Abstract
microRNA are small non-coding RNA molecules which inhibit gene expression by binding mRNA, preventing its translation. As important regulators of gene expression, there is increasing interest in microRNAs as potential diagnostic biomarkers and therapeutic targets. Studies investigating the role of one of the miRNA—miR-652-3p—detail diverse roles for this miRNA in normal cell homoeostasis and disease states, including cancers, cardiovascular disease, mental health, and central nervous system diseases. Here, we review recent literature surrounding miR-652-3p, discussing its known target genes and their relevance to disease progression. These studies demonstrate that miR-652-3p targets LLGL1 and ZEB1 to modulate cell polarity mechanisms, with impacts on cancer metastasis and asymmetric cell division. Inhibition of the NOTCH ligand JAG1 by miR-652-3p can have diverse effects on angiogenesis and immune cell regulation. Investigation of miR-652-3p and other dysregulated miRNAs identified a number of pathways potentially regulated by miR-652-3p. This review demonstrates that miR-652-3p has great promise as a diagnostic or therapeutic target due to its activity across multiple cellular systems.
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Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403(6772):901–906
Ambros V (2004) The functions of animal microRNAs. Nature 431(7006):350–355
Dai R, Ahmed SA (2011) MicroRNA, a new paradigm for understanding immunoregulation, inflammation, and autoimmune diseases. Transl Res 157(4):163–179
Shi ZY, Liu B, Li YC, Liu FF, Yuan XH, Wang YQ (2019) MicroRNA-652-3p promotes the proliferation and invasion of the trophoblast HTR-8/SVneo cell line by targeting homeobox A9 to modulate the expression of ephrin receptor B4. Clin Exp Pharmacol Physiol 46(6):587–596
Wang B, Lv F, Zhao L, Yang K, Gao YS, Du MJ, Zhang YJ (2017) MicroRNA-652 inhibits proliferation and induces apoptosis of non-small cell lung cancer A549 cells. Int J Clin Exp Pathol 10(6):6719–6726
Zhu QL, Zhan DM, Chong YK, Ding L, Yang YG (2019) MiR-652-3p promotes bladder cancer migration and invasion by targeting KCNN3. Eur Rev Med Pharmacol Sci 23(20):8806–8812
Yang WH, Zhou CC, Luo M, Shi XJ, Li Y, Sun ZM, Zhou F, Chen ZL, He J (2016) MiR-652-3p is upregulated in non-small cell lung cancer and promotes proliferation and metastasis by directly targeting Lgl1. Oncotarget 7(13):16703–16715
Bonneau E, Neveu B, Kostantin E, Tsongalis GJ, De Guire V (2019) How close are miRNAs from clinical practice? A perspective on the diagnostic and therapeutic market. EJIFCC 30(2):114–127
Hanna J, Hossein GS, Kocerha J (2019) The potential for microRNA therapeutics and clinical research. Front Genet 10. https://doi.org/10.3389/fgene.2019.00478
Cummins JM, He YP, Leary RJ, Pagliarini R, Diaz LA, Sjoblom T, Barad O, Bentwich Z, Szafranska AE, Labourier E et al (2006) The colorectal microRNAome. Proc Natl Acad Sci U S A 103(10):3687–3692
Gerhard DS, Wagner L, Feingold EA, Shenmen CM, Grouse LH, Schuler G, Klein SL, Old S, Rasooly R, Good P et al (2004) The status, quality, and expansion of the NIH full-length cDNA project: the Mammalian Gene Collection (MGC). Genome Res 14(10B):2121–2127
de Rie D, Abugessaisa I, Alam T, Arner E, Arner P, Ashoor H, Astrom G, Babina M, Bertin N, Burroughs AM et al (2017) An integrated expression atlas of miRNAs and their promoters in human and mouse. Nat Biotechnol 35(9):872
Ruby JG, Jan CH, Bartel DP (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448(7149):83–86
Ramsingh G, Koboldt DC, Trissal M, Chiappinelli KB, Wylie T, Koul S, Chang LW, Nagarajan R, Fehniger TA, Goodfellow P et al (2010) Complete characterization of the microRNAome in a patient with acute myeloid leukemia. Blood 116(24):5316–5326
Ji FJ, Wu YY, An Z, Liu XS, Jiang JN, Chen FF, Fang XD (2017) Expression of both poly r(C) binding protein 1 (PCBP1) and miRNA-3978 is suppressed in peritoneal gastric cancer metastasis. Sci Rep 7. https://doi.org/10.1038/s41598-017-15448-9
Allantaz F, Cheng DT, Bergauer T, Ravindran P, Rossier MF, Ebeling M, Badi L, Reis B, Bitter H, D'Asaro M et al (2012) Expression profiling of human immune cell subsets identifies miRNA-mRNA regulatory relationships correlated with cell type specific expression. PLoS One 7(1):e29979
Meng QL, Liu F, Yang XY, Liu XM, Zhang X, Zhang C, Zhang ZD (2014) Identification of latent tuberculosis infection-related microRNAs in human U937 macrophages expressing Mycobacterium tuberculosis Hsp16.3. BMC Microbiol 14:37
Roderburg C, Mollnow T, Bongaerts B, Elfimova N, Cardenas DV, Berger K, Zimmermann H, Koch A, Vucur M, Luedde M et al (2012) Micro-RNA profiling in human serum reveals compartment-specific roles of miR-571 and miR-652 in liver cirrhosis. PLoS One 7(3). https://doi.org/10.1371/journal.pone.0032999
Xuan J, Guo SL, Huang A, Xu HB, Shao M, Yang Y, Wen W (2017) miR-29a and miR-652 attenuate liver fibrosis by inhibiting the differentiation of CD4+T cells. Cell Struct Funct 42(2):95–103
Deng SC, Li X, Niu Y, Zhu S, Jin Y, Deng SJ, Chen JY, Liu Y, He C, Yin T et al (2015) MiR-652 inhibits acidic microenvironment-induced epithelial-mesenchymal transition of pancreatic cancer cells by targeting ZEB1. Oncotarget 6(37):39661–39675
Sun XM, Dongol S, Qiu CP, Xu Y, Sun CG, Zhang ZW, Yang XS, Zhang Q, Kong BH (2018) miR-652 promotes tumor proliferation and metastasis by targeting RORA in endometrial cancer. Mol Cancer Res 16(12):1927–1939
Cheng L, Sun X, Scicluna BJ, Coleman BM, Hill AF (2014) Characterization and deep sequencing analysis of exosomal and non-exosomal miRNA in human urine. Kidney Int 86(2):433–444
Pergoli L, Cantone L, Favero C, Angelici L, Iodice S, Pinatel E, Hoxha M, Dioni L, Letizia M, Albetti B et al (2017) Extracellular vesicle-packaged miRNA release after short-term exposure to particulate matter is associated with increased coagulation. Part Fibre Toxicol 14:13
Barry SE, Ellis M, Yang YR, Guan GY, Wang XL, Britton WJ, Saunders BM (2018) Identification of a plasma microRNA profile in untreated pulmonary tuberculosis patients that is modulated by anti-mycobacterial therapy. J Inf Secur 77(4):341–348
Bruno N, ter Maaten JM, Ovchinnikova ES, Vegter EL, Valente MAE, van der Meer P, de Boer RA, van der Harst P, Schmitter D, Metra M et al (2016) MicroRNAs relate to early worsening of renal function in patients with acute heart failure. Int J Cardiol 203:564–569
Carreras-Badosa G, Bonmati A, Ortega FJ, Mercader JM, Guindo-Martinez M, Torrents D, Prats-Puig A, Martinez-Calcerrada JM, Platero-Gutierrez E, De Zegher F et al (2015) Altered circulating miRNA expression profile in pregestational and gestational obesity. J Clin Endocrinol Metab 100(11):E1446–E1456
Fernandez-Costa JM, Llamusi B, Bargiela A, Zulaica M, Alvarez-Abril MC, Perez-Alonso M, de Munain AL, Lopez-Castel A, Artero R (2016) Six serum miRNAs fail to validate as myotonic dystrophy type 1 biomarkers. PLoS One 11(2):13
Ji DB, Qiao M, Yao YF, Li M, Chen HL, Dong Q, Jia JY, Cui XX, Li ZW, Xia JH et al (2018) Serum-based microRNA signature predicts relapse and therapeutic outcome of adjuvant chemotherapy in colorectal cancer patients. Ebiomedicine 35:189–197
Sahlberg KK, Bottai G, Naume B, Burwinkel B, Calin GA, Borresen-Dale AL, Santarpia L (2015) A serum microRNA signature predicts tumor relapse and survival in triple-negative breast cancer patients. Clin Cancer Res 21(5):1207–1214
Zhou CC, Chen ZL, Dong JS, Li JG, Shi XJ, Sun N, Luo M, Zhou F, Tan FW, He J (2015) Combination of serum miRNAs with Cyfra21-1 for the diagnosis of non-small cell lung cancer. Cancer Lett 367(2):138–146
Gaedcke J, Grade M, Camps J, Sokilde R, Kaczkowski B, Schetter AJ, Difilippantonio MJ, Harris CC, Ghadimi BM, Moller S et al (2012) The rectal cancer microRNAome - microRNA expression in rectal cancer and matched normal mucosa. Clin Cancer Res 18(18):4919–4930
Matsui D, Zaidi AH, Martin SA, Omstead AN, Kosovec JE, Huleihel L, Saldin LT, DiCarlo C, Silverman JF, Hoppo T et al (2016) Primary tumor microRNA signature predicts recurrence and survival in patients with locally advanced esophageal adenocarcinoma. Oncotarget 7(49):81281–81291
Vestergaard AL, Bang-Berthelsen CH, Floyel T, Stahl JL, Christen L, Sotudeh FT, Horskjaer PD, Frederiksen KS, Kofod FG, Bruun C et al (2018) MicroRNAs and histone deacetylase inhibition-mediated protection against inflammatory beta-cell damage. PLoS One 13(9):22
Zuo ML, Wang AP, Song GL, Yang ZB (2020) miR-652 protects rats from cerebral ischemia/reperfusion oxidative stress injury by directly targeting NOX2. Biomed Pharmacother 124. https://doi.org/10.1016/j.biopha.2020.109860
Zurawek M, Dzikiewicz-Krawczyk A, Izykowska K, Ziolkowska-Suchanek I, Skowronska B, Czainska M, Podralska M, Fichna P, Przybylski G, Fichna M et al (2018) miR-487a-3p upregulated in type 1 diabetes targets CTLA4 and FOXO3. Diabetes Res Clin Pract 142:146–153
Meijer HA, Smith EM, Bushell M (2014) Regulation of miRNA strand selection: follow the leader? Biochem Soc Trans 42:1135–1140
Mensah GA, Roth GA, Fuster V (2019) The global burden of cardiovascular diseases and risk factors. J Am Coll Cardiol 74:2529–2532
Pilbrow AP, Cordeddu L, Cameron VA, Frampton CM, Troughton RW, Doughty RN, Whalley GA, Ellis CJ, Yandle TG, Richards AM et al (2014) Circulating miR-323-3p and miR-652: candidate markers for the presence and progression of acute coronary syndromes. Int J Cardiol 176(2):375–385
Ovchinnikova ES, Schmitter D, Vegter EL, ter Maaten JM, Valente MAE, Liu LCY, van der Harst P, Pinto YM, de Boer RA, Meyer S et al (2016) Signature of circulating microRNAs in patients with acute heart failure. Eur J Heart Fail 18(4):414–423
Vegter EL, Ovchinnikova ES, van Veldhuisen DJ, Jaarsma T, Berezikov E, van der Meer P, Voors AA (2017) Low circulating microRNA levels in heart failure patients are associated with atherosclerotic disease and cardiovascular-related rehospitalizations. Clin Res Cardiol 106(8):598–609
Vegter EL, Ovchinnikova ES, Sillje HHW, Meems LMG, van der Pol A, van der Velde AR, Berezikov E, Voors AA, de Boer RA, van der Meer P (2017) Rodent heart failure models do not reflect the human circulating microRNA signature in heart failure. PLoS One 12(5). https://doi.org/10.1371/journal.pone.0177242
Liu JL, Zhang HM, Li X, Wang L, Yu HN, Huang JH, Liu QJ, Wang C, Jiang AL (2020) Diagnostic and prognostic significance of aberrant miR-652-3p levels in patients with acute decompensated heart failure and acute kidney injury. J Int Med Res 48(11):1–12
Wang X, Sundquist K, Svensson PJ, Rastkhani H, Palmer K, Memon AA, Sundquist J, Zoller B (2019) Association of recurrent venous thromboembolism and circulating microRNAs. Clin Epigenetics 11. https://doi.org/10.1186/s13148-019-0627-z
Nordstrom BL, Evans MA, Murphy BR, Nutescu EA, Schein JR, Bookhart BK (2015) Risk of recurrent venous thromboembolism among deep vein thrombosis and pulmonary embolism patients treated with warfarin. Curr Med Res Opin 31(3):439–447
Wang Y, Liu CX, Wei W, Chen WL (2020) Predictive value of circulating coagulation related microRNAs expressions for major adverse cardiac and cerebral event risk in patients undergoing continuous ambulatory peritoneal dialysis: a cohort study. J Nephrol 33(1):157–165
Benjamin EJ, Muntner P, Alonso A, Bittencourt MS, Callaway CW, Carson AP, Chamberlain AM, Chang AR, Cheng S, Das SR et al (2019) Heart disease and stroke statistics-2019 update a report from the American Heart Association. Circulation 139(10):E56–E528
Raggi P, Genest J, Giles JT, Rayner KJ, Dwivedi G, Beanlands RS, Gupta M (2018) Role of inflammation in the pathogenesis of atherosclerosis and therapeutic interventions. Atherosclerosis 276:98–108
Vromman A, Ruvkun V, Shvartz E, Wojtkiewicz G, Masson GS, Tesmenitsky Y, Folco E, Gram H, Nahrendorf M, Swirski FK et al (2019) Stage-dependent differential effects of interleukin-1 isoforms on experimental atherosclerosis. Eur Heart J 40(30):2482–2491
Huang RZ, Hu ZC, Cao Y, Li HR, Zhang H, Su WH, Xu Y, Liang LW, Melgiri ND, Jiang LH (2019) MiR-652-3p inhibition enhances endothelial repair and reduces atherosclerosis by promoting Cyclin D2 expression. Ebiomedicine 40:685–694
Zhu WQ, Zhao M, Mattapally S, Chen SF, Zhang JY (2018) CCND2 overexpression enhances the regenerative potency of human induced pluripotent stem cell-derived cardiomyocytes: remuscularization of injured ventricle. Circ Res 122(1):88–96
Liang LW, Su WH, Zhou L, Cao Y, Zhou XL, Liu SQ, Zhao Y, Ding XX, Wang Q, Zhang H (2020) Statin downregulation of miR-652-3p protects dyslipidemia by promoting ISL1 expression endothelium from. Metab Clin Exp 107. https://doi.org/10.1016/j.metabol.2020.154226
Li HG, Horke S, Forstermann U (2014) Vascular oxidative stress, nitric oxide and atherosclerosis. Atherosclerosis 237(1):208–219
Huang PL, Huang ZH, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC (1995) Hypertension in mice lacking the gene for endothelial nitric-oxide synthase. Nature 377(6546):239–242
Kroll J, Waltenberger J (1998) VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem Biophys Res Commun 252(3):743–746
Bernardo BC, Nguyen SS, Winbanks CE, Gao XM, Boey EJH, Tham YK, Kiriazis H, Ooi JYY, Porrello ER, Igoor S et al (2014) Therapeutic silencing of miR-652 restores heart function and attenuates adverse remodeling in a setting of established pathological hypertrophy. FASEB J 28(12):5097–5110
Amsen D, Helbig C, Backer RA (2015) Notch in T cell differentiation: all things considered. Trends Immunol 36(12):802–814
Siebel C, Lendahl U (2017) Notch signaling in development, tissue homeostasis, and disease. Physiol Rev 97(4):1235–1294
MacGrogan D, Munch J, de la Pompa JL (2018) Notch and interacting signalling pathways in cardiac development, disease, and regeneration. Nat Rev Cardiol 15(11):685–704
Collesi C, Zentilin L, Sinagra G, Giacca M (2008) Notch1 signaling stimulates proliferation of immature cardiomyocytes. J Cell Biol 183(1):117–128
Palaga T, Ratanabunyong S, Pattarakankul T, Sangphech N, Wongchana W, Hadae Y, Kueanjinda P (2013) Notch signaling regulates expression of Mcl-1 and apoptosis in PPD-treated macrophages. Cell Mol Immunol 10(5):444–452
Tondera D, Czauderna F, Paulick K, Schwarzer R, Kaufmann J, Santel A (2005) The mitochondrial protein MTP18 contributes to mitochondrial fission in mammalian cells. J Cell Sci 118(14):3049–3059
Beg MS, Brenner AJ, Sachdev J, Borad M, Kang YK, Stoudemire J, Smith S, Bader AG, Kim S, Hong DS (2017) Phase I study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Investig New Drugs 35(2):180–188
Zhang L, Liao Y, Tang LL (2019) MicroRNA-34 family: a potential tumor suppressor and therapeutic candidate in cancer. J Exp Clin Cancer Res 38. https://doi.org/10.1186/s13046-019-1059-5
Xia ZX, Yang CY, Yang XX, Wu SD, Feng ZZ, Qu L, Chen XH, Liu LY, Ma YL (2019) miR-652 promotes proliferation and migration of uveal melanoma cells by targeting HOXA9. Med Sci Monit 25:8722–8732
Zhen C, Huang JS, Lu JB (2019) MicroRNA-652 inhibits the biological characteristics of esophageal squamous cell carcinoma by directly targeting fibroblast growth factor receptor 1. Exp Ther Med 18(6):4473–4480
Andersen M, Grauslund M, Ravn J, Sorensen JB, Andersen CB, Santoni-Rugiu E (2014) Diagnostic potential of miR-126, miR-143, miR-145, and miR-652 in malignant pleural mesothelioma. J Mol Diagn 16(4):418–430
Gao W, Shen H, Liu LX, Xu JA, Xu J, Shu YQ (2011) miR-21 overexpression in human primary squamous cell lung carcinoma is associated with poor patient prognosis. J Cancer Res Clin Oncol 137(4):557–566
Barry SE, Chan B, Ellis M, Yang YR, Plit ML, Guan GY, Wang XL, Britton WJ, Saunders BM (2015) Identification of miR-93 as a suitable miR for normalizing miRNA in plasma of tuberculosis patients. J Cell Mol Med 19(7):1606–1613
Cao F, Miao Y, Xu KD, Liu PJ (2015) Lethal (2) giant larvae: an indispensable regulator of cell polarity and cancer development. Int J Biol Sci 11(4):380–389
Krebs AM, Mitschke J, Losada ML, Schmalhofer O, Boerries M, Busch H, Boettcher M, Mougiakakos D, Reichardt W, Bronsert P et al (2017) The EMT-activator Zeb1 is a key factor for cell plasticity and promotes metastasis in pancreatic cancer. Nat Cell Biol 19(5):518–542
Aigner K, Dampier B, Descovich L, Mikula M, Sultan A, Schreiber M, Mikulits W, Brabletz T, Strand D, Obrist P et al (2007) The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 26(49):6979–6988
Russ A, Louderbough JMV, Zarnescu D, Schroeder JA (2012) Hugl1 and Hugl2 in mammary epithelial cells: polarity, proliferation, and differentiation. PLoS One 7(10). https://doi.org/10.1371/journal.pone.0047734
Stephens R, Lim K, Portela M, Kvansakul M, Humbert PO, Richardson HE (2018) The scribble cell polarity module in the regulation of cell signaling in tissue development and tumorigenesis. J Mol Biol 430(19):3585–3612
Cuk K, Zucknick M, Madhavan D, Schott S, Golatta M, Heil J, Marme F, Turchinovich A, Sinn P, Sohn C et al (2013) Plasma microrna panel for minimally invasive detection of breast cancer. PLoS One 8(10). https://doi.org/10.1371/journal.pone.0076729
Agarwal V, Bell GW, Nam JW, Bartel DP (2015) Predicting effective microRNA target sites in mammalian mRNAs. Elife 4. https://doi.org/10.7554/eLife.05005
Mangolini A, Ferracin M, Zanzi MV, Saccenti E, Ebnaof SO, Poma VV, Sanz JM, Passaro A, Pedriali M, Frassoldati A et al (2015) Diagnostic and prognostic microRNAs in the serum of breast cancer patients measured by droplet digital PCR. Biomark Res 3. https://doi.org/10.1186/s40364-015-0037-0
McDermott AM, Miller N, Wall D, Martyn LM, Ball G, Sweeney KJ, Kerin MJ (2014) Identification and validation of oncologic miRNA biomarkers for luminal A-like breast cancer. PLoS One 9(1). https://doi.org/10.1371/journal.pone.0087032
Madadi S, Schwarzenbach H, Lorenzen J, Soleimani M (2019) MicroRNA expression studies: challenge of selecting reliable reference controls for data normalization. Cell Mol Life Sci 76(18):3497–3514
Xiang MQ, Zeng Y, Yang RR, Xu HF, Chen Z, Zhong J, Xie HL, Xu YH, Zeng X (2014) U6 is not a suitable endogenous control for the quantification of circulating microRNAs. Biochem Biophys Res Commun 454(1):210–214
Arnold M, Abnet CC, Neale RE, Vignat J, Giovannucci EL, McGlynn KA, Bray F (2020) Global burden of 5 major types of gastrointestinal cancer. Gastroenterology 159(1):335–349
Schlesinger-Raab A, Werner J, Friess H, Holzel D, Engel J (2017) Age and outcome in gastrointestinal cancers: a population-based evaluation of oesophageal, gastric and colorectal cancer. Visceral Med 33(4):245–253
Zheng Q, Chen CY, Guan HY, Kang WBA, Yu CJ (2017) Prognostic role of microRNAs in human gastrointestinal cancer: a systematic review and meta-analysis. Oncotarget 8(28):46611–46623
Zhao BS, Liu SG, Wang TY, Ji YH, Qi B, Tao YP, Li HC, Wu XN (2013) Screening of microRNA in patients with esophageal cancer at same tumor node metastasis stage with different prognoses. Asian Pac J Cancer Prev 14(1):139–143
Dutt A, Ramos AH, Hammerman PS, Mermel C, Cho J, Sharifnia T, Chande A, Tanaka KE, Stransky N, Greulich H et al (2011) Inhibitor-sensitive FGFR1 amplification in human non-small cell lung cancer. PLoS One 6(6). https://doi.org/10.1371/journal.pone.0020351
Sugiura K, Ozawa S, Kitagawa Y, Ueda M, Kitajima M (2007) Co-expression of aFGF and FGFR-1 is predictive of a poor prognosis in patients with esophageal squamous cell carcinoma. Oncol Rep 17(3):557–564
Turner N, Pearson A, Sharpe R, Lambros M, Geyer F, Lopez-Garcia MA, Natrajan R, Marchio C, Iorns E, Mackay A et al (2010) FGFR1 amplification drives endocrine therapy resistance and is a therapeutic target in breast cancer. Cancer Res 70(5):2085–2094
Liu R, Zhang CN, Hu ZB, Li G, Wang C, Yang CH, Huang DZ, Chen X, Zhang HY, Zhuang R et al (2011) A five-microRNA signature identified from genome-wide serum microRNA expression profiling serves as a fingerprint for gastric cancer diagnosis. Eur J Cancer 47(5):784–791
Shin VY, Ng EKO, Chan VW, Kwong A, Chu KM (2015) A three-miRNA signature as promising non-invasive diagnostic marker for gastric cancer. Mol Cancer 14. https://doi.org/10.1186/s12943-015-0473-3
Hedayat S, Lampis A, Vlachogiannis G, Khan K, Cunningham D, Marchetti S, Fassan M, Begum R, Schirripa M, Loupakis F et al (2019) Circulating miR-652-3p as a biomarker of drug resistance in metastatic colorectal cancer patients. Paper presented at the Conference on Molecular Analysis for Personalised Therapy (MAP), London, 7-9 Nov 2019
Kanaan Z, Roberts H, Eichenberger MR, Billeter A, Ocheretner G, Pan JM, Rai SN, Jorden J, Williford A, Galandiuk S (2013) A plasma microRNA panel for detection of colorectal adenomas a step toward more precise screening for colorectal cancer. Ann Surg 258(3):400–408
Xu M, Kuang Y, Wang M, Han X, Yang Q (2017) A microRNA expression signature as a predictor of survival for colon adenocarcinoma. Neoplasma 64(1):56–64
Wing-Lun E, Eaton SA, Hur SSJ, Aiken A, Young PE, Buckland ME, Li CCY, Cropley JE, Suter CM (2016) Nutrition has a pervasive impact on cardiac microRNA expression in isogenic mice. Epigenetics 11(7):475–481
Dluzen DF, Hooten NN, Zhang YQ, Kim Y, Glover FE, Tajuddin SM, Jacob KD, Zonderman AB, Evans MK (2016) Racial differences in microRNA and gene expression in hypertensive women. Sci Rep 6. https://doi.org/10.1038/srep35815
Urquidi V, Netherton M, Gomes-Giacoia E, Serie DJ, Eckel-Passow J, Rosser CJ, Goodison S (2016) A microRNA biomarker panel for the non-invasive detection of bladder cancer. Oncotarget 7(52):86290–86299
Liu X, Wei LW, Zhao BB, Cai XX, Dong CH, Yin FQ (2018) Low expression of KCNN3 may affect drug resistance in ovarian cancer. Mol Med Rep 18(2):1377–1386
Potier M, Joulin V, Roger S, Besson P, Jourdan ML, LeGuennec JY, Bougnoux P, Vandier C (2006) Identification of SK3 channel as a new mediator of breast cancer cell migration. Mol Cancer Ther 5(11):2946–2953
Steinestel K, Eder S, Ehinger K, Schneider J, Genze F, Winkler E, Wardelmann E, Schrader AJ, Steinestel J (2016) The small conductance calcium-activated potassium channel 3 (SK3) is a molecular target for edelfosine to reduce the invasive potential of urothelial carcinoma cells. Tumor Biol 37(5):6275–6283
Chantome A, Girault A, Potier M, Collin C, Vaudin P, Pages JC, Vandier C, Joulin V (2009) KCa2.3 channel-dependent hyperpolarization increases melanoma cell motility. Exp Cell Res 315(20):3620–3630
Li JC, Zou XM (2019) MiR-652 serves as a prognostic biomarker in gastric cancer and promotes tumor proliferation, migration, and invasion via targeting RORA. Cancer Biomarkers 26(3):323–331
Kim H, Lee JM, Lee G, Bhin J, Oh SK, Kim K, Pyo KE, Lee JS, Yim HY, Kim KI et al (2011) DNA damage-induced ROR alpha is crucial for p53 stabilization and increased apoptosis. Mol Cell 44(5):797–810
McAvoy S, Ganapathiraju SC, Ducharme-Smith AL, Pritchett JR, Kosari F, Perez DS, Zhu Y, James CD, Smith DI (2007) Non-random inactivation of large common fragile site genes in different cancers. Cytogenet Genome Res 118(2-4):260–269
Wang YJ, Solt LA, Kojetin DJ, Burris TP (2012) Regulation of p53 stability and apoptosis by a ROR agonist. PLoS One 7(4). https://doi.org/10.1371/journal.pone.0034921
Liu Y, Ding W, Ge H, Ponnusamy M, Wang Q, Hao XD, Wu W, Zhang Y, Yu WP, Ao X et al (2019) FOXK transcription factors: regulation and critical role in cancer. Cancer Lett 458:1–12
Faber J, Krivtsov AV, Stubbs MC, Wright R, Davis TN, van den Heuvel-Eibrink M, Zwaan CM, Kung AL, Armstrong SA (2009) HOXA9 is required for survival in human MLL-rearranged acute leukemias. Blood 113(11):2375–2385
Hwang JA, Lee BB, Kim Y, Hong SH, Kim YH, Han J, Shim YM, Yoon CY, Lee YS, Kim DH (2015) HOXA9 inhibits migration of lung cancer cells and its hypermethylation is associated with recurrence in non-small cell lung cancer. Mol Carcinog 54:E72–E80
Ramos-Mejia V, Navarro-Montero O, Ayllon V, Bueno C, Romero T, Real PJ, Menendez P (2014) HOXA9 promotes hematopoietic commitment of human embryonic stem cells. Blood 124(20):3065–3075
Lulla RR, Costa FF, Bischof JM, Chou PM, Bonaldo MF, Vanin EF, Soares MB (2011) Identification of differentially expressed microRNAs in osteosarcoma. Sarcoma 2011:732690
Jin YP, Yang L, Li X (2020) MicroRNA-652 promotes cell proliferation and osteosarcoma invasion by directly targeting KLF9. Exp Ther Med 20(4):2953–2960
Li Y, Sun Q, Jiang MC, Li S, Zhang JY, Xu ZQ, Guo DY, Gu TN, Wang BY, Xiao L et al (2019) KLF9 suppresses gastric cancer cell invasion and metastasis through transcriptional inhibition of MMP28. FASEB J 33(7):7915–7928
Simmen FA, Su Y, Xiao RJ, Zeng ZY, Simmen RCM (2008) The Kruppel-like factor 9 (KLF9) network in HEC-1-A endometrial carcinoma cells suggests the carcinogenic potential of dys-regulated KLF9 expression. Reprod Biol Endocrinol 6. https://doi.org/10.1186/1477-7827-6-41
Gaudet AD, Fonken LK, Watkins LR, Nelson RJ, Popovich PG (2018) MicroRNAs: roles in regulating neuroinflammation. Neuroscientist 24(3):221–245
Im HI, Kenny PJ (2012) MicroRNAs in neuronal function and dysfunction. Trends Neurosci 35(5):325–334
Issler O, Chen A (2015) Determining the role of microRNAs in psychiatric disorders. Nat Rev Neurosci 16(4):201–212
Santarelli DM, Beveridge NJ, Tooney PA, Cairns MJ (2011) Upregulation of dicer and microRNA expression in the dorsolateral prefrontal cortex Brodmann area 46 in schizophrenia. Biol Psychiatry 69(2):180–187
Lewohl JM, Nunez YO, Dodd PR, Tiwari GR, Harris RA, Mayfield RD (2011) Up-regulation of microRNAs in brain of human alcoholics. Alcohol Clin Exp Res 35(11):1928–1937
Lai CY, Yu SL, Hsieh MH, Chen CH, Chen HY, Wen CC, Huang YH, Hsiao PC, Hsiao CK et al (2011) MicroRNA expression aberration as potential peripheral blood biomarkers for schizophrenia. PLoS One 6(6). https://doi.org/10.1371/journal.pone.0021635
Lai CY, Lee SY, Scarr E, Yu YH, Lin YT, Liu CM, Hwang TJ, Hsieh MH, Liu CC, Chien YL et al (2016) Aberrant expression of microRNAs as biomarker for schizophrenia: from acute state to partial remission, and from peripheral blood to cortical tissue. Transl Psychiatry 6:7
Lee M, Cho H, Jung SH, Yim SH, Cho SM, Chun JW, Paik SH, Park YE, Cheon DH, Lee JE et al (2018) Circulating microRNA expression levels associated with Internet gaming disorder. Front Psychiatry 9. https://doi.org/10.3389/fpsyt.2018.00081
Walker RM, Rybka J, Anderson SM, Torrance HS, Boxall R, Sussmann JE, Porteous DJ, McIntosh AM, Evans KL (2015) Preliminary investigation of miRNA expression in individuals at high familial risk of bipolar disorder. J Psychiatr Res 62:48–55
Schür RR, Draisma LWR, Wijnen JP, Boks MP, Koevoets M, Joels M, Klomp DW, Kahn RS, Vinkers CH (2016) Brain GABA levels across psychiatric disorders: a systematic literature review and meta-analysis of H-1-MRS studies. Hum Brain Mapp 37(9):3337–3352
Gladkevich A, Kauffman HF, Korf J (2004) Lymphocytes as a neural probe: potential for studying psychiatric disorders. Prog Neuro-Psychopharmacol Biol Psychiatry 28(3):559–576
Lindqvist D, Epel ES, Mellon SH, Penninx BW, Revesz D, Verhoeven JE, Reus VI, Lin J, Mahan L, Hough CM et al (2015) Psychiatric disorders and leukocyte telomere length: underlying mechanisms linking mental illness with cellular aging. Neurosci Biobehav Rev 55:333–364
Nuzziello N, Vilardo L, Pelucchi P, Consiglio A, Liuni S, Trojano M, Liguori M (2018) Investigating the role of microRNA and transcription factor co-regulatory networks in multiple sclerosis pathogenesis. Int J Mol Sci 19(11). https://doi.org/10.3390/ijms19113652
Bach TL, Kerr WT, Wang YF, Bauman EM, Kine P, Whiteman EL, Morgan RS, Williamson EK, Ostap EM, Burkhardt JK et al (2007) PI3K regulates pleckstrin-2 in T-cell cytoskeletal reorganization. Blood 109(3):1147–1155
Wu DM, Deng SH, Zhou J, Han R, Liu T, Zhang T, Li J, Chen JP, Xu Y (2020) PLEK2 mediates metastasis and vascular invasion via the ubiquitin-dependent degradation of SHIP2 in non-small cell lung cancer. Int J Cancer 146(9):2563–2575
Grube S, Gerchen MF, Adamcio B, Pardo LA, Martin S, Malzahn D, Papiol S, Begemann M, Ribbe K, Friedrichs H et al (2011) A CAG repeat polymorphism of KCNN3 predicts SK3 channel function and cognitive performance in schizophrenia. Embo Mol Med 3(6):309–319
Smolin B, Karry R, Gal-Ben-Ari S, Ben-Shachar D (2012) Differential expression of genes encoding neuronal ion-channel subunits in major depression, bipolar disorder and schizophrenia: implications for pathophysiology. Int J Neuropsychopharmacol 15(7):869–882
Kimura T, Takahashi MP, Okuda Y, Kaido M, Fujimura H, Yanagihara T, Sakoda S (2000) The expression of ion channel mRNAs in skeletal muscles from patients with myotonic muscular dystrophy. Neurosci Lett 295(3):93–96
Dahlman I, Belarbi Y, Laurencikiene J, Pettersson AM, Arner P, Kulyte A (2017) Comprehensive functional screening of miRNAs involved in fat cell insulin sensitivity among women. Am J Physiol Endocrinol Metab 312(6):E482–E494
Meyre D, Bouatia-Naji N, Tounian A, Samson C, Lecoeur C, Vatin V, Ghoussaini M, Wachter C, Hercberg S, Charpentier G et al (2005) Variants of ENPP1 are associated with childhood and adult obesity and increase the risk of glucose intolerance and type 2 diabetes. Nat Genet 37(8):863–867
Roberts F, Zhu DX, Farquharson C, Macrae VE (2019) ENPP1 in the regulation of mineralization and beyond. Trends Biochem Sci 44(7):616–628
Shi YF, Feng Y, Kang JH, Liu C, Li ZX, Li DS, Cao W, Qiu J, Guo ZL, Bi EG et al (2007) Critical regulation of CD4(+) T cell survival and autoimmunity by beta-arrestin 1. Nat Immunol 8(8):817–824
Wang YY, Tang YW, Teng L, Wu YL, Zhao XH, Pei G (2006) Association of beta-arrestin and TRAF6 negatively regulates Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 7(2):139–147
Buchanan FG, Gorden DL, Matta P, Shi Q, Matrisian LM, DuBois RN (2006) Role of beta-arrestin 1 in the metastatic progression of colorectal cancer. Proc Natl Acad Sci U S A 103(5):1492–1497
Kapoor N, Narayana Y, Patil SA, Balaji KN (2010) Nitric oxide is involved in Mycobacterium bovis bacillus Calmette-Guerin-activated Jagged1 and Notch1 signaling. J Immunol 184(6):3117–3126
Yuan XY, Berg N, Lee JW, Le TT, Neudecker V, Jing N, Eltzschig H (2018) MicroRNA miR-223 as regulator of innate immunity. J Leukoc Biol 104(3):515–524
Gao YL, Lin L, Li T, Yang JR, Wei YB (2017) The role of miRNA-223 in cancer: function, diagnosis and therapy. Gene 616:1–7
Zhi Y, Pan JH, Shen WH, He P, Zheng J, Zhou XZ, Lu GS, Chen ZW, Zhou ZS (2016) Ginkgolide B inhibits human bladder cancer cell migration and invasion through microRNA-223-3p. Cell Physiol Biochem 39(5):1787–1794
Akao Y, Nakagawa Y, Kitade Y, Kinoshita T, Naoe T (2007) Downregulation of microRNAs-143 and-145 in B-cell malignancies. Cancer Sci 98(12):1914–1920
Clape C, Fritz V, Henriquet C, Apparailly F, Fernandez PL, Iborra F, Avances C, Villalba M, Culine S, Fajas L (2009) miR-143 interferes with ERK5 signaling, and abrogates prostate cancer progression in mice. PLoS One 4 (10). https://doi.org/10.1371/journal.pone.0007542
Boucher JM, Peterson SM, Urs S, Zhang CX, Liaw L (2011) The miR-143/145 cluster is a novel transcriptional target of Jagged-1/Notch signaling in vascular smooth muscle cells. J Biol Chem 286(32):28312–28321
Shen KX, Cao Z, Zhu RZ, You L, Zhang TP (2019) The dual functional role of MicroRNA-18a (miR-18a) in cancer development. Clin Transl Med 8(1). https://doi.org/10.1186/s40169-019-0250-9
Xu XX, Zhu S, Tao ZW, Ye SL (2018) High circulating miR-18a, miR-20a, and miR-92a expression correlates with poor prognosis in patients with non-small cell lung cancer. Cancer Med 7(1):21–31
Jiang Y, Zhou JP, Zhao JS, Hou DQ, Zhang HY, Li L, Zou D, Hu JF, Zhang Y, Jing ZT (2020) MiR-18a-downregulated RORA inhibits the proliferation and tumorigenesis of glioma using the TNF-alpha-mediated NF-kappa B signaling pathway. Ebiomedicine 52. https://doi.org/10.1016/j.ebiom.2020.102651
Chen L, Xiao H, Wang ZH, Huang Y, Liu ZP, Ren H, Song H (2014) miR-29a suppresses growth and invasion of gastric cancer cells in vitro by targeting VEGF-A. BMB Rep 47(1):39–44
Sun XJ, Wei L, Chen Q, Terek RM (2015) MicroRNA regulates vascular endothelial growth factor expression in chondrosarcoma cells. Clin Orthop Relat Res 473(3):907–913
Takahashi Y, Forrest ARR, Maeno E, Hashimoto T, Daub CO, Yasuda J (2009) miR-107 and miR-185 can induce cell cycle arrest in human non small cell lung cancer cell lines. PLoS One 4 (8). https://doi.org/10.1371/journal.pone.0006677
Chen L, Chen XR, Chen FF, Liu Y, Li P, Zhang R, Yan K, Yi YJ, Xu ZM, Jiang XD (2013) MicroRNA-107 inhibits U87 glioma stem cells growth and invasion. Cell Mol Neurobiol 33(5):651–657
Xue XC, Cao AT, Cao XC, Yao SX, Carlsen ED, Soong L, Liu CG, Liu XP, Liu ZJ, Duck LW et al (2014) Downregulation of microRNA-107 in intestinal CD11c(+) myeloid cells in response to microbiota and proinflammatory cytokines increases IL-23p19 expression. Eur J Immunol 44(3):673–682
Hennessy EJ, Sheedy FJ, Santamaria D, Barbacid M, O’Neill LAJ (2011) Toll-like receptor-4 (TLR4) down-regulates microRNA-107, increasing macrophage adhesion via cyclin-dependent kinase 6. J Biol Chem 286(29):25531–25539
Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420(6915):520–562
Perlman RL (2016) Mouse models of human disease an evolutionary perspective. Evol Med Public Health 2016(1):170–176
Kozomara A, Birgaoanu M, Griffiths-Jones S (2019) miRBase: from microRNA sequences to function. Nucleic Acids Res 47(D1):D155–D162
Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233
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MS was a recipient of a UTS Research Excellence Scholarship.
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Stevens, M.T., Saunders, B.M. Targets and regulation of microRNA-652-3p in homoeostasis and disease. J Mol Med 99, 755–769 (2021). https://doi.org/10.1007/s00109-021-02060-8
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DOI: https://doi.org/10.1007/s00109-021-02060-8