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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Cited By22
Lorenzo Alibardi25
Estimated H-index: 25
(University of Bologna)
This review presents comparative aspects of epidermal keratinization in vertebrates, with emphasis on the evolution of the stratum corneum in land vertebrates. The epidermis of fish does not contain proteins connected with interkeratin matrix and corneous cell envelope formation. Mucus‐like material glues loose keratin filaments. In amphibians a cell corneous envelope forms but matrix proteins, aside from mucus/glycoproteins, are scarce or absent. In reptiles, birds, and mammals specific protein...
61 Citations Source Cite
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 Oct 1, 2009in Journal of Morphology 1.71
Paul F. A. Maderson20
Estimated H-index: 20
(Brooklyn College),
Willem J. Hillenius11
Estimated H-index: 11
(College of Charleston)
+ 1 AuthorsCarla C. Dove1
Estimated H-index: 1
(Smithsonian Institution)
Understanding of the regeneration of feathers, despite a 140 year tradition of study, has remained substantially incomplete. Moreover, accumulated errors and mis-statements in the literature have confounded the intrinsic difficulties in describing feather regeneration. Lack of allusion to Rudall's (Rudall [1947] Biochem Biophys Acta 1:549–562) seminal X-ray diffraction study that revealed two distinct keratins, β- and α-, in a mature feather, is one of the several examples where lack of citation...
26 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 Jan 1, 2009in Acta Zoologica 1.07
Lorenzo Alibardi25
Estimated H-index: 25
(University of Bologna)
The embryogenesis and cytology of the epidermis in different vertebrates is variable in relation to the formation of a stratum corneum of different complexity. The latter process was essential for land colonization during vertebrate evolution and produced an efficient barrier in amniotes. Keratinocytes are made of cross-linked keratins associated with specific proteins and lipids that are produced at advanced stages of embryogenesis when the epidermis becomes stratified. In these stages the epid...
23 Citations Source Cite
Published on Jun 1, 2010in Anatomical Science International 1.33
Lorenzo Alibardi27
Estimated H-index: 27
(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
Published on Jan 1, 2006in Cells Tissues Organs 1.27
Lorenzo Alibardi27
Estimated H-index: 27
(University of Bologna)
During the differentiation of cells in developing down feathers of the chick embryo, keratin and associated proteins are synthesized. Previous studies indicated that a histidine-rich protein with a di
5 Citations Source Cite
Published on Jun 1, 2007in Italian Journal of Zoology 0.60
L. Alibardi4
Estimated H-index: 4
(University of Bologna)
The epidermis of developing feathers comprises outer and inner periderm, subperiderm and germinal layer. The inner periderm gives origin to sheath and barb ridge vane cells that contain alpha‐keratin and form a belt around feather filaments. This produces mechanical resistance, forcing the inner epidermal cell layers to fold inward and form barb ridges. Mesenchymal‐epidermal contacts occur from the mesenchymal core to external regions of barb ridges and involve thin cytoplasmic processes (filopo...
13 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 ...
12 Citations Source Cite
Lorenzo Alibardi25
Estimated H-index: 25
(University of Bologna),
Mattia Toni19
Estimated H-index: 19
(University of Bologna)
Abstract Feathers are the most complex epidermal derivatives among vertebrates. The present review deals with the origin of feathers from archosaurian reptiles, the cellular and molecular aspects of feather morphogenesis, and focus on the synthesis of keratins and associated proteins. Feathers consist of different proteins among which exists a specialized group of small proteins called beta-keratins. Genes encoding these proteins in the chick genome are distributed in different chromosomes, and ...
45 Citations Source Cite