Daily Profile of miRNAs in the Rat Colon and In Silico Analysis of Their Possible Relationship to Colorectal Cancer
Abstract
1. Introduction
2. Materials and Methods
2.1. Patients
2.2. In Vitro Experiments
2.3. Animal Study
2.4. PCR
2.5. NGS
2.6. In Silico Analysis
2.7. Statistical Analysis
3. Results
4. Discussion
Limitations of the Study
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Patke, A.; Young, M.W.; Axelrod, S. Molecular mechanisms and physiological importance of circadian rhythms. Nat. Rev. Mol. Cell Biol. 2020, 21, 67–84. [Google Scholar] [CrossRef] [PubMed]
- Pilorz, V.; Astiz, M.; Heinen, K.O.; Rawashdeh, O.; Oster, H. The Concept of Coupling in the Mammalian Circadian Clock Network. J. Mol. Biol. 2020, 432, 3618–3638. [Google Scholar] [CrossRef]
- Pan, Y.; van der Watt, P.J.; Kay, S.A. E-box binding transcription factors in cancer. Front. Oncol. 2023, 13, 1223208. [Google Scholar] [CrossRef] [PubMed]
- Honma, S. The mammalian circadian system: A hierarchical multi-oscillator structure for generating circadian rhythm. J. Physiol. Sci. 2018, 68, 207–219. [Google Scholar] [CrossRef]
- Zhang, R.; Lahens, N.F.; Ballance, H.I.; Hughes, M.E.; Hogenesch, J.B. A circadian gene expression atlas in mammals: Implications for biology and medicine. Proc. Natl. Acad. Sci. USA 2014, 111, 16219–16224. [Google Scholar] [CrossRef] [PubMed]
- Hansen, K.F.; Sakamoto, K.; Obrietan, K. MicroRNAs: A potential interface between the circadian clock and human health. Genome Med. 2011, 3, 10. [Google Scholar] [CrossRef]
- Hasakova, K.; Reis, R.; Vician, M.; Zeman, M.; Herichova, I. Expression of miR-34a-5p is up-regulated in human colorectal cancer and correlates with survival and clock gene PER2 expression. PLoS ONE 2019, 14, e0224396. [Google Scholar] [CrossRef]
- Fu, Z.; Wang, L.; Li, S.; Chen, F.; Au-Yeung, K.K.-W.; Shi, C. MicroRNA as an Important Target for Anticancer Drug Development. Front. Pharmacol. 2021, 12, 736323. [Google Scholar] [CrossRef]
- Wang, H.; Fan, Z.; Zhao, M.; Li, J.; Lu, M.; Liu, W.; Ying, H.; Liu, M.; Yan, J. Oscillating primary transcripts harbor miRNAs with circadian functions. Sci. Rep. 2016, 6, 21598. [Google Scholar] [CrossRef]
- Xu, S.; Witmer, P.D.; Lumayag, S.; Kovacs, B.; Valle, D. MicroRNA (miRNA) Transcriptome of Mouse Retina and Identification of a Sensory Organ-specific miRNA Cluster. J. Biol. Chem. 2007, 282, 25053–25066. [Google Scholar] [CrossRef]
- Cheng, H.Y.M.; Papp, J.W.; Varlamova, O.; Dziema, H.; Russell, B.; Curfman, J.P.; Nakazawa, T.; Shimizu, K.; Okamura, H.; Impey, S.; et al. microRNA Modulation of Circadian-Clock Period and Entrainment. Neuron 2007, 54, 813–829. [Google Scholar] [CrossRef]
- Gao, Q.; Zhou, L.; Yang, S.-Y.; Cao, J.-M. A novel role of microRNA 17-5p in the modulation of circadian rhythm. Sci. Rep. 2016, 6, 30070. [Google Scholar] [CrossRef]
- Kiessling, S.; Ucar, A.; Chowdhury, K.; Oster, H.; Eichele, G. Genetic background-dependent effects of murine micro RNAs on circadian clock function. PLoS ONE 2017, 12, e0176547. [Google Scholar] [CrossRef]
- Aten, S.; Hansen, K.F.; Price, K.H.; Wheaton, K.; Kalidindi, A.; Garcia, A.; Alzate-Correa, D.; Hoyt, K.R.; Obrietan, K. miR-132 couples the circadian clock to daily rhythms of neuronal plasticity and cognition. Learn. Mem. 2018, 25, 214–229. [Google Scholar] [CrossRef]
- Balakrishnan, A.; Stearns, A.T.; Park, P.J.; Dreyfuss, J.M.; Ashley, S.W.; Rhoads, D.B.; Tavakkolizadeh, A. MicroRNA mir-16 is anti-proliferative in enterocytes and exhibits diurnal rhythmicity in intestinal crypts. Exp. Cell Res. 2010, 316, 3512–3521. [Google Scholar] [CrossRef]
- Tan, X.; Zhang, P.; Zhou, L.; Yin, B.; Pan, H.; Peng, X. Clock-controlled mir-142-3p can target its activator, Bmal1. BMC Mol. Biol. 2012, 13, 27. [Google Scholar] [CrossRef] [PubMed]
- Na, Y.-J.; Sung, J.H.; Lee, S.C.; Lee, Y.-J.; Choi, Y.J.; Park, W.-Y.; Shin, H.S.; Kim, J.H. Comprehensive analysis of microRNA-mRNA co-expression in circadian rhythm. Exp. Mol. Med. 2009, 41, 638. [Google Scholar] [CrossRef] [PubMed]
- Vollmers, C.; Schmitz, R.J.; Nathanson, J.; Yeo, G.; Ecker, J.R.; Panda, S. Circadian Oscillations of Protein-Coding and Regulatory RNAs in a Highly Dynamic Mammalian Liver Epigenome. Cell Metab. 2012, 16, 833–845. [Google Scholar] [CrossRef]
- Gatfield, D.; Le Martelot, G.; Vejnar, C.E.; Gerlach, D.; Schaad, O.; Fleury-Olela, F.; Ruskeepää, A.-L.; Oresic, M.; Esau, C.C.; Zdobnov, E.M.; et al. Integration of microRNA miR-122 in hepatic circadian gene expression. Genes Dev. 2009, 23, 1313–1326. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Tang, D.; Wang, W.; Yang, Y.; Wu, X.; Wang, L.; Wang, D. circLMTK2 acts as a sponge of miR-150-5p and promotes proliferation and metastasis in gastric cancer. Mol. Cancer 2019, 18, 162. [Google Scholar] [CrossRef]
- Pidíková, P.; Chovancová, B.; Mravec, B.; Herichová, I. The 24-h pattern of dgcr8, drosha, and dicer expression in the rat suprachiasmatic nuclei and peripheral tissues and its modulation by angiotensin II. Gen. Physiol. Biophys. 2022, 41, 417–430. [Google Scholar] [CrossRef]
- Herichová, I.; Tesáková, B.; Kršková, L.; Olexová, L. Food reward induction of rhythmic clock gene expression in the prefrontal cortex of rats is accompanied by changes in miR-34a-5p expression. Eur. J. Neurosci. 2021, 54, 7476–7492. [Google Scholar] [CrossRef]
- Chacolla-Huaringa, R.; Moreno-Cuevas, J.; Trevino, V.; Scott, S.-P. Entrainment of Breast Cell Lines Results in Rhythmic Fluctuations of MicroRNAs. Int. J. Mol. Sci. 2017, 18, 1499. [Google Scholar] [CrossRef]
- Figueredo, D.D.S.; Barbosa, M.R.; Gitaí, D.L.G.; de Andrade, T.G. Predicted MicroRNAs for Mammalian Circadian Rhythms. J. Biol. Rhythms 2013, 28, 107–116. [Google Scholar] [CrossRef]
- de Siqueira Figueredo, D.; Gitaí, D.L.G.; de Andrade, T.G. Daily variations in the expression of miR-16 and miR-181a in human leukocytes. Blood Cells Mol. Dis. 2015, 54, 364–368. [Google Scholar] [CrossRef] [PubMed]
- Heegaard, N.H.H.; Carlsen, A.L.; Lilje, B.; Ng, K.L.; Rønne, M.E.; Jørgensen, H.L.; Sennels, H.; Fahrenkrug, J. Diurnal Variations of Human Circulating Cell-Free Micro-RNA. PLoS ONE 2016, 11, e0160577. [Google Scholar] [CrossRef] [PubMed]
- Belcheva, A. MicroRNAs at the epicenter of intestinal homeostasis. BioEssays 2017, 39, 1600200. [Google Scholar] [CrossRef] [PubMed]
- McKenna, L.B.; Schug, J.; Vourekas, A.; McKenna, J.B.; Bramswig, N.C.; Friedman, J.R.; Kaestner, K.H. MicroRNAs Control Intestinal Epithelial Differentiation, Architecture, and Barrier Function. Gastroenterology 2010, 139, 1654–1664.e1. [Google Scholar] [CrossRef]
- Ye, D.; Guo, S.; Al–Sadi, R.; Ma, T.Y. MicroRNA Regulation of Intestinal Epithelial Tight Junction Permeability. Gastroenterology 2011, 141, 1323–1333. [Google Scholar] [CrossRef]
- Johnston, D.G.W.; Williams, M.A.; Thaiss, C.A.; Cabrera-Rubio, R.; Raverdeau, M.; McEntee, C.; Cotter, P.D.; Elinav, E.; O’Neill, L.A.J.; Corr, S.C. Loss of microRNA-21 influences the gut microbiota, causing reduced susceptibility in a murine model of colitis. J. Crohn’s Colitis 2018, 12, 835–848. [Google Scholar] [CrossRef]
- Bovari-Biri, J.; Garai, K.; Banfai, K.; Csongei, V.; Pongracz, J.E. miRNAs as Predictors of Barrier Integrity. Biosensors 2023, 13, 422. [Google Scholar] [CrossRef]
- Bi, K.; Zhang, X.; Chen, W.; Diao, H. MicroRNAs Regulate Intestinal Immunity and Gut Microbiota for Gastrointestinal Health: A Comprehensive Review. Genes 2020, 11, 1075. [Google Scholar] [CrossRef]
- Runtsch, M.C.; Round, J.L.; O’Connell, R.M. MicroRNAs and the regulation of intestinal homeostasis. Front. Genet. 2014, 5, 347. [Google Scholar] [CrossRef] [PubMed]
- Chivukula, R.R.; Shi, G.; Acharya, A.; Mills, E.W.; Zeitels, L.R.; Anandam, J.L.; Abdelnaby, A.A.; Balch, G.C.; Mansour, J.C.; Yopp, A.C.; et al. An Essential Mesenchymal Function for miR-143/145 in Intestinal Epithelial Regeneration. Cell 2014, 157, 1104–1116. [Google Scholar] [CrossRef] [PubMed]
- Peck, B.C.E.; Sincavage, J.; Feinstein, S.; Mah, A.T.; Simmons, J.G.; Lund, P.K.; Sethupathy, P. miR-30 Family Controls Proliferation and Differentiation of Intestinal Epithelial Cell Models by Directing a Broad Gene Expression Program That Includes SOX9 and the Ubiquitin Ligase Pathway. J. Biol. Chem. 2016, 291, 15975–15984. [Google Scholar] [CrossRef]
- Zhai, Z.; Wu, F.; Dong, F.; Chuang, A.Y.; Messer, J.S.; Boone, D.L.; Kwon, J.H. Human autophagy gene ATG16L1 is post-transcriptionally regulated by MIR142-3p. Autophagy 2014, 10, 468–479. [Google Scholar] [CrossRef] [PubMed]
- Liang, L.; He, X. Macro-management of microRNAs in cell cycle progression of tumor cells and its implications in anti-cancer therapy. Acta Pharmacol. Sin. 2011, 32, 1311–1320. [Google Scholar] [CrossRef]
- Szczepanek, J.; Skorupa, M.; Tretyn, A. MicroRNA as a Potential Therapeutic Molecule in Cancer. Cells 2022, 11, 1008. [Google Scholar] [CrossRef]
- Wu, Y.; Song, Y.; Xiong, Y.; Wang, X.; Xu, K.; Han, B.; Bai, Y.; Li, L.; Zhang, Y.; Zhou, L. MicroRNA-21 (Mir-21) Promotes Cell Growth and Invasion by Repressing Tumor Suppressor PTEN in Colorectal Cancer. Cell. Physiol. Biochem. 2017, 43, 945–958. [Google Scholar] [CrossRef]
- Asangani, I.A.; Rasheed, S.A.K.; Nikolova, D.A.; Leupold, J.H.; Colburn, N.H.; Post, S.; Allgayer, H. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 2008, 27, 2128–2136. [Google Scholar] [CrossRef]
- Wei, X.; Xiong, X.; Chen, Z.; Chen, B.; Zhang, C.; Zhang, W. MicroRNA155 in non-small cell lung cancer: A potential therapeutic target. Front. Oncol. 2025, 15, 1517995. [Google Scholar] [CrossRef]
- Seto, A.G.; Beatty, X.; Lynch, J.M.; Hermreck, M.; Tetzlaff, M.; Duvic, M.; Jackson, A.L. Cobomarsen, an oligonucleotide inhibitor of miR-155, co-ordinately regulates multiple survival pathways to reduce cellular proliferation and survival in cutaneous T-cell lymphoma. Br. J. Haematol. 2018, 183, 428–444. [Google Scholar] [CrossRef] [PubMed]
- Hong, L.; Lai, M.; Chen, M.; Xie, C.; Liao, R.; Kang, Y.J.; Xiao, C.; Hu, W.-Y.; Han, J.; Sun, P. The miR-17-92 Cluster of MicroRNAs Confers Tumorigenicity by Inhibiting Oncogene-Induced Senescence. Cancer Res. 2010, 70, 8547–8557. [Google Scholar] [CrossRef]
- Fang, L.-L.; Wang, X.-H.; Sun, B.-F.; Zhang, X.-D.; Zhu, X.-H.; Yu, Z.-J.; Luo, H. Expression, regulation and mechanism of action of the miR-17-92 cluster in tumor cells (Review). Int. J. Mol. Med. 2017, 40, 1624–1630. [Google Scholar] [CrossRef]
- Luo, H.; Zou, J.; Dong, Z.; Zeng, Q.; Wu, D.; Liu, L. Up-regulated miR-17 promotes cell proliferation, tumour growth and cell cycle progression by targeting the RND3 tumour suppressor gene in colorectal carcinoma. Biochem. J. 2012, 442, 311–321. [Google Scholar] [CrossRef]
- Zhao, W.; Gupta, A.; Krawczyk, J.; Gupta, S. The miR-17-92 cluster: Yin and Yang in human cancers. Cancer Treat. Res. Commun. 2022, 33, 100647. [Google Scholar] [CrossRef]
- Johnson, S.M.; Grosshans, H.; Shingara, J.; Byrom, M.; Jarvis, R.; Cheng, A.; Labourier, E.; Reinert, K.L.; Brown, D.; Slack, F.J. RAS Is Regulated by the let-7 MicroRNA Family. Cell 2005, 120, 635–647. [Google Scholar] [CrossRef] [PubMed]
- Wong, T.S.; Man, O.Y.; Tsang, C.M.; Tsao, S.W.; Tsang, R.K.Y.; Chan, J.Y.W.; Ho, W.K.; Wei, W.I.; To, V.S.H. MicroRNA let-7 suppresses nasopharyngeal carcinoma cells proliferation through downregulating c-Myc expression. J. Cancer Res. Clin. Oncol. 2011, 137, 415–422. [Google Scholar] [CrossRef]
- Lee, Y.S.; Dutta, A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 2007, 21, 1025–1030. [Google Scholar] [CrossRef]
- Wang, X.; Cao, L.; Wang, Y.; Wang, X.; Liu, N.; You, Y. Regulation of let-7 and its target oncogenes (Review). Oncol. Lett. 2012, 3, 955–960. [Google Scholar] [CrossRef] [PubMed]
- Christoffersen, N.R.; Shalgi, R.; Frankel, L.B.; Leucci, E.; Lees, M.; Klausen, M.; Pilpel, Y.; Nielsen, F.C.; Oren, M.; Lund, A.H. p53-independent upregulation of miR-34a during oncogene-induced senescence represses MYC. Cell Death Differ. 2010, 17, 236–245. [Google Scholar] [CrossRef] [PubMed]
- Chakraborty, S.; Mazumdar, M.; Mukherjee, S.; Bhattacharjee, P.; Adhikary, A.; Manna, A.; Chakraborty, S.; Khan, P.; Sen, A.; Das, T. Restoration of p53/miR-34a regulatory axis decreases survival advantage and ensures Bax-dependent apoptosis of non-small cell lung carcinoma cells. FEBS Lett. 2014, 588, 549–559. [Google Scholar] [CrossRef]
- Feng, J.; Yang, Y.; Zhang, P.; Wang, F.; Ma, Y.; Qin, H.; Wang, Y. miR-150 functions as a tumour suppressor in human colorectal cancer by targeting c-Myb. J. Cell. Mol. Med. 2014, 18, 2125–2134. [Google Scholar] [CrossRef]
- Zhang, Z.-C.; Wang, G.-P.; Yin, L.-M.; Li, M.; Wu, L.-L. Increasing miR-150 and lowering HMGA2 inhibit proliferation and cycle progression of colon cancer in SW480 cells. Eur. Rev. Med. Pharmacol. Sci. 2018, 22, 6793–6800. [Google Scholar] [CrossRef]
- Bian, Z.; Li, L.; Cui, J.; Zhang, H.; Liu, Y.; Zhang, C.; Zen, K. Role of miR-150-targeting c-Myb in colonic epithelial disruption during dextran sulphate sodium-induced murine experimental colitis and human ulcerative colitis. J. Pathol. 2011, 225, 544–553. [Google Scholar] [CrossRef]
- He, Z.; Dang, J.; Song, A.; Cui, X.; Ma, Z.; Zhang, Y. The involvement of miR-150/β-catenin axis in colorectal cancer progression. Biomed. Pharmacother. 2020, 121, 109495. [Google Scholar] [CrossRef]
- Zareifar, P.; Ahmed, H.M.; Ghaderi, P.; Farahmand, Y.; Rahnama, N.; Esbati, R.; Moradi, A.; Yazdani, O.; Sadeghipour, Y. miR-142-3p/5p role in cancer: From epigenetic regulation to immunomodulation. Cell Biochem. Funct. 2024, 42, e3931. [Google Scholar] [CrossRef]
- Mao, L.; Liu, S.; Hu, L.; Jia, L.; Wang, H.; Guo, M.; Chen, C.; Liu, Y.; Xu, L. miR-30 Family: A Promising Regulator in Development and Disease. BioMed Res. Int. 2018, 2018, 9623412. [Google Scholar] [CrossRef] [PubMed]
- Babaeenezhad, E.; Naghibalhossaini, F.; Rajabibazl, M.; Jangravi, Z.; Hadipour Moradi, F.; Fattahi, M.D.; Hoheisel, J.D.; Sarabi, M.M.; Shahryarhesami, S. The Roles of microRNA miR-185 in Digestive Tract Cancers. Non-Coding RNA 2022, 8, 67. [Google Scholar] [CrossRef] [PubMed]
- Sameti, P.; Amini, M.; Oroojalian, F.; Baghay Esfandyari, Y.; Tohidast, M.; Rahmani, S.A.; Azarbarzin, S.; Mokhtarzadeh, A.; Baradaran, B. MicroRNA-425: A Pivotal Regulator Participating in Tumorigenesis of Human Cancers. Mol. Biotechnol. 2024, 66, 1537–1551. [Google Scholar] [CrossRef]
- Xu, S.; Li, W.; Wu, J.; Lu, Y.; Xie, M.; Li, Y.; Zou, J.; Zeng, T.; Ling, H. The Role of miR-129-5p in Cancer: A Novel Therapeutic Target. Curr. Mol. Pharmacol. 2022, 15, 647–657. [Google Scholar] [CrossRef]
- Mo, W.-Y.; Cao, S.-Q. MiR-29a-3p: A potential biomarker and therapeutic target in colorectal cancer. Clin. Transl. Oncol. 2022, 25, 563–577. [Google Scholar] [CrossRef]
- Siegel, R.L.; Wagle, N.S.; Cercek, A.; Smith, R.A.; Jemal, A. Colorectal cancer statistics, 2023. CA Cancer J. Clin. 2023, 73, 233–254. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.; Yan, Q.; Chen, Z.; Wei, X.; Li, L.; Tang, D.; Tan, J.; Xu, C.; Yu, C.; Lai, Y.; et al. Overview of research progress and application of experimental models of colorectal cancer. Front. Pharmacol. 2023, 14, 1193213. [Google Scholar] [CrossRef]
- Murphy, N.; Moreno, V.; Hughes, D.J.; Vodicka, L.; Vodicka, P.; Aglago, E.K.; Gunter, M.J.; Jenab, M. Lifestyle and dietary environmental factors in colorectal cancer susceptibility. Mol. Asp. Med. 2019, 69, 2–9. [Google Scholar] [CrossRef] [PubMed]
- Xi, Y.; Xu, P. Global colorectal cancer burden in 2020 and projections to 2040. Transl. Oncol. 2021, 14, 101174. [Google Scholar] [CrossRef]
- Hasakova, K.; Vician, M.; Reis, R.; Zeman, M.; Herichova, I. Sex-dependent correlation between survival and expression of genes related to the circadian oscillator in patients with colorectal cancer. Chronobiol. Int. 2018, 35, 1423–1434. [Google Scholar] [CrossRef]
- Mazzoccoli, G.; Colangelo, T.; Panza, A.; Rubino, R.; De Cata, A.; Tiberio, C.; Valvano, M.R.; Pazienza, V.; Merla, G.; Augello, B.; et al. Deregulated expression of cryptochrome genes in human colorectal cancer. Mol. Cancer 2016, 15, 6. [Google Scholar] [CrossRef] [PubMed]
- Aroca-Siendones, M.I.; Moreno-SanJuan, S.; Puentes-Pardo, J.D.; Verbeni, M.; Arnedo, J.; Escudero-Feliu, J.; García-Costela, M.; García-Robles, A.; Carazo, Á.; León, J. Core Circadian Clock Proteins as Biomarkers of Progression in Colorectal Cancer. Biomedicines 2021, 9, 967. [Google Scholar] [CrossRef]
- Razi Soofiyani, S.; Ahangari, H.; Soleimanian, A.; Babaei, G.; Ghasemnejad, T.; Safavi, S.E.; Eyvazi, S.; Tarhriz, V. The role of circadian genes in the pathogenesis of colorectal cancer. Gene 2021, 804, 145894. [Google Scholar] [CrossRef]
- Chun, S.K.; Fortin, B.M.; Fellows, R.C.; Habowski, A.N.; Verlande, A.; Song, W.A.; Mahieu, A.L.; Lefebvre, A.E.Y.T.; Sterrenberg, J.N.; Velez, L.M.; et al. Disruption of the circadian clock drives Apc loss of heterozygosity to accelerate colorectal cancer. Sci. Adv. 2022, 8, eabo2389. [Google Scholar] [CrossRef] [PubMed]
- Fortin, B.M.; Pfeiffer, S.M.; Insua-Rodríguez, J.; Alshetaiwi, H.; Moshensky, A.; Song, W.A.; Mahieu, A.L.; Chun, S.K.; Lewis, A.N.; Hsu, A.; et al. Circadian Control of Tumor Immunosuppression Impacts Efficacy of Immune Checkpoint Blockade. Nat. Immunol. 2024, 25, 1257–1269. [Google Scholar] [CrossRef] [PubMed]
- Soták, M.; Sumová, A.; Pácha, J. Cross-talk between the circadian clock and the cell cycle in cancer. Ann. Med. 2014, 46, 221–232. [Google Scholar] [CrossRef]
- Zhou, Q.; Wang, R.; Su, Y.; Wang, B.; Zhang, Y.; Qin, X. The molecular circadian rhythms regulating the cell cycle. J. Cell. Biochem. 2024, 125, e30539. [Google Scholar] [CrossRef] [PubMed]
- Rao, X.; Lin, L. Circadian clock as a possible control point in colorectal cancer progression (Review). Int. J. Oncol. 2022, 61, 149. [Google Scholar] [CrossRef]
- Li, J.; Huang, L.; Zhao, H.; Yan, Y.; Lu, J. The Role of Interleukins in Colorectal Cancer. Int. J. Biol. Sci. 2020, 16, 2323–2339. [Google Scholar] [CrossRef]
- Fu, L.; Pelicano, H.; Liu, J.; Huang, P.; Lee, C.C. The Circadian Gene Period2 Plays an Important Role in Tumor Suppression and DNA Damage Response In Vivo. Cell 2002, 111, 41–50. [Google Scholar] [CrossRef]
- Griniatsos, J.; Michail, O.P.; Theocharis, S.; Arvelakis, A.; Papaconstantinou, I.; Felekouras, E.; Pikoulis, E.; Karavokyros, I.; Bakoyiannis, C.; Marinos, G.; et al. Circadian variation in expression of G 1 phase cyclins D 1 and E and cyclin-dependent kinase inhibitors p16 and p21 in human bowel mucosa. World J. Gastroenterol. 2006, 12, 2109. [Google Scholar] [CrossRef]
- Gaucher, J.; Montellier, E.; Sassone-Corsi, P. Molecular Cogs: Interplay between Circadian Clock and Cell Cycle. Trends Cell Biol. 2018, 28, 368–379. [Google Scholar] [CrossRef]
- Li, X.; Chen, W.; Jin, Y.; Xue, R.; Su, J.; Mu, Z.; Li, J.; Jiang, S. miR-142-5p enhances cisplatin-induced apoptosis in ovarian cancer cells by targeting multiple anti-apoptotic genes. Biochem. Pharmacol. 2019, 161, 98–112. [Google Scholar] [CrossRef]
- Schober, A.; Blay, R.M.; Saboor Maleki, S.; Zahedi, F.; Winklmaier, A.E.; Kakar, M.Y.; Baatsch, I.M.; Zhu, M.; Geißler, C.; Fusco, A.E.; et al. MicroRNA-21 Controls Circadian Regulation of Apoptosis in Atherosclerotic Lesions. Circulation 2021, 144, 1059–1073. [Google Scholar] [CrossRef] [PubMed]
- Bartman, C.M.; Oyama, Y.; Brodsky, K.; Khailova, L.; Walker, L.; Koeppen, M.; Eckle, T. Intense light-elicited upregulation of miR-21 facilitates glycolysis and cardioprotection through Per2-dependent mechanisms. PLoS ONE 2017, 12, e0176243. [Google Scholar] [CrossRef]
- Kochan, D.Z.; Ilnytskyy, Y.; Golubov, A.; Deibel, S.H.; McDonald, R.J.; Kovalchuk, O. Circadian disruption-induced microRNAome deregulation in rat mammary gland tissues. Oncoscience 2015, 2, 428–442. [Google Scholar] [CrossRef]
- Herichová, I. miRNA-mediated regulation of clock gene expression in men and women with colorectal cancer and possible consequences for disease management. Biomed. J. 2025, 48, 100784. [Google Scholar] [CrossRef]
- Kumar, M.; Lu, Z.; Takwi, A.A.L.; Chen, W.; Callander, N.S.; Ramos, K.S.; Young, K.H.; Li, Y. Negative regulation of the tumor suppressor p53 gene by microRNAs. Oncogene 2011, 30, 843–853. [Google Scholar] [CrossRef]
- Rac, M. Synthesis and Regulation of miRNA, Its Role in Oncogenesis, and Its Association with Colorectal Cancer Progression, Diagnosis, and Prognosis. Diagnostics 2024, 14, 1450. [Google Scholar] [CrossRef]
- Cui, S.; Yu, S.; Huang, H.-Y.; Lin, Y.; Huang, Y.; Zhang, B.; Xiao, J.; Zuo, H.; Wang, J.; Li, Z.; et al. miRTarBase 2025: Updates to the collection of experimentally validated microRNA–target interactions. Nucleic Acids Res. 2025, 53, D147–D156. [Google Scholar] [CrossRef]
- Mi, H.; Ebert, D.; Muruganujan, A.; Mills, C.; Albou, L.-P.; Mushayamaha, T.; Thomas, P.D. PANTHER version 16: A revised family classification, tree-based classification tool, enhancer regions and extensive API. Nucleic Acids Res. 2021, 49, D394–D403. [Google Scholar] [CrossRef] [PubMed]
- Herichová, I.; Šoltésová, D.; Szántóová, K.; Mravec, B.; Neupauerová, D.; Veselá, A.; Zeman, M. Effect of angiotensin II on rhythmic per2 expression in the suprachiasmatic nucleus and heart and daily rhythm of activity in Wistar rats. Regul. Pept. 2013, 186, 49–56. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.-J.; Servant, N.; Toedling, J.; Sarazin, A.; Marchais, A.; Duvernois-Berthet, E.; Cognat, V.; Colot, V.; Voinnet, O.; Heard, E.; et al. ncPRO-seq: A tool for annotation and profiling of ncRNAs in sRNA-seq data. Bioinformatics 2012, 28, 3147–3149. [Google Scholar] [CrossRef]
- Langmead, B.; Trapnell, C.; Pop, M.; Salzberg, S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10, R25. [Google Scholar] [CrossRef]
- Klemfuss, H.; Clopton, P.L. Seeking tau: A comparison of six methods. J. Interdisiplinary Cycle Res. 1993, 24, 1–16. [Google Scholar] [CrossRef]
- Sun, L.; Ma, J.; Turck, C.W.; Xu, P.; Wang, G.-Z. Genome-wide circadian regulation: A unique system for computational biology. Comput. Struct. Biotechnol. J. 2020, 18, 1914–1924. [Google Scholar] [CrossRef]
- Tognini, P.; Murakami, M.; Liu, Y.; Eckel-Mahan, K.L.; Newman, J.C.; Verdin, E.; Baldi, P.; Sassone-Corsi, P. Distinct Circadian Signatures in Liver and Gut Clocks Revealed by Ketogenic Diet. Cell Metab. 2017, 26, 523–538.e5. [Google Scholar] [CrossRef] [PubMed]
- Guo, W.-T.; Wang, Y. Dgcr8 knockout approaches to understand microRNA functions in vitro and in vivo. Cell. Mol. Life Sci. 2019, 76, 1697–1711. [Google Scholar] [CrossRef]
- Gulyaeva, L.F.; Kushlinskiy, N.E. Regulatory mechanisms of microRNA expression. J. Transl. Med. 2016, 14, 143. [Google Scholar] [CrossRef] [PubMed]
- Hill, M.; Tran, N. miRNA interplay: Mechanisms and consequences in cancer. Dis. Model. Mech. 2021, 14, dmm047662. [Google Scholar] [CrossRef]
- Liu, F.; Di Wang, X. miR-150-5p represses TP53 tumor suppressor gene to promote proliferation of colon adenocarcinoma. Sci. Rep. 2019, 9, 6740. [Google Scholar] [CrossRef]
- Foubert, F.; Matysiak-Budnik, T.; Touchefeu, Y. Options for metastatic colorectal cancer beyond the second line of treatment. Dig. Liver Dis. 2014, 46, 105–112. [Google Scholar] [CrossRef]
- Therkildsen, C.; Bergmann, T.K.; Henrichsen-Schnack, T.; Ladelund, S.; Nilbert, M. The predictive value of KRAS, NRAS, BRAF, PIK3CA and PTEN for anti-EGFR treatment in metastatic colorectal cancer: A systematic review and meta-analysis. Acta Oncol. 2014, 53, 852–864. [Google Scholar] [CrossRef]
- Xu, Y.; Pasche, B. TGF-β signaling alterations and susceptibility to colorectal cancer. Hum. Mol. Genet. 2007, 16, R14–R20. [Google Scholar] [CrossRef]
- Cortés-Ballinas, L.; López-Pérez, T.; Rocha-Zavaleta, L. STAT3 and the STAT3-regulated inhibitor of apoptosis protein survivin as potential therapeutic targets in colorectal cancer (Review). Biomed. Rep. 2024, 21, 175. [Google Scholar] [CrossRef] [PubMed]
- Bocchi, M.; de Sousa Pereira, N.; de Oliveira, K.B.; Amarante, M.K. Involvement of CXCL12/CXCR4 axis in colorectal cancer: A mini-review. Mol. Biol. Rep. 2023, 50, 6233–6239. [Google Scholar] [CrossRef] [PubMed]
- Kadomoto, S.; Izumi, K.; Mizokami, A. The CCL20-CCR6 Axis in Cancer Progression. Int. J. Mol. Sci. 2020, 21, 5186. [Google Scholar] [CrossRef]
- Yang, X.; Li, P.; Tao, J.; Qin, C.; Cao, Q.; Gu, J.; Deng, X.; Wang, J.; Liu, X.; Wang, Z.; et al. Association between NFKB1 −94ins/del ATTG Promoter Polymorphism and Cancer Susceptibility: An Updated Meta-Analysis. Int. J. Genomics 2014, 2014, 612972. [Google Scholar] [CrossRef]
- Vassilev, A.; Tibbles, H.; DuMez, D.; Venkatachalam, T.; Uckun, F. Targeting JAK3 and BTK Tyrosine Kinases with Rationally-Designed Inhibitors. Curr. Drug Targets 2006, 7, 327–343. [Google Scholar] [CrossRef]
- He, B.; Liang, J.; Qin, Q.; Zhang, Y.; Shi, S.; Cao, J.; Zhang, Z.; Bie, Q.; Zhao, R.; Wei, L.; et al. IL-13/IL-13RA2 signaling promotes colorectal cancer stem cell tumorigenesis by inducing ubiquitinated degradation of p53. Genes Dis. 2024, 11, 495–508. [Google Scholar] [CrossRef]
- Zhang, J.; Zhang, H.; Liu, J.; Tu, X.; Zang, Y.; Zhu, J.; Chen, J.; Dong, L.; Zhang, J. MiR-30 inhibits TGF-β1-induced epithelial-to-mesenchymal transition in hepatocyte by targeting Snail1. Biochem. Biophys. Res. Commun. 2012, 417, 1100–1105. [Google Scholar] [CrossRef]
- Kumarswamy, R.; Mudduluru, G.; Ceppi, P.; Muppala, S.; Kozlowski, M.; Niklinski, J.; Papotti, M.; Allgayer, H. MicroRNA-30a inhibits epithelial-to-mesenchymal transition by targeting Snai1 and is downregulated in non-small cell lung cancer. Int. J. Cancer 2012, 130, 2044–2053. [Google Scholar] [CrossRef] [PubMed]
- Zhao, J.-J.; Lin, J.; Zhu, D.; Wang, X.; Brooks, D.; Chen, M.; Chu, Z.; Takada, K.; Ciccarelli, B.; Admin, S.; et al. miR-30-5p Functions as a Tumor Suppressor and Novel Therapeutic Tool by Targeting the Oncogenic Wnt/β-Catenin/BCL9 Pathway. Cancer Res. 2014, 74, 1801–1813. [Google Scholar] [CrossRef]
- Liu, Y.; Bodmer, W.F. Analysis of P53 mutations and their expression in 56 colorectal cancer cell lines. Proc. Natl. Acad. Sci. USA 2006, 103, 976–981. [Google Scholar] [CrossRef] [PubMed]
- Robles, A.I.; Jen, J.; Harris, C.C. Clinical Outcomes of TP53 Mutations in Cancers. Cold Spring Harb. Perspect. Med. 2016, 6, a026294. [Google Scholar] [CrossRef]
- Chen, X.; Xu, X.; Pan, B.; Zeng, K.; Xu, M.; Liu, X.; He, B.; Pan, Y.; Sun, H.; Wang, S. Correction for: miR-150-5p suppresses tumor progression by targeting VEGFA in colorectal cancer. Aging 2021, 13, 13372–13373. [Google Scholar] [CrossRef]
- Li, C.; Du, X.; Xia, S.; Chen, L. MicroRNA-150 inhibits the proliferation and metastasis potential of colorectal cancer cells by targeting iASPP. Oncol. Rep. 2018, 40, 252–260. [Google Scholar] [CrossRef]
- Kim, T.H.; Jeong, J.-Y.; Park, J.-Y.; Kim, S.-W.; Heo, J.H.; Kang, H.; Kim, G.; An, H.J. miR-150 enhances apoptotic and anti-tumor effects of paclitaxel in paclitaxel-resistant ovarian cancer cells by targeting Notch3. Oncotarget 2017, 8, 72788–72800. [Google Scholar] [CrossRef]
- Meng, X.; Sun, W.; Yu, J.; Zhou, Y.; Gu, Y.; Han, J.; Zhou, L.; Jiang, X.; Wang, C. LINC00460-miR-149-5p/miR-150-5p-Mutant p53 Feedback Loop Promotes Oxaliplatin Resistance in Colorectal Cancer. Mol. Ther. Nucleic Acids 2020, 22, 1004–1015. [Google Scholar] [CrossRef]
- Biroccio, A.; Benassi, B.; D’Agnano, I.; D’Angelo, C.; Buglioni, S.; Mottolese, M.; Ricciotti, A.; Citro, G.; Cosimelli, M.; Ramsay, R.G.; et al. c-Myb and Bcl-x Overexpression Predicts Poor Prognosis in Colorectal Cancer. Am. J. Pathol. 2001, 158, 1289–1299. [Google Scholar] [CrossRef]
- Xiao, C.; Calado, D.P.; Galler, G.; Thai, T.-H.; Patterson, H.C.; Wang, J.; Rajewsky, N.; Bender, T.P.; Rajewsky, K. MiR-150 Controls B Cell Differentiation by Targeting the Transcription Factor c-Myb. Cell 2007, 131, 146–159. [Google Scholar] [CrossRef]
- Pizarro, A.; Hayer, K.; Lahens, N.F.; Hogenesch, J.B. CircaDB: A database of mammalian circadian gene expression profiles. Nucleic Acids Res. 2013, 41, D1009–D1013. [Google Scholar] [CrossRef] [PubMed]
- Hughes, M.E.; DiTacchio, L.; Hayes, K.R.; Vollmers, C.; Pulivarthy, S.; Baggs, J.E.; Panda, S.; Hogenesch, J.B. Harmonics of Circadian Gene Transcription in Mammals. PLoS Genet. 2009, 5, e1000442. [Google Scholar] [CrossRef] [PubMed]
- Mure, L.S.; Le, H.D.; Benegiamo, G.; Chang, M.W.; Rios, L.; Jillani, N.; Ngotho, M.; Kariuki, T.; Dkhissi-Benyahya, O.; Cooper, H.M.; et al. Diurnal transcriptome atlas of a primate across major neural and peripheral tissues. Science 2018, 359, 243–262. [Google Scholar] [CrossRef] [PubMed]
- Frenzel, A.; Grespi, F.; Chmelewskij, W.; Villunger, A. Bcl2 family proteins in carcinogenesis and the treatment of cancer. Apoptosis 2009, 14, 584–596. [Google Scholar] [CrossRef]
- Sala, A. B-MYB, a transcription factor implicated in regulating cell cycle, apoptosis and cancer. Eur. J. Cancer 2005, 41, 2479–2484. [Google Scholar] [CrossRef] [PubMed]
- Drabsch, Y.; Ramsay, R.G.; Gonda, T.J. MYBsuppresses differentiation and apoptosis of human breast cancer cells. Breast Cancer Res. 2010, 12, R55. [Google Scholar] [CrossRef]
- Jia, M.; Su, B.; Mo, L.; Qiu, W.; Ying, J.; Lin, P.; Yang, B.; Li, D.; Wang, D.; Xu, L.; et al. Circadian clock protein CRY1 prevents paclitaxel-induced senescence of bladder cancer cells by promoting p53 degradation. Oncol. Rep. 2020, 45, 1033–1043. [Google Scholar] [CrossRef] [PubMed]
- Han, G.H.; Kim, J.; Yun, H.; Cho, H.; Chung, J.-Y.; Kim, J.-H.; Hewitt, S.M. CRY1 Regulates Chemoresistance in Association With NANOG by Inhibiting Apoptosis via STAT3 Pathway in Patients With Cervical Cancer. Cancer Genom. Proteom. 2021, 18, 699–713. [Google Scholar] [CrossRef]
- Slattery, M.L.; Wolff, E.; Hoffman, M.D.; Pellatt, D.F.; Milash, B.; Wolff, R.K. MicroRNAs and colon and rectal cancer: Differential expression by tumor location and subtype. Genes Chromosom. Cancer 2011, 50, 196–206. [Google Scholar] [CrossRef] [PubMed]
- Ma, Y.; Zhang, P.; Wang, F.; Zhang, H.; Yang, J.; Peng, J.; Liu, W.; Qin, H. miR-150 as a potential biomarker associated with prognosis and therapeutic outcome in colorectal cancer. Gut 2012, 61, 1447–1453. [Google Scholar] [CrossRef]
- Aherne, S.T.; Madden, S.F.; Hughes, D.J.; Pardini, B.; Naccarati, A.; Levy, M.; Vodicka, P.; Neary, P.; Dowling, P.; Clynes, M. Circulating miRNAs miR-34a and miR-150 associated with colorectal cancer progression. BMC Cancer 2015, 15, 329. [Google Scholar] [CrossRef]
- Zhang, Y.; Liu, W.-S.; Zhang, X.-Y.; Tong, H.-X.; Yang, H.; Liu, W.-F.; Fan, J.; Zhou, J.; Hu, J. Low expression of exosomal miR-150 predicts poor prognosis in colorectal cancer patients after surgical resections. Carcinogenesis 2022, 43, 930–940. [Google Scholar] [CrossRef]
- Watanabe, A.; Tagawa, H.; Yamashita, J.; Teshima, K.; Nara, M.; Iwamoto, K.; Kume, M.; Kameoka, Y.; Takahashi, N.; Nakagawa, T.; et al. The role of microRNA-150 as a tumor suppressor in malignant lymphoma. Leukemia 2011, 25, 1324–1334. [Google Scholar] [CrossRef]
- Yokobori, T.; Suzuki, S.; Tanaka, N.; Inose, T.; Sohda, M.; Sano, A.; Sakai, M.; Nakajima, M.; Miyazaki, T.; Kato, H.; et al. MiR-150 is associated with poor prognosis in esophageal squamous cell carcinoma via targeting the EMT inducer ZEB 1. Cancer Sci. 2013, 104, 48–54. [Google Scholar] [CrossRef] [PubMed]
- Osako, Y.; Seki, N.; Koshizuka, K.; Okato, A.; Idichi, T.; Arai, T.; Omoto, I.; Sasaki, K.; Uchikado, Y.; Kita, Y.; et al. Regulation of SPOCK1 by dual strands of pre-miR-150 inhibit cancer cell migration and invasion in esophageal squamous cell carcinoma. J. Hum. Genet. 2017, 62, 935–944. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.J.; Zhang, Y.X.; Wang, P.Y.; Chi, Y.L.; Zhang, C.; Ma, Y.; Lv, C.J.; Xie, S.Y. Regression of A549 lung cancer tumors by anti-miR-150 vector. Oncol. Rep. 2012, 27, 129–134. [Google Scholar] [CrossRef] [PubMed]
- Dai, F.-Q.; Li, C.-R.; Fan, X.-Q.; Tan, L.; Wang, R.-T.; Jin, H. miR-150-5p Inhibits Non-Small-Cell Lung Cancer Metastasis and Recurrence by Targeting HMGA2 and β-Catenin Signaling. Mol. Ther.-Nucleic Acids 2019, 16, 675–685. [Google Scholar] [CrossRef]
- Zhang, J.; Luo, N.; Luo, Y.; Peng, Z.; Zhang, T.; Li, S. microRNA-150 inhibits human CD133-positive liver cancer stem cells through negative regulation of the transcription factor c-Myb. Int. J. Oncol. 2012, 40, 747–756. [Google Scholar] [CrossRef]
- Han, Y.; Ma, Z. LncRNA highly upregulated in liver cancer regulates imatinib resistance in chronic myeloid leukemia via the miR-150-5p/MCL1 axis. Anticancer Drugs 2021, 32, 427–436. [Google Scholar] [CrossRef]
- Wu, Q.; Jin, H.; Yang, Z.; Luo, G.; Lu, Y.; Li, K.; Ren, G.; Su, T.; Pan, Y.; Feng, B.; et al. MiR-150 promotes gastric cancer proliferation by negatively regulating the pro-apoptotic gene EGR2. Biochem. Biophys. Res. Commun. 2010, 392, 340–345. [Google Scholar] [CrossRef]
- Quan, X.; Chen, D.; Li, M.; Chen, X.; Huang, M. MicroRNA-150-5p and SRC kinase signaling inhibitor 1 involvement in the pathological development of gastric cancer. Exp. Ther. Med. 2019, 18, 2667–2674. [Google Scholar] [CrossRef]
- Huang, S.; Chen, Y.; Wu, W.; Ouyang, N.; Chen, J.; Li, H.; Liu, X.; Su, F.; Lin, L.; Yao, Y. miR-150 Promotes Human Breast Cancer Growth and Malignant Behavior by Targeting the Pro-Apoptotic Purinergic P2X7 Receptor. PLoS ONE 2013, 8, e80707. [Google Scholar] [CrossRef]
- Wang, Y.; Cao, Z.; Wang, L.; Liu, S.; Cai, J. Downregulation of microRNA-142-3p and its tumor suppressor role in gastric cancer. Oncol. Lett. 2018, 15, 8172–8180. [Google Scholar] [CrossRef]
- Sugita, B.M.; Rodriguez, Y.; Fonseca, A.S.; Nunes Souza, E.; Kallakury, B.; Cavalli, I.J.; Ribeiro, E.M.S.F.; Aneja, R.; Cavalli, L.R. MiR-150-5p Overexpression in Triple-Negative Breast Cancer Contributes to the In Vitro Aggressiveness of This Breast Cancer Subtype. Cancers 2022, 14, 2156. [Google Scholar] [CrossRef]
- Arndt, G.M.; Dossey, L.; Cullen, L.M.; Lai, A.; Druker, R.; Eisbacher, M.; Zhang, C.; Tran, N.; Fan, H.; Retzlaff, K.; et al. Characterization of global microRNA expression reveals oncogenic potential of miR-145 in metastatic colorectal cancer. BMC Cancer 2009, 9, 374. [Google Scholar] [CrossRef]
- Balaguer, F.; Moreira, L.; Lozano, J.J.; Link, A.; Ramirez, G.; Shen, Y.; Cuatrecasas, M.; Arnold, M.; Meltzer, S.J.; Syngal, S.; et al. Colorectal Cancers with Microsatellite Instability Display Unique miRNA Profiles. Clin. Cancer Res. 2011, 17, 6239–6249. [Google Scholar] [CrossRef]
- Gaedcke, J.; Grade, M.; Camps, J.; Søkilde, R.; Kaczkowski, B.; Schetter, A.J.; Difilippantonio, M.J.; Harris, C.C.; Ghadimi, B.M.; Møller, S.; et al. The Rectal Cancer microRNAome—microRNA Expression in Rectal Cancer and Matched Normal Mucosa. Clin. Cancer Res. 2012, 18, 4919–4930. [Google Scholar] [CrossRef]
- Nagy, Z.B.; Wichmann, B.; Kalmár, A.; Galamb, O.; Barták, B.K.; Spisák, S.; Tulassay, Z.; Molnár, B. Colorectal adenoma and carcinoma specific miRNA profiles in biopsy and their expression in plasma specimens. Clin. Epigenet. 2017, 9, 22. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Ren, R.; Wan, D.; Wang, Y.; Xue, X.; Jiang, M.; Shen, J.; Han, Y.; Liu, F.; Shi, J.; et al. Hsa_circ_101555 functions as a competing endogenous RNA of miR-597-5p to promote colorectal cancer progression. Oncogene 2019, 38, 6017–6034. [Google Scholar] [CrossRef]
- Yan, L.; Qiu, J.; Yao, J. Downregulation of microRNA-30d promotes cell proliferation and invasion by targeting LRH-1 in colorectal carcinoma. Int. J. Mol. Med. 2017, 39, 1371–1380. [Google Scholar] [CrossRef]
- Zhang, R.; Xu, J.; Zhao, J.; Bai, J. Mir-30d suppresses cell proliferation of colon cancer cells by inhibiting cell autophagy and promoting cell apoptosis. Tumor Biol. 2017, 39, 101042831770398. [Google Scholar] [CrossRef]
- Muhammad, S.; Tang, Q.; Wei, L.; Zhang, Q.; Wang, G.; Muhammad, B.; Kaur, K.; Kamchedalova, T.; Gang, Z.; Jiang, Z.; et al. miRNA-30d serves a critical function in colorectal cancer initiation, progression and invasion via directly targeting the GNA13 gene. Exp. Ther. Med. 2018, 17, 260–272. [Google Scholar] [CrossRef]
- Chen, D.; Guo, W.; Qiu, Z.; Wang, Q.; Li, Y.; Liang, L.; Liu, L.; Huang, S.; Zhao, Y.; He, X. MicroRNA-30d-5p inhibits tumour cell proliferation and motility by directly targeting CCNE2 in non-small cell lung cancer. Cancer Lett. 2015, 362, 208–217. [Google Scholar] [CrossRef]
- Wu, Y.; Zhang, J.; Hou, S.; Cheng, Z.; Yuan, M. Non-small cell lung cancer: miR-30d suppresses tumor invasion and migration by directly targeting NFIB. Biotechnol. Lett. 2017, 39, 1827–1834. [Google Scholar] [CrossRef] [PubMed]
- Gao, L.; He, R.; Wu, H.; Zhang, T.; Liang, H.; Ye, Z.; Li, Z.; Xie, T.; Shi, Q.; Ma, J.; et al. Expression Signature and Role of miR-30d-5p in Non-Small Cell Lung Cancer: A Comprehensive Study Based on in Silico Analysis of Public Databases and in Vitro Experiments. Cell. Physiol. Biochem. 2018, 50, 1964–1987. [Google Scholar] [CrossRef] [PubMed]
- Song, K.; Jiang, Y.; Zhao, Y.; Xie, Y.; Zhou, J.; Yu, W.; Wang, Q. Members of the miR-30 family inhibit the epithelial-to-mesenchymal transition of non-small-cell lung cancer cells by suppressing XB130 expression levels. Oncol. Lett. 2020, 130, 68. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Chen, Z.; Xu, S.; Zhang, Q. LncRNA SOX2-OT/miR-30d-5p/PDK1 Regulates PD-L1 Checkpoint Through the mTOR Signaling Pathway to Promote Non-small Cell Lung Cancer Progression and Immune Escape. Front. Genet. 2021, 12, 674856. [Google Scholar] [CrossRef]
- Kanthaje, S.; Baikunje, N.; Kandal, I.; Ratnacaram, C.K. Repertoires of MicroRNA-30 family as gate-keepers in lung cancer. Front. Biosci. 2021, 13, 141–156. [Google Scholar] [CrossRef]
- Xu, X.; Zong, K.; Wang, X.; Dou, D.; Lv, P.; Zhang, Z.; Li, H. miR-30d suppresses proliferation and invasiveness of pancreatic cancer by targeting the SOX4/PI3K-AKT axis and predicts poor outcome. Cell Death Dis. 2021, 12, 350. [Google Scholar] [CrossRef]
- Hou, Y.; Zhang, Q.; Pang, W.; Hou, L.; Liang, Y.; Han, X.; Luo, X.; Wang, P.; Zhang, X.; Li, L.; et al. YTHDC1-mediated augmentation of miR-30d in repressing pancreatic tumorigenesis via attenuation of RUNX1-induced transcriptional activation of Warburg effect. Cell Death Differ. 2021, 28, 3105–3124. [Google Scholar] [CrossRef]
- Ying, L.; Li, K.; Chen, C.; Wang, Y.; Zhao, Q.; Wang, Y.; Xu, L.; Huang, H.; Song, G.; Li, W.; et al. OIP5-AS1 enhances the malignant characteristics and resistance to chemotherapy of pancreatic cancer cells by targeting miR-30d-5p/MARCH8. Heliyon 2024, 10, e33835. [Google Scholar] [CrossRef]
- Ye, Y.; Mei, J.; Xiang, S.; Li, H.; Ma, Q.; Song, X.; Wang, Z.; Zhang, Y.-C.; Liu, Y.-C.; Jin, Y.; et al. MicroRNA-30a-5p inhibits gallbladder cancer cell proliferation, migration and metastasis by targeting E2F7. Cell Death Dis. 2018, 9, 410. [Google Scholar] [CrossRef]
- He, Y.; Chen, X.; Yu, Y.; Li, J.; Hu, Q.; Xue, C.; Chen, J.; Shen, S.; Luo, Y.; Ren, F.; et al. LDHA is a direct target of miR-30d-5p and contributes to aggressive progression of gallbladder carcinoma. Mol. Carcinog. 2018, 57, 772–783. [Google Scholar] [CrossRef]
- Xuan, H.; Xue, W.; Pan, J.; Sha, J.; Dong, B.; Huang, Y. Downregulation of miR-221, -30d, and -15a contributes to pathogenesis of prostate cancer by targeting Bmi-1. Biochemistry 2015, 80, 276–283. [Google Scholar] [CrossRef]
- Song, Y.; Song, C.; Yang, S. Tumor-Suppressive Function of miR-30d-5p in Prostate Cancer Cell Proliferation and Migration by Targeting NT5E. Cancer Biother. Radiopharm. 2018, 33, 203–211. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, N.; Uemura, H.; Nagahama, K.; Okudela, K. Identification of miR-30d as a novel prognostic maker of prostate cancer. Oncotarget 2012, 3, 1455–1471. [Google Scholar] [CrossRef]
- Han, M.; Wang, Y.; Guo, G.; Li, L.; Dou, D.; Ge, X.; Lv, P.; Wang, F.; Gu, Y. microRNA-30d mediated breast cancer invasion, migration, and EMT by targeting KLF11 and activating STAT3 pathway. J. Cell. Biochem. 2018, 119, 8138–8145. [Google Scholar] [CrossRef]
- Zhang, L.; Ren, S.; Sang, Y.; Hu, Y.; Wang, C.; Wang, X.; Li, Y. miR-30d-5p inhibits proliferation, invasion and migration of breast cancer cells by targeting SERPINE1 and promoting fatty acid β-oxidation. Aging 2024, 16, 5856–5865. [Google Scholar] [CrossRef]
- Xu, F.; Wang, Y.; Ling, Y.; Zhou, C.; Wang, H.; Teschendorff, A.E.; Zhao, Y.; Zhao, H.; He, Y.; Zhang, G.; et al. dbDEMC 3.0: Functional Exploration of Differentially Expressed miRNAs in Cancers of Human and Model Organisms. Genom. Proteom. Bioinform. 2022, 20, 446–454. [Google Scholar] [CrossRef]
- Shen, W.; Zeng, Z.; Zhu, W.; Fu, G. MiR-142-3p functions as a tumor suppressor by targeting CD133, ABCG2, and Lgr5 in colon cancer cells. J. Mol. Med. 2013, 91, 989–1000. [Google Scholar] [CrossRef]
- Zhu, X.; Ma, S.; Yang, D.; Liu, Y.; Wang, Y.; Lin, T.; Li, Y.; Yang, S.; Zhang, W.; Wang, X. miR-142-3p Suppresses Cell Growth by Targeting CDK4 in Colorectal Cancer. Cell. Physiol. Biochem. 2018, 51, 1969–1981. [Google Scholar] [CrossRef] [PubMed]
- Liu, P.; Cao, F.; Sui, J.; Hong, Y.; Liu, Q.; Gao, X.; Gong, H.; Hao, L.; Lou, Z.; Zhang, W. MicroRNA-142-3p Inhibits Tumorigenesis of Colorectal Cancer via Suppressing the Activation of Wnt Signaling by Directly Targeting to β-Catenin. Front. Oncol. 2021, 10, 552944. [Google Scholar] [CrossRef] [PubMed]
- Gao, X.; Xu, W.; Lu, T.; Zhou, J.; Ge, X.; Hua, D. MicroRNA-142-3p Promotes Cellular Invasion of Colorectal Cancer Cells by Activation of RAC1. Technol. Cancer Res. Treat. 2018, 17, 1533033818790508. [Google Scholar] [CrossRef]
- Shang, A.; Gu, C.; Wang, W.; Wang, X.; Sun, J.; Zeng, B.; Chen, C.; Chang, W.; Ping, Y.; Ji, P.; et al. Exosomal circPACRGL promotes progression of colorectal cancer via the miR-142-3p/miR-506-3p-TGF-β1 axis. Mol. Cancer 2020, 19, 117. [Google Scholar] [CrossRef]
- Tsang, F.H.; Au, S.L.; Wei, L.; Fan, D.N.; Lee, J.M.; Wong, C.C.; Ng, I.O.; Wong, C.-M. MicroRNA-142-3p and microRNA-142-5p are downregulated in hepatocellular carcinoma and exhibit synergistic effects on cell motility. Front. Med. 2015, 9, 331–343. [Google Scholar] [CrossRef]
- He, C.; Liu, Z.; Jin, L.; Zhang, F.; Peng, X.; Xiao, Y.; Wang, X.; Lyu, Q.; Cai, X. lncRNA TUG1-Mediated Mir-142-3p Downregulation Contributes to Metastasis and the Epithelial-to-Mesenchymal Transition of Hepatocellular Carcinoma by Targeting ZEB1. Cell. Physiol. Biochem. 2018, 48, 1928–1941. [Google Scholar] [CrossRef]
- Hua, S.; Liu, C.; Liu, L.; Wu, D. miR-142-3p inhibits aerobic glycolysis and cell proliferation in hepatocellular carcinoma via targeting LDHA. Biochem. Biophys. Res. Commun. 2018, 496, 947–954. [Google Scholar] [CrossRef]
- Yu, Q.; Xiang, L.; Chen, Z.; Liu, X.; Ou, H.; Zhou, J.; Yang, D. MALAT1 functions as a competing endogenous RNA to regulate SMAD5 expression by acting as a sponge for miR-142-3p in hepatocellular carcinoma. Cell Biosci. 2019, 9, 39. [Google Scholar] [CrossRef]
- Cui, D.; Ni, C. LncRNA Lnc712 Promotes Tumorigenesis in Hepatocellular Carcinoma by Targeting miR-142-3p/Bach-1 Axis. Cancer Manag. Res. 2020, 12, 11285–11294. [Google Scholar] [CrossRef]
- Feng, T.; Yao, Y.; Luo, L.; Zou, H.; Xiang, G.; Wei, L.; Yang, Q.; Shi, Y.; Huang, X.; Lai, C. ST8SIA6-AS1 contributes to hepatocellular carcinoma progression by targeting miR-142-3p/HMGA1 axis. Sci. Rep. 2023, 13, 650. [Google Scholar] [CrossRef]
- Mahboobnia, K.; Kabir, T.D.; Hou, R.; Liu, P.; Forrest, A.; Beveridge, D.J.; Richardson, K.L.; Stuart, L.M.; Yeoh, G.C.; Leedman, P.J. MicroRNA-142-3p Overcomes Drug Resistance in Hepatocellular Carcinoma by Targeting YES1 and TWF1. Int. J. Mol. Sci. 2025, 26, 4161. [Google Scholar] [CrossRef] [PubMed]
- Gao, J.; Wu, N.; Liu, X.; Xia, Y.; Chen, Y.; Li, S.; Deng, Z. MicroRNA-142-3p inhibits cell proliferation and chemoresistance in ovarian cancer via targeting sirtuin 1. Exp. Ther. Med. 2018, 15, 5205–5214. [Google Scholar] [CrossRef]
- Gao, G.; Guo, X.; Gu, W.; Lu, Y.; Chen, Z. miRNA-142-3p functions as a potential tumor suppressor directly targeting FAM83D in the development of ovarian cancer. Aging 2022, 14, 3387–3399. [Google Scholar] [CrossRef]
- Lu, J.; Ma, Y.; Zhao, Z. MiR-142 suppresses progression of gastric carcinoma via directly targeting LRP8. Clin. Res. Hepatol. Gastroenterol. 2021, 45, 101520. [Google Scholar] [CrossRef]
- Cheng, Z.; Liu, G.; Huang, C.; Zhao, X. Upregulation of circRNA_100395 sponges miR-142-3p to inhibit gastric cancer progression by targeting the PI3K/AKT axis. Oncol. Lett. 2021, 21, 419. [Google Scholar] [CrossRef]
- Peng, L.; Sang, H.; Wei, S.; Li, Y.; Jin, D.; Zhu, X.; Li, X.; Dang, Y.; Zhang, G. circCUL2 regulates gastric cancer malignant transformation and cisplatin resistance by modulating autophagy activation via miR-142-3p/ROCK2. Mol. Cancer 2020, 19, 156. [Google Scholar] [CrossRef]
- Li, Y.; Chen, D.; Jin, L.; Liu, J.; Li, Y.; Su, Z.; Qi, Z.; Shi, M.; Jiang, Z.; Yang, S.; et al. Oncogenic microRNA-142-3p is associated with cellular migration, proliferation and apoptosis in renal cell carcinoma. Oncol. Lett. 2016, 11, 1235–1241. [Google Scholar] [CrossRef]
- Zhang, Y.; Ma, S.; Zhang, J.; Lou, L.; Liu, W.; Gao, C.; Miao, L.; Sun, F.; Chen, W.; Cao, X.; et al. MicroRNA-142-3p promotes renal cell carcinoma progression by targeting RhoBTB3 to regulate HIF-1 signaling and GGT/GSH pathways. Sci. Rep. 2023, 13, 5935. [Google Scholar] [CrossRef]
- Tan, Y.; Chen, Z.; Wang, L.; Wang, M.; Liu, X. MiR-142-3p functions as an oncogene in prostate cancer by targeting FOXO1. J. Cancer 2020, 11, 1614–1624. [Google Scholar] [CrossRef] [PubMed]
- Liu, Z.; Selby, C.P.; Yang, Y.; Lindsey-Boltz, L.A.; Cao, X.; Eynullazada, K.; Sancar, A. Circadian regulation of c-MYC in mice. Proc. Natl. Acad. Sci. USA 2020, 117, 21609–21617. [Google Scholar] [CrossRef] [PubMed]
- Chang, T.; Yu, D.; Lee, Y.; Wentzel, E.A.; Arking, D.E.; West, K.M.; Dang, C.V.; Thomas-Tikhonenko, A.; Mendell, J.T. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat. Genet. 2008, 40, 43–50. [Google Scholar] [CrossRef] [PubMed]
- Robertus, J.; Kluiver, J.; Weggemans, C.; Harms, G.; Reijmers, R.M.; Swart, Y.; Kok, K.; Rosati, S.; Schuuring, E.; Van Imhoff, G.; et al. MiRNA profiling in B non-Hodgkin lymphoma: A MYC -related miRNA profile characterizes Burkitt lymphoma. Br. J. Haematol. 2010, 149, 896–899. [Google Scholar] [CrossRef]
- Tang, X.; Muniappan, L.; Tang, G.; Özcan, S. Identification of glucose-regulated miRNAs from pancreatic β cells reveals a role for miR-30d in insulin transcription. RNA 2009, 15, 287–293. [Google Scholar] [CrossRef]
- Damiola, F.; Le Minh, N.; Preitner, N.; Kornmann, B.; Fleury-Olela, F.; Schibler, U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000, 14, 2950–2961. [Google Scholar] [CrossRef] [PubMed]
- Szántóová, K.; Zeman, M.; Veselá, A.; Herichová, I. Effect of phase delay lighting rotation schedule on daily expression of per2, bmal1, rev-erbα, pparα, and pdk4 genes in the heart and liver of Wistar rats. Mol. Cell. Biochem. 2011, 348, 53–60. [Google Scholar] [CrossRef]
- Pácha, J.; Sumová, A. Circadian regulation of epithelial functions in the intestine. Acta Physiol. 2013, 208, 11–24. [Google Scholar] [CrossRef] [PubMed]
- Štefánik, P.; Morová, M.; Herichová, I. Impact of Long-Lasting Environmental Factors on Regulation Mediated by the miR-34 Family. Biomedicines 2024, 12, 424. [Google Scholar] [CrossRef]
- Zhu, P.; Pei, Y.; Yu, J.; Ding, W.; Yang, Y.; Liu, F.; Liu, L.; Huang, J.; Yuan, S.; Wang, Z.; et al. High-throughput sequencing approach for the identification of lncRNA biomarkers in hepatocellular carcinoma and revealing the effect of ZFAS1/miR-150-5p on hepatocellular carcinoma progression. PeerJ 2023, 11, e14891. [Google Scholar] [CrossRef]
- Oishi, K.; Sakamoto, K.; Okada, T.; Nagase, T.; Ishida, N. Antiphase circadian expression between BMAL1 and period homologue mRNA in the suprachiasmatic nucleus and peripheral tissues of rats. Biochem. Biophys. Res. Commun. 1998, 253, 199–203. [Google Scholar] [CrossRef]
- Yan, L.; Takekida, S.; Shigeyoshi, Y.; Okamura, H. Per1 and Per2 gene expression in the rat suprachiasmatic nucleus: Circadian profile and the compartment-specific response to light. Neuroscience 1999, 94, 141–150. [Google Scholar] [CrossRef]
- Reppert, S.M.; Weaver, D.R. Molecular analysis of mammalian circadian rhythms. Annu. Rev. Physiol. 2001, 63, 647–676. [Google Scholar] [CrossRef] [PubMed]
- van der Watt, P.J.; Roden, L.C.; Davis, K.T.; Parker, M.I.; Leaner, V.D. Circadian Oscillations Persist in Cervical and Esophageal Cancer Cells Displaying Decreased Expression of Tumor-Suppressing Circadian Clock Genes. Mol. Cancer Res. 2020, 18, 1340–1353. [Google Scholar] [CrossRef]
- Iacomino, G. miRNAs: The Road from Bench to Bedside. Genes 2023, 14, 314. [Google Scholar] [CrossRef] [PubMed]
3.8% | 2.2% | 1.9% | 1.9% |
---|---|---|---|
75–100 | 50–75 | 25–50 | 0–25 |
Very High Expression | High Expression | Low Expression | Very Low Expression |
miR-30d-5p | miR-26b-3p | miR-18a-5p | miR-351-3p |
miR-7a-5p | miR-363-3p | miR-20b-5p | miR-186-3p |
miR-185-5p | miR-15b-5p | miR-153-3p | miR-543-5p |
miR-425-5p | miR-3068-3p | miR-200c-5p | miR-344b-1-3p |
miR-150-5p | miR-9a-3p | miR-146a-3p | miR-3084b-3p |
miR-128-3p | miR-130a-3p | miR-299b-5p | miR-3084d |
miR-455-5p | miR-3590-5p | miR-129-2-3p | miR-3084a-3p |
miR-129-5p | miR-342-5p | ||
miR-139-5p | |||
miR-24-2-5p | |||
let-7g-5p | |||
miR-148b-3p | |||
miR-148a-3p | |||
miR-142-3p |
2.2% | 1.3% | 0.9% | 0.2% |
---|---|---|---|
75–100 | 50–75 | 25–50 | 0–25 |
Very High Expression | High Expression | Low Expression | Very Low Expression |
mir-30d | mir-185 | mir-20b | mir-3572 |
mir-7a-2 | mir-425 | mir-153 | |
mir-7a-1 | mir-15b | mir-219a-1 | |
mir-150 | mir-363 | mir-877 | |
mir-128-1 | mir-129-1 | ||
mir-128-2 | mir-129-2 | ||
mir-139 | |||
let-7g | |||
mir-148b | |||
mir-148a |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Herichová, I.; Vanátová, D.; Reis, R.; Stebelová, K.; Olexová, L.; Morová, M.; Ghosh, A.; Baláž, M.; Štefánik, P.; Kršková, L. Daily Profile of miRNAs in the Rat Colon and In Silico Analysis of Their Possible Relationship to Colorectal Cancer. Biomedicines 2025, 13, 1865. https://doi.org/10.3390/biomedicines13081865
Herichová I, Vanátová D, Reis R, Stebelová K, Olexová L, Morová M, Ghosh A, Baláž M, Štefánik P, Kršková L. Daily Profile of miRNAs in the Rat Colon and In Silico Analysis of Their Possible Relationship to Colorectal Cancer. Biomedicines. 2025; 13(8):1865. https://doi.org/10.3390/biomedicines13081865
Chicago/Turabian StyleHerichová, Iveta, Denisa Vanátová, Richard Reis, Katarína Stebelová, Lucia Olexová, Martina Morová, Adhideb Ghosh, Miroslav Baláž, Peter Štefánik, and Lucia Kršková. 2025. "Daily Profile of miRNAs in the Rat Colon and In Silico Analysis of Their Possible Relationship to Colorectal Cancer" Biomedicines 13, no. 8: 1865. https://doi.org/10.3390/biomedicines13081865
APA StyleHerichová, I., Vanátová, D., Reis, R., Stebelová, K., Olexová, L., Morová, M., Ghosh, A., Baláž, M., Štefánik, P., & Kršková, L. (2025). Daily Profile of miRNAs in the Rat Colon and In Silico Analysis of Their Possible Relationship to Colorectal Cancer. Biomedicines, 13(8), 1865. https://doi.org/10.3390/biomedicines13081865