Novel Corrector for Variants of SLC6A8: A Therapeutic Opportunity for Creatine Transporter Deficiency

Mutations in creatine transporter SLC6A8 cause creatine transporter deficiency (CTD), which is responsible for 2% of all cases of X-linked intellectual disability. CTD has no current treatments and has a high unmet medical need. Inspired by the transformational therapeutic impact of small molecule "correctors" for the treatment of cystic fibrosis, which bind to mutated versions of the CFTR ion channel to promote its trafficking to the cell surface, we sought to identify small molecules that could stabilize SLC6A8 as a potential treatment for CTD. We leveraged a novel chemoproteomic technology for ligand discovery, reactive affinity probe interaction discovery, to identify small-molecule fragments with photoaffinity handles that bind to SLC6A8 in a cellular environment. We synthesized a library of irreversible covalent analogs of these molecules to characterize in functional assays, which revealed molecules that could promote the trafficking of mutant SLC6A8 variants to the cell surface. Further medicinal chemistry was able to identify reversible drug-like small molecules that both promoted trafficking of the transporter and also rescued creatine uptake. When profiled across the 27 most prevalent SLC6A8 missense variants, we found that 10-20% of patient mutations were amenable to correction by our molecules. These results were verified in an endogenous setting using the CRISPR knock-in of selected missense alleles. We established in vivo proof-of-mechanism for correctors in a novel CTD mouse model with the P544L patient-defined variant knocked in to the SLC6A8 locus, where treatment with our orally bioavailable and brain penetrant tool corrector increased brain creatine levels in heterozygous female mice, validating correctors as a potential therapeutic approach for CTD.

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Publication Details

Journal
ACS Chemical Biology
Published
2024-10-17
DOI
https://doi.org/10.1021/acschembio.4c00571
Citations
7
Primary Topic
Cystic Fibrosis Research Advances
Type
article
Field-Weighted Citation Impact
2.93
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article

Novel Corrector for Variants of SLC6A8: A Therapeutic Opportunity for Creatine Transporter Deficiency

Lyn H. Jones, T.J. Rettenmaier, Chloe Deshusses, Leslie Conway et al.
7 citations
ACS Chemical Biology
Cystic Fibrosis Research Advances
2.93
article

Novel Corrector for Variants of SLC6A8: A Therapeutic Opportunity for Creatine Transporter Deficiency

Lyn H. Jones, T.J. Rettenmaier, Chloe Deshusses, Leslie Conway, Giuseppina Iantosca, Benjamin Rabin, Lara Gechijian, William J. Crotty, Matthew Lyons, Matthew Labenski, Victor Rusu, Joel C. Barrish, Heather Blanchette, Giovanni Muncipinto, Nick Pullen, Nicholas J. Brandon, Dean G. Brown, Christina Westgate, Daniel van Kalken, Hyejin Park, R I Mathis, Liam Gross, Lea Rosskamp
article en
7 citations

Abstract

Mutations in creatine transporter SLC6A8 cause creatine transporter deficiency (CTD), which is responsible for 2% of all cases of X-linked intellectual disability. CTD has no current treatments and has a high unmet medical need. Inspired by the transformational therapeutic impact of small molecule "correctors" for the treatment of cystic fibrosis, which bind to mutated versions of the CFTR ion channel to promote its trafficking to the cell surface, we sought to identify small molecules that could stabilize SLC6A8 as a potential treatment for CTD. We leveraged a novel chemoproteomic technology for ligand discovery, reactive affinity probe interaction discovery, to identify small-molecule fragments with photoaffinity handles that bind to SLC6A8 in a cellular environment. We synthesized a library of irreversible covalent analogs of these molecules to characterize in functional assays, which revealed molecules that could promote the trafficking of mutant SLC6A8 variants to the cell surface. Further medicinal chemistry was able to identify reversible drug-like small molecules that both promoted trafficking of the transporter and also rescued creatine uptake. When profiled across the 27 most prevalent SLC6A8 missense variants, we found that 10-20% of patient mutations were amenable to correction by our molecules. These results were verified in an endogenous setting using the CRISPR knock-in of selected missense alleles. We established in vivo proof-of-mechanism for correctors in a novel CTD mouse model with the P544L patient-defined variant knocked in to the SLC6A8 locus, where treatment with our orally bioavailable and brain penetrant tool corrector increased brain creatine levels in heterozygous female mice, validating correctors as a potential therapeutic approach for CTD.

ACS Chemical BiologyVol. 19(11)
University of North Carolina at Chapel Hill (US), Brigham and Women's Hospital (US), Oregon State University (US), Harvard University (US), University of California, San Francisco (US), Harmonic (United States) (US), New England Research Institutes (US), Jnana Therapeutics (United States) (US), Dana-Farber Cancer Institute (US), BG Medicine (United States) (US), Apple (United States) (US)
Zero hunger
Openalex Percentile: Top 8%
Cystic Fibrosis Research Advances
2.93
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