Retinal stem cells modulate proliferative parameters to coordinate post-embryonic morphogenesis in the eye of fish

Author:

Tsingos Erika1ORCID,Höckendorf Burkhard1,Sütterlin Thomas2,Kirchmaier Stephan1,Grabe Niels2,Centanin Lazaro1ORCID,Wittbrodt Joachim1ORCID

Affiliation:

1. Centre for Organismal Studies Heidelberg, Heidelberg University, Heidelberg, Germany

2. National Center for Tumor Diseases, Hamamatsu TIGA Center, Bioquant, Heidelberg University, Heidelberg, Germany

Abstract

Combining clonal analysis with a computational agent based model, we investigate how tissue-specific stem cells for neural retina (NR) and retinal pigmented epithelium (RPE) of the teleost medaka (Oryzias latipes) coordinate their growth rates. NR cell division timing is less variable, consistent with an upstream role as growth inducer. RPE cells divide with greater variability, consistent with a downstream role responding to inductive signals. Strikingly, the arrangement of the retinal ciliary marginal zone niche results in a spatially biased random lineage loss, where stem- and progenitor cell domains emerge spontaneously. Further, our data indicate that NR cells orient division axes to regulate organ shape and retinal topology. We highlight an unappreciated mechanism for growth coordination, where one tissue integrates cues to synchronize growth of nearby tissues. This strategy may enable evolution to modulate cell proliferation parameters in one tissue to adapt whole-organ morphogenesis in a complex vertebrate organ.

Funder

European Union Seventh Framework Programme

Research Training Group Mathematical Modelling for the Quantitative Biosciences

Heidelberg Biosciences International Graduate School HBIGS

Joachim Herz Stiftung

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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