Abstract Telomere length (TL) is associated with biological aging, consequently influencing the risk of age-related diseases such as Alzheimer’s disease (AD). We aimed to evaluate the potential causal role of TL in AD endophenotypes (i.e . , cognitive performance, N = 2233; brain age and AD-related signatures, N = 1134; and cerebrospinal fluid biomarkers (CSF) of AD and neurodegeneration, N = 304) through a Mendelian randomization (MR) analysis. Our analysis was conducted in the context of the ALFA (ALzheimer and FAmilies) study, a population of cognitively healthy individuals at risk of AD. A total of 20 single nucleotide polymorphisms associated with TL were used to determine the effect of TL on AD endophenotypes. Analyses were adjusted by age, sex, and years of education. Stratified analyses by APOE -ɛ4 status and polygenic risk score of AD were conducted. MR analysis revealed significant associations between genetically predicted longer TL and lower levels of CSF Aβ and higher levels of CSF NfL only in APOE -ɛ4 non-carriers. Moreover, inheriting longer TL was associated with greater cortical thickness in age and AD-related brain signatures and lower levels of CSF p-tau among individuals at a high genetic predisposition to AD. Further observational analyses are warranted to better understand these associations. Graphical Abstract
Abstract INTRODUCTION In 2013, the ALzheimer's and FAmilies (ALFA) project was established to investigate pathophysiological changes in preclinical Alzheimer's disease (AD), and to foster research on early detection and preventive interventions. METHODS We conducted a comprehensive genetic characterization of ALFA participants with respect to neurodegenerative/cerebrovascular diseases, AD biomarkers, brain endophenotypes, risk factors and aging biomarkers. We placed particular emphasis on amyloid/tau status and assessed gender differences. Multiple polygenic risk scores were computed to capture different aspects of genetic predisposition. We additionally compared AD risk in ALFA to that across the full disease spectrum from the Alzheimer's Disease Neuroimaging Initiative (ADNI). RESULTS Results show that the ALFA project has been successful at establishing a cohort of cognitively unimpaired individuals at high genetic predisposition of AD. DISCUSSION It is, therefore, well‐suited to study early pathophysiological changes in the preclinical AD continuum . Highlights Prevalence of ε4 carriers in ALzheimer and FAmilies (ALFA) is higher than in the general European population The ALFA study is highly enriched in Alzheimer's disease (AD) genetic risk factors beyond APOE AD genetic profiles in ALFA are similar to clinical groups along the continuum ALFA has succeeded in establishing a cohort of cognitively unimpaired individuals at high genetic AD risk ALFA is well suited to study pathogenic events/early pathophysiological changes in AD
Abstract In 2013, the ALFA (ALzheimer and FAmilies) project was established to investigate pathophysiological changes in preclinical Alzheimer’s disease (AD), and to foster research on early detection and preventive interventions. Since then, it has prospectively followed cognitively unimpaired late/middle-aged participants, most of whom are adult children of AD patients. Risk stratification of cognitively unimpaired individuals, including genetic factors is key for implementing AD prevention strategies. Here, we report the genetic characterization of ALFA participants with respect to neurodegenerative/cerebrovascular diseases, AD biomarkers, brain endophenotypes, risk factors and aging biomarkers, emphasizing amyloid/tau status and gender differences. We additionally compared AD risk in ALFA to that across the full disease spectrum from the Alzheimer’s Disease Neuroimaging Initiative (ADNI). Results show that the ALFA project has been successful at establishing a cohort of cognitively unimpaired individuals at high genetic risk of AD. It is, therefore, well-suited to study early pathophysiological changes in the preclinical AD continuum . Highlights Prevalence of ε4 carriers in ALFA is higher than in the general European population. The ALFA study is highly enriched in AD genetic risk factors beyond APOE . AD genetic profiles in ALFA are similar to clinical groups along the continuum . ALFA has succeeded in establishing a cohort of CU individuals at high genetic AD risk. ALFA is well suited to study pathogenic events/early pathophysiological changes in AD.
Abstract Background Alzheimer’s disease (AD) is a complex neurodegenerative disorder characterized by early changes in brain structure and cognitive function before the age of onset. This study investigated whether the genetic load for clinical AD and AD pathology predicts AD‐related brain and cognitive changes over a 3‐year period, targeting the preclinical phase in cognitively unimpaired (CU) middle‐aged individuals. Method The sample of the study was defined by 429 CU middle‐aged participants at risk of AD from the ALFA+ nested cohort with available information on genetics, brain imaging markers and cognitive data [Table 1]. A subset of them had information at two‐time points (N=367) [Figure 1]. Genetic predisposition for clinical AD (PRSAD and PRSADnoAPOE) and AD pathology (PRSAβ42‐CSF and PRSpTau‐CSF) were calculated. We used linear regression models to assess the association between each PRS and global amyloid PET deposition expressed in Centiloids, AD Dickerson MRI‐signature, hippocampal volume and cognitive outcomes, at baseline and rate of change over visits after controlling for confounders. PET and MRI outcomes were defined as the annual rate of change. Cognitive outcomes were z‐scores of the two‐time points difference. Models were adjusted for time between visits. Result At baseline, higher genetic predisposition to clinical AD was associated with increased amyloid‐PET levels and higher average thickness of AD‐affected regions. Additionally, higher PRSAD was associated with reduced AD‐related cognitive performance and worse language [Figure 2]. Over the three‐year period, AD‐genetic load predicted higher annual amyloid accumulation in the brain, independently of APOE . Conversely, genetic predisposition to higher CSF Aβ42 levels predicted lower annual rate of change for Centiloids. PRSAD was also associated with annual reduction of hippocampal volume. Finally, genetic predisposition to AD beyond the APOE region was associated with executive functioning rate of change [Figure 2]. Conclusion The results of this study showed the role of genetic predisposition to AD, affecting amyloid PET deposition, brain structure changes, and cognitive decline. These findings emphasized the importance of considering a comprehensive range of genetic markers in risk assessments for AD, particularly in its early stages, and highlight the potential of personalized genetic approaches to enhance predictions and interventions in the management of AD.
Abstract Background Aging is the primary risk factor for Alzheimer’s disease. Experiments in mice have identified circulating proteins with an “aging/rejuvenating” effect on the brain. However, whether these proteins have an effect on the human brain remains unknown. Here, we leverage genetic data to study links between the predicted plasma levels of these proteins and human brain age. Methods This study includes 1,394 cognitively unimpaired individuals of the ALFA study. Plasma proteins with an effect on mice brain aging were identified through a systematic review [ Figure 1 ]. Summary statistics data of protein quantitative trait loci (pQTLs) associated to these proteins in human (inclusion threshold<5×10 −5 ) were acquired from a previous study (Pietzner et al.,2021), and used for computing protein genetic scores (pPRS). For each ALFA cohort participant, DeltaAge scores was calculated by subtracting chronological age from MRI‐based estimation of brain age (Cumplido et al.,2022). Positive values are interpreted as brain age older than chronological age, and viceversa . The associations between brain DeltaAge measurements and pPRSs were assessed through general linear regression models stratified by sex, amyloid‐β (Aβ) status (CSF‐Aβ42/40<0.071 [Milà‐Alomà et al.,2020]) and APOE‐ε4 carriership. Results were reported for nominal and group‐correction (two experimental aging groups) level of significance (p<0.05, p<0.025, respectively). All pQTLs included in the significant pPRS were functionally annotated and an enrichment analysis was performed. Results Genetically predicted plasma levels of CSF2, VCAM1, HP, GHRH and BGLAP were associated with negative values of brain DeltaAge, while KLOTHO with positive values. Results for GHRH (Aβ+ and APOE‐ε4 non‐carriers) and BGLAP ( APOE‐ε4 carriers) remained significant after p‐value correction, with an effect in agreement with their brain rejuvenation role as found in mice [ Figure 2 ]. Enrichment analysis found immune response and complement activation processes associated with negative values of DeltaAge [ Figure 3 ]. Conclusions These results show that plasma levels of the brain aging/rejuvenating proteins discovered in mice may also influence human brain aging. In particular, genetically predicted levels of two rejuvenating factors in mice (BGLAP and GHRH) were associated with a younger brain age than chronological age. Follow‐up analyses will include protein level measurements to unravel the molecular complexity of brain aging.
AbstractBackground While numerous studies have identified blood proteins that modulate brain aging in mice, the direct translation of these findings to human health remains a substantial challenge. Bridging this gap is critical for developing interventions that can effectively target human brain aging and associated diseases.Methods We first identified 12 proteins with aging or rejuvenating properties in murine brains through a systematic review. Using protein quantitative trait loci data for these proteins, we developed polygenic scores to predict plasma protein levels, which we then validated in two independent human cohorts. We employed association models to explore the association between these genetically predicted protein levels and cognitive performance, focusing specifically on their interaction with key genetic markers such as sex, APOE-ε4 and Aβ42 status.Results Predicted plasma levels of Tissue Inhibitor of Metalloproteinases 2 (TIMP2) were significantly associated with improved global cognition and memory performance in humans, also when the models were stratified by sex, APOE-ε4, and Aβ42 status.Conclusions This finding aligns with TIMP2's brain-rejuvenating role in murine models, suggesting it as a promising therapeutic target for brain aging and age-related brain diseases in humans.
Abstract Background Evidence shows sex differences in cognitive performance in Alzheimer’s disease (AD). However, studies exploring whether genetic predisposition to AD differs in cognition among sex are scarce. We aimed to evaluate whether the influence of AD genetic liability in cognition differs among sex in cognitively unimpaired (CU) individuals in the AD continuum . Method We included 318 CU individuals from the ALFA+ cohort (Table 1). Cognitive change (∼3‐year follow‐up) was measured with a PACC and for individual cognitive domains. Polygenic scores estimating each participant’s genetic predisposition to AD were calculated with (PRS‐AD) and without (PRS‐ADnoAPOE) considering the APOE region (threshold = 5×10‐6). Amyloid positivity (Aβ+) was defined as cerebrospinal fluid (CSF) Aβ42/40<0.0071. Generalized linear models stratified by sex and amyloid status were performed to assess the association between cognitive change and genetic predisposition to AD. Models were corrected by age, years of education, and time between visits. Models were additionally corrected by baseline Jack’s cortical thickness AD signature as a marker of neurodegeneration. Result In Aβ+ women (n = 65), a higher genetic predisposition to AD was associated with steeper memory ( p PRS_AD = 0.04; p PRS_ADnoAPOE = 0.01) and executive function ( p PRS_ADnoAPOE = 0.001) decline after correcting by brain AD signature. In Aβ+ men (n = 44), a higher genetic predisposition to AD was associated with worse follow‐up performance on attention ( p PRS_AD = 0.05, p PRS_ADnoAPOE = 0.04), and results did not remain significant after correcting by brain AD signature (Figure 1). In Aβ‐, genetic predisposition to AD was also associated with executive function decline in women (n = 122) ( p PRS_AD = 0.16, p PRS_ADnoAPOE = 0.02), while Aβ‐ men (n = 87) showed worse follow‐up performance on visual processing ( p PRS_AD = 0.251, p PRS_ADnoAPOE = 0.001). Results remained significant after correcting by brain AD signature (Figure 2). Conclusion Our results showed that genetic predisposition to AD is associated with changes in different cognitive domains in men and women. These findings will contribute to developing precision medicine approaches in AD encompassing sex‐sensitive strategies for prevention.
Abstract Background Murine studies have identified blood proteins that influence brain aging, but translating these findings to humans remains challenging. We used an innovative approach to investigate whether genetically predicted blood levels of proteins linked to brain aging in animal models are associated with cognitive performance in individuals at risk of Alzheimer’s disease (AD) [ Figure 1 ]. Method Through systematic review, we identified 13 circulating proteins with an aging/rejuvenating effect on the mouse brain. We retrieved summary statistics of protein quantitative trait loci (pQTLs) associated with these proteins in human plasma from the Fenland study (Pietzner et al., 2021). We validated their predictive capacity by computing protein‐based genetic scores (protPRS) in 1,380 cognitively unimpaired (CU) individuals from the Knight‐ADRC cohort and analyzing their association with plasma protein levels (measured by Somalogic). We also computed the protPRS for 410 CU individuals at risk for AD from the ALFA+ study (60% women, 55% APOE‐ε4 carriers; Table 1 ) and assessed their associations with cognitive performance through linear models adjusted by age, sex, and years of education. Stratified models by sex, APOE‐ε4 carriership, and Aβ status were also assessed. pQTLs included in the significant scores were annotated to explore their biological significance. Result Most computed protPRS (10/13) significantly predicted plasma protein levels in the Knight‐ADRC cohort. In ALFA+, we found a significant association between genetic predisposition to elevated plasma TIMP2 (TIMP2‐protPRS) and better cognitive performance (PACC and episodic memory composites). Associations of TIMP2‐protPRS with PACC remained significant in stratified models [ Figure 2 ]. TIMP2‐protPRS was associated with the actual plasma TIMP2 levels in ALFA+. The annotated pQTLs included in the TIMP2‐protPRS were associated with traits related with cognition and neuropsychiatric disorders. We also found an age‐dependent expression of genes regulating blood TIMP2 levels in the human brain. Conclusion Protein‐based PRS computation may overcome translational challenges encountered in animal studies. Through this method, we showed that genetically predicted levels of plasma TIMP2, known for its rejuvenating effect on mice’s brain, are linked to cognitive performance in CU at risk of AD. This highlights TIMP2 as a potential therapeutic target for age‐related brain diseases.
Abstract Background Current evidence suggests that hippocampal subfields have partially different genetic architecture and may improve the sensitivity of the detection of Alzheimer’s disease (AD). In this study, we investigated whether genetic predisposition to AD contributes to the accelerated rate of hippocampal volume atrophy across sex and AD stages and how this contribution is specifically driven by functional variants located in the APOE gene. Methods The study comprised 1,051 participants from ADNI cohort (75.2 yo; 42.3% women), with complete demographic, genetic, and magnetic resonance imaging scans at baseline and every 6 months for a total of 96 months (Controls (amyloid negative), CUN = 363; mild cognitive impairment, MCIN = 474, AD patients, ADN = 214). Hippocampal subfields were extracted using the longitudinal processing method within FreeSurfer (v6.0). Genetic predisposition to AD was assessed through polygenic scoring with and without considering the APOE región. Effects of polygenicity of plasma APOE, functional APOE brain eQTLs and CSF pQTL were also considered. Linear mixed‐effect models with random‐ time slope and intercept for individuals were used to investigate the association between genetic predisposition to AD and hippocampal subfields volumetric trajectories over time. Models were adjusted by age, sex, AD disease status, years of education and total hippocampal volume. Disease and sex status‐specific trajectories dependent on genetics predisposition were assessed by including an interaction term. Results Significant hippocampal subfield volume reductions were observed, with more pronounced atrophy in MCI and AD participants [Figure 1A]. High genetic predisposition to AD was associated with accelerated atrophy in various subfields [Figure 1B]. MCI individuals with high genetic predisposition showed more severe atrophy in several subfields, with sex‐related differences observed, particularly in women [Figure 2]. Notably, these effects were non‐significant when excluding APOE variants. Further functional analyses pinpointed CSF pQTLS of the APOE gene and APOE‐e4 carriership status as primary drivers [Figure 3]. Conclusions Our findings underscore the significance of genetic predisposition, especially functional APOE variants, in understanding AD progression and sex‐specific trajectories. The results reveal varying atrophy patterns across disease stages, offering crucial insights for refining AD detection and tailoring interventions for more effective management.
Abstract INTRODUCTION Traditional brain imaging genetics studies have primarily focused on how genetic factors influence the volume of specific brain regions, often neglecting the overall complexity of brain architecture and its genetic underpinnings. METHODS This study analyzed data from participants across the Alzheimer’s disease (AD) continuum from the ALFA and ADNI studies. We exploited compositional data analysis to examine relative brain volumetric variations that (i) differentiate cognitively unimpaired (CU) individuals, defined as amyloid-negative (A-) based on CSF profiling, from those at different AD stages, and (ii) associated with increased genetic susceptibility to AD, assessed using polygenic risk scores. RESULTS Distinct brain signatures differentiated CU A-individuals from amyloid-positive MCI and AD. Moreover, disease stage-specific signatures were associated with higher genetic risk of AD. DISCUSSION The findings underscore the complex interplay between genetics and disease stages in shaping brain structure, which could inform targeted preventive strategies and interventions in preclinical AD.
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