Phylogeny and effects of anoxia on hyperpolarization-activated, cyclic nucleotide-gated channel gene expression in the heart of a primitive chordate, the Pacific Hagfish (<i>eptatretus stoutii</i>)

Wilson, Christopher M.; Stecyk, Jonathan A. W.; Couturier, Christine S.; Nilsson, Göran; Farrell, Anthony P.

doi:10.1242/jeb.094912

Cited by 21 publications

(11 citation statements)

References 59 publications

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“…Myocardiocytes exhibit low resting membrane potentials (Jensen, ) and are rich in hyperpolarization‐activated cyclic nucleotide‐gated (HCN) ionic channels (Wilson and Farrel, 2013). In E. stoutii , HCN channels appear to control heart rate and chamber synchrony by allowing the spread of excitation from the atrium to the ventricle (Wilson and Farrel, 2013; Wilson et al, ). In this sense, the presence of a sinus venosus with a morphologically or functionally well‐defined pacemaker may not be strictly necessary.…”

Section: Discussionmentioning

confidence: 99%

Morphological analysis of the hagfish heart. II. The venous pole and the pericardium

Icardo

Colvée

Schorno

et al. 2016

Journal of Morphology

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The morphological characteristics of the venous pole and pericardium of the heart were examined in three hagfish species, Myxine glutinosa, Eptatretus stoutii, and Eptatretus cirrhatus. In these species, the atrioventricular (AV) canal is long, funnel-shaped and contains small amounts of myocardium. The AV valve is formed by two pocket-like leaflets that lack a papillary system. The atrial wall is formed by interconnected muscle trabeculae and a well-defined collagenous system. The sinus venosus (SV) shows a collagenous wall and is connected to the left side of the atrium. An abrupt collagen-muscle boundary marks the SV-atrium transition. It is hypothesized that the SV is not homologous to that of other vertebrates which could have important implications for understanding heart evolution. In M. glutinosa and E. stoutii, the pericardium is a closed bag that hangs from the tissues dorsal to the heart and encloses both the heart and the ventral aorta. In contrast, the pericardium is continuous with the loose periaortic tissue in E. cirrhatus. In all three species, the pericardium ends at the level of the SV excluding most of the atrium from the pericardial cavity. In M. glutinosa and E. stoutii, connective bridges extend between the base of the aorta and the ventricular wall. In E. cirrhatus, the connections between the periaortic tissue and the ventricle may carry blood vessels that reach the ventricular base. A further difference specific to E. cirrhatus is that the adipose tissue associated with the pericardium contains thyroid follicles. J. Morphol. 277:853-865, 2016. © 2016 Wiley Periodicals, Inc.

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Section: Discussionmentioning

confidence: 99%

Morphological analysis of the hagfish heart. II. The venous pole and the pericardium

Icardo

Colvée

Schorno

et al. 2016

Journal of Morphology

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“…In the heart of the hagfish orthologues of all members of the HCN channel family (HCN1-4) were expressed, but the dominant form present was HCN3 (Wilson et al, 2013). In the goldfish heart HCN4 immunohistochemistry labels cells in the sinoatrial valve leaflets (Newton et al, 2014).…”

Section: Putative Pacemaker Cellsmentioning

confidence: 99%

Intrinsic and extrinsic innervation of the heart in zebrafish (Danio rerio)

Stoyek

Croll

Smith

2015

J of Comparative Neurology

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In the vertebrate heart the intracardiac nervous system is the final common pathway for autonomic control of cardiac output, but the neuroanatomy of this system is not well understood. In this study we investigated the innervation of the heart in a model vertebrate, the zebrafish. We used antibodies against acetylated tubulin, human neuronal protein C/D, choline acetyltransferase, tyrosine hydroxylase, neuronal nitric oxide synthase, and vasoactive intestinal polypeptide to visualize neural elements and their neurotransmitter content. Most neurons were located at the venous pole in a plexus around the sinoatrial valve; mean total number of cells was 197 ± 23, and 92% were choline acetyltransferase positive, implying a cholinergic role. The plexus contained cholinergic, adrenergic, and nitrergic axons and vasoactive intestinal polypeptide-positive terminals, some innervating somata. Putative pacemaker cells near the plexus showed immunoreactivity for hyperpolarization-activated cyclic nucleotide-gated channel 4 (HCN4) and the transcription factor Islet-1 (Isl1). The neurotracer neurobiotin showed that extrinsic axons from the left and right vagosympathetic trunks innervated the sinoatrial plexus proximal to their entry into the heart; some extrinsic axons from each trunk also projected into the medial dorsal plexus region. Extrinsic axons also innervated the atrial and ventricular walls. An extracardiac nerve trunk innervated the bulbus arteriosus and entered the arterial pole of the heart to innervate the proximal ventricle. We have shown that the intracardiac nervous system in the zebrafish is anatomically and neurochemically complex, providing a substrate for autonomic control of cardiac effectors in all chambers.

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“…Transcription factors Isl1 and Tbx3 are only expressed in the sinus node part of the sinus myocardium with greatest rate of spontaneous depolarization 4 , 19 , 20 . Pacemaker activity is strongly influenced by the so-called funny current carried by the family of hyperpolarization-activated cyclic nucleotide-gated K + -channels, including Hcn4 4 , 18 , 21 .…”

Section: Introductionmentioning

confidence: 99%

Morpho-functional characterization of the systemic venous pole of the reptile heart

Jensen

Vesterskov

Boukens

et al. 2017

Sci Rep

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Mammals evolved from reptile-like ancestors, and while the mammalian heart is driven by a distinct sinus node, a sinus node is not apparent in reptiles. We characterized the myocardial systemic venous pole, the sinus venosus, in reptiles to identify the dominant pacemaker and to assess whether the sinus venosus remodels and adopts an atrium-like phenotype as observed in mammals. Anolis lizards had an extensive sinus venosus of myocardium expressing Tbx18. A small sub-population of cells encircling the sinuatrial junction expressed Isl1, Bmp2, Tbx3, and Hcn4, homologues of genes marking the mammalian sinus node. Electrical mapping showed that hearts of Anolis lizards and Python snakes were driven from the sinuatrial junction. The electrical impulse was delayed between the sinus venosus and the right atrium, allowing the sinus venosus to contract and aid right atrial filling. In proximity of the systemic veins, the Anolis sinus venosus expressed markers of the atrial phenotype Nkx2-5 and Gja5. In conclusion, the reptile heart is driven by a pacemaker region with an expression signature similar to that of the immature sinus node of mammals. Unlike mammals, reptiles maintain a sinuatrial delay of the impulse, allowing the partly atrialized sinus venosus to function as a chamber.

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Phylogeny and effects of anoxia on hyperpolarization-activated, cyclic nucleotide-gated channel gene expression in the heart of a primitive chordate, the Pacific Hagfish (eptatretus stoutii)

Cited by 21 publications

References 59 publications

Morphological analysis of the hagfish heart. II. The venous pole and the pericardium

Morphological analysis of the hagfish heart. II. The venous pole and the pericardium

Intrinsic and extrinsic innervation of the heart in zebrafish (Danio rerio)

Morpho-functional characterization of the systemic venous pole of the reptile heart

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