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Genetic susceptibility to high myopia in Han Chinese population

  • Yufei Li , Yong Zhang , Ping Zhang , Lei Gao , Qingyue Ma , Jin Li , Shengxia Wang , Bing Liu , Xinye Wang and Chao Meng EMAIL logo
Published/Copyright: May 17, 2022
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Open Life Sciences
From the journal Open Life Sciences Volume 17 Issue 1

Abstract

High myopia is a common ocular genetic disease in the world. The study sought to investigate the effect of the Insulin-like growth factor-1 (IGF-1) and Matrix metalloproteinase-9 (MMP-9) genes polymorphisms on high myopia in a Han population of China. This study recruited 216 unrelated Han Chinese subjects, including 103 cases with high myopia and 113 controls. Four tagging single nucleotide polymorphisms (SNPs) of IGF-1 and MMP-9 genes were genotyped using the Sequenom MassARRAY method. The chi-square test showed that the family history was significantly correlated with myopia. The SNP genotypes were all in Hardy–Weinberg equilibrium (P > 0.05). Among the four SNPs, there were statistically significant differences in the genotype and allele frequencies of rs2236416 between the groups (P = 0.024). The significant associations of rs2236416 between cases and controls also appeared after Bonferroni multiple correction (P = 0.024). Then, there were significant differences in the genotypes dominant model and codominant model of rs2236416 between groups (P = 0.007 and P = 0.004, respectively). rs5742632 showed a significant difference between the cases and the controls in the recessive model (P = 0.037). Our findings indicated that rs2236416 of MMP-9 was associated with myopia in the population. The result suggested MMP-9 gene locus may play a role in myopia.

Keywords: high myopia; single nucleotide polymorphism; IGF-1 ; MMP9 ; association study

1 Introduction

High myopia is a common genetic eye disease characterized by axis oculi elongation and pathological changes. The incidence of myopia is increasing and has become one of the major public health problems [1]. Notably, the incidence of high myopia in Chinese high school students has reached 10–20%, while among college and graduate students, the rate has reached 18 and 23%, respectively [2,3]. Myopia causes serious complications, including retinal detachment, macular degeneration, and vision loss [4]. There is no effective way to treat and prevent high myopia now. Family and twin studies have shown a high heritability of high myopia [5,6,7]. Candidate genes, including collagen genes, growth factor genes, and transcription factor genes, have been found to be physically linked with genetic markers of myopia [8]. Insulin-like growth factor-1 (IGF-1) is a pluripotent cytokine exerting its effects in virtually all cell types and plays a vital role in the nervous system [9]. IGF-1 gene also regulates the growth of eyeballs. Matrix metalloproteinase-9 (MMP-9) could remodel and degrade extracellular matrix (ECM). The genes may play an important role in the occurrence and development of high myopia [10,11]. It is shown that the potential association between IGF-1 polymorphisms and myopia has been investigated in a recent study [12]. However, the association studies of IGF-1 and MMP-9 genes were performed in a different population, and more single nucleotide polymorphisms (SNPs) on the way [13,14]. The signal for establishing the causes of myopia serves as a tool for the development of research [15].

Here we verify the hypothesis that these polymorphisms were the genetic factors that may influence myopia. Therefore, the present study will explore the association of polymorphisms with myopia and possible pathogenic factors in a Han population. A total of four SNPs in IGF-1 and MMP-9 were selected, including rs5742632, rs10860860, rs17576, and rs2236416.

2 Materials and methods

2.1 Participants

One hundred and three cases with high myopia were recruited. The subjects who met the following criteria were selected for the current study: (1) age between 17 and 23 years, (2) spherical equivalent (SE) in the eye of more than −6.00 diopter (D), (3) axial length more than or equal to 26 mm, and (4) without ocular disease and systemic diseases. One hundred and thirteen cases of normal control group had a SE less than −0.5 D, axial length less than 26 mm, and without systemic diseases. Cases and controls were both Han Population of Shandong Province.

  1. Informed consent: Informed consent has been obtained from all the 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 Shandong First Medical University.

2.2 DNA extraction

Peripheral venous blood (5 mL) of the subjects was collected, placed in EDTA blood vessels, numbered, and stored at –80°. Genomic DNA was extracted using TIANamp Genomic DNA Kit (Tiangen Biotech (Beijing) Co., Ltd), according to the instructions. The quality of the DNA was identified by agarose gel electrophoresis.

2.3 Selection and genotyping of SNPs

Based on HapMap data for Han Chinese, the taggers used the following criteria for SNP selection: pairwise tagging algorithm, r 2 > 0.8, and minor allele frequency (MAF) >0.05. The selected candidate sites, rs5742632, rs10860860, rs17576, and rs2236416, were available in GenBank.

Genotyping was performed by using the Sequenom MassARRAY platform. The primers were designed by Assay Design 3.1 software.

2.4 Statistical analysis

Genotype and allelic frequencies were calculated, and the data were tested for Hardy–Weinberg (HWE) equilibrium using SPSS 20.0 software. The differences of genotype and allele frequencies were compared among the groups by chi-square test. Logistics regression analysis was used to calculate the genotype and allele ratio (odds ratio) and 95% confidence interval ( CI). Bonferroni’s correction was applied for multiple comparisons. P < 0.05 was defined as statistical significance.

3 Results

3.1 Study participants

The study included 216 unrelated Chinese Han population subjects, including 103 cases (64 female and 39 male, age 17–20) with high myopia and 113 controls (67 female and 46 male, age 17–20). There was no significant difference in age and gender between the cases and controls (P = 0.212 and P = 0.671, respectively). The proportion of cases with family history was 55.4%. The prevalence of myopia among students whose parents were not myopic was 44.66%. The data showed an association between family history and the presence of myopia (P < 0 .001).

3.2 SNP analysis and genetic association study

The selected SNPs were successfully genotyped within HWE in both the groups (P > 0.05, Table 1). The information on the SNPs is shown in Table 1. There were significant differences in genotype distributions of rs2236416 between the two groups after Bonferroni correction (P = 0.024) (Table 1). There were significant differences between the genotypes dominant and codominant models of rs2236416 between groups (P = 0.007 and P = 0.004, respectively). rs5742632 showed a significant difference between the cases and the controls in the recessive model (P = 0.037) (Table 2).

Table 1

Genotype distributions for the SNPs in groups

SNP Location Alleles Minor alleles Genotype Case Control P-value HWE-P
rs5742632 102462696 A G GG/GA/AA 14/56/29 29/51/33 0.090 0.116
rs10860860 102387055 A T AA/AT/TT 68/27/6 73/34/5 0.777 0.153
rs17576 46011586 G A AA/AG/GG 5/48/50 7/54/52 0.877 0.123
rs2236416 46011936 A G AA/GA/GG 88/14/1 79/31/3 0.024 0.603

HWE-p, the P value of Hardy–Weinberg equilibrium.

Table 2

Genotype distributions for the 4 SNPs in high myopia and control groups

Codominant Dominant Recessive
SNP Genotype Case Control OR (95%CI) P OR (95%CI) P OR (95%CI) P
rs5742632 GG 14 29 1.140 (0.642–2.025) 0.654 0.996 (0.550–1.802) 0.989 2.096 (1.035–4.244) 0.037
GA 56 51
AA 29 33
rs10860860 AA 68 73 1.051 (0.611–1.809) 0.858 1.101 (0.623–1.945) 0.741 0.740 (0219–2.502) 0.627
AT 27 34
TT 6 5
rs17576 AA 5 7 1.127 (0.668–1.902) 0.653 1.107 (0.648–1.889) 0.710 1.294 (0.398–4.212) 0.668
AG 48 54
GG 50 52
rs2236416 AA 88 79 2.576 (1.331–4.986) 0.004 2.525 (1.280–4.980) 0.007 2.782 (0.285–27.174) 0.359
AG 14 31
GG 1 3

OR, odds ratio; CI, confidence interval.

The mean age of onset with the G allele of rs2236416 SNP (G/G or G/A genotype; 11.00 ± 0.000 years or 11.29 ± 1.773 years) was lower than those without (A/A genotype; 11.42 ± 1.910 years), which did not reach a statistical significance (P = 0.104). There were no significant differences between the age of onset and the genotype distribution of rs5742632, rs1086086,0, and rs17576 (P = 0.902, P = 0.342, and P = 0.870, respectively) (Table 3).

Table 3

Association between genotypes of 4 SNPs and age of onset in case group

SNP Genotype Age of onset SD F value P value
rs5742632 AA/GA/GG 11.48/11.29/11.36 1.844/1.826/2.240 0.104 0.902
rs10860860 AA/AT/TT 11.51/11.00/12.00 1.706/2.201/1.549 1.085 0.342
rs17576 AA/AG/GG 11.20/11.32/11.50 1.924/1.810/1.963 0.140 0.870
rs2236416 AA/GA/GG 11.42/11.29/11.00 1.910/1.773/0.000 0.053 0.948

SD standard deviation; F value for the joint hypotheses test.

4 Discussion

The study explored the association between the SNPs (rs5742632, rs10860860, rs17576, and rs2236416) of IGF-1 and MMP-9 and high myopia in a Han population. Consistent with expectations, we found a significant association between rs2236416 and high myopia. These results are, to some extent, in line with the previous research [13,15].

IGF-1 gene is located in the MYP3 locus on chromosome 12q23.2, which is similar to insulin in structure and takes part in many physiological processes, including aging, apoptosis, development, cellular growth metabolism, and protein translation [16]. It is a single-chain peptide composed of 70 amino acids which play an important role in human growth and development [17]. IGF-1 has been listed as a potential myopia-related gene in animal experiments and in-body research and is considered to play an important role in controlling eyeball growth. The associations between two SNPs of IGF-1 (rs10860860 and rs2946834) and high myopia (P < 0.05) have been indicated to be significant in a Polish population [18]. rs2162679 in IGF-1 was associated with myopia in a young Chinese population [12]. These results do not agree with our findings. The phenomenon may be due to different geographical ethnic groups. Our result was confirmed by additional analyses confirmed in Japanese patients [19]. Miyake reported rs6214 and rs5742632 were not associated with high myopia from the different statistical analysis methods [19]. Furthermore, Zidan demonstrated that rs6214 was associated with high myopia in an Egyptian population [20]. The phenotype of high myopia-causing genes may change as a result of ethnic differences. The varied genetic background of patients may also lead to different results in the association studies.

MMP-9 gene, located on chromosome 20q11.2-q13.1, is an endopeptidase that is considered as an important factor in the development of the axial length of the eye. The established study suggested that MMP-9 could remodel and degrade the extracellular matrix (ECM) [21]. It has an important effect on the growth and development process of the eye by cleaving denatured collagen and type IV collagen in the basement membrane [22]. The association studies became focused on the effects of MMP-9 on glaucoma [23]. According to clinical statistics, patients with myopia have higher intraocular pressure and are more susceptible to open-angle glaucoma. The debate about the role of myopia in the progress of glaucoma is still continuing. Schache found no association between rs17156 and high myopia in an Australian population [14]. However, our findings suggested that rs2236416 was significantly associated with high myopia in the Han Chinese population. This conclusion was confirmed in another report [24]. rs2236416 is an intron variant. Although the precise molecular mechanism observations are unclear, a possible explanation is that this variant of the MMP-9 gene may lead to the modified expression of this gene in high myopia.

Family history has an important effect on the occurrence of myopia, especially when both parents suffer from this disease [25]. Pacella investigated that the probability of children with two myopia parents falling ill to the disease was 6.42 times higher than children with one or both healthy parents [26]. Similar to the result, this study shows that cases with two or one myopia parents are more likely to develop myopia (P < 0.001) than without myopia parents.

The association between genes and the age of onset of high myopia had been found in previous research [27,28]. In the present study, question regarding the relationship between polymorphisms and the age of onset of high myopia also appeared. An unexpected answer is that no significant association was found. Large sample size is needed to give a certain level of confidence in further research. Further replication studies are needed to validate our findings.

5 Conclusion

We found the significant effect of genetic factors on high myopia and identified an association between rs2236416 and high myopia in some Han Chinese populations. The study focused on some new loci in a specific population. Interestingly, the associations between rs5742632 and high myopia have been indicated to be significant in the genotypes recessive model. This conclusion requires further research. The polymorphisms were significantly correlated to the occurrence risk of high myopia. The association of the polymorphisms with family history and the age of onset of high myopia were investigated. Larger sample size and more SNPs are needed to explore the mechanism of myopia.

Acknowledgements

We would like to thank all the subjects participating in this research.

  1. Funding information: This research was supported by National Natural Science Foundation of China (32000477), Medical Health Science and Technology Project of Shandong Provincial Health Commission (2018WS139 and 2019WS391), Shandong Provincial Natural Science Foundation (ZR2020MC061), and Innovation and Entrepreneurship Project for College Students in Shandong Province (S202010439070).

  2. Conflict of interest: 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: 2021-08-03
Revised: 2022-01-17
Accepted: 2022-02-04
Published Online: 2022-05-17

© 2022 Yufei Li et al., published by De Gruyter

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

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  103. Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
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  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
  118. Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
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  121. Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
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  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
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  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
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  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
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  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
  159. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
  162. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
https://doi.org/10.1515/biol-2022-0055
Keywords for this article
high myopia; single nucleotide polymorphism; IGF-1; MMP9; association study
Creative Commons
BY 4.0

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  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
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  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
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  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
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  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
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  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
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