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Could Micrornas Be Useful Tools to Improve the Diagnosis and Treatment of Rare Gynecological Cancers? a Brief Overview

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Could Micrornas Be Useful Tools to Improve the Diagnosis and Treatment of Rare Gynecological Cancers? a Brief Overview International Journal of Molecular Sciences Review Could MicroRNAs Be Useful Tools to Improve the Diagnosis and Treatment of Rare Gynecological Cancers? A Brief Overview Riccardo Di Fiore 1,2,* , Sherif Suleiman 1, Francesca Pentimalli 3 , Sharon A. O’Toole 4 , John J. O’Leary 5, Mark P. Ward 5, Neil T. Conlon 6 , Maja Sabol 7 , Petar Ozreti´c 7 , Ayse Elif Erson-Bensan 8 , Nicholas Reed 9, Antonio Giordano 2,10, C. Simon Herrington 11 and Jean Calleja-Agius 1,* 1 Department of Anatomy, Faculty of Medicine and Surgery, University of Malta, MSD 2080 Msida, Malta; [email protected] 2 Center for Biotechnology, Sbarro Institute for Cancer Research and Molecular Medicine, College of Science and Technology, Temple University, Philadelphia, PA 19122, USA; [email protected] 3 Cell Biology and Biotherapy Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. Pascale, I-80131 Napoli, Italy; [email protected] 4 Departments of Obstetrics and Gynaecology and Histopathology, Trinity St James’s Cancer Institute, Trinity College Dublin, 8 Dublin, Ireland; [email protected] 5 Department of Histopathology, Trinity St James’s Cancer Institute, Trinity College Dublin, 8 Dublin, Ireland; [email protected] (J.J.O.); [email protected] (M.P.W.) 6 National Institute for Cellular Biotechnology, Dublin City University, Glasnevin, 9 Dublin, Ireland; [email protected] 7 Laboratory for Hereditary Cancer, Division of Molecular Medicine, Ruder¯ Boškovi´cInstitute, 10000 Zagreb, Croatia; [email protected] (M.S.); [email protected] (P.O.) Citation: Di Fiore, R.; Suleiman, S.; 8 Department of Biological Sciences, Middle East Technical University, Ankara 06810, Turkey; Pentimalli, F.; O’Toole, S.A.; O’Leary, [email protected] J.J.; Ward, M.P.; Conlon, N.T.; Sabol, 9 Beatson Oncology Centre, Gartnavel General Hospital, 1053 Great Western Road, Glasgow G12 0YN, UK; M.; Ozreti´c,P.; Erson-Bensan, A.E.; [email protected] 10 et al. Could MicroRNAs Be Useful Department of Medical Biotechnologies, University of Siena, 53100 Siena, Italy 11 Tools to Improve the Diagnosis and Cancer Research UK Edinburgh Centre, Western General Hospital, University of Edinburgh, Treatment of Rare Gynecological Crewe Road South, Edinburgh EH4 2XR, UK; [email protected] * Correspondence: riccardo.difi[email protected] (R.D.F.); [email protected] (J.C.-A.); Cancers? A Brief Overview. Int. J. Tel.: +356-2340-3871 (R.D.F.); +356-2340-1892 (J.C.-A.) Mol. Sci. 2021, 22, 3822. https:// doi.org/10.3390/ijms22083822 Abstract: Gynecological cancers pose an important public health issue, with a high incidence among Academic Editor: Miguel Hueso women of all ages. Gynecological cancers such as malignant germ-cell tumors, sex-cord-stromal tumors, uterine sarcomas and carcinosarcomas, gestational trophoblastic neoplasia, vulvar carci- Received: 17 March 2021 noma and melanoma of the female genital tract, are defined as rare with an annual incidence of Accepted: 5 April 2021 <6 per 100,000 women. Rare gynecological cancers (RGCs) are associated with poor prognosis, and Published: 7 April 2021 given the low incidence of each entity, there is the risk of delayed diagnosis due to clinical inexperi- ence and limited therapeutic options. There has been a growing interest in the field of microRNAs Publisher’s Note: MDPI stays neutral (miRNAs), a class of small non-coding RNAs of ∼22 nucleotides in length, because of their potential with regard to jurisdictional claims in to regulate diverse biological processes. miRNAs usually induce mRNA degradation and transla- published maps and institutional affil- tional repression by interacting with the 30 untranslated region (30-UTR) of target mRNAs, as well as iations. other regions and gene promoters, as well as activating translation or regulating transcription under certain conditions. Recent research has revealed the enormous promise of miRNAs for improving the diagnosis, therapy and prognosis of all major gynecological cancers. However, to date, only a few studies have been performed on RGCs. In this review, we summarize the data currently available Copyright: © 2021 by the authors. regarding RGCs. Licensee MDPI, Basel, Switzerland. This article is an open access article Keywords: rare gynecological cancers; microRNAs; miRNAs; cancer stem cells; circulating biomark- distributed under the terms and ers; extracellular vesicles; microRNA-based therapy conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Int. J. Mol. Sci. 2021, 22, 3822. https://doi.org/10.3390/ijms22083822 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 3822 2 of 26 1. Introduction Gynecological cancers are cancers that arise in the female reproductive organs, en- compassing ovarian, fallopian tubal, uterine/endometrial, cervical, vaginal and vulval cancers, and gestational trophoblastic disease [1]. Each gynecological cancer has its own signs, symptoms and risk factors. Gynecological cancers pose an important public health issue, with a high incidence among women of all ages [2]. Patients are often diagnosed at a late stage. This could be due to several reasons including lack of awareness of specific differential symptoms, improper screening and even misdiagnosis [3]. Late diagnosis, combined with limited treatment options for advanced gynecological cancers are major contributing factors to the high mortality, thus emphasizing the need for further advance- ment in the area. These issues are further exacerbated in the case of rare gynecological cancers (RGCs) [4]. Many gynecological cancers, for example malignant germ-cell tumors, sex cord- stromal tumors, gestational trophoblastic neoplasia, vaginal/vulvar carcinoma, and melanoma of the female genital tract, are uncommon and have different clinicopatho- logical characteristics, thus implicating diverse molecular biological pathogeneses. These tumors are defined as “rare”, with an annual incidence of <6 per 100,000 women and cumu- latively account for over 50% of gynecological cancers [5–8]. RGCs are generally associated with poor prognosis. Since these cancers are rare, patient management becomes difficult in terms of correct diagnosis and limited therapy options, and given the low incidence of each disease, this poses a major hurdle in the management of patients. The field of miRNAs has been increasingly investigated because of their potential role in the regulation of different biological processes [9]. miRNAs are a class of non-coding RNAs that are approximately 20–22 nucleotides in length, and are involved in the regulation of gene expression. Usually, miRNAs induce mRNA degradation and/or translational repression by interacting with the 30 untranslated region (30-UTR) of target mRNAs. There are few cases of miRNAs interacting with different regions on genes including promoters. They have also been reported to be involved in the or activation of and regulation of gene transcription [10]. According to the latest miRbase [11], 38,589 hairpin precursors and 48,860 mature miRNAs have been reported for nearly 300 organisms. For the human genome, the current numbers are 1917 annotated hairpin precursors, and 2654 mature sequences [11]. Given the rate of discovery of new miRNAs, it is predicted that, in fact, miRNAs may regulate the expression of almost one-third of all human genes [12]. Recent research has revealed the enormous promise for miRNAs to improve the diagnosis, and management of all major gynecological cancers (cervical, endometrial and ovarian cancers) [1]. This is backed up by research on miRNAs in other cancers such as thyroid, breast and gastric cancer [13–15]. Numerous miRNAs are believed to influence multiple biological functions, leading to modulation of the tumor microenvironment, including stemness, growth, proliferation, invasion and metastasis [1]. In addition, miRNA signatures have been proposed as potential biomarkers that can be used for early detection of gynecological cancers, as well as predictors of response to ongoing therapies [1]. Based on the available and emerging data, miRNAs could impact future therapeutic strategies for ovarian, cervical, and endometrial carcinomas. Almost 15 years have passed since the first publication on the aberrant expression of miRNAs in human epithelial ovarian cancer [16]. However, to date, only a few studies have been performed on RGCs. In this review, we summarize the data currently available, in order to assess the progress made to date. 2. Biogenesis and Function of miRNAs In the search for novel diagnostic and therapeutic targets for cancer, miRNAs have become of significant interest, particularly because of their abundance and potential ease of detection in both tissue and plasma, and therefore they represent potential non-invasive molecular markers for cancer diagnosis and therapeutic response. miRNA biogenesis is a multi-step process that starts in the nucleus (Figure1)[ 17–20]. Here, miRNAs are Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 3 of 26 Int. J. Mol. Sci. 2021, 22, 3822 of detection in both tissue and plasma, and therefore they represent potential non-3inva- of 26 sive molecular markers for cancer diagnosis and therapeutic response. miRNA biogenesis is a multi-step process that starts in the nucleus (Figure 1) [17–20]. Here, miRNAs are gen- erallygenerally transcribed transcribed by RNA by RNA Polymerase Polymerase II into II intolong long primary primary transcripts transcripts (pri-miRNA) (pri-miRNA) that arethat further are further processed processed in the
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