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Peripheral expression of brain-penetrant progranulin rescues pathologies in mouse models of frontotemporal lobar degeneration.
Reich, Marvin; Simon, Matthew J; Polke, Beate; Paris, Iñaki; Werner, Georg; Schrader, Christian; Spieth, Lena; Davis, Sonnet S; Robinson, Sophie; de Melo, Gabrielly Lunkes; Schlaphoff, Lennart; Buschmann, Katrin; Berghoff, Stefan; Logan, Todd; Nuscher, Brigitte; de Weerd, Lis; Edbauer, Dieter; Simons, Mikael; Suh, Jung H; Sandmann, Thomas; Kariolis, Mihalis S; DeVos, Sarah L; Lewcock, Joseph W; Paquet, Dominik; Capell, Anja; Di Paolo, Gilbert; Haass, Christian.
Afiliación
  • Reich M; German Center for Neurodegenerative Diseases (DZNE), 81377 Munich, Germany.
  • Simon MJ; Graduate School of Systemic Neurosciences (GSN), LMU Munich, 82152 Planegg, Germany.
  • Polke B; Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, 81377 Munich, Germany.
  • Paris I; Denali Therapeutics Inc., South San Francisco, CA 94080, USA.
  • Werner G; Metabolic Biochemistry, Biomedical Centre (BMC), Faculty of Medicine, LMU Munich, 81377 Munich, Germany.
  • Schrader C; Metabolic Biochemistry, Biomedical Centre (BMC), Faculty of Medicine, LMU Munich, 81377 Munich, Germany.
  • Spieth L; Metabolic Biochemistry, Biomedical Centre (BMC), Faculty of Medicine, LMU Munich, 81377 Munich, Germany.
  • Davis SS; Metabolic Biochemistry, Biomedical Centre (BMC), Faculty of Medicine, LMU Munich, 81377 Munich, Germany.
  • Robinson S; German Center for Neurodegenerative Diseases (DZNE), 81377 Munich, Germany.
  • de Melo GL; Institute of Neuronal Cell Biology, Technical University Munich, 80802 Munich, Germany.
  • Schlaphoff L; Max Planck Institute for Multidisciplinary Sciences, 37077 Göttingen, Germany.
  • Buschmann K; Denali Therapeutics Inc., South San Francisco, CA 94080, USA.
  • Berghoff S; Graduate School of Systemic Neurosciences (GSN), LMU Munich, 82152 Planegg, Germany.
  • Logan T; Institute for Stroke and Dementia Research (ISD), University Hospital, LMU Munich, 81377 Munich, Germany.
  • Nuscher B; Metabolic Biochemistry, Biomedical Centre (BMC), Faculty of Medicine, LMU Munich, 81377 Munich, Germany.
  • de Weerd L; Denali Therapeutics Inc., South San Francisco, CA 94080, USA.
  • Edbauer D; German Center for Neurodegenerative Diseases (DZNE), 81377 Munich, Germany.
  • Simons M; Graduate School of Systemic Neurosciences (GSN), LMU Munich, 82152 Planegg, Germany.
  • Suh JH; Institute of Neuronal Cell Biology, Technical University Munich, 80802 Munich, Germany.
  • Sandmann T; Metabolic Biochemistry, Biomedical Centre (BMC), Faculty of Medicine, LMU Munich, 81377 Munich, Germany.
  • Kariolis MS; German Center for Neurodegenerative Diseases (DZNE), 81377 Munich, Germany.
  • DeVos SL; Institute of Neuronal Cell Biology, Technical University Munich, 80802 Munich, Germany.
  • Lewcock JW; Max Planck Institute for Multidisciplinary Sciences, 37077 Göttingen, Germany.
  • Paquet D; Denali Therapeutics Inc., South San Francisco, CA 94080, USA.
  • Capell A; Metabolic Biochemistry, Biomedical Centre (BMC), Faculty of Medicine, LMU Munich, 81377 Munich, Germany.
  • Di Paolo G; German Center for Neurodegenerative Diseases (DZNE), 81377 Munich, Germany.
  • Haass C; German Center for Neurodegenerative Diseases (DZNE), 81377 Munich, Germany.
Sci Transl Med ; 16(750): eadj7308, 2024 Jun 05.
Article en En | MEDLINE | ID: mdl-38838131
ABSTRACT
Progranulin (PGRN) haploinsufficiency is a major risk factor for frontotemporal lobar degeneration with TAR DNA-binding protein 43 (TDP-43) pathology (FTLD-GRN). Multiple therapeutic strategies are in clinical development to restore PGRN in the CNS, including gene therapy. However, a limitation of current gene therapy approaches aimed to alleviate FTLD-associated pathologies may be their inefficient brain exposure and biodistribution. We therefore developed an adeno-associated virus (AAV) targeting the liver (L) to achieve sustained peripheral expression of a transferrin receptor (TfR) binding, brain-penetrant (b) PGRN variant [AAV(L)bPGRN] in two mouse models of FTLD-GRN, namely, Grn knockout and GrnxTmem106b double knockout mice. This therapeutic strategy avoids potential safety and biodistribution issues of CNS-administered AAVs and maintains sustained concentrations of PGRN in the brain after a single dose. AAV(L)bPGRN treatment reduced several FTLD-GRN-associated pathologies including severe motor function deficits, aberrant TDP-43 phosphorylation, dysfunctional protein degradation, lipid metabolism, gliosis, and neurodegeneration in the brain. The potential translatability of our findings was tested in an in vitro model using cocultured human induced pluripotent stem cell (hiPSC)-derived microglia lacking PGRN and TMEM106B and wild-type hiPSC-derived neurons. As in mice, aberrant TDP-43, lysosomal dysfunction, and neuronal loss were ameliorated after treatment with exogenous TfR-binding protein transport vehicle fused to PGRN (PTVPGRN). Together, our studies suggest that peripherally administered brain-penetrant PGRN replacement strategies ameliorate FTLD-GRN relevant phenotypes including TDP-43 pathology, neurodegeneration, and behavioral deficits. Our data provide preclinical proof of concept for the use of this AAV platform for treatment of FTLD-GRN and potentially other CNS disorders.
Asunto(s)

Texto completo: 1 Colección: 01-internacional Base de datos: MEDLINE Asunto principal: Encéfalo / Ratones Noqueados / Dependovirus / Modelos Animales de Enfermedad / Degeneración Lobar Frontotemporal / Progranulinas Límite: Animals / Humans Idioma: En Revista: Sci Transl Med Asunto de la revista: CIENCIA / MEDICINA Año: 2024 Tipo del documento: Article País de afiliación: Alemania Pais de publicación: Estados Unidos

Texto completo: 1 Colección: 01-internacional Base de datos: MEDLINE Asunto principal: Encéfalo / Ratones Noqueados / Dependovirus / Modelos Animales de Enfermedad / Degeneración Lobar Frontotemporal / Progranulinas Límite: Animals / Humans Idioma: En Revista: Sci Transl Med Asunto de la revista: CIENCIA / MEDICINA Año: 2024 Tipo del documento: Article País de afiliación: Alemania Pais de publicación: Estados Unidos