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Peripheral origin exosomal micro RNAs aggravate glymphatic system dysfunction in diabetic cognitive impairment

药学学报:英文版 2023年第7期13卷 2817-2825页

作者： Lin Zhang Dongna Li Pengrong Yi Jiangwei Shi Mengqing Guo Qingsheng Yin Dingbin Liu Pengwei Zhuang Yanjun Zhang State Key Laboratory of Component-based Chinese Medicine Tianjin University of Traditional Chinese MedicineTianjin 301617China Haihe Laboratory of Modern Chinese Medicine Tianjin 301617China First Teaching Hospital of Tianjin University of Traditional Chinese Medicine Tianjin 300193China National Clinical Research Center for Chinese Medicine Acupuncture and Moxibustion Tianjin 300193China State Key Laboratory of Medicinal Chemical Biology Research Center for Analytical Sciencesand Tianjin Key Laboratory of Molecular Recognition and BiosensingCollege of ChemistryNankai UniversityTianjin 300071China

Cognitive dysfunction is one of the common central nervous systems(CNS)complications of diabetes mellitus,which seriously affects the quality of life of patients and results in a huge economic burden.The glymphatic system dysfunction mediated by aquaporin-4(AQP4)loss or redistribution in perivascular astrocyte endfeet plays a crucial role in diabetes-induced cognitive impairment(DCI).However,the mechanism of AQP4 loss or redistribution in the diabetic states remains unclear.Accumulating evidence suggests that peripheral insulin resistance target tissues and CNS communication affect brain homeostasis and that exosomal miRNAs are key mediators.Glucose and lipid metabolism disorder is an important pathological feature of diabetes mellitus,and skeletal muscle,liver and adipose tissue are the key target insulin resistance organs.In this review,the changes in exosomal miRNAs induced by peripheral metabolism disorders in diabetes mellitus were systematically reviewed.We focused on exosomal miRNAs that could induce low AQP4 expression and redistribution in perivascular astrocyte endfeet,which could provide an interorgan communication pathway to illustrate the pathogenesis of DCI.Furthermore,the mechanisms of exosome secretion from peripheral insulin resistance target tissue and absorption to the CNS were summarized,which will be beneficial for proposing novel and feasible strategies to optimize DCI prevention and/or treatment in diabetic patients.

关键词： Diabetic cognitive impairment AQP4 Peripheral-central communication Exosomal miRNAs Central nervous system glymphatic system Diabetes mellitus Astrocyte

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Interplay between the glymphatic system and neurotoxic proteins in Parkinson’s disease and related disorders:current knowledge and future directions

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Neural Regeneration Research 2024年第9期19卷 1973-1980页

作者： Yumei Yue Xiaodan Zhang Wen Lv Hsin-Yi Lai Ting Shen Department of Neurology of Sir Run Run Shaw Hospital Zhejiang University School of MedicineZhejiang UniversityHangzhouZhejiang ProvinceChina Department of Emergency Medicine The University of Hong KongHong Kong Special Administrative RegionChina Department of Neurology of the Second Affiliated Hospital and School of Brain Science and Brain Medicine Interdisciplinary Institute of Neuroscience and TechnologyKey Laboratory of Medical Neurobiology of Zhejiang ProvinceZhejiang University School of MedicineHangzhouZhejiang ProvinceChina College of Biomedical Engineering and Instrument Science Zhejiang UniversityHangzhouZhejiang ProvinceChina MOE Frontier Science Center for Brain Science and Brain-Machine Integration State Key Laboratory of Brain-machine IntelligenceSchool of Brain Science and Brain MedicineZhejiang UniversityHangzhouZhejiang ProvinceChina

Parkinson’s disease is a common neurodegenerative disorder that is associated with abnormal aggregation and accumulation of neurotoxic proteins,includingα-synuclein,amyloid-β,and tau,in addition to the impaired elimination of these neurotoxic protein.Atypical parkinsonism,which has the same clinical presentation and neuropathology as Parkinson’s disease,expands the disease landscape within the continuum of Parkinson’s disease and related disorders.The glymphatic system is a waste clearance system in the brain,which is responsible for eliminating the neurotoxic proteins from the interstitial fluid.Impairment of the glymphatic system has been proposed as a significant contributor to the development and progression of neurodegenerative disease,as it exacerbates the aggregation of neurotoxic proteins and deteriorates neuronal damage.Therefore,impairment of the glymphatic system could be considered as the final common pathway to neurodegeneration.Previous evidence has provided initial insights into the potential effect of the impaired glymphatic system on Parkinson’s disease and related disorders;however,many unanswered questions remain.This review aims to provide a comprehensive summary of the growing literature on the glymphatic system in Parkinson’s disease and related disorders.The focus of this review is on identifying the manifestations and mechanisms of interplay between the glymphatic system and neurotoxic proteins,including loss of polarization of aquaporin-4 in astrocytic endfeet,sleep and circadian rhythms,neuroinflammation,astrogliosis,and gliosis.This review further delves into the underlying pathophysiology of the glymphatic system in Parkinson’s disease and related disorders,and the potential implications of targeting the glymphatic system as a novel and promising therapeutic strategy.

关键词： atypical parkinsonism glymphatic system magnetic resonance imaging neurotoxic proteins Parkinson’s disease

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From static to dynamic:live observation of the support system after ischemic stroke by two photon-excited fluorescence laser-scanning microscopy

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Neural Regeneration Research 2023年第10期18卷 2093-2107页

作者： Xuan Wu Jia-Rui Li Yu Fu Dan-Yang Chen Hao Nie Zhou-Ping Tang Department of Neurology Tongji HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhanHubei ProvinceChina Department of Geriatrics Tongji HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhanHubei ProvinceChina

Ischemic stroke is one of the most common causes of mortality and disability worldwide.However,treatment efficacy and the progress of research remain unsatisfactory.As the critical support system and essential components in neurovascular units,glial cells and blood vessels(including the bloodbrain barrier)together maintain an optimal microenvironment for neuronal function.They provide nutrients,regulate neuronal excitability,and prevent harmful substances from entering brain tissue.The highly dynamic networks of this support system play an essential role in ischemic stroke through processes including brain homeostasis,supporting neuronal function,and reacting to injuries.However,most studies have focused on postmortem animals,which inevitably lack critical information about the dynamic changes that occur after ischemic stroke.Therefore,a high-precision technique for research in living animals is urgently needed.Two-photon fluorescence laser-scanning microscopy is a powerful imaging technique that can facilitate live imaging at high spatiotemporal resolutions.Twophoton fluorescence laser-scanning microscopy can provide images of the whole-cortex vascular 3D structure,information on multicellular component interactions,and provide images of structure and function in the cranial window.This technique shifts the existing research paradigm from static to dynamic,from flat to stereoscopic,and from single-cell function to multicellular intercommunication,thus providing direct and reliable evidence to identify the pathophysiological mechanisms following ischemic stroke in an intact brain.In this review,we discuss exciting findings from research on the support system after ischemic stroke using two-photon fluorescence laser-scanning microscopy,highlighting the importance of dynamic observations of cellular behavior and interactions in the networks of the brain’s support systems.We show the excellent application prospects and advantages of two-photon fluorescence laser-scanning microscopy and predict future research develo

关键词： astrocytes blood-brain barrier calcium signaling glymphatic system ischemic stroke microglia network remodel two-photon fluorescence laser-scanning microscopy vessels

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Updated Understanding of the Glial-Vascular Unit in Central Nervous system Disorders

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Neuroscience Bulletin 2023年第3期39卷 503-518页

作者： Di Yao Ruoying Zhang Minjie Xie Fengfei Ding Minghuan Wang Wei Wang Department of Neurology Tongji HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430030China Department of Pharmacology School of Basic Medical SciencesFudan UniversityShanghai 200032China Key Laboratory of Neurological Diseases of the Chinese Ministry of Education School of Basic MedicineTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430030China

The concept of the glial-vascular unit(GVU)was raised recently to emphasize the close associations between brain cells and cerebral vessels,and their coordinated reactions to diverse neurological insults from a“glio-centric”view.GVU is a multicellular structure composed of glial cells,perivascular cells,and perivascular space.Each component is closely linked,collectively forming the GVU.The central roles of glial and perivascular cells and their multi-level interconnections in the GVU under normal conditions and in central nervous system(CNS)disorders have not been elucidated in detail.Here,we comprehensively review the intensive interactions between glial cells and perivascular cells in the niche of perivascular space,which take part in the modulation of cerebral blood flow and angiogenesis,formation of the blood-brain barrier,and clearance of neurotoxic wastes.Next,we discuss dysfunctions of the GVU in various neurological diseases,including ischemic stroke,spinal cord injury,Alzheimer’s disease,and major depression disorder.In addition,we highlight the possible therapies targeting the GVU,which may have potential clinical applications.

关键词： Glial-vascular unit Perivascular space Blood-brain barrier glymphatic system Ischemic stroke Spinal cord injury Alzheimer's disease Major depression disorder

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Novel therapeutic strategies targeting mitochondria as a gateway in neurodegeneration

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Neural Regeneration Research 2023年第5期18卷 991-995页

作者： Diogo Trigo Jose Joao Vitoria Odete A.B.da Cruz e Silva Neuroscience and Signalling Laboratory Institute of Biomedicine(iBiMED)Department of Medical SciencesUniversity of AveiroAveiroPortugal

In recent years, multiple disciplines have focused on mitochondrial biology and contributed to understanding its relevance towards adult-onset neurodegenerative disorders. These are complex dynamic organelles that have a variety of functions in ensuring cellular health and homeostasis. The plethora of mitochondrial functionalities confers them an intrinsic susceptibility to internal and external stressors(such as mutation accumulation or environmental toxins), particularly so in long-lived postmitotic cells such as neurons. Thus, it is reasonable to postulate an involvement of mitochondria in aging-associated neurological disorders, notably neurodegenerative pathologies including Alzheimer’s disease and Parkinson’s disease. On the other hand, biological effects resulting from neurodegeneration can in turn affect mitochondrial health and function, promoting a feedback loop further contributing to the progression of neuronal dysfunction and cellular death. This review examines state-of-the-art knowledge, focus on current research exploring mitochondrial health as a contributing factor to neuroregeneration, and the development of therapeutic approaches aimed at restoring mitochondrial homeostasis in a pathological setting.

关键词： Alzheimer’s disease axon energy homeostasis glymphatic system mitochondria mitostasis neurodegeneration neuroregeneration Parkinson’s disease therapeutical strategies

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The lymphatic system:a therapeutic target for central nervous system disorders

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Neural Regeneration Research 2023年第6期18卷 1249-1256页

作者： Jia-Qi Xu Qian-Qi Liu Sheng-Yuan Huang Chun-Yue Duan Hong-Bin Lu Yong Cao Jian-Zhong Hu Department of Spine Surgery and Orthopaedics Xiangya HospitalCentral South UniversityChangshaHunan ProvinceChina Key Laboratory of Organ Injury Aging and Regenerative Medicine of Hunan ProvinceChangshaHunan ProvinceChina Mobile Health Ministry of Education-China Mobile Joint Laboratory ChangshaHunan ProvinceChina National Clinical Research Center for Geriatric Disorders Xiangya HospitalCentral South UniversityChangshaHunan ProvinceChina Department of Cardiovascular Surgery The Second Xiangya HospitalCentral South UniversityChangshaHunan ProvinceChina Department of Sports Medicine Xiangya HospitalCentral South UniversityChangshaHunan ProvinceChina

The lymphatic vasculature forms an organized network that covers the whole body and is involved in fluid homeostasis,metabolite clearance,and immune surveillance.The recent identification of functional lymphatic vessels in the meninges of the brain and the spinal cord has provided novel insights into neurophysiology.They emerge as major pathways for fluid exchange.The abundance of immune cells in lymphatic vessels and meninges also suggests that lymphatic vessels are actively involved in neuroimmunity.The lymphatic system,through its role in the clearance of neurotoxic proteins,autoimmune cell infiltration,and the transmission of pro-inflammatory signals,participates in the pathogenesis of a variety of neurological disorders,including neurodegenerative and neuroinflammatory diseases and traumatic injury.Vascular endothelial growth factor C is the master regulator of lymphangiogenesis,a process that is critical for the maintenance of central nervous system homeostasis.In this review,we summarize current knowledge and recent advances relating to the anatomical features and immunological functions of the lymphatic system of the central nervous system and highlight its potential as a therapeutic target for neurological disorders and central nervous system repair.

关键词： central nervous system central nervous system injury glymphatic system lymphatic vessels meninges neurodegenerative disorders neuroinflammatory diseases vascular endothelial growth factor C

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The lymphatic drainage systems in the brain:a novel target for ischemic stroke?

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Neural Regeneration Research 2023年第3期18卷 485-491页

作者： Ying-Jie Wang Yan-Rong Sun Yan-Hong Pei Hao-Wen Ma Ya-Kun Mu Li-Hua Qin Jun-Hao Yan Department of Anatomy and Histology School of Basic Medical SciencesPeking UniversityBeijingChina

Recent studies have proposed three lymphatic drainage systems in the brain,that is,the glymphatic system,the intramural periarterial drainage pathway,and meningeal lymphatic vessels,whose roles in various neurological diseases have been widely explored.The glymphatic system is a fluid drainage and waste clearance pathway that utilizes perivascular space and aquaporin-4 protein located in the astrocyte endfeet to provide a space for exchange of cerebrospinal fluid and interstitial fluid.The intramural periarterial drainage pathway drives the flow of interstitial fluid through the capillary basement membrane and the arterial tunica media.Meningeal lymphatic vessels within the dura mater are involved in the removal of cerebral macromolecules and immune responses.After ischemic stroke,impairment of these systems could lead to cerebral edema,accumulation of toxic factors,and activation of neuroinflammation,while restoration of their normal functions can improve neurological outcomes.In this review,we summarize the basic concepts of these drainage systems,including drainage routes,physiological functions,regulatory mechanisms,and detection technologies.We also focus on the roles of lymphatic drainage systems in brain injury after ischemic stroke,as well as recent advances in therapeutic strategies targeting these drainage systems.These findings provide information for potential novel strategies for treatment of stroke.

关键词： aquaporin-4 brain edema glymphatic system intramural periarterial drainage ischemic stroke lymphatic drainage meningeal lymphatic vessels neuroinflammation neurotoxicity

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glymphatic imaging and modulation of the optic nerve

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Neural Regeneration Research 2022年第5期17卷 937-947页

作者： Anisha Kasi Crystal Liu Muneeb A.Faiq Kevin C.Chan Department of Ophthalmology NYU Grossman School of MedicineNYU Langone HealthNew York UniversityNew YorkNYUSA Department of Radiology NYU Grossman School of MedicineNYU Langone HealthNew York UniversityNew YorkNYUSA Neuroscience Institute NYU Grossman School of MedicineNYU Langone HealthNew York UniversityNew YorkNYUSA Center for Neural Science College of Arts and ScienceNew York UniversityNew YorkNYUSA

Optic nerve health is essential for proper function of the visual system.However,the pathophysiology of certain neurodegenerative disease processes affecting the optic nerve,such as glaucoma,is not fully understood.Recently,it was hypothesized that a lack of proper clearance of neurotoxins contributes to neurodegenerative diseases.The ability to clear metabolic waste is essential for tissue homeostasis in mammals,including humans.While the brain lacks the traditional lymphatic drainage system identified in other anatomical regions,there is growing evidence of a glymphatic system in the central nervous system,which structurally includes the optic nerve.Named to acknowledge the supportive role of astroglial cells,this perivascular fluid drainage system is essential to remove toxic metabolites from the central nervous system.Herein,we review existing literature describing the physiology and dysfunction of the glymphatic system specifically as it relates to the optic nerve.We summarize key imaging studies demonstrating the existence of a glymphatic system in the optic nerves of wild-type rodents,aquaporin 4-null rodents,and humans;glymphatic imaging studies in diseases where the optic nerve is impaired;and current evidence regarding pharmacological and lifestyle interventions that may help promote glymphatic function to improve optic nerve health.We conclude by highlighting future research directions that could be applied to improve imaging detection and guide therapeutic interventions for diseases affecting the optic nerve.

关键词： aquaporin-4 cerebrospinal fluid glaucoma glymphatic system hydrocephalus imaging metabolic waste clearance optic nerve perivascular pharmacological and lifestyle interventions

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Digoxin Ameliorates glymphatic Transport and Cognitive Impairment in a Mouse Model of Chronic Cerebral Hypoperfusion

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Neuroscience Bulletin 2022年第2期38卷 181-199页

作者： Jie Cao Di Yao Rong Li Xuequn Guo Jiahuan Hao Minjie Xie Jia Li Dengji Pan Xiang Luo Zhiyuan Yu Minghuan Wang Wei Wang Department of Neurology Tongji HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430030China Department of Pediatrics Tongji HospitalTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430030China Department of Respiratory Medicine Quanzhou First Hospital Affiliated to Fujian Medical UniversityQuanzhou 362000China Key Laboratory of Neurological Diseases of the Chinese Ministry of Education School of Basic MedicineTongji Medical CollegeHuazhong University of Science and TechnologyWuhan 430030China

The glymphatic system plays a pivotal role in maintaining cerebral homeostasis.Chronic cerebral hypoperfusion,arising from small vessel disease or carotid stenosis,results in cerebrometabolic disturbances ultimately manifesting in white matter injury and cognitive dysfunction.However,whether the glymphatic system serves as a potential therapeutic target for white matter injury and cognitive decline during hypoperfusion remains unknown.Here,we established a mouse model of chronic cerebral hypoperfusion via bilateral common carotid artery stenosis.We found that the hypoperfusion model was associated with significant white matter injury and initial cognitive impairment in conjunction with impaired glym・phatic system function.The glymphatic dysfunction was associated with altered cerebral perfusion and loss of aquaporin 4 polarization.Treatment of digoxin rescued changes in glymphatic transport,white matter structure,and cognitive function.Suppression of glymphatic functions by treatment with the AQP4 inhibitor TGN-020 abolished this protective effect of digoxin from hypoperfusion injury.Our research yields new insight into the relationship between hemodynamics,glymphatic transport,white matter injury,and cognitive changes after chronic cerebral hypoperfusion.

关键词： Chronic cerebral hypoperfusion Cognitive impairment Digoxin glymphatic system White matter injury

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Aquaporin 4 deficiency eliminates the beneficial effects of voluntary exercise in a mouse model of Alzheimer’s disease

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Neural Regeneration Research 2022年第9期17卷 2079-2088页

作者： Yun Liu Pan-Pan Hu Shuang Zhai Wei-Xi Feng Rui Zhang Qian Li Charles Marshall Ming Xiao Ting Wu Department of Neurology the First Affiliated Hospital of Nanjing Medical UniversityNanjingJiangsu ProvinceChina Jiangsu Province Key Laboratory of Neurodegeneration Nanjing Medical UniversityNanjingJiangsu ProvinceChina Brain Institute the Affiliated Nanjing Brain Hospital of Nanjing Medical UniversityNanjingJiangsu ProvinceChina College of Health Sciences University of Kentucky Center of Excellence in Rural HealthHazardKYUSA

Regular exercise has been shown to reduce the risk of Alzheimer’s disease(AD).Our previous study showed that the protein aquaporin 4(AQP4),which is specifically expressed on the paravascular processes of astrocytes,is necessary for glymphatic clearance of extracellular amyloid beta(Aβ)from the brain,which can delay the progression of Alzheimer’s disease.However,it is not known whether AQP4-regulated glymphatic clearance of extracellular Aβis involved in beneficial effects of exercise in AD patients.Our results showed that after 2 months of voluntary wheel exercise,APP/PS1 mice that were 3 months old at the start of the intervention exhibited a decrease in Aβburden,glial activation,perivascular AQP4 mislocalization,impaired glymphatic transport,synapse protein loss,and learning and memory defects compared with mice not subjected to the exercise intervention.In contrast,APP/PS1 mice that were 7 months old at the start of the intervention exhibited impaired AQP4 polarity and reduced glymphatic clearance of extracellular Aβ,and the above-mentioned impairments were not alleviated after the 2-month exercise intervention.Compared with age-matched APP/PS1 mice,AQP4 knockout APP/PS1 mice had more serious defects in glymphatic function,Aβplaque deposition,and cognitive impairment,which could not be alleviated after the exercise intervention.These findings suggest that AQP4-dependent glymphatic transport is the neurobiological basis for the beneficial effects of voluntary exercises that protect against the onset of AD.

关键词： Alzheimer’s disease amyloid-beta astrocytes aquaporin-4 glymphatic system learning and memory synaptic protein transgenic mice voluntary exercise

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