Proteomics and Bioinformatics Identify Drug-Resistant-Related Genes with Prognostic Potential in Cholangiocarcinoma
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cell Culture
2.2. Establishment of Drug-Resistant CCA Cell Lines
2.3. Chemotherapeutic Drug Sensitivity Assay
2.4. Cell Migration and Invasion Assay
2.5. Proteomics Analysis Using LC-MS/MS
2.6. Identification of Differentially Expressed Proteins
2.7. Bioinformatics Analysis
2.8. Survival Analysis
2.9. RT-qPCR
2.10. Gene Knockdown Using siRNA
2.11. Statistical Analysis
3. Results
3.1. Drug-Resistant CCA Cell Lines Exhibit Aggressive Behaviors
3.2. Comparative Proteomic Analysis of Drug-Resistant CCA Cell Lines
3.3. Gene Ontology Analysis
3.4. The mRNA Expression of Upregulated Proteins in CCA Patients’ Tissues
3.5. Identification of Protein–Protein Interaction Networks
3.6. Assessment of the Prognostic Value of Six Selected Genes
3.7. Correlation among Six Genes in the Focused Network
3.8. siRNA-Mediated Knockdown of Six Selected Genes Attenuates Cell Migration, Cell Invasion, and Reverses Drug-Resistant Phenotypes
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Banales, J.M.; Marin, J.J.; Lamarca, A.; Rodrigues, P.M.; Khan, S.A.; Roberts, L.R.; Cardinale, V.; Carpino, G.; Andersen, J.B.; Braconi, C. Cholangiocarcinoma 2020: The next horizon in mechanisms and management. Nat. Rev. Gastroenterol. Hepatol. 2020, 17, 557–588. [Google Scholar] [CrossRef] [PubMed]
- Tawarungruang, C.; Khuntikeo, N.; Chamadol, N.; Laopaiboon, V.; Thuanman, J.; Thinkhamrop, K.; Kelly, M.; Thinkhamrop, B. Survival after surgery among patients with cholangiocarcinoma in Northeast Thailand according to anatomical and morphological classification. BMC Cancer 2021, 21, 497. [Google Scholar] [CrossRef]
- Marin, J.J.; Lozano, E.; Herraez, E.; Asensio, M.; Di Giacomo, S.; Romero, M.R.; Briz, O.; Serrano, M.A.; Efferth, T.; Macias, R.I. Chemoresistance and chemosensitization in cholangiocarcinoma. Biochim. Biophys. Acta Mol. Basis Dis. 2018, 1864, 1444–1453. [Google Scholar] [CrossRef] [PubMed]
- Kamangar, F.; Dores, G.M.; Anderson, W.F. Patterns of cancer incidence, mortality, and prevalence across five continents: Defining priorities to reduce cancer disparities in different geographic regions of the world. J. Clin. Oncol. 2006, 24, 2137–2150. [Google Scholar] [CrossRef] [PubMed]
- Govindan, S.V.; Kulsum, S.; Pandian, R.S.; Das, D.; Seshadri, M.; Hicks, W.; Kuriakose, M.A.; Suresh, A. Establishment and characterization of triple drug resistant head and neck squamous cell carcinoma cell lines. Mol. Med. Rep. 2015, 12, 3025–3032. [Google Scholar] [CrossRef] [PubMed]
- Tan, Y.; Li, J.; Zhao, G.; Huang, K.-C.; Cardenas, H.; Wang, Y.; Matei, D.; Cheng, J.-X. Metabolic reprogramming from glycolysis to fatty acid uptake and beta-oxidation in platinum-resistant cancer cells. Nat. Commun. 2022, 13, 4554. [Google Scholar] [CrossRef]
- Zuo, Q.; Liu, J.; Zhang, J.; Wu, M.; Guo, L.; Liao, W. Development of trastuzumab-resistant human gastric carcinoma cell lines and mechanisms of drug resistance. Sci. Rep. 2015, 5, 11634. [Google Scholar] [CrossRef]
- Posadas, E.; Simpkins, F.; Liotta, L.; MacDonald, C.; Kohn, E. Proteomic analysis for the early detection and rational treatment of cancer—Realistic hope? Ann. Oncol. 2005, 16, 16–22. [Google Scholar] [CrossRef]
- Nanjundan, M.; Byers, L.A.; Carey, M.S.; Siwak, D.R.; Raso, M.G.; Diao, L.; Wang, J.; Coombes, K.R.; Roth, J.A.; Mills, G.B. Proteomic profiling identifies pathways dysregulated in non-small cell lung cancer and an inverse association of AMPK and adhesion pathways with recurrence. J. Thorac. Oncol. 2010, 5, 1894–1904. [Google Scholar] [CrossRef]
- Sahukar Shruthi, B.; Vinodhkumar, P.; Amani, S. Proteomics: A new perspective for cancer. Adv. Biomed. Res. 2016, 2016, 67. [Google Scholar] [CrossRef]
- Chang, L.; Ni, J.; Beretov, J.; Wasinger, V.C.; Hao, J.; Bucci, J.; Malouf, D.; Gillatt, D.; Graham, P.H.; Li, Y. Identification of protein biomarkers and signaling pathways associated with prostate cancer radioresistance using label-free LC-MS/MS proteomic approach. Sci. Rep. 2017, 7, 41834. [Google Scholar] [CrossRef] [PubMed]
- Gao, Q.; Zhu, H.; Dong, L.; Shi, W.; Chen, R.; Song, Z.; Huang, C.; Li, J.; Dong, X.; Zhou, Y. Integrated proteogenomic characterization of HBV-related hepatocellular carcinoma. Cell 2019, 179, 561–577.e22. [Google Scholar] [CrossRef]
- Brandi, J.; Dando, I.; Dalla Pozza, E.; Biondani, G.; Jenkins, R.; Elliott, V.; Park, K.; Fanelli, G.; Zolla, L.; Costello, E. Proteomic analysis of pancreatic cancer stem cells: Functional role of fatty acid synthesis and mevalonate pathways. J. Proteomics 2017, 150, 310–322. [Google Scholar] [CrossRef]
- Gupta, M.K.; Polisetty, R.V.; Sharma, R.; Ganesh, R.A.; Gowda, H.; Purohit, A.K.; Ankathi, P.; Prasad, K.; Mariswamappa, K.; Lakshmikantha, A. Altered transcriptional regulatory proteins in glioblastoma and YBX1 as a potential regulator of tumor invasion. Sci. Rep. 2019, 9, 10986. [Google Scholar] [CrossRef]
- Lignitto, L.; LeBoeuf, S.E.; Homer, H.; Jiang, S.; Askenazi, M.; Karakousi, T.R.; Pass, H.I.; Bhutkar, A.J.; Tsirigos, A.; Ueberheide, B. Nrf2 activation promotes lung cancer metastasis by inhibiting the degradation of Bach1. Cell 2019, 178, 316–329.e18. [Google Scholar] [CrossRef] [PubMed]
- Sripa, B.; Leungwattanawanit, S.; Nitta, T.; Wongkham, C.; Bhudhisawasdi, V.; Puapairoj, A.; Sripa, C.; Miwa, M. Establishment and characterization of an opisthorchiasis-associated cholangiocarcinoma cell line (KKU-100). World J. Gastroenterol. 2005, 11, 3392. [Google Scholar] [CrossRef]
- Sripa, B.; Seubwai, W.; Vaeteewoottacharn, K.; Sawanyawisuth, K.; Silsirivanit, A.; Kaewkong, W.; Muisuk, K.; Dana, P.; Phoomak, C.; Lert-Itthiporn, W. Functional and genetic characterization of three cell lines derived from a single tumor of an Opisthorchis viverrini- associated cholangiocarcinoma patient. Human Cell 2020, 33, 695–708. [Google Scholar] [CrossRef]
- Wattanawongdon, W.; Hahnvajanawong, C.; Namwat, N.; Kanchanawat, S.; Boonmars, T.; Jearanaikoon, P.; Leelayuwat, C.; Techasen, A.; Seubwai, W. Establishment and characterization of gemcitabine-resistant human cholangiocarcinoma cell lines with multidrug resistance and enhanced invasiveness. Int. J. Oncol. 2015, 47, 398–410. [Google Scholar] [CrossRef] [PubMed]
- Johansson, C.; Samskog, J.; Sundström, L.; Wadensten, H.; Björkesten, L.; Flensburg, J. Differential expression analysis of Escherichia coli proteins using a novel software for relative quantitation of LC-MS/MS data. Proteomics 2006, 6, 4475–4485. [Google Scholar] [CrossRef]
- Thorsell, A.; Portelius, E.; Blennow, K.; Westman-Brinkmalm, A. Evaluation of sample fractionation using micro-scale liquid-phase isoelectric focusing on mass spectrometric identification and quantitation of proteins in a SILAC experiment. Rapid Commun. Mass Spectrom. 2007, 21, 771–778. [Google Scholar] [CrossRef]
- Perkins, D.N.; Pappin, D.J.; Creasy, D.M.; Cottrell, J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. ELECTROPHORESIS Int. J. 1999, 20, 3551–3567. [Google Scholar] [CrossRef]
- Pang, Z.; Zhou, G.; Ewald, J.; Chang, L.; Hacariz, O.; Basu, N.; Xia, J. Using MetaboAnalyst 5.0 for LC–HRMS spectra processing, multi-omics integration and covariate adjustment of global metabolomics data. Nat. Protoc. 2022, 17, 1735–1761. [Google Scholar] [CrossRef]
- Mi, H.; Muruganujan, A.; Ebert, D.; Huang, X.; Thomas, P.D. PANTHER version 14: More genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic Acids Res. 2019, 47, D419–D426. [Google Scholar] [CrossRef]
- Chandrashekar, D.S.; Karthikeyan, S.K.; Korla, P.K.; Patel, H.; Shovon, A.R.; Athar, M.; Netto, G.J.; Qin, Z.S.; Kumar, S.; Manne, U. UALCAN: An update to the integrated cancer data analysis platform. Neoplasia 2022, 25, 18–27. [Google Scholar] [CrossRef] [PubMed]
- Szklarczyk, D.; Gable, A.L.; Nastou, K.C.; Lyon, D.; Kirsch, R.; Pyysalo, S.; Doncheva, N.T.; Legeay, M.; Fang, T.; Bork, P. The STRING database in 2021: Customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 2021, 49, D605–D612. [Google Scholar] [CrossRef] [PubMed]
- Housman, G.; Byler, S.; Heerboth, S.; Lapinska, K.; Longacre, M.; Snyder, N.; Sarkar, S. Drug resistance in cancer: An overview. Cancers 2014, 6, 1769–1792. [Google Scholar] [CrossRef] [PubMed]
- Thongprasert, S. The role of chemotherapy in cholangiocarcinoma. Ann. Oncol. 2005, 16, ii93–ii96. [Google Scholar] [CrossRef]
- Uchibori, K.; Kasamatsu, A.; Sunaga, M.; Yokota, S.; Sakurada, T.; Kobayashi, E.; Yoshikawa, M.; Uzawa, K.; Ueda, S.; Tanzawa, H. Establishment and characterization of two 5-fluorouracil-resistant hepatocellular carcinoma cell lines. Int. J. Oncol. 2012, 40, 1005–1010. [Google Scholar] [CrossRef]
- He, L.; Zhu, H.; Zhou, S.; Wu, T.; Wu, H.; Yang, H.; Mao, H.; SekharKathera, C.; Janardhan, A.; Edick, A.M. Wnt pathway is involved in 5-FU drug resistance of colorectal cancer cells. Exp. Mol. Med. 2018, 50, 1–12. [Google Scholar] [CrossRef]
- Wang, W.; Cassidy, J.; O’Brien, V.; Ryan, K.M.; Collie-Duguid, E. Mechanistic and predictive profiling of 5-Fluorouracil resistance in human cancer cells. Cancer Res. 2004, 64, 8167–8176. [Google Scholar] [CrossRef]
- Takahashi, K.; Tanaka, M.; Inagaki, A.; Wanibuchi, H.; Izumi, Y.; Miura, K.; Nagayama, K.; Shiota, M.; Iwao, H. Establishment of a 5-fluorouracil-resistant triple-negative breast cancer cell line. Int. J. Oncol. 2013, 43, 1985–1991. [Google Scholar] [CrossRef] [PubMed]
- Chung, Y.M.; Park, S.-H.; Park, J.K.; Kim, Y.-T.; Kang, Y.-K.; Do Yoo, Y. Establishment and characterization of 5-fluorouracil-resistant gastric cancer cells. Cancer Lett. 2000, 159, 95–101. [Google Scholar] [CrossRef] [PubMed]
- Yu, Y.; Ding, F.; Gao, M.; Jia, Y.F.; Ren, L. Establishment and characterization of the gemcitabine-resistant human pancreatic cancer cell line SW1990/gemcitabine. Oncol. Lett. 2019, 18, 3065–3071. [Google Scholar] [CrossRef] [PubMed]
- Togawa, A.; Ito, H.; Kimura, F.; Shimizu, H.; Ohtsuka, M.; Shimamura, F.; Yoshidome, H.; Katoh, A.; Miyazaki, M. Establishment of gemcitabine-resistant human pancreatic cancer cells and effect of brefeldin-a on the resistant cell line. Pancreas 2003, 27, 220–224. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Zhang, W.; Fu, M.; Yang, A.; Huang, H.; Xie, J. Establishment of human pancreatic cancer gemcitabine-resistant cell line with ribonucleotide reductase overexpression. Oncol. Rep. 2015, 33, 383–390. [Google Scholar] [CrossRef] [PubMed]
- Fujiwara-Tani, R.; Sasaki, T.; Takagi, T.; Mori, S.; Kishi, S.; Nishiguchi, Y.; Ohmori, H.; Fujii, K.; Kuniyasu, H. Gemcitabine resistance in pancreatic ductal carcinoma cell lines stems from reprogramming of energy metabolism. Int. J. Mol. Sci. 2022, 23, 7824. [Google Scholar] [CrossRef] [PubMed]
- Mansoori, B.; Mohammadi, A.; Davudian, S.; Shirjang, S.; Baradaran, B. The different mechanisms of cancer drug resistance: A brief review. Adv. Pharm. Bull. 2017, 7, 339. [Google Scholar] [CrossRef] [PubMed]
- Khan, S.U.; Fatima, K.; Aisha, S.; Malik, F. Unveiling the mechanisms and challenges of cancer drug resistance. Cell Commun. Signal 2024, 22, 109. [Google Scholar] [CrossRef]
- Rao, L.; Ma, N.; Liu, Y.; Du, L.; Qu, B. Correlation between adjuvant chemotherapy regimen, recurrence pattern and prognosis of cholangiocarcinoma after radical surgery. Front. Oncol. 2022, 12, 324. [Google Scholar] [CrossRef]
- Rahl, P.B.; Lin, C.Y.; Seila, A.C.; Flynn, R.A.; McCuine, S.; Burge, C.B.; Sharp, P.A.; Young, R.A. c-Myc regulates transcriptional pause release. Cell 2010, 141, 432–445. [Google Scholar] [CrossRef]
- Cichowski, K.; Jacks, T. NF1 tumor suppressor gene function: Narrowing the GAP. Cell 2001, 104, 593–604. [Google Scholar] [CrossRef]
- Krook, M.A.; Reeser, J.W.; Ernst, G.; Barker, H.; Wilberding, M.; Li, G.; Chen, H.-Z.; Roychowdhury, S. Fibroblast growth factor receptors in cancer: Genetic alterations, diagnostics, therapeutic targets and mechanisms of resistance. Br. J. Cancer 2021, 124, 880–892. [Google Scholar] [CrossRef]
- Sharma, S.V.; Bell, D.W.; Settleman, J.; Haber, D.A. Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 2007, 7, 169–181. [Google Scholar] [CrossRef]
- Morova, T.; McNeill, D.R.; Lallous, N.; Gönen, M.; Dalal, K.; Wilson, D.M., III; Gürsoy, A.; Keskin, Ö.; Lack, N.A. Androgen receptor-binding sites are highly mutated in prostate cancer. Nat. Commun. 2020, 11, 832. [Google Scholar] [CrossRef]
- Fantini, M.C.; Pallone, F. Cytokines: From gut inflammation to colorectal cancer. Curr. Drug Targets 2008, 9, 375–380. [Google Scholar] [CrossRef]
- Matanić, D.; Beg-Zec, Z.; Stojanović, D.; Matakorić, N.; Flego, V.; Milevoj-Ribić, F. Cytokines in patients with lung cancer. Scand. J. Immunol. 2003, 57, 173–178. [Google Scholar] [CrossRef]
- Nikolaou, M.; Pavlopoulou, A.; Georgakilas, A.G.; Kyrodimos, E. The challenge of drug resistance in cancer treatment: A current overview. Clin. Exp. Metastasis 2018, 35, 309–318. [Google Scholar] [CrossRef]
- Holm, P.S.; Lage, H.; Bergmann, S.; Jürchott, K.; Glockzin, G.; Bernshausen, A.; Mantwill, K.; Ladhoff, A.; Wichert, A.; Mymryk, J.S. Multidrug-resistant cancer cells facilitate E1-independent adenoviral replication: Impact for cancer gene therapy. Cancer Res. 2004, 64, 322–328. [Google Scholar] [CrossRef] [PubMed]
- Cole, S.; Bhardwaj, G.; Gerlach, J.; Mackie, J.; Grant, C.; Almquist, K.; Stewart, A.; Kurz, E.; Duncan, A.; Deeley, R.G. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992, 258, 1650–1654. [Google Scholar] [CrossRef]
- Morrow, C.; Cowan, K. Glutathione S-transferases and drug resistance. Cancer Cells 1990, 2, 15–22. [Google Scholar] [CrossRef]
- Sharma, S.; Shah, N.A.; Joiner, A.M.; Roberts, K.H.; Canman, C.E. DNA polymerase ζ is a major determinant of resistance to platinum-based chemotherapeutic agents. Mol. Pharmacol. 2012, 81, 778–787. [Google Scholar] [CrossRef] [PubMed]
- Zamble, D.B.; Lippard, S.J. Cisplatin and DNA repair in cancer chemotherapy. Trends Biochem. Sci. 1995, 20, 435–439. [Google Scholar] [CrossRef] [PubMed]
- Pang, B.; Qiao, X.; Janssen, L.; Velds, A.; Groothuis, T.; Kerkhoven, R.; Nieuwland, M.; Ovaa, H.; Rottenberg, S.; Van Tellingen, O. Drug-induced histone eviction from open chromatin contributes to the chemotherapeutic effects of doxorubicin. Nat. Commun. 2013, 4, 1908. [Google Scholar] [CrossRef] [PubMed]
- Kamphorst, A.O.; Pillai, R.N.; Yang, S.; Nasti, T.H.; Akondy, R.S.; Wieland, A.; Sica, G.L.; Yu, K.; Koenig, L.; Patel, N.T. Proliferation of PD-1+ CD8 T cells in peripheral blood after PD-1–targeted therapy in lung cancer patients. Proc. Natl. Acad. Sci. USA 2017, 114, 4993–4998. [Google Scholar] [CrossRef] [PubMed]
- Roninson, I.B.; Broude, E.V.; Chang, B.-D. If not apoptosis, then what? Treatment-induced senescence and mitotic catastrophe in tumor cells. Drug Resist. Updat. 2001, 4, 303–313. [Google Scholar] [CrossRef] [PubMed]
- O’Brien, S.; Golubovskaya, V.M.; Conroy, J.; Liu, S.; Wang, D.; Liu, B.; Cance, W.G. FAK inhibition with small molecule inhibitor Y15 decreases viability, clonogenicity, and cell attachment in thyroid cancer cell lines and synergizes with targeted therapeutics. Oncotarget 2014, 5, 7945. [Google Scholar] [CrossRef]
- Wang, Z.; Li, Y.; Kong, D.; Banerjee, S.; Ahmad, A.; Azmi, A.S.; Ali, S.; Abbruzzese, J.L.; Gallick, G.E.; Sarkar, F.H. Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res. 2009, 69, 2400–2407. [Google Scholar] [CrossRef]
- Erdogan, B.; Webb, D.J. Cancer-associated fibroblasts modulate growth factor signaling and extracellular matrix remodeling to regulate tumor metastasis. Biochem. Soc. Trans. 2017, 45, 229–236. [Google Scholar] [CrossRef]
- Sprenger, C.C.; Plymate, S.R.; Reed, M.J. Aging-related alterations in the extracellular matrix modulate the microenvironment and influence tumor progression. Int. J. Cancer 2010, 127, 2739–2748. [Google Scholar] [CrossRef]
- He, W.; Liang, B.; Wang, C.; Li, S.; Zhao, Y.; Huang, Q.; Liu, Z.; Yao, Z.; Wu, Q.; Liao, W. MSC-regulated lncRNA MACC1-AS1 promotes stemness and chemoresistance through fatty acid oxidation in gastric cancer. Oncogene 2019, 38, 4637–4654. [Google Scholar] [CrossRef]
- Iwamoto, H.; Abe, M.; Yang, Y.; Cui, D.; Seki, T.; Nakamura, M.; Hosaka, K.; Lim, S.; Wu, J.; He, X. Cancer lipid metabolism confers antiangiogenic drug resistance. Cell Metab. 2018, 28, 104–117.e5. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Fahrmann, J.F.; Lee, H.; Li, Y.-J.; Tripathi, S.C.; Yue, C.; Zhang, C.; Lifshitz, V.; Song, J.; Yuan, Y. JAK/STAT3-regulated fatty acid β-oxidation is critical for breast cancer stem cell self-renewal and chemoresistance. Cell Metab. 2018, 27, 136–150. [Google Scholar] [CrossRef] [PubMed]
- Peruzzi, B.; Bottaro, D.P. Targeting the c-Met signaling pathway in cancer. Clin. Cancer Res. 2006, 12, 3657–3660. [Google Scholar] [CrossRef]
- Comoglio, P.M.; Trusolino, L. Series Introduction: Invasive growth: From development to metastasis. J. Clin. Investig. 2002, 109, 857–862. [Google Scholar] [CrossRef]
- Aumailley, M. The laminin family. Cell Adh. Migr. 2013, 7, 48–55. [Google Scholar] [CrossRef]
- Chen, Z.; Yang, X.; Bi, G.; Liang, J.; Hu, Z.; Zhao, M.; Li, M.; Lu, T.; Zheng, Y.; Sui, Q. Ligand-receptor interaction atlas within and between tumor cells and T cells in lung adenocarcinoma. Int. J. Biol. Sci. 2020, 16, 2205. [Google Scholar] [CrossRef] [PubMed]
- Ran, T.; Chen, Z.; Zhao, L.; Ran, W.; Fan, J.; Hong, S.; Yang, Z. LAMB1 is related to the T stage and indicates poor prognosis in gastric cancer. Technol. Cancer Res. Treat. 2021, 20, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.; Kim, W.-J.; Kang, H.-G.; Jang, J.-H.; Choi, I.J.; Chun, K.-H.; Kim, S.-J. Upregulation of LAMB1 via ERK/c-Jun axis promotes gastric cancer growth and motility. Int. J. Mol. Sci. 2021, 22, 626. [Google Scholar] [CrossRef] [PubMed]
- Sakaguchi, T.; Yoshino, H.; Yonemori, M.; Miyamoto, K.; Sugita, S.; Matsushita, R.; Itesako, T.; Tatarano, S.; Nakagawa, M.; Enokida, H. Regulation of ITGA3 by the dual-stranded microRNA-199 family as a potential prognostic marker in bladder cancer. Br. J. Cancer 2017, 116, 1077–1087. [Google Scholar] [CrossRef]
- Stoeck, A.; Lejnine, S.; Truong, A.; Pan, L.; Wang, H.; Zang, C.; Yuan, J.; Ware, C.; MacLean, J.; Garrett-Engele, P.W. Discovery of biomarkers predictive of GSI response in triple-negative breast cancer and adenoid cystic carcinoma. Cancer Discov. 2014, 4, 1154–1167. [Google Scholar] [CrossRef]
- Wang, N.J.; Sanborn, Z.; Arnett, K.L.; Bayston, L.J.; Liao, W.; Proby, C.M.; Leigh, I.M.; Collisson, E.A.; Gordon, P.B.; Jakkula, L. Loss-of-function mutations in Notch receptors in cutaneous and lung squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 2011, 108, 17761–17766. [Google Scholar] [CrossRef]
- Pancewicz, J.; Taylor, J.M.; Datta, A.; Baydoun, H.H.; Waldmann, T.A.; Hermine, O.; Nicot, C. Notch signaling contributes to proliferation and tumor formation of human T-cell leukemia virus type 1–associated adult T-cell leukemia. Proc. Natl. Acad. Sci. USA 2010, 107, 16619–16624. [Google Scholar] [CrossRef]
- Kuhnert, F.; Chen, G.; Coetzee, S.; Thambi, N.; Hickey, C.; Shan, J.; Kovalenko, P.; Noguera-Troise, I.; Smith, E.; Fairhurst, J. Dll4 blockade in stromal cells mediates antitumor effects in preclinical models of ovarian cancer. Cancer Res. 2015, 75, 4086–4096. [Google Scholar] [CrossRef]
- Lu, J.; Ye, X.; Fan, F.; Xia, L.; Bhattacharya, R.; Bellister, S.; Tozzi, F.; Sceusi, E.; Zhou, Y.; Tachibana, I. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 2013, 23, 171–185. [Google Scholar] [CrossRef]
- Zou, Y.; Fang, F.; Ding, Y.J.; Dai, M.Y.; Yi, X.; Chen, C.; Tao, Z.Z.; Chen, S.M. Notch 2 signaling contributes to cell growth, anti-apoptosis and metastasis in laryngeal squamous cell carcinoma. Mol. Med. Rep. 2016, 14, 3517–3524. [Google Scholar] [CrossRef]
- Beverly, L.J.; Felsher, D.W.; Capobianco, A.J. Suppression of p53 by Notch in lymphomagenesis: Implications for initiation and regression. Cancer Res. 2005, 65, 7159–7168. [Google Scholar] [CrossRef]
- Dotto, G.P. Crosstalk of Notch with p53 and p63 in cancer growth control. Nat. Rev. Cancer 2009, 9, 587–595. [Google Scholar] [CrossRef]
- Capaccione, K.M.; Pine, S.R. The Notch signaling pathway as a mediator of tumor survival. Carcinogenesis 2013, 34, 1420–1430. [Google Scholar] [CrossRef]
- Qu, J.; Song, M.; Xie, J.; Huang, X.-Y.; Hu, X.-M.; Gan, R.-H.; Zhao, Y.; Lin, L.-S.; Chen, J.; Lin, X. Notch2 signaling contributes to cell growth, invasion, and migration in salivary adenoid cystic carcinoma. Mol. Cell. Biochem. 2016, 411, 135–141. [Google Scholar] [CrossRef]
- Zhu, H.-M.; Jiang, X.-S.; Li, H.-Z.; Qian, L.-X.; Du, M.-Y.; Lu, Z.-W.; Wu, J.; Tian, X.-K.; Fei, Q.; He, X. miR-184 inhibits tumor invasion, migration and metastasis in nasopharyngeal carcinoma by targeting Notch2. Cell. Physiol. Biochem. 2018, 49, 1564–1576. [Google Scholar] [CrossRef]
- Tanaka, M.; Setoguchi, T.; Hirotsu, M.; Gao, H.; Sasaki, H.; Matsunoshita, Y.; Komiya, S. Inhibition of Notch pathway prevents osteosarcoma growth by cell cycle regulation. Br. J. Cancer 2009, 100, 1957–1965. [Google Scholar] [CrossRef] [PubMed]
- Zhao, W.-X.; Wu, Z.-M.; Liu, W.; Lin, J.-H. Notch2 and Notch3 suppress the proliferation and mediate invasion of trophoblast cell lines. Biol. Open 2017, 6, 1123–1129. [Google Scholar] [CrossRef] [PubMed]
- Craene, B.D.; Berx, G. Regulatory networks defining EMT during cancer initiation and progression. Nat. Rev. Cancer 2013, 13, 97–110. [Google Scholar] [CrossRef] [PubMed]
- Thiery, J.P.; Acloque, H.; Huang, R.Y.; Nieto, M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139, 871–890. [Google Scholar] [CrossRef] [PubMed]
- Otte, J.; Dizdar, L.; Behrens, B.; Goering, W.; Knoefel, W.T.; Wruck, W.; Stoecklein, N.H.; Adjaye, J. FGF signalling in the self-renewal of colon cancer organoids. Sci. Rep. 2019, 9, 17365. [Google Scholar] [CrossRef] [PubMed]
- Ye, S.; Chen, Y.; Hu, B.; Huang, H.; Sun, Y.; Stewart, J.P.; Johnson, S.K.; Barlogie, B.; Zangari, M.; Tricot, G. N-Cadherin Stabilizes β-Catenin and Promotes β-Catenin/TCF Transcriptional Activation and Cell Adhesion-Mediated Drug Resistance in Multiple Myeloma. Blood 2021, 138, 1572. [Google Scholar] [CrossRef]
- Ciołczyk-Wierzbicka, D.; Laidler, P. The inhibition of invasion of human melanoma cells through N-cadherin knock-down. Med. Oncol. 2018, 35, 42. [Google Scholar] [CrossRef]
- Li, K.; He, W.; Lin, N.; Wang, X.; Fan, Q.-X. N-cadherin knock-down decreases invasiveness of esophageal squamous cell carcinoma in vitro. World J. Gastroenterol. WJG 2009, 15, 697. [Google Scholar] [CrossRef] [PubMed]
- Joshi, V.; Lakhani, S.R.; McCart Reed, A.E. NDRG1 in Cancer: A Suppressor, Promoter, or Both? Cancers 2022, 14, 5739. [Google Scholar] [CrossRef]
- Guan, R.J.; Ford, H.L.; Fu, Y.; Li, Y.; Shaw, L.M.; Pardee, A.B. Drg-1 as a differentiation-related, putative metastatic suppressor gene in human colon cancer. Cancer Res. 2000, 60, 749–755. [Google Scholar]
- Maruyama, Y.; Ono, M.; Kawahara, A.; Yokoyama, T.; Basaki, Y.; Kage, M.; Aoyagi, S.; Kinoshita, H.; Kuwano, M. Tumor growth suppression in pancreatic cancer by a putative metastasis suppressor gene Cap43/NDRG1/Drg-1 through modulation of angiogenesis. Cancer Res. 2006, 66, 6233–6242. [Google Scholar] [CrossRef] [PubMed]
- Bandyopadhyay, S.; Pai, S.K.; Hirota, S.; Hosobe, S.; Takano, Y.; Saito, K.; Piquemal, D.; Commes, T.; Watabe, M.; Gross, S.C. Role of the putative tumor metastasis suppressor gene Drg-1 in breast cancer progression. Oncogene 2004, 23, 5675–5681. [Google Scholar] [CrossRef] [PubMed]
- Akiba, J.; Ogasawara, S.; Kawahara, A.; Nishida, N.; Sanada, S.; Moriya, F.; Kuwano, M.; Nakashima, O.; Yano, H. N-myc downstream regulated gene 1 (NDRG1)/Cap43 enhances portal vein invasion and intrahepatic metastasis in human hepatocellular carcinoma. Oncol. Rep. 2008, 20, 1329–1335. [Google Scholar] [CrossRef] [PubMed]
- Ai, R.; Sun, Y.; Guo, Z.; Wei, W.; Zhou, L.; Liu, F.; Hendricks, D.T.; Xu, Y.; Zhao, X. NDRG1 overexpression promotes the progression of esophageal squamous cell carcinoma through modulating Wnt signaling pathway. Cancer Biol. Ther. 2016, 17, 943–954. [Google Scholar] [CrossRef]
- Ureshino, H.; Murakami, Y.; Watari, K.; Izumi, H.; Kawahara, A.; Kage, M.; Arao, T.; Nishio, K.; Yanagihara, K.; Kinoshita, H. N-myc downstream regulated gene 1 (NDRG1) promotes metastasis of human scirrhous gastric cancer cells through epithelial mesenchymal transition. PLoS ONE 2012, 7, e41312. [Google Scholar] [CrossRef]
Gene | Sequence (5′ to 3′) | |
---|---|---|
ACTB | For: | GGATTCCTATGTGGGCGACG |
Rev: | TTGTAGAAGGTGTGGTGCCAG | |
MET | For: | CGCACAAAGCAAGCCAGATT |
Rev: | AGTGCTCATGATTGGGTCCG | |
LAMB1 | For: | GGCAATCTGAAAATGGTGTGGA |
Rev: | ACGAGGCCTCACAGTCATAG | |
ITGA3 | For: | GGGACAGTGATGGGTGAGTC |
Rev: | GTAGGGCCACTCCAGACCTA | |
NOTCH2 | For: | AGGTGTCAGAATGGAGGGGT |
Rev: | GCCGTTGACACATACACAGC | |
CDH2 | For: | TGCAAGACTGGATTTCCTGAAGA |
Rev: | AGCTTCTCACGGCATACACC | |
NDRG1 | For: | ATTGGCATGGGAACAGGAGC |
Rev: | CATCCTGAGATCTTGGAGGCG |
siRNA | Target Gene | siRNA Sequence (5′ to 3′) |
---|---|---|
siMET | MET | GGACCGGUUCAUCAACUUCTT |
siLAMB1 | LAMB1 | AAUGUAACUGCAAUGAACATT |
siITGA3 | ITGA3 | GGAAAGGAAACAGCUACAUGATT |
siNOTCH2 | NOTCH2 | GAAUUGUCAGACAGUAUUGTT |
siCDH2 | CDH2 | UGACAACAGACCUGAGUUCTT |
siNDRG1 | NDRG1 | GACCACUCUCCUCAAGAUGTT |
siNC | - | UUCUCCGAACGUGUCACGUTT |
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Kerdkumthong, K.; Roytrakul, S.; Songsurin, K.; Pratummanee, K.; Runsaeng, P.; Obchoei, S. Proteomics and Bioinformatics Identify Drug-Resistant-Related Genes with Prognostic Potential in Cholangiocarcinoma. Biomolecules 2024, 14, 969. https://doi.org/10.3390/biom14080969
Kerdkumthong K, Roytrakul S, Songsurin K, Pratummanee K, Runsaeng P, Obchoei S. Proteomics and Bioinformatics Identify Drug-Resistant-Related Genes with Prognostic Potential in Cholangiocarcinoma. Biomolecules. 2024; 14(8):969. https://doi.org/10.3390/biom14080969
Chicago/Turabian StyleKerdkumthong, Kankamol, Sittiruk Roytrakul, Kawinnath Songsurin, Kandawasri Pratummanee, Phanthipha Runsaeng, and Sumalee Obchoei. 2024. "Proteomics and Bioinformatics Identify Drug-Resistant-Related Genes with Prognostic Potential in Cholangiocarcinoma" Biomolecules 14, no. 8: 969. https://doi.org/10.3390/biom14080969