Avian cardiomyocyte architecture and what it reveals about the evolution of the vertebrate heart

Abstract

Bird cardiomyocytes are long, thin and lack transverse (t)-tubules, which is akin to the cardiomyocyte morphology of ectothermic non-avian reptiles, who are typified by low maximum heart rates and low pressure development. However, birds can achieve greater contractile rates and developed pressures than mammals, whose wide cardiomyocytes contain a dense t-tubular network allowing for uniform excitation–contraction coupling and strong contractile force. To address this apparent paradox, this paper functionally links recent electrophysiological studies on bird cardiomyocytes with decades of ultrastructure measurements. It shows that it is the strong transsarcolemmal Ca 2+ influx via the L-type Ca 2+ current ( I CaL ) and the high gain of Ca 2+ -induced Ca 2+ release from the sarcoplasmic reticulum (SR), coupled with an internal SR Ca 2+ release relay system, that facilitates the strong fast contractions in the long thin bird cardiomyocytes, without the need for t-tubules. The maintenance of an elongated myocyte morphology following the post-hatch transition from ectothermy to endothermy in birds is discussed in relation to cardiac load, myocyte ploidy, and cardiac regeneration potential in adult cardiomyocytes. Overall, the paper shows how little we know about cellular Ca 2+ dynamics in the bird heart and suggests how increased research efforts in this area would provide vital information in our quest to understand the role of myocyte architecture in the evolution of the vertebrate heart. This article is part of the theme issue ‘The cardiomyocyte: new revelations on the interplay between architecture and function in growth, health, and disease’. Please see glossary at the end of the paper for definitions of specialized terms.

Homeostasis and evolution in relation to regeneration and repair

“…Indeed, all birds are ectothermic in novo and achieve endothermy post‐hatching. Precocious species hatching birds that are feathered, as well as active and capable of finding their own food, reach endothermic thermoregulatory capacity at birth through the rapid development of aerobic capacity to withstand greater energy demands (Shiels, 2022).…”

“…The regulation of regeneration, repair and progression of some tumours could be part of the physiological adaptation to conditions of hypoxia (Cadiz & Jonz, 2020; Guenin‐Mace et al., 2023; Liu et al., 2022), thyroid regulation (Hirose et al., 2019), ecto‐endothermy (Cadiz & Jonz, 2020; Chang et al., 2009; Hirose et al., 2019; Jacob et al., 2021; Rennolds & Bely, 2023; Shiels, 2022), and epigenetics and chromatin organization (Palacios, 2019; Pillai et al., 2021) (Fig. 5).…”

Long-Term Transcriptomic Changes and Cardiomyocyte Hyperpolyploidy after Lactose Intolerance in Neonatal Rats

“…One of the fruitful approaches may be a comprehensive analysis of epidemiologic, evolutionary, and cross-species studies [ 8 , 15 , 16 , 17 ]. Therefore, we compared the data of epidemiological studies concerning the diseases triggering the main causes of developmental programming of CVD, including growth retardation, inflammation, and malnutrition in babies, toddlers, and children [ 18 , 19 , 20 , 21 ], and the literature describing the data on developmental adaptation of cardiovascular system in more than 30 bird and 40 mammal species [ 14 , 22 , 23 , 24 , 25 , 26 ]. The data of epidemiological studies revealed early life gastroenteritis of various etiologies [ 18 , 20 , 27 , 28 , 29 , 30 ].…”

“…The data of epidemiological studies revealed early life gastroenteritis of various etiologies [ 18 , 20 , 27 , 28 , 29 , 30 ]. Comparative cross-species analysis indicated that early life cardiac functional load can be an important trigger of the developmental programming of adult CVD, because it is inversely related to heart aerobic capacity in adults [ 23 , 24 , 25 ].…”

Comparison of changes in Ca²⁺ concentration in quail and rat cardiomyocytes using Fura-4F

“…Cardiomyocytes (CMs) are the main cellular components of the myocardium and are responsible for effectively executing the contraction-relaxation cycle of the heart. Although birds and mammals have the same heart structure with two atria and two ventricles, the control method for intracellular calcium ions (Ca 2+ ), the regulator of CM contraction-relaxation, differs greatly between them [1][2][3]. Mammalian CMs have T-tubule membranes which are invaginations of the cell membrane perpendicular to the direction of contraction [1,3,4].…”