Molecular and Functional Changes in Voltage-Gated Na+ Channels in Cardiomyocytes During Mouse Embryogenesis

Yu, Liangzhu; Gao, Shijun; Tang, Ming; Huang, Weifeng; Luo, Haitao; Hu, Xiao; Xi, Jun; Zhu, Minyan; Zheng, Yongqiang; Gao, Lina; Zhang, Lanqiu; Song, Yuanlong; Hescheler, Jürgen; Liang, Huamin

doi:10.1253/circj.cj-10-1212

Cited by 12 publications

(13 citation statements)

References 36 publications

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“…4,13, 14 Human embryonic stem cell-derived cardiomyocytes (hESCCMs) are reported to follow a roughly similar maturation process to that reported both in vivo and in an in-vitro murine ES model. 19- 24 The hiPSC-CMs in the present study showed a similar maturation process to that of hESC-CMs. 25 At first, narrow, diffusely distributed, and frequently not well aligned myofibrils, resembling those of hiPSC-CMs at 14 days, developed into sarcomeres with clear band patterns including the Z-, I-, and A-bands, responding to hiPSC-CMs at between 30 and 90 days, and ultimately resulted in the generation of welldesigned sarcomeres with A-, H-, I-, and M-bands.…”

Section: Discussionsupporting

confidence: 59%

Ultrastructural Maturation of Human-Induced Pluripotent Stem Cell-Derived Cardiomyocytes in a Long-Term Culture

Kamakura

Makiyama

Sasaki

et al. 2013

Circ J

262

224

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Background:In the short-to mid-term, cardiomyocytes generated from human-induced pluripotent stem cells (hiPSC-CMs) have been reported to be less mature than those of adult hearts. However, the maturation process in a long-term culture remains unknown. Methods and Results:A hiPSC clone generated from a healthy control was differentiated into CMs through embryoid body (EB) formation. The ultrastructural characteristics and gene expressions of spontaneously contracting EBs were analyzed through 1-year of culture after cardiac differentiation was initiated. The 14-day-old EBs contained a low number of myofibrils, which lacked alignment, and immature high-density Z-bands lacking A-, H-, I-, and Mbands. Through the long-term culture up to 180 days, the myofibrils became more tightly packed and formed parallel arrays accompanied by the appearance of mature Z-, A-, H-, and I-bands, but not M-bands. Notably, M-bands were finally detected in 360-day-old EBs. The expression levels of the M-band-specific genes in hiPSC-CMs remained lower in comparison with those in the adult heart. Immunocytochemistry indicated increasing number of MLC2v-positive/MLC2a-negative cells with decreasing number of MLC2v/MLC2a double-positive cells, indicating maturing of ventricular-type CMs. Conclusions:The structural maturation process of hiPSC-CMs through 1-year of culture revealed ultrastructural sarcomeric changes accompanied by delayed formation of M-bands. Our study provides new insight into the maturation process of hiPSC-CMs. (Circ J 2013; 77: 1307 -1314

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Section: Discussionsupporting

confidence: 59%

Ultrastructural Maturation of Human-Induced Pluripotent Stem Cell-Derived Cardiomyocytes in a Long-Term Culture

Kamakura

Makiyama

Sasaki

et al. 2013

Circ J

262

224

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“…I Na current density at early phases of mouse embryonic development (E11–E13) is low (around ‐10 pA/pF) and some cardiomyocytes (22%) present only L‐type calcium current; by E17–E20 I Na was found in all the cell tested and the current density was markedly increased (around ‐120 pA/pF) (Davies et al, ; van den Heuvel et al, ). Further studies evidenced that Na v 1.5 expression increases perinatally and postnatally (Harrell et al, ; Yu et al, ). In humans, the study of I Na expression during in vivo development are limited.…”

Section: Sodium Current (Ina)mentioning

confidence: 99%

Human derived cardiomyocytes: A decade of knowledge after the discovery of induced pluripotent stem cells

Barbuti

Benzoni

Campostrini

et al. 2016

Developmental Dynamics

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Ten years ago Yamanaka's lab identified a way to reprogram terminally differentiated cells to a pluripotent state, similar to that of embryonic stem cell. This procedure opened the road for the generation of postmitotic human cells, that have completely lost the replication potential. The initial excitement waned when it was observed that the cells produced by this method are somehow immature and do not resemble the adult phenotype. In the absence of cellular markers that recognize the various maturation steps of induced pluripotent stem cell-derived human cardiomyocytes, we propose to follow their maturation looking at their electrophysiological profile. For this reason, we are first reviewing the most common methods of differentiation, from the preliminary complex procedures to the newly-identified two-step protocols and, second, we report the electrical characteristics of the cells, through electrophysiological analysis of ionic currents that give rise to the action potential. We are aware that each protocol leads to the generation of different cardiomyocyte precursors, thus suggesting the need for a wider standardization. The identification of the electrophysiological characteristics of the cells could help in identifying the type and the maturation stage of the obtained cardiomyocyte, thus compensating for the lack of specific markers. Developmental Dynamics 245:1145-1158,

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“…In excitable cells, I Na maturation is characterized by changes in the voltage dependence of activation and inactivation (Cummins et al, 1994;Costa, 1996;Gao & Ziskind-Conhaim, 1998;Fry, 2006;Donnelly, 2011;Yu et al, 2011;Tadros et al, 2015;Calvigioni et al, 2017). It is believed that these changes are necessary to adapt membrane excitability to the functional properties of mature cells.…”

Section: Discussionmentioning

confidence: 99%

“…The biophysical properties of I Na change significantly during the development of excitable cells. Typically, the maturation of this current consists of a gradual increase in amplitude along with changes in the voltage dependence of the activation and inactivation processes, which affect membrane excitability in fully differentiated cells (Cummins et al, 1994;Costa, 1996;Gao & Ziskind-Conhaim, 1998;Fry, 2006;Donnelly, 2011;Yu et al, 2011;Tadros et al, 2015;Calvigioni et al, 2017). Apart from a study on the amphibian Necturus maculosus (Mackay-Sim et al, 1996), it is mostly ignored whether and how I Na changes in mammalian taste cells during their maturation.…”

Section: Introductionmentioning

confidence: 99%

Changes of the biophysical properties of voltage-gated Na⁺currents during maturation of the sodium-taste cells in rat fungiform papillae

Bigiani

Tirindelli

Bigiani³

2021

Preprint

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Taste cells are a heterogeneous population of sensory receptors that undergoes a continuous turnover. Different chemo-sensitive cell lines rely on action potentials to release the neurotransmitter onto nerve endings. The electrical excitability is due to the presence of a tetrodotoxin-sensitive, voltage-gated sodium current (INa) similar to that found in neurons. Since the biophysical properties of INa change during neuronal development, we wondered whether the same also occurred in taste cells. Here, we used the patch-clamp recording technique to study INa in sodium sensing cells of rat fungiform papillae. We identified these cells by exploiting the known blocking effect of amiloride on ENaC, the sodium (salt) receptor. Then, based on the amplitude of INa and a morphological analysis, we subdivided sodium cells into two broad developmental groups, namely immature and mature cells. We found that: the voltage dependence of activation and inactivation changed in the transition from immature to mature state (depolarizing shift); the membrane capacitance significantly decreased in mature cells, enhancing the density of INa; a persistent sodium current, absent in immature cells, appeared in mature cells. mRNA expression analysis of the α-subunits of voltage-gated sodium channels in fungiform taste buds supported the electrophysiological data. As a whole, our findings provide evidence for a noticeable change in membrane excitability during development, which is consistent with the key role played by electrical signaling in the release of neurotransmitter by mature sodium cells.

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Molecular and Functional Changes in Voltage-Gated Na+ Channels in Cardiomyocytes During Mouse Embryogenesis

Cited by 12 publications

References 36 publications

Ultrastructural Maturation of Human-Induced Pluripotent Stem Cell-Derived Cardiomyocytes in a Long-Term Culture

Ultrastructural Maturation of Human-Induced Pluripotent Stem Cell-Derived Cardiomyocytes in a Long-Term Culture

Human derived cardiomyocytes: A decade of knowledge after the discovery of induced pluripotent stem cells

Changes of the biophysical properties of voltage-gated Na⁺currents during maturation of the sodium-taste cells in rat fungiform papillae

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Molecular and Functional Changes in Voltage-Gated Na+ Channels in Cardiomyocytes During Mouse Embryogenesis

Cited by 12 publications

References 36 publications

Ultrastructural Maturation of Human-Induced Pluripotent Stem Cell-Derived Cardiomyocytes in a Long-Term Culture

Ultrastructural Maturation of Human-Induced Pluripotent Stem Cell-Derived Cardiomyocytes in a Long-Term Culture

Human derived cardiomyocytes: A decade of knowledge after the discovery of induced pluripotent stem cells

Changes of the biophysical properties of voltage-gated Na+currents during maturation of the sodium-taste cells in rat fungiform papillae

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Changes of the biophysical properties of voltage-gated Na⁺currents during maturation of the sodium-taste cells in rat fungiform papillae