Evolutionary origin and diversification of epidermal barrier proteins in amniotes

Strasser, Bettina; Mlitz, Veronika; Hermann, Marcela; Rice, Robert H.; Eigenheer, Richard A.; Alibardi, Lorenzo; Tschachler, Erwin; Eckhart, Leopold

doi:10.1093/molbev/msu251

Cited by 135Skin and Cellular Biology ResearchGenomics and Phylogenetic StudiesDevelopmental Biology and Gene Regulation

Evolutionary origin and diversification of epidermal barrier proteins in amniotes

Open access

Strasser, Bettina, Mlitz, Veronika, Hermann, Marcela, Rice, Robert H., Eigenheer, Richard A., Alibardi, Lorenzo, Tschachler, Erwin, Eckhart, Leopold·2014·Molecular Biology and Evolution

DOI 10.1093/molbev/msu251PMC PMC4245816

Open this paper in CoChat — free account Open PDF

Abstract

The evolution of amniotes has involved major molecular innovations in the epidermis. In particular, distinct structural proteins that undergo covalent cross-linking during cornification of keratinocytes facilitate the formation of mechanically resilient superficial cell layers and help to limit water loss to the environment. Special modes of cornification generate amniote-specific skin appendages such as claws, feathers, and hair. In mammals, many protein substrates of cornification are encoded by a cluster of genes, termed the epidermal differentiation complex (EDC). To provide a basis for hypotheses about the evolution of cornification proteins, we screened for homologs of the EDC in non-mammalian vertebrates. By comparative genomics, de novo gene prediction and gene expression analyses, we show that, in contrast to fish and amphibians, the chicken and the green anole lizard have EDC homologs comprising genes that are specifically expressed in the epidermis and in skin appendages. Our data suggest that an important component of the cornified protein envelope of mammalian keratinocytes, that is, loricrin, has originated in a common ancestor of modern amniotes, perhaps during the acquisition of a fully terrestrial lifestyle. Moreover, we provide evidence that the sauropsid-specific beta-keratins have evolved as a subclass of EDC genes. Based on the comprehensive characterization of the arrangement, exon-intron structures and conserved sequence elements of EDC genes, we propose new scenarios for the evolutionary origin of epidermal barrier proteins via fusion of neighboring S100A and peptidoglycan recognition protein genes, subsequent loss of exons and highly divergent sequence evolution.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1093/molbev/msu251

Cites

55 of 55 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Fishes lack many of the key proteins that constitute the mature SC in amniotes.
“Though fishes lack many of the key proteins that constitute the mature SC in amniotes (Strasser et al., 2014), our transcriptional data provide evidence that the molecular machinery that supports formation of the SC in amniotes is activated during air exposure.”
From Genomic and physiological mechanisms underlying skin plasticity during water to air transition in an amphibious fish (2020) · cites this paper as Strasser et al., 2014

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

WebLogo: A Sequence Logo Generator: Figure 1Preprint
Crooks, G. E., Hon, G. C., Chandonia, J., & Brenner, S. E. (2004) · Genome Research · doi:10.1101/gr.849004 · Cited by 12,433 · see citing works
Multiple sequence alignment with hierarchical clustering.
Corpet, F. (1988) · Nucleic Acids Research · doi:10.1093/nar/16.22.10881 · Cited by 5,575 · see citing works
Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis
Palmer, C. N. A., Irvine, A. D., Terron-Kwiatkowski, A., Zhao, Y., Liao, H., Lee, S. P., Goudie, D. R., Sandilands, A., Campbell, L. E., Smith, F. J. D., et al. (2006) · Nature Genetics · doi:10.1038/ng1767 · Cited by 2,978 · see citing works
The cornified envelope: a model of cell death in the skin
Candi, E., Schmidt, R., & Melino, G. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1619 · Cited by 1,776 · see citing works
Orthologs, Paralogs, and Evolutionary Genomics
Koonin, E. V. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.114725 · Cited by 1,323 · see citing works
Concerted and Birth-and-Death Evolution of Multigene Families
Nei, M., & Rooney, A. P. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.112240 · Cited by 1,298 · see citing works
Barrier Function of the Skin: “La Raison d'Être” of the Epidermis
Madison, K. C. (2003) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2003.12359.x · Cited by 1,192 · see citing works
The origin of new genes: Glimpses from the young and old
Long, M., Betrán, E., Thornton, K., & Wang, W. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1204 · Cited by 933 · see citing works
Presence in human epidermal cells of a soluble protein precursor of the cross-linked envelope: Activation of the cross-linking by calcium ions
Rice, R. H., & Green, H. (1979) · Cell · doi:10.1016/0092-8674(79)90123-5 · Cited by 785 · see citing works
Self-citation
New consensus nomenclature for mammalian keratins
Schweizer, J., Bowden, P. E., Coulombe, P. A., Langbein, L., Lane, E. B., Magin, T. M., Maltais, L. J., Omary, M. B., Parry, D. A. D., Rogers, M. A., et al. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200603161 · Cited by 740 · see citing works
The cornified envelope of terminally differentiated human epidermal keratinocytes consists of cross-linked protein
Rice, R. H., & Green, H. (1977) · Cell · doi:10.1016/0092-8674(77)90059-9 · Cited by 535 · see citing works
Self-citation
Deletion of the late cornified envelope LCE3B and LCE3C genes as a susceptibility factor for psoriasis
de Cid, R., Riveira‐Muñoz, E., Zeeuwen, P. L. J. M., Robarge, J., Liao, W. J., Dannhauser, E. N., Giardina, E., Stuart, P. E., Nair, R. P., Helms, C. A., et al. (2009) · Nature Genetics · doi:10.1038/ng.313 · Cited by 533 · see citing works
The Proteins Elafin, Filaggrin, Keratin Intermediate Filaments, Loricrin, and Small Proline-rich Proteins 1 and 2 Are Isodipeptide Cross-linked Components of the Human Epidermal Cornified Cell Envelope
Steinert, P. M., & Marekov, L. N. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.30.17702 · Cited by 519 · see citing works
Cell death by cornification
Eckhart, L., Lippens, S., Tschachler, E., & Declercq, W. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.06.010 · Cited by 515 · see citing works
Self-citation
The sheep genome illuminates biology of the rumen and lipid metabolism
Jiang, Y., Xie, M., Chen, W., Talbot, R., Maddox, J. F., Faraut, T., Wu, C., Muzny, D. M., Li, Y., Zhang, W., et al. (2014) · Science · doi:10.1126/science.1252806 · Cited by 514 · see citing works
Genes Encoding Structural Proteins of Epidermal Cornification and S100 Calcium-Binding Proteins Form a Gene Complex (“Epidermal Differentiation Complex”) on Human Chromosome 1q21
Mischke, D., Korge, B. P., Marenholz, I., Volz, A., & Ziegler, A. (1996) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12338501 · Cited by 505 · see citing works
Epithelial barrier function: assembly and structural features of the cornified cell envelope
Kalinin, A. E., Kajava, A. V., & Steinert, P. M. (2002) · BioEssays · doi:10.1002/bies.10144 · Cited by 481 · see citing works
Identification of a major keratinocyte cell envelope protein, loricrin
Mehrel, T., Hohl, D., Rothnagel, J. A., Longley, M. A., Bundman, D. S., Cheng, C., Lichti, U. F., Bisher, M. E., Steven, A. C., Steinert, P. M., et al. (1990) · Cell · doi:10.1016/0092-8674(90)90073-n · Cited by 436 · see citing works
New genes as drivers of phenotypic evolution
Chen, S., Krinsky, B. H., & Long, M. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3521 · Cited by 428 · cited 1× · see citing works
“Although any model for the evolution of EDC genes must include speculative elements, a key role of gene duplications and fusions, as demonstrated for other cases of gene origin (Long et al. 2003; Chen et al. 2013) is supported by the results of the present study.”
Result
Preparation of Genomic DNA from Mammalian Tissue
Strauss, W. M. (1998) · Current Protocols in Molecular Biology · doi:10.1002/0471142727.mb0202s42 · Cited by 302 · see citing works
Contoversies in Experimental Dermatology
Chuong, C., Nickoloff, B. J., Elias, P. M., Goldsmith, L. A., Macher, E., Maderson, P. A., Sundberg, J. P., Tagami, H., Plonka, P. M., Thestrup-Pederson, K., et al. (2002) · Experimental Dermatology · doi:10.1034/j.1600-0625.2002.00112.x · Cited by 288 · see citing works
A molecular defect in loricrin, the major component of the cornified cell envelope, underlies Vohwinkel's syndrome
Maestrini, E., Monaco, A. P., McGrath, J. A., Ishida‐Yamamoto, A., Camisa, C., Hovnanian, A., Weeks, D. E., Lathrop, M. G., Uitto, J., & Christiano, A. M. (1996) · Nature Genetics · doi:10.1038/ng0596-70 · Cited by 240 · see citing works
Adaptation to the land: The skin of reptiles in comparison to that of amphibians and endotherm amniotes
Alibardi, L. (2003) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.24 · Cited by 234 · see citing works
Self-citation
S100A11, S100A10, Annexin I, Desmosomal Proteins, Small Proline-rich Proteins, Plasminogen Activator Inhibitor-2, and Involucrin Are Components of the Cornified Envelope of Cultured Human Epidermal Keratinocytes
Robinson, N. A., Lapic, S. K., Welter, J. F., & Eckert, R. L. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.18.12035 · Cited by 215 · see citing works
La raison d'être
Vatin, J.-C. (1992) · doi:10.4000/books.cedej.1338 · Cited by 199 · see citing works
Evo-Devo of amniote integuments and appendages.
Wu, P., Hou, L., Plikus, M. V., Hughes, M. W., Scehnet, J. S., Suksaweang, S., Widelitz, R. B., Jiang, T., & Chuong, C. (2004) · The International Journal of Developmental Biology · doi:10.1387/ijdb.15272390 · Cited by 199 · see citing works
Cornified Cell Envelope
Hohl, D. (2009) · Dermatologica · doi:10.1159/000248031 · Cited by 185 · see citing works
Evo-Devo of amniote integuments and appendages
Wu, P., Hou, L., Plikus, M. V., Hughes, M. W., Scehnet, J. S., Suksaweang, S., Widelitz, R. B., Jiang, T. X., & Chuong, C. (2004) · The International Journal of Developmental Biology · doi:10.1387/ijdb.041825pw · Cited by 181 · see citing works
Preparation of Genomic DNA from Mammalian Tissue
Strauss, W. M. (1999) · Current Protocols in Neuroscience · doi:10.1002/0471142301.nsa01hs06 · Cited by 178 · see citing works
Peptidoglycan recognition proteins kill bacteria by activating protein-sensing two-component systems
Kashyap, D. R., Wang, M. H., Liu, L.-H., Boons, G., Gupta, D., & Dziarski, R. (2011) · Nature Medicine · doi:10.1038/nm.2357 · Cited by 160 · see citing works
Extensive and Continuous Duplication Facilitates Rapid Evolution and Diversification of Gene Families
Chang, D., & Duda, T. F. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss068 · Cited by 157 · see citing works
Update on the epidermal differentiation complex
Henry, J. (2011) · Frontiers in bioscience · doi:10.2741/4001 · Cited by 153 · see citing works
Barrier function of the skin.
Paépe, K. D. (1996) · VUBIR (Vrije Universiteit Brussel) · Cited by 146 · see citing works
Profilaggrin is a Major Epidermal Calcium-Binding Protein
Markova, N. G., Marekov, L. N., Chipev, C. C., Gan, S.-Q., Idler, W. W., & Steinert, P. M. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.1.613-625.1993 · Cited by 140 · see citing works
Evolution of the S100 family of calcium sensor proteins
Zimmer, D. B., Eubanks, J. O., Ramakrishnan, D., & Criscitiello, M. F. (2012) · Cell Calcium · doi:10.1016/j.ceca.2012.11.006 · Cited by 128 · see citing works
Identification of reptilian genes encoding hair keratin-like proteins suggests a new scenario for the evolutionary origin of hair
Eckhart, L., Valle, L. D., Jaeger, K., Ballaun, C., Szabo, S., Nardi, A., Buchberger, M., Hermann, M., Alibardi, L., & Tschachler, E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805154105 · Cited by 113 · see citing works
Self-citation
A common origin for cornified envelope proteins?
Backendorf, C., & Hohl, D. (1992) · Nature Genetics · doi:10.1038/ng1092-91 · Cited by 107 · see citing works
Evolution of hard proteins in the sauropsid integument in relation to the cornification of skin derivatives in amniotes
Alibardi, L., Valle, L. D., Nardi, A., & Toni, M. (2009) · Journal of Anatomy · doi:10.1111/j.1469-7580.2009.01045.x · Cited by 101 · see citing works
Self-citation
Mammalian skin evolution: a reevaluation
MADERSON, P. F. A. (2003) · Experimental Dermatology · doi:10.1034/j.1600-0625.2003.00069.x · Cited by 98 · see citing works
Structural and Immunocytochemical Characterization of Keratinization in Vertebrate Epidermis and Epidermal Derivatives
Alibardi, L. (2006) · International review of cytology · doi:10.1016/s0074-7696(06)53005-0 · Cited by 83 · see citing works
Self-citation
Radiation and Functional Diversification of Alpha Keratins during Early Vertebrate Evolution
Vandebergh, W., & Bossuyt, F. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr269 · Cited by 83 · see citing works
Forty keratin‐associated β‐proteins (β‐keratins) form the hard layers of scales, claws, and adhesive pads in the green anole lizard, Anolis carolinensis
Valle, L. D., Nardi, A., Bonazza, G., Zucal, C., Emera, D., & Alibardi, L. (2009) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21306 · Cited by 80 · see citing works
Self-citation
A comparison of genomic coding sequences for feather and scale keratins: structural and evolutionary implications.
Gregg, K., Wilton, S. D., Parry, D. A. D., & Rogers, G. E. (1984) · The EMBO Journal · doi:10.1002/j.1460-2075.1984.tb01779.x · Cited by 78 · see citing works
Genomic organization and molecular phylogenies of the beta (β) keratin multigene family in the chicken (Gallus gallus) and zebra finch (Taeniopygia guttata): implications for feather evolution
Greenwold, M. J., & Sawyer, R. H. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-148 · Cited by 76 · see citing works
Trichohyalin-Like Proteins Have Evolutionarily Conserved Roles in the Morphogenesis of Skin Appendages
Mlitz, V., Strasser, B., Jaeger, K., Hermann, M., Ghannadan, M., Buchberger, M., Alibardi, L., Tschachler, E., & Eckhart, L. (2014) · Journal of Investigative Dermatology · doi:10.1038/jid.2014.204 · Cited by 76 · see citing works
Self-citation
Molecular evolution and expression of archosaurian β‐keratins: Diversification and expansion of archosaurian β‐keratins and the origin of feather β‐keratins
Greenwold, M. J., & Sawyer, R. H. (2013) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22514 · Cited by 64 · see citing works
β‐keratins of the crocodilian epidermis: composition, structure, and phylogenetic relationships
Valle, L. D., Nardi, A., Gelmi, C., Toni, M., Emera, D., & Alibardi, L. (2008) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21241 · Cited by 58 · see citing works
Self-citation
Transcriptomic Analysis of Endangered Chinese Salamander: Identification of Immune, Sex and Reproduction-Related Genes and Genetic Markers
Che, R., Sun, Y., Wang, R., & Xu, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087940 · Cited by 53 · see citing works
Ancient origin of the gene encoding involucrin, a precursor of the cross-linked envelope of epidermis and related epithelia
Vanhoutteghem, A., Djian, P., & Green, H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807643105 · Cited by 52 · see citing works
Linking the molecular evolution of avian beta (β) keratins to the evolution of feathers
Greenwold, M. J., & Sawyer, R. H. (2011) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21436 · Cited by 49 · see citing works
Loss of Keratin K2 Expression Causes Aberrant Aggregation of K10, Hyperkeratosis, and Inflammation
Fischer, H., Langbein, L., Reichelt, J., Praetzel‐Wunder, S., Buchberger, M., Ghannadan, M., Tschachler, E., & Eckhart, L. (2014) · Journal of Investigative Dermatology · doi:10.1038/jid.2014.197 · Cited by 46 · see citing works
Self-citation
Evolutionary origin of peptidoglycan recognition proteins in vertebrate innate immune system
Montaño, A. M., Tsujino, F., Takahata, N., & Satta, Y. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-79 · Cited by 39 · see citing works
The involucrin genes of the mouse and the rat: study of their shared repeats.
Djian, P., Phillips, M. A., Easley, K. W., Huang, E., Simon, M., Rice, R. H., & Green, H. (1993) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040069 · Cited by 38 · see citing works
Self-citation
Chicken Corneocyte Cross-Linked Proteome
Rice, R. H., Winters, B. R., Durbin-Johnson, B. P., & Rocke, D. M. (2012) · Journal of Proteome Research · doi:10.1021/pr301036k · Cited by 29 · see citing works
Self-citation
The involucrin gene of the tree shrew: recent repeat additions and the relocation of cysteine codons
Phillips, M. A., Rice, R. H., Djian, P., & Green, H. (1997) · Gene · doi:10.1016/s0378-1119(96)00654-3 · Cited by 5 · see citing works
Self-citation

Flagged first, then by citations

1 of the 56 references couldn’t be matched to a known paper.

Sorted by citations

Keratin: Structure, mechanical properties, occurrence in biological organisms, and efforts at bioinspiration
Wang, B., Yang, W., McKittrick, J. M., & Meyers, M. A. (2015) · Progress in Materials Science · doi:10.1016/j.pmatsci.2015.06.001 · Cited by 879 · see citing works
Dissecting the formation, structure and barrier function of the stratum corneum
Matsui, T., & Amagai, M. (2015) · International Immunology · doi:10.1093/intimm/dxv013 · Cited by 368 · see citing works
Genetic Basis for Red Coloration in Birds
Lopes, R. J., Johnson, J. D., Toomey, M. B., Ferreira, M. S., Araújo, P. M., Melo‐Ferreira, J., Andersson, L., Hill, G. E., Corbo, J. C., & Carneiro, M. (2016) · Current Biology · doi:10.1016/j.cub.2016.03.076 · Cited by 238 · see citing works
Epidemiology of adult atopic dermatitis
Sacotte, R. M., & Silverberg, J. I. (2018) · Clinics in Dermatology · doi:10.1016/j.clindermatol.2018.05.007 · Cited by 235 · see citing works
The Evolution and Genetics of Carotenoid Processing in Animals
Toews, D. P. L., Hofmeister, N. R., & Taylor, S. A. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.01.002 · Cited by 185 · see citing works
Review: Evolution and diversification of corneous beta‐proteins, the characteristic epidermal proteins of reptiles and birds
Holthaus, K. B., Eckhart, L., Valle, L. D., & Alibardi, L. (2018) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22840 · Cited by 94 · see citing works
Self-citation
Comparison of vertebrate skin structure at class level: A review
Akat, E., Yenmiş, M., Pombal, M. A., Molíst, P., Megı́as, M., Arman, S., Veselý, M., Anderson, R. O., & Ayaz, D. (2022) · The Anatomical Record · doi:10.1002/ar.24908 · Cited by 93 · see citing works
Convergent evolution of cysteine-rich proteins in feathers and hair
Strasser, B., Mlitz, V., Hermann, M., Tschachler, E., & Eckhart, L. (2015) · BMC Evolutionary Biology · doi:10.1186/s12862-015-0360-y · Cited by 83 · see citing works
Self-citation
The molecular organization of the beta-sheet region in Corneous beta-proteins (beta-keratins) of sauropsids explains its stability and polymerization into filaments
Calvaresi, M., Eckhart, L., & Alibardi, L. (2016) · Journal of Structural Biology · doi:10.1016/j.jsb.2016.03.004 · Cited by 73 · see citing works
Self-citation
Genetic and Molecular Basis of Feather Diversity in Birds
Ng, C. S., & Li, W. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy180 · Cited by 70 · see citing works
Loricrin: Past, Present, and Future
Ishitsuka, Y., & Roop, D. R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21072271 · Cited by 71 · see citing works
The process of cornification evolved from the initial keratinization in the epidermis and epidermal derivatives of vertebrates: a new synthesis and the case of sauropsids
(2016) · International Review of Cell and Molecular Biology · doi:10.1016/bs.ircmb.2016.06.005 · Cited by 64 · see citing works
Self-citation
Convergent Evolution of Cysteine-Rich Keratins in Hard Skin Appendages of Terrestrial Vertebrates
Ehrlich, F., Lachner, J., Hermann, M., Tschachler, E., & Eckhart, L. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz279 · Cited by 64 · see citing works
Self-citation
Shades of complexity: New perspectives on the evolution and genetic architecture of human skin
Quillen, E. E., Norton, H. L., Parra, E. J., Lona‐Durazo, F., Ang, K. C., Illiescu, F. M., Pearson, L. N., Shriver, M. D., Lasisi, T., Gokcumen, O., et al. (2019) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23737 · Cited by 67 · see citing works
New Genes and Functional Innovation in Mammals
Villanueva‐Cañas, J. L., Ruiz‐Orera, J., Agea, M. I., Gallo, M., Andreu, D., & Albà, M. M. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx136 · Cited by 59 · see citing works
Review: cornification, morphogenesis and evolution of feathers
Alibardi, L. (2016) · PROTOPLASMA · doi:10.1007/s00709-016-1019-2 · Cited by 58 · see citing works
Self-citation
Recent evolution of the human skin barrier
Brettmann, E. A., & Strong, C. D. G. (2018) · Experimental Dermatology · doi:10.1111/exd.13689 · Cited by 57 · see citing works
Comparative Genomics Identifies Epidermal Proteins Associated with the Evolution of the Turtle Shell
Holthaus, K. B., Strasser, B., Sipos, W., Schmidt, H. A., Mlitz, V., Sukseree, S., Weissenbacher, A., Tschachler, E., Alibardi, L., & Eckhart, L. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv265 · Cited by 55 · see citing works
Self-citation
Array-based sequencing of filaggrin gene for comprehensive detection of disease-associated variants
Wong, X. F. C. C., Denil, S. L. I. J., Foo, J. N., Chen, H., Tay, A. S. L., Haines, R. L., Tang, M. B. Y., McLean, W. H. I., Sandilands, A., Smith, F. J. D., et al. (2017) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.10.001 · Cited by 49 · see citing works
Lce1 Family Members Are Nrf2-Target Genes that Are Induced to Compensate for the Loss of Loricrin
Ishitsuka, Y., Huebner, A. J., Rice, R. H., Koch, P. J., Speransky, V. V., Steven, A. C., & Roop, D. R. (2016) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2016.04.022 · Cited by 43 · see citing works
Self-citation
Comparative genomics reveals conservation of filaggrin and loss of caspase‐14 in dolphins
Strasser, B., Mlitz, V., Fischer, H., Tschachler, E., & Eckhart, L. (2015) · Experimental Dermatology · doi:10.1111/exd.12681 · Cited by 42 · see citing works
Self-citation
Atopic Dermatitis Susceptibility Variants in Filaggrin Hitchhike Hornerin Selective Sweep
Eaaswarkhanth, M., Xu, D., Flanagan, C., Rzhetskaya, M., Hayes, M. G., Blekhman, R., Jablonski, N. G., & Gökçümen, Ö. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw242 · Cited by 40 · see citing works
Combination of novel and public RNA-seq datasets to generate an mRNA expression atlas for the domestic chicken
Bush, S. J., Freem, L. J., MacCallum, A. J., O’Dell, J., Wu, C., Afrasiabi, C., Psifidi, A., Stevens, M. P., Smith, J., SUMMERS, K. M., et al. (2018) · BMC Genomics · doi:10.1186/s12864-018-4972-7 · Cited by 39 · see citing works
Comparative Analysis of Epidermal Differentiation Genes of Crocodilians Suggests New Models for the Evolutionary Origin of Avian Feather Proteins
Holthaus, K. B., Strasser, B., Lachner, J., Sukseree, S., Sipos, W., Weissenbacher, A., Tschachler, E., Alibardi, L., & Eckhart, L. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy035 · Cited by 36 · see citing works
Self-citation
Identification and comparative analysis of the epidermal differentiation complex in snakes
Holthaus, K. B., Mlitz, V., Strasser, B., Tschachler, E., Alibardi, L., & Eckhart, L. (2017) · Scientific Reports · doi:10.1038/srep45338 · Cited by 35 · see citing works
Self-citation
The KEAP1/NRF2 Signaling Pathway in Keratinization
Ishitsuka, Y., Ogawa, T., & Roop, D. R. (2020) · Antioxidants · doi:10.3390/antiox9080751 · Cited by 34 · see citing works
Review: mapping proteins localized in adhesive setae of the tokay gecko and their possible influence on the mechanism of adhesion
Alibardi, L. (2018) · PROTOPLASMA · doi:10.1007/s00709-018-1270-9 · Cited by 31 · see citing works
Self-citation
Immunolocalization of a Histidine-Rich Epidermal Differentiation Protein in the Chicken Supports the Hypothesis of an Evolutionary Developmental Link between the Embryonic Subperiderm and Feather Barbs and Barbules
Alibardi, L., Holthaus, K. B., Sukseree, S., Hermann, M., Tschachler, E., & Eckhart, L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0167789 · Cited by 28 · see citing works
Self-citation
Sauropsids Cornification is Based on Corneous Beta‐Proteins, a Special Type of Keratin‐Associated Corneous Proteins of the Epidermis
Alibardi, L. (2016) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22689 · Cited by 30 · see citing works
Self-citation
Recent Positive Selection in Genes of the Mammalian Epidermal Differentiation Complex Locus
Goodwin, Z. A., & Strong, C. D. G. (2017) · Frontiers in Genetics · doi:10.3389/fgene.2016.00227 · Cited by 27 · see citing works
NRF2 Augments Epidermal Antioxidant Defenses and Promotes Atopy
Ogawa, T., Ishitsuka, Y., Nakamura, Y., Kubota, N., Saito, A., Fujisawa, Y., Watanabe, R., Okiyama, N., Suga, Y., Roop, D. R., et al. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.2000274 · Cited by 28 · see citing works
Evolution of Trichocyte Keratins
Eckhart, L., & Ehrlich, F. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-8195-8_4 · Cited by 27 · see citing works
Self-citation
Vertebrate keratinization evolved into cornification mainly due to transglutaminase and sulfhydryl oxidase activities on epidermal proteins: An immunohistochemical survey
Alibardi, L. (2021) · The Anatomical Record · doi:10.1002/ar.24705 · Cited by 26 · see citing works
Self-citation
Localization of Alpha‐Keratin and Beta‐Keratin (Corneous Beta Protein) in the Epithelium on the Ventral Surface of the Lingual Apex and Its Lingual Nail in the Domestic Goose (Anser Anser f. domestica) by Using Immunohistochemistry and Raman Microspectroscopy Analysis
Skieresz‐Szewczyk, K., Jackowiak, H., Buchwald, T., & Szybowicz, M. (2017) · The Anatomical Record · doi:10.1002/ar.23591 · Cited by 26 · see citing works
Epidermal Barrier Development via Corneoptosis: A Unique Form of Cell Death in Stratum Granulosum Cells
Matsui, T. (2023) · Journal of Developmental Biology · doi:10.3390/jdb11040043 · Cited by 25 · see citing works
Preservation potential of keratin in deep time
Schweitzer, M. H., Zheng, W., Moyer, A. E., Sjövall, P., & Lindgren, J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0206569 · Cited by 24 · see citing works
The Story of the Finest Armor: Developmental Aspects of Reptile Skin
Yenmiş, M., & Ayaz, D. (2023) · Journal of Developmental Biology · doi:10.3390/jdb11010005 · Cited by 22 · see citing works
Development-Associated Genes of the Epidermal Differentiation Complex (EDC)
Holthaus, K. B., & Eckhart, L. (2024) · Journal of Developmental Biology · doi:10.3390/jdb12010004 · Cited by 22 · see citing works
Self-citation
Immunolocalization and phylogenetic profiling of the feather protein with the highest cysteine content
Lachner, J., Ehrlich, F., Mlitz, V., Hermann, M., Alibardi, L., Tschachler, E., & Eckhart, L. (2019) · PROTOPLASMA · doi:10.1007/s00709-019-01381-3 · Cited by 21 · see citing works
Self-citation
Phylogenetic profiling and gene expression studies implicate a primary role of PSORS 1C2 in terminal differentiation of keratinocytes
Zadeh, S. A., Mlitz, V., Lachner, J., Golabi, B., Mildner, M., Pammer, J., Tschachler, E., & Eckhart, L. (2016) · Experimental Dermatology · doi:10.1111/exd.13272 · Cited by 20 · see citing works
Self-citation
Genomic and physiological mechanisms underlying skin plasticity during water to air transition in an amphibious fish
Dong, Y.-W., Blanchard, T. S., Noll, A., Vasquez, P., Schmitz, J., Kelly, S. P., Wright, P. A., & Whitehead, A. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.235515 · Cited by 18 · see citing works
Loricrin at the Boundary between Inside and Outside
Ishitsuka, Y., & Roop, D. R. (2022) · Biomolecules · doi:10.3390/biom12050673 · Cited by 18 · see citing works
A molecular mechanism for bright color variation in parrots
Arbore, R., Barbosa, S., Brejcha, J., Ogawa, Y., Liu, Y., Nicolaï, M. P. J., Pereira, P., Sabatino, S. J., Cloutier, A., Poon, E. S. K., et al. (2024) · Science · doi:10.1126/science.adp7710 · Cited by 18 · see citing works
Filaggrin has evolved from an “S100 fused‐type protein” ( SFTP ) gene present in a common ancestor of amphibians and mammals
Mlitz, V., Hussain, T., Tschachler, E., & Eckhart, L. (2017) · Experimental Dermatology · doi:10.1111/exd.13317 · Cited by 18 · see citing works
Self-citation
Gene duplications and gene loss in the epidermal differentiation complex during the evolutionary land-to-water transition of cetaceans
Holthaus, K. B., Lachner, J., Ebner, B., Tschachler, E., & Eckhart, L. (2021) · Scientific Reports · doi:10.1038/s41598-021-91863-3 · Cited by 17 · see citing works
Self-citation
The Epidermis: Redox Governor of Health and Diseases
Ishitsuka, Y., & Roop, D. R. (2021) · Antioxidants · doi:10.3390/antiox11010047 · Cited by 17 · see citing works
Organizational principles of integumentary organs: Maximizing variations for effective adaptation
Chuong, C., Wu, P., Zhou, Y., Liang, Y. C., & Widelitz, R. B. (2025) · Developmental Biology · doi:10.1016/j.ydbio.2025.03.011 · Cited by 19 · see citing works
Loricrin Confers Photoprotective Function against UVB in Corneocytes
Ishitsuka, Y., & Roop, D. R. (2018) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2018.06.164 · Cited by 17 · see citing works
Identification of epidermal differentiation genes of the tuatara provides insights into the early evolution of lepidosaurian skin
Holthaus, K. B., Alibardi, L., Tschachler, E., & Eckhart, L. (2020) · Scientific Reports · doi:10.1038/s41598-020-69885-0 · Cited by 17 · see citing works
Self-citation
Transglutaminase Activity Is Conserved in Stratified Epithelia and Skin Appendages of Mammals and Birds
Sachslehner, A. P., Surbek, M., Golabi, B., Geiselhofer, M., Jäger, K., Hess, C., Kuchler, U., Gruber, R., & Eckhart, L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032193 · Cited by 16 · see citing works
Self-citation
Evolutionary origin of Hoxc13-dependent skin appendages in amphibians
Carron, M., Sachslehner, A. P., Cicekdal, M. B., Bruggeman, I., Demuynck, S., Golabi, B., Baere, E. B. W. D., Declercq, W., Tschachler, E., Vleminckx, K., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-46373-x · Cited by 16 · see citing works
Self-citation
Keratinization and Cornification are not equivalent processes but keratinization in fish and amphibians evolved into cornification in terrestrial vertebrates
Alibardi, L. (2022) · Experimental Dermatology · doi:10.1111/exd.14525 · Cited by 16 · see citing works
Self-citation
Review: mapping epidermal beta-protein distribution in the lizard Anolis carolinensis shows a specific localization for the formation of scales, pads, and claws
Alibardi, L. (2015) · PROTOPLASMA · doi:10.1007/s00709-015-0909-z · Cited by 16 · see citing works
Self-citation
Duplications in Corneous Beta Protein Genes and the Evolution of Gecko Adhesion
Gamble, T. (2019) · Integrative and Comparative Biology · doi:10.1093/icb/icz010 · Cited by 15 · see citing works
Seeing Keratinocyte Proteins through the Looking Glass of Intrinsic Disorder
Shamilov, R., Robinson, V. L., & Aneskievich, B. J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22157912 · Cited by 15 · see citing works
Regional Specific Differentiation of Integumentary Organs: Regulation of Gene Clusters within the Avian Epidermal Differentiation Complex and Impacts of SATB2 Overexpression
Lin, G., Lai, Y., Liang, Y., Widelitz, R. B., Wu, P., & Chuong, C. (2021) · Genes · doi:10.3390/genes12081291 · Cited by 15 · see citing works
The Effect of Single CpG Demethylation on the Pattern of DNA-Protein Binding
Sobiak, B., & Leśniak, W. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20040914 · Cited by 15 · see citing works
Expression of specific corneous beta proteins in the developing digits of the Japanese gecko (Gekko japonicus) reveals their role in the growth of adhesive setae
Wang, F., Chen, M., Cai, F., Li, P., Yan, J., & Zhou, K. (2019) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2019.110370 · Cited by 14 · see citing works
Structures of the ß-Keratin Filaments and Keratin Intermediate Filaments in the Epidermal Appendages of Birds and Reptiles (Sauropsids)
Parry, D. A. D. (2021) · Genes · doi:10.3390/genes12040591 · Cited by 14 · see citing works
Complex Gene Loss and Duplication Events Have Facilitated the Evolution of Multiple Loricrin Genes in Diverse Bird Species
Davis, A. C., Greenwold, M. J., & Sawyer, R. H. (2019) · Genome Biology and Evolution · doi:10.1093/gbe/evz054 · Cited by 14 · see citing works
Histology of the Skin of Three Limbless Squamates Dwelling in Mesic and Arid Environments
Allam, A. A., Daza, J. D., & Abo‐Eleneen, R. E. (2016) · The Anatomical Record · doi:10.1002/ar.23356 · Cited by 14 · see citing works
Loss of the ability to regenerate body appendages in vertebrates: from side effects of evolutionary innovations to gene loss
Zaraisky, A. G., Araslanova, K. R., Shitikov, A. D., & Tereshina, M. B. (2024) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.13102 · Cited by 14 · see citing works
Analysis and comparison of protein secondary structures in the rachis of avian flight feathers
Lin, P.-Y., Huang, P., Lee, Y.-C., & Ng, C. S. (2022) · PeerJ · doi:10.7717/peerj.12919 · Cited by 13 · see citing works
Transcriptome analyses of reprogrammed feather / scale chimeric explants revealed co-expressed epithelial gene networks during organ specification
Lai, Y., Liang, Y., Jiang, T., Widelitz, R. B., Wu, P., & Chuong, C. (2018) · BMC Genomics · doi:10.1186/s12864-018-5184-x · Cited by 13 · see citing works
Molecular and functional identification of a short-type peptidoglycan recognition protein, PGRP-S, in the Chinese soft-shelled turtle Pelodiscus sinensis
Huang, L., Chen, S. N., Gan, Z., & Nie, P. (2020) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2020.103965 · Cited by 13 · see citing works
Evolution of an Epidermal Differentiation Complex (EDC) Gene Family in Birds
Davis, A., & Greenwold, M. J. (2021) · Genes · doi:10.3390/genes12050767 · Cited by 13 · see citing works
An In Vitro Model of Avian Skin Reveals Evolutionarily Conserved Transcriptional Regulation of Epidermal Barrier Formation
Lachner, J., Derdak, S. V., Mlitz, V., Wagner, T., Holthaus, K. B., Ehrlich, F., Mildner, M., Tschachler, E., & Eckhart, L. (2021) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2021.04.029 · Cited by 13 · see citing works
Self-citation
Dynamics and Epigenetics of the Epidermal Differentiation Complex
Leśniak, W. (2024) · Epigenomes · doi:10.3390/epigenomes8010009 · Cited by 12 · see citing works
The Evolution of Transglutaminases Underlies the Origin and Loss of Cornified Skin Appendages in Vertebrates
Sachslehner, A. P., Surbek, M., Holthaus, K. B., Steinbinder, J., Golabi, B., Hess, C., & Eckhart, L. (2024) · Molecular Biology and Evolution · doi:10.1093/molbev/msae100 · Cited by 13 · see citing works
Self-citation
The Trichohyalin-Like Protein Scaffoldin Is Expressed in the Multilayered Periderm during Development of Avian Beak and Egg Tooth
Mlitz, V., Hermann, M., Buchberger, M., Tschachler, E., & Eckhart, L. (2021) · Genes · doi:10.3390/genes12020248 · Cited by 12 · see citing works
Self-citation
General aspects on skin development in vertebrates with emphasis on sauropsids epidermis
Alibardi, L. (2023) · Developmental Biology · doi:10.1016/j.ydbio.2023.05.007 · Cited by 12 · see citing works
Self-citation
Identification of Chicken Transglutaminase 1 and In Situ Localization of Transglutaminase Activity in Avian Skin and Esophagus
Sachslehner, A. P., Surbek, M., Lachner, J., Paudel, S., & Eckhart, L. (2021) · Genes · doi:10.3390/genes12101565 · Cited by 12 · see citing works
Self-citation
Skin Appendage Proteins of Tetrapods: Building Blocks of Claws, Feathers, Hair and Other Cornified Epithelial Structures
Holthaus, K. B., Steinbinder, J., Sachslehner, A. P., & Eckhart, L. (2025) · Animals · doi:10.3390/ani15030457 · Cited by 12 · see citing works
Self-citation
Development, structure, and protein composition of the corneous beak in turtles
Alibardi, L. (2021) · The Anatomical Record · doi:10.1002/ar.24604 · Cited by 11 · see citing works
Self-citation
Evolutionary diversification of epidermal barrier genes in amphibians
Sachslehner, A. P., & Eckhart, L. (2022) · Scientific Reports · doi:10.1038/s41598-022-18053-7 · Cited by 11 · see citing works
Self-citation
Immunolocalization of sulfhydryl oxidase in reptilian epidermis indicates that the enzyme participates mainly to the hardening process of the beta-corneous layer
Alibardi, L. (2015) · PROTOPLASMA · doi:10.1007/s00709-015-0782-9 · Cited by 11 · see citing works
Self-citation
Alpha‐keratin and corneous beta protein in the parakeratinized epithelium of the tongue in the domestic goose (Anser anser f. domestica)
Skieresz‐Szewczyk, K., Buchwald, T., Szybowicz, M., & Jackowiak, H. (2019) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22892 · Cited by 11 · see citing works
Lepidosaur ß-keratin chains with four 34-residue repeats: Modelling reveals a potential filament-crosslinking role
Fraser, R., & Parry, D. A. D. (2019) · Journal of Structural Biology · doi:10.1016/j.jsb.2019.107413 · Cited by 10 · see citing works
Immunolocalization of corneous proteins including a serine-tyrosine-rich beta-protein in the adhesive pads in the tokay gecko
Alibardi, L. (2020) · Microscopy Research and Technique · doi:10.1002/jemt.23483 · Cited by 10 · see citing works
Self-citation
Transition from embryonic to adult epidermis in reptiles occurs by the production of corneous beta-proteins
Alibardi, L. (2014) · The International Journal of Developmental Biology · doi:10.1387/ijdb.140325la · Cited by 10 · see citing works
Self-citation
Development, structure, and protein composition of reptilian claws and hypotheses of their evolution
Alibardi, L. (2020) · The Anatomical Record · doi:10.1002/ar.24515 · Cited by 9 · see citing works
Self-citation
Immunolocalization of epidermal differentiation complex proteins reveals distinct molecular compositions of cells that control structure and mechanical properties of avian skin appendages
Alibardi, L., & Eckhart, L. (2021) · Journal of Morphology · doi:10.1002/jmor.21357 · Cited by 9 · see citing works
Self-citation
Comparative genomics of monotremes provides insights into the early evolution of mammalian epidermal differentiation genes
Steinbinder, J., Sachslehner, A. P., Holthaus, K. B., & Eckhart, L. (2024) · Scientific Reports · doi:10.1038/s41598-024-51926-7 · Cited by 8 · see citing works
Self-citation
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
Alibardi, L. (2015) · Journal of Morphology · doi:10.1002/jmor.20415 · Cited by 8 · see citing works
Self-citation
Regional specific differentiation of integumentary organs: SATB2 is involved in α‐ and β‐keratin gene cluster switching in the chicken
Lin, G., Liang, Y., Wu, P., Chen, C.-K., Lai, Y., Jiang, T., Haung, Y., & Chuong, C. (2021) · Developmental Dynamics · doi:10.1002/dvdy.396 · Cited by 8 · see citing works
Single-cell transcriptomics defines keratinocyte differentiation in avian scutate scales
Lachner, J., Ehrlich, F., Wielscher, M., Farlik, M., Hermann, M., Tschachler, E., & Eckhart, L. (2022) · Scientific Reports · doi:10.1038/s41598-021-04082-1 · Cited by 8 · see citing works
Self-citation
Comparative genomics of sirenians reveals evolution of filaggrin and caspase-14 upon adaptation of the epidermis to aquatic life
Steinbinder, J., Sachslehner, A. P., Holthaus, K. B., & Eckhart, L. (2024) · Scientific Reports · doi:10.1038/s41598-024-60099-2 · Cited by 7 · see citing works
Self-citation
Selective sweep for an enhancer involucrin allele identifies skin barrier adaptation out of Africa
Mathyer, M., Brettmann, E., Schmidt, A., Goodwin, Z. A., Oh, I., Quiggle, A., Tycksen, E., Ramakrishnan, N., Matkovich, S., Guttman-Yassky, E., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22821-w · Cited by 8 · see citing works
A previously uncharacterized Factor Associated with Metabolism and Energy (FAME/C14orf105/CCDC198/1700011H14Rik) is related to evolutionary adaptation, energy balance, and kidney physiology
Petersen, J., Englmaier, L., Artemov, A. V., Poverennaya, I. V., Mahmoud, R., Bouderlique, T., Tesarova, M., Deviatiiarov, R. M., Szilvásy‐Szabó, A., Akkuratov, E. E., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38663-7 · Cited by 6 · see citing works
Epidermal Differentiation Genes of the Common Wall Lizard Encode Proteins with Extremely Biased Amino Acid Contents
Holthaus, K. B., Sachslehner, A. P., Steinbinder, J., & Eckhart, L. (2024) · Genes · doi:10.3390/genes15091136 · Cited by 6 · see citing works
Self-citation
Late cornified envelope 1C (LCE1C), a transcriptional target of TAp63 phosphorylated at T46/T281, interacts with PRMT5
Yabuta, N., Ota, C., Sasakura, T., Naito, Y., Okuzaki, D., Fukushima, K., & Nojima, H. (2018) · Scientific Reports · doi:10.1038/s41598-018-23045-7 · Cited by 6 · see citing works
Alpha-Keratin, Keratin-Associated Proteins and Transglutaminase 1 Are Present in the Ortho- and Parakeratinized Epithelium of the Avian Tongue
Skieresz‐Szewczyk, K., Jackowiak, H., & Skrzypski, M. (2022) · Cells · doi:10.3390/cells11121899 · Cited by 5 · see citing works
Scales of non-avian reptiles and their derivatives contain corneous beta proteins coded from genes localized in the Epidermal Differentiation Complex
Alibardi, L. (2023) · Tissue and Cell · doi:10.1016/j.tice.2023.102228 · Cited by 5 · see citing works
Self-citation
Immunolocalization of loricrin in the maturing α‐layer of normal and regenerating epidermis of the lizardAnolis carolinensis
Alibardi, L., Strasser, B., & Eckhart, L. (2015) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22610 · Cited by 5 · see citing works
Self-citation
Unique pattern of histogenesis of the parakeratinized epithelium on lingual prominence in the domestic goose embryos (Anser anser f. domestica)
Skieresz‐Szewczyk, K., Jackowiak, H., & Ratajczak, M. (2021) · Scientific Reports · doi:10.1038/s41598-021-02020-9 · Cited by 4 · see citing works
Epidermal cell cultures from white and green sturgeon (Acipenser transmontanus and medirostris): Expression of TGM1-like transglutaminases and CYP4501A
Karim, N., Lin, L.-W., Eenennaam, J. P. V., Fangue, N. A., Schreier, A. D., Phillips, M. A., & Rice, R. H. (2022) · PLoS ONE · doi:10.1371/journal.pone.0265218 · Cited by 4 · see citing works
Self-citation
Disulfide-bond-mediated cross-linking of corneous beta-proteins in lepidosaurian epidermis
Holthaus, K. B., & Alibardi, L. (2017) · Zoology · doi:10.1016/j.zool.2017.10.004 · Cited by 4 · see citing works
Self-citation
The Animals
Ligrone, R. (2019) · Springer eBooks · doi:10.1007/978-3-030-16057-9_10 · Cited by 3 · see citing works
Transcriptomic characterization of transitioning cell types in the skin of Atlantic salmon
Daniels, R. R., Salisbury, S. J., Sveen, L. R., Villamayor, P. R., Taylor, R. S., Vaadal, M., Tengs, T., Krasnov, A., Monaghan, S. J., Ballantyne, M., et al. (2025) · BMC Biology · doi:10.1186/s12915-025-02196-w · Cited by 3 · see citing works
Immunolabeling for filaggrin and acidic keratins in the granular layer of mammalian epidermis indicates that an acidic-basic interaction is involved in cornification
Alibardi, L. (2024) · Tissue and Cell · doi:10.1016/j.tice.2024.102397 · Cited by 3 · see citing works
Self-citation

The process of cornification evolved from the initial keratinization in the epidermis and epidermal derivatives of vertebrates: a new synthesis and the case of sauropsids
(2016) · International Review of Cell and Molecular Biology · doi:10.1016/bs.ircmb.2016.06.005 · Cited by 64 · see citing works
Self-citation
Evolution of an amphibian-specific family of epidermal differentiation-associated genes
Sachslehner, A. P., Steinbinder, J., Wagner, A., Kratochwill, K., & Eckhart, L. (2026) · Molecular Biology and Evolution · doi:10.1093/molbev/msag196
Self-citation
Sauropsids Cornification is Based on Corneous Beta‐Proteins, a Special Type of Keratin‐Associated Corneous Proteins of the Epidermis
Alibardi, L. (2016) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22689 · Cited by 30 · see citing works
Self-citation
125 Comparative genomics suggests evolutionary adaptations of epidermal differentiation in squamate reptiles
Holthaus, K. B., Mlitz, V., Strasser, B., Alibardi, L., Tschachler, E., & Eckhart, L. (2016) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2016.06.143
Self-citation
Complex Gene Loss and Duplication Events Have Facilitated the Evolution of Multiple Loricrin Genes in Diverse Bird Species
Davis, A. C., Greenwold, M. J., & Sawyer, R. H. (2019) · Genome Biology and Evolution · doi:10.1093/gbe/evz054 · Cited by 14 · see citing works

Authors: Strasser, B., Mlitz, V., Hermann, M., Rice, R. H., Eigenheer, R. A., Alibardi, L., Tschachler, E., & Eckhart, L.
Affiliations: Medical University of Vienna (AT)
University of California, Davis (US)
University of Bologna (IT)
Corresponding author: Eckhart, Leopold
ORCID: Mlitz, Veronika
Hermann, Marcela
Rice, Robert H.
Alibardi, Lorenzo
Tschachler, Erwin
Eckhart, Leopold
Venue: Molecular Biology and Evolution
Publisher: Oxford University Press (OUP)
Published: 2014-08-27
Volume: 31
Issue: 12
Pages: 3194-3205
ISSN: 0737-4038 (ISSN-L)
1537-1719
DOI: 10.1093/molbev/msu251
PMC: PMC4245816
OpenAlex: W2125050942
Cited by: 135
References: 56
Citations by year: 2026: 4 · 2025: 9 · 2024: 14 · 2023: 10 · 2022: 14 · 2021: 16 · 2020: 9 · 2019: 10 · 2018: 16 · 2017: 10 · 2016: 12 · 2015: 9 · 2014: 2
FWCI: 5.48
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
Locations: Molecular Biology and Evolution (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by)
Funders: Austrian Science Fund (P23801)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Skin and Cellular Biology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: epidermal differentiation complex, keratinization, amniote evolution, loricrin, beta-keratin, peptidoglycan recognition proteins, gene fusion, chickens, skin appendages, exon-intron structure, comparative genomics
MeSH terms: Animals, Chickens, Epidermis, Keratins, Molecular Sequence Data, Organ Specificity, Reptiles, Transcription, Genetic, Keratinocytes, Sequence Analysis, DNA, Evolution, Molecular, Amino Acid Motifs, Gene Expression Profiling, Avian Proteins, Reptilian Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Evolutionary origin and diversification of epidermal barrier proteins in amniotes

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks