Structural and Functional Characterization of the FGF Signaling Pathway in Regeneration of the Polychaete Worm Alitta virens (Annelida, Errantia)
Epimorphic regeneration of lost body segments is a widespread phenomenon across annelids. However, the molecular inducers of the cell sources for this reparative morphogenesis have not been identified. In this study, we focused on the role of fibroblast growth factor (FGF) signaling in the posterior...
Saved in:
Published in | Genes Vol. 12; no. 6; p. 788 |
---|---|
Main Authors | , , |
Format | Journal Article |
Language | English |
Published |
Switzerland
MDPI AG
21.05.2021
MDPI |
Subjects | |
Online Access | Get full text |
Cover
Loading…
Abstract | Epimorphic regeneration of lost body segments is a widespread phenomenon across annelids. However, the molecular inducers of the cell sources for this reparative morphogenesis have not been identified. In this study, we focused on the role of fibroblast growth factor (FGF) signaling in the posterior regeneration of
. For the first time, we showed an early activation of FGF ligands and receptor expression in an annelid regenerating after amputation. The expression patterns indicate that the entire regenerative bud is competent to FGFs, whose activity precedes the initiation of cell proliferation. The critical requirement of FGF signaling, especially at early stages, is also supported by inhibitor treatments followed by proliferation assay, demonstrating that induction of blastemal cells depends on FGFs. Our results show that FGF signaling pathway is a key player in regenerative response, while the FGF-positive wound epithelium, ventral nerve cord and some mesodermal cells around the gut could be the inducing tissues. This mechanism resembles reparative regeneration of vertebrate appendages suggesting such a response to the injury may be ancestral for all bilaterians. |
---|---|
AbstractList | Epimorphic regeneration of lost body segments is a widespread phenomenon across annelids. However, the molecular inducers of the cell sources for this reparative morphogenesis have not been identified. In this study, we focused on the role of fibroblast growth factor (FGF) signaling in the posterior regeneration of
. For the first time, we showed an early activation of FGF ligands and receptor expression in an annelid regenerating after amputation. The expression patterns indicate that the entire regenerative bud is competent to FGFs, whose activity precedes the initiation of cell proliferation. The critical requirement of FGF signaling, especially at early stages, is also supported by inhibitor treatments followed by proliferation assay, demonstrating that induction of blastemal cells depends on FGFs. Our results show that FGF signaling pathway is a key player in regenerative response, while the FGF-positive wound epithelium, ventral nerve cord and some mesodermal cells around the gut could be the inducing tissues. This mechanism resembles reparative regeneration of vertebrate appendages suggesting such a response to the injury may be ancestral for all bilaterians. Epimorphic regeneration of lost body segments is a widespread phenomenon across annelids. However, the molecular inducers of the cell sources for this reparative morphogenesis have not been identified. In this study, we focused on the role of fibroblast growth factor (FGF) signaling in the posterior regeneration of Alitta virens. For the first time, we showed an early activation of FGF ligands and receptor expression in an annelid regenerating after amputation. The expression patterns indicate that the entire regenerative bud is competent to FGFs, whose activity precedes the initiation of cell proliferation. The critical requirement of FGF signaling, especially at early stages, is also supported by inhibitor treatments followed by proliferation assay, demonstrating that induction of blastemal cells depends on FGFs. Our results show that FGF signaling pathway is a key player in regenerative response, while the FGF-positive wound epithelium, ventral nerve cord and some mesodermal cells around the gut could be the inducing tissues. This mechanism resembles reparative regeneration of vertebrate appendages suggesting such a response to the injury may be ancestral for all bilaterians. Epimorphic regeneration of lost body segments is a widespread phenomenon across annelids. However, the molecular inducers of the cell sources for this reparative morphogenesis have not been identified. In this study, we focused on the role of fibroblast growth factor (FGF) signaling in the posterior regeneration of Alitta virens . For the first time, we showed an early activation of FGF ligands and receptor expression in an annelid regenerating after amputation. The expression patterns indicate that the entire regenerative bud is competent to FGFs, whose activity precedes the initiation of cell proliferation. The critical requirement of FGF signaling, especially at early stages, is also supported by inhibitor treatments followed by proliferation assay, demonstrating that induction of blastemal cells depends on FGFs. Our results show that FGF signaling pathway is a key player in regenerative response, while the FGF-positive wound epithelium, ventral nerve cord and some mesodermal cells around the gut could be the inducing tissues. This mechanism resembles reparative regeneration of vertebrate appendages suggesting such a response to the injury may be ancestral for all bilaterians. |
Author | Shalaeva, Alexandra Y Kozin, Vitaly V Kostyuchenko, Roman P |
AuthorAffiliation | Department of Embryology, St. Petersburg State University, Universitetskaya nab. 7–9, 199034 St. Petersburg, Russia; st041951@spbu.ru (A.Y.S.); r.kostyuchenko@spbu.ru (R.P.K.) |
AuthorAffiliation_xml | – name: Department of Embryology, St. Petersburg State University, Universitetskaya nab. 7–9, 199034 St. Petersburg, Russia; st041951@spbu.ru (A.Y.S.); r.kostyuchenko@spbu.ru (R.P.K.) |
Author_xml | – sequence: 1 givenname: Alexandra Y orcidid: 0000-0002-4621-136X surname: Shalaeva fullname: Shalaeva, Alexandra Y organization: Department of Embryology, St. Petersburg State University, Universitetskaya nab. 7-9, 199034 St. Petersburg, Russia – sequence: 2 givenname: Roman P orcidid: 0000-0001-5232-1461 surname: Kostyuchenko fullname: Kostyuchenko, Roman P organization: Department of Embryology, St. Petersburg State University, Universitetskaya nab. 7-9, 199034 St. Petersburg, Russia – sequence: 3 givenname: Vitaly V orcidid: 0000-0003-1109-3508 surname: Kozin fullname: Kozin, Vitaly V organization: Department of Embryology, St. Petersburg State University, Universitetskaya nab. 7-9, 199034 St. Petersburg, Russia |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34063978$$D View this record in MEDLINE/PubMed |
BookMark | eNpdkVFrFDEUhYNUbK199FUCvlRw9CaTmcm8CMvSrULBYhUfhzszd3ZSZpM2yVTWf-E_Nktr6ZqX5CYfh5NzXrID6ywx9lrAhzyv4eOaLAUhoYRK62fsSEKVZ0rJ4uDJ-ZCdhHANaSmQAMULdpgrKPO60kfsz1X0cxdnjxNH2_PVbLtonE3jckSPXSRvfuPuiruBx5H46nzFr8w6Icau-SXG8RduubH8G-38-D340k3bbkSKxH86v-GLycSI_M54soGfLqylyfT4np95jzYafPeKPR9wCnTysB-zH6uz78vP2cXX8y_LxUXWKVHETIEYBl0PWqmibaXOsajqAWRfCNFKELXSEqu-RV1qNSgpq7qtCMquJipb0Pkx-3SvezO3G-o7sjGF0Nx4s0G_bRyaZv_FmrFZu7tGS5mCrJLA6YOAd7czhdhsTOhomtCSm0Mji7xUGqSAhL79D712s08J7iiVnAqQZaKye6rzLgRPw6MZAc2u72av78S_efqDR_pfu_lfUo2plw |
CitedBy_id | crossref_primary_10_1134_S1062360423030037 crossref_primary_10_3390_genes12081148 crossref_primary_10_31857_S0475145023030035 crossref_primary_10_3390_genes13020270 crossref_primary_10_3390_cells12101354 crossref_primary_10_1186_s12864_023_09602_z crossref_primary_10_3390_genes12111769 crossref_primary_10_1096_fba_2021_00116 |
Cites_doi | 10.1046/j.1440-169X.2002.00634.x 10.1155/2012/298147 10.1186/1741-7007-12-24 10.1098/rstb.2015.0477 10.1016/j.ydbio.2015.04.001 10.1242/dev.014282 10.1007/s00427-015-0496-1 10.1046/j.1440-169X.2001.00594.x 10.1007/BF01380649 10.1134/S1062359016030067 10.1134/S1062360417030079 10.1007/s00427-009-0309-5 10.1134/S1062359020030048 10.1134/S1062359016030079 10.1242/dev.037689 10.1038/nature17972 10.1002/dvdy.7 10.1111/dgd.12696 10.1093/icb/icu109 10.1016/j.ydbio.2013.04.010 10.1242/dev.180760 10.1002/bdrc.20182 10.1186/gb-2001-2-3-reviews3005 10.1002/wdev.176 10.1016/j.ydbio.2015.12.012 10.1093/gigascience/giz023 10.1134/S1022795413010043 10.1242/dev.140699 10.1002/bies.20261 10.1007/s00427-007-0192-x 10.1002/ar.22529 10.1016/j.mod.2016.03.003 10.3389/fcell.2017.00058 10.1038/s41559-020-01327-6 10.1242/dev.083790 10.1016/j.ydbio.2018.11.004 10.1016/j.cellsig.2016.06.001 10.1242/dev.152587 10.1073/pnas.1014235108 10.1016/j.ydbio.2013.05.010 10.1210/er.2003-0040 10.1016/0305-0491(92)90228-J 10.1242/dev.196089 10.1007/s00435-003-0073-4 10.1186/s12862-018-1235-9 10.1007/BF00576934 10.1002/dvdy.21388 10.1038/nature11696 10.1016/j.ydbio.2008.01.032 10.1134/S1062360420030042 10.1201/9780429423604 10.1016/j.cell.2016.05.038 10.1242/dev.051573 10.1186/s12864-016-3027-1 10.1016/bs.ctdb.2018.11.020 10.1242/dev.020784 10.1007/s00427-014-0480-1 10.1007/s00427-006-0122-3 10.1093/molbev/mst222 10.1242/dev.097261 10.1016/j.margen.2015.07.006 10.1038/srep32387 10.1016/j.gde.2013.03.002 10.1016/j.ydbio.2015.09.025 10.1387/ijdb.140148gb |
ContentType | Journal Article |
Copyright | 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2021 by the authors. 2021 |
Copyright_xml | – notice: 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2021 by the authors. 2021 |
DBID | CGR CUY CVF ECM EIF NPM AAYXX CITATION 8FD 8FE 8FH ABUWG AFKRA AZQEC BBNVY BENPR BHPHI CCPQU DWQXO FR3 GNUQQ HCIFZ LK8 M7P P64 PIMPY PQEST PQQKQ PQUKI PRINS RC3 7X8 5PM |
DOI | 10.3390/genes12060788 |
DatabaseName | Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed CrossRef Technology Research Database ProQuest SciTech Collection ProQuest Natural Science Collection ProQuest Central (Alumni) ProQuest Central UK/Ireland ProQuest Central Essentials Biological Science Collection AUTh Library subscriptions: ProQuest Central ProQuest Natural Science Collection ProQuest One Community College ProQuest Central Engineering Research Database ProQuest Central Student SciTech Premium Collection Biological Sciences Biological Science Database Biotechnology and BioEngineering Abstracts Publicly Available Content Database ProQuest One Academic Eastern Edition (DO NOT USE) ProQuest One Academic ProQuest One Academic UKI Edition ProQuest Central China Genetics Abstracts MEDLINE - Academic PubMed Central (Full Participant titles) |
DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) CrossRef Publicly Available Content Database ProQuest Central Student Technology Research Database ProQuest Biological Science Collection ProQuest Central Essentials ProQuest One Academic Eastern Edition ProQuest Central (Alumni Edition) SciTech Premium Collection ProQuest One Community College ProQuest Natural Science Collection Biological Science Database ProQuest SciTech Collection ProQuest Central China Biotechnology and BioEngineering Abstracts ProQuest Central Genetics Abstracts ProQuest One Academic UKI Edition Natural Science Collection ProQuest Central Korea Biological Science Collection Engineering Research Database ProQuest One Academic MEDLINE - Academic |
DatabaseTitleList | MEDLINE Publicly Available Content Database CrossRef |
Database_xml | – sequence: 1 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database – sequence: 3 dbid: BENPR name: AUTh Library subscriptions: ProQuest Central url: https://www.proquest.com/central sourceTypes: Aggregation Database |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Biology |
EISSN | 2073-4425 |
ExternalDocumentID | 10_3390_genes12060788 34063978 |
Genre | Research Support, Non-U.S. Gov't Journal Article |
GroupedDBID | --- 53G 5VS 8FE 8FH AADQD AAFWJ AAHBH ADBBV AENEX AFKRA AFPKN AFZYC ALMA_UNASSIGNED_HOLDINGS AOIJS BAWUL BBNVY BCNDV BENPR BHPHI CCPQU CGR CUY CVF DIK EBD ECM EIF GROUPED_DOAJ HCIFZ HYE IAO IHR KQ8 LK8 M48 M7P MODMG M~E NPM OK1 PGMZT PIMPY PROAC RIG RPM AAYXX CITATION 8FD ABUWG AZQEC DWQXO FR3 GNUQQ P64 PQEST PQQKQ PQUKI PRINS RC3 7X8 ITC 5PM |
ID | FETCH-LOGICAL-c415t-401ff89f8445bb283a579f02d511b2019482a7dba8684f42279b7e06c9ee6b083 |
IEDL.DBID | RPM |
ISSN | 2073-4425 |
IngestDate | Tue Sep 17 21:19:47 EDT 2024 Fri Aug 16 22:48:05 EDT 2024 Thu Oct 10 18:58:45 EDT 2024 Thu Sep 26 21:53:02 EDT 2024 Sat Sep 28 08:22:31 EDT 2024 |
IsDoiOpenAccess | true |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 6 |
Keywords | axis elongation fibroblast growth factor annelids blastema induction dedifferentiation segmentation Nereis SU5402 evolution invertebrates |
Language | English |
License | Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). |
LinkModel | DirectLink |
MergedId | FETCHMERGED-LOGICAL-c415t-401ff89f8445bb283a579f02d511b2019482a7dba8684f42279b7e06c9ee6b083 |
Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
ORCID | 0000-0002-4621-136X 0000-0001-5232-1461 0000-0003-1109-3508 |
OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8224027/ |
PMID | 34063978 |
PQID | 2544821026 |
PQPubID | 2032392 |
ParticipantIDs | pubmedcentral_primary_oai_pubmedcentral_nih_gov_8224027 proquest_miscellaneous_2536480210 proquest_journals_2544821026 crossref_primary_10_3390_genes12060788 pubmed_primary_34063978 |
PublicationCentury | 2000 |
PublicationDate | 20210521 |
PublicationDateYYYYMMDD | 2021-05-21 |
PublicationDate_xml | – month: 5 year: 2021 text: 20210521 day: 21 |
PublicationDecade | 2020 |
PublicationPlace | Switzerland |
PublicationPlace_xml | – name: Switzerland – name: Basel |
PublicationTitle | Genes |
PublicationTitleAlternate | Genes (Basel) |
PublicationYear | 2021 |
Publisher | MDPI AG MDPI |
Publisher_xml | – name: MDPI AG – name: MDPI |
References | Lange (ref_9) 2014; 224 Kozin (ref_4) 2015; 225 Ornitz (ref_14) 2001; 2 ref_12 Vellutini (ref_39) 2016; 6 ref_55 Makanae (ref_31) 2012; 295 Pirotte (ref_56) 2016; 409 Grigoryan (ref_30) 2013; 49 Nokin (ref_61) 1962; 93 Nacu (ref_28) 2016; 533 Lin (ref_11) 2008; 316 Kozin (ref_47) 2016; 140 Makanae (ref_33) 2016; 410 ref_15 Zhang (ref_57) 2013; 367 Niehrs (ref_17) 2005; 26 Jandzik (ref_22) 2014; 141 Tanaka (ref_29) 2016; 165 Beermann (ref_72) 2008; 218 Kostyuchenko (ref_2) 2020; 47 Vellutini (ref_41) 2020; 5 McMahon (ref_58) 2010; 137 Morales (ref_24) 2017; 5 Kostyuchenko (ref_51) 2016; 43 Berenzen (ref_53) 2003; 122 Matus (ref_64) 2007; 217 Novikova (ref_60) 2013; 4 Babonis (ref_65) 2017; 372 Gerrits (ref_45) 1991; 1 ref_62 Planques (ref_5) 2019; 445 Niwa (ref_7) 2013; 381 Dorey (ref_21) 2010; 137 Arimoto (ref_43) 2019; 8 (ref_54) 1931; 123 Ogawa (ref_37) 2002; 44 Maddaluno (ref_10) 2017; 144 ref_71 Hill (ref_49) 1970; 10 Avel (ref_52) 1961; 86 Boilly (ref_48) 1969; 162 Kozin (ref_73) 2016; 43 Sharma (ref_68) 2015; 402 Makanae (ref_32) 2013; 381 ref_36 ref_35 Kish (ref_59) 2016; 28 Tulin (ref_18) 2010; 90 Kim (ref_70) 2001; 43 Simakov (ref_44) 2013; 493 Fan (ref_26) 2015; 24 Kozin (ref_3) 2017; 48 Green (ref_67) 2013; 140 Ornitz (ref_19) 2015; 4 Rebscher (ref_46) 2009; 219 Popovici (ref_16) 2005; 27 Bertrand (ref_27) 2011; 108 Balavoine (ref_63) 2014; 58 Blanckaert (ref_34) 1992; 103 Dondua (ref_42) 1975; 6 ref_40 Rentzsch (ref_66) 2008; 135 Shibata (ref_8) 2016; 143 Kostyuchenko (ref_1) 2019; 248 Brand (ref_23) 2013; 23 Itoh (ref_20) 2008; 237 Bertrand (ref_13) 2014; 31 Auwal (ref_38) 2020; 62 Nikanorova (ref_6) 2020; 51 Bely (ref_50) 2014; 54 Ornitz (ref_25) 2019; Volume 133 Saudemont (ref_69) 2008; 135 |
References_xml | – volume: 44 start-page: 191 year: 2002 ident: ref_37 article-title: Planarian fibroblast growth factor receptor homologs expressed in stem cells and cephalic ganglions publication-title: Dev. Growth Differ. doi: 10.1046/j.1440-169X.2002.00634.x contributor: fullname: Ogawa – ident: ref_15 doi: 10.1155/2012/298147 – ident: ref_35 doi: 10.1186/1741-7007-12-24 – ident: ref_55 – volume: 372 start-page: 20150477 year: 2017 ident: ref_65 article-title: Phylogenetic evidence for the modular evolution of metazoan signalling pathways publication-title: Philos. Trans. R. Soc. B doi: 10.1098/rstb.2015.0477 contributor: fullname: Babonis – volume: 402 start-page: 264 year: 2015 ident: ref_68 article-title: The single FGF receptor gene in the beetle Tribolium castaneum codes for two isoforms that integrate FGF8-and branchless-dependent signals publication-title: Dev. Biol. doi: 10.1016/j.ydbio.2015.04.001 contributor: fullname: Sharma – volume: 135 start-page: 353 year: 2008 ident: ref_69 article-title: FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis and regulate gastrulation during sea urchin development publication-title: Development doi: 10.1242/dev.014282 contributor: fullname: Saudemont – volume: 225 start-page: 129 year: 2015 ident: ref_4 article-title: Vasa, PL10, and Piwi gene expression during caudal regeneration of the polychaete annelid Alitta virens publication-title: Dev. Genes Evol. doi: 10.1007/s00427-015-0496-1 contributor: fullname: Kozin – volume: 43 start-page: 521 year: 2001 ident: ref_70 article-title: Role of the FGF and MEK signaling pathway in the ascidian embryo publication-title: Dev. Growth Differ. doi: 10.1046/j.1440-169X.2001.00594.x contributor: fullname: Kim – volume: 123 start-page: 649 year: 1931 ident: ref_54 article-title: Die überzähligen Bildungen des Körperstammes von Lumbriculus variegatus Müll. und ihre kausale Analyse publication-title: Wilhelm Roux Arch. Entwickl. Org. doi: 10.1007/BF01380649 – volume: 43 start-page: 185 year: 2016 ident: ref_51 article-title: Regeneration and asexual reproduction in annelids: Cells, genes, and evolution publication-title: Biol. Bull. doi: 10.1134/S1062359016030067 contributor: fullname: Kostyuchenko – volume: 48 start-page: 198 year: 2017 ident: ref_3 article-title: Regeneration of the nervous and muscular system after caudal amputation in the Polychaete Alitta virens (Annelida: Nereididae) publication-title: Russ. J. Dev. Biol. doi: 10.1134/S1062360417030079 contributor: fullname: Kozin – volume: 219 start-page: 455 year: 2009 ident: ref_46 article-title: Conserved intron positions in FGFR genes reflect the modular structure of FGFR and reveal stepwise addition of domains to an already complex ancestral FGFR publication-title: Dev. Genes Evol. doi: 10.1007/s00427-009-0309-5 contributor: fullname: Rebscher – volume: 47 start-page: 237 year: 2020 ident: ref_2 article-title: Morphallaxis versus epimorphosis? Cellular and molecular aspects of regeneration and asexual reproduction in annelids publication-title: Biol. Bull. doi: 10.1134/S1062359020030048 contributor: fullname: Kostyuchenko – volume: 43 start-page: 216 year: 2016 ident: ref_73 article-title: Evolutionary conservation and variability of the mesoderm development in spiralia: A peculiar pattern of nereid polychaetes publication-title: Biol. Bull. doi: 10.1134/S1062359016030079 contributor: fullname: Kozin – volume: 137 start-page: 3731 year: 2010 ident: ref_21 article-title: FGF signalling: Diverse roles during early vertebrate embryogenesis publication-title: Development doi: 10.1242/dev.037689 contributor: fullname: Dorey – volume: 533 start-page: 407 year: 2016 ident: ref_28 article-title: FGF8 and SHH substitute for anterior-posterior tissue interactions to induce limb regeneration publication-title: Nature doi: 10.1038/nature17972 contributor: fullname: Nacu – volume: 248 start-page: 728 year: 2019 ident: ref_1 article-title: FoxA Expression pattern in two polychaete species, Alitta virens and Platynereis dumerilii: Examination of the conserved key regulator of the gut development from cleavage through larval life, postlarval growth, and regeneration publication-title: Dev. Dyn. doi: 10.1002/dvdy.7 contributor: fullname: Kostyuchenko – volume: 62 start-page: 527 year: 2020 ident: ref_38 article-title: Identification and characterization of a fibroblast growth factor gene in the planarian Dugesia japonica publication-title: Dev. Growth Differ. doi: 10.1111/dgd.12696 contributor: fullname: Auwal – volume: 54 start-page: 688 year: 2014 ident: ref_50 article-title: Early events in annelid regeneration: A cellular perspective publication-title: Integr. Comp. Biol. doi: 10.1093/icb/icu109 contributor: fullname: Bely – volume: 1 start-page: 1 year: 1991 ident: ref_45 article-title: A Versatile, Low toxicity glycol methacrylate embedding medium for use in biological research, and for recovered biomaterials prostheses publication-title: Cells Mater. contributor: fullname: Gerrits – volume: 381 start-page: 460 year: 2013 ident: ref_7 article-title: Homeogenetic inductive mechanism of segmentation in polychaete tail regeneration publication-title: Dev. Biol. doi: 10.1016/j.ydbio.2013.04.010 contributor: fullname: Niwa – ident: ref_12 doi: 10.1242/dev.180760 – volume: 90 start-page: 214 year: 2010 ident: ref_18 article-title: Extending the family table: Insights from beyond vertebrates into the regulation of embryonic development by FGFs publication-title: Birth Defects Res. C Embryo Today Rev. doi: 10.1002/bdrc.20182 contributor: fullname: Tulin – volume: 2 start-page: reviews3005.1 year: 2001 ident: ref_14 article-title: Fibroblast growth factors publication-title: Genome Biol. doi: 10.1186/gb-2001-2-3-reviews3005 contributor: fullname: Ornitz – volume: 4 start-page: 215 year: 2015 ident: ref_19 article-title: The fibroblast growth factor signaling pathway publication-title: Wiley Interdiscip. Rev. Dev. Biol. doi: 10.1002/wdev.176 contributor: fullname: Ornitz – volume: 10 start-page: 101 year: 1970 ident: ref_49 article-title: Origin of the regeneration blastema in polychaete annelids publication-title: Integr. Comp. Biol. contributor: fullname: Hill – volume: 410 start-page: 45 year: 2016 ident: ref_33 article-title: Cooperative inputs of BMP and FGF signaling induce tail regeneration in urodele amphibians publication-title: Dev. Biol. doi: 10.1016/j.ydbio.2015.12.012 contributor: fullname: Makanae – volume: 8 start-page: 8 year: 2019 ident: ref_43 article-title: A draft nuclear-genome assembly of the acoel flatworm Praesagittifera naikaiensis publication-title: GigaScience doi: 10.1093/gigascience/giz023 contributor: fullname: Arimoto – volume: 49 start-page: 46 year: 2013 ident: ref_30 article-title: Study of regeneration in amphibians in age of molecular-genetic approaches and methods publication-title: Russ. J. Genet. doi: 10.1134/S1022795413010043 contributor: fullname: Grigoryan – volume: 143 start-page: 2920 year: 2016 ident: ref_8 article-title: FGF signalling controls diverse aspects of fin regeneration publication-title: Development doi: 10.1242/dev.140699 contributor: fullname: Shibata – volume: 27 start-page: 849 year: 2005 ident: ref_16 article-title: An evolutionary history of the FGF superfamily publication-title: BioEssays doi: 10.1002/bies.20261 contributor: fullname: Popovici – volume: 218 start-page: 153 year: 2008 ident: ref_72 article-title: Sites of FGF signalling and perception during embryogenesis of the beetle Tribolium castaneum publication-title: Dev. Genes Evol. doi: 10.1007/s00427-007-0192-x contributor: fullname: Beermann – volume: 295 start-page: 1566 year: 2012 ident: ref_31 article-title: Early regulation of axolotl limb regeneration publication-title: Anat. Rec. doi: 10.1002/ar.22529 contributor: fullname: Makanae – volume: 140 start-page: 1 year: 2016 ident: ref_47 article-title: Mesoderm patterning and morphogenesis in the polychaete Alitta virens (Spiralia, Annelida): Expression of mesodermal markers twist, mox, evx and functional role for MAP kinase signaling publication-title: Mech. Dev. doi: 10.1016/j.mod.2016.03.003 contributor: fullname: Kozin – volume: 86 start-page: 464 year: 1961 ident: ref_52 article-title: L’influence du systeme nerveux sur la regeneration chez les urodeles et les oligochetes publication-title: Bull. Soc. Zool. Fr. contributor: fullname: Avel – volume: 5 start-page: 58 year: 2017 ident: ref_24 article-title: The multiple roles of FGF signaling in the developing spinal cord publication-title: Front. Cell Dev. Biol. doi: 10.3389/fcell.2017.00058 contributor: fullname: Morales – volume: 5 start-page: 231 year: 2020 ident: ref_41 article-title: Conservative route to genome compaction in a miniature annelid publication-title: Nat. Ecol. Evol. doi: 10.1038/s41559-020-01327-6 contributor: fullname: Vellutini – volume: 140 start-page: 1024 year: 2013 ident: ref_67 article-title: FGF signaling induces mesoderm in the hemichordate Saccoglossus kowalevskii publication-title: Development doi: 10.1242/dev.083790 contributor: fullname: Green – volume: 445 start-page: 189 year: 2019 ident: ref_5 article-title: Morphological, cellular and molecular characterization of posterior regeneration in the marine annelid Platynereis dumerilii publication-title: Dev. Biol. doi: 10.1016/j.ydbio.2018.11.004 contributor: fullname: Planques – volume: 28 start-page: 1196 year: 2016 ident: ref_59 article-title: FGF regulates dedifferentiation during skeletal muscle regeneration in adult zebrafish publication-title: Cell. Signal. doi: 10.1016/j.cellsig.2016.06.001 contributor: fullname: Kish – volume: 144 start-page: 4047 year: 2017 ident: ref_10 article-title: Fibroblast growth factors: Key players in regeneration and tissue repair publication-title: Development doi: 10.1242/dev.152587 contributor: fullname: Maddaluno – volume: 4 start-page: 1 year: 2013 ident: ref_60 article-title: Expression of hox genes during regeneration of nereid polychaete Alitta (Nereis) nirens (Annelida, Lophotrochozoa) publication-title: EvoDevo contributor: fullname: Novikova – volume: 108 start-page: 9160 year: 2011 ident: ref_27 article-title: Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits publication-title: Proc. Natl. Acad. Sci. USA doi: 10.1073/pnas.1014235108 contributor: fullname: Bertrand – volume: 381 start-page: 213 year: 2013 ident: ref_32 article-title: Nerve independent limb induction in axolotls publication-title: Dev. Biol. doi: 10.1016/j.ydbio.2013.05.010 contributor: fullname: Makanae – volume: 26 start-page: 63 year: 2005 ident: ref_17 article-title: Fibroblast growth factor signaling during early vertebrate development publication-title: Endocr. Rev. doi: 10.1210/er.2003-0040 contributor: fullname: Niehrs – volume: 103 start-page: 991 year: 1992 ident: ref_34 article-title: Identification of a heparin-binding growth factor and of its affinity binding sites in the marine annelid nereis diversicolor publication-title: Comp. Biochem. Physiol. B Biochem. doi: 10.1016/0305-0491(92)90228-J contributor: fullname: Blanckaert – ident: ref_40 doi: 10.1242/dev.196089 – volume: 122 start-page: 95 year: 2003 ident: ref_53 article-title: Experiments on anterior regeneration in Eurythoe complanata (“Polychaeta”, Amphinomidae): Reconfiguration of the nervous system and its function for Regeneration publication-title: Zoomorphology doi: 10.1007/s00435-003-0073-4 contributor: fullname: Berenzen – ident: ref_71 doi: 10.1186/s12862-018-1235-9 – volume: 162 start-page: 286 year: 1969 ident: ref_48 article-title: Origine des cellules régénératrices chez Nereis diversicolor O. F. Müller (Annélide Polychète) publication-title: Wilhelm Roux Arch. Für Entwickl. Org. doi: 10.1007/BF00576934 contributor: fullname: Boilly – volume: 237 start-page: 18 year: 2008 ident: ref_20 article-title: Functional evolutionary history of the mouse FGF gene family publication-title: Dev. Dyn. doi: 10.1002/dvdy.21388 contributor: fullname: Itoh – volume: 493 start-page: 526 year: 2013 ident: ref_44 article-title: Insights into bilaterian evolution from three spiralian genomes publication-title: Nature doi: 10.1038/nature11696 contributor: fullname: Simakov – volume: 316 start-page: 323 year: 2008 ident: ref_11 article-title: Requirement for Wnt and FGF signaling in xenopus tadpole tail regeneration publication-title: Dev. Biol. doi: 10.1016/j.ydbio.2008.01.032 contributor: fullname: Lin – volume: 51 start-page: 148 year: 2020 ident: ref_6 article-title: Regeneration in annelids: Cell sources, tissue remodeling, and differential gene expression publication-title: Russ. J. Dev. Biol. doi: 10.1134/S1062360420030042 contributor: fullname: Nikanorova – ident: ref_62 doi: 10.1201/9780429423604 – volume: 165 start-page: 1598 year: 2016 ident: ref_29 article-title: The molecular and cellular choreography of appendage regeneration publication-title: Cell doi: 10.1016/j.cell.2016.05.038 contributor: fullname: Tanaka – volume: 367 start-page: 253 year: 2013 ident: ref_57 article-title: Cell cycle regulation and regeneration publication-title: Curr. Top. Microbiol. Immunol. contributor: fullname: Zhang – volume: 137 start-page: 2167 year: 2010 ident: ref_58 article-title: Mesoderm migration in drosophila is a multi-step process requiring FGF signaling and integrin activity publication-title: Development doi: 10.1242/dev.051573 contributor: fullname: McMahon – ident: ref_36 doi: 10.1186/s12864-016-3027-1 – volume: Volume 133 start-page: 195 year: 2019 ident: ref_25 article-title: Fibroblast growth factors in skeletal development publication-title: Current Topics in Developmental Biology doi: 10.1016/bs.ctdb.2018.11.020 contributor: fullname: Ornitz – volume: 135 start-page: 1761 year: 2008 ident: ref_66 article-title: FGF Signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis publication-title: Development doi: 10.1242/dev.020784 contributor: fullname: Rentzsch – volume: 93 start-page: 137 year: 1962 ident: ref_61 article-title: Cicatrisation et premiers stades de regeneration pygidiale chez nereis diversicolor publication-title: Ann. Soc. Zool. Belg. contributor: fullname: Nokin – volume: 224 start-page: 235 year: 2014 ident: ref_9 article-title: Dynamic expression of a hydra FGF at boundaries and termini publication-title: Dev. Genes Evol. doi: 10.1007/s00427-014-0480-1 contributor: fullname: Lange – volume: 217 start-page: 137 year: 2007 ident: ref_64 article-title: FGF signaling in gastrulation and neural development in Nematostella vectensis, an Anthozoan cnidarian publication-title: Dev. Genes. Evol. doi: 10.1007/s00427-006-0122-3 contributor: fullname: Matus – volume: 31 start-page: 310 year: 2014 ident: ref_13 article-title: FGF Signaling emerged concomitantly with the origin of eumetazoans publication-title: Mol. Biol. Evol. doi: 10.1093/molbev/mst222 contributor: fullname: Bertrand – volume: 141 start-page: 629 year: 2014 ident: ref_22 article-title: Roles for FGF in lamprey pharyngeal pouch formation and skeletogenesis highlight ancestral functions in the vertebrate head publication-title: Development doi: 10.1242/dev.097261 contributor: fullname: Jandzik – volume: 6 start-page: 475 year: 1975 ident: ref_42 article-title: Influence of actinomycin D and sibiromycin upon the embryonic and larval development in Nereis virens (Sars.) publication-title: Ontogenez contributor: fullname: Dondua – volume: 24 start-page: 167 year: 2015 ident: ref_26 article-title: FGF Signaling repertoire of the indirect developing hemichordate Ptychodera flava publication-title: Mar. Genom. doi: 10.1016/j.margen.2015.07.006 contributor: fullname: Fan – volume: 6 start-page: 32387 year: 2016 ident: ref_39 article-title: Expression of segment polarity genes in brachiopods supports a non-segmental ancestral role of engrailed for bilaterians publication-title: Sci. Rep. doi: 10.1038/srep32387 contributor: fullname: Vellutini – volume: 23 start-page: 415 year: 2013 ident: ref_23 article-title: Generation and interpretation of FGF morphogen gradients in vertebrates publication-title: Curr. Opin. Genet. Dev. doi: 10.1016/j.gde.2013.03.002 contributor: fullname: Brand – volume: 409 start-page: 4 year: 2016 ident: ref_56 article-title: Do you have the nerves to regenerate? The importance of neural signalling in the regeneration process publication-title: Dev. Biol. doi: 10.1016/j.ydbio.2015.09.025 contributor: fullname: Pirotte – volume: 58 start-page: 469 year: 2014 ident: ref_63 article-title: Segment formation in annelids: Patterns, processes and evolution publication-title: Int. J. Dev. Biol. doi: 10.1387/ijdb.140148gb contributor: fullname: Balavoine |
SSID | ssj0000402005 |
Score | 2.3031166 |
Snippet | Epimorphic regeneration of lost body segments is a widespread phenomenon across annelids. However, the molecular inducers of the cell sources for this... |
SourceID | pubmedcentral proquest crossref pubmed |
SourceType | Open Access Repository Aggregation Database Index Database |
StartPage | 788 |
SubjectTerms | Alitta virens Amino acids Amputation Animals Annelida - genetics Annelida - metabolism Annelida - physiology Cell cycle Cell Proliferation Epithelium Fibroblast growth factors Fibroblast Growth Factors - genetics Fibroblast Growth Factors - metabolism Genomes Glycerol Growth factors Kinases Labeling Ligands Mammals Minors Morphogenesis Phylogenetics Receptors, Fibroblast Growth Factor - genetics Receptors, Fibroblast Growth Factor - metabolism Regeneration Seawater Signal Transduction Structure-function relationships Ventral nerve cord Wound healing |
SummonAdditionalLinks | – databaseName: AUTh Library subscriptions: ProQuest Central dbid: BENPR link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3daxQxEA_aIvhS_Pa0yggiCi7NZrPZ7JOc5dbiQzlai31bkktyHpRs9U7l_oz-x53Z3Vt7Cj4nZJdMMvObj_yGsdfO5U6GTCTcmDKRhuvEGMUTI5XTgXOvQlttcayOzuTn8_y8D7gt-7LKjU5sFbVrZhQjPyAqLU3-ifpw-T2hrlGUXe1baNxmuyKVlKbd_Tg5np4MURZO7hHPO3LNDP37gzmpkFRwhbZRbxujfxDm34WSNyxPdY_t9ZARxp2M77NbPj5gd7omkuuH7Oq0pYAl-gww0UGFlqoL8MHhwMbcPbaEJgACPqg-VXC6mBMGj3OYIgj8bdawiHDi5y0N9c3J0-ZiTaX1Kw9fEeDCGIH7ysAv1JVxCW_HVCizcOY9TH6g3UOF8e4RO6smXw6Pkr7RQjJD-71CHzINQZdBS5lbi4DD5EUZuHCIxiwihBJ33hTOGq20DJJIB23huZqV3iuLIO4x24lN9E8ZSMF95mapMwLX5tpK46wLGm96VqBvN2JvNjteX3Z8GjX6ISSaeks0I7a_kUfdX6tl_ecQjNirYRgvBGU5TPTNT5qTKanJlR2xJ534hi9lsk1k4uLFlmCHCUS2vT0SF99a0u222lYUz_7_W8_ZXUFFLzxPRLrPdvAA-BeIWlb2ZX80rwGEHPB9 priority: 102 providerName: ProQuest – databaseName: Scholars Portal Open Access Journals dbid: M48 link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3fSxwxEA5WEfoitrXtVVtGKEWh2-ay2Wz2oZRDXEVQpHro25JckvNAcv64tt6f4X_cmd27q6elz8lml8xk5vs2ky-MfXQuczKkIuHGFIk0XCfGKJ4YqZwOnHsV6mqLI7XflQfn2flfSaHJBN7-k9rRfVLdm8svd9fj77jgvxHjRMr-tU9RoS24wnSnn7ElIVNJzn44Qfp1UCaexLNGZfPpU_NZ6QnUfFwx-SAFlatsZYIdodMY-wVb8PElW25ukxy_YvcntRYs6WiAiQ5KTFnNnz7YmckyN6cuYRgAkR-UeyWcDPoExmMfjhEN_jZjGET44fu1HvXDzsfDyzHV2I88nCHShQ4i-JGBXxg04y1sdahiZuDMZ9i9wQSIkWN7jXXL3dOd_WRy40LSw0Q-QjLZDkEXQUuZWYvIw2R5EbhwCMssQoVCamFyZ41WWgZJ6oM291z1Cu-VRTT3mi3GYfRvGUjBfep6bWcEjs21lcZZFzQu-TRHktdin6YzXl01whoVEhIyTTVnmhbbmNqjmrpHRcJqmtiqarHNWTOuDNruMNEPf1KfVElNnLbF3jTmm70plfWOJg6ezxl21oFUt-db4uCiVt-uy25F_u7_n7XOnguqfuFZItobbBEdwL9H-DKyH2rH_APB__I5 priority: 102 providerName: Scholars Portal |
Title | Structural and Functional Characterization of the FGF Signaling Pathway in Regeneration of the Polychaete Worm Alitta virens (Annelida, Errantia) |
URI | https://www.ncbi.nlm.nih.gov/pubmed/34063978 https://www.proquest.com/docview/2544821026 https://search.proquest.com/docview/2536480210 https://pubmed.ncbi.nlm.nih.gov/PMC8224027 |
Volume | 12 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1da9swFL00HYO9lH3PXRc0GGODuVFsWZYfsxCvDFpCu7K-GcmSMkOrlDbdyM_oP-6VHIdke9uz5A98r3TPsY6OAD5onWlm0ySmUhYxk1TEUnIaS8a1sJQaboPa4oQfnbPvF9nFDmTdXpgg2q9Vc-gurw5d8ytoK6-v6kGnExtMj8dB-YicvQe9PE03KHqYfj0jolnrp5kipR_M_KwxTCjHcujP50tZWM4S26XoH3z5t0xyo-6UT2FvBRjJqH2xZ7Bj3HN43B4huXwB92fBANabZxDpNCmxTrW_98h47cXcbrUkc0sQ7pHyW0nOmplH4G5GpggB_8glaRw5NbNgQr3ZeTq_XHph_cKQnwhvyQhh-0KS3zhTulvyaeRlMo2WX8jkBqseThefX8J5OfkxPopXxyzENVbvBTLIobWisIKxTCmEGzLLC0sTjVhMIT4omEhkrpUUXDDLvOWgyg3ldWEMVwjhXsGumzvzBghLqEl1PdQywXtToZjUSluB4zzNkdlF8LH74tV166ZRIQvxUaq2ohTBQRePajWobivvpiY8ReURvF8343DwaxzSmfmd75NyJjyRjeB1G771k7q4R5BvBXbdwVttb7dgBgbL7VXG7f_3lW_hSeLVMDSLk-EB7GJumHcIZxaqD4--Tk6mp33oHTPRD8n8AGNC-pA |
link.rule.ids | 230,315,733,786,790,891,2236,21416,24346,27955,27956,33777,33778,43838,53825,53827,74657 |
linkProvider | National Library of Medicine |
linkToHtml | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3bjtMwEB1BVwheEHcKCxgJIZCI1k0cx3lCZdVQYKmqvYh9i-zaLpVWzi4toH4Gf8xMkoYtSDzbSiKPPXPOeHIG4IW1qRU-iSOudR4JzVWkteSRFtIqz7mTvq62mMjxifh4mp62CbdlW1a58Ym1o7bVjHLkeySlpYifyLfnFxF1jaLb1baFxlXYIclN1YOdd6PJ9LDLsnCiRzxtxDUT5Pd7c3Ihg5hLjI1qOxj9gzD_LpS8FHmKW3CzhYxs2Nj4Nlxx4Q5ca5pIru_Cr6NaApbkM5gOlhUYqZoEH9vv1Jibny1Z5RkCPla8L9jRYk4YPMzZFEHgT71mi8AO3byWob48eVqdram0fuXYFwS4bIjAfaXZD_SVYcleDalQZmH1Gzb6hnEPHcbre3BSjI73x1HbaCGaYfxeIYcceK9yr4RIjUHAodMs9zy2iMYMIoQcV15n1mgllfCCRAdN5ric5c5JgyDuPvRCFdxDYCLmLrGzgdUxPpsrI7Q11is86UmG3K4PLzcrXp43ehol8hAyTbllmj7sbuxRtsdqWf7ZBH143g3jgaBbDh1c9Z3mJFIoorJ9eNCYr3tTIuqLTHx4tmXYbgKJbW-PhMXXWnS7rraNs0f__6xncH18_PmgPPgw-fQYbsRUAMPTKB7sQg83g3uCCGZlnrbb9DcKcvNz |
linkToPdf | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1tb9MwELZgE2hf0HgvDDgkhEAiqps4jvNpKqNhvKiqNib2LbJru6s0ORstoP4M_jF3SRpWkPhsy4ly57vn7CfPMfbC2tQKn8QR1zqPhOYq0lrySAtplefcSV-zLcby8ER8PE1PW_7ToqVVrmNiHahtNaUz8j5JaSmqT2Tft7SIybti_-Iyog5SdNPattO4zrYzIVMsxLbfjsaTo-7EhVOpxNNGaDPBWr8_o3AyiLnEPKk2E9M_aPNv0uSVLFTsslstfIRhY-_b7JoLd9iNpqHk6i77dVzLwZKUBuhgocCs1Rz2wUGnzNz8eAmVBwR_ULwv4Hg-IzweZjBBQPhTr2Ae4MjNaknqq5Mn1fmKaPZLB18R7MIQQfxSww-Mm2EBr4ZEmplb_QZG3zAHYvB4fY-dFKMvB4dR23QhmmIuX2I9OfBe5V4JkRqD4EOnWe55bBGZGUQLOVpBZ9ZoJZXwggQITea4nObOSYOA7j7bClVwDxmImLvETgdWx7g2V0Zoa6xXuOuTDOu8Hnu5_uLlRaOtUWJNQqYpN0zTY3tre5TtFluUfxyix553w7g56MZDB1d9pzmJFIrK2h570Jive1Ii6ktNXDzbMGw3gYS3N0fC_KwW4K6Zt3H26P-v9YzdRA8tP38Yf3rMdmLiwvA0igd7bAt9wT1BMLM0T1sv_Q0y9Pen |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Structural+and+Functional+Characterization+of+the+FGF+Signaling+Pathway+in+Regeneration+of+the+Polychaete+Worm+Alitta+virens+%28Annelida%2C+Errantia%29&rft.jtitle=Genes&rft.au=Shalaeva%2C+Alexandra+Y&rft.au=Kostyuchenko%2C+Roman+P&rft.date=2021-05-21&rft.pub=MDPI+AG&rft.eissn=2073-4425&rft.volume=12&rft.issue=6&rft.spage=788&rft_id=info:doi/10.3390%2Fgenes12060788&rft.externalDBID=HAS_PDF_LINK |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2073-4425&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2073-4425&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2073-4425&client=summon |