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. 2020 Mar 6:12:53.
doi: 10.3389/fnagi.2020.00053. eCollection 2020.

Contra-Directional Expression of Plasma Superoxide Dismutase with Lipoprotein Cholesterol and High-Sensitivity C-reactive Protein as Important Markers of Parkinson's Disease Severity

Wanlin Yang  1 , Zihan Chang  1 , Rongfang Que  1 , Guomei Weng  2 , Bin Deng  1 , Ting Wang  1 , Zifeng Huang  1 , Fen Xie  1 , Xiaobo Wei  1 , Qin Yang  1 , Mengyan Li  3 , Kefu Ma  4 , Fengli Zhou  5 , Beisha Tang  6 , Vincent C T Mok  7 , Shuzhen Zhu  1 , Qing Wang  1
Affiliations

Contra-Directional Expression of Plasma Superoxide Dismutase with Lipoprotein Cholesterol and High-Sensitivity C-reactive Protein as Important Markers of Parkinson's Disease Severity

Wanlin Yang et al. Front Aging Neurosci. .

Abstract

Aim: Oxidative stress and inflammation play critical roles in the neuropathogenesis of PD. We aimed to evaluate oxidative stress and inflammation status by measuring serum superoxide dismutase (SOD) with lipoprotein cholesterol and high-sensitivity C-reactive protein (hsCRP) respectively in PD patients, and explore their correlation with the disease severity. Methods: We performed a cross-sectional study that included 204 PD patients and 204 age-matched healthy controls (HCs). Plasma levels of SOD, hsCRP, total cholesterol, high-density lipoprotein cholesterol (HDL-C) and low-density lipoprotein cholesterol (LDL-C) were measured. A series of neuropsychological assessments were performed to rate the severity of PD. Results: The plasma levels of SOD (135.7 ± 20.14 vs. 147.2 ± 24.34, P < 0.0001), total cholesterol, HDL-C and LDL-C in PD were significantly lower than those in HCs; the hsCRP level was remarkably increased in PD compared to HC (2.766 ± 3.242 vs. 1.637 ± 1.597, P < 0.0001). The plasma SOD was negatively correlated with the hsCRP, while positively correlated with total cholesterol, HDL-C, and LDL-C in PD patients. The plasma SOD were negatively correlated with H&Y, total UPDRS, UPDRS (I), UPDRS (II), and UPDRS (III) scores, but positively correlated with MoCA and MMSE scores. Besides, hsCRP was negatively correlated with MoCA; while total cholesterol, HDL-C and LDL-C were positively correlated with the MoCA, respectively. Conclusion: Our findings suggest that lower SOD along with cholesterol, HDL-C and LDL-C, and higher hsCRP levels might be important markers to assess the PD severity. A better understanding of SOD and hsCRP may yield insights into the pathogenesis of PD.

Keywords: Parkinson’s disease; high-sensitivity C-reactive protein; inflammation; lipoprotein cholesterol; oxidative stress; superoxide dismutase.

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Figures

Figure 1
Figure 1
Comparisons of plasma biomarker levels between PD patients and healthy controls (HCs). (A) Comparison of superoxide dismutase (SOD) levels between the PD patients and HCs. ****PD (total) vs. Ctrl (total), P < 0.0001; ##PD (male) vs. Ctrl (male), P < 0.01; ††††PD (female) vs. Ctrl (female), P < 0.0001. (B) Comparison of high-sensitivity C-reactive protein (hsCRP) levels between the PD patients and HCs. ****PD (total) vs. Ctrl (total), P < 0.0001; ####PD (male) vs. Ctrl (male), P < 0.0001; †PD (female) vs. Ctrl (female), P < 0.05. (C) Comparison of cholesterol levels between the PD patients and HCs. ***PD (total) vs. Ctrl (total), P < 0.001; #PD (male) vs. Ctrl (male), P < 0.05; ††PD (female) vs. Ctrl (female), P < 0.01. (D) Comparison of high-density lipoprotein cholesterol (HDL-C) levels between the PD patients and HCs. **PD (total) vs. Ctrl (total), P < 0.01; ##PD (male) vs. Ctrl (male), P < 0.01. (E) Comparison of low-density lipoprotein cholesterol (LDL-C) levels between the PD patients and HCs. ***PD (total) vs. Ctrl (total), P < 0.001; ##PD (male) vs. Ctrl (male), P < 0.01. ††PD (female) vs. Ctrl (female), P < 0.01.
Figure 2
Figure 2
Correlation analysis between plasma SOD and hsCRP/cholesterol/HDL-C/LDL-C in PD Patients. (A) A significant negative correlation between SOD and hsCRP in PD Patients. (B) A significant positive correlation between SOD and cholesterol in PD Patients. (C) A significant positive correlation between SOD and HDL-C in PD Patients. (D) A significant positive correlation between SOD and LDL-C in PD Patients. ****P < 0.0001.
Figure 3
Figure 3
Correlation analysis between plasma SOD and UPDRS/H&Y/MoCA/MMSE scores in PD Patients. (A) A significant negative correlation between SOD and total UPDRS scores in PD Patients. (B) A significant negative correlation between SOD and UPDRS (I) scores in PD Patients. (C) A significant negative correlation between SOD and UPDRS (II) scores in PD Patients. (D) A significant negative correlation between SOD and UPDRS (III) scores in PD Patients. (E) A significant negative correlation between SOD and H&Y scores in PD Patients. (F) A significant positive correlation between SOD and MoCA scores in PD Patients. (G) A significant positive correlation between SOD and MMSE scores in PD Patients. ****P < 0.0001.
Figure 4
Figure 4
ROC curves to evaluate the utility of plasma levels of SOD, hsCRP, cholesterol, HDL-C and LDL-C for the discrimination of PD patients from healthy controls. (A) The area under the curves (AUCs) of the ROC curves for SOD, hsCRP and SOD+hsCRP. (B) The AUCs of the ROC curves for SOD, Chol, and SOD+Chol. (C) The AUCs of the ROC curves for SOD, HDL-C and SOD+HDL-C. (D) The AUCs of the ROC curves for SOD, LDL-C and SOD+LDL-C. (E) The AUCs of the ROC curves for SOD, SOD+Chol+HDL-C+LDL-C and SOD+Chol+HDL-C+LDL-C+hsCRP. A, area under the curves. *P < 0.05, **P < 0.01, ****P < 0.0001.
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