Vol. 52, No. 2
THE JOURNAL OF INVESTIGATIVE DERMATOLOGY
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LANGERHANS' CELLS OF THE NORMAL HUMAN PILOSEBACEOUS SYSTEM AN ELECTRON MICROSCOPIC INVESTIGATION*
KOWICHI JIMBOW, M.D., SYOZO SATO, M.D. AND ATSUSHI KUKITA, MD. RESULTs Recently considerable attention has been paid to the nature of the Langerhans' cell, The Langerhans' cells were observed in the and a number of authors have proposed hy- outer root sheath of the hair follicle between
potheses concerning the histogenesis of these
the infundibulum and the hair bulge, and in the excretory duct of the sebaeeous gland.
cells. They have been considered as effete melanocytes (1, 2, 3, 4), postmelanin-synthetic
Hair. Langerhans' cells in the outer root
cells (5, 6), melanocyte precursors (7), post- sheath of the hair follicle could be readily divisional stages of previously melanogenic distinguished from the surrounding keratinomelanocytes (5), intraepidermal nerve endings eytes by the virtue of the clear cytoplasm, (9, 10) or self-perpetuating macrophagcs (11). devoid of tonofilaments, and the absence of Despite numerous histochemical and electron desmosomes along the plasma membrane. They microscopic studies, the nature of these cells were also characterized by the indented nucleus, is still unsettled. In order to provide further numerous rod and racquet-shaped granules, evidence, it is of great value to study the dis- mitoehondria, Golgi membranes, lysosomestribution of Langerhans' cells in the various like granules and endoplasmie reticulum. Some parts of normal and diseased skin. Several light microscopic investigations have
of these rod-shaped granules open to the extracellular spaces as described by Zelickson (5). been carried out as to the distribution of these Neither premelanosomes nor melanosomes were cells in the human pilosebaeeous system detected in the cytoplasm of Langerhans' cells (12—16). Nevertheless, these light microscopic (Fig. 1). Dendritie processes of these cells were studies were limited because of lack of specificity and difficulty in demonstrating these cells.
We report on the electron microscopic study
observed even between the cells in the third and fourth row of the outer root sheath (Fig. 2). Langerhans' cells in the other parts of the
of Langerhans' cells in the normal human
hair follicle could not be found in this study. Sebaceous gland. In the excretory duet of the
pilosebaceous system.
sehaceous gland, Langerhans' cells were also observed. The fine structure of these cells was identical with the cells in the outer root sheath
MATERIAL5 AND METHODS
Observations were carried out in the hair folli- of the hair follicle (Fig. 3). cles below the infundibulum and the sebaceous glands of the normal human scalp. Active hair DISCUSSION follicles (anagen phase) were removed with the surrounding appendages and dissected under the The distribution of Langerhans' cells in the stereoscopic microscope. These specimens were normal human pilosebaeeous system is of sigimmediately fixed in 2 per cent buffered (pH 7.4) osmium tetroxide for 2 hours, dehydrated in etha- nificance in relation to the nature and function nol and embedded in epoxy resins. Sections were of these cells. Mishima and Miller-Milinska made longitudinally to the hair follicle by means (12) demonstrated the osmium iodide positive of a Porter-Blum ultramicrotome MT-2. These dendritie cells at the various levels in the mulsections were stained with uranyl acetate and lead tiple layers of the outer root sheath, and even citrate, and then examined in a Hitachi HU-li A in the Huxley layer of the inner root sheath of electron microscope. the hair follicle. However, Langerhans' cells and This study was supported in part by a grant melanoeytes (both amelanotie and melanotie) from the Far East Basic Research Fund of Sears, show the same behavior towards the osmium Roebuck and Co., Inc., Chicago, Illinois. * From The Department of Dermatology, Sap- iodide reaction revealing similar morphologic poro Medical College, Sapporo, Japan. patterns. Starieco (17, 18, 19) reported 177
. I... •
'p.
V FIG. 1. The Langerhans cell is present between the first and second row of the outer
root sheath. Within the cytoplasm, characteristic Langerhans' granules, some of which open directly to the extracellular spaces, are present (Arrow). Langerhans' cell (LC), Keratinocyte (KC), Basement membrane (BM).
FIG. 2. Dendritic process of the Langerhans' cell is present among the cells of the outer roet sheath. Dendrite of Langerharis' cell (LD), Keratinocyte (KC). 178
LANGERHANS' CELL OF HUMAN PILOSEBACEOUS SYSTEM
179
-.
Fie. 3. The Langerhans' cell and its dendritie process are present in the excretory duet of the sehaeeous gland. Langerhans' cell (LC), Dendrite of Langerhans' cell (LD), Keratmoeyte (KC), Basement membrane (BM).
hair follicle and the duet of the sebaeeous of the middle and lower parts of the human gland, where amelanotic mclanocytes of Stahair follicle by orcein and Giemsa staining. rieco, gold chloride positive cells of Breathnach, Breathnaeh (13) and Breathnaeh et al. (14) osmium iodide positive cells of Mishima et al. amelanotic melanocytes in the outer root sheath
showed the distribution of gold chloride positive dendritic cells in the pilary canal, the outer reot sheath of the hair follicle between the infundib-
ulum and the hair bulge, and the various parts of the sebaceous gland. Wolff (15) and Wolff and Winkelmann (16) demonstrated the ATPase positive dendritic cells were present in the
pilary canal and the outer root sheath of the hair follicle, whereas they could not be detected in the sebaeeeus gland, because of the intense enzymatic activities of tile peripheral sebaeeons gland. These studies mentioned above were all
and ATP-ase positive cells of Wolff were present. Masson (1, 2), Billingham and Medawar (3), and Fan et ol. (4) suggested Langerhans' cells are "worn-out" mclanocytes of the epidermis, but recent studies proved that they are healthy, vital and actively engaged in protein synthesis (5, 21, 22).
Breathnaeh (8), Breathnaeh et al. (23, 24)
and Mishima (6) hypothesized that Langerhans'
cells represent an immediate postdivisional state of the mature previously melanogenic carried ant with the light microscope, and no melanocyte, .immature melanocytes in an arone has yet shown Langerhans' cells with char- rested phase of development or postmelaninacteristic granules in the normal human pilo- synthetic cells acquiring the ability of synthesebaceous system (20). The study of Breath- sizing Langerhans' granule after ceasing melanin nach and Goodwin (7) was the first proof of the biosynthesis. However, we have been unable to presence of Langerhans' cells in the outer root observe the Langerhans' cell in the melanocytic
sheath of the guinea pig white hair follicle, zone of the hair bulb where the melanogenic using the electron microscope.
activities are greatly increased.
In our study, Langerhans' cells have been Breathnach (8) suggested that Langerhans' demonstrated in the outer root sheath of the cells may have some function to accomplish in
180
THE JOURNAL OF INVESTIGATIVE DERMATOLOGY
relation to the malpighian cells of the supra- 10. Niebauer, G. and Sekido, K.: IJeber die Dendritenzellen der Epidermis: Eine Studie iiher basal layers. Riley (25, 26), and Jarrett and die Langerhanszellen in der normalen und ekzematosen Haut des Meersehweinchens. Spearman (27) reported that ATP-ase posiArch. klin. exp. Derm., 222: 23, 1965. tive dendritie cells may influence keratiniza11. Hashimoto, K. and Tarnowski, W. M.: Some tion. Wolff and Winkehnann (16, 28) stressed new aspects of the Langerhans cell. Arch. Derm., 97: 450, 1968. that Langerhans' cells may play an integral part Y. and Miller-Mihnska, A.: Juncin the biology of the epidermis and proposed 12. Mishima, tional and high dendritic cells revealed with that ultrastructural localization of ATP-ase in osmium iodide reaction in the human and animal epidermis under the conditions of the cytomembranes indicates a cell to cell interhyperpigmentation and depigmentation. J. relationship between Langerhans' cells and kernInvest. Derm., 37: 107, 1961. 13. Breathnach, A. S.: The distribution of Langertinocytes.
On the basis of the present findings it may
hans' cells within the human hair folhcles and
some observations on its staining properties with gold chloride. J. Anat., 97: 73, 1963. cytes constitute two distinct and independent 14. Breathnach, A. S., Birbeck, M. S. C. and Everall, J. D.: Observations hearing on the relaintraepithelial systems. However, the nature tionship between Langerhans' cells and meland function of Langerhans' cells in the piloanocytes. Ann. N. V. Acad. Sci., 100: 223, 1963. sebaceous system still remains to be determined. 15. Wolff, K.: Histologische Beobachtungen aus
be presumed that Langerhans' cells and melano-
5UMMAaY
1. Langerhans' cells were observed in the
der normalen menschlichen Haut bei der
Durchfflhrung ferment-histochemischer Untersuchungea mit Adenosintriphosphat. Arch.
kIm. exp. Derm., 216: 1, 1963. outer root sheath of hair follicles between the K. and Winkehnann, R. K.: Non-piginfundibulum and the hair bulge and in the ex- 16. Wolff, mentary enzymes of the melanocyte-Langer-
cretory duct of sebaceous glands in normal human skin.
hans' cell system, pp. 135—167, Advonces in
Biology of Skin, Vol. 8. Pergamon Press, Oxford, 1967.
2. The ultrastructural findings of these cells 17. Staricco, R. G.: Amelanotic melanocytes in the outer sheath of the human hair follicle. J. were identical with those described in human Invest. Derm., 33: 295, 1959.
epidermis.
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