Paper - Studies on the human corpus luteum 2
Embryology - 16 Apr 2024    Expand to Translate
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Adams EC. and Hertig AT. Studies on the human corpus luteum 2. (1969) J Cell Biol. 41(3):716-35. PMID 5768871
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Studies on the Human Corpus Luteum
II. Observations on the Ultrastructure of Luteal Cells during Pregnancy
Adams EC, Hertig AT.
Abstract
The ultrastructure of human corpora lutea obtained during the 6th, 10th, 16th, and 35th week of pregnancy is reported. Differences between the established luteal cell of pregnancy and the transitory luteal cell of the menstrual cycle are noted. In pregnancy the luteal cell is more compartmentalized into a peripheral mass of ER (endoplasmic reticulum) and a central area where mitochondria and Golgi complexes are concentrated. The latter area extends to a cell surface where microvilli face on a perivascular space. Long bundles of filaments are prominent within the luteal cell cytoplasm and, in contiguous cells, appear to arise from adjacent desmosomal regions. Bilateral subsurface cisternae of granular ER at lateral cell borders appear to be areas of specialized junctional surfaces. Certain luteal cells with irregular nuclear membranes are also characterized by vesicular aggregates enclosed within a single membrane. These aggregates are found within the peripheral nucleoplasm or the perinuclear cytoplasm. Their single limiting membrane often appears continuous with either the inner or outer leaflet of the nuclear membrane.
Introduction
In contrast to our preceding paper on the development and regression of luteal cells in the transitory corpus luteum of the menstrual cycle (1), this study examines these same steroidogenic cells after they have become established as the corpus luteum of pregnancy. Within a few weeks (not precisely determined) after the implantation of the fertilized ovum, the corpus luteum is no longer essential to the maintenance of pregnancy. Nevertheless the present ultrastructural study of the relationship of organelles in luteal cells from the sixth through the 35th week of pregnancy indicates that massive regression in this tissue in the later months of pregnancy does not take place. Green et al. (7) likewise concluded in their electron microscopic study that luteal cells from term pregnancies could be capable of secretion. In a study of the incorporation of acetate—l—“C into progesterone in corpora lutea from the luteal phase of the cycle and from the eighth and 40th weeks of pregnancy, Savard et al. (16) reported high rates of incorporation in specimens from pregnant patients and in those from patients at days 15-21 of the menstrual cycle. They further reported that the specimens from pregnant patients form less progesterone in vitro in terms of micrograms of steroid than do cyclic corpora lutea. They conclude that the corpus luteum undergoes profound metabolic changes throughout its lifespan.
Materials and Methods
Five corpora lutea from human pregnancies have been studied (Table I) by the same methods of TABLEI Clinical Age of the Fine Human Corpora Luisa of Pregnancy Used in This Study Case no. Stage of Pregnancy in weeks H51 6 H49 10 H42 16 HB 16 H43 35 (Caesarean section) preparations reported in the preceding paper on cyclic human luteal cells (1).
Observations
Throughout pregnancy the predominant type of. luteal cell is very irregularly shaped and large lobules of its peripheral cytoplasm are closely enveloped by adjacent cells (Fig. 1). Extensive portions of the extremely peripheral cytoplasm are filled with tubular endoplasmic reticulum (ER), a few small, very osmiophilic lipid droplets, small vesicles containing a flocculent electron-opaque material, and only sparsely distributed mitochondria (Fig. 3). As pregnancy progresses, the relative volume of this type of cytoplasm in each cell appears to decrease somewhat. In what may be optimal planes of section these peripheral areas of the cytoplasm appear to be connected to the more central cytoplasm by parallel arrays o’ cisternae of granular ER. The central cytoplasm contains a concentration of mitochondria and Golgi complexes both of which are surrounded by tubular ER that is closely associated with mitochondria (Fig. 3). The central cytoplasm containing multiple Golgi complexes, membrane—bounded dense bodies, mitochondria, and agranular ER extends to a cell surface whose microvilli face on a perivascular space (Figs. 1 and 2). Closely adjoining cells which lie in the perivascular channel and appear to be phagocytic (Fig. 2) become more prominent as pregnancy progresses. In a corpus luteum from the 35th week of pregnancy, some of these phagocytic cells contain large electron-opaque deposits of crystalline material which may represent calcium.
The Golgi complex of these luteal cells is a crescentic, glomerulus—shaped structure with many small vesicles in the matrix between the saccules (Fig. 4) . As pregnancy approaches term the saccules become interdigitated and show elaborate crescentic configurations associated with a variety of vesicles (Fig. 5). Frequently, a granular sphere surrounded by a halo of small vesicles lies near the Golgi complex (Fig. 4). Homogeneous dense bodies and other dense bodies of irregular shape and containing vesicles of a variety of sizes are prominently associated with the Golgi complex (Fig. 33) and accumulate in the cytoplasm near perivascular spaces. The structure of the vesicular dense bodies differs from that of the vesicular granules in the active cyclic luteal cell by the presence of a homogeneous electron—opaque matrix and by the absence of a halo of surrounding small, uniform vesicles (1) (Fig. 6). In addition, the granule—containing cytoplasmic projections or blebs that are so prominent in the intercellular spaces or attached to the surface of developing cyclic luteal cells are not observed in pregnancy.
Mitochondria are, for the most part, elongate with both tubular and lamellar cristae (Fig. 3). (Many mitochondrial cristae in the term corpus luteum seem to be more lamellar than tubular.) Other mitochondria within any one cell are irregular in shape, while still others contain large, spherical, amorphous electron—opaque deposits (Fig. 15). Some cells contain many mitochondria with these deposits or with cristae of unusual contours (Fig. 7).
The electron-opacity of adjoining cells differs (Fig. 15), as may that of the cytoplasm of various areas within any one cell (Fig. 1). This variation appears to be related to the dilation and /or close-packing of the tubular ER as well as to the density of the cytoplasmic matrix. Folded membrane complexes (Fig. 13) and a few spherical inclusions similar to those described in the cyclic luteal cell (1) are present in the peripheral cytoplasm. Peripheral whorled membranes that oiten enclose a large lipid droplet become prominent in a few cells toward term (Fig. 9).
Extensive bundles of intracytoplasmic filaments, some of which are associated with dense regions (Fig. 13), are present in the 6-week corpus luteum and become more prominent as pregnancy progresses. In many instances they appear to form a network that compartmentalizes the cell into a peripheral mass of agranular and granular ER and a central mass of mitochondria, agranular ER, and Golgi complexes (Fig. 10). These long bundles of filaments may traverse the entire cell cytoplasm, and in contiguous cells may arise from adjacent desmosomal regions (Fig. 12). Other filamentous Hyalin (colloid) bodies, histologically character- istic of luteal cells of pregnancy, and/or large vacuoles are seen within occasional cells. The hyalin bodies contain an electron—opaque homogeneous material with occasional needle—like crystals (Fig. 8) or vesicular structures. The apparently intracellular vacuoles, often large enough to distort the entire luteal cell, are lined by attenuated microvilli and contain an electron- translucent material.
Where luteal cells are closely adj oined, segments of their cell membranes often are bilaterally associated with subsurface cisternae of granular ER (Fig. 3). These cisternae have ribosomes only on the membrane at the cytoplasmic side (Fig. 14). The other membrane which is agranular is separated by only 60-70 A from the cell surface. Adjoining luteal cells also have agranular ER in close apposition to the cell surface facing a narrow intercellular space (Fig. 16). Elsewhere along such narrow spaces, which apparently are freely continuous with the perivascular spaces (Fig. 15), there are patches of microvilli (Fig. 18). These microvilli often surround an intercellular space or channel containing vesicular or foamy material (Figs. 19 and 20). In early pregnancy, these lateral margins form deep, narrow folds into the luteal cell cytoplasm which terminate in microvilli situated near a paranuclear Golgi complex with associated vesicular dense bodies (Fig. 17). Within the intercellular space surrounded by these microvilli, granular and vesicular material also can often be seen.
Another type of luteal cell present in all stages of pregnancy is characterized by an irregular nuclear membrane, ER that is usually vesicular, and variable forms of mitochondria (Figs. 2l~23). This cell is also distinguished by the presence within the nucleus or the perinuclear cytoplasm of multiple aggregates of vesicles enclosed within a single smooth membrane (Figs. 21 and 24). Such vesicular aggregates were never seen within similar cells in active corpora lutea of the menstrual cycle (1) but are prominent in most cells of this type during pregnancy. Small vesicles are often present either singly or in aggregates within the perinuclear space. These vesicles are similar in size to those clustered within a single smooth membrane either apparently free in the peripheral nucleo-plasm or attached to the inner leaflet of the nuclear membrane. Many cells with nuclear vesicular aggregates also have similar structures either in the convoluted perinuclear cytoplasm or attached to the outer leaflet of the nuclear membrane (F ig. 24). In some instances these single membrane« bounded vesicular aggregates resemble structures associated with nearby Golgi complexes, but many others within the same section do not appear to be related to Golgi areas (Fig. 24). In some of the more electron—opaque cells with nuclear vesicular aggregates, vesicular ER that is sparsely granular and that contains an inner small vesicle can be seen to be in continuity with the outer leaflet of the nuclear membrane (Fig. 25). Many nuclei of this type of luteal cell contain one or more spheroidal bodies, in addition to the nuclear or perinuclear vesicular aggregates (Figs. 24 and 29). Occasional spheroidal bodies have a large granular core and a halo of granular or fibrillar material (Fig. 30), whereas others are formed of irregular concentric rings of granular or fibrillar material (Figs. 29, 31, and 32). Only very rarely are such structured nuclear bodies seen in the more prevalent type of luteal cell containing a spherical nucleus and tubular ER (Fig. 31).
FIGURE 1 A survey View of a luteal cell from the sixth week of pregnancy. Note peripheral cytoplasmic masses of agranular ER, parallel cisternae of granular ER, and a large central area where mitochondria and Golgi complexes are concentrated. This area extends to a cell surface containing microvilli that face a vascular space. H51. X 3800.
FIGURE 2 A luteal cell surface at a vascular channel from a 16-week pregnancy. Phagocytes become closely apposed to the luteal mierovilli and accumulate electron-opaque deposits. A collapsed vascular channel is present at right. H42. X 10,000. FIGURE 3 A higher magnification of the peripheral cytoplasm of the luteal cell seen in Fig. 1. Note subsurface cisternae of granular ER at lower left, peripheral mass of agranular ER whose membranes are often in continuity with granular ER, and, at top, the more central agranular ER that is closely associated with mitochondria. H51. X 22,000. bundles terminate in microvilli, either at the cell surface (Fig. ll) or in those surfaces seen near the nucleus at the terminal end of a deep fold of the lateral cell membrane. The bundles of filaments usually are surrounded by an organelle——free, fibrillar matrix which merges with the matrix throughout the cytoplasm.
FIGURE 4 A crescentic Golgi complex from a 16-week pregnancy. Note the small Vesicles between Golgi saccules and the associated two granular spheres at top. H42. X 22,000.
FIGURE 5 A portion of an elaborate Golgi complex from a 35-week pregnancy. Note interdigitation of expanded Golgi saccules and the variety of associated vesicles. H43. X 22,000.
FIGURE 6 Dense bodies containing vesicles of a variety of sizes from a 6-week pregnancy. H5l. X 34,000.
FIGURE 7 A few luteal cells contain clustered mitochondria with electron-opaque deposits in their matrix and short or distorted cristae. From a 10-week pregnancy. H49. X 22,000.
FIGURE 8 A hyalin (colloid) body in a luteal cell from a 16-week pregnancy. Note needle-like crystals within the homogeneous, electron-opaque material. Some smaller hyalin bodies such as this one are surrounded by granular ER, but other larger ones are not. H42. X 28,000.
FIGURE 9 A whorled membranous structure in the peripheral cytoplasm of a 35-week pregnancy. H43. X 22,000.
Clumps of the luteal cells with irregular nuclear membranes can be seen along the larger vascular channels and in the basal layer of the corpus luteum. Other such luteal cells are seen singly and surrounded by luteal cells of the more prevalent type. Toward term they form a plaque along vascular channels where they are associated with large extracellular vacuoles, luteal debris, and red blood cells (Fig. 23). Some of these luteal cells are very electron—opaque with clumped, apparently pycnotic nuclear elements, a dense cytoplasmic matrix, and mitochondria of various sizes and shapes (Fig. 22). Their projections ap— pear to engulf and /or invade the peripheral cytoplasm of neighboring luteal cells whose tubular ER is often in close apposition to the cell membrane (Figs. 22 and 28). Other cells with nuclear vesicular aggregates have mitochondria and vesicular ER dispersed in a cytoplasmic matrix that is no more electron—opaque than that of neighboring cells (Figs. 21 and 33). Granular ER which is often dilated to form vacuolar structures and which is associated with clumps of ribosomes in the surrounding matrix is prominent in the peripheral cytoplasm (Fig. 27). Where the surface membrane of these cells borders a perivascular space, it often appears incomplete or indistinct and vesicles appear to be liberated into the extracellular space (Fig. 26).
A thecal layer is prominent in our specimens obtained during the first half of pregnancy but was not observed in the 35-week specimen. Cells in the thecal layer can be distinguished by their smaller size, their cuboidal shape, their closely apposed straight membranes, and their greater electron—opacity. Their cytoplasm contains closely packed agranular ER, a few peripheral parallel arrays of granular ER, elongate mitochondria with both tubular and lamellar cristae, and conspicuous dense bodies (Fig. 34). Lipid droplets are not present in any thecal cell we observed.
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Cite this page: Hill, M.A. (2024, April 16) Embryology Paper - Studies on the human corpus luteum 2. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Studies_on_the_human_corpus_luteum_2
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