Topical application of a BCL-2 inhibitor ameliorates imiquimod-induced psoriasiform dermatitis by eliminating senescent cells

J Dermatol Sci. 2024 Aug;115(2):54-63. doi: 10.1016/j.jdermsci.2024.06.002. Epub 2024 Jun 18.

Abstract

Background: Psoriasis is an inflammatory skin disease with unclear pathogenesis and unmet therapeutic needs.

Objective: To investigate the role of senescent CD4+ T cells in psoriatic lesion formation and explore the application of senolytics in treating psoriasis.

Methods: We explored the expression levels of p16INK4a and p21, classical markers of cellular senescence, in CD4+ T cells from human psoriatic lesions and imiquimod (IMQ)-induced psoriatic lesions. We prepared a senolytic gel using B-cell lymphoma 2 (BCL-2) inhibitor ABT-737 and evaluated its therapeutic efficacy in treating psoriasis.

Results: Using multispectrum immunohistochemistry (mIHC) staining, we detected increased expression levels of p16INK4a and p21 in CD4+ T cells from psoriatic lesions. After topical application of ABT-737 gel, significant alleviation of IMQ-induced psoriatic lesions was observed, with milder pathological alterations. Mechanistically, ABT-737 gel significantly decreased the percentage of senescent cells, expression of T cell receptor (TCR) α and β chains, and expression of Tet methylcytosine dioxygenase 2 (Tet2) in IMQ-induced psoriatic lesions, as determined by mIHC, high-throughput sequencing of the TCR repertoire, and RT-qPCR, respectively. Furthermore, the severity of psoriatic lesions in CD4creTet2f/f mice was milder than that in Tet2f/f mice in the IMQ-induced psoriasis model.

Conclusion: We revealed the roles of senescent CD4+ T cells in developing psoriasis and highlighted the therapeutic potential of topical ABT-737 gel in treating psoriasis through the elimination of senescent cells, modulation of the TCR αβ repertoire, and regulation of the TET2-Th17 cell pathway.

Keywords: BCL-2 inhibitor; Cellular senescence; Psoriasis; Senolytics.

MeSH terms

  • Administration, Cutaneous
  • Animals
  • Biphenyl Compounds* / administration & dosage
  • Biphenyl Compounds* / pharmacology
  • Biphenyl Compounds* / therapeutic use
  • CD4-Positive T-Lymphocytes* / drug effects
  • CD4-Positive T-Lymphocytes* / immunology
  • CD4-Positive T-Lymphocytes* / metabolism
  • Cellular Senescence* / drug effects
  • Cyclin-Dependent Kinase Inhibitor p16 / genetics
  • Cyclin-Dependent Kinase Inhibitor p16 / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Dioxygenases*
  • Disease Models, Animal*
  • Female
  • Gels
  • Humans
  • Imiquimod* / administration & dosage
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Nitrophenols* / administration & dosage
  • Nitrophenols* / pharmacology
  • Piperazines* / administration & dosage
  • Piperazines* / pharmacology
  • Proto-Oncogene Proteins / antagonists & inhibitors
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-bcl-2* / genetics
  • Proto-Oncogene Proteins c-bcl-2* / metabolism
  • Psoriasis* / chemically induced
  • Psoriasis* / drug therapy
  • Psoriasis* / immunology
  • Psoriasis* / pathology
  • Senotherapeutics / administration & dosage
  • Senotherapeutics / pharmacology
  • Senotherapeutics / therapeutic use
  • Skin / drug effects
  • Skin / immunology
  • Skin / pathology
  • Sulfonamides* / administration & dosage
  • Sulfonamides* / pharmacology

Substances

  • Imiquimod
  • ABT-737
  • Nitrophenols
  • Sulfonamides
  • Dioxygenases
  • Proto-Oncogene Proteins c-bcl-2
  • Piperazines
  • Biphenyl Compounds
  • DNA-Binding Proteins
  • Proto-Oncogene Proteins
  • Tet2 protein, mouse
  • Senotherapeutics
  • TET2 protein, human
  • Gels
  • Cyclin-Dependent Kinase Inhibitor p16
  • BCL2 protein, human