Epithelial proliferation in inflammatory skin disease is regulated by tetratricopeptide repeat domain 7 (Ttc7) in fibroblasts and lymphocytes

J Allergy Clin Immunol. 2019 Jan;143(1):292-304.e8. doi: 10.1016/j.jaci.2018.02.057. Epub 2018 Jun 14.

Abstract

Background: Mutations in tetratricopeptide repeat domain 7A (TTC7A) and its mouse orthologue, Ttc7, result in a multisystemic disease, mostly affecting the epithelial barriers and immune system. Despite successful hematopoietic stem cell transplantation, ongoing progression of gastrointestinal manifestations can be life-threatening in TTC7A-deficient patients.

Objective: We sought to identify whether TTC7A mutations dysregulate epithelial cells only or whether a cell-intrinsic defect in lymphocytes or other cells contributes to disease manifestations.

Methods: Ttc7-mutated (Ttc7fsn/fsn) mice were crossed to generate double-mutant (Rag2-/-Ttc7fsn/fsn) and triple-mutant (Rag2-/-IL2rg-/-Ttc7fsn/fsn) mice. These models, together with bone marrow chimeras, were used to explore the role of adaptive and innate lymphocytes in the flaky skin phenotype. The effect of the Ttc7fsn/fsn mutation on stromal cells was tested in a xenograft model in conjunction with transcriptomic analysis of Ttc7fsn/fsn fibroblasts.

Results: We observed that the severity of epithelial hyperproliferation was accentuated by lymphocytes, whereas the phenotype was not induced by transfer of Ttc7-mutated hematopoietic cells. Furthermore, mice completely lacking the lymphocytic compartment were not protected from epithelial hyperproliferation. Ttc7-mutated mouse fibroblasts expressed increased transcript levels of insulin-like growth factor 1 (Igf1) and the antimicrobial protein regenerating islet-derived protein 3γ (Reg3γ). In a xenograft model Ttc7-mutated fibroblasts markedly increased epithelial proliferation of keratinocytes. Thus Ttc7-mutated fibroblasts were identified as potent instigators of epithelial hyperproliferation.

Conclusion: Our results reveal a previously unsuspected fundamental cell-extrinsic role of Ttc7. We have identified potential candidates for molecularly targeted treatment strategies that will need to be evaluated in future preclinical studies.

Keywords: Primary immunodeficiency; TTC7A mutation; fibroblasts; mouse model; psoriasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • BALB 3T3 Cells
  • Cell Proliferation*
  • Dermatitis / genetics
  • Dermatitis / immunology*
  • Dermatitis / pathology
  • Epithelial Cells / immunology*
  • Epithelial Cells / pathology
  • Fibroblasts / immunology*
  • Fibroblasts / pathology
  • Genetic Diseases, Inborn / genetics
  • Genetic Diseases, Inborn / immunology*
  • Genetic Diseases, Inborn / pathology
  • Humans
  • Lymphocytes / immunology*
  • Lymphocytes / pathology
  • Mice
  • Mice, Knockout
  • Mutation*
  • Proteins / genetics
  • Proteins / immunology*

Substances

  • Proteins
  • TTC7 protein, mouse
  • TTC7A protein, human