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Insulin-degrading enzyme: A link between insulin resistance and Alzheimer's disease
Sophiahemmet University.ORCID iD: 0000-0002-0785-7029
2023 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Background: Prior research has demonstrated an elevated risk of Alzheimer's disease (AD) among individuals diagnosed with type 2 diabetes mellitus (T2DM). Insulin resistance is a potential common link between these conditions, and it is associated with AD due to the insulin-degrading enzyme (IDE), which also degrades amyloid-β (Aβ) in the brain. It has been suggested that high insulin levels may hinder IDE's effective degradation of Aβ, contributing to plaque formation. IDE is measurable in blood and is a promising biomarker for AD risk assessment and diagnosis. IDE has been demonstrated to decrease in blood from patients with cognitive impairment, but the overall knowledge about IDE in human blood is sparse. The aim of the thesis was to increase knowledge of the relationship between insulin resistance and AD, focusing on IDE as a biomarker for risk assessment and diagnosis of AD.

Study participants: In study I, we included patients with type 2 diabetes (n=46) and compared them with patients without metabolic diseases (n=18). Serum samples were obtained from the Sophiahemmet biobank. In study II, we used post-mortem plasma samples from patients with Alzheimer's disease (n=18) and compared them with non-demented controls (n=6). These samples were obtained from the Netherlands Brain Bank. In study III, where we had three groups, we recruited patients with Alzheimer's disease (n=9) from a dementia care facility and healthy volunteers from Sophiahemmet University and Sophiahemmet Health Center (n=64). The serum samples from these individuals were then compared with serum samples from patients diagnosed with type 2 diabetes from Study I.

In Study IV, we utilized data from the Swedish BPSD (Behavioral and Psychological Symptoms of Dementia) registry. This registry is used by healthcare units that work with patients with neurocognitive disorders and contains information about the patient's diagnosis, drug treatment, and behavioral and psychological symptoms. We selected a group of AD patients prescribed some form of antidiabetic drug treatment and analyzed whether the type of treatment impacted the registered behavioral and psychological symptoms.

Methods: In study I-III, ELISA was used to analyze blood samples for levels of IDE and other metabolic markers. In study II, Luminex multiplex was used to measure inflammatory markers. These biomarkers and clinical data were analyzed statistically to investigate differences between groups and correlations between variables. In study IV, the association between BPSD and antidiabetic drug treatment was investigated using a bivariate logistic regression model, adjusted for age, sex, specific diagnosis, and drug treatment.

Results: The results showed that patients with T2DM had higher serum IDE levels than patients without metabolic diseases, patients diagnosed with AD, and healthy volunteers. The results also indicated that higher IDE levels were associated with older age, higher weight, and elevated blood glucose. In the samples from the brain bank, we found that higher IDE levels were correlated to increased levels of inflammatory markers and total tau.

In the analysis of registry data, we found that the prescription of metformin, one of the most common drugs for type 2 diabetes, was associated with lower odds for symptoms of depression and anxiety. This association was not observed for any other antidiabetic drug.

Conclusion: The results suggest that IDE may be an essential factor in metabolic function but may also be associated with significant risk factors for neurocognitive disorders, such as inflammation. Although based on smaller studies, these findings contribute to the limited knowledge of IDE in human blood. Reduced IDE levels have been linked to an increased risk of AD. If patients diagnosed with T2DM have elevated IDE levels, a decrease in IDE levels possibly would indicate that the patient is at higher risk of or even in an early stage of AD. As interest in blood-based biomarkers grows, IDE emerges as a stable and reliable candidate in this thesis. Additionally, the research raises attractive possibilities for enhancing treatment strategies for AD patients experiencing affective symptoms. Metformin is believed to increase IDE levels and has previously been suggested to treat affective disorders and AD. Further investigation is needed to explore this promising avenue.

Place, publisher, year, edition, pages
Stockholm: Sophiahemmet , 2023. , p. 78
Series
Sophiahemmet University Dissertations, ISSN 2004-7479, E-ISSN 2004-7460 ; 3
National Category
Health Sciences
Identifiers
URN: urn:nbn:se:shh:diva-5051ISBN: 978-91-988733-4-4 (print)ISBN: 978-91-988733-5-1 (electronic)OAI: oai:DiVA.org:shh-5051DiVA, id: diva2:1809802
Public defence
2023-12-01, Erforssalen, Sophiahemmet Högskola, Valhallavägen 91, hus R, Stockholm, 09:30 (Swedish)
Opponent
Supervisors
Available from: 2023-11-06 Created: 2023-11-06 Last updated: 2024-06-24Bibliographically approved
List of papers
1. Increased levels of insulin-degrading enzyme in patients with type 2 diabetes mellitus
Open this publication in new window or tab >>Increased levels of insulin-degrading enzyme in patients with type 2 diabetes mellitus
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2022 (English)In: Endocrine, ISSN 1355-008X, E-ISSN 1559-0100, Vol. 77, no 3, p. 561-565Article in journal (Refereed) Epub ahead of print
Abstract [en]

PURPOSE: Decreasing levels of serum insulin-degrading enzyme (IDE) have been associated with an increased risk for Alzheimer´s disease (AD) in patients with type 2 diabetes mellitus (T2DM). Research on serum IDE levels in patients with T2DM is sparse and the aim of this study was to explore serum levels of IDE in patients with T2DM.

METHOD: Blood serum samples were obtained from a biobank. Samples from subjects with T2DM and without metabolic disease were divided into subgroups; lifestyle treatment (n = 10), oral antidiabetic treatment (n = 17), insulin treatment (n = 20) and metabolically healthy controls (n = 18). Serum levels of IDE were analysed using specific ELISA assays.

RESULTS: Serum levels of IDE were elevated in subjects with T2DM compared to metabolically healthy individuals (p = 0.033). No significant differences were detected between treatment subgroups.

CONCLUSION: The present study indicates that patients with T2DM have increased serum IDE levels, compared to metabolically healthy individuals. However, for IDE to be clinically useful as a biomarker, its full function and possible use needs to be further elucidated in larger studies showing reproducible outcomes.

Keywords
Insulin resistance, Insulin-degrading enzyme, Type 2 diabetes mellitus
National Category
Endocrinology and Diabetes
Identifiers
urn:nbn:se:shh:diva-4539 (URN)10.1007/s12020-022-03123-7 (DOI)35751775 (PubMedID)
Available from: 2022-12-14 Created: 2022-12-14 Last updated: 2023-11-06Bibliographically approved
2. Correlation between insulin-degrading enzyme versus total tau and selected cytokines in patients with Alzheimer´s disease compared to non-demented controls.
Open this publication in new window or tab >>Correlation between insulin-degrading enzyme versus total tau and selected cytokines in patients with Alzheimer´s disease compared to non-demented controls.
2023 (English)In: Neuroendocrinology Letters, ISSN 2354-4716, Vol. 44, no 4, p. 199-205Article in journal (Refereed) Published
Abstract [en]

OBJECTIVE: It has been increasingly recognized that the pathological progress of Alzheimer´s disease (AD) is connected to metabolic function and inflammation. Insulin-degrading enzyme (IDE) is essential for glucose metabolism and the degradation of amyloid-β. We aimed to explore the associations between IDE, total tau, and cytokines levels in plasma from subjects with AD and non-demented controls.

METHODS AND MATERIAL: Plasma samples (18 patients diagnosed with AD and 6 non-demented controls) from the Netherlands Brain Bank were used to analyze IDE levels and total tau with an enzyme-linked immunosorbent assay. Cytokines were analyzed with Luminex custom plex assays for interleukin (IL)-6, IL-8, IL-10, and tumor necrosis factor-alpha (TNF-α). Results were analyzed using the Mann-Whitney U and Spearman´s rank correlation tests.

RESULTS: Total tau in plasma was significantly increased in AD subjects compared to non-demented control subjects (p = 0.044). Total tau was positively correlated with IDE levels in plasma in all subjects (r = 0.494, p = 0.017). Significant correlations could be demonstrated between plasma levels of IDE and IL-6 (r = 0.546, p = 0.019), IL-8 (r = 0.664, p = 0.003), IL-10 (r = 0.833, p < 0.001), and TNF-α (r = 0.633, p = 0.005) in subjects with AD, but not in non-demented controls.

CONCLUSION: Results from this study suggest that plasma IDE levels may be associated with inflammation and neurodegeneration and could potentially be a target for future diagnostic and treatment strategies.

National Category
Endocrinology and Diabetes
Identifiers
urn:nbn:se:shh:diva-5043 (URN)37466059 (PubMedID)
Available from: 2023-10-27 Created: 2023-10-27 Last updated: 2024-02-01Bibliographically approved
3. Correlations between insulin-degrading enzyme and metabolic markers in patients diagnosed with type 2 diabetes, Alzheimer's disease, and healthy controls: A comparative study
Open this publication in new window or tab >>Correlations between insulin-degrading enzyme and metabolic markers in patients diagnosed with type 2 diabetes, Alzheimer's disease, and healthy controls: A comparative study
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2024 (English)In: Endocrine, ISSN 1355-008X, E-ISSN 1559-0100, Vol. 84, no 2, p. 450-458Article in journal (Refereed) Published
Abstract [en]

PURPOSE: This study aimed to explore correlations between insulin-degrading enzyme (IDE) and markers of metabolic function in a group of patients diagnosed with type 2 diabetes mellitus (T2DM) or Alzheimer's disease (AD) and metabolically healthy volunteers.

METHOD: We included 120 individuals (47 with T2DM, 9 with AD, and 64 healthy controls). Serum levels of IDE were measured with commercial kits for ELISA. Differences in IDE levels between groups were analyzed with non-parametric ANCOVA, and correlations were analyzed with Spearman's rank correlations. We also investigated the influence of age, sex, and the use of insulin on the correlation using a non-parametric version of partial correlation.

RESULTS: Patients diagnosed with T2DM had higher IDE levels than patients diagnosed with AD and healthy controls after adjustment for age and sex. IDE was increasingly associated with body mass index (BMI), fasting blood glucose, C-peptide, hemoglobin A1c (HbA1c), insulin resistance, and triglycerides. In stratified analyses, we found a decreasing partial correlation between IDE and HbA1c in patients diagnosed with AD and a decreasing partial correlation between IDE and C-peptide in healthy controls. In patients diagnosed with T2DM, we found no partial correlations.

CONCLUSION: These results indicate that IDE is essential in metabolic function and might reflect metabolic status, although it is not yet a biomarker that can be utilized in clinical practice. Further research on IDE in human blood may provide crucial insights into the full function of the enzyme.

Keywords
Alzheimer’s disease, Insulin resistance, Insulin-degrading enzyme, Metabolic disorder, Serum, Type 2 diabetes mellitus
National Category
Endocrinology and Diabetes
Identifiers
urn:nbn:se:shh:diva-5079 (URN)10.1007/s12020-023-03603-4 (DOI)37980298 (PubMedID)
Note

As manuscript in dissertation.

Available from: 2023-11-23 Created: 2023-11-23 Last updated: 2024-06-24Bibliographically approved
4. Associations between the use of metformin and behavioral and psychological symptoms in patients with Alzheimer's disease, and type 2 diabetes mellitus: A register-based study
Open this publication in new window or tab >>Associations between the use of metformin and behavioral and psychological symptoms in patients with Alzheimer's disease, and type 2 diabetes mellitus: A register-based study
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2023 (English)In: Current Alzheimer Research, ISSN 1567-2050, E-ISSN 1875-5828, Vol. 20, no 2, p. 109-119Article in journal (Refereed) Published
Abstract [en]

BACKGROUND: Metformin, the first-line anti-diabetic drug treatment in patients with type 2 diabetes mellitus (T2DM), is suggested to be anti-inflammatory, antioxidative, and improve cognitive function, making it a promising contribution to treating Alzheimer´s disease (AD). However, the effect of metformin on behavioral and psychological symptoms of dementia (BPSD) in patients with AD has not been explored.

OBJECTIVE: To investigate the associations between metformin and BPSD in patients with AD and T2DM and explore possible interaction with other antidiabetic drugs.

METHODS: This cross-sectional study was based on data from the Swedish BPSD register. A total of 3745 patients with AD and antidiabetic drug treatment were included. Associations and interactions between antidiabetic drugs and BPSD were investigated by binary logistic regression.

RESULTS: The use of metformin was associated with lower odds for symptoms of depression (OR 0.77, CI (95%) 0.61-0.96, p = 0.022) and anxiety (OR 0.74, CI (95%) 0.58-0.94, p = 0.015) after adjustment for age, gender, specific diagnosis, and drugs. We could not demonstrate this association with another antidiabetic drug. Interaction effects were limited to an increasing association in eating and appetite disorders using metformin and other antidiabetic drugs (i.e., drugs other than insulin, sulfonylurea, or dipeptidyl peptidase-4 inhibitors).

CONCLUSION: The result of this study suggests that metformin could be beneficial for patients diagnosed with AD, other than for blood glucose control. Although, more knowledge is needed before assigning metformin a role in treating BPSD.

Keywords
Alzheimer' acute;s disease, BPSD, Depression, Metformin, Neuropsychiatric inventory, Register data, Type 2 diabetes mellitus
National Category
Endocrinology and Diabetes
Identifiers
urn:nbn:se:shh:diva-4925 (URN)10.2174/1567205020666230522102641 (DOI)37221687 (PubMedID)
Available from: 2023-05-26 Created: 2023-05-26 Last updated: 2023-11-06Bibliographically approved

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