A potential screening method for epigenetic drugs: uncovering stress-induced gene silencing in Chlamydomonas

References

• Li G, Reinberg D. Chromatin higher-order structures and gene regulation. Curr Opin Genet Dev. 2011;21(2):175–186.
   PubMed Web of Science ®Google Scholar
• Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128(4):707–719.
   PubMed Web of Science ®Google Scholar
• Sen S, Block KF, Pasini A, et al. Genome-wide positioning of bivalent mononucleosomes. BMC Med Genomics. 2016;9(1):60.
   PubMed Web of Science ®Google Scholar
• Allis CD, Jenuwein T. The molecular hallmarks of epigenetic control. Nat Rev Genet. 2016;17(8):487–500.
   PubMed Web of Science ®Google Scholar
• Bej S, Basak J. Abiotic stress induced epigenetic modifications in plants: how much do we know?. New York, NY: Springer; 2017.
   Google Scholar
• O’Hagan HM, Wang W, Sen S, et al. Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands. Cancer Cell. 2011;20(5):606–619.
   PubMed Web of Science ®Google Scholar
• Wenbing Xie HE, Kagiampakis I, Pan L, et al. DNA methylation patterns separate senescence from transformation potential and indicate cancer risk. Cancer Cell. 2017;33:309–321.e5.
   Web of Science ®Google Scholar
• Raynal NJM, Costa EM, Lee JT, et al. Repositioning FDA-approved drugs in combination with epigenetic drugs to reprogram colon cancer epigenome. Mol Cancer Ther. 2017;16(2):397–407.
   PubMed Web of Science ®Google Scholar
• Cui Y, Hausheer F, Beaty R, et al. A recombinant reporter system for monitoring reactivation of an endogenously DNA hypermethylated gene. Cancer Res. 2014;74(14):3834–3843.
   PubMed Web of Science ®Google Scholar
• Stelzer Y, Shivalila CS, Soldner F, et al. Tracing dynamic changes of DNA methylation at single-cell resolution. Cell. 2015;163(1):218–229.
   PubMed Web of Science ®Google Scholar
• Johnson RL, Huang W, Jadhav A, et al. A quantitative high-throughput screen identifies potential epigenetic modulators of gene expression. Anal Biochem. 2008;375(2):237–248.
   PubMed Web of Science ®Google Scholar
• Danishuddin N, Subbarao M, Faheem SN. Polycomb repressive complex 2 inhibitors: emerging epigenetic modulators. Drug Discov Today. 2019;24:179–188.
   PubMed Web of Science ®Google Scholar
• Gall Trošelj K, Novak Kujundzic R, Ugarkovic D. Polycomb repressive complex's evolutionary conserved function: the role of EZH2 status and cellular background. Clin Epigenet. 2016;8(1):55.
   PubMed Web of Science ®Google Scholar
• Lewis ZA. Polycomb group systems in fungi: new models for understanding polycomb repressive complex 2. Trends Genet. 2017;33(3):220–231.
   PubMed Web of Science ®Google Scholar
• Shaver S, Casas-Mollano JA, Cerny RL, et al. Origin of the Polycomb repressive complex 2 and gene silencing by an E(z) homolog in the unicellular alga Chlamydomonas. Epigenetics. 2010;5(4):301–312.
   PubMed Web of Science ®Google Scholar
• Zhong X. Comparative epigenomics: a powerful tool to understand the evolution of DNA methylation. New Phytol. 2016;210(1):76–80.
   PubMed Web of Science ®Google Scholar
• Feng S, Cokus SJ, Zhang X, et al. Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci USA. 2010;107(19):8689–8694.
   PubMed Web of Science ®Google Scholar
• Yamasaki T, Miyasaka H, Ohama T. Unstable RNAi effects through epigenetic silencing of an inverted repeat transgene in Chlamydomonas reinhardtii. Genetics. 2008;180(4):1927–1944.
   PubMed Web of Science ®Google Scholar
• D’Souza N, Joshi P, Kaginkar S, et al. Generating nucleosomal ladders in vivo by releasing endogenous endonucleases in Chlamydomonas reinhardtii. Plant Mol Biol Rep. 2018;36(2):363–371.
   Web of Science ®Google Scholar
• Potdar P, Pinto P, D’Souza N, et al. A novel method to generate MNase ladders reveal rapid chromatin remodeling upon gametogenesis and mating in Chlamydomonas. Protist. 2018;169(5):632–644.
   PubMed Web of Science ®Google Scholar
• Rohr J, Sarkar N, Balenger S, et al. Tandem inverted repeat system for selection of effective transgenic RNAi strains in Chlamydomonas. Plant J. 2004;40(4):611–621.
   PubMed Web of Science ®Google Scholar
• Griffin R, Binari R, Perrimon N. Genetic odyssey to generate marked clones in Drosophila mosaics. Proc Natl Acad Sci USA. 2014;111(13):4756–4763.
   PubMed Web of Science ®Google Scholar
• Reddy GV. Fluorescence activated cell sorting of shoot apical meristem cell types. Methods Mol Biol. 2014;1110:315–321.
   PubMedGoogle Scholar
• Sizova I, Fuhrmann M, Hegemann P. A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. Gene. 2001;277(1–2):221–229.
   PubMed Web of Science ®Google Scholar
• Timms RT, Tchasovnikarova IA, Lehner PJ. Position-effect variegation revisited: HUSHing up heterochromatin in human cells. Bioessays. 2016;38(4):333–343.
   PubMed Web of Science ®Google Scholar
• Kronholm I, Bassett A, Baulcombe D, et al. Epigenetic and genetic contributions to adaptation in Chlamydomonas. Mol Biol Evol. 2017;34(9):2285–2306.
   PubMed Web of Science ®Google Scholar
• van Dijk K, Marley KE, Jeong B-r, et al. Monomethyl histone H3 lysine 4 as an epigenetic mark for silenced euchromatin in Chlamydomonas. Plant Cell. 2005;17(9):2439–2453.
   PubMed Web of Science ®Google Scholar
• McGarvey KM, Fahrner JA, Greene E, et al. Silenced tumor suppressor genes reactivated by DNA demethylation do not return to a fully euchromatic chromatin state. Cancer Res. 2006;66(7):3541–3549.
   PubMed Web of Science ®Google Scholar
• Motiwalla MJ, Sequeira MP, D'Souza JS. Two calcium-dependent protein kinases from Chlamydomonas reinhardtii are transcriptionally regulated by nutrient starvation. Plant Signal Behav. 2014;9(1):e27969.
   PubMed Web of Science ®Google Scholar
• Wagle MD, Sen S, Rao BJ. Local repeat sequence organization of an intergenic spacer in the chloroplast genome of Chlamydomonas reinhardtii leads to DNA expansion and sequence scrambling: a complex mode of "copy-choice replication"? J Biosci. 2001;26(5):583–594.
   PubMed Web of Science ®Google Scholar
• Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual (2 ed.). Cold Spring Harbor. NY, USA: Cold Spring Harbor Laboratory Press; 1989.
   Google Scholar
• Harris EH, Stern DB, Witman G. The Chlamydomonas sourcebook. 2nd ed. London: Academic Press; 2008.
   Google Scholar
• Stoiber TL, Shafer MM, Armstrong DE. Induction of reactive oxygen species in *Chlamydomonas reinhardtii in response to contrasting trace metal exposures. Environ Toxicol. 2013;28(9):516–523.
   PubMed Web of Science ®Google Scholar
• Lee DY, Fiehn O. High quality metabolomic data for Chlamydomonas reinhardtii. Plant Methods. 2008;4(1):7.
   PubMed Web of Science ®Google Scholar
• Davies JP, Grossman AR. Sequences controlling transcription of the Chlamydomonas reinhardtii beta 2-tubulin gene after deflagellation and during the cell cycle. Mol Cell Biol. 1994;14(8):5165–5174.
   PubMed Web of Science ®Google Scholar
• Barth J, Bergner SV, Jaeger D, et al. The interplay of light and oxygen in the reactive oxygen stress response of Chlamydomonas reinhardtii dissected by quantitative mass spectrometry. Mol Cell Proteomics. 2014;13(4):969–989.
   PubMed Web of Science ®Google Scholar
• Vaz M, Hwang SY, Kagiampakis I, et al. Chronic cigarette smoke-induced epigenomic changes precede sensitization of bronchial epithelial cells to single-step transformation by KRAS mutations. Cancer Cell. 2017;32(3):360–376.e6.
   PubMed Web of Science ®Google Scholar
• Merchant SS, Allen MD, Kropat J, et al. Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochim Biophys Acta – Mol Cell Res. 2006;1763(7):578–594.
   Web of Science ®Google Scholar
• Allen MD, Kropat J, Tottey S, et al. Manganese deficiency in Chlamydomonas results in loss of photosystem II and MnSOD function, sensitivity to peroxides, and secondary phosphorus and iron deficiency. Plant Physiol. 2007;143(1):263–277.
   PubMed Web of Science ®Google Scholar
• Zhu B, Shang B, Li Y, et al. Inhibition of histone deacetylases by trans-cinnamic acid and its antitumor effect against colon cancer xenografts in athymic mice. Mol Med Rep. 2016;13(5):4159–4166.
   PubMed Web of Science ®Google Scholar
• Lee T-f, Zhai J, Meyers BC. Conservation and divergence in eukaryotic DNA methylation. Proc Natl Acad Sci U S A. 2010;107(20):9027–9028.
   PubMed Web of Science ®Google Scholar
• Lin H, Kwan AL, Dutcher SK. Synthesizing and salvaging NAD: lessons learned from Chlamydomonas reinhardtii. PLoS Genet. 2010;6(9):e1001105.
   PubMed Web of Science ®Google Scholar
• Javaid N, Choi S. Acetylation- and methylation-related epigenetic proteins in the context of their targets. Genes (Basel). 2017;8(8):196.
   Web of Science ®Google Scholar
• Zaky A, Mahmoud M, Awad D, et al. Valproic acid potentiates curcumin-mediated neuroprotection in lipopolysaccharide induced rats. Front Cell Neurosci. 2014;8:337.
   PubMed Web of Science ®Google Scholar
• Suzuki K, Ohbayashi F, Nikaido I, et al. Integration of exogenous DNA into mouse embryonic stem cell chromosomes shows preference into genes and frequent modification at junctions. Chromosome Res. 2010;18(2):191–201.
   PubMed Web of Science ®Google Scholar
• Sonoda E, Hochegger H, Saberi A, et al. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst). 2006;5(9–10):1021–1029.
   PubMed Web of Science ®Google Scholar
• Specht EA, Nour-Eldin HH, Hoang KTD, et al. An improved ARS2-derived nuclear reporter enhances the efficiency and ease of genetic engineering in Chlamydomonas. Biotechnol J. 2015;10(3):473–479.
   PubMed Web of Science ®Google Scholar
• Rodriguez H, Akman SA. Mapping oxidative DNA damage at nucleotide level. Free Radic Res. 1998;29(6):499–510.
   PubMed Web of Science ®Google Scholar
• Kropat J, et al. Copper economy in Chlamydomonas: prioritized allocation and eallocation of copper to respiration vs. Photosynthesis. Proc Natl Acad Sci U S A. 2015;112(9):2644–2651.
   PubMed Web of Science ®Google Scholar
• Brito S, Lee MG, Bin BH, et al. Zinc and its transporters in epigenetics. Mol Cells. 2020;43(4):323–330.
   PubMed Web of Science ®Google Scholar
• Pluciński B, Waloszek A, Rutkowska J, et al. Copper excess-induced large reversible and small irreversible adaptations in a population of Chlamydomonas reinhardtii CW15 (Chlorophyta). Acta Soc Bot Pol. 2018;7:30–387.
   Google Scholar
• Foyer CH, Noctor G. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants Redox Signal. 2009;11(4):861–905.
   PubMed Web of Science ®Google Scholar
• Aramayo R, Selker EU. Neurospora crassa, a model system for epigenetics research. Cold Spring Harb Perspect Biol. 2013;5(10):a017921.
   PubMed Web of Science ®Google Scholar
• Saldanha SN, Kala R, Tollefsbol TO. Molecular mechanisms for inhibition of colon cancer cells by combined epigenetic-modulating epigallocatechin gallate and sodium butyrate. *Exp Cell Res. 2014;324(1):40–53.
   PubMed Web of Science ®Google Scholar
• Teiten M-H, Dicato M, Diederich M. Curcumin as a regulator of epigenetic events. Mol Nutr Food Res. 2013;57(9):1619–1629.
   PubMed Web of Science ®Google Scholar