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Article • Braz. J. Pharm. Sci. 60 • 2024 • https://doi.org/10.1590/s2175-97902024e24015 copy

Single nucleotide polymorphisms in apolipoprotein A-I (rs670) and B (rs693) associated with serum lipoproteins and endothelial activation in COVID-19 outpatients

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

This cross-sectional study investigated the association of SNPs rs670 (C>T) and rs693 (G>A) with parameters of lipid metabolism and endothelial activation in 167 subjects, including 86 COVID-19 outpatients and 81 healthy subjects (control group) matched for sex and age. Serum levels of total cholesterol (TC), high-density lipoprotein cholesterol (HDL-c), low-density lipoprotein cholesterol (LDL-c), non-high-density lipoprotein cholesterol (non-HDL-c), triglycerides (TG), apolipoproteins (Apo A-I and B), and vascular cell adhesion molecule-1 (VCAM-1) were determined. The SNPs were genotyped by quantitative polymerase chain reaction (qPCR). A p -value<0.05 was assumed. COVID-19 outpatients showed increases in TC (187.0±48.3 vs . 160.8±32.0 mg/dL), LDL-c (110.3±41.5 vs . 98.8±28.2 mg/dL), non-HDL-c (138.3±45.8 vs . 115.6±31.6 mg/dL), TG (139.7±80.3 vs . 84.9±35.1 mg/dL), and Apo A-I (149.5±40.0 vs . 133.3±20.9 mg/dL), along with a high frequency of hypercholesterolemia and hypertriglyceridemia. VCAM-1 levels were double those of the control (682.7±231.8 vs. 299.3±102.9 ng/mL) and a strong predictor of COVID-19 (AUC=0.946). Moreover, VCAM-1 correlated with TC (r = -0.223) and HDL-c (r = -0.225). The decrease in TG and VCAM-1 is predicted by the dominance of the T allele (rs670) and its codominance with the A (rs693) allele in COVID-19 outpatients. COVID-19 has been shown to be associated with dyslipidemias and endothelial activation, and apolipoprotein polymorphisms may influence this.

Keywords
SARS-CoV-2; Single nucleotide polymorphism; Lipid metabolism; Vascular cell adhesion molecule-1

Parameters	Control ± SD	COVID-19 ± SD	p ^a	RV	Control N = 81 (%)	COVID-19 N = 86 (%)	p ^b
TC (mg/dL)	160.8 ± 32.0	187.0 ± 48.3	< 0.001	<190 mg/dL	69 (85.2%)	48 (55.8%)	< 0.001
TC (mg/dL)	160.8 ± 32.0	187.0 ± 48.3	< 0.001	>190 mg/dL	12 (14.8%)	38 (44.2%)	< 0.001
HDL-c (mg/dL)	45.2 ± 12.6	48.8 ± 13.6	0.074	>40 mg/dL	53 (65.4%)	56 (65.1%)	0.966
HDL-c (mg/dL)	45.2 ± 12.6	48.8 ± 13.6	0.074	<40 mg/dL	28 (34.6%)	30 (34.9%)	0.966
non-HDL-c (mg/dL)	115.6 ± 31.6	138.3 ± 45.8	< 0.001	<130 mg/dL	56 (69.1%)	38 (44.2%)	0.001
non-HDL-c (mg/dL)	115.6 ± 31.6	138.3 ± 45.8	< 0.001	>130 mg/dL	25 (30.9%)	48 (55.8%)	0.001
LDL-c (mg/dL)	98.8 ± 28.2	110.3 ± 41.5	0.036	<130 mg/dL	70 (86.4%)	66 (76.7%)	0.108
LDL-c (mg/dL)	98.8 ± 28.2	110.3 ± 41.5	0.036	>130 mg/dL	11 (13.6%)	20 (23.3%)	0.108
TG (mg/dL)	84.9 ± 35.1	139.7 ± 80.3	< 0.001	<175 mg/dL	77 (95.1%)	62 (72.1%)	< 0.001
TG (mg/dL)	84.9 ± 35.1	139.7 ± 80.3	< 0.001	>175 mg/dL	4 (4.9%)	24 (27.9%)	< 0.001
Apo A-I (mg/dL)	133.3 ± 20.9	149.5 ± 40.0	0.001
Apo B (mg/dL)	85.4 ± 18.9	80.3 ± 21.7	0.107
VCAM-1 (ng/mL)	299.3 ± 102.9	682.7 ± 231.8	< 0.001

Parameters	Control		COVID-19
Parameters	r	p	r	p
TC (mg/dL)	-0.083	0.463	-0.223	0.039
HDL-c (mg/dL)	-0.108	0.337	-0.225	0.037
non-HDL-c (mg/dL)	-0.040	0.720	-0.169	0.121
LDL-c (mg/dL)	-0.047	0.678	-0.206	0.057
TG (mg/dL)	-0.012	0.914	0.052	0.636
Apo A-I (mg/dL)	-0.166	0.138	0.001	0.994
Apo B (mg/dL)	-0.101	0.370	-0.004	0.970

SNP	Alleles and Genotypes	Control N = 81 (%)	COVID-19 N = 86 (%)	p
rs670	C	75.93%	80.81%
	T	24.07%	19.19%
	CC	48 (59.3%)	54 (62.8%)	0.148
	CT	27 (33.3%)	31 (36.0%)
	TT	6 (7.4%)	1 (1.2%)
rs693	G	59.26%	61.05%
	A	40.74%	38.95%
	GG	28 (34.6%)	31 (36.0%)	0.954
	GA	40 (49.4%)	43 (50.0%)
	AA	13 (16.0%)	12 (14.0%)

SNP	Classifications	Genotypes	Control N = 81 (%)	COVID-19 N = 86 (%)
rs670	Without T allele	CC	48 (59.3%)	54 (62.8%)
rs670	With T allele	CT/TT	33 (40.7%)	32 (37.2%)
rs693	Without A allele	GG	28 (34.6%)	31 (36.0%)
rs693	With A allele	GA/AA	53 (65.4%)	55 (64.0%)
rs670 and rs693	Without T and A alleles	CC and GG	13 (16.0%)	17 (19.8%)
rs670 and rs693	With T and A alleles	CT/TT and GA/AA	18 (22.2%)	18 (20.9%)

Parameters	Control ± SD			COVID-19 ± SD
Parameters	Without T allele N = 48	With T allele N = 33	p	Without T allele N = 54	With T allele N = 32	p
TC (mg/dL)	160.5 ± 35.3	161.1 ± 26.9	0.937	187.6 ± 52.0	186.1 ± 42.1	0.887
HDL-c (mg/dL)	44.4 ± 12.8	46.3 ± 12.3	0.499	47.0 ± 11.0	51.9 ± 16.8	0.146
non-HDL-c (mg/dL)	116.2 ± 34.0	114.8 ± 28.3	0.843	140.6 ± 50.2	134.3 ± 37.4	0.504
LDL-c (mg/dL)	99.3 ± 30.6	98.0 ± 24.9	0.825	109.7 ± 44.2	111.5 ± 37.1	0.843
TG (mg/dL)	85.4 ± 36.3	84.1 ± 33.8	0.865	155.0 ± 86.8	114.0 ± 61.1	0.012
Apo A-I (mg/dL)	131.6 ± 22.2	135.8 ± 18.9	0.357	146.4 ± 36.1	154.8 ± 45.9	0.376
Apo B (mg/dL)	86.2 ± 19.8	84.2 ± 17.7	0.636	82.8 ± 22.5	76.1 ± 19.9	0.160
VCAM-1 (ng/mL)	281.2 ± 92.2	325.5 ± 113.1	0.068	719.6 ± 238.7	620.5 ± 208.6	0.048

Parameters	Control ± SD			COVID-19 ± SD
Parameters	Without A allele N = 28	With A allele N = 53	p	Without A allele N = 31	Without A allele N = 55	p
TC (mg/dL)	157.3 ± 27.4	162.6 ± 34.2	0.454	183.2 ± 49.5	189.2 ± 48.0	0.589
HDL-c (mg/dL)	44.8 ± 13.2	45.3 ± 12.4	0.864	46.5 ± 13.8	50.1 ± 13.4	0.237
non-HDL-c (mg/dL)	112.5 ± 26.9	117.3 ± 34.0	0.494	136.8 ± 46.2	139.1 ± 45.9	0.824
LDL-c (mg/dL)	96.6 ± 24.3	99.9 ± 30.2	0.598	107.8 ± 42.4	111.8 ± 41.3	0.674
TG (mg/dL)	79.4 ± 32.5	87.8 ± 36.3	0.292	144.9 ± 74.5	136.8 ± 84.0	0.644
Apo A-I (mg/dL)	130.7 ± 20.3	134.7 ± 21.2	0.404	148.2 ± 38.9	150.2 ± 40.9	0.821
Apo B (mg/dL)	82.9 ± 17.9	86.7 ± 19.4	0.386	82.4 ± 23.6	79.1 ± 20.6	0.513
VCAM-1 (ng/mL)	309.3 ± 105.9	294.0 ± 101.9	0.533	724.6 ± 241.0	659.1 ± 225.2	0.220

Parameters	Control ± SD			COVID-19 ± SD
Parameters	Without T and A alleles N = 13	With T and A alleles N = 18	p	Without T and A alleles N = 17	With T and A alleles N = 18	p
TC (mg/dL)	156.5 ± 25.5	163.6 ± 24.7	0.442	191.4 ± 60.6	196.1 ± 47.8	0.801
HDL-c (mg/dL)	41.5 ± 11.3	45.1 ± 10.6	0.371	41.6 ± 10.0	51.5 ± 18.1	0.053
non-HDL-c (mg/dL)	115.0 ± 24.1	118.5 ± 27.2	0.709	149.8 ± 57.6	144.6 ± 45.0	0.768
LDL-c (mg/dL)	99.7 ± 22.1	101.3 ± 23.6	0.849	114.8 ± 53.4	120.9 ± 43.9	0.715
TG (mg/dL)	76.4 ± 22.2	85.8 ± 28.8	0.311	175.3 ± 75.1	118.7 ± 65.6	0.024
Apo A-I (mg/dL)	129.0 ± 23.4	139.0 ± 19.6	0.225	142.0 ± 39.2	154.1 ± 52.0	0.441
Apo B (mg/dL)	81.9 ± 16.5	84.5 ± 16.6	0.666	90.1 ± 27.4	78.5 ± 23.7	0.191
VCAM-1 (ng/mL)	279.2 ± 77.5	317.3 ± 108.0	0.263	756.2 ± 247.5	569.3 ± 174.3	0.016

Predicted variables	Models	COVID-19
Predicted variables	Models	β	SE	β _standardised	p
TG	T allele	-42.57	17.65	-0.258	0.018
	A allele	-13.43	17.77	-0.081	0.452
	T and A alleles	-56.63	23.81	-0.383	0.023
VCAM-1	T allele	-108.78	50.86	-0.228	0.035
	A allele	-79.06	51.20	-0.165	0.126
	T and A alleles	-186.86	72.01	-0.412	0.014

Universidade de São Paulo, Faculdade de Ciências Farmacêuticas Av. Prof. Lineu Prestes, n. 580, 05508-000 S. Paulo/SP Brasil, Tel.: (55 11) 3091-3824 - São Paulo - SP - Brazil
E-mail: bjps@usp.br

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