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[Preprint]. 2024 Jan 30:2024.01.29.577876. [Version 1] doi: 10.1101/2024.01.29.577876

Cellular Modeling of CLN6 with IPSC-derived Neurons and Glia

Maria Gabriela Otero, Jaemin Kim, Yogesh Kumar Kushwaha, Alex Rajewski, Fabian David Nonis, Chintda Santiskulvong, Serguei I Bannykh, Hiral Oza, Hafiz Muhammad Umer Farooqi, Madeline Babros, Christina Freeman, Lucie Dupuis, Saadat Mercimek-Andrews, Roberto Mendoza-Londono, Catherine Bresee, David R Adams, Cynthia J Tifft, Camilo Toro, Negar Khanlou, William A Gahl, Noriko Salamon, Tyler Mark Pierson
PMCID: PMC10862716  PMID: 38352418

ABSTRACT

Neuronal ceroid lipofuscinosis (NCL), type 6 (CLN6) is a neurodegenerative disorder associated with progressive neurodegeneration leading to dementia, seizures, and retinopathy. CLN6 encodes a resident-ER protein involved in trafficking lysosomal proteins to the Golgi. CLN6p deficiency results in lysosomal dysfunction and deposition of storage material comprised of Nile Red + lipids/proteolipids that include subunit C of the mitochondrial ATP synthase (SUBC). White matter involvement has been recently noted in several CLN6 animal models and several CLN6 subjects had neuroimaging was consistent with leukodystrophy. CLN6 patient-derived induced pluripotent stem cells (IPSCs) were generated from several of these subjects. IPSCs were differentiated into oligodendroglia or neurons using well-established small-molecule protocols. A doxycycline-inducible transgenic system expressing neurogenin-2 (the I3N-system) was also used to generate clonal IPSC-lines (I3N-IPSCs) that could be rapidly differentiated into neurons (I3N-neurons). All CLN6 IPSC-derived neural cell lines developed significant storage material, CLN6-I3N-neuron lines revealed significant Nile Red + and SUBC + storage within three and seven days of neuronal induction, respectively. CLN6-I3N-neurons had decreased tripeptidyl peptidase-1 activity, increased Golgi area, along with increased LAMP1 + in cell bodies and neurites. SUBC + signal co-localized with LAMP1 + signal. Bulk-transcriptomic evaluation of control- and CLN6-I3N-neurons identified >1300 differentially-expressed genes (DEGs) with Gene Ontogeny (GO) Enrichment and Canonical Pathway Analyses having significant changes in lysosomal, axonal, synaptic, and neuronal-apoptotic gene pathways. These findings indicate that CLN6-IPSCs and CLN6-I3N-IPSCs are appropriate cellular models for this disorder. These I3N-neuron models may be particularly valuable for developing therapeutic interventions with high-throughput drug screening assays and/or gene therapy.

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