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Current Pharmaceutical Biotechnology

Editor-in-Chief

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

Research Article

Immunohistochemical Expression of the SERPINA3 Protein in Uterine Fibroids

Author(s): Mateusz de Mezer*, Anna Markowska, Janina Markowska, Monika Krzyżaniak, Beniamin Oskar Grabarek, Filip Pokusa and Jakub Żurawski

Volume 25, Issue 13, 2024

Published on: 09 January, 2024

Page: [1758 - 1765] Pages: 8

DOI: 10.2174/0113892010264673231111082438

Price: $65

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Abstract

Background: SERPINA3 (α-1-antichymotrypsin, AACT, ACT) is produced by the liver and released into plasma in an anti-inflammatory response and plays a role as a modulator of extracellular matrix (ECM) by inhibiting serine proteases. Numerous studies proved an increased level of SERPINA3 in many types of cancer, which could be linked to SERPINA3’s anti-apoptotic function.

Aim: In the context of progressive ECM fibrosis during the development of uterine fibroids, which are one of the most common hypertrophic changes within the uterus, it is interesting to describe the level of SERPINA3 protein in this type of lesion and the surrounding tissues.

Methods: We used immunohistochemical staining of the SERPINA3 protein and compared the intensity of the signal between the myoma tissue and the surrounding normal tissue.

Results: We showed a surprising reduction in the amount of the SERPINA3 protein within uterine fibroids compared to surrounding tissues.

Conclusion: This observation sheds new light on the role of this protein in the formation of proliferative changes and suggests that understanding the mechanism of its action may become the basis for the development of new diagnostic and therapeutic tools.

Keywords: SERPINA3, α-1-antichymotrypsin (AACT, ACT), extracellular matrix (ECM), uterine fibroids, myoma, monoclonal tumors, complications in childbirth.

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[1]
Stewart, E.A.; Cookson, C.L.; Gandolfo, R.A.; Schulze-Rath, R. Epidemiology of uterine fibroids: A systematic review. BJOG, 2017, 124(10), 1501-1512.
[http://dx.doi.org/10.1111/1471-0528.14640] [PMID: 28296146]
[2]
Vilos, G.A.; Allaire, C.; Laberge, P.Y.; Leyland, N.; Vilos, A.G.; Murji, A.; Chen, I. The management of uterine leiomyomas. J. Obstet. Gynaecol. Can., 2015, 37(2), 157-178.
[http://dx.doi.org/10.1016/S1701-2163(15)30338-8] [PMID: 25767949]
[3]
Pavone, D.; Clemenza, S.; Sorbi, F.; Fambrini, M.; Petraglia, F. Epidemiology and risk factors of uterine fibroids. Best Pract. Res. Clin. Obstet. Gynaecol., 2018, 46, 3-11.
[http://dx.doi.org/10.1016/j.bpobgyn.2017.09.004] [PMID: 29054502]
[4]
Reis, F.M.; Bloise, E.; Ortiga-Carvalho, T.M. Hormones and pathogenesis of uterine fibroids. Best Pract. Res. Clin. Obstet. Gynaecol., 2016, 34, 13-24.
[http://dx.doi.org/10.1016/j.bpobgyn.2015.11.015] [PMID: 26725037]
[5]
Moravek, M.B.; Yin, P.; Ono, M.; Coon V, J.S.; Dyson, M.T.; Navarro, A.; Marsh, E.E.; Chakravarti, D.; Kim, J.J.; Wei, J.J.; Bulun, S.E. Ovarian steroids, stem cells and uterine leiomyoma: Therapeutic implications. Hum. Reprod. Update, 2015, 21(1), 1-12.
[http://dx.doi.org/10.1093/humupd/dmu048] [PMID: 25205766]
[6]
Islam, M.S.; Ciavattini, A.; Petraglia, F.; Castellucci, M.; Ciarmela, P. Extracellular matrix in uterine leiomyoma pathogenesis: A potential target for future therapeutics. Hum. Reprod. Update, 2018, 24(1), 59-85.
[http://dx.doi.org/10.1093/humupd/dmx032] [PMID: 29186429]
[7]
Cardozo, E.R.; Foster, R.; Karmon, A.E.; Lee, A.E.; Gatune, L.W.; Rueda, B.R.; Styer, A.K. MicroRNA 21a-5p overexpression impacts mediators of extracellular matrix formation in uterine leiomyoma. Reprod. Biol. Endocrinol., 2018, 16(1), 46.
[http://dx.doi.org/10.1186/s12958-018-0364-8] [PMID: 29747655]
[8]
Carneiro, M.M. Stem cells and uterine leiomyomas: What is the evidence? JBRA Assist. Reprod., 2016, 20(1), 33-37.
[http://dx.doi.org/10.5935/1518-0557.20160008] [PMID: 27203304]
[9]
Cetin, E.; Al-Hendy, A.; Ciebiera, M. Non-hormonal mediators of uterine fibroid growth. Curr. Opin. Obstet. Gynecol., 2020, 32(5), 361-370.
[http://dx.doi.org/10.1097/GCO.0000000000000650] [PMID: 32739973]
[10]
Galindo, L.J.; Hernández-Beeftink, T.; Salas, A.; Jung, Y.; Reyes, R.; de Oca, F.M.; Hernández, M.; Almeida, T.A. HMGA2 and MED12 alterations frequently co-occur in uterine leiomyomas. Gynecol. Oncol., 2018, 150(3), 562-568.
[http://dx.doi.org/10.1016/j.ygyno.2018.07.007] [PMID: 30017537]
[11]
Liu, X.; Liu, Y.; Zhao, J.; Liu, Y. Screening of potential biomarkers in uterine leiomyomas disease via gene expression profiling analysis. Mol. Med. Rep., 2018, 17(5), 6985-6996.
[http://dx.doi.org/10.3892/mmr.2018.8756] [PMID: 29568968]
[12]
Moravek, M.; Yin, P.; Ono, M.; Coon, V. J.; Dyson, M.; Navarro, A.; Marsh, E.; Zhao, H.; Maruyama, T.; Chakravarti, D.; Kim, J.; Wei, J-J.; Bulun, S. Uterine leiomyoma stem cells: Linking progesterone to growth. Semin. Reprod. Med., 2015, 33(5), 357-365.
[http://dx.doi.org/10.1055/s-0035-1558451] [PMID: 26251118]
[13]
Mäkinen, N.; Kämpjärvi, K.; Frizzell, N.; Bützow, R.; Vahteristo, P. Characterization of MED12, HMGA2, and FH alterations reveals molecular variability in uterine smooth muscle tumors. Mol. Cancer, 2017, 16(1), 101.
[http://dx.doi.org/10.1186/s12943-017-0672-1] [PMID: 28592321]
[14]
Lewis, T.D.; Malik, M.; Britten, J.; San Pablo, A.M.; Catherino, W.H. A comprehensive review of the pharmacologic management of uterine leiomyoma. BioMed Res. Int., 2018, 2018, 1-11.
[http://dx.doi.org/10.1155/2018/2414609] [PMID: 29780819]
[15]
Rizzello, A.; Franck, J.; Pellegrino, M.; Nuccio, F.; Simeone, P.; Fiore, G.; Tommaso, S.; Malvasi, A.; Tinelli, A.; Fournier, I.; Salzet, M.; Maffia, M.; Vergara, D. A proteomic analysis of human uterine myoma. Curr. Protein Pept. Sci., 2016, 18(2), 167-174.
[http://dx.doi.org/10.2174/1389203717666160322150603] [PMID: 27001059]
[16]
Travis, J.; Bowen, J.; Baugh, R. Human α-1-antichymotrypsin: Interaction with chymotrypsin-like proteinases. Biochemistry, 1978, 17(26), 5651-5656.
[http://dx.doi.org/10.1021/bi00619a011] [PMID: 728423]
[17]
Sanchez-Navarro, A.; González-Soria, I.; Caldiño-Bohn, R.; Bobadilla, N.A. An integrative view of serpins in health and disease: The contribution of SerpinA3. Am. J. Physiol. Cell Physiol., 2020, 320(1), C106-C118.
[http://dx.doi.org/10.1152/ajpcell.00366.2020]
[18]
Sun, Y-X.; Wright, H.T.; Janciauskiene, S. Alpha1-antichymotrypsin/Alzheimer’s peptide Abeta(1-42) complex perturbs lipid metabolism and activates transcription factors PPARgamma and NFkappaB in human neuroblastoma (Kelly) cells. J. Neurosci. Res., 2002, 67(4), 511-522.
[http://dx.doi.org/10.1002/jnr.10144] [PMID: 11835318]
[19]
Duranton, J.; Boudier, C.; Belorgey, D.; Mellet, P.; Bieth, J.G. DNA strongly impairs the inhibition of cathepsin G by alpha(1)-antichymotrypsin and alpha(1)-proteinase inhibitor. J. Biol. Chem., 2000, 275(6), 3787-3792.
[http://dx.doi.org/10.1074/jbc.275.6.3787] [PMID: 10660528]
[20]
Granger, D.N.; Senchenkova, E. Inflammation and the Microcirculation; Morgan & Claypool Life Sciences: San Rafael, CA, 2010.
[http://dx.doi.org/10.4199/C00013ED1V01Y201006ISP008]
[21]
Anada, R.P.; Wong, K.T.; Jayapalan, J.J.; Hashim, O.H.; Ganesan, D. Panel of serum protein biomarkers to grade the severity of traumatic brain injury. Electrophoresis, 2018, 39(18), 2308-2315.
[http://dx.doi.org/10.1002/elps.201700407] [PMID: 29570807]
[22]
Sobieska, M.; Steiner, I.; Olejnik, J.; Szydłowski, J.; Antyborzec, J.; Grzegorowski, M.; Wiktorowicz, K. Increased concentration of A1-antichymotrypsin as a marker of necrotic processes during chronic tonsillitis. Nowa Pediatr., 1999, 3, 237-240.
[23]
Jin, Y.; Wang, W.; Wang, Q.; Zhang, Y.; Zahid, K.R.; Raza, U.; Gong, Y. Alpha-1-antichymotrypsin as a novel biomarker for diagnosis, prognosis, and therapy prediction in human diseases. Cancer Cell Int., 2022, 22(1), 156.
[http://dx.doi.org/10.1186/s12935-022-02572-4] [PMID: 35439996]
[24]
Murphy, C.E.; Kondo, Y.; Walker, A.K.; Rothmond, D.A.; Matsumoto, M.; Shannon Weickert, C. Regional, cellular and species difference of two key neuroinflammatory genes implicated in schizophrenia. Brain Behav. Immun., 2020, 88, 826-839.
[http://dx.doi.org/10.1016/j.bbi.2020.05.055] [PMID: 32450195]
[25]
Korkmaz, B.; Horwitz, M.S.; Jenne, D.E.; Gauthier, F. Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases. Pharmacol. Rev., 2010, 62(4), 726-759.
[http://dx.doi.org/10.1124/pr.110.002733] [PMID: 21079042]
[26]
Santamaria, M.; Pardo-Saganta, A.; Alvarez-Asiain, L.; Di Scala, M.; Qian, C.; Prieto, J.; Avila, M.A. Nuclear α1-antichymotrypsin promotes chromatin condensation and inhibits proliferation of human hepatocellular carcinoma cells. Gastroenterology, 2013, 144(4), 818-828.e4.
[http://dx.doi.org/10.1053/j.gastro.2012.12.029] [PMID: 23295442]
[27]
Naidoo, N.; Cooperman, B.S.; Wang, Z.; Liu, X.; Rubin, H. Identification of lysines within alpha 1-antichymotrypsin important for DNA binding. An unusual combination of DNA-binding elements. J. Biol. Chem., 1995, 270(24), 14548-14555.
[http://dx.doi.org/10.1074/jbc.270.24.14548] [PMID: 7782318]
[28]
Chasman, D.; Walters, K.B.; Lopes, T.J.S.; Eisfeld, A.J.; Kawaoka, Y.; Roy, S. Integrating transcriptomic and proteomic data using predictive regulatory network models of host response to pathogens. PLOS Comput. Biol., 2016, 12(7), e1005013.
[http://dx.doi.org/10.1371/journal.pcbi.1005013] [PMID: 27403523]
[29]
Abbasi, S.; Hosseinkhan, N.; Shafiei Jandaghi, N.Z.; Sadeghi, K.; Foroushani, A.R.; Hassani, S.A.; Yavarian, J.; Azad, T.M. Impact of human rhinoviruses on gene expression in pediatric patients with severe acute respiratory infection. Virus Res., 2021, 300, 198408.
[http://dx.doi.org/10.1016/j.virusres.2021.198408] [PMID: 33878402]
[30]
Burgener, A.; Rahman, S.; Ahmad, R.; Lajoie, J.; Ramdahin, S.; Mesa, C.; Brunet, S.; Wachihi, C.; Kimani, J.; Fowke, K.; Carr, S.; Plummer, F.; Ball, T.B. Comprehensive proteomic study identifies serpin and cystatin antiproteases as novel correlates of HIV-1 resistance in the cervicovaginal mucosa of female sex workers. J. Proteome Res., 2011, 10(11), 5139-5149.
[http://dx.doi.org/10.1021/pr200596r] [PMID: 21973077]
[31]
Woollard, S.M.; Bhargavan, B.; Yu, F.; Kanmogne, G.D. Differential effects of Tat proteins derived from HIV-1 subtypes B and recombinant CRF02_AG on human brain microvascular endothelial cells: Implications for blood-brain barrier dysfunction. J. Cereb. Blood Flow Metab., 2014, 34(6), 1047-1059.
[http://dx.doi.org/10.1038/jcbfm.2014.54] [PMID: 24667918]
[32]
Ferrarini, M.G.; Lal, A.; Rebollo, R.; Gruber, A.J.; Guarracino, A.; Gonzalez, I.M.; Floyd, T.; de Oliveira, D.S.; Shanklin, J.; Beausoleil, E.; Pusa, T.; Pickett, B.E.; Aguiar-Pulido, V. Genome-wide bioinformatic analyses predict key host and viral factors in SARS-CoV-2 pathogenesis. Commun. Biol., 2021, 4(1), 590.
[http://dx.doi.org/10.1038/s42003-021-02095-0] [PMID: 34002013]
[33]
Suvarna, K.; Biswas, D.; Pai, M.G.J.; Acharjee, A.; Bankar, R.; Palanivel, V.; Salkar, A.; Verma, A.; Mukherjee, A.; Choudhury, M.; Ghantasala, S.; Ghosh, S.; Singh, A.; Banerjee, A.; Badaya, A.; Bihani, S.; Loya, G.; Mantri, K.; Burli, A.; Roy, J.; Srivastava, A.; Agrawal, S.; Shrivastav, O.; Shastri, J.; Srivastava, S. Proteomics and machine learning approaches reveal a set of prognostic markers for COVID-19 severity with drug repurposing potential. Front. Physiol., 2021, 12, 652799.
[http://dx.doi.org/10.3389/fphys.2021.652799] [PMID: 33995121]
[34]
Zhang, Y.; Tian, J.; Qu, C.; Peng, Y.; Lei, J.; Li, K.; Zong, B.; Sun, L.; Liu, S. Overexpression of SERPINA3 promotes tumor invasion and migration, epithelial-mesenchymal-transition in triple-negative breast cancer cells. Breast Cancer, 2021, 28(4), 859-873.
[http://dx.doi.org/10.1007/s12282-021-01221-4] [PMID: 33569740]
[35]
Lara-Velazquez, M.; Zarco, N.; Carrano, A.; Phillipps, J.; Norton, E.S.; Schiapparelli, P.; Al-kharboosh, R.; Rincon-Torroella, J.; Jeanneret, S.; Corona, T.; Segovia, J.; Jentoft, M.E.; Chaichana, K.L.; Asmann, Y.W.; Quiñones-Hinojosa, A.; Guerrero-Cazares, H. Alpha 1-antichymotrypsin contributes to stem cell characteristics and enhances tumorigenicity of glioblastoma. Neuro-oncol., 2021, 23(4), 599-610.
[http://dx.doi.org/10.1093/neuonc/noaa264] [PMID: 33249487]
[36]
Nimbalkar, V.P.; Kruthika, B.S.; Sravya, P.; Rao, S.; Sugur, H.S.; Verma, B.K.; Chickabasaviah, Y.T.; Arivazhagan, A.; Kondaiah, P.; Santosh, V. Differential gene expression in peritumoral brain zone of glioblastoma: Role of SERPINA3 in promoting invasion, stemness and radioresistance of glioma cells and association with poor patient prognosis and recurrence. J. Neurooncol., 2021, 152(1), 55-65.
[http://dx.doi.org/10.1007/s11060-020-03685-4] [PMID: 33389566]
[37]
Cao, L.L.; Pei, X.F.; Qiao, X.; Yu, J.; Ye, H.; Xi, C.L.; Wang, P.Y.; Gong, Z.L. SERPINA3 silencing inhibits the migration, invasion, and liver metastasis of colon cancer cells. Dig. Dis. Sci., 2018, 63(9), 2309-2319.
[http://dx.doi.org/10.1007/s10620-018-5137-x] [PMID: 29855767]
[38]
Ko, E.; Kim, J.S.; Bae, J.W.; Kim, J.; Park, S.G.; Jung, G. SERPINA3 is a key modulator of HNRNP-K transcriptional activity against oxidative stress in HCC. Redox Biol., 2019, 24, 101217.
[http://dx.doi.org/10.1016/j.redox.2019.101217] [PMID: 31121493]
[39]
Koivuluoma, S.; Tervasmäki, A.; Kauppila, S.; Winqvist, R.; Kumpula, T.; Kuismin, O.; Moilanen, J.; Pylkäs, K. Exome sequencing identifies a recurrent variant in SERPINA3 associating with hereditary susceptibility to breast cancer. Eur. J. Cancer, 2021, 143, 46-51.
[http://dx.doi.org/10.1016/j.ejca.2020.10.033] [PMID: 33279852]
[40]
Zhao, J.; Fan, Y.X.; Yang, Y.; Liu, D.L.; Wu, K.; Wen, F.B.; Zhang, C.Y.; Zhu, D.Y.; Zhao, S. Identification of potential plasma biomarkers for esophageal squamous cell carcinoma by a proteomic method. Int. J. Clin. Exp. Pathol., 2015, 8(2), 1535-1544.
[PMID: 25973038]
[41]
Li, Q.; Zeng, H.; Zhao, Y.; Gong, Y.; Ma, X. Proteomic analysis of cerebrospinal fluid from patients with extranodal NK-/T-Cell lymphoma of nasal-type with ethmoidal sinus metastasis. Front. Oncol., 2020, 9, 1489.
[http://dx.doi.org/10.3389/fonc.2019.01489] [PMID: 31998645]
[42]
Zhang, J.; Wang, W.; Zhu, S.; Chen, Y. Increased SERPINA3 level is associated with ulcerative colitis. Diagnostics, 2021, 11(12), 2371.
[http://dx.doi.org/10.3390/diagnostics11122371] [PMID: 34943607]
[43]
Lewandowska, A.; Rudzki, G.; Lewandowski, T.; Stryjkowska-Góra, A.; Rudzki, S. Risk factors for the diagnosis of colorectal cancer. Cancer Contr., 2022, 29.
[http://dx.doi.org/10.1177/10732748211056692] [PMID: 35000418]
[44]
Jin, Y.; Wang, J.; Ye, X.; Su, Y.; Yu, G.; Yang, Q.; Liu, W.; Yu, W.; Cai, J.; Chen, X.; Liang, Y.; Chen, Y.; Wong, B.H.C.; Fu, X.; Sun, H. Identification of GlcNAcylated alpha-1-antichymotrypsin as an early biomarker in human non-small-cell lung cancer by quantitative proteomic analysis with two lectins. Br. J. Cancer, 2016, 114(5), 532-544.
[http://dx.doi.org/10.1038/bjc.2015.348] [PMID: 26908325]
[45]
de Mezer, M.; Rogaliński, J.; Przewoźny, S.; Chojnicki, M.; Niepolski, L.; Sobieska, M.; Przystańska, A. SERPINA3: Stimulator or inhibitor of pathological changes. Biomedicines, 2023, 11(1), 156.
[http://dx.doi.org/10.3390/biomedicines11010156] [PMID: 36672665]
[46]
Higashiyama, M.; Doi, O.; Yokouchi, H.; Kodama, K.; Nakamori, S.; Tateishi, R. Alpha-1-antichymotrypsin expression in lung adenocarcinoma and its possible association with tumor progression. Biochemistry, 1995, 22, 5055-5061.
[http://dx.doi.org/10.1002/1097-0142(19951015)76:8<1368::AID-CNCR2820760812>3.0.CO;2-N]
[47]
Zhou, J.; Cheng, Y.; Tang, L.; Martinka, M.; Kalia, S. Up-regulation of SERPINA3 correlates with high mortality of melanoma patients and increased migration and invasion of cancer cells. Oncotarget, 2017, 8(12), 18712-18725.
[http://dx.doi.org/10.18632/oncotarget.9409] [PMID: 27213583]
[48]
Luo, D.; Chen, W.; Tian, Y.; Li, J.; Xu, X.; Chen, C.; Li, F. Serpin peptidase inhibitor, clade A member 3 (SERPINA3), is overexpressed in glioma and associated with poor prognosis in glioma patients. OncoTargets Ther., 2017, 10, 2173-2181.
[http://dx.doi.org/10.2147/OTT.S133022] [PMID: 28458560]
[49]
Yang, G-D.; Yang, X-M.; Lu, H.; Ren, Y.; Ma, M-Z.; Zhu, L-Y.; Wang, J-H.; Song, W-W.; Zhang, W-M.; Zhang, R.; Zhang, Z.G. SERPINA3 promotes endometrial cancer cells growth by regulating G2/M cell cycle checkpoint and apoptosis. Int. J. Clin. Exp. Pathol., 2014, 7(4), 1348-1358.
[PMID: 24817931]
[50]
Tahara, E.; Ito, H.; Taniyama, K.; Yokozaki, H.; Hata, J. Alpha1-antitrypsin, alpha1-antichymotrypsin, and alpha2-macroglobulin in human gastric carcinomas: A retrospective immunohistochemical study. Hum. Pathol., 1984, 15(10), 957-964.
[http://dx.doi.org/10.1016/S0046-8177(84)80125-2] [PMID: 6207098]
[51]
Meijers, W.C.; Maglione, M.; Bakker, S.J.L.; Oberhuber, R.; Kieneker, L.M.; de Jong, S.; Haubner, B.J.; Nagengast, W.B.; Lyon, A.R.; van der Vegt, B.; van Veldhuisen, D.J.; Westenbrink, B.D.; van der Meer, P.; Silljé, H.H.W.; de Boer, R.A. Heart failure stimulates tumor growth by circulating factors. Circulation, 2018, 138(7), 678-691.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.117.030816] [PMID: 29459363]
[52]
Zhou, M.L.; Chen, F.S.; Mao, H. Clinical significance and role of up-regulation of SERPINA3 expression in endometrial cancer. World J. Clin. Cases, 2019, 7(15), 1996-2002.
[http://dx.doi.org/10.12998/wjcc.v7.i15.1996] [PMID: 31423431]
[53]
Markowska, A.; Kurzawa, P.; Bednarek, W.; Gryboś, A.; Mardas, M.; Krzyżaniak, M.; Majewski, J.; Markowska, J.; Gryboś, M.; Żurawski, J. Immunohistochemical expression of Vitamin D receptor in uterine fibroids. Nutrients, 2022, 14(16), 3371.
[http://dx.doi.org/10.3390/nu14163371] [PMID: 36014877]
[54]
Chalcarz, M.; Żurawski, J. Injection of aquafilling® for breast augmentation causes inflammatory responses independent of visible symptoms. Aesthetic Plast. Surg., 2021, 45(2), 481-490.
[http://dx.doi.org/10.1007/s00266-020-01949-y] [PMID: 32939601]
[55]
Chalcarz, M.; Żurawski, J. The absence of early malignant changes in women subjected to Aquafilling breast augmentation on the basis of E-cadherin and N-cadherin immunohistochemical expression. Cent. Eur. J. Immunol., 2022, 47(4), 350-356.
[http://dx.doi.org/10.5114/ceji.2022.124070] [PMID: 36817402]
[56]
The Human Protein Atlas Available from: https://www.proteinatlas.org/ (accessed on 1 September 2023).
[57]
Kulesza, D.W.; Ramji, K.; Maleszewska, M.; Mieczkowski, J.; Dabrowski, M.; Chouaib, S.; Kaminska, B. Search for novel STAT3-dependent genes reveals SERPINA3 as a new STAT3 target that regulates invasion of human melanoma cells. Lab. Invest., 2019, 99(11), 1607-1621.
[http://dx.doi.org/10.1038/s41374-019-0288-8] [PMID: 31278347]
[58]
Bogusiewicz, M.; Stryjecka-Zimmer, M.; Postawski, K.; Jakimiuk, A.J.; Rechberger, T. Activity of matrix metalloproteinase-2 and -9 and contents of their tissue inhibitors in uterine leiomyoma and corresponding myometrium. Gynecol. Endocrinol., 2007, 23(9), 541-546.
[http://dx.doi.org/10.1080/09513590701557416] [PMID: 17943549]
[59]
Malik, M.; Norian, J.; McCarthy-Keith, D.; Britten, J.; Catherino, W. Why leiomyomas are called fibroids: The central role of extracellular matrix in symptomatic women. Semin. Reprod. Med., 2010, 28(3), 169-179.
[http://dx.doi.org/10.1055/s-0030-1251475] [PMID: 20414841]
[60]
Bergers, G.; Brekken, R.; McMahon, G.; Vu, T.H.; Itoh, T.; Tamaki, K.; Tanzawa, K.; Thorpe, P.; Itohara, S.; Werb, Z.; Hanahan, D. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol., 2000, 2(10), 737-744.
[http://dx.doi.org/10.1038/35036374] [PMID: 11025665]
[61]
Lee, S.; Jilani, S.M.; Nikolova, G.V.; Carpizo, D.; Iruela-Arispe, M.L. Processing of VEGF: A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J. Cell Biol., 2005, 169(4), 681-691.
[http://dx.doi.org/10.1083/jcb.200409115] [PMID: 15911882]
[62]
Kurachi, O.; Matsuo, H.; Samoto, T.; Maruo, T. Tumor necrosis factor-α expression in human uterine leiomyoma and its down-regulation by progesterone. J. Clin. Endocrinol. Metab., 2001, 86(5), 2275-2280.
[http://dx.doi.org/10.1210/jc.86.5.2275] [PMID: 11344239]
[63]
Plewka, A.; Madej, P.; Plewka, D.; Kowalczyk, A.; Miskiewicz, A.; Wittek, P.; Leks, T.; Bilski, R. Immunohistochemical localization of selected pro-inflammatory factors in uterine myomas and myometrium in women of various ages. Folia Histochem. Cytobiol., 2013, 51(1), 73-83.
[http://dx.doi.org/10.5603/FHC.2013.0011] [PMID: 23690221]
[64]
Wang, Y.; Feng, G.; Wang, J.; Zhou, Y.; Liu, Y.; Shi, Y.; Zhu, Y.; Lin, W.; Xu, Y.; Li, Z. Differential effects of tumor necrosis factor-α on matrix metalloproteinase-2 expression in human myometrial and uterine leiomyoma smooth muscle cells. Hum. Reprod., 2015, 30(1), 61-70.
[http://dx.doi.org/10.1093/humrep/deu300] [PMID: 25398968]
[65]
Islam, M.S.; Protic, O.; Giannubilo, S.R.; Toti, P.; Tranquilli, A.L.; Petraglia, F.; Castellucci, M.; Ciarmela, P. Uterine leiomyoma: Available medical treatments and new possible therapeutic options. J. Clin. Endocrinol. Metab., 2013, 98(3), 921-934.
[http://dx.doi.org/10.1210/jc.2012-3237] [PMID: 23393173]
[66]
Islam, M.S.; Catherino, W.H.; Protic, O.; Janjusevic, M.; Gray, P.C.; Giannubilo, S.R.; Ciavattini, A.; Lamanna, P.; Tranquilli, A.L.; Petraglia, F.; Castellucci, M.; Ciarmela, P. Role of activin: A and myostatin and their signaling pathway in human myometrial and leiomyoma cell function. J. Clin. Endocrinol. Metab., 2014, 99(5), E775-E785.
[http://dx.doi.org/10.1210/jc.2013-2623] [PMID: 24606069]
[67]
Joseph, D.S.; Malik, M.; Nurudeen, S.; Catherino, W.H. Myometrial cells undergo fibrotic transformation under the influence of transforming growth factor β-3. Fertil. Steril., 2010, 93(5), 1500-1508.
[http://dx.doi.org/10.1016/j.fertnstert.2009.01.081] [PMID: 19328471]
[68]
Zhang, H.; Wang, L.; Cui, J.; Wang, S.; Han, Y.; Shao, H.; Wang, C.; Hu, Y.; Li, X.; Zhou, Q.; Guo, J.; Zhuang, X.; Sheng, S.; Zhang, T.; Zhou, D.; Chen, J.; Wang, F.; Gao, Q.; Jing, Y.; Chen, X.; Su, J. Maintaining hypoxia environment of subchondral bone alleviates osteoarthritis progression. Sci. Adv., 2023, 9(14), eabo7868.
[http://dx.doi.org/10.1126/sciadv.abo7868] [PMID: 37018403]
[69]
He, X.; Zhang, X.; Li, B.; Zhou, S.; Zhao, Y.; Wang, L.; Xu, J.; Yan, H. Capacity degradation mechanism of ternary La–Y–Ni-based hydrogen storage alloys. Chem. Eng. J., 2023, 465, 142840.
[http://dx.doi.org/10.1016/j.cej.2023.142840]
[70]
Garmaroudi, G.A.; Karimi, F.; Naeini, L.G.; Kokabian, P.; Givtaj, N. Therapeutic efficacy of oncolytic viruses in fighting cancer: Recent advances and perspective. Oxid. Med. Cell. Longev., 2022, 2022, 1-14.
[http://dx.doi.org/10.1155/2022/3142306] [PMID: 35910836]
[71]
Zhang, Y.; Wang, C.; Zhang, W.; Li, X. Bioactive peptides for anticancer therapies. Biomater Transl, 2023, 4(1), 5-17.
[http://dx.doi.org/10.12336/biomatertransl.2023.01.003] [PMID: 37206303]

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