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Article: Translating Organoids into Artificial Kidneys.

Kalejaiye, Titilola D / Barreto, Amanda D / Musah, Samira

Current transplantation reports

2022 Volume 9, Issue 4, Page(s) 276–286

Abstract: Purpose of review: Kidney disease affects more than 13% of the world population, and current treatment options are limited to dialysis and organ transplantation. The generation of kidney organoids from human-induced pluripotent stem (hiPS) cells could ... ...

Abstract	Purpose of review: Kidney disease affects more than 13% of the world population, and current treatment options are limited to dialysis and organ transplantation. The generation of kidney organoids from human-induced pluripotent stem (hiPS) cells could be harnessed to engineer artificial organs and help overcome the challenges associated with the limited supply of transplantable kidneys. The purpose of this article is to review the progress in kidney organoid generation and transplantation and highlight some existing challenges in the field. We also examined possible improvements that could help realize the potential of organoids as artificial organs or alternatives for kidney transplantation therapy. Recent findings: Organoids are useful for understanding the mechanisms of kidney development, and they provide robust platforms for drug screening, disease modeling, and generation of tissues for organ replacement therapies. Efforts to design organoids rely on the ability of cells to self-assemble and pattern themselves into recognizable tissues. While existing protocols for generating organoids result in multicellular structures reminiscent of the developing kidney, many do not yet fully recapitulate the complex cellular composition, structure, and functions of the intact kidney. Recent advances toward achieving these goals include identifying cell culture conditions that produce organoids with improved vasculature and cell maturation and functional states. Still, additional improvements are needed to enhance tissue patterning, specialization, and function, and avoid tumorigenicity after transplantation. Summary: This report focuses on kidney organoid studies, advancements and limitations, and future directions for improvements towards transplantation.
Language	English
Publishing date	2022-10-25
Publishing country	Switzerland
Document type	Journal Article ; Review
ISSN	2196-3029
ISSN	2196-3029
DOI	10.1007/s40472-022-00383-0
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Adriamycin-Induced Podocyte Injury Disrupts the YAP-TEAD1 Axis and Downregulates Cyr61 and CTGF Expression.

Burt, Morgan A / Kalejaiye, Titilola D / Bhattacharya, Rohan / Dimitrakakis, Nikolaos / Musah, Samira

ACS chemical biology

2021 Volume 17, Issue 12, Page(s) 3341–3351

Abstract: The most severe forms of kidney diseases are often associated with irreversible damage to the glomerular podocytes, the highly specialized epithelial cells that encase glomerular capillaries and regulate the removal of toxins and waste from the blood. ... ...

Abstract	The most severe forms of kidney diseases are often associated with irreversible damage to the glomerular podocytes, the highly specialized epithelial cells that encase glomerular capillaries and regulate the removal of toxins and waste from the blood. Several studies revealed significant changes to podocyte cytoskeletal structure during disease onset, suggesting possible roles of cellular mechanosensing in podocyte responses to injury. Still, this topic remains underexplored partly due to the lack of appropriate
MeSH term(s)	Humans ; Podocytes/metabolism ; Doxorubicin/pharmacology ; Connective Tissue Growth Factor/genetics ; Connective Tissue Growth Factor/metabolism ; Induced Pluripotent Stem Cells ; Signal Transduction ; TEA Domain Transcription Factors
Chemical Substances	Doxorubicin (80168379AG) ; Connective Tissue Growth Factor (139568-91-5) ; TEAD1 protein, human ; TEA Domain Transcription Factors
Language	English
Publishing date	2021-12-10
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1554-8937
ISSN (online)	1554-8937
DOI	10.1021/acschembio.1c00678
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Article: A Biomimetic Electrospun Membrane Supports the Differentiation and Maturation of Kidney Epithelium from Human Stem Cells.

Mou, Xingrui / Shah, Jessica / Bhattacharya, Rohan / Kalejaiye, Titilola D / Sun, Bowen / Hsu, Po-Chun / Musah, Samira

Bioengineering (Basel, Switzerland)

2022 Volume 9, Issue 5

Abstract: Podocytes derived from human induced pluripotent stem (hiPS) cells are enabling studies of kidney development and disease. However, many of these studies are carried out in traditional tissue culture plates that do not accurately recapitulate the ... ...

Abstract	Podocytes derived from human induced pluripotent stem (hiPS) cells are enabling studies of kidney development and disease. However, many of these studies are carried out in traditional tissue culture plates that do not accurately recapitulate the molecular and mechanical features necessary for modeling tissue- and organ-level functionalities. Overcoming these limitations requires the design and application of tunable biomaterial scaffolds. Silk fibroin is an attractive biomaterial due to its biocompatibility and versatility, which include its ability to form hydrogels, sponge-like scaffolds, and electrospun fibers and membranes appropriate for tissue engineering and biomedical applications. In this study, we show that hiPS cells can be differentiated into post-mitotic kidney glomerular podocytes on electrospun silk fibroin membranes functionalized with laminin. The resulting podocytes remain viable and express high levels of podocyte-specific markers consistent with the mature cellular phenotype. The resulting podocytes were propagated for at least two weeks, enabling secondary cell-based applications and analyses. This study demonstrates for the first time that electrospun silk fibroin membrane can serve as a supportive biocompatible platform for human podocyte differentiation and propagation. We anticipate that the results of this study will pave the way for the use of electrospun membranes and other biomimetic scaffolds for kidney tissue engineering, including the development of co-culture systems and organs-on-chips microphysiological devices.
Language	English
Publishing date	2022-04-26
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2746191-9
ISSN	2306-5354
ISSN	2306-5354
DOI	10.3390/bioengineering9050188
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Article: SARS-CoV-2 Employ BSG/CD147 and ACE2 Receptors to Directly Infect Human Induced Pluripotent Stem Cell-Derived Kidney Podocytes.

Kalejaiye, Titilola D / Bhattacharya, Rohan / Burt, Morgan A / Travieso, Tatianna / Okafor, Arinze E / Mou, Xingrui / Blasi, Maria / Musah, Samira

Frontiers in cell and developmental biology

2022 Volume 10, Page(s) 855340

Abstract: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes the Coronavirus disease 2019 (COVID-19), which has resulted in over 5.9 million deaths worldwide. While cells in the respiratory system are the initial target of SARS-CoV-2, there is ... ...

Abstract	Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes the Coronavirus disease 2019 (COVID-19), which has resulted in over 5.9 million deaths worldwide. While cells in the respiratory system are the initial target of SARS-CoV-2, there is mounting evidence that COVID-19 is a multi-organ disease. Still, the direct affinity of SARS-CoV-2 for cells in other organs such as the kidneys, which are often targeted in severe COVID-19, remains poorly understood. We employed a human induced pluripotent stem (iPS) cell-derived model to investigate the affinity of SARS-CoV-2 for kidney glomerular podocytes, and examined the expression of host factors for binding and processing of the virus. We studied cellular uptake of the live SARS-CoV-2 virus as well as a pseudotyped virus. Infection of podocytes with live SARS-CoV-2 or spike-pseudotyped lentiviral particles revealed cellular uptake even at low multiplicity of infection (MOI) of 0.01. We found that direct infection of human iPS cell-derived podocytes by SARS-CoV-2 virus can cause cell death and podocyte foot process retraction, a hallmark of podocytopathies and progressive glomerular diseases including collapsing glomerulopathy observed in patients with severe COVID-19 disease. We identified BSG/CD147 and ACE2 receptors as key mediators of spike binding activity in human iPS cell-derived podocytes. These results show that SARS-CoV-2 can infect kidney glomerular podocytes
Language	English
Publishing date	2022-04-20
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2737824-X
ISSN	2296-634X
ISSN	2296-634X
DOI	10.3389/fcell.2022.855340
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Article ; Online: A Biomimetic Electrospun Membrane Supports the Differentiation and Maturation of Kidney Epithelium from Human Stem Cells

Xingrui Mou / Jessica Shah / Rohan Bhattacharya / Titilola D. Kalejaiye / Bowen Sun / Po-Chun Hsu / Samira Musah

Bioengineering, Vol 9, Iss 188, p

2022 Volume 188

Abstract	Podocytes derived from human induced pluripotent stem (hiPS) cells are enabling studies of kidney development and disease. However, many of these studies are carried out in traditional tissue culture plates that do not accurately recapitulate the molecular and mechanical features necessary for modeling tissue- and organ-level functionalities. Overcoming these limitations requires the design and application of tunable biomaterial scaffolds. Silk fibroin is an attractive biomaterial due to its biocompatibility and versatility, which include its ability to form hydrogels, sponge-like scaffolds, and electrospun fibers and membranes appropriate for tissue engineering and biomedical applications. In this study, we show that hiPS cells can be differentiated into post-mitotic kidney glomerular podocytes on electrospun silk fibroin membranes functionalized with laminin. The resulting podocytes remain viable and express high levels of podocyte-specific markers consistent with the mature cellular phenotype. The resulting podocytes were propagated for at least two weeks, enabling secondary cell-based applications and analyses. This study demonstrates for the first time that electrospun silk fibroin membrane can serve as a supportive biocompatible platform for human podocyte differentiation and propagation. We anticipate that the results of this study will pave the way for the use of electrospun membranes and other biomimetic scaffolds for kidney tissue engineering, including the development of co-culture systems and organs-on-chips microphysiological devices.
Keywords	silk fibroin ; electrospinning ; stem cells ; human induced pluripotent stem cells ; podocytes ; biomaterials ; Technology ; T ; Biology (General) ; QH301-705.5
Subject code	571
Language	English
Publishing date	2022-04-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article: BSG/CD147 and ACE2 receptors facilitate SARS-CoV-2 infection of human iPS cell-derived kidney podocytes.

Kalejaiye, Titilola D / Bhattacharya, Rohan / Burt, Morgan A / Travieso, Tatianna / Okafor, Arinze E / Mou, Xingrui / Blasi, Maria / Musah, Samira

bioRxiv : the preprint server for biology

2021

Abstract: Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes the Coronavirus disease 2019 (COVID-19), which was declared a pandemic by the World Health Organization (WHO) in March 2020. The disease has caused more than 5.1 million ... ...

Abstract	Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes the Coronavirus disease 2019 (COVID-19), which was declared a pandemic by the World Health Organization (WHO) in March 2020. The disease has caused more than 5.1 million deaths worldwide. While cells in the respiratory system are frequently the initial target for SARS-CoV-2, clinical studies suggest that COVID-19 can become a multi-organ disease in the most severe cases. Still, the direct affinity of SARS-CoV-2 for cells in other organs such as the kidneys, which are often affected in severe COVID-19, remains poorly understood. Method: In this study, we employed a human induced pluripotent stem (iPS) cell-derived model to investigate the affinity of SARS-CoV-2 for kidney glomerular podocytes. We studied uptake of the live SARS-CoV-2 virus as well as pseudotyped viral particles by human iPS cell derived podocytes using qPCR, western blot, and immunofluorescence. Global gene expression and qPCR analyses revealed that human iPS cell-derived podocytes express many host factor genes (including ACE2, BSG/CD147, PLS3, ACTR3, DOCK7, TMPRSS2, CTSL CD209, and CD33) associated with SARS-CoV-2 binding and viral processing. Result: Infection of podocytes with live SARS-CoV-2 or spike-pseudotyped lentiviral particles revealed viral uptake by the cells at low Multiplicity of Infection (MOI of 0.01) as confirmed by RNA quantification and immunofluorescence studies. Our results also indicate that direct infection of human iPS cell-derived podocytes by SARS-CoV-2 virus can cause cell death and podocyte foot process retraction, a hallmark of podocytopathies and progressive glomerular diseases including collapsing glomerulopathy observed in patients with severe COVID-19 disease. Additionally, antibody blocking experiments identified BSG/CD147 and ACE2 receptors as key mediators of spike binding activity in human iPS cell-derived podocytes. Conclusion: These results show that SARS-CoV-2 can infect kidney glomerular podocytes Significant statement: Many patients with COVID19 disease exhibit multiorgan complications, suggesting that SARS-CoV-2 infection can extend beyond the respiratory system. Acute kidney injury is a common COVID-19 complication contributing to increased morbidity and mortality. Still, SARS-Cov-2 affinity for specialized kidney cells remain less clear. By leveraging our protocol for stem cell differentiation, we show that SARS-CoV-2 can directly infect kidney glomerular podocytes by using multiple Spike-binding proteins including ACE2 and BSG/CD147. Our results also indicate that infection by SARS-CoV-2 virus can cause podocyte cell death and foot process effacement, a hallmark of podocytopathies including collapsing glomerulopathy observed in patients with severe COVID-19 disease. This stem cell-derived model is potentially useful for kidney-specific antiviral drug screening and mechanistic studies of COVID-19 organotropism.
Language	English
Publishing date	2021-11-17
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.11.16.468893
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Article ; Online: Tetrahydrophthalazinone Inhibitor of Phosphodiesterase with

de Araújo, Julianna Siciliano / Peres, Raiza Brandão / Bernardino da Silva, Patrícia / Batista, Marcos Meuser / Sterk, Geert Jan / Maes, Louis / Caljon, Guy / Leurs, Rob / de Koning, Harry P / Kalejaiye, Titilola D / Soeiro, Maria de Nazaré Correia

Antimicrobial agents and chemotherapy

2021 Volume 65, Issue 3

Abstract: The phosphodiesterase inhibitor tetrahydrophthalazinone NPD-008 was explored by ... ...

Abstract	The phosphodiesterase inhibitor tetrahydrophthalazinone NPD-008 was explored by phenotypic
MeSH term(s)	Antiprotozoal Agents/therapeutic use ; Chagas Disease/drug therapy ; Humans ; Leishmania mexicana ; Phosphoric Diester Hydrolases ; Trypanosoma cruzi
Chemical Substances	Antiprotozoal Agents ; Phosphoric Diester Hydrolases (EC 3.1.4.-)
Language	English
Publishing date	2021-02-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	217602-6
ISSN	1098-6596 ; 0066-4804
ISSN (online)	1098-6596
ISSN	0066-4804
DOI	10.1128/AAC.00960-20
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Article ; Online: BSG/CD147 and ACE2 receptors facilitate SARS-CoV-2 infection of human iPS cell-derived kidney podocytes

Kalejaiye, Titilola D / Bhattacharya, Rohan / Burt, Morgan A / Travieso, Tatianna / Okafor, Arinze E / Mou, Xingrui / Blasi, Maria / Musah, Samira

bioRxiv

Abstract	Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes the Coronavirus disease 2019 (COVID-19), which was declared a pandemic by the World Health Organization (WHO) in March 2020. The disease has caused more than 5.1 million deaths worldwide. While cells in the respiratory system are frequently the initial target for SARS-CoV-2, clinical studies suggest that COVID-19 can become a multi-organ disease in the most severe cases. Still, the direct affinity of SARS-CoV-2 for cells in other organs such as the kidneys, which are often affected in severe COVID-19, remains poorly understood. Method: In this study, we employed a human induced pluripotent stem (iPS) cell-derived model to investigate the affinity of SARS-CoV-2 for kidney glomerular podocytes. We studied uptake of the live SARS-CoV-2 virus as well as pseudotyped viral particles by human iPS cell derived podocytes using qPCR, western blot, and immunofluorescence. Global gene expression and qPCR analyses revealed that human iPS cell-derived podocytes express many host factor genes (including ACE2, BSG/CD147, PLS3, ACTR3, DOCK7, TMPRSS2, CTSL CD209, and CD33) associated with SARS-CoV-2 binding and viral processing. Result: Infection of podocytes with live SARS-CoV-2 or spike-pseudotyped lentiviral particles revealed viral uptake by the cells at low Multiplicity of Infection (MOI of 0.01) as confirmed by RNA quantification and immunofluorescence studies. Our results also indicate that direct infection of human iPS cell-derived podocytes by SARS-CoV-2 virus can cause cell death and podocyte foot process retraction, a hallmark of podocytopathies and progressive glomerular diseases including collapsing glomerulopathy observed in patients with severe COVID-19 disease. Additionally, antibody blocking experiments identified BSG/CD147 and ACE2 receptors as key mediators of spike binding activity in human iPS cell-derived podocytes. Conclusion: These results show that SARS-CoV-2 can infect kidney glomerular podocytes in vitro. These results also show that the uptake of SARS-CoV-2 by kidney podocytes occurs via multiple binding interactions and partners, which may underlie the high affinity of SARS-CoV-2 for kidney tissues. This stem cell-derived model is potentially useful for kidney-specific antiviral drug screening and mechanistic studies of COVID-19 organotropism.
Keywords	covid19
Language	English
Publishing date	2021-11-17
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2021.11.16.468893
Database	COVID19

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Article: The ever unfolding story of cAMP signaling in trypanosomatids: vive la difference!

Tagoe, Daniel N A / Kalejaiye, Titilola D / de Koning, Harry P

Frontiers in pharmacology

2015 Volume 6, Page(s) 185

Abstract: ... cyclic nucleotide-specific phosphodiesterases (PDEA-D), which have highly similar catalytic domains to that of human ...

Abstract	Kinetoplastids are unicellular, eukaryotic, flagellated protozoans containing the eponymous kinetoplast. Within this order, the family of trypanosomatids are responsible for some of the most serious human diseases, including Chagas disease (Trypanosoma cruzi), sleeping sickness (Trypanosoma brucei spp.), and leishmaniasis (Leishmania spp). Although cAMP is produced during the life cycle stages of these parasites, its signaling pathways are very different from those of mammals. The absence of G-protein-coupled receptors, the presence of structurally different adenylyl cyclases, the paucity of known cAMP effector proteins and the stringent need for regulation of cAMP in the small kinetoplastid cells all suggest a significantly different biochemical pathway and likely cell biology. However, each of the main kinetoplastid parasites express four class 1-type cyclic nucleotide-specific phosphodiesterases (PDEA-D), which have highly similar catalytic domains to that of human PDEs. To date, only TbrPDEB, expressed as two slightly different isoforms TbrPDEB1 and B2, has been found to be essential when ablated. Although the genomes contain reasonably well conserved genes for catalytic and regulatory domains of protein kinase A, these have been shown to have varied structural and functional roles in the different species. Recent discovery of a role of cAMP/AMP metabolism in a quorum-sensing signaling pathway in T. brucei, and the identification of downstream cAMP Response Proteins (CARPs) whose expression levels correlate with sensitivity to PDE inhibitors, suggests a complex signaling cascade. The interplay between the roles of these novel CARPs and the quorum-sensing signaling pathway on cell division and differentiation makes for intriguing cell biology and a new paradigm in cAMP signal transduction, as well as potential targets for trypanosomatid-specific cAMP pathway-based therapeutics.
Language	English
Publishing date	2015-09-07
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2587355-6
ISSN	1663-9812
ISSN	1663-9812
DOI	10.3389/fphar.2015.00185
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Article ; Online: Imidazole Derivatives as Promising Agents for the Treatment of Chagas Disease.

de Araújo, Julianna Siciliano / García-Rubia, Alfonso / Sebastián-Pérez, Victor / Kalejaiye, Titilola D / Bernardino da Silva, Patrícia / Fonseca-Berzal, Cristina Rosa / Maes, Louis / De Koning, Harry P / Soeiro, Maria de Nazaré Correia / Gil, Carmen

Antimicrobial agents and chemotherapy

2019 Volume 63, Issue 4

Abstract: More than 100 years after being first described, Chagas disease remains endemic in 21 Latin American countries and has spread to other continents. Indeed, this disease, which is caused by the protozoan ... ...

Abstract	More than 100 years after being first described, Chagas disease remains endemic in 21 Latin American countries and has spread to other continents. Indeed, this disease, which is caused by the protozoan parasite
MeSH term(s)	3',5'-Cyclic-AMP Phosphodiesterases/antagonists & inhibitors ; Animals ; Antiparasitic Agents/pharmacology ; Autophagy/drug effects ; Cells, Cultured ; Chagas Disease/drug therapy ; Drug Discovery ; Imidazoles/chemical synthesis ; Imidazoles/pharmacology ; Mice ; Parasitic Sensitivity Tests ; Structure-Activity Relationship ; Trypanosoma cruzi/drug effects
Chemical Substances	Antiparasitic Agents ; Imidazoles ; 3',5'-Cyclic-AMP Phosphodiesterases (EC 3.1.4.17)
Language	English
Publishing date	2019-03-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	217602-6
ISSN	1098-6596 ; 0066-4804
ISSN (online)	1098-6596
ISSN	0066-4804
DOI	10.1128/AAC.02156-18
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