GENETIC TESTING AND MOLECULAR BIOMARKERS Volume 18, Number 12, 2014 ª Mary Ann Liebert, Inc. Pp. 826–831 DOI: 10.1089/gtmb.2014.0222

Genetic Polymorphism of Matrix Metalloproteinase-1 and Coronary Artery Disease Susceptibility: A Case–Control Study in a Han Chinese Population Cui Qintao,1 Li Yan,2 Duan Changhong,3 Guo Xiaoliang,1 and Liu Xiaochen1

Coronary artery disease (CAD) receives intensive research due to its high incidence and severe impact on the quality of life. One member of the matrix metalloproteinases (MMPs), MMP-1, has been reported to be associated with CAD. To identify the markers contributing to the genetic susceptibility to CAD, nine singlenucleotide polymorphisms (rs1799750, rs498186, rs475007, rs514921, rs494379, rs996999, rs2071232, rs1938901, and rs2239008) throughout the MMP-1 gene were genotyped using MALDI-TOF within the MassARRAY system, and the allele and genotype distributions were compared between 438 healthy controls and 411 patients with CAD from a Chinese Han population. The analysis revealed a weak association between the rs1799750 (in the promoter region) genotype distribution and CAD ( p = 0.022). An increased risk of CAD was significantly associated with the 2G allele of rs1799750 ( p = 0.005, odds ratio = 1.329, 95% confidence interval = 1.090– 1.620, after Bonferroni corrections). Strong linkage disequilibrium was observed in three blocks (D¢ > 0.9). Significantly more C-2G (rs498186–rs1799750) haplotypes ( p = 0.001 after Bonferroni corrections) were found in CAD subjects. These findings point to a role for the polymorphism in the MMP-1 promoter in CAD among a Han Chinese population and may be informative for future genetic or biological studies on CAD.

Introduction

C

oronary artery disease (CAD) is a complex, multifactorial, chronic, and highly prevalent vascular disorder (Ross, 1999). Twin and family studies have suggested that CAD is closely associated with the interaction of genetic factors and environmental modulators (Wilson et al., 1998; Evans et al., 2003; Hauser et al., 2004). The studies have also indicated that genetic predispositions provide the basic conditions for CAD (Scheuner, 2001; Funke, 2003). Polymorphisms in one member of the matrix metalloproteinases (MMPs), MMP-1, have been reported to be associated with CAD (Kato et al., 2005; Drzewoski et al., 2008). The pathogenesis of CAD is described as follows. First, atherosclerotic plaques form and change with the gradual progression of atherosclerosis and could develop to an unstable plaque that is prone to rupture. Interstitial collagen is a major component of atherosclerotic plaques (Mayne, 1986; Rekhter et al., 1993). The synthesis of collagen is generally upregulated in plaques (Rekhter et al., 1993). The regulation of the expression of the extracellular matrix (ECM) is the predominant cause of vascular remodeling during the pathogenesis of atherosclerosis (Falk et al., 1995). MMPs are implicated in the degradation of the ECM of the coronary

plaque, including thinning of the fibrous cap (Libby, 2001). One member of the MMPs, MMP-1, the major human interstitial collagenase, is produced by macrophages, smooth muscle cells, and endothelial cells in atherosclerotic plaques, especially in vulnerable plaques (Galis et al., 1994; Sukhova et al., 1999). Pathological studies have shown that the expression of MMP-1 is localized to the fibrous cap and shoulder regions of atherosclerotic plaques and the two regions are prone to expand, rupture, and hemorrhage (Nikkari et al., 1995). Previous studies suggest that high MMP-1 levels in patients with CAD may predict plaque instability in coronary arteries (Kato et al., 2005). Therefore, MMP-1 may serve as a biomarker of atherosclerosis (Wu et al., 2008), and the MMP-1 level in patients with CAD may reflect plaque instability in coronary arteries and other vascular beds. MMP-1 is a candidate gene, which has been reported to modify the risk of atherosclerosis and CAD in humans, and several polymorphisms of the MMP-1 gene have been examined in several case–control studies (Rutter et al., 1998; Ye et al., 2003; Pearce et al., 2005; Armstrong et al., 2007; Han et al., 2008; Dey et al., 2014). One polymorphism, rs1799750, which is defined as the insertion of a G at position - 1607 bp (rs1799750) in the promoter of the MMP-1 gene, creates a binding site for ETS-1, a transcription factor (Rutter

Departments of 1Cardiothoracic Surgery, 2General Surgery, and 3Outpatient, First Affiliated Hospital of Xinxiang Medical University, Weihui, People’s Republic of China.

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SNPS OF MMP-1 AND CAD SUSCEPTIBILITY

et al., 1998). The MMP-1 rs1799750 variant has been reported to be associated with several cancers (Rutter et al., 1998; Dey et al., 2014) and CAD (Ye et al., 2003). It has been reported that the rs1144393 ( - 519 A/G) and rs514921 ( - 340 T/C) polymorphisms may have an allele-specific effect on the transcription of MMP-1 (Pearce et al., 2005). The haplotypes of the rs1144393 and rs514921 polymorphisms have been reported to be associated with myocardial infarction (MI) in the British, Swedish, and Chinese populations (Pearce et al., 2005; Han et al., 2008), and the rs1144393 polymorphism is also reported to be associated with hypertension, which is a common risk factor for CAD (Armstrong et al., 2007). Moreover, haplotypes of these polymorphisms could increase the promoter activity and gene expression of MMP-1 (Pearce et al., 2005), suggesting a relationship between these variants and the unregulated expression of MMP-1 in atherosclerotic plaques. Although the unregulated expression of MMP-1 has been reported to be associated with the poor prognosis of patients with CAD (Ye et al., 2003), the role of the MMP-1 promoter single-nucleotide polymorphisms (SNPs) and their haplotypes in the development of CAD remains to be elucidated in humans. In most previous studies, only a few loci were analyzed and thus inconsistent findings were obtained. Furthermore, several important SNPs, such as rs498186 (promoter), rs475007 (promoter), rs494379 (promoter), and rs2239008 (3¢-untranslated region, 3¢-UTR), had not been studied, resulting in an ineffective capture of true causative SNPs in MMP-1 due to the weak linkage disequilibrium between them (Clarke et al., 2011). In the present study, to verify the putative association between the MMP-1 SNPs and CAD, we investigated the association between nine SNPs (rs1799750, rs498186, rs475007, rs514921, rs494379, rs996999, rs2071232, rs1938901, and rs2239008) of the MMP-1 gene and the risk of CAD in a Chinese Han population. Subjects and Methods Subjects

A hospital-based case–control study was conducted in 411 patients with CAD (mean – SD age: 60.2 – 5.6 years) and 438 healthy controls (mean – SD age: 61.3 – 5.5 years). The patients underwent the following examinations: coronary angiography, electrocardiogram (ECG), blood tests, and/or stress tests. The process of interview/response was also performed on the patients. Inclusion criteria were as follows: (1) At least one diseased vessel ( ‡ 25% stenosis) in the coronary angiograph. (2) Patients with stable angina pectoris showing a long-term and stable effort angina, which had lasted for at least 3 months, and a positive stress test. (3) Patients with unstable angina pectoris showing either angina with a progressive crescendo pattern or angina, which occurred at rest without a recent MI. (4) The ECG of the patients showed transient ST-T segment depression and T-wave inversion, without significant elevated levels of cardiac enzymes. (5) Patients with acute MI showed typical angina associated with ST-segment elevations in ECG, and the frequency of occurrence of elevated levels of creatine kinase and troponin-I in serum in these patients was more than three. Exclusion criteria were as follows: noncardiac diseases, including acute or chronic infections, malignancies, autoimmune diseases, hyperthyroidism, and medication with immunosuppressive

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agents. The healthy control group consisted of 438 unrelated healthy subjects who underwent health examinations in the Medical Examination Center of our Hospital. The selection criteria included no individual history of CAD, frequency matching to cases on sex and age, and individuals were unrelated ethnic Han Chinese. The study was approved by Human Research and Ethics Committee of the First Affiliated Hospital of Xinxiang Medical University (Xinxiang, China) and conducted according to all current ethical guidelines. SNP Selection

The genomic sequence of the MMP-1 gene spans 8 kb. In most previous studies, only one or two SNPs were analyzed and this analysis is insufficient to cover the gene locus. A total of nine SNPs throughout the MMP-1 gene and the 5¢ and 3¢-flanking regions were selected for the present study. SNPs rs1799750, rs498186, rs475007, rs514921, and rs494379 are located in the promoter, rs996999 in intron 4, rs2071232 in intron 6, rs1938901 in intron 8, and rs2239008 in the 3¢-UTR. Marker selection was based on previous studies (Ye et al., 2003; Pearce et al., 2005; Armstrong et al., 2007; Han et al., 2008), and preliminary analysis was performed using the HapMap data. We examined tagSNPs in the Haploview software v4.2 using the Chinese Han in Beijing (CHB) population and a minor allele frequency cutoff ‡ 5% (the HapMap Data Release 27). The LD pattern of this gene was determined in the Chinese population using the preliminary data from the HapMap. These SNPs were further analyzed in an association study. Genotyping

Genomic DNA was extracted from blood leukocytes using the TIANamp Blood Genomic DNA Purification Kit (Tiangen Biotech, Beijing, China) according to the manufacturer’s protocol. The selected SNPs were genotyped in the patients and controls by using MALDI-TOF within the MassARRAY system (Sequenom, Inc., San Diego, CA). Primers for polymerase chain reaction and single base extension were designed using the Assay Designer software package (Sequenom, Inc.). The completed genotyping reactions were spotted onto a 384 well spectroCHIP (Sequenom) using the MassARRAY Nanodispenser (Sequenom) and determined by the matrix-assisted, laser desorptionionization time-of-flight mass spectrometer. The resulting spectra were processed with the Typer Analyzer software (Sequenom) and genotype data were generated for the samples. According to the results of genotyping, we excluded rs17662626 from the study, which showed no polymorphic variation in our samples and was consistent with the HapMap HCB data. The final genotype call rate of each SNP was > 98% and the overall genotyping call rate was 98.6%, ensuring the reliability of further statistical analysis Statistical analysis

We calculated the statistical power as previously described (Dupont and Plummer, 1998). Differences between the patients and controls in the frequency of the alleles, genotypes, and haplotypes were evaluated by chi-square tests or Fisher’s exact test. Unconditional logistic regression was used to calculate the odds ratio (OR) and 95% confidence interval (CI) in independent association between each locus and the

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presence of CAD, which were used to evaluate the strength of association between each locus and the presence of disease. Generalized linear regression was used to evaluate the interaction effects between gene and gender or age. Gender and age of subjects were treated as covariants in binary logistic regression. Haplotype blocks were defined according to the criteria developed by Gabriel et al. (2002). Pair-wise LD statistics (D¢ and r2) and haplotype frequency were calculated, and haplotype blocks were constructed using the Haploview 4.0 (Barrett et al., 2005). To ensure that the LD blocks most closely reflect the population level LD patterns, definition of the blocks were based on the control samples alone. The significance of any haplotypic association was evaluated using a likelihood ratio test, followed by permutation testing that compared estimated haplotype frequencies in cases and controls (Zhao et al., 2000; Curtis et al., 2006). The Bonferroni correction was used to adjust the test level when multiple comparisons were conducted, and the p-value was divided by the total number of loci or haplotypes. Results

The results showed that more than 99% of the samples were genotyped successfully for each SNP, and the replicate experiment for the randomly selected 96 samples (11.3%) acquired completely consistent genotype data with the original analysis. No significant deviation from the Hardy– Weinberg equilibrium was found for any of the SNPs in the

FIG. 1. The LD plot of the 9 SNPs in the MMP-1 gene. Values in squares are the pair-wise calculation of r2 (left) or D¢ (right). Black squares indicate r2 = 1 (i.e., perfect LD between a pair of SNPs). Empty squares indicate D¢ = 1 (i.e., complete LD between a pair of SNPs). LD, linkage disequilibrium; MMP, matrix metalloproteinase; SNPs, single-nucleotide polymorphisms.

QINTAO ET AL.

controls and patients with CAD. The analysis of strong LD in the patients with CAD and the healthy controls revealed that the two SNPs (rs2239008 and rs1938901), two SNPs (rs2071232 and rs996999), and two SNPs (rs498186 and rs1799750) were located in haplotype block 1, block 2, and block 3, respectively (D¢ > 0.9, Fig. 1). The genotype distribution, allelic frequencies, and haplotypes in the patients with CAD and the healthy controls are shown in Tables 1–4. After adjusting for multiple testing, threshold significance p-value was set at 0.006 in Table 1. The analysis revealed a weak association between the rs1799750 (promoter region) genotype distribution and CAD ( p = 0.022). An increased risk of CAD was significantly associated with the 2G allele of rs1799750 ( p = 0.005, OR = 1.329, 95% CI = 1.090–1.620, after Bonferroni corrections). We performed an association analysis to determine whether the haplotypes were associated with the risk of CAD. Compared with the healthy controls, the C-2G haplotype (rs498186–rs1799750) occurred significantly more frequently ( p = 0.001, OR = 2.151, 95% CI = 1.384–3.343, after Bonferroni corrections) in block 3 in the patients with CAD. Discussion

The relationship between the MMP-1 gene and the susceptibility to CAD remains controversial. It has been reported that ApoE knockout mice expressing human MMP-1 had less advanced atherosclerotic lesions compared with their

SNPS OF MMP-1 AND CAD SUSCEPTIBILITY

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Table 1. Genotypic and Allelic Frequencies of MMP-1 Polymorphisms in the Controls and Patients with Coronary Artery Disease Controls (n = 438) Variable rs1799750 2G/2G 2G/1G 1G/1G Per 1G allele rs498186 A/A A/C C/C Per C allele rs475007 A/A A/T T/T Per T allele rs514921 A/A A/G G/G Per G allele rs494379 A/A A/G G/G Per G allele rs996999 C/C C/T T/T Per T allele rs2071232 C/C C/T T/T Per T allele rs1938901 C/C C/T T/T Per T allele rs2239008 A/A A/G G/G Per G allele

ID

Position

MAF

CAD (n = 411)

No.

%

No.

%

162 200 76 352

37.0 45.7 17.4 40.2

184 178 49 276

44.8 43.3 11.9 33.6

124 214 100 414

28.3 48.9 22.8 47.3

104 214 93 400

25.3 52.1 22.6 48.7

120 200 118 436

27.4 45.7 26.9 49.8

108 207 96 399

26.3 50.4 23.4 48.5

138 228 70 368

31.7 52.3 16.1 42.0

128 194 87 362

31.3 47.4 21.3 44.0

184 204 50 304

42.0 46.6 11.4 34.7

175 192 44 280

42.6 46.7 10.7 34.1

184 200 54 308

42.0 45.7 12.3 35.2

179 184 48 280

43.6 44.8 11.7 34.1

122 200 116 432

27.9 45.7 26.5 49.3

111 194 106 406

27.0 47.2 25.8 49.4

130 220 88 396

63.2 18.5 18.3 45.2

130 188 93 376

31.6 45.7 22.6 45.7

114 236 88 412

26.0 53.9 20.1 47.0

124 194 93 380

30.2 47.2 22.6 46.2

102670496 Promoter 0.402

102669645 Promoter 0.473

102669312 Promoter 0.498

102669230 Promoter 0.422

102669210 Promoter 0.347

102667063 Intron 4

102665669 Intron 6

102661665 Intron 8

102661080 3¢-UTR

0.352

0.493

0.447

0.470

p-Valuea 0.022 0.021 0.484 0.026 0.005 0.562 0.361 0.315 0.948 0.563 0.340 0.718 0.171 0.228 0.612 0.129 0.916 0.157 0.051 0.398 0.945 0.859 0.978 0.746 0.781 0.891 0.649 0.787 0.778 0.635 0.904 0.779 0.655 0.823 0.975 0.408 0.538 2.569 0.367 0.824 0.149 0.180 0.051 0.361 0.359

OR, 95% CI 0.724, 1.102, 1.555, 0.752,

0.550–0.953 0.840–1.446 1.053–2.297 0.617–0.917

1.152, 0.871, 1.011, 1.058,

0.850–1.562 0.665–1.140 0.733–1.394 0.874–1.280

1.058, 0.828, 1.211, 0.952,

0.780–1.434 0.632–1.085 0.887–1.654 0.787–1.152

1.016, 1.215, 0.709, 1.086,

0.760–1.357 0.928–1.593 0.501–1.002 0.896–1.317

0.976, 0.996, 1.074, 0.972,

0.742–1.282 0.759–1.307 0.698–1.651 0.796–1.188

0.939, 1.038, 1.062, 0.953,

0.715–1.232 0.792–1.361 0.701–1.609 0.180–1.164

1.044, 0.940, 1.036, 1.003,

0.772–1.413 0.718–1.232 0.762–1.407 0.829–1.213

1.096, 0.109, 1.163, 1.022,

0.819–1.468 0.803–0.614 0.837–1.616 0.844–1.237

0.814, 1.130, 0.858, 0.914,

0.603–1.099 0.999–1.717 0.617–1.192 0.154–1.108

Alpha value is adjusted by Bonferroni correction and statistically significant results ( p < 0.006). a p-Value was calculated by 2 · 3 and 2 · 2 chi-squared tests based on codominant, dominant for the rare allele, heterosis and recessive for the rare allele models of inheritance. CAD, coronary artery disease; CI, confidence interval; MAF, minor allele frequency in controls; MMP, matrix metalloproteinase; OR, odds ratio.

littermates that do not express MMP-1 (Lemaitre et al., 2001). This suggests that MMP-1 may play a dual role in CAD: on one hand, it could remodel the atherosclerotic lesions, but on the other hand, enhanced expression of MMP-1 expression could cause rupture of the plaque (Newby, 2005). In humans, the expression of MMP-1 is increased in carotid

atherosclerosis and its increased expression contributes toward plaque instability (Nikkari et al., 1995). Our results provide direct evidence that the SNPs of MMP-1 are linked to CAD in humans and extend the list of variants that may affect the development of CAD (Drzewoski et al., 2008; JguirimSouissi et al., 2011; Li et al., 2012).

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Table 2. MMP-1 Haplotype in Block 1 Frequencies and the Results of Their Associations with Risk of Coronary Artery Disease Haplotypea ID HAP1 HAP2

Table 4. MMP-1 Haplotype in Block 3 Frequencies and the Results of Their Associations with Risk of Coronary Artery Disease Haplotype

Frequency (%)

rs2239008 rs1938901 Cases Controls p-Valueb A G

C T

0.533 0.450

0.527 0.445

0.884 0.886

a

Haplotypes with frequency < 0.05 were excluded. Based on the comparison of frequency distribution of all haplotypes for the combination of SNPs. SNPs, single-nucleotide polymorphisms. b

MMP-1 overexpression may be attributed to two factors. One is the juxtaposition of transcription factor binding sites and the other is the cooperativity among the factors that bind to these sites within the promoter region of the MMP-1 gene (Rutter et al., 1998). A guanine insertion/deletion polymorphism (1G/2G polymorphism) at position–1607 is in the promoter region of the MMP-1 gene, which generates the sequence 5¢-GGA-3¢, which has a 2G allele. The transcriptional activity of endogenous MMP-1 could be increased by the presence of a 2G polymorphism, since the guanine insertion creates a binding site for a member of the Ets transcription factor family (Rutter et al., 1998). In this study, the analysis revealed a weak association between the rs1799750 genotype distribution and CAD. The frequency of the 2G allele was significantly higher in the CAD patients than in the healthy controls. It is suggested that the GG allele of rs1799750, related to an increase in MMP-1 expression, may contribute to the progression of CAD by increasing the degradation of interstitial collagen and thinning the fibrous cap leading to plaque disruption or erosion. The meta-analysis suggested that genetic polymorphism of MMP-1 rs1799750 had small to moderate effects on the incidence of coronary disease. In addition, the 2G allele plays a more significant role in Asian populations (Li et al., 2012). Numerous studies have indicated that rs1799750 polymorphisms in the promoter region of MMP-1 genes might be associated with acute coronary syndrome, CAD progression in diabetic patients, MI, and progression of vascular complications in diabetic patients ( Jormsjo et al., 2000; Maeda et al., 2001; Liu et al., 2003; Liu et al., 2006; Horne et al., 2007; Drzewoski et al., 2008). Collectively, our results confirmed the strong association between MMP-1 rs1799750

ID HAP1 HAP2 HAP2

Frequency (%)

rs498186 rs1799750 Cases Controls p-Valuea A C C

C T 2G

0.510 0.331 0.154

0.520 0.394 0.078

0.780 0.235 0.001

a Based on the comparison of frequency distribution of all haplotypes for the combination of SNPs.

and CAD, suggesting that MMP-1 represents a strong genetic risk factor for CAD. In the MMP-1 gene, the effects of the MMP-1 SNPs and predicted haplotypes of the LD block on the genetic susceptibility to CAD were further investigated. Strikingly, a C-2G haplotype formed by the two SNPs (block 3, rs498186– rs1799750) was found to be associated with increased risk of developing CAD (D¢ > 0.9 in both cases and controls). These results indicated that the patients with C-2G haplotypes of the MMP-1 gene were more prone to CAD. To some extent, this finding further supports a role of MMP-1 polymorphisms in CAD, while ethnic group differences may exist. A systematic screening of the functional SNPs in the promoter region, 5¢- and 3¢-UTR, exons of the MMP-1 gene, and the homogeneity of the study subjects representing the Chinese Han are the main strengths of this study. Furthermore, the deficient study that investigates the association of the protein level of MMP-1 with CAD is a potential limitation of this study. In conclusion, our study suggests a potential role of the MMP-1 gene rs1799750 and the related haplotype (rs498186–rs1799750) in the genetic susceptibility to CAD. Further studies will be required to determine the MMP-1 haplotypes and their frequencies in other populations. Acknowledgments

Thanks to all our colleagues working in the Department of Cardiothoracic Surgery, First Affiliated Hospital of Xinxiang Medical University. Author Disclosure Statement

No competing financial interests exist. References

Table 3. MMP-1 Haplotype in Block 2 Frequencies and the Results of Their Associations with Risk of Coronary Artery Disease Haplotype ID HAP1 HAP2 HAP2

Frequency (%)

rs2071232 rs996999 Cases Controls p-Valuea C T T

C T C

0.503 0.338 0.156

0.507 0.352 0.142

0.926 0.682 0.562

a Based on the comparison of frequency distribution of all haplotypes for the combination of SNPs.

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Address correspondence to: Cui Qintao, MD Department of Cardiothoracic Surgery First Affiliated Hospital of Xinxiang Medical University Jiankang Road Weihui 453100 Henan Province People’s Republic of China E-mail: [email protected]

Genetic polymorphism of matrix metalloproteinase-1 and coronary artery disease susceptibility: a case-control study in a Han Chinese population.

Coronary artery disease (CAD) receives intensive research due to its high incidence and severe impact on the quality of life. One member of the matrix...
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