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Article ; Online: Defining protein expression in the kidney at large scale: from antibody validation to cytometry analysis.

Sabo, Angela R / Winfree, Seth / El-Achkar, Tarek M

American journal of physiology. Renal physiology

2022 Volume 324, Issue 2, Page(s) F135–F137

MeSH term(s)	Antibodies ; Kidney ; Flow Cytometry
Chemical Substances	Antibodies
Language	English
Publishing date	2022-12-01
Publishing country	United States
Document type	Editorial ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	603837-2
ISSN	1522-1466 ; 0363-6127
ISSN (online)	1522-1466
ISSN	0363-6127
DOI	10.1152/ajprenal.00262.2022
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Article ; Online: Evolving Concepts in Uromodulin Biology, Physiology, and Its Role in Disease: a Tale of Two Forms.

LaFavers, Kaice A / Micanovic, Radmila / Sabo, Angela R / Maghak, Lauren A / El-Achkar, Tarek M

Hypertension (Dallas, Tex. : 1979)

2022 Volume 79, Issue 11, Page(s) 2409–2418

Abstract: Uromodulin (or Tamm-Horsfall protein) is a glycoprotein uniquely produced in the kidney by tubular cells of the thick ascending limb of the loop of Henle and early distal tubules. This protein exhibits bidirectional secretion in the urine and in the ... ...

Abstract	Uromodulin (or Tamm-Horsfall protein) is a glycoprotein uniquely produced in the kidney by tubular cells of the thick ascending limb of the loop of Henle and early distal tubules. This protein exhibits bidirectional secretion in the urine and in the renal interstitium and circulation. The role of this protein in maintaining renal and systemic homeostasis is becoming increasingly appreciated. Furthermore, perturbations of its functions may play a role in various diseases affecting the kidney and distant organs. In this review, we will discuss important advances in understanding its biology, highlighting the recent discoveries of its secretion and differential precursor processing that generates 2 forms: (1) a highly polymerizing form that is apically excreted in the urine and generates filaments and (2) a nonpolymerizing form that retains a polymerization inhibitory pro-peptide and is released basolaterally in the kidney interstitium and circulation, but can also be found in the urine. We will also discuss factors regulating its production and release, taking into account its intricate physiology, and propose best practices to report its levels. We also discuss breaking advances in its role in hypertension, acute kidney injury and progression to chronic disease, immunomodulation and regulating renal and systemic oxidative stress. We anticipate that this work will be a great resource for researchers and clinicians. This review will highlight the importance of defining what regulates the 2 forms of uromodulin, so that modulation of uromodulin levels and function could become a novel tool in our therapeutic armamentarium against kidney disease.
MeSH term(s)	Humans ; Uromodulin/metabolism ; Kidney/metabolism ; Acute Kidney Injury/metabolism ; Hypertension/metabolism ; Biology
Chemical Substances	Uromodulin
Language	English
Publishing date	2022-08-12
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	423736-5
ISSN	1524-4563 ; 0194-911X ; 0362-4323
ISSN (online)	1524-4563
ISSN	0194-911X ; 0362-4323
DOI	10.1161/HYPERTENSIONAHA.122.18567
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Article ; Online: Integrated Cytometry With Machine Learning Applied to High-Content Imaging of Human Kidney Tissue for In Situ Cell Classification and Neighborhood Analysis.

Winfree, Seth / McNutt, Andrew T / Khochare, Suraj / Borgard, Tyler J / Barwinska, Daria / Sabo, Angela R / Ferkowicz, Michael J / Williams, James C / Lingeman, James E / Gulbronson, Connor J / Kelly, Katherine J / Sutton, Timothy A / Dagher, Pierre C / Eadon, Michael T / Dunn, Kenneth W / El-Achkar, Tarek M

Laboratory investigation; a journal of technical methods and pathology

2023 Volume 103, Issue 6, Page(s) 100104

Abstract: The human kidney is a complex organ with various cell types that are intricately organized to perform key physiological functions and maintain homeostasis. New imaging modalities, such as mesoscale and highly multiplexed fluorescence microscopy, are ... ...

Abstract	The human kidney is a complex organ with various cell types that are intricately organized to perform key physiological functions and maintain homeostasis. New imaging modalities, such as mesoscale and highly multiplexed fluorescence microscopy, are increasingly being applied to human kidney tissue to create single-cell resolution data sets that are both spatially large and multidimensional. These single-cell resolution high-content imaging data sets have great potential to uncover the complex spatial organization and cellular makeup of the human kidney. Tissue cytometry is a novel approach used for the quantitative analysis of imaging data; however, the scale and complexity of such data sets pose unique challenges for processing and analysis. We have developed the Volumetric Tissue Exploration and Analysis (VTEA) software, a unique tool that integrates image processing, segmentation, and interactive cytometry analysis into a single framework on desktop computers. Supported by an extensible and open-source framework, VTEA's integrated pipeline now includes enhanced analytical tools, such as machine learning, data visualization, and neighborhood analyses, for hyperdimensional large-scale imaging data sets. These novel capabilities enable the analysis of mesoscale 2- and 3-dimensional multiplexed human kidney imaging data sets (such as co-detection by indexing and 3-dimensional confocal multiplexed fluorescence imaging). We demonstrate the utility of this approach in identifying cell subtypes in the kidney on the basis of labels, spatial association, and their microenvironment or neighborhood membership. VTEA provides an integrated and intuitive approach to decipher the cellular and spatial complexity of the human kidney and complements other transcriptomics and epigenetic efforts to define the landscape of kidney cell types.
MeSH term(s)	Humans ; Kidney/diagnostic imaging ; Imaging, Three-Dimensional/methods ; Image Processing, Computer-Assisted/methods ; Software ; Machine Learning
Language	English
Publishing date	2023-02-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80178-1
ISSN	1530-0307 ; 0023-6837
ISSN (online)	1530-0307
ISSN	0023-6837
DOI	10.1016/j.labinv.2023.100104
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Article ; Online: The kidney releases a nonpolymerizing form of uromodulin in the urine and circulation that retains the external hydrophobic patch domain.

Micanovic, Radmila / LaFavers, Kaice A / Patidar, Kavish R / Ghabril, Marwan S / Doud, Emma H / Mosley, Amber L / Sabo, Angela R / Khan, Shehnaz / El-Achkar, Tarek M

American journal of physiology. Renal physiology

2022 Volume 322, Issue 4, Page(s) F403–F418

Abstract: Uromodulin [Tamm-Horsfall protein (THP)] is a glycoprotein uniquely produced in the kidney. It is released by cells of the thick ascending limbs apically in the urine and basolaterally in the renal interstitium and systemic circulation. Processing of ... ...

Abstract	Uromodulin [Tamm-Horsfall protein (THP)] is a glycoprotein uniquely produced in the kidney. It is released by cells of the thick ascending limbs apically in the urine and basolaterally in the renal interstitium and systemic circulation. Processing of mature urinary THP, which polymerizes into supramolecular filaments, requires cleavage of an external hydrophobic patch (EHP) at the COOH-terminus. However, THP in the circulation is not polymerized, and it remains unclear if nonaggregated forms of THP exist natively in the urine. We propose that an alternative processing path, which retains the EHP domain, can lead to a nonpolymerizing form of THP. We generated an antibody that specifically recognizes THP with retained EHP (THP + EHP) and established its presence in the urine in a nonpolymerized native state. Proteomic characterization of urinary THP + EHP revealed its COOH-terminus ending at F617. In the human kidney, THP + EHP was detected in thick ascending limb cells and less strongly in the renal parenchyma. Using immunoprecipitation followed by proteomic sequencing and immunoblot analysis, we then demonstrated that serum THP has also retained EHP. In a small cohort of patients at risk for acute kidney injury, admission urinary THP + EHP was significantly lower in patients who subsequently developed acute kidney injury during hospitalization. Our findings uncover novel insights into uromodulin biology by establishing the presence of an alternative path for cellular processing, which could explain the release of nonpolymerizing THP in the circulation. Larger studies are needed to establish the utility of urinary THP + EHP as a sensitive biomarker of kidney health and susceptibility to injury.
MeSH term(s)	Acute Kidney Injury/metabolism ; Humans ; Kidney/metabolism ; Proteomics ; Uromodulin/chemistry ; Uromodulin/urine
Chemical Substances	Uromodulin
Language	English
Publishing date	2022-01-31
Publishing country	United States
Document type	Journal Article
ZDB-ID	603837-2
ISSN	1522-1466 ; 0363-6127
ISSN (online)	1522-1466
ISSN	0363-6127
DOI	10.1152/ajprenal.00322.2021
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Article ; Online: Label-free imaging of non-deparaffinized sections of the human kidney to determine tissue quality and signatures of disease.

Sabo, Angela R / Winfree, Seth / Bledsoe, Sharon B / Phillips, Carrie L / Lingeman, James E / Eadon, Michael T / Williams, James C / El-Achkar, Tarek M

Physiological reports

2022 Volume 10, Issue 3, Page(s) e15167

Abstract: Label-free fluorescence imaging of kidney sections can provide important morphological information, but its utility has not been tested in a histology processing workflow. We tested the feasibility of label-free imaging of paraffin-embedded sections ... ...

Abstract	Label-free fluorescence imaging of kidney sections can provide important morphological information, but its utility has not been tested in a histology processing workflow. We tested the feasibility of label-free imaging of paraffin-embedded sections without deparaffinization and its potential usefulness in generating actionable data. Kidney tissue specimens were obtained during percutaneous nephrolithotomy or via diagnostic needle biopsy. Unstained non-deparaffinized sections were imaged using widefield fluorescence microscopy to capture endogenous fluorescence. Some samples were also imaged with confocal microscopy and multiphoton excitation to collect second harmonic generation (SHG) signal to obtain high-quality autofluorescence images with optical sectioning. To adjudicate the label-free signal, the samples or corresponding contiguous sections were subsequently deparaffinized and stained with Lillie's allochrome. Label-free imaging allowed the recognition of various kidney structures and enabled morphological qualification for adequacy. SHG and confocal imaging yielded quantifiable high-quality images for tissue collagens and revealed specific patterns in glomeruli and various tubules. Disease specimens from patients with diabetic kidney disease and focal segmental glomerulosclerosis showed distinctive signatures compared to specimens from healthy controls with normal kidney function. Quantitative cytometry could also be performed when DAPI is added in situ before imaging. These results show that label-free imaging of non-deparaffinized sections provides useful information about tissue quality that could be beneficial to nephropathologists by maximizing the use of scarce kidney tissue. This approach also provides quantifiable features that could inform on the biology of health and disease.
MeSH term(s)	Collagen/metabolism ; Diabetic Nephropathies/pathology ; Humans ; Kidney/metabolism ; Kidney/pathology ; Optical Imaging/methods ; Paraffin Embedding/methods ; Tissue Fixation/methods
Chemical Substances	Collagen (9007-34-5)
Language	English
Publishing date	2022-02-10
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2724325-4
ISSN	2051-817X ; 2051-817X
ISSN (online)	2051-817X
ISSN	2051-817X
DOI	10.14814/phy2.15167
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Article ; Online: A spatially anchored transcriptomic atlas of the human kidney papilla identifies significant immune injury in patients with stone disease.

Nature communications

2023 Volume 14, Issue 1, Page(s) 4140

Abstract: Kidney stone disease causes significant morbidity and increases health care utilization. In this work, we decipher the cellular and molecular niche of the human renal papilla in patients with calcium oxalate (CaOx) stone disease and healthy subjects. In ... ...

Abstract	Kidney stone disease causes significant morbidity and increases health care utilization. In this work, we decipher the cellular and molecular niche of the human renal papilla in patients with calcium oxalate (CaOx) stone disease and healthy subjects. In addition to identifying cell types important in papillary physiology, we characterize collecting duct cell subtypes and an undifferentiated epithelial cell type that was more prevalent in stone patients. Despite the focal nature of mineral deposition in nephrolithiasis, we uncover a global injury signature characterized by immune activation, oxidative stress and extracellular matrix remodeling. We also identify the association of MMP7 and MMP9 expression with stone disease and mineral deposition, respectively. MMP7 and MMP9 are significantly increased in the urine of patients with CaOx stone disease, and their levels correlate with disease activity. Our results define the spatial molecular landscape and specific pathways contributing to stone-mediated injury in the human papilla and identify associated urinary biomarkers.
MeSH term(s)	Humans ; Kidney Medulla/metabolism ; Matrix Metalloproteinase 9/metabolism ; Matrix Metalloproteinase 7 ; Calcium Oxalate/metabolism ; Transcriptome ; Kidney Calculi/genetics ; Kidney Calculi/metabolism
Chemical Substances	Matrix Metalloproteinase 9 (EC 3.4.24.35) ; Matrix Metalloproteinase 7 (EC 3.4.24.23) ; Calcium Oxalate (2612HC57YE)
Language	English
Publishing date	2023-07-19
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-38975-8
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Article ; Online: Large-scale, three-dimensional tissue cytometry of the human kidney: a complete and accessible pipeline.

Ferkowicz, Michael J / Winfree, Seth / Sabo, Angela R / Kamocka, Malgorzata M / Khochare, Suraj / Barwinska, Daria / Eadon, Michael T / Cheng, Ying-Hua / Phillips, Carrie L / Sutton, Timothy A / Kelly, Katherine J / Dagher, Pierre C / El-Achkar, Tarek M / Dunn, Kenneth W

Laboratory investigation; a journal of technical methods and pathology

2021 Volume 101, Issue 5, Page(s) 661–676

Abstract: The advent of personalized medicine has driven the development of novel approaches for obtaining detailed cellular and molecular information from clinical tissue samples. Tissue cytometry is a promising new technique that can be used to enumerate and ... ...

Abstract	The advent of personalized medicine has driven the development of novel approaches for obtaining detailed cellular and molecular information from clinical tissue samples. Tissue cytometry is a promising new technique that can be used to enumerate and characterize each cell in a tissue and, unlike flow cytometry and other single-cell techniques, does so in the context of the intact tissue, preserving spatial information that is frequently crucial to understanding a cell's physiology, function, and behavior. However, the wide-scale adoption of tissue cytometry as a research tool has been limited by the fact that published examples utilize specialized techniques that are beyond the capabilities of most laboratories. Here we describe a complete and accessible pipeline, including methods of sample preparation, microscopy, image analysis, and data analysis for large-scale three-dimensional tissue cytometry of human kidney tissues. In this workflow, multiphoton microscopy of unlabeled tissue is first conducted to collect autofluorescence and second-harmonic images. The tissue is then labeled with eight fluorescent probes, and imaged using spectral confocal microscopy. The raw 16-channel images are spectrally deconvolved into 8-channel images, and analyzed using the Volumetric Tissue Exploration and Analysis (VTEA) software developed by our group. We applied this workflow to analyze millimeter-scale tissue samples obtained from human nephrectomies and from renal biopsies from individuals diagnosed with diabetic nephropathy, generating a quantitative census of tens of thousands of cells in each. Such analyses can provide useful insights that can be linked to the biology or pathology of kidney disease. The approach utilizes common laboratory techniques, is compatible with most commercially-available confocal microscope systems and all image and data analysis is conducted using the VTEA image analysis software, which is available as a plug-in for ImageJ.
MeSH term(s)	Cytological Techniques ; Fluorescent Dyes ; Humans ; Imaging, Three-Dimensional ; Kidney/cytology ; Microscopy, Confocal ; Microscopy, Fluorescence, Multiphoton ; Software
Chemical Substances	Fluorescent Dyes
Language	English
Publishing date	2021-01-06
Publishing country	United States
Document type	Evaluation Study ; Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80178-1
ISSN	1530-0307 ; 0023-6837
ISSN (online)	1530-0307
ISSN	0023-6837
DOI	10.1038/s41374-020-00518-w
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Article ; Online: The chromatin landscape of healthy and injured cell types in the human kidney.

Gisch, Debora L / Brennan, Michelle / Lake, Blue B / Basta, Jeannine / Keller, Mark S / Melo Ferreira, Ricardo / Akilesh, Shreeram / Ghag, Reetika / Lu, Charles / Cheng, Ying-Hua / Collins, Kimberly S / Parikh, Samir V / Rovin, Brad H / Robbins, Lynn / Stout, Lisa / Conklin, Kimberly Y / Diep, Dinh / Zhang, Bo / Knoten, Amanda /

Barwinska, Daria / Asghari, Mahla / Sabo, Angela R / Ferkowicz, Michael J / Sutton, Timothy A / Kelly, Katherine J / De Boer, Ian H / Rosas, Sylvia E / Kiryluk, Krzysztof / Hodgin, Jeffrey B / Alakwaa, Fadhl / Winfree, Seth / Jefferson, Nichole / Türkmen, Aydın / Gaut, Joseph P / Gehlenborg, Nils / Phillips, Carrie L / El-Achkar, Tarek M / Dagher, Pierre C / Hato, Takashi / Zhang, Kun / Himmelfarb, Jonathan / Kretzler, Matthias / Mollah, Shamim / Jain, Sanjay / Rauchman, Michael / Eadon, Michael T

Nature communications

2024 Volume 15, Issue 1, Page(s) 433

Abstract: There is a need to define regions of gene activation or repression that control human kidney cells in states of health, injury, and repair to understand the molecular pathogenesis of kidney disease and design therapeutic strategies. Comprehensive ... ...

Abstract	There is a need to define regions of gene activation or repression that control human kidney cells in states of health, injury, and repair to understand the molecular pathogenesis of kidney disease and design therapeutic strategies. Comprehensive integration of gene expression with epigenetic features that define regulatory elements remains a significant challenge. We measure dual single nucleus RNA expression and chromatin accessibility, DNA methylation, and H3K27ac, H3K4me1, H3K4me3, and H3K27me3 histone modifications to decipher the chromatin landscape and gene regulation of the kidney in reference and adaptive injury states. We establish a spatially-anchored epigenomic atlas to define the kidney's active, silent, and regulatory accessible chromatin regions across the genome. Using this atlas, we note distinct control of adaptive injury in different epithelial cell types. A proximal tubule cell transcription factor network of ELF3, KLF6, and KLF10 regulates the transition between health and injury, while in thick ascending limb cells this transition is regulated by NR2F1. Further, combined perturbation of ELF3, KLF6, and KLF10 distinguishes two adaptive proximal tubular cell subtypes, one of which manifested a repair trajectory after knockout. This atlas will serve as a foundation to facilitate targeted cell-specific therapeutics by reprogramming gene regulatory networks.
MeSH term(s)	Humans ; Chromatin/genetics ; Kidney ; Kidney Tubules, Proximal ; Health Status ; Cell Count
Chemical Substances	Chromatin
Language	English
Publishing date	2024-01-10
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-44467-6
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Article ; Online: Integration of spatial and single-cell transcriptomics localizes epithelial cell-immune cross-talk in kidney injury.

Melo Ferreira, Ricardo / Sabo, Angela R / Winfree, Seth / Collins, Kimberly S / Janosevic, Danielle / Gulbronson, Connor J / Cheng, Ying-Hua / Casbon, Lauren / Barwinska, Daria / Ferkowicz, Michael J / Xuei, Xiaoling / Zhang, Chi / Dunn, Kenneth W / Kelly, Katherine J / Sutton, Timothy A / Hato, Takashi / Dagher, Pierre C / El-Achkar, Tarek M / Eadon, Michael T

JCI insight

2021 Volume 6, Issue 12

Abstract: Single-cell sequencing studies have characterized the transcriptomic signature of cell types within the kidney. However, the spatial distribution of acute kidney injury (AKI) is regional and affects cells heterogeneously. We first optimized coordination ... ...

Abstract	Single-cell sequencing studies have characterized the transcriptomic signature of cell types within the kidney. However, the spatial distribution of acute kidney injury (AKI) is regional and affects cells heterogeneously. We first optimized coordination of spatial transcriptomics and single-nuclear sequencing data sets, mapping 30 dominant cell types to a human nephrectomy. The predicted cell-type spots corresponded with the underlying histopathology. To study the implications of AKI on transcript expression, we then characterized the spatial transcriptomic signature of 2 murine AKI models: ischemia/reperfusion injury (IRI) and cecal ligation puncture (CLP). Localized regions of reduced overall expression were associated with injury pathways. Using single-cell sequencing, we deconvoluted the signature of each spatial transcriptomic spot, identifying patterns of colocalization between immune and epithelial cells. Neutrophils infiltrated the renal medulla in the ischemia model. Atf3 was identified as a chemotactic factor in S3 proximal tubules. In the CLP model, infiltrating macrophages dominated the outer cortical signature, and Mdk was identified as a corresponding chemotactic factor. The regional distribution of these immune cells was validated with multiplexed CO-Detection by indEXing (CODEX) immunofluorescence. Spatial transcriptomic sequencing complemented single-cell sequencing by uncovering mechanisms driving immune cell infiltration and detection of relevant cell subpopulations.
MeSH term(s)	Acute Kidney Injury/immunology ; Acute Kidney Injury/metabolism ; Acute Kidney Injury/pathology ; Animals ; Epithelial Cells/immunology ; Epithelial Cells/metabolism ; Female ; Humans ; Kidney/immunology ; Kidney/metabolism ; Kidney/pathology ; Mice ; Middle Aged ; Reperfusion Injury/immunology ; Reperfusion Injury/metabolism ; Reperfusion Injury/pathology ; Single-Cell Analysis ; Transcriptome/genetics ; Transcriptome/immunology
Language	English
Publishing date	2021-06-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.147703
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Article: The chromatin landscape of healthy and injured cell types in the human kidney.

Gisch, Debora L / Brennan, Michelle / Lake, Blue B / Basta, Jeannine / Keller, Mark / Ferreira, Ricardo Melo / Akilesh, Shreeram / Ghag, Reetika / Lu, Charles / Cheng, Ying-Hua / Collins, Kimberly S / Parikh, Samir V / Rovin, Brad H / Robbins, Lynn / Conklin, Kimberly Y / Diep, Dinh / Zhang, Bo / Knoten, Amanda / Barwinska, Daria /

bioRxiv : the preprint server for biology

2023

Abstract	There is a need to define regions of gene activation or repression that control human kidney cells in states of health, injury, and repair to understand the molecular pathogenesis of kidney disease and design therapeutic strategies. However, comprehensive integration of gene expression with epigenetic features that define regulatory elements remains a significant challenge. We measured dual single nucleus RNA expression and chromatin accessibility, DNA methylation, and H3K27ac, H3K4me1, H3K4me3, and H3K27me3 histone modifications to decipher the chromatin landscape and gene regulation of the kidney in reference and adaptive injury states. We established a comprehensive and spatially-anchored epigenomic atlas to define the kidney's active, silent, and regulatory accessible chromatin regions across the genome. Using this atlas, we noted distinct control of adaptive injury in different epithelial cell types. A proximal tubule cell transcription factor network of
Language	English
Publishing date	2023-06-08
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.06.07.543965
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