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Ultrastructure of Human Chordoma

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Ultrastructure of Human Chordoma (CANCER RESEARCH 28, 2115-2125, OctOber 1968] Ultrastructure of Human' RobertA. Erlandson, Bernard Tandler,2Philip H. Lieberman, and Norman 1.Higinbotham Division of Cytology, Sloan-Kettering Institute for Cancer Research, and Department of Pathology and the Bone Service of the De partment of Surgery, Memorial Hospital for Cancer and Allied Diseases, New York, New York 10021 SUMMARY published (5, 15, 29) ; each deals with a single case. The present article describes the fine structure of three sacrococcygeal Three sacrococcygeal chordomas, two of which were recur chordomas, with special emphasis on a unique complex of cyto rent, were examined by electron microscopy. The three tumors, plasmic organelles which was observed in each case. which were quite similar, consisted of cords, lobules, and clusters of cells embedded in a mucinous matrix. The so-called stellate MATERIALS AND METHODS and physaliferous cells represented the extremes of a develop mental sequence of tumor cells and were separated by a spec Specimens of sacrococcygeal chordomas were obtained from trum of morphologically intermediate cells. The physaliferous three patients by aspiration biopsy. Their case histories are cells appeared to arise from the stellate cells by a process of briefly summarized below: progressive cytoplasmic vacuolization. Some of the resulting Case 1. The patient was a 78-year-old white Jewish male vacuoles were so large that the nucleus and the cytoplasmic or who in 1950 underwent partial sacrectomy because of chordoma. ganelles were displaced to the cell periphery. Many vacuoles He remained symptom-free until 1965, when recurrent tumor contained deposits of glycogen. necessitated cobalt-60 therapy (6300 made, tumor dose) . The The most striking feature of the tumor cells was the consist tissue specimen was obtained late in 1966 about three hours ent association of mitochondria and endoplasmic reticulum in a after a single treatment of 300 mads. structurally ordered complex. In such complexes, single mito Case 2. The patient was a 60-year-old white Jewish female chondria alternated with single cistemnae, each organelle being who had undergone a partial sacrectomy for chordoma after separated from its neighbor by an interval of constant width. six months of rectal pain. The present specimen was from a The central portions of the mitochondria were so flattened that recurrent lesion removed in 1966. No radiotherapy had been the limiting membranes of opposite sides almost met ; at their given. ends, the mitochondria were bulbous and possessed a few Case 3. The patient was a 65-year-old white Jewish male angulated cristae. Beyond the lateral boundaries of the complex, who in 1966 underwent partial sacrectomy because of the the cisternae abruptly became smooth surfaced. The function presence of a chordoma. The specimen was obtained without of these unusual complexes is unknown. antecedent radiotherapy. For electron microscopy, small blocks of tissue were fixed INThODUCTION for one hour in a mixture of 2% acrolein and 6% glutaraldehyde (28) and postfixed for one hour in 2% osmium tetroxide (24) Chordoma, a tumor which usually appears in middle or late with added sucrose (7) . Both fixing solutions were buffered adult life, arises from remnants of the embryonic notochord with veronal acetate. After dehydration, the specimens were (20, 27) . The majority of these tumors occur at sites corre embedded in Maraglas-Dow Epoxy Resin 732 (11) . Thin see sponding to the ends of the notochord, 45 to 56% of reported tions were doubly stained with methanolic uranyl acetate (30) cases occurring in the sacrococcygeal region (25, 32) . While of and with lead citrate (26) , and were examined in a Siemens low malignancy, chordomas have a tendency to be locally in Elmiskop I electron microscope. vasive and destructive. A recent report by Higinbotham et at. Specimens for routine light microscopy were fixed in phos (19) has shown that following surgical removal, local recur phate-buffered formalin, embedded in paraffin, and stained with rences and metastases commonly occur. hematoxylin and eosin. Half-micron thick sections of epoxy Although the light microscopic characteristics of human embedded tissue were stained with toluidine blue using the chordomas have been described in numerous articles (6, 10, 12, method of Björkman (2) . Photomicrographs were taken with 14, 17, 31 ) , few studies of their ultrastructural organization a Zeiss standard WL microscope. have appeared. To date, only three such works have been OBSERVATIONS 1 This investigation was supported in part by Grant CA-08748 Light Microscopy from the National Cancer Institute, NIH. 2 Present address : School of Dentistry, Case Western Reserve In hematoxylin and eosin-stained paraffin sections, the tumors University, Cleveland, Ohio 44106. appeared to consist of two distinct cell types. The larger cell Received December 20, 1967; accepted June 13, 1968. type contained prominent vacuoles, and it is because of this OCTOBER 1968 2115 Downloaded from cancerres.aacrjournals.org on October 2, 2021. © 1968 American Association for Cancer Research. Robert A. Erlandson, Bernard Tandler, Philip H. Lieberman, and Norman L. Higinbot ham feature that they are called “physaliferouscells.―The smaller, The most striking feature of all the tumor cells was the con spindly cells, which appeared to be nonvacuolated, are usually sistent association of mitochondria and endoplasmic reticulum referred to as “stellatecells.―Both cell types, intermixed, were in a structurally ordered complex (Fig. 11) . In such a complex, arranged in cords, lobules, and clusters (Figs. 1, 2) . The rela single mitochondria alternated with single ergastoplasmic cis tive proportion of the two cell types varied from tumor to tu ternae, each organelle being separated from its neighbor by an mom and also in different sites within each specimen. The cell interval of approximately 500 A. As many as 10 layers of mito groupings were separated by a homogenous, mucinous matrix, chondria and 10 cistemnae were observed in some arrays. The and in one specimen they were surrounded by fibrous connec mitochondmia usually were long (about 2.3 @z)and dumbbell tive tissue as well as matrix. shaped. In their central portions, they were so attenuated that Much greater detail could be discerned in the thinner, tolu membranes of opposite sides almost met. At such points the idine blue-stained epoxy sections (Figs. 3—5).Not only physalif total thickness of the mitochondria measured as little as 340 erous and stellate cells were apparent, but a spectrum of A. The bulbous ends of the mitochondria were 10 times as morphologically intermediate cells as well. While the latter cells thick, measuring about 3400 A. These end portions frequently resembled stellate cells in form, they also possessed small cyto contained a few angulated cristae. The cistemnae were of the plasmic vacuoles. Many of the physaliferous cells contained rough-surfaced variety (RER), but at the lateral boundaries such large vacuoles that they assumed a typical “signetring― of the complex, which can be defined as the point where the shape (Fig. 3) . Some of the larger vacuoles contained a floe mitochondria end, the membranes abruptly became smooth culent material (Figs. 4, 5). (Figs. 13, 14) . In many cells, especially the physaliferous cells, The nuclei of the tumor cells frequently were highly irregular the smooth endoplasmic reticulum (SER) ramified throughout in size and contour. Many were multilobulated or had deep the cytoplasm (Figs. 7, 13). clefts. Occasional cells appeared to be binucleate. Intranuclear Solitary mitochondria, as well as solitary elements of RER, inclusions were present in many of the tumor cells, irrespective were infrequently seen. In contrast, a single distended cistern of cell type (Fig. 5) . These inclusions consisted of either a was frequently observed with several mitochondria in close dense spherical structure delimited by a light halo or a large relation (Fig. 12) . In such cistemnae, ribosomes were present mass of intermediate density surrounded by a very dense rim. primarily where mitochondria were apposed to the cistemnal The matrix, which appeared to be structureless, was stained membrane ; at other sites, the membranes usually were smooth. pink by the metachromatic toluidine blue, a tinctorial response Golgi complexes were present in many of the tumor cells, which was not shared by any other component of the tumors. being most abundant in the physaliferous cells, where they were usually situated near to or contiguous with the cytoplasmic Electron Microscopy vacuoles (Fig. 15) . The Golgi complexes consisted of closely Specimens from each of the three tumors studied were very packed, smooth cistemnae showing many fenestrations. Small similar at the ultrastructural level and are therefore described vesicles were numerous, and some were observed that were in composite. The electron microscope observations confirmed either budding or fusing with the Golgi cistemnae (Fig. 16). that stellate and physaliferous cells are not disparate cell types, Similar vesicles were sometimes joined to the limiting membrane but are related by a continuum of intermediate cells. Never of the vacuoles. theless, for the sake of convenience, this terminology is retained Many of the cytoplasmic vacuoles, large and small, con in this report. tamed glycogen (Figs. 6, 11) . Clusters of glycogen also were The aggregations of tumor cells were easily recognized at low abundant in both
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