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Article ; Online: Temporal transcriptomic analysis using TrendCatcher identifies early and persistent neutrophil activation in severe COVID-19.

Wang, Xinge / Sanborn, Mark A / Dai, Yang / Rehman, Jalees

JCI insight

2022 Volume 7, Issue 7

Abstract: Studying temporal gene expression shifts during disease progression provides important insights into the biological mechanisms that distinguish adaptive and maladaptive responses. Existing tools for the analysis of time course transcriptomic data are not ...

Abstract	Studying temporal gene expression shifts during disease progression provides important insights into the biological mechanisms that distinguish adaptive and maladaptive responses. Existing tools for the analysis of time course transcriptomic data are not designed to optimally identify distinct temporal patterns when analyzing dynamic differentially expressed genes (DDEGs). Moreover, there are not enough methods to assess and visualize the temporal progression of biological pathways mapped from time course transcriptomic data sets. In this study, we developed an open-source R package TrendCatcher (https://github.com/jaleesr/TrendCatcher), which applies the smoothing spline ANOVA model and break point searching strategy, to identify and visualize distinct dynamic transcriptional gene signatures and biological processes from longitudinal data sets. We used TrendCatcher to perform a systematic temporal analysis of COVID-19 peripheral blood transcriptomes, including bulk and single-cell RNA-Seq time course data. TrendCatcher uncovered the early and persistent activation of neutrophils and coagulation pathways, as well as impaired type I IFN (IFN-I) signaling in circulating cells as a hallmark of patients who progressed to severe COVID-19, whereas no such patterns were identified in individuals receiving SARS-CoV-2 vaccinations or patients with mild COVID-19. These results underscore the importance of systematic temporal analysis to identify early biomarkers and possible pathogenic therapeutic targets.
MeSH term(s)	COVID-19/genetics ; Gene Expression Profiling/methods ; Humans ; Neutrophil Activation ; SARS-CoV-2/genetics ; Transcriptome
Language	English
Publishing date	2022-04-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.157255
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Article: Systematic temporal analysis of peripheral blood transcriptomes using

Wang, Xinge / Sanborn, Mark / Dai, Yang / Rehman, Jalees

bioRxiv : the preprint server for biology

2021

Abstract	Studying temporal gene expression shifts during disease progression provides important insights into the biological mechanisms that distinguish adaptive and maladaptive responses. Existing tools for the analysis of time course transcriptomic data are not designed to optimally identify distinct temporal patterns when analyzing dynamic differentially expressed genes (DDEGs). Moreover, there is a lack of methods to assess and visualize the temporal progression of biological pathways mapped from time course transcriptomic datasets. In this study, we developed an open-source R package
Language	English
Publishing date	2021-12-07
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.05.04.442617
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Article ; Online: SenePy: Unveiling the Cell-Type Specific Landscape of Cellular Senescence through Single-Cell Analysis in Living Organisms

Sanborn, Mark A / Wang, Xinge / Gao, Shang / Dai, Yang / Rehman, Jalees

bioRxiv

Abstract: Senescent cells accumulate in tissues with organismal age and contribute causally to multiple chronic diseases. In vivo senescent cell phenotypes are heterogeneous because cellular context and stressors vary by cell type and tissue. Due to the ... ...

Abstract	Senescent cells accumulate in tissues with organismal age and contribute causally to multiple chronic diseases. In vivo senescent cell phenotypes are heterogeneous because cellular context and stressors vary by cell type and tissue. Due to the variability of senescence programs, there is no universal method to identify senescent cells and even widely used markers, such as CDKN2A, are not ubiquitous. Therefore, we interrogated the Tabula Muris Senis mouse single-cell aging atlas and an array of single-cell datasets from human donors that spanned many ages to find cell-specific signatures of cellular senescence. We derived 75 mouse and 65 human senescence signatures from individual cell populations. CDKN2A and other markers of senescence were overrepresented in these signatures but there were many novel senescence genes present at higher rates. Within individual cell populations, we observed multiple programs of senescence with distinct temporal and transcriptional characteristics. We packaged the signatures along with a single-cell scoring method into an open-source package: SenePy. SenePy signatures better recapitulate cellular senescence than available methods when tested on multiple in vivo RNA-seq datasets and a p16ink4a reporter single-cell dataset. We used SenePy to map the kinetics of senescent cell accumulation across 97 cell types from humans and mice. SenePy also generalizes to disease-associate senescence and we used it to identify an increased burden of senescent cells in COVID-19 and myocardial infarction. This work provides a significant advancement towards our ability to identify and characterize in vivo cellular senescence.
Keywords	covid19
Language	English
Publishing date	2023-08-31
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2023.08.30.555644
Database	COVID19

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Article ; Online: Engineered Wnt7a ligands rescue blood-brain barrier and cognitive deficits in a COVID-19 mouse model.

Trevino, Troy N / Fogel, Avital B / Otkiran, Guliz / Niladhuri, Seshadri B / Sanborn, Mark A / Class, Jacob / Almousawi, Ali A / Vanhollebeke, Benoit / Tai, Leon M / Rehman, Jalees / Richner, Justin M / Lutz, Sarah E

Brain : a journal of neurology

2024 Volume 147, Issue 5, Page(s) 1636–1643

Abstract: Respiratory infection with SARS-CoV-2 causes systemic vascular inflammation and cognitive impairment. We sought to identify the underlying mechanisms mediating cerebrovascular dysfunction and inflammation following mild respiratory SARS-CoV-2 infection. ... ...

Abstract	Respiratory infection with SARS-CoV-2 causes systemic vascular inflammation and cognitive impairment. We sought to identify the underlying mechanisms mediating cerebrovascular dysfunction and inflammation following mild respiratory SARS-CoV-2 infection. To this end, we performed unbiased transcriptional analysis to identify brain endothelial cell signalling pathways dysregulated by mouse adapted SARS-CoV-2 MA10 in aged immunocompetent C57Bl/6 mice in vivo. This analysis revealed significant suppression of Wnt/β-catenin signalling, a critical regulator of blood-brain barrier (BBB) integrity. We therefore hypothesized that enhancing cerebrovascular Wnt/β-catenin activity would offer protection against BBB permeability, neuroinflammation, and neurological signs in acute infection. Indeed, we found that delivery of cerebrovascular-targeted, engineered Wnt7a ligands protected BBB integrity, reduced T-cell infiltration of the brain, and reduced microglial activation in SARS-CoV-2 infection. Importantly, this strategy also mitigated SARS-CoV-2 induced deficits in the novel object recognition assay for learning and memory and the pole descent task for bradykinesia. These observations suggest that enhancement of Wnt/β-catenin signalling or its downstream effectors could be potential interventional strategies for restoring cognitive health following viral infections.
MeSH term(s)	Animals ; Blood-Brain Barrier/metabolism ; COVID-19/complications ; Mice ; Wnt Proteins/metabolism ; Disease Models, Animal ; Mice, Inbred C57BL ; Cognitive Dysfunction/metabolism ; Cognitive Dysfunction/etiology ; Wnt Signaling Pathway/physiology ; Ligands ; SARS-CoV-2 ; Male ; Brain/metabolism
Chemical Substances	Wnt Proteins ; Wnt7a protein, mouse ; Ligands
Language	English
Publishing date	2024-02-02
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	80072-7
ISSN	1460-2156 ; 0006-8950
ISSN (online)	1460-2156
ISSN	0006-8950
DOI	10.1093/brain/awae031
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Article: Matrimeres are systemic nanoscale mediators of tissue integrity and function.

Debnath, Koushik / Qayoom, Irfan / O'Donnell, Steven / Ekiert, Julia / Wang, Can / Sanborn, Mark A / Liu, Chang / Rivera, Ambar / Cho, Ik Sung / Saichellappa, Saiumamaheswari / Toth, Peter T / Mehta, Dolly / Rehman, Jalees / Du, Xiaoping / Gao, Yu / Shin, Jae-Won

bioRxiv : the preprint server for biology

2024

Abstract: Tissue barriers must be rapidly restored after injury to promote regeneration. However, the mechanism behind this process is unclear, particularly in cases where the underlying extracellular matrix is still compromised. Here, we report the discovery of ... ...

Abstract	Tissue barriers must be rapidly restored after injury to promote regeneration. However, the mechanism behind this process is unclear, particularly in cases where the underlying extracellular matrix is still compromised. Here, we report the discovery of matrimeres as constitutive nanoscale mediators of tissue integrity and function. We define matrimeres as non-vesicular nanoparticles secreted by cells, distinguished by a primary composition comprising at least one matrix protein and DNA molecules serving as scaffolds. Mesenchymal stromal cells assemble matrimeres from fibronectin and DNA within acidic intracellular compartments. Drawing inspiration from this biological process, we have achieved the successful reconstitution of matrimeres without cells. This was accomplished by using purified matrix proteins, including fibronectin and vitronectin, and DNA molecules under optimal acidic pH conditions, guided by the heparin-binding domain and phosphate backbone, respectively. Plasma fibronectin matrimeres circulate in the blood at homeostasis but exhibit a 10-fold decrease during systemic inflammatory injury
Language	English
Publishing date	2024-03-29
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.25.586585
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Article ; Online: Trained immunity of alveolar macrophages enhances injury resolution via KLF4-MERTK-mediated efferocytosis.

Chakraborty, Sreeparna / Singh, Abhalaxmi / Wang, Li / Wang, Xinge / Sanborn, Mark A / Ye, Zijing / Maienschein-Cline, Mark / Mukhopadhyay, Amitabha / Ganesh, Balaji B / Malik, Asrar B / Rehman, Jalees

The Journal of experimental medicine

2023 Volume 220, Issue 11

Abstract: Recent studies suggest that training of innate immune cells such as tissue-resident macrophages by repeated noxious stimuli can heighten host defense responses. However, it remains unclear whether trained immunity of tissue-resident macrophages also ... ...

Abstract	Recent studies suggest that training of innate immune cells such as tissue-resident macrophages by repeated noxious stimuli can heighten host defense responses. However, it remains unclear whether trained immunity of tissue-resident macrophages also enhances injury resolution to counterbalance the heightened inflammatory responses. Here, we studied lung-resident alveolar macrophages (AMs) prechallenged with either the bacterial endotoxin or with Pseudomonas aeruginosa and observed that these trained AMs showed greater resilience to pathogen-induced cell death. Transcriptomic analysis and functional assays showed greater capacity of trained AMs for efferocytosis of cellular debris and injury resolution. Single-cell high-dimensional mass cytometry analysis and lineage tracing demonstrated that training induces an expansion of a MERTKhiMarcohiCD163+F4/80low lung-resident AM subset with a proresolving phenotype. Reprogrammed AMs upregulated expression of the efferocytosis receptor MERTK mediated by the transcription factor KLF4. Adoptive transfer of these trained AMs restricted inflammatory lung injury in recipient mice exposed to lethal P. aeruginosa. Thus, our study has identified a subset of tissue-resident trained macrophages that prevent hyperinflammation and restore tissue homeostasis following repeated pathogen challenges.
MeSH term(s)	Animals ; Mice ; Adoptive Transfer ; c-Mer Tyrosine Kinase/genetics ; Macrophages, Alveolar ; Phagocytosis ; Trained Immunity
Chemical Substances	c-Mer Tyrosine Kinase (EC 2.7.10.1) ; Mertk protein, mouse (EC 2.7.10.1) ; Klf4 protein, mouse
Language	English
Publishing date	2023-08-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20221388
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Article: Differential Genome Replication of a Unique Single-Amino-Acid Mutation in the Adenovirus-4 Component of the Live Oral Adenovirus Type 4 and Type 7 Vaccine.

Collins, Natalie D / Beaty, Shannon / Wallace, Elana / Li, Yuanzhang / Sanborn, Mark / Yang, Yu / Adhikari, Anima / Shabram, Paul / Warfield, Kelly / Karasavvas, Nicos / Kuschner, Robert A / Hang, Jun

Vaccines

2023 Volume 11, Issue 7

Abstract: The FDA-approved Adenovirus Type 4 and Type 7 Vaccine, Live, Oral is highly effective and essential in preventing acute respiratory diseases (ARDs) in U.S. military recruits. Our study revealed the presence of a previously undetected mutation, not found ... ...

Abstract	The FDA-approved Adenovirus Type 4 and Type 7 Vaccine, Live, Oral is highly effective and essential in preventing acute respiratory diseases (ARDs) in U.S. military recruits. Our study revealed the presence of a previously undetected mutation, not found in the wild-type human adenovirus type 4 (HAdV-4) component of the licensed vaccine, which contains an amino acid substitution (P388T) in the pre-terminal protein (pTP). This study demonstrated that replication of the T388 HAdV-4 vaccine mutant virus is favored over the wild type in WI-38 cells, the cell type utilized in vaccine manufacturing. However, results from serial human stool specimens of vaccine recipients support differential genome replication in the gastrointestinal tract (GI), demonstrated by the steady decline of the percentage of mutant T388 vaccine virus. Since vaccine efficacy depends upon GI replication and the subsequent immune response, the mutation can potentially impact vaccine efficacy.
Language	English
Publishing date	2023-06-25
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2703319-3
ISSN	2076-393X
ISSN	2076-393X
DOI	10.3390/vaccines11071144
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Article ; Online: Hematopoietic Jagged1 is a fetal liver niche factor required for functional maturation and engraftment of fetal hematopoietic stem cells.

Shao, Lijian / Paik, Na Yoon / Sanborn, Mark A / Bandara, Thilinie / Vijaykumar, Anjali / Sottoriva, Kilian / Rehman, Jalees / Nombela-Arrieta, Cesar / Pajcini, Kostandin V

Proceedings of the National Academy of Sciences of the United States of America

2023 Volume 120, Issue 20, Page(s) e2210058120

Abstract: Notch signaling is essential for the emergence of definitive hematopoietic stem cells (HSCs) in the embryo and their development in the fetal liver niche. However, how Notch signaling is activated and which fetal liver cell type provides the ligand for ... ...

Abstract	Notch signaling is essential for the emergence of definitive hematopoietic stem cells (HSCs) in the embryo and their development in the fetal liver niche. However, how Notch signaling is activated and which fetal liver cell type provides the ligand for receptor activation in HSCs is unknown. Here we provide evidence that endothelial Jagged1 (Jag1) has a critical early role in fetal liver vascular development but is not required for hematopoietic function during fetal HSC expansion. We demonstrate that Jag1 is expressed in many hematopoietic cells in the fetal liver, including HSCs, and that its expression is lost in adult bone marrow HSCs. Deletion of hematopoietic Jag1 does not affect fetal liver development; however, Jag1-deficient fetal liver HSCs exhibit a significant transplantation defect. Bulk and single-cell transcriptomic analysis of HSCs during peak expansion in the fetal liver indicates that loss of hematopoietic Jag1 leads to the downregulation of critical hematopoietic factors such as GATA2, Mllt3, and HoxA7, but does not perturb Notch receptor expression. Ex vivo activation of Notch signaling in Jag1-deficient fetal HSCs partially rescues the functional defect in a transplant setting. These findings indicate a new fetal-specific niche that is based on juxtracrine hematopoietic Notch signaling and reveal Jag1 as a fetal-specific niche factor essential for HSC function.
MeSH term(s)	Adult ; Humans ; Endothelium/metabolism ; Fetus/metabolism ; Hematopoietic Stem Cells/metabolism ; Liver/metabolism ; Receptors, Notch/genetics ; Receptors, Notch/metabolism
Chemical Substances	Receptors, Notch ; JAG1 protein, human
Language	English
Publishing date	2023-05-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2210058120
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Article ; Online: A comparative recombination analysis of human coronaviruses and implications for the SARS-CoV-2 pandemic.

Pollett, Simon / Conte, Matthew A / Sanborn, Mark / Jarman, Richard G / Lidl, Grace M / Modjarrad, Kayvon / Maljkovic Berry, Irina

Scientific reports

2021 Volume 11, Issue 1, Page(s) 17365

Abstract: The SARS-CoV-2 pandemic prompts evaluation of recombination in human coronavirus (hCoV) evolution. We undertook recombination analyses of 158,118 public seasonal hCoV, SARS-CoV-1, SARS-CoV-2 and MERS-CoV genome sequences using the RDP4 software. We found ...

Abstract	The SARS-CoV-2 pandemic prompts evaluation of recombination in human coronavirus (hCoV) evolution. We undertook recombination analyses of 158,118 public seasonal hCoV, SARS-CoV-1, SARS-CoV-2 and MERS-CoV genome sequences using the RDP4 software. We found moderate evidence for 8 SARS-CoV-2 recombination events, two of which involved the spike gene, and low evidence for one SARS-CoV-1 recombination event. Within MERS-CoV, 229E, OC43, NL63 and HKU1 datasets, we noted 7, 1, 9, 14, and 1 high-confidence recombination events, respectively. There was propensity for recombination breakpoints in the non-ORF1 region of the genome containing structural genes, and recombination severely skewed the temporal structure of these data, especially for NL63 and OC43. Bayesian time-scaled analyses on recombinant-free data indicated the sampled diversity of seasonal CoVs emerged in the last 70 years, with 229E displaying continuous lineage replacements. These findings emphasize the importance of genomic based surveillance to detect recombination in SARS-CoV-2, particularly if recombination may lead to immune evasion.
MeSH term(s)	Bayes Theorem ; Databases, Genetic ; Genome, Viral ; Humans ; Immune Evasion ; Middle East Respiratory Syndrome Coronavirus/classification ; Middle East Respiratory Syndrome Coronavirus/genetics ; Recombination, Genetic ; Severe acute respiratory syndrome-related coronavirus/classification ; Severe acute respiratory syndrome-related coronavirus/genetics ; SARS-CoV-2/classification ; SARS-CoV-2/genetics ; Spike Glycoprotein, Coronavirus/genetics ; Viral Nonstructural Proteins/genetics
Chemical Substances	Spike Glycoprotein, Coronavirus ; Viral Nonstructural Proteins ; nonstructural protein, coronavirus
Language	English
Publishing date	2021-08-30
Publishing country	England
Document type	Comparative Study ; Journal Article ; Research Support, Non-U.S. Gov't ; 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/s41598-021-96626-8
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Article ; Online: A comparative recombination analysis of human coronaviruses and implications for the SARS-CoV-2 pandemic

Pollett, Simon / Conte, Matthew A / Sanborn, Mark A / Jarman, Richard G / Lidl, Grace M / Modjarrad, Kayvon / Maljkovic Berry, Irina

bioRxiv

Abstract	The SARS-CoV-2 pandemic prompts evaluation of recombination in human coronavirus (hCoV) evolution. We undertook recombination analyses of 158,118 public seasonal hCoV, SARS-CoV-1, SARS-CoV-2 and MERS-CoV genome sequences using the RDP4 software. We found moderate evidence for 8 SARS-CoV-2 recombination events, two of which involved the spike gene, and low evidence for one SARS-CoV-1 recombination event. Within MERS-CoV, 229E, OC43, NL63 and HKU1 datasets, we noted 7, 1, 9, 14, and 1 high-confidence recombination events, respectively. There was propensity for recombination breakpoints in structural genes, and recombination severely skewed the temporal structure of these data, especially for NL63 and OC43. Bayesian time-scaled analyses on recombinant-free data indicated the sampled diversity of seasonal CoVs emerged in the last 70 years, with 229E displaying continuous lineage replacements. These findings emphasize the importance of genomic based surveillance to detect recombination in SARS-CoV-2, particularly if recombination may lead to immune evasion.
Keywords	covid19
Language	English
Publishing date	2021-03-08
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2021.03.07.434287
Database	COVID19

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