Aβ25-35-induced autophagy and apoptosis are prevented by the CRMP2-derived peptide ST2-104 (R9-CBD3) via a CaMKKβ/AMPK/mTOR signaling hub
We previously reported that the peptide ST2-104 (CBD3, for Ca2+ channel-binding domain 3), derived from the collapsin response mediator protein 2 (CRMP2)-a cytosolic phosphoprotein, protects neuroblastoma cells against β-amyloid (Aβ) peptide-mediated toxicity through engagement of a phosphorylated CRMP2/NMDAR pathway. Abnormal aggregation of Aβ peptides (e.g., Aβ25-35) leads to programmed cell death (apoptosis) as well autophagy-both of which contribute to Alzheimer's disease (AD) progression. Here, we asked if ST2-104 affects apoptosis and autophagy in SH-SY5Y neuroblastoma challenged with the toxic Aβ25-35 peptide and subsequently mapped the downstream signaling pathways involved. ST2-104 protected SH-SY5Y cells from death following Aβ25-35 peptide challenge by reducing apoptosis and autophagy as well as limiting excessive calcium entry. Cytotoxicity of SHY-SY5Y cells challenged with Aβ25-35 peptide was blunted by ST2-104. The autophagy activator Rapamycin blunted the anti-apoptotic activity of ST2-104. ST2-104 reversed Aβ25-35-induced apoptosis via inhibiting Ca2+/CaM-dependent protein kinase kinase β (CaMKKβ)-mediated autophagy, which was partly enhanced by STO-609 (an inhibitor of CaMKKβ). ST2-104 attenuated neuronal apoptosis by inhibiting autophagy through a CaMKKβ/AMPK/mTOR signaling hub. These findings identify a mechanism whereby, in the face of Aβ25-35, the concerted actions of ST2-104 leads to a reduction in intracellular calcium overload and inhibition of the CaMKKβ/AMPK/mTOR pathway resulting in attenuation of autophagy and cellular apoptosis. These findings define a mechanistic framework for how ST2-104 transduces "outside" (calcium channels) to "inside" signaling (CaMKKβ/AMPK/mTOR) to confer neuroprotection in AD.
Authors
- Rajesh Khanna (ORCID: https://orcid.org/0000-0002-9066-2969)
- Yingshi Ji
- Jinghong Ren
- Li Sun (ORCID: https://orcid.org/0000-0003-1169-4653)
- Qian Yuan (ORCID: https://orcid.org/0000-0002-8639-835X)
- Huanyu Liu (ORCID: https://orcid.org/0000-0002-6158-9627)
- Jianfeng Sun (ORCID: https://orcid.org/0009-0009-1876-3317)
- Yuan Yao (ORCID: https://orcid.org/0000-0002-9303-5856)
- Jiaxin Li (ORCID: https://orcid.org/0000-0002-8594-0506)
Institutions
- Jilin University (CN)
- Peking University (CN)
- Beijing Jishuitan Hospital (CN)
- University of Florida (US)
- First Hospital of Jilin University (CN)
- Jilin Medical University (CN)
- Jilin Agricultural University (CN)
Publication Details
- Journal
- PLoS ONE
- Published
- 2024-09-26
- DOI
- https://doi.org/10.1371/journal.pone.0309794
- Citations
- 2
- Primary Topic
- Axon Guidance and Neuronal Signaling
- Type
- article
- Field-Weighted Citation Impact
- 0.54
Funders
- National Natural Science Foundation of China
- Department of Finance of Jilin Province