Advertisement

Anatomical Science International

, Volume 93, Issue 4, pp 548–558 | Cite as

Transmission electron microscopic and immunohistochemical observations of resting follicles of feathers in chicken show massive cell degeneration

  • Lorenzo AlibardiEmail author
Original Article

Abstract

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 numerous cells present increased heterochromatin and free collagen fibrils in the extracellular matrix. Degeneration of the germinal epithelium of the follicle—the papillary collar—occurs with an initial substantial contraction of cells followed by an increase in heterochromatin, vesicle and lipid accumulation, and membrane and organelle degeneration. Desmosomes are still present between degenerating epithelial cells, but ribosomes and tonofilaments disappear. This suggests that cell necrosis initially proceeds as a major contraction resembling apoptosis—a process termed necroptosis, which was previously also shown to occur during the formation of barbs and barbules in mature down and pennaceous feathers. This study suggests that, aside from apoptosis, the collar epithelium degenerates due to external factors, in particular the retraction of blood vessels supplying the dermal papilla. In contrast, revascularization of the dermal papilla triggers a new phase of feather growth (anagen).

Keywords

Chick Feather Follicle Dermal papilla Regression Ultrastructure 

Notes

Acknowledgments

This research, in particular the entire electron microscopy study, was self-supported (Comparative Histolab).

Compliance with ethical standards

Conflict of interest

I declare no conflict of interest in relation to the present manuscript.

References

  1. Alibardi L (2004) Dermo–epidermal interactions in reptilian scales: speculations on the evolution of scales, feathers and hairs. J Exp Zool 302B:365–383Google Scholar
  2. Alibardi L (2005a) Cell structure of developing barbs and barbules in downfeathers of the chick: central role of barb ridge morphogenesis for the evolution of feathers. J Subm Cytol Pathol 37:19–41Google Scholar
  3. Alibardi L (2005b) Fine structure of juvenile feathers of the zebrafinch in relation to the evolution and diversification of pennaceous feathers. J Subm Cytol Pathol 37:323–343Google Scholar
  4. Alibardi L (2007a) Cell interactions in barb ridges of developing chick downfeather and the origin of feather branching. Ital J Zool 74:143–155CrossRefGoogle Scholar
  5. Alibardi L (2007b) Wedge cells during regeneration of juvenile and adult feathers and their role in carving out the branching pattern of barbs. Ann Anat 189:234–242CrossRefPubMedGoogle Scholar
  6. Alibardi L (2007c) Cytological aspects of the differentiation of barb cells during the formation of the ramus in feathers. Int J Morphol 25:73–83CrossRefGoogle Scholar
  7. Alibardi L (2008) Follicular patterns during feather morphogenesis in relation to the formation of asymmetric feathers, filoplumes and bristles Ital. J Zool 76:279–290Google Scholar
  8. Alibardi L (2009a) Molding and carving cell surfaces: the joke of a fold and the origin and evolution of feathers. In: Gorb S (ed) Surface biology, vol 9. Springer, Berlin, pp 163–176Google Scholar
  9. Alibardi L (2009b) Cornification of the pulp epithelium and formation of pulp cups in downfeathers and regenerating feathers. Anat Sci Int 84:269–279CrossRefPubMedGoogle Scholar
  10. Alibardi L (2010) Ultrastructure of cells of the dermal papilla in pennaceous feathers. Trends Dev Biol 5:51–60Google Scholar
  11. Alibardi L (2016) Review: cornification, morphogenesis and evolution of feathers. Protoplasma 254:1259–1281CrossRefPubMedGoogle Scholar
  12. Alibardi L, Sawyer RH (2006) Cell structure of developing downfeathers in the zebrafinch with emphasis on barb ridge morphogenesis. J Anat 208:621–642CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chang CH, Yu MY, Wu P, Jiang TX, Yu HS, Widelitz RB, Chuong MC (2004) Sculpting skin appendages out of epidermal layers via temporally and spatially regulated apoptotic events. J Inv Dermatol 122:1348–1355CrossRefGoogle Scholar
  14. Charriaut-Marlague C, Ben-Ari Y (1995) A cautionary note on the use of the TUNEL stain to determine apoptosis. NeuroReport 7:61–64CrossRefGoogle Scholar
  15. Chodankar R, Cheng CH, Yue Z, Jiang TX, Suskaweang S, Burrus LW, Chuong CM, Widelitz RB (2002) Shift of localized growth zones contributes to skin appendage morphogenesis: role of the Wnt/-β-catenin pathway. J Inv Dermat 120:20–26CrossRefGoogle Scholar
  16. Chu Q, Cai L, Chen X, Yan Z, Lin X, Zhou G, Han H, Widelitz RB, Chuong CM, Wu W, Yue Z (2014) Dkk2/Frzb in the dermal papillae regulates feather regeneration. Dev Biol 387:167–178CrossRefPubMedPubMedCentralGoogle Scholar
  17. Demarchez M, Mauger A, Sengel P (1981) The dermal-epidermal junction during the development of the skin and cutaneous appendages in the chick embryo. Arch Anat Microsc Morphol Experim 70:206–218Google Scholar
  18. Dhouailly D (2009) A new scenario for the evolutionary origin of hair, feather, and avian scales. J Anat 214:587–606CrossRefPubMedPubMedCentralGoogle Scholar
  19. Goff RA (1949) Development of the mesodermal costituents of feather germs of chick embryos. J Morphol 85:443–481CrossRefPubMedGoogle Scholar
  20. Heryanto B, Yoshimura Y, Tamura T, Okamoto T (1997) Involvement of apoptosis and lysosomal hydrolase activity in the oviductal regression during induced molting in chickens: a cytochemical study for end labeling of fragmented DNA and acid phosphatase. Poultry Sci 76:67–72CrossRefGoogle Scholar
  21. Li A, Figueroa S, Jiang TX, Wu P, Widelitz R, Nie Q, Chuong CM (2017) Diverse feather shape evolution enabled by coupling anisotropic signaling modules with self-organizing branching programme. Nat Commun 8:ncomms14139.  https://doi.org/10.1038/ncomms14139
  22. Lucas AM, Stettenheim PR (1972) Growth of follicles and feathers. Color of feathers and integument. Avian anatomy. Integument. Agriculture Handbook 362, 7th edn. US Department of Agriculture, Washington, DC, pp 341–419Google Scholar
  23. Maderson PFA, Hillenius WJ, Hiller U, Dove CC (2009) Toward a comprehensive model of feather regeneration. J Morph 270:1166–1208CrossRefPubMedGoogle Scholar
  24. Mayhew TM, Myklebust R, Whybrow A, Jenkins R (1999) Epithelial integrity, cell death and cell loss in mammalian small intestine. Histol Histopathol 14:257–267PubMedGoogle Scholar
  25. Mesa KR, Rompolas P, Zito G, Myung P, Sun TY, Brown R, Gonzales DG, Blagoev KB, Haberman AM, Greco V (2015) Niche-induced cell death and epithelial phagocytosis regulate hair follicle stem cell pool. Nature 522:94–97CrossRefPubMedPubMedCentralGoogle Scholar
  26. Mlitz V, Strasser B, Jaeger K, Hermann M, Ghannadan M, Buchberger M, Alibardi L, Tschachler E, Eckhart L (2014) Trichohyalin-like proteins have evolutionarily conserved roles in the morphogenesis of skin appendages. J Invest Dermatol 134:2682–2692CrossRefGoogle Scholar
  27. Olivera-Martinez Viallet JP, Michon F, Peraston DJ, Dhouailly D (2004) The different steps of skin formation in vertebrates. Int J Dev Biol 48:107–115CrossRefPubMedGoogle Scholar
  28. Parakkal PF (1966) The fine structure of the dermal papilla of the guinea pig hair follicle. J Ultrastr Res 14:133–142CrossRefGoogle Scholar
  29. Prum RO, Brush AH (2002) The evolutionary origin and diversification of feathers. Quart Rev Biol 77:261–295CrossRefPubMedGoogle Scholar
  30. Roth SI (1965) The cytology of the murine resting (telogen) hair follicle. In: Lyne AG, Short BF (eds) Biology of the skin and hair growth. Angus and Robertson Pbl, Sydney, pp 233–250Google Scholar
  31. Roth SI, Helwig EB (1964) The cytology of the dermal papilla, the bulb, and the roots of the mouse hair. J Ultrastr Res 11:33–51CrossRefGoogle Scholar
  32. Sawyer RH, Knapp LW (2003) Avian skin development and the evolutionary origin of feathers. J Exp Zool 298B:57–72CrossRefGoogle Scholar
  33. Sawyer RH, Rogers L, Washington L, Glenn TC, Knapp LW (2005) Evolutionary origin of the feather epidermis. Dev Dyn 232:256–267CrossRefPubMedGoogle Scholar
  34. Schwartz LM, Smith SW, Jones MEE, Osborne BA (1993) Do all programmed cell death occur via apoptosis? PNAS 90:980–984CrossRefPubMedGoogle Scholar
  35. Sengel P (1975) Morphogenesis of skin. Cambridge University Press, CambridgeGoogle Scholar
  36. Spearman RIC, Hardy JA (1985) Integument. In: King AS, McLelland J (eds) Form and function of birds, vol 3. Academic, London, pp 1–56Google Scholar
  37. Stenn KS, Paus R (2001) Controls of hair follicle cycling. Phys Rev 81:449–494Google Scholar
  38. Sugiyama S, Takahashi M, Kamimura M (1976) The ultrastructure of the hair follicle in early and late catagen, with special references to the alteration of the junctional structure between the dermal papilla and epithelial component. J Ultrastr Res 54:359–373CrossRefGoogle Scholar
  39. Suksaweang S, Jiang TX, Robyal P, Chuong CM, Widelitz R (2012) Role of EphB3/ephrin B1 in feather morphogenesis. Int J Dev Biol 56:719–728CrossRefPubMedPubMedCentralGoogle Scholar
  40. Weinlich R, Oberst A, Beere HM, Green DR (2017) Necroptosis in development, inflammation and disease. Nat Rev Mol Cell Biol 18:127–136CrossRefPubMedGoogle Scholar
  41. Yu M, Yue Z, Wu P, Wu DY, Mayer JA, Medina M, Widelitz RB, Jiang TX, Chuong CM (2004) The developmental biology of feather follicle. Int J Dev Biol 48:181–191CrossRefPubMedPubMedCentralGoogle Scholar
  42. Yuan J, Kroemer G (2010) Alternative cell death mechanisms in development and beyond. Genes Devel 24:2592–2602CrossRefPubMedGoogle Scholar
  43. Yue Z, Jiang TX, Widelitz RB, Chuong CM (2005) Mapping stem cell activities in the feather follicle. Nature 438:1026–1029CrossRefPubMedPubMedCentralGoogle Scholar
  44. Yue Z, Jiang TX, Wu P, Widelitz RB, Chuong CM (2012) Sprouty/FGF signaling regulates the proximal-distal feather morphology and the size of dermal papillae. Dev Biol 372:45–54CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Japanese Association of Anatomists 2018

Authors and Affiliations

  1. 1.Comparative Histolab Padova, Dipartimento di BiologiaUniversità di BolognaBolognaItaly

Personalised recommendations