Summary
Actin-containing cytoplasmic fibers were visualized in the mesenteric mesothelial cells of the large intestine of bullfrog tadpoles by rhodamine-phalloidin staining of en face preparations of mesothelial cells. These fibers were concurrently stained by immunofluorescence using antibodies to myosin or α-actinin. Electron microscopy showed the presence of bundles of microfilaments in the basal cytoplasm of the cells. Such fibers in the mesothelial cells may be comparable to the stress fibers present in cultured cells. The mesothelial cells initially formed axially oriented stress fibers when they changed from a rhombic to a slender spindle-like shape. On the other hand, stress fibers disappeared as cells transformed from elongated to polygonal shapes during the period of metamorphic climax. Expression of stress fibers in these cells appears to be related to the degree of tension loaded on the mesentery, which may be generated by mesenteric winding. These stress fibers in the mesothelial cells may serve to regulate cellular transformation. They may also help to maintain cellular integrity by strengthening the cellular attachment to subepithelial tissue against tensile stress exerted on the mesentery.
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Abercrombie M, Heaysman JEM, Pogrum SM (1971) The locomotion of fibroblasts in culture. IV. Electron microscopy of the leading lamella. Exp Cell Res 67:359–367
Buckley IK, Porter KP (1967) Cytoplasmic fibers in living cultured cells. A light and electron microscope-study. Protoplasma 64:349–380
Burridge K (1981) Are stress fibers contractile? Nature 294:691–692
Byers HR, Fujiwara K (1982) Stress fibers in cells in situ: Immunofluorescence visualization with antiactin, antimyosin, and antialpha-actinin. J Cell Biol 93:804–811
Byers HR, White GE, Fujiwara K (1984) Organization and function of stress fibers in cells in vitro and in situ. In: Dawben RM, Shay JW (eds) Cell and Muscle Motility. Plenum Publishing Co, New York, pp 83–137
Couchman JR, Rees DA (1979) The behaviour of fibroblasts migrating from chick heart explants: Changes in adhesion, locomotion and growth, and in the distribution of actomyosin and fibronectin. J Cell Sci 39:149–165
Craig SW, Pollard TD (1982) Actin-binding proteins. Trend Biochem Sci 7:88–92
Drenckhahn D, Wagner J (1986) Stress fibers in the splenic sinus endothelium in situ: Molecular structure, relationship to the extracellular matrix, and contractility. J Cell Biol 102:1738–1747
Franke R-P, Gräfe M, Schnittler H, Seiffge D, Mittermayer C, Drenckhahn D (1984) Induction of human vascular endothelial stress fibers by fluid shear stress. Nature 307:648–649
Fujiwara K, Pollard TD (1976) Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow, and mitotic spindle of human cells. J Cell Biol 71:848–875
Fujiwara K, White GE, White LD (1985) Role of in situ stress fibers in cellular adhesion. In: Ishikawa H, Hatano S, Sato H (eds) Cell Motility: Mechanism and Regulation. University of Tokyo Press, Tokyo, pp 477–492
Gabbiani G, Gabbiani F, Lombardi D, Schwartz SM (1983) Organization of actin cytoskeleton in normal and regenerating arterial endothelial cells. Proc Natl Acad Sci USA 80:2361–2364
Geiger B, Avnur Z, Rinnerthaler G, Hinssen H, Small V (1984) Microfilament-organizing centers in areas of cell contact: Cytoskeletal interactions during cell attachment and locomotion. J Cell Biol 99:83s-91s
Goldman RD, Chojnacki B, Yerna M-J (1979) Ultrastructure of microfilament bundles in baby hamster kidney (BHK-21) cells: The use of tannic acid. J Cell Biol 80:759–766
Gordon SR, Essner E, Rothstein H (1982) In situ demonstration of actin in normal and injured occular tissues using 7-nitrobenz-2-oxa-1,3-diazole phallacidin. Cell Motil 2:343–354
Gröschel-Stewart U (1980) Immunocytochemistry of cytoplasmic contractile proteins. Int Rev Cytol 65:193–254
Herman IM, Crisona NJ, Pollard TD (1981) Relation between cell activity and the distribution of cytoplasmic actin and myosin. J Cell Biol 90:84–91
Herman IM, Pollard TD, Wong AJ (1982) Contractile proteins in endothelial cells. Ann NY Acad Sci 401:50–60
Herman IM, Brant AM, Warty VS, Bonaccorso J, Klein E, Kormos RL, Borovetz H (1987) Hemodynamics and the vascular endothelial cytoskeleton. J Cell Biol 105:291–302
Hirai S, Hirabayashi T (1983) Developmental change of protein constituents in chicken gizzards. Dev Biol 97:483–493
Hirai S, Hirabayashi T (1986) Development of myofibrils in the gizzard of chicken embryos: Intracellular, distribution of structural proteins and development of contractility. Cell Tissue Res 243:487–493
Hirokawa N (1982) Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method. J Cell Biol 94:129–142
Hüttner J, Walker C, Gabbiani G (1985) Aortic endothelial cell during regeneration. Remodeling of cell junctions, stress fibers, and stress fiber membrane attachment domains. Lab Invest 53:287–302
Krawczyk WS (1971) A, pattern of epidermal cell migration during wound healing. J Cell Biol 49:247–263
Lazarides E, Burridge K (1975) Alpha-actinin immunofluorescent localization of a muscle structural protein in non-muscle cells. Cell 6:289–298
Romeis B (1968) Mikroskopische Technik. R. Oldenbourg Verlag, München
Singer II (1979) The fibronexus: a transmembrane association of fibronectin-containing fibers and bundles of 5 nm microfilaments in hamster and human fibroblasts. Cell 16:675–685
Soranno T, Bell E (1982) Cytostructural dynamics of spreading and translocating cells. J Cell Biol 95:127–136
Spooner BS, Yamada KM, Wessells NK (1971) Microfilaments and cell locomotion. J Cell Biol 49:595–613
Sugimoto K, Ichikawa Y, Nakamura I (1985) Peroxidase activity in the epithelium of the digestive tract of the bullfrog, Rana catesbeiana. J Exp Zool 233:209–219
Sugimoto K, Fujii S, Ichikawa Y, Nakamura I (1986) The fate and role of openings formed in the mesentery of bullfrog tadpoles, with reference to the contour of mesothelial cells. J Morphol 188:119–127
Sugimoto K, Fujii S, Ichikawa Y, Nakamura I (1988) Role of actin filaments in shape formation of mesenteric mesothelial cells of the bullfrog. J Morphol 198:321–329
Sugimoto K, Fujii S, Ichikawa Y, Nakamura I, (1989) Expression of stress fibers in bullfrog mesothelial cells in situ. Cell Tissue Res 258:373–380
Taylor AC, Kollros JJ (1946) Stages in the normal development of Rana pipiens larvae. Anat Rec 94:7–23
White GE, Gimbrone MA, Fujiwara K (1983) Factors, influencing the expression of stress fibers in vascular endothelial cells in situ. J Cell Biol 97:416–425
Wong AJ, Pollard TD, Herman IM (1983) Actin filament stress fibers in vascular endothelial cells in vivo. Science 219:867–869
Wulf E, Deboben A, Bautz FA, Faulstich H, Wieland T (1979) Fluorescent phalloidin, a tool for the visualization of cellular actin. Proc Natl Acad Sci USA 76:4498–4502
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Sugimoto, K., Fujii, S., Kaiho, M. et al. Stress fibers in the mesenteric mesothelial cells of the large intestine of the bullfrog, Rana catesbeiana . Cell Tissue Res 261, 509–516 (1990). https://doi.org/10.1007/BF00313530
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DOI: https://doi.org/10.1007/BF00313530