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Article: The Metamorphic Nature of the Tau Protein: Dynamic Flexibility Comes at a Cost.

Sabbagh, Jonathan J / Dickey, Chad A

2016 Volume 10, Page(s) 3

Abstract: Accumulation of the microtubule associated protein tau occurs in several neurodegenerative diseases including Alzheimer's disease (AD). The tau protein is intrinsically disordered, giving it unique structural properties that can be dynamically altered by ...

Abstract	Accumulation of the microtubule associated protein tau occurs in several neurodegenerative diseases including Alzheimer's disease (AD). The tau protein is intrinsically disordered, giving it unique structural properties that can be dynamically altered by post-translational modifications such as phosphorylation and cleavage. Over the last decade, technological advances in nuclear magnetic resonance (NMR) spectroscopy and structural modeling have permitted more in-depth insights into the nature of tau. These studies have helped elucidate how metamorphism of tau makes it ideally suited for dynamic microtubule regulation, but how it also facilitates tau self-assembly, oligomerization, and neurotoxicity. This review will focus on how the distinct structure of tau governs its function, accumulation, and toxicity as well as how other cellular factors such as molecular chaperones control these processes.
Language	English
Publishing date	2016-01-21
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2411902-7
ISSN	1662-453X ; 1662-4548
ISSN (online)	1662-453X
ISSN	1662-4548
DOI	10.3389/fnins.2016.00003
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Article ; Online: Hippocampal Neurogenesis Is Enhanced in Adult Tau Deficient Mice.

Criado-Marrero, Marangelie / Sabbagh, Jonathan J / Jones, Margaret R / Chaput, Dale / Dickey, Chad A / Blair, Laura J

Cells

2020 Volume 9, Issue 1

Abstract: Tau dysfunction is common in several neurodegenerative diseases including Alzheimer's disease (AD) and frontotemporal dementia (FTD). Affective symptoms have often been associated with aberrant tau pathology and are commonly comorbid in patients with ... ...

Abstract	Tau dysfunction is common in several neurodegenerative diseases including Alzheimer's disease (AD) and frontotemporal dementia (FTD). Affective symptoms have often been associated with aberrant tau pathology and are commonly comorbid in patients with tauopathies, indicating a connection between tau functioning and mechanisms of depression. The current study investigated depression-like behavior in
MeSH term(s)	Animals ; Disease Models, Animal ; Hippocampus/metabolism ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Neurogenesis ; Neurons/cytology ; Neurons/metabolism ; tau Proteins/deficiency ; tau Proteins/metabolism
Chemical Substances	Mapt protein, mouse ; tau Proteins
Language	English
Publishing date	2020-01-14
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells9010210
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Article ; Online: Torpor Does Not Influence Spatial Memory in Hibernating Golden-Mantled Ground Squirrels (

Hensleigh, Emily / Murtishaw, Andrew S / Treat, Michael D / Heaney, Chelcie F / Bolton, Monica M / Sabbagh, Jonathan J / Calvin, Kirsten N / Kinney, Jefferson W / van Breukelen, Frank

Physiological and biochemical zoology : PBZ

2022 Volume 95, Issue 5, Page(s) 390–399

Abstract: AbstractMammalian hibernation in ground squirrels is characterized by periods of torpor wherein body temperature approaches ambient temperature and metabolism is reduced to as low as 1/100th of active rates. It is unclear how hibernation affects long- ... ...

Abstract	AbstractMammalian hibernation in ground squirrels is characterized by periods of torpor wherein body temperature approaches ambient temperature and metabolism is reduced to as low as 1/100th of active rates. It is unclear how hibernation affects long-term spatial memory, as tremendous remodeling of neurons is associated with torpor use. Given the suspected links between remodeling and memory formation and retention, we examined long-term spatial memory retention throughout a hibernation season. Animals were trained on a Barnes maze before entering torpor. Animals were tested for memory retention once a month throughout a hibernation season. Results indicate marked variation between individuals. Some squirrels retained memory across multiple torpor bouts, while other squirrels did not. No relationship was found between the number of torpor bouts, duration of bouts, or time spent torpid on long-term memory retention. However, that some squirrels successfully retain memory suggests that the profound remodeling of dendritic spines during torpor does not always lead to memory loss.
MeSH term(s)	Animals ; Body Temperature/physiology ; Hibernation/physiology ; Sciuridae/physiology ; Seasons ; Spatial Memory
Language	English
Publishing date	2022-08-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1473845-4
ISSN	1537-5293 ; 1522-2152
ISSN (online)	1537-5293
ISSN	1522-2152
DOI	10.1086/721185
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Article: Psychedelic Harm Reduction and Integration: A Transtheoretical Model for Clinical Practice.

Gorman, Ingmar / Nielson, Elizabeth M / Molinar, Aja / Cassidy, Ksenia / Sabbagh, Jonathan

Frontiers in psychology

2021 Volume 12, Page(s) 645246

Abstract: Psychedelic Harm Reduction and Integration (PHRI) is a transtheoretical and transdiagnostic clinical approach to working with patients who are using or considering using psychedelics in any context. The ongoing discussion of psychedelics in academic ... ...

Abstract	Psychedelic Harm Reduction and Integration (PHRI) is a transtheoretical and transdiagnostic clinical approach to working with patients who are using or considering using psychedelics in any context. The ongoing discussion of psychedelics in academic research and mainstream media, coupled with recent law enforcement deprioritization of psychedelics and compassionate use approvals for psychedelic-assisted therapy, make this model exceedingly timely. Given the prevalence of psychedelic use, the therapeutic potential of psychedelics, and the unique cultural and historical context in which psychedelics are placed, it is important that mental health providers have an understanding of the unique motivations, experiences, and needs of people who use them. PHRI incorporates elements of harm reduction psychotherapy and psychedelic-assisted psychotherapy, and can be applied in both brief and ongoing psychotherapy interactions. PHRI represents a shift away from assessment limited to untoward outcomes of psychedelic use and abstinence-based addiction treatment paradigms and toward a stance of compassionate, destigmatizing acceptance of patients' choices. Considerations for assessment, preparation, and working with difficult experiences are presented.
Language	English
Publishing date	2021-03-15
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2563826-9
ISSN	1664-1078
ISSN	1664-1078
DOI	10.3389/fpsyg.2021.645246
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Article: Roadmap for C9ORF72 in Frontotemporal Dementia and Amyotrophic Lateral Sclerosis: Report on the C9ORF72 FTD/ALS Summit.

Neurology and therapy

2023 Volume 12, Issue 6, Page(s) 1821–1843

Abstract: A summit held March 2023 in Scottsdale, Arizona (USA) focused on the intronic hexanucleotide expansion in the C9ORF72 gene and its relevance in frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS; C9ORF72-FTD/ALS). The goal of this ... ...

Abstract	A summit held March 2023 in Scottsdale, Arizona (USA) focused on the intronic hexanucleotide expansion in the C9ORF72 gene and its relevance in frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS; C9ORF72-FTD/ALS). The goal of this summit was to connect basic scientists, clinical researchers, drug developers, and individuals affected by C9ORF72-FTD/ALS to evaluate how collaborative efforts across the FTD-ALS disease spectrum might break down existing disease silos. Presentations and discussions covered recent discoveries in C9ORF72-FTD/ALS disease mechanisms, availability of disease biomarkers and recent advances in therapeutic development, and clinical trial design for prevention and treatment for individuals affected by C9ORF72-FTD/ALS and asymptomatic pathological expansion carriers. The C9ORF72-associated hexanucleotide repeat expansion is an important locus for both ALS and FTD. C9ORF72-FTD/ALS may be characterized by loss of function of the C9ORF72 protein and toxic gain of functions caused by both dipeptide repeat (DPR) proteins and hexanucleotide repeat RNA. C9ORF72-FTD/ALS therapeutic strategies discussed at the summit included the use of antisense oligonucleotides, adeno-associated virus (AAV)-mediated gene silencing and gene delivery, and engineered small molecules targeting RNA structures associated with the C9ORF72 expansion. Neurofilament light chain, DPR proteins, and transactive response (TAR) DNA-binding protein 43 (TDP-43)-associated molecular changes were presented as biomarker candidates. Similarly, brain imaging modalities (i.e., magnetic resonance imaging [MRI] and positron emission tomography [PET]) measuring structural, functional, and metabolic changes were discussed as important tools to monitor individuals affected with C9ORF72-FTD/ALS, at both pre-symptomatic and symptomatic disease stages. Finally, summit attendees evaluated current clinical trial designs available for FTD or ALS patients and concluded that therapeutics relevant to FTD/ALS patients, such as those specifically targeting C9ORF72, may need to be tested with composite endpoints covering clinical symptoms of both FTD and ALS. The latter will require novel clinical trial designs to be inclusive of all patient subgroups spanning the FTD/ALS spectrum.
Language	English
Publishing date	2023-10-17
Publishing country	New Zealand
Document type	Journal Article
ISSN	2193-8253
ISSN	2193-8253
DOI	10.1007/s40120-023-00548-8
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Article ; Online: Discordance Rate Among Bilateral Simultaneous and Sequential Temporal Artery Biopsies in Giant Cell Arteritis: Role of Frozen Sectioning Based on the Mayo Clinic Experience.

Cohen, Devon A / Chen, John J / Neth, Bryan J / Sabbagh, Nouran / Hodge, David / Warrington, Kenneth J / Fillmore, Jonathan / Maleszewski, Joseph J / Salomao, Diva R / Bhatti, M Tariq

JAMA ophthalmology

2021 Volume 139, Issue 4, Page(s) 406–413

Abstract: Importance: Frozen section temporal artery biopsy (TAB) may prevent a contralateral biopsy from being performed.: Objective: To evaluate the sensitivity and specificity of TAB frozen vs permanent section pathology results for giant cell arteritis ( ... ...

Abstract	Importance: Frozen section temporal artery biopsy (TAB) may prevent a contralateral biopsy from being performed. Objective: To evaluate the sensitivity and specificity of TAB frozen vs permanent section pathology results for giant cell arteritis (GCA) and determine the discordance rate of bilateral TABs. Design, setting, and participants: In this retrospective cohort study, medical records were reviewed from 795 patients 40 years or older who underwent TAB from January 1, 2010, to December 1, 2018, treated at a single tertiary care center with the ability to perform both frozen and permanent histologic sections. Data were analyzed from January 2019 to December 2020. Main outcomes and measures: Sensitivity and specificity of frozen section TAB for detecting GCA, and discordance rates of bilateral permanent section TAB. Results: Of the 795 included participants, 329 (41.4%) were male, and the mean (SD) age was 72 (10) years. From the 795 patients with 1162 TABs, 119 patients (15.0%) and 138 TABs had positive findings on permanent section. Of these 119 patients, 103 (86.6%) also had positive results on the frozen section, with 4 false-positives (0.6%) and 20 false-negatives (16.8%). Frozen section had a specificity of 99.4% (95% CI, 98.5-99.8), sensitivity of 83.2% (95% CI, 75.2-89.4), positive predictive value of 96.1% (95% CI, 90.4-98.9), negative predictive value of 96.6% (95% CI, 94.9-97.8), positive likelihood ratio of 140.6 (95% CI, 72.7-374.8), and a negative likelihood ratio of 0.17 (95% CI, 0.11-0.25). Simultaneous bilateral TABs were performed in 60 patients (7.5%) with a 5% discordance rate on permanent section. In comparison, bilateral frozen section-guided sequential TABs were performed in 307 patients (38.6%) with 5.5% discordance based on permanent section. In multivariate models, there was a greater odds of positive findings with age (odds ratio [OR], 1.04; 95% CI, 1.01-1.07; P = .008), vision loss (OR, 2.72; 95% CI, 1.25-5.75; P = .01), diplopia (OR, 3.33; 95% CI, 1.00-10.29; P = .04), headache (OR, 2.32; 95% CI, 1.25-4.53; P = .01), weight loss (OR, 2.37; 95% CI, 1.26-4.43; P = .007), and anorexia (OR, 5.65; 95% CI, 2.70-11.89; P < .001). Conclusions and relevance: These results support the hypothesis that negative findings from frozen sections should not be solely relied on to refute the diagnosis of GCA, whereas positive findings from frozen sections can be reliably used to defer a contralateral biopsy pending the permanent section results.
MeSH term(s)	Aged ; Biopsy/methods ; Female ; Frozen Sections ; Giant Cell Arteritis/diagnosis ; Humans ; Male ; Retrospective Studies ; Temporal Arteries/pathology
Language	English
Publishing date	2021-02-18
Publishing country	United States
Document type	Journal Article
ZDB-ID	2701705-9
ISSN	2168-6173 ; 2168-6165
ISSN (online)	2168-6173
ISSN	2168-6165
DOI	10.1001/jamaophthalmol.2020.6896
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Article ; Online: Targeting Hsp90 and its co-chaperones to treat Alzheimer's disease.

Blair, Laura J / Sabbagh, Jonathan J / Dickey, Chad A

Expert opinion on therapeutic targets

2014 Volume 18, Issue 10, Page(s) 1219–1232

Abstract: Introduction: Alzheimer's disease, characterized by the accumulation of hyperphosphorylated tau and β amyloid (Aβ), currently lacks effective treatment. Chaperone proteins, such as the heat shock protein (Hsp) 90, form macromolecular complexes with co- ... ...

Abstract	Introduction: Alzheimer's disease, characterized by the accumulation of hyperphosphorylated tau and β amyloid (Aβ), currently lacks effective treatment. Chaperone proteins, such as the heat shock protein (Hsp) 90, form macromolecular complexes with co-chaperones, which can regulate tau metabolism and Aβ processing. Although small molecule inhibitors of Hsp90 have been successful at ameliorating tau and Aβ burden, their development into drugs to treat disease has been slow due to the off- and on-target effects of this approach as well as challenges with the pharmacology of current scaffolds. Thus, other approaches are being developed to improve these compounds and to target co-chaperones of Hsp90 in an effort to limit these liabilities. Areas covered: This article discusses the most current developments in Hsp90 inhibitors including advances in blood-brain barrier permeability, decreased toxicity and homolog-specific small-molecule inhibitors. In addition, we discuss current strategies targeting Hsp90 co-chaperones rather than Hsp90 itself to reduce off-target effects. Expert opinion: Although Hsp90 inhibitors have proven their efficacy at reducing tau pathology, they have yet to meet with success in the clinic. The development of Hsp90/tau complex-specific inhibitors and further development of Hsp90 co-chaperone-specific drugs should yield more potent, less toxic therapeutics.
MeSH term(s)	Alzheimer Disease/drug therapy ; Alzheimer Disease/physiopathology ; Animals ; Blood-Brain Barrier/metabolism ; Drug Design ; HSP90 Heat-Shock Proteins/antagonists & inhibitors ; HSP90 Heat-Shock Proteins/metabolism ; Humans ; Molecular Chaperones/metabolism ; Molecular Targeted Therapy ; tau Proteins/metabolism
Chemical Substances	HSP90 Heat-Shock Proteins ; Molecular Chaperones ; tau Proteins
Language	English
Publishing date	2014-07-29
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2055208-7
ISSN	1744-7631 ; 1472-8222
ISSN (online)	1744-7631
ISSN	1472-8222
DOI	10.1517/14728222.2014.943185
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Article ; Online: Hippocampal Neurogenesis Is Enhanced in Adult Tau Deficient Mice

Marangelie Criado-Marrero / Jonathan J. Sabbagh / Margaret R. Jones / Dale Chaput / Chad A. Dickey / Laura J. Blair

Cells, Vol 9, Iss 1, p

2020 Volume 210

Abstract: Tau dysfunction is common in several neurodegenerative diseases including Alzheimer’s disease (AD) and frontotemporal dementia (FTD). Affective symptoms have often been associated with aberrant tau pathology and are commonly comorbid in patients with ... ...

Abstract	Tau dysfunction is common in several neurodegenerative diseases including Alzheimer’s disease (AD) and frontotemporal dementia (FTD). Affective symptoms have often been associated with aberrant tau pathology and are commonly comorbid in patients with tauopathies, indicating a connection between tau functioning and mechanisms of depression. The current study investigated depression-like behavior in Mapt −/− mice, which contain a targeted deletion of the gene coding for tau. We show that 6-month Mapt −/− mice are resistant to depressive behaviors, as evidenced by decreased immobility time in the forced swim and tail suspension tests, as well as increased escape behavior in a learned helplessness task. Since depression has also been linked to deficient adult neurogenesis, we measured neurogenesis in the hippocampal dentate gyrus and subventricular zone using 5-bromo-2-deoxyuridine (BrdU) labeling. We found that neurogenesis is increased in the dentate gyrus of 14-month-old Mapt −/− brains compared to wild type, providing a potential mechanism for their behavioral phenotypes. In addition to the hippocampus, an upregulation of proteins involved in neurogenesis was observed in the frontal cortex and amygdala of the Mapt −/− mice using proteomic mass spectrometry. All together, these findings suggest that tau may have a role in the depressive symptoms observed in many neurodegenerative diseases and identify tau as a potential molecular target for treating depression.
Keywords	tauopathies ; depression ; hippocampal neurogenesis ; stress ; glucocorticoid receptor ; alzheimer’s disease ; Biology (General) ; QH301-705.5
Subject code	572 ; 333
Language	English
Publishing date	2020-01-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
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Article ; Online: The emerging role of peptidyl-prolyl isomerase chaperones in tau oligomerization, amyloid processing, and Alzheimer's disease.

Blair, Laura J / Baker, Jeremy D / Sabbagh, Jonathan J / Dickey, Chad A

Journal of neurochemistry

2015 Volume 133, Issue 1, Page(s) 1–13

Abstract: Peptidyl-prolyl cis/trans isomerases (PPIases), a unique family of molecular chaperones, regulate protein folding at proline residues. These residues are abundant within intrinsically disordered proteins, like the microtubule-associated protein tau. Tau ... ...

Abstract	Peptidyl-prolyl cis/trans isomerases (PPIases), a unique family of molecular chaperones, regulate protein folding at proline residues. These residues are abundant within intrinsically disordered proteins, like the microtubule-associated protein tau. Tau has been shown to become hyperphosphorylated and accumulate as one of the two main pathological hallmarks in Alzheimer's disease, the other being amyloid beta (Ab). PPIases, including Pin1, FK506-binding protein (FKBP) 52, FKBP51, and FKBP12, have been shown to interact with and regulate tau biology. This interaction is particularly important given the numerous proline-directed phosphorylation sites found on tau and the role phosphorylation has been found to play in pathogenesis. This regulation then affects downstream aggregation and oligomerization of tau. However, many PPIases have yet to be explored for their effects on tau biology, despite the high likelihood of interaction based on proline content. Moreover, Pin1, FKBP12, FKBP52, cyclophilin (Cyp) A, CypB, and CypD have been shown to also regulate Ab production or the toxicity associated with Ab pathology. Therefore, PPIases directly and indirectly regulate pathogenic protein multimerization in Alzheimer's disease and represent a family rich in targets for modulating the accumulation and toxicity.
MeSH term(s)	Alzheimer Disease/enzymology ; Alzheimer Disease/metabolism ; Amyloid beta-Peptides/metabolism ; Animals ; Humans ; Molecular Chaperones/metabolism ; Peptidylprolyl Isomerase/metabolism ; tau Proteins/metabolism
Chemical Substances	Amyloid beta-Peptides ; Molecular Chaperones ; tau Proteins ; Peptidylprolyl Isomerase (EC 5.2.1.8)
Language	English
Publishing date	2015-02-24
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	80158-6
ISSN	1471-4159 ; 0022-3042 ; 1474-1644
ISSN (online)	1471-4159
ISSN	0022-3042 ; 1474-1644
DOI	10.1111/jnc.13033
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Article: Alzheimer's disease biomarkers in animal models: closing the translational gap.

Sabbagh, Jonathan J / Kinney, Jefferson W / Cummings, Jeffrey L

American journal of neurodegenerative disease

2013 Volume 2, Issue 2, Page(s) 108–120

Abstract: The rising prevalence of Alzheimer's disease (AD) is rapidly becoming one of the largest health and economic challenges in the world. There is a growing need for the development and implementation of reliable biomarkers for AD that can be used to assist ... ...

Abstract	The rising prevalence of Alzheimer's disease (AD) is rapidly becoming one of the largest health and economic challenges in the world. There is a growing need for the development and implementation of reliable biomarkers for AD that can be used to assist in diagnosis, inform disease progression, and monitor therapeutic efficacy. Preclinical models permit the evaluation of candidate biomarkers and assessment of pipeline agents before clinical trials are initiated and provide a translational opportunity to advance biomarker discovery. Fast and inexpensive data can be obtained from examination of peripheral markers, though they currently lack the sensitivity and consistency of imaging techniques such as MRI or PET. Plasma and cerebrospinal fluid (CSF) biomarkers in animal models can assist in development and implementation of similar approaches in clinical populations. These biomarkers may also be invaluable in decisions to advance a treatment to human testing. Longitudinal studies in AD models can determine initial presentation and progression of biomarkers that may also be used to evaluate disease-modifying efficacy of drugs. The refinement of biomarker approaches in preclinical systems will not only aid in drug development, but may facilitate diagnosis and disease monitoring in AD patients.
Language	English
Publishing date	2013-06-21
Publishing country	United States
Document type	Journal Article
ZDB-ID	2695563-5
ISSN	2165-591X
ISSN	2165-591X
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