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Article ; Online: Hippo signaling and histone methylation control cardiomyocyte cell cycle re-entry through distinct transcriptional pathways

Zhenhe Zhang / Miles Freeman / Yiqiang Zhang / Danny El-Nachef / George Davenport / Allison Williams / W. Robb MacLellan

PLoS ONE, Vol 18, Iss

2023 Volume 2

Abstract: Aims Accumulating data demonstrates that new adult cardiomyocytes (CMs) are generated throughout life from pre-existing CMs, although the absolute magnitude of CM self-renewal is very low. Modifying epigenetic histone modifications or activating the ... ...

Abstract	Aims Accumulating data demonstrates that new adult cardiomyocytes (CMs) are generated throughout life from pre-existing CMs, although the absolute magnitude of CM self-renewal is very low. Modifying epigenetic histone modifications or activating the Hippo-Yap pathway have been shown to promote adult CM cycling and proliferation. Whether these interventions work through common pathways or act independently is unknown. For the first time we have determined whether lysine demethylase 4D (KDM4D)-mediated CM-specific H3K9 demethylation and Hippo pathways inhibition have additive or redundant roles in promoting CM cell cycle re-entry. Methods and results We found that activating Yap1 in cultured neonatal rat ventricular myocytes (NRVM) through overexpressing Hippo pathway inhibitor, miR-199, preferentially increased S-phase CMs, while H3K9me3 demethylase KDM4D preferentially increased G2/M markers in CMs. Together KDM4D and miR-199 further increased total cell number of NRVMs in culture. Inhibition of Hippo signaling via knock-down of Salvador Family WW Domain Containing Protein 1 (Sav1) also led to S-phase reactivation and additional cell cycle re-entry was seen when combined with KDM4D overexpression. Inducible activating KDM4D (iKDM4D) in adult transgenic mice together with shRNA mediated knock-down of Sav1 (iKDM4D+Sav1-sh) resulted in a significant increase in cycling CMs compared to either intervention alone. KDM4D preferentially induced expression of genes regulating late (G2/M) phases of the cell cycle, while miR-199 and si-Sav1 preferentially up-regulated genes involved in G1/S phase. KDM4D upregulated E2F1 and FoxM1 expression, whereas miR-199 and si-Sav1 induced Myc. Using transgenic mice over-expressing KDM4D together with Myc, we demonstrated that KDM4D/Myc significantly increased CM cell cycling but did not affect cardiac function. Conclusions KDM4D effects on CM cell cycle activity are additive with the Hippo-Yap1 pathway and appear to preferentially regulate different cell cycle regulators. This may ...
Keywords	Medicine ; R ; Science ; Q
Subject code	500
Language	English
Publishing date	2023-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
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Article ; Online: Hippo signaling and histone methylation control cardiomyocyte cell cycle re-entry through distinct transcriptional pathways.

Zhenhe Zhang / Miles Freeman / Yiqiang Zhang / Danny El-Nachef / George Davenport / Allison Williams / W Robb MacLellan

PLoS ONE, Vol 18, Iss 2, p e

2023 Volume 0281610

Abstract	Aims Accumulating data demonstrates that new adult cardiomyocytes (CMs) are generated throughout life from pre-existing CMs, although the absolute magnitude of CM self-renewal is very low. Modifying epigenetic histone modifications or activating the Hippo-Yap pathway have been shown to promote adult CM cycling and proliferation. Whether these interventions work through common pathways or act independently is unknown. For the first time we have determined whether lysine demethylase 4D (KDM4D)-mediated CM-specific H3K9 demethylation and Hippo pathways inhibition have additive or redundant roles in promoting CM cell cycle re-entry. Methods and results We found that activating Yap1 in cultured neonatal rat ventricular myocytes (NRVM) through overexpressing Hippo pathway inhibitor, miR-199, preferentially increased S-phase CMs, while H3K9me3 demethylase KDM4D preferentially increased G2/M markers in CMs. Together KDM4D and miR-199 further increased total cell number of NRVMs in culture. Inhibition of Hippo signaling via knock-down of Salvador Family WW Domain Containing Protein 1 (Sav1) also led to S-phase reactivation and additional cell cycle re-entry was seen when combined with KDM4D overexpression. Inducible activating KDM4D (iKDM4D) in adult transgenic mice together with shRNA mediated knock-down of Sav1 (iKDM4D+Sav1-sh) resulted in a significant increase in cycling CMs compared to either intervention alone. KDM4D preferentially induced expression of genes regulating late (G2/M) phases of the cell cycle, while miR-199 and si-Sav1 preferentially up-regulated genes involved in G1/S phase. KDM4D upregulated E2F1 and FoxM1 expression, whereas miR-199 and si-Sav1 induced Myc. Using transgenic mice over-expressing KDM4D together with Myc, we demonstrated that KDM4D/Myc significantly increased CM cell cycling but did not affect cardiac function. Conclusions KDM4D effects on CM cell cycle activity are additive with the Hippo-Yap1 pathway and appear to preferentially regulate different cell cycle regulators. This may ...
Keywords	Medicine ; R ; Science ; Q
Subject code	500
Language	English
Publishing date	2023-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Evaluation of an automated grid artifact detection system for quality control in digital mammography.

MacLellan, Christopher J / Layman, Rick R / Geiser, William / Gress, Dustin A / Jones, A Kyle

Medical physics

2019 Volume 46, Issue 8, Page(s) 3442–3450

Abstract: Purpose: Grid artifacts occur in digital mammography when synchronization between the grid assembly and generator is not achieved, including when malfunctions occur in the grid assembly or generator subsystems. Such artifacts are not explicitly ... ...

Abstract	Purpose: Grid artifacts occur in digital mammography when synchronization between the grid assembly and generator is not achieved, including when malfunctions occur in the grid assembly or generator subsystems. Such artifacts are not explicitly monitored or evaluated by existing mammography quality control programs. In this study, we developed an automated method for quantifying the presence of grid artifacts in two-dimensional (2D) digital mammography images and assessed its utility as a supplement to existing quality control programs. Methods: Four digital mammography systems (Hologic Dimensions 3D 5000) were configured to automatically transfer 2D images to a server where the strength of the grid pattern, γ Results: All systems exhibited a gradual increase in γ Conclusions: Automated monitoring of
MeSH term(s)	Algorithms ; Artifacts ; Automation ; Humans ; Mammography ; Phantoms, Imaging ; Quality Control
Language	English
Publishing date	2019-06-27
Publishing country	United States
Document type	Evaluation Study ; Journal Article
ZDB-ID	188780-4
ISSN	2473-4209 ; 0094-2405
ISSN (online)	2473-4209
ISSN	0094-2405
DOI	10.1002/mp.13621
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Article ; Online: JACC: Basic to Translational Science

Annex, Brian H / Bristow, Michael R / Frangogiannis, Nikolaos G / Kelly, Daniel P / Kontaridis, Maria I / Libby, Peter / Robb MacLellan, William / McNamara, Coleen A / Mann, Douglas L / Pitt, Geoffrey S / Sipido, Karin R

JACC. Basic to translational science

2022 Volume 7, Issue 2, Page(s) 192

Language	English
Publishing date	2022-02-28
Publishing country	United States
Document type	Editorial
ISSN	2452-302X
ISSN (online)	2452-302X
DOI	10.1016/j.jacbts.2022.01.007
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Article: Association of vesicoureteral reflux and gastroesophageal reflux disease in children: A population-based study.

Hosier, Gregory W / McKay, Jeffrey P / Thomas, Heather Lynn / Romao, Rodrigo / Szudek, Ewa / MacLellan, Dawn L

Canadian Urological Association journal = Journal de l'Association des urologues du Canada

2020 Volume 14, Issue 9, Page(s) E432–E434

Abstract: Introduction: Practitioners have anecdotally hinted at a possible association between gastroesophageal reflux disease (GERD) and vesicoureteral reflux (VUR). We sought to identify an association in diagnosis between GERD and VUR using a population-based ...

Abstract	Introduction: Practitioners have anecdotally hinted at a possible association between gastroesophageal reflux disease (GERD) and vesicoureteral reflux (VUR). We sought to identify an association in diagnosis between GERD and VUR using a population-based dataset in a well-defined geographic area covered by a single-payer healthcare system. Methods: A retrospective review of individuals aged 0-16 years registered in the Nova Scotia Medical Service Insurance database from January 1997 to December 2012 was completed. Presence of GERD and VUR were ascertained based on billing codes. The baseline prevalence of GERD and VUR was calculated for this population for the same time period. Proportions of VUR patients with and without GERD were compared. The risk of being diagnosed with VUR in patients with GERD controlling for sex was calculated. Results: Of 404 300 patients identified, 6.6% had a diagnosis of GERD (n=27 092), 0.33% had a diagnosis of VUR (n=1348), and 0.08% were diagnosed with both (n=327). Among patients with VUR, the prevalence of GERD was 24.3% compared to 6.6% in patients without VUR (p<0.0001). Among patients with GERD, the prevalence of VUR was 1.2% compared to 0.27% in patients without (p<0.0001). The risk of being diagnosed with VUR was higher in the presence of GERD (odds ratio [OR] 4.49; 95% confidence interval [CI] 3.96-5.09; p<0.0001), irrespective of sex. Conclusions: The odds of being diagnosed with VUR is more than 4.5 times higher in an individual with GERD. The clinical significance of this association remains to be explored.
Language	English
Publishing date	2020-04-03
Publishing country	Canada
Document type	Journal Article
ZDB-ID	2431403-1
ISSN	1911-6470
ISSN	1911-6470
DOI	10.5489/cuaj.6308
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Article: Psychosocial Distress in Parents with Children Awaiting Surgery during the COVID-19 Pandemic.

Forner, David / Leslie, Patricia K / Aldaihani, Abdullah / Bezuhly, Michael / Noel, Christopher W / Horne, David / Walling, Simon / Robitaille, Johane / MacLellan, Dawn L / El-Hawary, Ron / Logan, Karl / Romao, Rodrigo / LaRoche, Robert / Sett, Suvro / Urquhart, Robin / Hong, Paul

Children (Basel, Switzerland)

2022 Volume 9, Issue 1

Abstract: Due to resource restrictions related to the COVID-19 pandemic, many pediatric patients are facing substantial delays for surgery, potentially resulting in additional distress for caregivers. We aimed to assess the experiences and psychosocial distress of ...

Abstract	Due to resource restrictions related to the COVID-19 pandemic, many pediatric patients are facing substantial delays for surgery, potentially resulting in additional distress for caregivers. We aimed to assess the experiences and psychosocial distress of parents during COVID-19 as they relate to the pandemic, waiting for surgery, and the combined effects of both events. The was a cross-sectional qualitative study. Parents with children who faced treatment delays during the initial wave of the COVID-19 pandemic for elective, non-emergent procedures across a variety of surgical specialties were recruited. Semi-structured telephone interviews and thematic analysis were utilized. Thematic saturation was reached with eighteen participants. Four themes were identified: coping with COVID-19, distress levels, quality and nature of communication with the surgical team, and the experience of COVID-19 related hospital restrictions. Participants reported varying levels of distress due to the delay in surgery, such as the fear of developmental delay or disease progression for their child. They also indicated their own physical and mental health had been impacted by emotional distress related to both COVID-19 and delays in treatment. Most participants experienced the COVID-19-related hospital restrictions as distressing. This related predominantly to limiting in-hospital caregivers to only one caregiver. Participants were found to have substantial levels of psychosocial distress. Targeted social and emotional support may be helpful in reducing parental distress as the pandemic timeframe continues. Within the limits of individual health systems, reducing restrictions to the number of allowed care givers may help allay distress felt by parents.
Language	English
Publishing date	2022-01-09
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2732685-8
ISSN	2227-9067
ISSN	2227-9067
DOI	10.3390/children9010087
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Article ; Online: Gene editing to prevent ventricular arrhythmias associated with cardiomyocyte cell therapy.

Marchiano, Silvia / Nakamura, Kenta / Reinecke, Hans / Neidig, Lauren / Lai, Michael / Kadota, Shin / Perbellini, Filippo / Yang, Xiulan / Klaiman, Jordan M / Blakely, Leslie P / Karbassi, Elaheh / Fields, Paul A / Fenix, Aidan M / Beussman, Kevin M / Jayabalu, Anu / Kalucki, Faith A / Potter, Jennifer C / Futakuchi-Tsuchida, Akiko / Weber, Gerhard J /

Dupras, Sarah / Tsuchida, Hiroshi / Pabon, Lil / Wang, Lili / Knollmann, Björn C / Kattman, Steven / Thies, R Scott / Sniadecki, Nathan / MacLellan, W Robb / Bertero, Alessandro / Murry, Charles E

Cell stem cell

2023 Volume 30, Issue 5, Page(s) 741

Language	English
Publishing date	2023-04-25
Publishing country	United States
Document type	Published Erratum
ZDB-ID	2375354-7
ISSN	1875-9777 ; 1934-5909
ISSN (online)	1875-9777
ISSN	1934-5909
DOI	10.1016/j.stem.2023.04.010
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Article ; Online: Gene editing to prevent ventricular arrhythmias associated with cardiomyocyte cell therapy.

Dupras, Sarah / Tsuchida, Hiroshi / Pabon, Lil / Wang, Lili / Knollmann, Björn C / Kattman, Steven / Thies, R Scott / Sniadecki, Nathan / MacLellan, W Robb / Bertero, Alessandro / Murry, Charles E

Cell stem cell

2023 Volume 30, Issue 4, Page(s) 396–414.e9

Abstract: Human pluripotent stem cell-derived cardiomyocytes (hPSC-CMs) offer a promising cell-based therapy for myocardial infarction. However, the presence of transitory ventricular arrhythmias, termed engraftment arrhythmias (EAs), hampers clinical applications. ...

Abstract	Human pluripotent stem cell-derived cardiomyocytes (hPSC-CMs) offer a promising cell-based therapy for myocardial infarction. However, the presence of transitory ventricular arrhythmias, termed engraftment arrhythmias (EAs), hampers clinical applications. We hypothesized that EA results from pacemaker-like activity of hPSC-CMs associated with their developmental immaturity. We characterized ion channel expression patterns during maturation of transplanted hPSC-CMs and used pharmacology and genome editing to identify those responsible for automaticity in vitro. Multiple engineered cell lines were then transplanted in vivo into uninjured porcine hearts. Abolishing depolarization-associated genes HCN4, CACNA1H, and SLC8A1, along with overexpressing hyperpolarization-associated KCNJ2, creates hPSC-CMs that lack automaticity but contract when externally stimulated. When transplanted in vivo, these cells engrafted and coupled electromechanically with host cardiomyocytes without causing sustained EAs. This study supports the hypothesis that the immature electrophysiological prolife of hPSC-CMs mechanistically underlies EA. Thus, targeting automaticity should improve the safety profile of hPSC-CMs for cardiac remuscularization.
MeSH term(s)	Humans ; Animals ; Swine ; Myocytes, Cardiac/metabolism ; Gene Editing ; Cell Line ; Arrhythmias, Cardiac/genetics ; Arrhythmias, Cardiac/therapy ; Arrhythmias, Cardiac/metabolism ; Cell- and Tissue-Based Therapy ; Cell Differentiation/genetics
Language	English
Publishing date	2023-04-06
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2375354-7
ISSN	1875-9777 ; 1934-5909
ISSN (online)	1875-9777
ISSN	1934-5909
DOI	10.1016/j.stem.2023.03.010
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Article ; Online: Pharmacologic therapy for engraftment arrhythmia induced by transplantation of human cardiomyocytes.

Nakamura, Kenta / Neidig, Lauren E / Yang, Xiulan / Weber, Gerhard J / El-Nachef, Danny / Tsuchida, Hiroshi / Dupras, Sarah / Kalucki, Faith A / Jayabalu, Anu / Futakuchi-Tsuchida, Akiko / Nakamura, Daisy S / Marchianò, Silvia / Bertero, Alessandro / Robinson, Melissa R / Cain, Kevin / Whittington, Dale / Tian, Rong / Reinecke, Hans / Pabon, Lil /

Knollmann, Björn C / Kattman, Steven / Thies, R Scott / MacLellan, W Robb / Murry, Charles E

Stem cell reports

2021 Volume 16, Issue 10, Page(s) 2473–2487

Abstract: Heart failure remains a significant cause of morbidity and mortality following myocardial infarction. Cardiac remuscularization with transplantation of human pluripotent stem cell-derived cardiomyocytes is a promising preclinical therapy to restore ... ...

Abstract	Heart failure remains a significant cause of morbidity and mortality following myocardial infarction. Cardiac remuscularization with transplantation of human pluripotent stem cell-derived cardiomyocytes is a promising preclinical therapy to restore function. Recent large animal data, however, have revealed a significant risk of engraftment arrhythmia (EA). Although transient, the risk posed by EA presents a barrier to clinical translation. We hypothesized that clinically approved antiarrhythmic drugs can prevent EA-related mortality as well as suppress tachycardia and arrhythmia burden. This study uses a porcine model to provide proof-of-concept evidence that a combination of amiodarone and ivabradine can effectively suppress EA. None of the nine treated subjects experienced the primary endpoint of cardiac death, unstable EA, or heart failure compared with five out of eight (62.5%) in the control cohort (hazard ratio = 0.00; 95% confidence interval: 0-0.297; p = 0.002). Pharmacologic treatment of EA may be a viable strategy to improve safety and allow further clinical development of cardiac remuscularization therapy.
MeSH term(s)	Amiodarone/therapeutic use ; Animals ; Anti-Arrhythmia Agents/therapeutic use ; Arrhythmias, Cardiac/drug therapy ; Cell Line ; Cell- and Tissue-Based Therapy/adverse effects ; Disease Models, Animal ; Drug Combinations ; Humans ; Ivabradine/therapeutic use ; Male ; Myocardial Infarction/drug therapy ; Myocytes, Cardiac/transplantation ; Pluripotent Stem Cells/transplantation ; Stem Cell Transplantation/adverse effects ; Swine ; Tachycardia/drug therapy
Chemical Substances	Anti-Arrhythmia Agents ; Drug Combinations ; Ivabradine (3H48L0LPZQ) ; Amiodarone (N3RQ532IUT)
Language	English
Publishing date	2021-09-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2720528-9
ISSN	2213-6711 ; 2213-6711
ISSN (online)	2213-6711
ISSN	2213-6711
DOI	10.1016/j.stemcr.2021.08.005
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Article: Advances in the molecular mechanisms of heart failure.

MacLellan, W R

Current opinion in cardiology

2000 Volume 15, Issue 3, Page(s) 128–135

Abstract: Congestive heart failure is a common clinical problem resulting in significant morbidity and mortality. Although considerable progress has been made in elucidating the pathophysiologic mechanisms that lead to the development of this process, much remains ...

Abstract	Congestive heart failure is a common clinical problem resulting in significant morbidity and mortality. Although considerable progress has been made in elucidating the pathophysiologic mechanisms that lead to the development of this process, much remains unknown. The techniques of modern molecular biology now allow a detailed and systematic analysis of this disease. Recent data linking cardiac hypertrophy, aberrant signaling, or cytoskeletal abnormalities to the development of heart failure have provided new insights into this process. These studies have confirmed the importance of many classical pathways but also revealed novel pathways. This review will focus on the recent advances that have been made and will highlight the importance they have had in our understanding and treatment of heart failure.
MeSH term(s)	Angiotensins/physiology ; Antigens, CD/physiology ; Apoptosis/physiology ; Calcineurin/physiology ; Cardiomegaly/complications ; Cytokine Receptor gp130 ; Cytokines/physiology ; Cytoskeleton/physiology ; Gene Expression/physiology ; Growth Substances/physiology ; Heart Failure/complications ; Heart Failure/etiology ; Heart Failure/pathology ; Heart Failure/physiopathology ; Heart Failure/therapy ; Hemodynamics ; Humans ; Membrane Glycoproteins/physiology ; Molecular Biology ; Protein Kinases/physiology ; Signal Transduction/physiology
Chemical Substances	Angiotensins ; Antigens, CD ; Cytokines ; Growth Substances ; IL6ST protein, human ; Membrane Glycoproteins ; Cytokine Receptor gp130 (133483-10-0) ; Protein Kinases (EC 2.7.-) ; Calcineurin (EC 3.1.3.16)
Language	English
Publishing date	2000-05
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	645186-x
ISSN	1531-7080 ; 0268-4705
ISSN (online)	1531-7080
ISSN	0268-4705
DOI	10.1097/00001573-200005000-00002
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