484
Views
3
CrossRef citations to date
0
Altmetric
Research Paper

Hexavalent chromium promotes differential binding of CTCF to its cognate sites in Euchromatin

ORCID Icon, , , , ORCID Icon & ORCID Icon
Pages 1361-1376 | Received 11 Aug 2020, Accepted 10 Dec 2020, Published online: 07 Jan 2021

References

  • Wilbur  S, Abadin H, Fay M, et al. Toxicological profile for chromium. 2012.
  • Deng Y, Wang M, Tian T, et al. The effect of hexavalent chromium on the incidence and mortality of human cancers: a meta-analysis based on published epidemiological cohort studies. Front Oncol. 2019;9:24.
  • Howard J Criteria for a recommended standard occupational exposure to hexavalent chromium DHHS (NIOSH) publication No. 2013–128. 2013.
  • Thompson  CM, Proctor DM, Haes LC, et al. Investigation of the mode of action underlying the tumorigenic response induced in B6C3F1 mice exposed orally to hexavalent chromium. Toxicol Sci. 2011;123:58–70.
  • Sanchez-Martin  FJ, Fan Y, Carreira V, et al. Long-term coexposure to hexavalent chromium and B[a]P causes tissue-specific differential biological effects in liver and gastrointestinal tract of mice. Toxicol Sci. 2015;146:52–64.
  • Thompson  CM, Seiter J, Chappell MA, et al. Synchrotron-based imaging of chromium and γ -H2AX immunostaining in the duodenum following repeated exposure to Cr(VI) in drinking water. Toxicol Sci. 2015;143:16–25.
  • Sun H, Brocato J, Costa M. Oral chromium exposure and toxicity. Curr Environ Health Rep. 2015;2:295–303.
  • De Flora  S, Camoirano A, Bagnasco M, et al. Estimates of the chromium(VI) reducing capacity in human body compartments as a mechanism for attenuating its potential toxicity and carcinogenicity. Carcinogenesis. 1997;18:531–537.
  • Zhitkovich A. Chromium in drinking water: sources, metabolism, and cancer risks. Chem Res Toxicol. 2011;24:1617–1629.
  • Zhitkovich A. Importance of chromium-DNA adducts in mutagenicity and toxicity of chromium(VI). Chem Res Toxicol. 2005;18:3–11.
  • Reynolds, M, Stoddard L, Bespalov I, et al. Ascorbate acts as a highly potent inducer of chromate mutagenesis and clastogenesis: linkage to DNA breaks in G2 phase by mismatch repair. Nucleic Acids Res. 2006;35(2):465–476.
  • Ha L, Ceryak S, Patierno SR. Chromium(VI) activates ataxia telangiectasia mutated (ATM) protein requirement of ATM for both apoptosis and recovery from terminal growth arrest. J Biol Chem. 2003;278:17885–17894.
  • Ha L, Ceryak S, Patierno SR. Generation of S phase-dependent DNA double-strand breaks by Cr(VI) exposure: involvement of ATM in Cr(VI) induction of γ -H2AX. Carcinogenesis. 2004;25:2265–2274.
  • Holmes  AL, Wise SS, Sandwick SJ, et al. Chronic exposure to lead chromate causes centrosome abnormalities and aneuploidy in human lung cells. Cancer Res. 2006;66:4041–4048.
  • Chen L, Ovesen JL, Puga A, et al. Distinct contributions of JNK and p38 to chromium cytotoxicity and inhibition of murine embryonic stem cell differentiation. Environ Health Perspect. 2009;117:1124–1130.
  • Kim G, Yurkow EJ. Chromium induces a persistent activation of mitogen-activated protein kinases by a redox-sensitive mechanism in H4 rat hepatoma cells. Cancer Res. 1996;56:2045–2051.
  • Chen F, Ye J, Zhang X, et al. One-electron reduction of chromium(VI) by γ -lipoic acid and related hydroxyl radical generation, dG hydroxylation and nuclear transcription factor- ĸ B activation. Arch Biochem Biophys. 1997;338:165–172.
  • Holmes  AL, Wise SS, Pelsue SC, et al. Chronic exposure to zinc chromate induces centrosome amplification and spindle assembly checkpoint bypass in human lung fibroblasts. Chem Res Toxicol. 2010;23:386–395.
  • Qin  Q, Xie H, Wise SS, et al. Homologous recombination repair signaling in chemical carcinogenesis: prolonged particulate hexavalent chromium exposure suppresses the Rad51 response in human lung cells. Toxicol Sci. 2014;142:117–125.
  • Wise SS, Holmes AL, Wise Sr JP. Hexavalent chromium-induced DNA damage and repair mechanisms. Rev Environ Health. 2008;23:39–58.
  • Xie H, Holmes AL, Young JL, et al. Zinc chromate induces chromosome instability and DNA double strand breaks in human lung cells. Toxicol Appl Pharmacol. 2009;234:293–299.
  • Fan Y, Ovesen JL, Puga A. Long-term exposure to hexavalent chromium inhibits expression of tumor suppressor genes in cultured cells and in mice. J Trace Elem Med Biol. 2012;26:188–191.
  • Schnekenburger M, Talaska G, Puga A. Chromium cross-links HDAC1 DNMT1 complexes to chromatin inhibiting histone remodeling marks critical for transcriptional activation. Mol Cell Biol. 2007. DOI:https://doi.org/10.1128/MCB.00838-07
  • Ovesen  JL, Fan Y, Zhang X, et al. Formaldehyde-assisted isolation of regulatory elements (FAIRE) analysis uncovers broad changes in chromatin structure resulting from hexavalent chromium exposure. PloS One. 2014;9. DOI:https://doi.org/10.1371/journal.pone.0097849.
  • VonHandorf A, Sanchez-Martin FJ, Biesiada J, et al. Chromium disrupts chromatin organization and CTCF access to its cognate sites in promoters of differentially expressed genes. Epigenetics. 2018;13:363–375.
  • Lutz M, Burke LJ, Barreto G, et al. Transcriptional repression by the insulator protein CTCF involves histone deacetylases. Nucleic Acids Res. 2000;28:1707–1713.
  • Ong C-T, Corces VG. CTCF: an architectural protein bridging genome topology and function. Nat Rev Genet. 2014;15:234–246.
  • Phillips JE, Corces VG. CTCF: master weaver of the genome. Cell. 2009;137:1194–1211.
  • Splinter E, Heath H, Kooren J, et al. CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus. Genes Dev. 2006;20:2349–2354.
  • Filippova GN, Qi CF, Ulmer JE, et al. Tumor-associated zinc finger mutations in the CTCF transcription factor selectively alter its DNA-binding specificity. Cancer Res. 2002;62:48–52.
  • Klenova EM, Morse III HC, Ohlsson R, et al. The novel BORIS + CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer. In: Seminars in cancer biology. vol. 12. Elsevier, 2002:399–414.
  • Katainen R, Dave K, Pitkänen E, et al. CTCF/cohesin-binding sites are frequently mutated in cancer. Nat Genet. 2015;47:818–821.
  • Tang Z, Luo OJ, Li X, et al. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell. 2015;163:1611–1627.
  • Consortium EP, others. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57–74.
  • Davis CA, Hitz BC, Sloan CA, et al. The Encyclopedia of DNA elements (ENCODE): data portal update. Nucleic Acids Res. 2018;46:D794–D801.
  • Pickrell JK, Gaffney DJ, Gilad Y, et al. False positive peaks in ChIP-seq and other sequencing-based functional assays caused by unannotated high copy number regions. Bioinformatics. 2011;27:2144–2146.
  • Zuin J, Dixon JR, van der Reijden MI, et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc Nat Acad Sci. 2014;111:996–1001.
  • Ohlsson R, Renkawitz R, Lobanenkov V. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet. 2001;17:520–527.
  • Cuddapah S, Jothi R, Schones DE, et al. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 2009;19:24–32.
  • Rubio ED, Reis DJ, Welcsh PL, et al. CTCF physically links cohesin to chromatin. Proc Nat Acad Sci. 2008;105:8309–8314.
  • Rudan MV, Barrington C, Henderson S, et al. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 2015;10:1297–1309.
  • deWit E, Vos ES, Holwerda SJ, et al. CTCF binding polarity determines chromatin looping. Mol Cell. 2015;60:676–684.
  • Nora E, Goloborodko A, Valton A, et al. Targeted degradation of ctcf decouples local insulation of chromosome domains from genomic compartmentalization. Cell. 2017;169:930–944. e22
  • Ovesen JL, Fan Y, Chen J, et al. Long-term exposure to low-concentrations of Cr(VI) induce DNA damage and disrupt the transcriptional response to benzo[a]pyrene. Toxicology. 2014;316:14–24.
  • Chen EY, Tan CM, Kou Y, et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics. 2013;14:128.
  • Kuleshov MV, Jones MR, Rouillard AD, et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 2016;44:W90–W97.
  • He J, Qian X, Carpentier R, et al. Repression of miR-143 Mediates Cr(VI)-Induced Tumor Angiogenesis via IGF-IR/IRS1/ERK/IL-8 Pathway. Toxicol Sci. 2013;134:26–38.
  • Kim D, Dai J, Fai LY, et al. Constitutive activation of epidermal growth factor receptor promotes tumorigenesis of Cr(VI)-transformed cells through decreased reactive oxygen species and apoptosis resistance development. J Biol Chem. 2015;290:2213–2224.
  • Reynolds MF, Peterson-Roth EC, Bespaloc IA, et al. Rapid DNA double-strand breaks resulting from processing of Cr-DNA cross-links by both MutS dimers. Cancer Res. 2009;69:1071–1079.
  • Xie Y, Zhuang Z. Chromium(VI)-induced production of reactive oxygen species, change of plasma membrane potential and dissipation of mitochondria membrane potential in Chinese hamster lung cell cultures. Biomed Environ Sci. 2001;14:199–206.
  • Zhitkovich A, Peterson-Roth E, Reynolds M. Killing of chromium-damaged cells by mismatch repair and its relevance to carcinogenesis. Cell Cycle. 2005;4:4050–4052.
  • Taudt A, Nguyen MA, Heinig M, et al. chromstaR: tracking combinatorial chromatin state dynamics in space and time. bioRxiv. 2016;038612.
  • Matthews BJ, Waxman DJ. Computational prediction of CTCF/cohesin-based intra-TAD loops that insulate chromatin contacts and gene expression in mouse liver. Elife. 2018;7:e34077.
  • Stark R, Brown G, others. DiffBind: differential binding analysis of ChIP-Seq peak data. R Package Version. 2011;100:3–4.
  • Ross-Innes CS, Stark R, Teschendorff AE, et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature. 2012;481:389–393.
  • DeLoughery Z, Luczak MW, Ortega-Atienza S, et al. DNA double-strand breaks by Cr(VI) are targeted to euchromatin and cause ATR-dependent phosphorylation of histone H2AX and its ubiquitination. Toxicol Sci. 2015;143:54–63.
  • Chen D, Kluz T, Fang L, et al. Hexavalent chromium (Cr(VI)) down-regulates acetylation of histone H4 at lysine 16 through induction of stressor protein Nupr1. PloS One. 2016;11-17.
  • Jia R, Chai P, Zhang H, et al. Novel insights into chromosomal conformations in cancer. Mol Cancer. 2017;16:173.
  • Taberlay PC, Achinger-Kawecka J, Lun ATL, et al. Three-dimensional disorganization of the cancer genome occurs coincident with long-range genetic and epigenetic alterations. Genome Res. 2016;26(6):719–731.
  • Al Bkhetan Z, Plewczynski D. Three-dimensional epigenome statistical model: genome-wide chromatin looping prediction. Sci Rep. 2018;8:1–11.
  • Kharchenko PV, Tolstorukov MY, Park PJ. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nat Biotechnol. 2008;26:1351–1359.
  • Landt SG, Marinov CK, Kundaje A, et al. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res. 2012;22:1813–1831.
  • Zhang Y, Liu T, Meyer CA, et al. Model-based analysis of chip-seq (macs). Genome Biol. 2008;9:R137.
  • Heinz S, Benner C, Spann N, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38:576–589.
  • Ramirez F, Ryan DP, Grüning B, et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016;44:W160–W165.
  • Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842.
  • Bailey TL, Boden M, Buske FA, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–W208.
  • Core Team R. R: A language and environment for statistical computing. R Foundation for Statistical Computing, 2020.
  • Wickham H, Averick M, Bryan J, et al. Welcome to the tidyverse. J Open Source Software. 2019;4:1686.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.