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Role of MicroRNAs in Cancer Development and Treatment

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Oncology".

Deadline for manuscript submissions: closed (30 September 2022) | Viewed by 30912

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Dr. Nikolay Mehterov

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Department of Medical Biology, Medical University-Plovdiv, 4002 Plovdiv, Bulgaria
Interests: identification of cancer-related miRNAs and their targets; role of ncRNA in molecular oncology; personalized medicine; non-coding RNAs; transcriptomics; cancer pathobiology; head and neck cancer; colorectal cancer
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Dear Colleagues,

MicroRNAs (miRNAs) represent a prominent part of the non-coding landscape of the human genome. Their role is performed on post-transcriptional level and is accomplished by base pairing with the 3’-UTR of target messenger RNAs (mRNAs). As a consequence, mRNA degradation or translational inhibition occurs, which finally leads to the absence of a protein product. Being part of the human non-coding transcriptome, miRNAs reside in regions which frequently undergo alterations in malignancies. As a consequence, specific deregulation of miRNAs that control genes involved in the cell cycle, senescence and apoptosis is observed in all human cancers. Therefore, the specific expression profile of miRNA in different cancers, together with their stability and easy detection, provides excellent biomarker properties of miRNAs that can be used for diagnosis, staging, and may have wide clinical application.

This Special Issue focuses on the information of the readers regarding the potential of miRNAs to regulate protein-coding gene expression at a post-transcriptional level in cancer development and treatment. The authors are encouraged to submit their original research studies concerning this topic. Review articles will also be taken into consideration. We hope that this Special Issue regarding the identity, biological role, and/or clinical utility of miRNAs will arouse the interest of the readers of this journal.

Dr. Nikolay Mehterov
Guest Editor

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Keywords

microRNAs (miRNAs)
transcriptomics
functional studies
cancer pathobiology
solid tumors
hematological malignancies
molecular biomarkers
therapeutic targets
apoptosis
anticancer drugs
radiotherapy and chemotharapy failure

Published Papers (12 papers)

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Editorial

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4 pages, 201 KiB

Open AccessEditorial

Role of MicroRNAs in Cancer Development and Treatment

by Nikolay Mehterov

Int. J. Mol. Sci. 2023, 24(13), 11058; https://doi.org/10.3390/ijms241311058 - 04 Jul 2023

Cited by 2 | Viewed by 665

Abstract

MicroRNAs (miRNAs) represent a prominent part of the non-coding landscape of the human genome [...] Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

Research

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13 pages, 1460 KiB

Open AccessArticle

Associations of miR-181a with Health-Related Quality of Life, Cognitive Functioning, and Clinical Data of Patients with Different Grade Glioma Tumors

by Indre Valiulyte, Aiste Pranckeviciene, Adomas Bunevicius, Arimantas Tamasauskas, Hanna Svitina, Inessa Skrypkina and Paulina Vaitkiene

Int. J. Mol. Sci. 2022, 23(19), 11149; https://doi.org/10.3390/ijms231911149 - 22 Sep 2022

Cited by 2 | Viewed by 1355

Abstract

Gliomas are central nervous system tumors with a lethal prognosis. Small micro-RNA molecules participate in various biological processes, are tissue-specific, and, therefore, could be promising targets for cancer treatment. Thus, this study aims to examine miR-181a as a potent biomarker for the diagnosis and prognosis of glioma patients and, for the first time, to find associations between the expression level of miR-181a and patient quality of life (QoL) and cognitive functioning. The expression level of miR-181a was analyzed in 78 post-operative II-IV grade gliomas by quantitative real-time polymerase chain reaction. The expression profile was compared with patient clinical data (age, survival time after the operation, tumor grade and location, mutation status of isocitrate dehydrogenase 1 (IDH1), and promoter methylation of O-6-methylguanine methyltransferase). Furthermore, the health-related QoL was assessed using the Karnofsky performance scale and the quality of life questionnaires; while cognitive assessment was assessed by the Hopkins verbal learning test-revised, trail-making test, and phonemic fluency tasks. The expression of miR-181a was significantly lower in tumors of grade III and IV and was associated with IDH1 wild-type gliomas and a worse prognosis of patient overall survival. Additionally, a positive correlation was observed between miR-181a levels and functional status and QoL of glioma patients. Therefore, miR-181a is a unique molecule that plays an important role in gliomagenesis, and is also associated with changes in patients’ quality of life. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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22 pages, 2848 KiB

Open AccessArticle

The Profile of MicroRNA Expression and Potential Role in the Regulation of Drug-Resistant Genes in Doxorubicin and Topotecan Resistant Ovarian Cancer Cell Lines

by Piotr Stasiak, Dominika Kaźmierczak, Karol Jopek, Michał Nowicki, Marcin Rucinski and Radosław Januchowski

Int. J. Mol. Sci. 2022, 23(10), 5846; https://doi.org/10.3390/ijms23105846 - 23 May 2022

Cited by 5 | Viewed by 2278

Abstract

Epithelial ovarian cancer has the highest mortality among all gynecological malignancies. The main reasons for high mortality are late diagnosis and development of resistance to chemotherapy. Resistance to chemotherapeutic drugs can result from altered expression of drug-resistance genes regulated by miRNA. The main goal of our study was to detect differences in miRNA expression levels in two doxorubicin (DOX)- and two topotecan (TOP)-resistant variants of the A2780 drug-sensitive ovarian cancer cell line by miRNA microarray. The next aim was to recognize miRNAs as factors responsible for the regulation of drug-resistance genes. We observed altered expression of 28 miRNA that may be related to drug resistance. The upregulation of miR-125b-5p and miR-935 and downregulation of miR-218-5p was observed in both DOX-resistant cell lines. In both TOP-resistant cell lines, we noted the overexpression of miR-99a-5p, miR-100-5p, miR-125b-5p, and miR-125b-2-3p and decreased expression of miR-551b-3p, miR-551b-5p, and miR-383-5p. Analysis of the targets suggested that expression of important drug-resistant genes such as the collagen type I alpha 2 chain (COL1A2), protein Tyrosine Phosphatase Receptor Type K (PTPRK), receptor tyrosine kinase—EPHA7, Roundabout Guidance Receptor 2 (ROBO2), myristoylated alanine-rich C-kinase substrate (MARCK), and the ATP-binding cassette subfamily G member 2 (ABCG2) can be regulated by miRNA. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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20 pages, 2488 KiB

Open AccessArticle

Cellular and Molecular Profiling of Tumor Microenvironment and Early-Stage Lung Cancer

by Radu Pirlog, Paul Chiroi, Ioana Rusu, Ancuta Maria Jurj, Liviuta Budisan, Cecilia Pop-Bica, Cornelia Braicu, Doinita Crisan, Jean-Christophe Sabourin and Ioana Berindan-Neagoe

Int. J. Mol. Sci. 2022, 23(10), 5346; https://doi.org/10.3390/ijms23105346 - 11 May 2022

Cited by 12 | Viewed by 2743

Abstract

Lung cancers are broadly divided into two categories: non-small-cell lung carcinoma (NSCLC), which accounts for 80–85% of all cancer cases, and small-cell lung carcinoma (SCLC), which covers the remaining 10–15%. Recent advances in cancer biology and genomics research have allowed an in-depth characterization of lung cancers that have revealed new therapy targets (EGFR, ALK, ROS, and KRAS mutations) and have the potential of revealing even more biomarkers for diagnostic, prognostic, and targeted therapies. A new source of biomarkers is represented by non-coding RNAs, especially microRNAs (miRNAs). MiRNAs are short non-coding RNA sequences that have essential regulatory roles in multiple cancers. Therefore, we aim to investigate the tumor microenvironment (TME) and miRNA tumor profile in a subset of 51 early-stage lung cancer samples (T1 and T2) to better understand early tumor and TME organization and molecular dysregulation. We analyzed the immunohistochemistry expression of CD4 and CD8 as markers of the main TME immune populations, E-cadherin to evaluate early-stage epithelial-to-mesenchymal transition (EMT), and p53, the main altered tumor suppressor gene in lung cancer. Starting from these 4 markers, we identified and validated 4 miRNAs that target TP53 and regulate EMT that can be further investigated as potential early-stage lung cancer biomarkers. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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22 pages, 34881 KiB

Open AccessArticle

Aberrant Methylation of 20 miRNA Genes Specifically Involved in Various Steps of Ovarian Carcinoma Spread: From Primary Tumors to Peritoneal Macroscopic Metastases

by Vitaly I. Loginov, Irina V. Pronina, Elena A. Filippova, Alexey M. Burdennyy, Svetlana S. Lukina, Tatiana P. Kazubskaya, Leonid A. Uroshlev, Marina V. Fridman, Olga I. Brovkina, Natalya V. Apanovich, Alexander V. Karpukhin, Ivan S. Stilidi, Nikolay E. Kushlinskii, Alexey A. Dmitriev and Eleonora A. Braga

Int. J. Mol. Sci. 2022, 23(3), 1300; https://doi.org/10.3390/ijms23031300 - 24 Jan 2022

Cited by 15 | Viewed by 2666

Abstract

Our work aimed to differentiate 20 aberrantly methylated miRNA genes that participate at different stages of development and metastasis of ovarian carcinoma (OvCa) using methylation-specific qPCR in a representative set of clinical samples: 102 primary tumors without and with metastases (to lymph nodes, peritoneum, or distant organs) and 30 peritoneal macroscopic metastases (PMM). Thirteen miRNA genes (MIR107, MIR124-2, MIR124-3, MIR125B-1, MIR127, MIR129-2, MIR130B, MIR132, MIR193A, MIR339, MIR34B/C, MIR9-1, and MIR9-3) were hypermethylated already at the early stages of OvCa, while hypermethylation of MIR1258, MIR137, MIR203A, and MIR375 was pronounced in metastatic tumors, and MIR148A showed high methylation levels specifically in PMM. We confirmed the significant relationship between methylation and expression levels for 11 out of 12 miRNAs analyzed by qRT-PCR. Moreover, expression levels of six miRNAs were significantly decreased in metastatic tumors in comparison with nonmetastatic ones, and downregulation of miR-203a-3p was the most significant. We revealed an inverse relationship between expression levels of miR-203a-3p and those of ZEB1 and ZEB2 genes, which are EMT drivers. We also identified three miRNA genes (MIR148A, MIR9-1, and MIR193A) that likely regulate EMT–MET reversion in the colonization of PMM. According to the Kaplan–Meier analysis, hypermethylation of several examined miRNA genes was associated with poorer overall survival of OvCa patients, and high methylation levels of MIR130B and MIR9-1 were related to the greatest relative risk of death. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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19 pages, 3792 KiB

Open AccessArticle

Potential Anti-Metastatic Role of the Novel miR-CT3 in Tumor Angiogenesis and Osteosarcoma Invasion

by Lavinia Raimondi, Alessia Gallo, Nicola Cuscino, Angela De Luca, Viviana Costa, Valeria Carina, Daniele Bellavia, Matteo Bulati, Riccardo Alessandro, Milena Fini, Pier Giulio Conaldi and Gianluca Giavaresi

Int. J. Mol. Sci. 2022, 23(2), 705; https://doi.org/10.3390/ijms23020705 - 09 Jan 2022

Cited by 5 | Viewed by 2046

Abstract

Osteosarcoma (OS) is the most common primary bone tumor mainly occurring in young adults and derived from primitive bone-forming mesenchyme. OS develops in an intricate tumor microenvironment (TME) where cellular function regulated by microRNAs (miRNAs) may affect communication between OS cells and the surrounding TME. Therefore, miRNAs are considered potential therapeutic targets in cancer and one of the goals of research is to accurately define a specific signature of a miRNAs, which could reflect the phenotype of a particular tumor, such as OS. Through NGS approach, we previously found a specific molecular profile of miRNAs in OS and discovered 8 novel miRNAs. Among these, we deepen our knowledge on the fifth candidate renamed now miR-CT3. MiR-CT3 expression was low in OS cells when compared with human primary osteoblasts and healthy bone. Through TargetScan, VEGF-A was predicted as a potential biological target of miR-CT3 and luciferase assay confirmed it. We showed that enforced expression of miR-CT3 in two OS cell lines, SAOS-2 and MG-63, reduced expression of VEGF-A mRNA and protein, inhibiting tumor angiogenesis. Enforced expression of miR-CT3 also reduced OS cell migration and invasion as confirmed by soft agar colony formation assay. Interestingly, we found that miR-CT3 behaves inducing the activation of p38 MAP kinase pathway and modulating the epithelial-mesenchymal transition (EMT) proteins, in particular reducing Vimentin expression. Overall, our study highlights the novel role of miR-CT3 in regulating tumor angiogenesis and progression in OS cells, linking also to the modulation of EMT proteins. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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21 pages, 2398 KiB

Open AccessArticle

The Profile of MicroRNA Expression and Potential Role in the Regulation of Drug-Resistant Genes in Cisplatin- and Paclitaxel-Resistant Ovarian Cancer Cell Lines

by Dominika Kazmierczak, Karol Jopek, Karolina Sterzynska, Michal Nowicki, Marcin Rucinski and Radoslaw Januchowski

Int. J. Mol. Sci. 2022, 23(1), 526; https://doi.org/10.3390/ijms23010526 - 04 Jan 2022

Cited by 12 | Viewed by 2650

Abstract

Ovarian cancer is the most lethal gynecological malignancy. The high mortality results from late diagnosis and the development of drug resistance. Drug resistance results from changes in the expression of different drug-resistance genes that may be regulated miRNA. The main aim of our study was to detect changes in miRNA expression levels in two cisplatin (CIS) and two paclitaxel (PAC)—resistant variants of the A2780 drug-sensitive ovarian cancer cell line—by miRNA microarray. The next goal was to identify miRNAs responsible for the regulation of drug-resistance genes. We observed changes in the expression of 46 miRNA that may be related to drug resistance. The overexpression of miR-125b-5p, miR-99a-5p, miR-296-3p, and miR-887-3p and downregulation of miR-218-5p, miR-221-3p, and miR-222-3p was observed in both CIS-resistant cell lines. In both PAC-resistant cell lines, we observed the upregulation of miR-221-3p, miR-222-3p, and miR-4485, and decreased expression of miR-551b-3p, miR-551b-5p, and miR-218-5p. Analysis of targets suggest that expression of important drug-resistant genes like protein Tyrosine Phosphatase Receptor Type K (PTPRK), receptor tyrosine kinase—EPHA7, Semaphorin 3A (SEMA3A), or the ATP-binding cassette subfamily B member 1 gene (ABCB1) can be regulated by miRNA. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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Review

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24 pages, 1476 KiB

Open AccessReview

MicroRNAs: A Link between Mammary Gland Development and Breast Cancer

by Diana Wu, Lilian U. Thompson and Elena M. Comelli

Int. J. Mol. Sci. 2022, 23(24), 15978; https://doi.org/10.3390/ijms232415978 - 15 Dec 2022

Cited by 3 | Viewed by 4567

Abstract

Breast cancer is among the most common cancers in women, second to skin cancer. Mammary gland development can influence breast cancer development in later life. Processes such as proliferation, invasion, and migration during mammary gland development can often mirror processes found in breast cancer. MicroRNAs (miRNAs), small, non-coding RNAs, can repress post-transcriptional RNA expression and can regulate up to 80% of all genes. Expression of miRNAs play a key role in mammary gland development, and aberrant expression can initiate or promote breast cancer. Here, we review the role of miRNAs in mammary development and breast cancer, and potential parallel roles. A total of 32 miRNAs were found to be expressed in both mammary gland development and breast cancer. These miRNAs are involved in proliferation, metastasis, invasion, and apoptosis in both processes. Some miRNAs were found to have contradictory roles, possibly due to their ability to target many genes at once. Investigation of miRNAs and their role in mammary gland development may inform about their role in breast cancer. In particular, by studying miRNA in development, mechanisms and potential targets for breast cancer treatment may be elucidated. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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23 pages, 2184 KiB

Open AccessReview

Role of MicroRNA-7 (MiR-7) in Cancer Physiopathology

by Mario Morales-Martínez and Mario I. Vega

Int. J. Mol. Sci. 2022, 23(16), 9091; https://doi.org/10.3390/ijms23169091 - 13 Aug 2022

Cited by 10 | Viewed by 2803

Abstract

miRNAs are non-coding RNA sequences of approximately 22 nucleotides that interact with genes by inhibiting their translation through binding to their 3′ or 5′ UTR regions. Following their discovery, the role they play in the development of various pathologies, particularly cancer, has been studied. In this context, miR-7 is described as an important factor in the development of cancer because of its role as a tumor suppressor, regulating a large number of genes involved in the development and progression of cancer. Recent data support the function of miR-7 as a prognostic biomarker in cancer, and miR-7 has been proposed as a strategy in cancer therapy. In this work, the role of miR-7 in various types of cancer is reviewed, illustrating its regulation, direct targets, and effects, as well as its possible relationship to the clinical outcome of cancer patients. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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31 pages, 1000 KiB

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The Dysregulation of MicroRNAs in the Development of Cervical Pre-Cancer—An Update

by Pui-Wah Choi, Tin Lun Liu, Chun Wai Wong, Sze Kei Liu, Yick-Liang Lum and Wai-Kit Ming

Int. J. Mol. Sci. 2022, 23(13), 7126; https://doi.org/10.3390/ijms23137126 - 27 Jun 2022

Cited by 3 | Viewed by 2847

Abstract

Globally in 2020, an estimated ~600,000 women were diagnosed with and 340,000 women died from cervical cancer. Compared to 2012, the number of cases increased by 7.5% and the number of deaths increased by 17%. MiRNAs are involved in multiple processes in the pathogenesis of cervical cancer. Dysregulation of miRNAs in the pre-stage of cervical cancer is the focus of this review. Here we summarize the dysregulated miRNAs in clinical samples from cervical pre-cancer patients and relate them to the early transformation process owing to human papillomavirus (HPV) infection in the cervical cells. When HPV infects the normal cervical cells, the DNA damage response is initiated with the involvement of HPV’s E1 and E2 proteins. Later, cell proliferation and cell death are affected by the E6 and E7 proteins. We find that the expressions of miRNAs in cervical pre-cancerous tissue revealed by different studies seldom agreed with each other. The discrepancy in sample types, samples’ HPV status, expression measurement, and methods for analysis contributed to the non-aligned results across studies. However, several miRNAs (miR-34a, miR-9, miR-21, miR-145, and miR-375) were found to be dysregulated across multiple studies. In addition, there are hints that the DNA damage response and cell growth response induced by HPV during the early transformation of the cervical cells are related to these miRNAs. Currently, no review articles analyse the relationship between the dysregulated miRNAs in cervical pre-cancerous tissue and their possible roles in the early processes involving HPV’s protein encoded by the early genes and DNA damage response during normal cell transformation. Our review provides insight on spotting miRNAs involved in the early pathogenic processes and pointing out their potential as biomarker targets of cervical pre-cancer. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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21 pages, 3888 KiB

Open AccessReview

Implication of microRNAs in Carcinogenesis with Emphasis on Hematological Malignancies and Clinical Translation

by Zsuzsanna Gaál

Int. J. Mol. Sci. 2022, 23(10), 5838; https://doi.org/10.3390/ijms23105838 - 23 May 2022

Cited by 6 | Viewed by 2615

Abstract

MicroRNAs (miRNAs) are evolutionarily conserved small non-coding RNAs, that are involved in the multistep process of carcinogenesis, contributing to all established hallmarks of cancer. In this review, implications of miRNAs in hematological malignancies and their clinical utilization fields are discussed. As components of the complex regulatory network of gene expression, influenced by the tissue microenvironment and epigenetic modifiers, miRNAs are “micromanagers” of all physiological processes including the regulation of hematopoiesis and metabolic pathways. Dysregulated miRNA expression levels contribute to both the initiation and progression of acute leukemias, the metabolic reprogramming of malignantly transformed hematopoietic precursors, and to the development of chemoresistance. Since they are highly stable and can be easily quantified in body fluids and tissue specimens, miRNAs are promising biomarkers for the early detection of hematological malignancies. Besides novel opportunities for differential diagnosis, miRNAs can contribute to advanced chemoresistance prediction and prognostic stratification of acute leukemias. Synthetic oligonucleotides and delivery vehicles aim the therapeutic modulation of miRNA expression levels. However, major challenges such as efficient delivery to specific locations, differences of miRNA expression patterns between pediatric and adult hematological malignancies, and potential side effects of miRNA-based therapies should be considered. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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26 pages, 2346 KiB

Open AccessReview

miRNAs in Lymphocytic Leukaemias—The miRror of Drug Resistance

by Yordan Sbirkov, Bozhidar Vergov, Nikolay Mehterov and Victoria Sarafian

Int. J. Mol. Sci. 2022, 23(9), 4657; https://doi.org/10.3390/ijms23094657 - 22 Apr 2022

Cited by 3 | Viewed by 2328

Abstract

Refractory disease and relapse remain the main causes of cancer therapy failure. Refined risk stratification, treatment regimens and improved early diagnosis and detection of minimal residual disease have increased cure rates in malignancies like childhood acute lymphoblastic leukaemia (ALL) to 90%. Nevertheless, overall survival in the context of drug resistance remains poor. The regulatory role of micro RNAs (miRNAs) in cell differentiation, homeostasis and tumorigenesis has been under extensive investigation in different cancers. There is accumulating data demonstrating the significance of miRNAs for therapy outcomes in lymphoid malignancies and some direct demonstrations of the interplay between these small molecules and drug response. Here, we summarise miRNAs’ impact on chemotherapy resistance in adult and paediatric ALL and chronic lymphocytic leukaemia (CLL). The main focus of this review is on the modulation of particular signaling pathways like PI3K-AKT, transcription factors such as NF-κB, and apoptotic mediators, all of which are bona fide and pivotal elements orchestrating the survival of malignant lymphocytic cells. Finally, we discuss the attractive strategy of using mimics, antimiRs and other molecular approaches pointing at miRNAs as promising therapeutic targets. Such novel strategies to circumvent ALL and CLL resistance networks may potentially improve patients’ responses and survival rates. Full article

(This article belongs to the Special Issue Role of MicroRNAs in Cancer Development and Treatment)

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