The Trem2 R47H Alzheimer's risk variant impairs splicing and reduces Trem2 mRNA and protein in mice but not in humans
Open accessAbstract
BACKGROUND: The R47H variant of the Triggering Receptor Expressed on Myeloid cells 2 (TREM2) significantly increases the risk for late onset Alzheimer's disease. Mouse models accurately reproducing phenotypes observed in Alzheimer' disease patients carrying the R47H coding variant are required to understand the TREM2 related dysfunctions responsible for the enhanced risk for late onset Alzheimer's disease. METHODS: A CRISPR/Cas9-assisted gene targeting strategy was used to generate Trem2 R47H knock-in mice. Trem2 mRNA and protein levels as well as Trem2 splicing patterns were assessed in these mice, in iPSC-derived human microglia-like cells, and in human brains from Alzheimer's patients carrying the TREM2 R47H risk factor. RESULTS: Two independent Trem2 R47H knock-in mouse models show reduced Trem2 mRNA and protein production. In both mouse models Trem2 haploinsufficiency was due to atypical splicing of mouse Trem2 R47H, which introduced a premature stop codon. Cellular splicing assays using minigene constructs demonstrate that the R47H variant induced abnormal splicing only occurs in mice but not in humans. TREM2 mRNA levels and splicing patterns were both normal in iPSC-derived human microglia-like cells and patient brains with the TREM2 R47H variant. CONCLUSIONS: The Trem2 R47H variant activates a cryptic splice site that generates miss-spliced transcripts leading to Trem2 haploinsufficiency only in mice but not in humans. Since Trem2 R47H related phenotypes are mouse specific and do not occur in humans, humanized TREM2 R47H knock-in mice should be generated to study the cellular consequences caused by the human TREM2 R47H coding variant. Currently described phenotypes of Trem2 R47H knock-in mice can therefore not be translated to humans.
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iPSC-derived microglial-like cells were generated using established protocols.
“iPSC-derived microglial-like cells were generated using established protocols [64,65].”
From Selective suppression of oligodendrocyte-derived amyloid beta rescues neuronal dysfunction in Alzheimer’s disease (2024) · cites this paper as [65]
p.R47H and p.R62H reduce ligand binding.
“such as reduced ligand binding (p.R47H [96], p.R62H [97])”
From TREM2/PLCγ2 signalling in immune cells: function, structural insight, and potential therapeutic modulation (2021) · cites this paper as [96]
About 75% of mutations in PLCG2 previously implicated in various inflammatory diseases map to the autoinhibitory interface on the PLCγ2 model structure and can be considered pathogenic.
“A number of mutations in PLCG2 (about 75%), that have been previously implicated in various inflammatory diseases [92–102], actually map to the autoinhibitory interface on the PLCγ2 model structure and can be considered as pathogenic (Fig. 2c)”
From TREM2/PLCγ2 signalling in immune cells: function, structural insight, and potential therapeutic modulation (2021) · cites this paper as [96]
The Background discusses TREM2 and microglial activity, while the References list a study mentioning PLCG2. Searches for the 75% figure, the PLCγ2 autoinhibitory interface, and inflammatory-disease mutations found no passage in our copy addressing the claim. (LLM, conf=0.76)
Experimental — accuracy not yet measuredThe decreased Trem2 expression in Trem2 R47H knock-in mice is due to a splice effect that occurs in mice but not in humans.
“This has been shown to be due to a splice effect that seems to occur in mice but not in humans (36).”
From <i>Trem2</i> promotes anti-inflammatory responses in microglia and is suppressed under pro-inflammatory conditions (2020) · cites this paper as [36]
The decrease in Trem2 expression in Trem2 R47H KI mice has been described by Cheng-Hathaway et al. and Xiang et al.
“This effect has been described by Cheng-Hathaway et al. (37) and Xiang et al. (36) studying the same mouse line used here from the Jackson Laboratory, and an independent Trem2 R47H KI mouse line.”
From <i>Trem2</i> promotes anti-inflammatory responses in microglia and is suppressed under pro-inflammatory conditions (2020) · cites this paper as [36]
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- Authors
- Xiang, X., Piers, T. M., Wefers, B., Zhu, K., Mallach, A., Brunner, B., Kleinberger, G., Song, W., Colonna, M., Herms, J., Wurst, W., Pocock, J. M., & Haass, C.
- Affiliations
- Ludwig-Maximilians-Universität München (DE)
- UCL Queen Square Institute of Neurology (GB)
- German Center for Neurodegenerative Diseases (DE)
- Munich Cluster for Systems Neurology (DE)
- Washington University in St. Louis (US)
- Corresponding author
- Xiang, Xianyuan
- Piers, Thomas M.
- Wefers, Benedikt
- Zhu, Kaichuan
- Mallach, Anna
- Brunner, Bettina
- Kleinberger, Gernot
- Song, Wilbur
- Colonna, Marco
- Herms, Jochen
- Wurst, Wolfgang
- Pocock, Jennifer M.
- Haass, Christian
- ORCID
- Venue
- Molecular Neurodegeneration
- Published
- 2018-09-06
- Volume
- 13
- Issue
- 1
- Pages
- 49-49
- ISSN
- 1750-1326 (ISSN-L)
- PMC
- PMC6126019
- OpenAlex
- W2890074452
- Cited by
- 170
- References
- 45
- Citations by year
- 2026: 10 · 2025: 13 · 2024: 18 · 2023: 43 · 2022: 10 · 2021: 26 · 2020: 35 · 2019: 11 · 2018: 3
- FWCI
- 13.58
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Molecular Neurodegeneration (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UCL Discovery (University College London) (submittedVersion)
- Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion, cc-by)
- DZNE Pub (submittedVersion, other-oa)
- PuSH - Publication Server of Helmholtz Zentrum München (submittedVersion, cc-by)
- Funders
- Deutsche Forschungsgemeinschaft (EXC 1010 SyNergy)
- Koselleck Project (HA1737/16-1)
- German Federal Ministry of Education and Research (01EK1605C)
- Biotechnology and Biological Sciences Research Council (BB/M009513/1)
- Innovative Medicines Initiative 2 Joint Undertaking (No 115976)
- National Institute on Aging (RF1 AG051485)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- TREM2, Alzheimer's disease, late-onset Alzheimer's disease, splicing, haploinsufficiency, cryptic splice site, knock-in mice, premature stop codon, microglia, species differences, humanized mice
- MeSH terms
- Alzheimer Disease, Animals, Brain, Disease Models, Animal, Humans, Membrane Glycoproteins, Mice, Transgenic, Receptors, Immunologic, RNA Splicing, RNA, Messenger, Genetic Variation, Microglia, Genetic Predisposition to Disease
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