BTK regulates microglial function and neuroinflammation in human stem cell models and mouse models of multiple sclerosis

Nat Commun. 2024 Nov 22;15(1):10116. doi: 10.1038/s41467-024-54430-8.

Abstract

Neuroinflammation in the central nervous system (CNS), driven largely by resident phagocytes, has been proposed as a significant contributor to disability accumulation in multiple sclerosis (MS) but has not been addressed therapeutically. Bruton's tyrosine kinase (BTK) is expressed in both B-lymphocytes and innate immune cells, including microglia, where its role is poorly understood. BTK inhibition may provide therapeutic benefit within the CNS by targeting adaptive and innate immunity-mediated disease progression in MS. Using a CNS-penetrant BTK inhibitor (BTKi), we demonstrate robust in vivo effects in mouse models of MS. We further identify a BTK-dependent transcriptional signature in vitro, using the BTKi tolebrutinib, in mouse microglia, human induced pluripotent stem cell (hiPSC)-derived microglia, and a complex hiPSC-derived tri-culture system composed of neurons, astrocytes, and microglia, revealing modulation of neuroinflammatory pathways relevant to MS. Finally, we demonstrate that in MS tissue BTK is expressed in B-cells and microglia, with increased levels in lesions. Our data provide rationale for targeting BTK in the CNS to diminish neuroinflammation and disability accumulation.

MeSH terms

  • Agammaglobulinaemia Tyrosine Kinase* / antagonists & inhibitors
  • Agammaglobulinaemia Tyrosine Kinase* / genetics
  • Agammaglobulinaemia Tyrosine Kinase* / metabolism
  • Animals
  • Astrocytes / metabolism
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • Disease Models, Animal*
  • Encephalomyelitis, Autoimmune, Experimental / genetics
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Female
  • Humans
  • Induced Pluripotent Stem Cells* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microglia* / metabolism
  • Multiple Sclerosis* / genetics
  • Multiple Sclerosis* / immunology
  • Multiple Sclerosis* / metabolism
  • Multiple Sclerosis* / pathology
  • Neuroinflammatory Diseases / immunology
  • Neuroinflammatory Diseases / metabolism

Substances

  • Agammaglobulinaemia Tyrosine Kinase
  • Btk protein, mouse
  • BTK protein, human