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Article ; Online: Spatiotemporally specific roles of TLR4, TNF, and IL-17A in murine endotoxin-induced inflammation inferred from analysis of dynamic networks.

Zamora, Ruben / Chavan, Sangeeta / Zanos, Theodoros / Simmons, Richard L / Billiar, Timothy R / Vodovotz, Yoram

2021 Volume 27, Issue 1, Page(s) 65

Abstract: ... memory T cells-in the spleen and blood.: Conclusions: We have derived novel, systems-level insights ...

Abstract	Background: Bacterial lipopolysaccharide (LPS) induces a multi-organ, Toll-like receptor 4 (TLR4)-dependent acute inflammatory response. Methods: Using network analysis, we defined the spatiotemporal dynamics of 20, LPS-induced, protein-level inflammatory mediators over 0-48 h in the heart, gut, lung, liver, spleen, kidney, and systemic circulation, in both C57BL/6 (wild-type) and TLR4-null mice. Results: Dynamic Network Analysis suggested that inflammation in the heart is most dependent on TLR4, followed by the liver, kidney, plasma, gut, lung, and spleen, and raises the possibility of non-TLR4 LPS signaling pathways at defined time points in the gut, lung, and spleen. Insights from computational analyses suggest an early role for TLR4-dependent tumor necrosis factor in coordinating multiple signaling pathways in the heart, giving way to later interleukin-17A-possibly derived from pathogenic Th17 cells and effector/memory T cells-in the spleen and blood. Conclusions: We have derived novel, systems-level insights regarding the spatiotemporal evolution acute inflammation.
MeSH term(s)	Animals ; Biomarkers ; Computational Biology/methods ; Cytokines/metabolism ; Disease Models, Animal ; Disease Susceptibility ; Endotoxins/adverse effects ; Inflammation/etiology ; Inflammation/metabolism ; Inflammation/pathology ; Inflammation Mediators/metabolism ; Interleukin-17/genetics ; Interleukin-17/metabolism ; Male ; Mice ; Mice, Transgenic ; Toll-Like Receptor 4/genetics ; Toll-Like Receptor 4/metabolism ; Tumor Necrosis Factor-alpha/genetics ; Tumor Necrosis Factor-alpha/metabolism
Chemical Substances	Biomarkers ; Cytokines ; Endotoxins ; Inflammation Mediators ; Interleukin-17 ; Toll-Like Receptor 4 ; Tumor Necrosis Factor-alpha
Language	English
Publishing date	2021-06-24
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1283676-x
ISSN	1528-3658 ; 1076-1551
ISSN (online)	1528-3658
ISSN	1076-1551
DOI	10.1186/s10020-021-00333-z
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Article ; Online: LONGITUDINAL ANALYSIS OF TRANSCRIPTOMIC SUBTYPES IN TRAUMA PATIENTS.

Chen, Tianmeng / Wei, Yue / Vodovotz, Yoram / Chen, Wei / Billiar, Timothy R

Shock (Augusta, Ga.)

2022 Volume 58, Issue 1, Page(s) 34–37

Abstract: Abstract: Objective: We previously identified two transcriptomic subtypes (Signature Groups: SG1 vs. SG2) in trauma patients at 12 hours postinjury, with SG1 associated with worse outcomes. In this study, we aimed to further characterize the changes in ... ...

Abstract	Abstract: Objective: We previously identified two transcriptomic subtypes (Signature Groups: SG1 vs. SG2) in trauma patients at 12 hours postinjury, with SG1 associated with worse outcomes. In this study, we aimed to further characterize the changes in SG subtype categorization of trauma patients over time after injury and define the corresponding association with outcomes based on the timing of the subtype designation. Methods and Results: This study was a secondary analysis of published data of whole-blood leukocyte transcriptomics, a longitudinal data from 167 severe blunt trauma patients. We assigned trauma patients to SG1 or SG2 subtype for time points between 12 hours and 28 days, inclusive, postinjury and characterized their longitudinal outcomes. SG1 assignment, regardless of time point, was associated consistently with slower recovery. Further analysis revealed that additional prognostic information could be obtained by assessing SG subtype at both 12 hours and 1 day. Conclusions: This study provides a proof of concept that immune status can worsen after admission and highlights the benefit of longitudinally monitoring SG subtypes in trauma patients.
MeSH term(s)	Humans ; Prognosis ; Transcriptome/genetics ; Wounds, Nonpenetrating
Language	English
Publishing date	2022-07-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1185432-7
ISSN	1540-0514 ; 1073-2322
ISSN (online)	1540-0514
ISSN	1073-2322
DOI	10.1097/SHK.0000000000001958
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Article ; Online: Intraperitoneal injection of class A TLR9 agonist enhances anti-PD-1 immunotherapy in colorectal peritoneal metastases.

Jiang, Ting / Zhang, Hongji / Li, Yiming / Jayakumar, Preethi / Liao, Hong / Huang, Hai / Billiar, Timothy R / Deng, Meihong

JCI insight

2022 Volume 7, Issue 20

Abstract: ... reduced the numbers of Tim4+ PRMs and enhanced CD8+ T cell antitumor immunity. Mechanistically, treatment ...

Abstract	Peritoneal metastases are associated with a low response rate to immune checkpoint blockade (ICB) therapy. The numbers of peritoneal resident macrophages (PRMs) are reversely correlated with the response rate to ICB therapy. We have previously shown that TLR9 in fibroblastic reticular cells (FRCs) plays a critical role in regulating peritoneal immune cell recruitment. However, the role of TLR9 in FRCs in regulating PRMs is unclear. Here, we demonstrated that the class A TLR9 agonist, ODN1585, markedly enhanced the efficacy of anti-PD-1 therapy in mouse models of colorectal peritoneal metastases. ODN1585 injected i.p. reduced the numbers of Tim4+ PRMs and enhanced CD8+ T cell antitumor immunity. Mechanistically, treatment of ODN1585 suppressed the expression of genes required for retinoid metabolism in FRCs, and this was associated with reduced expression of the PRM lineage-defining transcription factor GATA6. Selective deletion of TLR9 in FRCs diminished the benefit of ODN1585 in anti-PD-1 therapy in reducing peritoneal metastases. The crosstalk between PRMs and FRCs may be utilized to develop new strategies to improve the efficacy of ICB therapy for peritoneal metastases.
MeSH term(s)	Mice ; Animals ; Toll-Like Receptor 9/metabolism ; Injections, Intraperitoneal ; GATA6 Transcription Factor ; Immune Checkpoint Inhibitors/pharmacology ; Immune Checkpoint Inhibitors/therapeutic use ; Peritoneal Neoplasms/drug therapy ; Immunotherapy ; Adjuvants, Immunologic ; Colorectal Neoplasms/drug therapy ; Retinoids
Chemical Substances	Toll-Like Receptor 9 ; GATA6 Transcription Factor ; Immune Checkpoint Inhibitors ; Adjuvants, Immunologic ; Retinoids ; Tlr9 protein, mouse
Language	English
Publishing date	2022-10-24
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.160063
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Article ; Online: The independent prognostic value of global epigenetic alterations: An analysis of single-cell ATAC-seq of circulating leukocytes from trauma patients followed by validation in whole blood leukocyte transcriptomes across three etiologies of critical illness.

Chen, Tianmeng / Conroy, Julia / Wang, Xinjun / Situ, Michelle / Namas, Rami A / Vodovotz, Yoram / Chen, Wei / Singh, Harinder / Billiar, Timothy R

EBioMedicine

2022 Volume 76, Page(s) 103860

Abstract: ... 1R35GM127027-01 (T.B.). ...

Abstract	Background: While bulk and single cell transcriptomic patterns in circulating leukocytes from trauma patients have been reported, how these relate to changes in open chromatin patterns remain unstudied. Here, we investigated whether single-cell ATAC-seq would provide further resolution of transcriptomic patterns that align with patient outcomes. Methods: We performed scATAC-seq on peripheral blood mononuclear cells from four trauma patients at <4 h, 24 h, 72 h post-injury and four matched healthy controls, and extracted the features associated with the global epigenetic alterations. Three large-scale bulk transcriptomic datasets from trauma, burn and sepsis patients were used to validate the scATAC-seq derived signature, explore patient epigenetic heterogeneity (Epigenetic Groups: EG_hi vs. EG_lo), and associate patterns with clinical outcomes in critical illness. Findings: Patient subsets with gene expression patterns in blood leukocytes representative of a high global epigenetic signature (EG_hi) had worse outcomes across three etiologies of critical illness. EG_hi designation contributed independent of the known immune leukocyte transcriptomic responses to patient prognosis (Trauma: HR=0.62 [95% CI: 0.43-0.89, event set as recovery], p=0.01, n=167; Burns: HR=4.35 [95% CI: 0.816-23.2, event set as death], p=0.085, n=121; Sepsis: HR=1.60 [95% CI: 1.10-2.33, event set as death], p=0.013, n=479; Cox proportional hazards regression). Interpretation: The inclusion of gene expression patterns that associate with global epigenetic changes in circulating leukocytes improves the resolution of transcriptome-based patient classification in acute critical illnesses. Early detection of both the global epigenetic signature and the known immune transcriptomic patterns associates with the worse prognosis in trauma, burns and sepsis. Funding: This project was supported by an R35 grant from National Institutes of Health: 1R35GM127027-01 (T.B.).
MeSH term(s)	Chromatin Immunoprecipitation Sequencing ; Critical Illness ; Epigenesis, Genetic ; Humans ; Leukocytes ; Leukocytes, Mononuclear ; Prognosis ; Transcriptome
Language	English
Publishing date	2022-02-03
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2851331-9
ISSN	2352-3964
ISSN (online)	2352-3964
DOI	10.1016/j.ebiom.2022.103860
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Article ; Online: Protective/reparative cytokines are suppressed at high injury severity in human trauma.

Cai, Jinman / McKinley, Todd / Billiar, Isabel / Zenati, Mazen S / Gaski, Greg / Vodovotz, Yoram / Gruen, Danielle S / Billiar, Timothy R / Namas, Rami A

Trauma surgery & acute care open

2021 Volume 6, Issue 1, Page(s) e000619

Abstract: Background: Trauma elicits a complex inflammatory response that, among multiple presenting factors, is greatly impacted by the magnitude of injury severity. Herein, we compared the changes in circulating levels of mediators with known proinflammatory ... ...

Abstract	Background: Trauma elicits a complex inflammatory response that, among multiple presenting factors, is greatly impacted by the magnitude of injury severity. Herein, we compared the changes in circulating levels of mediators with known proinflammatory roles to those with known protective/reparative actions as a function of injury severity in injured humans. Methods: Clinical and biobank data were obtained from 472 (trauma database-1 (TD-1), University of Pittsburgh) and 89 (trauma database-2 (TD-2), Indiana University) trauma patients admitted to the intensive care unit (ICU) and who survived to discharge. Injury severity was estimated based on the Injury Severity Score (ISS), and this was used as both a continuous variable and for the purpose of grouping patients into severity-based cohorts. Samples within the first 24 hours were obtained from all patients and then daily up to day 7 postinjury in TD-1. Sixteen cytokines were assayed using Luminex and were analyzed using two-way analysis of variance (p<0.05). Results: Patients with higher ISSs had longer ICU and hospital stays, days on mechanical ventilation and higher rates of nosocomial infection when compared with the mild and moderate groups. Time course analysis and correlations with ISS showed that 11 inflammatory mediators correlated positively with injury severity, consistent with previous reports. However, five mediators (interleukin (IL)-9, IL-21, IL-22, IL-23 and IL-17E/25) were suppressed in patients with high ISS and inversely correlated with ISS. Discussion: These findings suggest that severe injury is associated with a suppression of a subset of cytokines known to be involved in tissue protection and regeneration (IL-9, IL-22 and IL-17E/25) and lymphocyte differentiation (IL-21 and IL-23), which in turn correlates with adverse clinical outcomes. Thus, patterns of proinflammatory versus protective/reparative mediators diverge with increasing ISS.
Language	English
Publishing date	2021-03-02
Publishing country	England
Document type	Journal Article
ISSN	2397-5776
ISSN (online)	2397-5776
DOI	10.1136/tsaco-2020-000619
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Article ; Online: Inferring Tissue-Specific, TLR4-Dependent Type 17 Immune Interactions in Experimental Trauma/Hemorrhagic Shock and Resuscitation Using Computational Modeling.

Shah, Ashti M / Zamora, Ruben / Korff, Sebastian / Barclay, Derek / Yin, Jinling / El-Dehaibi, Fayten / Billiar, Timothy R / Vodovotz, Yoram

Frontiers in immunology

2022 Volume 13, Page(s) 908618

Abstract: Trauma/hemorrhagic shock followed by resuscitation (T/HS-R) results in multi-system inflammation ... to Toll-like Receptor 4 (TLR4). We carried out experimental T/HS-R (pseudo-fracture plus 2 h of shock followed by 0-22 h ...

Abstract	Trauma/hemorrhagic shock followed by resuscitation (T/HS-R) results in multi-system inflammation and organ dysfunction, in part driven by binding of damage-associated molecular pattern molecules to Toll-like Receptor 4 (TLR4). We carried out experimental T/HS-R (pseudo-fracture plus 2 h of shock followed by 0-22 h of resuscitation) in C57BL/6 (wild type [WT]) and TLR4-null (TLR4
MeSH term(s)	Animals ; Computer Simulation ; Granulocyte-Macrophage Colony-Stimulating Factor ; Inflammation Mediators ; Interleukin-10 ; Interleukin-17 ; Mice ; Mice, Inbred C57BL ; Shock, Hemorrhagic ; Signal Transduction ; Toll-Like Receptor 4/genetics ; Toll-Like Receptor 4/metabolism
Chemical Substances	Inflammation Mediators ; Interleukin-17 ; Tlr4 protein, mouse ; Toll-Like Receptor 4 ; Interleukin-10 (130068-27-8) ; Granulocyte-Macrophage Colony-Stimulating Factor (83869-56-1)
Language	English
Publishing date	2022-05-19
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.908618
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Article: RNA Editing, ADAR1, and the Innate Immune Response.

Wang, Qingde / Li, Xiaoni / Qi, Ruofan / Billiar, Timothy

Genes

2017 Volume 8, Issue 1

Abstract: RNA editing, particularly A-to-I RNA editing, has been shown to play an essential role in mammalian embryonic development and tissue homeostasis, and is implicated in the pathogenesis of many diseases including skin pigmentation disorder, autoimmune and ... ...

Abstract	RNA editing, particularly A-to-I RNA editing, has been shown to play an essential role in mammalian embryonic development and tissue homeostasis, and is implicated in the pathogenesis of many diseases including skin pigmentation disorder, autoimmune and inflammatory tissue injury, neuron degeneration, and various malignancies. A-to-I RNA editing is carried out by a small group of enzymes, the adenosine deaminase acting on RNAs (ADARs). Only three members of this protein family, ADAR1-3, exist in mammalian cells. ADAR3 is a catalytically null enzyme and the most significant function of ADAR2 was found to be in editing on the neuron receptor GluR-B mRNA. ADAR1, however, has been shown to play more significant roles in biological and pathological conditions. Although there remains much that is not known about how ADAR1 regulates cellular function, recent findings point to regulation of the innate immune response as an important function of ADAR1. Without appropriate RNA editing by ADAR1, endogenous RNA transcripts stimulate cytosolic RNA sensing receptors and therefore activate the IFN-inducing signaling pathways. Overactivation of innate immune pathways can lead to tissue injury and dysfunction. However, obvious gaps in our knowledge persist as to how ADAR1 regulates innate immune responses through RNA editing. Here, we review critical findings from ADAR1 mechanistic studies focusing on its regulatory function in innate immune responses and identify some of the important unanswered questions in the field.
Language	English
Publishing date	2017-01-18
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2527218-4
ISSN	2073-4425
ISSN	2073-4425
DOI	10.3390/genes8010041
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Article ; Online: Transcriptomic and Proteomic Characterization of the Immune Response to Elective Spinal Reconstructive Surgery: Impact of Aging and Comparison with Traumatic Injury Response.

Bonaroti, Jillian W / Ozel, Mehves / Chen, Tianmeng / Darby, Jennifer L / Sun, Xuejing / Moheimani, Hamed / Reitz, Katherine M / Kar, Upendra K / Zuckerbraun, Brian S / Das, Jishnu / Okonkwo, David O / Billiar, Timothy R

Journal of the American College of Surgeons

2023 Volume 238, Issue 5, Page(s) 924–941

Abstract: Background: Major surgery triggers trauma-like stress responses linked to age, surgery duration, and blood loss, resembling polytrauma. This similarity suggests elective surgery as a surrogate model for studying polytrauma immune responses. We ... ...

Abstract	Background: Major surgery triggers trauma-like stress responses linked to age, surgery duration, and blood loss, resembling polytrauma. This similarity suggests elective surgery as a surrogate model for studying polytrauma immune responses. We investigated stress responses across age groups and compared them with those of polytrauma patients. Study design: Patients undergoing major spinal reconstruction surgery were divided into older (age >65 years, n = 5) and young (age 18 to 39 years, n = 6) groups. A comparison group consisted of matched trauma patients (n = 8). Blood samples were collected before, during, and after surgery. Bone marrow mononuclear cells and peripheral blood mononuclear cells were analyzed using cellular indexing of transcriptomes and epitopes sequencing or single-cell RNA sequencing. Plasma was subjected to dual-platform proteomic analysis (SomaLogic and O-link). Results: Response to polytrauma was highest within 4 hours. By comparison, the response to surgery was highest at 24 hours. Both insults triggered significant changes in cluster of differentiation 14 monocytes, with increased inflammation and lower major histocompatibility complex-class 2 expression. Older patient's cluster of differentiation 14 monocytes displayed higher inflammation and less major histocompatibility complex-class 2 suppression; a trend was also seen in bone marrow mononuclear cells. Although natural killer cells were markedly activated after polytrauma, they were suppressed after surgery, especially in older patients. In plasma, innate immunity proteins dominated at 24 hours, shifting to adaptive immunity proteins by 6 weeks with heightened inflammation in older patients. Senescence-associated secretory phenotype proteins were higher in older patients at baseline and further elevated during and after surgery. Conclusions: Although both major surgery and polytrauma initiate immune and stress responses, substantial differences exist in timing and cellular profiles, suggesting major elective surgery is not a suitable surrogate for the polytrauma response. Nonetheless, distinct responses in young vs older patients highlight the utility of elective spinal in studying patient-specific factors affecting outcomes after major elective surgery.
MeSH term(s)	Humans ; Aged ; Adolescent ; Young Adult ; Adult ; Transcriptome ; Leukocytes, Mononuclear ; Proteomics ; Surgery, Plastic ; Aging ; Multiple Trauma/surgery ; Gene Expression Profiling ; Immunity ; Inflammation
Language	English
Publishing date	2023-12-14
Publishing country	United States
Document type	Journal Article
ZDB-ID	1181115-8
ISSN	1879-1190 ; 1072-7515
ISSN (online)	1879-1190
ISSN	1072-7515
DOI	10.1097/XCS.0000000000000922
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Article ; Online: The Use of Multiplexing to Identify Cytokine and Chemokine Networks in the Immune-Inflammatory Response to Trauma.

Bonaroti, Jillian / Abdelhamid, Sultan / Kar, Upendra / Sperry, Jason / Zamora, Ruben / Namas, Rami Ahmd / McKinley, Todd / Vodovotz, Yoram / Billiar, Timothy

Antioxidants & redox signaling

2021 Volume 35, Issue 16, Page(s) 1393–1406

Abstract: Significance: ...

Abstract	Significance:
MeSH term(s)	Cytokines/immunology ; Humans ; Immunity/immunology ; Inflammation/immunology ; Wounds and Injuries/immunology
Chemical Substances	Cytokines
Language	English
Publishing date	2021-05-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1483836-9
ISSN	1557-7716 ; 1523-0864
ISSN (online)	1557-7716
ISSN	1523-0864
DOI	10.1089/ars.2021.0054
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Article ; Online: Central role for neurally dysregulated IL-17A in dynamic networks of systemic and local inflammation in combat casualties.

Zamora, Ruben / Forsberg, Jonathan A / Shah, Ashti M / Unselt, Desiree / Grey, Scott / Lisboa, Felipe A / Billiar, Timothy R / Schobel, Seth A / Potter, Benjamin K / Elster, Eric A / Vodovotz, Yoram

Scientific reports

2023 Volume 13, Issue 1, Page(s) 6618

Abstract: ... upregulation of pathogenic Th17 cells, non-pathogenic Th17 cells, and memory/effector T cells. This was ...

Abstract	Dynamic Network Analysis (DyNA) and Dynamic Hypergraphs (DyHyp) were used to define protein-level inflammatory networks at the local (wound effluent) and systemic circulation (serum) levels from 140 active-duty, injured service members (59 with TBI and 81 non-TBI). Interleukin (IL)-17A was the only biomarker elevated significantly in both serum and effluent in TBI vs. non-TBI casualties, and the mediator with the most DyNA connections in TBI wounds. DyNA combining serum and effluent data to define cross-compartment correlations suggested that IL-17A bridges local and systemic circulation at late time points. DyHyp suggested that systemic IL-17A upregulation in TBI patients was associated with tumor necrosis factor-α, while IL-17A downregulation in non-TBI patients was associated with interferon-γ. Correlation analysis suggested differential upregulation of pathogenic Th17 cells, non-pathogenic Th17 cells, and memory/effector T cells. This was associated with reduced procalcitonin in both effluent and serum of TBI patients, in support of an antibacterial effect of Th17 cells in TBI patients. Dysregulation of Th17 responses following TBI may drive cross-compartment inflammation following combat injury, counteracting wound infection at the cost of elevated systemic inflammation.
MeSH term(s)	Humans ; Interleukin-17/pharmacology ; Inflammation ; Tumor Necrosis Factor-alpha/pharmacology ; Interferon-gamma/pharmacology ; Biomarkers ; Th17 Cells
Chemical Substances	Interleukin-17 ; Tumor Necrosis Factor-alpha ; Interferon-gamma (82115-62-6) ; Biomarkers
Language	English
Publishing date	2023-04-24
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-023-33623-z
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