Cardiac-like musculature of the intrapulmonary venous wall of the long-clawed shrew (Sorex unguiculatus), common tree shrew (Tupaia glis) and common marmoset (Callithrix jacchus)

Endo, Hideki; Mifune, Hiroharu; Maeda, Seishi; Kimura, Junko; Yamada, Junzo; Rerkamnuaychoke, Worawut; Chungsamarnyart, Narong; Ogawa, Kenji; Kurohmaru, Masamichi; Hayashi, Yoshihiro; Nishida, Takao

doi:10.1002/(sici)1097-0185(199701)247:1<46::aid-ar7>3.0.co;2-d

Cited by 10 publications

(6 citation statements)

References 22 publications

(14 reference statements)

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“…Subsequently the presence of cardiac myocytes in the wall of intrapulmonary veins has been noted in squirrel, rat, marmoset and shrew lung (19, 68, 69, 157, 206). The wall of large intrapulmonary veins from rat lung ( Figure 20 ) includes the endothelium, scant smooth muscle, and abundant striated myocytes.…”

Section: Veinsmentioning

confidence: 97%

Structure and Composition of Pulmonary Arteries, Capillaries, and Veins

Townsley¹

2012

Comprehensive Physiology

242

215

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The pulmonary vasculature is comprised of three anatomic compartments connected in series: the arterial tree, an extensive capillary bed, and the venular tree. Although in general this vasculature is thin-walled, structure is nonetheless complex. Contributions to structure (and thus potentially to function) from cells other than endothelial and smooth muscle cells as well as those from the extracellular matrix should be considered. This review is multifaceted, bringing together information regarding 1) classification of pulmonary vessels, 2) branching geometry in the pulmonary vascular tree, 3) a quantitative view of structure based on morphometry of the vascular wall, 4) the relationship of nerves, a variety of interstitial cells, matrix proteins, and striated myocytes to smooth muscle and endothelium in the vascular wall, 5) heterogeneity within cell populations and between vascular compartments, 6) homo- and heterotypic cell-cell junctional complexes, and 7) the relation of the pulmonary vasculature to that of airways. These issues for pulmonary vascular structure are compared, when data is available, across species from human to mouse and shrew. Data from studies utilizing vascular casting, light and electron microscopy, as well as models developed from those data, are discussed. Finally, the need for rigorous quantitative approaches to study of vascular structure in lung is highlighted.

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Section: Veinsmentioning

confidence: 97%

Structure and Composition of Pulmonary Arteries, Capillaries, and Veins

Townsley¹

2012

Comprehensive Physiology

242

215

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“…Although the presence of striated muscle in smaller intrapulmonary veins inversely correlates with body mass (and positively with heart rate) [17], the appearance of striated muscles in distal segments of numerous intrapulmonary veins begs for a model other than direct cardiomyocyte extension/ migration from the left atrium. Striated myocytes were found in pulmonary veins with a diameter of 70-250 microns and even in pulmonary veins of 30 micronsin diameter in numerous species [18][19][20][21][22][23]. A quest for an alternative model also appears logical because cardiomyocyte extension/migration to distal pulmonary veins has been never demonstrated; the evidence has shown similarity in gene expression between striated muscle of pulmonary veins and heart myocytes [3,4,24], which neither is a proof of cell migration nor the same developmental origin [25].…”

Section: Correspondencementioning

confidence: 99%

“…While I read 'The Vertebrate as a Dual Animal-Somatic and Visceral' long ago, only recently did I realize that the puzzling doi: 10.7243/2055-091X-3-3 morphology of distal intrapulmonary veins constitutes the same phenomenon that Romer described as "the functional need for more efficient musculature" [26] because pulmonary veins rhythmically contract and propel blood to the left atrium [3,[18][19][20].…”

Section: Implication #1mentioning

confidence: 99%

Striated muscles in visceral organs of vertebrates

Субботин¹

2016

J Histol Histopathol

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Pathologists involved in the examination of small rodent tissues are familiar with the presence of striated muscle in walls of intrapulmonary veins. Because these striated muscles express cardiomyocyte markers and are involved in rhythmical contraction during systole, this morphologic arrangement was named "pulmonary myocardium". Striated cardiac muscles of intrapulmonary veins have also been found in numerous species, including non-human primates. Great attention has been given to animal striated pulmonary veins because in humans, the presence of cardiomyocytes in the pulmonary veins (myocardial sleeves) is a major origin of paroxysmal atrial fibrillation. It is unequivocally suggested that direct extension/migration of cardiomyocytes from the left atrium into pulmonary veins is the origin of "pulmonary myocardium". This model sounds logical in regard to humans and large mammals because in these cases, striated myocytes extend into pulmonary veins only by 10-30 mm from the left atrium. However, the cardiomyocyte direct extension/migration model becomes less parsimonious when applied to the numerous small intrapulmonary veins with striated muscles in their walls in small mammals. In 1972, Alfred Sherwood Romer, renowned for his contributions to the study of vertebrate evolution, suggested that visceral smooth muscle cells developed a striated phenotype due to the need for more efficient musculature. Romer theorized that the primary anatomical division of the vertebrate muscular system should be not into smooth and striated types but into somatic and visceral systems, because the line of division along the gut between striated and smooth musculature is not a fixed point. Romer's work offered a parsimonious model for the presence of striated muscle in the walls of the intrapulmonary veins-visceral smooth muscle cells, which are capable of differentiating into striated muscle cells, are always present; whether they differentiate depends on functional demands. From Romer's hypothesis, it also could be foreseen that striated muscle could appear in visceral compartments other than the blood circulatory system and pharyngeal muscles to facilitate functional needs. Indeed, it was shown that 1) the lymphatic system of many low vertebrates acquired a lymphatic heart with striated muscle cells; 2) some vertebrates also acquire striated muscles in tunica Muscularis of the stomach and intestine. The facts above undoubtedly corroborate Prof. Romer's notion on the evolution of the vertebrate muscular system.

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“…Perhaps the most unusual morphological trait of the shrew heart is the extent of the pulmonary venous myocardium. It was previously demonstrated that pulmonary venous myocardium is present in shrews (Endo et al, 1997) and mice, for example, have myocardial sleeves that extend three bifurcations up the pulmonary venous tree (Mommersteeg et al, 2007).…”

Section: Highly Unusual Traits Of the Shrew Heartmentioning

confidence: 99%

Anatomy of the Heart with the Highest Heart Rate

Chang

Sheftel

Jensen

2021

Preprint

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Shrews occupy the lower extreme of the seven orders of magnitude mammals range in size. Their hearts are large relative to body weight and heart rate can exceed a thousand beats a minute. To investigate whether cardiac traits that are typical mammalian scale to these extremes, we assessed the heart of three species of shrew (genus Sorex) following the sequential segmental analysis developed for human hearts. Using micro-computed tomography we describe the overall structure and find, in agreement with previous studies, a large and elongate ventricle. The atrial and ventricular septums and the atrioventricular and arterial valves are typically mammalian. The ventricular walls comprise mostly compact myocardium and especially the right ventricle has few trabeculations on the luminal side. A developmental process of compaction is thought to reduce trabeculations in mammals, but in embryonic shrews the volume of trabeculations increase for every gestational stage, only slower than the compact volume. By expression of Hcn4, we identify a sinus node and an atrioventricular conduction axis which is continuous with the ventricular septal crest. Outstanding traits include pulmonary venous sleeve myocardium that reaches farther into the lungs than in any other mammals. Typical proportions of coronary arteries-to-aorta do not scale and the shrew coronary arteries are proportionally enormous, presumably to avoid the high resistance to blood flow of narrow vessels. In conclusion, most cardiac traits do scale to the miniscule shrews. The shrew heart, nevertheless, stands out by its relative size, elongation, proportionally large coronary vessels, and extent of pulmonary venous myocardium.

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Cardiac-like musculature of the intrapulmonary venous wall of the long-clawed shrew (Sorex unguiculatus), common tree shrew (Tupaia glis) and common marmoset (Callithrix jacchus)

Cited by 10 publications

References 22 publications

Structure and Composition of Pulmonary Arteries, Capillaries, and Veins

Structure and Composition of Pulmonary Arteries, Capillaries, and Veins

Striated muscles in visceral organs of vertebrates

Anatomy of the Heart with the Highest Heart Rate

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