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Amelanotic Melanocytes in the Outer Sheath of the Human Hair Follicle1
Preliminary and Short Report AMELANOTIC MELANOCYTES IN THE OUTER SHEATH OF THE HUMAN HAIR FOLLICLE* RENATO G. STAEJCCO, M.D.
The melanocyte is a pigmented dendritic cell which, during its developmental phases, contains granules reacting specifically with Masson's ammoniaeal silver nitrate and with dopa. In active hair follicles, melanocytes are characteristically
in the wall of the pilary canal (infundibulum),
possibly furnish a clue to the genesis and metamorphosis of pigment melanoeytes. For this study,
vertical and horizontal serial sections of normal and pathological scalp were stained with hematoxylin and eosin, toluidine blue, thionine, Dopa and Masson silver. These preparations all show the
pigmented melanocytes in the bulb and in the upper part of the dermal papilla. In the embryo, upper part of the hair follicle. Preparations stained with toluidine blue and, pigmented melanoeytes are also found in the outer sheath of the middle and lower part of the follicle to a lesser degree, thionine, show the presence of (1, 2). Montagna and Chase found amelanotic round cells with a distinct dark nucleus, often and in the pigmented part of the bulb, close to the
6
•
•0
Fm. 1: Melaneeytes between the basal portion of the epithelial cells forming the outer peripheral
layer. Mid hair follicle; Orcein-Giemsa X913.
melanoeytes in the outer root sheath three weeks surrounded by a clear space (Figs. 1, 2). These cells are located irregularly along the outer root following roentgen irradiation (3).
An organ as active as the hair follicle could * From
the Departments of Dermatology,
Wayne State University College of Medicine and
Detroit Receiving Hospital, Detroit, Michigan (Hermann Pinkus, M.D., Chairman). Supported in part by research grant RG-4435 and C-2072 from the National Institutes of Health, U. S. Public Health Service, and in part by re-
search contract DA-49-007-MD-584 from the Research and Development Division, Office of the Surgeon General, Department of the Army. Received for publication August 18, 1959. 295
sheath of the middle and lower parts of the follicle,
between the basal portions of the tall epithelial cells forming the outer peripheral layer. These cells are Dopa negative and do not stain with silver; several of these contain refringent granules.
Rarely, especially in sections from pathological biopsy specimens, one of them shows some pigmentation. These dark nucleated cells disappear near the upper part of the follicle which contain distinct dendritic melanoeytes. Occasional bipolar melanocytes similar to the immature or young
296
THE JOURNAL OF INVESTIGATIVE DERMATOLOGY
FIG. 3: Melanocytes in the outer sheath of the hair bulb; Masson silver X486.
FIG. 2: Melanocytes along the outer sheath of the lower hair follicle; Toluidine blue X931.
types described by Zimmermano (4) and flu (5, 6) are also found on the outer sheath of the bulb (Figs. 3, 4). DIscUSsION
Clear cells like those described by Massoo at the dermal-epidermal junction, but smaller and with a distinctive dark staining nucleus, are found along the outer sheath of the hair follicle. Except in pathological condition these cells do not contain melanin or premelanin, if one considers the Masson stain specific for premelanin.
The disappearance in the wall of the pilary canal, where the pigmented melanocytes are present, suggests that such cells probably repre-
S FIG. 4: X891 enlargement of figure 3. SUMMARY
sent a phase of melanocytic development in which
the melanin is either not yet produced, or the Distinctive cells believed to be non-functioning enzymatic mechanism is temporarily blocked. amelanotic melanocytes are present along the Therefore, there appear to be two forms of melanocytes in the hair follicle: (a) an amelanotic melanocyte and (b) a dendritic Dopa-positive melanocyte.
periphery of the outer root sheath of the human hair follicle.
REFERENCES Further work is under way to confirm these observations and to clarify the mechanism of 1. ZIMMERMANN, A. A.: Die Entwicklung der Hautfarbe beim Neger vnr der Geburt. pigment cell genesis in the hair follicle and the Mittl. Thurgauischen Naturforsch. Ges., follicle-melanocyte relationship.
37:
34—71, 1953.
AMELANOTIC MELANOCYTES IN HUMAN HAIR FOLLICLE
2. PJNKIJS, H.: Embryology of Hair. From "The Biology of Hair Growth" (Montagna, W. and
Ellis, R. A., edr.), pp. 1—38, New YorkLondon. Academic Press, Inc.
3. MONTAGNA, W. AND CHASE, H. B.: Histology
and Cytochemistry of Human Skin. X. X-irradiation of the Scalp. Am. J. Anat., 99: 415— 446, 1956.
4. ZIMMEaMANN, A. A. AND Bacscaa, S. W., Ja.:
Melanoblasts and Melanocytes in Fetal
Negro Skin. Illinois Monographs in Medical
297
Sciences, Vol. VI, No. 3, University of Il-
linois Press. Urbana, 1959. 5. Ho, F.: Cytological Studies of Human Pigment Cells in Tissue Culture. From "Pigment Cell Biology" by Gordon, M., pp. 147—158, New York-London. Academic Press Inc. 6. Ho, F., STARICCO, It. J., PINKOS, H. AND FOSNAIJGH, It. P.: Human melanocytes in tissue culture. J. Invest. Dermat. 28: 15—32, 1957.
THE JOURNAL OF INVESTIGATIVE DERMATOLOGY
94
linolenic acid extract. Arch. This pdf is a scanned copy UV of irradiated a printed document.
24. Wynn, C. H. and Iqbal, M.: Isolation of rat
skin lysosomes and a comparison with liver Path., 80: 91, 1965. and spleen lysosomes. Biochem. J., 98: lOP, 37. Nicolaides, N.: Lipids, membranes, and the 1966.
human epidermis, p. 511, The Epidermis
Eds., Montagna, W. and Lobitz, W. C. Acascopic localization of acid phosphatase in demic Press, New York. human epidermis. J. Invest. Derm., 46: 431, 38. Wills, E. D. and Wilkinson, A. E.: Release of 1966. enzymes from lysosomes by irradiation and 26. Rowden, C.: Ultrastructural studies of kerathe relation of lipid peroxide formation to tinized epithelia of the mouse. I. Combined enzyme release. Biochem. J., 99: 657, 1966. electron microscope and cytochemical study 39. Lane, N. I. and Novikoff, A. B.: Effects of of lysosomes in mouse epidermis and esoarginine deprivation, ultraviolet radiation and X-radiation on cultured KB cells. J. phageal epithelium. J. Invest. Derm., 49: 181, 25. Olson, R. L. and Nordquist, R. E.: Ultramicro-
No warranty is given about the accuracy of the copy.
Users should refer to the original published dermal cells. Nature, 216: 1031, 1967. version of1965. the material. vest. Derm., 45: 448, 28. Hall, J. H., Smith, J. G., Jr. and Burnett, S. 41. Daniels, F., Jr. and Johnson, B. E.: In prepa1967.
Cell Biol., 27: 603, 1965.
27. Prose, P. H., Sedlis, E. and Bigelow, M.: The 40. Fukuyama, K., Epstein, W. L. and Epstein, demonstration of lysosomes in the diseased J. H.: Effect of ultraviolet light on RNA skin of infants with infantile eczema. J. Inand protein synthesis in differentiated epi-
C.: The lysosome in contact dermatitis: A ration. histochemical study. J. Invest. Derm., 49: 42. Ito, M.: Histochemical investigations of Unna's oxygen and reduction areas by means of 590, 1967. 29. Pearse, A. C. E.: p. 882, Histochemistry Theoultraviolet irradiation, Studies on Melanin, retical and Applied, 2nd ed., Churchill, London, 1960.
30. Pearse, A. C. E.: p. 910, Histacheini.stry Thearetscal and Applied, 2nd ed., Churchill, London, 1960.
31. Daniels, F., Jr., Brophy, D. and Lobitz, W. C.: Histochemical responses of human skin fol-
lowing ultraviolet irradiation. J. Invest. Derm.,37: 351, 1961.
32. Bitensky, L.: The demonstration of lysosomes by the controlled temperature freezing section method. Quart. J. Micr. Sci., 103: 205, 1952.
33. Diengdoh, J. V.: The demonstration of lysosomes in mouse skin. Quart. J. Micr. Sci., 105: 73, 1964.
34. Jarret, A., Spearman, R. I. C. and Hardy, J. A.:
Tohoku, J. Exp. Med., 65: Supplement V, 10, 1957.
43. Bitcnsky, L.: Lysosomes in normal and pathological cells, pp. 362—375, Lysasames Eds., de Reuck, A. V. S. and Cameron, M. Churchill, London, 1953.
44. Janoff, A. and Zweifach, B. W.: Production of inflammatory changes in the microcirculation by cationic proteins extracted from lysosomes. J. Exp. Med., 120: 747, 1964.
45. Herion, J. C., Spitznagel, J. K., Walker, R. I. and Zeya, H. I.: Pyrogenicity of granulocyte lysosomes. Amer. J. Physiol., 211: 693, 1966.
46. Baden, H. P. and Pearlman, C.: The effect of ultraviolet light on protein and nucleic acid synthesis in the epidermis. J. Invest. Derm.,
Histochemistry of keratinization. Brit. J. 43: 71, 1964. Derm., 71: 277, 1959. 35. De Duve, C. and Wattiaux, R.: Functions of 47. Bullough, W. S. and Laurence, E. B.: Mitotic control by internal secretion: the role of lysosomes. Ann. Rev. Physiol., 28: 435, 1966. the chalone-adrenalin complex. Exp. Cell. 36. Waravdekar, V. S., Saclaw, L. D., Jones, W. A. and Kuhns, J. C.: Skin changes induced by
Res., 33: 176, 1964.
The melanocyte is a pigmented dendritic cell which, during its developmental phases, contains granules reacting specifically with Masson's ammoniaeal silver nitrate and with dopa. In active hair follicles, melanocytes are characteristically
in the wall of the pilary canal (infundibulum),
possibly furnish a clue to the genesis and metamorphosis of pigment melanoeytes. For this study,
vertical and horizontal serial sections of normal and pathological scalp were stained with hematoxylin and eosin, toluidine blue, thionine, Dopa and Masson silver. These preparations all show the
pigmented melanocytes in the bulb and in the upper part of the dermal papilla. In the embryo, upper part of the hair follicle. Preparations stained with toluidine blue and, pigmented melanoeytes are also found in the outer sheath of the middle and lower part of the follicle to a lesser degree, thionine, show the presence of (1, 2). Montagna and Chase found amelanotic round cells with a distinct dark nucleus, often and in the pigmented part of the bulb, close to the
6
•
•0
Fm. 1: Melaneeytes between the basal portion of the epithelial cells forming the outer peripheral
layer. Mid hair follicle; Orcein-Giemsa X913.
melanoeytes in the outer root sheath three weeks surrounded by a clear space (Figs. 1, 2). These cells are located irregularly along the outer root following roentgen irradiation (3).
An organ as active as the hair follicle could * From
the Departments of Dermatology,
Wayne State University College of Medicine and
Detroit Receiving Hospital, Detroit, Michigan (Hermann Pinkus, M.D., Chairman). Supported in part by research grant RG-4435 and C-2072 from the National Institutes of Health, U. S. Public Health Service, and in part by re-
search contract DA-49-007-MD-584 from the Research and Development Division, Office of the Surgeon General, Department of the Army. Received for publication August 18, 1959. 295
sheath of the middle and lower parts of the follicle,
between the basal portions of the tall epithelial cells forming the outer peripheral layer. These cells are Dopa negative and do not stain with silver; several of these contain refringent granules.
Rarely, especially in sections from pathological biopsy specimens, one of them shows some pigmentation. These dark nucleated cells disappear near the upper part of the follicle which contain distinct dendritic melanoeytes. Occasional bipolar melanocytes similar to the immature or young
296
THE JOURNAL OF INVESTIGATIVE DERMATOLOGY
FIG. 3: Melanocytes in the outer sheath of the hair bulb; Masson silver X486.
FIG. 2: Melanocytes along the outer sheath of the lower hair follicle; Toluidine blue X931.
types described by Zimmermano (4) and flu (5, 6) are also found on the outer sheath of the bulb (Figs. 3, 4). DIscUSsION
Clear cells like those described by Massoo at the dermal-epidermal junction, but smaller and with a distinctive dark staining nucleus, are found along the outer sheath of the hair follicle. Except in pathological condition these cells do not contain melanin or premelanin, if one considers the Masson stain specific for premelanin.
The disappearance in the wall of the pilary canal, where the pigmented melanocytes are present, suggests that such cells probably repre-
S FIG. 4: X891 enlargement of figure 3. SUMMARY
sent a phase of melanocytic development in which
the melanin is either not yet produced, or the Distinctive cells believed to be non-functioning enzymatic mechanism is temporarily blocked. amelanotic melanocytes are present along the Therefore, there appear to be two forms of melanocytes in the hair follicle: (a) an amelanotic melanocyte and (b) a dendritic Dopa-positive melanocyte.
periphery of the outer root sheath of the human hair follicle.
REFERENCES Further work is under way to confirm these observations and to clarify the mechanism of 1. ZIMMERMANN, A. A.: Die Entwicklung der Hautfarbe beim Neger vnr der Geburt. pigment cell genesis in the hair follicle and the Mittl. Thurgauischen Naturforsch. Ges., follicle-melanocyte relationship.
37:
34—71, 1953.
AMELANOTIC MELANOCYTES IN HUMAN HAIR FOLLICLE
2. PJNKIJS, H.: Embryology of Hair. From "The Biology of Hair Growth" (Montagna, W. and
Ellis, R. A., edr.), pp. 1—38, New YorkLondon. Academic Press, Inc.
3. MONTAGNA, W. AND CHASE, H. B.: Histology
and Cytochemistry of Human Skin. X. X-irradiation of the Scalp. Am. J. Anat., 99: 415— 446, 1956.
4. ZIMMEaMANN, A. A. AND Bacscaa, S. W., Ja.:
Melanoblasts and Melanocytes in Fetal
Negro Skin. Illinois Monographs in Medical
297
Sciences, Vol. VI, No. 3, University of Il-
linois Press. Urbana, 1959. 5. Ho, F.: Cytological Studies of Human Pigment Cells in Tissue Culture. From "Pigment Cell Biology" by Gordon, M., pp. 147—158, New York-London. Academic Press Inc. 6. Ho, F., STARICCO, It. J., PINKOS, H. AND FOSNAIJGH, It. P.: Human melanocytes in tissue culture. J. Invest. Dermat. 28: 15—32, 1957.
THE JOURNAL OF INVESTIGATIVE DERMATOLOGY
94
linolenic acid extract. Arch. This pdf is a scanned copy UV of irradiated a printed document.
24. Wynn, C. H. and Iqbal, M.: Isolation of rat
skin lysosomes and a comparison with liver Path., 80: 91, 1965. and spleen lysosomes. Biochem. J., 98: lOP, 37. Nicolaides, N.: Lipids, membranes, and the 1966.
human epidermis, p. 511, The Epidermis
Eds., Montagna, W. and Lobitz, W. C. Acascopic localization of acid phosphatase in demic Press, New York. human epidermis. J. Invest. Derm., 46: 431, 38. Wills, E. D. and Wilkinson, A. E.: Release of 1966. enzymes from lysosomes by irradiation and 26. Rowden, C.: Ultrastructural studies of kerathe relation of lipid peroxide formation to tinized epithelia of the mouse. I. Combined enzyme release. Biochem. J., 99: 657, 1966. electron microscope and cytochemical study 39. Lane, N. I. and Novikoff, A. B.: Effects of of lysosomes in mouse epidermis and esoarginine deprivation, ultraviolet radiation and X-radiation on cultured KB cells. J. phageal epithelium. J. Invest. Derm., 49: 181, 25. Olson, R. L. and Nordquist, R. E.: Ultramicro-
No warranty is given about the accuracy of the copy.
Users should refer to the original published dermal cells. Nature, 216: 1031, 1967. version of1965. the material. vest. Derm., 45: 448, 28. Hall, J. H., Smith, J. G., Jr. and Burnett, S. 41. Daniels, F., Jr. and Johnson, B. E.: In prepa1967.
Cell Biol., 27: 603, 1965.
27. Prose, P. H., Sedlis, E. and Bigelow, M.: The 40. Fukuyama, K., Epstein, W. L. and Epstein, demonstration of lysosomes in the diseased J. H.: Effect of ultraviolet light on RNA skin of infants with infantile eczema. J. Inand protein synthesis in differentiated epi-
C.: The lysosome in contact dermatitis: A ration. histochemical study. J. Invest. Derm., 49: 42. Ito, M.: Histochemical investigations of Unna's oxygen and reduction areas by means of 590, 1967. 29. Pearse, A. C. E.: p. 882, Histochemistry Theoultraviolet irradiation, Studies on Melanin, retical and Applied, 2nd ed., Churchill, London, 1960.
30. Pearse, A. C. E.: p. 910, Histacheini.stry Thearetscal and Applied, 2nd ed., Churchill, London, 1960.
31. Daniels, F., Jr., Brophy, D. and Lobitz, W. C.: Histochemical responses of human skin fol-
lowing ultraviolet irradiation. J. Invest. Derm.,37: 351, 1961.
32. Bitensky, L.: The demonstration of lysosomes by the controlled temperature freezing section method. Quart. J. Micr. Sci., 103: 205, 1952.
33. Diengdoh, J. V.: The demonstration of lysosomes in mouse skin. Quart. J. Micr. Sci., 105: 73, 1964.
34. Jarret, A., Spearman, R. I. C. and Hardy, J. A.:
Tohoku, J. Exp. Med., 65: Supplement V, 10, 1957.
43. Bitcnsky, L.: Lysosomes in normal and pathological cells, pp. 362—375, Lysasames Eds., de Reuck, A. V. S. and Cameron, M. Churchill, London, 1953.
44. Janoff, A. and Zweifach, B. W.: Production of inflammatory changes in the microcirculation by cationic proteins extracted from lysosomes. J. Exp. Med., 120: 747, 1964.
45. Herion, J. C., Spitznagel, J. K., Walker, R. I. and Zeya, H. I.: Pyrogenicity of granulocyte lysosomes. Amer. J. Physiol., 211: 693, 1966.
46. Baden, H. P. and Pearlman, C.: The effect of ultraviolet light on protein and nucleic acid synthesis in the epidermis. J. Invest. Derm.,
Histochemistry of keratinization. Brit. J. 43: 71, 1964. Derm., 71: 277, 1959. 35. De Duve, C. and Wattiaux, R.: Functions of 47. Bullough, W. S. and Laurence, E. B.: Mitotic control by internal secretion: the role of lysosomes. Ann. Rev. Physiol., 28: 435, 1966. the chalone-adrenalin complex. Exp. Cell. 36. Waravdekar, V. S., Saclaw, L. D., Jones, W. A. and Kuhns, J. C.: Skin changes induced by
Res., 33: 176, 1964.