{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T07:23:19Z","timestamp":1789024999827,"version":"build-2803163510"},"reference-count":60,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2024,11,6]],"date-time":"2024-11-06T00:00:00Z","timestamp":1730851200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"DoD","award":["W81XWH-11-1-0597"],"award-info":[{"award-number":["W81XWH-11-1-0597"]}]},{"name":"DoD","award":["W81XWH-11-1-0598"],"award-info":[{"award-number":["W81XWH-11-1-0598"]}]},{"name":"DoD","award":["09BR-02"],"award-info":[{"award-number":["09BR-02"]}]},{"name":"DoD","award":["1R43CA195882-01A1"],"award-info":[{"award-number":["1R43CA195882-01A1"]}]},{"name":"Florida Department of Health Bankhead Coley Cancer Research Program","award":["W81XWH-11-1-0597"],"award-info":[{"award-number":["W81XWH-11-1-0597"]}]},{"name":"Florida Department of Health Bankhead Coley Cancer Research Program","award":["W81XWH-11-1-0598"],"award-info":[{"award-number":["W81XWH-11-1-0598"]}]},{"name":"Florida Department of Health Bankhead Coley Cancer Research Program","award":["09BR-02"],"award-info":[{"award-number":["09BR-02"]}]},{"name":"Florida Department of Health Bankhead Coley Cancer Research Program","award":["1R43CA195882-01A1"],"award-info":[{"award-number":["1R43CA195882-01A1"]}]},{"name":"NCI\/SBIR","award":["W81XWH-11-1-0597"],"award-info":[{"award-number":["W81XWH-11-1-0597"]}]},{"name":"NCI\/SBIR","award":["W81XWH-11-1-0598"],"award-info":[{"award-number":["W81XWH-11-1-0598"]}]},{"name":"NCI\/SBIR","award":["09BR-02"],"award-info":[{"award-number":["09BR-02"]}]},{"name":"NCI\/SBIR","award":["1R43CA195882-01A1"],"award-info":[{"award-number":["1R43CA195882-01A1"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Lymphoma growth, progression, and dissemination require tumor cell interaction with supporting vessels and are facilitated through tumor-promoted angiogenesis, lymphangiogenesis, and\/or lymphoma vessel co-option. Vessel co-option has been shown to be responsible for tumor initiation, metastasis, and resistance to anti-angiogenic treatment but is largely uncharacterized in the setting of lymphoma. We developed an in vitro model to study lymphoma\u2013vessel interactions and found that mantle cell lymphoma (MCL) cells co-cultured on Matrigel with human umbilical vein (HUVEC) or human lymphatic (HLEC) endothelial cells migrate to and anneal with newly formed capillary-like (CLS) or lymphatic-like (LLS) structures, consistent with lymphoma\u2013vessel co-option. To inhibit this interaction, we constructed an antibody fusion protein, \u03b1CD20-EndoP125A, linking mutant anti-angiogenic endostatin (EndoP125A) to an \u03b1CD20-IgG1-targeting antibody. \u03b1CD20-EndoP125A inhibited both CLS and LLS formation, as well as MCL migration and vessel co-option. Lymphoma vessel co-option requires cell migration, which is regulated by chemokine\u2013chemokine receptor interactions. CXCL12 and its receptor, CXCR4, are highly expressed by both endothelial cells forming CLS and by MCL cells during vessel co-option. \u03b1CD20-EndoP125A suppressed expression of both CXCL12 and CXCR4, which were required to facilitate CLS assembly and vessel co-option. We also tested \u03b1CD20-EndoP125A effects in vivo using an aggressive murine B cell lymphoma model, 38c13-hCD20, which demonstrated rapid growth and dissemination to tumor-draining lymph nodes (TDLNs) and the spleen, lung, and brain. The pattern of lymphoma distribution and growth within the lung was consistent with vessel co-option. As predicted by our in vitro model, \u03b1CD20-EndoP125A treatment inhibited primary tumor growth, angiogenesis, and lymphangiogenesis, and markedly reduced the number of circulating tumor cells and lymphoma dissemination to TDLNs and the lungs, spleen, and brain. \u03b1CD20-EndoP125A inhibited lymphoma vessel co-option within the lung. Marked inhibition of MCL primary tumor growth and dissemination were also seen using an MCL xenograft model. The ability of \u03b1CD20-EndoP125A to inhibit angiogenesis, lymphangiogenesis, and lymphoma vessel co-option provides a novel therapeutic approach for inhibition of lymphoma progression and dissemination.<\/jats:p>","DOI":"10.3390\/cells13221835","type":"journal-article","created":{"date-parts":[[2024,11,6]],"date-time":"2024-11-06T06:27:39Z","timestamp":1730874459000},"page":"1835","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Modeling Lymphoma Angiogenesis, Lymphangiogenesis, and Vessel Co-Option, and the Effects of Inhibition of Lymphoma\u2013Vessel Interactions with an \u03b1CD20-EndoP125A Antibody Fusion Protein"],"prefix":"10.3390","volume":"13","author":[{"given":"Christian","family":"Elledge","sequence":"first","affiliation":[{"name":"Division of Hematology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sheila & David Fuente Graduate Program in Cancer Biology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Zhang","sequence":"additional","affiliation":[{"name":"Division of Hematology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seung-Uon","family":"Shin","sequence":"additional","affiliation":[{"name":"Division of Hematology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hyun-Mi","family":"Cho","sequence":"additional","affiliation":[{"name":"Division of Hematology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sundaram","family":"Ramakrishnan","sequence":"additional","affiliation":[{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Surgery, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ankita","family":"Sankar","sequence":"additional","affiliation":[{"name":"Division of Hematology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sheila & David Fuente Graduate Program in Cancer Biology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer R.","family":"Chapman","sequence":"additional","affiliation":[{"name":"Division of Hematology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Pathology and Laboratory Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1630-8811","authenticated-orcid":false,"given":"Daniel","family":"Bilbao","sequence":"additional","affiliation":[{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Pathology and Laboratory Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rathin","family":"Das","sequence":"additional","affiliation":[{"name":"Synergys Biotherapeutics Inc., Alamo, CA 94595, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4064-0478","authenticated-orcid":false,"given":"Hava","family":"Gil-Henn","sequence":"additional","affiliation":[{"name":"The Azrieli Faculty of Medicine, Bar-Ilan University, Safed 13115, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9346-9013","authenticated-orcid":false,"given":"Izidore S.","family":"Lossos","sequence":"additional","affiliation":[{"name":"Division of Hematology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sheila & David Fuente Graduate Program in Cancer Biology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph D.","family":"Rosenblatt","sequence":"additional","affiliation":[{"name":"Division of Hematology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Department of Medicine, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sheila & David Fuente Graduate Program in Cancer Biology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"},{"name":"Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,11,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1007\/s10456-020-09729-7","article-title":"B-cell non-Hodgkin lymphoma: Importance of angiogenesis and antiangiogenic therapy","volume":"23","author":"Jiang","year":"2020","journal-title":"Angiogenesis"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2495","DOI":"10.1056\/NEJMra2202672","article-title":"Mantle-Cell Lymphoma","volume":"386","author":"Armitage","year":"2022","journal-title":"N. 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