Publications

Hope Center Member Publications: December 1, 2024

Two cardinal features of ALS, reduced STMN2 and pathogenic TDP-43, synergize to accelerate motor decline in mice(2025) Experimental Neurology

Two cardinal features of ALS, reduced STMN2 and pathogenic TDP-43, synergize to accelerate motor decline in mice
(2025) Experimental Neurology, 384, art. no. 115068, . 

Krus, K.L.a , Benitez, A.M.a , Strickland, A.b , Milbrandt, J.b c d , Bloom, A.J.b c , DiAntonio, A.a d

a Department of Developmental Biology, Washington University School of Medicine, St. Louis, 63110, United States
b Department of Genetics, Washington University School of Medicine, St. Louis, 63110, United States
c McDonnell Genome Institute, Washington University School of Medicine, St. Louis, 63110, United States
d Needleman Center for Neurometabolism and Axonal Therapeutics, St. Louis, 63110, United States

Abstract
Pathological TDP-43 loss from the nucleus and cytoplasmic aggregation occurs in almost all cases of ALS and half of frontotemporal dementia patients. Stathmin2 (Stmn2) is a key target of TDP-43 regulation and aberrantly spliced Stmn2 mRNA is found in patients with ALS, frontotemporal dementia, and Alzheimer’s Disease. STMN2 participates in the axon injury response and its depletion in vivo partially replicates ALS-like symptoms including progressive motor deficits and distal NMJ denervation. The interaction between STMN2 loss and TDP-43 dysfunction has not been studied in mice because TDP-43 regulates human but not murine Stmn2 splicing. Therefore, we generated trans-heterozygous mice that lack one functional copy of Stmn2 and express one mutant TDP-43Q331K knock-in allele to investigate whether reduced STMN2 function exacerbates TDP-43-dependent pathology. Indeed, we observe synergy between these two alleles, resulting in an early onset, progressive motor deficit. Surprisingly, this behavioral defect is not accompanied by detectable neuropathology in the brain, spinal cord, peripheral nerves or at neuromuscular junctions (NMJs). However, the trans-heterozygous mice exhibit abnormal mitochondrial morphology in their distal axons and NMJs. As both STMN2 and TDP-43 affect mitochondrial dynamics, and neuronal mitochondrial dysfunction is a cardinal feature of many neurodegenerative diseases, this abnormality likely contributes to the observed motor deficit. These findings demonstrate that partial loss of STMN2 significantly exacerbates TDP-43-associated phenotypes, suggesting that STMN2 restoration could ameliorate TDP-43 related disease before the onset of degeneration. © 2024 The Author(s)

Author Keywords
ALS;  FTD;  Neurodegeneration;  Neuropathy;  Stathmin;  STMN2;  TARDBP;  TDP-43

Funding details
Institute of Clinical and Translational SciencesICTS
National Center for Advancing Translational SciencesNCATS
National Institutes of HealthNIHRF1AG013730, R01NS119812, R01NS087632, R37NS065053
Georgia Clinical and Translational Science AllianceGaCTSA#UL1 TR002345

Document Type: Article
Publication Stage: Final
Source: Scopus

Cerebral Oxygen Metabolic Stress in Children and Adults With Large Vessel Vasculopathy Due to Sickle Cell Disease” (2024) Neurology

Cerebral Oxygen Metabolic Stress in Children and Adults With Large Vessel Vasculopathy Due to Sickle Cell Disease
(2024) Neurology, 103 (11), p. e210032. 

Wang, Y., Fellah, S., Reis, M., Guilliams, K.P., Fields, M.E., Steger-May, K., Mirro, A.E., Lewis, J.B., Ying, C., Cohen, R.A., Hulbert, M.L., King, A.A., Chen, Y., Lee, J.-M., An, H., Ford, A.L.

From the Department of Neurology (Y.W., S.F., K.G., M.E.F., J.B.L., Y.C., J.-M.L.), Mallinckrodt Institute of Radiology (M.R., K.G., M.E.F., C.Y., J.-M.L., H.A.), and Division of Pediatrics (K.G., A.E.M., M.L.H.), Center for Biostatistics and Data Science (K.S.-M.), Washington University School of Medicine; Washington University in St. Louis (R.A.C.); and Division of Hematology/Oncology (A.A.K., A.L.F.), Department of Medicine, Washington University School of Medicine, St. Louis, MO

Abstract
BACKGROUND AND OBJECTIVES: Large vessel vasculopathy (LVV), or moyamoya syndrome, increases the risk of stroke in patients with sickle cell disease (SCD), yet effective treatments are lacking. In atherosclerotic carotid disease, previous studies demonstrated elevated oxygen extraction fraction (OEF) as a predictor of ipsilateral stroke. In a SCD cohort, we examined hemispheric hemodynamic and oxygen metabolic dysfunction as tissue-based biomarkers of cerebral ischemic risk in patients with LVV. METHODS: Children and adults with SCD were recruited from a SCD clinic associated with a tertiary medical center and underwent prospective brain MRI and MR angiography. LVV was defined as ≥75% stenosis in a major anterior circulation artery, excluding occlusion or previous revascularization surgery. Baseline characteristics, cerebral blood flow (CBF), normalized OEF (nOEF), infarct volume, white matter microstructure, and brain volume were compared in hemispheres with vs without LVV. In a cross-sectional analysis, mixed-effects linear multivariable models examined the effect of LVV on: (1) CBF and nOEF, as tissue markers of hemodynamic and oxygen metabolic stress, respectively, and (2) endpoints of cerebral ischemic injury including infarct volume, white matter microstructure, and brain volume. RESULTS: Of 155 patients (22 [12-31] years, 57% female), 33 (21%) had ≥25% stenosis, 22 (14%) had ≥50% stenosis, 14 (9%) had 75%-99% stenosis, and 5 (3%) had 100% occlusion. After excluding hemispheres with previous revascularization surgery, LVV was present in 16 hemispheres from 11 patients. Hemispheres with (N = 16) vs without (N = 283) LVV had lower CBF (25.2 vs 32.1 mL/100 g/min, p = 0.01) and higher nOEF (0.99 vs 0.95, p = 0.02). On multivariable analysis, CBF was nonsignificantly lower (β = -0.16, p = 0.07) while nOEF remained higher in hemispheres with LVV (β = 0.04, p = 0.03). Moreover, LVV was associated with greater hemispheric infarct volume, microstructural disruption, and atrophy. DISCUSSION: Beyond greater infarct burden, LVV was associated with hemispheric atrophy and white matter microstructural injury. As an indicator of active hypoxia, elevated nOEF likely represents a compensatory response to flow-limiting stenosis in hemispheres with LVV. The study is limited by a small number of patients with severe stenosis. Future studies are needed to evaluate the potential of tissue-based CBF and nOEF in assessing stroke risk and guide timely treatment of vasculopathy in SCD.

Document Type: Article
Publication Stage: Final
Source: Scopus

Comparative neurofilament light chain trajectories in CSF and plasma in autosomal dominant Alzheimer’s disease” (2024) Nature Communications

Comparative neurofilament light chain trajectories in CSF and plasma in autosomal dominant Alzheimer’s disease
(2024) Nature Communications, 15 (1), art. no. 9982, . 

Hofmann, A.a b , Häsler, L.M.a b , Lambert, M.a b , Kaeser, S.A.a b , Gräber-Sultan, S.a , Obermüller, U.a b , Kuder-Buletta, E.a , la Fougere, C.a c , Laske, C.a b d , Vöglein, J.e f g , Levin, J.e f g , Fox, N.C.h , Ryan, N.S.h , Zetterberg, H.i j , Llibre-Guerra, J.J.k , Perrin, R.J.k l , Ibanez, L.k m n , Schofield, P.R.o p , Brooks, W.S.o q , Day, G.S.r , Farlow, M.R.s , Allegri, R.F.t , Chrem Mendez, P.t , Ikeuchi, T.u , Kasuga, K.u , Lee, J.-H.v , Roh, J.H.w , Mori, H.x , Lopera, F.y , Bateman, R.J.k , McDade, E.k , Gordon, B.A.z , Chhatwal, J.P.aa ab ac , Jucker, M.a b , Schultz, S.A.aa ab , Xu, J.z , Xu, X.ae , Xiong, C.ae , Wang, Q.z , Wang, G.ae , Vöglein, J.e f g , Vazquez, S.t , Surace, E.t , Supnet-Bell, C.ae , Stout, S.k , Stauber, J.k , Smith, H.ae , Smith, J.k , Simmons, A.ae , Seyfried, N.T.ah , Scott, J.ae , Sanchez-Valle, R.ao , Salloway, S.ag , Sabaredzovic, E.ae , Rosa-Neto, P.an , Roedenbeck, Y.e f g , Rizzo, J.ae , Ringman, J.am , Renton, A.E.af , Ramirez, L.y , Pulizos, C.ae , Picarello, D.M.af , Obermueller, U.a b , Noble, J.M.al , Niimi, Y.ak , Nicklaus, J.z , Nadkarni, N.K.ad , Morris, J.C.ae , Minton, M.ae , McKay, N.z , McCullough, A.z , Masters, C.aj , Massoumzadeh, P.ae , Martins, R.ai , Marsh, J.ae , Lu, R.ae , Li, Y.af , Levey, A.I.ah , Leon, Y.M.y , Koudelis, D.ae , Keefe, S.z , Karch, C.M.m , Joseph-Mathurin, N.z , Johnson, E.C.B.ah , Jerome, G.ae , Jarman, S.ae , Jackson, K.ae , Ikonomovic, S.ad , Huey, E.D.ag , Hornbeck, R.z , Holtzman, D.M.k , Herries, E.k , Hassenstab, J.k , Gremminger, E.ae , Graff-Radford, N.R.r , Graber-Sultan, S.ae , Goate, A.M.af , Franklin, E.l , Flores, S.z , Farlow, M.g , Fagan, A.M.k , Day, G.S.r , Daniels, A.J.ae , Cruchaga, C.m , Courtney, L.ae , Mendez, P.C.t , Chhatwal Chhatwal, J.P.aa ab ac , Chen, C.z , Chen, A.z , Cash, D.M.h , Berman, S.B.ad , Benzinger, T.z , Bechara, J.A.o , Bateman, R.k , Barthelemy, N.k , Baker, B.k , Aschenbrenner, A.J.k , Aguillon, D.y , Dominantly Inherited Alzheimer Networkap

a German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany
b Department of Cellular Neurology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
c Nuclear Medicine and Clinical Molecular Imaging, University Hospital Tübingen, Tübingen, Germany
d Section for Dementia Research, Hertie Institute for Clinical Brain Research and Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany
e German Center for Neurodegenerative Diseases (DZNE), Munich, Germany
f Department of Neurology, Ludwig Maximilians-Universität München, Munich, Germany
g Munich Cluster of Systems Neurology (SyNergy), Munich, Germany
h Dementia Research Centre, UCL Queen Square Institute of Neurology, London, United Kingdom
i Department Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, the Sahlgrenska Academy at the University of Gothenburg, Mölndal, Sweden
j Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden
k Department of Neurology, Washington University School of Medicine, St. Louis, MO, United States
l Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, United States
m Department of Psychiatry, Washington University School of Medicine, St. Louis, MO, United States
n NeuroGenomics and Informatics Center, Washington University School of Medicine, St. Louis, MO, United States
o Neuroscience Research Australia, Randwick, NSW, Australia
p School of Biomedical Sciences, Faculty of Medicine and Health, University of New South Wales, Sydney, Australia
q School of Clinical Medicine, Faculty of Medicine and Health Sydney, University of New South Wales, Sydney, Australia
r Department of Neurology, Mayo Clinic in Florida, Jacksonville, FL, United States
s Indiana Alzheimer Disease Center and Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, IN, United States
t Instituto Neurológico FLENI, Buenos Aires, Argentina
u Brain Research Institute, Niigata University, Niigata, Japan
v Department of Neurology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, South Korea
w Departments of Neurology and Physiology, Korea University Anam Hospital, Korea University College of Medicine, Seoul, South Korea
x Faculty of Medicine, Osaka Metropolitan University, Nagaoka Sutoku University, Osaka, Japan
y Grupo de Neurociencias de Antioquia (GNA), Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia
z Department of Radiology, Washington University School of Medicine, St. Louis, MO, United States
aa Department of Neurology, Harvard Medical School, Boston, MA, United States
ab Massachusetts General Hospital, Boston, MA, United States
ac Brigham and Women’s Hospital Boston, Boston, MA, United States
ad University of Pittsburgh, Pittsburgh, PA, United States
ae Washington University in St. Louis, School of Medicine, St. Louis, MO, United States
af Dept. of Genetics & amp; Genomic Sciences, Dept. of Neuroscience, Ronald M. Loeb Center for Alzheimer’s disease, Icahn School of Medicine at Mount Sinai, Mount Sinai, NY, United States
ag Memory and Aging Program, Butler Hospital, Departments of Psychiatry and Human Behavior and Neurology, Alpert Medical School, Brown University, Providence, RI, United States
ah Goizueta Alzheimer’s Disease Research Center, Emory University, Atlanta, GA, United States
ai Edith Cowan University, Joondalup, Australia
aj Florey Institute, The University of Melbourne, Melbourne, Australia
ak Specially appointed lecturer, Unit for Early and Exploratory Clinical Development, The University of Tokyo, Tokyo, Japan
al Taub Institute for Research on Alzheimer’s Disease and the Aging Brain, G.H. Sergievsky Center, Department of Neurology, Columbia University Irving Medical Center, New York, NY, United States
am Department of Neurology, Keck School of Medicine of USC, University of Southern California, Los Angeles, CA, United States
an McGill University, Montreal, Canada
ao Hospital Clínic de Barcelona. FRCB-IDIBAPS. University of Barcelona, Barcelona, Spain

Abstract
Disease-modifying therapies for Alzheimer’s disease (AD) are likely to be most beneficial when initiated in the presymptomatic phase. To track the benefit of such interventions, fluid biomarkers are of great importance, with neurofilament light chain protein (NfL) showing promise for monitoring neurodegeneration and predicting cognitive outcomes. Here, we update and complement previous findings from the Dominantly Inherited Alzheimer Network Observational Study by using matched cross-sectional and longitudinal cerebrospinal fluid (CSF) and plasma samples from 567 individuals, allowing timely comparative analyses of CSF and blood trajectories across the entire disease spectrum. CSF and plasma trajectories were similar at presymptomatic stages, discriminating mutation carriers from non-carrier controls 10-20 years before the estimated onset of clinical symptoms, depending on the statistical model used. However, after symptom onset the rate of change in CSF NfL continued to increase steadily, whereas the rate of change in plasma NfL leveled off. Both plasma and CSF NfL changes were associated with grey-matter atrophy, but not with Aβ-PET changes, supporting a temporal decoupling of Aβ deposition and neurodegeneration. These observations support NfL in both CSF and blood as an early marker of neurodegeneration but suggest that NfL measured in the CSF may be better suited for monitoring clinical trial outcomes in symptomatic AD patients. © The Author(s) 2024.

Funding details
Deutsches Zentrum für Neurodegenerative ErkrankungenDZNE
Fleni
Ministry of Health and WelfareMOHW
Korea Dementia Research CenterKDRC
National Institute on AgingNIA
Korea Health Industry Development InstituteKHIDI
National Institutes of HealthNIHK01AG084816
National Institutes of HealthNIH
RS-2024-00344521
Alzheimer’s AssociationAASG-20-690363-DIAN
Alzheimer’s AssociationAA
Instituto de Salud Carlos IIIISCIIIAARF-21-846786
Instituto de Salud Carlos IIIISCIII
U19AG032438
Japan Agency for Medical Research and DevelopmentAMEDAMED JP23dk0207066, JP22dk0207049
Japan Agency for Medical Research and DevelopmentAMED

Document Type: Article
Publication Stage: Final
Source: Scopus

Polygenic score analyses on antidepressant response in late-life depression, results from the IRL-GRey study” (2024) Pharmacogenomics Journal

Polygenic score analyses on antidepressant response in late-life depression, results from the IRL-GRey study
(2024) Pharmacogenomics Journal, 24 (6), art. no. 38, . 

Elsheikh, S.S.M.a , Marshe, V.S.b , Men, X.a c , Islam, F.a c , Gonçalves, V.F.a c d e , Paré, G.f g h i , Felsky, D.a d e j , Kennedy, J.L.a d e , Mulsant, B.H.a d e , Reynolds, C.F., 3rdk , Lenze, E.J.l , Müller, D.J.a c d e m

a Campbell Family Mental Health Research Institute, Center for Addiction and Mental Health, Toronto, ON, Canada
b Columbia University Irving Medical Center, New York, NY, United States
c Department of Pharmacology & amp; Toxicology, University of Toronto, Toronto, ON, Canada
d Department of Psychiatry, University of Toronto, Toronto, ON, Canada
e Institute of Medical Science, University of Toronto, Toronto, ON, Canada
f Population Health Research Institute, David Braley Cardiac, Vascular and Stroke Research Institute, 237 Barton Street East, Hamilton, ON, Canada
g Thrombosis and Atherosclerosis Research Institute, David Braley Cardiac, Vascular and Stroke Research Institute, 237 Barton Street East, Hamilton, ON, Canada
h Department of Pathology and Molecular Medicine, Michael G. DeGroote School of Medicine, McMaster University, 1280 Main Street West, Hamilton, ON, Canada
i Department of Health Research Methods, Evidence, and Impact, McMaster University, Hamilton, ON, Canada
j Division of Biostatistics, Dalla Lana School of Public Health, University of Toronto, Toronto, ON, Canada
k Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, United States
l Healthy Mind Lab, Department of Psychiatry, Washington University, St. Louis, MO, United States
m Department of Psychiatry, Psychosomatics and Psychotherapy, Center of Mental Health, University Hospital of Würzburg, Würzburg, Germany

Abstract
Late-life depression (LLD) is often accompanied by medical comorbidities such as psychiatric disorders and cardiovascular diseases, posing challenges to antidepressant treatment. Recent studies highlighted significant associations between treatment-resistant depression (TRD) and polygenic risk score (PRS) for attention deficit hyperactivity disorder (ADHD) in adults as well as a negative association between antidepressant symptom improvement with both schizophrenia and bipolar. Here, we sought to validate these findings with symptom remission in LLD. We analyzed the Incomplete Response in Late Life Depression: Getting to Remission (IRL-GRey) sample consisting of adults aged 60+ with major depression (N = 342) treated with venlafaxine for 12 weeks. We constructed PRSs for ADHD, depression, schizophrenia, bipolar disorder, neuroticism, general intelligence, antidepressant symptom remission and antidepressant percentage symptom improvement using summary statistics from the Psychiatric Genomics Consortium and the GWAS Catalog. Logistic regression was used to test the association of PRSs with venlafaxine symptom remission and percentage symptom improvement, co-varying for the genomic principal components, age, sex and depressive symptoms severity at baseline. We found a nominal (i.e., p value ≤ 0.05) association between symptom remission and both PRS for ADHD and (OR = 1.36 [1.07, 1.73], p = 0.011) and PRS for bipolar disorder (OR = 0.75 [0.58, 0.97], p = 0.031), as well as between percentage symptom improvement and PRS for general intelligence (beta = 6.81 (SE = 3.122), p = 0.03). However, the ADHD association was in the opposite direction as expected, and both associations did not survive multiple testing corrections. Altogether, these findings suggest that previous findings regarding ADHD PRS and antidepressant response (measured with various outcomes) do not replicate in older adults. © The Author(s), under exclusive licence to Springer Nature Limited 2024.

Funding details
Canada Foundation for InnovationCFI
Centre for Addiction and Mental Health FoundationCAMH
Canadian Statistical Sciences InstituteCANSSI
Canadian Institutes of Health ResearchCIHR

Document Type: Article
Publication Stage: Final
Source: Scopus

Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroids” (2024) Translational Psychiatry

Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroids
(2024) Translational Psychiatry, 14 (1), art. no. 474, . 

Izumi, Y.a b , Reiersen, A.M.a b , Lenze, E.J.a b , Mennerick, S.J.a b , Zorumski, C.F.a b

a Department of Psychiatry & amp; Taylor Family Institute for Innovative Psychiatric Research, Washington University School of Medicine, St. Louis, MO, United States
b Center for Brain Research in Mood Disorders, Washington University School of Medicine, St. Louis, MO, United States

Abstract
In addition to modulating serotonin transport, selective serotonin reuptake inhibitors (SSRIs) have multiple other mechanisms that may contribute to clinical effects, and some of these latter actions prompt repurposing of SSRIs for non-psychiatric indications. In a recent study of the SSRIs fluvoxamine, fluoxetine and sertraline we found that, unlike the other two SSRIs, sertraline acutely inhibited LTP at a low micromolar concentration through inverse agonism of sigma 1 receptors (S1Rs). In the present studies, we pursued mechanisms contributing to sertraline modulation of LTP in rat hippocampal slices. We found that sertraline partially inhibits synaptic responses mediated by N-methyl-D-aspartate receptors (NMDARs) via effects on NMDARs that contain GluN2B subunits. A selective S1R antagonist (NE-100), but not an S1R agonist (PRE-084) blocked effects on NMDARs, even though both S1R ligands were previously shown to prevent LTP inhibition. Both NE-100 and PRE-084, however, prevented adverse effects of sertraline on one-trial learning. Because of the important role that S1Rs play in modulating endoplasmic reticulum stress, we examined whether inhibitors of cellular stress alter effects of sertraline. We found that two stress inhibitors, ISRIB and quercetin, prevented LTP inhibition, as did inhibitors of the synthesis of endogenous neurosteroids, which are homeostatic regulators of cellular stress. These studies highlight complex effects of sertraline, S1Rs and neurosteroids on hippocampal function and have relevance for understanding therapeutic and adverse drug actions. © The Author(s) 2024.

Document Type: Article
Publication Stage: Final
Source: Scopus

Mitochondrial pyruvate transport regulates presynaptic metabolism and neurotransmission” (2024) Science Advances

Mitochondrial pyruvate transport regulates presynaptic metabolism and neurotransmission
(2024) Science Advances, 10 (46), art. no. eadp7423, . 

Tiwari, A.a , Myeong, J.a , Hashemiaghdam, A.a , Stunault, M.I.a , Zhang, H.b , Niu, X.b , Laramie, M.A.a , Sponagel, J.a , Shriver, L.P.b , Patti, G.J.b , Klyachko, V.A.a , Ashrafi, G.a c

a Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, MO, United States
b Department of Chemistry, Department of Medicine, Center for Mass Spectrometry and Metabolic Tracing, Washington University in St. Louis, St. Louis, MO, United States
c Needleman Centerfor Neurometabolism and Axonal Therapeutics, Washington University School of Medicine, St. Louis, MO, United States

Abstract
Glucose has long been considered the primary fuel source for the brain. However, glucose levels fluctuate in the brain during sleep or circuit activity, posing major metabolic stress. Here, we demonstrate that the mammalian brain uses pyruvate as a fuel source, and pyruvate can support neuronal viability in the absence of glucose. Nerve terminals are sites of metabolic vulnerability, and we show that mitochondrial pyruvate uptake is a critical step in oxidative ATP production in hippocampal terminals. We find that the mitochondrial pyruvate carrier is post-translationally modified by lysine acetylation, which, in turn, modulates mitochondrial pyruvate uptake. Our data reveal that the mitochondrial pyruvate carrier regulates distinct steps in neurotransmission, namely, the spatiotemporal pattern of synaptic vesicle release and the efficiency of vesicle retrieval—functions that have profound implications for synaptic plasticity. In summary, we identify pyruvate as a potent neuronal fuel and mitochondrial pyruvate uptake as a critical node for the metabolic control of neurotransmission in hippocampal terminals. © 2024 The Authors, some rights reserved;

Funding details
Center for Cellular Imaging, Washington UniversityWUCCI
Institute of Clinical and Translational SciencesICTS
Whitehall Foundation
Alvin J. Siteman Cancer CenterSCC
National Institute of Neurological Disorders and StrokeNINDS
Office of Research Infrastructure ProgramsORIP, NIH
Genome Technology Access CenterGTAC
National Center for Research ResourcesNCRR
National Center for Advancing Translational SciencesNCATS
University of WashingtonUW
Ul1TR002345
National Cancer InstituteNCI#P30 CA91842
Georgia Clinical and Translational Science AllianceGaCTSAUL1TR002345
National Institute of General Medical SciencesNIGMSR35 NS111596, R35GM147222
National Institutes of HealthNIHOD021629

Document Type: Article
Publication Stage: Final
Source: Scopus

Hippocampal volumes in UK Biobank are associated with APOE only in older adults” (2024) Alzheimer’s and Dementia: Diagnosis, Assessment and Disease Monitoring

Hippocampal volumes in UK Biobank are associated with APOE only in older adults
(2024) Alzheimer’s and Dementia: Diagnosis, Assessment and Disease Monitoring, 16 (4), art. no. e70024, . 

Chaloemtoem, A.a , Thornton, V.a , Chang, Y.a , Anokhin, A.P.a , Belloy, M.E.b c , Bijsterbosch, J.d , Gordon, B.A.b d , Hartz, S.M.a , Bierut, L.J.a

a Department of Psychiatry, Washington University School of Medicine, St. Louis, MO, United States
b NeuroGenomics and Informatics Center, Washington University School of Medicine, St. Louis, MO, United States
c Department of Neurology, Washington University School of Medicine, St. Louis, MO, United States
d Department of Radiology, Washington University School of Medicine, St. Louis, MO, United States

Abstract
INTRODUCTION: The hippocampus atrophies with age and is implicated in neurodegenerative disorders including Alzheimer’s disease (AD). We examined the interplay between age and apolipoprotein E (APOE) genotype on total hippocampal volume. METHODS: Using neuroimaging data from 37,463 UK Biobank participants, we applied linear regression to quantify the association of age and APOE with hippocampal volume and identified the age when volumes of ε2/ε3, ε3/ε4, and ε4/ε4 carriers significantly deviated from ε3/ε3 using generalized additive modeling. RESULTS: Total hippocampal volume declined with age, with significant differences by APOE genotype emerging after age 60. ε3/ε4 and ε4/ε4 carriers displayed reduced volumes from ages 69 and 61, respectively, while ε2/ε3 showed delayed decline starting at the age of 76. DISCUSSION: The association of APOE and hippocampal volume is age-dependent, with differences in volumes of ε4/ε4 carriers detected as early as age 61. This work underscores the importance of APOE genotype in determining when to begin screening for AD. Highlights: Apolipoprotein E (APOE) genotype shows an age-dependent association with total hippocampal volume. No association between APOE and total hippocampal volume was detected before age 60. Accelerated decline was observed in ε4/ε4 carriers at age 61 and ε3/ε4 at age 69. Delayed decline was evident in ε2/ε3 carriers starting at age 76. © 2024 The Author(s). Alzheimer’s & Dementia: Diagnosis, Assessment & Disease Monitoring published by Wiley Periodicals LLC on behalf of Alzheimer’s Association.

Author Keywords
age;  Alzheimer’s disease;  apolipoprotein E;  hippocampus;  neurodegeneration;  UK Biobank

Funding details
National Institutes of HealthNIH
National Institute on Alcohol Abuse and AlcoholismNIAAAU10AA008401, R01AA027049, R01AA029308
National Institute on Alcohol Abuse and AlcoholismNIAAA
National Institute of Child Health and Human DevelopmentNICHDR21HD112910, R01AA025646
National Institute of Child Health and Human DevelopmentNICHD
Institute of Clinical and Translational SciencesICTS47267, 48123, TL1TR002344
Institute of Clinical and Translational SciencesICTS
National Institute on AgingNIARF1AG079569, R01AG065234, RF1AG082030, U19AG032438, R01AG070139, P01AG026276, RF1AG073424, R01AG073267
National Institute on AgingNIA
National Institute on Drug AbuseNIDAR01DA058114
National Institute on Drug AbuseNIDA
National Institute of Mental HealthNIMHR01MH132962, R01MH128286, R00AG075238
National Institute of Mental HealthNIMH

Document Type: Article
Publication Stage: Final
Source: Scopus

Unlocking Cognitive Analysis Potential in Alzheimer’s Disease Clinical Trials: Investigating Hierarchical Linear Models for Analyzing Novel Measurement Burst Design Data” (2024) Statistics in Medicine

Unlocking Cognitive Analysis Potential in Alzheimer’s Disease Clinical Trials: Investigating Hierarchical Linear Models for Analyzing Novel Measurement Burst Design Data
(2024) Statistics in Medicine, . 

Wang, G.a b , Hassenstab, J.a , Li, Y.a , Aschenbrenner, A.J.a , McDade, E.M.a , Llibre-Guerra, J.a , Bateman, R.J.a , Xiong, C.b

a Department of Neurology, Washington University School of Medicine, St. Louis, MO, United States
b Division of Biostatistics, Washington University School of Medicine, St. Louis, MO, United States

Abstract
Measurement burst designs typically administer brief cognitive tests four times per day for 1 week, resulting in a maximum of 28 data points per week per test for every 6 months. In Alzheimer’s disease clinical trials, utilizing measurement burst designs holds great promise for boosting statistical power by collecting huge amount of data. However, appropriate methods for analyzing these complex datasets are not well investigated. Furthermore, the large amount of burst design data also poses tremendous challenges for traditional computational procedures such as SAS mixed or Nlmixed. We propose to analyze burst design data using novel hierarchical linear mixed effects models or hierarchical mixed models for repeated measures. Through simulations and real-world data applications using the novel SAS procedure Hpmixed, we demonstrate these hierarchical models’ efficiency over traditional models. Our sample simulation and analysis code can serve as a catalyst to facilitate the methodology development for burst design data. © 2024 John Wiley & Sons Ltd.

Author Keywords
Alzheimer’s disease;  hierarchical linear mixed effects model;  hierarchical mixed models for repeated measures;  measurement burst design data;  SAS

Funding details
National Institute on AgingNIAR01 AG059798, R01AG057840
National Institute on AgingNIA
GHR FoundationGHRR01AG057840
GHR FoundationGHR
National Institutes of HealthNIHU19 AG032438, U01 AG042791‐01A1
National Institutes of HealthNIH

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Benchmarking of a multi-biomarker low-volume panel for Alzheimer’s disease and related dementia research” (2024) Alzheimer’s and Dementia

Benchmarking of a multi-biomarker low-volume panel for Alzheimer’s disease and related dementia research
(2024) Alzheimer’s and Dementia, . 

Ibanez, L.a b c , Liu, M.a c , Beric, A.a c , Timsina, J.a c , Kohlfeld, P.a c , Bergmann, K.a c , Lowery, J.a c , Sykora, N.a c , Sanchez-Montejo, B.a c , Brock, W.a c , Budde, J.P.a c , Bateman, R.J.b d e f , Barthelemy, N.b e , Schindler, S.E.b d f , Holtzman, D.M.b d f , Benzinger, T.L.S.d f g , Xiong, C.h , Tarawneh, R.i , Moulder, K.b f , Morris, J.C.b f , Sung, Y.J.a c , Cruchaga, C.a b c d f j

a Department of Psychiatry, Washington University School of Medicine, St. Louis, MO, United States
b Department of Neurology, Washington University School of Medicine, St. Louis, MO, United States
c NeuroGenomics and Informatics Center, Washington University School of Medicine, St. Louis, MO, United States
d Hope Center for Neurologic Diseases, Washington University School of Medicine, St. Louis, MO, United States
e The Tracy Family SILQ Center, Washington University School of Medicine, St. Louis, MO, United States
f Knight Alzheimer Disease Research Center, Washington University School of Medicine, St. Louis, MO, United States
g Department of Radiology, Washington University School of Medicine, St. Louis, MO, United States
h Division of Biostatistics, Washington University School of Medicine, St. Louis, MO, United States
i Department of Neurology, University of New Mexico School of Medicine, Albuquerque, NM, United States
j Department of Genetics, Washington University School of Medicine, St. Louis, MO, United States

Abstract
INTRODUCTION: In the research setting, obtaining accurate established biomarker measurements and maximizing use of the precious samples is key. Accurate technologies are available for Alzheimer’s disease (AD), but no platform can measure all the established and emerging biomarkers in one run. The NUcleic acid Linked Immuno-Sandwich Assay (NULISA) is a technology that requires 15 µL of sample to measure more than 100 analytes. METHODS: We compared AD-relevant biomarkers included in the NULISA against validated assays in cerebrospinal fluid (CSF) and plasma. RESULTS: CSF measures of amyloid beta 42/40, and phosphorylated tau (p-tau)217 are highly correlated when measured by immunoassay, mass spectrometry, or NULISA. In plasma, p-tau217 performance is similar to that reported with other technologies when predicting amyloidosis. Other biomarkers show a wide range of correlation values depending on the fluid and the platform. DISCUSSION: The NULISA multiplexed platform produces reliable results for established biomarkers in CSF that are useful in research settings, with the advantage of measuring additional biomarkers using minimal sample volume. Highlights: We tested the novel technology NUcleic acid Linked Immuno-Sandwich Assay (NULISA) in the dementia research setting. NULISA multiplexed platform produces reliable results for established and emerging biomarkers using minimal sample volume. Cerebrospinal fluid measures of amyloid beta 42/40, and phosphorylated tau (p-tau)217 are highly correlated when measured by immunoassay, mass spectrometry, or NULISA. In plasma, p-tau217 performance is similar to that reported with other technologies when predicting amyloidosis. NULISA measures are useful in research settings, with the advantage of measuring additional biomarkers using minimal sample volume. © 2024 The Author(s). Alzheimer’s & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer’s Association.

Author Keywords
amyloidosis biomarkers;  biomarkers;  multiplex;  NUcleic acid Linked Immuno-Sandwich Assay

Funding details
Hope Center for Neurological Disorders, Washington University in St. Louis
Chan Zuckerberg InitiativeCZI
Michael J. Fox Foundation for Parkinson’s ResearchMJFF
Alzheimer’s Drug Discovery FoundationADDF
National Institutes of HealthNIHRF1AG053303, P01AG003991, U01AG058922, R01AG044546, RF1AG074007, R01AG070941, RF1AG058501, K99/R00‐AG062723
National Institutes of HealthNIH
Alzheimer’s AssociationAAZEN‐22‐848604
Alzheimer’s AssociationAA
Division of Social and Economic SciencesSESRF1AG083744
Division of Social and Economic SciencesSES
U.S. Department of DefenseDODW81XWH2010849
U.S. Department of DefenseDOD
P30AG066444, P01AG03991, P01AG026276

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Stereospecific Properties and Intracellular Transport of Novel Intrinsically Fluorescent Neurosteroids” (2024) ACS Chemical Neuroscience

Stereospecific Properties and Intracellular Transport of Novel Intrinsically Fluorescent Neurosteroids
(2024) ACS Chemical Neuroscience, . 

Akkerman, V.a , Reinholdt, P.b , Schnoor-Madsen, R.a , Lauritsen, L.a , Bader, J.c , Qian, M.d , Xu, Y.d , Akk, G.c , Scheidt, H.A.e , Müller, P.f , Covey, D.F.g , Evers, A.S.g , Kongsted, J.b , Wüstner, D.a

a Department of Biochemistry and Molecular Biology, University of Southern Denmark, Campusvej 55, Odense M, DK-5230, Denmark
b Department of Physics, Chemistry and Pharmacy, University of Southern Denmark, Campusvej 55, Odense M, DK-5230, Denmark
c Department of Anesthesiology, Washington University in St. Louis, St. Louis, MO 63110, United States
d Department of Developmental Biology, Washington University in St. Louis, St. Louis, MO 63110, United States
e Institute for Medical Physics and Biophysics, Leipzig University, Härtelstr. 16-18, Leipzig, 04107, Germany
f Department of Biology, Humboldt University Berlin, Invalidenstr. 42, Berlin, 10115, Germany
g Department of Developmental Biology, Taylor Family Institute for Innovative Psychiatric Research, Washington University in St. Louis, St. Louis, MO 63110, United States

Abstract
Allopregnanolone (AlloP) is an example of neuroactive steroids (NAS), which is a potent allosteric activator of the γ-aminobutyric acid A (GABAA) receptor. The mechanisms underlying the biological activity of AlloP and other NAS are only partially understood. Here, we present intrinsically fluorescent analogs of AlloP (MQ-323) and its 3β-epimer, epi-allopregnanolone (E-AlloP) (YX-11), and show, by a combination of spectroscopic and computational studies, that these analogs mimic the membrane properties of AlloP and E-AlloP very well. We found stereospecific differences in the orientation and dynamics of the NAS as well as in their impact on membrane permeability. However, all NAS are unable to condense the lipid bilayer, in stark contrast to cholesterol. Using Förster resonance energy transfer (FRET) and electrophysiological measurements, we show that MQ-323 but not YX-11 binds at the intersubunit site of the ELICα1GABAA receptor and potentiates GABA-induced receptor currents. In aqueous solvents, YX-11 forms aggregates at much lower concentrations than MQ-323, and loading both analogs onto cyclodextrin allows for their uptake by human astrocytes, where they become enriched in lipid droplets (LDs), as shown by quantitative fluorescence microscopy. Trafficking of the NAS analogs is stereospecific, as uptake and lipid droplet targeting is more pronounced for YX-11 compared to MQ-323. In summary, we present novel minimally modified analogs of AlloP and E-AlloP, which enable us to reveal stereospecific membrane properties, allosteric receptor activation, and intracellular transport of these neurosteroids. Our fluorescence design strategy will be very useful for the analysis of other NAS in the future. © 2024 American Chemical Society.

Author Keywords
allopregnanolone;  astrocytes;  fluorescence;  microscopy;  probes;  trafficking

Funding details
National Institutes of HealthNIH
National Institute of General Medical SciencesNIGMSR35GM149287, R35GM140947, 1 P50 MH122379
National Institute of General Medical SciencesNIGMS
Deutsche ForschungsgemeinschaftDFGMU 1017/14-1
Deutsche ForschungsgemeinschaftDFG
Lundbeck FoundationR366-2021-226
Lundbeck Foundation

Document Type: Article
Publication Stage: Article in Press
Source: Scopus

Family income and polygenic scores are independently but not interactively associated with cognitive performance among youth genetically similar to European reference populations” (2024) Development and Psychopathology

Family income and polygenic scores are independently but not interactively associated with cognitive performance among youth genetically similar to European reference populations
(2024) Development and Psychopathology, . 

Paul, S.E.a , Elsayed, N.M.a , Colbert, S.M.C.b , Bogdan, R.a , Hatoum, A.S.a , Barch, D.M.a b c

a Department of Psychological and Brain Sciences, Washington University in St. Louis, St. Louis, United States
b Department of Psychiatry, Washington University, School of Medicine, St. Louis, United States
c Department of Radiology, Washington University, School of Medicine, St. Louis, United States

Abstract
Cognitive abilities are heritable and influenced by socioeconomic status (SES). It is critical to understand the association between SES and cognition beyond genetic propensity to inform potential benefits of SES-based interventions and to determine if such associations vary across (i) cognitive domains, (ii) facets of SES, and/or (iii) genetic propensity for different aspects of cognition. We examined the contributions of neighborhood socioeconomic advantage, family income, and polygenic scores (PGS) for domains of cognition (i.e., general cognitive ability, executive function, learning and memory, fluid reasoning) in a sample of children (ages 9-10; n = 5549) most genetically similar to reference populations from Europe. With some variability across cognitive outcomes, family income and PGS were independently significantly associated with cognitive performance. Within-sibling analyses revealed that cognitive PGS associations were predominantly driven by between-family effects suggestive of non-direct genetic mechanisms. These findings provide evidence that SES and genetic propensity to cognition have unique associations with cognitive performance in middle childhood. These results underscore the importance of environmental factors and genetic influences in the development of cognitive abilities and caution against overinterpreting associations with PGS of cognitive and educational outcomes as predominantly direct genetic effects. © The Author(s), 2024.

Author Keywords
cognitive ability;  familial income;  gene-environment interaction;  neighborhood advantage;  polygenic risk scores

Document Type: Article
Publication Stage: Article in Press
Source: Scopus