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Mechanism-free repurposing of drugs for C9orf72-related ALS/FTD using large-scale genomic data

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Başak, Ayşe Nazlı
Bayraktar, Elif
Tunca, Ceren

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Saez-Atienzar S., Souza C.D.S., Chia R., Beal S.N., Lorenzini I., Huang R., Levy J., Burciu C., Ding J., Gibbs J.R., Jones A., Dewan R., Pensato V., Peverelli S., Corrado L., van Vugt J.J.F.A., van Rheenen W., Tunca C., Bayraktar E., Xia M., Baloh R.H., Bowser R., Brady C.B., Brice A., Broach J., Camu W., Chio A., Cooper-Knock J., Cusi D., Drepper C., Drory V.E., Dunckley T.L., Feldman E., Floeter M.K., Fratta P., Gerhard G., Gibson S.B., Glass J.D., Goutman S.A., Hardy J., Harms M.B., Heiman-Patterson T.D., Jansson L., Kirby J., Laaksovirta H., Landers J.E., Landi F., Le Ber I., Lumbroso S., Guissart C., MacGowan D.J., Maragakis N.J., Mora G., Mouzat K., Myllykangas L., Orrell R.W., Ostrow L.W., Pickering-Brown S., Pioro E.P., Pulst S.M., Ravits J.M., Renton A.E., Robberecht W., Rogaeva E., Rothstein J.D., Salvi E., Scholz S.W., Sendtner M., Shaw P.J., Sidle K.C., Simmons Z., Stone D.J., Tienari P.J., Traynor B.J., Trojanowski J.Q., Troncoso J.C., Valori M., Van Damme P., Van Deerlin V.M., Van Den Bosch L., Zinman L., Angelocola S.M., Ausiello F.P., Barberis M., Bartolomei I., Battistini S., Bersano E., Bisogni G., Borghero G., Brunetti M., Cabona C., Calvo A., Canale F., Canosa A., Cantisani T.A., Capasso M., Caponnetto C., Cardinali P., Carrera P., Casale F., Colletti T., Conforti F.L., Conte A., Conti E., Corbo M., Cuccu S., Bella E.D., D'Errico E., DeMarco G., Dubbioso R., Ferrarese C., Ferraro P.M., Filippi M., Fini N., Floris G., Fuda G., Gallone S., Gianferrari G., Giannini F., Grassano M., Greco L., Iazzolino B., Introna A., La Bella V., Lattante S., Lauria G., Liguori R., Logroscino G., Logullo F.O., Lunetta C., Mandich P., Mandrioli J., Manera U., Manganelli F., Marangi G., Marinou K., Marrosu M.G., Martinelli I., Messina S., Moglia C., Monsurrò M.R., Mosca L., Murru M.R., Origone P., Passaniti C., Petrelli C., Petrucci A., Pirisi A., Pozzi S., Pugliatti M., Quattrini A., Ricci C., Riolo G., Riva N., Russo M., Sabatelli M., Salamone P., Salivetto M., Salvi F., Santarelli M., Sbaiz L., Sideri R., Simone I., Simonini C., Spataro R., Tanel R., Tedeschi G., Ticca A., Torriello A., Tranquilli S., Tremolizzo L., Trojsi F., Vasta R., Vacchiano V., Vita G., Volanti P., Zollino M., Zucchi E., Silani V., Fogh I., Ticozzi N., Ratti A., Tiloca C., Gellera C., Pinter G.L., Taroni F., Castellotti B., Comi G.P., Corti S., Del Bo R., Cereda C., Ceroni M., Gagliardi S., Mazzini L., Sorarù G., Raggi F., Siciliano G., Simoncini C., Lo Gerfo A., Filosto M., Inghilleri M., Ferlini A., Corcia P., Couratier P., Vourc'h P., Hardiman O., McLaughlin R., Gotkine M., Drory V., van den Veldink J.H., Berg L.H., de Carvalho M., Mora Pardina J.S., Povedano M., Andersen P., Weber M., Başak A.N., Al-Chalabi A., Shaw C., Morrison K.E., Iacoangeli A., Shatunov A., Verde F., Kenna K., Al Khleifat A., Opie-Martin S., Piccinelli S.C., Padovani A., Galimberti D., Serpente M., Fenoglio C., Scarpini E., Curtis C.J., Lee S.H., Chung R., Patel H., Cooper-Knock J., Breen G., Dobson R.J.B., Dalgard C.L., Adeleye A., Alba C., Bacikova D., Hupalo D.N., McGrath Martinez E., Soltis A.R., Sukumar G., Viollet C., Wilkerson M.D., van den Berg L.H., D'Alfonso S., Chandran S., Pal S., Johnson K., Doucet-O'Hare T., Pasternack N., Wang T., Nath A., Veldink J.H., Chiò A., Sattler R., Shaw C.E., Ferraiuolo L., The International ALS Genomics Consortium, ITALSGEN Consortium, SLAGEN Consortium, Project MinE ALS Sequencing Consortium, The American Genome Center

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Repeat expansions in the C9orf72 gene are the most common genetic cause of (ALS) and frontotemporal dementia (FTD). Like other genetic forms of neurodegeneration, pinpointing the precise mechanism(s) by which this mutation leads to neuronal death remains elusive, and this lack of knowledge hampers the development of therapy for C9orf72-related disease. We used an agnostic approach based on genomic data (n = 41,273 ALS and healthy samples, and n = 1,516 C9orf72 carriers) to overcome these bottlenecks. Our drug-repurposing screen, based on gene- and expression-pattern matching and information about the genetic variants influencing onset age among C9orf72 carriers, identified acamprosate, a γ-aminobutyric acid analog, as a potentially repurposable treatment for patients carrying C9orf72 repeat expansions. We validated its neuroprotective effect in cell models and showed comparable efficacy to riluzole, the current standard of care. Our work highlights the potential value of genomics in repurposing drugs in situations where the underlying pathomechanisms are inherently complex. Video abstract: © 2024

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Cell Genomics

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Cell Press

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Medicine

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