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Codon Usage Bias and Cluster Analysis of the MMP-2 and MMP-9 Genes in Seven Mammals

Published online by Cambridge University Press:  01 January 2024

Tanliang Ouyang Open the ORCID record for Tanliang Ouyang [Opens in a new window] ,
Jincheng Zhong Open the ORCID record for Jincheng Zhong [Opens in a new window] ,
Zhixin Chai Open the ORCID record for Zhixin Chai [Opens in a new window] ,
Jiabo Wang Open the ORCID record for Jiabo Wang [Opens in a new window] ,
Ming Zhang Open the ORCID record for Ming Zhang [Opens in a new window] ,
Zhijuan Wu Open the ORCID record for Zhijuan Wu [Opens in a new window] ,
Jinwei Xin Open the ORCID record for Jinwei Xin [Opens in a new window]  and
Aldesia Provenzano
Tanliang Ouyang
Affiliation:
Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Southwest Minzu University, Chengdu 610225, China
Jincheng Zhong
Affiliation:
Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Southwest Minzu University, Chengdu 610225, China
Zhixin Chai
Affiliation:
Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Southwest Minzu University, Chengdu 610225, China
Jiabo Wang
Affiliation:
Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Southwest Minzu University, Chengdu 610225, China
Ming Zhang
Affiliation:
Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Southwest Minzu University, Chengdu 610225, China
Zhijuan Wu*
Affiliation:
Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Southwest Minzu University, Chengdu 610225, China State Key Laboratory of Hulless Barley and Yak Germplasm Resources and Genetic Improvement, Lhasa 850000, China
Jinwei Xin*
Affiliation:
State Key Laboratory of Hulless Barley and Yak Germplasm Resources and Genetic Improvement, Lhasa 850000, China
*
Correspondence should be addressed to Zhijuan Wu; wzjdream2005@163.com
Jinwei Xin; xinjinwei18@163.com
Rights & Permissions [Opens in a new window]

Abstract

Matrix metalloproteinase (MMP)-2 and MMP-9 are a family of Zn2+ and Ca2+-dependent gelatinase MMPs that regulate muscle development and disease treatment, and they are highly conservative during biological evolution. Despite increasing knowledge of MMP genes, their evolutionary mechanism for functional adaption remains unclear. Moreover, analysis of codon usage bias (CUB) is reliable to understand evolutionary associations. However, the distribution of CUB of MMP-2 and MMP-9 genes in mammals has not been revealed clearly. Multiple analytical software was used to study the genetic evolution, phylogeny, and codon usage pattern of these two genes in seven species of mammals. Results showed that the MMP-2 and MMP-9 genes have CUB. By comparing the content of synonymous codon bases amongst seven mammals, we found that MMP-2 and MMP-9 were low-expression genes in mammals with high codon conservation, and their third codon preferred the G/C base. RSCU analysis revealed that these two genes preferred codons encoding delicious amino acids. Analysing what factors influence CUB showed that the third base distributors of these two genes were C/A and C/T, and GC3S had a wide distribution range on the ENC plot reference curve under no selection or mutational pressure. Thus, mutational pressure is an important factor in CUB. This study revealed the usage characteristics of the MMP-2 and MMP-9 gene codons in different mammals and provided basic data for further study towards enhancing meat flavour, treating muscle disease, and optimizing codons.

Type
Research Article
Information
Genetics Research , Volume 2022 , 2022 , e33
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © 2022 Tanliang Ouyang et al.

1. Introduction

Codon usage bias (CUB) is defined as unequal utilisation in the frequency of synonymous codons in coding amino acids (AAs), and it has been used extensively for investigating gene phylogeny [Reference Chakraborty, Mazumder and Uddin1]. The synonymous codon characteristics include universality, degeneracy, and wobble, and they should be used randomly to encode corresponding AAs with no pressure of interference pressure. However, CUB can be affected by nucleotides composition, translation, hydrophobicity, tRNA abundance, and protein structure [Reference Li2–Reference Goodarzi, Tor Ab I, Najaf Ab Adi and Archetti6]. Notably, natural selection and mutational pressure, which drive the correct translation process, are the major factors associated with CUB [Reference Musto, Cruveiller, D’Onofrio, Romero and Bernardi7, Reference Comeron, Kreitman and Aguade8]. Natural selection affects the pattern of codon usage in organisms, and mutational pressure may arise whilst the proportion of codon bases changes. CUB greatly increases the variability of genetic information and reflects the genetic drift of codons to a certain extent [Reference Dehlinger, Jurss, Lychuk and Putonti9]. Therefore, CUB can reveal the evolution of genes or organisms and environmental adaptation [Reference Angellotti, Bhuiyan, Chen and Wan10].

CUB is assessed by using the effective number of codons (ENC), codon adaptation index (CAI), frequency of optimal codons (FOP), codon bias index (CBI), and relative usage of synonymous codons (RSCU). ENC is calculated by comparing the GC content of synonymous codon positions [Reference Wright11]. CAI is 0-1; the closer the value is to 1, the stronger the nucleotide bases prefer synonymous codons [Reference Sharp and Li12]. FOP and CBI are both 0-1. These two indicators are close to 1, and the optimal codon for encoding amino acids is preferred. However, if CBI is negative, the optimal codon usage is less than the average number of codons used [Reference Ikemura3, Reference Bennetzen and Hall13]. RSCU is the specific value between the actual observation and theoretical observation, amongst which the theoretical observation value is the observation value when the synonymous codon usage frequency is the same, namely, there is no codon bias. If RSCU = 1, there is no CUB. If RSCU > 1, the appearance frequency of the codon is higher than the other synonymous codon. By contrast, it indicates lower genes. If RSCU > 2, then the frequency of CUB is extremely high [Reference Sharp and Li14].

Matrix metalloproteinases (MMPs) are a family of Zn2+ and Ca2+-dependent proteolytic enzymes that are widely expressed in animal tissues and highly conservative during biological evolution [Reference Tian, Han, Yu, Shi and Wang15]. MMP-2 and MMP-9 can regulate muscle growth, repair, and some relative processes that affect biochemical reactions for muscle regulation [Reference Gill and Parks16]. Although recent research mainly focused on exploring MMP-2 and MMP-9 function for animal skeletal muscle development, healing diseased muscle and even meat [Reference Mu, Urso, Murray, Fu and Li17–Reference Qi, Zhang, Wang, Zhang, Zhang and Zhang23], studies on MMP codons is rare. Therefore, there is an urgent need for exploring mammals’ MMP-2 and MMP-9 genetic evolution and codon usage pattern regulating muscle growth.

In this study, seven mammals (Bos grunniens, Bos taurus, and Sus scrofa among Artiodactyla; Macaca mulatta in Primates; Canis lupus familiaris in Carnivora; Oryctolagus cuniculus in Lagomorpha; and Mus musculus in Rodentia) were chosen to analyse CUB and base pair composition dynamics. This study would give insight into the factors affecting CUB for MMP-2 and MMP-9 genes and provide basic data for enhancing the meat flavour and finding a promising gene treatment for muscle disease.

2. Materials and Methods

2.1. Software

MEGA 7.0, CodonW 1.4.2, pheatmap, and ggplot packages based on R 4.4.3 software were used to complete the relevant analysis.

2.2. Base Composition of MMP Genes’ CDS in Different Mammals

The coding sequence (CDS) of yak MMP-2 and MMP-9 genes were obtained in our laboratory, and the NCBI accession numbers were MZ476247 and MZ476248, respectively. The CDS of other animals’ genes were from NCBI GenBank, and their accession numbers are shown in Figure 1.

FIGURE 1: NJ trees of MMP-2 (a) and MMP-9 (b) genes of seven mammal species.

CodonW 1.4.2 software developed by J. Peden was used to analyse the MMP-2 and MMP-9 CDS in seven mammals for calculating A/T (A/T base content, the same below), G/C, T3S (third base of the codon is T content, the same below), C3S, A3S, G3S, GC3S, AT3S, ENC, CAI, CBI, FOP, and RSCU [Reference Wu, Li, Zhao and Tao24]. R packages pheatmap and ggplot2 were used to analyse the data.

2.3. PR2 Plot

PR2 plot could analyse the bias amongst ATCG under gene mutation [Reference Guo and Wei25]. If the frequency of the third base is A > T, then dots are scattered on the top of the PR2 plot. If the frequency is C > G, then dots are on the left. When the codon does not show usage bias, the dots are in the centre of the graph [Reference Sueoka26].

2.4. Codon Neutral Analysis

Codon neutral analysis was carried out by the correlation analysis of GC12 (the average of the GC content of the first and second bases) and GC3S to compare the influence of natural selection pressure and mutational pressure on CUB [Reference Tamura, Higashi and Kitamoto27]. A significant correlation between GC12 and GC3S indicated that mutational pressure had a strong influence on codon preference; otherwise, natural selection influenced CUB [Reference Sueoka28].

2.5. ENC Plot

The relationship between ENC and GC3S without environmental selection pressure could be simulated by the following formula (1). The ENC/GC3S reference curve shows the main characteristics of codon usage patterns [Reference Wu, Li, Zhao and Tao24]. If CUB is more affected by natural selection, it should be below the standard curve. By contrast, it should be above the standard curve if it is more affected by other factors such as gene mutation. In general, the ENC is from 35 to 61. If ENC > 35, CUB is weak [Reference Wright11].

(1) ENC = 2 + GC 3 S + 29 GC 3 S 2 + 1 − GC 3 S 2 .

3. Results

3.1. Phylogenetic Analysis

Neighbour joining (NJ) trees were established based on the MMP-2 and MMP-9 CDS in seven mammals. The results (Figure 1) showed that the MMP-2 and MMP-9 genes of Bos grunniens were similar to those of B. taurus. These two genes of S. scrofa were similar to those of B. grunniens and B. taurus. Interestingly, the MMP-9 genes of C. lupus familiaris showed closer proximity to those of S. scrofa but those of the MMP-2 gene was farther.

3.2. Nucleotide Composition of MMP-2 and MMP-9 Genes

Compared with the content of codon bases of the MMP-2 and MMP-9 genes in seven mammals, the results showed (Tables 1 and 2) that the G/C content was higher than the A/T content. Most mammals’ MMP-2 and MMP-9 GC3S were larger than AT3S, except for the MMP-2 gene of B. taurus and M. musculus. The above findings indicated that the MMP-2 and MMP-9 gene codons preferred GC3S.

TABLE 1: Nucleotide composition in the sequence of MMP-2 gene.

TABLE 2: Nucleotide composition in the sequence of MMP-9 gene.

The codon usage results (Tables 3 and 4) showed that ENCs of the MMP-2 and MMP-9 genes in seven mammals were 40–56, indicating that these two genes had low expression and their codon conservation was high.

TABLE 3: Codon analysis of MMP-2 gene.

TABLE 4: Codon analysis of MMP-9 gene.

CAI showed that the preference for synonymous codons of the MMP-9 genes in seven mammals was significantly better than that of MMP-2, but both were lower than 0.3, indicating that it failed to reflect the preference of synonymous codons.

FOP and CBI results of the MMP-2 and MMP-9 genes showed that the optimal codon usage of MMP-2 in B. grunniens and B. taurus was inferior to the five other animals, whilst the optimal codon usage of MMP-9 was better than that of MMP-2.

3.3. RSCU Analysis

The RSCU results of the MMP-2 and MMP-9 genes showed that these two genes had a preference for 27 and 20 codons, respectively (Tables 5 and 6). Amongst them, CUG (encoding leucine, Leu) of MMP-2, CUG (encoding leucine, Leu), ACC (encoding threonine, Thr), and CGC (encoding arginine, Arg) of MMP-9 had strong high CUB (RSCU > 2).

TABLE 5: RSCU for MMP-2 gene among seven species.

Note.

* RSCU > 1;

** RSCU > 2; AA. amino acid; TER. termination codon; the same below.

TABLE 6: RSCU for MMP-9 gene among seven species.

Heat map analysis of the correlation between codon base composition and GC3S (Figure 2) showed that most of the codons of the MMP-2 and MMP-9 genes in different mammals were positively correlated with GC3S and in line with AC-, CG-, AT-, TC-, GG-, CC-, GC-, and other codons whose third base was C.

FIGURE 2: Heat maps of MMP-2 (a) and MMP-9. (b) Correlation coefficient of codons with GC3S.

Cluster analysis of the RSCU of the MMP-2 and MMP-9 genes showed that the MMP-2 gene preferred CUG, GUG, UCC, GAG, AUC, AAC, UAC, GCC, AGA, UUG, and AGG codons, which were mainly involved in encoding Leu (leucine), Val (valine), Ser (serine), Glu (glutamic acid), Iso (isoleucine) Asn (asparagine), Tyr (tyrosine), Gly (glycine), and Arg (arginine), respectively (Figures 3 and 4). In addition to B. taurus and C. lupus familiaris, the five other species had a strong preference for CUG and GUG (RSCU > 2), amongst which the RSCU of O. cuniculus and B. grunniens > 3. The MMP-9 gene preferred UCC, ACC, CGC, CUG, and AUC codons, which are mainly involved in Ser, Thr, Arg, Leu, and Iso, respectively. Except for M. musculus and O. cuniculus, the last five species had strong preferences similar to one another, indicating that the MMP-9 gene was more conservative than MMP-2.

FIGURE 3: Clustering of RSCU values of each codon in MMP-2 gene.

FIGURE 4: Clustering of RSCU values of each codon in MMP-9 gene.

3.4. Factors Influenced CUB

The PR2 plot result (Figure 5) showed that the ATCG base distribution of the MMP-2 and MMP-9 genes amongst seven mammals was above 0.5 on the x-axis. The bases distribution of the MMP-2 genes was mainly on the x-axis and the upper right of the y-axis and that of the MMP-9 genes was to the x-axis and the upper right of the y-axis. The above results indicated that the contents of A3S and C3S for the MMP-2 gene and the content of T3S and C3S for the MMP-9 gene were high, respectively.

FIGURE 5: PR2 plot among seven species.

Neutral analysis (Figure 6 and Table 7) showed that GC3S of these two genes was in the range of 0.44–0.78, whereas GC12 was from 0.52 to 0.67. The difference was that GC12 and GC3S of the MMP-2 gene were strongly negatively correlated (Pearson r = −0.851, p value < 0.05), whilst GC12 and GC3S of the MMP-9 gene were not significantly correlated, indicating that the base composition of the MMP-2 gene codons was susceptible to mutational pressure, but the factor influencing the MMP-9 gene was natural selection.

FIGURE 6: Codon neutral analysis.

TABLE 7: Pearson relative analysis with GC3S.

Note.

* P value < 0.05;

** p value < 0.01; red represents strong correlation, blue represents moderate correlation, and black represents irrelevance.

The ENC plot showed (Figure 7 and Table 7) that all ENC/GC3S dots of the MMP-2 and MMP-9 genes were distributed below the reference line. ENC and GC3S had a strongly negative correlation (MMP-2: Pearson r = −0.993, p value < 0.01; MMP-9: Pearson r = −0.963, p value < 0.01), and the distribution range of GC3S was large, indicating that the CUB of these two genes was affected by mutational pressure.

FIGURE 7: ENC plot among seven species.

4. Discussion

This study found that gelatinase MMP genes had CUB for encoding amino acids such as Ile, Arg, Glu, and Ser related to muscle development and meat quality. Gly, Arg, and Leu can promote collagen synthesis, and animal muscle is the main way to obtain natural collagen for humans [Reference Mitchell, Wilkinson, Phillips, Lund, Smith and Atherton29, Reference Solaro, Rosevear and Kobayashi30]. Delicious amino acids (DAAs), including Glu, Gly, Ser, Asp, Arg, and Ile, are known as precursor substances that determine the flavour of meat and can improve the taste of chicken and keep the meat soft [Reference Rabie, Peres and Malcata31]. Recent research found that the quality of chicken improves and the content of DAAs increases [Reference Yan, Liu and Xu32]. Otherwise, Strecker amino acids (SAAs), including Phe (phenylalanine), Cys (cysteine), Ile (isoleucine), and Leu (leucine), are highly related to the production of flavour. The higher their content, the stronger the fragrance [Reference Rizzi33]. For the MMP-2 and MMP-9 genes, the RSCUs of AUC encoding Ile; UCC and AGC encoding Ser; CGC encoding Arg; GAC encoding Asp; GAG encoding Glu; UUC encoding Phe; and GGA, GGC, and GGG encoding Gly were > 1. In particular, the RSCUs of CUG encoding Leu and CGC encoding Arg > 2; this value indicated that MMP-2 and MMP-9 demonstrated CUB for DAAs and SAAs. Besides, Leu, Ile, and Val belong to branched-chain amino acids (BCAAs), and they are essential AAs in humans and animals, accounting for about 35% of muscle protein. Previous studies have found that skeletal muscle, as the initial site of BCAAs catabolism, can be activated by branched-chain keto acids (BCKAs) to increase BCAAs synthesis to relieve muscle wasting disorders [Reference Holecek34]. Also, Leu supplementation could be the prevention and treatment of sarcopenia with aging [Reference Fujita and Volpi35]. Thus, BCAAs are important regulators of metabolism and metabolic health in in vivo [Reference Li, An and Bao36]. The gelatinase MMP CUB associated with corresponding AAs can provide basic data for the improvement of meat quality and muscle disease of MMP molecular modification.

Mutational pressure may be the main factor influencing the CUB of MMPs. This study found that the clustering results of the RSCU were different from the NJ trees of the genes, indicating that the MMP genes were highly conserved but maybe subjected to mutations during the evolution of different species. This influence caused a decline in the accuracy of single-gene species classification. Nucleotide AT (U) CG base composition is an important feature of genes, and the GC content can reflect the overall trend of gene mutation which is a decisive factor affecting the frequency of nucleotide use. Changes in the third base of the codon did not affect the encoded AAs, so GC3S could be an important reference for analysing the codon usage pattern. The gene mutation will affect the composition of the synonymous codon third bases with no natural selection, and the stronger the CUB, the more the codon is inclined to GC3S [Reference Novembre37, Reference Carlini, Chen and Stephan38]. Novembre et al. also found that the third base distribution of the MMP-2 and MMP-9 genes is mainly AC3S and CT3S, respectively, and the ENC/GC3S dot distribution can reach a wide range compared with the reference curve with gene mutation pressure. Thus, mutational pressure may play an important role in affecting the CUB for MMP-2 and MMP-9 genes, which also explains the difference in RSCU clustering in the seven mammals.

Interestingly, we also found that the clustering results based on the RSCU of the MMP-2 gene were not completely consistent with the phylogenetic results based on the MMP-2 gene’s CDS. Given that wild yak and Tibetan antelope grow in harsh environments with low altitudes and oxygen consumption, their EGLN1 gene has mutated changing nucleotide bases and leading to CUB changes [Reference Christianson39, Reference Wang, Zhang and Zhang40]. Therefore, we believe that the phylogenetic evolution of MMP-2 genes should not only refer to gene sequence but also CUB, which could be a supplement to species classification.

5. Conclusion

MMP-2 and MMP-9 are low-expression genes in mammals, and their codons are highly conservative. Both have a CUB at GC3S and prefer codons encoding DAAs and SAAs for improving soft meat and muscle disease treatment.

Data Availability

The yak MMP-2 and MMP-9 genes data used to support the findings of this study are included within the article and are available from the corresponding author upon request.

Ethical Approval

The procedures for care and use of experimental animals were in accordance with the Regulations on the Administration of Experimental Animals issued by the China State Council in 2017 and the guidance on Treating Experimental Animals developed by China’s Ministry of Science and Technology in 2006.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This work was supported by the Open Project Program of State Key Laboratory of Hulless Barley and Yak Germplasm Resources and Genetic Improvement (XZNKY-2021-C-014-K08), The Major Special Projects of Tibet Autonomous Region (XZ202101ZD0002N-01), and Program of National Beef Cattle and Yak Industrial Technology System (CARS-37). The authors thank KGSupport (https://www.kgsupport.com) for its linguistic assistance during the preparation of this manuscript.

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Figure 0

FIGURE 1: NJ trees of MMP-2 (a) and MMP-9 (b) genes of seven mammal species.

Figure 1

TABLE 1: Nucleotide composition in the sequence of MMP-2 gene.

Figure 2

TABLE 2: Nucleotide composition in the sequence of MMP-9 gene.

Figure 3

TABLE 3: Codon analysis of MMP-2 gene.

Figure 4

TABLE 4: Codon analysis of MMP-9 gene.

Figure 5

TABLE 5: RSCU for MMP-2 gene among seven species.

Figure 6

TABLE 6: RSCU for MMP-9 gene among seven species.

Figure 7

FIGURE 2: Heat maps of MMP-2 (a) and MMP-9. (b) Correlation coefficient of codons with GC3S.

Figure 8

FIGURE 3: Clustering of RSCU values of each codon in MMP-2 gene.

Figure 9

FIGURE 4: Clustering of RSCU values of each codon in MMP-9 gene.

Figure 10

FIGURE 5: PR2 plot among seven species.

Figure 11

FIGURE 6: Codon neutral analysis.

Figure 12

TABLE 7: Pearson relative analysis with GC3S.

Figure 13

FIGURE 7: ENC plot among seven species.