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Characterizing the Invasive Tumor Front of Aggressive Uterine Adenocarcinoma and Leiomyosarcoma

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Characterizing the Invasive Tumor Front of Aggressive Uterine Adenocarcinoma and Leiomyosarcoma Characterizing the invasive tumor front of aggressive uterine adenocarcinoma and leiomyosarcoma Sabina Sanegre1, Núria Eritja2, 3, 4, 5, 6, Carlos de Andrea2, 7, Juan Díaz-Martín2, 8, 9, 10, 11, Ángel Díaz-Lagares2, 12, 13, María Amalia Jácome14, Carmen Salguero-Aranda8, 9, 10, 11, David García-Ros7, Ben Davidson15, 16, 17, Rafael López2, 13, 12, Ignacio Melero2, 18, Samuel Navarro2, 1, Santiago Ramon Y Cajal2, 19, Enrique De Álava2, 8, 9, 10, 11, Xavier Matias-Guiu2, 3, 5, 6, 4*, Rosa Noguera2, 20, 1* 1Institute of Health Research (INCLIVA), Spain, 2Centro de Investigaciónació Biomédica en Red del Cáncer (CIBERONC), Spain, 3Department of Pathology, University Hospital ArnauAr de Vilanova, Spain, 4Bellvitge University Hospital, Spain, 5Universitatt de Lleida, Spain, 6Universityniversity of Barcelona, Spain, 7University Clinic of Navarra, Spain, 8Institutetute of Biomedicine of Seville (IBIS), Spain,Sp 9Virgen del Rocío University Hospital, Spain, 10Consejo Superior de Investigaciones CientífiCientíficas (CSIC), Spain, 11Sevilla University, 12 13 Spain, University Clinical Hospital of Santiago, Spain,Spa Health Research Institute of Santiago de Compostelapostela (IDIS), Spain, 14Facultyculty of Science,Scie University of A Coruña, Spain, 15Institute of Clinical Medicine,ne, Faculty of Medicine,Me University of Oslo, Norway, 16Department of Pathology, Oslo University Hospital,l, Norway,Nor 17Norwegian Radium Hospital, Oslo University Hospital, Norway, 18Departamento de Dermatología,D Clínica Universidad de Navarra, Spain, 19Department of Pathology, Vall d'Hebron University Hospital, Spain, 20Department of Pathology, University of Valencia, Spain InSubmitted review to Journal: Frontiers in Cell and Developmental Biology Specialty Section: Cell Adhesion and Migration Article type: Original Research Article Manuscript ID: 670185 Received on: 20 Feb 2021 Journal website link: www.frontiersin.org Conflict of interest statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest Author contribution statement RN, and MX contributed to conception and design of the study. SS wrote the first draft of the manuscript. SS, NE, CA, JD, AD, EA, XM and RN wrote sections of the manuscript. BD, RL, SR, EA, XM provided clinicopathological data. NE provided the collaborative consortium with microdissected samples. SS and RN designed and performed the morphometric characterization of the reticulin fibers. CA and DR performed the multiplex staining and analysis. JD, CS and EA evaluated the transcriptomic profile. AD and AJ performed the genome-wide methylation analysis. All authors contributed to manuscript revision, read, and approved the submitted version. Keywords tumor-host interface, Tumor Microenvironment, Extracellular Matrix, Reticularticular fibers, immune cells,c Gene Expression, epigenetic profiles Abstractt Word count:nt: 200 The tumor-host-host interface is vitally importantimport in malignant cell progression and metastasis. Tumor cell interactions with resident and infiltratingting host cells and with the surrounding extracellular matrix and secreted factors ultimately determine the fate of the tumor. Hereinin we focus on the invasive tumor front, making an in-depth characterization of reticular fiber scaffolding, infiltrating immune cells,ells gene expression and epigenetic profiles of classified aggressive primary uterine adenocarcinomas (ADC=24) and leiomyosarcomasIn (LMS=11). Sections review of formalin-fixed samples before and after microdissection were scanned and studied. Reticular fiber architecture and immune cell infiltration were analyzed by automatized algorithms in the same small regions of interest. Despite morphometric resemblance between reticular fibers and high presence of macrophages, we found some variance in other immune cell populations and distinctive gene expression and cell adhesion-related methylation signatures. Although no evident overall differences in immune response were detected at the gene expression and methylation level, impaired antimicrobial humoral response might be involved in LMS spread. Similarities found at the invasive tumor front of uterine ADC and LMS could facilitate use of common biomarkers and therapies, and additionally, molecular and architectural characterization of the invasive front of uterine malignancies may provide additional prognostic information beyond established prognostic factors. Contribution to the field We present a comprehensive study of the tumor-host interface in uterine tumors. We have characterized this interface, the invasive tumor front, at different levels. We know now that the fiber architectural pattern at the invasive front, as well as the immune infiltrate, epigenomic landscape and trancrptomic profile share a lot in common in the two uterine tumors that we have studied. We have also unveiled a very narrow differential gene signature regulated by epigenetic mechanisms. We hope our findings lead to new perspectives for biomarker development and provide additional information over the current prognostic factors. Funding statement This research was supported by grants from ISCIII and ERDF (PI17/01558 and PI20/01107), by CIBERONC (contracts CB16/12/00484, CB16/12/0328, CB16/12/00363, CB16/12/00364, CB16/12/00481, CB16/12/00231) and by Grupos Coordinados Estables from Asociación Española Contra el Cáncer (AECC). AD is funded by a contract “Juan Rodés” from ISCIII (JR17/00016). The funders had no involvement in the research process nor in the preparation and submission of the article. Ethics statements Studies involving animal subjects Generated Statement: No animal studies are presented in this manuscript. Studies involving human subjects Generated Statement: The studies involving human participants were reviewed and approved by Comité Coordinador de Ética de la Investigación Biomédica de Andalucía: Deciphering the site-specific tumor microenvironment of advanced uterine tumors (Biobank code: S1800086) and Comité de Ética de la Investigación with the codes CEIC-1892, CEIC-2083 and CEIC-1858.. Written informed consent for participation was not required for this study in accordance with the national legislation and the institutional requirements. Inclusion of identifiable human data Generated Statement: No potentially identifiable human images or data is presented in this study. In review Data availability statement Generated Statement: The authors acknowledge that the data presented in this study must be deposited and made publicly available in an acceptable repository, prior to publication. Frontiers cannot accept a manuscript that does not adhere to our open data policies. In review Characterizing the invasive tumor front of aggressive uterine adenocarcinoma and leiomyosarcoma 1 Sanegre S1,2, Eritja N1,3, de Andrea C1,4, Diaz-Martin J1,5, Diaz-Lagares A1,6, Jácome A7, 2 Salguero-Aranda C1,5, García Ros D4, Davidson B8, Lopez R1,9,10, Melero I1,4, Navarro S1,2, 3 Ramon y Cajal S1,11, de Alava E1,5, Matias-Guiu X1,3, †,*, Noguera R1,2, †, * 4 1Cancer CIBER (CIBERONC), Madrid. 5 2Pathology Department, Medical School, University of Valencia-INCLIVA, Valencia. 6 3Pathology Department, Hospital U Arnau de Vilanova and Hospital U de Bellvitge, Universities of 7 Lleida and Barcelona, IRBLLEIDA, IDIBELL. 8 4Clínica Universidad de Navarra, University of Navarra, Pamplona,amplona, SpainSpain.. 9 5Institute of Biomedicine of Sevilla (IBiS), Virgen del Rocio University HospHospitHospital/CSIC/University of 10 Sevilla/CIBERONC, 41013 Seville,e, Spain. 11 6Cancer Epigenomics,cs, Translational Medical Oncology Group (Oncomet), HHealth Research Institute 12 of Santiagoo (IDIS), University Clinical Hospital of Santiago (CH(C(CHUS/SERGAS), 15760 Santiago de 13 Compostela,tela, Spain.Spain 14 7Departmententnt of Mathematics, MODES grogroup, CITIC, Faculty of Science, Universidade da Coruña, A 15 Coruña, Spain.painin. 16 8 Institute off Clinical CliniClin Medicine, Faculty of Medicine, University of Oslo, 0424 Oslo, Norway; 17 Department Inof Pathology, Oslo reviewUniversity Hospital, Norwegian Radium Hospital, 0310 Oslo, 18 Norway. 19 9Translational Medical Oncology Group (Oncomet), Health Research Institute of Santiago (IDIS), 20 University Clinical Hospital of Santiago (CHUS/SERGAS), 15760 Santiago de Compostela, Spain. 21 10Roche-Chus Joint Unit, Translational Medical Oncology Group (Oncomet), Health Research 22 Institute of Santiago (IDIS), 15760 Santiago de Compostela, Spain. 23 11Department of Pathology, Vall d'Hebron University Hospital, Autonoma University of Barcelona. 24 25 †These authors contributed equally to this work. 26 27 *Correspondence: Rosa Noguera ([email protected]) and Xavier Matias-Guiu 28 ([email protected]) 29 Keywords: tumor-host interface, tumor microenvironment, extracellular matrix, reticular 30 fibers, immune cells, gene expression, epigenetic profiles 31 Running Title: Uterine-myometrial tumor interface 32 Uterine-myometrial tumor interface 33 34 Abstract 35 The tumor-host interface is vitally important in malignant cell progression and metastasis. Tumor cell 36 interactions with resident and infiltrating host cells and with the surrounding extracellular matrix and 37 secreted factors ultimately determine the fate of the tumor. Herein we focus on the invasive tumor 38 front, making an in-depth characterization of reticular fiber scaffolding, infiltrating immune cells, 39 gene expression and epigenetic profiles
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