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PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
The input data for this calculation are the inter-labelling matrix M that reflects the extent to which infusion of any nutrient i (of n total nutrients of interest) labels every other circulating nutrient j and the carbon atom circulatory turnover flux for each circulating nutrient .
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
The procedure first uses M to calculate the direct contributions to each nutrient i from all other circulating nutrients j, creating a new n × n matrix N whose entries Nij reflect the direct contributions of circulating nutrient j to circulating nutrient i. It then utilizes the matrix N and to calculate the direct contributing fluxes from any circulating nutrient to any other circulating nutrient, resulting in a complete determination of the inter-converting fluxes in units of nmolC min g between circulating nutrients.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Fluxes were computed using Matlab (v.R2019a).
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
The network was visualized using Cytoscape (v2.9.0).
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
All omics were analysed and visualized in R (Statistical Computing, v.4.1.0).
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Gene set enrichment was performed using fgsea (https://bioconductor.org/packages/release/bioc/html/fgsea.html) using as input gene or protein list rank by relative changes (log2-transformed fold change of comparison).
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Gene sets were taken from the Mouse MSigDB Collections using the gene sets MH (Hallmark) and the M2 (canonical pathways) using the Reactome subset.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
We used 1,000 permutations of the gene-level values to calculate NES and statistical significance.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
The super enhancer core regulatory circuitry has been described by Durbin et al. and modified by Decaesteker et al.. The retino-sympathetic and adrenergic circuit has been described by Zimmerman et al.. To determine cell-type abundance a deconvolution approach was used leveraging the bulk gene-expression profiles of the Th-MYCN tumours for the four treatment groups: CD, ProArg-free diet, CD plus DFMO and ProArg-free diet plus DFMO.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
We used the CIBERSORTx, a machine learning method to infer cell-type proportions without physical cell isolation based on the creation of a signature matrix of cell types identified in Th-MYCN tumour model in published single-cell RNA-sequencing data by Costa et al.. Using this high-resolution single-cell annotation of the tumour microenvironment in Th-MYCN mice the digital cytometry tool was run on bulk tumour expression to extract cell-type abundances and dissect the effect of treatment on the tumour microenvironment.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
The number of human and mouse samples is recorded in the figure captions.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
For human tumour measurements, n represents the number of patients.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
For mouse experiments, n represents the number of mice.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
P values were computed using an unpaired two-sided Welch’s t-test using the Welch–Satterthwaite equation (not assuming equal variances) unless specified otherwise.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Regression between adenosine-ending codon and protein levels were calculated with the R function stat_cor (package ggpubr) to compute Pearson’s r and geom_smooth (package ggplot2) using ‘linear model’ to display the regression line.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Statistics were performed using R (v.4.1.0).
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
A two-tailed unpaired Welch’s t-test was used to calculate P values.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Metabolomics data were corrected for multiple comparisons using the Benjamini–Hochberg method, with a FDR cut-off of 0.05 used to determine statistical significance.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
P values were corrected for multiple hypothesis testing using the Benjamini–Hochberg method, with a FDR cut-off of 0.05 used to determine statistical significance.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Two-sided Student’s t-tests were calculated with a permutation-based FDR cut-off of 0.05 and s0 = 1 if not otherwise declared.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
A two-tailed unpaired Welch’s t-test was used to calculate P values.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Modifications were corrected for multiple comparisons using the Benjamini–Hochberg method, with an FDR cut-off of 0.05 used to determine statistical significance.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Comparisons of outcome between groups were performed by a two-sided log-rank test, tumour-related death is counted as an event, with mice censored at the time of death without tumour or necropsy.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Survival was statistically assessed according to the method of Kaplan and Meier according to Peto and Peto.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Representative results, such as blots and H&E staining, were independently validated in at least two independent experiments yielding similar results.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
This include Fig. 6g,h, Extended Data Figs. 8d,e,n and 9i and Supplementary Figs. 2b, 3b, 4f and 7b.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Animal studies followed protocols approved by the Princeton University and Children’s Hospital of Philadelphia Institutional Animal Care and Use Committees.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Patient samples obtained from the COG (Neuroblastoma Biology Committee) underwent review and approval through a Cancer Therapy Evaluation Program overseen process: application ANBL16B2 Q, principal investigator J.D.R. Further information on research design is available in the Nature Portfolio Reporting Summary linked to this article.
PMC12527938
Reprogramming neuroblastoma by diet-enhanced polyamine depletion
Any methods, additional references, Nature Portfolio reporting summaries, source data, extended data, supplementary information, acknowledgements, peer review information; details of author contributions and competing interests; and statements of data and code availability are available at 10.1038/s41586-025-09564-0.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
There is growing interest in the relationship between Alzheimer’s disease (AD) and diabetes mellitus (DM), and the glucagon-like peptide-1 receptor (GLP-1R) may be an important link between these two diseases.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
The role of GLP-1R in DM is principally to regulate glycemic control by stimulating insulin secretion, inhibiting glucagon secretion, and improving insulin signaling, thereby reducing blood glucose levels.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In AD, GLP-1R attenuates the pathological features of AD through mechanisms such as anti-inflammatory effects, the reduction in amyloid-beta (Aβ) deposition, the promotion of Aβ clearance, and improvements in insulin signaling.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Notably, AD and DM share numerous pathophysiological mechanisms, most notably the disruption of insulin signaling pathways in the brain.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
These findings further underscore the notion that GLP-1R plays pivotal roles in both diseases.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Taken together, these findings lead us to conclude that GLP-1R not only plays an important role in the treatment of DM and AD but also may serve as a bridge between these two diseases.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Future research should focus on elucidating the detailed molecular mechanisms underlying the actions of GLP-1R in both diseases and exploring the development of GLP-1R agonists with dual therapeutic benefits for AD and DM.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
This could pave the way for innovative integrated treatment strategies to improve outcomes for patients affected by these intertwined conditions.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Alzheimer’s disease (AD) is a progressive neurodegenerative condition characterized by memory loss and cognitive dysfunction (Scheltens et al., 2021).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
According to statistics, there are currently approximately 50 million people living with AD worldwide, and this number is expected to increase to 152 million by 2050 as the population ages, making it a major challenge for global public health (Dissanayaka et al., 2024).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Despite extensive research and clinical trials conducted on the underlying mechanisms, the etiology and pathogenesis of AD remain incompletely understood.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
The glucagon-like peptide-1 receptor (GLP-1R) is a key target for diabetes mellitus (DM) treatment, and GLP-1R agonists are pharmaceutical compounds employed in the treatment of DM.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
However, recent studies have revealed the potential for these compounds to also impact the pathological process of AD.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
These impacts include anti-inflammatory effects, reduced amyloid-beta (Aβ) deposition, reduced tau protein hyperphosphorylation, and improved insulin signaling (Calsolaro and Edison, 2016; Kang et al., 2023).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Therefore, the utilization of GLP-1R medications in the treatment of AD may represent a promising approach.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Notably, AD and DM share multiple pathophysiological mechanisms, and in particular, both AD and type 2 DM (T2DM) disrupt insulin signaling pathways in the brain (Barone et al., 2021).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In addition, 60–70% of patients with T2DM suffer from cognitive impairment (Biessels and Despa, 2018).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Thus, GLP-1R may be a potential link between DM and AD, and we look forward to discovering more about the mechanism of the link between these two diseases, as well as new applications of GLP-1R agonists in the treatment of AD.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
GLP-1R plays a key role in AD.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
The role of GLP-1R in AD is reflected mainly in the following aspects: it can decrease Aβ deposition and inhibit tau protein hyperphosphorylation, reduce neuroinflammation and oxidative stress (OS) (Du et al., 2022).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Aβ is a protein fragment produced by the cleavage of amyloid precursor protein (APP) by a series of enzymes and is one of the key factors in AD research (Hardy and Selkoe, 2002; Sambamurti et al., 2002; Figure 1).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Two main forms of the Aβ protein have been identified: Aβ40 and Aβ42, which contain 40 and 42 amino acid residues respectively (Sambamurti et al., 2002).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In AD, the Aβ protein exists as insoluble aggregates that can form larger plaques called amyloid plaques or senile plaques, which are deposited in the brain and interfere with the function of nerve cells (Roher et al., 1996).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Abnormal accumulation of Aβ proteins is thought to be associated with neurodegenerative processes that may lead to disruption of communication between neurons, causing an inflammatory response and ultimately neuronal damage and death (Hardy and Allsop, 1991).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Therefore, an imbalance in the production and clearance of the Aβ protein is a key part of AD pathology.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Simplified schematic of the four major pathological changes present in the brains of patients with AD and the role of GLP-1R.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Multiple pathological changes, including Aβ deposition, tau protein hyperphosphorylation, neuroinflammation, and mitochondrial dysfunction, occur in the brains of patients with AD.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
GLP-1R activation plays significant modulatory roles in all these pathological mechanisms.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Several studies have confirmed that GLP-1R reduces Aβ production and deposition.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
GLP-1R agonists (e.g., exendin-4 and liraglutide) reduce APP expression and processing in the brains of AD model mice through the activation of GLP-1R, decrease Aβ protein production and plaque aggregation, and thus improve their spatial memory capacity (McClean et al., 2015; Wang et al., 2016).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Studies have shown that liraglutide reduces the numbers of Aβ and dense core plaques in the cortex by 40–50% (McClean et al., 2011).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In addition, defects in the insulin pathway lead to Aβ accumulation (Kellar and Craft, 2020).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Jantrapirom et al. reported that liraglutide effectively reversed the deleterious effects of insulin overstimulation and attenuated neuronal insulin resistance in the human neuroblastoma cell line SH-SY5Y, which resulted in reductions in β-amyloid formation and tau hyperphosphorylation (Jantrapirom et al., 2020).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
GLP-1R activation also enhances the clearance of Aβ.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
GLP-1R is expressed predominantly at perivascular sites in astrocytes of the normal mouse cerebral cortex.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Increased GLP-1R signaling promotes the phosphorylation and translocation of aquaporin 4, which may facilitate Aβ efflux clearance from the brain parenchyma by increasing intracerebral water flux (Sasaki et al., 2024).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In summary, GLP-1R can influence the pathological process of Aβ in diverse ways, including Aβ production, deposition and degradation.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Hyperphosphorylated tau is a major component of intracellular neurofibrillary tangles (NFTs), which, together with amyloid plaques, are a distinguishing marker of AD (Tracy et al., 2022; Figure 1).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Normally, tau proteins exist in a microtubule-bound form, but in AD, tau proteins become hyperphosphorylated, forming NFTs (Samudra et al., 2023).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
These NFTs accumulate inside neurons and interfere with intracellular transport, leading to impaired cell function and neuronal death (Macdonald et al., 2019).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In recent years, studies on the use of GLP-1R and GLP-1R agonists to reduce tau protein hyperphosphorylation have progressed.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Liraglutide and dulaglutide, as GLP-1R agonists, can improve AD-related cognitive dysfunction by inhibiting tau protein hyperphosphorylation and NFTs formation through activation of the protein kinase B/glycogen synthase kinase 3 beta (Akt/GSK-3β) signaling pathway (Shu et al., 2019; Zhou et al., 2019).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
This effect can be specifically blocked by the GLP-1R antagonist exendin (9–39) amide.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Furthermore, exendin-4 can stimulate the cyclic adenosine monophosphate/protein kinase A (cAMP-PKA) pathway by activating GLP-1R, which then increases the level of non-phosphorylated β-catenin to stimulate the Wnt/β-catenin/NeuroD1 pathway and inhibits the activity of GSK-3β, ultimately decreasing the hyperphosphorylation of AD-associated tau proteins regulated by GSK-3β (Kang et al., 2023).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In summary, GLP-1 agonists do not affect tau phosphatase activity but rather inhibit tau hyperphosphorylation by the activation of Akt-driven GSK-3β inhibition by GLP-1R during AD (Reich and Hölscher, 2022).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Although studies in animal models have shown that GLP-1R agonists reduce Aβaccumulation and tau hyperphosphorylation, few human studies have evaluated these effects.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Clinical trials are still needed to validate their safety and efficacy in human patients before they can be widely used in AD therapy.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
And Clinical trials have been conducted to investigate the potential cognitive benefits of GLP-1R agonists in patients with AD.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
For example, the REWIND trial revealed that dulaglutide may reduce the risk of cognitive decline in patients with T2DM (Cukierman-Yaffe et al., 2020; Table 1).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Novo Nordisk conducted a randomized, double-blind, placebo-controlled phase 2b clinical trial called ELAD to evaluate the neuroprotective effects of liraglutide in patients with mild AD (Femminella et al., 2019).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Unfortunately, its primary endpoint was not met due to study limitations.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In addition, two large-scale, double-blind, placebo-controlled phase 3 clinical studies called Evoke and Evoke + are underway to investigate the disease-mitigating potential of semaglutide in patients with AD with early symptoms and to explore its effects on AD biomarkers and neuroinflammation (Cummings et al., 2025).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
GLP-1R agonists show great potential in AD, but key challenges, such as blood brain barrier (BBB) penetration, clinical trial inconsistency, long-term safety and precision therapy, need to be addressed.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In the future, multitargeted drugs, novel delivery technologies, and individualized treatments may propel them to become breakthrough therapies for a wider range of diseases.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Summary of the mechanisms of action and effects of GLP-1R agonists in AD.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In addition to Aβ deposition and tau protein hyper- phosphorylation, pathological changes such as neuroinflammation and mitochondrial dysfunction are closely related to AD pathogenesis.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Research indicates that the activation of GLP-1R can alter the polarization of microglia, shifting them from a proinflammatory (M1) phenotype to an anti-inflammatory (M2) phenotype (Qian et al., 2022).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
This shift is crucial because the proinflammatory cytokines released by M1 microglia can exacerbate neuronal damage, whereas M2 microglia exert protective effects by promoting anti-inflammatory responses and repair processes (Jassam et al., 2017).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Therefore, GLP-1R is expressed in glial cells and has anti-inflammatory properties (Calsolaro and Edison, 2016).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
The activation of GLP-1R using agonists such as exendin-4 has been reported to reduce microglial activation and the production of proinflammatory cytokines (Qian et al., 2022).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
This effect contributes to the protection of neuronal tissue and the improvement of functional recovery after injury.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
OS is another key factor in AD, which leads to synaptic damage, and GLP-1R is able to reduce OS and protect synaptic structure and function (Kong et al., 2023; Liang et al., 2024).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
GLP-1R deletion impairs mitochondrial integrity in astrocytes, and a lack of GLP-1R signaling impairs mitochondrial function and induces a cellular stress response (Timper et al., 2020).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Recently, GLP-1 was shown to act on GLP-1R and exert its neuroprotective effects by promoting PTEN-induced kinase 1/Parkin-mediated mitochondrial autophagy and attenuating OS (Wang Y. et al., 2023).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
These findings further confirm the pleiotropic role of GLP-1R in neuroprotection.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Our previous chapter discussed the role of GLP-1R in AD.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Why is it that GLP-1R could be a potential link between DM and AD?
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
The mechanisms of action of GLP-1R in DM and AD overlap, which suggests that GLP-1R may be a bridge between these two diseases.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
For example, GLP-1R agonists were able to improve glucose metabolism function through the GLP-1R/SIRT1/GLUT4 pathway in an AD model (Wang Z. J. et al., 2023), suggesting that GLP-1R may influence AD progression by modulating metabolic pathways associated with DM.
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
In addition, GLP-1 activation in astrocytes by GLP-1R altered cellular glucose metabolism, revealing a novel mechanism by which GLP-1R improves cognitive function in patients with AD (Zheng et al., 2021).
PMC12328308
GLP-1R as a potential link between diabetes and Alzheimer’s disease
Taken together, these findings highlight the common mechanism of action of GLP-1R in DM and AD and its potential to regulate metabolism and neuroprotection (Figure 2), suggesting that GLP-1R may be a key factor linking these two diseases.