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Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Immunology".

Deadline for manuscript submissions: closed (30 September 2023) | Viewed by 22809

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Dr. Gabor J. Szebeni

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Guest Editor

Biological Research Centre, H-6726 Szeged, Hungary
Interests: antitumor immunity; inflammation; phenotypic screening in drug development; single cell mass cytometry; flow cytometry applications
Special Issues, Collections and Topics in MDPI journals

Dr. Attila Balog

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Guest Editor

Department of Rheumatology and Immunology, Faculty of Medicine, Albert Szent-Gyorgyi Health Centre, University of Szeged, H-6726 Szeged, Hungary
Interests: immunology; rheumatology; systemic autoimmune diseases; biomarkers; biologic and targeted therapies
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

This Special Issue is the continuation of our Special Issue “Immunophenotyping in Autoimmune Diseases and Cancer” and “Immunophenotyping in Autoimmune Diseases and Cancer 2.0”.

The mammalian immune system is a Janus-faced network of well-coordinated, highly specialized cells and biomolecules. The sensitive balance of reactive and suppressive signals maintains homeostasis in the physiological state. Under pathological conditions, however, responsiveness can escalate in autoimmune diseases or remain suppressed in cancer. In severe autoimmunity, the overwhelming immune response leads to devastating diseases, such as rheumatoid arthritis, systemic lupus erythematosus, systemic sclerosis, sclerosis multiplex, etc. Conversely, immune cells, e.g., professional antigen-presenting cells and cytotoxic T cells, are not able to execute their physiological function in cancer.

Recent progress in fluorescence flow cytometry and mass cytometry has contributed to a high-dimensional resolution of the complex immunophenotype, both in autoimmune diseases and cancer. We request that authors publish their latest achievements associated with the perturbance of the regulation of immune activation and the discovery of rare subpopulations of both innate and adaptive immune players in autoimmune diseases or cancer. This Special Issue will publish works presenting the description of different cellular subtypes and the identification of novel key molecular factors and biomarkers. The submission of mainly research articles is expected. Due to the recent developments in high-content, multilevel profiling technologies, review articles from pioneer scientists will also be considered.

Dr. Gabor J. Szebeni
Dr. Attila Balog
Guest Editors

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Keywords

immunophenotyping
immune regulation
multiparameter cytometry
immuno-oncology
anti-tumor immunity
autoimmunity
cancer immunology
protein–protein interactions
structure/function relationships
sulfur amino acids

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Published Papers (10 papers)

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Editorial

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5 pages, 201 KiB

Open AccessEditorial

Closing Editorial: Immunophenotyping in Autoimmune Diseases and Cancer 3.0

by Gábor J. Szebeni and Attila Balog

Int. J. Mol. Sci. 2024, 25(12), 6311; https://doi.org/10.3390/ijms25126311 - 7 Jun 2024

Viewed by 544

Abstract

The mammalian immune system is a Janus-faced network of well-coordinated highly specialized cells and biomolecules [...] Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

Research

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21 pages, 3135 KiB

Open AccessArticle

Lectin-Based Immunophenotyping and Whole Proteomic Profiling of CT-26 Colon Carcinoma Murine Model

by Anna Faragó, Ágnes Zvara, László Tiszlavicz, Éva Hunyadi-Gulyás, Zsuzsanna Darula, Zoltán Hegedűs, Enikő Szabó, Sára Eszter Surguta, József Tóvári, László G. Puskás and Gábor J. Szebeni

Int. J. Mol. Sci. 2024, 25(7), 4022; https://doi.org/10.3390/ijms25074022 - 4 Apr 2024

Viewed by 1697

Abstract

A murine colorectal carcinoma (CRC) model was established. CT26 colon carcinoma cells were injected into BALB/c mice’s spleen to study the primary tumor and the mechanisms of cell spread of colon cancer to the liver. The CRC was verified by the immunohistochemistry of Pan Cytokeratin and Vimentin expression. Immunophenotyping of leukocytes isolated from CRC-bearing BALB/c mice or healthy controls, such as CD19+ B cells, CD11+ myeloid cells, and CD3+ T cells, was carried out using fluorochrome-labeled lectins. The binding of six lectins to white blood cells, such as galectin-1 (Gal1), siglec-1 (Sig1), Sambucus nigra lectin (SNA), Aleuria aurantia lectin (AAL), Phytolacca americana lectin (PWM), and galectin-3 (Gal3), was assayed. Flow cytometric analysis of the splenocytes revealed the increased binding of SNA, and AAL to CD3 + T cells and CD11b myeloid cells; and increased siglec-1 and AAL binding to CD19 B cells of the tumor-bearing mice. The whole proteomic analysis of the established CRC-bearing liver and spleen versus healthy tissues identified differentially expressed proteins, characteristic of the primary or secondary CRC tissues. KEGG Gene Ontology bioinformatic analysis delineated the established murine CRC characteristic protein interaction networks, biological pathways, and cellular processes involved in CRC. Galectin-1 and S100A4 were identified as upregulated proteins in the primary and secondary CT26 tumor tissues, and these were previously reported to contribute to the poor prognosis of CRC patients. Modelling the development of liver colonization of CRC by the injection of CT26 cells into the spleen may facilitate the understanding of carcinogenesis in human CRC and contribute to the development of novel therapeutic strategies. Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

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13 pages, 3169 KiB

Open AccessArticle

Different Expression Pattern of G Protein-Coupled Estrogen Receptor GPER1 in Esophageal Squamous Cell Carcinoma and Adenocarcinoma

by Jingshi Liu, Yongdong Niu, Bin Zhang, Qisi Sun, Haiyi Li, Lu Bai and Zhongjing Su

Int. J. Mol. Sci. 2023, 24(18), 14055; https://doi.org/10.3390/ijms241814055 - 13 Sep 2023

Cited by 1 | Viewed by 1117

Abstract

Esophageal carcinoma is a male-dominant malignancy worldwide, and esophageal adenocarcinoma (EAC) shows more significant sex bias than esophageal squamous cell carcinoma (ESCC) in morbidity and mortality. The G protein-coupled estrogen receptor 1 (GPER1) is involved in several sex-related cancers; however, its expression level in esophageal carcinoma has been poorly investigated and its role is not precisely defined, depending on histological types. In the present study, the mRNA levels of GPER1 in esophageal carcinoma were collected from GEPIA and Oncomine databases for meta-analyses. The protein expression levels of GPER1 were detected by immunohistochemistry in the tissue microarray of EAC and ESCC. The GPER1 selective agonist G1, antagonist G15, and siRNA were applied in vitro to investigate their impacts on esophageal cell lines. Analysis of the RNA levels from the databases showed a decreased expression of GPER1 in overall esophageal carcinoma, and low expression levels of GPER1 were found to be associated with low survival of tumor patients. However, in the subgroup of EAC and its precancerous lesion, Barrett’s esophagus, overexpression of GPER1 RNA was increased when compared with the normal tissues. The average staining scores of GPER1 protein in the tissue microarray of EAC were significantly higher than normal esophageal samples, and the rate of positive staining increased with the grade of poor tumor differentiation. The scores of GPER1 protein in ESCC tissues were lower than those in the normal tissues. The results from cell line experiments in vitro showed that the GPER1 agonist G1 inhibited proliferation and promoted apoptosis of ESCC cells EC109 with positive expression of GPER1. G1 had no obvious effect on normal esophageal NE2 cells with weak expression of GPER1. In addition, GPER1 RNA knockdown and application of antagonist G15 reversed the effects of G1 on EC109. The results of this study indicate that the expression levels of GPER1 are higher in EAC than in ESCC, which might be correlated with the dimorphic estrogen signaling pathway in different types of esophageal carcinoma. Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

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24 pages, 22647 KiB

Open AccessArticle

A Novel Oncogenic Role of FDX1 in Human Melanoma Related to PD-L1 Immune Checkpoint

by Huijiao Lu, Jiahua Liang, Xue He, Huabin Ye, Chuangdong Ruan, Hongwei Shao, Rongxin Zhang and Yan Li

Int. J. Mol. Sci. 2023, 24(11), 9182; https://doi.org/10.3390/ijms24119182 - 24 May 2023

Cited by 2 | Viewed by 2220

Abstract

The aim of this study was to evaluate the association between Ferredoxin 1 (FDX1) expression and the prognostic survival of tumor patients and predict the efficacy of immunotherapy response to antitumor drug sensitivity. FDX1 plays an oncogenic role in thirty-three types of tumors, based on TCGA and GEO databases, and further experimental validation in vitro was provided through multiple cell lines. FDX1 was expressed highly in multiple types of cancer and differently linked to the survival prognosis of tumorous patients. A high phosphorylation level was correlated with the FDX1 site of S177 in lung cancer. FDX1 exhibited a significant association with infiltrated cancer-associated fibroblasts and CD8⁺ T cells. Moreover, FDX1 demonstrated correlations with immune and molecular subtypes, as well as functional enrichments in GO/KEGG pathways. Additionally, FDX1 displayed relationships with the tumor mutational burden (TMB), microsatellite instability (MSI), DNA methylation, and RNA and DNA synthesis (RNAss/DNAss) within the tumor microenvironment. Notably, FDX1 exhibited a strong connection with immune checkpoint genes in the co-expression network. The validity of these findings was further confirmed through Western blotting, RT-qPCR, and flow cytometry experiments conducted on WM115 and A375 tumor cells. Elevated FDX1 expression has been linked to the enhanced effectiveness of PD-L1 blockade immunotherapy in melanoma, as observed in the GSE22155 and GSE172320 cohorts. Autodocking simulations have suggested that FDX1 may influence drug resistance by affecting the binding sites of antitumor drugs. Collectively, these findings propose that FDX1 could serve as a novel and valuable biomarker and represent an immunotherapeutic target for augmenting immune responses in various human cancers when used in combination with immune checkpoint inhibitors. Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

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16 pages, 3918 KiB

Open AccessArticle

Identification of a Novel Linear B-Cell Epitope of HbpA Protein from Glaesserella parasuis Using Monoclonal Antibody

by Geyan Liu, Kang Wang, Zhen Yang, Xiaoyu Tang, Yung-Fu Chang, Ke Dai, Xinwei Tang, Bangdi Hu, Yiwen Zhang, Sanjie Cao, Xiaobo Huang, Qigui Yan, Rui Wu, Qin Zhao, Senyan Du, Xintian Wen and Yiping Wen

Int. J. Mol. Sci. 2023, 24(10), 8638; https://doi.org/10.3390/ijms24108638 - 12 May 2023

Cited by 2 | Viewed by 1561

Abstract

Glaesserella parasuis (G. parasuis.) is the etiological pathogen of Glässer’s disease, which causes high economic losses to the pig industry. The heme-binding protein A precursor (HbpA) was a putative virulence-associated factor proposed to be potential subunit vaccine candidate in G. parasuis. In this study, three monoclonal antibodies (mAb) 5D11, 2H81, and 4F2 against recombinant HbpA (rHbpA) of G. parasuis SH0165 (serotype 5) were generated by fusing SP2/0-Ag14 murine myeloma cells and spleen cells from BALB/c mice immunized with the rHbpA. Indirect enzyme-linked immunosorbent assay (ELISA) and indirect immunofluorescence assay (IFA) demonstrated that the antibody designated 5D11 showed a strong binding affinity with the HbpA protein and was chosen for subsequent experiments. The subtypes of the 5D11 were IgG1/κ chains. Western blot analysis showed that mAb 5D11 could react with all 15 serotype reference strains of G. parasuis. None of the other bacteria tested reacted with 5D11. In addition, a linear B-cell epitope recognized by 5D11 was identified by serial truncations of HbpA protein and then a series of truncated peptides were synthesized to define the minimal region that was required for mAb 5D11 binding. The 5D11 epitope was located on amino acids 324-LPQYEFNLEKAKALLA-339 by testing the 5D11 monoclonal for reactivity with 14 truncations. The minimal epitope 325-PQYEFNLEKAKALLA-339 (designated EP-5D11) was pinpointed by testing the mAb 5D11 for reactivity with a series of synthetic peptides of this region. The epitope was highly conserved among G. parasuis strains, confirmed by alignment analysis. These results indicated that mAb 5D11 and EP-5D11 might potentially be used to develop serological diagnostic tools for G. parasuis. Three-dimensional structural analysis revealed that amino acids of EP-5D11 were in close proximity and may be exposed on the surface of the HbpA protein. Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

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14 pages, 2772 KiB

Open AccessCommunication

T-Cells Subsets in Castleman Disease: Analysis of 28 Cases Including Unicentric, Multicentric and HHV8-Related Clinical Forms

by Sara Fraticelli, Marco Lucioni, Giuseppe Neri, Deborah Marchiori, Caterina Cristinelli, Michele Merli, Rodolfo Monaco, Tiziana Borra, Antonio Lazzaro, Silvia Uccella, Luca Arcaini and Marco Paulli

Int. J. Mol. Sci. 2023, 24(9), 7813; https://doi.org/10.3390/ijms24097813 - 25 Apr 2023

Cited by 2 | Viewed by 2146

Abstract

Castleman disease (CD) is a rare lymphoproliferative disorder that includes various clinico-pathological subtypes. According to clinical course, CD is divided into unicentric CD (UCD) and multicentric CD (MCD). MCD is further distinguished based on the etiological driver in herpes virus-8-related MCD (that can occur in the setting of HIV); in MCD associated with POEMS syndrome (polyneuropathy, organomegaly, endocrinopathy, monoclonal protein, and skin changes); and idiopathic MCD (iMCD). The latter can also be divided in iMCD-TAFRO (thrombocytopenia, anasarca, fever, myelofibrosis, organomegaly) and iMCD not otherwise specified. To date, CD pathogenesis is still uncertain, but CD may represent the histological and clinical result of heterogeneous pathomechanisms. Transcriptome investigations in CD lymph nodes have documented the expression and up-regulation of different cytokines; furthermore, few recent studies have shown alterations of different T-cell subsets in CD patients, suggesting a possible role of the nodal microenvironment in CD development. On this basis, our study aimed to investigate the distribution of T-cell subsets in the clinico-pathological spectrum of CD. We evaluated the CD4/CD8 ratio and the number of T-regulatory (T-reg) FOXP3+ cells in 28 CD cases. In total, 32% of cases showed a decreased CD4/CD8 ratio due to increased CD8+ T-cells, including both UCD, iMCD, and HHV8+ MCD cases. The T-reg subset analysis revealed a statistically significant (p < 0.0001) lower mean number of FOXP3+ T-reg cells in CD cases when compared with non-specific reactive lymph nodes. We did not find statistically significant differences in T-reg numbers between the different CD subtypes. These findings may suggest that alterations in T-cell subpopulations that can lead to disruption of immune system control may contribute to the numerous changes in different cellular compartments that characterize CD. Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

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18 pages, 3340 KiB

Open AccessArticle

PTGES Expression Is Associated with Metabolic and Immune Reprogramming in Pancreatic Ductal Adenocarcinoma

by Divya Murthy and Kuldeep S. Attri

Int. J. Mol. Sci. 2023, 24(8), 7304; https://doi.org/10.3390/ijms24087304 - 15 Apr 2023

Cited by 1 | Viewed by 2307

Abstract

Metabolic reprogramming is an established hallmark of multiple cancers, including pancreatic cancer. Dysregulated metabolism is utilized by cancer cells for tumor progression, metastasis, immune microenvironment remodeling, and therapeutic resistance. Prostaglandin metabolites have been shown to be critical for inflammation and tumorigenesis. While the functional role of prostaglandin E2 metabolite has been extensively studied, there is a limited understanding of the PTGES enzyme in pancreatic cancer. Here, we investigated the relationship between expression of prostaglandin E synthase (PTGES) isoforms and the pathogenesis and regulation of pancreatic cancer. Our analysis identified higher expression of PTGES in pancreatic tumors compared to normal pancreatic tissues, suggesting an oncogenic function. Only PTGES1 expression was significantly correlated with worse prognosis of pancreatic cancer patients. Further, utilizing cancer genome atlas data, PTGES was found to be positively correlated with epithelial-mesenchymal transition, metabolic pathways, mucin oncogenic proteins, and immune pathways in cancer cells. PTGES expression was also correlated with higher mutational burden in key driver genes, such as TP53 and KRAS. Furthermore, our analysis indicated that the oncogenic pathway controlled by PTGES1 could be regulated via DNA methylation-dependent epigenetic mechanisms. Notably, the glycolysis pathway was positively correlated with PTGES and may fuel cancer cell growth. PTGES expression was also associated with downregulation of the MHC pathway and negatively correlated with CD8+ T cell activation markers. In summary, our study established an association of PTGES expression with pancreatic cancer metabolism and the immune microenvironment. Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

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21 pages, 4539 KiB

Open AccessArticle

Single-Cell Sequencing-Based Validation of T Cell-Associated Diagnostic Model Genes and Drug Response in Crohn’s Disease

by Zhujiang Dai, Jie Zhang, Weimin Xu, Peng Du, Zhongchuan Wang and Yun Liu

Int. J. Mol. Sci. 2023, 24(7), 6054; https://doi.org/10.3390/ijms24076054 - 23 Mar 2023

Cited by 4 | Viewed by 3140

Abstract

Crohn’s disease is a highly heterogeneous autoimmune disease with a unique inflammatory phenotype of T cells at the lesion site. We aim to further explore the diagnosis of Crohn’s disease and drug prediction of T cell marker gene expression. We obtained single-cell expression profile data from 22 CDs or normal samples and performed cell annotation and cellular communication analysis. Through the intersection of T cell marker genes, differential genes, and WGCNA results, we identified T cell-specific key genes and their immune landscapes and potential pathogenesis, and validated them across multiple datasets and patient tissue samples. We also explored the differentiation characteristics of genes by pseudo-temporal analysis and assessed their diagnostic performance and drug sensitivity by molecular docking. Finally, we extended this study to the prognosis of IBD-associated colon cancer. TNF-centered 5-gene diagnostic model not only has excellent diagnostic efficacy, but is also closely associated with KRAS, P53, and IL6/JAK/STAT3 pathways and physiological processes, such as EMT, coagulation, and apoptosis. In addition, this diagnostic model may have potential synergistic immunotherapeutic effects, with positive correlations with immune checkpoints such as CTLA4, CD86, PDCD1LG2, and CD40. Molecular docking demonstrated that BIRC3 and ANXA1 have strong binding properties to Azathioprine and Glucoocorticoid. Furthermore, the 5-gene model may suggest antagonism to IFX and prognosis for colon cancer associated with inflammatory bowel disease. Single-cell sequencing targeting T cell-related features in patients with Crohn’s disease may aid in new diagnostic decisions, as well as the initial exploration of high-potential therapies. Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

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Review

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20 pages, 2629 KiB

Open AccessReview

CircRNAs: A Promising Star for Treatment and Prognosis in Oral Squamous Cell Carcinoma

by Mengyi Zhu, Daoyang Chen, Chuangdong Ruan, Penghui Yang, Jinrong Zhu, Rongxin Zhang and Yan Li

Int. J. Mol. Sci. 2023, 24(18), 14194; https://doi.org/10.3390/ijms241814194 - 17 Sep 2023

Cited by 1 | Viewed by 1454

Abstract

CircRNAs are a class of endogenous long non-coding RNAs with a single-stranded circular structure. Most circRNAs are relatively stable, highly conserved, and specifically expressed in tissue during the cell and developmental stages. Many circRNAs have been discovered in OSCC. OSCC is one of the most severe and frequent forms of head and neck cancer today, with a poor prognosis and low overall survival rate. Due to its prevalence, OSCC is a global health concern, characterized by genetic and epigenomic changes. However, the mechanism remains vague. With the advancement of biotechnology, a large number of circRNAs have been discovered in mammalian cells. CircRNAs are dysregulated in OSCC tissues and thus associated with the clinicopathological characteristics and prognosis of OSCC patients. Research studies have demonstrated that circRNAs can serve as biomarkers for OSCC diagnosis and treatment. Here, we summarized the properties, functions, and biogenesis of circRNAs, focusing on the progress of current research on circRNAs in OSCC. Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

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13 pages, 1786 KiB

Open AccessReview

Characterizing the Interplay of Lymphocytes in Graves’ Disease

by Mackenzie Hansen, Abigail Cheever, K. Scott Weber and Kim L. O’Neill

Int. J. Mol. Sci. 2023, 24(7), 6835; https://doi.org/10.3390/ijms24076835 - 6 Apr 2023

Cited by 4 | Viewed by 5549

Abstract

Graves’ disease (GD) is a thyroid-specific autoimmune disease with a high prevalence worldwide. The disease is primarily mediated by B cells, which produce autoantibodies against the thyroid-stimulating hormone receptor (TSHR), chronically stimulating it and leading to high levels of thyroid hormones in the body. Interest in characterizing the immune response in GD has motivated many phenotyping studies. The immunophenotype of the cells involved and the interplay between them and their secreted factors are crucial to understanding disease progression and future treatment options. T cell populations are markedly distinct, including increased levels of Th17 and follicular helper T cells (Tfh), while Treg cells appear to be impaired. Some B cells subsets are autoreactive, and anti-TSHR antibodies are the key disease-causing outcome of this interplay. Though some consensus across phenotyping studies will be discussed here, there are also complexities that are yet to be resolved. A better understanding of the immunophenotype of Graves’ disease can lead to improved treatment strategies and novel drug targets. Full article

(This article belongs to the Special Issue Immunophenotyping in Autoimmune Diseases and Cancer, 3rd Edition)

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