XB-ART-56280Anat Rec (Hoboken) January 1, 2020; 303 (5): 1327-1336.
Smooth Muscle in Cardiac Chambers is Common in Turtles and Extensive in the Emydid Turtle, Trachemys scripta.
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.
PubMed ID: 31509333
PMC ID: PMC7216914
Article link: Anat Rec (Hoboken)
Genes referenced: acta2 tnni3
Article Images: [+] show captions
|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 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. 1996, Pubmed