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Electron Microscopic Studies of the Differentiation of Fat Cells in Human Fetal Skin

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Electron Microscopic Studies of the Differentiation of Fat Cells in Human Fetal Skin THE JOURNAL OP INVESTIGATIVE DERMATOLOGY Vol. 53, No. 2 Copyright C 1959 by The Williams & Wilkins Co. Printed in U.S.A. ELECTRON MICROSCOPIC STUDIES OF THE DIFFERENTIATION OF FAT CELLS IN HUMAN FETAL SKIN* HIDESUKE FUJITA, M.D., CHIDORI ASAGAMI, M.D., YOSHIHIKO ODA, M.D., TAKASHI MORI, M.D. AND YOSHIKO SUETOMI. M.D. ABSTRACT 1) Electron microscopic studies of primitive fat organs showing various degrees of fat storage from human fetuses 20 to 26 weeks of age were undertaken, with special reference to the origin of fat cells and the lipid formations in them. Based on this study, three types of cells, namely an undifferentiated-type cell, a young-type fat cell and a mature- type fat cell were discerned ultrastructurally, but they are considered to be identical con- cerning the morphology of mitochondria, smooth endoplasmic reticula and glycogen granules. 2) Concerning the origin of white fat cells, it was revealed that young-type and mature- type fat cells are not derived from reticuloendothelial cells or fibroblasts but from a certain definite type of mesenchymal cell which we have referred to as the undifferentiated-type cell. 3) The finding that cytoplasmic microvesicles are more prominent in young-type fat cells than in mature-type ones might be interpreted that the young-type cells may be actively releasing lipids or free fatty acids according to Williamson's concept of these organelles. But, contrary to Williamson's postulation, the young-type fat cells seem to be accumulating lipids or free fatty acids. Despite previous embryological studies on RESULTS the differentiation of fat cells in human skin made by light microscopy, important prob- Light Microscopy lems still remain unsolved (1—5). The present As seen in Figure 1, two types of fat cells report concerns ultrastructural changes of fatwere found. They are the cell containing cells in human fetal skins during their differ-multiple small lipid droplets (Y) and the signet, entiation, with special reference to the originring-type cell (M). Those cells were studied of fat cells and the lipid formations in them. with the light microscope using primitive fat organs showing various degrees of fat storage MATERIALS AND METHODS in the skin of human fetuses 20 to 26 weeks old. Previously, as a result of light microscopic The materials were obtained from the skins ofstudies, these two types of cells were considered the limbs of human fetuses 20 to 26 weeks oldto represent the early to mid stage and end (approximately 30 mm long in foot length and 191 mm long in crown-rump length). Previous histo-stage in maturation of in utero fat cells (3—5). logical studies have indicated that fat cells begin to develop in the human fetal skin at about 20 Electron Microscopy weeks (5). Three types of fat cells were discerned by The specimens were fixed with 4—6.5% glutaral- debyde for 2 hours followed by postosmificationelectron microscopic investigations of primi- in 1% osmium tetroxide for one hour. After de-tive fat organs from the same skin samples hydration in graded ethanols, the materials wereas those of the light microscopic observations embedded in Epon 812. The sections for electronmentioned above: (1), a cell which seems to microscopy were stained with 2% uranyl acetatecorrespond to the cell containing multiple and 0.4% lead citrate. small lipid droplets observed by light micros- This investigation was supported by grants fromcopy and which is referred to hereafter as the the Ministry of Education, Ube Industries, Ltd.young-type fat cell; (2), a cell which seems to and Shiseido Co. correspond to the light microscopic signet ring- Received October 1, 1968; accepted for publi- cation March 7, 1969. type cell, which is referred to hereafter as the * From the Department of Dermatology, Yama-mature-type fat cell; (3), a cell which is con- guchi University, School of Medicine, Ube, Japan. sidered to be the precursor cell developing to- 122 FAT CELLS IN HUMAN FETAL SKIN 123 1 j 'J Fic. 1. Light micrograph of primitive fat organs with beginning fat storage found in the subepidermal mesenchyme of limb skin from a 21 week-old human fetus. Y: a cell con- taining two or more small lipid droplets. M: a signet-ring type cell with a large central lipid droplet. Stained with hematoxyline-eosin. (X 400) ward the young-type fat cell though it has not tioned filaments. Luckenbill and Cohen (7) yet developed any lipid droplets in its cytoplasm reported, in observations of avian sybsynovial and which is referred to hereafter as the undif- adipose cells, a series of fine filaments 70 to ferentiated-type cell. 100 A wide associated with lipid droplets. The pattern in which the latter filaments are ar- 1. Young-Type Fat Cells ranged seems to differ from that of the fila- Cells of this type are variable in size, usu- ments in the present investigations, in having ally being thick and short in shape, with the a grid-like pattern. cytoplasm having multiple lipid droplets ac- The lipid droplets are variable in size and companied by a large number of glycogen electron density. Some of them contain nu- granules, numerous mitochondria, well developed merous electron dense substances, especially in smooth endoplasmic reticula, numerous cyto- their peripheral portion, while others contain plasmic microvesicles compatible with those electron less dense structures which are needle- described by Williamson (6) and a relatively shaped, cleft-shaped or tubular (Fig. 2). small number of rough endoplasmic reticula. The majority of these structures is considered A brief description of each of these elements due to artifact, except for some of the tubular follows: ones which seemingly come from endoplasmic Lipid droplets are generally round to ovoid reticula. in shape but some are irregular in shape. Glycogen granules are predominantly a-type Some lipid-cytoplasmic interfaces of theseand distributed throughout the cytoplasm droplets are bordered by thin dense lines (Figs. 3—6). over much of their area, others by an array Mitochondria are usually round to ovoid in of parallel fine filaments approximately 50 Ashape and show a topographically close rela- wide with nearly regular spacing which makestionship to groups of lipid droplets (Figs. 2, 3). them appear as if they had been carefully Smooth endoplasmic reticula are numerous, brushed (Fig. 3). Wood (4) reported, inmost of them being long and tubular in shape observations of adipose cells from the chick,with random orientation among glycogen gran- fine filaments 40 to 50 A wide showing a simi-ules (Figs. 2, 4). lar ordered array to that of the above-men- Cytoplasmie microvesicles are located prin- 124 THEJOURNAL OF INVESTIGATIVE DERMATOLOGY I •! —, p. — I, V FIG. 2. Low power view of a portion of a young-type fat cell in the limb skin. Multiple lipid droplets (L) are clustered around the nucleus (N), and surrounded by numerous mitochondria (Mt), smooth endoplasmic reticula (sER) and abundant glycogen granules (G) CV: numerous cytoplasmic microvesicles in the peripheral zone of the cytoplasm. rER: rough endoplasmic reticula. (X 14,500, 1.45 cm =ig) FAT CELLS IN HUMAN FETAL SKIN 125 4* 4 'via 0 FIG.3. An ordered array of fine filaments (arrow) bordering lipid-cytoplasmic interfaces in the cytoplasm of a young-type cell. Mt: mitochondria. G: a-type glycogen granules. (X 43,500, 4.35 cm =1z) 126 JOURNAL OP VflOAflVI MR*&TCLOQT 4 *1 • 4 j W • 'I, 11W 4' r W Iso. & Cytoplsemic microvericla (CV) in the peripheral sane ofthecytoplawn of a younflrpe fat cat MB: mlcrovtlsr rte which eo- of several cytoplasinic microvacles. Snows SinS,flask-likeInvaginaliona ofthe cytopissnicmembrane. Go: 00W apparaths. eBB: unooth adcplanlc rriicula. Mt: mltochondria. 0: e-twpe cogen pnnln.BM:bunnent n1s0:collagen an CX d$O% 426 cm =lii) FAT CELLS IN HUMAN FETAL SKIN 127 Fie.5.Microvesicularrosette (MR) and flask-like invaginations. CV: numerous cyto- plasmic microvesicles in the peripheral zone of the cytoplasm. Arrows indicate flask-like invaginations of smooth surfaced vacuoles (SV). Mt: mitochondria. G: a-type glycogen granules. BM: basement membrane. (X 79,500) 128 THE JOURNAL OF INVESTIGATIVE DERMATOLOGY S I $4 r' Fm. 6. Rough endoplasmic retieula (rER) arranged in lamellar form of a young-type fat cell. Mt: mitoehondria. G: cc-type glycogen. N: nucleus. (X 32,400, 3.6 em =lc) cipally in the peripheral zone of the cytoplasm. 2. Mature-Type Fat Cells Among them are rosette-like structures which Most cells of this type are larger than the consist of several mierovesicles (Figs. 4, 5, MR).young-type cells, nearly ovoid in shape and In addition to these rosette-like structures,have a large central lipid droplet which seems there are some mierovesieles, whose limitingto be made up by the enlargement and coa- membrane fuse with those of smooth surfacedlescence of the multiple lipid droplets in young- intraeytoplasmie vacuoles, with infolded cavi-type cells. This central lipid droplet displaces ties of eytoplasmic membranes, or directlythe nucleus to the periphery of the cell, being with eytoplasmic membranes, forming flask-occasionally accompanied by a few small drop- like invaginations in each of these cases, similarlets. So, this type of cell frequently shows a to the observations of Williamson (Fig. 5,very thin rim of cytoplasm which encompasses arrows). a large central lipid droplet (Fig. 8). Cyto- Rough endoplasmie reticula are generallyplasmie microvesicles and microvesieular rosettes few in number and short and tubular in shape.markedly decrease in number, occasionally Occasional cells show them well developed inbeing absent. Except for these differences, this which case they have a lamellar arrangementtype of cell shows features almost identical con- (Fig. 6), or are dilated and cystiform. cerning mitoehondria, smooth endoplasmic re- Basement membranes are occasionally foundtieula and glyeogen granules to those of young- type cells (Fig.
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