Substantially Altered Expression Profile of Diabetes/Cardiovascular/Cerebrovascular Disease Associated microRNAs in Children Descending from Pregnancy Complicated by Gestational Diabetes Mellitus—One of Several Possible Reasons for an Increased Cardiovascular Risk
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants
2.2. BP and Echocardiography Measurements, BMI Assessment
2.3. Processing of Samples
2.4. Reverse Transcription
2.5. Relative Quantification of microRNAs
2.6. Statistical Analysis
2.7. Bioinformatics Analysis—microRNA-Target Interactions on Disease Ontologies, Human Phenotype Ontologies, and OMIM Disorders
2.8. Workflow of the Study
3. Results
3.1. Higher Incidence of Valve Problems and Heart Defects in a group of Children Descending from GDM Complicated Pregnancies
3.2. Only Just miR-21-5p Indicates a Trend Towards Differentiation between Children with Normal and Abnormal Clinical Findings (BMI, Blood Pressure, and Echocardiogram Findings) Descending from Normal Pregnancies
3.3. Only Just miR-29a-3p and miR-92a-3p Indicate a Slight Differentiation Between Children with Normal and Abnormal Clinical Findings (BMI, Blood Pressure, and Echocardiogram Findings) Descending from GDM Complicated Pregnancies
3.4. Substantially Altered Expression Profile of Diabetes/Cardiovascular/Cerebrovascular Disease Associated microRNAs in Children Descending from Pregnancy Complicated by Gestational Diabetes Mellitus
3.5. Dysregulation of Multiple microRNAs in Children Descending from GDM Complicated Pregnancies with Normal Clinical Findings (Normal BMI, Blood Pressure, and Echocardiogram Findings)
3.6. Dysregulation of Multiple microRNAs in Children Descending from GDM Complicated Pregnancies with Abnormal Clinical Findings (Abnormal BMI, Blood Pressure, and Echocardiogram Findings)
3.7. Information on microRNA-Target Interactions on Disease Ontologies, Human Phenotype Ontologies, and OMIM Disorders
4. Discussion
5. Conclusions
6. Patents
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
GDM | Gestational Diabetes Mellitus |
PE | Preeclampsia |
FGR | Fetal growth restriction |
GH | Gestational hypertension |
AUC | Area under the Curve |
ROC | Receive Operating Characteristic |
FPR | False Positive Rate |
CI | Confidence Interval |
LR+ | Positive Likelihood Ratio |
LR- | Negative Likelihood Ratio |
NP | Normal Pregnancies |
BP | Blood Pressure |
OGTT | Oral glucose tolerance test |
IADPSG | International Association of Diabetes and Pregnancy Study Groups |
BMI | Body Mass Index |
SBP | Systolic Blood Pressure |
DBP | Diastolic Blood Pressure |
LDL | Low-density Lipoprotein |
GA | Gestational age |
CS | Caesarean Section |
EDTA | Ethylenediaminetetraacetic Acid |
NTC | No template control |
NAC | No amplification control |
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miRBase ID | Gene Location on Chromosome | Role in the Pathogenesis of Diabetes Mellitus and Cardiovascular/Cerebrovascular Diseases |
---|---|---|
hsa-miR-1-3p | 20q13.3 [46] 18q11.2 | Acute myocardial infarction, heart ischemia, post-myocardial infarction complications [47], thoracic aortic aneurysm [48], diabetes mellitus [49,50], vascular endothelial dysfunction [51]. |
hsa-miR-16-5p | 13q14.2 | Myocardial infarction [52,53], heart failure [54], acute coronary syndrome, cerebral ischaemic events [55], gestational diabetes mellitus [9,13,20], diabetes mellitus [56,57,58]. |
hsa-miR-17-5p | 13q31.3 [59,60] | Cardiac development [61], ischemia/reperfusion-induced cardiac injury [62], kidney ischemia-reperfusion injury [63], diffuse myocardial fibrosis in hypertrophic cardiomyopathy [64], acute ischemic stroke [65], coronary artery disease [66], adipogenic differentiation [67], gestational diabetes mellitus [9,13], diabetes mellitus [58,68]. |
hsa-miR-20a-5p | 13q31.3 [69] | Pulmonary hypertension [70], gestational diabetes mellitus [9,13,17], diabetic retinopathy [71], diabetes with abdominal aortic aneurysm [72]. |
hsa-miR-20b-5p | Xq26.2 [69] | Hypertension-induced heart failure [73], insulin resistance [74], T2DM [75,76], diabetic retinopathy [77]. |
hsa-miR-21-5p | 17q23.2 [78] | Homeostasis of the cardiovascular system [79], cardiac fibrosis and heart failure [80,81], thoracic aortic aneurysm [48], ascending aortic aneurysm [82], regulation of hypertension-related genes [83], myocardial infarction [84], insulin resistance [74], T2DM [85], T2DM with major cardiovascular events [86], T1DM [87,88,89], diabetic nephropathy [90]. |
hsa-miR-23a-3p | 19p13.12 | Heart failure [91], coronary artery disease [92], cerebral ischemia-reperfusion [93], vascular endothelial dysfunction [51], small and large abdominal aortic aneurysm [94], obesity and insulin resistance [95]. |
hsa-miR-24-3p | 19p13.12 | Asymptomatic carotid stenosis [96], familial hypercholesterolemia and coronary artery disease [97], angina pectoris [98], ischemic dilated cardiomyopathy [99], small and large abdominal aortic aneurysm [94], myocardial ischemia/reperfusion [100,101], diabetes mellitus [50,58,62,64]. |
hsa-miR-26a-5p | 3p22.2 [102] 12q14.1 | Heart failure, cardiac hypertrophy [103], myocardial infarction [84,104,105], ischemia/reperfusion injury [106], pulmonary arterial hypertension [107], T1DM [108], diabetic nephropathy [90]. |
hsa-miR-29a-3p | 7q32.3 | Ischemia/reperfusion-induced cardiac injury [109], cardiac cachexia, heart failure [110], atrial fibrillation [111], diffuse myocardial fibrosis in hypertrophic cardiomyopathy [64], coronary artery disease [112], pulmonary arterial hypertension [107], gestational diabetes mellitus [12], diabetes mellitus [49,57,113,114]. |
hsa-miR-92a-3p | 13q31.3 Xq26.2 | Mitral chordae tendineae rupture [115], children with rheumatic carditis [116], myocardial infarction [117], heart failure [118], coronary artery disease [119], renal injury-associated atherosclerosis [120]. |
hsa-miR-100-5p | 11q24.1 | Failing human heart, idiopathic dilated cardiomyopathy, ischemic cardiomyopathy [99], regulation of hypertension-related genes [83], T1DM [87]. |
hsa-miR-103a-3p | 5q34 [121] 20p13 | Hypertension [122], hypoxia-induced pulmonary hypertension [123], myocardial ischemia/reperfusion injury, acute myocardial infarction [124], ischemic dilated cardiomyopathy [99], obesity, regulation of insulin sensitivity [125], T1DM [126]. |
hsa-miR-125b-5p | 11q24.1 [126] 21q21.1 | Acute ischemic stroke [127], acute myocardial infarction [128,129], ischemic dilated cardiomyopathy [99], ascending aortic aneurysm [82], gestational diabetes mellitus [19], T1DM [130,131], T2DM [132]. |
hsa-miR-126-3p | 9q34.3 [133] | Acute myocardial infarction [105], thoracic aortic aneurysm [48], T2DM [86,134], T2DM with major cardiovascular events [86], gestational diabetes mellitus [10]. |
hsa-miR-130b-3p | 22q11.21 | Hypertriglyceridemia [135,136], intracranial aneurysms [137], hyperacute cerebral infarction [138], T2DM [85,139,140], gestational diabetes mellitus [10]. |
hsa-miR-133a-3p | 18q11.2 [141] 20q13.33 | Heart failure [142], myocardial fibrosis in hypertrophic cardiomyopathy [64,143], arrhythmogenesis in the hypertrophic and failing hearts [144,145], coronary artery calcification [146], thoracic aortic aneurysm [48], ascending aortic aneurysm [82], diabetes mellitus [49,50]. |
hsa-miR-143-3p | 5q33 | Intracranial aneurysms [147], coronary heart disease [148], myocardial infarction [149], myocardial hypertrophy [150], dilated cardiomyopathy [151], pulmonary arterial hypertension [152], acute ischemic stroke [127], ascending aortic aneurysm [82]. |
hsa-miR-145-5p | 5q33 | Hypertension [153,154], dilated cardiomyopathy [155], myocardial infarction [156,157], stroke [157], acute cerebral ischemic/reperfusion [158], T2DM [58,159], T1DM [85], diabetic retinopathy [160], gestational diabetes mellitus [161]. |
hsa-miR-146a-5p | 5q33.3 [162,163] | Angiogenesis [164], hypoxia, ischemia/reperfusion-induced cardiac injury [165], myocardial infarction [53], coronary atherosclerosis, coronary heart disease in patients with subclinical hypothyroidism [166], thoracic aortic aneurysm [48], acute ischemic stroke, acute cerebral ischemia [167], T2DM [58,85], T1DM [108], diabetic nephropathy [90]. |
hsa-miR-155-5p | 21q21.3 | Thoracic aortic aneurysm [48], type 1 diabetes [125], gestational diabetes mellitus [20], adolescent obesity [168], diet-induced obesity and obesity resistance [168], atherosclerosis [170], hyperlipidemia—associated endotoxemia [171], coronary plaque rupture [172], children with cyanotic heart disease [173], chronic kidney disease and nocturnal hypertension [174], atrial fibrillation [175]. |
hsa-miR-181a-5p | 1q32.1 [176] 9q33.3 | Regulation of hypertension-related genes [65], atherosclerosis [176], metabolic syndrome, coronary artery disease [177], non-alcoholic fatty liver disease [178], ischaemic stroke, transient ischaemic attack, acute myocardial infarction [179,180], obesity and insulin resistance [95,176,177], T1DM [85,181], T2DM [176,180]. |
hsa-miR-195-5p | 17p13.1 [182] | Cardiac hypertrophy, heart failure [183,184], abdominal aortic aneurysms [185], aortic stenosis [186], T2DM [159], gestational diabetes mellitus [18]. |
hsa-miR-199a-5p | 1q24.3 19p13.2 | T1DM, T2DM, gestational diabetes mellitus [187], diabetic retinopathy [188], cerebral ischemic injury [189], heart failure [190], hypertension [191,192], congenital heart disease [193], pulmonary artery hypertension [194], unstable angina [195], hypoxia in myocardium [193], acute kidney injury [196]. |
hsa-miR-210-3p | 11p15.5 | Cardiac hypertrophy [197], acute kidney injury [198], myocardial infarction [199], atherosclerosis [200]. |
hsa-miR-221-3p | Xp11.3 | Asymptomatic carotid stenosis [96], cardiac amyloidosis [201], heart failure [202], atherosclerosis [203,204], aortic stenosis [205], acute myocardial infarction [206], acute ischemic stroke [207], focal cerebral ischemia [208], pulmonary artery hypertension [209], obesity [210]. |
hsa-miR-342-3p | 14q32.2 | Cardiac amyloidosis [201], obesity [211], T1DM [85,187,212], T2DM [187,213,214], gestational diabetes mellitus [187], endothelial dysfunction [215]. |
hsa-miR-499a-5p | 20q11.22 | Myocardial infarction [53,216], hypoxia [217], cardiac regeneration [218], vascular endothelial dysfunction [51]. |
hsa-miR-574-3p | 4p14 | Myocardial infarction [219], coronary artery disease [136], cardiac amyloidosis [201], stroke [220], T2DM [140,221]. |
Normal Pregnancies Normal Clinical Findings (n = 48) | Normal Pregnancies Abnormal Clinical Findings (n = 37) | Gestational Diabetes Mellitus (GDM) Normal Clinical Findings (n = 61) | GDM Abnormal Clinical Findings (n= 57) | p-Value1 | p-Value2 | p-Value3 | |
---|---|---|---|---|---|---|---|
Children at follow-up | |||||||
Age (years) | 5 (3–11) | 5 (3–11) | 5 (3–10) | 5 (3–9) | 0.228 | 0.980 | 0.358 |
Height (cm) | 115.5 (98–144.5) | 118.0 (100–153) | 114.0 (99–143.5) | 113.5 (98–153) | 0.332 | 0.546 | 0.274 |
Weight (kg) | 20.8 (14–37) | 22.3 (14.7–40.8) | 19.5 (14.4–37.4) | 19.6 (15–47.1) | 0.104 | 0.604 | 0.565 |
BMI (kg/m2) | 15.41 (13.22–18.09) | 15.80 (13.3–20) | 15.20 (13.53–18.09) | 15.58 (12.97–20.08) | 0.067 | 0.976 | 0.166 |
Systolic BP (mmHg) | 98 (84–115) | 104 (89–123) | 99 (82–113) | 101 (87–125) | <0.001 | 0.864 | 0.027 |
Diastolic BP (mmHg) | 60 (38–68) | 64.0 (43–81) | 60 (47–67) | 61 (49–79) | 0.002 | 0.795 | 0.008 |
Heart rate (n/min) | 90 (67–110) | 90.0 (51–120) | 96 (64–118) | 98 (78–122) | 0.954 | 0.022 | <0.001 |
During Gestation | |||||||
Maternal age at delivery (years) | 31.5 (21–40) | 32 (25–46) | 34 (27–42) | 33 (27–45) | 0.233 | 0.009 | 0.046 |
GA at delivery (weeks) | 39.86 (37.71–41.57) | 39.86 (37.86–41.86) | 39.72 (37.43–41.28) | 39.43 (37.00–41.14) | 0.852 | 0.111 | 0.020 |
Fetal birth weight (g) | 3425 (2730–4220) | 3280 (2530–4450) | 3500 (2700-4330) | 3420 (2770–4400) | 0.989 | 0.157 | 0.252 |
Mode of delivery | 0.698 | <0.001 | 0.001 | ||||
Vaginal | 44 (91.67%) | 33 (89.19%) | 38 (62.30%) | 37 (64.91%) | |||
CS | 4 (8.33%) | 4 (10.81%) | 23 (37.70%) | 20 (35.09%) | |||
Fetal sex | 0.346 | 0.771 | 0.273 | ||||
Boy | 27 (56.25%) | 17 (45.95%) | 36 (59.02%) | 38 (66.67%) | |||
Girl | 21 (43.75%) | 20 (54.05%) | 25 (40.98%) | 19 (33.33%) | |||
Primiparity | 0.069 | 0.181 | 0.091 | ||||
Yes | 29 (60.42%) | 15 (40.54%) | 29 (47.54%) | 25 (43.86%) | |||
No | 19 (39.58%) | 22 (59.46%) | 32 (52.46%) | 32 (56.14%) | |||
Birth order of index pregnancy | 0.058 | 0.080 | 0.294 | ||||
1st | 26 (54.17%) | 11 (29.73%) | 20 (32.79%) | 22 (38.60%) | |||
2nd | 16 (33.33%) | 14 (37.84%) | 23 (37.70%) | 22 (38.60%) | |||
3rd | 4 (8.33%) | 10 (27.03%) | 10 (16.39%) | 6 (10.52%) | |||
4th+ | 2 (4.17%) | 2 (5.40%) | 8 (13.11%) | 7 (12.28%) | |||
Infertility treatment | 0.852 | 0.014 | 0.084 | ||||
Yes | 1 (2.08%) | 1 (2.70%) | 10 (16.39%) | 6 (10.53%) | |||
No | 47 (97.92%) | 36 (97.30%) | 51 (83.61%) | 51 (89.47%) | |||
Maternal BMI (kg/m2) | |||||||
Prepregnancy BMI | 21.88 (14.77–30.3) | 21.22 (17.37–28.04) | 22.02 (16.3–30.85) | 22.64 (17.53–30.49) | 1.000 | 1.000 | 0.567 |
BMI < 18.5 | 4 (8.33%) | 5 (13.51%) | 5 (8.20%) | 1 (1.75%) | - | - | - |
BMI 18.5–24.9 | 38 (79.17%) | 31 (83.78%) | 43 (70.49%) | 37 (64.91%) | |||
BMI 25.0–29.9 | 5 (10.42%) | 1 (2.70%) | 11 (18.03%) | 17 (29.82%) | |||
BMI > 30 | 1 (2.08%) | 0 (0%) | 2 (3.28%) | 2 (3.51%) | |||
BMI at admission for delivery | 26.17 (20.88–34.82) | 26.45 (20.72–33.17) | 25.97 (19.84–36.85) | 27.53 (20.18–36.73) | 1.000 | 1.000 | 1.000 |
Total gestational weight gain (GWG) (kg) | 14.5 (8–25.5) | 14.5 (8–21) | 10 (2–21) | 11 (3–26) | 1.000 | <0.001 | 0.008 |
BMI at follow-up | 23.26 (17.7–39.08) | 22.11 (18.17–29.17) | 23.82 (17.39–32.14) | 23.42 (17.39–34.37) | 0.414 | 1.000 | 1.000 |
Serum Metabolic Biochemical Parameters of Mothers During the Third Trimester of Gestation | |||||||
HbA1c | - | - | 32 (26–42) | 32.5 (26–40) | - | - | - |
Creatinine (μmol/L) | 56.0 (44.0–70.0) | 52.5 (43.0–83.0) | 56.0 (40.0–78.0) | 55.0 (36.0–83.0) | 1.000 | 1.000 | 1.000 |
Uric acid (μmol/L) | 286.5 (200.0–377.0) | 294.5 (221.0–345.0) | 298 (180.0–419.0) | 289 (157.0–471.0) | 1.000 | 1.000 | 1.000 |
Total bilirubin (μmol/L) | 4.0 (3.0–7.0) | 4.0 (0.18–12.0) | 6.0 (2.70–20.0) | 6.0 (3.0–20.0) | 1.000 | 0.497 | 0.108 |
ALT (μkat/L) | 0.22 (0.11–2.4) | 0.17 (0.07–0.36) | 0.23 (0.11–1.09) | 0.22 (0.11–0.46) | 1.000 | 1.000 | 1.000 |
AST (μkat/L) | 0.38 (0.25–2.36) | 0.47 (0.22–2.29) | 0.38 (0.22–1.46) | 0.40 (0.24–0.84) | 1.000 | 1.000 | 1.000 |
ALP (μkat/L) | 2.12 (1.86–4.66) | 2.51 (1.71–3.52) | 2.67 (1.35–6.15) | 2.36 (1.46–5.32) | 1.000 | 1.000 | 1.000 |
Cholesterol (mmol/L) | 7.50 (6.30–11.40) | 9.2 (6.90–10.5)) | 7.71 (4.47–9.5) | 6.93 (6.13–9.10) | 1.000 | 1.000 | 1.000 |
Triglyceride (mmol/L) | 3.10 (3.00–3.20) | 2.9 (2.7–3.3) | 3.05 (1.80–4.80) | 3.35 (2.50–8.90) | 1.000 | 1.000 | 1.000 |
Total protein (g/L) | 63.7 (48.7–70.8) | 64,35 (47.2–68.9) | 60.3 (37.7–70.8) | 61.6 (43.8–67.9%) | 1.000 | 1.000 | 1.000 |
Albumin (g/L) | 37.35 (28.9–40.6) | 36.9 (27.9–41.6) | 36.5 (4.40–42.1) | 36.2(26.3–40.9) | 1.000 | 1.000 | 1.000 |
Blood glucose (mmol/L) | 4.7 (4.2–5.1) | 4.5 (4.3–5.8) | 4.65 (4.1–8.0) | 4.4 (3.8–5.6) | 1.000 | 1.000 | 1.000 |
Normal Pregnancy | GDM Pregnancy | OR (95% CI) | p-Value | |
---|---|---|---|---|
Overweight/obese | 8/85 (9.41%) | 6/118 (5.08%) | 0.515 (0.172–1.545) | 0.237 |
Prehypertension/ hypertension | 15/85 (17.65%) | 19/118 (16.10%) | 0.896 (0.426–1.883) | 0.771 |
Valve problems or heart defects | 17/85 (20.0%) | 42/118 (35.59%) | 2.240 (1.167–4.300) | 0.015 |
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Hromadnikova, I.; Kotlabova, K.; Dvorakova, L.; Krofta, L.; Sirc, J. Substantially Altered Expression Profile of Diabetes/Cardiovascular/Cerebrovascular Disease Associated microRNAs in Children Descending from Pregnancy Complicated by Gestational Diabetes Mellitus—One of Several Possible Reasons for an Increased Cardiovascular Risk. Cells 2020, 9, 1557. https://doi.org/10.3390/cells9061557
Hromadnikova I, Kotlabova K, Dvorakova L, Krofta L, Sirc J. Substantially Altered Expression Profile of Diabetes/Cardiovascular/Cerebrovascular Disease Associated microRNAs in Children Descending from Pregnancy Complicated by Gestational Diabetes Mellitus—One of Several Possible Reasons for an Increased Cardiovascular Risk. Cells. 2020; 9(6):1557. https://doi.org/10.3390/cells9061557
Chicago/Turabian StyleHromadnikova, Ilona, Katerina Kotlabova, Lenka Dvorakova, Ladislav Krofta, and Jan Sirc. 2020. "Substantially Altered Expression Profile of Diabetes/Cardiovascular/Cerebrovascular Disease Associated microRNAs in Children Descending from Pregnancy Complicated by Gestational Diabetes Mellitus—One of Several Possible Reasons for an Increased Cardiovascular Risk" Cells 9, no. 6: 1557. https://doi.org/10.3390/cells9061557
APA StyleHromadnikova, I., Kotlabova, K., Dvorakova, L., Krofta, L., & Sirc, J. (2020). Substantially Altered Expression Profile of Diabetes/Cardiovascular/Cerebrovascular Disease Associated microRNAs in Children Descending from Pregnancy Complicated by Gestational Diabetes Mellitus—One of Several Possible Reasons for an Increased Cardiovascular Risk. Cells, 9(6), 1557. https://doi.org/10.3390/cells9061557