Structural arrangement of collagen fibrils in the periarterial connective tissue of the kidney: their functional relevance as a structural stabilizer against arterial pressure

Abstract

Periarterial connective tissue with a moderate amount of collagen fibrils is known to be a specialized domain in the renal interstitium. This study aimed to clarify the microscopic architecture of the periarterial connective tissue as a mechanical supportive structure of the intrarenal arteries. Transmission and scanning electron microscopy revealed two populations of collagen fibrils in the periarterial connective tissue. The major one was composed of many bundles of collagen fibrils running in longitudinal directions, whereas the minor one was represented by a few circumferential bundles adjacent to the smooth muscles. The amount of collagen fibrils was obviously variable and correlated with the arterial caliber. The correlation between abundance of collagen fibrils and the arterial caliber was confirmed by morphometric analysis of the collagen fibril area per arterial perimeter on electron micrographs. The size of individual collagen fibrils was measured in periarterial connective tissue of arteries with various calibers. A positive correlation between the diameter of collagen fibrils and arterial caliber was confirmed, indicating the supportive function of collagen fibrils in the periarterial connective tissue. The accumulated morphological findings supported the hypothesis that the collagen fibrils in the periarterial connective tissue develop longitudinal tension with their tensile strength, whereas the smooth muscle cells in the media develop circumferential tension with active regulation of contracting force.

Organ Specificity and Functional Relevance of the Arterial Structure: A Comparative Study in the Kidney and the Skeletal Muscle with Electron Microscopy

“…The amount of collagen bundles increased as the arteries became larger both in the kidney and skeletal muscle, indicating an increase of mechanical stress by an incremental increase of wall tension in larger arteries, as shown in a previous study [2]. It was also shown that the diameter of collagen fibrils increased as the arteries became larger in the kidney, corresponding to increases of mechanical stress [2], and that in skeletal muscle the collagen fibrils were thicker in larger arteries than in smaller arteries, although quantitative analysis was not performed due to an inadequate sample size.…”

“…The parallel arrangement of the smooth muscle cells of arteries in circular directions was reported in the kidney by the present authors [2,19] and in the muscular arteries in the lung, whereas the elastic arteries in the lung possess several layers of smooth muscle cells arranged in parallel but in different orientations depending on the layers [5]. The muscular arteries in the other organs were reported to possess different arrangements.…”

“…Glomerular blood pressure at the end of the arterial tree in the kidney was maintained at a high level (about 50 mm Hg) against considerable change of systemic blood pressure to supply filtration pressure in the glomerulus mainly by myogenic control [18]. The length of the arteries in the kidney remained unchanged at any physiological status of the kidney due to the constant size of the kidney enclosed in a solid capsule [2]. …”

“…It was also shown that the diameter of collagen fibrils increased as the arteries became larger in the kidney, corresponding to increases of mechanical stress [2], and that in skeletal muscle the collagen fibrils were thicker in larger arteries than in smaller arteries, although quantitative analysis was not performed due to an inadequate sample size.…”

“…The structure of these minute vessels has been well visualized and studied with advanced microscopic techniques, including transmission and scanning electron microscopy and confocal microscopy. These studies elucidated the common basic structure of the arterial and venous wall, including the endothelium, the inner elastic lamina, smooth muscle cells in the media and adventitial connective tissue [1,2,3,4,5,6], as well as the different configuration of endothelial cells in the arteries [7] and in the capillaries [8]. …”