Generic placeholder image

Current Pharmaceutical Biotechnology

Author(s): Maciej Dąbala*, Magdalena Świder, Tomasz Kasela, Paulina Buda and Beniamin Oskar Grabarek

DOI: 10.2174/1389201024666230407122254

DownloadDownload PDF Flyer Cite As
Variances in the Expression Profile of DUSP1-7 and miRNAs Regulating their Expression in the HaCat Line under LPS and Cyclosporine A

Page: [1952 - 1963] Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

Introduction: Cyclosporin A (CsA) treats moderate to severe psoriasis vulgaris. Psoriasis is a chronic inflammatory disease in which hyperproliferation of keratinocytes occurs. One of the most relevant signaling cascades in the development of psoriasis is the mitogen-activated protein kinase (MAPK) signaling pathway. It has been observed that dual-specificity phosphatases (DUSPs) dephosphorylate signaling molecules, such as MAPKs.

Aims: This study aims to determine changes in the expression pattern of Dual Activity Protein Phosphatase (DUSP1-7) and micro RNAs (miRNAs), potentially regulating their expression in the human adult, low-calcium, high-temperature keratinocytes cell line (HaCaT) cultures exposed to lipopolysaccharide A (LPS)-induced inflammation, followed by CsA.

Methods: HaCaT cell line was exposed for 8 hours to 1 μg/mL LPS and then to 100 ng/mL CsA for 2, 8, and 24 hours compared to cultures not exposed to LPS and the drug. The molecular analysis included determining the DUSP1-7 expression and the miRNAs potentially regulating it using an expression microarray technique. An enzyme-linked immunosorbent assay (ELISA) was also performed to assess the concentration of DUSP1-7 in the culture medium. Statistical evaluation was performed assuming a statistical significance threshold (p) of < 0.05.

Results: Statistically significant differences were found in the expression of DUSP1-7 mRNAs and the miRNAs that regulate their expression. The most significant changes in expression were observed for DUSP1 and DUSP5, with the differences being most pronounced during the eighthour incubation period of the cells, with the drug predictive analysis showing that miR-34 potentially regulates the expression of DUSP1-4,7, miR-1275: DUSP2, mir-3188: DUSP4, miR-382: DUSP4, miR-27a and miR-27b: DUSP5,6 and miR-16: DUSP7. No expression of DUSP1-7 was demonstrated at the protein level in CsA-exposed cultures.

Conclusion: Our evaluation of the efficacy of CsA therapy on an in vitro model of HaCaT indicates that treatment with this drug is effective, resulting in changes in the expression of DUSP1-7 and, potentially, the miRNAs that regulate their expression. We also confirmed that the different expression pattern of mRNA and protein encoded by a given transcript is not only due to the regulatory role of miRNAs but also the lack of synchronization between transcription and translation processes.

Graphical Abstract

[1]
Onsun, N.; Pirmit, S.; Ozkaya, D.; Çelik, Ş.; Rezvani, A.; Cengiz, F.P.; Kekik, C. The HLA-Cw12 allele is an important susceptibility allele for psoriasis and is associated with resistant psoriasis in the turkish population. Sci. World J., 2019, 2019, 1-5.
[http://dx.doi.org/10.1155/2019/7848314] [PMID: 31341424]
[2]
Sakurai, K.; Dainichi, T.; Garcet, S.; Tsuchiya, S.; Yamamoto, Y.; Kitoh, A.; Honda, T.; Nomura, T.; Egawa, G.; Otsuka, A.; Nakajima, S.; Matsumoto, R.; Nakano, Y.; Otsuka, M.; Iwakura, Y.; Grinberg-Bleyer, Y.; Ghosh, S.; Sugimoto, Y.; Guttman-Yassky, E.; Krueger, J.G.; Kabashima, K. Cutaneous p38 mitogen-activated protein kinase activation triggers psoriatic dermatitis. J. Allergy Clin. Immunol., 2019, 144(4), 1036-1049.
[http://dx.doi.org/10.1016/j.jaci.2019.06.019] [PMID: 31378305]
[3]
Zhao, W.; Xiao, S.; Li, H.; Zheng, T.; Huang, J.; Hu, R.; Zhang, B.; Liu, X.; Huang, G. MAPK Phosphatase-1 deficiency exacerbates the severity of imiquimod-induced psoriasiform skin disease. Front. Immunol., 2018, 9, 569.
[http://dx.doi.org/10.3389/fimmu.2018.00569] [PMID: 29619028]
[4]
Mavropoulos, A.; Rigopoulou, E.I.; Liaskos, C.; Bogdanos, D.P.; Sakkas, L.I. The role of p38 MAPK in the aetiopathogenesis of psoriasis and psoriatic arthritis. Clin. Dev. Immunol., 2013, 2013, 1-8.
[http://dx.doi.org/10.1155/2013/569751] [PMID: 24151518]
[5]
Chen, H.F.; Chuang, H.C.; Tan, T.H. Regulation of Dual-Specificity Phosphatase (DUSP) ubiquitination and protein stability. Int. J. Mol. Sci., 2019, 20(11), 2668.
[http://dx.doi.org/10.3390/ijms20112668] [PMID: 31151270]
[6]
Karlsson, M.; Mathers, J.; Dickinson, R.J.; Mandl, M.; Keyse, S.M. Both nuclear-cytoplasmic shuttling of the dual specificity phosphatase MKP-3 and its ability to anchor MAP kinase in the cytoplasm are mediated by a conserved nuclear export signal. J. Biol. Chem., 2004, 279(40), 41882-41891.
[http://dx.doi.org/10.1074/jbc.M406720200] [PMID: 15269220]
[7]
Huang, C.Y.; Tan, T.H. DUSPs, to MAP kinases and beyond. Cell Biosci., 2012, 2(1), 24.
[http://dx.doi.org/10.1186/2045-3701-2-24] [PMID: 22769588]
[8]
Chuang, H-C.; Tan, T-H. MAP4K family kinases and DUSP family phosphatases in T-cell signaling and systemic lupus erythematosus. Cells, 2019, 8(11), 1433.
[http://dx.doi.org/10.3390/cells8111433] [PMID: 31766293]
[9]
Sun, F.; Yue, T.T.; Yang, C.L.; Wang, F.X.; Luo, J.H.; Rong, S.J.; Zhang, M.; Guo, Y.; Xiong, F.; Wang, C.Y. The MAPK dual specific phosphatase (DUSP) proteins: A versatile wrestler in T cell functionality. Int. Immunopharmacol., 2021, 98, 107906.
[http://dx.doi.org/10.1016/j.intimp.2021.107906] [PMID: 34198238]
[10]
O’Brien, J.; Hayder, H.; Zayed, Y.; Peng, C. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front. Endocrinol., 2018, 9, 402.
[http://dx.doi.org/10.3389/fendo.2018.00402] [PMID: 30123182]
[11]
Ali Syeda, Z.; Langden, S.S.S.; Munkhzul, C.; Lee, M.; Song, S.J. Regulatory mechanism of microrna expression in cancer. Int. J. Mol. Sci., 2020, 21(5), 1723.
[http://dx.doi.org/10.3390/ijms21051723] [PMID: 32138313]
[12]
Arora, A.; Simpson, D.A.C. Individual mRNA expression profiles reveal the effects of specific microRNAs. Genome Biol., 2008, 9(5), R82.
[http://dx.doi.org/10.1186/gb-2008-9-5-r82] [PMID: 18485210]
[13]
Reich, A.; Adamski, Z.; Chodorowska, G.; Kaszuba, A.; Krasowska, D.; Lesiak, A.; Maj, J.; Narbutt, J.; Osmola-Mańkowska, A.J.; Owczarczyk-Saczonek, A.; Owczarek, W.; Placek, W.J.; Rudnicka, L.; Szepietowski, J. Psoriasis. Diagnostic and therapeutic recommendations of the polish dermatological society. Part 1. Przegl. Dermatol., 2020, 107(2), 92-108.
[http://dx.doi.org/10.5114/dr.2020.95258]
[14]
Reich, A.; Adamski, Z.; Chodorowska, G.; Kaszuba, A.; Krasowska, D.; Lesiak, A.; Maj, J.; Narbutt, J.; Osmola-Mańkowska, A.J.; Owczarczyk-Saczonek, A.; Owczarek, W.; Placek, W.J.; Rudnicka, L.; Szepietowski, J. Psoriasis. Diagnostic and therapeutic recommendations of the polish dermatological society. Part 2. Przegl. Dermatol., 2020, 107(2), 110-137.
[http://dx.doi.org/10.5114/dr.2020.95259]
[15]
Zhou, L.L.; Georgakopoulos, J.R.; Ighani, A.; Yeung, J. Systemic monotherapy treatments for generalized pustular psoriasis: A systematic review. J. Cutan. Med. Surg., 2018, 22(6), 591-601.
[http://dx.doi.org/10.1177/1203475418773358] [PMID: 29707979]
[16]
Matsuda, S.; Koyasu, S. Mechanisms of action of cyclosporine. Immunopharmacology, 2000, 47(2-3), 119-125.
[http://dx.doi.org/10.1016/S0162-3109(00)00192-2] [PMID: 10878286]
[17]
Molyvdas, A.; Matalon, S. Cyclosporine: An old weapon in the fight against Coronaviruses. Eur. Respir. J., 2020, 56(5), 2002484.
[http://dx.doi.org/10.1183/13993003.02484-2020] [PMID: 32732332]
[18]
Kasela, T.; Dąbala, M.; Mistarz, M.; Wieczorek, W.; Wierzbik-Strońska, M.; Boroń, K.; Zawidlak-Węgrzyńska, B.; Oskar Grabarek, B. Effects of Cyclosporine A and Adalimumab on the expression profiles histaminergic system-associated genes and microRNAs regulating these genes in HaCaT cells. Cell Cycle, 2022, 21(23), 2499-2516.
[http://dx.doi.org/10.1080/15384101.2022.2103342] [PMID: 35899934]
[19]
Adwent, I.; Grabarek, B.O.; Kojs-Mrożkiewicz, M.; Brus, R.; Staszkiewicz, R.; Plewka, A.; Stasiowski, M.; Lyssek-Boroń, A. The influence of Adalimumab and Cyclosporine A on the expression profile of the genes related to TGF β signaling pathways in keratinocyte cells treated with lipopolysaccharide A. Mediators Inflamm., 2020, 2020, 1-11.
[http://dx.doi.org/10.1155/2020/3821279]
[20]
Adwent, I.; Schweizer, M.; Grabarek, B.O.; Boroń, D. Effect of adalimumab on the expression profile of MRNA, and protein associated with JAK/STAT signaling pathway in fibroblast exposed to lipopolysaccharide. Dermatol. Ther., 2020, 33(3), e13400.
[http://dx.doi.org/10.1111/dth.13400] [PMID: 32276291]
[21]
Grabarek, B.; Schweizer, P.; Adwent, I.; Wcisło-Dziadecka, D.; Krzaczyński, J.; Kruszniewska-Rajs, C.; Gola, J. Differences in expression of genes related to drug resistance and miRNAs regulating their expression in skin fibroblasts exposed to adalimumab and cyclosporine A. Postepy Dermatol. Alergol., 2021, 38(2), 249-255.
[http://dx.doi.org/10.5114/ada.2019.91506]
[22]
Grabarek, B.; Wcislo-Dziadecka, D.; Gola, J.; Kruszniewska-Rajs, C.; Brzezinska-Wcislo, L.; Zmarzly, N.; Mazurek, U. Changes in the expression profile of JAK/STAT signaling pathway genes and mirnas regulating their expression under the adalimumab therapy. Curr. Pharm. Biotechnol., 2018, 19(7), 556-565.
[http://dx.doi.org/10.2174/1389201019666180730094046] [PMID: 30058482]
[23]
Agarwal, V.; Bell, G.W.; Nam, J.W.; Bartel, D.P. Predicting effective microRNA target sites in mammalian mRNAs. eLife, 2015, 4, e05005.
[http://dx.doi.org/10.7554/eLife.05005] [PMID: 26267216]
[24]
Chen, Y.; Wang, X. miRDB: An online database for prediction of functional microRNA targets. Nucleic Acids Res., 2020, 48(D1), D127-D131.
[http://dx.doi.org/10.1093/nar/gkz757] [PMID: 31504780]
[25]
Liu, W.; Wang, X. Prediction of functional microRNA targets by integrative modeling of microRNA binding and target expression data. Genome Biol., 2019, 20(1), 18.
[http://dx.doi.org/10.1186/s13059-019-1629-z] [PMID: 30670076]
[26]
Harden, J.L.; Krueger, J.G.; Bowcock, A.M. The immunogenetics of Psoriasis: A comprehensive review. J. Autoimmun., 2015, 64, 66-73.
[http://dx.doi.org/10.1016/j.jaut.2015.07.008] [PMID: 26215033]
[27]
Anna, P.; Anna, C.; Stanisz-Wallis, K. Agnieszka, Zagórska application of biological drugs in psoriasis therapy. Postepy Hig. Med. Dosw., 2018, 72, 642-658.
[28]
Wcisło-Dziadecka, D.; Zbiciak, M.; Brzezińska-Wcisło, L.; Mazurek, U. Anti-cytokine therapy for psoriasis-not only TNF-α blockers. Overview of reports on the effectiveness of therapy with IL-12/IL-23 and T and B lymphocyte inhibitors. Postepy Hig. Med. Dosw., 2016, 70(0), 1198-1205.
[PMID: 28026823]
[29]
Jain, H.; Bhat, A.R.; Dalvi, H.; Godugu, C.; Singh, S.B.; Srivastava, S. Repurposing approved therapeutics for new indication: Addressing unmet needs in psoriasis treatment. Curr. Res. Pharmacol. Drug Discov., 2021, 2, 100041.
[http://dx.doi.org/10.1016/j.crphar.2021.100041] [PMID: 34909670]
[30]
Grabarek, B.O.; Dąbala, M.; Kasela, T.; Gralewski, M.; Gładysz, D. Changes in the expression pattern of DUSP1-7 and miRNA regulating their expression in the keratinocytes treated with LPS and adalimumab. Curr. Pharm. Biotechnol., 2022, 23(6), 873-881.
[http://dx.doi.org/10.2174/1389201022666210802102508] [PMID: 34342258]
[31]
Krawczyk, A.; Strzałka-Mrozik, B.; Juszczyk, K.; Kimsa-Dudek, M.; Wcisło-Dziadecka, D.; Gola, J. The MAP2K2 gene as potential diagnostic marker in monitoring adalimumab therapy of psoriatic arthritis. Curr. Pharm. Biotechnol., 2023, 24(2), 330-340.
[32]
Gorelik, G.; Richardson, B. Key role of ERK pathway signaling in lupus. Autoimmunity, 2010, 43(1), 17-22.
[http://dx.doi.org/10.3109/08916930903374832] [PMID: 19961364]
[33]
Schett, G.; Zwerina, J.; Firestein, G. The p38 mitogen-activated protein kinase (MAPK) pathway in rheumatoid arthritis. Ann. Rheum. Dis., 2008, 67(7), 909-916.
[http://dx.doi.org/10.1136/ard.2007.074278] [PMID: 17827184]
[34]
Poulikakos, P.I.; Solit, D.B. Resistance to MEK inhibitors: Should we co-target upstream? Sci. Signal., 2011, 4(166), pe16.
[http://dx.doi.org/10.1126/scisignal.2001948] [PMID: 21447797]
[35]
Chen, J.; Yuan, F.; Fan, X.; Wang, Y. Psoriatic arthritis: A systematic review of non‐HLA genetic studies and important signaling pathways. Int. J. Rheum. Dis., 2020, 23(10), 1288-1296.
[http://dx.doi.org/10.1111/1756-185X.13879] [PMID: 32761870]
[36]
Vogel, C.; Marcotte, E.M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet., 2012, 13(4), 227-232.
[http://dx.doi.org/10.1038/nrg3185] [PMID: 22411467]
[37]
Haider, S.; Pal, R. Integrated analysis of transcriptomic and proteomic data. Curr. Genomics, 2013, 14(2), 91-110.
[http://dx.doi.org/10.2174/1389202911314020003] [PMID: 24082820]
[38]
Rogers, S.; Girolami, M.; Kolch, W.; Waters, K.M.; Liu, T.; Thrall, B.; Wiley, H.S. Investigating the correspondence between transcriptomic and proteomic expression profiles using coupled cluster models. Bioinformatics, 2008, 24(24), 2894-2900.
[http://dx.doi.org/10.1093/bioinformatics/btn553] [PMID: 18974169]
[39]
Kristensen, A.R.; Gsponer, J.; Foster, L.J. Protein synthesis rate is the predominant regulator of protein expression during differentiation. Mol. Syst. Biol., 2013, 9(1), 689.
[http://dx.doi.org/10.1038/msb.2013.47] [PMID: 24045637]
[40]
Mehdi, A.M.; Patrick, R.; Bailey, T.L.; Bodén, M. Predicting the dynamics of protein abundance. Mol. Cell. Proteomics, 2014, 13(5), 1330-1340.
[http://dx.doi.org/10.1074/mcp.M113.033076] [PMID: 24532840]
[41]
Tuller, T.; Kupiec, M.; Ruppin, E. Determinants of protein abundance and translation efficiency in S. cerevisiae. PLOS Comput. Biol., 2007, 3(12), e248.
[http://dx.doi.org/10.1371/journal.pcbi.0030248] [PMID: 18159940]
[42]
Perl, K.; Ushakov, K.; Pozniak, Y.; Yizhar-Barnea, O.; Bhonker, Y.; Shivatzki, S.; Geiger, T.; Avraham, K.B.; Shamir, R. Reduced changes in protein compared to mRNA levels across non-proliferating tissues. BMC Genomics, 2017, 18(1), 305.
[http://dx.doi.org/10.1186/s12864-017-3683-9] [PMID: 28420336]
[43]
Zhang, Y.; Reynolds, J.M.; Chang, S.H.; Martin-Orozco, N.; Chung, Y.; Nurieva, R.I.; Dong, C. MKP-1 is necessary for T cell activation and function. J. Biol. Chem., 2009, 284(45), 30815-30824.
[http://dx.doi.org/10.1074/jbc.M109.052472] [PMID: 19748894]
[44]
Najar, M.; Fayyad-Kazan, H.; Faour, W.H.; Merimi, M.; Sokal, E.M.; Lombard, C.A.; Fahmi, H. Immunological modulation following bone marrow-derived mesenchymal stromal cells and Th17 lymphocyte co-cultures. Inflamm. Res., 2019, 68(3), 203-213.
[http://dx.doi.org/10.1007/s00011-018-1205-0] [PMID: 30506263]
[45]
Delmas, D.; Limagne, E.; Ghiringhelli, F.; Aires, V. Immune Th17 lymphocytes play a critical role in the multiple beneficial properties of resveratrol. Food Chem. Toxicol., 2020, 137, 111091.
[http://dx.doi.org/10.1016/j.fct.2019.111091] [PMID: 31883989]
[46]
Georgescu, S.R.; Tampa, M.; Caruntu, C.; Sarbu, M.I.; Mitran, C.I.; Mitran, M.I.; Matei, C.; Constantin, C.; Neagu, M. Advances in understanding the immunological pathways in psoriasis. Int. J. Mol. Sci., 2019, 20(3), 739.
[http://dx.doi.org/10.3390/ijms20030739] [PMID: 30744173]
[47]
Kanemaru, H.; Yamane, F.; Tanaka, H.; Maeda, K.; Satoh, T.; Akira, S. BATF2 activates DUSP2 gene expression and upregulates NF-κB activity via phospho-STAT3 dephosphorylation. Int. Immunol., 2018, 30(6), 255-265.
[http://dx.doi.org/10.1093/intimm/dxy023] [PMID: 29534174]
[48]
Grabarek, B.O.; Wcisło-Dziadecka, D.; Michalska-Bańkowska, A.; Gola, J. Evaluation of expression pattern of selected genes associated with IL12/23 signaling paths in psoriatic patients during cyclosporine A therapy. Dermatol. Ther., 2019, 32(6), e13129.
[http://dx.doi.org/10.1111/dth.13129] [PMID: 31631469]
[49]
Xin, P.; Xu, X.; Deng, C.; Liu, S.; Wang, Y.; Zhou, X.; Ma, H.; Wei, D.; Sun, S. The role of JAK/STAT signaling pathway and its inhibitors in diseases. Int. Immunopharmacol., 2020, 80, 106210.
[http://dx.doi.org/10.1016/j.intimp.2020.106210] [PMID: 31972425]
[50]
Hu, X.; li, J..; Fu, M.; Zhao, X.; Wang, W. The JAK/STAT signaling pathway: From bench to clinic. Signal Transduct. Target. Ther., 2021, 6(1), 402.
[http://dx.doi.org/10.1038/s41392-021-00791-1] [PMID: 34824210]
[51]
Lu, D.; Liu, L.; Ji, X.; Gao, Y.; Chen, X.; Liu, Y.; Liu, Y.; Zhao, X.; Li, Y.; Li, Y.; Jin, Y.; Zhang, Y.; McNutt, M.A.; Yin, Y. The phosphatase DUSP2 controls the activity of the transcription activator STAT3 and regulates TH17 differentiation. Nat. Immunol., 2015, 16(12), 1263-1273.
[http://dx.doi.org/10.1038/ni.3278] [PMID: 26479789]
[52]
Hamamura, K.; Nishimura, A.; Chen, A.; Takigawa, S.; Sudo, A.; Yokota, H. Salubrinal acts as a Dusp2 inhibitor and suppresses inflammation in anti-collagen antibody-induced arthritis. Cell. Signal., 2015, 27(4), 828-835.
[http://dx.doi.org/10.1016/j.cellsig.2015.01.010] [PMID: 25619567]
[53]
Mrowka, R. Recent advances in kidney research. Acta Physiol., 2022, 235(2), e13820.
[http://dx.doi.org/10.1111/apha.13820] [PMID: 35403838]
[54]
Huang, C.Y.; Lin, Y.C.; Hsiao, W.Y.; Liao, F.H.; Huang, P.Y.; Tan, T.H. DUSP4 deficiency enhances CD25 expression and CD4 + T-cell proliferation without impeding T-cell development. Eur. J. Immunol., 2012, 42(2), 476-488.
[http://dx.doi.org/10.1002/eji.201041295] [PMID: 22101742]
[55]
Loh, C.Y.; Arya, A.; Naema, A.F.; Wong, W.F.; Sethi, G.; Looi, C.Y. Signal transducer and activator of transcription (STATs) proteins in cancer and inflammation: Functions and therapeutic implication. Front. Oncol., 2019, 9, 48.
[http://dx.doi.org/10.3389/fonc.2019.00048] [PMID: 30847297]
[56]
Clevenger, C.V. Roles and regulation of stat family transcription factors in human breast cancer. Am. J. Pathol., 2004, 165(5), 1449-1460.
[http://dx.doi.org/10.1016/S0002-9440(10)63403-7] [PMID: 15509516]
[57]
Wan-Yi, H.; Yu-Chun, L.; Fang-Hsuean, L.; Yi-Chiao, C.; Ching-Yu, H. Dual-specificity phosphatase 4 regulates STAT5 protein stability and helper T cell polarization. PLoS One., 2015, 10(12), e0145880.
[58]
Johar, A.S.; Mastronardi, C.; Rojas-Villarraga, A.; Patel, H.R.; Chuah, A.; Peng, K.; Higgins, A.; Milburn, P.; Palmer, S.; Silva-Lara, M.F.; Velez, J.I.; Andrews, D.; Field, M.; Huttley, G.; Good-now, C.; Anaya, J.M.; Arcos-Burgos, M. Novel and rare functional genomic variants in multiple autoimmune syndrome and Sjögren’s syndrome. J. Transl. Med., 2015, 13(1), 173.
[http://dx.doi.org/10.1186/s12967-015-0525-x] [PMID: 26031516]
[59]
Liu, T.; Sun, H.; Liu, S.; Yang, Z.; Li, L.; Yao, N.; Cheng, S.; Dong, X.; Liang, X.; Chen, C.; Wang, Y.; Zhao, X. The suppression of DUSP5 expression correlates with paclitaxel resistance and poor prognosis in basal-like breast cancer. Int. J. Med. Sci., 2018, 15(7), 738-747.
[http://dx.doi.org/10.7150/ijms.24981] [PMID: 29910679]
[60]
Yan, X.; Liu, L.; Li, H.; Huang, L.; Yin, M.; Pan, C.; Qin, H.; Jin, Z. Dual specificity phosphatase 5 is a novel prognostic indicator for patients with advanced colorectal cancer. Am. J. Cancer Res., 2016, 6(10), 2323-2333.
[PMID: 27822421]
[61]
Bray, R.A.; Gebel, H.M.; Townsend, R.; Roberts, M.E.; Polinsky, M.; Yang, L.; Meier-Kriesche, H.U.; Larsen, C.P. Posttransplant reduction in preexisting donor-specific antibody levels after belatacept- versus cyclosporine-based immunosuppression: Post hoc analyses of BENEFIT and BENEFIT-EXT. Am. J. Transplant., 2018, 18(7), 1774-1782.
[http://dx.doi.org/10.1111/ajt.14738] [PMID: 29573335]
[62]
Mishra, A.; Oulès, B.; Pisco, A.O.; Ly, T.; Liakath-Ali, K.; Walko, G.; Viswanathan, P.; Tihy, M.; Nijjher, J.; Dunn, S.J.; Lamond, A.I.; Watt, F.M. A protein phosphatase network controls the temporal and spatial dynamics of differentiation commitment in human epidermis. eLife, 2017, 6, e27356.
[http://dx.doi.org/10.7554/eLife.27356] [PMID: 29043977]
[63]
Furukawa, T.; Tanji, E.; Xu, S.; Horii, A. Feedback regulation of DUSP6 transcription responding to MAPK1 via ETS2 in human cells. Biochem. Biophys. Res. Commun., 2008, 377(1), 317-320.
[http://dx.doi.org/10.1016/j.bbrc.2008.10.003] [PMID: 18848526]
[64]
Piya, S.; Kim, J.Y.; Bae, J.; Seol, D.W.; Moon, A.R.; Kim, T.H. DUSP6 is a novel transcriptional target of p53 and regulates p53-mediated apoptosis by modulating expression levels of Bcl-2 family proteins. FEBS Lett., 2012, 586(23), 4233-4240.
[http://dx.doi.org/10.1016/j.febslet.2012.10.031] [PMID: 23108049]
[65]
Muhammad, K.A.; Nur, A.A.; Nurul, H.S.; Narazah, M.Y.; Siti, R.A.R. Dual-specificity phosphatase 6 (DUSP6): A review of its molecular characteristics and clinical relevance in cancer. Cancer Biol. Med., 2018, 15(1), 14-28.
[http://dx.doi.org/10.20892/j.issn.2095-3941.2017.0107] [PMID: 29545965]
[66]
Addison, R.; Weatherhead, S.C.; Pawitri, A.; Smith, G.R.; Rider, A.; Grantham, H.J.; Cockell, S.J.; Reynolds, N.J. Therapeutic wavelengths of ultraviolet B radiation activate apoptotic, circadian rhythm, redox signalling and key canonical pathways in psoriatic epidermis. Redox Biol., 2021, 41, 101924.
[http://dx.doi.org/10.1016/j.redox.2021.101924] [PMID: 33812333]
[67]
Castro-Sánchez, P.; Ramirez-Munoz, R.; Lamana, A.; Ortiz, A.; González-Álvaro, I.; Roda-Navarro, P. mRNA profilin identifies low levels of phosphatases dual-specific phosphatase-7 (DUSP7) and cell division cycle-25B (CDC25B) in patients with early arthritis. Clin. Exp. Immunol., 2017, 189(1), 113-119.
[http://dx.doi.org/10.1111/cei.12953] [PMID: 28253537]
[68]
Xu, G.; Song, J.; Gokulnath, P.; Vulugundam, G.; Xiao, J. DUSP7: An unusual player in adverse cardiac remodeling. J. of Cardiovasc. Trans. Res., 2022.
[http://dx.doi.org/10.1007/s12265-022-10274-5]
[69]
Ludwig, N.; Leidinger, P.; Becker, K.; Backes, C.; Fehlmann, T.; Pallasch, C.; Rheinheimer, S.; Meder, B.; Stähler, C.; Meese, E.; Keller, A. Distribution of miRNA expression across human tissues. Nucleic Acids Res., 2016, 44(8), 3865-3877.
[http://dx.doi.org/10.1093/nar/gkw116] [PMID: 26921406]
[70]
Farr, R.J.; Rootes, C.L.; Rowntree, L.C.; Ngayen, T.H.O.; Hensen, L.; Kedzierski, L.; Cheng, A.C.; Kedzierska, K.; Au, G.G.; Marsh, G.A.; Vasan, S.S.; Foo, C.H.; Cowled, C.; Stewart, C.R. Altered microRNA expression in COVID-19 patients enables identification of SARS-CoV-2 infection. PLoS Pathog., 2021, 17(7), e1009759.
[71]
Lin, C-A.; Duan, K-Y.; Wang, X-W.; Zhang, Z-S. Study on the role of Hsa-miR-382-5p in epidural fibrosis. Eur. Rev. Med. Pharmacol. Sci., 2018, 22(12), 3663-3668.
[http://dx.doi.org/10.26355/eurrev_201806_15244] [PMID: 29949138]
[72]
Alatas, E.T.; Kara, M.; Dogan, G.; Akın Belli, A. Blood microRNA expressions in patients with mild to moderate psoriasis and the relationship between microRNAs and psoriasis activity. An. Bras. Dermatol., 2020, 95(6), 702-707.
[http://dx.doi.org/10.1016/j.abd.2020.07.001] [PMID: 32811699]