BACKGROUND: Xenopus embryonic skin is composed of the superficial layer with defined apicobasal polarity and the inner layer lacking the apical domain. Multiciliated cells (MCCs) originate in the inner layer of the epidermal ectoderm and subsequently migrate to the surface. How MCCs acquire the apicobasal polarity and intercalate into the superficial layer during neurulation is largely unknown. As Rab11-dependent vesicle trafficking has been implicated in ciliary membrane assembly and in apical domain formation in epithelial cells, we assessed the involvement of Rab11 in MCC development. RESULTS: Here we report that Rab11 is specifically enriched and becomes apically polarized in skin MCCs. Interference with Rab11 function by overexpression of a dominant negative mutant or injection of a specific morpholino oligonucleotide inhibited MCC intercalation into the superficial layer. Dominant negative Rab11-expressing MCC precursors revealed intrinsic apicobasal polarity, characterized by the apical domain, which is not normally observed in inner layer cells. Despite the presence of the apical domain, the cells with inhibited Rab11 function were randomly oriented relative to the plane of the tissue, thereby demonstrating a defect in planar polarity. CONCLUSIONS: These results establish a requirement for Rab11 in MCC development and support a two-step model, in which the initial polarization of MCC precursors is critical for their integration into the superficial cell layer.
BACKGROUND:Xenopusembryonic skin is composed of the superficial layer with defined apicobasal polarity and the inner layer lacking the apical domain. Multiciliated cells (MCCs) originate in the inner layer of the epidermal ectoderm and subsequently migrate to the surface. How MCCs acquire the apicobasal polarity and intercalate into the superficial layer during neurulation is largely unknown. As Rab11-dependent vesicle trafficking has been implicated in ciliary membrane assembly and in apical domain formation in epithelial cells, we assessed the involvement of Rab11 in MCC development. RESULTS: Here we report that Rab11 is specifically enriched and becomes apically polarized in skin MCCs. Interference with Rab11 function by overexpression of a dominant negative mutant or injection of a specific morpholino oligonucleotide inhibited MCC intercalation into the superficial layer. Dominant negative Rab11-expressing MCC precursors revealed intrinsic apicobasal polarity, characterized by the apical domain, which is not normally observed in inner layer cells. Despite the presence of the apical domain, the cells with inhibited Rab11 function were randomly oriented relative to the plane of the tissue, thereby demonstrating a defect in planar polarity. CONCLUSIONS: These results establish a requirement for Rab11 in MCC development and support a two-step model, in which the initial polarization of MCC precursors is critical for their integration into the superficial cell layer.
Authors: David M Bryant; Anirban Datta; Alejo E Rodríguez-Fraticelli; Johan Peränen; Fernando Martín-Belmonte; Keith E Mostov Journal: Nat Cell Biol Date: 2010-10-03 Impact factor: 28.824
Authors: Olga Ossipova; Chih-Wen Chu; Jonathan Fillatre; Barbara K Brott; Keiji Itoh; Sergei Y Sokol Journal: Dev Biol Date: 2015-06-14 Impact factor: 3.582
Authors: Talia Nasr; Pamela Mancini; Scott A Rankin; Nicole A Edwards; Zachary N Agricola; Alan P Kenny; Jessica L Kinney; Keziah Daniels; Jon Vardanyan; Lu Han; Stephen L Trisno; Sang-Wook Cha; James M Wells; Matthew J Kofron; Aaron M Zorn Journal: Dev Cell Date: 2019-12-05 Impact factor: 12.270