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Evaluating protein cross-linking as a therapeutic strategy to stabilize SOD1 variants in a mouse model of familial ALS.
Hossain, Md Amin; Sarin, Richa; Donnelly, Daniel P; Miller, Brandon C; Weiss, Alexandra; McAlary, Luke; Antonyuk, Svetlana V; Salisbury, Joseph P; Amin, Jakal; Conway, Jeremy B; Watson, Samantha S; Winters, Jenifer N; Xu, Yu; Alam, Novera; Brahme, Rutali R; Shahbazian, Haneyeh; Sivasankar, Durgalakshmi; Padmakumar, Swathi; Sattarova, Aziza; Ponmudiyan, Aparna C; Gawde, Tanvi; Verrill, David E; Yang, Wensheng; Kannapadi, Sunanda; Plant, Leigh D; Auclair, Jared R; Makowski, Lee; Petsko, Gregory A; Ringe, Dagmar; Agar, Nathalie Y R; Greenblatt, David J; Ondrechen, Mary Jo; Chen, Yunqiu; Yerbury, Justin J; Manetsch, Roman; Hasnain, S Samar; Brown, Robert H; Agar, Jeffrey N.
Afiliación
  • Hossain MA; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Sarin R; Barnett Institute of Chemical and Biological Analysis, Boston, Massachusetts, United States of America.
  • Donnelly DP; Department of Neurosurgery and Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, United States of America.
  • Miller BC; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Weiss A; Biogen Inc, Cambridge, Massachusetts, United States of America.
  • McAlary L; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Antonyuk SV; Barnett Institute of Chemical and Biological Analysis, Boston, Massachusetts, United States of America.
  • Salisbury JP; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Amin J; Department of Neurology, University of Massachusetts Medical School, Worcester, Massachusetts, United States of America.
  • Conway JB; Molecular Horizons and School of Chemistry and Molecular Bioscience, University of Wollongong, Wollongong, Australia.
  • Watson SS; Molecular Biophysics Group, Department of Biochemistry & Systems Biology, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, United Kingdom.
  • Winters JN; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Xu Y; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Alam N; Barnett Institute of Chemical and Biological Analysis, Boston, Massachusetts, United States of America.
  • Brahme RR; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Shahbazian H; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Sivasankar D; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Padmakumar S; Department of Pharmaceutical Sciences, Northeastern University, Boston, Massachusetts, United States of America.
  • Sattarova A; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Ponmudiyan AC; Barnett Institute of Chemical and Biological Analysis, Boston, Massachusetts, United States of America.
  • Gawde T; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Verrill DE; Barnett Institute of Chemical and Biological Analysis, Boston, Massachusetts, United States of America.
  • Yang W; School of Medicine, University of North Carolina, Chapel Hill, North Carolina, United States of America.
  • Kannapadi S; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Plant LD; Barnett Institute of Chemical and Biological Analysis, Boston, Massachusetts, United States of America.
  • Auclair JR; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Makowski L; Department of Pharmaceutical Sciences, Northeastern University, Boston, Massachusetts, United States of America.
  • Petsko GA; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Ringe D; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Agar NYR; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Greenblatt DJ; Barnett Institute of Chemical and Biological Analysis, Boston, Massachusetts, United States of America.
  • Ondrechen MJ; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Chen Y; Barnett Institute of Chemical and Biological Analysis, Boston, Massachusetts, United States of America.
  • Yerbury JJ; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Manetsch R; Department of Pharmaceutical Sciences, Northeastern University, Boston, Massachusetts, United States of America.
  • Hasnain SS; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
  • Brown RH; Barnett Institute of Chemical and Biological Analysis, Boston, Massachusetts, United States of America.
  • Agar JN; Department of Chemistry and Chemical Biology, Northeastern University, Boston, Massachusetts, United States of America.
PLoS Biol ; 22(1): e3002462, 2024 Jan.
Article en En | MEDLINE | ID: mdl-38289969
ABSTRACT
Mutations in the gene encoding Cu-Zn superoxide dismutase 1 (SOD1) cause a subset of familial amyotrophic lateral sclerosis (fALS) cases. A shared effect of these mutations is that SOD1, which is normally a stable dimer, dissociates into toxic monomers that seed toxic aggregates. Considerable research effort has been devoted to developing compounds that stabilize the dimer of fALS SOD1 variants, but unfortunately, this has not yet resulted in a treatment. We hypothesized that cyclic thiosulfinate cross-linkers, which selectively target a rare, 2 cysteine-containing motif, can stabilize fALS-causing SOD1 variants in vivo. We created a library of chemically diverse cyclic thiosulfinates and determined structure-cross-linking-activity relationships. A pre-lead compound, "S-XL6," was selected based upon its cross-linking rate and drug-like properties. Co-crystallographic structure clearly establishes the binding of S-XL6 at Cys 111 bridging the monomers and stabilizing the SOD1 dimer. Biophysical studies reveal that the degree of stabilization afforded by S-XL6 (up to 24°C) is unprecedented for fALS, and to our knowledge, for any protein target of any kinetic stabilizer. Gene silencing and protein degrading therapeutic approaches require careful dose titration to balance the benefit of diminished fALS SOD1 expression with the toxic loss-of-enzymatic function. We show that S-XL6 does not share this liability because it rescues the activity of fALS SOD1 variants. No pharmacological agent has been proven to bind to SOD1 in vivo. Here, using a fALS mouse model, we demonstrate oral bioavailability; rapid engagement of SOD1G93A by S-XL6 that increases SOD1G93A's in vivo half-life; and that S-XL6 crosses the blood-brain barrier. S-XL6 demonstrated a degree of selectivity by avoiding off-target binding to plasma proteins. Taken together, our results indicate that cyclic thiosulfinate-mediated SOD1 stabilization should receive further attention as a potential therapeutic approach for fALS.
Asunto(s)

Texto completo: 1 Colección: 01-internacional Base de datos: MEDLINE Asunto principal: Esclerosis Amiotrófica Lateral Límite: Animals Idioma: En Revista: PLoS Biol Asunto de la revista: BIOLOGIA Año: 2024 Tipo del documento: Article País de afiliación: Estados Unidos Pais de publicación: Estados Unidos

Texto completo: 1 Colección: 01-internacional Base de datos: MEDLINE Asunto principal: Esclerosis Amiotrófica Lateral Límite: Animals Idioma: En Revista: PLoS Biol Asunto de la revista: BIOLOGIA Año: 2024 Tipo del documento: Article País de afiliación: Estados Unidos Pais de publicación: Estados Unidos