An allosteric MALT1 inhibitor is a molecular corrector rescuing function in an immunodeficient patient

Nat Chem Biol. 2019 Mar;15(3):304-313. doi: 10.1038/s41589-018-0222-1. Epub 2019 Jan 28.

Abstract

MALT1 paracaspase is central for lymphocyte antigen-dependent responses including NF-κB activation. We discovered nanomolar, selective allosteric inhibitors of MALT1 that bind by displacing the side chain of Trp580, locking the protease in an inactive conformation. Interestingly, we had previously identified a patient homozygous for a MALT1 Trp580-to-serine mutation who suffered from combined immunodeficiency. We show that the loss of tryptophan weakened interactions between the paracaspase and C-terminal immunoglobulin MALT1 domains resulting in protein instability, reduced protein levels and functions. Upon binding of allosteric inhibitors of increasing potency, we found proportionate increased stabilization of MALT1-W580S to reach that of wild-type MALT1. With restored levels of stable MALT1 protein, the most potent of the allosteric inhibitors rescued NF-κB and JNK signaling in patient lymphocytes. Following compound washout, MALT1 substrate cleavage was partly recovered. Thus, a molecular corrector rescues an enzyme deficiency by substituting for the mutated residue, inspiring new potential precision therapies to increase mutant enzyme activity in other deficiencies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Gene Expression Regulation
  • Humans
  • Immunologic Deficiency Syndromes / genetics
  • Immunologic Deficiency Syndromes / therapy
  • Lymphocytes / metabolism
  • MAP Kinase Signaling System / genetics
  • MAP Kinase Signaling System / physiology
  • Male
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein / antagonists & inhibitors*
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein / genetics
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein / metabolism*
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein / ultrastructure
  • NF-kappa B / metabolism
  • Neoplasm Proteins
  • Signal Transduction

Substances

  • NF-kappa B
  • Neoplasm Proteins
  • MALT1 protein, human
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein