{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,25]],"date-time":"2026-03-25T23:59:16Z","timestamp":1774483156109,"version":"3.50.1"},"reference-count":65,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2022,1,24]],"date-time":"2022-01-24T00:00:00Z","timestamp":1642982400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["HL085210"],"award-info":[{"award-number":["HL085210"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["NS073815"],"award-info":[{"award-number":["NS073815"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["HL132264"],"award-info":[{"award-number":["HL132264"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Cardiovascular Research Institute of Vermont"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,3,16]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Transplantation of stem\/progenitor cells holds promise for cardiac regeneration in patients with myocardial infarction (MI). Currently, however, low cell survival and engraftment after transplantation present a major barrier to many forms of cell therapy. One issue is that ligands, receptors, and signaling pathways that promote graft success remain poorly understood. Here, we prospectively isolate uncommitted epicardial cells from the adult heart surface by CD104 (\u03b2-4 integrin) and demonstrate that C-terminal peptide from connective tissue growth factor (CTGF-D4), when combined with insulin, effectively primes epicardial-derived cells (EPDC) for cardiac engraftment after MI. Similar to native epicardial derivatives that arise from epicardial EMT at the heart surface, the grafted cells migrated into injured myocardial tissue in a rat model of MI with reperfusion. By echocardiography, at 1 month after MI, we observed significant improvement in cardiac function for animals that received epicardial cells primed with CTGF-D4\/insulin compared with those that received vehicle-primed (control) cells. In the presence of insulin, CTGF-D4 treatment significantly increased the phosphorylation of Wnt co-receptor LRP6 on EPDC. Competitive engraftment assays and neutralizing\/blocking studies showed that LRP6 was required for EPDC engraftment after transplantation. Our results identify LRP6 as a key target for increasing EPDC engraftment after MI and suggest amplification of LRP6 signaling with CTGF-D4\/insulin, or by other means, may provide an effective approach for achieving successful cellular grafts in regenerative medicine.<\/jats:p>","DOI":"10.1093\/stmcls\/sxab016","type":"journal-article","created":{"date-parts":[[2022,1,1]],"date-time":"2022-01-01T04:47:46Z","timestamp":1641012466000},"page":"204-214","source":"Crossref","is-referenced-by-count":5,"title":["CTGF-D4 Amplifies LRP6 Signaling to Promote Grafts of Adult Epicardial-derived Cells That Improve Cardiac Function After Myocardial Infarction"],"prefix":"10.1093","volume":"40","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2307-8583","authenticated-orcid":false,"given":"Krithika S","family":"Rao","sequence":"first","affiliation":[{"name":"Department of Medicine, Stem Cell Core, University of Vermont, Colchester, VT 05446, USA"},{"name":"Cardiovascular Research Institute, University of Vermont, Colchester, VT 05446, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jessica E","family":"Kloppenburg","sequence":"additional","affiliation":[{"name":"Department of Medicine, Stem Cell Core, University of Vermont, Colchester, VT 05446, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Taylor","family":"Marquis","sequence":"additional","affiliation":[{"name":"Department of Medicine, Stem Cell Core, University of Vermont, Colchester, VT 05446, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Laura","family":"Solomon","sequence":"additional","affiliation":[{"name":"Department of Medicine, Stem Cell Core, University of Vermont, Colchester, VT 05446, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Keara L","family":"McElroy-Yaggy","sequence":"additional","affiliation":[{"name":"Department of Medicine, Stem Cell Core, University of Vermont, Colchester, VT 05446, USA"},{"name":"Cardiovascular Research Institute, University of Vermont, Colchester, VT 05446, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeffrey L","family":"Spees","sequence":"additional","affiliation":[{"name":"Department of Medicine, Stem Cell Core, University of Vermont, Colchester, VT 05446, USA"},{"name":"Cardiovascular Research Institute, University of Vermont, Colchester, VT 05446, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2022,1,24]]},"reference":[{"key":"2022031609313087800_CIT0001","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1038\/nature10147","article-title":"Heart regeneration.","volume":"473","author":"Laflamme","year":"2011","journal-title":"Nature."},{"key":"2022031609313087800_CIT0002","doi-asserted-by":"crossref","first-page":"H2139","DOI":"10.1152\/ajpheart.00063.2012","article-title":"The role of neuregulin\/ErbB2\/ErbB4 signaling in the heart with special focus on effects on cardiomyocyte proliferation.","volume":"302","author":"Wadugu","year":"2012","journal-title":"Am J Physiol Heart Circ Physiol."},{"key":"2022031609313087800_CIT0003","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1016\/j.vph.2012.08.001","article-title":"Epicardial progenitor cells in cardiac regeneration and neovascularisation.","volume":"58","author":"Smart","year":"2013","journal-title":"Vascul Pharmacol."},{"key":"2022031609313087800_CIT0004","doi-asserted-by":"crossref","first-page":"2057","DOI":"10.1016\/j.jacc.2015.03.520","article-title":"Interacting resident epicardium-derived fibroblasts and recruited bone marrow cells form myocardial infarction scar.","volume":"65","author":"Ruiz-Villalba","year":"2015","journal-title":"J Am Coll Cardiol."},{"key":"2022031609313087800_CIT0005","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/B978-0-12-387786-4.00007-5","article-title":"An epicardial floor plan for building and rebuilding the mammalian heart.","volume":"100","author":"Riley","year":"2012","journal-title":"Curr Top Dev Biol."},{"key":"2022031609313087800_CIT0006","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.ydbio.2012.07.007","article-title":"Pan-epicardial lineage tracing reveals that epicardium derived cells give rise to myofibroblasts and perivascular cells during zebrafish heart regeneration.","volume":"370","author":"Gonzalez-Rosa","year":"2012","journal-title":"Dev Biol."},{"key":"2022031609313087800_CIT0007","doi-asserted-by":"crossref","first-page":"1719","DOI":"10.1089\/scd.2014.0019","article-title":"Re-activated adult epicardial progenitor cells are a heterogeneous population molecularly distinct from their embryonic counterparts.","volume":"23","author":"Bollini","year":"2014","journal-title":"Stem Cells Dev."},{"key":"2022031609313087800_CIT0008","first-page":"1056","article-title":"Epicardium-derived cells (EPDCs) in development, cardiac disease and repair of ischemia.","volume":"14","author":"Gittenberger-de Groot","year":"2010","journal-title":"J Cell Mol Med."},{"key":"2022031609313087800_CIT0009","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.diff.2012.05.002","article-title":"The arterial and cardiac epicardium in development, disease and repair.","volume":"84","author":"Gittenberger-de Groot","year":"2012","journal-title":"Differentiation."},{"key":"2022031609313087800_CIT0010","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.yjmcc.2013.10.005","article-title":"Differential expression of embryonic epicardial progenitor markers and localization of cardiac fibrosis in adult ischemic injury and hypertensive heart disease.","volume":"65","author":"Braitsch","year":"2013","journal-title":"J Mol Cell Cardiol."},{"key":"2022031609313087800_CIT0011","doi-asserted-by":"crossref","first-page":"904","DOI":"10.1161\/RES.0b013e31825332a3","article-title":"Epicardium-derived cardiac mesenchymal stem cells: 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