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Cell structure of developing barbs and barbules in downfeathers of the chick: Central role of barb ridge morphogenesis for the evolution of feathers.

Lorenzo Alibardi25
Estimated H-index: 25
Abstract
Abstract The present ultrastructural study shows how cells organize to form the complex structure of downfeathers in chick embryos. The embryonic epidermis of the apical part of feather filaments folds inward forming barb ridges which extend toward the base of the feather. The stratification of epidermal cells in barb ridges is maintained but the basal layer loses most of the germinal activity. New cells for the growth of feather filaments are mainly produced in its basal part. In barb ridges only the original four epidermal layers of the embryonic epidermis remain to form feathers: 1) the external periderm, 2) three-five layers of the feather sheath and barb vane ridge cells, 3) subperiderm cells, and 4) basal or cylindrical cells. Periderm, sheath, barb vane ridge and cylindrical cells synthesize only alpha-keratin. Instead, cells of the subperiderm layer synthesize a small type of beta-keratin: feather beta-keratin. At hatching, the subperiderm layer is lost in most areas of the skin of the chick (apteric and scaled), and is replaced by cells containing alpha-keratin (interfollicular-apteric epidermis), scale beta-keratin (scales), beak beta-keratin (beak), and claw beta-keratin (claws). Only in feathers, cells of the original subperiderm layer remain and give origin to barb and barbule cells. The formation of separated chains of barb and barbule cells is allowed by the presence of barb vane ridge cells that function as spacers between merging cells of barb and barbule cells. Subperiderm cells elongate and merge into a syncitium to form barbules and barbs. While barbule and barb cells accumulate feather-keratin, barb vane and cylindrical cells accumulate lipids, vesicles and little alpha-keratin. These cells eventually degenerate by necrosis leaving empty spaces and lipids between barbules and barbs. No apoptosis is necessary to explain the process of carving out of barb and barbules in feathers after dissolution of the external sheath. In fact, the retraction of blood vessels nourishing the apical part of the feather filament determines anoxia and eventually necrosis of all cells of the feather. While sheath, barb vane and cylindrical cells degenerate, the keratinized syncitium forming barbs and barbules simply remain in place to form the ramifications of feathers. The formation of barb ridges is considered as the evolutionary innovation necessary for the origin of feathers. The evolution of the morphogenetic process of barb ridge formation within epidermal tubular outgrowths of the integument of ancient archosaurians was an evolutionary novelty, a true avian and theropod characteristic. Barb ridges morphogenesis determines the contemporary formation of barb and barbule cells as a unique and inseparable process so that intermediate forms of evolving feathers with only barbs but not barbules are unlikely. Barb ridges can merge with a large ridge (rachis) or into branched ridges, a process which was at the origin of the ramogenic process from which pennaceous feathers evolved.
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Published on Sep 1, 2018in Anatomical Science International 1.33
Lorenzo Alibardi27
Estimated H-index: 27
(University of Bologna)
The molting cycle of feathers includes an anagen (growth) stage, a likely catagen stage where the feather follicles degenerate, and a resting stage where fully grown feathers remain in their follicles and are functional before molting. However, the cytological changes involved in the resting and molting stages are poorly known, so the results of an ultrastructural analysis of these processes in adult chick feathers are presented here. The study showed that the dermal papilla shrinks, and numerou...
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Published on Dec 1, 2016in Current Biology 9.25
Lida Xing18
Estimated H-index: 18
(China University of Geosciences),
Ryan C. McKellar5
Estimated H-index: 5
(University of Regina)
+ 11 AuthorsAlexander P. Wolfe47
Estimated H-index: 47
(University of Alberta)
Summary In the two decades since the discovery of feathered dinosaurs [1–3], the range of plumage known from non-avialan theropods has expanded significantly, confirming several features predicted by developmentally informed models of feather evolution [4–10]. However, three-dimensional feather morphology and evolutionary patterns remain difficult to interpret, due to compression in sedimentary rocks [9, 11]. Recent discoveries in Cretaceous amber from Canada, France, Japan, Lebanon, Myanmar, an...
32 Citations Source Cite
Published on Oct 1, 2014in Micron 1.73
Lorenzo Alibardi27
Estimated H-index: 27
(University of Bologna)
Abstract The change in the modality of cornification from embryonic to definitive epidermis in the chick has been studied using immunocytochemistry and electron microscopy to show that the initial soft cornification based on an acidic type I alpha-keratin transits to a definitive hard cornification based on beta-proteins in the claw, scales and feathers. The first two periderm layers contain acidic keratins associated with periderm granules and participate in a mild form of cornification before ...
4 Citations Source Cite
Published on Jul 1, 2014in Journal of Morphology 1.71
Lorenzo Alibardi27
Estimated H-index: 27
(University of Bologna),
Ping Wu23
Estimated H-index: 23
(University of Southern California),
Cheng-Ming Chuong61
Estimated H-index: 61
(University of Southern California)
Feathers regenerate from stem cells localized in a region of the follicle indicated as the bulge of the collar. Stem cells are slow cycling cells and some of these cells can be identified after labeling experiments using 5-bromo-deoxyuridine to detect label retaining cells (5BrdU LRCs). The present electron microscopic analysis of 5BrdU LRCs has described the ultrastructural characteristics of small cells present in the bulge region of the follicle in regenerating feathers of chickens that inclu...
1 Citations Source Cite
Published on Mar 1, 2013in Annals of Anatomy-anatomischer Anzeiger 1.85
Lorenzo Alibardi27
Estimated H-index: 27
(University of Bologna)
Summary The maturation of the corneous material of feathers is a special case of cornification in vertebrate epidermis and is believed to occur mainly by the accumulation of small proteins of about 100 amino acids and a central beta-pleated sheet region known as feather keratins. The present immunocytochemical study carried out using double-labeling immunogold shows that a small amount of alpha-keratins of intermediate filament type form the early keratin clumps in barb and barbule cells. These ...
13 Citations Source Cite
Published on Apr 7, 2012in Journal of the Royal Society Interface 3.35
Rafael Maia15
Estimated H-index: 15
(University of Akron),
Regina H. Macedo18
Estimated H-index: 18
,
Matthew D. Shawkey30
Estimated H-index: 30
Avian plumage colours are model traits in understanding the evolution of sexually selected ornamental traits. Paradoxically, iridescent structural colours, probably the most dazzling of these traits, remain the most poorly understood. Though some data suggest that expression of bright iridescent plumage colours produced by highly ordered arrays of melanosomes and keratin is condition-dependent, almost nothing is known of their ontogeny and thus of any developmental mechanisms that may be suscept...
30 Citations Source Cite
Xu Yl1
Estimated H-index: 1
,
Sun Jg1
Estimated H-index: 1
+ 1 AuthorsXi Ym1
Estimated H-index: 1
Feather follicles have the extraordinary ability to regenerate and undergo molting cycles. Being tissue-specific stem cells, feather follicle stem cells (FFSCs) have a strong capacity for proliferation and are presumed to be progenitor cells for various epidermal organs. In order to characterize FFSCs and to understand how the feather epidermis and FFSCs produce such a reliable differentiation program resulting in the formation of complex feathers, We developed a culture scheme to select and exp...
3 Citations
Published on Jan 1, 2011in Acta Zoologica 1.07
Lorenzo Alibardi27
Estimated H-index: 27
(University of Bologna)
Alibardi, L. 2011. Cell junctions during morphogenesis of feathers: general ultrastructure with emphasis on adherens junctions. —Acta Zoologica (Stockholm) 92: 89–100. The present ultrastructural and immunocytochemical study analyzes the cell junctions joining barb/barbule cells versus cell junctions connecting supportive cells in forming feathers. Differently from the epidermis or the sheath, desmosomes are not the prevalent junctions among feather cells. Numerous adherens junctions, some gap j...
1 Citations Source Cite
Published on Aug 1, 2010in Annals of Anatomy-anatomischer Anzeiger 1.85
Lorenzo Alibardi25
Estimated H-index: 25
(University of Bologna)
Summary The present study has focused on the distribution and ultrastructure of gap and tight junctions responsible for the formation of the barb/barbule branching in developing feathers using immunocytochemical detection. Apart from desmosomes, both tight and gap junctions are present between differentiating barb/barbule cells and during keratinization. While gap junctions are rare along the perimeter of these cells, tight junctions tend to remain localized in nodes joining barbule cells and be...
7 Citations Source Cite
Published on Jun 1, 2010in Anatomical Science International 1.33
Lorenzo Alibardi25
Estimated H-index: 25
(University of Bologna)
The present ultrastructural study on follicle of regenerating feathers of four different avian species focuses on the formation and cytology of the rachis. Epithelial cells within the bottom part of the follicle (the collar) are contacted from mesenchymal cells of the dermal papilla. The most basal part of the collar is formed by a circular epithelium containing germinal cells, while in the upper ramogenic part of the collar barb ridges are generated. Epithelial cells rest upon a basement membra...
5 Citations Source Cite