Lack of cathelicidin processing in Papillon-Lefèvre syndrome patients reveals essential role of LL-37 in periodontal homeostasis

Orphanet J Rare Dis. 2014 Sep 27:9:148. doi: 10.1186/s13023-014-0148-y.

Abstract

Background: Loss-of-function point mutations in the cathepsin C gene are the underlying genetic event in patients with Papillon-Lefèvre syndrome (PLS). PLS neutrophils lack serine protease activity essential for cathelicidin LL-37 generation from hCAP18 precursor.

Aim: We hypothesized that a local deficiency of LL-37 in the infected periodontium is mainly responsible for one of the clinical hallmark of PLS: severe periodontitis already in early childhood.

Methods: To confirm this effect, we compared the level of neutrophil-derived enzymes and antimicrobial peptides in gingival crevicular fluid (GCF) and saliva from PLS, aggressive and chronic periodontitis patients.

Results: Although neutrophil numbers in GCF were present at the same level in all periodontitis groups, LL-37 was totally absent in GCF from PLS patients despite the large amounts of its precursor, hCAP18. The absence of LL-37 in PLS patients coincided with the deficiency of both cathepsin C and protease 3 activities. The presence of other neutrophilic anti-microbial peptides in GCF from PLS patients, such as alpha-defensins, were comparable to that found in chronic periodontitis. In PLS microbial analysis revealed a high prevalence of Aggregatibacter actinomycetemcomitans infection. Most strains were susceptible to killing by LL-37.

Conclusions: Collectively, these findings imply that the lack of protease 3 activation by dysfunctional cathepsin C in PLS patients leads to the deficit of antimicrobial and immunomodulatory functions of LL-37 in the gingiva, allowing for infection with A. actinomycetemcomitans and the development of severe periodontal disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aggregatibacter actinomycetemcomitans / drug effects
  • Antimicrobial Cationic Peptides / metabolism*
  • Antimicrobial Cationic Peptides / pharmacology*
  • Blotting, Western
  • Cathelicidins
  • Cathepsin C / genetics
  • Cathepsin C / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Homeostasis*
  • Humans
  • Leukocyte Elastase / metabolism
  • Myeloblastin / metabolism
  • Papillon-Lefevre Disease / metabolism*
  • Papillon-Lefevre Disease / physiopathology
  • Periodontium / metabolism*
  • Periodontium / microbiology
  • Periodontium / physiopathology
  • Peroxidase / metabolism
  • Point Mutation

Substances

  • Antimicrobial Cationic Peptides
  • Peroxidase
  • Cathepsin C
  • Leukocyte Elastase
  • Myeloblastin
  • Cathelicidins