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ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

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Research Article

The Effect of Cyclosporine A on Dermal Fibroblast Cell - Transcriptomic Analysis of Inflammatory Response Pathway

Author(s): Grażyna Janikowska*, Ewa Kurzeja, Marcin Janikowski, Barbara Strzałka-Mrozik, Alina Pyka-Pająk and Tomasz Janikowski

Volume 21, Issue 12, 2020

Page: [1213 - 1223] Pages: 11

DOI: 10.2174/1389201021666200416103928

Price: $65

Abstract

Background: The first immunosuppressive drug - cyclosporine A (CsA) has many unquestioned merits in maintaining organ transplants in patients, as well as, in the treatment of many inflammatory diseases, also associated with cutaneous manifestations. The main task of this drug is to suppress the inflammatory response at the sites of action, which is not well known.

Objective: The objective of this study was to evaluate the influence of CsA in therapeutic concentration on the expression of genes associated with the inflammatory response pathway in normal human dermal fibroblasts (NHDF; CC-2511), and this study attempted to determine the mechanism of its action.

Methods: The cytotoxicity MTT test was performed. The expression of the inflammatory response pathway genes was determined using HG-U133A_2.0 oligonucleotide microarrays. Statistical analysis was performed by GeneSpring 13.0 software using the PL-Grid platform.

Results: Among the 5,300 mRNA, only 573 were changed significantly in response to CsA compared to the control fibroblasts (P≤0.05). CsA inhibited the expression of most genes associated with the inflammatory response in NHDFs. There were only 19 genes with a fold change (FC) lower than -2.0, among which EGR1, FOS, PBK, CDK1 and TOP2A had the lowest expression, as did CXCL2 which can directly impact inflammation. Furthermore, ZNF451 was strongly induced, and COL1A1, COL3A1, IL33, TNFRSFs were weakly up-regulated (FC lower than 2.0).

Conclusion: The CsA in therapeutic concentration influences the genes linked to the inflammatory response (in the transcriptional level) in human dermal fibroblasts. The findings suggest that the potential mechanism of CsA action in this concentration and on these genes can be associated with a profibrotic and proapoptotic, and genotoxic effects.

Keywords: CsA, oligonucleotide microarray, profibrotic, proapoptotic, human dermal fibroblasts, genotoxic action.

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[1]
Tolou-Ghamari, Z. Nephro and neurotoxicity of calcineurin inhibitors and mechanisms of rejections: A review on tacrolimus and cyclosporin in organ transplantation. J. Nephropathol., 2012, 1(1), 23-30.
[http://dx.doi.org/10.5812/jnp.6 ] [PMID: 24475383]
[2]
Magnasco, A.; Rossi, A.; Catarsi, P.; Gusmano, R.; Ginevri, F.; Perfumo, F.; Ghiggeri, G.M. Cyclosporin and organ specific toxicity: clinical aspects, pharmacogenetics and perspectives. Curr. Clin. Pharmacol., 2008, 3(3), 166-173.
[http://dx.doi.org/10.2174/157488408785747674 ] [PMID: 18781903]
[3]
Thomson, A.W., Ed.; Cyclosporine: Mode of Action and Clinical Applications; Springer Science & Business Media, 2012.
[4]
Khattri, S.; Shemer, A.; Rozenblit, M.; Dhingra, N.; Czarnowicki, T.; Finney, R.; Gilleaudeau, P.; Sullivan-Whalen, M.; Zheng, X.; Xu, H.; Cardinale, I.; de Guzman Strong, C.; Gonzalez, J.; Suárez-Fariñas, M.; Krueger, J.G.; Guttman-Yassky, E. Cyclosporine in patients with atopic dermatitis modulates activated inflammatory pathways and reverses epidermal pathology. J. Allergy Clin. Immunol., 2014, 133(6), 1626-1634.
[http://dx.doi.org/10.1016/j.jaci.2014.03.003 ] [PMID: 24786238]
[5]
Amor, K.T.; Ryan, C.; Menter, A. The use of cyclosporine in dermatology: part I. J. Am. Acad. Dermatol., 2010, 63(6), 925-946.
[http://dx.doi.org/10.1016/j.jaad.2010.02.063 ] [PMID: 21093659]
[6]
Bußmann, C.; Novak, N. Systemic therapy of atopic dermatitis. Allergol. Select, 2017, 1(1), 1-8.
[http://dx.doi.org/10.5414/ALX01285E ] [PMID: 30402595]
[7]
Lindelöf, B.; Sigurgeirsson, B.; Gäbel, H.; Stern, R.S. Incidence of skin cancer in 5356 patients following organ transplantation. Br. J. Dermatol., 2000, 143(3), 513-519.
[PMID: 10971322]
[8]
Muellenhoff, M.W.; Koo, J.Y. Cyclosporine and skin cancer: an international dermatologic perspective over 25 years of experience. A comprehensive review and pursuit to define safe use of cyclosporine in dermatology. J. Dermatolog. Treat., 2012, 23(4), 290-304.
[http://dx.doi.org/10.3109/09546634.2011.590792 ] [PMID: 21936704]
[9]
Mueller, M.M. Inflammation in epithelial skin tumours: old stories and new ideas. Eur. J. Cancer, 2006, 42(6), 735-744.
[http://dx.doi.org/10.1016/j.ejca.2006.01.014 ] [PMID: 16527478]
[10]
Smit, N.P.; Van Rossum, H.H.; Romijn, F.P.; Sellar, K.J.; Breetveld, M.; Gibbs, S.; Van Pelt, J. Calcineurin activity and inhibition in skin and (epi)dermal cell cultures. J. Invest. Dermatol., 2008, 128(7), 1686-1690.
[http://dx.doi.org/10.1038/sj.jid.5701244 ] [PMID: 18200052]
[11]
Chovatiya, R.; Medzhitov, R. Stress, inflammation, and defense of homeostasis. Mol. Cell, 2014, 54(2), 281-288.
[http://dx.doi.org/10.1016/j.molcel.2014.03.030 ] [PMID: 24766892]
[12]
Chen, L.; Deng, H.; Cui, H.; Fang, J.; Zuo, Z.; Deng, J.; Li, Y.; Wang, X.; Zhao, L. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget, 2017, 9(6), 7204-7218.
[PMID: 29467962]
[13]
Aaronson, D.S.; Horvath, C.M. A road map for those who don’t know JAK-. STAT. Science, 2002, 296(5573), 1653-1655.
[http://dx.doi.org/10.1126/science.1071545 ] [PMID: 12040185]
[14]
Medzhitov, R. Inflammation 2010: New adventures of an old flame. Cell, 2010, 140(6), 771-776.
[http://dx.doi.org/10.1016/j.cell.2010.03.006 ] [PMID: 20303867]
[15]
Tortola, L.; Rosenwald, E.; Abel, B.; Blumberg, H.; Schäfer, M.; Coyle, A.J.; Renauld, J.C.; Werner, S.; Kisielow, J.; Kopf, M. Psoriasiform dermatitis is driven by IL-36-mediated DC-keratinocyte crosstalk. J. Clin. Invest., 2012, 122(11), 3965-3976.
[http://dx.doi.org/10.1172/JCI63451 ] [PMID: 23064362]
[16]
Al-Daraji, W.I.; Grant, K.R.; Ryan, K.; Saxton, A.; Reynolds, N.J. Localization of calcineurin/NFAT in human skin and psoriasis and inhibition of calcineurin/NFAT activation in human keratinocytes by cyclosporin A. J. Invest. Dermatol., 2002, 118(5), 779-788.
[http://dx.doi.org/10.1046/j.1523-1747.2002.01709.x] [PMID: 11982754]
[17]
Abikhair, M.; Mitsui, H.; Yanofsky, V.; Roudiani, N.; Ovits, C.; Bryan, T.; Oberyszyn, T.M.; Tober, K.L.; Gonzalez, J.; Krueger, J.G.; Felsen, D.; Carucci, J.A. Cyclosporine A immunosuppression drives catastrophic squamous cell carcinoma through IL-22. JCI Insight, 2016, 1(8)e86434
[http://dx.doi.org/10.1172/jci.insight.86434 ] [PMID: 27699266]
[18]
Wolf, G.; Thaiss, F.; Stahl, R.A. Cyclosporine stimulates expression of transforming growth factor-beta in renal cells. Possible mechanism of cyclosporines antiproliferative effects. Transplantation, 1995, 60(3), 237-241.
[http://dx.doi.org/10.1097/00007890-199508000-00005] [PMID: 7645035]
[19]
Walsh, S.B.; Xu, J.; Xu, H.; Kurundkar, A.R.; Maheshwari, A.; Grizzle, W.E.; Timares, L.; Huang, C.C.; Kopelovich, L.; Elmets, C.A.; Athar, M. Cyclosporine a mediates pathogenesis of aggressive cutaneous squamous cell carcinoma by augmenting epithelial-mesenchymal transition: role of TGFβ signaling pathway. Mol. Carcinog., 2011, 50(7), 516-527.
[http://dx.doi.org/10.1002/mc.20744 ] [PMID: 21308804]
[20]
Gelse, K.; Pöschl, E.; Aigner, T. Collagens--structure, function, and biosynthesis. Adv. Drug Deliv. Rev., 2003, 55(12), 1531-1546.
[http://dx.doi.org/10.1016/j.addr.2003.08.002 ] [PMID: 14623400]
[21]
Wolf, K.; Alexander, S.; Schacht, V.; Coussens, L.M.; von Andrian, U.H.; van Rheenen, J.; Deryugina, E.; Friedl, P. Collagen-based cell migration models in vitro and in vivo. Semin. Cell Dev. Biol., 2009, 20(8), 931-941.
[http://dx.doi.org/10.1016/j.semcdb.2009.08.005 ] [PMID: 19682592]
[22]
Wong, V.W.; You, F.; Januszyk, M.; Gurtner, G.C.; Kuang, A.A. Transcriptional profiling of rapamycin-treated fibroblasts from hypertrophic and keloid scars. Ann. Plast. Surg., 2014, 72(6), 711-719.
[http://dx.doi.org/10.1097/SAP.0b013e31826956f6] [PMID: 24835866]
[23]
Verrecchia, F.; Mauviel, A. TGF-beta and TNF-alpha: Antagonistic cytokines controlling type I collagen gene expression. Cell. Signal., 2004, 16(8), 873-880.
[http://dx.doi.org/10.1016/j.cellsig.2004.02.007 ] [PMID: 15157666]
[24]
Naudé, P.J.W.; den Boer, J.A.; Luiten, P.G.; Eisel, U.L. Tumor necrosis factor receptor cross-talk. FEBS J., 2011, 278(6), 888-898.
[http://dx.doi.org/10.1111/j.1742-4658.2011.08017.x] [PMID: 21232019]
[25]
Gaur, U.; Aggarwal, B.B. Regulation of proliferation, survival and apoptosis by members of the TNF superfamily. Biochem. Pharmacol., 2003, 66(8), 1403-1408.
[http://dx.doi.org/10.1016/S0006-2952(03)00490-8] [PMID: 14555214]
[26]
Aganna, E.; Hammond, L.; Hawkins, P.N.; Aldea, A.; McKee, S.A.; van Amstel, H.K.; Mischung, C.; Kusuhara, K.; Saulsbury, F.T.; Lachmann, H.J.; Bybee, A.; McDermott, E.M.; La Regina, M.; Arostegui, J.I.; Campistol, J.M.; Worthington, S.; High, K.P.; Molloy, M.G.; Baker, N.; Bidwell, J.L.; Castañer, J.L.; Whiteford, M.L.; Janssens-Korpola, P.L.; Manna, R.; Powell, R.J.; Woo, P.; Solis, P.; Minden, K.; Frenkel, J.; Yagüe, J.; Mirakian, R.M.; Hitman, G.A.; McDermott, M.F. Heterogeneity among patients with tumor necrosis factor receptor-associated periodic syndrome phenotypes. Arthritis Rheum., 2003, 48(9), 2632-2644.
[http://dx.doi.org/10.1002/art.11215 ] [PMID: 13130484]
[27]
MacEwan, D.J. TNF receptor subtype signalling: differences and cellular consequences. Cell. Signal., 2002, 14(6), 477-492.
[http://dx.doi.org/10.1016/S0898-6568(01)00262-5] [PMID: 11897488]
[28]
Shukla, V.; Coumoul, X.; Lahusen, T.; Wang, R.H.; Xu, X.; Vassilopoulos, A.; Xiao, C.; Lee, M.H.; Man, Y.G.; Ouchi, M.; Ouchi, T.; Deng, C.X. BRCA1 affects global DNA methylation through regulation of DNMT1. Cell Res., 2010, 20(11), 1201-1215.
[http://dx.doi.org/10.1038/cr.2010.128 ] [PMID: 20820192]
[29]
Yoshimura, A.; Muto, G. TGF-β function in immune suppression. Curr. Top. Microbiol. Immunol., 2011, 350, 127-147.
[http://dx.doi.org/10.1007/82_2010_87 ] [PMID: 20680806]
[30]
Pagel, J.I.; Deindl, E. Early growth response 1--a transcription factor in the crossfire of signal transduction cascades. Indian J. Biochem. Biophys., 2011, 48(4), 226-235.
[PMID: 22053691]
[31]
Naidu, B.V.; Farivar, A.S.; Woolley, S.M.; Byrne, K.; Mulligan, M.S. Chemokine response of pulmonary artery endothelial cells to hypoxia and reoxygenation. J. Surg. Res., 2003, 114(2), 163-171.
[http://dx.doi.org/10.1016/S0022-4804(03)00330-5] [PMID: 14559442]
[32]
Cogswell, P.C.; Mayo, M.W.; Baldwin, A.S. Jr Involvement of Egr-1/RelA synergy in distinguishing T cell activation from tumor necrosis factor-α-induced NF-kappa B1 transcription. J. Exp. Med., 1997, 185(3), 491-497.
[http://dx.doi.org/10.1084/jem.185.3.491 ] [PMID: 9053449]
[33]
Decker, E.L.; Skerka, C.; Zipfel, P.F. The early growth response protein (EGR-1) regulates interleukin-2 transcription by synergistic interaction with the nuclear factor of activated T cells. J. Biol. Chem., 1998, 273(41), 26923-26930.
[http://dx.doi.org/10.1074/jbc.273.41.26923 ] [PMID: 9756940]
[34]
Inoue, K.; Fry, E.A. Tumor suppression by the EGR1, DMP1, ARF, p53, and PTEN Network. Cancer Invest., 2018, 5, 1-17.
[http://dx.doi.org/10.1080/07357907.2018.1533965] [PMID: 30396285]
[35]
Yang, J.; Sun, L.; Han, J.; Zheng, W.; Peng, W. DUSP1/MKP-1 regulates proliferation and apoptosis in keratinocytes through the ERK/Elk-1/Egr-1 signaling pathway. Life Sci., 2019, 223, 47-53.
[http://dx.doi.org/10.1016/j.lfs.2019.03.018 ] [PMID: 30858120]
[36]
Ahlborn, G.J.; Nelson, G.M.; Ward, W.O.; Knapp, G.; Allen, J.W.; Ouyang, M.; Roop, B.C.; Chen, Y.; O’Brien, T.; Kitchin, K.T.; Delker, D.A. Dose response evaluation of gene expression profiles in the skin of K6/ODC mice exposed to sodium arsenite. Toxicol. Appl. Pharmacol., 2008, 227(3), 400-416.
[http://dx.doi.org/10.1016/j.taap.2007.10.029 ] [PMID: 18191166]
[37]
Magócsi, M.; Apáti, A.; Gáti, R.; Kolonics, A. Signalling mechanisms and the role of calcineurin in erythropoiesis. Immunol. Lett., 1999, 68(1), 187-195.
[http://dx.doi.org/10.1016/S0165-2478(99)00048-6] [PMID: 10397175]
[38]
Ekblom, M.; Fässler, R.; Tomasini-Johansson, B.; Nilsson, K.; Ekblom, P. Downregulation of tenascin expression by glucocorticoids in bone marrow stromal cells and in fibroblasts. J. Cell Biol., 1993, 123(4), 1037-1045.
[http://dx.doi.org/10.1083/jcb.123.4.1037 ] [PMID: 7693719]
[39]
Nörenberg, U.; Wille, H.; Wolff, J.M.; Frank, R.; Rathjen, F.G. The chicken neural extracellular matrix molecule restrictin: Similarity with EGF-, fibronectin type III-, and fibrinogen-like motifs. Neuron, 1992, 8(5), 849-863.
[http://dx.doi.org/10.1016/0896-6273(92)90199-N ] [PMID: 1375037]
[40]
Ghatnekar, A.; Trojanowska, M. GATA-6 is a novel transcriptional repressor of the human Tenascin-C gene expression in fibroblasts. Biochim. Biophys. Acta, 2008, 1779(3), 145-151.
[http://dx.doi.org/10.1016/j.bbagrm.2007.11.012 ] [PMID: 18177748]
[41]
Chiovaro, F.; Chiquet-Ehrismann, R.; Chiquet, M. Transcriptional regulation of tenascin genes. Cell Adhes. Migr., 2015, 9(1-2), 34-47.
[http://dx.doi.org/10.1080/19336918.2015.1008333] [PMID: 25793574]
[42]
Karvonen, U.; Jääskeläinen, T.; Rytinki, M.; Kaikkonen, S.; Palvimo, J.J. ZNF451 is a novel PML body- and SUMO-associated transcriptional coregulator. J. Mol. Biol., 2008, 382(3), 585-600.
[http://dx.doi.org/10.1016/j.jmb.2008.07.016 ] [PMID: 18656483]
[43]
Feng, Y.; Wu, H.; Xu, Y.; Zhang, Z.; Liu, T.; Lin, X.; Feng, X.H. Zinc finger protein 451 is a novel Smad corepressor in transforming growth factor-β signaling. J. Biol. Chem., 2014, 289(4), 2072-2083.
[http://dx.doi.org/10.1074/jbc.M113.526905 ] [PMID: 24324267]
[44]
Schmitz, J.; Owyang, A.; Oldham, E.; Song, Y.; Murphy, E.; McClanahan, T.K.; Zurawski, G.; Moshrefi, M.; Qin, J.; Li, X.; Gorman, D.M.; Bazan, J.F.; Kastelein, R.A. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity, 2005, 23(5), 479-490.
[http://dx.doi.org/10.1016/j.immuni.2005.09.015 ] [PMID: 16286016]
[45]
Cayrol, C.; Girard, J.P. Interleukin-33 (IL-33): A nuclear cytokine from the IL-1 family. Immunol. Rev., 2018, 281(1), 154-168.
[http://dx.doi.org/10.1111/imr.12619 ] [PMID: 29247993]
[46]
Rankin, A.L.; Mumm, J.B.; Murphy, E.; Turner, S.; Yu, N.; McClanahan, T.K.; Bourne, P.A.; Pierce, R.H.; Kastelein, R.; Pflanz, S. IL-33 induces IL-13-dependent cutaneous fibrosis. J. Immunol., 2010, 184(3), 1526-1535.
[http://dx.doi.org/10.4049/jimmunol.0903306 ] [PMID: 20042577]
[47]
Zhu, J.; Carver, W. Effects of interleukin-33 on cardiac fibroblast gene expression and activity. Cytokine, 2012, 58(3), 368-379.
[http://dx.doi.org/10.1016/j.cyto.2012.02.008 ] [PMID: 22445500]
[48]
Borthwick, L.A. The IL-1 cytokine family and its role in inflammation and fibrosis in the lung. Semin. Immunopathol., 2016, 38(4), 517-534.
[http://dx.doi.org/10.1007/s00281-016-0559-z ] [PMID: 27001429]
[49]
Rozenblit, M.; Suarez-Farinas, M.; Shemer, A.; Khattri, S.; Gilleaudeau, P.; Sullivan-Whalen, M.; Zheng, X.; Xu, H.; Cardinale, I.; Krueger, J.G.; Guttman-Yassky, E. Residual genomic profile after cyclosporine treatment may offer insights into atopic dermatitis reoccurrence. J. Allergy Clin. Immunol., 2014, 134(4), 955-957.
[http://dx.doi.org/10.1016/j.jaci.2014.05.024 ] [PMID: 24996261]
[50]
Sundnes, O.; Pietka, W.; Loos, T.; Sponheim, J.; Rankin, A.L.; Pflanz, S.; Bertelsen, V.; Sitek, J.C.; Hol, J.; Haraldsen, G.; Khnykin, D. Epidermal expression and regulation of interleukin-33 during homeostasis and inflammation: Strong species differences. J. Invest. Dermatol., 2015, 135(7), 1771-1780.
[http://dx.doi.org/10.1038/jid.2015.85 ] [PMID: 25739051]
[51]
Molofsky, A.B.; Savage, A.K.; Locksley, R.M. Interleukin-33 in tissue homeostasis, injury, and inflammation. Immunity, 2015, 42(6), 1005-1019.
[http://dx.doi.org/10.1016/j.immuni.2015.06.006 ] [PMID: 26084021]
[52]
Cayrol, C.; Girard, J.P. IL-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy. Curr. Opin. Immunol., 2014, 31, 31-37.
[http://dx.doi.org/10.1016/j.coi.2014.09.004 ] [PMID: 25278425]
[53]
Manetti, M.; Ibba-Manneschi, L.; Liakouli, V.; Guiducci, S.; Milia, A.F.; Benelli, G.; Marrelli, A.; Conforti, M.L.; Romano, E.; Giacomelli, R.; Matucci-Cerinic, M.; Cipriani, P. The IL1-like cytokine IL33 and its receptor ST2 are abnormally expressed in the affected skin and visceral organs of patients with systemic sclerosis. Ann. Rheum. Dis., 2010, 69(3), 598-605.
[http://dx.doi.org/10.1136/ard.2009.119321 ] [PMID: 19778913]
[54]
Ali, S.; Mohs, A.; Thomas, M.; Klare, J.; Ross, R.; Schmitz, M.L.; Martin, M.U. The dual function cytokine IL-33 interacts with the transcription factor NF-κB to dampen NF-κB-stimulated gene transcription. J. Immunol., 2011, 187(4), 1609-1616.
[http://dx.doi.org/10.4049/jimmunol.1003080 ] [PMID: 21734074]
[55]
Burke, S.J.; Lu, D.; Sparer, T.E.; Masi, T.; Goff, M.R.; Karlstad, M.D.; Collier, J.J. NF-κB and STAT1 control CXCL1 and CXCL2 gene transcription. Am. J. Physiol. Endocrinol. Metab., 2014, 306(2), E131-E149.
[http://dx.doi.org/10.1152/ajpendo.00347.2013 ] [PMID: 24280128]
[56]
De Plaen, I.G.; Han, X.B.; Liu, X.; Hsueh, W.; Ghosh, S.; May, M.J. Lipopolysaccharide induces CXCL2/macrophage inflammatory protein-2 gene expression in enterocytes via NF-kappaB activation: independence from endogenous TNF-alpha and plateletactivating factor. Immunology, 2006, 118(2), 153-163.
[http://dx.doi.org/10.1111/j.1365-2567.2006.02344.x] [PMID: 16771850]
[57]
Malumbres, M. Physiological relevance of cell cycle kinases. Physiol. Rev., 2011, 91(3), 973-1007.
[http://dx.doi.org/10.1152/physrev.00025.2010 ] [PMID: 21742793]
[58]
Zhang, Z.; Ren, P.; Vashisht, A.A.; Wohlschlegel, J.A.; Quintana, D.G.; Zeng, F. Cdk1-interacting protein Cip1 is regulated by the S phase checkpoint in response to genotoxic stress. Genes Cells, 2017, 22(10), 850-860.
[http://dx.doi.org/10.1111/gtc.12518 ] [PMID: 28771906]
[59]
Forsburg, S.L. Eukaryotic MCM proteins: beyond replication initiation. Microbiol. Mol. Biol. Rev., 2004, 68(1), 109-131.
[http://dx.doi.org/10.1128/MMBR.68.1.109-131.2004] [PMID: 15007098]
[60]
Lally, C.; Healy, E.; Ryan, M.P. Cyclosporine A-induced cell cycle arrest and cell death in renal epithelial cells. Kidney Int., 1999, 56(4), 1254-1257.
[http://dx.doi.org/10.1046/j.1523-1755.1999.00696.x] [PMID: 10504468]
[61]
Powell, C.M.H.; Rudge, T.L.; Zhu, Q.; Johnson, L.F.; Hansen, U. Inhibition of the mammalian transcription factor LSF induces S-phase-dependent apoptosis by downregulating thymidylate synthase expression. EMBO J., 2000, 19(17), 4665-4675.
[http://dx.doi.org/10.1093/emboj/19.17.4665 ] [PMID: 10970859]
[62]
Foucault, F.; Vaury, C.; Barakat, A.; Thibout, D.; Planchon, P.; Jaulin, C.; Praz, F.; Amor-Guéret, M. Characterization of a new BLM mutation associated with a topoisomerase II alpha defect in a patient with Bloom’s syndrome. Hum. Mol. Genet., 1997, 6(9), 1427-1434.
[http://dx.doi.org/10.1093/hmg/6.9.1427 ] [PMID: 9285778]
[63]
Pommier, Y.; Leo, E.; Zhang, H.; Marchand, C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol., 2010, 17(5), 421-433.
[http://dx.doi.org/10.1016/j.chembiol.2010.04.012 ] [PMID: 20534341]
[64]
Jin, F.; Ma, T.; Guan, H.; Yang, Z.H.; Liu, X.D.; Wang, Y.; Jiang, Y.G.; Zhou, P.K. Inhibitory effect of uranyl nitrate on DNA double-strand break repair by depression of a set of proteins in the homologous recombination pathway. Toxicol. Res. (Camb.), 2017, 6(5), 711-718.
[http://dx.doi.org/10.1039/C7TX00125H ] [PMID: 30090538]
[65]
Jean-Philippe, J.; Paz, S.; Caputi, M. hnRNP A1: the Swiss army knife of gene expression. Int. J. Mol. Sci., 2013, 14(9), 18999-19024.
[http://dx.doi.org/10.3390/ijms140918999 ] [PMID: 24065100]
[66]
Li, S.; Wang, W.; Ding, H.; Xu, H.; Zhao, Q.; Li, J.; Li, H.; Xia, W.; Su, X.; Chen, Y.; Fang, T.; Shao, N.; Zhang, H. Aptamer BC15 against heterogeneous nuclear ribonucleoprotein A1 has potential value in diagnosis and therapy of hepatocarcinoma. Nucleic Acid Ther., 2012, 22(6), 391-398.
[http://dx.doi.org/10.1089/nat.2012.0363 ] [PMID: 23062008]
[67]
IARC Monographs on the evaluation of carcinogenic risks to humans, international agency for research on cancer working group on the evaluation of carcinogenic risk to humans. Lyon (FR), 2012, 100A

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