The chicken left right organizer has nonmotile cilia which are lost in a stage‐dependent manner in the talpid3 ciliopathy

Louise A Stephen,Edward J Johnson,Lynn Mcteir,Gemma M Davis,Megan G Davey,Jamie Pinkham,Neema Jaberi

doi:10.1002/dvg.22775

Louise A Stephen, Edward J Johnson + Show 5 more

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https://doi.org/10.1002/dvg.22775

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Abstract

Motile cilia are an essential component of the mouse, zebrafish, and Xenopus laevis Left Right Organizers, generating nodal flow and allowing the reception and transduction of mechanosensory signals. Nonmotile primary cilia are also an important component of the Left Right Organizer's chemosensory mechanism. It has been proposed in the chicken that signaling in Hensen's node, the Left Right Organizer of the chicken, is independent of cilia, based on a lack of evidence of motile cilia or nodal flow. It is speculated that the talpid3 chicken mutant, which has normal left–right patterning despite lacking cilia at many stages of development, is proof of this hypothesis. Here, we examine the evidence for cilia in Hensen's node and find that although cilia are present; they are likely to be immotile and incapable of generating nodal flow. Furthermore, we find that early planar cell polarity patterning and ciliogenesis is normal in early talpid3 chicken embryos. We conclude that patterning and development of the early talpid3 chicken is normal, but not necessarily independent of cilia. Although it appears that Hensen's node does not require motile cilia or the generation of motile flow, there may remain a requirement for cilia in the transduction of SHH signaling.ResultsFOXJ1 is expressed at low levels in the chicken node incompatible with motile cilia generationShort cilia are present in the mesodermal cells of the chicken nodeTalpid3 chicken embryos have normal VANGL2 localization early in developmentTalpid3 chicken embryos have primary cilia early in development

Highlights

IntroductionA loss of function mutation in TALPID3 was first mapped in the recessive, embryonic lethal, polydactylous talpid chicken breed (Davey et al, 2006), and TALPID3 has since been shown to be essential for motile and nonmotile ciliogenesis in the mouse, chicken, and zebrafish (Bangs et al, 2011; Ben et al, 2011; Stephen et al, 2013; Yin et al, 2009)
TALPID3 (KIAA0586) is an essential gene for vertebrate development
We have previously reported that the Talpid32/2 mouse exhibits randomization of laterality in abnormal cardiac looping (Bangs et al, 2011), whereas the talpid3 chicken heart has normal heart looping, liver lobe specification and stomach turning, the sample numbers were low (n 5 2 for liver and stomach patterning)

Summary

Introduction

A loss of function mutation in TALPID3 was first mapped in the recessive, embryonic lethal, polydactylous talpid chicken breed (Davey et al, 2006), and TALPID3 has since been shown to be essential for motile and nonmotile ciliogenesis in the mouse, chicken, and zebrafish (Bangs et al, 2011; Ben et al, 2011; Stephen et al, 2013; Yin et al, 2009). A loss of Additional Supporting Information may be found in the online version of this article.

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