The Trichohyalin-Like Protein Scaffoldin Is Expressed in the Multilayered Periderm During Development of Avian Beak and Egg Tooth

Overview

Journal Genes (Basel)

Publisher MDPI

Date 2021 Feb 13

PMID 33578693

Citations 5

Authors

Veronika Mlitz

Marcela Hermann

Maria Buchberger

Erwin Tschachler

Leopold Eckhart

Affiliations

Soon will be listed here.

Abstract

Scaffoldin, an S100 fused-type protein (SFTP) with high amino acid sequence similarity to the mammalian hair follicle protein trichohyalin, has been identified in reptiles and birds, but its functions are not yet fully understood. Here, we investigated the expression pattern of scaffoldin and cornulin, a related SFTP, in the developing beaks of birds. We determined the mRNA levels of both SFTPs by reverse transcription polymerase chain reaction (RT-PCR) in the beak and other ectodermal tissues of chicken () and quail () embryos. Immunohistochemical staining was performed to localize scaffoldin in tissues. Scaffoldin and cornulin were expressed in the beak and, at lower levels, in other embryonic tissues of both chickens and quails. Immunohistochemistry revealed scaffoldin in the peridermal compartment of the egg tooth, a transitory cornified protuberance (caruncle) on the upper beak which breaks the eggshell during hatching. Furthermore, scaffoldin marked a multilayered peridermal structure on the lower beak. The results of this study suggest that scaffoldin plays an evolutionarily conserved role in the development of the avian beak with a particular function in the morphogenesis of the egg tooth.

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References

Lynch V, Wagner G . Did egg-laying boas break Dollo's law? Phylogenetic evidence for reversal to oviparity in sand boas (Eryx: Boidae). Evolution. 2009; 64(1):207-16. DOI: 10.1111/j.1558-5646.2009.00790.x. View

Contzler R, Favre B, Huber M, Hohl D . Cornulin, a new member of the "fused gene" family, is expressed during epidermal differentiation. J Invest Dermatol. 2005; 124(5):990-7. DOI: 10.1111/j.0022-202X.2005.23694.x. View

U Basmanav F, Cau L, Tafazzoli A, Mechin M, Wolf S, Romano M . Mutations in Three Genes Encoding Proteins Involved in Hair Shaft Formation Cause Uncombable Hair Syndrome. Am J Hum Genet. 2016; 99(6):1292-1304. PMC: 5142115. DOI: 10.1016/j.ajhg.2016.10.004. View

Wang S, Stiegler J, Wu P, Chuong C, Hu D, Balanoff A . Heterochronic truncation of odontogenesis in theropod dinosaurs provides insight into the macroevolution of avian beaks. Proc Natl Acad Sci U S A. 2017; 114(41):10930-10935. PMC: 5642708. DOI: 10.1073/pnas.1708023114. View

Steinert P . A model for the hierarchical structure of the human epidermal cornified cell envelope. Cell Death Differ. 1995; 2(1):33-40. View

Greenwold M, Sawyer R . Genomic organization and molecular phylogenies of the beta (beta) keratin multigene family in the chicken (Gallus gallus) and zebra finch (Taeniopygia guttata): implications for feather evolution. BMC Evol Biol. 2010; 10:148. PMC: 2894828. DOI: 10.1186/1471-2148-10-148. View

Takase T, Hirai Y . Identification of the C-terminal tail domain of AHF/trichohyalin as the critical site for modulation of the keratin filamentous meshwork in the keratinocyte. J Dermatol Sci. 2012; 65(2):141-8. DOI: 10.1016/j.jdermsci.2011.12.014. View

Feng S, Stiller J, Deng Y, Armstrong J, Fang Q, Reeve A . Dense sampling of bird diversity increases power of comparative genomics. Nature. 2020; 587(7833):252-257. PMC: 7759463. DOI: 10.1038/s41586-020-2873-9. View

Mlitz V, Latreille J, Gardinier S, Jdid R, Drouault Y, Hufnagl P . Impact of filaggrin mutations on Raman spectra and biophysical properties of the stratum corneum in mild to moderate atopic dermatitis. J Eur Acad Dermatol Venereol. 2011; 26(8):983-90. DOI: 10.1111/j.1468-3083.2011.04198.x. View

10.

Wu P, Hou L, Plikus M, Hughes M, Scehnet J, Suksaweang S . Evo-Devo of amniote integuments and appendages. Int J Dev Biol. 2004; 48(2-3):249-70. PMC: 4386668. DOI: 10.1387/ijdb.041825pw. View

11.

Wu P, Ng C, Yan J, Lai Y, Chen C, Lai Y . Topographical mapping of α- and β-keratins on developing chicken skin integuments: Functional interaction and evolutionary perspectives. Proc Natl Acad Sci U S A. 2015; 112(49):E6770-9. PMC: 4679038. DOI: 10.1073/pnas.1520566112. View

12.

Holthaus K, Mlitz V, Strasser B, Tschachler E, Alibardi L, Eckhart L . Identification and comparative analysis of the epidermal differentiation complex in snakes. Sci Rep. 2017; 7:45338. PMC: 5366951. DOI: 10.1038/srep45338. View

13.

Strasser B, Mlitz V, Hermann M, Rice R, Eigenheer R, Alibardi L . Evolutionary origin and diversification of epidermal barrier proteins in amniotes. Mol Biol Evol. 2014; 31(12):3194-205. PMC: 4245816. DOI: 10.1093/molbev/msu251. View

14.

Nikolay B, Plieschnig J, Subik D, Schneider J, Schneider W, Hermann M . A novel estrogen-regulated avian apolipoprotein. Biochimie. 2013; 95(12):2445-53. PMC: 3898076. DOI: 10.1016/j.biochi.2013.09.005. View

15.

Fons J, Gaete M, Zahradnicek O, Landova M, Bandali H, Khannoon E . Getting out of an egg: Merging of tooth germs to create an egg tooth in the snake. Dev Dyn. 2019; 249(2):199-208. DOI: 10.1002/dvdy.120. View

16.

Fischer H, Eckhart L, Mildner M, Jaeger K, Buchberger M, Ghannadan M . DNase1L2 degrades nuclear DNA during corneocyte formation. J Invest Dermatol. 2006; 127(1):24-30. DOI: 10.1038/sj.jid.5700503. View

17.

KINGSBURY J, Allen V, ROTHERAM B . The histological structure of the beak in the chick. Anat Rec. 1953; 116(1):95-115. DOI: 10.1002/ar.1091160109. View

18.

Mlitz V, Strasser B, Jaeger K, Hermann M, Ghannadan M, Buchberger M . Trichohyalin-like proteins have evolutionarily conserved roles in the morphogenesis of skin appendages. J Invest Dermatol. 2014; 134(11):2685-2692. PMC: 4260798. DOI: 10.1038/jid.2014.204. View

19.

Holthaus K, Alibardi L, Tschachler E, Eckhart L . Identification of epidermal differentiation genes of the tuatara provides insights into the early evolution of lepidosaurian skin. Sci Rep. 2020; 10(1):12844. PMC: 7393497. DOI: 10.1038/s41598-020-69885-0. View

20.

Nimmagadda S, Buchtova M, Fu K, Geetha-Loganathan P, Hosseini-Farahabadi S, Trachtenberg A . Identification and functional analysis of novel facial patterning genes in the duplicated beak chicken embryo. Dev Biol. 2015; 407(2):275-88. DOI: 10.1016/j.ydbio.2015.09.007. View