{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,4]],"date-time":"2025-11-04T10:47:12Z","timestamp":1762253232151,"version":"build-2065373602"},"reference-count":103,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2020,1,1]],"date-time":"2020-01-01T00:00:00Z","timestamp":1577836800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["UID\/Multi\/04462\/2019","PD\/BD\/128337\/2017"],"award-info":[{"award-number":["UID\/Multi\/04462\/2019","PD\/BD\/128337\/2017"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Bone marrow contains endothelial progenitor cells (EPCs) that, upon pro-angiogenic stimuli, migrate and differentiate into endothelial cells (ECs) and contribute to re-endothelialization and neo-vascularization. There are currently no reliable markers to characterize EPCs, leading to their inaccurate identification. In the past, we showed that, in a panel of tumors, some cells on the vessel wall co-expressed CD14 (monocytic marker) and CD31 (EC marker), indicating a putative differentiation route of monocytes into ECs. Herein, we disclosed monocytes as potential EPCs, using in vitro and in vivo models, and also addressed the cancer context. Monocytes acquired the capacity to express ECs markers and were able to be incorporated into blood vessels, contributing to cancer progression, by being incorporated in tumor neo-vasculature. Reactive oxygen species (ROS) push monocytes to EC differentiation, and this phenotype is reverted by cysteine (a scavenger and precursor of glutathione), which indicates that angiogenesis is controlled by the interplay between the oxidative stress and the scavenging capacity of the tumor microenvironment.<\/jats:p>","DOI":"10.3390\/cells9010107","type":"journal-article","created":{"date-parts":[[2020,1,3]],"date-time":"2020-01-03T11:55:07Z","timestamp":1578052507000},"page":"107","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":38,"title":["Monocytes as Endothelial Progenitor Cells (EPCs), Another Brick in the Wall to Disentangle Tumor Angiogenesis"],"prefix":"10.3390","volume":"9","author":[{"given":"Filipa","family":"Lopes-Coelho","sequence":"first","affiliation":[{"name":"CEDOC, Chronic Diseases Research Centre, NOVA Medical School|Faculdade de Ci\u00eancias M\u00e9dicas, Universidade NOVA de Lisboa, Campo dos M\u00e1rtires da P\u00e1tria, 130, 1169-056 Lisboa, Portugal"},{"name":"Instituto Portugu\u00eas de Oncologia de Lisboa Francisco Gentil (IPOLFG), Rua Prof. Lima Basto 1099-023 Lisboa, Portugal"}]},{"given":"Fernanda","family":"Silva","sequence":"additional","affiliation":[{"name":"CEDOC, Chronic Diseases Research Centre, NOVA Medical School|Faculdade de Ci\u00eancias M\u00e9dicas, Universidade NOVA de Lisboa, Campo dos M\u00e1rtires da P\u00e1tria, 130, 1169-056 Lisboa, Portugal"},{"name":"Instituto Portugu\u00eas de Oncologia de Lisboa Francisco Gentil (IPOLFG), Rua Prof. Lima Basto 1099-023 Lisboa, Portugal"}]},{"given":"Sofia","family":"Gouveia-Fernandes","sequence":"additional","affiliation":[{"name":"CEDOC, Chronic Diseases Research Centre, NOVA Medical School|Faculdade de Ci\u00eancias M\u00e9dicas, Universidade NOVA de Lisboa, Campo dos M\u00e1rtires da P\u00e1tria, 130, 1169-056 Lisboa, Portugal"},{"name":"Instituto Portugu\u00eas de Oncologia de Lisboa Francisco Gentil (IPOLFG), Rua Prof. Lima Basto 1099-023 Lisboa, Portugal"}]},{"given":"Carmo","family":"Martins","sequence":"additional","affiliation":[{"name":"Instituto Portugu\u00eas de Oncologia de Lisboa Francisco Gentil (IPOLFG), Rua Prof. Lima Basto 1099-023 Lisboa, Portugal"}]},{"given":"Nuno","family":"Lopes","sequence":"additional","affiliation":[{"name":"Instituto de Biologia Experimental e Tecnol\u00f3gica, Avenida da Rep\u00fablica, Esta\u00e7\u00e3o Agron\u00f3mica, 2780-157 Oeiras, Portugal"}]},{"given":"Germana","family":"Domingues","sequence":"additional","affiliation":[{"name":"CEDOC, Chronic Diseases Research Centre, NOVA Medical School|Faculdade de Ci\u00eancias M\u00e9dicas, Universidade NOVA de Lisboa, Campo dos M\u00e1rtires da P\u00e1tria, 130, 1169-056 Lisboa, Portugal"},{"name":"Instituto Portugu\u00eas de Oncologia de Lisboa Francisco Gentil (IPOLFG), Rua Prof. Lima Basto 1099-023 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8926-279X","authenticated-orcid":false,"given":"Catarina","family":"Brito","sequence":"additional","affiliation":[{"name":"Instituto de Biologia Experimental e Tecnol\u00f3gica, Avenida da Rep\u00fablica, Esta\u00e7\u00e3o Agron\u00f3mica, 2780-157 Oeiras, Portugal"},{"name":"Instituto de Tecnologia Qu\u00edmica e Biol\u00f3gica Ant\u00f3nio Xavier, Universidade Nova de Lisboa, Av. da Rep\u00fablica, 2780-157 Oeiras, Portugal"}]},{"given":"Ant\u00f3nio M","family":"Almeida","sequence":"additional","affiliation":[{"name":"Instituto Portugu\u00eas de Oncologia de Lisboa Francisco Gentil (IPOLFG), Rua Prof. Lima Basto 1099-023 Lisboa, Portugal"},{"name":"Hospital da Luz, Av. Lus\u00edada 100, 1500-650 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8456-9995","authenticated-orcid":false,"given":"Sofia A","family":"Pereira","sequence":"additional","affiliation":[{"name":"CEDOC, Chronic Diseases Research Centre, NOVA Medical School|Faculdade de Ci\u00eancias M\u00e9dicas, Universidade NOVA de Lisboa, Campo dos M\u00e1rtires da P\u00e1tria, 130, 1169-056 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1548-5907","authenticated-orcid":false,"given":"Jacinta","family":"Serpa","sequence":"additional","affiliation":[{"name":"CEDOC, Chronic Diseases Research Centre, NOVA Medical School|Faculdade de Ci\u00eancias M\u00e9dicas, Universidade NOVA de Lisboa, Campo dos M\u00e1rtires da P\u00e1tria, 130, 1169-056 Lisboa, Portugal"},{"name":"Instituto Portugu\u00eas de Oncologia de Lisboa Francisco Gentil (IPOLFG), Rua Prof. Lima Basto 1099-023 Lisboa, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2020,1,1]]},"reference":[{"key":"ref_1","first-page":"XE01","article-title":"Tumour angiogenesis and angiogenic inhibitors: A review","volume":"9","author":"Yadav","year":"2015","journal-title":"J. Clin. Diagn. Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1159\/000488340","article-title":"Tumor Angiogenesis: A Key Target for Cancer Therapy","volume":"41","year":"2018","journal-title":"Oncol. Res. Treat."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1007\/s10456-014-9420-y","article-title":"Anti-angiogenic therapy for cancer: Current progress, unresolved questions and future directions","volume":"17","author":"Vasudev","year":"2014","journal-title":"Angiogenesis"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1007\/s13770-017-0043-4","article-title":"Endothelial Progenitor Cells\u2019 Classification and Application in Neurological Diseases","volume":"14","author":"Yuan","year":"2017","journal-title":"Tissue Eng. Regen. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"a006692","DOI":"10.1101\/cshperspect.a006692","article-title":"Human endothelial progenitor cells","volume":"2","author":"Yoder","year":"2012","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.yjmcc.2010.07.009","article-title":"Endothelial progenitor cells: Quo Vadis?","volume":"50","author":"Richardson","year":"2011","journal-title":"J. Mol. Cell. Cardiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2605","DOI":"10.1002\/art.22035","article-title":"Bone marrow endothelial progenitors are defective in systemic sclerosis","volume":"54","author":"Quirici","year":"2006","journal-title":"Arthritis Rheum."},{"key":"ref_8","first-page":"60","article-title":"Levels of circulating endothelial progenitor cells in systemic sclerosis","volume":"25","author":"Allanore","year":"2007","journal-title":"Clin. Exp. Rheumatol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1136\/ard.2007.082131","article-title":"Circulating endothelial progenitor cells in systemic sclerosis: Association with disease severity","volume":"67","author":"Avouac","year":"2008","journal-title":"Ann. Rheum. Dis."},{"key":"ref_10","first-page":"21","article-title":"Circulating endothelial progenitor cells in systemic sclerosis: Relation to impaired angiogenesis and cardiovascular manifestations","volume":"26","author":"Nevskaya","year":"2008","journal-title":"Clin. Exp. Rheumatol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1038\/s41586-018-0552-x","article-title":"Erythro-myeloid progenitors contribute endothelial cells to blood vessels","volume":"562","author":"Plein","year":"2018","journal-title":"Nature"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2511","DOI":"10.1161\/01.CIR.0000096483.29777.50","article-title":"Relevance of Monocytic Features for Neovascularization Capacity of Circulating Endothelial Progenitor Cells","volume":"108","author":"Urbich","year":"2003","journal-title":"Circulation"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1387\/ijdb.103227sn","article-title":"The interplay between macrophages and angiogenesis in development, tissue injury and regeneration","volume":"55","author":"Nucera","year":"2011","journal-title":"Int. J. Dev. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"8429","DOI":"10.1158\/0008-5472.CAN-07-1684","article-title":"Tie2-expressing monocytes and tumor angiogenesis: Regulation by hypoxia and angiopoietin-2","volume":"67","author":"Lewis","year":"2007","journal-title":"Cancer Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1016\/j.ccr.2011.02.005","article-title":"Targeting the ANG2\/TIE2 Axis Inhibits Tumor Growth and Metastasis by Impairing Angiogenesis and Disabling Rebounds of Proangiogenic Myeloid Cells","volume":"19","author":"Mazzieri","year":"2011","journal-title":"Cancer Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1182\/blood-2012-01-403386","article-title":"CCR2 recruits an inflammatory macrophage subpopulation critical for angiogenesis in tissue repair","volume":"120","author":"Willenborg","year":"2012","journal-title":"Blood"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1097\/CCO.0b013e32831bed7e","article-title":"Corrupt policemen: Inflammatory cells promote tumor angiogenesis","volume":"21","author":"Zumsteg","year":"2009","journal-title":"Curr. Opin. Oncol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.matbio.2015.04.004","article-title":"Tumor angiogenesis: MMP-mediated induction of intravasation-and metastasis-sustaining neovasculature","volume":"44","author":"Deryugina","year":"2015","journal-title":"Matrix Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1016\/S0008-6363(00)00270-4","article-title":"Monocytes coexpress endothelial and macrophagocytic lineage markers and form cord-like structures in Matrigel\u00ae under angiogenic conditions","volume":"49","author":"Schmeisser","year":"2001","journal-title":"Cardiovasc. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1801","DOI":"10.1182\/blood-2006-08-043471","article-title":"Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem\/progenitor cell principals","volume":"109","author":"Yoder","year":"2007","journal-title":"Blood"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1161\/CIRCRESAHA.111.243386","article-title":"Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use","volume":"110","author":"Fadini","year":"2012","journal-title":"Circ. Res."},{"unstructured":"Domingues, G., Fernandes, S., Salgado, D., Nunes, S., Pereira, S., Coelho, F., Silva, F., F\u00e9lix, A., and Serpa, J. (2015, January 20\u201323). Monocytes\/Macrophages in Cancer, from Tumor Aggressors to Vascular Components\u2014A new Insight for Anti-Angiogenic Therapy. Proceedings of the EACR-AACR-SIC Special Conference on Anticancer Drug Action and Drug Resistance from Cancer Biology to the Clinic, Florence, Italy.","key":"ref_22"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.cardiores.2005.06.021","article-title":"Hydrogen peroxide regulation of endothelial function: Origins, mechanisms, and consequences","volume":"68","author":"Cai","year":"2005","journal-title":"Cardiovasc. Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1016\/j.redox.2014.02.005","article-title":"Hydrogen peroxide signaling in vascular endothelial cells","volume":"2","author":"Lamas","year":"2014","journal-title":"Redox Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1097\/01.mat.0000247157.84350.e8","article-title":"Mechanisms of H2O2-induced oxidative stress in endothelial cells exposed to physiologic shear stress","volume":"53","author":"Coyle","year":"2007","journal-title":"ASAIO J."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.yjmcc.2013.12.022","article-title":"Dual roles of vascular-derived reactive oxygen species-With a special reference to hydrogen peroxide and cyclophilin A-","volume":"73","author":"Satoh","year":"2014","journal-title":"J. Mol. Cell. Cardiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"471","DOI":"10.3892\/ijmm.2012.1215","article-title":"The effects of exogenous H2O2 on cell death, reactive oxygen species and glutathione levels in calf pulmonary artery and human umbilical vein endothelial cells","volume":"31","author":"Park","year":"2013","journal-title":"Int. J. Mol. Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1279","DOI":"10.1111\/bph.13828","article-title":"Reactive oxygen species: Key regulators in vascular health and diseases","volume":"175","author":"Chen","year":"2018","journal-title":"Br. J. Pharmacol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.lfs.2014.07.016","article-title":"Hydrogen peroxide inhibits proliferation and endothelial differentiation of bone marrow stem cells partially via reactive oxygen species generation","volume":"112","author":"Xiao","year":"2014","journal-title":"Life Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1881","DOI":"10.1089\/ars.2012.4963","article-title":"Roles of Reactive Oxygen Species in the Fate of Stem Cells","volume":"20","author":"Chaudhari","year":"2014","journal-title":"Antioxid. Redox Signal."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.mvr.2013.07.009","article-title":"Hydrogen peroxide induced impairment of endothelial progenitor cell viability is mediated through a FoxO3a dependant mechanism","volume":"90","author":"Wang","year":"2013","journal-title":"Microvasc. Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"175","DOI":"10.3858\/emm.2010.42.3.018","article-title":"Reactive oxygen species enhance differentiation of human embryonic stem cells into mesendodermal lineage","volume":"42","author":"Ji","year":"2010","journal-title":"Exp. Mol. Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/0888-7543(95)80048-Q","article-title":"Comparative mapping of human alphoid sequences in great apes using fluorescence in situ hybridization","volume":"25","author":"Archidiacono","year":"1995","journal-title":"Genomics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1007\/BF00333470","article-title":"Characterisation of a human Y chromosome repeated sequence and related sequences in higher primates","volume":"87","author":"Cooke","year":"1982","journal-title":"Chromosoma"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1048","DOI":"10.1038\/modpathol.3800386","article-title":"PLAG1 gene alterations in salivary gland pleomorphic adenoma and carcinoma ex-pleomorphic adenoma: A combined study using chromosome banding, in situ hybridization and immunocytochemistry","volume":"18","author":"Martins","year":"2005","journal-title":"Mod. Pathol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3904645","DOI":"10.1155\/2019\/3904645","article-title":"Aldehyde Dehydrogenases: Not Just Markers, but Functional Regulators of Stem Cells","volume":"2019","author":"Vassalli","year":"2019","journal-title":"Stem Cells Int."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1016\/j.bbmt.2014.12.027","article-title":"Content of endothelial progenitor cells in autologous stem cellgrafts predict survival after transplantation for multiplemyeloma","volume":"21","author":"Blix","year":"2015","journal-title":"Biol. Blood Marrow Transplant."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1124\/pr.111.005538","article-title":"Aldehyde Dehydrogenase Inhibitors: A Comprehensive Review of the Pharmacology, Mechanism of Action, Substrate Specificity, and Clinical Application","volume":"64","author":"Koppaka","year":"2012","journal-title":"Pharmacol. Rev."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"32965","DOI":"10.1074\/jbc.M704388200","article-title":"Epithelial-derived fibronectin expression, signaling, and function in intestinal inflammation","volume":"282","author":"Kolachala","year":"2007","journal-title":"J. Biol. Chem."},{"doi-asserted-by":"crossref","unstructured":"Hielscher, A., Ellis, K., Qiu, C., Porterfield, J., and Gerecht, S. (2016). Fibronectin deposition participates in extracellular matrix assembly and vascular morphogenesis. PLoS ONE, 11.","key":"ref_40","DOI":"10.1371\/journal.pone.0147600"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"6893560","DOI":"10.1155\/2017\/6893560","article-title":"AM966, an Antagonist of Lysophosphatidic Acid Receptor 1, Increases Lung Microvascular Endothelial Permeability through Activation of Rho Signaling Pathway and Phosphorylation of VE-Cadherin","volume":"2017","author":"Cai","year":"2017","journal-title":"Mediat. Inflamm."},{"key":"ref_42","first-page":"H708","article-title":"Coupling of endothelial injury and repair: An analysis using an in vivo experimental model","volume":"294","author":"Nogueras","year":"2008","journal-title":"Am. J. Physiol"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1002\/iub.220","article-title":"Lysophosphatidic acid in vascular development and disease","volume":"61","author":"Teo","year":"2009","journal-title":"IUBMB Life"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.biomaterials.2018.02.030","article-title":"3D-3-culture: A tool to unveil macrophage plasticity in the tumour microenvironment","volume":"163","author":"Rebelo","year":"2018","journal-title":"Biomaterials"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1186\/s12944-018-0835-0","article-title":"ANGPTL3 possibly promotes cardiac angiogenesis through improving proangiogenic ability of endothelial progenitor cells after myocardial infarction","volume":"17","author":"Luo","year":"2018","journal-title":"Lipids Health Dis."},{"doi-asserted-by":"crossref","unstructured":"Montenegro, F.S., Correia, M., Muccillo, F., Souza Silva, C.G.E., and De Lorenzo, A. (2018). Associations between endothelial progenitor cells, clinical characteristics and coronary restenosis in patients undergoing percutaneous coronary artery intervention. BMC Res. Notes, 11.","key":"ref_46","DOI":"10.1186\/s13104-018-3401-y"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"969","DOI":"10.2217\/rme-2017-0074","article-title":"Endothelial progenitor cells for cellular angiogenesis and repair: Lessons learned from experimental animal models","volume":"12","author":"Haider","year":"2017","journal-title":"Regen. Med."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.bcmd.2013.11.004","article-title":"Endothelial progenitors","volume":"52","author":"Pelosi","year":"2014","journal-title":"Blood Cells Mol. Dis."},{"key":"ref_49","first-page":"10","article-title":"Circulating and Tissue Resident Endothelial Progenitor Cells","volume":"229","author":"Basile","year":"2014","journal-title":"J. Cell. Physiol"},{"unstructured":"Curry, C.V. (2016). Differential Blood Count: Reference Range, Interpretation, Collection and Panels, Medscape.","key":"ref_50"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1046","DOI":"10.1161\/hc3501.093817","article-title":"Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines","volume":"104","author":"Kamihata","year":"2001","journal-title":"Circulation"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"C123","DOI":"10.1152\/ajpcell.00164.2013","article-title":"Bone marrow mononuclear cell angiogenic competency is suppressed by a high-salt diet","volume":"306","author":"Karcher","year":"2013","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1038\/modpathol.2008.48","article-title":"Bone marrow-derived mononuclear cell therapy induces distal angiogenesis after local injection in critical leg ischemia","volume":"21","author":"Smadja","year":"2008","journal-title":"Mod. Pathol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1546","DOI":"10.1101\/gad.436307","article-title":"Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization","volume":"21","author":"Nolan","year":"2007","journal-title":"Genes Dev."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"36659","DOI":"10.1038\/srep36659","article-title":"Macrophages form functional vascular mimicry channels in vivo","volume":"11","author":"Barnett","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2461","DOI":"10.1111\/j.1538-7836.2006.02193.x","article-title":"Vascular endothelial growth factor expression in monocytes from patients with primary antiphospholipid syndrome","volume":"4","author":"Cuadrado","year":"2006","journal-title":"J. Thromb. Haemost."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"3336","DOI":"10.1182\/blood.V87.8.3336.bloodjournal8783336","article-title":"Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1","volume":"87","author":"Barleon","year":"1996","journal-title":"Blood"},{"doi-asserted-by":"crossref","unstructured":"Zhou, T., Prather, E.R., Garrison, D.E., and Zuo, L. (2018). Interplay between ROS and antioxidants during ischemia-reperfusion injuries in cardiac and skeletal muscle. Int. J. Mol. Sci., 19.","key":"ref_58","DOI":"10.3390\/ijms19020417"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"5801209","DOI":"10.1155\/2018\/5801209","article-title":"Reactive Oxygen Species-Mediated Tumor Microenvironment Transformation: The Mechanism of Radioresistant Gastric Cancer","volume":"2018","author":"Gu","year":"2018","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1177271918755391","DOI":"10.1177\/1177271918755391","article-title":"Reactive Oxygen Species: A Key Constituent in Cancer Survival","volume":"13","author":"Kumari","year":"2018","journal-title":"Biomark. Insights"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.scr.2018.06.007","article-title":"Mitochondrial ROS direct the differentiation of murine pluripotent P19 cells","volume":"30","author":"Pashkovskaia","year":"2018","journal-title":"Stem Cell Res."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1097\/00000478-200109000-00007","article-title":"CD31 expression in intratumoral macrophages: A potential diagnostic pitfall","volume":"25","author":"McKenney","year":"2001","journal-title":"Am. J. Surg. Pathol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1111\/j.1538-7836.2012.04702.x","article-title":"Reduced von Willebrand factor secretion is associated with loss of Weibel-Palade body formation","volume":"10","author":"Castaman","year":"2012","journal-title":"J. Thromb. Haemost."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/S0008-6363(03)00252-9","article-title":"Endothelial progenitor cell culture and differentiation in vitro: A methodological comparison using human umbilical cord blood","volume":"58","author":"Eggermann","year":"2003","journal-title":"Cardiovasc. Res."},{"key":"ref_65","first-page":"1739","article-title":"Function of Kr\u00fcppel like factor 2 in the shear stress induced cell differentiation of endothelial progenitor cells to endothelial cells","volume":"19","author":"Chu","year":"2019","journal-title":"Mol. Med. Rep."},{"key":"ref_66","first-page":"1667","article-title":"VEGF secreted by Mesenchymal stem cells mediates the differentiation of endothelial progenitor cells into endothelial cells via paracrine mechanisms","volume":"17","author":"Ge","year":"2018","journal-title":"Mol. Med. Rep."},{"doi-asserted-by":"crossref","unstructured":"Nunes, S.C., Lopes-Coelho, F., Gouveia-Fernandes, S., Ramos, C., Pereira, S.A., and Serpa, J. (2018). Cysteine boosters the evolutionary adaptation to CoCl2mimicked hypoxia conditions, favouring carboplatin resistance in ovarian cancer. BMC Evol. Biol., 18.","key":"ref_67","DOI":"10.1186\/s12862-018-1214-1"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"9513","DOI":"10.1038\/s41598-018-27753-y","article-title":"Cysteine allows ovarian cancer cells to adapt to hypoxia and to escape from carboplatin cytotoxicity","volume":"8","author":"Nunes","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1182\/blood-2006-10-047092","article-title":"Identification of functional endothelial progenitor cells suitable for the treatment of ischemic tissue using human umbilical cord blood","volume":"110","author":"Nagano","year":"2007","journal-title":"Blood"},{"doi-asserted-by":"crossref","unstructured":"Weinberg, F., Ramnath, N., and Nagrath, D. (2019). Reactive Oxygen Species in the Tumor Microenvironment: An Overview. Cancers, 11.","key":"ref_70","DOI":"10.3390\/cancers11081191"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1182\/blood-2013-09-512749","article-title":"Oxidative stress in angiogenesis and vascular disease","volume":"123","author":"Kim","year":"2014","journal-title":"Blood"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/cmi.2017.135","article-title":"The chemokine MCP-1 (CCL2) in the host interaction with cancer: A foe or ally?","volume":"15","author":"Yoshimura","year":"2018","journal-title":"Cell. Mol. Immunol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1089\/jir.2008.0027","article-title":"Monocyte Chemoattractant Protein-1 (MCP-1): An Overview","volume":"29","author":"Deshmane","year":"2009","journal-title":"J. Interface Cytokine Res."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"28697","DOI":"10.18632\/oncotarget.7376","article-title":"Targeting the CCL2-CCR2 signaling axis in cancer metastasis","volume":"7","author":"Lim","year":"2016","journal-title":"Oncotarget"},{"key":"ref_75","first-page":"751","article-title":"Macrophage Migration Inhibitory Factor: A Multifunctional Cytokine in Rheumatic Diseases","volume":"20","author":"Kasama","year":"2010","journal-title":"Arthritis"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"2399","DOI":"10.1172\/JCI80467","article-title":"Macrophage migration inhibitory factor promotes cyst growth in polycystic kidney disease","volume":"125","author":"Chen","year":"2015","journal-title":"J. Clin. Investig."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1089\/10799900050151012","article-title":"Macrophage migration inhibitory factor (MIF): Its essential role in the immune system and cell growth","volume":"20","author":"Nishihira","year":"2000","journal-title":"J. Interface Cytokine Res."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"5533","DOI":"10.4049\/jimmunol.1201161","article-title":"Macrophage Migration Inhibitory Factor Promotes Tumor Growth and Metastasis by Inducing Myeloid-Derived Suppressor Cells in the Tumor Microenvironment","volume":"189","author":"Simpson","year":"2012","journal-title":"J. Immunol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"10650","DOI":"10.18632\/oncotarget.12890","article-title":"Macrophage migration inhibitory factor: A potential driver and biomarker for head and neck squamous cell carcinoma","volume":"8","author":"Wang","year":"2017","journal-title":"Oncotarget"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"2095","DOI":"10.1038\/onc.2016.367","article-title":"CXCL2\/MIF-CXCR2 signaling promotes the recruitment of myeloid-derived suppressor cells and is correlated with prognosis in bladder cancer","volume":"36","author":"Zhang","year":"2017","journal-title":"Oncogene"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"9916","DOI":"10.3748\/wjg.v21.i34.9916","article-title":"Macrophage migration inhibitory factor as a potential prognostic factor in gastric cancer","volume":"21","author":"He","year":"2015","journal-title":"World J. Gastroenterol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"17951","DOI":"10.18632\/oncotarget.24885","article-title":"Pathogenic role for macrophage migration inhibitory factor in glioblastoma and its targeting with specific inhibitors as novel tailored therapeutic approach","volume":"9","author":"Mangano","year":"2018","journal-title":"Oncotarget"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"1498","DOI":"10.1038\/bjc.2012.392","article-title":"Macrophage migration inhibitory factor produced by the tumour stroma but not by tumour cells regulates angiogenesis in the B16-F10 melanoma model","volume":"107","author":"Girard","year":"2012","journal-title":"Br. J. Cancer"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.3892\/ijmm.2016.2542","article-title":"Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K\/Akt\/mTOR and AMPK pathways","volume":"37","author":"Cui","year":"2016","journal-title":"Int. J. Mol. Med."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"73486","DOI":"10.18632\/oncotarget.11970","article-title":"Oxidized macrophage migration inhibitory factor is a potential new tissue marker and drug target in cancer","volume":"7","author":"Schinagl","year":"2016","journal-title":"Oncotarget"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"ii105","DOI":"10.1093\/annonc\/mdw200.11","article-title":"Safety and efficacy analysis of imalumab, an anti-oxidized macrophage migration inhibitory factor (oxMIF) antibody, alone or in combination with 5-fluorouracil\/leucovorin (5-FU\/LV) or panitumumab, in patients with metastatic colorectal cancer (mCRC)","volume":"27","author":"Mahalingam","year":"2016","journal-title":"Ann. Oncol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1040","DOI":"10.1172\/JCI20465","article-title":"VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment","volume":"113","author":"Cursiefen","year":"2004","journal-title":"J. Clin. Investig."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"2637","DOI":"10.4049\/jimmunol.171.5.2637","article-title":"M-CSF Induces Vascular Endothelial Growth Factor Production and Angiogenic Activity From Human Monocytes","volume":"171","author":"Eubank","year":"2003","journal-title":"J. Immunol."},{"key":"ref_89","first-page":"2637","article-title":"A1 adenosine receptor activation promotes angiogenesis and release of VEGF from monocytes","volume":"171","author":"Clark","year":"2007","journal-title":"Circ. Res."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"2106","DOI":"10.1016\/j.bbadis.2014.07.008","article-title":"Vascular wall extracellular matrix proteins and vascular diseases","volume":"1842","author":"Xu","year":"2014","journal-title":"Biochim. Biophys. Acta"},{"doi-asserted-by":"crossref","unstructured":"Malinda, K.M. (2009). In vivo Matrigel Migration and Angiogenesis Assay. Methods in Molecular Biology, Springer.","key":"ref_91","DOI":"10.1007\/978-1-59745-241-0_17"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1186\/s13287-018-0769-5","article-title":"Evaluation of ex vivo produced endothelial progenitor cells for autologous transplantation in primates","volume":"9","author":"Qin","year":"2018","journal-title":"Stem Cell Res. Ther."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.jss.2018.06.066","article-title":"Exosomes of endothelial progenitor cells inhibit neointima formation after carotid artery injury","volume":"232","author":"Kong","year":"2018","journal-title":"J. Surg. Res."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1755","DOI":"10.1016\/j.metabol.2016.09.007","article-title":"Endothelial progenitor cells from human fetal aorta cure diabetic foot in a rat model","volume":"65","author":"Zhao","year":"2016","journal-title":"Metabolism"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"2333","DOI":"10.1172\/JCI27154","article-title":"Endothelial cell-restricted disruption of FoxM1 impairs endothelial repair following LPS-induced vascular injury","volume":"116","author":"Zhao","year":"2006","journal-title":"J. Clin. Investig."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1556\/EuJMI.2.2012.2.1","article-title":"Monocytes in health and disease\u2014Minireview","volume":"2","author":"Karlmark","year":"2012","journal-title":"Eur. J. Microbiol. Immunol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1002\/JLB.4RI0818-311R","article-title":"Monocyte heterogeneity and functions in cancer","volume":"106","author":"Olingy","year":"2019","journal-title":"J. Leukoc. Biol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"3336","DOI":"10.15252\/embj.201797345","article-title":"Tumor-associated macrophages (TAMs) depend on ZEB1 for their cancer-promoting roles","volume":"36","author":"Darling","year":"2017","journal-title":"EMBO J."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/s12943-019-0976-4","article-title":"Crosstalk between cancer cells and tumor associated macrophages is required for mesenchymal circulating tumor cell-mediated colorectal cancer metastasis","volume":"18","author":"Wei","year":"2019","journal-title":"Mol. Cancer"},{"key":"ref_100","first-page":"1010428318756203","article-title":"Metabolic cooperation between cancer and non-cancerous stromal cells is pivotal in cancer progression","volume":"40","author":"Serpa","year":"2018","journal-title":"Tumor Biol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1038\/s41467-017-00523-6","article-title":"Caspase-1 cleaves PPAR\u03b3 for potentiating the pro-tumor action of TAMs","volume":"8","author":"Niu","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1228","DOI":"10.1093\/biolre\/ioy265","article-title":"Bone-marrow-derived endothelial progenitor cells contribute to vasculogenesis of pregnant mouse uterus","volume":"100","author":"Tal","year":"2019","journal-title":"Biol. Reprod."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"556","DOI":"10.3389\/fphys.2018.00556","article-title":"Circulating endothelial progenitor cells present an inflammatory phenotype and function in patients with alcoholic liver cirrhosis","volume":"9","author":"Kaur","year":"2018","journal-title":"Front. Physiol."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/9\/1\/107\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T13:18:39Z","timestamp":1760361519000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/9\/1\/107"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,1]]},"references-count":103,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,1]]}},"alternative-id":["cells9010107"],"URL":"https:\/\/doi.org\/10.3390\/cells9010107","relation":{},"ISSN":["2073-4409"],"issn-type":[{"type":"electronic","value":"2073-4409"}],"subject":[],"published":{"date-parts":[[2020,1,1]]}}}