Cerebral organoids derived from patients with Alzheimer’s disease with PSEN1/2 mutations have defective tissue patterning and altered development

During the past two decades, induced pluripotent stem cells (iPSCs) have been widely used to study human neural development and disease. Especially in the field of Alzheimer’s disease (AD), remarkable effort has been put into investigating molecular mechanisms behind this disease. Then, with the adv...

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Published inCell reports (Cambridge) Vol. 42; no. 11; p. 113310
Main Authors Vanova, Tereza, Sedmik, Jiri, Raska, Jan, Amruz Cerna, Katerina, Taus, Petr, Pospisilova, Veronika, Nezvedova, Marketa, Fedorova, Veronika, Kadakova, Sona, Klimova, Hana, Capandova, Michaela, Orviska, Petra, Fojtik, Petr, Bartova, Simona, Plevova, Karla, Spacil, Zdenek, Hribkova, Hana, Bohaciakova, Dasa
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 28.11.2023
Elsevier
Subjects
Alzheimer Disease - genetics
Alzheimer Disease - pathology
Alzheimer’s disease
cerebral organoids
CP: Developmental biology
CP: Neuroscience
development
Humans
induced pluripotent stem cells
Induced Pluripotent Stem Cells - pathology
Mutation - genetics
Neurons
Organoids - pathology
Presenilin-1 - genetics
Presenilin-2 - genetics
single-cell mRNA sequencing
cerebral organoids
development
Alzheimer’s disease
CP: Neuroscience
induced pluripotent stem cells
single-cell mRNA sequencing
CP: Developmental biology
Online AccessGet full text
ISSN2211-1247
2639-1856
2211-1247
DOI10.1016/j.celrep.2023.113310

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Abstract During the past two decades, induced pluripotent stem cells (iPSCs) have been widely used to study human neural development and disease. Especially in the field of Alzheimer’s disease (AD), remarkable effort has been put into investigating molecular mechanisms behind this disease. Then, with the advent of 3D neuronal cultures and cerebral organoids (COs), several studies have demonstrated that this model can adequately mimic familial and sporadic AD. Therefore, we created an AD-CO model using iPSCs derived from patients with familial AD forms and explored early events and the progression of AD pathogenesis. Our study demonstrated that COs derived from three AD-iPSC lines with PSEN1(A246E) or PSEN2(N141I) mutations developed the AD-specific markers in vitro, yet they also uncover tissue patterning defects and altered development. These findings are complemented by single-cell sequencing data confirming this observation and uncovering that neurons in AD-COs likely differentiate prematurely. [Display omitted] •Cerebral organoids generated from patients with fAD forms develop AD-like pathology•AD organoids react to β- and γ-secretase inhibitors by decreasing levels of Aβ peptides•AD organoids show developmental and tissue patterning defects•Single-cell-seq data support altered development and the signs of premature differentiation Vanova et al. show that brain organoids differentiated from induced pluripotent stem cells with mutations in PSEN1 and PSEN2 genes mimic the development of Alzheimer’s disease-like pathology in vitro. Curiously, these brain organoids also exhibit developmental and tissue patterning defects, supported by mRNA single-cell sequencing data showing premature neuronal differentiation.
AbstractList During the past two decades, induced pluripotent stem cells (iPSCs) have been widely used to study human neural development and disease. Especially in the field of Alzheimer's disease (AD), remarkable effort has been put into investigating molecular mechanisms behind this disease. Then, with the advent of 3D neuronal cultures and cerebral organoids (COs), several studies have demonstrated that this model can adequately mimic familial and sporadic AD. Therefore, we created an AD-CO model using iPSCs derived from patients with familial AD forms and explored early events and the progression of AD pathogenesis. Our study demonstrated that COs derived from three AD-iPSC lines with PSEN1(A246E) or PSEN2(N141I) mutations developed the AD-specific markers in vitro, yet they also uncover tissue patterning defects and altered development. These findings are complemented by single-cell sequencing data confirming this observation and uncovering that neurons in AD-COs likely differentiate prematurely.During the past two decades, induced pluripotent stem cells (iPSCs) have been widely used to study human neural development and disease. Especially in the field of Alzheimer's disease (AD), remarkable effort has been put into investigating molecular mechanisms behind this disease. Then, with the advent of 3D neuronal cultures and cerebral organoids (COs), several studies have demonstrated that this model can adequately mimic familial and sporadic AD. Therefore, we created an AD-CO model using iPSCs derived from patients with familial AD forms and explored early events and the progression of AD pathogenesis. Our study demonstrated that COs derived from three AD-iPSC lines with PSEN1(A246E) or PSEN2(N141I) mutations developed the AD-specific markers in vitro, yet they also uncover tissue patterning defects and altered development. These findings are complemented by single-cell sequencing data confirming this observation and uncovering that neurons in AD-COs likely differentiate prematurely.
During the past two decades, induced pluripotent stem cells (iPSCs) have been widely used to study human neural development and disease. Especially in the field of Alzheimer's disease (AD), remarkable effort has been put into investigating molecular mechanisms behind this disease. Then, with the advent of 3D neuronal cultures and cerebral organoids (COs), several studies have demonstrated that this model can adequately mimic familial and sporadic AD. Therefore, we created an AD-CO model using iPSCs derived from patients with familial AD forms and explored early events and the progression of AD pathogenesis. Our study demonstrated that COs derived from three AD-iPSC lines with PSEN1(A246E) or PSEN2(N141I) mutations developed the AD-specific markers in vitro, yet they also uncover tissue patterning defects and altered development. These findings are complemented by single-cell sequencing data confirming this observation and uncovering that neurons in AD-COs likely differentiate prematurely.
During the past two decades, induced pluripotent stem cells (iPSCs) have been widely used to study human neural development and disease. Especially in the field of Alzheimer’s disease (AD), remarkable effort has been put into investigating molecular mechanisms behind this disease. Then, with the advent of 3D neuronal cultures and cerebral organoids (COs), several studies have demonstrated that this model can adequately mimic familial and sporadic AD. Therefore, we created an AD-CO model using iPSCs derived from patients with familial AD forms and explored early events and the progression of AD pathogenesis. Our study demonstrated that COs derived from three AD-iPSC lines with PSEN1(A246E) or PSEN2(N141I) mutations developed the AD-specific markers in vitro, yet they also uncover tissue patterning defects and altered development. These findings are complemented by single-cell sequencing data confirming this observation and uncovering that neurons in AD-COs likely differentiate prematurely. [Display omitted] •Cerebral organoids generated from patients with fAD forms develop AD-like pathology•AD organoids react to β- and γ-secretase inhibitors by decreasing levels of Aβ peptides•AD organoids show developmental and tissue patterning defects•Single-cell-seq data support altered development and the signs of premature differentiation Vanova et al. show that brain organoids differentiated from induced pluripotent stem cells with mutations in PSEN1 and PSEN2 genes mimic the development of Alzheimer’s disease-like pathology in vitro. Curiously, these brain organoids also exhibit developmental and tissue patterning defects, supported by mRNA single-cell sequencing data showing premature neuronal differentiation.
ArticleNumber 113310
Author Fedorova, Veronika
Fojtik, Petr
Klimova, Hana
Bartova, Simona
Amruz Cerna, Katerina
Capandova, Michaela
Bohaciakova, Dasa
Taus, Petr
Orviska, Petra
Nezvedova, Marketa
Hribkova, Hana
Raska, Jan
Vanova, Tereza
Pospisilova, Veronika
Kadakova, Sona
Spacil, Zdenek
Plevova, Karla
Sedmik, Jiri
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Issue 11
Keywords cerebral organoids
development
Alzheimer’s disease
CP: Neuroscience
induced pluripotent stem cells
single-cell mRNA sequencing
CP: Developmental biology
Language English
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Snippet During the past two decades, induced pluripotent stem cells (iPSCs) have been widely used to study human neural development and disease. Especially in the...
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SubjectTerms Alzheimer Disease - genetics
Alzheimer Disease - pathology
Alzheimer’s disease
cerebral organoids
CP: Developmental biology
CP: Neuroscience
development
Humans
induced pluripotent stem cells
Induced Pluripotent Stem Cells - pathology
Mutation - genetics
Neurons
Organoids - pathology
Presenilin-1 - genetics
Presenilin-2 - genetics
single-cell mRNA sequencing
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Title Cerebral organoids derived from patients with Alzheimer’s disease with PSEN1/2 mutations have defective tissue patterning and altered development
URI https://dx.doi.org/10.1016/j.celrep.2023.113310
https://www.ncbi.nlm.nih.gov/pubmed/37864790
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