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. 2024 Apr 16;10(8):e29817. doi: 10.1016/j.heliyon.2024.e29817

Bibliometric evaluation of global trends and characteristics of RNA methylation during angiogenesis

Bingyan Li a,b,c,1, Zicong Wang a,b,c,1, Haixiang Zhou a,b,c, Wei Tan a,b,c, Jingling Zou a,b,c, Yun Li a,b,c, Shigeo Yoshida d, Yedi Zhou a,b,c,⁎
PMCID: PMC11046201  PMID: 38681586

Abstract

Background

RNA methylation is involved in major life processes. Angiogenesis is a normal phenomenon that occurs constantly in the bodies of all mammals, once it is aberrant or something goes wrong, it may lead to pathological changes. The bibliometric analysis could produce a comprehensive overview of RNA methylation during angiogenesis.

Methods

The Web of Science Core Collection (WoSCC) database was used to screen publications about RNA methylation during angiogenesis from Jan 1, 2000 to Nov 24, 2022. Bibliometric and visualization analyses were conducted to understand publication trends by CiteSpace and VOSviewer.

Results

In total, 382 publications from 2000 to 2022 were included in the bibliometric and visualization analyses. On the whole, the number of publications had exponential growth. China was the country and Sun Yat-Sen University was the university associated with the largest number of publications, although publications from the United Kingdom and Soochow University were currently having the strongest impact. Cancer was the most studied topic in this field, and N6-methyladenosine is the most studied RNA methylation type.

Conclusion

There is a continuously increasing trend in publications related to RNA methylation and angiogenesis, which has attracted much attention, particularly since 2011. RNA methylation might be a promising target in the investigation of pathological angiogenesis and related disorders, which deserves further investigation.

Keywords: RNA methylation, Angiogenesis, Bibliometric analysis, CiteSpace, VOSviewer

1. Introduction

RNA methylation is a dynamic and reversible modification that transfers methyl groups from S-adenosyl-l-methionine to nucleophilic acceptors of RNA such as O, As, N, S, or C via methyltransferases (MTases) [1,2]. It does not change the nucleotide sequence but may alter its expression in an epigenetic way [3]. Significantly, it may contribute to RNA stability, translation, degradation, the immune response, metabolic processes, and other cellular functions [[4], [5], [6]]. N6-methyladenosine (m6A), N1-methyladenosine (m1A), 5-methylcytosine (m5C), 5-hydroxymethylcytosine (5hmC), pseudouridine (Ψ), ribose 2′-O-methylation (2′-O-Me) [7], N7-methylguanosine (m7G), and adenosine-to-inosine editing (A-to-I editing) are the main components of RNA methylations [8,9], and they play important roles in mechanisms of embryonic development [10], initiation and progression of tumor growth [11,12], learning and memory [13], angiogenesis [14], and immunity [15,16].

Angiogenesis is involved in many pathological diseases, and it can be considered as an indicator of cancer, ischemic and inflammatory diseases [17] such as ocular neovascular diseases [18,19], malignant tumors [20,21], cardiovascular diseases [22], and rheumatoid arthritis [23]. Aberrant new blood vessels are dysfunctional compared to normal ones; they may have abnormal structures (incomplete tube walls without a smooth muscle component), show high vascular permeability and/or vascular malformations, and exhibit chaotic blood flow [17,[24], [25], [26]]. Therapy targeting angiogenesis diseases mainly focuses on inhibiting proangiogenic signals, immunotherapy, and surgical excision [[27], [28], [29]]. Herein, the formation of pathological neovascularization may lead to decreased vision, neurological disorders, tumor invasion and metastasis, and other symptoms which would may reduce the quality of life, survival rate, and lifetime [30,31].

Bibliometrics is a quantitative method of studying the literature, which can reveal active scholars, hot topics, developmental trends, and the outlook for a topic in the future [[32], [33], [34]]. In this study, we evaluated RNA methylation during angiogenesis utilizing bibliometrics to reveal the developmental trends in this research field. Our results clarified the current research trends, and provided a perspective on RNA methylation and angiogenesis.

2. Methods

2.1. Data source

The Web of Science is one of the largest and most comprehensive databases housing high-quality academic articles [35]. We used the Web of Science Core Collection (WoSCC) database for the analyses, and exported information of publication time, authors, keywords, countries, institutions, journals, and references.

2.2. Search strategy

As described in Fig. 1, the search phrases were TS= ((m6A or N6-methyladenosine or m5C or 5-methylcytosine or m1A or N1-methyladenosine or m7G or N7-methylguanine or 2′-O-methylation or Pseudouridine or 5hmC or 5-hydroxymethylcytosine or Adenosine-to-inosine editing or A-to-I editing or RNA methylation) AND (neovascularization or angiogenesis or neovascular disease or new blood vessel)), to identify as many relevant publications as possible about RNA methylation and neovascularization. The language was restricted to English, publication types were limited to articles and reviews, and the publication period was from Jan 1, 2000 to Nov 24, 2022, which were sufficient to illustrate the developmental trend and characteristics of the study topic.

Fig. 1.

Fig. 1

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Flow diagram of publication search and exclusion.

2.3. Data extraction and collection

In total, 390 publications were identified and exported in a plain text file, which was convenient for bibliometric analysis. Next, we excluded 8 publications including 2 book chapters, 4 proceedings papers, and 2 retracted publications by CiteSpace, and reserved 382 publications for visualization analysis.

2.4. Analysis

We utilized Microsoft Excel 2019, CiteSpace 6.2.R4, VOSviewer 1.6.18 and R language 4.1.3 for the bibliometric analysis [36,37]. We mainly focused on several specific characteristics, such as publications, countries or institutions, authors, journals, keywords and references.

3. Results

3.1. Annual publication trends

As shown in Fig. 2, we quantify the number of annual publications from Jan. 1, 2000, to Nov. 24, 2022. Publication numbers increase exponentially in this domain during this period. The increase is particularly obvious in 2011, when it more than doubled versus previous years, indicating that the topic suddenly attracts the attention of a large number of scholars. Between 2011 and 2016, the volume of annual publications remains stable. Beginning in 2017, however, the number increases again. Publications in 2022 decrease may because we only count to November 24. These results indicate that RNA methylation during angiogenesis is a research hotspot.

Fig. 2.

Fig. 2

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Annual distribution trends of the study of RNA methylation during angiogenesis from 2000-01-01 to 2022-11-24.

3.2. Distribution and cooperation of countries or institutions

Next, we present the different countries and institutions which publish these papers. As shown in Table 1, China is the most productive country (n = 195), followed by the United States (the USA, n = 90), India (n = 21), Germany (n = 19), the United Kingdom (UK), and the Netherlands (n = 17). Fig. 3A shows the publication numbers all over the world in the format of the map of the world, and the color depth of the country marked on the map is proportional to the number of publications, which also indicates China has the most publication numbers. CiteSpace identifies the cooperation and mutual exchanges among countries in Fig. 3B. A node represents a country, the size of a node signifies publications, the purple ring outside of a node stands for centrality and a greater influence on the network, and the line thickness stands for the degree of cooperation relationship. The top 5 core countries of centrality are the UK, Germany, Greece, the USA, and Australia. The UK establishes cooperation with other 8 countries, such as Germany, Finland, Japan, and Sweden. Australia links with India, Netherlands, and other regions. China has the largest publications in this field, the international collaborations are found with Japan. Some countries do not have academic exchange within the research topic, such as Mexico and Brazil.

Table 1.

Top 10 countries in terms of publications and centrality.

Rank Publications Country Rank Centrality Country
1 195 China 1 0.52 UK
2 90 USA 2 0.45 Germany
3 21 India 3 0.44 Greece
4 19 Germany 4 0.42 USA
5 17 UK 5 0.42 Australia
6 17 Netherlands 6 0.37 Sweden
7 15 Japan 7 0.22 Netherlands
8 14 Italy 8 0.22 Italy
9 11 Canada 9 0.20 Turkey
10 11 Australia 10 0.19 Japan
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Fig. 3.

Fig. 3

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Publication numbers and international cooperation analysis of studies of RNA methylation during angiogenesis among countries and institutions. (A) Visualization of publications around the world by using R language. (B) Network visualization for different countries by CiteSpace. A node represents a country, and the size of a node stands for publications, the purple ring at the periphery of a node signifies centrality, and the line represents cooperation between countries. (C) Institutional cooperation network by VOSviewer. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

Sun Yat-Sen University has published the most papers (n = 16), followed by Nanjing Medical University (n = 14), Funan University (n = 11), Huazhong University of Science and Technology (9), and Harbin Medical University (n = 9) (Table 2). As is listed in Table 2, the top 5 institutions of centrality are Soochow University, the Second Military Medical University, Ningxia Medical University, Tongji University, Huazhong University of Science and Technology, and Harbin Medical University. These results lack consistency with the rank of publications, which suggests that publication numbers are not proportional to influence and importance. Moreover, only 353 out of 642 institutions have established mutual connections. Fig. 3C presents 28 clusters from 353 institutions by different colors which contain 4 to 19 institutions each. For example, China Medical University, Dalian Municipal Central Hospital, Imperial College London, University of Turku, and other 15 institutions formed a cluster labeled by red color.

Table 2.

Top 10 institutions in terms of publications and centrality.

Rank Publications Institution Rank Centrality Institution
1 16 Sun Yat-Sen Univ 1 0.23 Soochow Univ
2 14 Nanjing Med Univ 2 0.20 Second Mil Med Univ
3 11 Fudan Univ 3 0.20 Ningxia Med Univ
4 9 Huazhong University Sci & Technol 4 0.18 Tongji Univ
5 9 Harbin Med Univ 5 0.17 Huazhong University Sci & Technol
6 8 Capital Med Univ 6 0.17 Shanghai Jiao Tong Univ
7 8 Zhejiang Univ 7 0.15 Helmholtz Zentrum Munchen
8 8 Zhengzhou Univ 8 0.14 University Munich
9 7 Leiden Univ 9 0.14 University Leicester
10 7 Sichuan Univ 10 0.14 University Nottingham
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3.3. Analysis of published and cited journals

The top 10 publications and cited journals are enumerated in Table 3. Frontiers in Cell and Development Biology has the largest number of publications (n = 11), 6 of the top 10 publications are in Journal Citation Reports Quarter 1 (JCR Q1). Cancer Research is the most quoted journal, which is cited 835 times in total. At the same time, 8 of the top 10 cited journals are in JCR Q1; Cell, Nature, and Science are also cited many times. These results suggest that scholars are more inclined to publish and quote literature in high-quality journals. Next, we use a dual-map overlay of journals to explore the citation relationships among journals (Fig. 4). The left is the cited journal, and the right is the citing journal, and the discipline source of the journal is distinguished by different colors. Journals between Molecular/Biology/Immunology and Molecular/Biology/Genetics (the yellow link) show the strongest conjunction relationship. Scholars can focus on such journals to quickly find appropriate articles related to this topic.

Table 3.

Top 10 journals published and cited related to RNA methylation during angiogenesis.

Rank Journal Publications JCR IF (2021) Rank Journal Citation JCR IF (2021)
1 Frontiers in Cell and Developmental Biology 11 Q1 6.081 1 Cancer Research 835 Q1 13.312
2 Frontiers in Oncology 10 Q2 5.738 2 Nature 789 Q1 69.504
3 Oncotarget 10 – – 3 Proc Natl Acad Sci U S A 684 Q1 12.779
4 Frontiers in Genetics 8 Q1 4.772 4 Cell 648 Q1 66.850
5 Clinical Epigenetics 7 Q1 7.259 5 the Journal of Biological Chemistry 624 Q2 5.486
6 International Journal of Molecular Sciences 7 Q1 6.208 6 PLos One 489 Q2 3.752
7 Journal of Cellular Physiology 7 Q1 6.613 7 Oncogene 485 Q1 8.756
8 Molecular Cancer 7 Q1 41.444 8 Nucleic Acids Research 457 Q1 19.160
9 PLos One 7 Q2 3.752 9 Science 392 Q1 63.714
10 Cancer Cell International 5 Q2 6.429 10 Oncotarget 329 – –
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Proc Natl Acad Sci U S A: Proceedings of the National Academy of Sciences of the United States of America.

Fig. 4.

Fig. 4

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Dual-map overlay of publishing and cited journals generated by CiteSpace. The publishing journals are shown on the left, and the citing journals are listed on the right.

3.4. Author analysis

A co-citation relationship exists when publications by two authors are cited by a third author. The higher the co-citation frequency, the closer their academic relationship and the shorter their “distance” in the figure. Fig. 5A shows the results of co-citation analysis, a total of 173 authors with at least 10 citations are included. The top 5 authors with the largest total link strength are Wang X, Meyer KD, Wang Y, Dominissini D, and Liu J. The link strength of the top 2 is particularly high, above 1000, which indicates that their research has a profound impact on studies in RNA methylation and angiogenesis. Moreover, the top 5 authors account for 4/5 of the top 5 co-cited references, which once again confirms the importance and influence of their articles to others (Table 4). We only identify 58 co-authors, which suggests that individual research is the norm in this field; and a wide range of academic communities of authors has not yet been formed (Fig. 5B).

Fig. 5.

Fig. 5

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Author co-citation (A) and co-authorship (B) visualization map by VOSviewer.

Table 4.

Top 5 co-cited references related to RNA methylation during angiogenesis.

Rank Title First Author Co-citation Journal JCR IF (2021) Reference
1 N6-methyladenosine-dependent regulation of messenger RNA stability Xiao Wang 28 Nature Q1 69.504 [43]
2 Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq Dan Dominissini 28 Nature Q1 69.504 [44]
3 Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons Kate D Meyer 24 Cell Q1 66.850 [45]
4 N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO Guifang Jia 23 Nature Chemical Biology Q1 16.174 [46]
5 N (6)-methyladenosine Modulates Messenger RNA Translation Efficiency Xiao Wang 21 Cell Q1 66.850 [47]
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3.5. References analysis

Co-cited reference analysis is similar to author co-citation analysis, which represents the closeness of a partnership. The resulting networks of co-cited references are shown in Fig. 6A. The time of the citation bursts is only 1 or 2 years (Fig. 6B), which illustrates that the hotspot of study direction changes fast, enabling scholars to have a forward-looking perspective. We list the top 5 co-cited references in the field (Table 4), find that “N6-methyladnosine-dependent regulation of messenger RNA stability” reported by Wang X in Nature is the most frequently co-cited, and all of them are associated with the characteristics of m6A modification, such as functions of methylation modification-related enzymes, findings of recognition sites and technical analysis. As for the top 10 cited references shown in Table 5, there are 4 papers summarize the biological functions of RNA methylation, such as the stability of target RNA and the process of translation, 5 papers that are closely associated with cancers, and 1 paper on the cardiac system.

Fig. 6.

Fig. 6

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Reference analysis of studies of RNA methylation during angiogenesis. (A) Network map of co-cited references by VOSviewer. (B) Top 25 references with the strongest citation bursts by CiteSpace.

Table 5.

Top 10 cited references related to RNA methylation during angiogenesis.

Rank Reference citation Journal JCR IF(2021) Reference
1 Recognition of RNA N6-methyladenosine by IGF2BP proteins enhances mRNA stability and translation 19 Nature Cell Biology Q1 28.213 [48]
2 Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries 18 CA: A Cancer Journal for Clinicians Q1 286.130 [49]
3 Post-transcriptional gene regulation by mRNA modifications 16 Nature Reviews Molecular Cell Biology Q1 113.915 [50]
4 Dynamic RNA Modifications in Gene Expression Regulation 15 Cell Q1 66.850 [51]
5 RNA N6-methyladenosine methyltransferase-like 3 promotes liver cancer progression through YTHDF2-dependent posttranscriptional silencing of SOCS2 14 Hepatology Q1 17.298 [52]
6 FTO-Dependent N6-Methyladenosine Regulates Cardiac Function During Remodeling and Repair 14 Circulation Q1 39.918 [53]
7 Role of METTL3-Dependent N6-Methyladenosine mRNA Modification in the Promotion of Angiogenesis 13 Molecular Therapy Q1 12.910 [54]
8 FTO Plays an Oncogenic Role in Acute Myeloid Leukemia as a N6-Methyladenosine RNA Demethylase 11 Cancer Cell Q1 38.585 [55]
9 RNA N6-methyladenosine reader IGF2BP3 regulates cell cycle and angiogenesis in colon cancer 11 Journal of Experimental & Clinical Cancer Research Q1 12.658 [56]
10 m6A RNA Methylation Regulates the Self-Renewal and Tumorigenesis of Glioblastoma Stem Cells 10 Cell Reports Q1 9.995 [57]
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3.6. Trending topics

Keywords are crucial for a paper, which represent the core content and central idea of a paper. Table 6 lists the top 20 keywords of frequency, and Fig. 7A shows the results of co-occurrence analysis of keywords. Angiogenesis is the major keyword of our research topic. m6A is included in RNA methylation, METTL3 and IGF2BP3 are the two enzymes in m6A modification. VEGF is a growth factor, while inflammation and proliferation are crucial pathological processes which are involved in neovascularization. miRNA, lncRNA, and ncRNA are the target molecules of RNA methylation. Also, Fig. 7A indicates other targets of RNA methylations, such as p53, EZH2, BRCA1, MMP2, and TRAF1, and they have been intensively studied in the cancer field. Moreover, acute myeloid leukemia, hepatocellular carcinoma, glioma, metastasis, lung cancer, melanoma, breast cancer, colorectal cancer, and renal cell carcinoma are the keywords that are closely associated with tumor or cancer, which demonstrate that they are the research hotspots and trends of RNA methylation during angiogenesis. Also, some keywords are describing the technique analysis, such as RNA-seq and transcriptome which can be linked with some top co-cited references. Fig. 7B lists the top 25 keywords with the strongest citation bursts in time sequence, cancer or tumor occupy the majority of keywords since 2000; diabetic retinopathy and inflammation are new and developing topics that start trending in 2021.

Table 6.

Top 20 keywords related to RNA methylation during angiogenesis.

Rank Keywords Counts Rank Keywords Counts
1 angiogenesis 60 11 histone modification 16
2 DNA methylation 56 12 Mettl3 15
3 epigenetics 47 13 metastasis 14
4 miRNA 38 14 hypoxia 13
5 m6A 32 15 lung cancer 12
6 methylation 25 16 biomarker 11
7 cancer 20 17 ncRNA 11
8 lncRNA 18 18 colorectal cancer 10
9 prognosis 18 19 proliferation 9
10 VEGF 17 20 renal cell carcinoma 9
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Fig. 7.

Fig. 7

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Keywords analysis of studies on RNA methylation during angiogenesis. (A) Keyword co-occurrence map by VOSviewer. (B) Top 25 keywords with the strongest citation bursts by CiteSpace.

4. Discussion

As a common epigenetic modification, RNA methylation is widely included in research fields, such as angiogenesis, immunity and metabolic process [38,39]. Abnormal angiogenesis is a pathological process in many diseases, which has attracted the attention of a large number of scholars [40]. In this study, regarding RNA methylation during angiogenesis, bibliometric analysis has been conducted to summarize the developmental trends and other characteristics of publications and research in this field.

In all, 382 publications were included in our analysis. Original articles and reviews made up 290 and 92 of these papers, respectively, which indicated that most studies were original research. The annual publication trends (Fig. 2) demonstrated the appearance of a sudden increase in pertinent publications in 2011, with a continuous increase starting from 2017. We only included publications since 2000, because only one paper was published before 2000, which may not influence the results. These data showed that the study of RNA methylation during angiogenesis had expanded rapidly in recent years, and would likely maintain this trend in the future. We found that 7 of 10 countries with the top number of publications were in the list of the top 10 centrality ranking (Table 1). Moreover, there was only one overlap in the top 10 institutions in terms of publication and centrality ranking (Table 2). These results suggested that publication numbers did not equate to publication influence and quality. Fig. 3B and C illustrated that academic circles have been initially formed among countries or institutions. We believe that cooperation between different countries or institutions could promote academic exchanges and communications, stimulate novel research ideas, accelerate the progress of research, and even promote the transformation of achievements. High-influenced countries or institutions in this field may also drive academic progress in other countries.

The top cited and co-cited references in the field of RNA methylation during angiogenesis were closely linked with biological functions of RNA methylation and cancer-related diseases, especially for m6A modification. The reason for high citation frequency of these articles summarizing functions of RNA methylation is that they are the basic and an integral part of the studies and could help to deeply investigate the roles and mechanisms in the diseases.

Angiogenesis can be involved in multiple domains of research, such as immune rejection and wound healing [41,42]. Fig. 7A and Table 6 showed research highlights and focus by analysis of the keywords. m6A, METTL3, and IGF2BP3 were keywords for describing m6A modification, and the top cited or co-cited references were all under the theme of m6A evidencing m6A modification was the most widely studied direction in RNA methylation during angiogenesis. Moreover, cancer was the most widely and deeply explored in this field by the presentation of keywords, such as hepatocellular carcinoma, glioma, and metastasis, which may still be the promising research direction in the future.

In the present study, the results identified the developmental trends of RNA methylation and angiogenesis, the associated countries, institutions, authors, journals, references, and the involved keywords. Investigators may use the results as a guide for a quick and comprehensive understanding of the research field and to generate research ideas; the major research hotspots in the field have also been identified. However, some limitations still exist in our study. For example, we limited the search criteria to a specific period, specific article types, the English language, and only one database (WoSCC), which may result in possible bias in literature research. In addition, the citation frequency of a paper is related to the journal's influence and reputation, self-citation, and time of publication to some extent, thus, the citation number may not be exactly consistent with its real scientific worth and influence.

5. Conclusion

To sum up, the study presents the past patterns and prospects in RNA methylation during angiogenesis, which has been developing vigorously since 2011. Most included studies focused on this topic in the context of tumors, while there has been a recent increase in the number of studies focused on other aspects such as ocular diseases. Our results demonstrate that RNA methylation is a promising target in research of angiogenesis and related disorders, which deserves further investigations in the future.

Funding statement

This work was supported by grants from the National Natural Science Foundation of China (No. 82271110), and the Fundamental Research Funds for the Central Universities of Central South University (No. 2021zzts1068).

Data availability statement

Data included in article/supp. material/referenced in article.

CRediT authorship contribution statement

Bingyan Li: Data curation, Formal analysis, Visualization, Writing – original draft, Writing – review & editing, Funding acquisition. Zicong Wang: Writing – review & editing, Data curation, Formal analysis, Visualization, Writing – original draft. Haixiang Zhou: Data curation, Formal analysis. Wei Tan: Data curation, Formal analysis. Jingling Zou: Data curation, Formal analysis. Yun Li: Supervision, Writing – review & editing. Shigeo Yoshida: Supervision, Writing – review & editing. Yedi Zhou: Conceptualization, Funding acquisition, Supervision, Writing – original draft, Writing – review & editing.

Declaration of competing interest

The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: we declare that Yedi Zhou serves as an Associate Editor for Heliyon Clinical Research.

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