Functional screening in Drosophila identifies Alzheimer's disease susceptibility genes and implicates Tau-mediated mechanisms
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Using a Drosophila model of Alzheimer's disease (AD), we systematically evaluated 67 candidate genes based on AD-associated genomic loci (P < 10(-4)) from published human genome-wide association studies (GWAS). Genetic manipulation of 87 homologous fly genes was tested for modulation of neurotoxicity caused by human Tau, which forms neurofibrillary tangle pathology in AD. RNA interference (RNAi) targeting 9 genes enhanced Tau neurotoxicity, and in most cases reciprocal activation of gene expression suppressed Tau toxicity. Our screen implicates cindr, the fly ortholog of the human CD2AP AD susceptibility gene, as a modulator of Tau-mediated disease mechanisms. Importantly, we also identify the fly orthologs of FERMT2 and CELF1 as Tau modifiers, and these loci have been independently validated as AD susceptibility loci in the latest GWAS meta-analysis. Both CD2AP and FERMT2 have been previously implicated with roles in cell adhesion, and our screen additionally identifies a fly homolog of the human integrin adhesion receptors, ITGAM and ITGA9, as a modifier of Tau neurotoxicity. Our results highlight cell adhesion pathways as important in Tau toxicity and AD susceptibility and demonstrate the power of model organism genetic screens for the functional follow-up of human GWAS.
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Genetic screens identified p130CAS, Fak, Eph, Rab3-GEF, cindr, Fit1, Aret and Rhea, orthologs of CASS4, PTK2B, EPHA1, MADD, CD2AP, FERMT2, CELF1 and TLN2, as modulators of Tau toxicity.
“Beyond BIN1, this approach identified p130CAS, Fak, Eph, Rab3-GEF, cindr, Fit1, Aret and Rhea respective orthologs of CASS4, PTK2B, EPHA1, MADD, CD2AP, FERMT2, CELF1 and TLN2 [26, 42, 119].”
From The new genetic landscape of Alzheimer’s disease: from amyloid cascade to genetically driven synaptic failure hypothesis? (2019) · cites this paper as [119]
The Results section and Table 2 (page unavailable in our copy) support cindr–CD2AP, Fit1–FERMT2 and aret–CELF1 as fly genes whose manipulation modifies Tau toxicity. They do not identify p130CAS–CASS4, Fak–PTK2B, Eph–EPHA1, Rab3-GEF–MADD or Rhea–TLN2 as screen hits, so this source supports only part of the attributed list. (LLM, conf=0.90)
Experimental — accuracy not yet measuredFor previously reported loci, applying the same prioritization approach highlights several genes involved in APP metabolism (FERMT2, PICALM) or tau toxicity (BIN1, CD2AP, FERMT2, CASS4, PTK2B).
“For previously reported loci, applying the same prioritization approach highlights several genes, as described in Fig. 2, some of which are involved in APP metabolism (FERMT2, PICALM) or tau toxicity (BIN1, CD2AP, FERMT2, CASS4, PTK2B)98–101.”
From Genetic meta-analysis of diagnosed Alzheimer’s disease identifies new risk loci and implicates Aβ, tau, immunity and lipid processing (2019) · cites this paper as [100]
BDTOs increased expression of 4 genes including CD2AP (4.62 ± 0.45).
“BDTOs increased expression of 4 genes including CD2AP (4.62 ± 0.45), previously implicated in tau-mediated toxicity (Shulman et al., 2014).”
From iPSC-derived human microglia-like cells to study neurological diseases (2017) · cites this paper as Shulman et al., 2014
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- Authors
- Shulman, J. M., Imboywa, S., Giagtzoglou, N., Powers, M. P., Hu, Y., Devenport, D., Chipendo, P., Chibnik, L. B., Diamond, A., Perrimon, N., Brown, N. H., De Jager, P. L., & Feany, M. B.
- Affiliations
- Baylor College of Medicine (US)
- Broad Institute (US)
- Howard Hughes Medical Institute (US)
- University of Cambridge (GB)
- Corresponding author
- Shulman, J. M.
- Venue
- Human Molecular Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-09-25
- Volume
- 23
- Issue
- 4
- Pages
- 870-877
- ISSN
- 0964-6906 (ISSN-L)
- 1460-2083
- PMC
- PMC3900103
- OpenAlex
- W2137709496
- Cited by
- 167
- References
- 47
- Citations by year
- 2026: 3 · 2025: 13 · 2024: 13 · 2023: 10 · 2022: 6 · 2021: 15 · 2020: 16 · 2019: 20 · 2018: 12 · 2017: 14 · 2016: 19 · 2015: 16 · 2014: 9 · 2013: 1
- FWCI
- 10.44
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Human Molecular Genetics (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Funders
- Burroughs Wellcome Fund
- Ellison Medical Foundation
- Wellcome Trust (086451, 092096)
- National Institutes of Health (R01GM, R24OD011176)
- National Institute on Aging (K25AG041906, K08AG034290)
- National Institute of General Medical Sciences (R01GM084947, R25GM076321)
- National Center for Research Resources (C06RR029965)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD018655)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- Alzheimer's disease, neurofibrillary tangles, Drosophila model, genetic screen, CD2AP, FERMT2, CELF1, CD11b, ITGA9, cell adhesion, integrins, RNA interference
- MeSH terms
- Alzheimer Disease, Animals, Disease Models, Animal, Drosophila melanogaster, Humans, Integrins, tau Proteins, Genetic Predisposition to Disease, Drosophila Proteins, Animals, Genetically Modified, RNA Interference, CD11b Antigen, Gene Knockdown Techniques, Genetic Association Studies
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