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MicroRNAs as the Critical Regulators of Forkhead Box Protein Family in Pancreatic, Thyroid, and Liver Cancers

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Abstract

The metabolism of human body is mainly regulated by the pancreas, liver, and thyroid using the hormones or exocrine secretions that affect the metabolic processes from food digestion to intracellular metabolism. Therefore, metabolic organ disorders have wide clinical symptoms that severely affect the quality of patient’s life. The pancreatic, liver, and thyroid cancers as the main malignancies of the metabolic system have always been considered as one of the serious health challenges worldwide. Despite the novel therapeutic modalities, there are still significant high mortality and recurrence rates, especially in liver and pancreatic cancer patients which are mainly related to the late diagnosis. Therefore, it is required to assess the molecular bases of tumor progressions to introduce novel early detection and therapeutic markers in these malignancies. Forkhead box (FOX) protein family is a group of transcription factors that have pivotal roles in regulation of cell proliferation, migration, and apoptosis. They function as oncogene or tumor suppressor during tumor progression. MicroRNAs (miRNAs) are also involved in regulation of cellular processes. Therefore, in the present review, we discussed the role of miRNAs during pancreatic, thyroid, and liver tumor progressions through FOX regulation. It has been shown that miRNAs were mainly involved in tumor progression via FOXM and FOXO targeting. This review paves the way for the introduction of miR/FOX axis as an efficient early detection marker and therapeutic target in pancreatic, thyroid, and liver tumors.

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Data Availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Al-Azri MH (2016) Delay in cancer diagnosis: causes and possible solutions. Oman Med J 31(5):325

    Article  PubMed  PubMed Central  Google Scholar 

  • Ankasha SJ, Shafiee MN, Wahab NA, Ali RAR, Mokhtar NM (2018) Post-transcriptional regulation of microRNAs in cancer: from prediction to validation. Oncol Rev 12:1

    CAS  Google Scholar 

  • Bach DH, Long NP, Luu TT, Anh NH, Kwon SW, Lee SK (2018) The dominant role of Forkhead Box Proteins in cancer. Int J Mol Sci 19:10

    Article  Google Scholar 

  • Bates MF, Lamas MR, Randle RW, Long KL, Pitt SC, Schneider DF, Sippel RS (2018) Back so soon? Is early recurrence of papillary thyroid cancer really just persistent disease? Surgery 163(1):118–123

    Article  PubMed  Google Scholar 

  • Besnard V, Wert SE, Hull WM, Whitsett JA (2004) Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expr Patterns 5(2):193–208

    Article  CAS  PubMed  Google Scholar 

  • Bhat UG, Halasi M, Gartel AL (2009) FoxM1 is a general target for proteasome inhibitors. PLoS ONE 4(8):e6593

    Article  PubMed  PubMed Central  Google Scholar 

  • Bi C, Wang G (2021) LINC00472 suppressed by ZEB1 regulates the miR-23a-3p/FOXO3/BID axis to inhibit the progression of pancreatic cancer. J Cell Mol Med 25(17):8312–8328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowman CJ, Ayer DE, Dynlacht BD (2014) Foxk proteins repress the initiation of starvation-induced atrophy and autophagy programs. Nat Cell Biol 16(12):1202–1214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96(6):857–868

    Article  CAS  PubMed  Google Scholar 

  • Calissi G, Lam EW, Link W (2021) Therapeutic strategies targeting FOXO transcription factors. Nat Rev Drug Discov 20(1):21–38

    Article  CAS  PubMed  Google Scholar 

  • Cao MQ, You AB, Zhu XD, Zhang W, Zhang YY, Zhang SZ, Zhang KW, Cai H, Shi WK, Li XL, Li KS, Gao DM, Ma DN, Ye BG, Wang CH, Qin CD, Sun HC, Zhang T, Tang ZY (2018) miR-182-5p promotes hepatocellular carcinoma progression by repressing FOXO3a. J Hematol Oncol 11(1):12

    Article  PubMed  PubMed Central  Google Scholar 

  • Cautain B, Castillo F, Musso L, Ferreira BI, de Pedro N, Rodriguez Quesada L, Machado S, Vicente F, Dallavalle S, Link W (2016) Discovery of a novel, isothiazolonaphthoquinone-based small molecule activator of FOXO nuclear-cytoplasmic shuttling. PLoS ONE 11(12):e0167491

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang DL, Wei W, Yu ZP, Qin CK (2017) miR-152-5p inhibits proliferation and induces apoptosis of liver cancer cells by up-regulating FOXO expression. Pharmazie 72(6):338–343

    CAS  PubMed  Google Scholar 

  • Chang Y, Zhou C, Fan L, Qiu G, Wang G, Wei G, Chang X, Li XJOR (2018) Upregulation of microRNA-300 induces the proliferation of liver cancer by downregulating transcription factor FOXO1. Oncol Rep 40(6):3561–3572

    CAS  PubMed  Google Scholar 

  • Chari A, Vogl DT, Gavriatopoulou M, Nooka AK, Yee AJ, Huff CA, Moreau P, Dingli D, Cole C, Lonial S, Dimopoulos M, Stewart AK, Richter J, Vij R, Tuchman S, Raab MS, Weisel KC, Delforge M, Cornell RF, Kaminetzky D, Hoffman JE, Costa LJ, Parker TL, Levy M, Schreder M, Meuleman N, Frenzel L, Mohty M, Choquet S, Schiller G, Comenzo RL, Engelhardt M, Illmer T, Vlummens P, Doyen C, Facon T, Karlin L, Perrot A, Podar K, Kauffman MG, Shacham S, Li L, Tang S, Picklesimer C, Saint-Martin JR, Crochiere M, Chang H, Parekh S, Landesman Y, Shah J, Richardson PG, Jagannath S (2019) Oral Selinexor-Dexamethasone for Triple-Class Refractory Multiple Myeloma. N Engl J Med 381(8):727–738

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Fu Y, Guo Z, Zhou X (2022) MicroRNA-29c-3p participates in insulin function to modulate polycystic ovary syndrome via targeting Forkhead box O3. Bioengineered 13(2):4361–4371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S-Y, Ma D-N, Chen Q-D, Zhang J-J, Tian Y-R, Wang Z-C, Cai H, Lin Y, Sun H-C (2017) MicroRNA-200a inhibits cell growth and metastasis by targeting Foxa2 in hepatocellular carcinoma. J Cancer 8(4):617–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen T, Lei S, Zeng Z, Zhang J, Xue Y, Sun Y, Lan J, Xu S, Mao D, Guo B (2020) Linc00261 inhibits metastasis and the WNT signaling pathway of pancreatic cancer by regulating a miR5525p/FOXO3 axis. Oncol Rep 43(3):930–942

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen W, Li Y, Zhong J, Wen G (2021) circ-PRKCI targets miR-1294 and miR-186–5p by downregulating FOXK1 expression to suppress glycolysis in hepatocellular carcinoma. Mol Med Rep 23:6

    Article  Google Scholar 

  • Chen X, Li M, Zhou H, Zhang L (2019) miR-132 targets FOXA1 and exerts tumor-suppressing functions in thyroid cancer. Oncol Res 27(4):431–437

    Article  PubMed  PubMed Central  Google Scholar 

  • Choksi NY, Jahnke GD, St C, Hilaire and M. Shelby, (2003) Role of thyroid hormones in human and laboratory animal reproductive health. Birth Defects Res B 68(6):479–491

    Article  CAS  Google Scholar 

  • Colla S, Tagliaferri S, Morandi F, Lunghi P, Donofrio G, Martorana D, Mancini C, Lazzaretti M, Mazzera L, Ravanetti L, Bonomini S, Ferrari L, Miranda C, Ladetto M, Neri TM, Neri A, Greco A, Mangoni M, Bonati A, Rizzoli V, Giuliani N (2007) The new tumor-suppressor gene inhibitor of growth family member 4 (ING4) regulates the production of proangiogenic molecules by myeloma cells and suppresses hypoxia-inducible factor-1 alpha (HIF-1alpha) activity: involvement in myeloma-induced angiogenesis. Blood 110(13):4464–4475

    Article  CAS  PubMed  Google Scholar 

  • Condrat CE, Thompson DC, Barbu MG, Bugnar OL, Boboc A, Cretoiu D, Suciu N, Cretoiu SM, Voinea SC (2020) miRNAs as biomarkers in disease: latest findings regarding their role in diagnosis and prognosis. Cells 9(2):276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corno C, Stucchi S, De Cesare M, Carenini N, Stamatakos S, Ciusani E, Minoli L, Scanziani E, Argueta C, Landesman Y, Zaffaroni N, Gatti L, Perego P (2018) FoxO-1 contributes to the efficacy of the combination of the XPO1 inhibitor selinexor and cisplatin in ovarian carcinoma preclinical models. Biochem Pharmacol 147:93–103

    Article  CAS  PubMed  Google Scholar 

  • Cui S, Gao Y, Zhang K, Chen J, Wang R, Chen L (2015) The emerging role of inhibitor of growth 4 as a tumor suppressor in multiple human cancers. Cell Physiol Biochem 36(2):409–422

    Article  CAS  PubMed  Google Scholar 

  • Dai Y, Wang M, Wu H, Xiao M, Liu H, Zhang D (2017) Loss of FOXN3 in colon cancer activates beta-catenin/TCF signaling and promotes the growth and migration of cancer cells. Oncotarget 8(6):9783–9793

    Article  PubMed  Google Scholar 

  • Dehner M, Hadjihannas M, Weiske J, Huber O, Behrens J (2008) Wnt signaling inhibits Forkhead box O3a-induced transcription and apoptosis through up-regulation of serum- and glucocorticoid-inducible kinase 1. J Biol Chem 283(28):19201–19210

    Article  CAS  PubMed  Google Scholar 

  • DeLaughter DM, Christodoulou DC, Robinson JY, Seidman CE, Baldwin HS, Seidman J, Barnett JV (2013) Spatial transcriptional profile of the chick and mouse endocardial cushions identify novel regulators of endocardial EMT in vitro. J Mol Cell Cardiol 59:196–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dionigi G, Dionigi R, Bartalena L, Tanda ML, Piantanida E, Boni L, Rovera F (2007) An analysis on delays in diagnosis of papillary thyroid cancer. Endocrine Abstracts, Bioscientifica

  • Dou C, Wang Y, Li C, Liu Z, Jia Y, Li Q, Yang W, Yao Y, Liu Q, Tu K (2015) MicroRNA-212 suppresses tumor growth of human hepatocellular carcinoma by targeting FOXA1. Oncotarget 6(15):13216–13228

    Article  PubMed  PubMed Central  Google Scholar 

  • Duan X, Jiang B, Yang J, Zhou L, Tian B, Mao X (2018) FOXP3 inhibits MYC expression via regulating miR-198 and influences cell viability, proliferation and cell apoptosis in HepG2. Cancer Med 7(12):6182–6192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dumortier O, Hinault C, Van Obberghen E (2013) MicroRNAs and metabolism crosstalk in energy homeostasis. Cell Metab 18(3):312–324

    Article  CAS  PubMed  Google Scholar 

  • Estruch SB, Graham SA, Quevedo M, Vino A, Dekkers DH, Deriziotis P, Sollis E, Demmers J, Poot RA, Fisher SE (2018) Proteomic analysis of FOXP proteins reveals interactions between cortical transcription factors associated with neurodevelopmental disorders. Hum Mol Genet 27(7):1212–1227

    Article  CAS  PubMed  Google Scholar 

  • Feng Z, Chen R, Huang N, Luo C (2020) Long non-coding RNA ASMTL-AS1 inhibits tumor growth and glycolysis by regulating the miR-93-3p/miR-660/FOXO1 axis in papillary thyroid carcinoma. Life Sci 244:117298

    Article  CAS  PubMed  Google Scholar 

  • Friedman J, Kaestner K (2006) The Foxa family of transcription factors in development and metabolism. Cell Mol Life Sci CMLS 63(19):2317–2328

    Article  CAS  PubMed  Google Scholar 

  • Fukuchi H, Hayashida Y, Inoue K, Sadamura Y (2019) Forkhead box B2 inhibits the malignant characteristics of the pancreatic cancer cell line Panc-1 in vitro. Genes Cells 24(10):674–681

    Article  CAS  PubMed  Google Scholar 

  • Gabison EE, Huet E, Baudouin C, Menashi S (2009) Direct epithelial–stromal interaction in corneal wound healing: Role of EMMPRIN/CD147 in MMPs induction and beyond. Prog Retin Eye Res 28(1):19–33

    Article  CAS  PubMed  Google Scholar 

  • Garkavtsev I, Kozin SV, Chernova O, Xu L, Winkler F, Brown E, Barnett GH, Jain RK (2004) The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature 428(6980):328–332

    Article  CAS  PubMed  Google Scholar 

  • Gartel AL (2010) A new target for proteasome inhibitors: FoxM1. Expert Opin Investig Drugs 19(2):235–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge Y-F, Sun J, Jin C-J, Cao B-Q, Jiang Z-F, Shao J-F (2013) AntagomiR-27a targets FOXO3a in glioblastoma and suppresses U87 cell growth in vitro and in vivo. Asian Pac J Cancer Prev 14(2):963–968

    Article  PubMed  Google Scholar 

  • Guérillon C, Bigot N, Pedeux R (2014) The ING tumor suppressor genes: status in human tumors. Cancer Lett 345(1):1–16

    Article  PubMed  Google Scholar 

  • Guo S, Sonenshein GE (2004) Forkhead box transcription factor FOXO3a regulates estrogen receptor alpha expression and is repressed by the Her-2/neu/phosphatidylinositol 3-kinase/Akt signaling pathway. Mol Cell Biol 24(19):8681–8690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo X, Wang Y (2020) LncRNA TMPO-AS1 promotes hepatocellular carcinoma cell proliferation, migration and invasion through sponging miR-329-3p to stimulate FOXK1-mediated AKT/mTOR signaling pathway. Cancer Med 9(14):5235–5246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han S, Shi Y, Sun L, Liu Z, Song T, Liu Q (2019) MiR-4319 induced an inhibition of epithelial-mesenchymal transition and prevented cancer stemness of HCC through targeting FOXQ1. Int J Biol Sci 15(13):2936–2947

    Article  PubMed  PubMed Central  Google Scholar 

  • Henderson J, Moss M (1985) A morphometric study of the endocrine and exocrine capillaries of the pancreas. Q J Exp Physiol 70(3):347–356

    Article  CAS  PubMed  Google Scholar 

  • Hou Y, Zhu Q, Li Z, Peng Y, Yu X, Yuan B, Liu Y, Liu Y, Yin L, Peng Y (2017) The FOXM1–ABCC5 axis contributes to paclitaxel resistance in nasopharyngeal carcinoma cells. Cell Death Dis 8(3):e2659–e2659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang C, Du J, Xie K (2014) FOXM1 and its oncogenic signaling in pancreatic cancer pathogenesis. Biochim Biophys Acta 1845(2):104–116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Qin J, Lu S (2015) Up-regulation of miR-877 induced by paclitaxel inhibits hepatocellular carcinoma cell proliferation though targeting FOXM1. Int J Clin Exp Pathol 8(2):1515–1524

    PubMed  PubMed Central  Google Scholar 

  • Jägle S, Busch H, Freihen V, Beyes S, Schrempp M, Boerries M, Hecht A (2017) SNAIL1-mediated downregulation of FOXA proteins facilitates the inactivation of transcriptional enhancer elements at key epithelial genes in colorectal cancer cells. PLoS Genet 13(11):e1007109

    Article  PubMed  PubMed Central  Google Scholar 

  • Jia P, Wei G, Zhou C, Gao Q, Wu Y, Sun X, Li X (2018) Upregulation of MiR-212 inhibits migration and tumorigenicity and inactivates Wnt/β-catenin signaling in human hepatocellular carcinoma. Technol Cancer Res Treat 17:1533034618765221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiramongkol Y, Lam EW-F (2020) FOXO transcription factor family in cancer and metastasis. Cancer Metastasis Rev 39(3):681–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamaldinov T, Erndt-Marino J, Diaz-Rodriguez P, Chen H, Gharat T, Munoz-Pinto D, Arduini B, Hahn MS (2018) Tuning Forkhead Box D3 overexpression to promote specific osteogenic differentiation of human embryonic stem cells while reducing pluripotency in a three-dimensional culture system. J Tissue Eng Regen Med 12(12):2256–2265

    Article  CAS  PubMed  Google Scholar 

  • Katoh M, Katoh M (2004) Human FOX gene family (Review). Int J Oncol 25(5):1495–1500

    CAS  PubMed  Google Scholar 

  • Kim J-H, Hwang J, Jung JH, Lee H-J, Lee DY, Kim S-H (2019) Molecular networks of FOXP family: dual biologic functions, interplay with other molecules and clinical implications in cancer progression. Mol Cancer 18(1):1–19

    Article  Google Scholar 

  • Kobliakov VA (2016) Hypoxia and glycolysis as factors determining the malignant phenotype. Tsitologiia 58(7):499–506

    CAS  PubMed  Google Scholar 

  • Kong W, He L, Coppola M, Guo J, Esposito NN, Coppola D, Cheng JQ (2010) MicroRNA-155 regulates cell survival, growth, and chemosensitivity by targeting FOXO3a in breast cancer. J Biol Chem 285(23):17869–17879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong X, Li L, Li Z, Le X, Huang C, Jia Z, Cui J, Huang S, Wang L, Xie K (2013) Dysregulated expression of FOXM1 isoforms drives progression of pancreatic cancer. Cancer Res 73(13):3987–3996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuwahara K, Yamamoto-Ibusuki M, Zhang Z, Phimsen S, Gondo N, Yamashita H, Takeo T, Nakagata N, Yamashita D, Fukushima Y, Yamamoto Y, Iwata H, Saya H, Kondo E, Matsuo K, Takeya M, Iwase H, Sakaguchi N (2016) GANP protein encoded on human chromosome 21/mouse chromosome 10 is associated with resistance to mammary tumor development. Cancer Sci 107(4):469–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamadé W, Herfarth C (2001) Resection of recurrent liver cancer. Surgical Treatment: Evidence-Based and Problem-Oriented, Zuckschwerdt

  • Langlet F, Haeusler RA, Linden D, Ericson E, Norris T, Johansson A, Cook JR, Aizawa K, Wang L, Buettner C, Accili D (2017) Selective Inhibition of FOXO1 activator/repressor balance modulates hepatic glucose handling. Cell 171(4):824–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Martinka M, Li G (2008) Role of ING4 in human melanoma cell migration, invasion and patient survival. Carcinogenesis 29(7):1373–1379

    Article  PubMed  Google Scholar 

  • Li J, Qin X, Wu R, Wan L, Zhang L, Liu R (2020a) Circular RNA circFBXO11 modulates hepatocellular carcinoma progress and oxaliplatin resistance through miR-605/FOXO3/ABCB1 axis. J Cell Mol Med 24(9):5152–5161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Li Z, Kong X, Xie D, Jia Z, Jiang W, Cui J, Du Y, Wei D, Huang S, Xie K (2014) Down-regulation of microRNA-494 via loss of SMAD4 increases FOXM1 and beta-catenin signaling in pancreatic ductal adenocarcinoma cells. Gastroenterology 147(2):485–497

    Article  CAS  PubMed  Google Scholar 

  • Li W, Jiang H (2020) Up-regulation of miR-498 inhibits cell proliferation, invasion and migration of hepatocellular carcinoma by targeting FOXO3. Clin Res Hepatol Gastroenterol 44(1):29–37

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Hong X, Hussain M, Sarkar SH, Li R, Sarkar FH (2005a) Gene expression profiling revealed novel molecular targets of docetaxel and estramustine combination treatment in prostate cancer cells. Mol Cancer Ther 4(3):389–398

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Hussain M, Sarkar SH, Eliason J, Li R, Sarkar FH (2005b) Gene expression profiling revealed novel mechanism of action of Taxotere and Furtulon in prostate cancer cells. BMC Cancer 5:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Y, Wang X, Li Z, Liu B, Wu C (2020b) MicroRNA-4651 represses hepatocellular carcinoma cell growth and facilitates apoptosis via targeting FOXP4. Biosci ReP 40:6

    Article  CAS  Google Scholar 

  • Lin MF, Yang YF, Peng ZP, Zhang MF, Liang JY, Chen W, Liu XH, Zheng YL (2017) FOXK2, regulted by miR-1271-5p, promotes cell growth and indicates unfavorable prognosis in hepatocellular carcinoma. Int J Biochem Cell Biol 88:155–161

    Article  CAS  PubMed  Google Scholar 

  • Lin X, Zuo S, Luo R, Li Y, Yu G, Zou Y, Zhou Y, Liu Z, Liu Y, Hu Y, Xie Y, Fang W, Liu Z (2019) HBX-induced miR-5188 impairs FOXO1 to stimulate beta-catenin nuclear translocation and promotes tumor stemness in hepatocellular carcinoma. Theranostics 9(25):7583–7598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Link W (2019) Introduction to FOXO biology. FOXO Transcrip Factors 1:1–9

    Google Scholar 

  • Liu LL, Lu SX, Li M, Li LZ, Fu J, Hu W, Yang YZ, Luo RZ, Zhang CZ, Yun JP (2014) FoxD3-regulated microRNA-137 suppresses tumour growth and metastasis in human hepatocellular carcinoma by targeting AKT2. Oncotarget 5(13):5113–5124

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu S, Qiu J, He G, Liang Y, Wang L, Liu C, Pan H (2019a) LncRNA MALAT1 acts as a miR-125a-3p sponge to regulate FOXM1 expression and promote hepatocellular carcinoma progression. J Cancer 10(26):6649–6659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Ding W, Ge H, Ponnusamy M, Wang Q, Hao X, Wu W, Zhang Y, Yu W, Ao X (2019b) FOXK transcription factors: regulation and critical role in cancer. Cancer Lett 458:1–12

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Li Z, Xu B, Yao H, Qi S, Tai J (2020) Long Noncoding RNA PRR34-AS1 Aggravates the Progression of Hepatocellular Carcinoma by Adsorbing microRNA-498 and Thereby Upregulating FOXO3. Cancer Manag Res 12:10749–10762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lo P-K (2018) FOXF2 differentially regulates expression of metabolic genes in non-cancerous and cancerous breast epithelial cells. Trends Diabetes Metab 1:1

    Article  Google Scholar 

  • Lou K, Chen N, Li Z, Zhang B, Wang X, Chen Y, Xu H, Wang D, Wang H (2017) MicroRNA-142-5p overexpression inhibits cell growth and induces apoptosis by regulating FOXO in hepatocellular carcinoma cells. Oncol Res 25(1):65–73

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo W, Gao F, Li S, Liu L (2018) FoxM1 promotes cell proliferation, invasion, and stem cell properties in nasopharyngeal carcinoma. Front Oncol 483:1

    Google Scholar 

  • Malin D, Kim I-M, Boetticher E, Kalin TV, Ramakrishna S, Meliton L, Ustiyan V, Zhu X, Kalinichenko VV (2007) Forkhead box F1 is essential for migration of mesenchymal cells and directly induces integrin-beta3 expression. Mol Cell Biol 27(7):2486–2498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mecklenburg L, Tychsen B, Paus R (2005) Learning from nudity: lessons from the nude phenotype. Exp Dermatol 14(11):797–810

    Article  CAS  PubMed  Google Scholar 

  • Meng F, Liu J, Lu T, Zang L, Wang J, He Q, Zhou A (2021) SNHG1 knockdown upregulates miR-376a and downregulates FOXK1/Snail axis to prevent tumor growth and metastasis in HCC. Mol Ther Oncolytics 21:264–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitra V, Metcalf J (2012) Metabolic functions of the liver. Anaesthesia Intensive Care Med 13(2):54–55

    Article  Google Scholar 

  • Moghbeli M (2021) MicroRNAs as the critical regulators of Cisplatin resistance in ovarian cancer cells. J Ovarian Res 14(1):127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moghbeli M, Zangouei AS, Nasrpour Navaii Z, Taghehchian N (2021) Molecular mechanisms of the microRNA-132 during tumor progressions. Cancer Cell Int 21(1):439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moletta L, Serafini S, Valmasoni M, Pierobon ES, Ponzoni A, Sperti C (2019) Surgery for recurrent pancreatic cancer: is it effective? Cancers 11(7):991

    Article  PubMed  PubMed Central  Google Scholar 

  • Myatt SS, Lam EW-F (2007) The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer 7(11):847–859

    Article  CAS  PubMed  Google Scholar 

  • Nakamura TM, Morin GB, Chapman KB, Weinrich SL, Andrews WH, Lingner J, Harley CB, Cech TR (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science 277(5328):955–959

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi C, Toi M (2005) Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs. Nat Rev Cancer 5(4):297–309

    Article  CAS  PubMed  Google Scholar 

  • Nakayama S, Soejima K, Yasuda H, Yoda S, Satomi R, Ikemura S, Terai H, Sato T, Yamaguchi N, Hamamoto J (2015) FOXD1 expression is associated with poor prognosis in non-small cell lung cancer. Anticancer Res 35(1):261–268

    CAS  PubMed  Google Scholar 

  • Nguyen P, Leray V, Diez M, Serisier S, J. L. Bloc’h, B. Siliart and H. Dumon, (2008) Liver lipid metabolism. J Anim Physiol Anim Nutr 92(3):272–283

    Article  CAS  Google Scholar 

  • Nikolaou M, Pavlopoulou A, Georgakilas AG, Kyrodimos E (2018) The challenge of drug resistance in cancer treatment: a current overview. Clin Exp Metas 35(4):309–318

    Article  CAS  Google Scholar 

  • Nilsson G, Kannius-Janson M (2016) Forkhead Box F1 promotes breast cancer cell migration by upregulating lysyl oxidase and suppressing Smad2/3 signaling. BMC Cancer 16(1):1–12

    Article  Google Scholar 

  • Nowell CS, Bredenkamp N, Tetelin S, Jin X, Tischner C, Vaidya H, Sheridan JM, Stenhouse FH, Heussen R, Smith AJ (2011) Foxn1 regulates lineage progression in cortical and medullary thymic epithelial cells but is dispensable for medullary sublineage divergence. PLoS Genet 7(11):e1002348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pavlova NN, Thompson CB (2016) The emerging hallmarks of cancer metabolism. Cell Metab 23(1):27–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian F, Hu Q, Tian Y, Wu J, Li D, Tao M, Qin L, Shen B, Xie Y (2019) ING4 suppresses hepatocellular carcinoma via a NF-κB/miR-155/FOXO3a signaling axis. Int J Biol Sci 15(2):369–385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu H, Yin H, Yan S, Tao M, Xie Y, Chen W (2016) Inhibitor of growth 4 suppresses colorectal cancer growth and invasion by inducing G1 arrest, inhibiting tumor angiogenesis and reversing epithelial-mesenchymal transition. Oncol Rep 35(5):2927–2935

    Article  CAS  PubMed  Google Scholar 

  • Rao A, Rich NE, Marrero JA, Yopp AC, Singal AG (2021) Diagnostic and therapeutic delays in patients with hepatocellular carcinoma. J Natl Compr Canc Netw 19(9):1063–1071

    Article  PubMed  Google Scholar 

  • Ring A, Kim YM, Kahn M (2014) Wnt/catenin signaling in adult stem cell physiology and disease. Stem Cell Rev Rep 10(4):512–525

    Article  CAS  PubMed  Google Scholar 

  • Sahu B, Laakso M, Ovaska K, Mirtti T, Lundin J, Rannikko A, Sankila A, Turunen JP, Lundin M, Konsti J (2011) Dual role of FoxA1 in androgen receptor binding to chromatin, androgen signalling and prostate cancer. EMBO J 30(19):3962–3976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saito R-A, Micke P, Paulsson J, Augsten M, Peña C, Jönsson P, Botling J, Edlund K, Johansson L, Carlsson P (2010) Forkhead box F1 regulates tumor-promoting properties of cancer-associated fibroblasts in lung cancer. Can Res 70(7):2644–2654

    Article  CAS  Google Scholar 

  • Sellam F, Harir N, Khaled MB, Mrabent NM, Salah R, Benchouk A, Diaf M (2015) Delayed diagnosis of pancreatic cancer reported as more common in a population of North African young adults. J Gastrointestinal Oncol 6(5):505

    Google Scholar 

  • Shao J, Cao J, Liu Y, Mei H, Zhang Y, Xu W (2015) MicroRNA-519a promotes proliferation and inhibits apoptosis of hepatocellular carcinoma cells by targeting FOXF2. FEBS Open Bio 5:893–899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen JC, Unoki M, Ythier D, Duperray A, Varticovski L, Kumamoto K, Pedeux R, Harris CC (2007) Inhibitor of growth 4 suppresses cell spreading and cell migration by interacting with a novel binding partner, liprin alpha1. Cancer Res 67(6):2552–2558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi YY, Meng XT, Xu YN, Tian XJ (2021) Role of FOXO protein’s abnormal activation through PI3K/AKT pathway in platinum resistance of ovarian cancer. J Obstetr Gynaecol Res 47(6):1946–1957

    Article  CAS  Google Scholar 

  • Shiseki M, Nagashima M, Pedeux RM, Kitahama-Shiseki M, Miura K, Okamura S, Onogi H, Higashimoto Y, Appella E, Yokota J, Harris CC (2003) p29ING4 and p28ING5 bind to p53 and p300, and enhance p53 activity. Cancer Res 63(10):2373–2378

    CAS  PubMed  Google Scholar 

  • Shukla S, Bhaskaran N, MacLennan GT, Gupta S (2013) Deregulation of FoxO3a accelerates prostate cancer progression in TRAMP mice. Prostate 73(14):1507–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siegel RL, Miller KD, Fuchs HE, Jemal A (2021) Cancer Statistics, 2021. CA Cancer J Clin 71(1):7–33

    Article  PubMed  Google Scholar 

  • Sin C, Li H, Crawford DA (2015) Transcriptional regulation by FOXP1, FOXP2, and FOXP4 dimerization. J Mol Neurosci 55(2):437–448

    Article  CAS  PubMed  Google Scholar 

  • Song HM, Luo Y, Li DF, Wei CK, Hua KY, Song JL, Xu H, Maskey N, Fang L (2015) MicroRNA-96 plays an oncogenic role by targeting FOXO1 and regulating AKT/FOXO1/Bim pathway in papillary thyroid carcinoma cells. Int J Clin Exp Pathol 8(9):9889–9900

    PubMed  PubMed Central  Google Scholar 

  • Song Y, Zeng S, Zheng G, Chen D, Li P, Yang M, Luo K, Yin J, Gu Y, Zhang Z (2021) FOXO3a-driven miRNA signatures suppresses VEGF-A/NRP1 signaling and breast cancer metastasis. Oncogene 40(4):777–790

    Article  CAS  PubMed  Google Scholar 

  • Szylberg Ł, Karbownik D, Marszałek A (2016) The role of FOXP3 in human cancers. Anticancer Res 36(8):3789–3794

    CAS  PubMed  Google Scholar 

  • Tian C, Wu H, Li C, Tian X, Sun Y, Liu E, Liao X, Song W (2018) Downreguation of FoxM1 by miR-214 inhibits proliferation and migration in hepatocellular carcinoma. Gene Ther 25(4):312–319

    Article  CAS  PubMed  Google Scholar 

  • Toole BP, Slomiany MG (2008) Hyaluronan, CD44 and Emmprin: partners in cancer cell chemoresistance. Drug Resist Updat 11(3):110–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unoki M, Shen JC, Zheng ZM, Harris CC (2006) Novel splice variants of ING4 and their possible roles in the regulation of cell growth and motility. J Biol Chem 281(45):34677–34686

    Article  CAS  PubMed  Google Scholar 

  • Van Der Heide LP, Hoekman MF, Smidt MP (2004) The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem J 380(Pt 2):297–309

    Article  PubMed  Google Scholar 

  • van der Heide LP, Wijchers PJ, von Oerthel L, Burbach JPH, Hoekman MF, Smidt MP (2015) FoxK2 is required for cellular proliferation and survival. J Cell Physiol 230(5):1013–1023

    Article  PubMed  Google Scholar 

  • Vasan N, Baselga J, Hyman DM (2019) A view on drug resistance in cancer. Nature 575(7782):299–309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vernes SC, Spiteri E, Nicod J, Groszer M, Taylor JM, Davies KE, Geschwind DH, Fisher SE (2007) High-throughput analysis of promoter occupancy reveals direct neural targets of FOXP2, a gene mutated in speech and language disorders. Am J Hum Genet 81(6):1232–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Peng R, Wang J, Qin Z, Xue L (2018a) Circulating microRNAs as potential cancer biomarkers: the advantage and disadvantage. Clin Epigenetics 10(1):1–10

    Article  Google Scholar 

  • Wang J, Li W, Zhao Y, Kang D, Fu W, Zheng X, Pang X, Du G (2018b) Members of FOX family could be drug targets of cancers. Pharmacol Ther 181:183–196

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Yang X, Zhou X, Wu B, Zhu D, Jia W, Chu J, Wang J, Wu J, Kong L (2020) MiR-3174 promotes proliferation and inhibits apoptosis by targeting FOXO1 in hepatocellular carcinoma. Biochem Biophys Res Commun 526(4):889–897

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Xu M, Sun Z, Yu X, Deng Y, Chang H (2019a) LINC01018 confers a novel tumor suppressor role in hepatocellular carcinoma through sponging microRNA-182-5p. Am J Physiol Gastrointest Liver Physiol 317(2):G116-g126

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Dou N, Wang J, Zhang Y, Li Y, Gao Y (2021) FOXM1-induced miR-552 expression contributes to pancreatic cancer progression by targeting multiple tumor suppressor genes. Int J Biol Sci 17(4):915–925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y-G, Wang T, Shi M, Zhai B (2019b) Long noncoding RNA EPB41L4A-AS2 inhibits hepatocellular carcinoma development by sponging miR-301a-5p and targeting FOXL1. J Exp Clin Cancer Res 38(1):153

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Yang L, Chen T, Liu X, Guo Y, Zhu Q, Tong X, Yang W, Xu Q, Huang D, Tu K (2019c) A novel lncRNA MCM3AP-AS1 promotes the growth of hepatocellular carcinoma by targeting miR-194-5p/FOXA1 axis. Mol Cancer 18(1):28–28

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Zhou Y, Graves DT (2014) FOXO transcription factors: their clinical significance and regulation. BioMed Res Int 2014:1

    Article  Google Scholar 

  • Warburg O (1956) On the origin of cancer cells. Science 123(3191):309–314

    Article  CAS  PubMed  Google Scholar 

  • Webb AE, Brunet A (2014) FOXO transcription factors: key regulators of cellular quality control. Trends Biochem Sci 39(4):159–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei Y, Wang Z, Zong Y, Deng D, Chen P, Lu J (2020) LncRNA MFI2-AS1 promotes HCC progression and metastasis by acting as a competing endogenous RNA of miR-134 to upregulate FOXM1 expression. Biomed Pharmacother 125:109890

    Article  CAS  PubMed  Google Scholar 

  • Weiss MB, Abel EV, Dadpey N, Aplin AE (2014) FOXD3 modulates migration through direct transcriptional repression of TWIST1 in melanoma. Mol Cancer Res 12(9):1314–1323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wencong M, Jinghan W, Yong Y, Jianyang A, Bin L, Qingbao C, Chen L, Xiaoqing J (2020) FOXK1 promotes proliferation and metastasis of gallbladder cancer by activating AKT/mTOR signaling pathway. Front Oncol 10:545

    Article  PubMed  PubMed Central  Google Scholar 

  • Wierstra I, Alves J (2006) FOXM1c transactivates the human c-myc promoter directly via the two TATA boxes P1 and P2. Febs j 273(20):4645–4667

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Shang J, Zhan W, Liu J, Ning H, Chen N (2019) miR-425-5p promotes cell proliferation, migration and invasion by directly targeting FOXD3 in hepatocellular carcinoma cells. Mol Med Rep 20(2):1883–1892

    CAS  PubMed  Google Scholar 

  • Wu KJ, Grandori C, Amacker M, Simon-Vermot N, Polack A, Lingner J, Dalla-Favera R (1999) Direct activation of TERT transcription by c-MYC. Nat Genet 21(2):220–224

    Article  CAS  PubMed  Google Scholar 

  • Xie Y, Zhang H, Sheng W, Xiang J, Ye Z, Yang J (2008) Adenovirus-mediated ING4 expression suppresses lung carcinoma cell growth via induction of cell cycle alteration and apoptosis and inhibition of tumor invasion and angiogenesis. Cancer Lett 271(1):105–116

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Liu Y, Liu Z, Wang X, Lu X (2021) Forkhead box K1 facilitates growth of papillary thyroid carcinoma cells by regulating connective tissue growth factor expression. Hum Cell 34(2):457–467

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Chen W, Miao R, Zhou Y, Wang Z, Zhang L, Wan Y, Dong Y, Qu K, Liu C (2015) miR-34a induces cellular senescence via modulation of telomerase activity in human hepatocellular carcinoma by targeting FoxM1/c-Myc pathway. Oncotarget 6(6):3988–4004

    Article  PubMed  PubMed Central  Google Scholar 

  • Yaklichkin SY, Darnell DK, Pier MV, Antin PB, Hannenhalli S (2011) Accelerated evolution of 3’avian FOXE1 genes, and thyroid and feather specific expression of chicken FoxE1. BMC Evol Biol 11(1):1–14

    Article  Google Scholar 

  • Yan H, Li Q, Wu J, Hu W, Jiang J, Shi L, Yang X, Zhu D, Ji M, Wu C (2017) MiR-629 promotes human pancreatic cancer progression by targeting FOXO3. Cell Death Dis 8(10):e3154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang C, Zheng J, Xue Y, Yu H, Liu X, Ma J, Liu L, Wang P, Li Z, Cai H, Liu Y (2017a) The effect of MCM3AP-AS1/miR-211/KLF5/AGGF1 axis regulating glioblastoma angiogenesis. Front Mol Neurosci 10:437

    Article  PubMed  Google Scholar 

  • Yang G, Guo S, Liu HT, Yang G (2020) MiR-138-5p predicts negative prognosis and exhibits suppressive activities in hepatocellular carcinoma HCC by targeting FOXC1. Eur Rev Med Pharmacol Sci 24(17):8788–8800

    CAS  PubMed  Google Scholar 

  • Yang L, Deng WL, Zhao BG, Xu Y, Wang XW, Fang Y, Xiao HJ (2021a) FOXO3-induced lncRNA LOC554202 contributes to hepatocellular carcinoma progression via the miR-485–5p/BSG axis. Cancer Gene Ther 1:1

    Google Scholar 

  • Yang L, Peng F, Qin J, Zhou H, Wang B (2017b) Downregulation of microRNA-196a inhibits human liver cancer cell proliferation and invasion by targeting FOXO1. Oncol Rep 38(4):2148–2154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang M, Sun S, Guo Y, Qin J, Liu G (2019) Long non-coding RNA MCM3AP-AS1 promotes growth and migration through modulating FOXK1 by sponging miR-138-5p in pancreatic cancer. Mol Med 25(1):55

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang N, Wang C, Wang Z, Zona S, Lin S, Wang X, Yan M, Zheng F, Li S, Xu B (2017c) FOXM1 recruits nuclear Aurora kinase A to participate in a positive feedback loop essential for the self-renewal of breast cancer stem cells. Oncogene 36(24):3428–3440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang S, Pang L, Dai W, Wu S, Ren T, Duan Y, Zheng Y, Bi S, Zhang X, Kong J (2021b) Role of Forkhead Box O proteins in hepatocellular carcinoma biology and progression (review). Front Oncol 11:667730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu C, Wang M, Li Z, Xiao J, Peng F, Guo X, Deng Y, Jiang J, Sun C (2015) MicroRNA-138-5p regulates pancreatic cancer cell growth through targeting FOXC1. Cell Oncol (dordr) 38(3):173–181

    Article  PubMed  Google Scholar 

  • Yu Z, Lin X, Tian M, Chang W (2018) microRNA-196b promotes cell migration and invasion by targeting FOXP2 in hepatocellular carcinoma. Oncol Rep 39(2):731–738

    CAS  PubMed  Google Scholar 

  • Yuan S, Jin J, Shi J, Hou Y (2016) Inhibitor of growth-4 is a potential target for cancer therapy. Tumour Biol 37(4):4275–4279

    Article  CAS  PubMed  Google Scholar 

  • Zangouei AS, Alimardani M, Moghbeli M (2021) MicroRNAs as the critical regulators of Doxorubicin resistance in breast tumor cells. Cancer Cell Int 21(1):213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zangouei AS, Moghbeli M (2021) MicroRNAs as the critical regulators of cisplatin resistance in gastric tumor cells. Genes Environ 43(1):21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng J, Wang L, Li Q, Li W, Björkholm M, Jia J, Xu D (2009) FoxM1 is up-regulated in gastric cancer and its inhibition leads to cellular senescence, partially dependent on p27 kip1. J Pathol 218(4):419–427

    Article  CAS  PubMed  Google Scholar 

  • Zeng YB, Liang XH, Zhang GX, Jiang N, Zhang T, Huang JY, Zhang L, Zeng XC (2016) miRNA-135a promotes hepatocellular carcinoma cell migration and invasion by targeting forkhead box O1. Cancer Cell Int 16:63

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H, Huang H, Xue J, Liu M, Wang Y, Sawaya R, Xie K, Yung WK, Medema RH, He X, Huang S (2011) FoxM1 promotes beta-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell 20(4):427–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang R, Jin J, Shi J, Hou Y (2017) INGs are potential drug targets for cancer. J Cancer Res Clin Oncol 143(2):189–197

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y-L, Sun F-T, Zhang Z, Chen X-X, Liu A-X, Pan J-J, Peng F, Zhou S, Sun L-J (2015) Comprehensive expression analysis suggests functional overlapping of human FOX transcription factors in cancer. Asian Pac J Cancer Prev 15(23):10475–10481

    Article  Google Scholar 

  • Zhang Y, Huang B, Chen Z, Yang S (2020a) Knockdown of LINC00473 enhances radiosensitivity in hepatocellular carcinoma via regulating the miR-345-5p/FOXP1 axis. Onco Targets Ther 13:173–183

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Burnley P, Coder B, Su D-M (2012) Insights on FoxN1 biological significance and usages of the “nude” mouse in studies of T-lymphopoiesis. Int J Biol Sci 8(8):1156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang ZJ, Xiao Q, Li XY (2020b) MicroRNA-574-5p directly targets FOXN3 to mediate thyroid cancer progression via Wnt/beta-catenin signaling pathway. Pathol Res Pract 216(6):152939

    Article  CAS  PubMed  Google Scholar 

  • Zheng WW, Zhou J, Zhang CH, Liu XS (2016) MicroRNA-216b is downregulated in hepatocellular carcinoma and inhibits HepG2 cell growth by targeting Forkhead box protein M1. Eur Rev Med Pharmacol Sci 20(12):2541–2550

    PubMed  Google Scholar 

  • Zhou Y, Chen E, Tang Y, Mao J, Shen J, Zheng X, Xie S, Zhang S, Wu Y, Liu H, Zhi X, Ma T, Ni H, Chen J, Chai K, Chen W (2019) miR-223 overexpression inhibits doxorubicin-induced autophagy by targeting FOXO3a and reverses chemoresistance in hepatocellular carcinoma cells. Cell Death Dis 10(11):843

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Chen Y, Ding W, Hua Z, Wang L, Zhu Y, Qian H, Dai T (2018) LncRNA UCA1 impacts cell proliferation, invasion, and migration of pancreatic cancer through regulating miR-96/FOXO3. IUBMB Life 70(4):276–290

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Student Research Committee, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

    Iman Akhlaghipour & Amir Sadra Zangouei

  2. Student Research Committee, School of Medicine, Birjand University of Medical Sciences, Birjand, Iran

    Ali Fanoodi

  3. Medical Genetics Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

    Negin Taghehchian & Meysam Moghbeli

  4. Department of Medical Genetics and Molecular Medicine, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

    Ghazaleh Khalili-Tanha & Meysam Moghbeli

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IA, AF, ASZ, NT, and GKT were involved in search strategy and drafting. MM revised, structured, and edited the manuscript. All authors read and approved the final manuscript.

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Akhlaghipour, I., Fanoodi, A., Zangouei, A.S. et al. MicroRNAs as the Critical Regulators of Forkhead Box Protein Family in Pancreatic, Thyroid, and Liver Cancers. Biochem Genet 61, 1645–1674 (2023). https://doi.org/10.1007/s10528-023-10346-4

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