A computational framework for testing hypotheses of the minimal mechanical requirements for cell aggregation using early annual killifish embryogenesis as a model

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dc.contributor.authorMontenegro-Rojas, Ignacio
dc.contributor.authorYanez, Guillermo
dc.contributor.authorSkog, Emily
dc.contributor.authorGuerrero-Calvo, Oscar
dc.contributor.authorAndaur-Lobos, Martin
dc.contributor.authorDolfi, Luca
dc.contributor.authorCellerino, Alessandro
dc.contributor.authorCerda, Mauricio
dc.contributor.authorConcha, Miguel L.
dc.contributor.authorBertocchi, Cristina
dc.contributor.authorRojas, Nicolas O.
dc.contributor.authorRavasio, Andrea
dc.contributor.authorRudge, Timothy J.
dc.date.accessioned2024-01-10T12:37:18Z
dc.date.available2024-01-10T12:37:18Z
dc.date.issued2023
dc.description.abstractIntroduction: Deciphering the biological and physical requirements for the outset of multicellularity is limited to few experimental models. The early embryonic development of annual killifish represents an almost unique opportunity to investigate de novo cellular aggregation in a vertebrate model. As an adaptation to seasonal drought, annual killifish employs a unique developmental pattern in which embryogenesis occurs only after undifferentiated embryonic cells have completed epiboly and dispersed in low density on the egg surface. Therefore, the first stage of embryogenesis requires the congregation of embryonic cells at one pole of the egg to form a single aggregate that later gives rise to the embryo proper. This unique process presents an opportunity to dissect the self-organizing principles involved in early organization of embryonic stem cells. Indeed, the physical and biological processes required to form the aggregate of embryonic cells are currently unknown., Methods: Here, we developed an in silico, agent-based biophysical model that allows testing how cell-specific and environmental properties could determine the aggregation dynamics of early Killifish embryogenesis. In a forward engineering approach, we then proceeded to test two hypotheses for cell aggregation (cell-autonomous and a simple taxis model) as a proof of concept of modeling feasibility. In a first approach (cell autonomous system), we considered how intrinsic biophysical properties of the cells such as motility, polarity, density, and the interplay between cell adhesion and contact inhibition of locomotion drive cell aggregation into self-organized clusters. Second, we included guidance of cell migration through a simple taxis mechanism to resemble the activity of an organizing center found in several developmental models., Results: Our numerical simulations showed that random migration combined with low cell-cell adhesion is sufficient to maintain cells in dispersion and that aggregation can indeed arise spontaneously under a limited set of conditions, but, without environmental guidance, the dynamics and resulting structures do not recapitulate in vivo observations., Discussion: Thus, an environmental guidance cue seems to be required for correct execution of early aggregation in early killifish development. However, the nature of this cue (e.g., chemical or mechanical) can only be determined experimentally. Our model provides a predictive tool that could be used to better characterize the process and, importantly, to design informed experimental strategies.
dc.fechaingreso.objetodigital2024-05-23
dc.fuente.origenWOS
dc.identifier.doi10.3389/fcell.2023.959611
dc.identifier.issn2296-634X
dc.identifier.urihttps://doi.org/10.3389/fcell.2023.959611
dc.identifier.urihttps://repositorio.uc.cl/handle/11534/76812
dc.identifier.wosidWOS:000962318200001
dc.information.autorucFacultad de Ciencias Biológicas; Bertocchi No Informado, Cristina; S/I; 1078032
dc.language.isoen
dc.nota.accesocontenido completo
dc.publisherFRONTIERS MEDIA SA
dc.revistaFRONTIERS IN CELL AND DEVELOPMENTAL BIOLOGY
dc.rightsacceso abierto
dc.subjectmulticellularity
dc.subjectmechanics
dc.subjectbiophysics
dc.subjectkillifish
dc.subjectadhesion
dc.subjectmodeling
dc.subject.ods03 Good Health and Well-being
dc.subject.odspa03 Salud y bienestar
dc.titleA computational framework for testing hypotheses of the minimal mechanical requirements for cell aggregation using early annual killifish embryogenesis as a model
dc.typeartículo
dc.volumen11
sipa.codpersvinculados1078032
sipa.indexWOS
sipa.trazabilidadCarga SIPA;09-01-2024
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