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Ultrastructural Localization of Calcium in Psoriatic and Normal Human Epidermis

Ultrastructural Localization of Calcium in Psoriatic and Normal Human Epidermis Abstract • With ion capture cytochemistry, we previously demonstrated the distribution of calcium ions in murine epidermis, a pattern consistent with a role for this ion in the regulation of epidermal differentiation. Because of the known proliferation and differentiation defects in psoriasis, we compared the calcium distribution of involved vs uninvolved psoriatic lesions and normal human epidermis. Whereas normal human and uninvolved psoriatic epidermis revealed increased calcium-containing precipitates in the uppermost stratum granulosum, in contrast the basal layer of psoriatic lesions contained less extracellular calcium, a condition that favored enhanced proliferation. Moreover, all psoriatic suprabasal cell layers displayed heavier than normal concentrations of calcium, indicating loss of the normal calcium gradient that programs terminal differentiation. This abnormal profile may account for the differentiation defects (eg, parakeratosis) that occur in psoriasis. Finally, psoriatic lesions displayed retained ionic Ca in intercellular domains of the upper stratum granulosum with absence of normal intercellular bilayers, findings that may underlie the abnormal desquamation and permeability barrier in psoriasis. (Arch Dermatol. 1991;127:57-63) References 1. Hesketh TR, Moore JP, Morris JD, et al. A common sequence of calcium and pH signals in the mitogenic stimulation of eukaryotic cells . Nature. 1985;313:481-484.Crossref 2. Fairley JA. Calcium and the skin . Arch Dermatol. 1988;124:443-444.Crossref 3. Rubin RP, ed. In: Calcium and Cellular Secretion . New York, NY: Plenum Press; 1982:276. 4. Hennings H, Michael D, Cheng C, et al. Calcium regulation of growth and differentiation of mouse epidermal cells in culture . Cell. 1980;19:245-254.Crossref 5. Elgjo K, Hennings H, Clausen OPF. Altered growth kinetics precede calcium-induced differentiation in mouse epidermal cells . In Vitro. 1986;22:332-336. 6. Menon GK, Grayson S, Elias PM. Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization with ion capture cytochemistry . J Invest Dermatol. 1985;84:508-512.Crossref 7. Elias PM, Menon GK, Grayson S, Brown BS. Membrane structural alterations in murine stratum corneum: relationship to the localization of polar lipids and phospholipases . J Invest Dermatol. 1988;91:3-10.Crossref 8. Hennings H, Steinert P, Buxman MM. Calcium induction of transglutaminase and formation of (γ-glutamyl) ε-lysine cross-links in cultured mouse epidermal cells . Biochem Biophys Res Commun. 1981;102:739-745.Crossref 9. Weinstein GD, Ross P, McCullough JL, Colton A. Proliferative defects in psoriasis . In: Wright NA, Camplejohn RS, eds. Psoriasis: Cell Proliferation . New York, NY: Churchill Livingstone Inc; 1983:189-208. 10. Brody I. The ultrastructure of the epidermis in psoriasis vulgaris as revealed by electron microscopy, IV: stratum corneum in parakeratosis without keratohyalin . J Ultrastruct Res. 1982;6:354-357.Crossref 11. Tucker WFC, MacNeil S, Bleehen SS, Tomlinson S. Biologically active calmodulin levels are elevated in both involved and uninvolved epidermis in psoriasis . J Invest Dermatol. 1984;82:298-299.Crossref 12. Fairley JA, Marcelo CL, Hogan VA, et al. Increased calmodulin levels in psoriasis and low calcium-regulated mouse epidermal keratinocyte cultures . J Invest Dermatol. 1985;84:195-198.Crossref 13. Pillai S, Menon GK. Quantitation of intracellular free calcium (Cai) by spectrofluorometry and correlative ultrastructural localization by ion capture cytochemistry in human keratinocytes . J Invest Dermatol. 1990;94:566. 14. McNutt NS, Crain WL. Quantitative electron microscope comparison of lymphatic nuclear contours in mycosis fungoides and in benign infiltrates in the skin . Cancer. 1981;47:163-166.Crossref 15. Hou ESY, Menon GK, Elias PM. Abnormalities in lamellar body and stratum corneum lamellae in essential fatty acid deficiency visualized by a modified ruthenium staining protocol . J Invest Dermatol. 1989;92:448. Abstract. 16. Ravazzola M. Intracellular localization of calcium in the chromaffin cells of the rat adrenal medulla . Endocrinology. 1976;98:950-953.Crossref 17. Borgers M, Thore F, Van Nuetten JM. The subcellular distribution of calcium and the effects of calcium-antagonists as evaluated with a combined oxalate-pyroantimonate method . Acta Histochem Suppl (Jena). 1981;24:327-332. 18. McGraw CF, Somlyo AV, Blaustein MP. Probing for calcium at the synaptic nerve terminals . Fed Proc. 1980;39:2796. 19. Ornberg RL, Reese TS. A freeze-substitution method for localizing divalent cations: examples from secretory systems . Fed Proc. 1980;39:2802. 20. Malmquist KC, Carlson LE, Forslind B, Roomans GM. Proton and electron microprobe analysis of human skin . Nuclear Inst Meth Phys Res. 1984;3:611-617.Crossref 21. Yuspa SH, Kildenny AE, Steinert PM, Roop DR. Expression of murine epidermal differentiation markers is tightly regulated by restricted extracellular calcium concentrations in vitro . J Cell Biol. 1989;109:1207-1217.Crossref 22. Heng MCY, Kloss SG, Kuehm CS, Chase DG. Significance and pathogenesis of basal keratinocyte herniations in psoriasis . J Invest Dermatol. 1986;87:362-366.Crossref 23. Watt FM, Mattey DL, Garrod DR. Calcium induced reorganization of desmosomal components in cultured human keratinocytes . J Cell Biol. 1984;99:2211-2215.Crossref 24. Mercer EH, Maibach HI. Intercellular adhesion and surface coats of epidermal cells in psoriasis . J Invest Dermatol. 1968;51:215-221.Crossref 25. Christophers E, Schubert C. Psoriasis . In: Thody AJ, Friedmann PS, eds. Scientific Basis of Dermatology: A Physiological Approach . New York, NY: Churchill Livingstone Inc; 1986:151-174. 26. Pillai S, Bikle DD, Hincenbergs M, Elias PM. Biochemical and morphological characterization of growth and differentiation of normal human neonatal keratinocytes in a serum free medium . J Cell Physiol. 1988;134:229-237.Crossref 27. Hennings H, Holbrook KA. Calcium regulation of cell-cell contact and differentiation of epidermal cells in culture: an ultrastructural study . Exp Cell Res. 1983;143:127-142.Crossref 28. Hickie RA, Wei J-W, Blyth LM, Wong DYW, Klassen DJ. Cations and calmodulin in normal and neoplastic cell growth and regulation . Can J Biochem Cell Biol. 1983;61:934-941.Crossref 29. Means AR, Rasmussen CD. Calcium, calmodulin and cell proliferation . Cell Calcium. 1988;9:313-319.Crossref 30. Wollina U, Klinger R, Wetzker R, Knopf B. Increase of epidermal calmodulin precedes the formation of a psoriatic lesion . Arch Dermatol Res. 1989;281:73-74.Crossref 31. Klee CB, Newton DL. Calmodulin: an overview . In: Pavratt JR, ed. Control and Manipulation of Calcium Movement . New York, NY: Raven Press; 1985:131-146. 32. Rubin RP, Laychoc SG. Prostaglandins, calcium and cyclic nucleotides in stimulus-response coupling . In: Weiss GB, ed. Calcium in Drug Action . New York, NY: Plenum Press; 1978:135-155. 33. Bernard BA, Robinson SM, Vandaele S, Mansbridge JN, Darmon M. Abnormal maturation pathways of keratinocytes in psoriatic skin . Br J Dermatol. 1985;112:647-653.Crossref 34. Bernard BA, Reano A, Darmon YM, Thivolet J. Precocious appearance of involucrin and epidermal trans-glutaminase during differentiation of psoriatic skin . Br J Dermatol. 1986;114:279-283.Crossref 35. Jones JC, Goldman AE, Steinert P, Yuspa SH, Goldman RD. Dynamic aspects of the supramolecular organization of intermediate filament networks in cultured epidermal cells . Cell Motil. 1982;2:197-213.Crossref 36. Skerrow CJ, Clelland D, Skerrow D. Abnormal retention of desmosomes in psoriatic scale . Br J Dermatol. 1988;118:283-284. 37. Abraham W, Wertz PW, Downing DT. Fusion patterns of liposomes formed from stratum corneum lipids . J Invest Dermatol. 1988;90:259-262.Crossref 38. Lampe MA, Williams ML, Elias PM. Human epidermal lipids: characterization and modulations during differentiation . J Lipid Res. 1983;24:131-140. 39. Seimaya T, Ohki S. Ionic structure of phospholipid membranes and binding of calcium ions . Biochim Biophys Acta. 1973;298:546-561.Crossref http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Dermatology American Medical Association

Ultrastructural Localization of Calcium in Psoriatic and Normal Human Epidermis

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Publisher
American Medical Association
Copyright
Copyright © 1991 American Medical Association. All Rights Reserved.
ISSN
0003-987X
eISSN
1538-3652
DOI
10.1001/archderm.1991.01680010067010
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Abstract

Abstract • With ion capture cytochemistry, we previously demonstrated the distribution of calcium ions in murine epidermis, a pattern consistent with a role for this ion in the regulation of epidermal differentiation. Because of the known proliferation and differentiation defects in psoriasis, we compared the calcium distribution of involved vs uninvolved psoriatic lesions and normal human epidermis. Whereas normal human and uninvolved psoriatic epidermis revealed increased calcium-containing precipitates in the uppermost stratum granulosum, in contrast the basal layer of psoriatic lesions contained less extracellular calcium, a condition that favored enhanced proliferation. Moreover, all psoriatic suprabasal cell layers displayed heavier than normal concentrations of calcium, indicating loss of the normal calcium gradient that programs terminal differentiation. This abnormal profile may account for the differentiation defects (eg, parakeratosis) that occur in psoriasis. Finally, psoriatic lesions displayed retained ionic Ca in intercellular domains of the upper stratum granulosum with absence of normal intercellular bilayers, findings that may underlie the abnormal desquamation and permeability barrier in psoriasis. (Arch Dermatol. 1991;127:57-63) References 1. Hesketh TR, Moore JP, Morris JD, et al. A common sequence of calcium and pH signals in the mitogenic stimulation of eukaryotic cells . Nature. 1985;313:481-484.Crossref 2. Fairley JA. Calcium and the skin . Arch Dermatol. 1988;124:443-444.Crossref 3. Rubin RP, ed. In: Calcium and Cellular Secretion . New York, NY: Plenum Press; 1982:276. 4. Hennings H, Michael D, Cheng C, et al. Calcium regulation of growth and differentiation of mouse epidermal cells in culture . Cell. 1980;19:245-254.Crossref 5. Elgjo K, Hennings H, Clausen OPF. Altered growth kinetics precede calcium-induced differentiation in mouse epidermal cells . In Vitro. 1986;22:332-336. 6. Menon GK, Grayson S, Elias PM. Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization with ion capture cytochemistry . J Invest Dermatol. 1985;84:508-512.Crossref 7. Elias PM, Menon GK, Grayson S, Brown BS. Membrane structural alterations in murine stratum corneum: relationship to the localization of polar lipids and phospholipases . J Invest Dermatol. 1988;91:3-10.Crossref 8. Hennings H, Steinert P, Buxman MM. Calcium induction of transglutaminase and formation of (γ-glutamyl) ε-lysine cross-links in cultured mouse epidermal cells . Biochem Biophys Res Commun. 1981;102:739-745.Crossref 9. Weinstein GD, Ross P, McCullough JL, Colton A. Proliferative defects in psoriasis . In: Wright NA, Camplejohn RS, eds. Psoriasis: Cell Proliferation . New York, NY: Churchill Livingstone Inc; 1983:189-208. 10. Brody I. The ultrastructure of the epidermis in psoriasis vulgaris as revealed by electron microscopy, IV: stratum corneum in parakeratosis without keratohyalin . J Ultrastruct Res. 1982;6:354-357.Crossref 11. Tucker WFC, MacNeil S, Bleehen SS, Tomlinson S. Biologically active calmodulin levels are elevated in both involved and uninvolved epidermis in psoriasis . J Invest Dermatol. 1984;82:298-299.Crossref 12. Fairley JA, Marcelo CL, Hogan VA, et al. Increased calmodulin levels in psoriasis and low calcium-regulated mouse epidermal keratinocyte cultures . J Invest Dermatol. 1985;84:195-198.Crossref 13. Pillai S, Menon GK. Quantitation of intracellular free calcium (Cai) by spectrofluorometry and correlative ultrastructural localization by ion capture cytochemistry in human keratinocytes . J Invest Dermatol. 1990;94:566. 14. McNutt NS, Crain WL. Quantitative electron microscope comparison of lymphatic nuclear contours in mycosis fungoides and in benign infiltrates in the skin . Cancer. 1981;47:163-166.Crossref 15. Hou ESY, Menon GK, Elias PM. Abnormalities in lamellar body and stratum corneum lamellae in essential fatty acid deficiency visualized by a modified ruthenium staining protocol . J Invest Dermatol. 1989;92:448. Abstract. 16. Ravazzola M. Intracellular localization of calcium in the chromaffin cells of the rat adrenal medulla . Endocrinology. 1976;98:950-953.Crossref 17. Borgers M, Thore F, Van Nuetten JM. The subcellular distribution of calcium and the effects of calcium-antagonists as evaluated with a combined oxalate-pyroantimonate method . Acta Histochem Suppl (Jena). 1981;24:327-332. 18. McGraw CF, Somlyo AV, Blaustein MP. Probing for calcium at the synaptic nerve terminals . Fed Proc. 1980;39:2796. 19. Ornberg RL, Reese TS. A freeze-substitution method for localizing divalent cations: examples from secretory systems . Fed Proc. 1980;39:2802. 20. Malmquist KC, Carlson LE, Forslind B, Roomans GM. Proton and electron microprobe analysis of human skin . Nuclear Inst Meth Phys Res. 1984;3:611-617.Crossref 21. Yuspa SH, Kildenny AE, Steinert PM, Roop DR. Expression of murine epidermal differentiation markers is tightly regulated by restricted extracellular calcium concentrations in vitro . J Cell Biol. 1989;109:1207-1217.Crossref 22. Heng MCY, Kloss SG, Kuehm CS, Chase DG. Significance and pathogenesis of basal keratinocyte herniations in psoriasis . J Invest Dermatol. 1986;87:362-366.Crossref 23. Watt FM, Mattey DL, Garrod DR. Calcium induced reorganization of desmosomal components in cultured human keratinocytes . J Cell Biol. 1984;99:2211-2215.Crossref 24. Mercer EH, Maibach HI. Intercellular adhesion and surface coats of epidermal cells in psoriasis . J Invest Dermatol. 1968;51:215-221.Crossref 25. Christophers E, Schubert C. Psoriasis . In: Thody AJ, Friedmann PS, eds. Scientific Basis of Dermatology: A Physiological Approach . New York, NY: Churchill Livingstone Inc; 1986:151-174. 26. Pillai S, Bikle DD, Hincenbergs M, Elias PM. Biochemical and morphological characterization of growth and differentiation of normal human neonatal keratinocytes in a serum free medium . J Cell Physiol. 1988;134:229-237.Crossref 27. Hennings H, Holbrook KA. Calcium regulation of cell-cell contact and differentiation of epidermal cells in culture: an ultrastructural study . Exp Cell Res. 1983;143:127-142.Crossref 28. Hickie RA, Wei J-W, Blyth LM, Wong DYW, Klassen DJ. Cations and calmodulin in normal and neoplastic cell growth and regulation . Can J Biochem Cell Biol. 1983;61:934-941.Crossref 29. Means AR, Rasmussen CD. Calcium, calmodulin and cell proliferation . Cell Calcium. 1988;9:313-319.Crossref 30. Wollina U, Klinger R, Wetzker R, Knopf B. Increase of epidermal calmodulin precedes the formation of a psoriatic lesion . Arch Dermatol Res. 1989;281:73-74.Crossref 31. Klee CB, Newton DL. Calmodulin: an overview . In: Pavratt JR, ed. Control and Manipulation of Calcium Movement . New York, NY: Raven Press; 1985:131-146. 32. Rubin RP, Laychoc SG. Prostaglandins, calcium and cyclic nucleotides in stimulus-response coupling . In: Weiss GB, ed. Calcium in Drug Action . New York, NY: Plenum Press; 1978:135-155. 33. Bernard BA, Robinson SM, Vandaele S, Mansbridge JN, Darmon M. Abnormal maturation pathways of keratinocytes in psoriatic skin . Br J Dermatol. 1985;112:647-653.Crossref 34. Bernard BA, Reano A, Darmon YM, Thivolet J. Precocious appearance of involucrin and epidermal trans-glutaminase during differentiation of psoriatic skin . Br J Dermatol. 1986;114:279-283.Crossref 35. Jones JC, Goldman AE, Steinert P, Yuspa SH, Goldman RD. Dynamic aspects of the supramolecular organization of intermediate filament networks in cultured epidermal cells . Cell Motil. 1982;2:197-213.Crossref 36. Skerrow CJ, Clelland D, Skerrow D. Abnormal retention of desmosomes in psoriatic scale . Br J Dermatol. 1988;118:283-284. 37. Abraham W, Wertz PW, Downing DT. Fusion patterns of liposomes formed from stratum corneum lipids . J Invest Dermatol. 1988;90:259-262.Crossref 38. Lampe MA, Williams ML, Elias PM. Human epidermal lipids: characterization and modulations during differentiation . J Lipid Res. 1983;24:131-140. 39. Seimaya T, Ohki S. Ionic structure of phospholipid membranes and binding of calcium ions . Biochim Biophys Acta. 1973;298:546-561.Crossref

Journal

Archives of Dermatology – American Medical Association

Published: Jan 1, 1991

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