{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T17:34:11Z","timestamp":1792690451355,"version":"4.5.0"},"reference-count":57,"publisher":"National Academy of Sciences","issue":"30","license":[{"start":{"date-parts":[[2020,1,3]],"date-time":"2020-01-03T00:00:00Z","timestamp":1578009600000},"content-version":"vor","delay-in-days":184,"URL":"https:\/\/www.pnas.org\/site\/aboutpnas\/licenses.xhtml"}],"funder":[{"DOI":"10.13039\/501100003593","name":"MCTI | Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["403248\/2016-7"],"award-info":[{"award-number":["403248\/2016-7"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002322","name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior","doi-asserted-by":"publisher","award":["Finance Code 001"],"award-info":[{"award-number":["Finance Code 001"]}],"id":[{"id":"10.13039\/501100002322","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["1853949"],"award-info":[{"award-number":["1853949"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"HHS | National Institutes of Health","doi-asserted-by":"publisher","award":["R01OD011116"],"award-info":[{"award-number":["R01OD011116"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003593","name":"MCTI | Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["307479\/2016-1"],"award-info":[{"award-number":["307479\/2016-1"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002322","name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior","doi-asserted-by":"publisher","award":["88887.130628\/2016-00"],"award-info":[{"award-number":["88887.130628\/2016-00"]}],"id":[{"id":"10.13039\/501100002322","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002322","name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior","doi-asserted-by":"publisher","award":["88887.198757\/2018-00"],"award-info":[{"award-number":["88887.198757\/2018-00"]}],"id":[{"id":"10.13039\/501100002322","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2019,7,23]]},"abstract":"<jats:p>\n                    Salamanders and lungfishes are the only sarcopterygians (lobe-finned vertebrates) capable of paired appendage regeneration, regardless of the amputation level. Among actinopterygians (ray-finned fishes), regeneration after amputation at the fin endoskeleton has only been demonstrated in polypterid fishes (Cladistia). Whether this ability evolved independently in sarcopterygians and actinopterygians or has a common origin remains unknown. Here we combine fin regeneration assays and comparative RNA-sequencing (RNA-seq) analysis of\n                    <jats:italic>Polypterus<\/jats:italic>\n                    and axolotl blastemas to provide support for a common origin of paired appendage regeneration in Osteichthyes (bony vertebrates). We show that, in addition to polypterids, regeneration after fin endoskeleton amputation occurs in extant representatives of 2 other nonteleost actinopterygians: the American paddlefish (Chondrostei) and the spotted gar (Holostei). Furthermore, we assessed regeneration in 4 teleost species and show that, with the exception of the blue gourami (Anabantidae), 3 species were capable of regenerating fins after endoskeleton amputation: the white convict and the oscar (Cichlidae), and the goldfish (Cyprinidae). Our comparative RNA-seq analysis of regenerating blastemas of axolotl and\n                    <jats:italic>Polypterus<\/jats:italic>\n                    reveals the activation of common genetic pathways and expression profiles, consistent with a shared genetic program of appendage regeneration. Comparison of RNA-seq data from early\n                    <jats:italic>Polypterus<\/jats:italic>\n                    blastema to single-cell RNA-seq data from axolotl limb bud and limb regeneration stages shows that\n                    <jats:italic>Polypterus<\/jats:italic>\n                    and axolotl share a regeneration-specific genetic program. Collectively, our findings support a deep evolutionary origin of paired appendage regeneration in Osteichthyes and provide an evolutionary framework for studies on the genetic basis of appendage regeneration.\n                  <\/jats:p>","DOI":"10.1073\/pnas.1900475116","type":"journal-article","created":{"date-parts":[[2019,7,3]],"date-time":"2019-07-03T18:35:17Z","timestamp":1562178917000},"page":"15106-15115","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":74,"title":["Deep evolutionary origin of limb and fin regeneration"],"prefix":"10.1073","volume":"116","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6351-0903","authenticated-orcid":false,"given":"Sylvain","family":"Darnet","sequence":"first","affiliation":[{"name":"Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal do Par\u00e1, 66075-900 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aline C.","family":"Dragalzew","sequence":"additional","affiliation":[{"name":"Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal do Par\u00e1, 66075-900 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Danielson B.","family":"Amaral","sequence":"additional","affiliation":[{"name":"Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal do Par\u00e1, 66075-900 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Josane F.","family":"Sousa","sequence":"additional","affiliation":[{"name":"Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal do Par\u00e1, 66075-900 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew W.","family":"Thompson","sequence":"additional","affiliation":[{"name":"Department of Integrative Biology, Program in Ecology, Evolutionary Biology, and Behavior, Michigan State University, East Lansing, MI 48824;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amanda N.","family":"Cass","sequence":"additional","affiliation":[{"name":"Department of Biology, James Madison University, Harrisonburg, VA 22807;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jamily","family":"Lorena","sequence":"additional","affiliation":[{"name":"Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal do Par\u00e1, 66075-900 Bel\u00e9m, Brazil;"},{"name":"Instituto Tecnol\u00f3gico Vale, 66055-090 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eder S.","family":"Pires","sequence":"additional","affiliation":[{"name":"Instituto Tecnol\u00f3gico Vale, 66055-090 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carinne M.","family":"Costa","sequence":"additional","affiliation":[{"name":"Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal do Par\u00e1, 66075-900 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcos P.","family":"Sousa","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Biologia Molecular, Museu Paraense Em\u00edlio Goeldi, 66077-530 Bel\u00e9m, Par\u00e1, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadia B.","family":"Fr\u00f6bisch","sequence":"additional","affiliation":[{"name":"Museum f\u00fcr Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, 10115 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0054-3438","authenticated-orcid":false,"given":"Guilherme","family":"Oliveira","sequence":"additional","affiliation":[{"name":"Instituto Tecnol\u00f3gico Vale, 66055-090 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patricia N.","family":"Schneider","sequence":"additional","affiliation":[{"name":"Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal do Par\u00e1, 66075-900 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcus C.","family":"Davis","sequence":"additional","affiliation":[{"name":"Department of Biology, James Madison University, Harrisonburg, VA 22807;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ingo","family":"Braasch","sequence":"additional","affiliation":[{"name":"Department of Integrative Biology, Program in Ecology, Evolutionary Biology, and Behavior, Michigan State University, East Lansing, MI 48824;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9046-7338","authenticated-orcid":false,"given":"Igor","family":"Schneider","sequence":"additional","affiliation":[{"name":"Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal do Par\u00e1, 66075-900 Bel\u00e9m, Brazil;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2019,7,3]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1146\/annurev.ecolsys.38.091206.095546","article-title":"Ever since Owen: Changing perspectives on the early evolution of tetrapods","volume":"39","author":"Coates M. 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Shubin, The origin of the tetrapod limb: From expeditions to enhancers. Trends Genet. 29, 419\u2013426 (2013).","journal-title":"Trends Genet."},{"key":"e_1_3_4_4_2","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1002\/wdev.73","article-title":"Limb regeneration","volume":"2","author":"Simon A.","year":"2013","unstructured":"A. Simon, E. M. Tanaka, Limb regeneration. Wiley Interdiscip. Rev. Dev. Biol. 2, 291\u2013300 (2013).","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"e_1_3_4_5_2","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1042\/BST20140002","article-title":"Mechanisms underlying vertebrate limb regeneration: Lessons from the salamander","volume":"42","author":"Brockes J. P.","year":"2014","unstructured":"J. P. Brockes, P. B. Gates, Mechanisms underlying vertebrate limb regeneration: Lessons from the salamander. Biochem. Soc. Trans. 42, 625\u2013630 (2014).","journal-title":"Biochem. Soc. 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Morphol."},{"key":"e_1_3_4_8_2","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1038\/nature15397","article-title":"Deep-time evolution of regeneration and preaxial polarity in tetrapod limb development","volume":"527","author":"Fr\u00f6bisch N. B.","year":"2015","unstructured":"N. B. Fr\u00f6bisch, C. Bickelmann, J. C. Olori, F. Witzmann, Deep-time evolution of regeneration and preaxial polarity in tetrapod limb development. Nature 527, 231\u2013234 (2015).","journal-title":"Nature"},{"key":"e_1_3_4_9_2","first-page":"20141550","article-title":"Early evolution of limb regeneration in tetrapods: Evidence from a 300-million-year-old amphibian","volume":"281","author":"Frobisch N. B.","year":"2014","unstructured":"N. B. Frobisch, C. Bickelmann, F. Witzmann, Early evolution of limb regeneration in tetrapods: Evidence from a 300-million-year-old amphibian. Proc. Biol. Sci. 281, 20141550 (2014).","journal-title":"Proc. Biol. Sci."},{"key":"e_1_3_4_10_2","doi-asserted-by":"crossref","first-page":"e23052","DOI":"10.1002\/dvg.23052","article-title":"Fins into limbs: Recent insights from sarcopterygian fish","volume":"56","author":"Amaral D. B.","year":"2018","unstructured":"D. B. Amaral, I. Schneider, Fins into limbs: Recent insights from sarcopterygian fish. Genesis 56, e23052 (2018).","journal-title":"Genesis"},{"key":"e_1_3_4_11_2","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1002\/dvdy.10248","article-title":"Old questions, new tools, and some answers to the mystery of fin regeneration","volume":"226","author":"Akimenko M.-A.","year":"2003","unstructured":"M.-A. Akimenko, M. Mar\u00ed-Beffa, J. Becerra, J. G\u00e9raudie, Old questions, new tools, and some answers to the mystery of fin regeneration. Dev. Dyn. 226, 190\u2013201 (2003).","journal-title":"Dev. Dyn."},{"key":"e_1_3_4_12_2","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1046\/j.1525-142X.2003.03028.x","article-title":"Why is limb regeneration possible in amphibians but not in reptiles, birds, and mammals?","volume":"5","author":"Galis F.","year":"2003","unstructured":"F. Galis, G. P. Wagner, E. L. Jockusch, Why is limb regeneration possible in amphibians but not in reptiles, birds, and mammals? Evol. Dev. 5, 208\u2013220 (2003).","journal-title":"Evol. Dev."},{"key":"e_1_3_4_13_2","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1002\/jez.b.21295","article-title":"Fin regeneration from tail segment with musculature, endoskeleton, and scales","volume":"312","author":"Shao J.","year":"2009","unstructured":"J. Shao, X. Qian, C. Zhang, Z. Xu, Fin regeneration from tail segment with musculature, endoskeleton, and scales. J. Exp. Zoolog. B Mol. Dev. Evol. 312, 762\u2013769 (2009).","journal-title":"J. Exp. Zoolog. B Mol. Dev. Evol."},{"key":"e_1_3_4_14_2","doi-asserted-by":"crossref","first-page":"3838","DOI":"10.1073\/pnas.1006619109","article-title":"Full regeneration of the tribasal Polypterus fin","volume":"109","author":"Cuervo R.","year":"2012","unstructured":"R. Cuervo, R. Hern\u00e1ndez-Mart\u00ednez, J. Chimal-Monroy, H. Merchant-Larios, L. Covarrubias, Full regeneration of the tribasal Polypterus fin. Proc. Natl. Acad. Sci. U.S.A. 109, 3838\u20133843 (2012).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_15_2","first-page":"136","article-title":"[Characteristics of the reparative regeneration of fins in the polypterid fish (Polypteridae, Actinopterygii)] [in Russian]","volume":"43","author":"Nikiforova A. I.","year":"2012","unstructured":"A. I. Nikiforova, V. A. Golichenkov, [Characteristics of the reparative regeneration of fins in the polypterid fish (Polypteridae, Actinopterygii)] [in Russian]. Ontogenez 43, 136\u2013142 (2012).","journal-title":"Ontogenez"},{"key":"e_1_3_4_16_2","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1186\/s12862-017-0958-3","article-title":"Phylogenetic classification of bony fishes","volume":"17","author":"Betancur-R R.","year":"2017","unstructured":"R. Betancur-R ., Phylogenetic classification of bony fishes. BMC Evol. Biol. 17, 162 (2017).","journal-title":"BMC Evol. Biol."},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"6249","DOI":"10.1073\/pnas.1719358115","article-title":"Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data","volume":"115","author":"Hughes L. C.","year":"2018","unstructured":"L. C. Hughes ., Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data. Proc. Natl. Acad. Sci. U.S.A. 115, 6249\u20136254 (2018).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_18_2","unstructured":"S. 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Science 362, eaaq0681 (2018).","journal-title":"Science"},{"key":"e_1_3_4_29_2","doi-asserted-by":"crossref","first-page":"dev169128","DOI":"10.1242\/dev.169128","article-title":"Blastemal progenitors modulate immune signaling during early limb regeneration","volume":"146","author":"Tsai S. L.","year":"2019","unstructured":"S. L. Tsai, C. Baselga-Garriga, D. A. Melton, Blastemal progenitors modulate immune signaling during early limb regeneration. Development 146, dev169128 (2019).","journal-title":"Development"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"9415","DOI":"10.1073\/pnas.1300290110","article-title":"Macrophages are required for adult salamander limb regeneration","volume":"110","author":"Godwin J. W.","year":"2013","unstructured":"J. W. Godwin, A. R. Pinto, N. A. Rosenthal, Macrophages are required for adult salamander limb regeneration. Proc. Natl. Acad. Sci. U.S.A. 110, 9415\u20139420 (2013).","journal-title":"Proc. Natl. Acad. Sci. 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