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Immunogenetics

, Volume 71, Issue 5–6, pp 363–372 | Cite as

Convergent inactivation of the skin-specific C-C motif chemokine ligand 27 in mammalian evolution

  • Mónica Lopes-MarquesEmail author
  • Luís Q. Alves
  • Miguel M. Fonseca
  • Giulia Secci-Petretto
  • André M. Machado
  • Raquel RuivoEmail author
  • L. Filipe C. CastroEmail author
Original Article
  • 32 Downloads

Abstract

The appearance of mammalian-specific skin features was a key evolutionary event contributing for the elaboration of physiological processes such as thermoregulation, adequate hydration, locomotion, and inflammation. Skin inflammatory and autoimmune processes engage a population of skin-infiltrating T cells expressing a specific C-C chemokine receptor (CCR10) which interacts with an epidermal CC chemokine, the skin-specific C-C motif chemokine ligand 27 (CCL27). CCL27 is selectively produced in the skin by keratinocytes, particularly upon inflammation, mediating the adhesion and homing of skin-infiltrating T cells. Here, we examined the evolution and coding condition of Ccl27 in 112 placental mammalian species. Our findings reveal that a number of open reading frame inactivation events such as insertions, deletions, and start and stop codon mutations independently occurred in Cetacea, Pholidota, Sirenia, Chiroptera, and Rodentia, totalizing 18 species. The diverse habitat settings and lifestyles of Ccl27-eroded lineages probably implied distinct evolutionary triggers rendering this gene unessential. For example, in Cetacea, the rapid renewal of skin layers minimizes the need for an elaborate inflammatory mechanism, mirrored by the absence of epidermal scabs. Our findings suggest that the convergent and independent loss of Ccl27 in mammalian evolution concurred with unique adaptive roads for skin physiology.

Keywords

Chemokines Gene loss Skin Inflammation 

Notes

Funding information

This work was supported by Project No. 031342 co-financed by COMPETE 2020, Portugal 2020, and the European Union through the ERDF, and by FCT through national funds.

Supplementary material

251_2019_1114_MOESM1_ESM.pdf (80 kb)
Supplementary Material 1: Phylogeny calculated with HKY85 +G+I modelusing 92 nucleotide sequences translation aligned, 396 position and branch support posterior probabilities were determined using aBayes. Species acronyms are available in corresponding Supplementary Table 1. (PDF 79.6 kb)
251_2019_1114_MOESM2_ESM.pdf (1.3 mb)
Supplementary Material 2: SSRA Validation of identified mutations in cetacea. (PDF 1.29 mb)
251_2019_1114_MOESM3_ESM.pdf (15 kb)
Supplementary Material 3: Sequence alignment of Ccl27 exon 3 from Cetacea, H. amphibius and H. sapiens. (PDF 14.9 kb)
251_2019_1114_MOESM4_ESM.pdf (397 kb)
Supplementary Material 4: SRA validation of inactivating mutations of Ccl27 transcripts in Cetacea. (PDF 396 kb)
251_2019_1114_MOESM5_ESM.pdf (565 kb)
Supplementary Material 5: SRA Validation of identified mutations in other mammals. (PDF 565 kb)
251_2019_1114_MOESM6_ESM.pdf (149 kb)
Supplementary Material 6 Analysis of the coding status of Ccr10 in species with Ccl27 pseudogenes. (PDF 149 kb)
251_2019_1114_MOESM7_ESM.docx (41 kb)
Supplementary Table 1 Accession numbers of the analysed sequences * tagged low-quality, a assembled genomes without annotation. (DOCX 40.6 kb)
251_2019_1114_MOESM8_ESM.docx (32 kb)
Supplementary Table 2: In-depth description of the available transcriptomic NCBI sequence read archive (SRA) projects, scrutinized in the transcriptomic analysis of the 6 represented cetaceans. (DOCX 31.7 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Mónica Lopes-Marques
    • 1
    Email author
  • Luís Q. Alves
    • 1
    • 2
  • Miguel M. Fonseca
    • 1
  • Giulia Secci-Petretto
    • 1
    • 2
  • André M. Machado
    • 1
    • 2
  • Raquel Ruivo
    • 1
    Email author
  • L. Filipe C. Castro
    • 1
    • 2
    Email author
  1. 1.CIIMAR-UPMatosinhosPortugal
  2. 2.Department of BiologyFaculty of SciencesPortoPortugal

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