Cancer Epigenetics: Tumor Heterogeneity, Plasticity of Stem-like States, and Drug Resistance
Open accessAbstract
The existence of subpopulations of cells in cancers with increased tumor-initiating capacities and self-renewal potential, often termed "cancer stem cells," is a much discussed and key area of cancer biology. Such cellular heterogeneity is very important because of its impact on therapy and especially states of treatment resistance. A major question is whether there is plasticity for evolution of these cell states during tumorigenesis that can involve movement between cell populations in a reversible fashion. In this review, we discuss the possible role of epigenetic abnormalities as well as genetic alterations in such dynamics and in the creation of cellular heterogeneity in cancers of all types.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The blood circulation system is a key component in metastasis because many malignant cells migrate as circulating cancer cells through blood vessels.
“The blood circulation system is also a key component in metastasis because many malignant cells migrate as circulating cancer cells through blood vessels [105].”
From Microfluidic modelling of the tumor microenvironment for anti-cancer drug development (2019) · cites this paper as [105]
The sections on tumor heterogeneity discuss differences between primary tumors and metastases, and the section on epigenetic alterations mentions migratory capabilities. Neither addresses whether malignant cells travel through blood vessels as circulating cancer cells or establishes the blood circulation system’s role in metastasis. Searches for circulating tumor cells, blood vessels, bloodstream, and vascular dissemination found no supporting passage. (LLM, conf=0.76)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
An integrated encyclopedia of DNA elements in the human genome
The ENCODE Project Consortium (2012) · Nature · doi:10.1038/nature11247 · Cited by 18,072 · see citing works
Epithelial-Mesenchymal Transitions in Development and Disease
Thiery, J. P., Acloque, H., Huang, R. Y. J., & Nieto, M. A. (2009) · Cell · doi:10.1016/j.cell.2009.11.007 · Cited by 9,931 · see citing works
Vogelstein, B., Papadopoulos, N., Velculescu, V. E., Zhou, S., Diaz, L. A., & Kinzler, K. W. (2013) · Science · doi:10.1126/science.1235122 · Cited by 7,863 · see citing works
Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing
Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1113205 · Cited by 7,774 · see citing works
Nowell, P. C. (1976) · Science · doi:10.1126/science.959840 · Cited by 6,471 · see citing works
An Integrated Genomic Analysis of Human Glioblastoma Multiforme
Parsons, D. W., Jones, S., Zhang, X., Lin, J. C.-H., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Siu, I.-M., Gallia, G. L., et al. (2008) · Science · doi:10.1126/science.1164382 · Cited by 5,857 · see citing works
<i>IDH1</i> and <i>IDH2</i> Mutations in Gliomas
Yan, H., Parsons, D. W., Jin, G., McLendon, R., Rasheed, B. A., Yuan, W., Kos, I., Batinic-Haberle, I., Jones, S., Riggins, G. J., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0808710 · Cited by 5,847 · see citing works
A bivalent chromatin structure marks key developmental genes in embryonic stem cells
Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., et al. (2006) · Cell · doi:10.1016/j.cell.2006.02.041 · Cited by 5,361 · see citing works
Cancer-associated IDH1 mutations produce 2-hydroxyglutarate
Dang, L., White, D. W., Gross, S., Bennett, B. D., Bittinger, M. A., Driggers, E. M., Fantin, V. R., Jang, H. G., Jin, S., Keenan, M. C., et al. (2009) · Nature · doi:10.1038/nature08617 · Cited by 4,154 · see citing works
Stratton, M. R., Campbell, P. J., & Futreal, P. A. (2009) · Nature · doi:10.1038/nature07943 · Cited by 3,458 · see citing works
Cancer epigenetics: from mechanism to therapy
Dawson, M. A., & Kouzarides, T. (2012) · Cell · doi:10.1016/j.cell.2012.06.013 · Cited by 3,203 · see citing works
Greaves, M., & Maley, C. C. (2012) · Nature · doi:10.1038/nature10762 · Cited by 3,162 · see citing works
Bird, A. (2007) · Nature · doi:10.1038/nature05913 · Cited by 3,011 · see citing works
Xu, W., Yang, H., Liu, Y., Yang, Y., Wang, P., Kim, S.-H., Ito, S., Yang, C., Wang, P., Xiao, M.-T., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2010.12.014 · Cited by 2,875 · see citing works
A decade of exploring the cancer epigenome—biological and translational implications
Baylin, S. B., & Jones, P. A. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3130 · Cited by 2,871 · see citing works
Self-citationA Chromatin-Mediated Reversible Drug-Tolerant State in Cancer Cell Subpopulations
Sharma, S. V., Lee, D. Y., Li, B., Quinlan, M. P., Takahashi, F., Maheswaran, S., McDermott, U., Azizian, N., Zou, L., Fischbach, M. A., et al. (2010) · Cell · doi:10.1016/j.cell.2010.02.027 · Cited by 2,770 · see citing works
Figueroa, M. E., Abdel-Wahab, O., Lu, C., Ward, P. S., Patel, J., Shih, A., Li, Y., Bhagwat, N., Vasanthakumar, A., Fernandez, H. F., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2010.11.015 · Cited by 2,766 · see citing works
Tumour evolution inferred by single-cell sequencing
Navin, N., Kendall, J., Troge, J., Andrews, P., Rodgers, L., McIndoo, J., Cook, K., Stepansky, A., Levy, D., Esposito, D., et al. (2011) · Nature · doi:10.1038/nature09807 · Cited by 2,598 · see citing works
CpG island methylator phenotype in colorectal cancer
Toyota, M., Ahuja, N., Ohe-Toyota, M., Herman, J. G., Baylin, S. B., & Issa, J. J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.15.8681 · Cited by 2,506 · see citing works
Self-citationDistant metastasis occurs late during the genetic evolution of pancreatic cancer
Yachida, S., Jones, S., Bozic, I., Antal, T., Leary, R., Fu, B., Kamiyama, M., Hruban, R. H., Eshleman, J. R., Nowak, M. A., et al. (2010) · Nature · doi:10.1038/nature09515 · Cited by 2,502 · see citing works
Tumour heterogeneity and cancer cell plasticity
Meacham, C., & Morrison, S. (2013) · Nature · doi:10.1038/nature12624 · Cited by 2,350 · see citing works
Identification of a CpG Island Methylator Phenotype that Defines a Distinct Subgroup of Glioma
Noushmehr, H., Weisenberger, D. J., Diefes, K., Phillips, H. S., Pujara, K., Berman, B. P., Pan, F., Pelloski, C. E., Sulman, E. P., Bhat, K. P., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2010.03.017 · Cited by 2,337 · see citing works
Self-citationWeisenberger, D. J., Siegmund, K. D., Campan, M., Young, J. P., Long, T. I., Faasse, M. A., Kang, G. H., Widschwendter, M., Weener, D., Buchanan, D. D., et al. (2006) · Nature Genetics · doi:10.1038/ng1834 · Cited by 1,990 · see citing works
IDH mutation impairs histone demethylation and results in a block to cell differentiation
Lu, C., Ward, P. S., Kapoor, G. S., Rohle, D., Turcan, S., Abdel-Wahab, O., Edwards, C. R., Khanin, R., Figueroa, M. E., Melnick, A., et al. (2012) · Nature · doi:10.1038/nature10860 · Cited by 1,985 · see citing works
IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype
Turcan, S., Rohle, D., Goenka, A., Walsh, L. A., Fang, F., Yilmaz, E., Campos, C., Fabius, A. W. M., Lu, C., Ward, P. S., et al. (2012) · Nature · doi:10.1038/nature10866 · Cited by 1,974 · see citing works
Conserved role of intragenic DNA methylation in regulating alternative promoters
Maunakea, A. K., Nagarajan, R. P., Bilenky, M., Ballinger, T. J., D’Souza, C., Fouse, S. D., Johnson, B. E., Hong, C., Nielsen, C., Zhao, Y., et al. (2010) · Nature · doi:10.1038/nature09165 · Cited by 1,743 · see citing works
Mutation selection and the natural history of cancer
Cairns, J. (1975) · Nature · doi:10.1038/255197a0 · Cited by 1,592 · see citing works
Stochastic State Transitions Give Rise to Phenotypic Equilibrium in Populations of Cancer Cells
Gupta, P. B., Fillmore, C. M., Jiang, G., Shapira, S. D., Tao, K., Kuperwasser, C., & Lander, E. S. (2011) · Cell · doi:10.1016/j.cell.2011.07.026 · Cited by 1,475 · see citing works
Chromatin signatures of pluripotent cell lines
Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jørgensen, H. F., John, R. M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M., et al. (2006) · Nature Cell Biology · doi:10.1038/ncb1403 · Cited by 1,357 · see citing works
Inhibition of PRC2 Activity by a Gain-of-Function H3 Mutation Found in Pediatric Glioblastoma
Lewis, P. W., Müller, M. M., Koletsky, M. S., Cordero, F., Lin, S., Banaszynski, L. A., Garcia, B. A., Muir, T. W., Becher, O. J., & Allis, C. D. (2013) · Science · doi:10.1126/science.1232245 · Cited by 1,345 · see citing works
Lessons from the Cancer Genome
Garraway, L. A., & Lander, E. S. (2013) · Cell · doi:10.1016/j.cell.2013.03.002 · Cited by 1,322 · see citing works
Schlesinger, Y., Straussman, R., Keshet, I., Farkash, S., Hecht, M., Zimmerman, J., Eden, E., Yakhini, Z., Ben-Shushan, E., Reubinoff, B. E., et al. (2007) · Nature Genetics · doi:10.1038/ng1950 · Cited by 1,226 · see citing works
Braakhuis, B. J. M., Tabor, M. P., Kummer, J. A., Leemans, C. R., & Brakenhoff, R. H. (2003) · PubMed · Cited by 1,208 · see citing works
Cancer stem cells: an evolving concept
Nguyen, L. V., Vanner, R., Dirks, P., & Eaves, C. (2012) · Nature Reviews. Cancer · doi:10.1038/nrc3184 · Cited by 1,191 · see citing works
Cancer Genetics and Epigenetics: Two Sides of the Same Coin?
You, J. S., & Jones, P. A. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.06.008 · Cited by 1,163 · see citing works
Roesch, A., Fukunaga‐Kalabis, M., Schmidt, E. C., Zabierowski, S. E., Brafford, P. A., Vultur, A., Basu, D., Gimotty, P. A., VOGT, T. M., & Herlyn, M. (2010) · Cell · doi:10.1016/j.cell.2010.04.020 · Cited by 1,162 · see citing works
The epigenetics of epithelial-mesenchymal plasticity in cancer
Tam, W. L., & Weinberg, R. A. (2013) · Nature Medicine · doi:10.1038/nm.3336 · Cited by 1,159 · see citing works
Epigenetic stem cell signature in cancer
Widschwendter, M., Fiegl, H., Egle, D., Mueller-Holzner, E., Spizzo, G., Marth, C., Weisenberger, D. J., Campan, M., Young, J., Jacobs, I., et al. (2007) · Nature Genetics · doi:10.1038/ng1941 · Cited by 1,143 · see citing works
Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state
Chaffer, C. L., Brueckmann, I., Scheel, C., Kaestli, A. J., Wiggins, P. A., Rodrigues, L. O., Brooks, M. W., Reinhardt, F., Su, Y., Polyák, K., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102454108 · Cited by 1,137 · see citing works
Ohm, J. E., McGarvey, K. M., Yu, X., Cheng, L., Schuebel, K. E., Cope, L., Mohammad, H. P., Chen, W., Daniel, V. C., Yu, W., et al. (2007) · Nature Genetics · doi:10.1038/ng1972 · Cited by 1,130 · see citing works
Self-citationWaddington, C. H. (2012) · International Journal of Epidemiology · doi:10.1093/ije/dyr184 · Cited by 1,082 · see citing works
Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer
Suzuki, H., Watkins, D. N., Jair, K.-W., Schuebel, K. E., Markowitz, S. D., Chen, W. D., Pretlow, T. P., Yang, B., Akiyama, Y., van Engeland, M., et al. (2004) · Nature Genetics · doi:10.1038/ng1330 · Cited by 1,070 · see citing works
Self-citationPreexistence and clonal selection of MET amplification in EGFR mutant NSCLC
Turke, A. B., Zejnullahu, K., Wu, Y.-L., Song, Y., Dias-Santagata, D., Lifshits, E., Toschi, L., Rogers, A., Mok, T., Sequist, L., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.11.022 · Cited by 1,059 · see citing works
Increased methylation variation in epigenetic domains across cancer types
Hansen, K. D., Timp, W., Bravo, H. C., Sabunciyan, S., Langmead, B., McDonald, O. G., Wen, B., Wu, H., Liu, Y., Diep, D. H., et al. (2011) · Nature Genetics · doi:10.1038/ng.865 · Cited by 1,053 · see citing works
Amary, M. F., Bacsi, K., Maggiani, F., Damato, S., Halai, D., Berisha, F., Pollock, R., O'Donnell, P., Grigoriadis, A., Diss, T., et al. (2011) · The Journal of Pathology · doi:10.1002/path.2913 · Cited by 1,023 · see citing works
Belinsky, S. A., Nikula, K. J., Palmisano, W. A., Michels, R., Saccomanno, G., Gabrielson, E. W., Baylin, S. B., & Herman, J. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11891 · Cited by 957 · see citing works
Self-citationJordan, C., Guzman, M., & Noble, M. (2006) · New England Journal of Medicine · doi:10.1056/nejmra061808 · Cited by 948 · see citing works
Interplay between the Cancer Genome and Epigenome
Shen, H., & Laird, P. W. (2013) · Cell · doi:10.1016/j.cell.2013.03.008 · Cited by 912 · see citing works
Unravelling cancer stem cell potential
Beck, B., & Blanpain, C. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3597 · Cited by 895 · see citing works
Transcriptional regulation by Polycomb group proteins
Di Croce, L., & Helin, K. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2669 · Cited by 864 · see citing works
Comparative lesion sequencing provides insights into tumor evolution
Jones, S., Chen, W.-D. D., Parmigiani, G., Diehl, F., Beerenwinkel, N., Tibor Antal, A., Traulsen, A., Nowak, M. A., Siegel, C., Velculescu, V. E., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712345105 · Cited by 817 · see citing works
Genomic Analysis of the Clonal Origins of Relapsed Acute Lymphoblastic Leukemia
Mullighan, C. G., Phillips, L. A., Su, X., Ma, J., Miller, C. B., Shurtleff, S. A., & Downing, J. R. (2008) · Science · doi:10.1126/science.1164266 · Cited by 806 · see citing works
Genetic variegation of clonal architecture and propagating cells in leukaemia
Anderson, K., Lutz, C., van Delft, F. W., Bateman, C. M., Guo, Y., Colman, S., Kempski, H. M., Moorman, A. V., Titley, I., Swansbury, J. G., et al. (2010) · Nature · doi:10.1038/nature09650 · Cited by 803 · see citing works
Juergens, R. A., Wrangle, J. M., Vendetti, F. P., Murphy, S. C., Zhao, M., Coleman, B., Sebree, R., Rodgers, K., Hooker, C. M., Franco, N. C., et al. (2011) · Cancer Discovery · doi:10.1158/2159-8290.cd-11-0214 · Cited by 686 · see citing works
Self-citationBerman, B. P., Weisenberger, D. J., Aman, J. F., Hinoue, T., Ramjan, Z., Liu, Y., Noushmehr, H., Lange, C. P. E., van Dijk, C. M., Tollenaar, R. A. E. M., et al. (2012) · Nature Genetics · doi:10.1038/ng.969 · Cited by 660 · see citing works
Aging and DNA methylation in colorectal mucosa and cancer.
Ahuja, N., Li, Q., MOHAN, A. L., Baylin, S. B., & Issa, J. J. (1998) · PubMed · Cited by 618 · see citing works
Self-citationHon, G. C., Hawkins, R. D., Caballero, O. L., Lo, C., Lister, R., Pelizzola, M., Valsesia, A., Ye, Z., Kuan, S., Edsall, L. E., et al. (2012) · Genome Research · doi:10.1101/gr.125872.111 · Cited by 583 · see citing works
O’Hagan, H. M., Wang, W., Sen, S., Shields, C. E. D., Lee, S. S., Zhang, Y. W., Clements, E. G., Cai, Y., Neste, L. V., Easwaran, H., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.09.012 · Cited by 569 · see citing works
Self-citationA chemical probe selectively inhibits G9a and GLP methyltransferase activity in cells
Vedadi, M., Baršytė-Lovejoy, D., Liu, F., Rival‐Gervier, S., Allali‐Hassani, A., Labrie, V., Wigle, T. J., DiMaggio, P. A., Wasney, G. A., Siarheyeva, A., et al. (2011) · Nature Chemical Biology · doi:10.1038/nchembio.599 · Cited by 547 · see citing works
DeVita, Hellman, and Rosenberg's cancer : principles & practice of oncology
DeVita, V. T., Lawrence, T. S., & Rosenberg, S. A. (2011) · Cited by 539 · see citing works
Analysis of adenomatous polyposis coli promoter hypermethylation in human cancer.
Esteller, M., Sparks, A. B., Toyota, M., et al. (2000) · PubMed · Cited by 526 · see citing works
IDH1(R132H) mutation increases murine haematopoietic progenitors and alters epigenetics
Sasaki, M., Knobbe, C. B., Munger, J. C., Lind, E. F., Brenner, D., Brüstle, A., Harris, I. S., Holmes, R., Wakeham, A., Haight, J., et al. (2012) · Nature · doi:10.1038/nature11323 · Cited by 513 · see citing works
MGMT Promoter Methylation and Field Defect in Sporadic Colorectal Cancer
Shen, L., Kondo, Y., Rosner, G. L., Xiao, L., Hernandez, N., Vilaythong, J. N., Houlihan, P., Krouse, R. S., Prasad, A. R., Einspahr, J. G., et al. (2005) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dji275 · Cited by 492 · see citing works
Asymmetrically Modified Nucleosomes
Voigt, P., LeRoy, G., Drury, W. J., Zee, B. M., Son, J., Beck, D. B., Young, N. L., Garcia, B. A., & Reinberg, D. (2012) · Cell · doi:10.1016/j.cell.2012.09.002 · Cited by 457 · see citing works
Oncogenic Isocitrate Dehydrogenase Mutations: Mechanisms, Models, and Clinical Opportunities
Cairns, R. A., & Mak, T. W. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0083 · Cited by 452 · see citing works
Cell Plasticity and Heterogeneity in Cancer
Marjanovic, N. D., Weinberg, R. A., & Chaffer, C. L. (2012) · Clinical Chemistry · doi:10.1373/clinchem.2012.184655 · Cited by 399 · see citing works
Investigating stem cells in human colon by using methylation patterns
Yatabe, Y., Tavaré, S., & Shibata, D. K. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191225998 · Cited by 368 · see citing works
The future of epigenetic therapy in solid tumours—lessons from the past
Azad, N. S., Zahnow, C. A., Rudin, C. M., & Baylin, S. B. (2013) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2013.42 · Cited by 338 · see citing works
Self-citationOn the use of the word ‘epigenetic’
Ptashne, M. (2007) · Current Biology · doi:10.1016/j.cub.2007.02.030 · Cited by 335 · see citing works
Regulating RNA polymerase pausing and transcription elongation in embryonic stem cellsPreprint
Min, I. M., Waterfall, J. J., Core, L. J., Munroe, R. J., Schimenti, J. C., & Lis, J. T. (2011) · Genes & Development · doi:10.1101/gad.2005511 · Cited by 297 · see citing works
A DNA hypermethylation module for the stem/progenitor cell signature of cancerPreprint
Easwaran, H., Johnstone, S. E., Neste, L. V., Ohm, J. E., Mosbruger, T., Wang, Q., Aryee, M. J., Joyce, P., Ahuja, N., Weisenberger, D., et al. (2012) · Genome Research · doi:10.1101/gr.131169.111 · Cited by 293 · see citing works
Self-citationDNA Methylation Screening Identifies Driver Epigenetic Events of Cancer Cell Survival
Carvalho, D. D. D., Sharma, S., You, J. S., Su, S., Taberlay, P. C., Kelly, T. K., Yang, X., Liang, G., & Jones, P. A. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.03.045 · Cited by 282 · see citing works
Aryee, M. J., Liu, W., Engelmann, J. C., Nuhn, P., Gurel, M., Haffner, M. C., Esopi, D., Irizarry, R. A., Getzenberg, R. H., Nelson, W. G., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005211 · Cited by 277 · see citing works
Brookes, E., de Santiago, I., Hebenstreit, D., Morris, K. J., Carroll, T., Xie, S. Q., Stock, J. K., Heidemann, M., Eick, D., Nozaki, N., et al. (2012) · Cell stem cell · doi:10.1016/j.stem.2011.12.017 · Cited by 276 · see citing works
Liu, F., Killian, J. K., Yang, M., Walker, R. L., Hong, J. A., Zhang, M., Davis, S. R., Zhang, Y., Hussain, M., Shi, X., et al. (2010) · Oncogene · doi:10.1038/onc.2010.129 · Cited by 273 · see citing works
Rheinbay, E., Suvà, M. L., Gillespie, S. M., Wakimoto, H., Patel, A. P., Shahid, M., Oksuz, O., Rabkin, S. D., Martuza, R. L., Rivera, M. N., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.04.021 · Cited by 268 · see citing works
Breast Cancer Methylomes Establish an Epigenomic Foundation for Metastasis
Fang, F., Turcan, Ş., Rimner, A., Kaufman, A., Giri, D. D., Morris, L. G. T., Shen, R., Seshan, V., Mo, Q., Heguy, A., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3001875 · Cited by 267 · see citing works
Self-citationEpigenetic Field for Cancerization
Ushijima, T. (2007) · BMB Reports · doi:10.5483/bmbrep.2007.40.2.142 · Cited by 251 · see citing works
Chemical probes for histone-modifying enzymes
Cole, P. A. (2008) · Nature Chemical Biology · doi:10.1038/nchembio.111 · Cited by 249 · see citing works
Turcan, S., Fabius, A. W. M., Borodovsky, A., Pedraza, A., Brennan, C., Huse, J., Viale, A., Riggins, G. J., & Chan, T. A. (2013) · Oncotarget · doi:10.18632/oncotarget.1412 · Cited by 240 · see citing works
Bestor, T. H. (1990) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1990.0002 · Cited by 231 · see citing works
Molecular mechanisms of acquired resistance to tyrosine kinase targeted therapy
Sierra, J. R., Cepero, V., & Giordano, S. (2010) · Molecular Cancer · doi:10.1186/1476-4598-9-75 · Cited by 230 · see citing works
Mutator activity induced by microRNA-155 ( miR-155 ) links inflammation and cancer
Tili, E., Michaille, J., Wernicke, D., Alder, H., Costinean, S., Volinia, S., & Croce, C. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101795108 · Cited by 227 · see citing works
Methylation of Polycomb Target Genes in Intestinal Cancer Is Mediated by Inflammation
Hahn, M. A., Hahn, T., Lee, D.-H., Esworthy, R. S., Kim, B.-W., Riggs, A. D., Chu, F., & Pfeifer, G. P. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-1957 · Cited by 212 · see citing works
Lo, P., & Sukumar, S. V. (2008) · Pharmacogenomics · doi:10.2217/14622416.9.12.1879 · Cited by 183 · see citing works
Intragenic DNA methylation: implications of this epigenetic mechanism for cancer research
Shenker, N. S., & Flanagan, J. M. (2011) · British Journal of Cancer · doi:10.1038/bjc.2011.550 · Cited by 180 · see citing works
Induction of sarcomas by mutant IDH2Preprint
Lü, C., Venneti, S., Akalin, A., Fang, F., Ward, P. S., Dematteo, R. G., Intlekofer, A. M., Chen, C., Ye, J., Hameed, M., et al. (2013) · Genes & Development · doi:10.1101/gad.226753.113 · Cited by 157 · see citing works
Borodovsky, A., Salmasi, V., Turcan, Ş., Fabius, A. W. M., Baía, G. S., Eberhart, C. G., WEINGART, J. D., Gallia, G. L., Baylin, S. B., Chan, T. A.-T., et al. (2013) · Oncotarget · doi:10.18632/oncotarget.1408 · Cited by 156 · see citing works
Self-citationEvidence for field cancerization of the prostate
Nonn, L., Ananthanarayanan, V., & Gann, P. H. (2009) · The Prostate · doi:10.1002/pros.20983 · Cited by 150 · see citing works
Resistance mechanisms to cancer chemotherapy
Redmond, K. M. (2008) · Frontiers in bioscience · doi:10.2741/3070 · Cited by 150 · see citing works
Abnormal DNA Methylation of CD133 in Colorectal and Glioblastoma Tumors
Yi, J. M., Tsai, H.-C., Glöckner, S. C., Lin, S. H., Ohm, J. E., Easwaran, H., James, C. D., Costello, J., Riggins, G. J., Eberhart, C. G., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-6208 · Cited by 144 · see citing works
Self-citationIdentification of higher-order functional domains in the human ENCODE regionsPreprint
Thurman, R. E., Day, N., Noble, W. S., & Stamatoyannopoulos, J. A. (2007) · Genome Research · doi:10.1101/gr.6081407 · Cited by 134 · see citing works
Promoter Hypermethylation of Hallmark Cancer Genes in Atypical Adenomatous Hyperplasia of the Lung
Licchesi, J. D. F., Westra, W. H., Hooker, C. M., & Herman, J. G. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-2033 · Cited by 133 · see citing works
Yang, J., Luo, H., Li, Y., Li, J., Cai, Z., Su, X., Dai, D., Du, W., Chen, T., & Chen, M. (2011) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-011-9286-1 · Cited by 101 · see citing works
Age-related epigenetic drift in the pathogenesis of MDS and AMLPreprint
Maegawa, S., Gough, S. M., Watanabe‐Okochi, N., Lu, Y., Zhang, N., Castoro, R. J., Estecio, M. R., Jelı́nek, J., Liang, S., Kitamura, T., et al. (2014) · Genome Research · doi:10.1101/gr.157529.113 · Cited by 82 · see citing works
Quantitative, spatial resolution of the epigenetic field effect in prostate cancer
Mehrotra, J., Varde, S. A., Wang, H., et al. (2007) · The Prostate · doi:10.1002/pros.20675 · Cited by 79 · see citing works
Swapping Function of Two Chromatin Remodeling Complexes
Fan, H.-Y., Trotter, K. W., Archer, T., & Kingston, R. E. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.02.024 · Cited by 69 · see citing works
Induction of Epigenetic Alterations by Chronic Inflammation and Its Significance on Carcinogenesis
Niwa, T., & Ushijima, T. (2010) · Advances in genetics · doi:10.1016/b978-0-12-380864-6.00002-x · Cited by 59 · see citing works
Generation of bivalent chromatin domains during cell fate decisions
Gobbi, M. D., Garrick, D., Lynch, M., Vernimmen, D., Hughes, J. R., Goardon, N., Luc, S., Lower, K. M., Sloane-Stanley, J. A., Pina, C., et al. (2011) · Epigenetics & Chromatin · doi:10.1186/1756-8935-4-9 · Cited by 57 · see citing works
Alterations of histone modifications by cobalt compounds
Li, Q., Ke, Q., & Costa, M. (2009) · Carcinogenesis · doi:10.1093/carcin/bgp088 · Cited by 45 · see citing works
The epigenome of AML stem and progenitor cells
Yamazaki, J., Estecio, M. R., Lu, Y., Long, H., Malouf, G. G., Graber, D., Huo, Y., Ramagli, L. S., Liang, S., Kornblau, S. M., et al. (2012) · Epigenetics · doi:10.4161/epi.23243 · Cited by 41 · see citing works
Epigenetic alterations in RASSF1A in human aberrant crypt foci
Greenspan, E. J., Jablonski, M., Rajan, T. V., et al. (2006) · Carcinogenesis · doi:10.1093/carcin/bgi373 · Cited by 31 · see citing works
Nucleosome dynamics and epigenetic stability
Korber, P., & Becker, P. B. (2010) · Essays in Biochemistry · doi:10.1042/bse0480063 · Cited by 26 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [2]Allis CD Jenuwein T Reinberg D 2008 Epigenetics 1st Cold Spring Harbor Laboratory Press
Cited by
Sorted by citations
EMT, CSCs, and drug resistance: the mechanistic link and clinical implications
Shibue, T., & Weinberg, R. A. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.44 · Cited by 2,539 · see citing works
Epigenetic plasticity and the hallmarks of cancer
Flavahan, W. A., Gaskell, E., & Bernstein, B. E. (2017) · Science · doi:10.1126/science.aal2380 · Cited by 1,340 · see citing works
Targeting epigenetic regulators for cancer therapy: mechanisms and advances in clinical trials
Cheng, Y., He, C., Wang, M., Ma, X., Mo, F., Yang, S., Han, J., & Wei, X. (2019) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-019-0095-0 · Cited by 1,097 · see citing works
DNA Methylation in Cancer and Aging
Klutstein, M., Nejman, D., Greenfield, R., & Cedar, H. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-3278 · Cited by 810 · see citing works
Mechanisms and Implications of Metabolic Heterogeneity in Cancer
Kim, J., & DeBerardinis, R. J. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.08.013 · Cited by 606 · see citing works
Barkley, D., Moncada, R., Pour, M., Liberman, D. A., Dryg, I., Werba, G., Wang, W., Baron, M., Rao, A., Xia, B., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01141-9 · Cited by 532 · see citing works
Adaptive Chromatin Remodeling Drives Glioblastoma Stem Cell Plasticity and Drug Tolerance
Liau, B. B., Sievers, C., Donohue, L. K., Gillespie, S. M., Flavahan, W. A., Miller, T. E., Venteicher, A. S., Hebert, C. H., Carey, C. D., Rodig, S. J., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2016.11.003 · Cited by 535 · see citing works
The emerging role of epigenetic therapeutics in immuno-oncology
Topper, M. J., Vaz, M., Marrone, K. A., Brahmer, J. R., & Baylin, S. B. (2020) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-019-0266-5 · Cited by 433 · see citing works
Self-citationPoised epigenetic states and acquired drug resistance in cancer
Brown, R., Curry, E., Magnani, L., Wilhelm-Benartzi, C. S., & Borley, J. (2014) · Nature Reviews Cancer · doi:10.1038/nrc3819 · Cited by 301 · see citing works
Lee, H.-S. (2015) · Nutrients · doi:10.3390/nu7115467 · Cited by 236 · see citing works
Microfluidic modelling of the tumor microenvironment for anti-cancer drug development
Shang, M., Soon, R. H., Lim, C. T., Khoo, B. L., & Han, J. (2019) · Lab on a Chip · doi:10.1039/c8lc00970h · Cited by 227 · see citing works
The combination of disulfiram and copper for cancer treatment
Li, H., Wang, J., Wu, C., Wang, L., Chen, Z.-S., & Cui, W. (2020) · Drug Discovery Today · doi:10.1016/j.drudis.2020.04.003 · Cited by 185 · see citing works
Epigenetic modifications: Key players in cancer heterogeneity and drug resistance
Sadida, H. Q., Abdulla, A., Marzooqi, S. A., Hashem, S., Macha, M. A., Akil, A. S. A.-S., & Bhat, A. A. (2024) · Translational Oncology · doi:10.1016/j.tranon.2023.101821 · Cited by 151 · see citing works
DNA Methylation Patterns Separate Senescence from Transformation Potential and Indicate Cancer Risk
Xie, W., Kagiampakis, I., Pan, L., Zhang, Y. W., Murphy, L., Tao, Y., Kong, X., Kang, B., Xia, L., Carvalho, F. L. F., et al. (2018) · Cancer Cell · doi:10.1016/j.ccell.2018.01.008 · Cited by 122 · see citing works
Self-citationJia, D., Li, L., Andrew, S., Allan, D., Li, X., Lee, J., Ji, G., Yao, Z., Gadde, S., Figeys, D., et al. (2017) · Cell Death & Disease · doi:10.1038/cddis.2017.319 · Cited by 105 · see citing works
Next-generation DNA damage sequencing
Mingard, C., Wu, J., McKeague, M., & Sturla, S. J. (2020) · Chemical Society Reviews · doi:10.1039/d0cs00647e · Cited by 92 · see citing works
Cell signaling and cancer: a mechanistic insight into drug resistance
Panda, M., & Biswal, B. K. (2019) · Molecular Biology Reports · doi:10.1007/s11033-019-04958-6 · Cited by 89 · see citing works
Chang, Z., Billmyre, R. B., Lee, S. C., & Heitman, J. (2019) · PLOS Genetics · doi:10.1371/journal.pgen.1007957 · Cited by 72 · see citing works
Deciphering mechanisms of brain metastasis in melanoma - the gist of the matter
Redmer, T. (2018) · Molecular Cancer · doi:10.1186/s12943-018-0854-5 · Cited by 67 · see citing works
Suphavilai, C., Chia, S., Sharma, A., Tu, L., Da Silva, R. P., Mongia, A., DasGupta, R., & Nagarajan, N. (2021) · Genome Medicine · doi:10.1186/s13073-021-01000-y · Cited by 58 · see citing works
- Authors
- Easwaran, H., Tsai, H.-C., & Baylin, S. B.
- Affiliations
- Johns Hopkins University (US)
- Corresponding author
- Baylin, Stephen B.
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2014-06
- Volume
- 54
- Issue
- 5
- Pages
- 716-727
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC4103691
- OpenAlex
- W2064442490
- Cited by
- 915
- References
- 103
- Citations by year
- 2026: 33 · 2025: 44 · 2024: 62 · 2023: 61 · 2022: 94 · 2021: 104 · 2020: 97 · 2019: 105 · 2018: 77 · 2017: 73 · 2016: 68 · 2015: 80 · 2014: 16
- FWCI
- 8.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Heart, Lung, and Blood Institute (U01HL099775, HL099775)
- National Cancer Institute (R01CA043318, CA 043318, P30CA006973)
- National Institute of Environmental Health Sciences (R01ES011858, ES011858)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Keywords
- cancer epigenetics, tumor heterogeneity, cancer stem cells, drug resistance, epigenetic abnormalities, self-renewal, genetic alterations, carcinogenesis
- MeSH terms
- Animals, Humans, Neoplasms, Neoplastic Stem Cells, Gene Expression Regulation, Neoplastic, Drug Resistance, Neoplasm, Epigenesis, Genetic, Carcinogenesis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
