Gentamicin induces LAMB3 nonsense mutation readthrough and restores functional laminin 332 in junctional epidermolysis bullosa

Proc Natl Acad Sci U S A. 2018 Jul 10;115(28):E6536-E6545. doi: 10.1073/pnas.1803154115. Epub 2018 Jun 26.

Abstract

Herlitz junctional epidermolysis bullosa (H-JEB) is an incurable, devastating, and mostly fatal inherited skin disease for which there is only supportive care. H-JEB is caused by loss-of-function mutations in LAMA3, LAMB3, or LAMC2, leading to complete loss of laminin 332, the major component of anchoring filaments, which mediate epidermal-dermal adherence. LAMB3 (laminin β3) mutations account for 80% of patients with H-JEB, and ∼95% of H-JEB-associated LAMB3 mutations are nonsense mutations leading to premature termination codons (PTCs). In this study, we evaluated the ability of gentamicin to induce PTC readthrough in H-JEB laminin β3-null keratinocytes transfected with expression vectors encoding eight different LAMB3 nonsense mutations. We found that gentamicin induced PTC readthrough in all eight nonsense mutations tested. We next used lentiviral vectors to generate stably transduced H-JEB cells with the R635X and C290X nonsense mutations. Incubation of these cell lines with various concentrations of gentamicin resulted in the synthesis and secretion of full-length laminin β3 in a dose-dependent and sustained manner. Importantly, the gentamicin-induced laminin β3 led to the restoration of laminin 332 assembly, secretion, and deposition within the dermal/epidermal junction, as well as proper polarization of α6β4 integrin in basal keratinocytes, as assessed by immunoblot analysis, immunofluorescent microscopy, and an in vitro 3D skin equivalent model. Finally, newly restored laminin 332 corrected the abnormal cellular phenotype of H-JEB cells by reversing abnormal cell morphology, poor growth potential, poor cell-substratum adhesion, and hypermotility. Therefore, gentamicin may offer a therapy for H-JEB and other inherited skin diseases caused by PTC mutations.

Keywords: epidermolysis bullosa; gentamicin; readthrough.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Cell Adhesion Molecules* / genetics
  • Cell Adhesion Molecules* / metabolism
  • Codon, Nonsense*
  • Epidermolysis Bullosa, Junctional* / genetics
  • Epidermolysis Bullosa, Junctional* / metabolism
  • Epidermolysis Bullosa, Junctional* / pathology
  • Gentamicins / pharmacology*
  • HEK293 Cells
  • Humans
  • Integrin alpha6beta4 / genetics
  • Integrin alpha6beta4 / metabolism
  • Kalinin
  • Keratinocytes / metabolism*
  • Keratinocytes / pathology
  • Mutagenesis / drug effects*

Substances

  • Cell Adhesion Molecules
  • Codon, Nonsense
  • Gentamicins
  • Integrin alpha6beta4