Functional and molecular effects of TNF-α on human iPSC-derived cardiomyocytes

Treatment of human iPSC-cardiomyocytes with proinflammatory cytokine TNF-α resulted in increased ROS, caspase activity and cell death, as well as abnormal calcium handling and abnormal contractility. Numerous molecular pathways were affected that correlated to cardiomyocyte function, including up-re...

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Published inStem cell research Vol. 52; p. 102218
Main Authors Saraf, Anita, Rampoldi, Antonio, Chao, Myra, Li, Dong, Armand, Lawrence, Hwang, Hyun, Liu, Rui, Jha, Rajnesh, Fu, Haian, Maxwell, Joshua T., Xu, Chunhui
Format Journal Article
LanguageEnglish
Published England Elsevier B.V 01.04.2021
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Abstract Treatment of human iPSC-cardiomyocytes with proinflammatory cytokine TNF-α resulted in increased ROS, caspase activity and cell death, as well as abnormal calcium handling and abnormal contractility. Numerous molecular pathways were affected that correlated to cardiomyocyte function, including up-regulation of IL-32 (a human specific cytokine, not present in rodents) and IL-34. [Display omitted] •Cardiomyocytes from human iPSCs display numerous catabolic responses to TNF-α, similar to primary cardiomyocytes.•IL-32, a human specific cytokine, is most upregulated in hiPSC-cardiomyocytes response to TNF-α.•Glutamate receptors are markedly dysregulated in hiPSC-cardiomyocytes in addition to other ion channels in response to TNF-α.•TNF-α causes abnormal Ca+2 transients and propagation in hiPSC-CMs, creating a pro-arrhythmogenic substrate. Proinflammatory molecule tumor necrosis factor alpha (TNF-α) is predominantly elevated in cytokine storm as well as worsening cardiac function. Here we model the molecular and functional effects of TNF-α in cardiomyocytes (CMs) derived from human induced pluripotent stem cells (hiPSC). We found that treatment of hiPSC-CMs with TNF-α increased reactive oxygen species (ROS) and caspase 3/7 activity and caused cell death and apoptosis. TNF-α treatment also resulted in dysregulation of cardiomyocyte function with respect to the increased abnormal calcium handling, calcium wave propagation between cells and excitation–contraction coupling. We also uncovered significant changes in gene expression and protein localization caused by TNF-α treatment. Notably, TNF-α treatment altered the expression of ion channels, dysregulated cadherins, and affected the localization of gap-junction protein connexin-43. In addition, TNF-α treatment up-regulated IL-32 (a human specific cytokine, not present in rodents and an inducer of TNF-α) and IL-34 and down-regulated glutamate receptors and cardiomyocyte contractile proteins. These findings provide insights into the molecular and functional consequences from the exposure of human cardiomyocytes to TNF-α. Our study provides a model to incorporate inflammatory factors into hiPSC-CM-based studies to evaluate mechanistic aspects of heart disease.
AbstractList Treatment of human iPSC-cardiomyocytes with proinflammatory cytokine TNF-α resulted in increased ROS, caspase activity and cell death, as well as abnormal calcium handling and abnormal contractility. Numerous molecular pathways were affected that correlated to cardiomyocyte function, including up-regulation of IL-32 (a human specific cytokine, not present in rodents) and IL-34. [Display omitted] •Cardiomyocytes from human iPSCs display numerous catabolic responses to TNF-α, similar to primary cardiomyocytes.•IL-32, a human specific cytokine, is most upregulated in hiPSC-cardiomyocytes response to TNF-α.•Glutamate receptors are markedly dysregulated in hiPSC-cardiomyocytes in addition to other ion channels in response to TNF-α.•TNF-α causes abnormal Ca+2 transients and propagation in hiPSC-CMs, creating a pro-arrhythmogenic substrate. Proinflammatory molecule tumor necrosis factor alpha (TNF-α) is predominantly elevated in cytokine storm as well as worsening cardiac function. Here we model the molecular and functional effects of TNF-α in cardiomyocytes (CMs) derived from human induced pluripotent stem cells (hiPSC). We found that treatment of hiPSC-CMs with TNF-α increased reactive oxygen species (ROS) and caspase 3/7 activity and caused cell death and apoptosis. TNF-α treatment also resulted in dysregulation of cardiomyocyte function with respect to the increased abnormal calcium handling, calcium wave propagation between cells and excitation–contraction coupling. We also uncovered significant changes in gene expression and protein localization caused by TNF-α treatment. Notably, TNF-α treatment altered the expression of ion channels, dysregulated cadherins, and affected the localization of gap-junction protein connexin-43. In addition, TNF-α treatment up-regulated IL-32 (a human specific cytokine, not present in rodents and an inducer of TNF-α) and IL-34 and down-regulated glutamate receptors and cardiomyocyte contractile proteins. These findings provide insights into the molecular and functional consequences from the exposure of human cardiomyocytes to TNF-α. Our study provides a model to incorporate inflammatory factors into hiPSC-CM-based studies to evaluate mechanistic aspects of heart disease.
Proinflammatory molecule tumor necrosis factor alpha (TNF-α) is predominantly elevated in cytokine storm as well as worsening cardiac function. Here we model the molecular and functional effects of TNF-α in cardiomyocytes (CMs) derived from human induced pluripotent stem cells (hiPSC). We found that treatment of hiPSC-CMs with TNF-α increased reactive oxygen species (ROS) and caspase 3/7 activity and caused cell death and apoptosis. TNF-α treatment also resulted in dysregulation of cardiomyocyte function with respect to the increased abnormal calcium handling, calcium wave propagation between cells and excitation–contraction coupling. We also uncovered significant changes in gene expression and protein localization caused by TNF-α treatment. Notably, TNF-α treatment altered the expression of ion channels, dysregulated cadherins, and affected the localization of gap-junction protein connexin-43. In addition, TNF-α treatment up-regulated IL-32 (a human specific cytokine, not present in rodents and an inducer of TNF-α) and IL-34 and down-regulated glutamate receptors and cardiomyocyte contractile proteins. These findings provide insights into the molecular and functional consequences from the exposure of human cardiomyocytes to TNF-α. Our study provides a model to incorporate inflammatory factors into hiPSC-CM-based studies to evaluate mechanistic aspects of heart disease.
ArticleNumber 102218
Author Liu, Rui
Maxwell, Joshua T.
Saraf, Anita
Li, Dong
Rampoldi, Antonio
Hwang, Hyun
Xu, Chunhui
Chao, Myra
Fu, Haian
Armand, Lawrence
Jha, Rajnesh
AuthorAffiliation c Emory Chemical Biology Discovery Center and the Department of Pharmacology and Chemical Biology, Emory University School of Medicine, Atlanta, GA 30322, USA
d Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, GA 30322, USA
b Department of Pediatrics, Emory University School of Medicine and Children’s Healthcare of Atlanta, Atlanta, GA 30322, USA
e University of Pittsburgh, Department of Medicine and Pediatrics and McGowan Regenerative Institute, 200 Lothorop Street, PUH, Pittsburgh, PA 15213, USA
a Department of Medicine, Emory University School of Medicine, Atlanta, GA 30322, USA
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Keywords Cardiomyocytes
TNFα
Cytokines
Ca2+ transients
Ca2+propagation
Human iPSC
Ca(2+)propagation
Ca(2+) transients
Language English
License This is an open access article under the CC BY-NC-ND license.
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Snippet Treatment of human iPSC-cardiomyocytes with proinflammatory cytokine TNF-α resulted in increased ROS, caspase activity and cell death, as well as abnormal...
Proinflammatory molecule tumor necrosis factor alpha (TNF-α) is predominantly elevated in cytokine storm as well as worsening cardiac function. Here we model...
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StartPage 102218
SubjectTerms Ca2+ transients
Ca2+propagation
Calcium
Cardiomyocytes
Cell Differentiation
Cytokines
Human iPSC
Humans
Induced Pluripotent Stem Cells
Myocytes, Cardiac
TNFα
Tumor Necrosis Factor-alpha
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Title Functional and molecular effects of TNF-α on human iPSC-derived cardiomyocytes
URI https://dx.doi.org/10.1016/j.scr.2021.102218
https://www.ncbi.nlm.nih.gov/pubmed/33592567
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