Cell Tiss. Res. 195, 381-394 (1978)

Cell and Tissue Research 9 by Springer-Verlag 1978

Fine Structure of the Mammalian Renal Capsule: The Atypical Smooth Muscle Cell and Its Functional Meaning Kazuo Kobayashi* Second Department of Internal Medicineand Department of Anatomy, Kyushu University,Fukuoka, Japan

Summary. The present electron microscopic study on the fine structure of the renal capsule of some mammals (mouse, rat, mole, guinea pig and rabbit) shows" that, although there are some variations in the structure, the general morphology is the same. The renal capsule of these animals consists of two layers, a connective tissue layer and an atypical smooth muscle cell layer, and is bound to the renal parenchyma by a thin peritubular loose connective tissue. The atypical smooth muscle cell is characterized by the existence of fine cytoplasmic filaments usually arranged along the long axis of the cell, and the cells also show a complicated interlocking among adjacent cells. The atypical smooth muscle cells gradually undergo a transition to fibroblasts 6f the upper connective tissue layer, losing their similarities to smooth muscle cells. When intrarenal pressure is elevated and the renal capsule is distended, the intercellular space among interdigitating or overlapping atypical smooth muscle cells is extensively dilated. Tracers such as horseradish peroxidase and ferritin injected intravenously or intraperitoneally can transverse the renal capsule. From the present study, it is concluded that the renal capsule of mammals possesses common structures, and contains atypical smooth muscle cells. These morphological characteristics suggest that the renal capsule could play a certain role related to the renal function. Key words: Renal capsule - Smooth muscle cell - Fibroblast. Light microscopic studies have shown that the renal capsule consists of a tunica fibrosa and a tunica muscularis, and that smooth muscle cells occur in the capsule (von M611endorff, 1930, Niessing, 1935). The ultrastructure of the rat renal capsule has recently been described, and shown to contain unique squamous cells different from smooth muscle cells (Bulger, 1973). Kazuo Kobayashi,M.D., SecondDepartmentof Internal Medicine,Facultyof Medicine, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812, Japan * The author wishes to acknowledge the helpful advioes of Prof. T. Yamamoto Send offprint requests to:

0302-766X/78/0195/0381 / $02.80

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A f l u o r e s c e n t h i s t o c h e m i c a l s t u d y has s h o w n its a d r e n e r g i c i n n e r v a t i o n , p r o v i d i n g a m o r p h o l o g i c a l basis for a d r e n e r g i c r e g u l a t i o n o f the elasticity o f the c a p s u l e ( I n a g a k i a n d T a n a k a , 1977). P h y s i o l o g i c a l l y , it h a s b e e n d e s c r i b e d t h a t the elastic p r o p e r t y o f the r e n a l c a p s u l e p r o v i d e s the m a j o r force o p p o s i n g e x p a n s i o n o f the o u t e r c o r t e x w h e n i n t r a r e n a l p r e s s u r e is i n c r e a s e d , a n d is a n i m p o r t a n t d e t e r m i n a n t o f the w h o l e k i d n e y v o l u m e / p r e s s u r e r e l a t i o n s h i p ( H e b e r t et al., 1975). T h e s e facts suggest t h a t the r e n a l c a p s u l e plays a c e r t a i n role r e l a t e d to the f u n c t i o n o f the k i d n e y . T h e p r e s e n t s t u d y was c a r r i e d o u t to clarify the fine s t r u c t u r e o f r e n a l c a p s u l e o f s o m e m a m m a l s w i t h reference to the existence o f a t y p i c a l s m o o t h m u s c l e cells. T h e i r f u n c t i o n a l significance is also discussed.

Materials and Methods Mice, rats, moles, guinea pigs and rabbits were used in the present study. Small pieces of the kidney were removed from the ventral and dorsal surfaces, and hilus area respectively. Some were fixed by immersion or in situ in 3 % glutaraldehyde buffered with 0.1 M cacodylate at pH 7.4 (Sabatini et al., 1963) or halfstrength Karnovsky's fixative (Karnovsky, 1967) for two hours. Others were fixed by retrograde perfusion through the abdominal aorta using half-strength Karnovsky's fixative (Maunsbach, 1966). In some cases, 3 % tannic acid (van Deurs, 1975) or 1% colloidal lanthanum (Revel and Karnovsky, 1967) was added to the fixative. The tissues were rinsed several times in the same buffer solution and then postfixed in ice cold 1% osmium tetroxide for two hours. They were dehydrated in graded ethanols, and embedded in Epon 812 (Luft, 1961). After post-fixation, some materials were placed in 4% aqueous uranyl acetate for one hour at room temperature for block staining. Experimental Conditions. 1) 0.1 ml of Pelikan Indian Ink diluted 10 times with saline (Giinther Wagner Co., Germ.) was slowly injected intrarenallyunder slight anesthesia (Ohkuma, 1973). Portions of kidney tissue were removed, apart from the border of the injected area, and fixed in 15, 30 and 60 min after injection. 2) 10 mg per I00 gm body weight of horseradish peroxidase (Sigma type II, Sigma Chemical Co., St. Louis, Missouri) or 100 mg per 100 gm body weight of ferritin (2 x crystalline, horse spleen, cadmium free, Nutritional Biochemicals Co., Cleveland, Ohio) dissolved in saline was injected intravenously through the dorsal tail vein. The injection volume was 1.0 ml per 100 gm body weight. Kidney samples were removed and fixed in 5, 30 and 60rain after injection. 3) The same dose of horseradish peroxidase and ferritin were dissolved in 5 ml of saline and injected intraperitoneally, and then some kidney material was removed and fixed at same intervals as the intravenous injection. Control animals for 1), 2) and 3) received the same volume of saline. In the animals treated with horseradish peroxidase and control animals for the horseradish peroxidase injection, specimens were incubated in DAB medium for 30 rain at room temperature (Graham and Karnovsky, 1966). 4) In order to elevate the intrarenal pressure and distend the renal capsule, the renal vein was clipped for one minute during the fixation with intravenous perfusion, when infusion started. The materials in these experimental conditions were treated the same as the usual fixation, and embedded in Epon 812. Thick sections were stained with toluidine blue for light microscopy. Thin sections were made from all these materials with glass knives on a Porter-Blum microtome, and then stained with lead tartrate (Millonig, 1961). All specimens were examined in a Hitachi-HU-12A electron microscope.

Results A l t h o u g h there are s o m e m i n o r v a r i a t i o n s in the s t r u c t u r e o f the r e n a l c a p s u l e in different species, the basic s t r u c t u r e is essentially the same. T h e r e n a l c a p s u l e o f

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Fig. 1. Electron micrograph of the mouse renal capsule. The renal capsule consists of the connective tissue layer and atypical smooth muscle cell layer. The mesothelial cell layer of peritoneum borders between the renal capsule and peritoneal cavity. AS atypical smooth muscle cell layer; CT connective tissue layer; M mesothelial cell. x 10,000

mouse, rat, mole, guinea pig and rabbit is composed of the following layers; 1) a connective tissue layer and 2) an atypical smooth muscle cell layer (Figs. 1, 2). These layers are bound to the renal parenchyma, a thin peritubular loose connective tissue. The mesothelial cell layer of peritoneum separates the renal capsule from the peritoneal cavity (Fig. 1). Atypical smooth muscle cells which possess morphological similarities to both smooth muscle cells and fibroblasts, occur in the renal capsule of all the animals studied (Figs. 1, 2, 3, 4). The connective tissue layer is a major component of the renal capsule, and is composed of several strata (Figs. 1, 2) of irregular dense connective tissue. The fibers of each stratum are mostly collagenous in nature and are not arranged parallel to one another. Besides these collagenous fibers, microfibrils of 100A in diameter are associated with small globules of material in the connective tissue layer. They are amorphous in appearance and show little affinity for either lead or

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Fig. 2. Electronmicrographof the rabbit renal capsule. The connectivetissuelayer and atypicalsmooth muscle cell layer are well developed.AS atypical smooth muscle cell layer; CT connectivetissue layer. x 2000 uranyl acetate, but great affinity for tannic acid. These elastic fibers are usually situated in the superficial stratum of the connective tissue layer. The fibroblasts in this layer are flattened or spindle-shaped with long sheet-like processes. They lie almost parallel to each other, and separate some of collagenous strata (Figs. 1, 2). The cytoplasm is relatively sparse, and contains a small amount of mitochondria, rough endoplasmic reticulum and Golgi complexes. The basement membrane is not associated with these fibroblasts. In the collagenous interstitium of this layer, small arterial, venous and lymphatic vessels are sometimes observed. In addition to these vessels, cellular components such as mast cells and eosinophilic leukocytes are also observed (Fig. 15). Small non-myelinated nerve fibers are sometimes situated in the perivascular area. The atypical smooth muscle cell layer is the innermost layer of the renal capsule, and consists of several cell sheets (Figs. 1, 2, 3). These atypical smooth muscle cells

Fig. 3. Electron micrograph of the atypical smooth muscle cells in the guinea pig renal capsule. The electron dense areas are located beneath the plasma membrane. Arrow; interlocking between adjacent cells; AC atypical cilium; G Golgi complex, x 16,000 Fig. 4. Electron micrograph of the atypical smooth muscle cells in the rat renal capsule. The cytoplasm contains abundant filaments and electron dense areas among filamentous bundles. Arrow; dense body; AS atypical smooth muscle cell. x 15,000

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have two outstanding morphological features. One is the presence of cytoplasmic filaments usually arranged along the long axis of the cell (Figs. 3, 4), and another is their complex interlocking with adjacent cells (Figs. 3, 6, 7). These cells are elongated and strap-like in shape, and exhibit long sheet-like processes (Figs. 1, 2). The surface is covered with a relative thick basement membrane. The nucleus is elongated or oval in shape with marginal masses of chromatin, and the nucleolus is not prominent. The cell organelles are mainly aggregated in the cytoplasm adjacent to the nuclear pole, and as a whole, are scanty. They consist of small areas of rough endoplasmic reticulum containing homogenous materials, small rounded or elongated mitochondria, free ribosomes and glycogen particles (Figs. 3, 5, 6). The Golgi complex is well developed, compared with other cell organelles. There are relatively large number of pinocytotic vesicles located at the bilateral surfaces of the cell and the surface facing the intercellular space between adjacent cells (Figs. 7, 8, 13). The cytoplasmic filaments in some instances occupy a large portion of the cytoplasm (Fig. 4), but in most cases they are sparse, and found beneath the plasma membrane (Fig. 3). They are usually arranged parallel to the long axis of the cell. Two different kinds of filaments can be identified, measuring mostly 40-60A and 90-110A in diameter respectively (Fig. 5). These cells contain some electron dense material beneath the plasma membrane and among filaments in the cytoplasm (Figs. 3, 4), resembling the fusiform density or attachment plaque in typical smooth muscle cell. Autonomic nerves sometimes terminate at these atypical smooth muscle cells. Naked nerve endings containing both cored vesicles and agranular vesicles, which are not surrounded with the basement membrane or Schwann cell, are located close to the plasma membrane. The basement membrane surrounding the atypical smooth muscle cell separates the nerve ending and the cell. These autonomic nerves may also penetrate the cell (Fig. 6). The atypical smooth muscle cells are extensively interdigitated or overlap with each other, and the intercellular spaces appear to form a kind of lumen (Figs. 3, 5, 6, 7, 8). The luminar surface is not covered with the basement membrane, while the abluminar surface is. The lumen is formed between adjacent cells by means of tight junctions (Fig. 7). There are some homogenous materials of low electron density in these lumina. A single cilium frequently projects into this intercellular lumen. The structure of the cilium is somewhat different from the typical cilium showing nine peripheral doublets and two central microtubules, namely this kind of cilium shows the atypical constitution of doublets and microtubules such as 5+ 0 or 7+ 1 (Fig. 3). Focal junctions similar in appearance to the intermediate type and tight junctions are frequently observed among interdigitating or overlapping cells (Figs. 5, 7, 9). Gap junctions are also sometimes observed among adjacent cells (Fig. 10). The atypical smooth muscle cells gradually undergo transition into a fibroblast in the upper connective tissue layer losing their similarities to the smooth muscle cell. The cell process of a fibroblast in the connective tissue layer is sometimes interlocked with that of the outermost cell in the atypical smooth muscle cell layer. At the hilus of the kidney, these cells also undergo transition into the fibroblast of the hilar connective tissue. There are no regional differences in the structure of the renal capsule. As the size of the animal increases among the animals used in the

Fig. 5. Electron micrograph of the atypical smooth muscle cells in the rat renal capsule. Single arrow; filament of 60A in diameter, Double arrow; filament of 100A in diameter, T J tight junction, x 82,000

Fig. 6. Electron micrograph of the autonomic innervation of atypical smooth muscle cells in the rat renal capsule. Nerve endings containing cored vesicles are closely associated with atypical smooth muscle cells. A S 1-3 atypical smooth muscle cell; IL intercellular lumen; N E nerve ending, x 23,000

Fig. 7. The interdigitation among adjacent atypical smooth muscle cells of rat renal capsule is well developed, and tannic acid permeates into the intercellular lumen through the tight junction. Arrow; tight junction, x 46,000 Fig. 8. Electron micrograph of the atypical smooth muscle cells in the rat renal capsule. Pinocytotic vesicles are well developed. F filament, P pinocytotic vesicle, x 36,000 Fig. 9. Electron micrograph of the atypical smooth muscle cells in the rat renal capsule. Lanthanum permeates into the intercellular space through the tight junction. Arrow; tight junction. • 100,000 Fig. 10. Gap junction between atypical smooth muscle cells of the rat renal capsule, x 100,000

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Fig. 11. Electron micrograph of the rat renal capsule 5 min after intravenous injection of horseradish peroxidase. Horseradish peroxidase permeates into the intercellular space beyond the tight junction. Arrow; tight junction; CS cytosome containing peroxidase, x 65,000 Fig. 12. Electron micrograph of the rat renal capsule in 60 min after intraperitoneal injection of ferritin. The ferritin particles localize in the cytosomes of atypical smooth muscle cell, but never in the intercellular space between overlapping cells. Arrow; intercellular space between adjacent overlapping cells; CS cytosome containing ferritin; N nucleus, x 70,000 Fig. 13. The atypical smooth muscle cell of rat renal capsule shows the image of endo- or exocytosis of particulate material, x 90,000

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Fig. 14. Electron micrograph of the rat renal capsule in the condition of renal vein constriction. The intercellular lumen (arrow) formed by interdigitation or overlapping among atypical smooth muscle cells is extensively dilated, x 8500 Fig. 15. Mast ceils and eosinophilic leukocytes are observed in the edematous interstitium of the connective tissue layer of rat renal capsule in the condition of renal vein constriction, x 3000

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present study, the renal capsule becomes thicker, and atypical smooth muscle cells are more highly developed (Figs. 1, 2). The colloidal lanthanum and tannic acid penetrate into the intercellular space among atypical smooth muscle cells beyond the intercellular junctions (Figs. 7, 9). The colloidal carbon injected intrarenally prior to fixation, however, is not found in this intercellular space, but in the lumen of lymphatic vessel in the connective tissue layer. Soon after intraperitoneal injection, tracers are localized within pinocytotic vesicles and vacuoles of the peritoneal mesothelium, and also in the cytosomes of fibroblast in the connective tissue layer. By 60 min after injection, these tracers had gained access to the atypical smooth muscle cells. Horseradish peroxidase penetrates into the intercellular space among atypical smooth muscle cells beyond the tight junction (Fig. 11). However, ferritin particles never penetrate into this space through the intercellular pathway, but they are transported by pinocytotic vesicles in the same way as other large particulate materials (Figs. 12, 13). Intravenously injected tracers show a similar time sequence passage in the opposite direction. When intrarenal pressure is elevated and the renal capsule distended by renal vein constriction, the interdigitation between atypical smooth muscle cells becomes loose. The intercellular space is extensively dilated (Fig. 14). However, neither the intercellular tight junctions between these cells forming a lumen become dissociated, nor do the atypical smooth muscle cells become discontinuous. On the other hand, the interstitium of connective tissue layer becomes edematous (Fig. 15).

Discussion

An early light microscopic study revealed that the renal capsule contained two different layers: the tunica fibrosa and tunica muscularis (von M611endorff, 1930). Smooth muscle cells were also mentioned as a component of the renal capsule in a number of species. It has also been noted that the renal capsule is a closed system and plays a role in relation to renal function (Niessing, 1935). The fine structure of the rat renal capsule observed by electron microscopy has shown the existence of unique squamous cells that are different from smooth muscle cells (Bulger, 1973). The present study has demonstrated that the basic structure of the renal capsule is essentially the same in a variety of mammalian species, and atypical smooth muscle cell is a component in them all. These cells possess morphological characteristics similar to both smooth muscle cell (Rhodin, 1962; Gabella, 1973) and fibroblast (Movat and Fernando, 1962), and are referred to as "atypical smooth muscle cells". They contain fibrillar components and electron dense bodies beneath the plasma membrane or within the fibrillar bundles, which are similar to those found in typical smooth muscle cells (Rhodin, 1962; Gabella, 1973). Furthermore, they are covered with a basement membrane, and are interconnected with each other by means of tight, intermediate and gap junctions, as in smooth muscle (Oosaki and Ishii, 1964; Uehara and Burnstock, 1970), and are similarly also innervated with autonomic nerves (Richardson, 1962).

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While they can be recognized as smooth muscle cells according to the above mentioned characteristics, they differ from typical smooth muscle cells in some aspects. Thus, they contain fewer filaments and less developed dense bodies. The shape of the cell is elongated or strap-like, and it possesses long sheet-like processes, These latter morphological characteristics are more similar to those of fibroblasts (Movat and Fernando,1962). An intermediate form between smooth muscle cell and fibroblast has been observed in the outer elastic layer of aortic media (Moss and Benditt, 1970) and also in the lamina propria of the small intestine (Pitha, 1968). Under pathological conditions, smooth muscle cells resembling fibroblast have also been observed in the uterus of rat treated with estrogen (Ross and Klebeanoff, 1967) and atherosclerotic lesions, and described as modified smooth muscle cells (Thomas et al., 1963). Conversely, fibroblasts resembling smooth muscle cell have been described in the normal human umbilical cord (Parry, 1970), and also in the granulation tissue of wound where they have been called myofibroblasts (Gabbiani et al., 1971). It is to be noted that smooth muscle cells behave like fibroblasts, and can synthesize connective tissue proteins such as collagen and elastin in vivo and in vitro (Ross and Klebanoff, 1971; Ross, 1971). Recent studies have revealed that non-muscular cells such as fibroblast contain contractile elements like actin and myosin (Ishikawa et al., 1969; Jorgensen et al., 1975; Abercrombie et al., 1976). In the kidney, the existence of myofilaments has also been described in the tubular epithelium, parietal and visceral epithelium of Bowman's capsule and interstitial cell (Newstead, 1971; Trenchev et al., 1976). These facts raise the question of what the relationship between smooth muscle cell and fibroblast is, and suggests that both cells are much more closely related than classical histology would have allowed one to suppose. It seems possible that either smooth muscle cell or fibroblast may transform through an intermediate type into the other, and may be interchangable. The intercellular lumen formed by the interdigitation or overlapping among atypical smooth muscle cells contains homogenous materials, and single atypical cilium projects into this lumen. It may be postulated that this kind of lumen provides a preferential pathway for interstitial fluid (Bulger, 1973), and the cilium might participate in the fluid transport by its stirring action (Webber and Lee, 1975). A functional communication between the renal capsule and deep renal interstitium has been demonstrated using 1311labelled albumin (Wunderlich et al., 1971), and the time sequence study using tracers in the present investigation also suggests that there is a communication between the renal capsule and renal parenchyma. Physiologically, a change in the overall kidney volume contributes to a change of renal pressue, and this phenomenon must at least partially be related to the elastic property of the renal capsule (Hebert et al., 1975). The irregular dense connective tissue layer of the capsule contains collagenous fibers intermingled with elastic fibers that are interwoven in many directions, and in addition, the atypical smooth muscle cells which are innervated with autonomic nerves, may participate in the regulation of this elasticity (Inagaki and Tanaka, 1977). The elastic property of the renal capsule provides the major force against the expansion of the outer cortex,

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and is thus an important determinant of the whole kidney volume/pressure relationship (Hebert et al., 1975). When intrarenal pressure is elevated and renal capsule is distended, the interdigitation between atypical smooth muscle cells becomes loose, and the intercellular space is extensively dilated. This may represent morphological evidence of the adaptation of the renal capsule to elevated intrarenal pressure. Thus, it may be that the atypical smooth muscle cells of the renal capsule play an important role by their contraction, in adjusting kidney volume, and thereby intrarenal pressure. References Abercrombie, M., Dunn, G.A., Heath, J.P.: Locomotion and contraction in non-muscle cells. In: Contractile systems in non-muscle tissue. (S.V. Perry, A. Margretb and R.S. Adelstein., eds.), pp. 311. Amsterdam-Oxford-New York: North-Holand 1976 Bulger, R.E.: Rat renal capsule: Presence of layers of unique squamous cells. Anat. Rec. 117, 393--408 (1973) Deurs, B. van: The use of a tannic acid-glutaraldehyde fixative to visualize gap and tight junctions. J. Ultrastruct. Res 50, 185-192 (1975) Gabbiani, G., Ryan, G.B., Majno, G.: Presence of modified fibroblasts in granulation tissue and their possible role in wound contraction. Experientia 27, 549-550 (t971) Gabella, G.: I. Cellular structures and electrophysiological behaviour. Fine structure of smooth muscle. Philos. Trans. R. Soc. Lond. [Biol]. 265, 7-16 (1973) Graham, R.C., Jr., Karnovsky, M.J.: The early stages of absorption of injected horseradish peroxidase in the proximal tubules of the mouse kidney: ultrastructural cytochemistry by a new technique. J. Histochem. Cytochem. 14, 291-302 (1966) Hebert, L.A., Stuart, K.A., Stemper, J.A.: Whole kidney volume/pressure relationships. Kidney Int. 7, 45-54 (1975) Inagaki, C., Tanaka, C.: Histochemical demonstration of adrenergic nerve fibers in the renal capsule of rats. Experientia 33, 1222 1223 (1977) Ishikawa, H., Bishoff, R., Holtzer, H.: Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J. Cell Biol. 43, 312-328 (1969) Jorgensen, A.O., Subrahmanyan, L., Kalnins, V.I.: Localization of tropomyosin in mouse embryo fibroblasts. Am. J. Anat. 142, 519-525 (1975) Karnovsky, M.J.: The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol. 35, 213-236 (1967) Luft, J.H.: Improvements in epoxy resin embedding methods. J. Biophys. Biochem. Cytiol. 9, 409~,14 (1961) Maunsbach, A.B.: The influence of different fixatives and fixation methods on the ultrastructure of rat kidney proximal tubule cells. I. Comparison of different perfusion fixation methods and of glutaraldehyde, formaldehyde and osmium tetroxide fixatives. J. Ultrastruct. Res. 15, 242-282 (1966) Millonig, G.: A modified procedure for lead staining of thin section. J. Biophys. Biochem. Cytol. 11, 736-739 (1961) M611endorff, W. von: H a m und Geschlechtsapparat. In: Handbuch der Mikroskopischen Anatomie des Menschen. Bd. VII. pp. 140-143. Bedim Springer 1930 Moss, N.S., Benditt, E.P.: Spontaneous and experimentally induced arterial lesions. I. An ultrastructural survey of the normal chicken aorta. Lab. Invest. 22, 166-183 (1970) Movat, H.Z., Fernando, N.V.P.: The fine structure of connective tissue. I. The fibroblast. Exp. Mol. Pathol. 1, 509-534 (1962) Newstead, J.D.: Filaments in renal parenchymal and interstitial cells. J. Ultrastruct. Res. 34, 316-328 (1971) Niessing, K.: Nierenkapsel und Gitterfasernsysteme in ihren funktionellen Beziehungen zur Form und Architektur der Niere. Gegenbaurs Morphol. Jahrb. 75, 331-373 (1935)

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Ohkuma, M.: Electron microscopic observation of the renal lymphatic capillary after injection of ink solution. Lymphology 6, 175-181 (1973) Oosaki, T., Ishii, S.: Junctional structure of smooth muscle cells. The ultrastructural of the regions of junction between smooth muscle cells in the rat small intestine. J. Ultrastruct. Res. 10, 567-577 (1964) Parry, E.W.: Some electron microscope observations on the mesenchymal structures of full-term umbilical cord. J. Anat. 107, 505-518 (1970) Pitha, J.: The fine structure of clear fibroblast-like cells in the lamina propria of small intestine. J. Ultrastruct. Res. 22, 231-239 (1968) Revel, J.P., Karnovsky, M.J. : Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33, C7 (1967) Rhodin, J.A.G.: Fine structure of vascular walls in mammals. With special reference to smooth muscle component. Physiol. Rev. 42, Suppl. 5, 48-81 (1962) Richardson, K.C.: The fine structure of autonomic nerve endings in smooth muscle of the rat vas deferens. J. Anat. 96, 427~142 (1962) Ross, R.: The smooth muscle cell. II. Growth of smooth muscle in culture and formation of elastic fibers. J. Cell Biol. 50, 172-186 (1971) Ross, R., Klebanoff, S.I.: Fine structural changes in uterine smooth muscle and fibroblasts in response to estrogen. J. Cell Biol. 32, 155-167 (1967) Ross, R., Klebanoff, S.I.: The smooth muscle cell. I. In vitro synthesis of connective tissue proteins. J. Cell Biol. 511, 159-171 (1971) Sabatini, D.D., Bensch, K., Barrnett, R.J.: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 19-58 (1963) Thomas, W.A., Jones, R., Scott, R.F., Morrison, E., Goodale, F., Imai, H.: Production of early atherosclerotic lesions in rats characterized by proliferation of"modified smooth muscle cells". Exp. Mol. Pathol. 1, Suppl. 1, 40-61 (1963) Trenchev, P., Dorling, J., Webb, J., Hilborow, E.J.: Localization of smooth muscle-like contractile proteins in kidney by immunoelectron microscopy. J. Anat. 121, 85-95 (1976) Uehara, Y., Burnstock, G.: Demonstration of"gap junction" between smooth muscle cells. J. Cell Biol. 44, 215-217 (1970) Webber, W.A., Lee, J.: Fine structure of mammalian renal cilia. Anat Rec. 182, 339-344 (1975) Wunderlich, P., Persson, E., Schnermann, J., Ulfendahl, H., Wolgast, M.: Hydrostatic pressure in the subcapsular interstitial space of rat and dog kidneys. Pfluegers Arch. 328, 307-319 (1971)

Accepted October 11, 1978

Fine structure of the mammalian renal capsule: the atypical smooth muscle cell and its functional meaning.

Cell Tiss. Res. 195, 381-394 (1978) Cell and Tissue Research 9 by Springer-Verlag 1978 Fine Structure of the Mammalian Renal Capsule: The Atypical S...
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