Dinosaur's feather and chicken's tooth? Tissue engineering of the integument - PubMed (original) (raw)

Review

. 2001 Jul-Aug;11(4):286-92.

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Review

Dinosaur's feather and chicken's tooth? Tissue engineering of the integument

C M Chuong et al. Eur J Dermatol. 2001 Jul-Aug.

Abstract

The integument forms the interface between animals and the environment. During evolution, diverse integument and integument appendages have evolved to adapt animals to different niches. The formation of these different integument forms is based on the acquisition of novel developmental mechanisms. This is the way Nature does her tissue/organ engineering and experiments. To do tissue engineering of the integument in the new century for medical applications, we need to learn more principles from developmental and evolutionary studies. A novel diagram showing the evolution and development of integument complexity is presented, and the molecular pathways involved discussed. We then discuss two examples in which the gain and loss of appendages are modulated: transformation of avian scale epidermis into feathers with mutated beta catenin, and induction of chicken tooth like appendages with FGF, BMP and feather mesenchyme.

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Figures

Figure 1

Figure 1

(A) A prototype animal with various epithelial appendages. From Chuong, 1998 [5]. (B) Restoration of a Sinosauropteryx (Sinosauropteryx prima). Notice this theropod dinosaurs has elongated skin appendages which are hair like or some call proto-feathers. They are of the same type over the body and are more likely to be involved in keeping temperature rather than flight. The animal also has long legs, long tails, and sharp teeth. Adopted from National Geographic [48] based on Chen et al. [26]. (C) Restoration of a mesozoic bird Largirostronis sexdentoris. Notice this mesozoic bird has evolved different types of feathers over the body and should be a good flyer. It has a beak which still has teeth. Adopted from Hou et al. [49]. (D) Restoration of a Confuciusornis sanctus [30, 31]. Note the claws on the wing still remain but a beak without teeth has evolved. Adopted from Hou et al. [49]. (E) Conceptual model of integument appendage forms. Arrows imply the progression from simple to more complex integument appendage forms, with some possible underlying morphogenetic processes. Under each form, examples from current and ancient integument appendages are listed. Arrows do not indicate specific evolutionary steps, nor that one appendage is directly evolved from another. Sometimes evolution can occur in the opposite direction of the arrows when it is advantageous. For example, the loss of chicken teeth and wing claws. Glands, teeth and other epithelial organs can be complex too but are not elaborated because we focus on feathers here.

Figure 1

Figure 1

(A) A prototype animal with various epithelial appendages. From Chuong, 1998 [5]. (B) Restoration of a Sinosauropteryx (Sinosauropteryx prima). Notice this theropod dinosaurs has elongated skin appendages which are hair like or some call proto-feathers. They are of the same type over the body and are more likely to be involved in keeping temperature rather than flight. The animal also has long legs, long tails, and sharp teeth. Adopted from National Geographic [48] based on Chen et al. [26]. (C) Restoration of a mesozoic bird Largirostronis sexdentoris. Notice this mesozoic bird has evolved different types of feathers over the body and should be a good flyer. It has a beak which still has teeth. Adopted from Hou et al. [49]. (D) Restoration of a Confuciusornis sanctus [30, 31]. Note the claws on the wing still remain but a beak without teeth has evolved. Adopted from Hou et al. [49]. (E) Conceptual model of integument appendage forms. Arrows imply the progression from simple to more complex integument appendage forms, with some possible underlying morphogenetic processes. Under each form, examples from current and ancient integument appendages are listed. Arrows do not indicate specific evolutionary steps, nor that one appendage is directly evolved from another. Sometimes evolution can occur in the opposite direction of the arrows when it is advantageous. For example, the loss of chicken teeth and wing claws. Glands, teeth and other epithelial organs can be complex too but are not elaborated because we focus on feathers here.

Figure 1

Figure 1

(A) A prototype animal with various epithelial appendages. From Chuong, 1998 [5]. (B) Restoration of a Sinosauropteryx (Sinosauropteryx prima). Notice this theropod dinosaurs has elongated skin appendages which are hair like or some call proto-feathers. They are of the same type over the body and are more likely to be involved in keeping temperature rather than flight. The animal also has long legs, long tails, and sharp teeth. Adopted from National Geographic [48] based on Chen et al. [26]. (C) Restoration of a mesozoic bird Largirostronis sexdentoris. Notice this mesozoic bird has evolved different types of feathers over the body and should be a good flyer. It has a beak which still has teeth. Adopted from Hou et al. [49]. (D) Restoration of a Confuciusornis sanctus [30, 31]. Note the claws on the wing still remain but a beak without teeth has evolved. Adopted from Hou et al. [49]. (E) Conceptual model of integument appendage forms. Arrows imply the progression from simple to more complex integument appendage forms, with some possible underlying morphogenetic processes. Under each form, examples from current and ancient integument appendages are listed. Arrows do not indicate specific evolutionary steps, nor that one appendage is directly evolved from another. Sometimes evolution can occur in the opposite direction of the arrows when it is advantageous. For example, the loss of chicken teeth and wing claws. Glands, teeth and other epithelial organs can be complex too but are not elaborated because we focus on feathers here.

Figure 2

Figure 2

Transformation of avian scale epidermis into feathers with beta catenin. (A) Schematic drawing showing that beta catenin can cause epidermis to become more “activated” and the pathway may work in concert with other molecular pathways. (B) Whole mount view and tissue sections showing the feather follicles and filaments induced by RCAS beta catenin retroviral transduction. Adopted from Widelitz et al., 2000 [37].

Figure 3

Figure 3

Induction of tooth-like appendages from chicken oral mucosa by feather mesenchyme. (A) A schematic drawing of normal tooth development. Normal chickens can form dental laminae (marked by 1), which can be promoted by FGF and BMP to the cap stage (marked 2), and by feather mesenchyme to form follicles (marked 3). (B) Recombination of a single piece of chicken oral mucosa (red) and aboral epithelium (green) is recombined with dermal mesenchyme from the trunk (blue). The results show oral mucosa, which otherwise will be smooth, form many tooth-like appendages. Sections show the epithelium invaginate to form cap like structures, and eventually form a nice epithelial appendage follicle. Adopted from Chen et al., 2000 [40].

Figure 4

Figure 4

Strategy of skin engineering using different stages of epithelial and mesenchymal precursor cells. Through recombination assay and gene alteration, we should be able to characterize the properties of different stages of epithelial and dermal stem cells, and learn to regenerate different integument structures (hair, teeth, glands, etc.) with different combinations. E: epithelial cells, also in blue color; M: mesenchymal cells, or dermal cells, also in orange color. Arrows represent progression and reversibility.

References

    1. Chuong CM. The making of a feather: homeoproteins, retinoids and adhesion molecules. Bioessays. 1993;15:513–21. - PubMed
    1. Chuong CM, Chodankar R, Widelitz RB, Jiang TX. Evo-devo of feathers and scales: building complex epithelial appendages. Current Opinion in Development and Genetics. 2000;10:449–56. - PMC - PubMed
    1. Oro AE, Scott MP. Splitting hairs: dissecting roles of signaling systems in epidermal development. Cell. 1998;95:575–8. - PubMed
    1. Paus R, Cotsarerllis G. The biology of hair follicles. N Engl J Med. 1999;341:491–7. - PubMed
    1. Chuong CM. Morphogenesis of epithelial appendage: variations of a common theme and implications in regeneration. In: Chuong CM, editor. Molecular Basis of epithelial appendage morphogenesis. Landes Bioscience; Austin: 1998. pp. 3–14.

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