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Research Paper

Targeted epigenetic silencing of UCHL1 expression suppresses collagen-1 production in human lung epithelial cells

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Article: 2175522 | Received 02 Sep 2022, Accepted 11 Jan 2023, Published online: 22 Feb 2023

References

  • Doran JF, Jackson P, Kynoch PA, Thompson RJ. Isolation of PGP 9.5, a new human neurone-specific protein detected by high-resolution two-dimensional electrophoresis. J Neurochem. 1983;40(6):1542–21.
  • Carolan BJ, Heguy A, Harvey BG, Leopold PL, Ferris B, Crystal RG. Up-regulation of expression of the ubiquitin carboxyl-terminal hydrolase L1 gene in human airway epithelium of cigarette smokers. Cancer Res. 2006;66(22):10729–10740.
  • Min T, Bodas M, Mazur S, Vij N, et al. Critical role of proteostasis-imbalance in pathogenesis of COPD and severe emphysema. J Mol Med. 2011;89(6):577–593.
  • Li L, Tao Q, Jin H, et al. The tumor suppressor UCHL1 forms a complex with p53/MDM2/ARF to promote p53 signaling and is frequently silenced in nasopharyngeal carcinoma. Clin Cancer Res. 2010;16(11):2949–2958
  • Jin C, Yu W, Lou X, Zhou F, et al. UCHL1 Is a Putative Tumor Suppressor in Ovarian Cancer Cells and Contributes to Cisplatin Resistance. J Cancer. 2013;4(8):662–670.
  • Boelens MC, van den Berg A, Fehrmann RS, et al. Current smoking-specific gene expression signature in normal bronchial epithelium is enhanced in squamous cell lung cancer. J Pathol. 2009;218(2):182–191.
  • Hibi K, Westra WH, Borges M, et al. PGP9.5 as a candidate tumor marker for non-small-cell lung cancer. Am J Pathol. 1999;155(3):711–715.
  • Gong B, Cao Z, Zheng P, et al. Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell. 2006;126(4):775–788.
  • Sakurai M, Ayukawa K, Setsuie R, et al. Ubiquitin C-terminal hydrolase L1 regulates the morphology of neural progenitor cells and modulates their differentiation. J Cell Sci. 2006;119(1):162–171.
  • Hogg JC, Timens W. The pathology of chronic obstructive pulmonary disease. Annu Rev Pathol. 2009;4:435–459.
  • Pain M, Bermudez O, Lacoste P, et al. Tissue remodelling in chronic bronchial diseases: from the epithelial to mesenchymal phenotype. Eur Respir Rev. 2014;23(131):118–130.
  • Zuo HX, Trombetta-Lima M, Heijink IH, et al. A-Kinase Anchoring Proteins Diminish TGF-beta(1)/Cigarette Smoke-Induced Epithelial-To-Mesenchymal Transition. Cells. 2020;9(2):356.
  • Wilson CL, Murphy LB, Leslie J, et al. Ubiquitin C-terminal hydrolase 1: a novel functional marker for liver myofibroblasts and a therapeutic target in chronic liver disease. J Hepatol. 2015;63(6):1421–1428.
  • Cheng J-C. Activation of hepatic stellate cells by the ubiquitin C-terminal hydrolase 1 protein secreted from hepatitis C virus-infected hepatocytes. Sci Rep. 2017;7(1):1–12.
  • Gong Z, Ye Q, Wu JW, et al. UCHL1 inhibition attenuates cardiac fibrosis via modulation of nuclear factor-κB signaling in fibroblasts. Eur J Pharmacol. 2021;900:174045.
  • Lei Q, Yi T, Li H, et al. Ubiquitin C-terminal hydrolase L1 (UCHL1) regulates post-myocardial infarction cardiac fibrosis through glucose-regulated protein of 78kDa (GRP78). Sci Rep. 2020;10(1):10604.
  • Cortés-Mancera FM, Sarno F, Goubert D, Rots MG, et al. Gene-targeted DNA methylation: towards long-lasting reprogramming of gene expression? Adv Exp Med Biol. 2022;10:515.
  • Spira A, Beane J, Shah V, et al. Effects of cigarette smoke on the human airway epithelial cell transcriptome. Pro Natl Acad Sci USA. 2004;101(27):10143–10148.
  • Moses E, Wang T, Corbett S, et al. Molecular Impact of Electronic Cigarette Aerosol Exposure in Human Bronchial Epithelium. Toxicol Sci. 2017;155(1):248–257.
  • Wu DD, Xu YM, Chen DJ, et al. Ubiquitin carboxyl-terminal hydrolase isozyme L1/UCHL1 suppresses epithelial-mesenchymal transition and is under-expressed in cadmium-transformed human bronchial epithelial cells. Cell Biol Toxicol. 2021;37(4):497–513.
  • Ghandi M, Huang FW, Jané-Valbuena J, et al. Next-generation characterization of the Cancer Cell Line Encyclopedia. Nature. 2019;569(7757):503–508.
  • Cerami E, Gao J, Dogrusoz U, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401–404.
  • Gao JJ, Aksoy BA, Dogrusoz U, et al. Integrative Analysis of Complex Cancer Genomics and Clinical Profiles Using the cBioPortal. Sci Signal. 2013;6(269).
  • Liu YC, Lashuel HA, Choi S, et al. Discovery of inhibitors that elucidate the role of UCH-L1 activity in the H1299 lung cancer cell line. Chem Biol. 2003;10(9):837–846.
  • Hosper NA, van den Berg PP, de Rond S, et al. Epithelial-to-mesenchymal transition in fibrosis: collagen type I expression is highly upregulated after EMT, but does not contribute to collagen deposition. Exp Cell Res. 2013;319(19):3000–3009.
  • Konermann S, Brigham MD, Trevino AE, et al. Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature. 2015;517(7536):583–U332.
  • Saunderson EA, Stepper P, Gomm JJ, et al. Hit-and-run epigenetic editing prevents senescence entry in primary breast cells from healthy donors. Nat Commun. 2017;8(1):1450.
  • Amabile A, Migliara A, Capasso P, et al. Inheritable Silencing of Endogenous Genes by Hit-and-Run Targeted Epigenetic Editing. Cell. 2016;167(1):219–232 e14.
  • Nuñez JK, Chen J, Pommier GC, et al. Genome-wide programmable transcriptional memory by CRISPR-based epigenome editing. Cell. 2021;184(9):2503–2519.e17.
  • Rosas SLB, Caballero OL, Dong SM, et al. Methylation status in the promoter region of the human PGP9.5 gene in cancer and normal tissues. Cancer Lett. 2001;170(1):73–79.
  • Mandelker DL, Yamashita K, Tokumaru Y, et al. PGP9.5 promoter methylation is an independent prognostic factor for esophageal squamous cell carcinoma. Cancer Res. 2005;65(11):4963–4968.
  • Tokumaru Y, Yamashita K, Kim MS, et al. The role of PGP9.5 as a tumor suppressor gene in human cancer. Int J Cancer. 2008;123(4):753–759.
  • Fujikane T, Nishikawa N, Toyota M, et al. Genomic screening for genes upregulated by demethylation revealed novel targets of epigenetic silencing in breast cancer. Breast Cancer Res Treat. 2010;122(3):699–710.
  • Wang G, Zhang W, Zhou B, et al. The diagnosis value of promoter methylation of UCHL1 in the serum for progression of gastric cancer. BioMed Res Int. 2015;2015:741030.
  • Lee CH, Pan KL, Tang YC, et al. LDOC1 silenced by cigarette exposure and involved in oral neoplastic transformation. Oncotarget. 2015;6(28):25188–25201.
  • Kim JE, Koo KH, Kim YH, et al. Identification of potential lung cancer biomarkers using an in vitro carcinogenesis model. Exp Mol Med. 2008;40(6):709–720.
  • Milara J, Peiró T, Serrano A, et al. Roflumilast N-oxide inhibits bronchial epithelial to mesenchymal transition induced by cigarette smoke in smokers with COPD. Pulm Pharmacol Ther. 2014;28(2):138–148.
  • Akishima-Fukasawa Y, Ino Y, Nakanishi Y, et al. Significance of PGP9.5 expression in cancer-associated fibroblasts for prognosis of colorectal carcinoma. Am J Clin Pathol. 2010;134(1):71–79.
  • Olerud JE, Chiu DS, Usui ML, et al. Protein gene product 9.5 is expressed by fibroblasts in human cutaneous wounds. J Invest Dermatol. 1998;111(4):565–572.
  • Doerner AM, Zuraw BL. TGF-beta1 induced epithelial to mesenchymal transition (EMT) in human bronchial epithelial cells is enhanced by IL-1beta but not abrogated by corticosteroids. Respir Res. 2009;10:100.
  • Wang R, Zhang M, Zhou W, et al. NF-kappaB signaling inhibits ubiquitin carboxyl-terminal hydrolase L1 gene expression. J Neurochem. 2011;116(6):1160–1170.
  • Chen X. Construction and validation of the CRISPR/dCas9-EZH2 system for targeted H3K27Me3 modification. Biochem Biophys Res Commun. 2019;511(2):246–252.
  • Wang H, Guo R, Du Z, et al. Epigenetic Targeting of Granulin in Hepatoma Cells by Synthetic CRISPR dCas9 Epi-suppressors. Mol Ther Nucleic Acids. 2018;11:23–33.
  • Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature. 2011;469(7330):343–349.
  • Bheda A, Shackelford J, Pagano JS, et al. Expression and Functional Studies of Ubiquitin C-Terminal Hydrolase L1 Regulated Genes. PloS one. 2009;4(8):e6764.
  • O’Geen H, Ren C, Nicolet CM, et al. dCas9-based epigenome editing suggests acquisition of histone methylation is not sufficient for target gene repression. Nucleic Acids Res. 2017;45(17):9901–9916.
  • Cano-Rodriguez D, Gjaltema RA, Jilderda LJ, et al. Writing of H3K4Me3 overcomes epigenetic silencing in a sustained but context-dependent manner. Nature Commun. 2016;7:12284.
  • Song J, Cano-Rodriquez D, Winkle M, et al. Targeted epigenetic editing of SPDEF reduces mucus production in lung epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2017;312(3):L334–L347.
  • Mlambo T, Nitsch S, Hildenbeutel M, et al. Designer Epigenome Modifiers Enable Robust and Sustained Gene Silencing in Clinically Relevant Human Cells. Mol Ther. 2018;26(5):365.
  • Bintu L, Yong J, Antebi YE, et al. Dynamics of epigenetic regulation at the single-cell level. Science. 2016;351(6274):720–724.
  • O’Geen H, Bates SL, Carter SS, et al. Ezh2-dCas9 and KRAB-dCas9 enable engineering of epigenetic memory in a context-dependent manner. Epigenetics Chromatin. 2019;12(1):26.
  • Heijink IH, Brandenburg SM, Postma DS, et al. Cigarette smoke impairs airway epithelial barrier function and cell-cell contact recovery. Eur Respir J. 2012;39(2):419–428.
  • Goubert D, Koncz M, Kiss A, et al. Establishment of Cell Lines Stably Expressing dCas9-Fusions to Address Kinetics of Epigenetic Editing. Methods Mol Biol. 2018;1767:395–415.
  • Darii MV, Cherepanova NA, Subach OM, et al. Mutational analysis of the CG recognizing DNA methyltransferase SssI: insight into enzyme-DNA interactions. Biochim Biophys Acta. 2009;1794:1654–1662.
  • Kim JH, Lee SR, Li LH, et al. High Cleavage Efficiency of a 2A Peptide Derived from Porcine Teschovirus-1 in Human Cell Lines, Zebrafish and Mice. PLoS One. 2011;6(4):e18556.