https://doi.org/10.4081/ejh.2021.3246
NOP14 regulates the growth, migration, and invasion of colorectal cancer cells by modulating the NRIP1/GSK-3β/β-catenin signaling pathway
Submitted: 15 March 2021
Accepted: 25 May 2021
Published: 2 July 2021
Accepted: 25 May 2021
Abstract Views: 1808
PDF: 549
HTML: 26
HTML: 26
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Colorectal cancer (CRC) is the third most common cancer diagnosed worldwide. Recently, nucleolar complex protein 14 (NOP14) has been discovered to play a critical role in cancer development and progression, but the mechanisms of action of NOP14 in colorectal cancer remain to be elucidated. In this study, we used collected colorectal cancer tissues and cultured colorectal cancer cell lines (SW480, HT29, HCT116, DLD1, Lovo), and measured the mRNA and protein expression levels of NOP14 in colorectal cancer cells using qPCR and western blotting. GFP-NOP14 was constructed and siRNA fragments against NOP14 were synthesized to investigate the importance of NOP14 for the development of colorectal cells. Transwell migration assays were used to measure cell invasion and migration, CCK-8 kits were used to measure cell activity, and flow cytometry was applied to the observation of apoptosis. We found that both the mRNA and protein levels of NOP14 were significantly upregulated in CRC tissues and cell lines. Overexpression of GFP-NOP14 markedly promoted the growth, migration, and invasion of the CRC cells HT19 and SW480, while genetic knockdown of NOP14 inhibited these behaviors. Overexpression of NOP14 promoted the expression of NRIP1 and phosphorylated inactivation of GSK-3β, leading to the upregulation of β-catenin. Genetic knockdown of NOP14 had the opposite effect on NRIP1/GSK-3/β-catenin signals. NOP14 therefore appears to be overexpressed in clinical samples and cell lines of colorectal cancer, and promotes the proliferation, growth, and metastasis of colorectal cancer cells by modulating the NRIP1/GSK-3β/β-catenin signaling pathway.
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68:394-424.
DOI: https://doi.org/10.3322/caac.21492
Zhou Z, Mo S, Dai W, Xiang W, Han L, Li Q, et al. Prognostic nomograms for predicting cause-specific survival and overall survival of stage I-III colon cancer patients: a large population-based study. Cancer Cell Int 2019;19:355.
DOI: https://doi.org/10.1186/s12935-019-1079-4
Advani SM, Advani PS, Brown DW, DeSantis SM, Korphaisarn K, VonVille HM, et al. Global differences in the prevalence of the CpG island methylator phenotype of colorectal cancer. BMC Cancer 2019;19:964.
DOI: https://doi.org/10.1186/s12885-019-6144-9
Zheng J, Park MH, Son DJ, Choi MG, Choi JS, Nam KT, et al. (E)-4-(3-(3,5-dimethoxyphenyl)allyl)-2-methoxyphenol inhibits growth of colon tumors in mice. Oncotarget 2015;6:41929-43.
DOI: https://doi.org/10.18632/oncotarget.5861
Cao G, Cheng D, Ye L, Pan Y, Yang F, Lyu S. Surgical resection of pulmonary metastases from colorectal cancer: 11 years of experiences. PLoS One 2017;12:e0175284.
DOI: https://doi.org/10.1371/journal.pone.0175284
Araghi M, Soerjomataram I, Jenkins M, Brierley J, Morris E, Bray F, et al. Global trends in colorectal cancer mortality: projections to the year 2035. Int J Cancer 2019;144:2992-3000.
DOI: https://doi.org/10.1002/ijc.32055
Keum N, Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol 2019;16:713-32.
DOI: https://doi.org/10.1038/s41575-019-0189-8
Dawson H, Kirsch R, Messenger D, Driman D. A review of current challenges in colorectal cancer reporting. Arch Pathol Lab Med 2019;143:869-82.
DOI: https://doi.org/10.5858/arpa.2017-0475-RA
Saad AM, Abdel-Rahman O. Initial systemic chemotherapeutic and targeted therapy strategies for the treatment of colorectal cancer patients with liver metastases. Expert Opin Pharmacother 2019;20:1767-75.
DOI: https://doi.org/10.1080/14656566.2019.1642324
Zhu DJ, Chen XW, OuYang MZ, Lu Y. Three surgical planes identified in laparoscopic complete mesocolic excision for right-sided colon cancer. World J Surg Oncol 2016;14:7.
DOI: https://doi.org/10.1186/s12957-015-0758-4
Zhang Y, Chen Z, Li J. The current status of treatment for colorectal cancer in China: A systematic review. Medicine (Baltimore) 2017;96:e8242.
DOI: https://doi.org/10.1097/MD.0000000000008242
Gu MJ, Huang QC, Bao CZ, Li YJ, Li XQ, Ye D, et al. Attributable causes of colorectal cancer in China. BMC Cancer 2018;18:38.
DOI: https://doi.org/10.1186/s12885-017-3968-z
Siegel R, DeSantis C, Virgo K, Stein K, Mariotto A, Smith T, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 2012;62:220-41.
DOI: https://doi.org/10.3322/caac.21149
Catalano I, Trusolino L. The Stromal and Immune Landscape of Colorectal Cancer Progression during Anti-EGFR Therapy. Cancer Cell 2019;36:1-3.
DOI: https://doi.org/10.1016/j.ccell.2019.06.001
Kennedy SA, Jarboui MA, Srihari S, Raso C, Bryan K, Dernayka L, et al. Extensive rewiring of the EGFR network in colorectal cancer cells expressing transforming levels of KRAS(G13D). Nat Commun 2020;11:499.
DOI: https://doi.org/10.1038/s41467-019-14224-9
Khan K, Valeri N, Dearman C, Rao S, Watkins D, Starling N, et al. Targeting EGFR pathway in metastatic colorectal cancer- tumour heterogeniety and convergent evolution. Crit Rev Oncol Hematol 2019;143:153-63.
DOI: https://doi.org/10.1016/j.critrevonc.2019.09.001
Rahbari NN, Kedrin D, Incio J, Liu H, Ho WW, Nia HT, et al. Anti-VEGF therapy induces ECM remodeling and mechanical barriers to therapy in colorectal cancer liver metastases. Sci Transl Med 2016;8:360ra135.
DOI: https://doi.org/10.1126/scitranslmed.aaf5219
Bhattacharya R, Ye XC, Wang R, Ling X, McManus M, Fan F, et al. Intracrine VEGF Signaling Mediates the Activity of Prosurvival Pathways in Human Colorectal Cancer Cells. Cancer Res 2016;76:3014-24.
DOI: https://doi.org/10.1158/0008-5472.CAN-15-1605
Firestein R, Bass AJ, Kim SY, Dunn IF, Silver SJ, Guney I, et al. CDK8 is a colorectal cancer oncogene that regulates beta-catenin activity. Nature 2008;455:547-51.
DOI: https://doi.org/10.1038/nature07179
Chatel G, Ganeff C, Boussif N, Delacroix L, Briquet A, Nolens G, et al. Hedgehog signaling pathway is inactive in colorectal cancer cell lines. Int J Cancer 2007;121:2622-7.
DOI: https://doi.org/10.1002/ijc.22998
Qiao L, Wong BC. Role of Notch signaling in colorectal cancer. Carcinogenesis 2009;30:1979-86.
DOI: https://doi.org/10.1093/carcin/bgp236
Matsushita M, Matsuzaki K, Date M, Watanabe T, Shibano K, Nakagawa T, et al. Down-regulation of TGF-beta receptors in human colorectal cancer: implications for cancer development. Br J Cancer 1999;80:194-205.
DOI: https://doi.org/10.1038/sj.bjc.6690339
Slattery ML, Lundgreen A, Kadlubar SA, Bondurant KL, Wolff RK. JAK/STAT/SOCS-signaling pathway and colon and rectal cancer. Mol Carcinog 2013;52:155-66.
DOI: https://doi.org/10.1002/mc.21841
Wach A, Kałuzińska K, Frączek P. PI3K-Akt and Ras-Raf-MAPK signaling in colorectal cancer - Comparison of activity in primary tumor tissues and primary tumour - Derived human colorectal cancer cell lines: PS122. Porto Biomed J 2017;2:215-6.
DOI: https://doi.org/10.1016/j.pbj.2017.07.097
Milkereit P, Strauss D, Bassler J, Gadal O, Kühn H, Schütz S, et al. A Noc complex specifically involved in the formation and nuclear export of ribosomal 40 S subunits. J Biol Chem 2003;278:4072-81.
DOI: https://doi.org/10.1074/jbc.M208898200
Kühn H, Hierlmeier T, Merl J, Jakob S, Aguissa-Touré AH, Milkereit P, et al. The Noc-domain containing C-terminus of Noc4p mediates both formation of the Noc4p-Nop14p submodule and its incorporation into the SSU processome. PLoS One 2009;4:e8370.
DOI: https://doi.org/10.1371/journal.pone.0008370
Hannes F, Hammond P, Quarrell O, Fryns JP, Devriendt K, Vermeesch JR. A microdeletion proximal of the critical deletion region is associated with mild Wolf-Hirschhorn syndrome. Am J Med Genet A 2012;158a:996-1004.
DOI: https://doi.org/10.1002/ajmg.a.35299
Li J, Fang R, Wang J, Deng L. NOP14 inhibits melanoma proliferation and metastasis by regulating Wnt/β-catenin signaling pathway. Braz J Med Biol Res 2018;52:e7952.
Ying Y, Li J, Xie H, Yan H, Jin K, He L, et al. CCND1, NOP14 and DNMT3B are involved in miR-502-5p-mediated inhibition of cell migration and proliferation in bladder cancer. Cell Prolif 2020;53:e12751.
DOI: https://doi.org/10.1111/cpr.12751
Du Y, Liu Z, You L, Hou P, Ren X, Jiao T, et al. Pancreatic Cancer Progression Relies upon Mutant p53-Induced Oncogenic Signaling Mediated by NOP14. Cancer Res 2017;77:2661-73.
DOI: https://doi.org/10.1158/0008-5472.CAN-16-2339
Chang SY, Huang J, Niu H, Wang J, Si Y, Bai ZG, et al. Epigenetic regulation of osteopontin splicing isoform c defines its role as a microenvironmental factor to promote the survival of colon cancer cells from 5-FU treatment. Cancer Cell Int. 2020;14;20:452.
DOI: https://doi.org/10.1186/s12935-020-01541-z
Zhou B, Wu Q, Chen G, Zhang TP, Zhao YP. NOP14 promotes proliferation and metastasis of pancreatic cancer cells. Cancer Lett 2012;322:195-203.
DOI: https://doi.org/10.1016/j.canlet.2012.03.010
Liu PC, Thiele DJ. Novel stress-responsive genes EMG1 and NOP14 encode conserved, interacting proteins required for 40S ribosome biogenesis. Mol Biol Cell 2001;12:3644-57.
DOI: https://doi.org/10.1091/mbc.12.11.3644
Zhou B, Irwanto A, Guo YM, Bei JX, Wu Q, Chen G, et al. Exome sequencing and digital PCR analyses reveal novel mutated genes related to the metastasis of pancreatic ductal adenocarcinoma. Cancer Biol Ther 2012;13:871-9.
DOI: https://doi.org/10.4161/cbt.20839
Cao Q, Wang X, Zhao M, Yang R, Malik R, Qiao Y, et al. The central role of EED in the orchestration of polycomb group complexes. Nat Commun 2014;5:3127.
DOI: https://doi.org/10.1038/ncomms4127
Woods NT, Mesquita RD, Sweet M, Carvalho MA, Li X, Liu Y, et al. Charting the landscape of tandem BRCT domain-mediated protein interactions. Sci Signal 2012;5:rs6.
DOI: https://doi.org/10.1126/scisignal.2002255
Kirsch VC, Orgler C, Braig S, Jeremias I, Auerbach D, Müller R, et al. The cytotoxic natural product vioprolide A targets nucleolar protein 14, which is essential for ribosome biogenesis. Angew Chem Int Ed Engl 2020;59:1595-600.
DOI: https://doi.org/10.1002/anie.201911158
Lei JJ, Peng RJ, Kuang BH, Yuan ZY, Qin T, Liu WS, et al. NOP14 suppresses breast cancer progression by inhibiting NRIP1/Wnt/β-catenin pathway. Oncotarget 2015;6:25701-14.
Goyal A, Fiskin E, Gutschner T, Polycarpou-Schwarz M, Gross M, Neugebauer J, et al. A cautionary tale of sense-antisense gene pairs: independent regulation despite inverse correlation of expression. Nucleic Acids Res 2017;45:12496-508.
DOI: https://doi.org/10.1093/nar/gkx952
Li J, Zhao R, Fang R, Wang J. [miR-122-5p inhibits the proliferation of melanoma cells by targeting NOP14].[Article in Chinese]. Nan Fang Yi Ke Da Xue Xue Bao 2018;38:1360-5.
Isaksson HS, Sorbe B, Nilsson TK. Whole genome expression profiling of blood cells in ovarian cancer patients-prognostic impact of the CYP1B1, MTSS1, NCALD, and NOP14. Oncotarget 2014;5:4040-9.
DOI: https://doi.org/10.18632/oncotarget.1938
Wang H, Sun L, Jiang J, Yu S, Zhou Q. Suppression of the proliferation and invasion of breast cancer cells by ST7L occurs through inhibition of activation of Wnt/GSK-3beta/beta-catenin signalling. Clin Exp Pharmacol Physiol 2020;47:119-26.
DOI: https://doi.org/10.1111/1440-1681.13166
Liu C, Liu L, Zhang Y, Jing H. Molecular mechanism of aquapontin (AQP3) in regulating differentiation and apoptosis of lung cancer stem cells through Wnt/GSK-3beta/beta-Catenin pathway. J BUON 2020;25:828-34.
Lv YF, Dai H, Yan GN, Meng G, Zhang X, Guo QN. Downregulation of tumor suppressing STF cDNA 3 promotes epithelial-mesenchymal transition and tumor metastasis of osteosarcoma by the Wnt/GSK-3beta/beta-catenin/Snail signaling pathway. Cancer Lett 2016;373:164-73.
DOI: https://doi.org/10.1016/j.canlet.2016.01.046
Lv S, Zhang J, He Y, Liu Q, Wang Z, Liu B, et al. MicroRNA-520e targets AEG-1 to suppress the proliferation and invasion of colorectal cancer cells through Wnt/GSK-3beta/beta-catenin signalling. Clin Exp Pharmacol Physiol 2020;47:158-67.
DOI: https://doi.org/10.1111/1440-1681.13185
White BD, Chien AJ, Dawson DW. Dysregulation of Wnt/beta-catenin signaling in gastrointestinal cancers. Gastroenterology 2012;142:219-32.
DOI: https://doi.org/10.1053/j.gastro.2011.12.001
Polakis P. Wnt signaling in cancer. Cold Spring Harb Perspect Biol 2012;4:a008052.
DOI: https://doi.org/10.1101/cshperspect.a008052
Zhou D, Quach KM, Yang C, Lee SY, Pohajdak B, Chen S. PNRC: a proline-rich nuclear receptor coregulatory protein that modulates transcriptional activation of multiple nuclear receptors including orphan receptors SF1 (steroidogenic factor 1) and ERRalpha1 (estrogen related receptor alpha-1). Mol Endocrinol 2000;14:986-98.
DOI: https://doi.org/10.1210/mend.14.7.0480
Cavailles V, Dauvois S, L'Horset F, Lopez G, Hoare S, Kushner PJ, et al. Nuclear factor RIP140 modulates transcriptional activation by the estrogen receptor. EMBO J 1995;14:3741-51.
DOI: https://doi.org/10.1002/j.1460-2075.1995.tb00044.x
Lei JJ, Peng RJ, Kuang BH, Yuan ZY, Qin T, Liu WS, et al. NOP14 suppresses breast cancer progression by inhibiting NRIP1/Wnt/beta-catenin pathway. Oncotarget 2015;6:25701-14.
DOI: https://doi.org/10.18632/oncotarget.4573
Lapierre M, Bonnet S, Bascoul-Mollevi C, Ait-Arsa I, Jalaguier S, Del Rio M, et al. RIP140 increases APC expression and controls intestinal homeostasis and tumorigenesis. J Clin Invest 2014;124:1899-913.
DOI: https://doi.org/10.1172/JCI65178
Li J, Fang R, Wang J, Deng L. NOP14 inhibits melanoma proliferation and metastasis by regulating Wnt/beta-catenin signaling pathway. Braz J Med Biol Res 2018;52:e7952.
DOI: https://doi.org/10.1590/1414-431x20187952
How to Cite
Zhu, X., Jia, W., Yan, Y., Huang, Y., & Wang, B. (2021). NOP14 regulates the growth, migration, and invasion of colorectal cancer cells by modulating the NRIP1/GSK-3β/β-catenin signaling pathway. European Journal of Histochemistry, 65(3). https://doi.org/10.4081/ejh.2021.3246
Copyright (c) 2021 The Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.
Similar Articles
- A Sun, S Noriki, Y Imamura, M Fukuda, Detection of cancer clones in human gastric adenoma by increased DNA-instability and other biomarkers , European Journal of Histochemistry: Vol. 47 No. 2 (2003)
- F. Perdoni, M. Falleni, D. Tosi, D, Cirasola, S. Romagnoli, P. Braidotti, E. Clementi, G. Bulfamante, E. Borghi, A histological procedure to study fungal infection in the wax moth Galleria mellonella , European Journal of Histochemistry: Vol. 58 No. 3 (2014)
- E. I. Cortés-Gutiérrez, M. I. Dávila-RodrÃguez, J. L. Fernández, C. López-Fernández, J. Gosálvez, Koilocytes are enriched for alkaline-labile sites , European Journal of Histochemistry: Vol. 54 No. 4 (2010)
- N. Kiga, I. Tojyo, T. Matsumoto, Y. Hiraishi, Y. Shinohara, S. Makino, S. Fujita, Expression of lumican and fibromodulin following interleukin-1 beta stimulation of disc cells of the human temporomandibular joint , European Journal of Histochemistry: Vol. 55 No. 2 (2011)
- V. Ferretti, Ã. Segal-Eiras, C.G. Barbeito, M.V. Croce, Muc5ac mucin expression during rat skin development , European Journal of Histochemistry: Vol. 59 No. 1 (2015)
- G. Cutroneo, G. Vermiglio, A. Centofanti, G. Rizzo, M. Runci, A. Favaloro, M.G. Piancino, P. Bracco, G. Ramieri, F. Bianchi, F. Speciale, A. Arco, F. Trimarchi, Morphofunctional compensation of masseter muscles in unilateral posterior crossbite patients , European Journal of Histochemistry: Vol. 60 No. 2 (2016)
- M.G. Bottone, G. Santin, C. Soldani, P. Veneroni, A.I. Scovassi, C. Alpini, Intracellular distribution of Tankyrases as detected by multicolor immunofluorescence techniques , European Journal of Histochemistry: Vol. 56 No. 1 (2012)
- Francesca Diomede, Soundara Rajan Thangavelu, Ilaria Merciaro, Monica D'Orazio, Placido Bramanti, Emanuela Mazzon, Oriana Trubiani, Porphyromonas gingivalis lipopolysaccharide stimulation in human periodontal ligament stem cells: role of epigenetic modifications to the inflammation , European Journal of Histochemistry: Vol. 61 No. 3 (2017)
- M.L. Escobar Sánchez, O.M. EcheverrÃa MartÃnez, G.H. Vázquez-Nin, Immunohistochemical and ultrastructural visualization of different routes of oocyte elimination in adult rats , European Journal of Histochemistry: Vol. 56 No. 2 (2012)
- Giuliano Mazzini, The Feulgen reaction: from pink-magenta to rainbow fluorescent at the Maffo Vialli’s School of Histochemistry , European Journal of Histochemistry: Vol. 68 No. 1 (2024): 1954-2024: 70 Years of Histochemical Research
<< < 17 18 19 20 21 22 23 24 25 26 > >>
You may also start an advanced similarity search for this article.
