel, Anoop P ^a,b   Wakimoto, Hiroaki ^b   Rabkin, Samuel D ^b   Riggi, Nicolo ^b,c   Chi, Andrew S ^b   Cahill, Daniel P ^b   Nahed, Brian V ^b   Curry, William T ^b   Martuza, Robert L ^b   Rivera, Miguel N ^b,c   Rossetti, Nikki ^b,c   Kasif, Simon ^d,e   Beik, Samantha ^c   Kadri, Sabah ^c   Tirosh, Itay ^c   Wortman, Ivo ^c   Shalek, Alex K ^f   Rozenblatt Rosen, Orit ^c   Regev, Aviv ^a,c   Louis, David N ^b   Bernstein, Bradley E ^a,b,c   more..

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d BOSTON UNIVERSITY   (United States)

^e Boston University   (United States)

^f HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; TRANSCRIPTION FACTOR;

ARTICLE; BRAIN TUMOR; CELL DIFFERENTIATION; CELL TYPE; CONTROLLED STUDY; EPIGENETICS; FLOW CYTOMETRY; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; STEM LIKE TUMOR PROPAGATING CELL; TUMOR CELL;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELLS, CULTURED; CO-REPRESSOR PROTEINS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; NEOPLASTIC STEM CELLS; NERVE TISSUE PROTEINS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; TRANSCRIPTION FACTORS;

EID: 84899524502     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.02.030     Document Type: Article

References (63)

1. J. Anido, A. Sáez-Borderías, A. Gonzàlez- Juncà, L. Rodón, G. Folch, M.A. Carmona, R.M. Prieto- Sánchez, I. Barba, E. Martínez-Sáez, and L. Prudkin et al. TGF-β receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma Cancer Cell 18 2010 655 668
2. S. Bao, Q. Wu, R.E. McLendon, Y. Hao, Q. Shi, A.B. Hjelmeland, M.W. Dewhirst, D.D. Bigner, and J.N. Rich Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature 444 2006 756 760
3. L.E. Barrett, Z. Granot, C. Coker, A. Iavarone, D. Hambardzumyan, E.C. Holland, H.S. Nam, and R. Benezra Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma Cancer Cell 21 2012 11 24
4. E. Binda, A. Visioli, F. Giani, G. Lamorte, M. Copetti, K.L. Pitter, J.T. Huse, L. Cajola, N. Zanetti, and F. DiMeco et al. The EphA2 receptor drives self-renewal and tumorigenicity in stem-like tumor-propagating cells from human glioblastomas Cancer Cell 22 2012 765 780
5. M. Bulger, and M. Groudine Functional and mechanistic diversity of distal transcription enhancers Cell 144 2011 327 339
6. C.L. Chaffer, N.D. Marjanovic, T. Lee, G. Bell, C.G. Kleer, F. Reinhardt, A.C. D'Alessio, R.A. Young, and R.A. Weinberg Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity Cell 154 2013 61 74
7. R. Chen, M.C. Nishimura, S.M. Bumbaca, S. Kharbanda, W.F. Forrest, I.M. Kasman, J.M. Greve, R.H. Soriano, L.L. Gilmour, and C.S. Rivers et al. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma Cancer Cell 17 2010 362 375
8. J. Chen, Y. Li, T.S. Yu, R.M. McKay, D.K. Burns, S.G. Kernie, and L.F. Parada A restricted cell population propagates glioblastoma growth after chemotherapy Nature 488 2012 522 526
9. Y. Chudnovsky, D. Kim, S. Zheng, W.A. Whyte, M. Bansal, M.A. Bray, S. Gopal, M.A. Theisen, S. Bilodeau, and P. Thiru et al. ZFHX4 interacts with the NuRD core member CHD4 and regulates the glioblastoma tumor-initiating cell state Cell Rep. 6 2014 313 324
10. M.P. Creyghton, A.W. Cheng, G.G. Welstead, T. Kooistra, B.W. Carey, E.J. Steine, J. Hanna, M.A. Lodato, G.M. Frampton, and P.A. Sharp et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state Proc. Natl. Acad. Sci. USA 107 2010 21931 21936
11. B.W. Day, B.W. Stringer, F. Al-Ejeh, M.J. Ting, J. Wilson, K.S. Ensbey, P.R. Jamieson, Z.C. Bruce, Y.C. Lim, and C. Offenhäuser et al. EphA3 maintains tumorigenicity and is a therapeutic target in glioblastoma multiforme Cancer Cell 23 2013 238 248
12. J. Ernst, P. Kheradpour, T.S. Mikkelsen, N. Shoresh, L.D. Ward, C.B. Epstein, X. Zhang, L. Wang, R. Issner, and M. Coyne et al. Mapping and analysis of chromatin state dynamics in nine human cell types Nature 473 2011 43 49
13. D. Friedmann-Morvinski, E.A. Bushong, E. Ke, Y. Soda, T. Marumoto, O. Singer, M.H. Ellisman, and I.M. Verma Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice Science 338 2012 1080 1084
14. R.M. Gangemi, F. Griffero, D. Marubbi, M. Perera, M.C. Capra, P. Malatesta, G.L. Ravetti, G.L. Zona, A. Daga, and G. Corte SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity Stem Cells 27 2009 40 48
15. J.H. Hanna, K. Saha, and R. Jaenisch Pluripotency and cellular reprogramming: facts, hypotheses, unresolved issues Cell 143 2010 508 525
16. W.J. Harris, X. Huang, J.T. Lynch, G.J. Spencer, J.R. Hitchin, Y. Li, F. Ciceri, J.G. Blaser, B.F. Greystoke, and A.M. Jordan et al. The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells Cancer Cell 21 2012 473 487
17. G.C. Hon, R.D. Hawkins, and B. Ren Predictive chromatin signatures in the mammalian genome Hum. Mol. Genet. 18 R2 2009 R195 R201
18. K. Ito, R. Bernardi, A. Morotti, S. Matsuoka, G. Saglio, Y. Ikeda, J. Rosenblatt, D.E. Avigan, J. Teruya-Feldstein, and P.P. Pandolfi PML targeting eradicates quiescent leukaemia-initiating cells Nature 453 2008 1072 1078
19. M. Janiszewska, M.L. Suvà, N. Riggi, R.H. Houtkooper, J. Auwerx, V. Clément-Schatlo, I. Radovanovic, E. Rheinbay, P. Provero, and I. Stamenkovic Imp2 controls oxidative phosphorylation and is crucial for preserving glioblastoma cancer stem cells Genes Dev. 26 2012 1926 1944
20. M. Jansen, S. Yip, and D.N. Louis Molecular pathology in adult gliomas: diagnostic, prognostic, and predictive markers Lancet 9 2010 717 726
21. E. Kim, M. Kim, D.H. Woo, Y. Shin, J. Shin, N. Chang, Y.T. Oh, H. Kim, J. Rheey, and I. Nakano et al. Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells Cancer Cell 23 2013 839 852
22. M. Ku, R.P. Koche, E. Rheinbay, E.M. Mendenhall, M. Endoh, T.S. Mikkelsen, A. Presser, C. Nusbaum, X. Xie, and A.S. Chi et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains PLoS Genet. 4 2008 e1000242
23. J.D. Lathia, J. Gallagher, J.M. Heddleston, J. Wang, C.E. Eyler, J. Macswords, Q. Wu, A. Vasanji, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich Integrin alpha 6 regulates glioblastoma stem cells Cell Stem Cell 6 2010 421 432
24. T.I. Lee, and R.A. Young Transcriptional regulation and its misregulation in disease Cell 152 2013 1237 1251
25. J. Lee, S. Kotliarova, Y. Kotliarov, A. Li, Q. Su, N.M. Donin, S. Pastorino, B.W. Purow, N. Christopher, and W. Zhang et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines Cancer Cell 9 2006 391 403
26. M.A. Lodato, C.W. Ng, J.A. Wamstad, A.W. Cheng, K.K. Thai, E. Fraenkel, R. Jaenisch, and L.A. Boyer SOX2 co-occupies distal enhancer elements with distinct POU factors in ESCs and NPCs to specify cell state PLoS Genet. 9 2013 e1003288
27. E. Lujan, S. Chanda, H. Ahlenius, T.C. Südhof, and M. Wernig Direct conversion of mouse fibroblasts to self-renewing, tripotent neural precursor cells Proc. Natl. Acad. Sci. USA 109 2012 2527 2532
28. S. Mehta, E. Huillard, S. Kesari, C.L. Maire, D. Golebiowski, E.P. Harrington, J.A. Alberta, M.F. Kane, M. Theisen, and K.L. Ligon et al. The central nervous system-restricted transcription factor Olig2 opposes p53 responses to genotoxic damage in neural progenitors and malignant glioma Cancer Cell 19 2011 359 371
29. E.M. Mendenhall, K.E. Williamson, D. Reyon, J.Y. Zou, O. Ram, J.K. Joung, and B.E. Bernstein Locus-specific editing of histone modifications at endogenous enhancers Nat. Biotechnol. 31 2013 1133 1136
30. T.S. Mikkelsen, M. Ku, D.B. Jaffe, B. Issac, E. Lieberman, G. Giannoukos, P. Alvarez, W. Brockman, T.K. Kim, and R.P. Koche et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells Nature 448 2007 553 560
31. S. Mimasu, N. Umezawa, S. Sato, T. Higuchi, T. Umehara, and S. Yokoyama Structurally designed trans-2-phenylcyclopropylamine derivatives potently inhibit histone demethylase LSD1/KDM1 Biochemistry 49 2010 6494 6503
32. S.A. Morris, and G.Q. Daley A blueprint for engineering cell fate: current technologies to reprogram cell identity Cell Res. 23 2013 33 48
33. A. Natsume, M. Ito, K. Katsushima, F. Ohka, A. Hatanaka, K. Shinjo, S. Sato, S. Takahashi, Y. Ishikawa, and I. Takeuchi et al. Chromatin regulator PRC2 is a key regulator of epigenetic plasticity in glioblastoma Cancer Res. 73 2013 4559 4570
34. S.H. Orkin, and K. Hochedlinger Chromatin connections to pluripotency and cellular reprogramming Cell 145 2011 835 850
35. Z.P. Pang, N. Yang, T. Vierbuchen, A. Ostermeier, D.R. Fuentes, T.Q. Yang, A. Citri, V. Sebastiano, S. Marro, T.C. Südhof, and M. Wernig Induction of human neuronal cells by defined transcription factors Nature 476 2011 220 223
36. S.G. Piccirillo, B.A. Reynolds, N. Zanetti, G. Lamorte, E. Binda, G. Broggi, H. Brem, A. Olivi, F. Dimeco, and A.L. Vescovi Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells Nature 444 2006 761 765
37. A. Rada-Iglesias, R. Bajpai, T. Swigut, S.A. Brugmann, R.A. Flynn, and J. Wysocka A unique chromatin signature uncovers early developmental enhancers in humans Nature 470 2011 279 283
38. E. Rheinbay, M.L. Suva, S.M. Gillespie, H. Wakimoto, A.P. Patel, M. Shahid, O. Oksuz, S.D. Rabkin, R.L. Martuza, and M.N. Rivera et al. An aberrant transcription factor network essential for Wnt signaling and stem cell maintenance in glioblastoma Cell Rep. 3 2013 1567 1579
39. A. Roesch, M. Fukunaga-Kalabis, E.C. Schmidt, S.E. Zabierowski, P.A. Brafford, A. Vultur, D. Basu, P. Gimotty, T. Vogt, and M. Herlyn A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth Cell 141 2010 583 594
40. Y.J. Shi, C. Matson, F. Lan, S. Iwase, T. Baba, and Y. Shi Regulation of LSD1 histone demethylase activity by its associated factors Mol. Cell 19 2005 857 864
41. S.K. Singh, C. Hawkins, I.D. Clarke, J.A. Squire, J. Bayani, T. Hide, R.M. Henkelman, M.D. Cusimano, and P.B. Dirks Identification of human brain tumour initiating cells Nature 432 2004 396 401
42. M.J. Son, K. Woolard, D.H. Nam, J. Lee, and H.A. Fine SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma Cell Stem Cell 4 2009 440 452
43. S.H. Stricker, A. Feber, P.G. Engström, H. Carén, K.M. Kurian, Y. Takashima, C. Watts, M. Way, P. Dirks, and P. Bertone et al. Widespread resetting of DNA methylation in glioblastoma-initiating cells suppresses malignant cellular behavior in a lineage-dependent manner Genes Dev. 27 2013 654 669
44. D. Sturm, H. Witt, V. Hovestadt, D.A. Khuong-Quang, D.T. Jones, C. Konermann, E. Pfaff, M. Tönjes, M. Sill, and S. Bender et al. Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma Cancer Cell 22 2012 425 437
45. M.L. Suvà, N. Riggi, and B.E. Bernstein Epigenetic reprogramming in cancer Science 339 2013 1567 1570
46. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676
47. R.G. Verhaak, K.A. Hoadley, E. Purdom, V. Wang, Y. Qi, M.D. Wilkerson, C.R. Miller, L. Ding, T. Golub, J.P. Mesirov Cancer Genome Atlas Research Network Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1 Cancer Cell 17 2010 98 110
48. T. Vierbuchen, and M. Wernig Direct lineage conversions: unnatural but useful? Nature Biotechnol. 29 2011 892 907
49. A. Visel, M.J. Blow, Z. Li, T. Zhang, J.A. Akiyama, A. Holt, I. Plajzer-Frick, M. Shoukry, C. Wright, and F. Chen et al. ChIP-seq accurately predicts tissue-specific activity of enhancers Nature 457 2009 854 858
50. J.E. Visvader, and G.J. Lindeman Cancer stem cells: current status and evolving complexities Cell Stem Cell 10 2012 717 728
51. H. Wakimoto, S. Kesari, C.J. Farrell, W.T. Curry Jr., C. Zaupa, M. Aghi, T. Kuroda, A. Stemmer-Rachamimov, K. Shah, and T.C. Liu et al. Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors Cancer Res. 69 2009 3472 3481
52. J.C. Wang, and J.E. Dick Cancer stem cells: lessons from leukemia Trends Cell Biol. 15 2005 494 501
53. P. Yang, Y. Wang, J. Chen, H. Li, L. Kang, Y. Zhang, S. Chen, B. Zhu, and S. Gao RCOR2 is a subunit of the LSD1 complex that regulates ESC property and substitutes for SOX2 in reprogramming somatic cells to pluripotency Stem Cells 29 2011 791 801
54. O.K. Yoon, and R.B. Brem Noncanonical transcript forms in yeast and their regulation during environmental stress RNA 16 2010 1256 1267
55. X. Zhang, F. Lu, J. Wang, F. Yin, Z. Xu, D. Qi, X. Wu, Y. Cao, W. Liang, Y. Liu, and H. Sun et al. Pluripotent stem cell protein Sox2 confers sensitivity to LSD1 inhibition in cancer cells Cell Rep. 5 2013 445 457
56. J. Zhu, M. Adli, J.Y. Zou, G. Verstappen, M. Coyne, X. Zhang, T. Durham, M. Miri, V. Deshpande, and P.L. De Jager et al. Genome-wide chromatin state transitions associated with developmental and environmental cues Cell 152 2013 642 654
57. S. Heinz, C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Mol. Cell 38 2010 576 589
58. A. Jolma, J. Yan, T. Whitington, J. Toivonen, K.R. Nitta, P. Rastas, E. Morgunova, M. Enge, M. Taipale, and G. Wei et al. DNA-binding specificities of human transcription factors Cell 152 2013 327 339
59. K.L. Meerbrey, G. Hu, J.D. Kessler, K. Roarty, M.Z. Li, J.E. Fang, J.I. Herschkowitz, A.E. Burrows, A. Ciccia, and T. Sun et al. The pINDUCER lentiviral toolkit for inducible RNA interference in vitro and in vivo Proc. Natl. Acad. Sci. USA 108 2011 3665 3670
60. M.D. Robinson, D.J. McCarthy, and G.K. Smyth edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Bioinformatics 26 2010 139 140
61. H. Thorvaldsdóttir, J.T. Robinson, and J.P. Mesirov Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration Brief. Bioinform. 14 2013 178 192
62. H. Wakimoto, G. Mohapatra, R. Kanai, W.T. Curry Jr., S. Yip, M. Nitta, A.P. Patel, Z.R. Barnard, A.O. Stemmer-Rachamimov, and D.N. Louis et al. Maintenance of primary tumor phenotype and genotype in glioblastoma stem cells Neuro-oncol. 14 2012 132 144
63. Y. Zhang, T. Liu, C.A. Meyer, J. Eeckhoute, D.S. Johnson, B.E. Bernstein, C. Nusbaum, R.M. Myers, M. Brown, W. Li, and X.S. Liu Model-based analysis of ChIP-Seq (MACS) Genome Biol. 9 2008 R137