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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

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Front. Med.    2021, Vol. 15 Issue (6) : 887-902    https://doi.org/10.1007/s11684-021-0879-9
RESEARCH ARTICLE
Loss of monocarboxylate transporter 1 aggravates white matter injury after experimental subarachnoid hemorrhage in rats
Xin Wu, Zongqi Wang, Haiying Li, Xueshun Xie, Jiang Wu, Haitao Shen, Xiang Li, Zhong Wang(), Gang Chen()
Department of Neurosurgery & Brain and Nerve Research Laboratory, The First Affiliated Hospital of Soochow University, Suzhou 215006, China
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Abstract

Monocarboxylic acid transporter 1 (MCT1) maintains axonal function by transferring lactic acid from oligodendrocytes to axons. Subarachnoid hemorrhage (SAH) induces white matter injury, but the involvement of MCT1 is unclear. In this study, the SAH model of adult male Sprague-Dawley rats was used to explore the role of MCT1 in white matter injury after SAH. At 48 h after SAH, oligodendrocyte MCT1 was significantly reduced, and the exogenous overexpression of MCT1 significantly improved white matter integrity and long-term cognitive function. Motor training after SAH significantly increased the number of ITPR2+SOX10+ oligodendrocytes and upregulated the level of MCT1, which was positively correlated with the behavioral ability of rats. In addition, miR-29b and miR-124 levels were significantly increased in SAH rats compared with non-SAH rats. Further intervention experiments showed that miR-29b and miR-124 could negatively regulate the level of MCT1. This study confirmed that the loss of MCT1 may be one of the mechanisms of white matter damage after SAH and may be caused by the negative regulation of miR-29b and miR-124. MCT1 may be involved in the neurological improvement of rehabilitation training after SAH.
Keywords microRNAs      monocarboxylate transporter 1      motor training      subarachnoid hemorrhage      white matter injury     
Corresponding Author(s): Zhong Wang,Gang Chen   
Just Accepted Date: 09 November 2021   Online First Date: 06 December 2021    Issue Date: 27 December 2021
 Cite this article:   
Xin Wu,Zongqi Wang,Haiying Li, et al. Loss of monocarboxylate transporter 1 aggravates white matter injury after experimental subarachnoid hemorrhage in rats[J]. Front. Med., 2021, 15(6): 887-902.
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https://academic.hep.com.cn/fmd/EN/10.1007/s11684-021-0879-9
https://academic.hep.com.cn/fmd/EN/Y2021/V15/I6/887
Fig.1  Levels of MCT1 were significantly decreased in brain tissues after SAH induction for 48 h. (A) Time course of MCT1 expression in the rat brain tissues after SAH. Top: representative Western blot bands of MCT1 at 3, 6, 12, 24, and 48 h after SAH. Bottom: quantitative analysis of the relative protein level. (B) Mean density (sum integrated optical density/sum pixel area) of MCT1. (C) Double-immunofluorescent analysis was performed with antibodies against MCT1 (green) and Olig2 (oligodendrocyte marker, red), and nuclei were fluorescently labeled with DAPI (blue). Representative images of the expression of MCT1 in rat corpus callosum oligodendrocytes at 48 h after SAH. Scale bar= 100 μm. Data are presented as mean±SD. n = 10 in A, n = 6 in B. *P≤0.05, **P≤0.01 vs. the sham group. N.S., not significant.
Fig.2  Effect of MCT1 overexpression on acute axonal injury after SAH. (A) Efficacy of MCT1 overexpression in brain tissues based on Western blot analysis. Top: representative Western blot bands of MCT1 in the sham, SAH, SAH+ Vector, and SAH+ Over-MCT1 groups. Bottom: quantitative analysis of the relative protein level. (B) Double-immunofluorescent analysis was performed with antibodies against MCT1 (green) and Olig2 (oligodendrocyte marker, red), and nuclei were fluorescently labeled with DAPI (blue). Representative images of the expression of MCT1 in rat corpus callosum oligodendrocytes at 48 h after SAH. Scale bar= 100 μm. (C) Quantification of the relative fluorescence intensity of MCT1. (D) Representative images of β-APP (green) and 200 kDa neurofilament heavy antibody (NF200, red) in the corpus callosum at 48 h after SAH or sham operation. Scale bar= 100 μm. (E) Quantification of the number of β-APP per square millimeter. Data are presented as mean±SD. n = 6 per group. *P≤0.05, ***P≤0.001.
Fig.3  Effect of MCT1 overexpression on acute white matter injury after SAH. (A) Effect of MCT1 overexpression on the level of myelin basic protein (MBP) as shown by Western blot analysis. Top: representative Western blot bands of MBP in the sham, SAH, SAH+ Vector, and SAH+ Over-MCT1 groups. Bottom: quantitative analysis of the relative protein level. (B) Effect of MCT1 overexpression in the level of non-phosphorylated neurofilament H (monoclonal clone ID: SMI 32) based on Western blot analysis. Top: representative Western blot bands of SMI 32 in the sham, SAH, SAH+ Vector, and SAH+ Over-MCT1 groups. Bottom: quantitative analysis of the relative protein level. (C) Representative images of MBP (green) and SMI 32 (red) in the corpus callosum at 48 h after SAH or sham operation. Scale bar= 100 μm. (D) Quantification of the ratios of SMI 32 to MBP fluorescence intensity in the corpus callosum, illustrated as fold change compared with the sham group average value. Data are presented as mean±SD. n = 6 per group. *P≤0.05, ***P≤0.001.
Fig.4  Effect of MCT1 overexpression on SAH-induced long-term neurobehavioral outcomes. (A) Latency to fall in the rotarod test before (3 days of pretraining before SAH) and up to 35 days after SAH. (B) Time to remove the adhesive tapes in the adhesive removal test before (3 days of pretraining before SAH) and up to 35 days after SAH. (C) Escape latency in the Morris water maze test at 29 to 33 days after SAH. (D) Representative images illustrate swim paths on 33 days (learning) and 34 days (memory) after SAH or sham operation. (E) Target quadrant time in the Morris water maze test at 34 days after SAH. (F) Swimming speed in the Morris water maze test at 34 days after SAH. Data are presented as mean±SD. n = 10–12 per group. *P≤0.05, **P≤0.01. N.S., not significant.
Fig.5  Rotarod training increases the level of MCT1 in ITPR2+SOX10+ oligodendrocytes. (A) Representative images of ITPR2+ (green) out of SOX10+ (red) cells; nuclei were fluorescently labeled with DAPI (blue) in the corpus callosum in the sham, sham+ training, SAH, and SAH+ training groups after 2 days of rotarod training. Scale bar= 100 μm. (B) Quantification of ITPR2+ of SOX10+ cells in the corpus callosum. (C) Representative Western blot bands of MCT1 in the corpus callosum region in the sham, sham+ training, SAH, and SAH+ training groups after 7 days of rotarod training. (D) Quantitative analysis of the relative protein level. (E) Representative images of MCT1+ (green) out of SOX10+ (red) cells in the corpus callosum in the sham, sham+ training, SAH, and SAH+ training groups after 7 days of rotarod training. Scale bar= 100 μm. (F) Quantification of MCT1+ out of SOX10+ cells in the corpus callosum. Data are presented as mean±SD. n = 4–6 per group. *P≤0.05, **P≤0.01.
Fig.6  Rotarod training accelerates long-term neurobehavioral recovery after SAH. (A) Correlation between the percentage of MCT1+ out of SOX10+ cells and the latency to fall in the rotarod test on day 35 after sham operation. (B) Correlation between the percentage of MCT1+ out of SOX10+ cells and the latency to fall in the rotarod test on day 35 after SAH operation. (C) Correlation between the percentage of MCT1+ out of SOX10+ cells and the time to remove the adhesive tapes in the adhesive removal test on day 35 after sham operation. (D) Correlation between the percentage of MCT1+ out of SOX10+ cells and the time to remove the adhesive tapes in the adhesive removal test on day 35 after SAH operation. n = 9–10 per group.
Fig.7  Role of miRNA-29b and miRNA-124 in regulating MCT1. (A) Relative expression level of miR-29b-3p in the CSF of SD rats in the sham and SAH groups. (B) Relative expression level of miR-124-3p in the CSF of SD rats in the sham and SAH groups. (C) Top: representative Western blot bands of MCT1 in the corpus callosum region in five different groups at 48 h after experimental SAH. Bottom: quantitative analysis of the relative protein level. (D) Double-immunofluorescent analysis was performed with antibodies against MCT1 (green) and Olig2 (red), and nuclei were fluorescently labeled with DAPI (blue). Representative images of the expressions of MCT1 in rat corpus callosum oligodendrocytes at 48 h after SAH. Scale bar= 100 μm. (E) Quantification of the relative fluorescence intensity of MCT1. (F) Schematic diagram for the role of MCT1 in white matter injury after experimental subarachnoid hemorrhage. After the onset of SAH, a rapid degeneration and demyelination of white matter occurs; however, the decrease of MCT1in oligodendrocytes in the white matter region interferes with the energy supply of oligodendrocytes to axons, thus further aggravating white matter injury. The upregulation of miR-29b and miR-124 may be entirely or partially involved in the decrease of MCT1 after SAH, and motor training might be a promising rescue conversely. Data are presented as mean±SD. n = 6–8 per group. *P≤0.05, **P≤0.01, ***P≤0.001.
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