Lametschwandtner A et al. (2012), Maturation of the gastric microvasculature in X...

XB-ART-44676

Anat Sci Int 2012 Jun 01;872:88-100. doi: 10.1007/s12565-011-0124-8.

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Maturation of the gastric microvasculature in Xenopus laevis (Lissamphibia, Anura) occurs at the transition from the herbivorous to the carnivorous lifestyle, predominantly by intussuceptive microvascular growth (IMG): a scanning electron microscope study of microvascular corrosion casts and correlative light microscopy.

Lametschwandtner A , Höll M , Bartel H , Anupunpisit V , Minnich B .

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The microvascular bed of the stomach of Xenopus laevis and the changes it undergoes when the herbivorous tadpole becomes a carnivorous adult were studied by scanning electron microscopy of vascular corrosion casts and light microscopy of stained tissue sections. In tadpoles an upper and a lower gastric artery supplied, and upper, middle and lower medial and lateral gastric veins drained the vertically extending stomach. During metamorphosis, the stomach gained a horizontal cranio-caudal extension and vessels accordingly become dorsal and ventral gastric arteries, and anterior, middle and posterior gastric veins, respectively. Up to stage 64 (late climax) mucosal capillaries formed a polygonal network of wide immature-looking capillaries ensheathing gastric glands in a basket-like manner. From stage 64 onwards, blood vessels of the stomach appeared mature, revealed a clear hierarchy and were correlated closely with the histomorphology of the stomach, which had also gained the adult pattern. Within the gastric mucosa, ascending arterioles branched in a fountain-like pattern into wide subepithelial capillaries establishing a centripetal blood flow along the gastric glands, which makes an ultrashort control loop of glandular cells within the branched tubular gastric glands very unlikely. Formation of the stomach external muscular layer started at stage 57 when smooth muscle cells locally formed a single longitudinal and one-to-two single circular layers. Abundant signs of intussusceptive microvascular growth and rare vascular sprouts in vascular corrosion casts indicated that the larval-to-adult microvascular pattern formation of the stomach of Xenopus laevis Daudin occurs predominantly by non-sprouting angiogenesis.

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Species referenced: Xenopus laevis
Genes referenced: gda lta myh3 rbfox2

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	Figs. 1–7. Fig. 1 Scanning electron micrograph (SEM) of the surface of a resin cast of an artery displaying characteristic longish endothelial cell nuclei imprints (arrows) orientated parallel to the long axis of the vessel. Note the slight circular narrowings caused by the circularly arranged vascular smooth muscle cells (arrowheads). Fig. 2 SEM of the surface of a resin cast of a vein displaying characteristic oval-to-roundish endothelial cell nuclei imprints (arrows) orientated randomly. Note faint circularly orientated imprints (arrowheads). Fig. 3 Histomorphology of the stomach of larval Xenopus at Nieuwkopp and Faber (NF) stage 55. Transverse section (7 μm) through whole tadpole. Cleveland-Wolfe-staining. Note the transition from the esophagus (es) to the glandular stomach (Manicotto glandulare) (st). ki Kidney, li large intestine, l lung, si small intestine, sp spleen, tm trunk muscles. Fig. 4 Stomach at NF stage 55. Transverse section at the level indicated in Fig. 3 (dashed line). Note the ciliated (ci) gastric epithelium bordering the lumen (lu). li Large intestine, pa pancreas, pe pigmented peritoneum, si small intestine. Fig. 5 Wall of the stomach at NF stage 55. Note a branched tubular gastric gland (gg) opening (arrow) into the lumen (lu). ci Ciliated columnar gastric epithelium. Fig. 6 Histomorphology of the stomach of larval Xenopus at Nieuwkopp and Faber (NF) stage 55. Transverse section (7 μm) through whole tadpole at the level of the origin of the celiac-mesenteric artery (cma) from the abdominal aorta (aa). Goldner staining. Note origin of left (lma) and right mesenteric artery (rma) from the cma. ki Kidney, li large intestine, l lung, si small intestine, st stomach. Fig. 7 Tangential section through the proximal portion of the stomach. Detail from Fig. 6 (boxed area) showing the single circular layer of smooth muscle cells forming the muscularis. Note the tangentially and transversely sectioned smooth muscle cells (arrowheads). Asterisks Gastric vessels, ep gastric epithelium, gg gastric gland, lp lamina propria, lu lumen, mu muscularis, se serosa
	Figs. 8–13. Fig. 8 SEM of gross arterial supply and venous drainage of the larval stomach at NF stage 56. Lateral view. Cranial is to the left. Part of liver, pancreas and intestines are removed to expose the lateral (left) surface of the dorso-ventral orientated stomach. Note the large left middle gastric vein (lmgv) and the artery (a) running close along the posterior curvature of the slightly sickle-shaped stomach. aa Abdominal aorta, cma celiac-mesenteric artery, es esophagus, hpv hepatic portal vein, li liver, lma left mesenteric artery, lta left thoracic aorta, rta right thoracic aorta, si small intestine, st stomach. Fig. 9 Same as Fig. 6, but lateral view at the medial (right) surface of the stomach. Cranial is to the right. Kidneys with most of abdominal aorta, posterior caval vein, intestines, pancreas and liver were removed to expose origin, course and branches of the celiac artery (ca). aa Abdominal aorta, av abdominal vein, cma celiac-mesenteric artery, es esophagus, hpv hepatic portal vein, lma left mesenteric artery, li liver, pcv posterior caval vein, rma right mesenteric artery, rugv right upper gastric veins, rmgv right middle gastric vein, si small intestine, st stomach. Fig. 10 Vascular corrosion cast (VCC) of the microangioarchitecture of the larval stomach at NF stage 55. Lateral aspect. Cranial is at top, dorsal is at right. Note the large calibre of the left middle gastric vein (lmgv). dd Duodenum, es esophagus, li liver, pa pancreas, hpv hepatic portal vein, sp spleen, st stomach. Fig. 11 VCC of microvascular pattern of the larval stomach at NF stage 55. Transverse section at the level of the corpus. Note the longitudinal folds (lf) protruding into the lumen (lu). a Artery. Asterisks “Conductive bridges”. Fig. 12 SEM of microvascular anatomy of the stomach wall at NF stage 55. Arterial vessels are colored red, venous vessels are colored blue. Arrows mark direction of blood flow. a Artery, c capillary, lu lumen, v vein. Fig. 13 Subepithelial capillary bed at NF stage 55. Luminal view. Note the wide vessels (asterisks; cf. Fig. 7) giving off centrifugally running capillaries (c). Arrows indicate direction of blood flow
	Figs. 14–19. Fig. 14 Histomorphology (Goldner staining) of the larval stomach at NF stage 57. Transverse section (7 μm). Note the thick gastric mucosa composed mainly of wide tubular glands. ep Columnar mucosal epithelium, li large intestine, lu lumen, mbw muscles of the body wall, pa pancreas, si small intestine, sk skin, st stomach. Fig. 15 Detail from Fig. 8. Note wide branched tubular gastric glands (gg) opening (arrow) into the lumen (lu) of the stomach. ep Columnar mucosal epithelium, mbw muscles of the body wall, pe pigmented peritoneum, se serosa. Fig. 16 Microangioarchitecture of the stomach at NF stage 57. Transverse section at the level of the corpus. Note the wide immature imposing capillaries (c) embracing tubular gastric glands. a Artery, lu lumen, v vein. Arrows indicate direction of blood flow. Fig. 17 Arteriolar supply of the glandular mucosa at NF stage 57. Transverse section at the level of the corpus. Detailed view. Note two arterioles (aa) running centripetally towards the lumen (lu) where they capillarize into centrifugally running capillaries (c) ensheathing the tubular gastric glands. Arrows indicate direction of blood flow. a Artery, v vein. Fig. 18 Microangioarchitecture of the stomach at NF stage 57. Longitudinal section. Luminal view. The wide meshes of the subepithelial capillary bed (c) indicate the locations of tubular gastric glands (gg). Note the many small holes (arrows) in the wide capillaries reflecting ongoing intussuceptive microvascular growth (IMG). a Artery, v vein. Fig. 19 Detail from Fig. 18. Vascular pattern of the subepithelial capillary bed of the gastric mucosa at NF stage 57. Luminal view. Dashed line outlines the capillaries ensheathing a branched tubular gastric gland (gg). Note the many signs of ongoing IMG (arrows)
	Figs. 20–25. Fig. 20 Histomorphology (Goldner stain) of the stomach at NF stage 64. Transverse section (7 μm). Note the presence of a submucosa (sm) with loose connective tissue. ac Abdominal cavity, bw body wall, cbd common bile duct, cm circular layer of muscularis, dd duodenum, ki kidney, lm longitudinal layer of muscularis, lu lumen, mu mucosa, pa pancreas, se serosa, sm submucosa, sp spleen. Fig. 21 Detail of Fig. 20 (boxed area). Note gastric pits (arrows) and thin muscular layer of the mucosa (arrowheads). cm Circular layer of muscularis, ep epithelium, lm longitudinal layer of muscularis, lp lamina propria, lu lumen, se serosa, sm submucosa. Fig. 22 SEM/VCC of gross arterial supply and venous drainage of the larval stomach at NF stage 64. Dorsal view. Cranial is on top. Part of liver, pancreas, intestines and kidneys are removed to expose the dorsal surface of the horizontally extending stomach. Note the dorsal gastric artery (dga) running close along the inner curvature of the slightly sickle-shaped stomach. Inset Origin of the dorsal gastric artery (dga) from the celiac artery (ca). aa Abdominal aorta, cma celiac-mesenteric artery, hpv hepatic portal vein, li large intestine, lma left mesenteric artery, pcv posterior caval vein, rma right mesenteric artery, si small intestine, sp spleen, st stomach. Fig. 23 Microvascular patterns of the isolated larval stomach at NF stage 64. Ventral view. Cranial is to the right, medial is on top. Note the course of the ventral gastric artery (vga) ascending from the duodenum to the stomach. Cranial (cvgv), middle (mvgv) and caudal ventral gastric veins (cavgv) form a strong ventral gastric vein (vgv). dd Duodenum, es esophagus, st stomach. Fig. 24 Lateral region of the stomach at NF stage 64 still displaying many signs of ongoing intussusceptive microvascular growth (arrows). Fig. 25 Microangioarchitecture of the stomach at NF stage 64 (late metamorphic climax). Transverse section at the level of the corpus. Note the prominent gastric mucosal folds (mf) bulging into the stomach lumen (lu). Asterisks mark “conductive bridges”
	Figs. 26, 27. Fig. 26 Microvascular anatomy of a mucosal fold at NF stage 64. Transverse section. Note centripetally ascending arteriole (aa) and descending centrifugally running venule (vv) draining subepithelial capillaries and capillaries (c) embracing tubular gastric glands. Arterial vessels are colored red, venous vessels are colored blue. Arrows indicated direction of (centrifugal) blood flow. a Artery, lu lumen. Fig. 27 Microvasculature of the stomach at NF stage 64. Detail. Serosal aspect. Note the few capillaries (arrowheads) of the muscular layer and two veno-venous anastomoses (arrows). a Artery, v vein
	Figs. 28–32. Fig. 28 Histomorphology (Goldner stain) of the wall of the stomach in adult Xenopus. Transverse section (7 μm). cm Circular layer of muscularis, ep epithelium, lp lamina propria with gastric glands (gg) composed of neck cells (1 mucus producing cells), oxyntic cells (2 gastric acid producing cells) and chief-cells (3 pepsinogen-producing cells), lm longitudinal layer of muscularis, lu lumen, mm muscular layer of mucosa, sm submucosa, se serosa, v vein. Arrow Subepithelial blood vessel. Fig. 29 VCC/stereomicroscopy of the digestive tract in adult Xenopus. Dorsal aspect. dd Duodenum, es esophagus, li large intestine, pa pancreas, si small intestine, sp spleen, st stomach. Fig. 30 VCC/SEM of microvasculature of the stomach of adult Xenopus. Ventral aspect. Serosal view. Cranial is at the right, lateral is at the bottom. Arterial vessels are colored red, venous vessels are colored blue. cavgv Caudal ventral gastric vein, cvgv cranial ventral gastric vein, dd duodenum, es esophagus, hpv hepatic portal vein, lbav left branch of abdominal vein, mvgv middle ventral gastric vein, pa pancreas, pua pulmonary artery, puv pulmonary vein, st stomach, vga ventral gastric artery, vgv ventral gastric vein. Fig. 31 Vascular bed of the muscular layer of the adult stomach. Serosal view. Note the rectangular capillary meshwork with outer capillaries (c1) paralleling the longitudinal layer and inner capillaries (c2) paralleling the circular layer of the muscular layer. Arterioles (colored red) located in the submucosa feed muscular capillaries. Arrowhead Origin of a feeding arteriole. Arrows indicate direction of blood flow. Fig. 32 Microangioarchitecture of the wall of the stomach in adult Xenopus. Longitudinal section. Detail view. Note the mucosal capillary bed (mcb) embracing gastric glands, the convoluted arteries (colored red) within the submucosa (sm), and the capillary bed of the muscular layer (ml). lu Lumen
	Figs. 33–35. Fig. 33 Microangioarchitecture of the stomach in adult Xenopus. Transverse section at the level indicated in Figs. 34 and 35. Overview. Note the intense folding of the gastric mucosa. aa Arteriole, lp lamina propria, lu lumen, ml muscular layer, sm submucosa, v vein. Fig. 34 Vascular corrosion cast of stomach (st) and duodenum (dd). Dorsal aspect. Serosal view. Cranial is to the left. Dashed line indicates level of the transverse section shown in Fig. 33. pa Pancreas, dga dorsal gastric artery, dgv dorsal gastric vein. Fig. 35 Same as Fig. 34, but ventral aspect. dd Duodenum, dga dorsal gastric artery, gda gastro-duodenal artery, pa pancreas, st stomach, vga ventral gastric artery, vgv ventral gastric vein
	Figs. 36–38. Fig. 36 Microvascular pattern of gastric mucosal folds (mf) in adult Xenopus. Detail from a transverse section. Note strongly undulating arteries (a) with ascending arterioles (aa). lu Lumen, ml muscular layer (muscularis), sm submucosa. Fig. 37 Microvascular pattern of a single mucosal fold. Detail from Fig. 33 (boxed area). Note two ascending arterioles (colored red) and two descending venules (colored blue) supplying/draining the mucosal capillary bed. Arrows indicate direction of blood flow. lu Lumen. Fig. 38 Microvascular pattern of the mucosa of the stomach in adult Xenopus. Detail from Fig. 37 (boxed area). Note that ascending arterioles (colored red) capillarize close below the mucosal epithelium. Mucosal capillaries descend centrifugally and drain into venules (colored blue) located at the base of the mucosa. Arrows indicate direction of blood flow. lu Lumen
	Figs. 39–42. Fig. 39 Microvascular patterns of the gastric mucosa in adult Xenopus. Detail from a transverse sectioned stomach. Oblique serosal view. Note small submucosal arteries (a), ascending arterioles (colored red), descending venules and submucosal small veins (v) (colored blue). Dashed lines outline gastric glands (gg) ensheathed by descending capillaries (c). Arrows indicate direction of blood flow. Fig. 40 Microvascular patterns of the gastric mucosa in adult Xenopus. The ascending arteriole (aa) branches terminally into subepithelial capillaries (c). Arteries (a) are red, veins (v) are blue. Arrows indicate direction of blood flow. Fig. 41 Same as Figs. 39 and 40, but arteriole (aa) ascends slightly obliquely and continues into the uppermost subepithelial capillary meshes (c). Note the narrowing (arrowhead) at the origin of the ascending arteriole (aa) from the submucosal artery (a). Arrows indicate direction of blood flow. Fig. 42 Vascular patterns of the gastric mucosa in adult Xenopus. Luminal view. Note the large capillary meshes (outlined by dashed lines) encircling smaller ones
	Fig. 43. Scheme depicting the blood supply of the gastric mucosa in adult Xenopus laevis. Note the ascending (centripetal) arterioles that capillarize into subepithelial capillaries (c), and descending (centrifugal) venules that drain into submucosal veins. cm Vessels of the inner circular muscle layer, ep columnar gastric epithelium, gg gastric glands, lm vessels of the outer longitudinal muscle layer, lp lamina propria, sm submucosa. Arrows indicate direction of blood flow

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