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Perspective

Proteomic profiling and network biology of colorectal cancer liver metastasis

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Pages 357-370 | Received 05 Jul 2023, Accepted 23 Oct 2023, Published online: 27 Oct 2023

References

  • Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet. 2014;383(9927):1490–1502. doi:10.1016/S0140-6736(13)61649-9
  • Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol. 2011;6(1):479–507. doi: 10.1146/annurev-pathol-011110-130235
  • Guinney J, Dienstmann R, Wang X, et al. The consensus molecular subtypes of colorectal cancer. Nat Med. 2015;21(11):1350–1356. doi: 10.1038/nm.3967
  • Isella C, Brundu F, Bellomo SE, et al. Selective analysis of cancer-cell intrinsic transcriptional traits defines novel clinically relevant subtypes of colorectal cancer. Nat Commun. 2017;8(1):15107. doi: 10.1038/ncomms15107
  • Lambert AW, Pattabiraman DR, Weinberg RA. Emerging biological principles of metastasis. Cell. 2017;168(4):670–691. doi:10.1016/j.cell.2016.11.037
  • Hanahan D. Hallmarks of cancer: new dimensions. Cancer Discov. 2022;12(1):31–46. doi:10.1158/2159-8290.CD-21-1059
  • Ell B, Kang Y. Transcriptional control of cancer metastasis. Trends Cell Biol. 2013;23(12):603–611. doi:10.1016/j.tcb.2013.06.001
  • Casal JI, Bartolomé RA. RGD cadherins and α2β1 integrin in cancer metastasis: a dangerous liaison. Biochim Biophys Acta Rev Cancer. 2018;1869(2):321–332. doi:10.1016/j.bbcan.2018.04.005
  • Cox TR. The matrix in cancer. Nat Rev Cancer. 2021;21(4):217–238. doi:10.1038/s41568-020-00329-7
  • Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90. doi:10.3322/caac.20107
  • Munro MJ, Wickremesekera SK, Peng L, et al. Cancer stem cells in colorectal cancer: a review. J Clin Pathol. 2018;71(2):110–116. doi:10.1136/jclinpath-2017-204739
  • Oskarsson T, Batlle E, Massague J. Metastatic stem cells: sources, niches, and vital pathways. Cell Stem Cell. 2014;14(3):306–321. doi:10.1016/j.stem.2014.02.002
  • Peitzsch C, Tyutyunnykova A, Pantel K, et al. Cancer stem cells: the root of tumor recurrence and metastases. Semin Cancer Biol. 2017;44:10–24. doi:10.1016/j.semcancer.2017.02.011
  • Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell. 2014;14(3):275–291. doi:10.1016/j.stem.2014.02.006
  • Donnenberg VS, Donnenberg AD. Multiple drug resistance in cancer revisited: the cancer stem cell hypothesis. J Clin Pharmacol. 2005;45(8):872–877. doi:10.1177/0091270005276905
  • Hsu CS, Tung CY, Yang CY, et al. Response to stress in early tumor colonization modulates switching of CD133-positive and CD133-negative subpopulations in a human metastatic colon cancer cell line, SW620. PLoS One. 2013;8(4):e61133. doi:10.1371/journal.pone.0061133
  • Wong GYM, Diakos C, Hugh TJ, et al. Proteomic profiling and biomarker discovery in colorectal liver metastases. Int J Mol Sci. 2022;23(11):6091. doi: 10.3390/ijms23116091
  • de Wit M, Fijneman RJ, Verheul HM, et al. Proteomics in colorectal cancer translational research: biomarker discovery for clinical applications. Clin Biochem. 2013;46(6):466–479. doi:10.1016/j.clinbiochem.2012.10.039
  • Li C, Sun YD, Yu GY, et al. Integrated omics of metastatic colorectal cancer. Cancer Cell. 2020;38(5):734–747 e739. doi: 10.1016/j.ccell.2020.08.002
  • Zhang B, Wang J, Wang X, et al. Proteogenomic characterization of human colon and rectal cancer. Nature. 2014;513(7518):382–387. doi: 10.1038/nature13438
  • Bartolome RA, Barderas R, Torres S, et al. Cadherin-17 interacts with alpha2beta1 integrin to regulate cell proliferation and adhesion in colorectal cancer cells causing liver metastasis. Oncogene. 2014;33(13):1658–1669. doi: 10.1038/onc.2013.117
  • Dunham WH, Mullin M, Gingras AC. Affinity-purification coupled to mass spectrometry: basic principles and strategies. Proteomics. 2012;12(10):1576–1590. doi:10.1002/pmic.201100523
  • McIntyre RE, Buczacki SJ, Arends MJ, et al. Mouse models of colorectal cancer as preclinical models. BioEssays. 2015;37(8):909–920. doi:10.1002/bies.201500032
  • Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science. 1990;247(4940):322–324. doi:10.1126/science.2296722
  • Sakai E, Nakayama M, Oshima H, et al. Combined mutation of Apc, Kras, and Tgfbr2 effectively drives metastasis of intestinal cancer. Cancer Res. 2018;78(5):1334–1346. doi: 10.1158/0008-5472.CAN-17-3303
  • Jackstadt R, van Hooff SR, Leach JD, et al. Epithelial NOTCH signaling rewires the tumor microenvironment of colorectal cancer to drive poor-prognosis subtypes and metastasis. Cancer Cell. 2019;36(3):319–336 e317. doi: 10.1016/j.ccell.2019.08.003
  • Barderas R, Villar-Vázquez R, Fernández-Aceñero MJ, et al. Sporadic colon cancer murine models demonstrate the value of autoantibody detection for preclinical cancer diagnosis. Sci Rep. 2013;3(1):2938. doi: 10.1038/srep02938
  • Neufert C, Heichler C, Brabletz T, et al. Inducible mouse models of colon cancer for the analysis of sporadic and inflammation-driven tumor progression and lymph node metastasis. Nat Protoc. 2021;16(1):61–85. doi: 10.1038/s41596-020-00412-1
  • Torres S, Bartolome RA, Mendes M, et al. Proteome profiling of cancer-associated fibroblasts identifies novel proinflammatory signatures and prognostic markers for colorectal cancer. Clin Cancer Res. 2013;19(21):6006–6019. doi: 10.1158/1078-0432.CCR-13-1130
  • Torres S, Garcia-Palmero I, Herrera M, et al. LOXL2 is highly expressed in cancer-associated fibroblasts and associates to poor colon cancer survival. Clin Cancer Res. 2015;21(21):4892–4902. doi: 10.1158/1078-0432.CCR-14-3096
  • Wong CC, Tse AP, Huang YP, et al. Lysyl oxidase-like 2 is critical to tumor microenvironment and metastatic niche formation in hepatocellular carcinoma. Hepatology. 2014;60(5):1645–1658. doi: 10.1002/hep.27320
  • García-Palmero I, Torres S, Bartolomé RA, et al. Twist1-induced activation of human fibroblasts promotes matrix stiffness by upregulating palladin and collagen α1(VI). Oncogene. 2016;35(40):5224–5236. doi: 10.1038/onc.2016.57
  • Bose S, Clevers H, Shen X. Promises and challenges of organoid-Guided Precision Medicine. Med. 2021;2(9):1011–1026. doi:10.1016/j.medj.2021.08.005
  • Fumagalli A, Suijkerbuijk SJE, Begthel H, et al. A surgical orthotopic organoid transplantation approach in mice to visualize and study colorectal cancer progression. Nat Protoc. 2018;13(2):235–247. doi: 10.1038/nprot.2017.137
  • Codrich M, Dalla E, Mio C, et al. Integrated multi-omics analyses on patient-derived CRC organoids highlight altered molecular pathways in colorectal cancer progression involving PTEN. J Exp Clin Cancer Res. 2021;40(1):198. doi: 10.1186/s13046-021-01986-8
  • O’Rourke KP, Loizou E, Livshits G, et al. Transplantation of engineered organoids enables rapid generation of metastatic mouse models of colorectal cancer. Nat Biotechnol. 2017;35(6):577–582. doi: 10.1038/nbt.3837
  • de Sousa EMF, Harnoss JM, Kljavin N, et al. Modeling colorectal cancer progression through orthotopic implantation of organoids. Methods Mol Biol. 2020;2171:331–346.
  • Cristobal A, van den Toorn HWP, van de Wetering M, et al. Personalized Proteome profiles of healthy and tumor human colon organoids reveal both individual diversity and basic features of colorectal cancer. Cell Rep. 2017;18(1):263–274. doi:10.1016/j.celrep.2016.12.016
  • Dijkstra JJ, Neikes HK, Rezaeifard S, et al. Multiomics of colorectal cancer organoids reveals putative mediators of cancer progression resulting from SMAD4 inactivation. J Proteome Res. 2023;22(1):138–151. doi: 10.1021/acs.jproteome.2c00551
  • Lindeboom RG, van Voorthuijsen L, Oost KC, et al. Integrative multi-omics analysis of intestinal organoid differentiation. Mol Syst Biol. 2018;14(6):e8227. doi: 10.15252/msb.20188227
  • Medico E, Russo M, Picco G, et al. The molecular landscape of colorectal cancer cell lines unveils clinically actionable kinase targets. Nat Commun. 2015;6(1):7002. doi: 10.1038/ncomms8002
  • Barderas R, Bartolome RA, Fernandez-Acenero MJ, et al. High expression of IL-13 receptor alpha2 in colorectal cancer is associated with invasion, liver metastasis, and poor prognosis. Cancer Res. 2012;72(11):2780–2790. doi:10.1158/0008-5472.CAN-11-4090
  • Luque-Garcia JL, Martinez-Torrecuadrada JL, Epifano C, et al. Differential protein expression on the cell surface of colorectal cancer cells is associated to tumor metastasis. Proteomics. 2010;10(5):940–952. doi:10.1002/pmic.200900441
  • Hegde P, Qi R, Gaspard R, et al. Identification of tumor markers in models of human colorectal cancer using a 19,200-element complementary DNA microarray. Cancer Res. 2001;61(21):7792–7797.
  • Tay PN, Tan P, Lan Y, et al. Palladin, an action-associated protein, is required for adherens junction formation and intercellular adhesion in HCT116 colorectal cancer cells. Int J Oncol. 2010;37(4):909–926. doi: 10.3892/ijo_00000742
  • Leibovitz A, Stinson JC, WB M, 3rd, CE M, Mazur KC, Mabry ND. Classification of human colorectal adenocarcinoma cell lines. Cancer Res. 1976;36(12): 4562–4569. 3rd.
  • Morikawa K, Walker SM, Nakajima M, et al. Influence of organ environment on the growth, selection, and metastasis of human colon carcinoma cells in nude mice. Cancer Res. 1988;48(23):6863–6871.
  • Berg KCG, Eide PW, Eilertsen IA, et al. Multi-omics of 34 colorectal cancer cell lines - a resource for biomedical studies. Mol Cancer. 2017;16(1):116. doi: 10.1186/s12943-017-0691-y
  • Mendes M, Peláez-García A, López-Lucendo M, et al. Mapping the spatial Proteome of metastatic cells in colorectal cancer. Proteomics. 2017;17(19):1700094. doi: 10.1002/pmic.201700094
  • Dang Y, Zhang S, Wang Y, et al. State-of-the-art: exosomes in colorectal cancer. Curr Cancer Drug Targets. 2022;22(1):2–17. doi:10.2174/1568009621666211110094442
  • Solis-Fernandez G, Montero-Calle A, Sanchez-Martinez M, et al. Aryl-hydrocarbon receptor-interacting protein regulates tumorigenic and metastatic properties of colorectal cancer cells driving liver metastasis. Br J Cancer. 2022;126(11):1604–1615. doi: 10.1038/s41416-022-01762-1
  • Tan HT, Wu W, Ng YZ, et al. Proteomic analysis of colorectal cancer metastasis: stathmin-1 revealed as a player in cancer cell migration and prognostic marker. J Proteome Res. 2012;11(2):1433–1445. doi: 10.1021/pr2010956
  • Lei Y, Huang K, Gao C, et al. Proteomics identification of ITGB3 as a key regulator in reactive oxygen species-induced migration and invasion of colorectal cancer cells. Mol & Cell Proteomics. 2011;10(10):M110 005397. doi: 10.1074/mcp.M110.005397
  • van Huizen NA, Coebergh van den Braak RRJ, Doukas M, et al. Up-regulation of collagen proteins in colorectal liver metastasis compared with normal liver tissue. J Biol Chem. 2019;294(1):281–289. doi:10.1074/jbc.RA118.005087
  • Yang Q, Bavi P, Wang JY, et al. Immuno-proteomic discovery of tumor tissue autoantigens identifies olfactomedin 4, CD11b, and integrin alpha-2 as markers of colorectal cancer with liver metastases. J Proteomics. 2017;168:53–65. doi:10.1016/j.jprot.2017.06.021
  • Bartolomé RA, Peláez-García A, Gomez I, et al. An RGD motif present in cadherin 17 induces integrin activation and tumor growth. J Biol Chem. 2014;289(50):34801–34814. doi: 10.1074/jbc.M114.600502
  • Bartolomé RA, Torres S, de Val S I, et al. VE-cadherin RGD motifs promote metastasis and constitute a potential therapeutic target in melanoma and breast cancers. Oncotarget. 2017;8(1):215–227. doi: 10.18632/oncotarget.13832
  • Casal JI, Bartolomé RA. Beyond N-Cadherin, relevance of cadherins 5, 6 and 17 in cancer progression and metastasis. Int J Mol Sci. 2019;20(13):3373. doi: 10.3390/ijms20133373
  • Bartolome RA, Robles J, Martin-Regalado A, et al. CDH6-activated αIIbβ3 crosstalks with α2β1 to trigger cellular adhesion and invasion in metastatic ovarian and renal cancers. Mol Oncol. 2021;15(7):1849–1865. doi: 10.1002/1878-0261.12947
  • Tian X, Han Z, Zhu Q, et al. Silencing of cadherin-17 enhances apoptosis and inhibits autophagy in colorectal cancer cells. Biomed Pharmacother. 2018;108:331–337. doi: 10.1016/j.biopha.2018.09.020
  • Ko S, Chu KM, Luk JM, et al. Overexpression of LI-cadherin in gastric cancer is associated with lymph node metastasis. Biochem Biophys Res Commun. 2004;319(2):562–568. doi: 10.1016/j.bbrc.2004.04.197
  • Tournier B, Aucagne R, Truntzer C, et al. Integrative clinical and DNA methylation analyses in a Population-based Cohort identifies CDH17 and LRP2 as risk recurrence factors in stage II colon cancer. Cancers (Basel). 2022;15(1):158. doi: 10.3390/cancers15010158
  • Lee CW, Lin SE, Tsai HI, et al. Cadherin 17 is related to recurrence and poor prognosis of cytokeratin 19-positive hepatocellular carcinoma. Oncol Lett. 2018;15(1):559–567. doi: 10.3892/ol.2017.7320
  • Bartolomé RA, Aizpurua C, Jaén M, et al. Monoclonal antibodies directed against cadherin RGD exhibit therapeutic activity against melanoma and colorectal cancer metastasis. Clin Cancer Res. 2018;24(2):433–444. doi: 10.1158/1078-0432.CCR-17-1444
  • Feng Z, He X, Zhang X, et al. Potent suppression of neuroendocrine tumors and gastrointestinal cancers by CDH17CAR T cells without toxicity to normal tissues. Nat Cancer. 2022;3(5):581–594. doi: 10.1038/s43018-022-00344-7
  • Wong KK. Integrated transcriptomics and proteomics data analysis identifies CDH17 as a key cell surface target in colorectal cancer. Comput Biol Chem. 2023;105:107897. doi:10.1016/j.compbiolchem.2023.107897
  • Bialucha CU, Collins SD, Li X, et al. Discovery and optimization of HKT288, a cadherin-6-targeting ADC for the treatment of ovarian and renal cancers. Cancer Discov. 2017;7(9):1030–1045. doi: 10.1158/2159-8290.CD-16-1414
  • de Wit M, Jimenez CR, Carvalho B, et al. Cell surface proteomics identifies glucose transporter type 1 and prion protein as candidate biomarkers for colorectal adenoma-to-carcinoma progression. Gut. 2012;61(6):855–864. doi: 10.1136/gutjnl-2011-300511
  • Schunter AJ, Yue X, Hummon AB. Phosphoproteomics of colon cancer metastasis: comparative mass spectrometric analysis of the isogenic primary and metastatic cell lines SW480 and SW620. Anal Bioanal Chem. 2017;409(7):1749–1763. doi:10.1007/s00216-016-0125-5
  • Nataraj NB, Marrocco I, Yarden Y. Roles for growth factors and mutations in metastatic dissemination. Biochem Soc Trans. 2021;49(3):1409–1423. doi:10.1042/BST20210048
  • Jaén M, Á M-R, Bartolomé RA, et al. Interleukin 13 receptor alpha 2 (IL13Rα2): expression, signaling pathways and therapeutic applications in cancer. Biochim Biophys Acta Rev Cancer. 2022;1877(5):188802. doi:10.1016/j.bbcan.2022.188802
  • Bartolome RA, Garcia-Palmero I, Torres S, et al. IL13 receptor alpha2 signaling requires a scaffold protein, FAM120A, to activate the FAK and PI3K pathways in colon cancer metastasis. Cancer Res. 2015;75(12):2434–2444. doi:10.1158/0008-5472.CAN-14-3650
  • Bartolome RA, Martin-Regalado A, Jaen M, et al. Protein tyrosine phosphatase-1B inhibition disrupts IL13Rα2-promoted invasion and metastasis in cancer cells. Cancers (Basel). 2020;12(2):500. doi: 10.3390/cancers12020500
  • Liu X, Brodeur SR, Gish G, et al. Regulation of c-src tyrosine kinase activity by the src SH2 domain. Oncogene. 1993;8(5):1119–1126.
  • Lupardus PJ, Birnbaum ME, Garcia KC. Molecular basis for shared cytokine recognition revealed in the structure of an unusually high affinity complex between IL-13 and IL-13Ralpha2. Structure. 2010;18(3):332–342. doi:10.1016/j.str.2010.01.003
  • Bartolome RA, Jaen M, Casal JI. An IL13Ralpha2 peptide exhibits therapeutic activity against metastatic colorectal cancer. Br J Cancer. 2018;119(8):940–949. doi:10.1038/s41416-018-0259-7
  • Jaén M, Bartolomé RA, Aizpurua C, et al. Inhibition of liver metastasis in colorectal cancer by targeting IL-13/IL13Rα2 binding site with specific monoclonal antibodies. Cancers (Basel). 2021;13(7):1731. doi: 10.3390/cancers13071731
  • Krishnan N, Koveal D, Miller DH, et al. Targeting the disordered C terminus of PTP1B with an allosteric inhibitor. Nat Chem Biol. 2014;10(7):558–566. doi: 10.1038/nchembio.1528
  • Marquez-Ortiz RA, Contreras-Zarate MJ, Tesic V, et al. IL13Ralpha2 promotes proliferation and outgrowth of breast cancer brain metastases. Clin Cancer Res. 2021;27(22):6209–6221. doi: 10.1158/1078-0432.CCR-21-0361
  • Fujisawa T, Joshi B, Nakajima A, et al. A novel role of interleukin-13 receptor alpha2 in pancreatic cancer invasion and metastasis. Cancer Res. 2009;69(22):8678–8685. doi:10.1158/0008-5472.CAN-09-2100
  • Mende AL, Schulte JD, Okada H, et al. Current advances in immunotherapy for glioblastoma. Curr Oncol Rep. 2021;23(2):21. doi:10.1007/s11912-020-01007-5
  • Knudson KM, Hwang S, McCann MS, et al. Recent advances in IL-13Ralpha2-directed cancer immunotherapy. Front Immunol. 2022;13:878365. doi:10.3389/fimmu.2022.878365
  • Zhao L, Liu L, Wang S, et al. Differential proteomic analysis of human colorectal carcinoma cell lines metastasis-associated proteins. J Cancer Res Clin Oncol. 2007;133(10):771–782. doi:10.1007/s00432-007-0222-0
  • Zhu L, Ren S, Daniels MJ, et al. Exogenous HMGB1 promotes the proliferation and metastasis of pancreatic cancer cells. Front Med. 2021;8:756988. doi: 10.3389/fmed.2021.756988
  • Barderas R, Mendes M, Torres S, et al. In-depth characterization of the secretome of colorectal cancer metastatic cells identifies key proteins in cell adhesion, migration, and invasion. Mol & Cell Proteomics. 2013;12(6):1602–1620. doi: 10.1074/mcp.M112.022848
  • Escudero-Paniagua B, Bartolomé RA, Rodríguez S, et al. PAUF/ZG16B promotes colorectal cancer progression through alterations of the mitotic functions and the Wnt/β-catenin pathway. Carcinogenesis. 2020;41(2):203–213. doi: 10.1093/carcin/bgz093
  • Youn SE, Jiang F, Won HY, et al. PAUF induces migration of human pancreatic cancer cells exclusively via the TLR4/MyD88/NF-κB signaling pathway. Int J Mol Sci. 2022;23(19):11414. doi: 10.3390/ijms231911414
  • Kim SJ, Lee Y, Kim NY, et al. Pancreatic adenocarcinoma upregulated factor, a novel endothelial activator, promotes angiogenesis and vascular permeability. Oncogene. 2013;32(31):3638–3647. doi: 10.1038/onc.2012.366
  • Gao H, Chakraborty G, Lee-Lim AP, et al. The BMP inhibitor coco reactivates breast cancer cells at lung metastatic sites. Cell. 2012;150(4):764–779. doi: 10.1016/j.cell.2012.06.035
  • Bartolomé RA, Pintado-Berninches L, Jaén M, et al. SOSTDC1 promotes invasion and liver metastasis in colorectal cancer via interaction with ALCAM/CD166. Oncogene. 2020;39(38):6085–6098. doi:10.1038/s41388-020-01419-4
  • Yang Y, Sanders AJ, Dou QP, et al. The clinical and theranostic values of activated leukocyte cell adhesion molecule (ALCAM)/CD166 in human solid cancers. Cancers (Basel). 2021;13(20):5187. doi: 10.3390/cancers13205187
  • Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020;367(6478). doi: 10.1126/science.aau6977
  • Choi DS, Choi DY, Hong BS, et al. Quantitative proteomics of extracellular vesicles derived from human primary and metastatic colorectal cancer cells. J Extracell Vesicles. 2012;1(1). doi: 10.3402/jev.v1i0.18704
  • Ji H, Greening DW, Barnes TW, et al. Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics. 2013;13(10–11):1672–1686. doi: 10.1002/pmic.201200562
  • Suwakulsiri W, Rai A, Xu R, et al. Proteomic profiling reveals key cancer progression modulators in shed microvesicles released from isogenic human primary and metastatic colorectal cancer cell lines. Biochim Biophys Acta Proteins Proteom. 2019;1867(12):140171. doi:10.1016/j.bbapap.2018.11.008
  • Robles J, Pintado-Berninches L, Boukich I, et al. A prognostic six-gene expression risk-score derived from proteomic profiling of the metastatic colorectal cancer secretome. J Pathol Clin Res. 2022;8(6):495–508. doi: 10.1002/cjp2.294
  • Miyahara Y, Takano S, Sogawa K, et al. Prosaposin, tumor-secreted protein, promotes pancreatic cancer progression by decreasing tumor-infiltrating lymphocytes. Cancer Sci. 2022;113(8):2548–2559. doi: 10.1111/cas.15444
  • Hatsuzawa Y, Yamaguchi K, Takanashi T, et al. CD109 promotes the tumorigenic ability and metastatic motility of pancreatic ductal adenocarcinoma cells. Pancreatology. 2020;20(3):493–500. doi: 10.1016/j.pan.2020.01.013
  • Huang Y, Chang A, Zhou W, et al. IGFBP3 as an indicator of lymph node metastasis and unfavorable prognosis for papillary thyroid carcinoma. Clin Exp Med. 2020;20(4):515–525. doi:10.1007/s10238-020-00642-3
  • Cruz PM, Mo H, McConathy WJ, et al. The role of cholesterol metabolism and cholesterol transport in carcinogenesis: a review of scientific findings, relevant to future cancer therapeutics. Front Pharmacol. 2013;4:119. doi:10.3389/fphar.2013.00119
  • Ding C, Chan DW, Liu W, et al. Proteome-wide profiling of activated transcription factors with a concatenated tandem array of transcription factor response elements. Proc Natl Acad Sci U S A. 2013;110(17):6771–6776. doi: 10.1073/pnas.1217657110
  • Torres S, Garcia-Palmero I, Marin-Vicente C, et al. Proteomic characterization of transcription and splicing factors associated with a metastatic phenotype in colorectal cancer. J Proteome Res. 2018;17(1):252–264. doi: 10.1021/acs.jproteome.7b00548
  • Okumura N, Yoshida H, Kitagishi Y, et al. Alternative splicings on p53, BRCA1 and PTEN genes involved in breast cancer. Biochem Biophys Res Commun. 2011;413(3):395–399. doi:10.1016/j.bbrc.2011.08.098
  • Sen S, Langiewicz M, Jumaa H, et al. Deletion of serine/arginine-rich splicing factor 3 in hepatocytes predisposes to hepatocellular carcinoma in mice. Hepatology. 2015;61(1):171–183. doi:10.1002/hep.27380
  • Liu J, Huang B, Xiao Y, et al. Aberrant expression of splicing factors in newly diagnosed acute myeloid leukemia. Onkologie. 2012;35(6):335–340. doi: 10.1159/000338941
  • Jansson EA, Are A, Greicius G, et al. The Wnt/beta-catenin signaling pathway targets PPARgamma activity in colon cancer cells. Proc Natl Acad Sci U S A. 2005;102(5):1460–1465. doi: 10.1073/pnas.0405928102
  • Zanocco-Marani T, Vignudelli T, Parenti S, et al. TFE3 transcription factor regulates the expression of MAFB during macrophage differentiation. Exp Cell Res. 2009;315(11):1798–1808. doi: 10.1016/j.yexcr.2009.03.018
  • Fang M, Ou J, Hutchinson L, et al. The BRAF oncoprotein functions through the transcriptional repressor MAFG to mediate the CpG island methylator phenotype. Mol Cell. 2014;55(6):904–915. doi:10.1016/j.molcel.2014.08.010
  • Kasuya K, Nagakawa Y, Hosokawa Y, et al. RhoA activity increases due to hypermethylation of ARHGAP28 in a highly liver-metastatic colon cancer cell line. Biomed Rep. 2016;4(3):335–339. doi: 10.3892/br.2016.582
  • Chen DL, Wang ZQ, Zeng ZL, et al. Identification of microRNA-214 as a negative regulator of colorectal cancer liver metastasis by way of regulation of fibroblast growth factor receptor 1 expression. Hepatology. 2014;60(2):598–609. doi: 10.1002/hep.27118
  • Chen HY, Lin YM, Chung HC, et al. miR-103/107 promote metastasis of colorectal cancer by targeting the metastasis suppressors DAPK and KLF4. Cancer Res. 2012;72(14):3631–3641. doi: 10.1158/0008-5472.CAN-12-0667
  • Gao J, Li N, Dong Y, et al. miR-34a-5p suppresses colorectal cancer metastasis and predicts recurrence in patients with stage II/III colorectal cancer. Oncogene. 2014;34(31):4142–4152. doi: 10.1038/onc.2014.348
  • Geng L, Chaudhuri A, Talmon G, et al. MicroRNA-192 suppresses liver metastasis of colon cancer. Oncogene. 2014;33(46):5332–5340. doi: 10.1038/onc.2013.478
  • Hur K, Toiyama Y, Schetter AJ, et al. Identification of a metastasis-specific MicroRNA signature in human colorectal cancer. J Natl Cancer Inst. 2015;107(3). doi: 10.1093/jnci/dju492
  • Hur K, Toiyama Y, Takahashi M, et al. MicroRNA-200c modulates epithelial-to-mesenchymal transition (EMT) in human colorectal cancer metastasis. Gut. 2013;62(9):1315–1326. doi: 10.1136/gutjnl-2011-301846
  • Jahid S, Sun J, Edwards RA, et al. miR-23a promotes the transition from indolent to invasive colorectal cancer. Cancer Discov. 2012;2(6):540–553. doi: 10.1158/2159-8290.CD-11-0267
  • Okamoto K, Ishiguro T, Midorikawa Y, et al. miR-493 induction during carcinogenesis blocks metastatic settlement of colon cancer cells in liver. EMBO J. 2012;31(7):1752–1763. doi: 10.1038/emboj.2012.25
  • Loo JM, Scherl A, Nguyen A, et al. Extracellular metabolic energetics can promote cancer progression. Cell. 2015;160(3):393–406. doi: 10.1016/j.cell.2014.12.018
  • Torres S, Garcia-Palmero I, Bartolome RA, et al. Combined miRNA profiling and proteomics demonstrates that different miRnas target a common set of proteins to promote colorectal cancer metastasis. J Pathol. 2017;242(1):39–51. doi: 10.1002/path.4874
  • Wu Y, Wang W, Yang AG, et al. The microRNA-424/503 cluster: a master regulator of tumorigenesis and tumor progression with paradoxical roles in cancer. Cancer Lett. 2020;494:58–72. doi:10.1016/j.canlet.2020.08.027
  • Vasaikar S, Huang C, Wang X, et al. Proteogenomic analysis of human colon cancer reveals new therapeutic opportunities. Cell. 2019;177(4):1035–1049 e1019. doi: 10.1016/j.cell.2019.03.030

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