Molecular mechanisms of tubulogenesis revealed in the sea star hydro-vascular organ

Abstract

A fundamental goal in the organogenesis field is to understand how cells organize into tubular shapes. Toward this aim, we have established the hydro-vascular organ in the sea star Patiria miniata as a model for tubulogenesis. In this animal, bilateral tubes grow out from the tip of the developing gut, and precisely extend to specific sites in the larva. This growth involves cell migration coupled with mitosis in distinct zones. Cell proliferation requires FGF signaling, whereas the three-dimensional orientation of the organ depends on Wnt signaling. Specification and maintenance of tube cell fate requires Delta/Notch signaling. Moreover, we identify target genes of the FGF pathway that contribute to tube morphology, revealing molecular mechanisms for tube outgrowth. Finally, we report that FGF activates the Six1/2 transcription factor, which serves as an evolutionarily ancient regulator of branching morphogenesis. This study uncovers distinct mechanisms of tubulogenesis in vivo and we propose that cellular dynamics in the sea star hydro-vascular organ represents a key comparison for understanding the evolution of vertebrate organs.

A description of the bat star nervous system throughout larval ontogeny

“…Three larval stages were chosen to describe neural organization through the development of P. miniata. These are referred to as early larva, bipinnaria, and brachiolaria, following previous descriptions of larval development in asteroids (Byrne & Barker, 1991;Koren & Danielssen, 1857;Mayorova et al, 2016;Muller, 1852;Perillo et al, 2023). Though these stages have been described in detail by other authors, the staging used for this study is re-described here briefly to clarify the specific developmental timepoints used in following in situ hybridization experiments.…”

“…At the early stage, the ciliary band comprised two connected ventral loops: the anteriorly located transverse preoral ciliary band (TPrO) and posteriorly located transverse postoral ciliary band (TPO) (Figure 1a,b). At this stage, larvae had a functional tripartite digestive system, a pair of dorsal muscles enabling lateral contractions, circumesophageal muscles involved in digestion, and two ciliated coeloms connecting to the ciliated hydropore (Perillo et al, 2023;Strathmann, 1971) (Figure 1b,c). At the bipinnaria stage (Figure 1d), folds forming appendages developed in the ciliary band (Figure 1d,e) and longer aboral muscles were present, projecting from the apical regions towards the esophagus (Figure 1f).…”

Detection of TALEN‐mediated genome cleavage during the early embryonic stage of the starfish Patiria pectinifera

“…They also reported that knockout of Gus suppressed its gene function of Vasa clearance from somatic cells in 5‐dpf larvae 24 . In addition, Perillo et al carried out CRISPR‐Cas9‐driven knockouts of delta , six1/2 , fgfr1 , and fz1/2/7 in P. miniata 13 . They observed each effect of knockout on the tubulogenesis of late gastrula to early bipinnaria larvae.…”

“…In particular, echinoderms are often used to study the genetic control of developmental processes and their evolution 2,3 . Among echinoderms, starfish have been used to investigate various developmental phenomena such as whole‐body regeneration, germline formation, and early specification 4‐14 . For example, gene regulatory networks (GRNs) of early specification have been unraveled in starfish embryos and compared with other echinoderms to elucidate the evolutionary transition of GRN circuits 5,6,8‐12,14 .…”

“…It should be noted that a homozygous mutant was generated using the CRISPR/Cas9 system in the sea urchins Temnopleurus reevesii and Lytechinus pictus 20,21 . Recently, genome editing techniques have been also employed in studies using starfish 10,13,22‐25 . For example, we previously reported the feasibility of the genome editing method TALEN in the starfish Patiria pectinifera 10,23 .…”