0.

(Department of Histology, Karolinaka Institutet; and the Radiumlzemmei, Stockholm, Sweden)

SUMMARY

The cancer cells were arranged in membranes or formed globelike groups. The shapeof the cells varied from columnar to squamous. The apical cell surface was irregular orpossessed microvilli, but no correlation of this appearance to some consistent featureof the cytoplasm was observed. The basal cell surface of some squamous cells madedeep projections into the connective tissue. This was interpreted as a sign of reducedcontact inhibition. Sometimes a row of cancer cells lacked the basement membrane.These cells had a zone of ground substance, with a high density at the basal cell sunface. The A cells of the adenocarcinomas contained both an increased number of freeribonucleoprotein particles and a cytoplasmic ground substance of higher density thanthe B cells.

The cell organelles had mainly a normal ultrastructure but varied in number. However, some mitochondria were large and contained fewer cnistae than normal. Severaltypes of cell inclusion were observed. No cellular component on virus-like particle thatmight be specific for this type of cancer cell was observed.

The interphasic cancer cells of the glandularepitheium in the uterine body of man have avarying structure as seen under the light microscope. In general, the cell is characterized by alarge, irregular nucleus with hypentrophic nucleoliand a cytoplasm showing signs of dedifferentiation.With regard to the amount of nucleic acid, it issometimes possible to classify the cancer cellsinto type A and type B cells (4).

A further knowledge of several of the cellular

components in the cancer cell requires the higherresolution of the electron microscope. Results ofelectron microscopy of the normal endometniumhave been published by several authors (1—3,5—7,9—12, 15—21), but the reports on the endometnial

carcinoma still are few (16, 17). The present paperwill add some information on the ultrastructuneof the different types of cancer cell which areobserved in adenocarcinomas of the uterine body.

MATERIALS AND METHODS

The specimens of the endometnial carcinomaswere obtained during diagnostic curettage fromfour women, one being in the late secretory phaseof the menstrual cycle and three in the menopause.

For electron microscopy a small piece of the

S This work was supported by a grant from “Riksforeningen

mot cancer,― Stockholm, Sweden.

mucosa of the uterine wall was removed with abiopsy curette and immediately placed in a buffened 1 per cent solution of osmium tetnoxide.After dehydration in ethyl alcohol, the specimenswere embedded in butyl methacrylate. The seetions were made on an ultramicrotome designedby Sjöstrand and examined in an RCA EMU-2Cmicroscope.

RESULTSLight microscopy.—Light microscopy revealed

adenocarcinoma of high or moderate differentiation in all the cases.

Electron microscopy.—The epithelial cells of theadenocarcinoma in the uterus varied from tallcolumnar cells to low squamous cells. Sometimesthe cancer cells did not form epithelial membranesbut were arranged in globelike groups. These cellswere polygonal. Some cancer cells showed a higherelectron density than did the surrounding cells(Figs. 1, 6). The higher density of the cytoplasmwas caused by an increased number of free-lyingnibonucleoprotein (RNP) particles and by a higherdensity of the ground substance of the cell.

The apical cell surface in the epithelial membranes either had an irregular course (Fig. 8)on was specialized into microvilli (Figs. 1, 2, 4, 5),but the cell surface of the groups of polygonal

492

Electron Microscopy of the Human Endometrial Carcinoma*

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NILssoN—Electron Microscopy of Human Endometrial Carcinoma 493

cells was always irregular (Figs. 6, 9). The basalcell surface in the epithelial membranes generallywas slightly irregular (Fig. 8). However, the lowsquamous type of cell showed several deep projections into the connective tissue (Fig. 4). Thebasal cell membrane generally adhered to a basemont membrane, but sometimes a cluster of cellswas lying freely among the connective tissuecells. A zone of the cytoplasm at the basal cellsurface of these cells showed a dense ground substance, which lacked most of the other cell components (Fig. 8).

The mitochondnia were observed to vary innumber in the different cells. The structure ofmost of the mitochondnia was similar to that ofthe mitochondria of a normal glandular epithelium, but some large mitochondnia had cnistae lyingmore apart than is normal (Fig. 8).

The Golgi apparatus was visible in the upperpart of the cell. The ultrastructure of the differentGolgi components was similar to that of thesecomponents in a normal uterine gland cell.

The rough-surfaced membranes were presentin varying numbers. Sometimes a group of thesemembranes was noticed in the vicinity of thenuclear membrane (Fig. 5). The number of freelying RNP particles varied in the different cells.

Some inclusions of the cytoplasm were lipideglobules, small and large vesicles, granules, andlamellated bodies. The large vesicles and the granules have not yet been observed in normal uterineepithelium.

Lipide globules were frequent in some cells;they were noticed as areas with an irregular outline(Figs. 6, 7, 10, 11). A few of them containedvacuoles, a dense substance, or groups of parallelmembranes.

Vesicles of two types were observed. One typeof vesicle had a maximum size of 0.5 @.Thesevesicles were surrounded by a single membrane,and some vesicles contained an irregularly distributed substance (Figs. 2, 5—7,9—11).The othertype of vesicle was larger, with a maximum sizeof 2@ It was bounded by a varying numberof membranes, and it usually contained membranes which ran irregularly in a diffusely scattered substance (Figs. 9—li).

Granules of a varying ultrastructure were present in some cells (Figs. 2, 9). They were mostfrequent in the apical parts of the cells. Thegranules had a maximum size of about 1@ Asingle membrane surrounded some granules. Theinterior of the granules was composed of a dense,granulated substance with areas of vacuoles, membranes, and dark structures.

Lamellated bodies with a maximum size of

2@ were observed in different parts of the cells(Figs. 7, 10). They were surrounded by manyparallel membranes and contained a dense substance.

DISCUSSION

The microscopic diagnosis of endometrial adenocarcinoma sometimes is difficult due to the similanity in appearance between some endometnialhyperplasia and adenocancinoma (8, 18). Furthermore, the altered surroundings of the normal epithelium in a cancerous uterus might change thestructure of the normal cells to render a classification difficult. It cannot always be stated, therefore, that a certain epithelial cell of a biopsyreally is a cancer cell. In the present materialthe described cells are probably all malignant,but this cannot be proved. However, with thisreservation in mind they have been called cancercells.

Several cells of the uterine adenocarcinoma hadan ultrastructure that was different from thatof the normal glandular epithelium. The differences were evident in the general shape of thecells and in the morphology of the intracellularstructures.

The outline of the cells in the adenocarcinomavaried with respect to both the apical and thebasal cell surface. The apical cell surface of theepithelial membranes either was irregular or possessed microvilli, but the cell surface in the groupsof the polygonal cells was always irregular. Thisvarying ultrastructure of the cell surface of thecancer cells might imply a difference in the properties of these cells. However, no correlation of theappearance of the cell membrane with some consistent feature of the cytoplasm in the cancercell was observed in the present investigation.

Several irregular projections from the surfaceof a cell are probably a sign that the cell membraneexhibits lively movements. Since the basal surfacesof normal epithelial cells are rather regular, mostof the movements of this part of the cell membranemight be inhibited by the contact of the connective tissue cells. However, the low squamous typeof the adenocarcinoma cells showed several longprojections into the connective tissue. Since some

cancer cells seem to lack the property of havingthe movements of their cell membrane inhibitedby contact, the long projections of some adenocarcinoma cells might be signs of a reduced contact inhibition of these cells.

Cancer cells of different origin are known byboth light and electron microscopy to show a

higher variance in the number of intracellularstructures than do the normal cells (14). The

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494 Cancer Research Vol.292,May 1962

present investigation demonstrated that this isalso valid in the cells of the uterine adenocarcinoma. The change mostly comprised a decrease, butsometimes the number of a cellular componentwas increased. This was the case, for example, withRNP particles and some of the cytoplasmic inclu

sions.The higher amount of free RNP particles in the

cytoplasm of some cells caused these cells toappear more dense than the other cells in theelectron micrographs. These dense cells probablycorrespond to the A cells, introduced by Caspersson and Santesson (4). The density of these cells,however, seems to be caused not only by theRNP particles but also by some dense homogene

ous material of the ground substance in the cell.A similar material also was present basally inthose epithelial cells that were lacking the basement membrane. The significance of this materialis not yet known.

Some cellular inclusions, such as lipide globules,vesicles, and granules, were more frequently observed in some cancer cells compared with thenormal cells. The ultrastructures of the lipideglobules and the small vesicles were similar tothese inclusions in normal cells, but the largemembrane-containing vesicles and the granuleshave not been observed in the normal humanuterine epithelium. Probably, these structures aresigns of degeneration in the cancer cells. It mightalso be that the granules are ingested bacteria.

Some mitochondria of the cancer cells werelarge and irregular. Similar mitochondnia werealso observed during the secretory phase of themenstrual cycle (6, 12, 17, 19) . However, whereasthe mitochondnial cnistae of cancer cells werescanty and irregularly distributed, the mitochondrial cnistae of the normal gland cells were paralleland tightly packed. Since the cancer cells containing the large mitochondnia had the appearanceof anaplasia, the arrangement of the cnistae inthese mitochondria might be a sign of dedifferentiation.

The results of the present investigation demonstrated that the ultrastructure of cells in theadenocarcinoma of the uterus varies. It was notpossible to observe any cellular component orvirus-like particle that might be specific for thistype of cancer cell.

REFERENCES

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2. C@urriEn,R. Recherchesau moyen du microscopeélectronique sur la structure de l'endomètre en état follicolutenique a glycogene massif basal. BUlL FM. soc. gynéc.et obst., 11:363—67, 1959.

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9. L,&r@z@tvsccrna,G., and Moi@No, E. Ultrastruttura dellacellula ghiandolare dell' endometrio umano. Minerva ginec.,10:882—84,1958.

10. Moiwio, E. ; Snerom, C. ; and Vnccmsrrz, G. Ultrastruttura dell' endometrio umano. Tumori, 45: 1—12,1959.

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Hyperplasia SimUlating Adenocarcinoma. Am. J. Obst. &Gynec., 55:46-68, 1948.

14. OBnnwio, Ca., and Banxuasw, W. The Morphologyof theCancerCell.In: J. Baacua@rand A. E. Mmxs@(eds.), TheCell, 5:405—96. New York: Academic Press, Inc., 1961.

15. DEPALO,A., and STOPPELI,L L'endometrioal microscopioelettronico. Monit. ostet. ginecoL endoer. metaboL, 30:917—23,1959.

16. SmToai, C. Ultrastructures de l'endomêtrehumain normalet tumoraL Bull. Soc. roy. beIge gynec. et obst., 30:341-46,1960.

17. Surrom, C., and Moit@&No,E. Normal and Cancerous Human Endometrium and Remarks on Its Stroma Cells. In:A. L. Hmiwnrs and B. J. Spry (eds.), The Proceedings ofthe European Regional Conference on Electron Microscopy, 2:886-90. The Hague: N. V. Drukkerij Trio, 1961.

18. VsccmE'rTI, G., and Mois@No,E. Investigation of HumanEndometrium by the Electron Microscope. Int. J. Fertil.,4:109—14, 1959.

19. WEaSEL, W. Das elektronenmikroskopische Bild menschlicher endometrialer Drilsenzellen während des menstruellen Zyklus. Ztschr. Zellforsch., 51:633-57, 1960.

20. WurzsTEne, IL Elektroneumikroskopische Studien amEndometrium. Aunt. Ass., 105:218-26, 1958.

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FIG. 1.—Apical part of adenocarcinoma cells. The cell tothe left has a dense cytoplasm. This cell is probably an A cell.The mitochondria of both the cells are ratherlarge, and thoseof the A cell show changes of a degenerative type. Somegranules are observed among the mitochondria of the cell tothe right. Portions of nuclei are noticed in the lower part ofthe figure. Mag. X21,000.

FIG. 2.—Apical part of adenocarcinoma cells. The cell surface possesses microvilli. Granules and small vesicles occur frequently in the cytoplasm. Portions of nuclei are noticed in thelower right- and left-hand parts of the picture. Mag. X23,000.

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FIG. 3.—Apical part of adenocarcinoma cells. The cell surface has an irregular course. Some large mitochondria with disordered inner lamellae are noticed. Some RNP-coated membranes are observed. Mag. X21,000.

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FIG. 4.—Squamous type of adenocarcinoma cell with long

processes into the connective tissue. Mag. X7,000.Fia. 5.—Apical part of adenocarcinoma cells. Several

RNP-coated membranes are located at the nuclear membranein close vicinity to a nucleolus. Mag. X 16,000.

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FIG. 6.—Partof adenocarcinoma cellsgrowing in a globelikecell group. The irregular cell membrane is noticed. The rowof small vesicles from the surface into the cytoplasm mightindicate pinocytosis. In the middle of the picture a part of acell with a rather electron-dense cytoplasm is observed. Thiscell probably is an A cell. Lipide globules (L) also are noticed.Mag. X42,000.

FIG. 7.—Partof adenocarcinoma cell growing in a globelikecell group. Mitochondria, lipide globules (L), small vesicles,and lamellated bodies (airoll's) are noticed. Mag. X42,000.

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FIG. 8.—Basal part of a row of adenocarcinoma cells whichare lacking the basement membrane. A zone of cytoplasmadjacent to the cell membrane has a dense ground substance,with few cell constituents. Mag. X26,000.

FIG. 9.—Part of adenocarcinoma cells growing in a globelikecell group. Among the different cell constituents, a vesicle contaming a dense substance is noticed. The bounding membraneof the vesicle has ruptured. Mag. X19,000.

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FIG. 10.—Part ofadenocarcinoma cell growing in a globelikecell group. Mitochondria, lipide globules, small vesicles, largemembrane-containing vesicles, and lamellated bodies arenoticed. Mag. X47,000.

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Fia. 11.—Partof adenocarcinoma cell growing in a globelike cell group. Several large membrane-containing vesiclesare noticed. Mag. X56,000.

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1962;22:492-494. Cancer Res   O. Nilsson  Electron Microscopy of the Human Endometrial Carcinoma

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