Evo-Devo of feathers and scales: Building complex epithelial appendages. Commentary

Current Opinion in Genetics and Development

Volumn 10, Issue 4, 2000, Pages 449-456

  Chuong, Cheng Ming ^a   Chodankar, Rajas ^a   Widelitz, Randall B ^a   Jiang, Ting Xin ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEVELOPMENT; EVOLUTION; FEATHER; MORPHOGENESIS; NONHUMAN; OVARY FOLLICLE CELL; PRIORITY JOURNAL; REVIEW;

EID: 0033949688     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(00)00111-8     Document Type: Review

References (53)

1. Landmann L. The skin of reptiles: epidermis and dermis. Bereiter-Hahn J., Matoltsy A.G., Richards S. Biology of the Integument. 1984;150-187 Springer-Verlag, New York.
2. Lucas, A.M., Stettenheim, P.R. Avian anatomy: integument. In Agriculture Handbook, Vol. 362. Agricultural Research Services. US Department of Agriculture: Washington, DC; 1972:1-750. An excellent factual book with beautiful illustrations; it inspires us to wonder how molecules are used to form those complex morphologies - micro- and nano-structures.
3. Sawyer R.H., Goetinck P.F. Developmental genetics of the integument and limbs of the domestic chicken. Malacinski G.M., Bryant S.V. Pattern Formation. 1984;581-601 Macmillian, New York.
4. Tanaka S., Kato Y. Epigenesis in developing avian scales. I. and II. J Expt Zool. 225:1983;257-283. Using 3H thymidine, this is a careful study of the dynamic distribution of proliferating cells in scale morphogenesis. The question for us now is to find the molecular regulators behind those patterns. This paper also showed that proliferating cells are distributed widely in scale regions, unlike the much more localized distribution in feather follicles.
5. Gill F.B. Ornithology, edn 2. 1994;Freeman, New York.
6. Sengel P. Morphogenesis of Skin. 1976;Cambridge University Press, Cambridge. This is a beautifully written book covering the classic experimental embryology experiments achieved by the author and his peers from 1950-1976. The development of the book is very logical and clear and is a must-read for those who want to enter this field.
7. Chuong C-M. Molecular Basis of Epithelial Appendage Morphogenesis. 1998;Landes Bioscience Austin, TX. This book integrates classic studies with more recent molecular studies. Hypothesizing that all epithelial appendages are variations on top of a common (molecular pathway) theme, experts in feather, hair, lung, tooth, and gut morphogenesis discuss and compare the recently identified molecular mechanisms of different epithelial organs. An overview chapter on ectodermal dysplasia links the broader biology issues with human medical genetics.
8. Rawles M. Tissue interactions in scale and feather development as studies in dermal epidermal recombinations. J Embyol Exp Morphol. 11:1963;765-789.
9. Dhouailly D. Formation of cutaneous appendages in dermal epidermal recombinations between reptiles, birds, and mammals. Wilhelm Roux Arch Dev Biol. 177:1975;323-340. Creative ideas coupled to technically complex experiments, revealing that dermal messages can traverse vertebrate classes; however, the epidermis can only do as much as its genetic information allows.
10. Cairns J., Saunders J.W. The influence of embryonic mesoderm on the regional specification of epidermal derivatives in the chick. J Exp Zool. 127:1954;221-248. Classic recombination experiments showing specificity in mesenchyme.
11. Jiang T-X., Jung H-S., Widelitz R.B., Chuong C-M. Self-organization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordial. Development. 126:1999;4997-5009. Fundamental pattern formation issues are here addressed using the 'ideal feather' model and a novel feather reconstitution assay that is able to reset the patterning process back to ground zero. We show that the periodic feather patterning process involves mechanisms such as competitive equilibrium and reaction diffusion - the 'rules' that guide the final patterns. Whether a cell will become part of a feather primordium is an issue of probability, not predetermination, or coding in the promoters of some molecules. Therefore researchers should perhaps pursue the molecular bases of the rules, rather than the codes.
12. Jung H-S., Francis-West P.H., Widelitz R.B., Jiang T-X., Ting-Berreth S., Tickle C., Wolpert L., Chuong C-M. Local inhibitory action of BMPs and their relationships with activators in feather formation: implications for periodic patterning. Dev Biol. 196:1998;11-23. Using growth factor coated beads and skin explant cultures, the authors study and compare the roles of several signaling molecules in feather induction, some turn out to be activators, some are inhibitors, and both activators and inhibitors are expressed in feather primordia. The work also presents evidences that reaction diffusion mechanisms are involved during periodic feather patterning.
13. Ting-Berreth S.A., Chuong C-M. Local delivery of TGF β2 can substitute for placode epithelium to induce mesenchymal condensation during skin appendage morphogenesis. Dev Biol. 179:1996;347-359.
14. Ting-Berreth S.A., Chuong C-M. Sonic Hedgehog in feather morphogenesis: induction of mesenchymal condensation and association with cell death. Dev Dyn. 207:1996;157-170. Using RCAS to mediate the exogenous expression of SHH, the authors show that SHH can increase the size of feather buds. The paper also followed the striped expression pattern of SHH in the marginal plate of feather filaments, which is associated with cell death. This work demonstrates the involvement of SHH in size determination as well as apoptosis. Similar involvements were demonstrated in other organs later.
15. bgo].
16. Crowe R., Henrique D., Ish-Horowicz D., Niswander L. A new role for Notch and Delta in cell fate decisions: patterning the feather array. Development. 125:1998;767-775.
17. Viallet J.P., Prin F., Olivera-Martinez I., Hirsinger E., Pourquie O., Dhouailly D. Chick Delta-1 gene expression and the formation of the feather primordial. Mech Dev. 72:1998;159-168.
18. Song H., Wang Y., Goetinck P.F. Fibroblast growth factor 2 can replace ectodermal signaling for feather development. Proc Natl Acad Sci USA. 93:1996;10 246-10 249. The scaleless phenotype has long been thought to be an epithelial defect because mutant dermis can function normally if it is recombined with normal epithelium. However, the molecular defect is unknown. In this paper, it was shown that FGF-coated beads can rescue the scaleless phenotype, suggesting that FGF is part of the epithelial-derived signaling pathway that becomes defective in these mutants.
19. Widelitz R.B., Jiang T-X., Noveen A., Chen C-W., Chuong C-M. FGF induces new feather buds from developing avian skin. J Invest Dermatol. 107:1996;797-803. Activation of the FGF pathway has been shown to induce ectopic limb buds from the chicken embryonic body wall. Here, FGF1, 2, and 4 were shown to be able to induce new feather buds from apteric skin. This can be demonstrated by FGF-coated beads or by adding FGF in culturing media. The data suggest that FGFs are examples of the activators in feather induction.
20. Noveen A., Jiang T-X., Chuong C-M. Protein kinase A and protein kinase C modulators have reciprocal effects on mesenchymal condensation during skin appendage morphogenesis. Dev Biol. 171:1995;677-693.
21. Patel K., Makarenkova H., Jung H-S. The role of long range, local and direct signalling molecules during chick feather bud development involving the BMP's, follistatin and the Eph receptor tyrosine kinase Eph-A4. Mech Dev. 86:1999;51-62.
22. Novel G. Feather pattern stability and reorganization in cultured skin. J Embryol Exp Morph. 30:1973;605-633.
23. Desbiens X., Queva C., Jaffredo T., Stehelin D., Vandenbunder B. The relationship between cell proliferation and the transcription of the nuclear oncogenes c-myc, c-myb and c-ets-1 during feather morphogenesis in the chick embryo. Development. 111:1991;699-713. An important report that links cell proliferation and oncogene expression with morphogenesis.
24. Chen J.C-W., Jung H-S., Jiang T-X., Chuong C-M. Asymetric expression of Notch, Serrate and Delta is associated with the anterior posterior axis of feather buds. Dev Biol. 188:1997;181-187.
25. Widelitz R.B., Jiang T-X., Chen C-W., Stott N.S., Chuong C-M. Wnt-7a in feather morphogenesis: involvement of anterior-posterior asymmetry and proximal-distal elongation demonstrated with an in vitro reconstitution model. Development. 126:1999;2577-2587. In vitro experiments suggest a link between the A-P axis and P-D elongation of feather development, in a way analogous to the morphogenesis of the Drosophila wing and leg imaginal discs.
26. Chuong C-M., Edelman G.M. Expression of cell-adhesion molecules in embryonic induction. I. And II. Morphogenesis of nestling and adult feathers. J Cell Biol. 101:1985;1009-1043. In this paper, the highly specific spatial-temporal expression patterns of NCAM, LCAM, fibronectin, laminin (etc.) were mapped across different stages of feather development. Some of the most exquisite morphogenetic process in different stages of feather formation are highlighted by their striking expression patterns in different regions of feather buds, follicles and filaments.
27. Chen C.J., Chuong C-M. Dynamic expression of lunatic fringe during feather morphogenesis: a switch from medial-lateral to anterior-posterior asymmetry. Mech Dev. 91:2000;351-354.
28. Feduccia A., Tordoff H.B. Feather of Archaeopteryx: asymmetric vanes indicate aerodynamic function. Science. 203:1979;1021-1022. This is an excellent short paper that demonstrate the correlative relationship of feather flight feathers and the asymmetric vane. It provides a base to correlate function with forms during feather evolution.
29. Jiang T.X., Chuong C.M. Mechanism of skin morphogenesis. I. Analyses with antibodies to adhesion molecules tenascin, N-CAM, and integrin. Dev Biol. 150:1992;82-98.
30. Shames R.B., Jennings A.G., Sawyer R.H. Expression of the cell adhesion molecules, L-CAM and N-CAM during avian scale development. J Exp Zool. 257:1991;195-207.
31. Chiappe L.M. The first 85 million years of avian evolution. Nature. 378:1995;349-354.
32. Sereno P.C. The evolution of Dinosaurs. Science. 284:1999;2137-2147.
33. Prum R.O. Development and evolutionary origin of feathers. J Exp Zool. 285:1999;291-306. A well written review on the structures of feathers and their possible evolutionary and developmental origins.
34. Feduccia A. The Origin and Evolution of Birds. 1996;Yale University Press, New Haven, CT.
35. Chen P-J., Dong Z.M., Zhen S.N. An exceptionally well-preserved theropod dinosaur from the Yixian formation of China. Nature. 391:1998;147-152. A major documentation of the fossils bearing key importance to the evolution of feathers. Sinosauropteryx has a down-like short protofeather body covering.
36. Xu X., Tang Z.J., Wang X.J. A therinzinosauroid dinosaur with integumentary structures from China. Nature. 399:1999;350-354.
37. Ji Q., Currie P.J., Norell M.A., Ji S-A. Two feathered dinosaurs from northeastern China. Nature. 393:1998;753-761. A major documentation of the fossils key to the evolution of feathers. Both Caudipteryx and Protarchaeopteryx have evolved different types of feathers over the body, and have formed long symmetric pennaceous feathers in wings and tails.
38. Hou L., Martin L.D., Zhou Z., Feduccia A. Early adaptive radiation of birds: evidence from fossils from northeastern China. Science. 274:1996;1164-1167. Fossils records of confuciusornis imply that they evolved asymmetric flight feathers, sexually dimorphic tail feathers and lived socially as a group.
39. Jahoda C.A. Induction of follicle formation and hair growth by vibrissa dermal papillae implanted into rat ear wounds: vibrissa-type fibres are specified. Development. 115:1992;1103-1109. What is the potential of adult epidermal cells to form epithelial appendages? Epithelial-mesenchymal recombination experiments are often performed to determine the specificity and competence of inducers and target tissue. Embryonic tissues are often used but in this paper, adult tissues are used. The data showed that adult rat papillae retain the capacity to determine vibrissa specificity in induced follicles.
40. Tanaka S., Sugihara-Yamamoto H., Kato Y. Epigenesis in developing avian scales, III. Stage specific alterationso of the developmental program caused by 5-BrdU. Dev Biol. 121:1987;467-477.
41. Dhouailly D., Hardy M.H., Sengel P. Formation of feathers on chick foot scales: a stage-dependent morphogenetic response to retinoic acid. J Embryol Exp Morphol. 58:1980;63-78. A classic report that demonstrated the phenotypic exchangeability of skin appendages. It set the foundation for the two-stage hypothesis of skin appendage formation: the first stage being deciding whether to make an appendage (induction), and the second stage being deciding which phenotype to make (morphogenesis).
42. Chuong C., Ting S.A., Widelitz R.B., Lee Y. Mechanism of skin morphogenesis: II. Retinoic acid modulates axis orientation and phenotypes of skin appendages. Development. 115:1992;839-852.
43. Chuong C-M., Oliver G., Ting S.A., Jegalian B.G., Chen H.M., DeRobertis E.M. Gradients of homeoproteins in developing feather buds. Development. 110:1990;1021-1030. This was the first demonstration of regional differences of homeobox gene expression in the skin. It set the ground work for the Skin Hox code hypothesis: different combinations of Hox expression patterns are involved in setting different types of feathers and scales over the body of a bird.
44. Kanzler B., Prin F., Thelu J., Dhouailly L. CHOXC-8 and CHOXD-13 expression in embryonic chick skin and cutaneous appendage specification. Dev Dyn. 210:1997;247-287.
45. Zou H., Niswander L. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science. 272:1996;738-741. A surprise finding that the BMP pathway was also involved in the scale/feather fate decision. It opened new understanding to the molecular cascades involved in the phenotypic determination of skin appendages. The BMP pathway reported to function in scutate and scutella, but not reticulate scales.
46. Widelitz R.B., Jiang T-X., Lu J., Chuong C-M. β-catenin in epithelial morphogenesis: conversion of part of avian foot scales into feather buds with a mutated β-catenin. Dev Biol. 219:2000;98-114. In this recent study, the powerful β-catenin converts part of the scutate, scutella and reticulate scales into apparently wild-type feathers. These findings shed more new light on the molecular cascades involved in scale/feather metaplasia, forcing us to consider what took place during development and evolution. The molecular networks have to be defined.
47. ••].
48. Zhou P., Byrne C., Jacobs J., Fuchs E. Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev. 9:1995;700:713.
49. bgobgo].).
50. Crowe R., Niswander L. Disruption of scale development by Delta-1 misexpression. Dev Biol. 195:1998;70-74.
51. Chuong C-M., Noveen A. Phenotypic determination of epithelial appendages: genes, developmental pathways and evolution. J Invest Dermatol. 4:1999;307-311.
52. Chuong C-M., Lin J., Patel N., Jung H-S., Widelitz R.B. Sonic Hedgehog signaling pathway in vertebrate epithelial organ formation: perspectives in development and evolution. Cell Mol Life Sci. 2000;. in press.
53. Wu T., Chuong C-M. Developmental biology of skin appendages. Camacho F., Randall V.A., Price V.H. Hair Biology and Disorders. 2000;Martin Dunitz Publishers. in press. In this review, the developmental processes of different types of epithelial appendages are compared. It is considered that induction, morphogenesis, differentiation and cycling are common processes shared by many different skin appendages.