The role of clonal communication and heterogeneity in breast cancer
Identifieur interne : 000337 ( Main/Exploration ); précédent : 000336; suivant : 000338The role of clonal communication and heterogeneity in breast cancer
Auteurs : Ana Martín-Pardillos [Espagne] ; Ángeles Valls Chiva [Espagne] ; Gemma Bande Vargas [Espagne] ; Pablo Hurtado Blanco [Espagne] ; Roberto Pi Eiro Cid [Espagne] ; Pedro J. Guijarro [Espagne] ; Stefan Hümmer [Espagne] ; Eva Bejar Serrano [Espagne] ; Aitor Rodriguez-Casanova [Espagne] ; Ángel Diaz-Lagares [Espagne] ; Josep Castellvi [Espagne] ; Samuel Miravet-Verde [Espagne] ; Luis Serrano [Espagne] ; María Lluch-Senar [Espagne] ; Víctor Sebastian [Espagne] ; Ana Bribian [Espagne] ; Laura L Pez-Mascaraque [Espagne] ; Rafael L Pez-L Pez [Espagne] ; Santiago Ram N Y Cajal [Espagne]Source :
- BMC Cancer [ 1471-2407 ] ; 2019.
Abstract
Cancer is a rapidly evolving, multifactorial disease that accumulates numerous genetic and epigenetic alterations. This results in molecular and phenotypic heterogeneity within the tumor, the complexity of which is further amplified through specific interactions between cancer cells. We aimed to dissect the molecular mechanisms underlying the cooperation between different clones.
We produced clonal cell lines derived from the MDA-MB-231 breast cancer cell line, using the UbC-StarTrack system, which allowed tracking of multiple clones by color: GFP C3, mKO E10 and Sapphire D7. Characterization of these clones was performed by growth rate, cell metabolic activity, wound healing, invasion assays and genetic and epigenetic arrays. Tumorigenicity was tested by orthotopic and intravenous injections. Clonal cooperation was evaluated by medium complementation, co-culture and co-injection assays.
Characterization of these clones in vitro revealed clear genetic and epigenetic differences that affected growth rate, cell metabolic activity, morphology and cytokine expression among cell lines. In vivo, all clonal cell lines were able to form tumors; however, injection of an equal mix of the different clones led to tumors with very few mKO E10 cells. Additionally, the mKO E10 clonal cell line showed a significant inability to form lung metastases. These results confirm that even in stable cell lines heterogeneity is present. In vitro
These findings support a model where interplay between clones confers aggressiveness, and which may allow identification of the factors involved in cellular communication that could play a role in clonal cooperation and thus represent new targets for preventing tumor progression.
The online version of this article (10.1186/s12885-019-5883-y) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s12885-019-5883-y
PubMed: 31277602
PubMed Central: 6612119
Affiliations:
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first="Ana" last="Martín-Pardillos">Ana Martín-Pardillos</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1763 0287</institution-id><institution-id institution-id-type="GRID">grid.430994.3</institution-id><institution>Translational Molecular Pathology Group,</institution><institution>Vall d’Hebron Research Institute,</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation><affiliation wicri:level="3"><nlm:aff id="Aff2">CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation></author><author><name sortKey="Valls Chiva, Angeles" sort="Valls Chiva, Angeles" uniqKey="Valls Chiva A" first="Ángeles" last="Valls Chiva">Ángeles Valls Chiva</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1763 0287</institution-id><institution-id institution-id-type="GRID">grid.430994.3</institution-id><institution>Translational Molecular Pathology Group,</institution><institution>Vall d’Hebron Research Institute,</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation></author><author><name sortKey="Bande Vargas, Gemma" sort="Bande Vargas, Gemma" uniqKey="Bande Vargas G" first="Gemma" last="Bande Vargas">Gemma Bande Vargas</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1763 0287</institution-id><institution-id 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Eiro Cid, Roberto" sort="Pi Eiro Cid, Roberto" uniqKey="Pi Eiro Cid R" first="Roberto" last="Pi Eiro Cid">Roberto Pi Eiro Cid</name><affiliation wicri:level="3"><nlm:aff id="Aff2">CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8816 6945</institution-id><institution-id institution-id-type="GRID">grid.411048.8</institution-id><institution>Cancer Modelling Lab, Roche-CHUS Joint Unit,</institution></institution-wrap>Santiago de Compostela, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Santiago de Compostela</wicri:regionArea></affiliation></author><author><name sortKey="Guijarro, Pedro J" sort="Guijarro, Pedro J" uniqKey="Guijarro P" first="Pedro J." last="Guijarro">Pedro J. Guijarro</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1763 0287</institution-id><institution-id institution-id-type="GRID">grid.430994.3</institution-id><institution>Translational Molecular Pathology Group,</institution><institution>Vall d’Hebron Research Institute,</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation></author><author><name sortKey="Hummer, Stefan" sort="Hummer, Stefan" uniqKey="Hummer S" first="Stefan" last="Hümmer">Stefan Hümmer</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1763 0287</institution-id><institution-id institution-id-type="GRID">grid.430994.3</institution-id><institution>Translational Molecular Pathology Group,</institution><institution>Vall d’Hebron Research Institute,</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation><affiliation wicri:level="3"><nlm:aff id="Aff2">CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation></author><author><name sortKey="Bejar Serrano, Eva" sort="Bejar Serrano, Eva" uniqKey="Bejar Serrano E" first="Eva" last="Bejar Serrano">Eva Bejar Serrano</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1763 0287</institution-id><institution-id institution-id-type="GRID">grid.430994.3</institution-id><institution>Translational Molecular Pathology Group,</institution><institution>Vall d’Hebron Research Institute,</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation><affiliation wicri:level="3"><nlm:aff id="Aff2">CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation></author><author><name sortKey="Rodriguez Casanova, Aitor" sort="Rodriguez Casanova, Aitor" uniqKey="Rodriguez Casanova A" first="Aitor" last="Rodriguez-Casanova">Aitor Rodriguez-Casanova</name><affiliation wicri:level="1"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8816 6945</institution-id><institution-id institution-id-type="GRID">grid.411048.8</institution-id><institution>Cancer Epigenomics, Translational Medical Oncology (Oncomet), Health Research Institute of Santiago (IDIS),</institution><institution>University Clinical Hospital of Santiago (CHUS),</institution></institution-wrap>Santiago de Compostela, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Santiago de Compostela</wicri:regionArea></affiliation></author><author><name sortKey="Diaz Lagares, Angel" sort="Diaz Lagares, Angel" uniqKey="Diaz Lagares A" first="Ángel" last="Diaz-Lagares">Ángel Diaz-Lagares</name><affiliation wicri:level="3"><nlm:aff id="Aff2">CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8816 6945</institution-id><institution-id institution-id-type="GRID">grid.411048.8</institution-id><institution>Cancer Epigenomics, Translational Medical Oncology (Oncomet), Health Research Institute of Santiago (IDIS),</institution><institution>University Clinical Hospital of Santiago (CHUS),</institution></institution-wrap>Santiago de Compostela, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Santiago de Compostela</wicri:regionArea></affiliation></author><author><name sortKey="Castellvi, Josep" sort="Castellvi, Josep" uniqKey="Castellvi J" first="Josep" last="Castellvi">Josep Castellvi</name><affiliation wicri:level="1"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0675 8654</institution-id><institution-id institution-id-type="GRID">grid.411083.f</institution-id><institution>Hospital Vall d’Hebron, Anatomía Patológica,</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation></author><author><name sortKey="Miravet Verde, Samuel" sort="Miravet Verde, Samuel" uniqKey="Miravet Verde S" first="Samuel" last="Miravet-Verde">Samuel Miravet-Verde</name><affiliation wicri:level="3"><nlm:aff id="Aff6">EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), The Institute of Science and Technology, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), The Institute of Science and Technology, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation></author><author><name sortKey="Serrano, Luis" sort="Serrano, Luis" uniqKey="Serrano L" first="Luis" last="Serrano">Luis Serrano</name><affiliation wicri:level="3"><nlm:aff id="Aff6">EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), The Institute of Science and Technology, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), The Institute of Science and Technology, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff7"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2172 2676</institution-id><institution-id institution-id-type="GRID">grid.5612.0</institution-id><institution>Universitat Pompeu Fabra (UPF),</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff8"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9601 989X</institution-id><institution-id institution-id-type="GRID">grid.425902.8</institution-id><institution>Institució Catalana de Recerca i Estudis Avançats (ICREA),</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation></author><author><name sortKey="Lluch Senar, Maria" sort="Lluch Senar, Maria" uniqKey="Lluch Senar M" first="María" last="Lluch-Senar">María Lluch-Senar</name><affiliation wicri:level="3"><nlm:aff id="Aff6">EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), The Institute of Science and Technology, Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), The Institute of Science and Technology, Barcelona</wicri:regionArea><placeName><settlement type="city">Barcelone</settlement><region nuts="2" type="region">Catalogne</region></placeName></affiliation></author><author><name sortKey="Sebastian, Victor" sort="Sebastian, Victor" uniqKey="Sebastian V" first="Víctor" last="Sebastian">Víctor Sebastian</name><affiliation wicri:level="1"><nlm:aff id="Aff9"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2152 8769</institution-id><institution-id institution-id-type="GRID">grid.11205.37</institution-id><institution>Department of Chemical Engineering,</institution><institution>Aragon Institute of Nanoscience (INA), University of Zaragoza,</institution></institution-wrap>Zaragoza, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Zaragoza</wicri:regionArea></affiliation><affiliation wicri:level="3"><nlm:aff id="Aff10">Networking Research Centre on Bioengineering, Biomaterials and Nanomedicine, CIBER-BBN, Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Networking Research Centre on Bioengineering, Biomaterials and Nanomedicine, CIBER-BBN, Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation></author><author><name sortKey="Bribian, Ana" sort="Bribian, Ana" uniqKey="Bribian A" first="Ana" last="Bribian">Ana Bribian</name><affiliation wicri:level="1"><nlm:aff id="Aff11"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2177 5516</institution-id><institution-id institution-id-type="GRID">grid.419043.b</institution-id><institution>Department of Molecular, Cellular and Developmental Neurobiology,</institution><institution>Instituto Cajal-CSIC,</institution></institution-wrap>Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Madrid</wicri:regionArea></affiliation></author><author><name sortKey="L Pez Mascaraque, Laura" sort="L Pez Mascaraque, Laura" uniqKey="L Pez Mascaraque L" first="Laura" last="L Pez-Mascaraque">Laura L Pez-Mascaraque</name><affiliation wicri:level="1"><nlm:aff id="Aff11"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2177 5516</institution-id><institution-id institution-id-type="GRID">grid.419043.b</institution-id><institution>Department of Molecular, Cellular and Developmental Neurobiology,</institution><institution>Instituto Cajal-CSIC,</institution></institution-wrap>Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Madrid</wicri:regionArea></affiliation></author><author><name sortKey="L Pez L Pez, Rafael" sort="L Pez L Pez, Rafael" uniqKey="L Pez L Pez R" first="Rafael" last="L Pez-L Pez">Rafael L Pez-L Pez</name><affiliation wicri:level="1"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8816 6945</institution-id><institution-id institution-id-type="GRID">grid.411048.8</institution-id><institution>Cancer Epigenomics, Translational Medical Oncology (Oncomet), Health Research Institute of Santiago (IDIS),</institution><institution>University Clinical Hospital of Santiago (CHUS),</institution></institution-wrap>Santiago de Compostela, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Santiago de Compostela</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff12"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 8816 6945</institution-id><institution-id institution-id-type="GRID">grid.411048.8</institution-id><institution>Roche-CHUS Joint Unit,</institution><institution>University Clinical Hospital of Santiago (CHUS),</institution></institution-wrap>Santiago de Compostela, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Santiago de Compostela</wicri:regionArea></affiliation></author><author><name sortKey="Ram N Y Cajal, Santiago" sort="Ram N Y Cajal, Santiago" uniqKey="Ram N Y Cajal S" first="Santiago" last="Ram N Y Cajal">Santiago Ram N Y Cajal</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 1763 0287</institution-id><institution-id institution-id-type="GRID">grid.430994.3</institution-id><institution>Translational Molecular Pathology Group,</institution><institution>Vall d’Hebron Research Institute,</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation><affiliation wicri:level="3"><nlm:aff id="Aff2">CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>CIBERONC (Centro de Investigación Biomédica en Red de Cáncer), Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 0675 8654</institution-id><institution-id institution-id-type="GRID">grid.411083.f</institution-id><institution>Hospital Vall d’Hebron, Anatomía Patológica,</institution></institution-wrap>Barcelona, Spain</nlm:aff><country xml:lang="fr">Espagne</country><wicri:regionArea>Barcelona</wicri:regionArea></affiliation></author></analytic><series><title level="j">BMC Cancer</title><idno type="eISSN">1471-2407</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p id="Par1">Cancer is a rapidly evolving, multifactorial disease that accumulates numerous genetic and epigenetic alterations. This results in molecular and phenotypic heterogeneity within the tumor, the complexity of which is further amplified through specific interactions between cancer cells. We aimed to dissect the molecular mechanisms underlying the cooperation between different clones.</p></sec><sec><title>Methods</title><p id="Par2">We produced clonal cell lines derived from the MDA-MB-231 breast cancer cell line, using the UbC-StarTrack system, which allowed tracking of multiple clones by color: GFP C3, mKO E10 and Sapphire D7. Characterization of these clones was performed by growth rate, cell metabolic activity, wound healing, invasion assays and genetic and epigenetic arrays. Tumorigenicity was tested by orthotopic and intravenous injections. Clonal cooperation was evaluated by medium complementation, co-culture and co-injection assays.</p></sec><sec><title>Results</title><p id="Par3">Characterization of these clones in vitro revealed clear genetic and epigenetic differences that affected growth rate, cell metabolic activity, morphology and cytokine expression among cell lines. In vivo, all clonal cell lines were able to form tumors; however, injection of an equal mix of the different clones led to tumors with very few mKO E10 cells. Additionally, the mKO E10 clonal cell line showed a significant inability to form lung metastases. These results confirm that even in stable cell lines heterogeneity is present. In vitro<italic>,</italic> the complementation of growth medium with medium or exosomes from parental or clonal cell lines increased the growth rate of the other clones. Complementation assays, co-growth and co-injection of mKO E10 and GFP C3 clonal cell lines increased the efficiency of invasion and migration.</p></sec><sec><title>Conclusions</title><p id="Par4">These findings support a model where interplay between clones confers aggressiveness, and which may allow identification of the factors involved in cellular communication that could play a role in clonal cooperation and thus represent new targets for preventing tumor progression.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (10.1186/s12885-019-5883-y) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Siegel, Rl" uniqKey="Siegel R">RL Siegel</name></author><author><name sortKey="Miller, Kd" uniqKey="Miller K">KD Miller</name></author><author><name sortKey="Jemal, A" uniqKey="Jemal A">A 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uniqKey="Zhang X">X Zhang</name></author><author><name sortKey="Ye, L" uniqKey="Ye L">L Ye</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Feng, Q" uniqKey="Feng Q">Q Feng</name></author><author><name sortKey="Zhang, C" uniqKey="Zhang C">C Zhang</name></author><author><name sortKey="Lum, D" uniqKey="Lum D">D Lum</name></author><author><name sortKey="Druso, Je" uniqKey="Druso J">JE Druso</name></author><author><name sortKey="Blank, B" uniqKey="Blank B">B Blank</name></author><author><name sortKey="Wilson, Kf" uniqKey="Wilson K">KF Wilson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Jia, Y" uniqKey="Jia Y">Y Jia</name></author><author><name sortKey="Chen, Y" uniqKey="Chen Y">Y Chen</name></author><author><name sortKey="Wang, Q" uniqKey="Wang Q">Q Wang</name></author><author><name sortKey="Jayasinghe, U" uniqKey="Jayasinghe U">U Jayasinghe</name></author><author><name sortKey="Luo, X" uniqKey="Luo X">X Luo</name></author><author><name sortKey="Wei, Q" uniqKey="Wei Q">Q Wei</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="O Brien, K" uniqKey="O Brien K">K O'Brien</name></author><author><name sortKey="Rani, S" uniqKey="Rani S">S Rani</name></author><author><name sortKey="Corcoran, C" uniqKey="Corcoran C">C Corcoran</name></author><author><name sortKey="Wallace, R" uniqKey="Wallace R">R Wallace</name></author><author><name sortKey="Hughes, L" uniqKey="Hughes L">L Hughes</name></author><author><name sortKey="Friel, Am" uniqKey="Friel A">AM Friel</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Espagne</li></country><region><li>Catalogne</li><li>Communauté de Madrid</li></region><settlement><li>Barcelone</li><li>Madrid</li></settlement></list><tree><country name="Espagne"><noRegion><name sortKey="Martin Pardillos, Ana" sort="Martin Pardillos, Ana" uniqKey="Martin Pardillos A" first="Ana" last="Martín-Pardillos">Ana Martín-Pardillos</name></noRegion><name sortKey="Bande Vargas, Gemma" sort="Bande Vargas, Gemma" uniqKey="Bande Vargas G" first="Gemma" last="Bande Vargas">Gemma Bande Vargas</name><name sortKey="Bejar Serrano, Eva" sort="Bejar Serrano, Eva" uniqKey="Bejar Serrano E" first="Eva" last="Bejar Serrano">Eva Bejar Serrano</name><name sortKey="Bejar Serrano, Eva" sort="Bejar Serrano, Eva" uniqKey="Bejar Serrano E" first="Eva" last="Bejar Serrano">Eva Bejar Serrano</name><name sortKey="Bribian, Ana" sort="Bribian, Ana" uniqKey="Bribian A" first="Ana" last="Bribian">Ana Bribian</name><name sortKey="Castellvi, Josep" sort="Castellvi, Josep" uniqKey="Castellvi J" first="Josep" last="Castellvi">Josep Castellvi</name><name sortKey="Diaz Lagares, Angel" sort="Diaz Lagares, Angel" uniqKey="Diaz Lagares A" first="Ángel" last="Diaz-Lagares">Ángel Diaz-Lagares</name><name sortKey="Diaz Lagares, Angel" sort="Diaz Lagares, Angel" uniqKey="Diaz Lagares A" first="Ángel" last="Diaz-Lagares">Ángel Diaz-Lagares</name><name sortKey="Guijarro, Pedro J" sort="Guijarro, Pedro J" uniqKey="Guijarro P" first="Pedro J." last="Guijarro">Pedro J. Guijarro</name><name sortKey="Hummer, Stefan" sort="Hummer, Stefan" uniqKey="Hummer S" first="Stefan" last="Hümmer">Stefan Hümmer</name><name sortKey="Hummer, Stefan" sort="Hummer, Stefan" uniqKey="Hummer S" first="Stefan" last="Hümmer">Stefan Hümmer</name><name sortKey="Hurtado Blanco, Pablo" sort="Hurtado Blanco, Pablo" uniqKey="Hurtado Blanco P" first="Pablo" last="Hurtado Blanco">Pablo Hurtado Blanco</name><name sortKey="L Pez L Pez, Rafael" sort="L Pez L Pez, Rafael" uniqKey="L Pez L Pez R" first="Rafael" last="L Pez-L Pez">Rafael L Pez-L Pez</name><name sortKey="L Pez L Pez, Rafael" sort="L Pez L Pez, Rafael" uniqKey="L Pez L Pez R" first="Rafael" last="L Pez-L Pez">Rafael L Pez-L Pez</name><name sortKey="L Pez Mascaraque, Laura" sort="L Pez Mascaraque, Laura" uniqKey="L Pez Mascaraque L" first="Laura" last="L Pez-Mascaraque">Laura L Pez-Mascaraque</name><name sortKey="Lluch Senar, Maria" sort="Lluch Senar, Maria" uniqKey="Lluch Senar M" first="María" last="Lluch-Senar">María Lluch-Senar</name><name sortKey="Martin Pardillos, Ana" sort="Martin Pardillos, Ana" uniqKey="Martin Pardillos A" first="Ana" last="Martín-Pardillos">Ana Martín-Pardillos</name><name sortKey="Miravet Verde, Samuel" sort="Miravet Verde, Samuel" uniqKey="Miravet Verde S" first="Samuel" last="Miravet-Verde">Samuel Miravet-Verde</name><name sortKey="Pi Eiro Cid, Roberto" sort="Pi Eiro Cid, Roberto" uniqKey="Pi Eiro Cid R" first="Roberto" last="Pi Eiro Cid">Roberto Pi Eiro Cid</name><name sortKey="Pi Eiro Cid, Roberto" sort="Pi Eiro Cid, Roberto" uniqKey="Pi Eiro Cid R" first="Roberto" last="Pi Eiro Cid">Roberto Pi Eiro Cid</name><name sortKey="Ram N Y Cajal, Santiago" sort="Ram N Y Cajal, Santiago" uniqKey="Ram N Y Cajal S" first="Santiago" last="Ram N Y Cajal">Santiago Ram N Y Cajal</name><name sortKey="Ram N Y Cajal, Santiago" sort="Ram N Y Cajal, Santiago" uniqKey="Ram N Y Cajal S" first="Santiago" last="Ram N Y Cajal">Santiago Ram N Y Cajal</name><name sortKey="Ram N Y Cajal, Santiago" sort="Ram N Y Cajal, Santiago" uniqKey="Ram N Y Cajal S" first="Santiago" last="Ram N Y Cajal">Santiago Ram N Y Cajal</name><name sortKey="Rodriguez Casanova, Aitor" sort="Rodriguez Casanova, Aitor" uniqKey="Rodriguez Casanova A" first="Aitor" last="Rodriguez-Casanova">Aitor Rodriguez-Casanova</name><name sortKey="Sebastian, Victor" sort="Sebastian, Victor" uniqKey="Sebastian V" first="Víctor" last="Sebastian">Víctor Sebastian</name><name sortKey="Sebastian, Victor" sort="Sebastian, Victor" uniqKey="Sebastian V" first="Víctor" last="Sebastian">Víctor Sebastian</name><name sortKey="Serrano, Luis" sort="Serrano, Luis" uniqKey="Serrano L" first="Luis" last="Serrano">Luis Serrano</name><name sortKey="Serrano, Luis" sort="Serrano, Luis" uniqKey="Serrano L" first="Luis" last="Serrano">Luis Serrano</name><name sortKey="Serrano, Luis" sort="Serrano, Luis" uniqKey="Serrano L" first="Luis" last="Serrano">Luis Serrano</name><name sortKey="Valls Chiva, Angeles" sort="Valls Chiva, Angeles" uniqKey="Valls Chiva A" first="Ángeles" last="Valls Chiva">Ángeles Valls Chiva</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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