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Article ; Online: Prolonged Repetitive Head Trauma Induces a Singular Chronic Traumatic Encephalopathy-Like Pathology in White Matter Despite Transient Behavioral Abnormalities.

Briggs, Denise I / Angoa-Pérez, Mariana / Kuhn, Donald M

2016 Volume 186, Issue 11, Page(s) 2869–2886

Abstract: Repetitive mild traumatic brain injury (rmTBI), resulting from insults caused by an external mechanical force that disrupts normal brain function, has been linked to the development of neurodegenerative diseases, such as chronic traumatic encephalopathy ... ...

Abstract	Repetitive mild traumatic brain injury (rmTBI), resulting from insults caused by an external mechanical force that disrupts normal brain function, has been linked to the development of neurodegenerative diseases, such as chronic traumatic encephalopathy and Alzheimer disease; however, neither the severity nor frequency of head injury required to trigger adverse behavioral outcomes is well understood. In this study, the administration of 30 head impacts using two different weights to lightly anesthetized, completely unrestrained mice established a paradigm that simulates the highly repetitive nature of sports- and military-related head injury. As the number of head impacts increases, the time to recover consciousness diminishes; however, both the sensorimotor function and behavioral outcomes of impacted mice evolve during the ensuing weeks. Postmortem analyses reveal robust Alzheimer disease and chronic traumatic encephalopathy-like conditions that manifest in a singular manner throughout the white matter concomitant with evidence of chronic oligodendrogenesis. Our data suggest that latency to recover the righting reflex may be an inadequate measure of injury severity and imply that exposure to repeated head impacts may mask the severity of an underlying and developing neuropathologic condition that does not manifest itself until long after head collisions cease. In addition, our data indicate that there is a cumulative and dose-dependent effect of repetitive head impacts that induces the neurobehavioral and neuropathologic outcomes seen in humans with a history of rmTBI.
MeSH term(s)	Animals ; Behavior, Animal ; Brain Concussion/complications ; Brain Concussion/pathology ; Chronic Traumatic Encephalopathy/etiology ; Chronic Traumatic Encephalopathy/pathology ; Craniocerebral Trauma/complications ; Craniocerebral Trauma/pathology ; Disease Models, Animal ; Humans ; Male ; Mice ; Mice, Inbred C57BL ; White Matter/pathology
Language	English
Publishing date	2016-09-20
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	2943-9
ISSN	1525-2191 ; 0002-9440
ISSN (online)	1525-2191
ISSN	0002-9440
DOI	10.1016/j.ajpath.2016.07.013
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Article ; Online: Intracerebral Delivery of Brain-Derived Neurotrophic Factor Using HyStem

Ravina, Kristine / Briggs, Denise I / Kislal, Sezen / Warraich, Zuha / Nguyen, Tiffany / Lam, Rachel K / Zarembinski, Thomas I / Shamloo, Mehrdad

International journal of molecular sciences

2018 Volume 19, Issue 12

Abstract: Ischemic stroke is a leading cause of death and disability worldwide. Potential therapeutics aimed at neural repair and functional recovery are limited in their blood-brain barrier permeability and may exert systemic or off-target effects. We examined ... ...

Abstract	Ischemic stroke is a leading cause of death and disability worldwide. Potential therapeutics aimed at neural repair and functional recovery are limited in their blood-brain barrier permeability and may exert systemic or off-target effects. We examined the effects of brain-derived neurotrophic factor (BDNF), delivered via an extended release HyStem
MeSH term(s)	Animals ; Brain Ischemia/drug therapy ; Brain-Derived Neurotrophic Factor/administration & dosage ; Brain-Derived Neurotrophic Factor/therapeutic use ; Hydrogels/chemistry ; Immunohistochemistry ; Infarction, Middle Cerebral Artery/drug therapy ; Inflammation/drug therapy ; Male ; Rats ; Rats, Sprague-Dawley ; Recovery of Function/drug effects ; Stroke/drug therapy
Chemical Substances	Brain-Derived Neurotrophic Factor ; Hydrogels
Language	English
Publishing date	2018-11-28
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms19123782
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Article ; Online: Intracerebral Delivery of Brain-Derived Neurotrophic Factor Using HyStem ® -C Hydrogel Implants Improves Functional Recovery and Reduces Neuroinflammation in a Rat Model of Ischemic Stroke

Kristine Ravina / Denise I. Briggs / Sezen Kislal / Zuha Warraich / Tiffany Nguyen / Rachel K. Lam / Thomas I. Zarembinski / Mehrdad Shamloo

International Journal of Molecular Sciences, Vol 19, Iss 12, p

2018 Volume 3782

Abstract	Ischemic stroke is a leading cause of death and disability worldwide. Potential therapeutics aimed at neural repair and functional recovery are limited in their blood-brain barrier permeability and may exert systemic or off-target effects. We examined the effects of brain-derived neurotrophic factor (BDNF), delivered via an extended release HyStem ® -C hydrogel implant or vehicle, on sensorimotor function, infarct volume, and neuroinflammation, following permanent distal middle cerebral artery occlusion (dMCAo) in rats. Eight days following dMCAo or sham surgery, treatments were implanted directly into the infarction site. Rats received either vehicle, BDNF-only (0.167 µg/µL), hydrogel-only, hydrogel impregnated with 0.057 µg/µL of BDNF (hydrogel + BDNF LOW ), or hydrogel impregnated with 0.167 µg/µL of BDNF (hydrogel + BDNF HIGH ). The adhesive removal test (ART) and 28-point Neuroscore (28-PN) were used to evaluate sensorimotor function up to two months post-ischemia. The hydrogel + BDNF HIGH group showed significant improvements on the ART six to eight weeks following treatment and their behavioral performance was consistently greater on the 28-PN. Infarct volume was reduced in rats treated with hydrogel + BDNF HIGH as were levels of microglial, phagocyte, and astrocyte marker immunoexpression in the corpus striatum. These data suggest that targeted intracerebral delivery of BDNF using hydrogels may mitigate ischemic brain injury and restore functional deficits by reducing neuroinflammation.
Keywords	brain-derived neurotrophic factor ; functional recovery ; hydrogel ; ischemic stroke ; neuroinflammation ; Biology (General) ; QH301-705.5 ; Chemistry ; QD1-999
Subject code	616
Language	English
Publishing date	2018-11-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
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Article ; Online: Repetitive, mild traumatic brain injury results in a progressive white matter pathology, cognitive deterioration, and a transient gut microbiota dysbiosis.

Angoa-Pérez, Mariana / Zagorac, Branislava / Anneken, John H / Briggs, Denise I / Winters, Andrew D / Greenberg, Jonathan M / Ahmad, Madison / Theis, Kevin R / Kuhn, Donald M

Scientific reports

2020 Volume 10, Issue 1, Page(s) 8949

Abstract: Traumatic brain injury (TBI) is often accompanied by gastrointestinal and metabolic disruptions. These systemic manifestations suggest possible involvement of the gut microbiota in head injury outcomes. Although gut dysbiosis after single, severe TBI has ...

Abstract	Traumatic brain injury (TBI) is often accompanied by gastrointestinal and metabolic disruptions. These systemic manifestations suggest possible involvement of the gut microbiota in head injury outcomes. Although gut dysbiosis after single, severe TBI has been documented, the majority of head injuries are mild, such as those that occur in athletes and military personnel exposed to repetitive head impacts. Therefore, it is important to determine if repetitive, mild TBI (rmTBI) will also disrupt the gut microbiota. Male mice were exposed to mild head impacts daily for 20 days and assessed for cognitive behavior, neuropathology and disruptions in the gut microbiota at 0, 45 or 90 days after injury. Deficits in recognition memory were evident at the late post-injury points. Brains show an early increase in microglial activation at the 0-day time point that persisted until 90 days post-injury. This was compounded by substantial increases in astrocyte reactivity and phosphorylated tau at the 90-day time point. In contrast, changes in the microbial community were minor and transient, and very few differences were observed in mice exposed to rmTBI compared to controls. While the progressive emergence of white matter damage and cognitive alterations after rmTBI resembles the alterations observed in athletes and military personnel exposed to rmTBI, these changes could not be linked to systematic modifications in the gut microbiota.
MeSH term(s)	Animals ; Bacteria/genetics ; Brain/metabolism ; Brain Concussion/metabolism ; Brain Concussion/microbiology ; Brain Concussion/physiopathology ; Brain Injuries/pathology ; Cognition/physiology ; Cognition Disorders/pathology ; Disease Models, Animal ; Dysbiosis/microbiology ; Dysbiosis/physiopathology ; Gastrointestinal Microbiome/physiology ; Male ; Mice ; Mice, Inbred C57BL ; RNA, Ribosomal, 16S/genetics ; White Matter/metabolism ; White Matter/physiopathology
Chemical Substances	RNA, Ribosomal, 16S
Language	English
Publishing date	2020-06-02
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-020-65972-4
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Article ; Online: Repetitive, mild traumatic brain injury results in a progressive white matter pathology, cognitive deterioration, and a transient gut microbiota dysbiosis

Mariana Angoa-Pérez / Branislava Zagorac / John H. Anneken / Denise I. Briggs / Andrew D. Winters / Jonathan M. Greenberg / Madison Ahmad / Kevin R. Theis / Donald M. Kuhn

Scientific Reports, Vol 10, Iss 1, Pp 1-

2020 Volume 11

Abstract: Abstract Traumatic brain injury (TBI) is often accompanied by gastrointestinal and metabolic disruptions. These systemic manifestations suggest possible involvement of the gut microbiota in head injury outcomes. Although gut dysbiosis after single, ... ...

Abstract	Abstract Traumatic brain injury (TBI) is often accompanied by gastrointestinal and metabolic disruptions. These systemic manifestations suggest possible involvement of the gut microbiota in head injury outcomes. Although gut dysbiosis after single, severe TBI has been documented, the majority of head injuries are mild, such as those that occur in athletes and military personnel exposed to repetitive head impacts. Therefore, it is important to determine if repetitive, mild TBI (rmTBI) will also disrupt the gut microbiota. Male mice were exposed to mild head impacts daily for 20 days and assessed for cognitive behavior, neuropathology and disruptions in the gut microbiota at 0, 45 or 90 days after injury. Deficits in recognition memory were evident at the late post-injury points. Brains show an early increase in microglial activation at the 0-day time point that persisted until 90 days post-injury. This was compounded by substantial increases in astrocyte reactivity and phosphorylated tau at the 90-day time point. In contrast, changes in the microbial community were minor and transient, and very few differences were observed in mice exposed to rmTBI compared to controls. While the progressive emergence of white matter damage and cognitive alterations after rmTBI resembles the alterations observed in athletes and military personnel exposed to rmTBI, these changes could not be linked to systematic modifications in the gut microbiota.
Keywords	Medicine ; R ; Science ; Q
Subject code	150
Language	English
Publishing date	2020-06-01T00:00:00Z
Publisher	Nature Publishing Group
Document type	Article ; Online
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Article ; Online: Marble burying and nestlet shredding as tests of repetitive, compulsive-like behaviors in mice.

Angoa-Pérez, Mariana / Kane, Michael J / Briggs, Denise I / Francescutti, Dina M / Kuhn, Donald M

Journal of visualized experiments : JoVE

2013 , Issue 82, Page(s) 50978

Abstract: Obsessive-compulsive disorder (OCD) and autism spectrum disorders (ASD) are serious and debilitating psychiatric conditions and each constitutes a significant public health concern, particularly in children. Both of these conditions are highlighted by ... ...

Abstract	Obsessive-compulsive disorder (OCD) and autism spectrum disorders (ASD) are serious and debilitating psychiatric conditions and each constitutes a significant public health concern, particularly in children. Both of these conditions are highlighted by the repeated expression of meaningless behaviors. Individuals with OCD often show checking, frequent hand washing, and counting. Children with ASDs also engage in repetitive tapping, arm or hand flapping, and rocking. These behaviors can vary widely in intensity and frequency of expression. More intense forms of repetitive behaviors can even result in injury (e.g. excessive grooming, hand washing, and self-stimulation). These behaviors are therefore very disruptive and make normal social discourse difficult. Treatment options for repetitive behaviors in OCD and ASDs are somewhat limited and there is great interest in developing more effective therapies for each condition. Numerous animal models for evaluating compulsive-like behaviors have been developed over the past three decades. Perhaps the animal models with the greatest validity and ease of use are the marble burying test and the nestlet shredding test. Both tests take advantage of the fact that the target behaviors occur spontaneously in mice. In the marble burying test, 20 marbles are arrayed on the surface of clean bedding. The number of marbles buried in a 30 min session is scored by investigators blind to the treatment or status of the subjects. In the nestlet shredding test, a nestlet comprised of pulped cotton fiber is preweighed and placed on top of cage bedding and the amount of the nestlet remaining intact after a 30 min test session is determined. Presently, we describe protocols for and show movie documentation of marble burying and nestlet shredding. Both tests are easily and accurately scored and each is sensitive to small changes in the expression of compulsive-like behaviors that result from genetic manipulations, disease, or head injury.
MeSH term(s)	Animals ; Behavior, Animal ; Compulsive Behavior ; Disease Models, Animal ; Female ; Male ; Mice ; Nesting Behavior ; Obsessive-Compulsive Disorder
Language	English
Publishing date	2013-12-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Video-Audio Media
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/50978
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Article ; Online: Animal models of sports-related head injury: bridging the gap between pre-clinical research and clinical reality.

Angoa-Pérez, Mariana / Kane, Michael J / Briggs, Denise I / Herrera-Mundo, Nieves / Viano, David C / Kuhn, Donald M

Journal of neurochemistry

2014 Volume 129, Issue 6, Page(s) 916–931

Abstract: Sports-related head impact and injury has become a very highly contentious public health and medico-legal issue. Near-daily news accounts describe the travails of concussed athletes as they struggle with depression, sleep disorders, mood swings, and ... ...

Abstract	Sports-related head impact and injury has become a very highly contentious public health and medico-legal issue. Near-daily news accounts describe the travails of concussed athletes as they struggle with depression, sleep disorders, mood swings, and cognitive problems. Some of these individuals have developed chronic traumatic encephalopathy, a progressive and debilitating neurodegenerative disorder. Animal models have always been an integral part of the study of traumatic brain injury in humans but, historically, they have concentrated on acute, severe brain injuries. This review will describe a small number of new and emerging animal models of sports-related head injury that have the potential to increase our understanding of how multiple mild head impacts, starting in adolescence, can have serious psychiatric, cognitive and histopathological outcomes much later in life. Sports-related head injury (SRHI) has emerged as a significant public health issue as athletes can develop psychiatric and neurodegenerative disorders later in life. Animal models have always been an integral part of the study of human TBI but few existing methods are valid for studying SRHI. In this review, we propose criteria for effective animal models of SRHI. Movement of the head upon impact is judged to be of primary importance in leading to concussion and persistent CNS dysfunction.
MeSH term(s)	Animals ; Athletic Injuries/pathology ; Brain Concussion/physiopathology ; Craniocerebral Trauma/pathology ; Disease Models, Animal ; Humans ; Risk Reduction Behavior
Language	English
Publishing date	2014-03-19
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; 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.12690
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Article ; Online: Mice genetically depleted of brain serotonin do not display a depression-like behavioral phenotype.

Angoa-Pérez, Mariana / Kane, Michael J / Briggs, Denise I / Herrera-Mundo, Nieves / Sykes, Catherine E / Francescutti, Dina M / Kuhn, Donald M

ACS chemical neuroscience

2014 Volume 5, Issue 10, Page(s) 908–919

Abstract: Reductions in function within the serotonin (5HT) neuronal system have long been proposed as etiological factors in depression. Selective serotonin reuptake inhibitors (SSRIs) are the most common treatment for depression, and their therapeutic effect is ... ...

Abstract	Reductions in function within the serotonin (5HT) neuronal system have long been proposed as etiological factors in depression. Selective serotonin reuptake inhibitors (SSRIs) are the most common treatment for depression, and their therapeutic effect is generally attributed to their ability to increase the synaptic levels of 5HT. Tryptophan hydroxylase 2 (TPH2) is the initial and rate-limiting enzyme in the biosynthetic pathway of 5HT in the CNS, and losses in its catalytic activity lead to reductions in 5HT production and release. The time differential between the onset of 5HT reuptake inhibition by SSRIs (minutes) and onset of their antidepressant efficacy (weeks to months), when considered with their overall poor therapeutic effectiveness, has cast some doubt on the role of 5HT in depression. Mice lacking the gene for TPH2 are genetically depleted of brain 5HT and were tested for a depression-like behavioral phenotype using a battery of valid tests for affective-like disorders in animals. The behavior of TPH2(-/-) mice on the sucrose preference test, tail suspension test, and forced swim test and their responses in the unpredictable chronic mild stress and learned helplessness paradigms was the same as wild-type controls. While TPH2(-/-) mice as a group were not responsive to SSRIs, a subset responded to treatment with SSRIs in the same manner as wild-type controls with significant reductions in immobility time on the tail suspension test, indicative of antidepressant drug effects. The behavioral phenotype of the TPH2(-/-) mouse questions the role of 5HT in depression. Furthermore, the TPH2(-/-) mouse may serve as a useful model in the search for new medications that have therapeutic targets for depression that are outside of the 5HT neuronal system.
MeSH term(s)	Anhedonia/physiology ; Animals ; Brain/drug effects ; Brain/physiology ; Depression/physiopathology ; Dietary Sucrose/administration & dosage ; Female ; Helplessness, Learned ; Male ; Mice, Inbred C57BL ; Mice, Knockout ; Motor Activity/drug effects ; Motor Activity/physiology ; Neuropsychological Tests ; Phenotype ; Quinine/administration & dosage ; Serotonin/deficiency ; Serotonin Plasma Membrane Transport Proteins/metabolism ; Serotonin Uptake Inhibitors/pharmacology ; Stress, Psychological/drug therapy ; Stress, Psychological/physiopathology ; Synaptosomes/drug effects ; Synaptosomes/metabolism ; Taste Perception/physiology ; Tryptophan Hydroxylase/deficiency ; Tryptophan Hydroxylase/genetics
Chemical Substances	Dietary Sucrose ; Serotonin Plasma Membrane Transport Proteins ; Serotonin Uptake Inhibitors ; Slc6a4 protein, mouse ; Serotonin (333DO1RDJY) ; Quinine (A7V27PHC7A) ; Tph2 protein, mouse (EC 1.14.16.4) ; Tryptophan Hydroxylase (EC 1.14.16.4)
Language	English
Publishing date	2014-08-12
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1948-7193
ISSN (online)	1948-7193
DOI	10.1021/cn500096g
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Article ; Online: Author Correction: Genetic effects on the timing of parturition and links to fetal birth weight.

Solé-Navais, Pol / Flatley, Christopher / Steinthorsdottir, Valgerdur / Vaudel, Marc / Juodakis, Julius / Chen, Jing / Laisk, Triin / LaBella, Abigail L / Westergaard, David / Bacelis, Jonas / Brumpton, Ben / Skotte, Line / Borges, Maria C / Helgeland, Øyvind / Mahajan, Anubha / Wielscher, Matthias / Lin, Frederick / Briggs, Catherine / Wang, Carol A /

Moen, Gunn-Helen / Beaumont, Robin N / Bradfield, Jonathan P / Abraham, Abin / Thorleifsson, Gudmar / Gabrielsen, Maiken E / Ostrowski, Sisse R / Modzelewska, Dominika / Nohr, Ellen A / Hypponen, Elina / Srivastava, Amit / Talbot, Octavious / Allard, Catherine / Williams, Scott M / Menon, Ramkumar / Shields, Beverley M / Sveinbjornsson, Gardar / Xu, Huan / Melbye, Mads / Lowe, William / Bouchard, Luigi / Oken, Emily / Pedersen, Ole B / Gudbjartsson, Daniel F / Erikstrup, Christian / Sørensen, Erik / Lie, Rolv T / Teramo, Kari / Hallman, Mikko / Juliusdottir, Thorhildur / Hakonarson, Hakon / Ullum, Henrik / Hattersley, Andrew T / Sletner, Line / Merialdi, Mario / Rifas-Shiman, Sheryl L / Steingrimsdottir, Thora / Scholtens, Denise / Power, Christine / West, Jane / Nyegaard, Mette / Capra, John A / Skogholt, Anne H / Magnus, Per / Andreassen, Ole A / Thorsteinsdottir, Unnur / Grant, Struan F A / Qvigstad, Elisabeth / Pennell, Craig E / Hivert, Marie-France / Hayes, Geoffrey M / Jarvelin, Marjo-Riitta / McCarthy, Mark I / Lawlor, Deborah A / Nielsen, Henriette S / Mägi, Reedik / Rokas, Antonis / Hveem, Kristian / Stefansson, Kari / Feenstra, Bjarke / Njolstad, Pål / Muglia, Louis J / Freathy, Rachel M / Johansson, Stefan / Zhang, Ge / Jacobsson, Bo

Nature genetics

2023 Volume 55, Issue 7, Page(s) 1250

Language	English
Publishing date	2023-05-10
Publishing country	United States
Document type	Published Erratum
ZDB-ID	1108734-1
ISSN	1546-1718 ; 1061-4036
ISSN (online)	1546-1718
ISSN	1061-4036
DOI	10.1038/s41588-023-01412-z
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Article: Repeated mild traumatic brain injury causes focal response in lateral septum and hippocampus.

Acabchuk, Rebecca / Briggs, Denise I / Angoa-Pérez, Mariana / Powers, Meghan / Wolferz, Richard / Soloway, Melanie / Stern, Mai / Talbot, Lillian R / Kuhn, Donald M / Conover, Joanne C

Concussion (London, England)

2016 Volume 1, Issue 3

Abstract: Aim: To advance our understanding of regional and temporal cellular responses to repeated mild traumatic brain injury (rmTBI), we used a mouse model of rmTBI that incorporated acceleration, deceleration and rotational forces.: Materials & methods: A ... ...

Abstract	Aim: To advance our understanding of regional and temporal cellular responses to repeated mild traumatic brain injury (rmTBI), we used a mouse model of rmTBI that incorporated acceleration, deceleration and rotational forces. Materials & methods: A modified weight-drop method was used to compare two inter-injury intervals, rmTBI-short (five hits delivered over 3 days) and rmTBI-long (five hits delivered over 15 days). Regional investigations of forebrain and midbrain histological alterations were performed at three post-injury time points (immediate, 2 weeks and 6 weeks). Results: The rmTBI-short protocol generated an immediate, localized microglial and astroglial response in the dorsolateral septum and hippocampus, with the astroglial response persisting in the dorsolateral septum. The rmTBI-long protocol showed only a transitory astroglial response in the dorsolateral septum. Conclusion: Our results indicate that the lateral septum and hippocampus are particularly vulnerable regions in rmTBI, possibly contributing to memory and emotional impairments associated with repeated concussions.
Language	English
Publishing date	2016-05-25
Publishing country	England
Document type	Journal Article
ISSN	2056-3299
ISSN	2056-3299
DOI	10.2217/cnc-2015-0001
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