Enhancing face validity of mouse models of Alzheimer’s disease with natural genetic variation
Open accessAbstract
Classical laboratory strains show limited genetic diversity and do not harness natural genetic variation.Mouse models relevant to Alzheimer's disease (AD) have largely been developed using these classical laboratory strains, such as C57BL/6J (B6), and this has likely contributed to the failure of translation of findings from mice to the clinic.Therefore, here we test the potential for natural genetic variation to enhance the translatability of AD mouse models.Two widely used AD-relevant transgenes, APP swe and PS1 de9 (APP/PS1), were backcrossed from B6 to three wild-derived strains CAST/EiJ, WSB/EiJ, PWK/PhJ, representative of three Mus musculus subspecies.These new AD strains were characterized using metabolic, functional, neuropathological and transcriptional assays.Strain-, sex-and genotype-specific differences were observed in cognitive ability, neurodegeneration, plaque load, cerebrovascular health and cerebral amyloid angiopathy.Analyses of brain transcriptional data showed strain was the greatest driver of variation.We identified significant variation in myeloid cell numbers in wild type mice of different strains as well as significant differences in plaque-associated myeloid responses in APP/PS1 mice between the strains.Collectively, these data support the use of wild-derived strains to better model the complexity of human AD. Author summaryDespite the rise in incidence of Alzheimer's disease (AD), it has been over a decade since a new drug treatment has been introduced.Recently, a number of pharmaceutical giants have shut down their AD research units.One issue that these companies and researchers have struggled with is the lack of translatability of preclinical studies to the clinic.One aspect that has come under heavy scrutiny is whether the mouse can be an appropriate
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Onos and colleagues observed an increase in neuroinflammation in the cortex and hippocampus of PWK mice.
“Notably, Onos and colleagues observed an increase in neuroinflammation in the cortex and hippocampus of PWK mice.”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
The Discussion describes substantial neuroinflammation in PWK.APP/PS1 mice, and the Results report that PWK had the greatest difference in myeloid-related gene expression between wild-type and APP/PS1 mice. The cited passages do not establish an increase specifically in both the cortex and hippocampus, and the claim omits the APP/PS1 genotype. (LLM, conf=0.87)
Experimental — accuracy not yet measuredMice with APPswe and PSEN1de9 transgenes backcrossed onto wild-derived backgrounds had higher levels of amyloid-β compared with age-matched mice on a B6 background.
“These mice had higher levels of amyloid-β (Aβ) compared with age-matched mice on a B6 background (Onos et al., 2019).”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
The Results section, “Evidence of mixed pathologies in wild-derived APP/PS1 strains,” reports higher Aβ42 levels than in B6.APP/PS1 mice for female CAST.APP/PS1 and WSB.APP/PS1 mice at 8 months. It does not establish higher Aβ levels for all wild-derived backgrounds or for males; it also reports fewer cortical plaques in all three wild-derived strains. (LLM, conf=0.90)
Experimental — accuracy not yet measuredTranscriptomic data from Onos and colleagues showed a compelling effect of these three wild-derived strains on amyloid accumulation.
“Transcriptomic data from Onos and colleagues showed a compelling effect of these three wild-derived strains on amyloid accumulation (Onos et al., 2019; Yang et al., 2021).”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
The Results section on mixed pathologies reports significantly fewer cortical plaques in all three wild-derived APP/PS1 strains than in B6.APP/PS1, establishing strain differences in amyloid deposition. The transcriptional-profiling Results instead show strain-dependent gene expression and responses to amyloid; they do not themselves establish an effect on amyloid accumulation. Page numbers are not available in the supplied copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredOnos and colleagues reported a list of 35 genes associated with a wild-derived specific response to amyloid transgene, identified as the 'light yellow' module via WGCNA module-trait analyses for genetic background and presence of the APP/PS1 transgene.
“First, Onos and colleagues reported a list of genes associated with a wild-derived specific response to amyloid transgene (Onos et al., 2019). This list of 35 genes was identified as the “light yellow” module via WGCNA module–trait analyses for genetic background and presence of the APP/PS1 transgene (Onos et al., 2019).”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredWild-derived mouse variants include over 5 million SNPs, 116 novel genes not present in B6, and between 250 and 400 large structural variants.
“These variants include over 5 million single nucleotide polymorphisms (SNPs; Onos et al., 2019), 116 novel genes not present in B6 (Lilue et al., 2018), and between 250 and 400 large structural variants (Yalcin et al., 2011).”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
In comparison to the 35-gene module from Onos et al., 19 of their genes were significantly enriched also in the darkorange module (Fisher exact test, P = 1.62 × 10−19).
“In comparison to their 35-gene module, we found that 19 of their genes were significantly enriched also in our darkorange module (Fig. 6 C, highlighted in purple; Fisher exact test, P = 1.62 × 10−19).”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
A similar effect of genetic background was found via WGCNA when modeling Aβ.
“A similar effect of the genetic background was found via WGCNA when modeling Aβ (Onos et al., 2019).”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
Recent studies in AD have shown that mouse genetic background can modulate Aβ accumulation, immune response, and tau propagation.
“Recent studies in AD have shown that mouse genetic background can modulate Aβ accumulation (Onos et al., 2019), immune response (Yang et al., 2021), and tau propagation (Dujardin et al., 2022).”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
Neurodegenerative hub-genes were detected by comparing Signature C (darkorange) and wild-derived amyloid response (Fisher's exact test: P = 1.62 × 10−19).
“Neurodegenerative hub-genes (purple) were detected by comparing Signature C (darkorange) and wild-derived amyloid response (Fisher’s exact test: P = 1.62 × 10−19; Onos et al., 2019).”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
There is a considerable overlap when comparing the tau seeding-associated genes in wild-derived mouse strains to a previous study of amyloid response in wild-derived strains.
“Interestingly, we see a considerable overlap when comparing the tau seeding–associated genes in wild-derived mouse strains to a previous study of amyloid response in wild-derived strains (Onos et al., 2019).”
From Network analysis identifies strain-dependent response to tau and tau seeding-associated genes (2023) · cites this paper as Onos et al., 2019
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Additional file 1 of Variation under domestication in animal models: the case of the Mexican axolotl
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Self-citation
- Authors
- Onos, K. D., Uyar, A., Keezer, K. J., Jackson, H. M., Preuss, C., Acklin, C. J., O’Rourke, R., Buchanan, R., Cossette, T. L., Sukoff Rizzo, S. J., Soto, I., Carter, G. W., & Howell, G. R.
- Affiliations
- Jackson Laboratory (US)
- Rowan University (US)
- Tufts University (US)
- Corresponding author
- Onos, Kristen D.
- Howell, Gareth R.
- ORCID
- Venue
- PLOS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2019-05-31
- Volume
- 15
- Issue
- 5
- Pages
- e1008155
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC6576791
- OpenAlex
- W2947469782
- Cited by
- 93
- References
- 69
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 14 · 2023: 12 · 2022: 15 · 2021: 15 · 2020: 16 · 2019: 2
- FWCI
- 8.23
- Type
- journal article
- Language
- en
- Update notices
- new_version (2019-06-17)
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Rowan Digitals Works (Rowan University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
- Funders
- National Institute on Aging (RF1AG055104, U54AG054345)
- National Institute of General Medical Sciences (T32HD007065)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- Alzheimer's disease, mouse model, natural genetic variation, wild-derived mouse strains, APP/PS1 mice, backcrossing, CAST/EiJ, translational validity, amyloid plaques, cerebral amyloid angiopathy, cerebrovascular health, neurodegeneration, myeloid cells, brain transcriptome, sex differences, cognitive function
- MeSH terms
- Alzheimer Disease, Animals, Animals, Wild, Brain, Disease Models, Animal, Humans, Mice, Inbred C57BL, Mice, Transgenic, Genetic Variation, Reproducibility of Results, Amyloid beta-Peptides, Amyloid beta-Protein Precursor, Mice, Presenilin-1, Plaque, Amyloid
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