Joyce W et al. (2020), Smooth Muscle in Cardiac Chambers is Common in ...

XB-ART-56280

Anat Rec (Hoboken) 2020 May 01;3035:1327-1336. doi: 10.1002/ar.24257.

Show Gene links Show Anatomy links

Smooth Muscle in Cardiac Chambers is Common in Turtles and Extensive in the Emydid Turtle, Trachemys scripta.

Joyce W , Crossley DA , Wang T , Jensen B .

???displayArticle.abstract???
A prominent layer of smooth muscle lining the luminal side of the atria of freshwater turtles (Emydidae) was described more than a century ago. We recently demonstrated that this smooth muscle provides a previously unrecognized mechanism to change cardiac output in the emydid red-eared slider (Trachemys scripta) that possibly contributes to their tremendous diving capacity. The purpose of the present immunohistochemical study was firstly to screen major groups of vertebrates for the presence of cardiac smooth muscle. Secondly, we investigated the phylogenetic distribution of cardiac smooth muscle within the turtle order (Testudines), including terrestrial and aquatic species. Atrial smooth muscle was not detected in a range of vertebrates, including Xenopus laevis, Alligator mississippiensis, and Caiman crocodilus, all of which have pronounced diving capacities. However, we confirmed earlier reports that traces of smooth muscle are found in human atrial tissue. Only within the turtles (eight species) was there substantial amounts of nonvascular smooth muscle in the heart. This amount was greatest in the atria, while the amount in proportion to cardiac muscle was greater in the sinus venosus than in other chambers. T. scripta had more smooth muscle in the sinus venosus and atria than the other turtles. In some specimens, there was some smooth muscle in the ventricle and the pulmonary vein. Our study demonstrates that cardiac smooth muscle likely appeared early in turtle evolution and has become extensive within the Emydidae family, possibly in association with diving. Across other tetrapod clades, cardiac smooth muscle might not associate with diving. Anat Rec, 303:1327-1336, 2020. © 2019 The Authors. The Anatomical Record published by Wiley Periodicals, Inc. on behalf of American Association for Anatomy.

???displayArticle.pubmedLink??? 31509333
???displayArticle.pmcLink??? PMC7216914
???displayArticle.link??? Anat Rec (Hoboken)
???displayArticle.grants??? [+]

Species referenced: Xenopus laevis
Genes referenced: acta2 tnni3

???attribute.lit??? ???displayArticles.show???

	Figure 1. Luminal atrial smooth muscle was not detected in most vertebrates. Red represents cTnI and green represents SMA, as detected by fluorescent immunohistochemistry. (A) American alligator, (B) pink‐tongued skink, (C) African clawed frog, (D) longnose gar, (E) mouse, and (F) lesser redpoll bird (all detected SMA in B, E, F was within arterial walls). Scale bars are 1 mm. a, atrium; as, atrial septum; pv, pulmonary vein; sv, sinus venosus; v, ventricle; oft, outflow tract.
	Figure 2. Luminal smooth muscle was not detected in atrium from spectacled caiman (A), cane toad (B), or caecilian (C). Red represents cTnI and green represents SMA, as detected by fluorescent immunohistochemistry. Scale bars are 1 mm. (r/l)a, (right/left) atrium; as, atrial septum; sv, sinus venosus; c, conus.
	Figure 3. Smooth muscle in human atrial wall. Red represents cardiac cTnI and green represents SMA, as detected by fluorescent immunohistochemistry. (A) left anterior atrium and (B) left atrial appendage. Scale bars are 1 mm.
	Figure 4. The phylogenetic distribution of smooth muscle in different regions of the heart in eight turtle species. Red represents cTnI and green represents SMA, as detected by fluorescent immunohistochemistry. Scale bars are 100 μm for all species, except for C. senegalensis and T. scripta (500 μm), and C. carbonaria (1 mm). Phylogeny based on Crawford et al. (2015).
	Figure 5. Assessment across turtles of the proportion of signal from SMA (green) out the total signal from SMA and cTnI (red), measured by the ImageJ Plugin function “RGB measure.” The yellow lines indicate the region of interest within which the measurements were made. Two specimens of the Pond slider with intermediate (A) and high (B) proportions (numbers in green) of SMA in the sinus venosus and atria. (C) Across turtles, the sinus venosus was proportionally richer in SMA than the atria, which in turn were richer in SMA than the ventricle (P‐values of paired two‐tailed T‐tests, numbers in columns are the number of assessed sections). (D) The proportion of SMA in the sinus venosus was significantly positively related to the proportion of SMA in the atria (Pearson correlation, P < 0.001).
	Figure 6. The interspecific variation in atrial smooth muscle in turtles. (A) Mean area of smooth muscle as a percentage of total muscle (smooth + cardiac muscle) area in eight species. Values are means ± SD. (B–D) Red represents cardiac Troponin I and green represents smooth muscle actin, as detected by fluorescent immunohistochemistry. (B) A prominent case of atria smooth muscle in T. scripta. (C) Intermediate levels of smooth muscle seen in C. senegalensis. (D) Near absence of atrial smooth muscle in C. carbonaria. For B–D, scale bars are 1 mm. a, atrium; as, atrial septum; pv, pulmonary vein; sv, sinus venosus; v, ventricle; oft, outflow tract.
	Figure 7. There was no significant relationship between atrial smooth muscle (% area of total muscle) and body mass in Trachemys scripta (linear regression).

References [+] :

BLINKS, PHYSICAL FACTORS IN THE ANALYSIS OF THE ACTIONS OF DRUGS ON MYOCARDIAL CONTRACTILITY. 1963, Pubmed

BLINKS, PHYSICAL FACTORS IN THE ANALYSIS OF THE ACTIONS OF DRUGS ON MYOCARDIAL CONTRACTILITY. 1963, Pubmed
Barillot, Induction and modulation of smooth muscle differentiation in Xenopus embryonic cells. 2008, Pubmed , Xenbase
Blix, Adaptations to deep and prolonged diving in phocid seals. 2018, Pubmed
Bottazzi, The Oscillations of the Auricular Tonus in the Batrachian Heart, with a Theory on the Function of Sarcoplasma in Muscular Tissues. 1897, Pubmed
Bottazzi, On plain muscle. 1899, Pubmed
Carmona, Comparative developmental biology of the cardiac inflow tract. 2018, Pubmed
Chiari, Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria). 2012, Pubmed
Conklin, Rhythmic contractility in the hepatic portal "corkscrew" vein of the rat snake. 2009, Pubmed
Crawford, More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. 2012, Pubmed
Crawford, A phylogenomic analysis of turtles. 2015, Pubmed
DIMOND, Responses to phenethylamines and nicotine and histology of turtle atria. 1959, Pubmed
Douglas, Pulmonary vein, dorsal atrial wall and atrial septum abnormalities in podoplanin knockout mice with disturbed posterior heart field contribution. 2009, Pubmed
Douglas, Histology of vascular myocardial wall of left atrial body after pulmonary venous incorporation. 2006, Pubmed
Elsner, Angiography of the inferior vena cava of the harbor seal during simulated diving. 1971, Pubmed
Fong, A phylogenomic approach to vertebrate phylogeny supports a turtle-archosaur affinity and a possible paraphyletic lissamphibia. 2012, Pubmed
Galli, The role of the sarcoplasmic reticulum in the generation of high heart rates and blood pressures in reptiles. 2006, Pubmed
Glass, Ventilation in an aquatic and a terrestrial chelonian reptile. 1978, Pubmed
Jensen, Development of the hearts of lizards and snakes and perspectives to cardiac evolution. 2013, Pubmed
Jensen, Coronary blood flow in the anesthetized American alligator (Alligator mississippiensis). 2016, Pubmed
Jensen, Morpho-functional characterization of the systemic venous pole of the reptile heart. 2017, Pubmed
Joyce, Contraction of atrial smooth muscle reduces cardiac output in perfused turtle hearts. 2019, Pubmed
Joyce, Venous pressures and cardiac filling in turtles during apnoea and intermittent ventilation. 2018, Pubmed
Joyce, Purinoceptors exert negative inotropic effects on the heart in all major groups of reptiles. 2014, Pubmed
Kroneman, Comparative analysis of avian hearts provides little evidence for variation among species with acquired endothermy. 2019, Pubmed
Lillie, The caval sphincter in cetaceans and its predicted role in controlling venous flow during a dive. 2018, Pubmed
Maier, Ca(2+) handling in isolated human atrial myocardium. 2000, Pubmed
Meghji, An unusual excitatory action of adenosine on the ventricular muscle of the South African clawed toad (Xenopus laevis). 1983, Pubmed , Xenbase
Meyer, Influence of endothelin 1 on human atrial myocardium--myocardial function and subcellular pathways. 1996, Pubmed
Minerds, Lack of evidence for functional natriuretic peptide receptors in the heart of the cane toad, Bufo marinus. 1997, Pubmed
Moretti, Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. 2006, Pubmed
Nadler, Positive inotropic effect in the heart produced by acetylcholine. 1993, Pubmed
Nathan, Myocardial atrio-venous junctions and extensions (sleeves) over the pulmonary and caval veins. Anatomical observations in various mammals. 1970, Pubmed
O'Donnell, Pharmacological experiments demonstrate that toad (Bufo marinus) atrial beta-adrenoceptors are not identical with mammalian beta 2- or beta 1-adrenoceptors. 1982, Pubmed
Okada, Phenotype and physiological significance of the endocardial smooth muscle cells in human failing hearts. 2015, Pubmed
Park, The clinical significance of the atrial subendocardial smooth muscle layer and cardiac myofibroblasts in human atrial tissue with valvular atrial fibrillation. 2013, Pubmed
Robb, Specialized, conducting, tissue in the turtle heart. 1953, Pubmed
Roux, The myocardial sleeves of the pulmonary veins: potential implications for atrial fibrillation. 2004, Pubmed
Saint-Jeannet, Ventrolateral regionalization of Xenopus laevis mesoderm is characterized by the expression of alpha-smooth muscle actin. 1992, Pubmed , Xenbase
Shaffer, Phylogenomic analyses of 539 highly informative loci dates a fully resolved time tree for the major clades of living turtles (Testudines). 2017, Pubmed
Terasaki, Electron microscopic demonstration of intercellular junctions between subendocardial smooth muscle and myocardium in the sheep heart. 1993, Pubmed
Wang, Cardiorespiratory synchrony in turtles. 1996, Pubmed
Warkman, Organization and developmental expression of an amphibian vascular smooth muscle alpha-actin gene. 2005, Pubmed , Xenbase
de Bakker, Extreme variation in the atrial septation of caecilians (Amphibia: Gymnophiona). 2015, Pubmed