Publications by authors named "Anne Manyande"

56 Publications

Quantitative analysis of internal components of the human crystalline lens during accommodation in adults.

Sci Rep 2021 Mar 23;11(1):6688. Epub 2021 Mar 23.

Department of Ophthalmology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Jiefangroad1095#, Wuhan, 430030, Hubei, China.

To quantitatively analyze changes in the inner components of the human crystalline lens during accommodation in adults. Eyes of 23 subjects were sequentially examined using CASIA2 Optical Coherence Tomography under 0D, - 3D and - 6D accommodation states. The anterior chamber depth (ACD), anterior and posterior crystalline lens radius of the curvature (ALRC and PLRC) were obtained using built-in software. The lens thickness (LT), lenticular nucleus thickness (NT), anterior cortex thickness (ACT), posterior cortex thickness (PCT), anterior and posterior lenticular nucleus radius of the curvature (ANRC and PNRC), anterior and posterior lenticular nucleus vertex (ANV and PNV) were quantified manually with the Image-pro plus software. During accommodation, the ACD became significantly shallower and LT significantly increased. For changes in the lens, the ALRC decreased by an average magnitude (related to accommodative stimuli) 0.44 mm/D, and PLRC decreased 0.09 mm/D. There was no difference for the ACT and PCT in different accommodation states. For lenticular nucleus response, NT increased on average by 30 μm/D. Both the ANRC and PNRC decreased on average by 212 μm/D and 115 μm/D respectively. The ANV moved forward on average by 0.07 mm under - 3D accommodative stimuli and 0.16 mm for - 6D. However, there was no statistically significant difference between different accommodation states in the PNV movement. Under accommodation stimulation, lens thickness changed mainly due to the lenticular nucleus, but not the cortex. For the lenticular nucleus, both the ANRC and PNRC decreased and ANRC changed the most. The anterior surface of the nucleus moved forward while the posterior surface of the nucleus moved backward but only slightly.
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http://dx.doi.org/10.1038/s41598-021-86007-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7987977PMC
March 2021

Identification of metabolic kinetic patterns in different brain regions using metabolomics methods coupled with various discriminant approaches.

J Pharm Biomed Anal 2021 May 16;198:114027. Epub 2021 Mar 16.

Key Laboratory of Magnetic Resonance in Biological Systems, State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, National Center for Magnetic Resonance in Wuhan, Wuhan Institute of Physics and Mathematics, Innovation Academy for Precision Measurement Science and Technology, Chinese Academy of Sciences-Wuhan National Laboratory for Optoelectronics, 430071, Wuhan, PR China; University of Chinese Academy of Sciences, Beijing, 100049, PR China; Hebei Provincial Key Laboratory of Basic Medicine for Diabetes, 2nd Hospital of Shijiazhuang, Shijiazhuang, Hebei, 050051, PR China. Electronic address:

Metabolomics is widely used as a powerful technique for identifying metabolic patterns and functions of organs and biological systems. Normally, there are multiple groups/targets involved in data processed by discriminant analysis. This is more common in cerebral studies, as there are always several brain regions involved in neuronal studies or brain metabolic dysfunctions. Furthermore, neuronal activity is highly correlated with cerebral energy metabolism, such as oxidation of glucose, especially for glutamatergic (excitatory) and GABAergic (inhibitory) neuronal activities. Thus, regional cerebral energy metabolism recognition is essential for understanding brain functions. In the current study, ten different brain regions were considered for discrimination analysis. The metabolic kinetics were investigated with C enrichments in metabolic products of glucose and measured using the nuclear magnetic spectroscopic method. Multiple discriminative methods were used to construct classification models in order to screen out the best method. After comparing all the applied discriminatory analysis methods, the boost-decision tree method was found to be the best method for classification and every cerebral region exhibited its own metabolic pattern. Finally, the differences in metabolic kinetics among these brain regions were analyzed. We, therefore, concluded that the current technology could also be utilized in other multi-class metabolomics studies and special metabolic kinetic patterns could provide useful information for brain function studies.
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http://dx.doi.org/10.1016/j.jpba.2021.114027DOI Listing
May 2021

Long-term microstructure and cerebral blood flow changes in patients recovered from COVID-19 without neurological manifestations.

J Clin Invest 2021 04;131(8)

Department of Radiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China.

BACKGROUNDThe coronavirus disease 2019 (COVID-19) rapidly progressed to a global pandemic. Although some patients totally recover from COVID-19 pneumonia, the disease's long-term effects on the brain still need to be explored.METHODSWe recruited 51 patients with 2 subtypes of COVID-19 (19 mild and 32 severe) with no specific neurological manifestations at the acute stage and no obvious lesions on the conventional MRI 3 months after discharge. Changes in gray matter morphometry, cerebral blood flow (CBF), and white matter (WM) microstructure were investigated using MRI. The relationship between brain imaging measurements and inflammation markers was further analyzed.RESULTSCompared with healthy controls, the decrease in cortical thickness/CBF and the changes in WM microstructure were more severe in patients with severe disease than in those with mild disease, especially in the frontal and limbic systems. Furthermore, changes in brain microstructure, CBF, and tract parameters were significantly correlated (P < 0.05) with the inflammatory markers C-reactive protein, procalcitonin, and interleukin 6.CONCLUSIONIndirect injury related to inflammatory storm may damage the brain, altering cerebral volume, CBF, and WM tracts. COVID-19-related hypoxemia and dysfunction of vascular endothelium may also contribute to neurological changes. The abnormalities in these brain areas need to be monitored during recovery, which could help clinicians understand the potential neurological sequelae of COVID-19.FUNDINGNatural Science Foundation of China.
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http://dx.doi.org/10.1172/JCI147329DOI Listing
April 2021

The Spinal α7-Nicotinic Acetylcholine Receptor Contributes to the Maintenance of Cancer-Induced Bone Pain.

J Pain Res 2021 15;14:441-452. Epub 2021 Feb 15.

Department of Anesthesiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, People's Republic of China.

Introduction: Cancer-induced bone pain (CIBP) is acknowledged as a multifactorial chronic pain that tortures advanced cancer patients, but existing treatment strategies for CIBP have not been satisfactory yet. Investigators have demonstrated that the activation of α7-nAChRs exerts analgesic effects in some chronic pain models. However, the role of spinal α7-nAChRs in CIBP remains unknown. This study was designed to investigate the role of α7-nAChRs in a well-established CIBP model induced by Walker 256 rat mammary gland carcinoma cells.

Methods: The paw withdrawal threshold (PWT) of the ipsilateral hind paw was measured using von Frey filament. The expressions of spinal α7-nAChRs and NF-κB were measured with Western blotting analysis. Immunofluorescence was employed to detect the expression of α7-nAChRs and co-expressed of α7-nAChRs with NeuN or GFAP or Iba1.

Results: Experiment results showed that the expression of spinal α7-nAChRs was significantly downregulated over time in CIBP rats, and in both CIBP rats and sham rats, most of the α7-nAChRs located in neurons. Behavioral data suggested PNU-282,987, a selective α7-nAChRs agonist, dose-dependently produced analgesic effect and positive allosteric modulator could intensify its effects. Further, repeated administration of PNU-282,987 reversed the expression of α7-nAChRs, inhibited the nuclear factor kappa B (NF-κB) signaling pathway, and attenuates CIBP-induced mechanical allodynia state as well.

Conclusion: These results suggest that the reduced expression of spinal α7-nAChRs contributes to the maintenance of CIBP by upregulating NF-κB expression, which implying a novel pharmacological therapeutic target for the treatment of CIBP.
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http://dx.doi.org/10.2147/JPR.S286321DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7894822PMC
February 2021

The Role of Gut Microbiota in Chronic Itch-Evoked Novel Object Recognition-Related Cognitive Dysfunction in Mice.

Front Med (Lausanne) 2021 5;8:616489. Epub 2021 Feb 5.

Department of Anesthesiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China.

The high incidence of patients with chronic itch highlights the importance of fundamental research. Recent advances in the interface of gut microbiota have shed new light into exploring this phenomenon. However, it is unknown whether gut microbiota plays a role in chronic itch in rodents with or without cognitive dysfunction. In this study, the role of gut microbiota in diphenylcyclopropenone (DCP)-evoked chronic itch was investigated in mice and hierarchical cluster analysis of novel object recognition test (ORT) results were used to classify DCP-evoked itch model in mice with or without cognitive dysfunction (CD)-like phenotype and 16S ribosomal RNA (rRNA) gene sequencing was used to compare gut bacterial composition between CD (Susceptible) and Non-CD phenotypes (Unsusceptible) in chronic itch mice. Results showed that the microbiota composition was significantly altered by DCP-evoked chronic itch and chronic itch induced novel object recognition-related CD. However, abnormal gut microbiota composition induced by chronic itch may not be correlated with novel object recognition-related CD.
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http://dx.doi.org/10.3389/fmed.2021.616489DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7892771PMC
February 2021

Neurochemical alterations of different cerebral regions in rats with myocardial ischemia-reperfusion injury based on proton nuclear magnetic spectroscopy analysis.

Aging (Albany NY) 2020 12 14;13(2):2294-2309. Epub 2020 Dec 14.

Departments of Anesthesiology and Pain Medicine, Tongji Hospital of Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China.

Background: Recent studies have demonstrated a complex and dynamic neural crosstalk between the heart and brain. A heart-brain interaction has been described regarding cardiac ischemia, but the cerebral metabolic mechanisms involved are unknown.

Methods: Male Sprague Dawley rats were randomly allocated into 2 groups: those receiving myocardial ischemia-reperfusion surgery (IR group, n =10) and surgical controls (Con group, n=10). These patterns of metabolic abnormalities in different brain regions were assessed using proton magnetic resonance spectroscopy (PMRS).

Results: Results assessed by echocardiography showed resultant cardiac dysfunction following heart ischemia-reperfusion. Compared with the control group, the altered metabolites in the IR group were taurine and choline, and differences mainly occurred in the thalamus and brainstem.

Conclusions: Alterations in cerebral taurine and choline are important findings offering new avenues to explore neuroprotective strategies for myocardial ischemia-reperfusion injury. These results provide preliminary evidence for understanding the cerebral metabolic process underlying myocardial ischemia-reperfusion injury in rats.
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http://dx.doi.org/10.18632/aging.202250DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7880342PMC
December 2020

Qualitative and Quantitative Analysis of Regional Cerebral Free Fatty Acids in Rats Using the Stable Isotope Labeling Liquid Chromatography-Mass Spectrometry Method.

Molecules 2020 Nov 6;25(21). Epub 2020 Nov 6.

State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, National Center for Magnetic Resonance in Wuhan, Key Laboratory of Magnetic Resonance in Biological Systems, Wuhan Institute of Physics and Mathematics, Innovation Academy for Precision Measurement Science and Technology, Chinese Academy of Sciences, Wuhan 430071, China.

Free fatty acids serve as important bioactive molecules in the brain. They are involved in message transfer in the brain. There are many reports available in the literature regarding the role of cerebral fatty acids in message transfer; however, most of the studies are mainly focused on limited fatty acid species or only a few specific brain regions. To understand the relationship between cerebral functions and free fatty acids, it is necessary to investigate the distribution of the free fatty acids among different regions in the whole brain. In this study, free fatty acids were extracted from different brain regions and analyzed qualitatively and quantitatively using the stable isotopic labeling liquid chromatography-mass spectrometry approach. In total, 1008 potential free fatty acids were detected in the whole brain out of which 38 were found to be commonly present in all brain regions. Among different brain regions, the highest and the smallest amounts of potential free fatty acids were detected in the olfactory bulb and cerebellum, respectively. From a statistical point of view, 4-methyl-2-oxovaleric acid, -11, 14-eicosadienoic acid, tridecanoic acid, myristic acid, nonadecanoic acid, and arachidic acid were found to significantly vary among the four different brain regions (olfactory bulb, occipital lobe, hippocampus, and cerebellum). The variation in the composition of free fatty acids among different brain regions may be very important for investigating the relationship between free fatty acids and functions of cerebral regions.
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http://dx.doi.org/10.3390/molecules25215163DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7664212PMC
November 2020

Reply to Collins et al.

Clin Infect Dis 2020 Sep 16. Epub 2020 Sep 16.

Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Shanxi Medical University; Tongji Shanxi Hospital, Tongji Medical College, Huazhong University of Science and Technology, Taiyuan, China.

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http://dx.doi.org/10.1093/cid/ciaa1407DOI Listing
September 2020

Identification of novel antioxidant peptides from snakehead (Channa argus) soup generated during gastrointestinal digestion and insights into the anti-oxidation mechanisms.

Food Chem 2021 Feb 29;337:127921. Epub 2020 Aug 29.

College of Food Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, PR China; National R & D Branch Center for Conventional Freshwater Fish Processing, Wuhan, Hubei 430070, PR China. Electronic address:

Antioxidant peptides obtained from snakehead (Channa argus) soup (SHS) after simulated gastrointestinal (GI) digestion were separated, identified and characterized. Results showed that the fraction with MW < 3 kDa had the highest antioxidant capacity. Four novel antioxidant peptides were identified after RP-HPLC and UPLC-MS/MS. PGMLGGSPPGLLGGSPP and SDGSNIHFPN had the highest DPPH radical scavenging activity (IC = 1.39 mM) and Fe chelating ability (IC = 4.60 mM), respectively. Structures in silico for IVLPDEGK, PGMLGGSPPGLLGGSPP and SDGSNIHFPN suggest at least one β-turn and/or α-helix, which are associated with antioxidant activity. Moreover, our results showed that these three peptides docked with a recombinant Kelch-like ECH-associated protein 1 (Keap1) with a binding score greater than TX6, a good ligand of Keap1. The cell viability assay also showed significant cytoprotective effects against HO-induced cellular oxidative damage. This information implies that antioxidant mechanisms of novel SHS peptides occurred via activation of cellular anti-oxidation Keap1-Nrf2 signaling pathway.
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http://dx.doi.org/10.1016/j.foodchem.2020.127921DOI Listing
February 2021

Neuronal mechanisms of adenosine A receptors in the loss of consciousness induced by propofol general anesthesia with functional magnetic resonance imaging.

J Neurochem 2021 Mar 6;156(6):1020-1032. Epub 2020 Sep 6.

Department of Anesthesiology, Zhongnan Hospital of Wuhan University, Wuhan, P.R. China.

Propofol is the most common intravenous anesthetic agent for induction and maintenance of anesthesia, and has been used clinically for more than 30 years. However, the mechanism by which propofol induces loss of consciousness (LOC) remains largely unknown. The adenosine A receptor (A R) has been extensively proven to have an effect on physiological sleep. It is, therefore, important to investigate the role of A R in the induction of LOC using propofol. In the present study, the administration of the highly selective A R agonist (CGS21680) and antagonist (SCH58261) was utilized to investigate the function of A R under general anesthesia induced by propofol by means of animal behavior studies, resting-state magnetic resonance imaging and c-Fos immunofluorescence staining approaches. Our results show that CGS21680 significantly prolonged the duration of LOC induced by propofol, increased the c-Fos expression in nucleus accumbens (NAc) and suppressed the functional connectivity of NAc-dorsal raphe nucleus (DR) and NAc-cingulate cortex (CG). However, SCH58261 significantly shortened the duration of LOC induced by propofol, decreased the c-Fos expression in NAc, increased the c-Fos expression in DR, and elevated the functional connectivity of NAc-DR and NAc-CG. Collectively, our findings demonstrate the important roles played by A R in the LOC induced by propofol and suggest that the neural circuit between NAc-DR maybe controlled by A R in the mechanism of anesthesia induced by propofol.
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http://dx.doi.org/10.1111/jnc.15146DOI Listing
March 2021

Hippocampal glutamatergic synapses impairment mediated novel-object recognition dysfunction in rats with neuropathic pain.

Pain 2020 08 23;161(8):1824-1836. Epub 2020 Mar 23.

Department of Anesthesiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China.

Cognitive impairment is one of the most common complications associated with chronic pain. Almost 20% of chronic pain patients suffer from cognitive impairment, which may substantially influence their quality of life. Levels of major excitatory neurotransmitters in the central nervous system and alterations in the glutamatergic system may influence cognitive function and the pain sensory pathway. In this study, we adopted the spared nerve injury model to establish the progress of chronic pain and investigated the mechanism underlying the cognitive aspect related to it. At behavioral level, using the novel-object recognition test, mechanical hypersensitivity was observed in peripheral nerve-injured rats because they exhibited recognition deficits. We showed a dramatic decrease in hippocampal glutamate concentration using nuclear magnetic resonance and reduced glutamatergic synaptic transmission using whole-cell recordings. These were associated with deficient hippocampal long-term potentiation induced by high-frequency stimulation of the Schaffer collateral afferent. Ultra-high-performance liquid chromatography revealed lower levels of D-serine in the hippocampus of the spared nerve injury rats and that D-serine treatment could restore synaptic plasticity and cognitive dysfunction. The reduction of excitatory synapses was also increased by administering D-serine. These findings suggest that chronic pain has a critical effect on synaptic plasticity linked to cognitive function and may built up a new target for the development of cognitive impairment under chronic pain conditions.
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http://dx.doi.org/10.1097/j.pain.0000000000001878DOI Listing
August 2020

The mechanism of chlorogenic acid inhibits lipid oxidation: An investigation using multi-spectroscopic methods and molecular docking.

Food Chem 2020 Dec 9;333:127528. Epub 2020 Jul 9.

College of Food Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, PR China; National R & D Branch Center for Conventional Freshwater Fish Processing, Wuhan, Hubei 430070, PR China. Electronic address:

Endogenous lipase and lipoxygenase play important roles in accelerating lipid oxidation. Polyphenols are a series of commonly used chemicals for preserving fish and seafood products, due to their positive inhibitory effects on lipid oxidation. However, the mechanism involved is still unknown. The inhibitory effects of chlorogenic acid (CGA) on lipase and lipoxygenase were investigated and explored with multi- spectroscopic and molecular docking approaches. Results showed that CGA could inhibit the activities of lipase and lipoxygenase with concentration increased in a highly dose-dependent manner. CGA quenched intrinsic fluorescence intensities of enzymes by static quenching and binding with CGA which led to changes in 3D structures of enzymes. Results of the molecular docking confirmed binding modes, binding sites and major interaction forces between CGA and enzymes, which reduced the corresponding activity. Thus, this study could provide basic mechanisms of the inhibitory effects of polyphenols on lipid oxidation during food preservation.
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http://dx.doi.org/10.1016/j.foodchem.2020.127528DOI Listing
December 2020

Investigation of robust visual reaction and functional connectivity in the rat brain induced by rocuronium bromide with functional MRI.

Am J Transl Res 2020 15;12(6):2396-2408. Epub 2020 Jun 15.

Center of Brain Science, State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, National Center for Magnetic Resonance in Wuhan, Key Laboratory of Magnetic Resonance in Biological Systems, Wuhan Institute of Physics and Mathematics, Innovation Academy for Precision Measurement Science and Technology, Chinese Academy of Sciences Wuhan 430071, Hubei, P. R. China.

Functional magnetic resonance imaging (fMRI) has been used extensively to understand the brain function of a wide range of neurological and psychiatric disorders. When applied to animal studies, anesthesia is always used to reduce the movement of the animal and also reduce the impacts on the results of fMRI. Several awake models have been proposed by applying physical animal movement restrictions. However, restraining devices were designed for individual subject which limits the promotion of fMRI in awake animals. Here, a clinical muscle relaxant rocuronium bromide (RB) was introduced to restrain the animal in fMRI scanning time. The fMRI reactions of the animal induced with RB and the other two commonly used anesthesia protocols were investigated. The results of the fMRI showed that there were increased functional connectivity and well-round visual responses in the RB induced state. Furthermore, significant BOLD signal changes were found in the cortex and thalamus regions when the animal revived from isoflurane, which should be essential to further understand the effects of anesthesia on the brain.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7344061PMC
June 2020

Development and Validation of a Nomogram for Assessing Survival in Patients With COVID-19 Pneumonia.

Clin Infect Dis 2021 02;72(4):652-660

Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Shanxi Medical University, Shanxi Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Taiyuan, China.

Background: The outbreak of coronavirus disease 2019 (COVID-19) has spread worldwide and continues to threaten peoples' health as well as put pressure on the accessibility of medical systems. Early prediction of survival of hospitalized patients will help in the clinical management of COVID-19, but a prediction model that is reliable and valid is still lacking.

Methods: We retrospectively enrolled 628 confirmed cases of COVID-19 using positive RT-PCR tests for SARS-CoV-2 in Tongji Hospital, Wuhan, China. These patients were randomly grouped into a training (60%) and a validation (40%) cohort. In the training cohort, LASSO regression analysis and multivariate Cox regression analysis were utilized to identify prognostic factors for in-hospital survival of patients with COVID-19. A nomogram based on the 3 variables was built for clinical use. AUCs, concordance indexes (C-index), and calibration curves were used to evaluate the efficiency of the nomogram in both training and validation cohorts.

Results: Hypertension, higher neutrophil-to-lymphocyte ratio, and increased NT-proBNP values were found to be significantly associated with poorer prognosis in hospitalized patients with COVID-19. The 3 predictors were further used to build a prediction nomogram. The C-indexes of the nomogram in the training and validation cohorts were 0.901 and 0.892, respectively. The AUC in the training cohort was 0.922 for 14-day and 0.919 for 21-day probability of in-hospital survival, while in the validation cohort this was 0.922 and 0.881, respectively. Moreover, the calibration curve for 14- and 21-day survival also showed high coherence between the predicted and actual probability of survival.

Conclusions: We built a predictive model and constructed a nomogram for predicting in-hospital survival of patients with COVID-19. This model has good performance and might be utilized clinically in management of COVID-19.
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http://dx.doi.org/10.1093/cid/ciaa963DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7454485PMC
February 2021

Regional cerebral metabolic levels and turnover in awake rats after acute or chronic spinal cord injury.

FASEB J 2020 08 27;34(8):10547-10559. Epub 2020 Jun 27.

Department of Neurosurgery, General Hospital of Ningxia Medical University, Yinchuan, P.R. China.

Spinal cord injury (SCI) is a common cause of disability, which often leads to sensorimotor cortex dysfunction above the spinal injury site. However, the cerebral regional effects on metabolic information after SCI have been little studied. Here, adult Sprague-Dawley rats were divided into acute and chronic treatment groups and sham groups with day-matched periods. The Basso, Beatte, and Bresnahan scores method were utilized to evaluate the changes in behaviors during the recovery of the animals, and the metabolic information was measured with the H-observed/ C-edited NMR method. Total metabolic concentrations in every region were almost similar in both treated groups. However, the metabolic kinetics in most regions in the acute group were significantly altered (P < .05), particularly in the cortical area, thalamus and medulla (P < .01). After long-term recovery, some metabolic kinetics were recovered, especially in the temporal cortex, occipital cortex, and medulla. The metabolic kinetic changes revealed the alteration of metabolism and neurotransmission in different brain regions after SCI, which present evidence for the alternation of brain glucose oxidation. Therefore, this shows the significant influence of SCI on cerebral function and neuroscience research. This study also provides the theoretical basis for clinical therapy after SCI, such as mitochondrial transplantation.
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http://dx.doi.org/10.1096/fj.202000447RDOI Listing
August 2020

Disruption of the GABAergic system contributes to the development of perioperative neurocognitive disorders after anesthesia and surgery in aged mice.

CNS Neurosci Ther 2020 09 2;26(9):913-924. Epub 2020 Jun 2.

Department of Anesthesiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China.

Aims: Perioperative neurocognitive disorders (PND) are associated with cognitive impairment in the preoperative or postoperative period, and neuroinflammation is thought to be the most important mechanisms especially during the postoperative period. The GABAergic system is easily disrupted by neuroinflammation. This study investigated the impact of the GABAergic system on PND after anesthesia and surgery.

Methods: An animal model of laparotomy with inhalation anesthesia in 16-month-old mice was addressed. Effects of the GABAergic system were assessed using biochemical analysis. Pharmacological blocking of α5GABA Rs or P38 mitogen-activated protein kinase (MAPK) were applied to investigate the effects of the GABAergic system.

Results: After laparotomy, the hippocampus-dependent memory and long-term potentiation were impaired, the levels of IL-6, IL-1β and TNF-α up-regulated in the hippocampus, the concentration of GABA decreased, and the protein levels of the surface α5GABA Rs up-regulated. Pharmacological blocking of α5GABA Rs with L655,708 alleviated laparotomy induced cognitive deficits. Further studies found that the P38 MAPK signaling pathway was involved and pharmacological blocking with SB203,580 alleviated memory dysfunctions.

Conclusions: Anesthesia and surgery caused neuroinflammation in the hippocampus, which consequently disrupted the GABAergic system, increased the expressions of surface α5GABA Rs especially through the P38 MAPK signaling pathway, and eventually led to hippocampus-dependent memory dysfunctions.
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http://dx.doi.org/10.1111/cns.13388DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7415208PMC
September 2020

The impact of novel coronavirus SARS-CoV-2 among healthcare workers in hospitals: An aerial overview.

Am J Infect Control 2020 08 26;48(8):915-917. Epub 2020 May 26.

Department of Gastrointestinal Surgery, Wuhan Peritoneal Cancer Clinical Medical Research Center, Zhongnan Hospital of Wuhan University, Hubei Key Laboratory of Tumor Biological Behaviors and Hubei Cancer Clinical Study Center, Wuhan, Hubei, China. Electronic address:

The ongoing outbreak of COVID-19, caused by the novel coronavirus SARS-CoV-2, places healthcare workers at an increased risk of infection as they are in close contact with patients. In this article, we report an overview of cases of infected healthcare workers in China and Italy during the early periods of the COVID-19 epidemic. China's coronavirus response highlights the importance of implementing effective public health strategies. The authorities worldwide therefore, need to be extremely cautious when they implement stringent protective measures that safeguard healthcare workers in hospitals and counteract the threats created by the pandemic.
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http://dx.doi.org/10.1016/j.ajic.2020.05.020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7247977PMC
August 2020

The mechanism for improving the flesh quality of grass carp (Ctenopharyngodon idella) following the micro-flowing water treatment using a UPLC-QTOF/MS based metabolomics method.

Food Chem 2020 Oct 9;327:126777. Epub 2020 Apr 9.

Key Laboratory of Environment Correlative Dietology, Ministry of Education, College of Food Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, PR China; National R & D Branch Center for Conventional Freshwater Fish Processing, Wuhan, Hubei 430070, PR China. Electronic address:

The micro-flowing water system can improve the flesh quality of freshwater fish using the traditional pond farming method. However, the mechanism of this phenomenon has not yet been explored. This study intends to examine the changes of metabolites in freshwater fish after treatment with the micro-flowing purification system (MFPS). The UPLC-QTOF/MS based metabolomics method was utilized to screen the metabolites and predict the major possible metabolic pathways after MFPS treatment. There were 377 types of metabolites identified in the fish muscle, of which 54-71 represented significant different metabolites identified during different stages of MFPS treatments. The main mechanism of MFPS treatment in improving the quality of grass carp fish muscle was investigated, and the MFPS treatment was shown to improve the flesh quality and the flavor of grass carp fish muscle. This study could provide the theoretical basis for improving the quality of aquatic products.
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http://dx.doi.org/10.1016/j.foodchem.2020.126777DOI Listing
October 2020

Correction to: Regional Metabolic Patterns of Abnormal Postoperative Behavioral Performance in Aged Mice Assessed by H-NMR Dynamic Mapping Method.

Neurosci Bull 2020 May;36(5):565-566

Department of Anesthesiology, Peking University Third Hospital, Beijing, 100191, China.

The original version of this article unfortunately contained some mistakes.
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http://dx.doi.org/10.1007/s12264-020-00488-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7186279PMC
May 2020

H-NMR based metabolomics reveals the nutrient differences of two kinds of freshwater fish soups before and after simulated gastrointestinal digestion.

Food Funct 2020 Apr;11(4):3095-3104

Key Laboratory of Environment Correlative Dietology, Ministry of Education, College of Food Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, P.R. China. and National R & D Branch Center for Conventional Freshwater Fish Processing, Wuhan, 430070, Hubei, P.R. China.

Soups show diverse health functions, which could be linked to their original nutrient profiles and metabolites derived from digestion. NMR spectroscopy is a robust and rapid method that unveils or identifies the chemical composition of food or food-derived metabolites. In the current study, the 1H-NMR spectroscopy approach was applied to identify the differences in metabolic profiling of two kinds of home-cooked freshwater fish soups (crucian carp and snakehead fish) before and after in vitro gastrointestinal digestion. The nutritional profiles of these soups were studied using the 1H-NMR method for the first time. Two metabolomics methods, PCA (Principal Component Analysis) and OPLS-DA (Orthogonal Partial Least Squares Discriminant Analysis), were used to analyze the data. On the whole, levels of amino acid metabolites such as valine (Val), tyrosine, choline, taurine (Tau) and glycine were higher in the crucian carp soup, whereas higher levels of fatty acids and unsaturated fatty acids were found in the snakehead soup. Furthermore, the high content of seven metabolites valine, leucine, EPA C20:5 (PUFA eicosapentaenoic acid), acetic acid, taurine, GPCho (phosphatidylcholine) and creatine showed an upward trend after simulated gastrointestinal digestion. The results demonstrate that the 1H-NMR metabolic profile of different fish soups can shed some light on our understanding of food functional properties and dietary therapy. Furthermore, changes of metabolites in digested fish soups could reveal information about chemical compounds which play important roles in the body.
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http://dx.doi.org/10.1039/c9fo02661dDOI Listing
April 2020

Cell-Type-Specific Whole-Brain Direct Inputs to the Anterior and Posterior Piriform Cortex.

Front Neural Circuits 2020 7;14. Epub 2020 Feb 7.

Wuhan National Laboratory for Optoelectronics, Huazhong University of Science and Technology, Wuhan, China.

The piriform cortex (PC) is a key brain area involved in both processing and coding of olfactory information. It is implicated in various brain disorders, such as epilepsy, Alzheimer's disease, and autism. The PC consists of the anterior (APC) and posterior (PPC) parts, which are different anatomically and functionally. However, the direct input networks to specific neuronal populations within the APC and PPC remain poorly understood. Here, we mapped the whole-brain direct inputs to the two major neuronal populations, the excitatory glutamatergic principal neurons and inhibitory γ-aminobutyric acid (GABA)-ergic interneurons within the APC and PPC using the rabies virus (RV)-mediated retrograde trans-synaptic tracing system. We found that for both types of neurons, APC and PPC share some similarities in input networks, with dominant inputs originating from the olfactory region (OLF), followed by the cortical subplate (CTXsp), isocortex, cerebral nuclei (CNU), hippocampal formation (HPF) and interbrain (IB), whereas the midbrain (MB) and hindbrain (HB) were rarely labeled. However, APC and PPC also show distinct features in their input distribution patterns. For both types of neurons, the input proportion from the OLF to the APC was higher than that to the PPC; while the PPC received higher proportions of inputs from the HPF and CNU than the APC did. Overall, our results revealed the direct input networks of both excitatory and inhibitory neuronal populations of different PC subareas, providing a structural basis to analyze the diverse PC functions.
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http://dx.doi.org/10.3389/fncir.2020.00004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7019026PMC
February 2020

Src-family protein tyrosine kinases: A promising target for treating chronic pain.

Biomed Pharmacother 2020 May 25;125:110017. Epub 2020 Feb 25.

Department of Anesthesiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China. Electronic address:

Despite the growing knowledge of the mechanisms of chronic pain, the treatment of this disorder in the clinic remains a major challenge. Src-family protein tyrosine kinases (SFKs), a group of non-receptor protein tyrosine kinases, have been implicated in neuronal development and synaptic plasticity. SFKs are critical for the regulate of N-methyl-D-aspartic acid receptor (NMDAR) 2B subunit phosphorylation by various transmembrane receptors, e.g., G-protein coupled receptors (GPCRs), EphB receptors (EphBRs), increased intracellular calcium, epidermal growth factor (EGF) and other growth factors, and thus contribute to the development of chronic pain. SFKs have also been regarded as important points of convergence of intracellular signalling components for the regulation of microglial functions and the immune response. Additionally, the intrathecal administration of SFK inhibitors significantly alleviates mechanical allodynia in different chronic pain models. Here, we reviewed the current evidence for the role of SFKs in the development of chronic pain caused by complete Freund's adjuvant (CFA) injection, peripheral nerve injury (PNI), streptozotocin (STZ) injection and bone metastasis. Moreover, the role of SFKs in the development of morphine tolerance is also discussed. The regulation of SFKs therefore has emerged as a potential therapeutic target for the treatment of chronic pain in terms of safety and efficacy.
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http://dx.doi.org/10.1016/j.biopha.2020.110017DOI Listing
May 2020

Co-localization of two-color rAAV2-retro confirms the dispersion characteristics of efferent projections of mitral cells in mouse accessory olfactory bulb.

Zool Res 2020 Mar;41(2):148-156

Center of Brain Science, State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, National Center for Magnetic Resonance in Wuhan, Key Laboratory of Magnetic Resonance in Biological Systems, Wuhan Institute of Physics and Mathematics, Innovation Academy for Precision Measurement Science and Technology, Chinese Academy of Sciences, Wuhan, Hubei 430071, China.

The accessory olfactory bulb (AOB), located at the posterior dorsal aspect of the main olfactory bulb (MOB), is the first brain relay of the accessory olfactory system (AOS), which can parallelly detect and process volatile and nonvolatile social chemosignals and mediate different sexual and social behaviors with the main olfactory system (MOS). However, due to its anatomical location and absence of specific markers, there is a lack of research on the internal and external neural circuits of the AOB. This issue was addressed by single-color labeling and fluorescent double labeling using retrograde rAAVs injected into the bed nucleus of the stria terminalis (BST), anterior cortical amygdalar area (ACo), medial amygdaloid nucleus (MeA), and posteromedial cortical amygdaloid area (PMCo) in mice. We demonstrated the effectiveness of this AOB projection neuron labeling method and showed that the mitral cells of the AOB exhibited efferent projection dispersion characteristics similar to those of the MOB. Moreover, there were significant differences in the number of neurons projected to different brain regions, which indicated that each mitral cell in the AOB could project to a different number of neurons in different cortices. These results provide a circuitry basis to help understand the mechanism by which pheromone information is encoded and decoded in the AOS.
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http://dx.doi.org/10.24272/j.issn.2095-8137.2020.020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7109009PMC
March 2020

Elevated glutamate, glutamine and GABA levels and reduced taurine level in a schizophrenia model using an in vitro proton nuclear magnetic resonance method.

Am J Transl Res 2019 15;11(9):5919-5931. Epub 2019 Sep 15.

Department of Psychiatry, The First Affiliated Hospital of China Medical University Shenyang, Liaoning, P. R. China.

Accumulating evidence suggests that brain metabolic changes may be associated with the pathophysiology of schizophrenia. Both and studies have found glutamatergic and GABAergic abnormalities in different brain regions of individuals with schizophrenia. We report a longitudinal behavioral study in a methylazoxymethanol acetate (MAM) rat model of schizophrenia at three different age periods: prepuberty, late-puberty and early-adulthood. MAM-treated rats showed stable hypolocomotive activity, anxiety and cognitive deficits from late-puberty to early-adulthood. Therefore we detected the metabolites changes of adult MAM-treated rats using an proton nuclear magnetic resonance (H-NMR) method. In the MAM-treated rats, glutamate was increased in the thalamus and hypothalamus, glutamine was increased in the hippocampus and GABA was increased in the hippocampus and prefrontal cortex, while taurine showed a decrease in the striatum, temporal cortex and parietal cortex. These abnormalities may be helped further understanding the pathophysiology of schizophrenia.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6789232PMC
September 2019

Rabies Virus Pseudotyped with CVS-N2C Glycoprotein as a Powerful Tool for Retrograde Neuronal Network Tracing.

Neurosci Bull 2020 Mar 23;36(3):202-216. Epub 2019 Aug 23.

Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, Guangdong Provincial Key Laboratory of Brain Connectome and Behavior, CAS Center for Excellence in Brain Science and Intelligence Technology, Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen, 518055, China.

Efficient viral vectors for mapping and manipulating long-projection neuronal circuits are crucial in structural and functional studies of the brain. The SAD strain rabies virus with the glycoprotein gene deleted pseudotyped with the N2C glycoprotein (SAD-RV(ΔG)-N2C(G)) shows strong neuro-tropism in cell culture, but its in vivo efficiency for retrograde gene transduction and neuro-tropism have not been systematically characterized. We compared these features in different mouse brain regions for SAD-RV-N2C(G) and two other widely-used retrograde tracers, SAD-RV(ΔG)-B19(G) and rAAV2-retro. We found that SAD-RV(ΔG)-N2C(G) enhanced the infection efficiency of long-projecting neurons by ~10 times but with very similar neuro-tropism, compared with SAD-RV(ΔG)-B19(G). On the other hand, SAD-RV(ΔG)-N2C(G) had an infection efficiency comparable with rAAV2-retro, but a more restricted diffusion range, and broader tropism to different types and regions of long-projecting neuronal populations. These results demonstrate that SAD-RV(ΔG)-N2C(G) can serve as an effective retrograde vector for studying neuronal circuits.
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http://dx.doi.org/10.1007/s12264-019-00423-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7056755PMC
March 2020

Measuring changes in Schlemm's canal and trabecular meshwork in different accommodation states in myopia children: an observational study.

Eye (Lond) 2020 02 9;34(2):374-382. Epub 2019 Aug 9.

Department of Ophthalmology, Tongji hospital, Tongji medical College, Huazhong University of Science and Technology, 430030, Wuhan, Hubei, China.

Purpose: The aim of the study was to evaluate changes in size of Schlemm's canal (SC) and trabecular meshwork(TM) in response to accommodation stimuli and cycloplegia states in myopia children.

Methods: In total, 34 children were enroled in this study. A -6.0 D accommodation stimulus was achieved by looking at an optotype through a mirror. Cycloplegia state was induced with 1% tropicamide. Two states were confirmed by measuring the central lens thickness (CLT), anterior chamber depth and pupil diameter. The size of SC and TM was measured using swept-source optical coherence tomography. The association between changes in SC size and CLT was analysed.

Results: Compared with that in the relaxation state, SC size increased significantly under -6.0 D accommodation stimuli. SC area (SCA) increased from 6371 ± 2517 μm to 7824 ± 2727 μm, SC length (SCL) from 249 ± 10 μm to 295 ± 12 μm and SC width (SCW) from 27 ± 9 μm to 31 ± 8 μm. Under the cycloplegia state, SCA decreased to 5009 ± 2028 μm; SCL to 212 ± 14 μm, and SCW to 22 ± 5 μm. Changes in SCA (r = 0.35, P = 0.0007), SCL (r = 0.251, P = 0.0172) and SCW (r = 0.253, P = 0.016) were significantly correlated with changes in CLT. TM size was not significantly altered compared to that in the relaxation state. TM length (TML) increased from 562 ± 45 μm to 587 ± 47 μm after exposure to -6.0 D accommodation stimulus.

Conclusion: SC size enlarged in response to -6.0 D accommodation stimuli and shrunk under cycloplegia. TM length increased under the accommodation stimulus state.
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http://dx.doi.org/10.1038/s41433-019-0548-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7002585PMC
February 2020

Regional Metabolic Patterns of Abnormal Postoperative Behavioral Performance in Aged Mice Assessed by H-NMR Dynamic Mapping Method.

Neurosci Bull 2020 Jan 2;36(1):25-38. Epub 2019 Aug 2.

Department of Anesthesiology, Peking University Third Hospital, Beijing, 100191, China.

Abnormal postoperative neurobehavioral performance (APNP) is a common phenomenon in the early postoperative period. The disturbed homeostatic status of metabolites in the brain after anesthesia and surgery might make a significant contribution to APNP. The dynamic changes of metabolites in different brain regions after anesthesia and surgery, as well as their potential association with APNP are still not well understood. Here, we used a battery of behavioral tests to assess the effects of laparotomy under isoflurane anesthesia in aged mice, and investigated the metabolites in 12 different sub-regions of the brain at different time points using proton nuclear magnetic resonance (H-NMR) spectroscopy. The abnormal neurobehavioral performance occurred at 6 h and/or 9 h, and recovered at 24 h after anesthesia/surgery. Compared with the control group, the altered metabolite of the model group at 6 h was aspartate (Asp), and the difference was mainly displayed in the cortex; while significant changes at 9 h occurred predominantly in the cortex and hippocampus, and the corresponding metabolites were Asp and glutamate (Glu). All changes returned to baseline at 24 h. The altered metabolic changes could have occurred as a result of the acute APNP, and the metabolites Asp and Glu in the cortex and hippocampus could provide preliminary evidence for understanding the APNP process.
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http://dx.doi.org/10.1007/s12264-019-00414-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6940420PMC
January 2020

NMR Based Metabolomics Comparison of Different Blood Sampling Techniques in Awake and Anesthetized Rats.

Molecules 2019 Jul 12;24(14). Epub 2019 Jul 12.

Key Laboratory of Magnetic Resonance in Biological Systems, State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, Wuhan Institute of Physics and Mathematics, Chinese Academy of Sciences, Wuhan 430071, China.

The composition of body fluids has become one of the most commonly used methods for diagnosing various diseases or monitoring the drug responses, especially in serum/plasma. It is therefore vital for investigators to find an appropriate way to collect blood samples from laboratory animals. This study compared blood samples collected from different sites using the NMR based metabolomics approach. Blood samples were collected from the saphenous vein (awake state), tail vein (awake and anesthetized states after administration of sevoflurane or pentobarbital) and the inferior thoracic vena cava (ITVC, anesthetized state). These approaches from the saphenous and tail veins have the potential to enable the collection of multiple samples, and the approach from ITVC is the best method for the collection of blood for the terminate state. The compositions of small molecules in the serum were determined using the H-NMR method, and the data were analyzed with traditional correlation analysis, principle component analysis (PCA) and OPLS-DA methods. The results showed that acute anesthesia significantly influenced the composition of serum in a very short period, such as the significant increase in glucose, and decrease in lactate. This indicates that it is better to obtain blood samples under the awake state. From the perspective of animal welfare and multiple sampling, the current study shows that the saphenous vein and tail vein are the best locations to collect multiple blood samples for a reduced risk of injury in the awake state. Furthermore, it is also suitable for investigating pharmacokinetics and the effects of drug intervention on animals.
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http://dx.doi.org/10.3390/molecules24142542DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6681412PMC
July 2019

The therapeutic potential of GABA in neuron-glia interactions of cancer-induced bone pain.

Eur J Pharmacol 2019 Sep 19;858:172475. Epub 2019 Jun 19.

Department of Anesthesiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China. Electronic address:

The development of effective therapeutics for cancer-induced bone pain (CIBP) remains a tremendous challenge owing to its unclear mechanisms. Gamma-aminobutyric acid (GABA) is the major inhibitory neurotransmitter in the central nervous system (CNS). Emerging studies have shown that disinhibition in the spinal cord dorsal horn may account for the development of chronic pain. However, the role of GABA in the development of CIBP remains elusive. In addition, accumulating evidence has shown that neuroglial cells in the peripheral nervous system, especially astrocytes and microglial cells, played an important role in the maintenance of CIBP. In this study, we investigated the expression of GABA and Gamma-aminobutyric acid transporter-1 (GAT-1), a transporter of GABA. Our results demonstrate that GABA was decreased in CIBP rats as expected. However, the expression of glutamic acid decarboxylase (GAD) 65 was up-regulated on day 21 after surgery, while the expression of GAD 67 remained unchanged after surgery. We also found that the expression of GAT-1 was up-regulated mainly in the astrocytes of the spinal cord. Moreover, we evaluated the analgesic effect of exogenous GABA and the GAT-1 inhibitor. Intrathecal administration of exogenous GABA and NO-711 (a GAT-1 selective inhibitor) significantly reversed CIBP-induced mechanical allodynia in a dose-dependent manner. These results firstly show that neuron-glia interactions, especially on the GABAergic pathway, contribute to the development of CIBP. In conclusion, exogenous GABA and GAT-1 inhibitor might be alternative therapeutic strategies for the treatment of CIBP.
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http://dx.doi.org/10.1016/j.ejphar.2019.172475DOI Listing
September 2019

Alterations in amino acid levels and metabolite ratio of spinal cord in rat with myocardial ischemia-reperfusion injury by proton magnetic resonance spectroscopy.

Am J Transl Res 2019 15;11(5):3101-3108. Epub 2019 May 15.

Department of Anesthesiology and Pain Medicine, Tongji Hospital of Tongji Medical College, Huazhong University of Science and Technology Wuhan 430030, Hubei, PR China.

Objectives: The mechanism behind spinal metabolites and myocardial ischemia-reperfusion (IR) injury is not well understood. Proton magnetic resonance spectroscopic analysis of spinal cord extracts provides a quick evaluation of the specific metabolic activity in rats with myocardial IR injury. We investigated the relationship between the IR-related variables and the changes in spinal metabolites.

Methods: Proton magnetic resonance spectroscopy (H-MRS) was used to assess the spinal metabolites of adult rats with and without myocardial IR injury (n = 6 per group). Myocardial IR injury was reproduced using intermittent occlusion of the left anterior descending coronary artery. We studied the relationship between the metabolite ratio measurement and IR-related variables. All rats underwent H-MRS, with the ratio of interest placed in different spinal cord segments to measure levels of twelve metabolites including N-acetylaspartate (NAA), taurine (Tau), glutamate (Glu), gamma amino acid butyric acid (GABA), creatine (Cr), and myoinositol (MI), etc. Results: Rats with myocardial IR injury had higher concentration of Tau in the upper thoracic spinal cord (P < 0.05), and lower concentration of Gly and Glu in the cervical segment of the spinal cord (P < 0.05), when compared to the Control group. The ratios of glutamate/taurine (Glu/Tau), Glu/(GABA + Tau) and Glu/Total were significantly different between the IR group and the Control group in the upper thoracic spinal cord (P < 0.05). So were the ratios of Glu/(GABA + Tau) in the cervical segment (P < 0.05), and Glu/Tau and Glu/(GABA + Tau) in the lower thoracic spinal cord (P < 0.05).

Conclusions: These findings suggest that myocardial IR injury may be related to spinal biochemical alterations. It is speculated that these observed changes in the levels of spinal metabolites may be involved in the pathogenesis and regulation of myocardial IR injury.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6556651PMC
May 2019