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Review: mapping epidermal beta-protein distribution in the lizard Anolis carolinensis shows a specific localization for the formation of scales, pads, and claws

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Abstract

The epidermis of lizards is made of multiple alpha- and beta-layers with different characteristics comprising alpha-keratins and corneous beta-proteins (formerly beta-keratins). Three main modifications of body scales are present in the lizard Anolis carolinensis: gular scales, adhesive pad lamellae, and claws. The 40 corneous beta-proteins present in this specie comprise glycine-rich and glycine-cysteine-rich subfamilies, while the 41 alpha-keratins comprise cysteine-poor and cysteine-rich subfamilies, the latter showing homology to hair keratins. Other genes for corneous proteins are present in the epidermal differentiation complex, the locus where corneous protein genes are located. The review summarizes the main sites of immunolocalization of beta-proteins in different scales and their derivatives producing a unique map of body distribution for these structural proteins. Small glycine-rich beta-proteins participate in the formation of the mechanically resistant beta-layer of most scales. Small glycine-cysteine beta-proteins have a more varied localization in different scales and are also present in the pliable alpha-layer. In claws, cysteine-rich alpha-keratins prevail over cysteine-poor alpha-keratins and mix to glycine-cysteine-rich beta-proteins. The larger beta-proteins with a molecular mass similar to that of alpha-keratins participate in the formation of the fibrous meshwork present in differentiating beta-cells and likely interact with alpha-keratins. The diverse localization of alpha-keratins, beta-proteins, and other proteins of the epidermal differentiation complex gives rise to variably pliable, elastic, or hard corneous layers in different body scales. The corneous layers formed in the softer or harder scales, in the elastic pad lamellae, or in the resistant claws possess peculiar properties depending on the ratio of specific corneous proteins.

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References

  • Alexander NJ (1970) Comparison of alpha and beta keratin in reptiles. Z Zellfortsch 110:153–175

    CAS  Google Scholar 

  • Alexander NJ, Parakkal PF (1969) Formation of alpha and beta type keratin in lizard epidermis during the molting cycle. Z Zellforsch 110:72–87

    Article  Google Scholar 

  • Alfoldi J et al (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature. doi:10.1038/nature10390

    Google Scholar 

  • Alibardi L (2001) Keratohyalin-like granules in lizard epidermis: evidence from cytochemical, autoradiographic and microanalytic studies. J Morphol 248:64–79

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (2006) Structural and immunocytochemical characterization of keratinization in vertebrate epidermis and epidermal derivatives. Int Rev Cytol 253:177–259

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (2008a) Microscopic analysis of lizard claw morphogenesis and hypothesis on its evolution. Acta Zool 89:169–178

  • Alibardi L (2008b) Corneification in developing claws of the common Australian skin (Lampropholis guichenoti) (Squamata, Lacertidae). Ital J Zool 75:327–336

  • Alibardi L (2008c) Claw development and cornification in the Passeraceous Bird zebrafinch (Taeniatopygia guttata castanotis). Anat Sci Int. 2009(84):189–199

  • Alibardi L (2009) Cell biology of adhesive setae in gecko lizards. Zoology 112:403–424

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (2012) Immunolocalization of keratin associated beta-proteins (beta-keratins) in the regenerating lizard epidermis indicates a new process for the differentiation of the epidermis in lepidosaurians. J Morphol 273:1272–1279

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (2013a) Immunolocalization of alpha-keratins and feather beta-proteins in feather cells and comparison with the general process of cornification in the skin of mammals. Ann Anat 195:189–198

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (2013b) 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

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (2013c) Immunoreactivity of the pre-core box antibody shows that most glycine-rich beta proteins accumulate in lepidosaurian beta-layer and in the corneous layer of crocodilian and turtle epidermis. Micron 57:31–40

    Article  PubMed  Google Scholar 

  • Alibardi L (2013d) 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

    Article  PubMed  Google Scholar 

  • Alibardi L (2013e) Ultrastructural immunocytochemistry for the central region of keratin associated-beta-proteins (beta-keratins) shows the epitope is constantly expressed in reptilian epidermis. Tissue Cell 45:241–252

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (2013f) Immunolocalization of keratin-associated beta-proteins in developing epidermis of lizard suggests that adhesive setae contain glycine-cysteine-rich proteins. J Morphol 274:97–107

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (2014a) 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

    Article  Google Scholar 

  • Alibardi L (2014b) Immunocytochemical localization of cysteine-rich beta-proteins in the extensible epidermis of the dewlap in the lizard Anolis carolinensis. Acta Zool 95:465–471

    Article  Google Scholar 

  • Alibardi L (2014c) Immunolocalization of specific beta-proteins in pad lamellae of the digits in the lizard Anolis carolinensis suggests that cysteine-rich beta-proteins provide flexibility. J Morphol 275:504–513

    CAS  PubMed  Google Scholar 

  • Alibardi L (2014d) The corneous layer of the claw in the lizard Anolis carolinensis mainly contains the glycine–cysteine-rich beta-protein HgGC3 in addition to hard keratins. Tissue Cell 46:326–333

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L (2015) Immunolocalization of large corneous beta-proteins in the green anole lizard (Anolis carolinensis) suggests that they form filaments that associate to the smaller beta-proteins in the beta-layer of the epidermis. J Morphol 276:1244–1257

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L, Toni M (2005) Wound keratins in the regenerating epidermis of lizard suggest that the wound reaction is similar in the tail and limb. J Exp Zool 303A:845–860

  • Alibardi L, Toni M (2006) Cytochemical, biochemical and molecular aspects of the process of keratinization in the epidermis of reptilian scales. Prog Histochem Cytochem 40:73–134

    Article  CAS  PubMed  Google Scholar 

  • Alibardi L, Toni M (2007) Beta keratins of reptilian epidermis share a conserved common epitope termed the core-box. Res J Biol Sci 2:329–339

    Google Scholar 

  • Alibardi L, Maurizii MG, Taddei C (2000) Immunocytochemical and electrophoretic distribution of cytokeratins in the regenerating epidermis of the lizard Podarcis muralis. J Morphol 246:179–181

  • Alibardi L, Dalla Valle L, Nardi A, Toni M (2009) Evolution of hard proteins in the sauropsid integument in relation to the cornification of skin derivatives in amniotes. J Anat 214:560–586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alibardi L, Jaeger K, Dalla Valle L, Echkart L (2011) Ultrastructural localization of hair keratin homologs in the claw of the lizard Anolis carolinensis. J Morphol 272:363–370

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Baden HP, Maderson PF (1970) Morphological and biophysical identification of fibrous proteins in the amniote epidermis. J Exp Zool 174:225–232

    Article  CAS  PubMed  Google Scholar 

  • Bragulla HH, Homberger DG (2009) Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. J Anat 214:516–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brush HA (1983) Self-assembly of avian φ-keratins. J Protein Chem 2:63–75

    Article  CAS  Google Scholar 

  • Carver WE, Sawyer RH (1987) Development and keratinisation of the epidermis of the common lizard, Anolis carolinensis. J Exp Zool 243:435–443

    Article  CAS  PubMed  Google Scholar 

  • Chang C, Wu P, Baker RE, Maini PK, Alibardi L, Chuong CM (2009) Reptile scale paradigm. Evo-devo, pattern formation and regeneration. Int J Dev Biol 53:813–826

    Article  PubMed  PubMed Central  Google Scholar 

  • Coulombe PA, Omary MB (2002) ‘Hard’ and ‘soft’ principles defining the structure, function and regulation of keratin intermediate filaments. Curr Opin Cell Biol 14:110–122

    Article  CAS  PubMed  Google Scholar 

  • Dalla Valle L, Toffolo V, Belvedere P, Alibardi L (2005) Isolation of a mRNA encoding a glycine-proline-rich beta-keratin expressed in the regenerating epidermis of lizard. Dev Dyn 234:934–947

    Article  CAS  PubMed  Google Scholar 

  • Dalla Valle L, Nardi A, Toffolo V, Niero C, Toni M, Alibardi L (2007a) Cloning and characterization of scale beta-keratins in the differentiating epidermis of geckos show they are glycine-proline-serine-rich proteins with a central motif homologous to avian beta-keratins. Dev Dyn 236:374–388

    Article  CAS  PubMed  Google Scholar 

  • Dalla Valle L, Nardi A, Belvedere P, Toni M, Alibardi L (2007b) Beta-keratins of differentiating epidermis of snake comprise glycine-proline-serine-rich proteins with an avian-like gene organization. Dev Dyn 236:1939–1953

    Article  CAS  PubMed  Google Scholar 

  • Dalla Valle L, Nardi A, Gelmi C, Toni M, Emera D, Alibardi L (2008) Beta-keratins of the crocodilian epidermis: composition, structure, and phylogenetic relationships. J Exp Zool 312B:42–57

    Article  Google Scholar 

  • Dalla Valle L, Nardi A, Alibardi L (2009a) Isolation of a new class of cysteine-glycine-proline rich beta-proteins (beta-keratins) and their expression in snake epidermis. J Anat 216:356–367

    Article  Google Scholar 

  • Dalla Valle L, Nardi A, Toni M, Emera D, Alibardi L (2009b) Beta-keratins of turtle shell are glycine-proline-tyrosine-rich proteins similar to those of crocodilians and birds. J Anat 214:284–300

    Article  CAS  PubMed  Google Scholar 

  • Dalla Valle L, Nardi A, Bonazza G, Zuccal C, Emera D, 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

    Article  CAS  Google Scholar 

  • Dalla Valle L, Benato F, Rossi C, Alibardi L, Tschachler E, Eckhardt L (2011) Deleterious mutations of a claw keratin in multiple taxa of reptiles. J Mol Evol 72:265–273

    Article  CAS  PubMed  Google Scholar 

  • Eckhart L, Dalla Valle L, Jaeger K, Ballaun C, Szabo S, Nardi A, Buchberger M, Hermann M, Alibardi L, Tschachler E (2008) Identification of reptilian genes encoding hair keratin-like proteins suggests a new scenario for the evolutionary origin of hair. PNAS 105:18419–18423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eckhart L, Lippens S, Tschachler E, Declercq W (2013) Cell death by cornification. Biochim Biophys Acta 1833:3471–3480

    Article  CAS  PubMed  Google Scholar 

  • Ernst V, Ruibal R (1966) The structure and development of the digital lamellae of lizards. J Morphol 120:233–266

    Article  CAS  PubMed  Google Scholar 

  • Fraser RD, Parry DA (2008) Molecular packing in the feather keratin filament. J Struct Biol 162:1–13

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, Parry DAD (2011) The structural basis of the filament-matrix texture in the avian/reptilian group of hard beta-keratins. J Struct Biol 173:391–405

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, Parry DA (2014) Amino acid sequence homologies in the hard keratins of birds and reptiles, and their implications for molecular structure and physical properties. J Struct Biol 188:213–224

    Article  CAS  PubMed  Google Scholar 

  • Fraser RDB, MacRae TP, Rogers GE (1972) Keratins: their composition, structure and biosynthesis. Charles C. Thomas, Springfield

  • Frazer RDB, Parry DAD (1996) The molecular structure of reptilian keratin. Int J Biol Macromol 19:207–211

    Article  Google Scholar 

  • Fuchs E, Tyner AL, Giudice GJ, Marchuk D, RayChaudhury A, Rosember M (1987) The human keratin genes and their differential expression. Curr Top Dev Biol 22:5–34

  • Gillespie JM (1991) The structural proteins of hair: isolation, characterization and regulation of biosynthesis. In: Goldsmith LA (ed) Physiology, biochemistry and molecular biology of the skin. Oxford University Press, Oxford, pp 625–659

  • Gregg K, Rogers G (1986) Feather keratins: composition, structure and biogenesis. In: Bereither-Hahn J, Matoltsy G, Sylvia-Richards K (eds) Biology of the integument, vertebrates. Springer, New York, pp 666–694

    Chapter  Google Scholar 

  • Gregg K, Wilton S, Parry DA, Rogers G (1984) A comparison of genomic coding sequences for feather and scale keratins: structural and evolutionary implications. EMBO J 3:175–178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hallahan DL, Keiper-Hrynko NM, Shang TQ, Ganzke TS, Toni M, Dalla Valle L, Alibardi L (2008) Analysis of gene expression in gecko digital adhesive pads indicates significant production of cysteine- and glycine-rich beta-keratins. J Exp Zool 312B:58–73

    Article  Google Scholar 

  • Irish J, Williams EE, Feeling F (1988) Scanning electron microscopy of changes in epidermal structure occurring during the shedding cycle in squamate reptiles. J Morphol 197:105–126

    Article  Google Scholar 

  • Kalinin AE, Kajava AV, Steinert PM (2002) Epithelia barrier function: assembly and structural features of the cornified cell envelope. BioEssays 24:789–800.

  • Kreplak L, Doucet J, Dumas P, Briki F (2004) New aspects of the α-helix to β-sheet transition in stretched hard α-keratin fibers. Biophys J 87:640–647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landmann L (1986) The skin of reptiles: epidermis and dermis. In: Bereiter-Hahn J, Matoltsy AG, Sylvia-Richards K (eds) Biology of the integument, vertebrates 2. Springer, Berlin, pp 150–187

    Chapter  Google Scholar 

  • Lillywhite HB (2006) Review: water relations of tetrapod integument. J Exp Biol 209:202–226

    Article  PubMed  Google Scholar 

  • Maderson PFA (1970) Lizard glands and lizard hands: models for evolutionary study. Forma Functio 3:179–204

    Google Scholar 

  • Maderson PF (1985) Some developmental problems of the reptilian integument. In: Gans C, Billett F, Maderson PFA (eds) Biology of the reptilia, vol 14. Wiley, New York, pp 525–598

    Google Scholar 

  • Maderson PFA, Flaxman BA, Roth SI, Szabo G (1972) Ultrastructural contribution to the identification of cell types in the lizard epidermal generation. J Morphol 136:191–210

    Article  CAS  PubMed  Google Scholar 

  • Maderson PFA, Baranowitz S, Roth SI (1978) A histological study of the long-term response to trauma of squamate integument. J Morphol 157:121–136

    Article  Google Scholar 

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

    Article  Google Scholar 

  • McGowan KM, Coulombe PA (1998) The wound repair associated keratins 6, 16, and 17. Insights into the role of intermediate filaments in specifying keratinocyte cytoarchitecture. In: Herman H, Harris R (eds) Subcellular biochemistry, vol. 31: intermediate filaments. Plenum, New York, pp 173–204

    Google Scholar 

  • Menon GK, Maderson PFA, Drewes RC, Baptista LF, Price LF, Elias PM (1996) Ultrastructural organization of avian stratum corneum lipids as the basis for facultative cutaneous waterproofing. J Morphol 227:1–13

    Article  CAS  PubMed  Google Scholar 

  • Mischke D, Korge BP, Marenholz I, Volz A, Ziegler A (1996) Genes encoding structural proteins of epidermal cornification and S100 calcium-binding proteins form a gene complex (“epidermal differentiation complex”) on human chromosome 1q21. J Investig Dermatol 106:989–992

    Article  CAS  PubMed  Google Scholar 

  • 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 Investig Dermatol 134:2682–2692

    Article  Google Scholar 

  • O’Donnell IJ (1973) The complete amino acid sequence of a feather keratin from emu (Dromaius novae-hollandiae). Aust J Biol Sci 26:415–435

    Article  PubMed  Google Scholar 

  • Rogers GE (2004) Hair follicle differentiation and regulation. Int J Dev Biol 48:163–170

  • Rogers MA, Langbein L, Praetzel-Wunder S, Winter H, Schweizer J (2006) Human hair keratin-associated proteins (KAPs). Int Rev Cytol 251:209–263

    Article  CAS  PubMed  Google Scholar 

  • Rouse JG, Van Dyke ME (2010) A review of keratin based biomaterials for biomedical applications. Materials 3:999–1014

    Article  Google Scholar 

  • Rudall KM (1947) X-ray studies of the distribution of protein chain types in the vertebrate epidermis. Biochim Biophys Acta 1:549–562

    Article  CAS  Google Scholar 

  • Ruibal R, Ernst V (1965) The structure of the digital setae of lizards. J Morphol 117:271–293

    Article  CAS  PubMed  Google Scholar 

  • Sawyer RH, Knapp LW (2003) Avian skin development and the evolutionary origin of feathers. J Exp Zool B Mol Dev Evol 298:57–72

    Article  PubMed  Google Scholar 

  • Sawyer RH, Glenn T, French JO, Mays B, Shames RB, Barnes GL, Rhodes W, Ishikawa Y (2000) The expression of beta (b) keratins in the epidermal appendages of reptiles and birds. Am Zool 40:530–539

    CAS  Google Scholar 

  • Staudt K, Saxe FPM, Schmied H, Soeur R, Bohme W, Baumgartner W (2012) Comparative investigations of the sandfish’s beta-keratin (Reptilia: Scincidae: Scincus scincus). Part 1: surface and molecular examinations. J Biomim Biomater Tissue Eng 15:1–16

    Article  CAS  Google Scholar 

  • Steinert PM, Freedberg IM (1991) Molecular and cellular biology of keratins. In: Goldsmith LA (ed) Physiology, biochemistry, and molecular biology of the skin, vol 1. Oxford University Press, New York, pp 113–147

    Google Scholar 

  • Strasser B, Mlitz V, Hermann M, Rice RH, Eigenheer RA, Alibardi L, Tschachler E, Eckhart L (2014) Evolutionary origin and diversification of epidermal barrier proteins in amniotes. Mol Biol Evol 31:3194–3205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toni M, Dalla Valle L, Alibardi L (2007a) Hard (Beta-) keratins in the epidermis of reptiles: composition, sequence, and molecular organization. J Proteome Res 6:3377–3392

    Article  CAS  PubMed  Google Scholar 

  • Toni M, Dalla Valle L, Alibardi L (2007b) The epidermis of scales in gecko lizards contains multiple forms of beta-keratins including basic glycine-proline-serine-rich proteins. J Proteome Res 6:1792–1805

    Article  CAS  PubMed  Google Scholar 

  • Vandebergh W, Bossuyt F (2012) Radiation and functional diversification of alpha keratins during early vertebrate evolution. Mol Biol Evol 29:995–1004

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitbread LA, Gregg K, Rogers GE (1991) The structure and expression of a gene encoding chick claw keratin. Gene 101:223–229

    Article  CAS  PubMed  Google Scholar 

  • Wu P, Hou L, Plikus M, Hughes M, Scehnet J, Suksaweang S, Widelitz R, Jiang TX, Chuong CM (2004) Evo-Devo of amniote integuments and appendages. Int J Dev Biol 48:249–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wyld JA, Brush AH (1979) The molecular heterogeneity and diversity of reptilian keratins. J Mol Evol 12:331–347

  • Wyld JA, Brush AH (1983) Keratin diversity in the reptilian epidermis. J Exp Zool 225:387–396

    Article  CAS  Google Scholar 

  • Ye P, Wu X, Yan P, Amato G (2010) Beta-keratins in crocodiles reveal amino acid homology with avian keratins. Mol Biol Rep 37:1169–1174

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was mostly supported by the Comparative Histolab and in part funded by an Italian Ministry of Education and Scientific Research (Grant 2008 AXS E-002) and the University of Bologna (RFO small grants). Drs. Luisa Dalla Valle (University of Padova, Italy), Mattia Toni (University of Bologna, Italy), and Leopold Eckhart (Medical University of Wien, Austria) collaborated on the genomic and proteomic side of the study. The Review is dedicated to Dr. Luisa Dalla Valle for her fundamental role in the determination of the gene structure and sequencing of the first Corneous beta proteins in reptiles.

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  1. Comparative Histolab and Department of Biology, Geology and Environmental Sciences, University of Bologna, via Selmi 3, 40126, Bologna, Italy

    Lorenzo Alibardi

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Fig. 1S

Two-dimensional gel electrophoresis of separated protein spots from the epidermis of A. carolinensis (A-C) and schematic representation of the relative localization of the beta-protein cluster in the EDC (D). A, numerous protein spots of different intensity are detected (over 36) within the beta-protein range (βP, 7.0–24 kDa), mainly in the acidic range (pH 3.7–6.8), and a lower number of spots in the basic range (pH 7.2–9.8). In the alpha-keratin range (42–70 kDa) most of the proteins are acidic (pH 4.8–6.2) and a weaker not well resolved band is basic (pH 7.0–8.3). The question marks (?) indicate an intermediate molecular weight range where some protein spots (25–36 kDa) may include other types of proteins aside fragmented alpha-keratins or beta-proteins. B, immunoblot using the Phos-Tag method reveal in the beta-protein range that most proteins in the acid range (pH 4.2–6.2) are phosphorylated. C, virtual two-dimensional pattern of beta-proteins obtained plotting the deduced pI for each of the 40 beta-proteins detected in the genome of A. carolinensis. The larger dots indicate the localization of the isoforms for two beta-proteins (37, 39) and the large 40 beta-protein not included in the four families (Dalla Valle et al. 2010). D, the relative position of the Beta-Protein cluster in anole and chicken EDC is schematically shown between the loci occupied by S100A9 and S100A11 proteins, and more specifically between the Loricrin gene and Scaffoldin (SCF) genes (trichohyalin-like equivalent genes in sauropsids, TH-like). In the human EDC, the relative position of beta-proteins is instead occupied by other types of corneous protein genes such as SPRR (Small Proline-Rich proteins) and LCE (Late Cornified Envelope Proteins; see details in Strasser et al. 2014). Legends: CRNN, Chicken Cornulin gene; FH, feather-keratin genes; FIL, filaggrin gene; LOR, loricrin gene; PRP, gene; SC, sciellin gene; TH, trichohyalin gene. The arrows indicate the transcriptional orientation of the genes. (JPG 461 kb)

Fig. 2S

Four amino acid sequences of intermediate filament (α) keratins form A. carolinensis. It is reported the Accession Number, amino acid number, molecular weigh in kDa, and isoelectric point (pi). Also the percentage of glycine (in red) and cysteine (in green) are shown. The blue lines indicate the selected epitopes utilized to make the antibodies against these keratins. (JPG 2366 kb)

Fig. 3S

Aligned sequences for the 37 Corneous beta-proteins (Li-Ac_1-36, 38) subdivided into 4 subfamilies (HgG, HgGC, HC, and LwGC) detected in A. carolinensis (see equivalent Fig. 4 in Dalla Valle et al. 2010), showing the selected specific epitopes for antibody production (arrows). The arrowheads on the left indicate the specific proteins recognized by only one antibody (single colored arrowheads) or by two different antibodies (arrowheads of two different colors that match the colors of the selected epitopes) tagging the same protein in different regions. General antibodies for the precore box (yellow) and the core box (gray) region are also available. (JPG 4555 kb)

Fig. 4S

Prediction of the secondary structure for the longest beta-proteins, Ac37 and Ac40. The underlined sequences in pink indicate core box regions (1 for Ac37 and 3 for Ac40, corresponding to regions of the protein where red arrows are present) while the blue boxed sequences (arrowheads) indicate the selected epitopes for antibody production. The number of amino acids, deduced molecular weight (MW), isoelectric point (pI), and the net electrical charge are also indicated. (JPG 2147 kb)

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Alibardi, L. Review: mapping epidermal beta-protein distribution in the lizard Anolis carolinensis shows a specific localization for the formation of scales, pads, and claws. Protoplasma 253, 1405–1420 (2016). https://doi.org/10.1007/s00709-015-0909-z

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