Stages of Development of the Ribosome-Lamella Complex: An Ultrastructural Study

Ribosome-lamella complexes (RLC) are intracytoplasmic organelles observed in a wide variety of disorders, but mostly in hematologic malignancies. Although their close topographic relationship with rough endoplasmic reticulum (RER) suggests their derivation from it, their development and functional role are unclear. Their maturation phases were studied in 20 cases (19 hematologic neoplasms and 1 parathyroid adenoma) where electron microscopy had evidenced their presence. In 19 of these cases, RLC were in an advanced stage of maturation, whereas in one (acute monoblastic leukemia) they were observed in the early stages of development and appeared to arise from peculiar RER configurations within blast cells, which were rich in both organelles. In this case, the authors observed numerous RER cisternae with distinctive cylindric, concentric and/or whorl configurations, RLC associated and not associated with these configurations, and intermediate structures. The latter were characterized by lamellae devoid of ribosomes oriented parallel to the RER configurations. Reticulum configurations were observed in no other case. The ultrastructural aspects observed in these 20 cases suggest that RLC synthesis proceeds as follows: (1) arrangement of RER in cylindric configurations; (2) synthesis of lamellae oriented parallel to the cylindric configurations (pre-RLC); (3) formation of RLC when ribosomes appear between the lamellae associated with configurations (immature RLC); (4) formation of mature RLC with disappearance of the reticulum.     

Stages of Development of the Ribosome—Lamella Complex: An Ultrastructural Study

Ribosome-lamella complexes (RLC) are intracytoplasmic organelles observed in a wide variety of disorders, but mostly in hematologic malignancies. Although their close topographic relationship with rough endoplasmic reticulum (RER) suggests their derivation from it, their development and functional role are unclear. Their maturation phases were studied in 20 cases (19 hematologic neoplasms and 1 parathyroid adenoma) where electron microscopy had evidenced their presence. In 19 of these cases, RLC were in an advanced stage of maturation, whereas in one (acute monoblastic leukemia) they were observed in the early stages of development and appeared to arise from peculiar RER configurations within blast cells, which were rich in both organelles. In this case, the authors observed numerous RER cisternae with distinctive cylindric, concentric and/or whorl configurations, RLC associated and not associated with these configurations, and intermediate structures. The latter were characterized by lamellae devoid of ribosomes oriented parallel to the RER configurations. Reticulum configurations were observed in no other case. The ultrastructural aspects observed in these 20 cases suggest that RLC synthesis proceeds as follows: (1) arrangement of RER in cylindric configurations; (2) synthesis of lamellae oriented parallel to the cylindric configurations (pre-RLC); (3) formation of RLC when ribosomes appear between the lamellae associated with configurations (immature RLC); (4) formation of mature RLC with disappearance of the reticulum.     

Ribosome-lamella complexes observed in an Epstein-Barr virus-producing B-cell line, infected with human T-lymphotropic virus type I

Co-cultivation of peripheral blood mononuclear cells, from a 4-year-old boy with infectious mononucleosis, with a human T lymphotrophic virus type I (HTLV-I)-producing T-cell line resulted in the establishment of an HTLV-I infected Epstein-Barr virus (EBV)-producing B-cell line. Ultrastructural examination revealed the presence of ribosome-lamella complexes (RLCs), in a small proportion of long-term cultured cells. Evidence is presented of continuity between RLC and the rough endoplasmic reticulum, and in some instances there was also an intimate relationship with tubuloreticular structures. The findings support the view that RLC is derived from the rough endoplasmic reticulum and also provide further evidence of the non-specific nature of RLC in relation to cell type.     

Retroperitoneal Lymphoma with Ribosome-Lamellae Complexes, Cytoplasmic Projections, and Desmosome-like Junctions: An Ultrastructural Study

The ultrastructural finding of ribosome-lamellae complexes (RLC) in 15% of tumor cells in an unusual retroperitoneal lymphoma is reported. Tumor cells had numerous nuclear pockets, cytoplasmic projections, and, not infrequently, desmosomelike attachments. RLC were similar to those previously described in patients with hairy cell leukemia and less often in other leukemia types, with the basic configuration of a hollow cylinder. An intimate association with the rough endoplasmic reticulum was evident. A review of the literature disclosed only one other reported lymphoma with similar structures.     

HBsAg-induced hypertrophic smooth endoplasmic reticulum as a target for liver-kidney microsomal (LKM) antibodies.

To test the hypothesis that LKM antibodies are directed against antigen(s) of the smooth endoplasmic reticulum, liver biopsies from patients with HBsAg chronic hepatitis, rich in liver cells with HBsAg-induced hypertrophic SER, were used. A close correspondence was seen between cells with HBsAg-positive cytoplasm by immunoperoxidase and cells with a stronger and more homogeneous fluorescence by indirect immunofluorescence with LKM-positive sera. These results point to antigenic components of SER as reacting with LKM antibodies. The relevance of antigens present in the ribosomes and membranes of rough endoplasmic reticulum needs further evaluation.     

Fine structure of satellite cells in growing skeletal muscle

The morphology of satellite cells was investigated in skeletal muscle from mice of various ages between 7 days and 50 weeks. Satellite cells of very young muscle had abundant cytoplasm which was rich in organelles. Free ribosomes were abundant and usually arranged into polysomes of 5–6 units. Cisternae of rough endoplasmic reticulum were heavily studded with ribosomes and occupied the polar regions of the cytoplasm. Marked dilations of the cisternae, filled with an amorphous electron-lucent material, were a frequent and characteristic feature of satellite cells of very young muscle. The cytoplasm of young cells also contained a well developed Golgi apparatus as well as numerous mitochondria, microfilaments and microtubules. With increasing age there was a rapid reduction in organelles both qualitatively and quantitatively. For example, as the number of ribosomes decreased, their organization into polysomes was lost. The rough endoplasmic reticulum was present in cells of older muscle merely as small isolated rofiles that lacked dilations. These and other features demonstrated during this study are consistent with the concept that satellite cells are metabolically very activie in young muscle but rapidly become quiescent as the animal grows older.     

Structure of taste buds in foliate papillae of the rhesus monkey,Macaca mulatta

Taste buds in foliate papillae of the rhesus monkey were examined by electron microscopy. Three distinct cell types were identified. Type I cells were narrow elongated cells containing an oval nucleus, bundles of intermediate filaments, several Golgi bodies, and characteristic apical membrane-bounded dense granules. These cells exhibited morphological variations: some had a moderately dense cytoplasm, perinuclear free ribosomes, and flattened sacs of rough endoplasmic reticulum; others had a more lucent cytoplasm, dilated irregular rough endoplasmic reticulum, lysosome-like dense bodies, and lipid droplets. Type II cells typically contained a spherical, pale nucleus, a prominent nucleolus, supranuclear and infranuclear Golgi bodies, mitochondria with tubular cristae, and one or two centrioles. This cell type, too, showed some variation in the relative amounts of ribosomes and smooth endoplasmic reticulum, which varied inversely with each other. Type III cells were characterized by a clear apical cytoplasm essentially devoid of ribosomes and containing microtubules. In a few type III cells, the peri- and infranuclear regions contained many ribosomes and some rough endoplasmic reticulum. In most Type III cells, there were large numbers of dense and clear vesicles in the peri- and infranuclear regions; some of the vesicles were grouped in synapse-like arrangements with adjacent nerves. The morphological variations exhibited by all three cell types could be accounted for by age differences in each of the cells. This would be consistent with the notion that cell renewal occurs in each of the three cell populations.     

Ultrastructure of the normal adult human female prostate gland (Skene’s gland)

The predominant cells of female prostatic glands lining their lumen were found to be tall cylindrical secretory cells with short stubby microvilli, protuberances of the apical cytoplasm, and with bleb formation. Abundant secretory vacuoles and granules, rough endoplasmic reticulum, developed Golgi complexes and numerous mitochondria are characteristic of their active secretory configuration with apocrine (apical blebs) and merocrine (secretory vacuoles and granules) type of secretion. Basal (reserve) cells were seen to be located between the secretory (luminal) cells and the basement membrane. Their ground cytoplasm is dense with rough endoplasmic reticulum and mitochondria. Their nuclei, unlike those of secretory cells, possess more peripheral condensed chromatin, denser dispersed chromatin and sporadic nucleoli. Besides the two basic types of mature prostatic cells intermediary cells were also seen, located between the basal and secretory cells or in their close vicinity. Their cytoplasm exhibits numerous profiles of rough endoplasmic reticulum and free ribosomes. Secretory vacuoles and granules were mostly practically absent (type 1 intermediary cells) so that they resembled basal (reserve) cells. In some of them, however, as in secretory cells, such secretory elements do gradually appear (type 2 intermediary cells). The finding of intermediary cells in the lining of prostatic glands supports the role of basal (reserve) cells in the renewal of cells in glands of the female prostate. The first ultrastructural analysis of the normal female prostate performed by transmission electron microscopy showed that, as in the postpubertal male, the prostatic glands in the adult female display mature secretory and basal cells. The results of the presented study further corroborate the contemporary concept of the female prostate as a functional genitourinary organ.     

Ultrastructure of the normal adult human female prostate gland (Skene's gland)

The predominant cells of female prostatic glands lining their lumen were found to be tall cylindrical secretory cells with short stubby microvilli, protuberances of the apical cytoplasm, and with bleb formation. Abundant secretory vacuoles and granules, rough endoplasmic reticulum, developed Golgi complexes and numerous mitochondria are characteristic of their active secretory configuration with apocrine (apical blebs) and merocrine (secretory vacuoles and granules) type of secretion. Basal (reserve) cells were seen to be located between the secretory (luminal) cells and the basement membrane. Their ground cytoplasm is dense with rough endoplasmic reticulum and mitochondria. Their nuclei, unlike those of secretory cells, possess more peripheral condensed chromatin, denser dispersed chromatin and sporadic nucleoli. Besides the two basic types of mature prostatic cells intermediary cells were also seen, located between the basal and secretory cells or in their close vicinity. Their cytoplasm exhibits numerous profiles of rough endoplasmic reticulum and free ribosomes. Secretory vacuoles and granules were mostly practically absent (type 1 intermediary cells) so that they resembled basal (reserve) cells. In some of them, however, as in secretory cells, such secretory elements do gradually appear (type 2 intermediary cells). The finding of intermediary cells in the lining of prostatic glands supports the role of basal (reserve) cells in the renewal of cells in glands of the female prostate. The first ultrastructural analysis of the normal female prostate performed by transmission electron microscopy showed that, as in the postpubertal male, the prostatic glands in the adult female display mature secretory and basal cells. The results of the presented study further corroborate the contemporary concept of the female prostate as a functional genitourinary organ.     

Optical and ultrastructural studies of midgut and salivary glands of first instar of Dermatobia hominis (Diptera: Oestridae)

Midguts and salivary glands of newly hatched larvae (L1) of Dermatobia hominis (L., Jr.) were studied using light and electron microscopy. The larval midgut has a tubular, sinusoidal form and consists of a monolayer of epithelial cells with an underlying basement membrane and a surrounding layer of connective tissue. The fine structure of the midgut shows digestive cells with short microvilli, large nuclei, and cytoplasm containing few visible organelles (mitochondria, rough endoplasmic reticulum, and free ribosomes). In the basal region, the plasma membrane of the cells is folded into a labyrinth area. Hemidesmosomes link the basal surface to the basement membrane and septet junctions are present between adjacent cells. The connective tissue circling the basement membrane contains collagen fibrils, muscle fibers, and tracheal tubes. Prominent nuclei with evident nucleoli occur in the digestive cells. The salivary gland is simple and tubular. It has a monolayer of epithelial cells surrounded by basement membrane and connective tissue. The fine structure of the salivary gland shows epithelial cells, microvilli, secretion into the lumen, septate junctions at the lateral face and a basal labyrinth region. The cell nucleus is large and the cytoplasm contains rough endoplasmic reticulum, ribosomes and mitochondria.     

Rumpshaker mouse: A new X-linked mutation affecting myelination: Evidence for a defect in PLP expression

Summary This report describes a new X-linked mutation in mice, named rumpshaker (rsh) which is associated with hypomyelination of the central nervous system. Myelination commences appropriately but the majority of sheaths fail to develop normally. Oligodendrocytes are increased in number and have prominent Golgi apparatus, rough endoplasmic reticulum and free ribosomes. Occasional cisternae of rough endoplasmic reticulum are distended. Some dense lamellar inclusions occur in Oligodendrocytes but overall, degenerative changes and cell death are uncommon. Immunostaining demonstrates a major defect in expression of PLP/DM-20. Using site-specific antisera directed at different portions of the PLP/DM-20 molecule, the major defect appears to be with PLP where virtually no myelin sheaths are positive. Antiserum against the C-terminal common to PLP and DM-20 shows reduced but definite myelin staining. Genetic analysis indicates a locus at or close to the PLP/jimpy (jp) locus. The rsh mutation, however, differs fromjp in that affected mice have normal longevity, can breed, produce substantially more myelin and have increased numbers of Oligodendrocytes.     

Microtubular aggregates within rough endoplasmic reticulum in myxopapillary ependymoma of the filum terminale

Aggregates of microtubules with-in rough endoplasmic reticulum were found in many neoplastic cells of three cases of myxopapillary ependymoma of the filum terminale studied ultrastructurally. The cytoplasm and cellular processes of some neoplastic cells were distended by the aggregates. In general the involved rough endoplasmic reticulum contained three to six microtubules, but some enclosed more than 10 microtubules. The enclosed microtubules were straight parallel hollow cylindrical structures with fuzzy coats. They had an inner diameter of 12 to 15 nm, an outer diameter of 30 to 35 nm, and a center-to-center distance of 50 to 62 nm. The involved rough endoplasmic reticulum often showed various degrees of loss of surface ribosomes and some appeared totally degranulated. Vacuolar degeneration of involved rough endoplasmic reticulum with fragmentation and disintegration of the enclosed microtubules was frequent. Direct relationship of the enclosed microtubules to the cytoplasmic microtubules and ciliary formation was not found. This unusual microtubular aggregate has not been described in other types of ependymoma, or in other brain tumors. They may represent a characteristic ultrastructural feature of myxopapillary ependymoma.     

Fine structure of a diffuse undifferentiated small-cell carcinoma of the thyroid

Differentiating diffuse undifferentiated small-cell carcinoma of the thyroid from malignant lymphoma is difficult. A case of small-cell carcinoma was studied by electron microscopy and is reported here to illustrate the value of electron microscopy in separating epithelial thyroid tumor from lymphoma. Ultrastructurally, the tumor was composed of cells possessing occasional intercellularjunctional complexes and spaces with microvilli. There were abundant free ribosomes and well-developed rough endoplasmic reticulum in the cytoplasm. Golgi apparatus, smooth endoplasmic reticulum, membrane-bound cytosomes, and centrioles were also evident. Numerous swollen mitochondria were seen in some tumor cells. A few large tumor cells characterized by abundant cytoplasm containing few mitochondria, endoplasmic reticulum and numerous microfibrils were also observed. A few collagen fibers, lymphocytes and plasma cells were present among tumor cells. No basement membranes nor virus-like particles were seen.     

Ultrastructure of mouse egg-cylinder

Summary The mouse egg-cylinder prior to and after mesoderm formation was studied by means of electron microscopy. The ultrastructural appearance of the proximal entoderm of both embryonic and extraembryonic segments suggests an intensive absorptive and nutritional activity. Numerous pinocytotic vacuoles, microvilli, primary and secondary lysosomes and fair amounts of rough endoplasmic reticulum and free ribosomes were the most important characteristics of these cells. After mesoderm formation, the extraembryonic entoderm showed the aforementioned characteristics even more prominently, while the cells of embryonic entoderm became flattened and depleted of microvilli and of almost all organelles. The cells of the extraembryonic and embryonic ectoderm prior to and after mesoderm formation had the same ultrastructural appearance as mesodermal cells. The cytoplasm of these cells was replete with free ribosomes, but other organelles such as mitochondria and rough endoplasmic reticulum were few in number. The architecture of all cells of the egg-cylinder except those of the extraembryonic entoderm suggested a very low level of differentiation. The criteria and possibilities for the determination of the degree of differentiation on the ultrastructural level and possible differences in protein synthesis in extraembryonic entoderm as compared with other parts of the embryo are considered.     

Ultrastructural Study of a Clear Cell Chondrosarcoma

A lesion in the left humeral head of a 15-year-old Japanese boy was light-microscopically diagnosed as clear cell chondrosarcoma. Fresh tissues from the lesion were studied ultrastructurally. In most tumor cells, that is, clear cells, paucity of organelles, sparse free ribosomes, and low protein content in cytosol were most striking. Tumor cells had many microvilli characteristic of cartilage cells. Among scanty organelles, vesicles or cisternae of dilated rough endoplasmic reticulum were rather conspicuous, and well-developed Golgi complexes were sparse. Intercellular matrix was scanty. These results suggest that intercellular matrix substance may be synthesized substantially by rough endoplasmic reticulum, whereas the synthesized substance perhaps cannot be transported smoothly into extracellular spaces because of scanty well-developed Golgi complexes.     

Fine structure of the venom gland epithelium of the south american rattlesnake and radioautographic studies of protein formation by the secretory cells

The South American rattlesnake venom gland is made up of secretory tubules lined by a simple columnar epithelium containing horizontal cells, mitochondria-rich cells, and the principal cell type, the columnar secretory cells. This cell has a round basal nucleus and abundant rough endoplasmic reticulum, the cisternae of which are variably distended with flocculent material containing many dense intracisternal granules. The supranuclear Golgi apparatus is spherical, with stacks of flattened saccules at the periphery and large vacuoles containing masses of dense material, and other dense granules in the center. Similar but smaller granules are present at the apex where they fuse with the microvillus-covered apical membrane and release their content into the lumen. Protein synthesis was studied in snakes injected with ³H-tyrosine and sacrificed at several times after injection. Radioautographs showed reactions at one half and one hour over the ribosomes and membranes of the rough endoplasmic reticulum. At two hours the immature face of the Golgi apparatus was labeled. At four hours Golgi saccules and vacuoles with dense masses (secretory granules) were labeled, and at eight hours the dense masses within the secretory granules were heavily labeled both in the Golgi region and in the apex near the lumen. Labeled material was found in the lumen at two days. Intracisternal granules were first labeled at eight hours, and by two days reactions remained only over the flocculent content and intracisternal granules of the rough endoplasmic reticulum. Thus, venom protein was synthesized on the rough endoplasmic reticulum, migrated through the Golgi apparatus and accumulated in the dense masses of the secretory granules, which moved to the apex and were extruded. The labeling of intracisternal granules at eight hours and two days after injection indicated a storage nature for these granules.     

Visualization of polyribosomes in the postsynaptic area of the squid giant synapse by electron spectroscopic imaging

Summary Giant axons from squids (Loligo vulgaris andLoligo pealii) were studied by conventional electron microscopy and by electron spectroscopic imaging: electrons with a characteristic energy loss due to interaction with phosphorus atoms were used to image phosphorus-rich elements such as ribosomes. Patches of granular material were seen in the proximal region of giant axons, especially in the postsynaptic area of the giant synapse, but not on the presynaptic side. They were rare or absent in the more distal part of the axon. With electron spectroscopic imaging the patches emitted strong phosphorus signals, indistinguishable from signals of ribosomes in neuronal perikarya, confirming their identification as RNA-rich elements. In the part of the axon near the perikarya in the giant fibre lobe, the patches consisted of sacs of rough endoplasmic reticulum. It is suggested that patches of rough endoplasmic reticulum are transported to the synaptic region where ribosomes detach from the cisterns and aggregate into polyribosomes.     

Ultrastructure of rat liver cells after exhausting physical training

In rats, running of the maximum intensity caused death of some hepatocytes, an increase in the number of phagosomes in Kuppfer cells, and the emergence of connective tissue fibers in the space of Disse. Ultrastructural investigation of hepatocytes showed delayed release of bile products into bile capillaries, decrease in glycogen content, increase in the number of mitochondria (many of them were divided by the cristae), and irregular distribution of ribosomes in the rough endoplasmic reticulum. Accumulation of erythrocytes in the sinusoids, fragments of dead hepatocytes, Kuppfer cells with numerous phagosomes, and connective tissue fibers in the space of Disse were observed in rat liver after exhausting swimming. Study of hepatocyte ultrastructure revealed intense protein synthesis (as evidenced by increased number of ribosomes and unchanged mitochondria and cisternae of the rough endoplasmic reticulum), separation of cytoplasmic fragments with ribosomes into sinusoids, absence of glycogen, and lipid accumulation. Translated fromByulleten' Eksperimental'noi Biologii i Meditsiny, Vol. 126, No. 7, pp. 101–104, July, 1998     

Quantitative changes in the morphology of the aging canine prostate

Stereological methods at the light and electron microscopic levels were used to examine the morphological changes in the beagle prostate associated with increasing age and with the occurrence of spontaneous benign hyperplasia. Analyses of semithin sections of tissue embedded in plastic revealed that proliferation of prostatic glandular and stromal components, increase in epithelial cell numbers, and increase in epithelial cell size all contributed to the dramatic increase in prostate weight seen in aging dogs. Analyses at the electron microscopic level revealed that the volume densities of rough endoplasmic reticulum and secretion granules were significantly lower in epithelial cells of the immature prostate than in the prostate of mature dogs (greater than 1.5 years of age). In contrast, no significant differences were seen in the volume densities of rough endoplasmic reticulum, free ribosomes, secretion granules, smooth endoplasmic reticulum, or mitochondria in randomly selected prostatic epithelial cells of dogs 1.5 to 9 years of age, whether or not the prostates were hyperplastic.     

An electron microscopic study of uterine arteries during pregnancy

The mesometrial arteries of pregnant guinea pigs are not mere blood conducting channels. Instead they are dynamic in nature. The cells forming the intima and media exhibited significant structural modifications during pregnancy. The endothelial cells became hypertrophied and attenuated. Their cytoplasm showed an increase in the amount of ribosomes, rough endoplasmic reticulum and lysosome-like bodies during pregnancy. Dense bodies that were often closely associated with the Golgi apparatus were seen in pregnant animals. These bodies exhibited a graduation in size within each cell and were thought to be the precursors of the lysosome-like bodies. Similar structures were also seen in smooth muscle cells of the mesometrial arteries of pregnant animals. The endothelium of these arteries was often discontinuous in full term pregnant animals. In that case, the underlying smooth muscl4 cells provided the lining surface. Irrespective of which type of cells formed the lumen of these arteries, they became coated with a “fuzzy” layer which specifically stained intensely with phosphotungstic acid, suggesting that this layer might be a mucoprotein. The smooth muscle cell of the arterial media also became hypertrophied during pregnancy. The cytoplasm exhibited a gradual increase in free ribosomes and rough endoplasmic reticulum, mitochondria and microtubules throughout pregnancy. During the latter half of pregnancy many smooth muscle cells developed extensive amounts of smooth endoplasmic reticulum whose vesicles often were filled with an electron opaque secretory material. It is suggested that the development of unusually large quantities of smooth endoplasmic reticulum might be associated with steroid metabolism. Unusually thick basement membranes were formed around the modified smooth muscle cells of full term pregnant animals and the surfaces of these cells often exhibited large numbers of microvilli. The microvilli seemed to disrupt the continuous patterns of the basement membrane.