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The Expression Levels of Microrna-361-5P and Its Target VEGFA Are Inversely Correlated in Human Cutaneous Squamous Cell Carcinoma

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The Expression Levels of Microrna-361-5P and Its Target VEGFA Are Inversely Correlated in Human Cutaneous Squamous Cell Carcinoma Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2012 The expression levels of microRNA-361-5p and its target VEGFA are inversely correlated in human cutaneous squamous cell carcinoma Kanitz, Alexander ; Imig, Jochen ; Dziunycz, Piotr J ; Primorac, Adriana ; Galgano, Alessia ; Hofbauer, Günther F L ; Gerber, André P ; Detmar, Michael Abstract: Vascular endothelial growth factor A (VEGFA) plays a key role in the angiogenesis of human skin. Elevated levels of VEGFA are associated with several pathological conditions, including chronic inflammatory skin diseases and several types of skin cancer. In particular, squamous cell carcinoma (SCC) of the skin, the second most common skin cancer in the general population, is characterized by invasive growth, pronounced angiogenesis and elevated levels of VEGFA. The processing, turnover and production of VEGFA are extensively regulated at the post-transcriptional level, both by RNA-binding proteins and microRNAs (miRNAs). In the present study, we identified a new miRNA recognition element in a downstream conserved region of the VEGFA 3’-UTR. We confirmed the repressive effect of miR- 361-5p on this element in vitro, identifying the first target for this miRNA. Importantly, we found that miR-361-5p levels are inversely correlated with VEGFA expression in SCC and in healthy skin, indicating that miR-361-5p could play a role in cancers. DOI: https://doi.org/10.1371/journal.pone.0049568 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-76296 Journal Article Published Version The following work is licensed under a Creative Commons: Attribution 4.0 International (CC BY 4.0) License. Originally published at: Kanitz, Alexander; Imig, Jochen; Dziunycz, Piotr J; Primorac, Adriana; Galgano, Alessia; Hofbauer, Günther F L; Gerber, André P; Detmar, Michael (2012). The expression levels of microRNA-361-5p and its target VEGFA are inversely correlated in human cutaneous squamous cell carcinoma. PLoS ONE, 7(11):e49568. DOI: https://doi.org/10.1371/journal.pone.0049568 The Expression Levels of MicroRNA-361-5p and Its Target VEGFA Are Inversely Correlated in Human Cutaneous Squamous Cell Carcinoma Alexander Kanitz1, Jochen Imig1, Piotr J. Dziunycz2, Adriana Primorac1, Alessia Galgano1¤a, Gu¨ nther F. L. Hofbauer2, Andre´ P. Gerber1*¤b, Michael Detmar1* 1 Institute of Pharmaceutical Sciences, ETH Zurich, Zurich, Switzerland, 2 Department of Dermatology, University Hospital Zurich, Zurich, Switzerland Abstract Vascular endothelial growth factor A (VEGFA) plays a key role in the angiogenesis of human skin. Elevated levels of VEGFA are associated with several pathological conditions, including chronic inflammatory skin diseases and several types of skin cancer. In particular, squamous cell carcinoma (SCC) of the skin, the second most common skin cancer in the general population, is characterized by invasive growth, pronounced angiogenesis and elevated levels of VEGFA. The processing, turnover and production of VEGFA are extensively regulated at the post-transcriptional level, both by RNA-binding proteins and microRNAs (miRNAs). In the present study, we identified a new miRNA recognition element in a downstream conserved region of the VEGFA 39-UTR. We confirmed the repressive effect of miR-361-5p on this element in vitro, identifying the first target for this miRNA. Importantly, we found that miR-361-5p levels are inversely correlated with VEGFA expression in SCC and in healthy skin, indicating that miR-361-5p could play a role in cancers. Citation: Kanitz A, Imig J, Dziunycz PJ, Primorac A, Galgano A, et al. (2012) The Expression Levels of MicroRNA-361-5p and Its Target VEGFA Are Inversely Correlated in Human Cutaneous Squamous Cell Carcinoma. PLoS ONE 7(11): e49568. doi:10.1371/journal.pone.0049568 Editor: Amanda Ewart Toland, Ohio State University Medical Center, United States of America Received November 2, 2011; Accepted October 12, 2012; Published November 14, 2012 Copyright: ß 2012 Kanitz et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by National Institutes of Health (http://www.nih.gov/) grant CA69184, Swiss National Science Foundation (http://www.snf.ch/) grants 3100A0_108207 and 31003A_130627, European Research Council (http://erc.europa.eu/) Advanced Grant LYVICAM (Lymphatic Vessels in Inflammation and Cancer Metastasis), Oncosuisse (http://www2.oncosuisse.ch/), Krebsliga Zurich (http://www.krebsliga-zh.ch/) (to MD), the Bonizzi-Theler Foundation, ETH Zurich (http://www.ethz.ch/) grant ETH-19 09-1, Swiss National Science Foundation grant CRSII3_127454 (to APG), EMDO foundation, Olga-Mayenfisch-Foundation (to GFLH), the European Skin Research Foundation ESRF (http://www.euroskinresearch.org/), and the Rene´ Touraine Foundation (http://www.fondation-r-touraine. org/) (to PJD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have read the journal’s policy and have the following conflicts: Andre´ P. Gerber is a PLOS ONE Editorial Board member. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials. * E-mail: [email protected] (APG); [email protected] (MD) ¤a Current address: Faculte´ de Me´decine, Universite´ Paris Descartes, Paris, France ¤b Current address: Faculty of Health and Medical Sciences, University of Surrey, Guildford, United Kingdom Introduction Cutaneous squamous cell carcinoma (SCC) is the second most common skin cancer in the general population [3]. In contrast to Angiogenesis is a multi-step process leading to the formation of basal cell carcinoma – the most common skin cancer – it is vascular structures derived from preexisting blood vessels, either characterized by the risk for metastasis. Incidence of SCC is 60- to through remodeling or the formation (‘‘sprouting’’) of new vessels. 100-times higher among immunosuppressed patients, which It involves the induction of microvascular hyperpermeability, makes it the most common cancer following organ transplantation. breakdown of the vascular basement membrane, recruitment and Invasive SCC develops from atypical keratinocytes, clinically proliferation of endothelial cells (EC), and the formation of mature visible as actinic keratosis or Bowen’s disease, both considered blood vessels. Positive and negative regulators of angiogenesis have intraepithelial non-invasive forms of SCC [4]. Approximately 1% to be tightly regulated to maintain physiological tissue homeostasis of these intraepithelial lesions develop into an invasive SCC [5]. and function. For example, in healthy adult skin, angiogenesis is However, such tumor development requires intense interactions generally quiescent as angiogenic stimuli are overruled by with stromal cells and profound extracellular remodeling. Angio- inhibitory signals. However, environmental insults may tip this genesis is an essential part of the malignant phenotype as most balance, leading to initiation of angiogenesis in order to counteract tumors are apparently not able to exceed 1–2 mm of diameter tissue damage. Similarly, excessive angiogenesis in the skin, without developing new blood vessels [6]. Therefore they produce resulting from dysregulation of one or more of its regulators, is angiogenic factors at an early point of development. associated with a plethora of pathological conditions, such as Vascular endothelial growth factor A (VEGFA) is a homo- psoriasis and other inflammatory dermatoses, autoimmune blis- dimeric heparin-binding glycoprotein that mainly acts as a para- tering diseases, and many cancers, most prominently melanoma, crine mitogen, growth and survival factor for ECs, but it also basal cell carcinoma and squamous cell carcinoma. Anti-angio- causes vascular permeability, vasodilatation, and various changes genic therapy therefore holds promise for the treatment of a wide in immune cell properties upon binding to its main receptors spectrum of human ailments [1,2]. VEGF receptor 21 and 22. VEGFA has been identified as the PLOS ONE | www.plosone.org 1 November 2012 | Volume 7 | Issue 11 | e49568 VEGFA and miR-361-5p Expression in Human SCC predominant tumor angiogenesis factor in the majority of human VEGFA 39-UTR under hypoxia led to competitive displacement cancers, including those of the breast, colon, lung and prostate of miRNAs miR-297, -299, -567 and -605 and consequently [7,8]. Invasive SCC also expresses increased levels of VEGFA, derepression of VEGFA expression in tumor-associated macro- particularly in the leading front of the tumor, which is an intuitive phages [30]. Finally, microRNAs 200b, 93 and 29b were site for the induction of angiogenesis [9]. Furthermore, over- implicated in the non-malignant conditions diabetic retinopathy expression of (murine) VEGFA resulted in enhanced invasion and [49], diabetes [50], and pre-eclampsia [51], respectively. angiogenesis in experimental human SCC [10]. In some other In the present study, we have used miRNA target prediction cancers, such as head and neck squamous cell carcinoma, algorithms and luciferase reporter assays to identify a new increased expression of VEGF has been associated with pro-
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