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Centrioles and the Formation of Rudimentary Cilia by Fibroblasts and Smooth Muscle Cells

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Centrioles and the Formation of Rudimentary Cilia by Fibroblasts and Smooth Muscle Cells CENTRIOLES AND THE FORMATION OF RUDIMENTARY CILIA BY FIBROBLASTS AND SMOOTH MUSCLE CELLS SERGEI SOROKIN, M.D. From the Department of Anatomy, Harvard Medical School, Boston, Massachusetts ABSTRACT Cells from a variety of sources, principally differentiating fibroblasts and smooth muscle cells from neonatal chicken and mammalian tissues and from organ cultures of chicken duodenum, were used as materials for an electron microscopic study on the formation of rudimentary cilia. Among the differentiating tissues many cells possessed a short, solitary cilium, which projected from one of the cell's pair of centrioles. Many stages evidently intermediate in the fashioning of cilium from centriole were encountered and furnished the evidence from which a reconstruction of ciliogenesis was attempted. The whole process may be divided into three phases. At first a solitary vesicle appears at one end of a centriole. The ciliary bud grows out from the same end of the centriole and invaginates the sac, which then becomes the temporary ciliary sheath. During the second phase the bud lengthens into a shaft, while the sheath enlarges to contain it. Enlargement of the sheath is effected by the repeated appearance of secondary vesicles nearby and their fusion with the sheath. Shaft and sheath reach the surface of the cell, where the sheath fuses with the plasma membrane during the third phase. Up to this point, formation of cilia follows the classical descriptions in outline. Subsequently, internal development of the shaft makes the rudi- mentary cilia of the investigated material more like certain non-motile centriolar derivatives than motile cilia. The pertinent literature is examined, and the cilia are tentatively assigned a non-motile status and a sensory function. Centrioles have long been regarded as organizers Centrioles usually lie at the cell center adjacent of kinetic activity in the cytoplasm of both somatic to the nucleus but in columnar epithelium (38) and germinative animal cells. However, as the they lie more frequently near the apical surface. dimensions of a centriole are typically but 300 to During mitosis they occupy the poles of the 500 m/~ in height by 150 m/z in diameter (8), spindles. It is not certain to what extent centrioles knowledge of its detailed structure has awaited normally are essential to mitosis, for many cells, development of the electron microscope. Affected notably those of the higher plants, regularly by studies employing such a device (2, 4, 8, 14), divide in their absence. After experimental the term centriole has become restricted from alteration, even cells normally possessing cen- previous wider application to the nearly cylindrical trioles, such as the spermatocytes of crane-flies, organelle composed of a set of nine parallel may divide without their participation (10). triple-fibers radially arranged about a space of In certain cells, centrioles take part in the lesser density. However, current ideas on the formation of cilia and flagella. In ciliated epithe- functions of centrioles have resulted from earlier lium they first divide repeatedly to form many studies by light microscopists. basal bodies, which subsequently sprout the motile 363 processes (17, 3 I). The fine structure of the basal these cilium-like processes in developing fibroblasts bodies differs only in minor details from that of and smooth muscle cells, principally from the the parent centrioles. The development of flagella lamina propria, submucosa, and muscularis of the during spermatogenesis has been studied in a duodenum of both chick and rat, and from organ variety of forms (33), especially insects (3, 13-15, cultures of the chick's duodenum. The develop- 20) and mammals (6). One centriole of the pair ment of the cilia from their parent centrioles is present in the postnuclear region of the spermatid described in detail, and some consideration is sprouts a flagellum, but many details of the inter- given to their possible functional roles in these mediate steps of this process remain unclear. cells. An account by Sotelo and Trujillo-Cen6z Centrioles, basal bodies, and cilia have been shown (34) of the formation of somewhat similar solitary to form part of certain sensory structures of cells, cilia in neural epithelium of developing chick is of particularly photoreceptors. These range in particular interest in relation to this study. complexity from the simple association of eye spot and basal bodies in certain Protophyta to the MATERIALS AND METHODS extensively modified lamellar systems in rods and cones of mammalian retinas (12). The biological materials which form the basis of Recent studies in electron microscopy have this study represent both birds and mammals. Tissues produced some rather interesting observations on from the small intestine of newly hatched chicks and week-old rats, as well as from organ cultures of centrioles in cells of various embryological origins. developing chick duodenum, formed the principal In mesodermal cells a centriolar derivative materials. Corresponding tissues from the hen and resembling a cilium has occasionally been found. adult rat were also examined. A more cursory exami- Bernhard and de Harven (2) described such an nation was given tissues from the small intestine of incomplete cilium in connective tissue cells of other mammals, including the adult deer mouse chick spleen and mouse ovarian tumor. Mann- (Peromyscus maniculatus gracilis) and the short-tailed weiler and Bernhard (25) wrote of the formation shrew (Blarina brevicauda). In addition, centrioles or of a complete ciliated border in cells of a renal their derivatives were studied in the lungs and kid- tumor. A single ciliary process had been described neys of all these mammals, as well as in the kidneys in epithelial cells of the loop of Henle and collect- of a day-old kitten. The organ cultures, grown for another purpose, ing tubule of the kidney of rabbits by Zimmermann nevertheless provided material suited to this study of (38). With the electron microscope such cilia have centriolar derivatives. The first centimeter of small been seen in all segments of the nephron (24). A intestine in the 13-day developing chick was removed, similar solitary cilium may also protrude from slit longitudinally, and cut into two or more rectangu- cells of endodermal and ectodermal origin. lar pieces, which were then placed on solid nutrient Zimmermann saw this appendage in thyroid medium in culture flasks and incubated at 37.5°C. epithelium of man (38). Munger (28) found The medium contained 20 per cent chicken serum, solitary cilia in differentiating /3-cells of the 0.3 per cent glucose, and 100 units of penicillin G pancreatic islets of the mouse. Palay (29) referred per milliliter, mixed into balanced salt solution and to such cilia in neurosecretory cells of the preoptic solidified with addition of 1.5 per cent agar. The nucleus of the goldfish. To date the most complete cultures were transplanted to fresh medium every 2 days and were fixed for electron microscopy after 9 description of these centriolar derivatives is given days in vitro. Further details of the technique of by Barnes (1) in the hypophysis of the mouse. culture are given elsewhere (32). The method Among unpublished observations by members employed is such that virtually no outgrowth proceeds of the Department of Anatomy at Harvard from the explants. Medical School, several might be mentioned here. Tissues were prepared for electron microscopy by D. W. Fawcett has encountered solitary cilia in essentially routine methods, which included fixation centroacinar cells of the bat's pancreas; E. D. for 1 hour in cold 1 per cent osmium tetroxide Hay, in a rare precartilage or blastema cell from a buffered with barbiturate at pH 7.7, followed by regenerating amphibian limb; S. R. Hiller, in rapid dehydration in graded ethyl alcohols, and embedding in Epon. The thin sections were placed colloid cells of the young chick's thyroid gland; on coated grids and stained with lead plumbite (22), and J. P. Revel, in the glycogen body of the newly using unbuffered solutions, after which they were hatched chick. coated with a carbon film. The sections were ex- This paper reports the normal occurrence of amined and photographed in both RCA EMU 3E 364 THE JOURNAL OF CELL BIOLOGY • VOLUME 15, 196~ and Siemens Elmiskop I electron microscopes, using tend to be longer and thinner than those present accelerating voltages of 50 kv and 60 kv, respectively. in fibroblasts. It is relevant to add that each epithelial cell of OBSERVATIONS both intact and cultured duodenum contains a Cytological Characteristics of Participating pair of centrioles. At the time when cilia are forming in the connective tissues none of the Cells epithelial centrioles are similarly engaged. Light The stages of ciliogenesis about to be described and electron microscopic sections of this material occur most frequently in the mesodermal deriva- reveal an abundance of mitotic figures present in tives while they are actively differentiating. The both connective tissue and adjacent epithelium. duodenal wall of the newly hatched chick or of the The Formation of Cilia week-old rat is well demarcated into the various mucosal and submucosal layers. Fibroblasts are The process of ciliogenesis is similar in all cells basophilic and actively engaged in the production included in this study of avian and mammalian of collagen. Smooth muscle cells contain many material. Although the noun cilium is used freely in myofilaments but lack their full complement. the following account, it is to be understood as Nerve cell processes range widely through the preceded by the silent adjectives rudimentary, muscular layers. Much younger material, although vestigial, or modified. Attention is principally given studied far less thoroughly, provided no evidence the intestinal material; but similar stages of of ciliogenesis in fibroblasts or smooth muscle ciliogenesis are also encountered along the ceils. Adult tissues give evidence of continued nephrons of the mammalian kidneys examined, as ciliogenesis, although end stages are rarely seen.
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