Immunolocalization of the EDWM-Protein Indicates a Matrix Role in Cornification of Lizard Epidermis

Lorenzo Alibardi

Abstract


During epidermal differentiation in the scales of lizards and snakes, from the basal layer beta- and later alpha-keratinocytes are generated to form beta-and alpha-corneous layers. In the lizard Anolis carolinensis, minor proteins derived from the EDC (Epidermal Differentiation Complex) are added to the main constituent proteins, IFKs (Intermediate Filament Keratins) and CBPs (Corneous Beta Proteins, formerly indicated as beta keratins). One of these proteins that previous studies showed to be exclusively expressed in the skin, EDWM (EDC protein containing high GSRC amino acids) is rich in cysteine and arginine, amino acids that form numerous –S–S– and electro-static chemical bonds in the corneous material. Light and electron microscopy immunolbeling for EDWM show a diffuse localization in differentiating beta-cells and in some alpha-cells, in particular those of the clear-layer, involved in epidermal shedding. The study suggests that EDWM may function as a matrix protein that binds to IFKs and CBPs, contributing to the formation of the specific corneous material present in beta- and alpha-corneous layers. In particular, its higher immunolocalization in the maturing clear layer indicates that this protein is important for its differentiation and epidermal shedding in A. carolinensis and likely also in other lepidosaurian reptiles.

Keywords


lizard; epidermal differentiation; Epidermal Differentiation Complex; EDWM-protein; shedding complex; immunocytochemistry

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References


Alibardi L. (1995), «Electron microscopic analysis of the regenerating scales in lizard», Boll. Zool., 62, 109 – 120.

Alibardi L. (2013a), «Cornification in reptilian epidermis occurs through the deposition of keratin associated beta proteins (beta-keratins) onto a scaffold of intermediate filament keratins», J. Morphol., 274, 175 – 193.

Alibardi L. (2013b), «Comparative immunolocalization of Keratin-associated beta-proteins (Beta-keratins) supports a new explanation for the cyclical process of keratinocyte differentiation in lizard epidermis», Acta Zool., 95, 32 – 43.

Alibardi L. (2014), «Immunolocalization of alpha-keratins and associated beta-proteins in lizard epidermis shows that acidic keratins mix with basic keratin-associated beta-proteins», Protoplasma, 251, 827 – 837.

Alibardi L. (2016), «Review: mapping epidermal beta-proteins distribution in the lizard Anolis carolinensis shows a specific localization for the formation of scales, pads and claws», Protoplasma, 253, 1405 – 1420.

Alibardi L. and Eckhart L. (2021), «Immunolocalization of Epidermal Differentiation Complex proteins reveals distinct molecular compositions of cells that control structure and mechanical properties of avian skin appendages», J. Morphol. [in press].

Alibardi L., Segalla A, and Dalla Valle L. (2012), «Distribution of specific keratin associated beta-proteins (beta-keratins) in the epidermis of the lizard Anolis carolinensis clarifies the process of cornification in lepidosaurians», J. Exp. Zool., 318B, 388 – 403.

Alibardi L., Strasser B., and Eckhart L. (2015), «Immunolocalization of loricrin in the maturing α-layer of normal and regenerating epidermis of the lizard Anolis carolinensis», J. Exp. Zool., 234B, 159 – 167.

Dalla Valle L., Nardi A., Bonazza G., Zuccal C., Emera D., and Alibardi L. (2010), «Forty keratin-associated β-proteins (β-keratins) form the hard layers of scales, claws and adhesive pads in the green anole lizard, Anolis carolinensis», J. Exp. Zool., 314B, 11 – 32.

Fraser R. D. B., MacRae T. P., and Rogers G. E. (1972), Keratins: Their Composition, Structure and Biosynthesis, Charles C. Thomas, Springfield, IL.

Fraser R. D. B. and Parry D. A. (1996), «The molecular structure of reptilian keratin», Int. J. Biol. Macromol., 19, 207 – 211.

Holthaus K. B., Strasser B., Sipos W., Schmidt H. A., Mlitz V., Sukseree S., Weissenbacher A., Tschchler E., Alibardi L., and Eckhart L. (2015) «Comparative genomics identifies epidermal proteins associated with the evolution of the turtle shell», Mol. Biol. Evol., 33, 726 – 737.

Holthaus K. B., Mlitz V., Strasser B., Tschachler E., Alibardi L., and Eckhart L. (2017), «Comparative genomics of the epidermal differentiation complex suggests evolutionary adaptions of snake skin», Sci. Rep., 7, 45338.

Holthaus K. B., Strasser B., Lachner J., Sukseree S., Sipos W., Weissenbacher A., Tschachler E., Alibardi L., and Eckhart L. (2018), «Comparative analysis of epidermal differentiation genes in crocodilians suggests new models for evolutionary origin of avian feather proteins», Genome Biol. Evol., 10, 694 – 704.

Holthaus K. B., Eckhart L., Dalla Valle L., and Alibardi L. (2019), «Review: Evolution and diversification of corneous beta-proteins, the characteristic epidermal proteins of reptiles and birds», J. Exp. Zool., 330B, 438 – 453.

Irish F. J., Williams E. E., and Seling E. (1988), «Scanning electron microscopy of changes in epidermal structure occurring during the shedding cycle in squamate reptiles», J. Morphol., 197, 105 – 126.

Landmann L. (1986), «The skin of Reptiles: epidermis and dermis», in: Bereither-Hahn J., Matoltsy G. and Sylvia-Richards K. (eds.), Biology of the Integument, Vertebrates, Springer Verlag, Berlin – Heidelberg – New York, pp. 150 – 187.

Maderson P. F. A. (1985), «Some developmental problems of the reptilian integument», in: Gans C., Billett F., and Maderson P. F. A. (eds.), Biology of the Reptilia. Vol. 14, John Wiley & Sons, New York, pp. 525 – 598.

Maderson P. F. A., Flaxman B. A., Roth S. I., and Szabo G. (1972), «Ultrastructural contributions to the identification of cell types in the lizard epidermal generation», J. Morphol., 136, 191 – 209.

Maderson P. F. A., Rabinowitz T., Tandler B., and Alibardi L. (1998), «Ultrastructural contributions to an understanding of the cellular mechanisms involved in lizard skin shedding with comments on the function and evolution of a unique lepidosaurian phenomenon», J. Morphol., 236, 1 – 24.

Sawyer R. H., Glenn T. C., French J. O., Mays B., Shames R. B., Barnes G. L., Rhodes W., and Ishikawa Y. (2000), «The expression of beta (β) keratins in the epidermal appendages of reptiles and birds», Am. Zool., 40, 530 – 539.

Scala C., Cenacchi G., Ferrari C., Pasquinelli G., Preda P., and Manara G. C. (1992) «A new acrylic resin formulation: a useful tool for histological, ultrastructural, and immunocytochemical investigations», J. Histochem. Cytochem., 40, 1799 – 1804.

Strasser B., Mlitz V., Hermann M., Rice R. H., Eigenheer R. A., Alibardi L., Tschachler E., and Eckhart L. (2014) «Evolutionary origin and diversification of epidermal barrier proteins in amniotes», Mol. Biol. Evol., 31, 3194 – 3205.

Vanhoutteghem A., Djian P., and Green G. (2008) «Ancient origin of the gene encoding involucrin, a precursor of the cross-linked envelope of epidermis and related epithelia», PNAS, 105, 15481 – 15486.




DOI: https://doi.org/10.30906/1026-2296-2021-28-5-267-274

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