Skip to main content

Evolution of Trichocyte Keratins

  • Chapter
  • First Online:
The Hair Fibre: Proteins, Structure and Development

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1054))

Abstract

The evolution of keratins was closely linked to the evolution of epithelia and epithelial appendages such as hair. The characterization of keratins in model species and recent comparative genomics studies have led to a comprehensive scenario for the evolution of keratins including the following key events. The primordial keratin gene originated as a member of the ancient gene family encoding intermediate filament proteins. Gene duplication and changes in the exon-intron structure led to the origin of type I and type II keratins which evolved further by nucleotide sequence modifications that affected both the amino acid sequences of the encoded proteins and the gene expression patterns. The diversification of keratins facilitated the emergence of new and epithelium type-specific properties of the cytoskeleton. In a common ancestor of reptiles, birds, and mammals, a rise in the number of cysteine residues facilitated extensive disulfide bond-mediated cross-linking of keratins in claws. Subsequently, these cysteine-rich keratins were co-opted for an additional function in epidermal follicular structures that evolved into hair, one of the key events in the evolution of mammals. Further diversification of keratins occurred during the evolution of the complex multi-layered organisation of hair follicles. Thus, together with the evolution of other structural proteins, epithelial patterning mechanisms, and development programmes, the evolution of keratins underlied the evolution of the mammalian integument.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Ng, C. S., et al. (2012). The chicken frizzle feather is due to an alpha-keratin (KRT75) mutation that causes a defective rachis. PLoS Genetics, 8, e1002748.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Gandolfi, B., et al. (2013). A splice variant in KRT71 is associated with curly coat phenotype of Selkirk Rex cats. Scientific Reports, 3, 2000.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Taylor, J. S., & Raes, J. (2004). Duplication and divergence: The evolution of new genes and old ideas. Annual Review of Genetics, 38, 615–643.

    Article  CAS  PubMed  Google Scholar 

  4. Innan, H. K. F. (2010). The evolution of gene duplications: classifying and distinguishing between models. National Review of Genetics, 11, 97–108.

    Article  CAS  Google Scholar 

  5. Andersson, D. I., Jerlström-Hultqvist, J., & Näsvall, J. (2015). Evolution of new functions de novo and from preexisting genes. Cold Spring Harbour Perspectives in Biology, 7(pii: a017996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Arguello, J. R., et al. (2007). Origination of chimeric genes through DNA-level recombination. Genome Dynamics, 3, 131–146.

    Article  CAS  PubMed  Google Scholar 

  7. Ohno, S. (1970). Evolution by gene duplication. Berlin: Springer.

    Book  Google Scholar 

  8. Strasser, B., et al. (2014). Evolutionary origin and diversification of epidermal barrier proteins in amniotes. Molecular Biology and Evolution, 31, 3194–3205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Alibardi, L. (2016). 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. International Review of Cell and Molecular Biology, 327, 263–319.

    Google Scholar 

  10. Peter, A., & Stick, R. (2015). Evolutionary aspects in intermediate filament proteins. Current Opinion in Cell Biology, 32, 48–55.

    Article  CAS  PubMed  Google Scholar 

  11. Riemer, D., Karabinos, A., & Weber, K. (1998). Analysis of eight cDNAs and six genes for intermediate filament (IF) proteins in the cephalochordate Branchiostoma reveals differences in the IF multigene families of lower chordates and the vertebrates. Genetic Research, 211, 361–373.

    CAS  Google Scholar 

  12. Zimek, A., & Weber, K. (2005). Terrestrial vertebrates have two keratin gene clusters; Striking differences in teleost fish. European Journal of Cell Biology, 84, 623–635.

    Article  CAS  PubMed  Google Scholar 

  13. Strasser, B., et al. (2015). Convergent evolution of cysteine-rich proteins in feathers and hair. BMC Evolutionary Biology, 15, 82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Dodemont, H., Riemer, D., & Weber, K. (1990). Structure of an invertebrate gene encoding cytoplasmic intermediate filament (IF) proteins: Implications for the origin and the diversification of IF proteins. EMBO Journal, 9, 4083–4094.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Schaffeld, M., Höffling, S., & Jürgen, M. (2004). Sequence, evolution and tissue expression patterns of an epidermal type I keratin from the shark Scyliorhinus stellaris. European Journal of Cell Biology, 83, 359–368.

    Article  CAS  PubMed  Google Scholar 

  16. Lane, E. B., & McLean, W. H. (2004). Keratins and skin disorders. The Journal of Pathology, 204, 355–366.

    Article  CAS  PubMed  Google Scholar 

  17. Schweizer, J., et al. (2007). Hair follicle-specific keratins and their diseases. Experimental Cell Research, 313, 2010–2020.

    Article  CAS  PubMed  Google Scholar 

  18. Strnad, P., et al. (2011). Unique amino acid signatures that are evolutionarily conserved distinguish simple-type, epidermal and hair keratins. Journal of Cell Science, 124, 4221–4232.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Toivola, D. M., et al. (2015). Keratins in health and disease. Current Opinion in Cell Biology, 32, 73–81.

    Article  CAS  PubMed  Google Scholar 

  20. Coulombe, P. A. (2017). The molecular revolution in cutaneous biology: Keratin genes and their associated disease: Diversity, opportunities, and challenges. The Journal of Investigative Dermatology, 137, e67-e71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Parry, D. A. D., & Steinert, P. M. (1999). Intermediate filaments: Molecular architecture, assembly, dynamics and polymorphism. Quarterly Reviews of Biophysics, 32, 99–187.

    Article  CAS  PubMed  Google Scholar 

  22. Badowski, C., et al. (2017). Modeling the structure of keratin 1 and 10 terminal domains and their misassembly in keratoderma. Journal of Investigative Dermatology, 137, 1914–1923.

    Article  CAS  PubMed  Google Scholar 

  23. Eckhart, L., et al. (2008). Identification of reptilian genes encoding hair keratin-like proteins suggests a new scenario for the evolutionary origin of hair. Proceedings of the National Academy of Sciences of the United States of America, 105, 18419–18423.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Eckhart, L., Jaeger, K., & Tschachler, E. (2009). The tail domains of keratins contain conserved amino acid sequence motifs. Journal of Dermatological Science, 54, 208–209.

    Article  CAS  PubMed  Google Scholar 

  25. Moll, R., Divo, M., & Langbein, L. (2008). The human keratins: Biology and pathology. Histochemistry and Cell Biology, 129, 705–733.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Bragulla, H. H., & Homberger, D. G. (2009). Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. Journal of Anatomy, 214, 516–559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Eckert, R. L., et al. (1997). The epidermis: Genes on – Genes off. Journal of Investigative Dermatology, 109, 501–509.

    Article  CAS  PubMed  Google Scholar 

  28. Jave-Suarez, L. F., et al. (2002). HOXC13 is involved in the regulation of human hair keratin gene expression. The Journal of Biological Chemistry, 277, 3718–3726.

    Article  CAS  PubMed  Google Scholar 

  29. Gilon, M., et al. (2008). Transcriptional activation of a subset of hair keratin genes by the NF-kappaB effector p65/RelA. Differentiation, 76, 518–530.

    Article  CAS  PubMed  Google Scholar 

  30. Potter, C. S., et al. (2011). The nude mutant gene Foxn1 is a HOXC13 regulatory target during hair follicle and nail differentiation. Journal of Investigative Dermatology, 131, 828–837.

    Article  CAS  PubMed  Google Scholar 

  31. Findeisen, P., et al. (2014). Six subgroups and extensive recent duplications characterize the evolution of the eukaryotic tubulin protein family. Genome Biology and Evolution, 6, 2274–2288.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Nielsen, M. G., Gadagkar, S. R., & Gutzwiller, L. (2010). Tubulin evolution in insects: Gene duplication and subfunctionalization provide specialized isoforms in a functionally constrained gene family. BMC Evolutionary Biology, 10, 113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Langbein, L., et al. (2016). Localisation of keratin K78 in the basal layer and the first suprabasal layers of stratified epithelia completes the expression catalog of type II keratins and provides new insights into sequential keratin expression. Cell and Tissue Research, 363, 735–750.

    Article  CAS  PubMed  Google Scholar 

  34. Dhouailly, D. (2009). A new scenario for the evolutionary origin of hair, feather, and avian scales. Journal of Anatomy, 214, 587–606.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Alibardi, L. (2012). Perspectives on hair evolution based on some comparative studies on vertebrate cornification. Journal of Experimental Zoolology Part B: Molecular Developmental Evolution, 318, 325–343.

    Article  CAS  Google Scholar 

  36. Wagner, G. P. (2014). Homology, genes and evolutionary innovation. Princeton: Princeton University Press.

    Book  Google Scholar 

  37. Perrin, C., Langbein, L., & Schweizer, J. (2004). Expression of hair keratins in the adult nail unit: An immunohistochemical analysis of the onychogenesis in the proximal nail fold, matrix and nail bed. British Journal of Dermatology, 151, 362–371.

    Article  CAS  PubMed  Google Scholar 

  38. Bowden, P. E., Henderson, H., & Reilly, J. D. (2009). Defining the complex epithelia that comprise the canine claw with molecular markers of differentiation. Veterinary Dermatology, 20, 347–359.

    Article  PubMed  Google Scholar 

  39. Carter, R. A., et al. (2010). Novel keratins identified by quantitative proteomic analysis as the major cytoskeletal proteins of equine (Equus caballus) hoof lamellar tissue. Journal of Animal Science, 88, 3843–3855.

    Article  CAS  PubMed  Google Scholar 

  40. Langbein, L., & Schweizer, J. (2005). Keratins of the human hair follicle. International Review of Cytology, 243, 1–78.

    Article  CAS  PubMed  Google Scholar 

  41. Langbein, L., et al. (2001). The catalog of human hair keratins. II. Expression of the six type II members in the hair follicle and the combined catalog of human type I and II keratins. Journal of Biological Chemistry, 276, 35123–35132.

    Article  CAS  PubMed  Google Scholar 

  42. Gomez, C., et al. (2013). The interfollicular epidermis of adult mouse tail comprises two distinct cell lineages that are differentially regulated by Wnt, Edaradd, and Lrig1. Stem Cell Reports, 1, 19–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Solazzo, C., et al. (2013). Characterisation of novel α-keratin peptide markers for species identification in keratinous tissues using mass spectrometry. Rapid Communications in Mass Spectrometry, 27, 2685–2698.

    Article  CAS  PubMed  Google Scholar 

  44. Dhouailly, D., & Sun, T. T. (1989). The mammalian tongue filiform papillae: A theoretical model for primitive hairs. In D. Van Neste, J. M. Lachapelle, & J. L. Antoine (Eds.), Trends in human hair growth and alopecia research (pp. 29–34). Dordrecht: Springer.

    Chapter  Google Scholar 

  45. Maddin, H. C., et al. (2009). The anatomy and development of the claws of Xenopus laevis (Lissamphibia: Anura) reveal alternate pathways of structural evolution in the integument of tetrapods. Journal of Anatomy, 214, 607–619.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Kleinteich, T., & Gorb, S. N. (2016). Frog tongue surface microstructures: Functional and evolutionary patterns. Beilstein Journal of Nanotchnology, 7, 893–903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Alibardi, L. (2003). Adaptation to the land: The skin of reptiles in comparison to that of amphibians and endotherm amniotes. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 298, 12–41.

    Article  Google Scholar 

  48. Vandebergh, W., et al. (2013). Recurrent functional divergence of early tetrapod keratins in amphibian toe pads and mammalian hair. Biology Letters, 9, 20130051.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Suzuki, K. T., et al. (2017). Clustered Xenopus keratin genes: A genomic, transcriptomic, and proteomic analysis. Developmental Biology, 426, 384–392.

    Article  CAS  PubMed  Google Scholar 

  50. Vandebergh, W., & Bossuyt, F. (2012). Radiation and functional diversification of alpha keratins during early vertebrate evolution. Molecular Biology and Evolution, 29, 995–1004.

    Article  CAS  PubMed  Google Scholar 

  51. Mlitz, V., et al. (2014). Trichohyalin-like proteins have evolutionarily conserved roles in the morphogenesis of skin appendages. Journal of Investigative Dermatology, 134, 2685–2692.

    Article  CAS  PubMed  Google Scholar 

  52. Langbein, L., et al. (2013). New facets of keratin K77: Interspecies variations of expression and different intracellular location in embryonic and adult skin of humans and mice. Cell and Tissue Research, 354, 793–812.

    Article  CAS  PubMed  Google Scholar 

  53. Yu, Z., et al. (2011). Annotations of sheep keratin intermediate filament genes and their patterns of expression. Experimental Dermatology, 20, 582–588.

    Article  CAS  PubMed  Google Scholar 

  54. Nery, M. F., Arroyo, J. I., & Opazo, J. C. (2014). Increased rate of hair keratin gene loss in the cetacean lineage. BMC Genomics, 15, 869.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Dhouailly, D., et al. (2017). Getting to the root of scales, feather and hair: As deep as odontodes? Experimental Dermatology. https://doi.org/ 10.1111/exd.13391.

  56. Maderson, P. F. A. (2003). Mammalian skin evolution: A reevaluation. Experimental Dermatology, 12, 233–236.

    Article  CAS  PubMed  Google Scholar 

  57. Sundberg, J. P. (Ed.). (1994). Handbook of mouse mutations with skin and hair abnormalities. Boca Raton: CRC Press.

    Google Scholar 

  58. Langbein, L., et al. (1999). The catalog of human hair keratins. I. Expression of the nine type I members in the hair follicle. Journal of Biological Chemistry, 274, 19874–19884.

    Article  CAS  PubMed  Google Scholar 

  59. Plowman, J. E. (2007). The proteomics of keratin proteins. Journal of Chromatography B, 849, 181–189.

    Article  CAS  Google Scholar 

  60. Yu, Z., et al. (2009). Expression patterns of keratin intermediate filament and keratin associated protein genes in wool follicles. Differentiation, 77(3), 307–316.

    Article  PubMed  Google Scholar 

  61. Winter, H., et al. (2001). Human type I hair keratin pseudogene phihHaA has functional orthologs in the chimpanzee and gorilla: Evidence for recent inactivation of the human gene after the Pan-Homo divergence. Human Genetics, 108, 37–42.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leopold Eckhart .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Eckhart, L., Ehrlich, F. (2018). Evolution of Trichocyte Keratins. In: Plowman, J., Harland, D., Deb-Choudhury, S. (eds) The Hair Fibre: Proteins, Structure and Development. Advances in Experimental Medicine and Biology, vol 1054. Springer, Singapore. https://doi.org/10.1007/978-981-10-8195-8_4

Download citation

Publish with us

Policies and ethics