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Current Cancer Drug Targets

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ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

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Research Article

Silencing TRIM29 Sensitizes Non-small Cell Lung Cancer Cells to Anlotinib by Promoting Apoptosis via Binding RAD50

Author(s): Min Wu, Meng-Meng Jin, Xiao-Hui Cao, Lei Zhao* and Yong-Huai Li*

Volume 24, Issue 4, 2024

Published on: 19 September, 2023

Page: [445 - 454] Pages: 10

DOI: 10.2174/1568009623666230829143148

Abstract

Background: Previous studies have proposed that the transcriptional regulatory factor tripartite motif containing 29 (TRIM29) is involved in carcinogenesis via binding with nucleic acid. TRIM29 is confirmed to be highly expressed when the cancer cells acquire therapy-resistant properties. We noticed that TRIM29 levels were significantly increased in anlotinib-resistant NCIH1975 (NCI-H1975/AR) cells via mining data information from gene expression omnibus (GEO) gene microarray (GSE142031; log2 fold change > 1, p < 0.05).

Objective: Our study aimed to investigate the function of TRIM29 on the resistance to anlotinib in non-small cell lung cancer (NSCLC) cells, including NCI-H1975 and A549 cells.

Methods: Real-time RT-PCR and western blot were used to detect TRIM29 expression in anlotinib- resistant NSCLC (NSCLC/AR) cells. Apoptosis were determined through flow cytometry, acridine orange/ethidium bromide staining as well as western blot. ELISA was used to measure the content of C-X3-C motif chemokine ligand 1. Co-Immunoprecipitation assay was performed to verify the interaction between TRIM29 and RAD50 double-strand break repair protein (RAD50).

Results: TRIM29 expression was shown to be elevated in the cytoplasm and nucleus of NSCLC/ AR cells compared to normal NSCLC cells. Next, we demonstrated that TRIM29 knockdown facilitated apoptosis and enhanced the sensitivity to anlotinib in NSCLC/AR cells. Based on the refined results citing from the database BioGRID, it was proved that TRIM29 interacted with RAD50. Herein, RAD50 overexpression diminished the pro-apoptotic effect induced by silencing TRIM29 in anlotinib-resistant A549 (A549/AR) cells.

Conclusion: Finally, we concluded that the increased sensitivity to anlotinib in NSCLC/AR cells was achieved by knocking down TRIM29, besides, the positive effects of TRIM29 knockdown were attributed to the promotion of apoptosis via binding to RAD50 in NSCLC/AR cell nucleus. Therefore, TRIM29 might become a potential target for overcoming anlotinib resistance in NSCLC treatment.

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[1]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[2]
Jayan, A.P.; Anandu, K.R.; Madhu, K.; Saiprabha, V.N. A pharmacological exploration of targeted drug therapy in non-small cell lung cancer. Med. Oncol., 2022, 39(10), 147.
[http://dx.doi.org/10.1007/s12032-022-01744-6] [PMID: 35834033]
[3]
Miller, K.D.; Nogueira, L.; Devasia, T.; Mariotto, A.B.; Yabroff, K.R.; Jemal, A.; Kramer, J.; Siegel, R.L. Cancer treatment and survivorship statistics. CA Cancer J. Clin., 2022, 72(5), 409-436.
[http://dx.doi.org/10.3322/caac.21731] [PMID: 35736631]
[4]
Herbst, R.S.; Morgensztern, D.; Boshoff, C. The biology and management of non-small cell lung cancer. Nature, 2018, 553(7689), 446-454.
[http://dx.doi.org/10.1038/nature25183] [PMID: 29364287]
[5]
Osmani, L.; Askin, F.; Gabrielson, E.; Li, Q.K. Current WHO guidelines and the critical role of immunohistochemical markers in the subclassification of non-small cell lung carcinoma (NSCLC): Moving from targeted therapy to immunotherapy. Semin. Cancer Biol., 2018, 52(Pt 1), 103-109.
[http://dx.doi.org/10.1016/j.semcancer.2017.11.019] [PMID: 29183778]
[6]
Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer statistics, 2022. CA Cancer J. Clin., 2022, 72(1), 7-33.
[http://dx.doi.org/10.3322/caac.21708] [PMID: 35020204]
[7]
Molina, J.R.; Yang, P.; Cassivi, S.D.; Schild, S.E.; Adjei, A.A. Non-small cell lung cancer: Epidemiology, risk factors, treatment, and survivorship. Mayo Clin. Proc., 2008, 83(5), 584-594.
[http://dx.doi.org/10.1016/S0025-6196(11)60735-0] [PMID: 18452692]
[8]
Reck, M.; Rabe, K.F. Precision diagnosis and treatment for advanced non–small-cell lung cancer. N. Engl. J. Med., 2017, 377(9), 849-861.
[http://dx.doi.org/10.1056/NEJMra1703413] [PMID: 28854088]
[9]
Zhou, M.; Chen, X.; Zhang, H.; Xia, L.; Tong, X.; Zou, L.; Hao, R.; Pan, J.; Zhao, X.; Chen, D.; Song, Y.; Qi, Y.; Tang, L.; Liu, Z.; Gao, R.; Shi, Y.; Yang, Z. China national medical products administration approval summary: Anlotinib for the treatment of advanced non-small cell lung cancer after two lines of chemotherapy. Cancer Commun., 2019, 39(1), 36.
[http://dx.doi.org/10.1186/s40880-019-0383-7] [PMID: 31221221]
[10]
Han, B.; Li, K.; Wang, Q.; Zhang, L.; Shi, J.; Wang, Z.; Cheng, Y.; He, J.; Shi, Y.; Zhao, Y.; Yu, H.; Zhao, Y.; Chen, W.; Luo, Y.; Wu, L.; Wang, X.; Pirker, R.; Nan, K.; Jin, F.; Dong, J.; Li, B.; Sun, Y. Effect of anlotinib as a third-line or further treatment on overall survival of patients with advanced non–small cell lung cancer. JAMA Oncol., 2018, 4(11), 1569-1575.
[http://dx.doi.org/10.1001/jamaoncol.2018.3039] [PMID: 30098152]
[11]
Ozato, K.; Shin, D.M.; Chang, T.H.; Morse, H.C., III TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol., 2008, 8(11), 849-860.
[http://dx.doi.org/10.1038/nri2413] [PMID: 18836477]
[12]
Eberhardt, W.; Haeussler, K.; Nasrullah, U.; Pfeilschifter, J. Multifaceted roles of trim proteins in colorectal carcinoma. Int. J. Mol. Sci., 2020, 21(20), 7532.
[http://dx.doi.org/10.3390/ijms21207532] [PMID: 33066016]
[13]
Hatakeyama, S. TRIM family proteins: Roles in autophagy, immunity, and carcinogenesis. Trends Biochem. Sci., 2017, 42(4), 297-311.
[http://dx.doi.org/10.1016/j.tibs.2017.01.002] [PMID: 28118948]
[14]
Shen, H.; Zhang, J.; Zhang, Y.; Feng, Q.; Wang, H.; Li, G.; Jiang, W.; Li, X. Knockdown of tripartite motif 59 (TRIM59) inhibits proliferation in cholangiocarcinoma via the PI3K/AKT/mTOR signalling pathway. Gene, 2019, 698, 50-60.
[http://dx.doi.org/10.1016/j.gene.2019.02.044] [PMID: 30822475]
[15]
Tocchini, C.; Keusch, J.J.; Miller, S.B.; Finger, S.; Gut, H.; Stadler, M.B.; Ciosk, R. The TRIM-NHL protein LIN-41 controls the onset of developmental plasticity in Caenorhabditis elegans. PLoS Genet., 2014, 10(8), e1004533.
[http://dx.doi.org/10.1371/journal.pgen.1004533] [PMID: 25167051]
[16]
Nguyen, D.T.T.; Richter, D.; Michel, G.; Mitschka, S.; Kolanus, W.; Cuevas, E.; Wulczyn, F.G. The ubiquitin ligase LIN41/TRIM71 targets p53 to antagonize cell death and differentiation pathways during stem cell differentiation. Cell Death Differ., 2017, 24(6), 1063-1078.
[http://dx.doi.org/10.1038/cdd.2017.54] [PMID: 28430184]
[17]
Zhan, W.; Han, T.; Zhang, C.; Xie, C.; Gan, M.; Deng, K.; Fu, M.; Wang, J.B. TRIM59 promotes the proliferation and migration of non-small cell lung cancer cells by upregulating cell cycle related proteins. PLoS One, 2015, 10(11), e0142596.
[http://dx.doi.org/10.1371/journal.pone.0142596] [PMID: 26599082]
[18]
Xu, L.; Wu, Q.; Zhou, X.; Wu, Q.; Fang, M. TRIM13 inhibited cell proliferation and induced cell apoptosis by regulating NF-κB pathway in non-small-cell lung carcinoma cells. Gene, 2019, 715, 144015.
[http://dx.doi.org/10.1016/j.gene.2019.144015] [PMID: 31357025]
[19]
Kosaka, Y.; Inoue, H.; Ohmachi, T.; Yokoe, T.; Matsumoto, T.; Mimori, K.; Tanaka, F.; Watanabe, M.; Mori, M. Tripartite motif-containing 29 (TRIM29) is a novel marker for lymph node metastasis in gastric cancer. Ann. Surg. Oncol., 2007, 14(9), 2543-2549.
[http://dx.doi.org/10.1245/s10434-007-9461-1] [PMID: 17597343]
[20]
Farhadi, J.; Mehrzad, J.; Mehrad-Majd, H.; Motavalizadehkakhky, A. Clinical significance of TRIM29 expression in patients with gastric cancer. Gastroenterol. Hepatol. Bed Bench, 2022, 15(2), 131-138.
[PMID: 35845310]
[21]
Han, J.; Zuo, J.; Zhang, X.; Wang, L.; Li, D.; Wang, Y.; Liu, J.; Feng, L. TRIM29 is differentially expressed in colorectal cancers of different primary locations and affects survival by regulating tumor immunity based on retrospective study and bioinformatics analysis. J. Gastrointest. Oncol., 2022, 13(3), 1132-1151.
[http://dx.doi.org/10.21037/jgo-22-365] [PMID: 35837175]
[22]
Tan, S.T.; Liu, S.Y.; Wu, B. TRIM29 overexpression promotes proliferation and survival of bladder cancer cells through nf-κb signaling. Cancer Res. Treat., 2016, 48(4), 1302-1312.
[http://dx.doi.org/10.4143/crt.2015.381] [PMID: 26987391]
[23]
Tang, Z.P.; Dong, Q.Z.; Cui, Q.Z.; Papavassiliou, P.; Wang, E.D.; Wang, E.H. Ataxia-telangiectasia group D complementing gene (ATDC) promotes lung cancer cell proliferation by activating NF-κB pathway. PLoS One, 2013, 8(6), e63676.
[http://dx.doi.org/10.1371/journal.pone.0063676] [PMID: 23776433]
[24]
Wang, L.; Heidt, D.G.; Lee, C.J.; Yang, H.; Logsdon, C.D.; Zhang, L.; Fearon, E.R.; Ljungman, M.; Simeone, D.M. Oncogenic function of ATDC in pancreatic cancer through Wnt pathway activation and beta-catenin stabilization. Cancer Cell, 2009, 15(3), 207-219.
[http://dx.doi.org/10.1016/j.ccr.2009.01.018] [PMID: 19249679]
[25]
Deng, X.; Fu, X.; Teng, H.; Fang, L.; Liang, B.; Zeng, R.; Chen, L.; Zou, Y. E3 ubiquitin ligase TRIM29 promotes pancreatic cancer growth and progression via stabilizing Yes-associated protein 1. J. Transl. Med., 2021, 19(1), 332.
[http://dx.doi.org/10.1186/s12967-021-03007-w] [PMID: 34353343]
[26]
Purohit, V.; Wang, L.; Yang, H.; Li, J.; Ney, G.M.; Gumkowski, E.R.; Vaidya, A.J.; Wang, A.; Bhardwaj, A.; Zhao, E.; Dolgalev, I.; Zamperone, A.; Abel, E.V.; Magliano, M.P.D.; Crawford, H.C.; Diolaiti, D.; Papagiannakopoulos, T.Y.; Lyssiotis, C.A.; Simeone, D.M. ATDC binds to KEAP1 to drive NRF2-mediated tumorigenesis and chemoresistance in pancreatic cancer. Genes Dev., 2021, 35(3-4), 218-233.
[http://dx.doi.org/10.1101/gad.344184.120] [PMID: 33446568]
[27]
Wang, B.; Ma, A.; Zhang, L.; Jin, W.L.; Qian, Y.; Xu, G.; Qiu, B.; Yang, Z.; Liu, Y.; Xia, Q.; Liu, Y. POH1 deubiquitylates and stabilizes E2F1 to promote tumour formation. Nat. Commun., 2015, 6(1), 8704.
[http://dx.doi.org/10.1038/ncomms9704] [PMID: 26510456]
[28]
Hao, L.; Wang, J.M.; Liu, B.Q.; Yan, J.; Li, C.; Jiang, J.Y.; Zhao, F.Y.; Qiao, H.Y.; Wang, H.Q. m6A-YTHDF1-mediated TRIM29 upregulation facilitates the stem cell-like phenotype of cisplatin-resistant ovarian cancer cells. Biochim. Biophys. Acta Mol. Cell Res., 2021, 1868(1), 118878.
[http://dx.doi.org/10.1016/j.bbamcr.2020.118878] [PMID: 33011193]
[29]
Song, X.; Fu, C.; Yang, X.; Sun, D.; Zhang, X.; Zhang, J. Tripartite motif-containing 29 as a novel biomarker in non-small cell lung cancer. Oncol. Lett., 2015, 10(4), 2283-2288.
[http://dx.doi.org/10.3892/ol.2015.3623] [PMID: 26622835]
[30]
Masuda, Y.; Takahashi, H.; Sato, S.; Tomomori-Sato, C.; Saraf, A.; Washburn, M.P.; Florens, L.; Conaway, R.C.; Conaway, J.W.; Hatakeyama, S. TRIM29 regulates the assembly of DNA repair proteins into damaged chromatin. Nat. Commun., 2015, 6(1), 7299.
[http://dx.doi.org/10.1038/ncomms8299] [PMID: 26095369]
[31]
Karamat, U.; Ejaz, S. Overexpression of RAD50 is the marker of poor prognosis and drug resistance in breast cancer patients. Curr. Cancer Drug Targets, 2021, 21(2), 163-176.
[http://dx.doi.org/10.2174/1568009620666201009125507] [PMID: 33038913]
[32]
Ltan, B.; Yokobori, T.; Ide, M.; Bai, T.; Yanoma, T.; Kimura, A.; Kogure, N.; Suzuki, M.; Bao, P.; Mochiki, E.; Ogata, K.; Handa, T.; Kaira, K.; Nishiyama, M.; Asao, T.; Oyama, T.; Kuwano, H. High Expression of MRE11–RAD50–NBS1 is associated with poor prognosis and chemoresistance in gastric cancer. Anticancer Res., 2016, 36(10), 5237-5248.
[http://dx.doi.org/10.21873/anticanres.11094] [PMID: 27798884]
[33]
Li, Y.; Wang, S.; Li, P.; Li, Y.; Liu, Y.; Fang, H.; Zhang, X.; Liu, Z.; Kong, B. Rad50 promotes ovarian cancer progression through NF-κB activation. J. Cell. Mol. Med., 2021, 25(23), 10961-10972.
[http://dx.doi.org/10.1111/jcmm.17017] [PMID: 34734468]
[34]
Flores-Pérez, A.; Rafaelli, L.E.; Ramírez-Torres, N.; Aréchaga-Ocampo, E.; Frías, S.; Sánchez, S.; Marchat, L.A.; Hidalgo-Miranda, A.; Quintanar-Jurado, V.; Rodríguez-Cuevas, S.; Bautista-Piña, V.; Carlos-Reyes, Á.; López-Camarillo, C. RAD50 targeting impairs DNA damage response and sensitizes human breast cancer cells to cisplatin therapy. Cancer Biol. Ther., 2014, 15(6), 777-788.
[http://dx.doi.org/10.4161/cbt.28551] [PMID: 24642965]
[35]
Liang, L.; Hui, K.; Hu, C.; Wen, Y.; Yang, S.; Zhu, P.; Wang, L.; Xia, Y.; Qiao, Y.; Sun, W.; Fei, J.; Chen, T.; Zhao, F.; Yang, B.; Jiang, X. Autophagy inhibition potentiates the anti-angiogenic property of multikinase inhibitor anlotinib through JAK2/STAT3/VEGFA signaling in non-small cell lung cancer cells. J. Exp. Clin. Cancer Res., 2019, 38(1), 71.
[http://dx.doi.org/10.1186/s13046-019-1093-3] [PMID: 30755242]
[36]
Lu, J.; Xu, W.; Qian, J.; Wang, S.; Zhang, B.; Zhang, L.; Qiao, R.; Hu, M.; Zhao, Y.; Zhao, X.; Han, B. Transcriptome profiling analysis reveals that CXCL2 is involved in anlotinib resistance in human lung cancer cells. BMC Med. Genomics, 2019, 12(S2)(2), 38.
[http://dx.doi.org/10.1186/s12920-019-0482-y] [PMID: 30871526]
[37]
Wu, M.; Jin, M.; Cao, X.; Qian, K.; Zhao, L. RNA editing enzyme adenosine deaminases acting on RNA 1 deficiency increases the sensitivity of non-small cell lung cancer cells to anlotinib by regulating CX3CR1 -fractalkine expression. Drug Dev. Res., 2022, 83(2), 328-338.
[http://dx.doi.org/10.1002/ddr.21861] [PMID: 34319598]
[38]
Joazeiro, C.A.P.; Weissman, A.M. RING finger proteins: Mediators of ubiquitin ligase activity. Cell, 2000, 102(5), 549-552.
[http://dx.doi.org/10.1016/S0092-8674(00)00077-5] [PMID: 11007473]
[39]
Zhan, W.; Zhang, S. TRIM proteins in lung cancer: Mechanisms, biomarkers and therapeutic targets. Life Sci., 2021, 268, 118985.
[http://dx.doi.org/10.1016/j.lfs.2020.118985] [PMID: 33412211]
[40]
Cao, H.; Li, Y.; Chen, L.; Lu, Z.; You, T.; Wang, X.; Ji, B. Tripartite motif-containing 54 promotes gastric cancer progression by upregulating K63-linked ubiquitination of filamin C. Asia Pac. J. Clin. Oncol., 2022, 18(6), 669-677.
[http://dx.doi.org/10.1111/ajco.13747] [PMID: 35098666]
[41]
Berti, C.; Messali, S.; Ballabio, A.; Reymond, A.; Meroni, G. TRIM9 is specifically expressed in the embryonic and adult nervous system. Mech. Dev., 2002, 113(2), 159-162.
[http://dx.doi.org/10.1016/S0925-4773(02)00013-8] [PMID: 11960705]
[42]
Zhou, C.; Zhang, Z.; Zhu, X.; Qian, G.; Zhou, Y.; Sun, Y.; Yu, W.; Wang, J.; Lu, H.; Lin, F.; Shen, Z.; Zheng, S. N6-Methyladenosine modification of the TRIM7 positively regulates tumorigenesis and chemoresistance in osteosarcoma through ubiquitination of BRMS1. EBioMedicine, 2020, 59, 102955.
[http://dx.doi.org/10.1016/j.ebiom.2020.102955] [PMID: 32853985]
[43]
Zhang, S.; Cao, M.; Yan, S.; Liu, Y.; Fan, W.; Cui, Y.; Tian, F.; Gu, R.; Cui, Y.; Zhan, Y.; Sun, Y.; Xing, Y.; Cai, L.; Song, Y. TRIM44 promotes BRCA1 functions in HR repair to induce cisplatin chemoresistance in lung adenocarcinoma by deubiquitinating FLNA. Int. J. Biol. Sci., 2022, 18(7), 2962-2979.
[http://dx.doi.org/10.7150/ijbs.71283] [PMID: 35541909]
[44]
Tan, Z.; Song, L.; Wu, W.; Zhou, Y.; Zhu, J.; Wu, G.; Cao, L.; Song, J.; Li, J.; Zhang, W. TRIM14 promotes chemoresistance in gliomas by activating Wnt/β-catenin signaling via stabilizing Dvl2. Oncogene, 2018, 37(40), 5403-5415.
[http://dx.doi.org/10.1038/s41388-018-0344-7] [PMID: 29867201]
[45]
Nagasawa, S.; Ikeda, K.; Shintani, D.; Yang, C.; Takeda, S.; Hasegawa, K.; Horie, K.; Inoue, S. Identification of a novel oncogenic fusion gene SPON1-TRIM29 in clinical ovarian cancer that promotes cell and tumor growth and enhances chemoresistance in A2780 cells. Int. J. Mol. Sci., 2022, 23(2), 689.
[http://dx.doi.org/10.3390/ijms23020689] [PMID: 35054873]
[46]
Luo, S.; Shen, M.; Chen, H.; Li, W.; Chen, C. Long non-coding RNA TP73-AS1 accelerates the progression and cisplatin resistance of non-small cell lung cancer by upregulating the expression of TRIM29 via competitively targeting microRNA-34a-5p. Mol. Med. Rep., 2020, 22(5), 3822-3832.
[http://dx.doi.org/10.3892/mmr.2020.11473] [PMID: 32901838]
[47]
Xu, J.; Li, Z.; Su, Q.; Zhao, J.; Ma, J. TRIM29 promotes progression of thyroid carcinoma via activating P13K/AKT signaling pathway. Oncol. Rep., 2017, 37(3), 1555-1564.
[http://dx.doi.org/10.3892/or.2017.5364] [PMID: 28098872]
[48]
Bai, Y.; Wang, W.; Li, S.; Zhan, J.; Li, H.; Zhao, M.; Zhou, X.A.; Li, S.; Li, X.; Huo, Y.; Shen, Q.; Zhou, M.; Zhang, H.; Luo, J.; Sung, P.; Zhu, W.G.; Xu, X.; Wang, J. C1QBP promotes homologous recombination by stabilizing MRE11 and controlling the assembly and activation of MRE11/RAD50/NBS1 complex. Mol. Cell, 2019, 75(6), 1299-1314.e6.
[http://dx.doi.org/10.1016/j.molcel.2019.06.023] [PMID: 31353207]
[49]
Abad, E.; Civit, L.; Potesil, D.; Zdrahal, Z.; Lyakhovich, A. Enhanced DNA damage response through RAD50 in triple negative breast cancer resistant and cancer stem-like cells contributes to chemoresistance. FEBS J., 2021, 288(7), 2184-2202.
[http://dx.doi.org/10.1111/febs.15588] [PMID: 33090711]
[50]
Wang, Y.; Gudikote, J.; Giri, U.; Yan, J.; Deng, W.; Ye, R.; Jiang, W.; Li, N.; Hobbs, B.P.; Wang, J.; Swisher, S.G.; Fujimoto, J.; Wistuba, I.I.; Komaki, R.; Heymach, J.V.; Lin, S.H. RAD50 expression is associated with poor clinical outcomes after radiotherapy for resected non–small cell lung cancer. Clin. Cancer Res., 2018, 24(2), 341-350.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-1455] [PMID: 29030353]
[51]
Yuan, Z.; Villagra, A.; Peng, L.; Coppola, D.; Glozak, M.; Sotomayor, E.M.; Chen, J.; Lane, W.S.; Seto, E. The ATDC (TRIM29) protein binds p53 and antagonizes p53-mediated functions. Mol. Cell. Biol., 2010, 30(12), 3004-3015.
[http://dx.doi.org/10.1128/MCB.01023-09] [PMID: 20368352]
[52]
Wang, L.; Yang, H.; Abel, E.V.; Ney, G.M.; Palmbos, P.L.; Bednar, F.; Zhang, Y.; Leflein, J.; Waghray, M.; Owens, S.; Wilkinson, J.E.; Prasad, J.; Ljungman, M.; Rhim, A.D.; Pasca di Magliano, M.; Simeone, D.M. ATDC induces an invasive switch in KRAS-induced pancreatic tumorigenesis. Genes Dev., 2015, 29(2), 171-183.
[http://dx.doi.org/10.1101/gad.253591.114] [PMID: 25593307]
[53]
Xu, X.; Wang, Y.; Chen, J.; Ma, H.; Shao, Z.; Chen, H.; Jin, G. High expression of CX3CL1/CX3CR1 axis predicts a poor prognosis of pancreatic ductal adenocarcinoma. J. Gastrointest. Surg., 2012, 16(8), 1493-1498.
[http://dx.doi.org/10.1007/s11605-012-1921-7] [PMID: 22639377]
[54]
Geismann, C.; Erhart, W.; Grohmann, F.; Schreiber, S.; Schneider, G.; Schäfer, H.; Arlt, A. TRAIL/NF-κB/CX3CL1 mediated onco-immuno crosstalk leading to trail resistance of pancreatic cancer cell lines. Int. J. Mol. Sci., 2018, 19(6), 1661.
[http://dx.doi.org/10.3390/ijms19061661] [PMID: 29867042]
[55]
Chandrasekar, B.; Mummidi, S.; Perla, R.P.; Bysani, S.; Dulin, N.O.; Liu, F.; Melby, P.C. Fractalkine (CX3CL1) stimulated by nuclear factor kappaB (NF-kappaB)-dependent inflammatory signals induces aortic smooth muscle cell proliferation through an autocrine pathway. Biochem. J., 2003, 373(2), 547-558.
[http://dx.doi.org/10.1042/bj20030207] [PMID: 12729461]

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