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Aberrant expression of microRNA-132-3p and microRNA-146a-5p in Parkinson’s disease patients

  • Yu Shu , Jinjun Qian EMAIL logo and Chunyan Wang
Published/Copyright: September 2, 2020
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Open Life Sciences
From the journal Open Life Sciences Volume 15 Issue 1

Abstract

Parkinson’s disease (PD) is an age-related neurodegenerative disorder which is assessed based on the motor symptoms. A number of microRNAs (miRNAs) are dysregulated and involved in the pathogenesis or development of PD. However, no confirmed markers are used for the early detection of PD. The present study aimed to elucidate the potential two miRNAs (miR-132-3p and miR-146-5p) as novel markers for early PD diagnosis. In the present study, the expression levels of miR-132-3p and miR-146-5p in serum samples from 82 patients with PD and 44 healthy volunteers were measured by reverse transcription-quantitative polymerase chain reaction. Furthermore, the correlation analysis was performed between aberrant miRNAs and Braak staging, Part V of the Unified Parkinson’s Disease Rating Scale (UPDRS-V; the modified Hoehn and Yahr staging of PD) and Part III of the UPDRS-III. Subsequently, the receiver–operating characteristic (ROC) curve results of miR-132-3p and miR-146-5p from healthy volunteers for PD prediction and from severe PD patients were assessed. From the results it was observed that miR-132-3p and miR-146a-5p expressions were significantly decreased in the serum samples of patients with PD compared to those in the healthy volunteers. Moreover, the expressions of miR-132-3p and miR-146a-5p showed a dramatic decrease in severe PD patients as compared to the normal PD patients. Meanwhile, miR-132-3p and miR-146-5p expressions were negatively correlated with Braak staging (r = −0.45, P < 0.0001; r = −0.51, P < 0.0001), UPDRS-III (r = −0.55, P < 0.0001; r = −0.51, P < 0.0001) and UPDRS-V scores (r = − 0.46, P < 0.0001; r = −0.45, P < 0.0001) in PD patients. The area under the curve (AUC) results of miR-132-3p and miR-146a-5p in discriminating PD patients from the healthy controls were 0.7325 (95% CI = 0.6400–0.8251) and 0.7295 (95% CI = 0.3658–0.8232). Moreover, the AUC results of miR-132-3p and miR-146-5p concerning discriminating severe PD patients from normal PD patients were 0.8175 (95% CI = 0.7229–0.9121) and 0.7921 (95% CI = 0.6937–0.8905). In other words, both miR-132-3p and miR-146a-5p may function as promising biomarkers for early diagnosis of PD.

Keywords: Parkinson’s disease; biomarker; diagnosis; miRNAs

1 Introduction

Parkinson’s disease (PD), characterized by the loss of dopaminergic neurons in the substantia nigra, is the second most common age-related neurodegenerative disorder [1]. To date, dopamine replacement and pharmacological treatments were frequently applied for symptomatic therapies in order to slow the neurodegenerative process [2]. However, despite huge contributions to clinical treatment, the efficiency was not satisfactory due to the various adverse effects [3]. So far, the clinical diagnosis of PD mainly depends on histopathology, which in turn needs invasive surgical brain biopsy and clinical manifestations using Unified Parkinson’s Disease Rating Scale (UPDRS)-V and UPDRS-III scores [4,5]. These two golden criteria are subjective, invasive and limited, which will seriously interfere with the accuracy of early PD detection. Thus, it is necessary to identify crucial biomarkers for the early diagnosis of PD.

MicroRNAs (miRNAs) are a group of small, non-coding and endogenous RNAs that regulate gene expression by binding to complementary sequences in post-transcriptional processes [6]. As reported, a number of miRNAs participated in different cellular processes, including proliferation, apoptosis and differentiation so as to regulate pathogenesis resulting in the development of various diseases [7,8,9]. The miRNA profiles have documented that several miRNAs were aberrantly expressed in serum samples obtained from PD patients, such as miR-29a-3p, miR-30a-5p, miR-30b-5p, miR-103a-3p, miR-153, miR309-3p and so on [10,11,12]. In a previous study, the expressions of miR-132-3p and miR-146a-5p generally decreased in PD patients compared to the unaffected controls [3,13], suggesting that these two miRNAs may be good candidates for detecting PD progression. Also, several miRNAs were identified as promising biomarkers for PD [14,15]. However, the clinical values of miR-132-3p and miR-146a-5p concerning the early diagnosis of PD still remained to be elucidated.

According to the previous studies [16,17,18,19], PD patients were divided into five different stages; and based on the severity of symptoms, they were divided into mild PD, moderate PD and severe PD. Mild PD was described as speech abnormalities, rigidity of the muscles in the trunk, rigidity, loss of facial expression or rigidity. Moderate PD was described as loss of balance and slowness of movement. Severe PD was described as severely disabling, such as delusions, hallucinations, unable to rise, unable to walk or freeze or stumble when walking. The aim of the present study was to find out a novel adjuvant method to help improve the accuracy of early diagnosis of PD. Hence, based on the previous study, we divided the PD patients into normal PD and severe PD to discriminate the two different severities of PD.

In the present study, we focused on miR-132-3p and miR-146a-5p to better investigate and understand their potential clinical values as PD biomarkers.

2 Materials and methods

2.1 Patients

A total of 82 patients with PD and 44 healthy volunteers were recruited from the Fourth Affiliated People’s Hospital of Jiangsu University between June 2015 and October 2017 (Table 1). The clinical diagnosis of PD was based on the criteria of Part V of the UPDRS (UPDRS-V; the modified Hoehn and Yahr staging of PD), Part III of the UPDRS (UPDRS-III) and magnetic resonance imaging.

Table 1

Clinical data of PD patients and healthy volunteers

VariablesPD (n = 82)Healthy (n = 44)P value
Age (years)68.53 ± 7.5366.24 ± 8.620.1217
Gender
Male52 (63.3%)27 (61.4%)0.7816
Female30 (36.7%)17 (38.6%)
Family PD history30 (36.6%)2 (4.5%)P < 0.0001
Smoking11 (12.5%)6 (13.6%)0.8174
Alcohol abuse15 (18.3%)8 (18.2%)0.9854
Diabetes22 (26.8%)13 (15.9%)0.0600
Hypertension33 (40.2%)20 (45.5%)0.4489
MMSE scores28.2 ± 2.327.5 ± 3.20.1595
miR-132-3p (fold)0.67 ± 0.040.99 ± 0.06P < 0.0001
miR-146a-5p (fold)0.66 ± 0.041.02 ± 0.06P < 0.0001

PD, Parkinson’s disease; Healthy, healthy volunteers; MMSE, Mini-Mental State Examination. Data in age, MMSE scores, miR-132-3p and miR-146a-5p expression were analyzed by chi-square test, while other variables were analyzed using ANOVA followed by Bonferroni’s post hoc test.

Healthy controls fasted for 12 h before serum samples were taken, while PD patients were forbidden to take any anti-parkinsonian medications and fasted for 12 h before sample collection. Serum samples (5 mL) were taken and preserved in tubes without anticoagulant at room temperature following the protocols from Parkinson Progression Marker Initiative. Then the tubes were centrifuged for 15 min at 1,900 × g at 4°C. After centrifugation, all samples were immediately stored at −80°C until the subsequent analysis.

  1. Informed consent: Informed consent has been obtained from all individuals included in this study.

  2. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies and in accordance with the tenets of the Helsinki Declaration, and has been approved by the Ethics Committee of the Fourth Affiliated People’s Hospital of Jiangsu University.

2.2 Reverse transcription-quantitative polymerase chain reaction (RT-qPCR) assay

Total RNA was isolated and extracted from serum samples using TRIzol reagent (Invitrogen, Thermo Fisher Scientific, Inc., USA) by following the instruction. Complementary DNA was synthesized using the SuperScript III First-Strand Synthesis kit (Invitrogen, Thermo Fisher Scientific, Inc., USA). The amplification with specific primers of miR-132-3p and miR-146a-5p was conducted using FastStart Essential DNA Green Master (Roche, Mannheim, Germany) on ProFlex™ PCR machine according to the protocol. The PCR thermal cycling conditions were as follows: denaturation at 96°C for 5 min, followed by 40 cycles of 96°C for 5 s and 62°C for 10 s. The U6 served as an endogenous reference gene to normalize the miRNAs, and the relative expressions of miRNAs were calculated using the 2−ΔΔCt method. All the procedures were conducted in triplicate. The primers were as follows: miR-132-3p forward 5′-GCGCGCGTAACAGTCTACAGG-3′ and reverse 5′-GTCGTATCCAGTGCAGGGTCC-3′; miR-146a-5p forward 5′-CGAGTCCAGTTTTCCCAGGA′ and reverse 5′-GTCGTATCCAGTGCAGGG-3′; U6 forward 5′-CTCGCTTCGGCAGCACATATACT-3′ and reverse 5′-CGCTTCACGAATTTGCGTGT-3′.

2.3 Statistical analysis

Statistical analysis was carried out using SPSS version 20.0 software (IBM, USA). The chi-square test and ANOVA followed by Bonferroni’s post hoc test were used to distinguish between miR-132-3p and miR-146a-5p in patients with PD and healthy volunteers. Spearman’s rank correlation analysis was performed to assess the association between aberrant miRNAs and Braak staging, UPDRS-V, and UPDRS-III. Receiver–operating characteristic (ROC) curves were constructed and area under the curve (AUC) values were detected to identify the diagnostic values of miR-132-3p and miR-146a-5p for PD. Differences in all data were expressed as mean ± standard deviation (SD), and P < 0.05 was considered to be statistically significant.

3 Results

3.1 Clinical data

As demonstrated in Table 1, the clinical data of 82 PD patients and 44 healthy controls were compared. No differences were observed in age, gender, smoking, alcohol abuse, diabetes or hypertension. However, remarkable differences were detected in family PD history (P < 0.01), miR-132-3p (P < 0.01) and miR-146a-5p expression (P < 0.01) between PD patients and healthy volunteers.

3.2 The comparison of clinical data between groups divided based on PD severity

As described in Section 1, the PD patients were divided into normal PD and severe PD. As demonstrated in Table 2, no significant differences were observed in age and gender between the two groups. However, remarkable differences were found in UPDRS-III score (P = 0.0044), UPDRS-V score (P = 0.0006), Braak staging (P = 0.0006), miR-132-3p expression (P < 0.0001) and miR-146a-5p expression (P < 0.0001) between severe and normal PD groups.

Table 2

Different groups of PD patients divided by the severity of PD

VariablesPD (n = 82)Severe (n = 34)Normal PD (n = 48)P value
UPDRS-III
<10123 (8.82%)9 (18.75%)—
10–30347 (20.59%)27 (56.25%)
30–502116 (41.06%)5 (10.42%)
>50158 (23.53%)7 (14.58%)
UPDRS-V
I214 (11.76%)17 (35.42%)—
II–III5022 (64.71%)28 (58.33%)
IV–V75 (14.71%)2 (4.17%)
>V43 (8.82%)1 (2.08%)
Braak staging
I–II203 (8.82%)17 (35.42%)—
III–IV4923 (67.65%)26 (54.17%)
V–VI138 (23.53%)5 (10.42%)
Age (years)68.53 ± 7.5367.32 ± 7.6868.81 ± 7.040.3660
Gender
Male5223290.5126
Female301119
Disease severity
UPDRS-III scores29.77 ± 10.6335.68 ± 10.5225.58 ± 11.070.0044
UPDRS-V scores2.47 ± 0.64 3.03 ± 0.682.06 ± 0.560.0006
Braak staging3.23 ± 0.503.82 ± 0.482.75 ± 0.510.0006
miR-132-3p (fold)0.67 ± 0.070.52 ± 0.050.78 ± 0.09P < 0.0001
miR-146a-5p (fold)0.66 ± 0.060.57 ± 0.040.73 ± 0.07P < 0.0001

Severe, severe PD patients; PD, Parkinson’s disease; —, not applicable; UPDRS, Unified Parkinson’s Disease Rating Scale; Data in age, disease severity, miR-132-3p and miR-146a-5p expression were analyzed with ANOVA followed by Bonferroni’s post hoc test, while other variables were analyzed by chi-square test.

3.3 Expression levels of miR-132-3p and miR-146a-5p in serum samples of PD patients and healthy volunteers

As demonstrated in Figure 1a and b, the expression levels of miR-132-3p and miR-146a-5p significantly decreased in the serum samples of PD patients (P < 0.01), as compared with those in healthy controls. Furthermore, compared with normal PD patients, the expressions of miR-132-3p and miR-146a-5p were dramatically decreased in severe PD groups (P < 0.01).

Figure 1 The expressions of miR-132-3p (a) and miR-146a-5p (b) in serum samples of 82 PD patients and 44 healthy volunteers using RT-qPCR analysis. **P < 0.01, PD vs controls. PD, Parkinson’s disease; severe, severe PD patients; control, healthy volunteers.
Figure 1

The expressions of miR-132-3p (a) and miR-146a-5p (b) in serum samples of 82 PD patients and 44 healthy volunteers using RT-qPCR analysis. **P < 0.01, PD vs controls. PD, Parkinson’s disease; severe, severe PD patients; control, healthy volunteers.

3.4 Correlation analysis of miR-132-3p and miR-146a-5p with Braak stage, UPDRS-V and UPDRS-III scores at admission

Correlation analysis was performed using Pearson’s correlation analysis. As demonstrated in Figure 2a–c, the expression of miR-132-3p was negatively related to UPDRS-III (r = −0.45, P < 0.0001), UPDRS-V (r = −0.55, P < 0.0001) and Braak staging (r = −0.46, P < 0.0001). Meanwhile, the results were similar with regard to the expression of miR-146a-5p (r = − 0.51, P < 0.0001; r = −0.51, P < 0.0001; r = −0.45, P < 0.0001, respectively; Figure 2d–f).

Figure 2 miR-132-3p and miR-146a-5p expressions were correlated with UPDRS-III, UPDRS-V scores and Braak staging in PD patients. (a) Serum miR-132-3p was negatively correlated with the UPDRS-III scores in PD patients. (b) Serum miR-132-3p was negatively correlated with UPDRS-V scores in PD patients. (c) Serum miR-132-3p was negatively correlated with Braak staging in PD patients. (d) Serum miR-146a-5p was negatively correlated with the UPDRS-III scores in PD patients. (e) Serum miR-146a-5p was negatively correlated with UPDRS-V scores in PD patients. (f) Serum miR-146a-5p was negatively correlated with Braak staging in PD patients.
Figure 2

miR-132-3p and miR-146a-5p expressions were correlated with UPDRS-III, UPDRS-V scores and Braak staging in PD patients. (a) Serum miR-132-3p was negatively correlated with the UPDRS-III scores in PD patients. (b) Serum miR-132-3p was negatively correlated with UPDRS-V scores in PD patients. (c) Serum miR-132-3p was negatively correlated with Braak staging in PD patients. (d) Serum miR-146a-5p was negatively correlated with the UPDRS-III scores in PD patients. (e) Serum miR-146a-5p was negatively correlated with UPDRS-V scores in PD patients. (f) Serum miR-146a-5p was negatively correlated with Braak staging in PD patients.

3.5 ROC curve analysis

The ROC curve analysis was carried out so as to measure the diagnostic value of miR-132-3p and miR-146a-5p for PD. As demonstrated in Figure 3a and c, the AUC of miR-132-3p and miR-146a-5p in discriminating PD from healthy controls was 0.7325 (95% CI = 0.6400–0.8251) and 0.7295 (95% CI = 0.3658–0.8232), respectively. Meanwhile, the AUC of miR-132-3p and miR-146a-5p in discriminating severe PD from normal PD patients was 0.8175 (95% CI = 0.7229–0.9121) and 0.7921 (95% CI = 0.6937–0.8905), respectively (Figure 3b and d).

Figure 3 The ROC analysis of miR-132-3p (a and b) and miR-146a-5p (c and d) in discriminating PD cases from healthy controls and severe PD patients from normal PD patients.
Figure 3

The ROC analysis of miR-132-3p (a and b) and miR-146a-5p (c and d) in discriminating PD cases from healthy controls and severe PD patients from normal PD patients.

4 Discussion

To date, neurological detection and neuroimaging are the basic and golden standards for physicians in the diagnosis of PD. However, both these criteria lack sensitivity and are subjective. Therefore, there is an urgent need to discover non-invasive, sensitive and accurate indicators for PD.

To the best of our knowledge, certain miRNAs were reported to be dysregulated in PD patients and may serve as promising biomarkers for PD diagnosis [20,21]. A previous study [3] has demonstrated that miR-4639 served as a potential biomarker for PD by regulating DJ-1 expression; meanwhile dysregulation of miR-4639 was correlated with UPDRS-I, UPDRS-II and UPDRS-III as well. Moreover, another group also illustrated that miR-132-3p and miR-146a-5p were abnormally expressed in neurodegenerative diseases such as PD [13]. However, to our knowledge, no reports have elucidated their potential role and mechanism in PD.

Both miR-132-3p and miR-146a-5p were dysregulated in various solid malignancies and also involved in human cancer and inflammation-related diseases [22,23,24,25]. In the present study, we found that miR-132-3p and miR-146-5p expressions were significantly decreased in PD patients and further decreased in severe PD patients compared with healthy participants and normal PD patients. Previously, serum miR-132-3p and miR-146-5p were reported to be decreased in PD patients, which is consistent with our study [13,26]. However, our report further determined their clinical values concerning clinical diagnosis. Braak staging system classifies the degree of pathology in PD and is widely used in clinical diagnosis and research. This system is normally divided into six different stages, i.e., stages 1–6, characterized by abnormal pathology, in particular neurological structures. UPDRS-III and UPDRS-V scores were the golden criteria for clinical diagnosis of PD. UPDRS-III is clinician-score monitored motor evaluation, while UPDRS-V is Hoehn and Yahr staging of PD severity. As shown in our study, serum miR-132-3p and miR-146a-5p have strongly negative correlation with Braak staging, UPDRS-III and UPDRS-V scores. More importantly, significant differences were observed among Braak staging, UPDRS-III and UPDRS-V scores between severe and normal PD patients.

The AUC results of miR-132-3p and miR-146a-5p in discriminating PD from healthy controls were 0.7325 and 0.7295, respectively. Moreover, the AUC results of ROC miR-132-3p and miR-146a-5p in discriminating severe PD patients from normal PD patients were 0.8175 and 0.7921, respectively. Taken together, the decreased miR-132-3p and miR-146a-5p may indicate the severity of PD patients, which help in contributing to clinical diagnosis. The earlier the diagnosis, the more effective the treatment will alleviate the symptoms.

However, the present study still has some limitations. The samples recruited in our study are relatively small, which results in limited accuracy. Moreover, the samples were recruited only in China, so it needs to be confirmed whether the results are applicable worldwide. Finally, a 3-year or 5-year follow-up analysis needs to be performed in the future in order to evaluate the prognosis values of miR-132-3p and miR-146a-5p in PD.

Our findings elucidate the clinical potentials of serum miR-132-3p and miR-146a-5p for evaluating the diagnosis for PD patients.

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Acknowledgments

This study was supported by the Key research and development plan of Zhenjiang City (no. SH2019054).

  1. Author contributions: Yu Shu and Chunyan Wang were in charge of manuscript original writing, supervision, data analysis and study conception. Jinjun Qian was in charge of manuscript editing and revision, sample collection and supervision.

  2. Conflict of interest: The authors state no conflict of interest.

  3. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2019-12-17
Revised: 2020-06-14
Accepted: 2020-06-15
Published Online: 2020-09-02

© 2020 Yu Shu et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  32. Prevalence of dyslipidemia in Tibetan monks from Gansu Province, Northwest China
  33. Sevoflurane inhibits proliferation, invasion, but enhances apoptosis of lung cancer cells by Wnt/β-catenin signaling via regulating lncRNA PCAT6/ miR-326 axis
  34. MiR-542-3p suppresses neuroblastoma cell proliferation and invasion by downregulation of KDM1A and ZNF346
  35. Calcium Phosphate Cement Causes Nucleus Pulposus Cell Degeneration Through the ERK Signaling Pathway
  36. Human Dental Pulp Stem Cells Exhibit Osteogenic Differentiation Potential
  37. MiR-489-3p inhibits cell proliferation, migration, and invasion, and induces apoptosis, by targeting the BDNF-mediated PI3K/AKT pathway in glioblastoma
  38. Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating the microRNA-34a-5p/NOTCH1 signaling pathway
  39. Large Brunner’s gland adenoma of the duodenum for almost 10 years
  40. Neurotrophin-3 accelerates reendothelialization through inducing EPC mobilization and homing
  41. Hepatoprotective effects of chamazulene against alcohol-induced liver damage by alleviation of oxidative stress in rat models
  42. FXYD6 overexpression in HBV-related hepatocellular carcinoma with cirrhosis
  43. Risk factors for elevated serum colorectal cancer markers in patients with type 2 diabetes mellitus
  44. Effect of hepatic sympathetic nerve removal on energy metabolism in an animal model of cognitive impairment and its relationship to Glut2 expression
  45. Progress in research on the role of fibrinogen in lung cancer
  46. Advanced glycation end product levels were correlated with inflammation and carotid atherosclerosis in type 2 diabetes patients
  47. MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB
  48. Knockdown of DDX46 inhibits trophoblast cell proliferation and migration through the PI3K/Akt/mTOR signaling pathway in preeclampsia
  49. Buformin suppresses osteosarcoma via targeting AMPK signaling pathway
  50. Effect of FibroScan test in antiviral therapy for HBV-infected patients with ALT <2 upper limit of normal
  51. LncRNA SNHG15 regulates osteosarcoma progression in vitro and in vivo via sponging miR-346 and regulating TRAF4 expression
  52. LINC00202 promotes retinoblastoma progression by regulating cell proliferation, apoptosis, and aerobic glycolysis through miR-204-5p/HMGCR axis
  53. Coexisting flavonoids and administration route effect on pharmacokinetics of Puerarin in MCAO rats
  54. GeneXpert Technology for the diagnosis of HIV-associated tuberculosis: Is scale-up worth it?
  55. Circ_001569 regulates FLOT2 expression to promote the proliferation, migration, invasion and EMT of osteosarcoma cells through sponging miR-185-5p
  56. Lnc-PICSAR contributes to cisplatin resistance by miR-485-5p/REV3L axis in cutaneous squamous cell carcinoma
  57. BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells
  58. MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process
  59. Inhibition of lncRNA LINC00461/miR-216a/aquaporin 4 pathway suppresses cell proliferation, migration, invasion, and chemoresistance in glioma
  60. Upregulation of miR-150-5p alleviates LPS-induced inflammatory response and apoptosis of RAW264.7 macrophages by targeting Notch1
  61. Long non-coding RNA LINC00704 promotes cell proliferation, migration, and invasion in papillary thyroid carcinoma via miR-204-5p/HMGB1 axis
  62. Neuroanatomy of melanocortin-4 receptor pathway in the mouse brain
  63. Lipopolysaccharides promote pulmonary fibrosis in silicosis through the aggravation of apoptosis and inflammation in alveolar macrophages
  64. Influences of advanced glycosylation end products on the inner blood–retinal barrier in a co-culture cell model in vitro
  65. MiR-4328 inhibits proliferation, metastasis and induces apoptosis in keloid fibroblasts by targeting BCL2 expression
  66. Aberrant expression of microRNA-132-3p and microRNA-146a-5p in Parkinson’s disease patients
  67. Long non-coding RNA SNHG3 accelerates progression in glioma by modulating miR-384/HDGF axis
  68. Long non-coding RNA NEAT1 mediates MPTP/MPP+-induced apoptosis via regulating the miR-124/KLF4 axis in Parkinson’s disease
  69. PCR-detectable Candida DNA exists a short period in the blood of systemic candidiasis murine model
  70. CircHIPK3/miR-381-3p axis modulates proliferation, migration, and glycolysis of lung cancer cells by regulating the AKT/mTOR signaling pathway
  71. Reversine and herbal Xiang–Sha–Liu–Jun–Zi decoction ameliorate thioacetamide-induced hepatic injury by regulating the RelA/NF-κB/caspase signaling pathway
  72. Therapeutic effects of coronary granulocyte colony-stimulating factor on rats with chronic ischemic heart disease
  73. The effects of yam gruel on lowering fasted blood glucose in T2DM rats
  74. Circ_0084043 promotes cell proliferation and glycolysis but blocks cell apoptosis in melanoma via circ_0084043-miR-31-KLF3 axis
  75. CircSAMD4A contributes to cell doxorubicin resistance in osteosarcoma by regulating the miR-218-5p/KLF8 axis
  76. Relationship of FTO gene variations with NAFLD risk in Chinese men
  77. The prognostic and predictive value of platelet parameters in diabetic and nondiabetic patients with sudden sensorineural hearing loss
  78. LncRNA SNHG15 contributes to doxorubicin resistance of osteosarcoma cells through targeting the miR-381-3p/GFRA1 axis
  79. miR-339-3p regulated acute pancreatitis induced by caerulein through targeting TNF receptor-associated factor 3 in AR42J cells
  80. LncRNA RP1-85F18.6 affects osteoblast cells by regulating the cell cycle
  81. MiR-203-3p inhibits the oxidative stress, inflammatory responses and apoptosis of mice podocytes induced by high glucose through regulating Sema3A expression
  82. MiR-30c-5p/ROCK2 axis regulates cell proliferation, apoptosis and EMT via the PI3K/AKT signaling pathway in HG-induced HK-2 cells
  83. CTRP9 protects against MIA-induced inflammation and knee cartilage damage by deactivating the MAPK/NF-κB pathway in rats with osteoarthritis
  84. Relationship between hemodynamic parameters and portal venous pressure in cirrhosis patients with portal hypertension
  85. Long noncoding RNA FTX ameliorates hydrogen peroxide-induced cardiomyocyte injury by regulating the miR-150/KLF13 axis
  86. Ropivacaine inhibits proliferation, migration, and invasion while inducing apoptosis of glioma cells by regulating the SNHG16/miR-424-5p axis
  87. CD11b is involved in coxsackievirus B3-induced viral myocarditis in mice by inducing Th17 cells
  88. Decitabine shows anti-acute myeloid leukemia potential via regulating the miR-212-5p/CCNT2 axis
  89. Testosterone aggravates cerebral vascular injury by reducing plasma HDL levels
  90. Bioengineering and Biotechnology
  91. PL/Vancomycin/Nano-hydroxyapatite Sustained-release Material to Treat Infectious Bone Defect
  92. The thickness of surface grafting layer on bio-materials directly mediates the immuno-reacitivity of macrophages in vitro
  93. Silver nanoparticles: synthesis, characterisation and biomedical applications
  94. Food Science
  95. Bread making potential of Triticum aestivum and Triticum spelta species
  96. Modeling the effect of heat treatment on fatty acid composition in home-made olive oil preparations
  97. Effect of addition of dried potato pulp on selected quality characteristics of shortcrust pastry cookies
  98. Preparation of konjac oligoglucomannans with different molecular weights and their in vitro and in vivo antioxidant activities
  99. Animal Sciences
  100. Changes in the fecal microbiome of the Yangtze finless porpoise during a short-term therapeutic treatment
  101. Agriculture
  102. Influence of inoculation with Lactobacillus on fermentation, production of 1,2-propanediol and 1-propanol as well as Maize silage aerobic stability
  103. Application of extrusion-cooking technology in hatchery waste management
  104. In-field screening for host plant resistance to Delia radicum and Brevicoryne brassicae within selected rapeseed cultivars and new interspecific hybrids
  105. Studying of the promotion mechanism of Bacillus subtilis QM3 on wheat seed germination based on β-amylase
  106. Rapid visual detection of FecB gene expression in sheep
  107. Effects of Bacillus megaterium on growth performance, serum biochemical parameters, antioxidant capacity, and immune function in suckling calves
  108. Effects of center pivot sprinkler fertigation on the yield of continuously cropped soybean
  109. Special Issue On New Approach To Obtain Bioactive Compounds And New Metabolites From Agro-Industrial By-Products
  110. Technological and antioxidant properties of proteins obtained from waste potato juice
  111. The aspects of microbial biomass use in the utilization of selected waste from the agro-food industry
  112. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part I
  113. Automatic detection and segmentation of adenomatous colorectal polyps during colonoscopy using Mask R-CNN
  114. The impedance analysis of small intestine fusion by pulse source
  115. Errata
  116. Erratum to “Diagnostic performance of serum CK-MB, TNF-α and hs-CRP in children with viral myocarditis”
  117. Erratum to “MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process”
  118. Erratum to “Thermostable cellulase biosynthesis from Paenibacillus alvei and its utilization in lactic acid production by simultaneous saccharification and fermentation”
https://doi.org/10.1515/biol-2020-0060
Keywords for this article
Parkinson’s disease; biomarker; diagnosis; miRNAs
Creative Commons
BY 4.0

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  36. Human Dental Pulp Stem Cells Exhibit Osteogenic Differentiation Potential
  37. MiR-489-3p inhibits cell proliferation, migration, and invasion, and induces apoptosis, by targeting the BDNF-mediated PI3K/AKT pathway in glioblastoma
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  45. Progress in research on the role of fibrinogen in lung cancer
  46. Advanced glycation end product levels were correlated with inflammation and carotid atherosclerosis in type 2 diabetes patients
  47. MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB
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  49. Buformin suppresses osteosarcoma via targeting AMPK signaling pathway
  50. Effect of FibroScan test in antiviral therapy for HBV-infected patients with ALT <2 upper limit of normal
  51. LncRNA SNHG15 regulates osteosarcoma progression in vitro and in vivo via sponging miR-346 and regulating TRAF4 expression
  52. LINC00202 promotes retinoblastoma progression by regulating cell proliferation, apoptosis, and aerobic glycolysis through miR-204-5p/HMGCR axis
  53. Coexisting flavonoids and administration route effect on pharmacokinetics of Puerarin in MCAO rats
  54. GeneXpert Technology for the diagnosis of HIV-associated tuberculosis: Is scale-up worth it?
  55. Circ_001569 regulates FLOT2 expression to promote the proliferation, migration, invasion and EMT of osteosarcoma cells through sponging miR-185-5p
  56. Lnc-PICSAR contributes to cisplatin resistance by miR-485-5p/REV3L axis in cutaneous squamous cell carcinoma
  57. BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells
  58. MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process
  59. Inhibition of lncRNA LINC00461/miR-216a/aquaporin 4 pathway suppresses cell proliferation, migration, invasion, and chemoresistance in glioma
  60. Upregulation of miR-150-5p alleviates LPS-induced inflammatory response and apoptosis of RAW264.7 macrophages by targeting Notch1
  61. Long non-coding RNA LINC00704 promotes cell proliferation, migration, and invasion in papillary thyroid carcinoma via miR-204-5p/HMGB1 axis
  62. Neuroanatomy of melanocortin-4 receptor pathway in the mouse brain
  63. Lipopolysaccharides promote pulmonary fibrosis in silicosis through the aggravation of apoptosis and inflammation in alveolar macrophages
  64. Influences of advanced glycosylation end products on the inner blood–retinal barrier in a co-culture cell model in vitro
  65. MiR-4328 inhibits proliferation, metastasis and induces apoptosis in keloid fibroblasts by targeting BCL2 expression
  66. Aberrant expression of microRNA-132-3p and microRNA-146a-5p in Parkinson’s disease patients
  67. Long non-coding RNA SNHG3 accelerates progression in glioma by modulating miR-384/HDGF axis
  68. Long non-coding RNA NEAT1 mediates MPTP/MPP+-induced apoptosis via regulating the miR-124/KLF4 axis in Parkinson’s disease
  69. PCR-detectable Candida DNA exists a short period in the blood of systemic candidiasis murine model
  70. CircHIPK3/miR-381-3p axis modulates proliferation, migration, and glycolysis of lung cancer cells by regulating the AKT/mTOR signaling pathway
  71. Reversine and herbal Xiang–Sha–Liu–Jun–Zi decoction ameliorate thioacetamide-induced hepatic injury by regulating the RelA/NF-κB/caspase signaling pathway
  72. Therapeutic effects of coronary granulocyte colony-stimulating factor on rats with chronic ischemic heart disease
  73. The effects of yam gruel on lowering fasted blood glucose in T2DM rats
  74. Circ_0084043 promotes cell proliferation and glycolysis but blocks cell apoptosis in melanoma via circ_0084043-miR-31-KLF3 axis
  75. CircSAMD4A contributes to cell doxorubicin resistance in osteosarcoma by regulating the miR-218-5p/KLF8 axis
  76. Relationship of FTO gene variations with NAFLD risk in Chinese men
  77. The prognostic and predictive value of platelet parameters in diabetic and nondiabetic patients with sudden sensorineural hearing loss
  78. LncRNA SNHG15 contributes to doxorubicin resistance of osteosarcoma cells through targeting the miR-381-3p/GFRA1 axis
  79. miR-339-3p regulated acute pancreatitis induced by caerulein through targeting TNF receptor-associated factor 3 in AR42J cells
  80. LncRNA RP1-85F18.6 affects osteoblast cells by regulating the cell cycle
  81. MiR-203-3p inhibits the oxidative stress, inflammatory responses and apoptosis of mice podocytes induced by high glucose through regulating Sema3A expression
  82. MiR-30c-5p/ROCK2 axis regulates cell proliferation, apoptosis and EMT via the PI3K/AKT signaling pathway in HG-induced HK-2 cells
  83. CTRP9 protects against MIA-induced inflammation and knee cartilage damage by deactivating the MAPK/NF-κB pathway in rats with osteoarthritis
  84. Relationship between hemodynamic parameters and portal venous pressure in cirrhosis patients with portal hypertension
  85. Long noncoding RNA FTX ameliorates hydrogen peroxide-induced cardiomyocyte injury by regulating the miR-150/KLF13 axis
  86. Ropivacaine inhibits proliferation, migration, and invasion while inducing apoptosis of glioma cells by regulating the SNHG16/miR-424-5p axis
  87. CD11b is involved in coxsackievirus B3-induced viral myocarditis in mice by inducing Th17 cells
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  96. Modeling the effect of heat treatment on fatty acid composition in home-made olive oil preparations
  97. Effect of addition of dried potato pulp on selected quality characteristics of shortcrust pastry cookies
  98. Preparation of konjac oligoglucomannans with different molecular weights and their in vitro and in vivo antioxidant activities
  99. Animal Sciences
  100. Changes in the fecal microbiome of the Yangtze finless porpoise during a short-term therapeutic treatment
  101. Agriculture
  102. Influence of inoculation with Lactobacillus on fermentation, production of 1,2-propanediol and 1-propanol as well as Maize silage aerobic stability
  103. Application of extrusion-cooking technology in hatchery waste management
  104. In-field screening for host plant resistance to Delia radicum and Brevicoryne brassicae within selected rapeseed cultivars and new interspecific hybrids
  105. Studying of the promotion mechanism of Bacillus subtilis QM3 on wheat seed germination based on β-amylase
  106. Rapid visual detection of FecB gene expression in sheep
  107. Effects of Bacillus megaterium on growth performance, serum biochemical parameters, antioxidant capacity, and immune function in suckling calves
  108. Effects of center pivot sprinkler fertigation on the yield of continuously cropped soybean
  109. Special Issue On New Approach To Obtain Bioactive Compounds And New Metabolites From Agro-Industrial By-Products
  110. Technological and antioxidant properties of proteins obtained from waste potato juice
  111. The aspects of microbial biomass use in the utilization of selected waste from the agro-food industry
  112. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part I
  113. Automatic detection and segmentation of adenomatous colorectal polyps during colonoscopy using Mask R-CNN
  114. The impedance analysis of small intestine fusion by pulse source
  115. Errata
  116. Erratum to “Diagnostic performance of serum CK-MB, TNF-α and hs-CRP in children with viral myocarditis”
  117. Erratum to “MYL6B drives the capabilities of proliferation, invasion, and migration in rectal adenocarcinoma through the EMT process”
  118. Erratum to “Thermostable cellulase biosynthesis from Paenibacillus alvei and its utilization in lactic acid production by simultaneous saccharification and fermentation”
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