Looking back on 50 years of cell biology in Japan

Abstract

Cell Structure and Function (CSF), the official journal of the Japan Society for Cell Biology (JSCB), celebrates its 50th anniversary in 2025. This essay traces the scientific evolution of CSF from its founding in 1975 to the present, drawing on bibliometric data retrieved from OpenAlex at ten-year intervals. Over five decades, CSF published 1,737 articles, with the Field-Weighted Citation Impact (FWCI) showing a consistent upward trend, even as total output declined following the journal’s shift to electronic publication in 2005. A decade-by-decade analysis of the five most-cited articles reveals a clear evolution in research themes: early issues were dominated by plant cell biology and methodological papers in microscopy and biochemistry, while subsequent decades saw increasing focus on autophagy, the unfolded protein response, and intracellular membrane trafficking—fields in which Japanese researchers have played globally recognized pioneering roles. The turn of the millennium marked a peak in absolute citations, with landmark papers on bafilomycin A1, SNARE proteins, and a review of autophagy co-authored by Nobel Prize laureate Yoshinori Ohsumi. Two major milestones—electronic publication in 2005 and gold open-access adoption in 2016—fundamentally transformed the journal’s publishing model. Looking ahead, the essay considers the role of artificial intelligence in peer review, arguing that while AI can assist in assessing novelty and reproducibility, the judgment of a manuscript’s scientific significance must remain a human responsibility. CSF remains committed to disseminating reliable, foundational cell biology to the international community.

Key words: Cell Structure and Function (CSF), bibliometrics, open access, artificial intelligence in peer review

Graphical Abstract

Introduction

Cell Structure and Function (CSF) was first published in 1975, a few years before I started my research career (Table 1). In those days, the first step in beginning a research project was to search the literature using Index Medicus—scanning row upon row of volumes arranged along the dimly lit stacks of the library. Once a study was complete, a handwritten manuscript was transcribed on a manual typewriter. Two milestones stand out in the 50-year history of CSF: its transition to an electronic journal in 2005, and the adoption of gold open access in 2016. These developments reflect both the end of movable-type printing—a technology that had endured for 500 years—and a fundamental shift in the business model of academic publishing, whereby the financial burden of publication has moved from journal subscribers to article authors.

Table 1

Cell Structure and Function—Milestones in the context of global publishing

Year	Milestone	Global Context
1975	Launched as the English-language journal of the Japan Society for Cell Biology
1996		PubMed service launched
1999	Joined J-STAGE
2000	PDF articles made publicly available	PubMed Central established
2002	PubMed linking established; open access initiated
2004	HTML article publication began	Index Medicus discontinued
2005	Fully converted to electronic journal format
2006	Online submission and peer review system introduced
2014	Article Processing Charges (APC) implemented
2016	Gold Open Access adopted (CC-BY license)
2018		Plan S announced
2020	Redesigned article layout; J-Stage Data integration launched
2023	Indexed in PubMed Central (PMC)
2024	Listed in the Directory of Open Access Journals (DOAJ)
2026	Application to Committee on Publication Ethics (COPE) in progress

CSF has been serving as the official journal of the Japan Society for Cell Biology (JSCB), disseminating the work of its members to the international community. How, then, has the scientific content of the papers published in CSF evolved over this half-century? In this essay, I trace the shifting currents of research reflected in the journal from its founding to the present, and then discuss the future direction of this journal. Bibliometric data for CSF articles were downloaded from OpenAlex as CSV files in ten-year intervals (https://openalex.org/). The dataset was inspected to exclude errata and records not attributable to CSF. Table 2 presents the number of articles published, together with the mean and median citation counts and the Field-Weighted Citation Impact (FWCI) for each decade. Article output has declined substantially since 2005, when CSF adopted electronic publication. In fact, one of the main reasons why CSF moved to electronic publication is that CSF was no longer able to afford to continue bimonthly publishing due to the increasing publication costs. Across all decades, the mean citation count markedly exceeded the median, indicating that the overall average was inflated by a small number of highly cited papers. Mean citation counts were highest during the decade spanning the turn of the millennium. The FWCI, which captures citation impact relative to the global average within the same field and publication year, exceeded 1.0 during that same period and has shown an upward trend thereafter. Because FWCI is calculated by dividing the observed citation count by the world average for papers in the same field and year, a rise in FWCI despite a decline in absolute citations implies that the global field average has fallen even more steeply—a pattern consistent with the broader expansion of the literature, which tends to dilute mean citation rates across all journals. It is also possible that a thematic shift within CSF toward topics such as ER stress, autophagy, and intracellular trafficking—areas with strong ties to medicine and drug discovery—has contributed to the relative resilience of the journal’s citation impact, a point we will return to in the decade-by-decade analysis that follows.

Table 2

Changes in citation counts

Period	No. of Papers	Mean Citations	Median Citations	Total Citations	Mean FWCI
1975–1985	441	9.7	6	4,258	0.72
1986–1995	545	17.1	7	9,312	0.75
1996–2005	445	40.1	17	17,860	1.11
2006–2015	162	37.2	21	6,040	1.36
2016–2025	144	13.9	8	2,009	1.69

FWCI (Field-Weighted Citation Impact) is a normalized citation metric that compares the number of citations received by a given publication to the average number of citations received by all publications of the same document type, published in the same year, and indexed in the same field. A value of 1.0 indicates performance at the world average, values above 1.0 indicate above-average citation impact, and values below 1.0 indicate below-average impact. In the present analysis, FWCI values were retrieved from the OpenAlex database. Note that although OpenAlex applies the same Snowball Metrics formula as Scopus/SciVal, absolute FWCI values may differ between platforms due to differences in database coverage and subfield classification methods.

Looking back at the trend of CSF

To grasp the trend, I examine the five most-cited papers published in each decade (Table 3). The most frequently cited article from the first decade (1975–1985) was by Masashi Tazawa and colleagues, describing internodal cells of Characeae from which the tonoplast had been removed (Tazawa et al., 1976). The paper reported a method for selectively eliminating the tonoplast using EGTA while minimizing cellular damage, and it went on to inspire a substantial body of subsequent research. The second and third most cited papers of this decade, published by Tsuneyoshi Kuroiwa and Stuart L. Jacobson, respectively, described an improved protocol for staining chloroplast nuclei with 4',6-diamidino-2-phenylindole (DAPI) and a culture method for rat myocardial cells (Jacobson, 1977) (Kuroiwa and Suzuki, 1980). Taken together, all three of the most frequently cited papers from this period describe cell biological methods that laid the technical groundwork for the research that followed. Among the five top-cited papers of this decade, three dealt with plant cells, one with animal cells, and one addressed both. The character of the research published in this era can perhaps be appreciated from the following data: across all five papers, a total of 23 figures appeared. Of these, micrographs of cells featured in just two papers—the Kuroiwa et al. study included a single panel combining fluorescence and phase-contrast images (Fig. 1), while the Jacobson et al. paper contained two figures comprising photographs of the apparatus alongside phase-contrast micrographs. One can readily imagine the considerable effort that obtaining even a single micrograph demanded at the time. In the remaining papers, the analytical methods employed were predominantly biochemical measurements and electrophysiology. It is also noteworthy that a striking proportion of the top-cited papers list senior investigators as first authors—a characteristic feature of this era.

Table 3

Most cited papers in each decade since 1975

Year	Title	Citation count	First author	Last author
1976	Electric characteristics and cytoplasmic streaming of characeae cells lacking tonoplast (Tazawa et al., 1976)	166	Masashi Tazawa	Teruo Shimmen
1980	An improved method for the demonstration of the in situ chloroplast nuclei in higher plants (Kuroiwa and Suzuki, 1980)	114	Tsuneyoshi Kuroiwa	Takahito Suzuki
1977	Culture of spontaneously contracting myocardial cells from adult rats (Jacobson, 1977)	89	Stuart L. Jacobson	Stuart L. Jacobson
1975	Localization of myosin in the internodal cell of Nitella as suggested by differential treatment with N-Ethylmaleimide (Chen and Kamiya, 1975)	79	James C. W. Chen	Noburô KAMIYA
1980	Chromatin-associated DNA polymerase activity in meiotic cells of lily and mouse; its stimulation by meiotic helix-destabilizing protein (Sakaguchi et al., 1980)	72	Kengo Sakaguchi	Herbert Stern
1995	Functional analysis and DNA polymorphism of the tandemly repeated sequences in the 5'-terminal regulatory region of the human gene for Thymidylate synthase (Horie et al., 1995)	549	Nobuyuki Horie	Keiichi Takeishi
1988	Novel purification of vitronectin from human plasma by heparin affinity chromatography (Yatohgo et al., 1988)	515	Takemi Yatohgo	Masao Hayashi
1995	A novel method of preparing rat-monoclonal antibody-producing Hybridomas by using rat medial iliac lymph node cells (Kishiro et al., 1995)	189	Yumiko Kishiro	Yoshikazu Sado
1990	Flavonoids inhibit the expression of heat shock proteins (Hosokawa et al., 1990)	182	Nobuko Hosokawa	Kazuhiro Nagata
1986	N-linked oligosaccharides are not involved in the function of a cell-cell binding glycoprotein E-cadherin (Shirayoshi et al., 1986)	172	Yasuaki Shirayoshi	Masatoshi Takeichi
1998	Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E Cells (Yamamoto et al., 1998)	1284	Akitsugu Yamamoto	Yutaka Tashiro
2002	Autophagosome formation in mammalian cells [Review] (Mizushima et al., 2002)	862	Noboru Mizushima	Tamotsu Yoshimori
2004	Systematic analysis of SNARE molecules in Arabidopsis: Dissection of the post-Golgi Network in Plant Cells (Uemura et al., 2004)	538	Tomohiro Uemura	Masa H. Sato
2001	Structure and function of VEGF/VEGF-receptor system involved in angiogenesis [Review] (Shibuya, 2001)	500	Masabumi Shibuya	Masabumi Shibuya
2004	Immunohistochemical localization of Klotho protein in brain, kidney, and reproductive organs of mice (Li et al., 2004)	350	Shun-Ai Li	Kohji Takei
2008	ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum (Adachi et al., 2008)	474	Yusuke Adachi	Kazutoshi Mori
2008	Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes (S. Kimura et al., 2008)	411	Shunsuke Kimura	Tamotsu Yoshimori
2008	The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies (H. Kimura et al., 2008)	307	Hiroshi Kimura	Naohito Nozaki
2008	GFP-like proteins stably accumulate in lysosomes (Katayama et al., 2008)	236	Hiroyuki Katayama	Atsushi Miyawaki
2007	ARMET is a soluble ER Protein Induced by the Unfolded Protein Response via ERSE-II Element (Katayama et al., 2008)	177	Naomi Mizobuchi	Kazuhiro Nagata
2017	PI5P and PI(3,5)P2: Minor, but essential phosphoinositides [Review] (Hasegawa et al., 2017)	156	Junya Hasegawa	Lois S. Weisman
2017	TFE3, HSP47, and CREB3 pathways of the mammalian Golgi stress response [Review] (Taniguchi and Yoshida, 2017)	95	Mai Taniguchi	Hiderou Yoshida
2016	Multiplexed fluorescence imaging of ERK and Akt activities and cell-cycle progression (Maryu et al., 2016)	76	Gembu Maryu	Kazuhiro Aoki
2016	Multiple types of guanine nucleotide exchange Factors (GEFs) for Rab Small GTPases [Review] (Ishida et al., 2016) (Ishida et al., 2016)	70	Morié Ishida	Mitsunori Fukuda
2021	In vivo roles of Rab27 and its effectors in exocytosis [Review] (Izumi, 2021)	58	Tetsuro Izumi	Tetsuro Izumi

Fig. 1

Phase contrast (b) and fluorescent micrographs (a, c, d) reveal cells containing single nucleus (N) and chloroplast nuclei (arrows in c, d) with a cell wall (CW, a) or without cell wall of Vicia faba (b, d) and Pisum sativum (c) after DAPI staining. Adapted from (Kuroiwa and Suzuki, 1980).

In the 1986–1995 period, Horie and colleagues demonstrated that the expression of thymidylate synthase is regulated by a tandemly repeated sequence located within the 5' untranslated region. The polymorphism of this region was later used to predict the efficacy of chemotherapy, bringing this paper the honor of the most cited CSF paper published in this decade (Horie et al., 1995). The second and third most cited CSF papers during this decade are about methods. Yatohgo and colleagues described a simple and inexpensive method for purifying vitronectin using a heparin affinity column (Yatohgo et al., 1988) and Kishiro and colleagues, presented an efficient protocol for generating rat monoclonal antibodies (Kishiro et al., 1995). The fourth-ranked paper by Hosokawa and colleagues demonstrated that flavonoids, exemplified by quercetin, suppress the induction of heat shock proteins (HSPs) by various cellular stressors at the transcriptional level (Hosokawa et al., 1990). This work can be regarded as a pioneering contribution, as it established for the first time the concept that HSP induction can be suppressed at the transcriptional level by pharmacologically applicable small-molecule compounds. The fifth most cited paper by Shirayoshi, Takeichi and colleagues showed that N-linked oligosaccharides are dispensable for the cell–cell binding function of E-cadherin (Shirayoshi et al., 1986). Cell adhesion mechanisms mediated by cadherins, autophagy, the unfolded protein response (UPR), and molecular motors are all fields in which Japanese researchers have played pioneering roles, and the abundance of publications in these areas may be considered another hallmark of CSF.

The decade spanning the turn of the millennium was a period in which intracellular organelles took center stage. Yamamoto and colleagues demonstrated that bafilomycin A1, an inhibitor of vacuolar-type H⁺-ATPase (V-ATPase), blocks the fusion of autophagosomes with lysosomes (Fig. 2), a finding that established this compound as a widely used tool for inhibiting autophagy (Yamamoto et al., 1998). In the third most cited paper during this decade, Uemura and colleagues conducted a comprehensive analysis of all 53 SNARE proteins encoded in the Arabidopsis genome, laying the foundation for the systematic study of SNARE-mediated membrane trafficking in this model organism (Uemura et al., 2004). Notably, CSF began publishing review articles in 1996, a development that significantly strengthened the journal’s role in disseminating Japanese cell biology to the international community. The review paper by Mizushima, Ohsumi, and Yoshimori described the molecular mechanism of autophagy (Mizushima et al., 2002), for which Nobel Prize was awarded in 2016. Another excellent review paper about endothelial growth factor (VEGF) and its cognate receptors was contributed by Masabumi Shibuya (Shibuya, 2001), who discovered VEGF gene as a proto-oncogene Flt-1 (Shibuya et al., 1990). The fifth most cited paper by Li, Takei and colleagues described the localization of Klotho protein (Li et al., 2004), which was discovered by Nabeshima and colleagues and shown to cause progeria in mice (Kuro-o et al., 1997).

Fig. 2

Electron micrographs of H-4-II-E cells treated with bafilomycin A₁. Adapted from (Yamamoto et al., 1998).

Unfolded protein response (UPR) is another field that JSCB members greatly contributed to its understanding. In the most cited article of the 2005–2015 decade, Adachi and Mori identified 30 target genes of ATF6, a transcription factor that governs the expression of UPR-related proteins (Adachi et al., 2008). Mizobuchi and Nagata reported that ARMET is a soluble ER-resident protein whose expression is induced by UPR in fifth-ranked article (Mizobuchi et al., 2007). The second most cited paper concerned autophagy and molecular motors. Kimura and Yoshimori reported that autophagosomes are transported along microtubules in a dynein-dependent manner before fusing with lysosomes (S. Kimura et al., 2008) (Fig. 3). Meanwhile, development of novel tools is always major driving force of cell biology. Kimura and colleagues developed a series of monoclonal antibodies recognizing histone H3 modifications. The thorough characterization of these highly specific antibodies provided a solid technical foundation for chromatin immunoprecipitation (ChIP) analyses, which accounts for the frequent citation of this work (H. Kimura et al., 2008). Another tool that has become essential in cell biology is the fluorescent protein. One of the critical steps in refining each fluorescent protein derived from jellyfish or coral is their monomerization. Most fluorescent proteins are oligomeric in their native state, and when fused to proteins of interest they often produce punctate patterns in mammalian cells—an artifactual outcome that has frequently gone unrecognized. Katayama and Miyawaki investigated the nature of these fluorescent puncta and demonstrated that they represent protein accumulations within lysosomes (Katayama et al., 2008).

Fig. 3

Real time observation and trajectory analysis of GFP-Atg5 and GFP-LC3 dynamics. Adapted from (S. Kimura et al., 2008).

The striking change among the highly cited papers of the most recent decade is that four of the top five papers are review articles. Hasegawa and Weisman reviewed the roles of PI5P and PI(3,5)P₂ (Hasegawa et al., 2017), while Taniguchi and Yoshida reviewed the TFE3, HSP47, and CREB3 pathways of the mammalian Golgi stress response (Taniguchi and Yoshida, 2017). Two further reviews, by Ishida and Fukuda (Ishida et al., 2016) and by Izumi (Izumi, 2021), addressed regulation and function of Rab proteins, which dictate intracellular traffic. This predominance of review articles among the most frequently cited papers likely reflects a broader trend in citation practice: although many journals formally encourage the citation of primary literature, there is a growing tendency to cite review articles in place of the multiple original papers they summarize (Miranda and Garcia-Carpintero, 2018). The sole original research article in this group was by Maryu and Aoki, who reported multiplexed fluorescence live imaging of ERK and Akt activities and the cell cycle (Fig. 4) (Maryu et al., 2016). This paper is a good example of the trend of live imaging of cell functions.

Fig. 4

Establishment of the multicolor imaging system. Shown here are the representative unmixed images of Akt-FoxO3a-KTR-EGFP, ERK-KTR-mKO, mCherry-hGem, and H2B-iRFP obtained from HeLa cells stably expressing the four reporters by the polycistronic vector. Adapted from (Maryu et al., 2016).

Prospectives

Finally, let me consider the next fifty years. Given the astonishing changes of the past half-century, prediction is hardly possible—yet at least for the coming decade, the keyword must be AI—more specifically, generative AI. All aspects of scientific publication are now affected by AI now. The hottest topics may be whether AI can be listed as an author or to what extent the authors may ask AI to write their manuscripts. However, these issues are out of my scope, and I will limit myself to considering the role of AI in the review processes.

As explicitly stated by many journals, uploading submitted manuscripts is prohibited. Nevertheless, AI should be actively utilized to assess the novelty of a given manuscript. As illustrated by the case of Mendel’s discoveries, expert reviewers cannot be expected to be familiar with every published paper. The vast knowledge base that AI possesses should be leveraged, and peer reviewers will need to acquire proficiency in formulating effective prompts for this purpose. AI may also prove useful in judging whether the Materials and Methods section provides sufficient information to reproduce the data and whether the authors’ conclusions are supported by the data presented; however, since these sections constitute the core of a manuscript, uploading it is not permissible. This limitation may be alleviated as standalone analytical tools become available, thereby reducing the burden on peer reviewers. Finally, there is the matter of judging the importance of a manuscript. Whether a paper is important or not is inherently a subjective question and is not a determination that AI should make. This should represent the most human of responses—one in which the reviewer, drawing on personal experience, returns substantive comments to the authors. Crucially, in CSF, the significance of a manuscript is not among the criteria used by editors for acceptance decisions.

The era in which scientific journals served as the primary venue for first announcing “new” discoveries and establishing the priority of their authors is undergoing transformation, driven by the growing need to secure patents before publication and by the emergence of preprint archives. What remains unshaken, however, is the guarantee of credibility afforded by peer review. CSF is published by the Japan Society for Cell Biology (JSCB), an academic society, and both its editorial board members and peer reviewers serve as unpaid volunteers. It is therefore worth emphasizing that every scientist involved in the publication process shares a common purpose: to disseminate reliable knowledge in cell biology to the world, guided solely by scientific conscience. There is no necessity to increase the number of publications for the sake of profit, nor any felt need to raise the impact factor in order to inflate manuscript counts. Science resembles a pyramid constructed by stacking a great many stones. What matters most is not the size of each stone, but whether it is sturdy enough to support the next stone placed upon it. CSF aspires to remain a journal that provides exactly such foundational stones.

Author Declaration Statements

Funding

This work was supported by the Japan Society for the Promotion of Science (JSPS) (23K19200 and 25K08445).

Conflict of Interest Statement

The author serves as a scientific adviser to CMIC Pharma Science Inc.

Data Availability Statement

Not applicable.

Author Contribution Statement

Writing—Review & Editing: MM.

Ethics Approval and Consent to Participate

Not applicable.

Patient Consent for Publication

Not applicable.

Acknowledgments

The authors acknowledge the editorial office members for critical reading.

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