Tissue BarriersPub Date : 2024-01-16DOI: 10.1080/21688370.2024.2301799
Kursad Turksen
{"title":"Tissue barriers and their impact.","authors":"Kursad Turksen","doi":"10.1080/21688370.2024.2301799","DOIUrl":"https://doi.org/10.1080/21688370.2024.2301799","url":null,"abstract":"","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139472187","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The interplay between the epithelial permeability barrier, cell migration and mitochondrial metabolism of growth factors and their inhibitors in a human endometrial carcinoma cell line.","authors":"Takumi Konno, Takayuki Kohno, Shin Kikuchi, Arisa Kura, Kimihito Saito, Tadahi Okada, Hiroshi Shimada, Yuya Yamazaki, Tomoki Sugiyama, Motoki Matsuura, Yuki Ohsaki, Tsuyoshi Saito, Takashi Kojima","doi":"10.1080/21688370.2024.2304443","DOIUrl":"https://doi.org/10.1080/21688370.2024.2304443","url":null,"abstract":"<p><p>It is known that there are abnormalities of tight junction functions, cell migration and mitochondrial metabolism in human endometriosis and endometrial carcinoma. In this study, we investigated the effects of growth factors and their inhibitors on the epithelial permeability barrier, cell migration and mitochondrial metabolism in 2D and 2.5D cultures of human endometrioid endometrial carcinoma Sawano cells. We also investigated the changes of bicellular and tricellular tight junction molecules and ciliogenesis induced by these inhibitors. The growth factors TGF-β and EGF affected the epithelial permeability barrier, cell migration and expression of bicellular and tricellular tight junction molecules in 2D and 2.5D cultures of Sawano cells. EW-7197 (a TGF-β receptor inhibitor), AG1478 (an EGFR inhibitor) and SP600125 (a JNK inhibitor) affected the epithelial permeability barrier, cell migration and mitochondrial metabolism and prevented the changes induced by TGF-β and EGF in 2D and 2.5D cultures. EW-7197 and AG1478 induced ciliogenesis in 2.5D cultures. In conclusion, TGF-β and EGF promoted the malignancy of endometrial cancer via interplay among the epithelial permeability barrier, cell migration and mitochondrial metabolism. EW-7197 and AG1478 may be useful as novel therapeutic treatments options for endometrial cancer.</p>","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139472166","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tissue BarriersPub Date : 2024-01-05DOI: 10.1080/21688370.2023.2300580
Madhuriben H Panchal, Emily J Swindle, Theresa J Pell, Wendy C Rowan, Caroline E Childs, James Thompson, Benjamin L Nicholas, Ratko Djukanovic, Victoria M Goss, Anthony D Postle, Donna E Davies, Cornelia Blume
{"title":"Membrane lipid composition of bronchial epithelial cells influences antiviral responses during rhinovirus infection.","authors":"Madhuriben H Panchal, Emily J Swindle, Theresa J Pell, Wendy C Rowan, Caroline E Childs, James Thompson, Benjamin L Nicholas, Ratko Djukanovic, Victoria M Goss, Anthony D Postle, Donna E Davies, Cornelia Blume","doi":"10.1080/21688370.2023.2300580","DOIUrl":"https://doi.org/10.1080/21688370.2023.2300580","url":null,"abstract":"<p><p>Lipids and their mediators have important regulatory functions in many cellular processes, including the innate antiviral response. The aim of this study was to compare the lipid membrane composition of in vitro differentiated primary bronchial epithelial cells (PBECs) with ex vivo bronchial brushings and to establish whether any changes in the lipid membrane composition affect antiviral defense of cells from donors without and with severe asthma. Using mass spectrometry, we showed that the lipid membrane of in vitro differentiated PBECs was deprived of polyunsaturated fatty acids (PUFAs) compared to ex vivo bronchial brushings. Supplementation of the culture medium with arachidonic acid (AA) increased the PUFA-content to more closely match the ex vivo membrane profile. Rhinovirus (RV16) infection of AA-supplemented cultures from healthy donors resulted in significantly reduced viral replication while release of inflammatory mediators and prostaglandin E2 (PGE<sub>2</sub>) was significantly increased. Indomethacin, an inhibitor of prostaglandin-endoperoxide synthases, suppressed RV16-induced PGE<sub>2</sub> release and significantly reduced CXCL-8/IL-8 release from AA-supplemented cultures indicating a link between PGE<sub>2</sub> and CXCL8/IL-8 release. In contrast, in AA-supplemented cultures from severe asthmatic donors, viral replication was enhanced whereas <i>PTGS2</i> expression and PGE<sub>2</sub> release were unchanged and CXCL8/IL-8 was significantly reduced in response to RV16 infection. While the PTGS2/COX-2 pathway is initially pro-inflammatory, its downstream products can promote symptom resolution. Thus, reduced PGE<sub>2</sub> release during an RV-induced severe asthma exacerbation may lead to prolonged symptoms and slower recovery. Our data highlight the importance of reflecting the in vivo lipid profile in in vitro cell cultures for mechanistic studies.</p>","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139098720","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"8-Bromo-cAMP attenuates human airway epithelial barrier disruption caused by titanium dioxide fine and nanoparticles.","authors":"Claire E Lee, Andjela Raduka, Nannan Gao, Aabid Hussain, Fariba Rezaee","doi":"10.1080/21688370.2023.2300579","DOIUrl":"https://doi.org/10.1080/21688370.2023.2300579","url":null,"abstract":"<p><p>Titanium dioxide fine particles (TiO<sub>2</sub>-FPs) and nanoparticles (TiO<sub>2</sub>-NPs) are the most widely used whitening pigments worldwide. Inhalation of TiO<sub>2</sub>-FPs and TiO<sub>2</sub>-NPs can be harmful as it triggers toxicity in the airway epithelial cells. The airway epithelium serves as the respiratory system's first line of defense in which airway epithelial cells are significant targets of inhaled pathogens and environmental particles. Our group previously found that TiO<sub>2</sub>-NPs lead to a disrupted barrier in the polarized airway epithelial cells. However, the effect of TiO<sub>2</sub>-FPs on the respiratory epithelial barrier has not been examined closely. In this study, we aimed to compare the effects of TiO<sub>2</sub>-FPs and TiO<sub>2</sub>-NPs on the structure and function of the airway epithelial barrier. Additionally, we hypothesized that 8-Bromo-cAMP, a cyclic adenosine monophosphate (cAMP) derivative, would alleviate the disruptive effects of both TiO<sub>2</sub>-FPs and TiO<sub>2</sub>-NPs. We observed increased epithelial membrane permeability in both TiO<sub>2</sub>-FPs and TiO<sub>2</sub>-NPs after exposure to 16HBE cells. Immunofluorescent labeling showed that both particle sizes disrupted the structural integrity of airway epithelial tight junctions and adherens junctions. TiO<sub>2</sub>-FPs had a slightly more, but insignificant impact on the epithelial barrier disruption than TiO<sub>2</sub>-NPs. Treatment with 8-Bromo-cAMP significantly attenuated the barrier-disrupting impact of both TiO<sub>2</sub>-FPs and TiO<sub>2</sub>-NPs on cell monolayers. Our study demonstrates that both TiO<sub>2</sub>-FPs and TiO<sub>2</sub>-NPs cause comparable barrier disruption and suggests a protective role for cAMP signaling. The observed effects of TiO<sub>2</sub>-FPs and TiO<sub>2</sub>-NPs provide a necessary understanding for characterizing the pathways involved in the defensive role of the cAMP pathway on TiO<sub>2</sub>-induced airway barrier disruption.</p>","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139088748","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tissue BarriersPub Date : 2024-01-02Epub Date: 2023-01-21DOI: 10.1080/21688370.2022.2163820
Filipa Leal, Scarlett Zeiringer, Ramona Jeitler, Pedro F Costa, Eva Roblegg
{"title":"A comprehensive overview of advanced dynamic <i>in vitro</i> intestinal and hepatic cell culture models.","authors":"Filipa Leal, Scarlett Zeiringer, Ramona Jeitler, Pedro F Costa, Eva Roblegg","doi":"10.1080/21688370.2022.2163820","DOIUrl":"10.1080/21688370.2022.2163820","url":null,"abstract":"<p><p>Orally administered drugs pass through the gastrointestinal tract before being absorbed in the small intestine and metabolised in the liver. To test the efficacy and toxicity of drugs, animal models are often employed; however, they are not suitable for investigating drug-tissue interactions and making reliable predictions, since the human organism differs drastically from animals in terms of absorption, distribution, metabolism and excretion of substances. Likewise, simple static <i>in vitro</i> cell culture systems currently used in preclinical drug screening often do not resemble the native characteristics of biological barriers. Dynamic models, on the other hand, provide <i>in vivo</i>-like cell phenotypes and functionalities that offer great potential for safety and efficacy prediction. Herein, current microfluidic <i>in vitro</i> intestinal and hepatic models are reviewed, namely single- and multi-tissue micro-bioreactors, which are associated with different methods of cell cultivation, <i>i.e</i>., scaffold-based <i>versus</i> scaffold-free.</p>","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10832944/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9103818","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tissue BarriersPub Date : 2024-01-02Epub Date: 2023-04-20DOI: 10.1080/21688370.2023.2203841
Santhosh Kumar Duraisamy, Ashokkumar Srinivasan, Isaac Kirubakaran Sundar
{"title":"House dust mite and Th2 cytokine-mediated epithelial barrier dysfunction attenuation by KL001 in 16-HBE cells.","authors":"Santhosh Kumar Duraisamy, Ashokkumar Srinivasan, Isaac Kirubakaran Sundar","doi":"10.1080/21688370.2023.2203841","DOIUrl":"10.1080/21688370.2023.2203841","url":null,"abstract":"<p><p>House dust mite (HDM) is a common aeroallergen that can disrupt the airway epithelial barrier leading to dysregulated immune response, resulting in allergic lung diseases such as asthma. Cryptochrome (CRY), a circadian clock gene, plays an important role in the regulation of metabolism, and immune response. It remains unclear whether stabilizing CRY using KL001 can attenuate HDM/Th2 cytokine-induced epithelial barrier dysfunction in 16-HBE cells. We evaluate the effect of KL001 (20 µM) pre-treatment (4 hrs) in HDM/Th2 cytokine (IL-4 or IL-13)-mediated change in epithelial barrier function. HDM and Th2 cytokine-induced changes in transepithelial electrical resistance (TEER) were determined by an xCELLigence real-time cell analyzer and delocalization of adherens junction complex (AJC: E-cadherin and β-catenin) and tight junction proteins (TJP: Occludin and Zonula occludens-1) by immunostaining and confocal microscopy. Finally, quantitative real-time PCR (qRT-PCR) and Western blotting were used to measure altered gene expression and protein abundance of the epithelial barrier function and core clock genes, respectively. HDM and Th2 cytokine treatment significantly decreased TEER associated with altered gene expression and protein abundance of the selected epithelial barrier function and circadian clock genes. However, pre-treatment with KL001 attenuated HDM and Th2 cytokine-induced epithelial barrier dysfunction as early as 12-24 hrs. KL001 pre-treatment showed attenuation of HDM and Th2 cytokine-induced alteration in the localization and gene expression of AJP and TJP (<i>Cdh1, Ocln,</i> and <i>Zo1</i>) and core clock genes (<i>Clock, Arntl/Bmal1, Cry1/2, Per1/2, Nr1d1/Rev-erbα,</i> and <i>Nfil3</i>). We demonstrate, for the first time, the protective role of KL001 in HDM and Th2 cytokine-mediated epithelial barrier dysfunction.</p>","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10832928/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9753958","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tissue BarriersPub Date : 2024-01-02Epub Date: 2023-02-18DOI: 10.1080/21688370.2023.2182117
Sunisa Hankan, Pawin Pongkorpsakol
{"title":"Matrix metalloproteinase-7 and claudin-7 as novel identified therapeutic targets for restoration of intestinal epithelial barrier in inflammatory bowel diseases.","authors":"Sunisa Hankan, Pawin Pongkorpsakol","doi":"10.1080/21688370.2023.2182117","DOIUrl":"10.1080/21688370.2023.2182117","url":null,"abstract":"<p><p>Intestinal tight junction disruption and mucosal immune dysregulation contribute to pathogenesis and progression of inflammatory bowel diseases (IBD). A proteolytic enzyme matrix metalloproteinase 7 (MMP-7), which is highly expressed in intestinal tissue, is implicated to IBD and other immune overactivation-associated diseases. In the issue of the Frontiers in Immunology, Ying Xiao and colleagues demonstrate that MMP-7-mediated claudin-7 degradation promotes IBD pathogenesis and disease progression. Therefore, inhibition of MMP-7 enzymatic activity can be a therapeutic strategy for the treatment of IBD.</p>","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10832911/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9315537","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Yogurt starter strains ameliorate intestinal barrier dysfunction via activating AMPK in Caco-2 cells.","authors":"Kyosuke Kobayashi, Junko Mochizuki, Fuka Yamazaki, Toshihiro Sashihara","doi":"10.1080/21688370.2023.2184157","DOIUrl":"10.1080/21688370.2023.2184157","url":null,"abstract":"<p><p>Lactic acid bacteria (LAB) are commonly used probiotics that improve human health in various aspects. We previously reported that yogurt starter strains, <i>Lactobacillus delbrueckii</i> subsp. <i>bulgaricus</i> 2038 and <i>Streptococcus thermophilus</i> 1131, potentially enhance the intestinal epithelial barrier function by inducing the expression of antimicrobial peptides in the small intestine. However, their effects on physical barrier functions remain unknown. In this study, we found that both strains ameliorated the decreased trans-epithelial resistance and the increased permeability of fluorescein isothiocyanate-dextran induced by tumor necrosis factor (TNF)-α and interferon (IFN)-γ in Caco-2 cells. We also demonstrated that LAB prevented a decrease in the expression and disassembly of tight junctions (TJs) induced by TNF-α and IFN-γ. To assess the repair activity of TJs, a calcium switch assay was performed. Both strains were found to promote the reassembly of TJs, and their activity was canceled by the inhibitor of AMP-activated protein kinase (AMPK). Moreover, these strains showed increased AMPK phosphorylation. These observations suggest that the strains ameliorated physical barrier dysfunction via the activation of AMPK. The activities preventing barrier destruction induced by TNF-α and IFN-γ were strain-dependent. Several strains containing <i>L. bulgaricus</i> 2038 and <i>S. thermophilus</i> 1131 significantly suppressed the barrier impairment, and <i>L. bulgaricus</i> 2038 showed the strongest activity among them. Our findings suggest that the intake of <i>L. bulgaricus</i> 2038 and <i>S. thermophilus</i> 1131 is a potential strategy for the prevention and repair of leaky gut.</p>","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10832913/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10859859","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Tight junction and kidney stone disease.","authors":"Papart Rungrasameviriya, Aticha Santilinon, Palita Atichartsintop, Sudarat Hadpech, Visith Thongboonkerd","doi":"10.1080/21688370.2023.2210051","DOIUrl":"10.1080/21688370.2023.2210051","url":null,"abstract":"<p><p>Defects of tight junction (TJ) are involved in many diseases related to epithelial cell functions, including kidney stone disease (KSD), which is a common disease affecting humans for over a thousand years. This review provides brief overviews of KSD and TJ, and summarizes the knowledge on crystal-induced defects of TJ in renal tubular epithelial cells (RTECs) in KSD. Calcium oxalate (CaOx) crystals, particularly COM, disrupt TJ via p38 MAPK and ROS/Akt/p38 MAPK signaling pathways, filamentous actin (F-actin) reorganization and α-tubulin relocalization. Stabilizing p38 MAPK signaling, reactive oxygen species (ROS) production, F-actin and α-tubulin by using SB239063, N-acetyl-L-cysteine (NAC), phalloidin and docetaxel, respectively, successfully prevent the COM-induced TJ disruption and malfunction. Additionally, genetic disorders of renal TJ, including mutations and single nucleotide polymorphisms (SNPs) of CLDN2, CLDN10b, CLDN14, CLDN16 and CLDN19, also affect KSD. Finally, the role of TJ as a potential target for KSD therapeutics and prevention is also discussed.</p>","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10832927/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9494007","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tissue BarriersPub Date : 2024-01-02Epub Date: 2023-03-10DOI: 10.1080/21688370.2023.2186672
Mohan Liu, Rodolfo D Vicetti Miguel, Nirk E Quispe Calla, Kristen M Aceves, Linda Fritts, Christopher J Miller, John A Moss, Marc M Baum, Thomas L Cherpes
{"title":"Genital epithelial barrier function is conserved by intravaginal rings releasing etonogestrel and ethinyl estradiol.","authors":"Mohan Liu, Rodolfo D Vicetti Miguel, Nirk E Quispe Calla, Kristen M Aceves, Linda Fritts, Christopher J Miller, John A Moss, Marc M Baum, Thomas L Cherpes","doi":"10.1080/21688370.2023.2186672","DOIUrl":"10.1080/21688370.2023.2186672","url":null,"abstract":"<p><p>The injectable progestin depot-medroxyprogesterone acetate (DMPA) is a popular contraceptive choice in sub-Saharan Africa although mouse models indicate it weakens genital epithelial integrity and barrier function and increases susceptibility to genital infection. The intravaginal ring NuvaRing® is another contraceptive option that like DMPA suppresses hypothalamic pituitary ovarian (HPO) axis function with local release of progestin (etonogestrel) and estrogen (ethinyl estradiol). As we previously reported that treating mice with DMPA and estrogen averts the loss of genital epithelial integrity and barrier function induced by DMPA alone, in the current investigation we compared genital levels of the cell-cell adhesion molecule desmoglein-1 (DSG1) and genital epithelial permeability in rhesus macaques (RM) treated with DMPA or a NuvaRing®re-sized for RM (N-IVR). While these studies demonstrated comparable inhibition of the HPO axis with DMPA or N-IVR, DMPA induced significantly lower genital DSG1 levels and greater tissue permeability to intravaginally administered low molecular mass molecules. By identifying greater compromise of genital epithelial integrity and barrier function in RM administered DMPA vs. N-IVR, our results add to the growing body of evidence that indicate DMPA weakens a fundamental mechanism of anti-pathogen host defense in the female genital tract.</p>","PeriodicalId":23469,"journal":{"name":"Tissue Barriers","volume":null,"pages":null},"PeriodicalIF":3.1,"publicationDate":"2024-01-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10832912/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9092932","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}