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Neutrophil-Generated Active Oxygens in Linear IgA Bullous Dermatosis

Neutrophil-Generated Active Oxygens in Linear IgA Bullous Dermatosis Abstract • To examine the possible correlation between tissue injury and neutrophil-produced active oxygens (AOs) in patients with linear IgA bullous dermatosis (BD), we studied the capacity of neutrophils from six patients with BD to generate AOs. Cultured endothelial cells from human umbilical-cord vein were also incubated with the patients' neutrophils to assess AO-induced tissue injury. The AO production by patients' neutrophils was significantly elevated. The patients' neutrophils, as well as those from healthy controls preincubated with patients' serum, produced significantly increased levels of cytotoxic response on coincubation with chromium 51-labeled human endothelial cells. These results suggest that the tissue damage observed in BD may be partially due to both excessive production of AOs by neutrophils and a serum factor present in the patients, and further postulate the similar pathogenic process in dermatitis herpetiformis. (Arch Dermatol 1985;121:73-78) References 1. Fridovich I: Oxygen radicals, hydrogen peroxide and oxygen toxicity , in Pryor WA (ed): Free Radicals in Biology . New York, Academic Press Inc, 1976, pp 239-251. 2. Salin ML, McCord JM: Free radicals and inflammation: Protection of phagocytosing leukocytes by superoxide dismutase . J Clin Invest 1975;56:1319-1323.Crossref 3. McCord JM, Fridovich I: The biology and pathology of oxygen radicals . Ann Intern Med 1978;89:122-127.Crossref 4. Niwa Y, Miyake S, Sakane T, et al: Autooxidative damage in Behçet's disease: Endothelial cell damage following the elevated oxygen radicals generated by stimulated neutrophils . Clin Exp Immunol 1982;49:247-255. 5. Niwa Y, Sakane T, Shingu M, et al: Effect of stimulated neutrophils from the synovial fluid of patients with rheumatoid arthritis on lymphocytes: A possible role of increased oxygen radicals generated by the neutrophils . J Clin Immunol 1983;3:228-240.Crossref 6. Sacks T, Moldow CF, Craddock PR, et al: Oxygen radicals mediate endothelial cell damage by complement-stimulated granulocytes . J Clin Invest 1978;62:1161-1167.Crossref 7. Klebanoff SJ: Antimicrobial mechanisms in neutrophilic polymorphonuclear leukocytes . Semin Hematol 1975;12:117-142. 8. Niwa Y, Sohmiya K: Enhanced neutrophilic functions in mucocutaneous lymph node syndrome (MCLS): With special reference to the possible role of increased oxygen intermediate generation in the pathogenesis of coronary thromboarteritis . J Pediatr 1984;104:56-60.Crossref 9. Boxer LA, Oliver JM, Spielberg SP, et al: Protection of granulocytes by vitamin E in glutathione synthetase deficiency . N Engl J Med 1979;301:901-905.Crossref 10. Spielberg SP, Boxer LA, Corash LM: Improved erythrocyte survival with high-dose vitamin E chronic hemolyzing G6PD and glutathione synthetase deficiencies . Ann Intern Med 1979;90:53-54.Crossref 11. Necheles TF, Maldonado N, Barquet-Chediak H: Homozygous erythrocyte glutathione-peroxidase deficiency: Clinical and biochemical studies . Blood 1969;33:164-169. 12. Skosey JL, Chow DC, Musinow S, et al: Effect of oxygen tension on human peripheral blood leukocytes . J Cell Biol 1981;88:358-363.Crossref 13. Metzger Z, Hoffeld JT, Oppenheim JJ: Macrophage-mediated suppression . J Immunol 1980;124:983-988. 14. Nishida H, Tanimoto K, Akaoka H: Effect of free radicals on the lymphocytes . Clin Immunol Immunopathol 1981;19:319-324.Crossref 15. Murray HW, Cohn ZA: Macrophage oxygen-department antimicrobial activity: I. Susceptibility of toxoplasma gondii to oxygen intermediates . J Exp Med 1979;150:938-949.Crossref 16. Murray HW, Juangbhnich CW, Nathan CF, et al: Macrophage oxygen-department antimicrobial activity: II. The role of oxygen intermediates . J Exp Med 1979;150:950-964.Crossref 17. Babior MB: Oxygen-dependent microbial killing by phagocytes . N Engl J Med 1978;298:659-668.Crossref 18. Takayama K, Noguchi T, Nakano M, et al: Reactivities of diphenylfuran (a singlet oxygen trap) with singlet oxygen and hydroxyl radical in aqueous systems . Biochem Biophys 1977;75:1052-1058.Crossref 19. Heikkila RE, Cabbat FS: Chemiluminescence from autooxidizing 6-hydroxydopamine: The involvement of activated forms of oxygen . Photochem Photobiol 1978;28:677-680.Crossref 20. Ushijima Y, Nakano M: No or little production of singlet molecular oxygen in HOCl or HOCl/H2O2. A model system for myeloperoxidase/H2O2/Cl- . Biochem Biophys 1980;93:1232-1237.Crossref 21. Chorzelski TP, Jablonska S, Beutner EH: Linear IgA bullous dermatosis , in Beutner EH, Chorzelski TP, Bean SF (eds): Immunopathology of the Skin , ed 2. New York, John Wiley & Sons Inc, 1979, pp 315-323. 22. Stendahl O, Molin L, Dahlgren C: The inhibition of polymorphonuclear leukocyte cytotoxicity by dapsone . J Clin Invest 1978;62:214-220.Crossref 23. Cornbleet T: Sulfoxone (diasone) sodium for dermatitis herpetiformis . Arch Dermatol 1951;64:684-687.Crossref 24. Sheddon IB, Wilkinson DS: Subcorneal pustular dermatosis . Br J Dermatol 1956;68:385-394.Crossref 25. MacMillan AL, Champion RH: Generalized pustular psoriasis treated with dapsone . Br J Dermatol 1973;88:183-185.Crossref 26. Winkelmann RK, Ditto WB: Cutaneous and visceral symptoms of necrotizing or `allergic' angiitis: A study of 38 cases . Medicine 1964;43:59-89.Crossref 27. Williams K, Capstick RB, Lewis DA, et al: Anti-inflammatory actions of dapsone and its related biochemistry . J Pharm Pharmacol 1976;28:555-558.Crossref 28. Ward M, McManns JPA: Dapsone in Crohn's disease . Lancet 1975;1:1236-1237.Crossref 29. Niwa Y, Sakane T, Miyachi Y: Dissociation of the inhibitory effect of dapsone on the generation of oxygen intermediates: In comparison with that of colchicine and various scavengers . Biochem Pharmacol 1984;35:2355-2360.Crossref 30. Miyachi Y, Niwa Y: Effect of potassium iodide, colchicine and dapsone on the generation of polymorphonuclear leukocytederived oxygen intermediates . Br J Dermatol 1982;107:209-214.Crossref 31. Ikai M, Imamura S: Pemphygus-like antibodies in dermatitis herpetiformis . Dermatologica 1976;152:302-308.Crossref 32. Miller DR, Kaplan HG: Decreased nitroblue tetrazolium dye reduction in the phagocytes of patients receiving prednisone . Pediatrics 1970;45:861-865. 33. Oyanagui Y: Inhibition of superoxide anion production in macrophages by anti-inflammatory drugs . Biochem Pharmacol 1976;25:1473-1480.Crossref 34. Skosey JL, Chow DC, Damgaard E, et al: Effect of cytochalasin B on the response of human polymorphonuclear leukocytes to zymosan . J Cell Biol 1973;57:237-240.Crossref 35. Skosey JL, Damgaard E, Chow DC, et al: Modification of zymosan-induced release of lysosomal enzymes from human polymorphonuclear leukocytes by cytochalasin B . J Cell Biol 1974;62:625-634.Crossref 36. Cohen PP: Suspending media for normal tissues , in Umbreit WW (ed): Monometric Techniques and Tissues Metabolism . Minneapolis, Burgess Publishing Co, 1957, pp 149-150. 37. Jaffe EA, Nachman RL, Becker CG, et al: Culture of human endothelial cells derived from umbilical veins . J Clin Invest 1973;52:2745-2756.Crossref 38. Maciag T, Hoover GA, Stemerman MB, et al: Serial propagation of human endothelial cells in vitro . J Cell Biol 1981;91:420-426.Crossref 39. Johnson AR, Erdos G: Metabolism of vasoactive peptides by human endothelial cells in culture . J Clin Invest 1977;59:684-695.Crossref 40. Hoyer LW, Santos RP, Hoyer JR: Antihemophilic factor antigen: Localization in endothelial cells by immunofluorescence microscopy . J Clin Invest 1976;52:2737-2744.Crossref 41. Jaffe EA: Endothelial cells and biology of the factor 8 . N Engl J Med 1976;296:377-383. 42. Cochrane CG: Mechanisms involved in the deposition of immune complexes in tissues . J Exp Med 1971;134( (suppl) ):75s-89s.Crossref 43. Kniker WT, Cochrane CG: The localization of immune complexes in experimental serum sickness: The role of vasoactive amines and hydrodynamic forces . J Exp Med 1968;127:119-136.Crossref 44. Weissman G, Znrier RB, Spieler PJ, et al: Mechanisms of lysosomal enzyme release from leukocytes exposed to immune complexes and other particles . J Exp Med 1971;134( (suppl) ):149s-165s. 45. Michelson AM: Oxygen radicals , in Parnham MJ, Winkelmann J (eds): Agents and Actions . Basel, Switzerland, Birkhäuser Verlag, 1982, vol 11 ( (suppl) ), pp 179-201. 46. Emerit I, Michelson AM: Mechanism of photosensitivity in systemic lupus erythematosus patients . Proc Natl Acad Sci USA 1981;78:2537-2540.Crossref 47. Cochrane CG: Immunologic tissue injury mediated by neutrophilic leukocytes . Adv Immunol 1968;9:97-162. 48. Weissman G: Lysosomal mechanisms of tissue injury in arthritis . N Engl J Med 1972;286:141-147.Crossref 49. Janoff A: At least three human neutrophil lysosomal proteases are capable of degrading joint connective tissues . Ann NY Acad Sci 1975;256:402-408.Crossref 50. Cochrane CG, Unanue ER, Dixon FJ: A role of polymorphonuclear leukocytes and complement in nephrotoxic nephritis . J Exp Med 1965;122:99-116.Crossref 51. Katz SI, Strober W: The pathogenesis of dermatitis herpetiformis . J Invest Dermatol 1978;70:63-75.Crossref http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Dermatology American Medical Association

Neutrophil-Generated Active Oxygens in Linear IgA Bullous Dermatosis

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American Medical Association
Copyright
Copyright © 1985 American Medical Association. All Rights Reserved.
ISSN
0003-987X
eISSN
1538-3652
DOI
10.1001/archderm.1985.01660010077023
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Abstract

Abstract • To examine the possible correlation between tissue injury and neutrophil-produced active oxygens (AOs) in patients with linear IgA bullous dermatosis (BD), we studied the capacity of neutrophils from six patients with BD to generate AOs. Cultured endothelial cells from human umbilical-cord vein were also incubated with the patients' neutrophils to assess AO-induced tissue injury. The AO production by patients' neutrophils was significantly elevated. The patients' neutrophils, as well as those from healthy controls preincubated with patients' serum, produced significantly increased levels of cytotoxic response on coincubation with chromium 51-labeled human endothelial cells. These results suggest that the tissue damage observed in BD may be partially due to both excessive production of AOs by neutrophils and a serum factor present in the patients, and further postulate the similar pathogenic process in dermatitis herpetiformis. (Arch Dermatol 1985;121:73-78) References 1. Fridovich I: Oxygen radicals, hydrogen peroxide and oxygen toxicity , in Pryor WA (ed): Free Radicals in Biology . New York, Academic Press Inc, 1976, pp 239-251. 2. Salin ML, McCord JM: Free radicals and inflammation: Protection of phagocytosing leukocytes by superoxide dismutase . J Clin Invest 1975;56:1319-1323.Crossref 3. McCord JM, Fridovich I: The biology and pathology of oxygen radicals . Ann Intern Med 1978;89:122-127.Crossref 4. Niwa Y, Miyake S, Sakane T, et al: Autooxidative damage in Behçet's disease: Endothelial cell damage following the elevated oxygen radicals generated by stimulated neutrophils . Clin Exp Immunol 1982;49:247-255. 5. Niwa Y, Sakane T, Shingu M, et al: Effect of stimulated neutrophils from the synovial fluid of patients with rheumatoid arthritis on lymphocytes: A possible role of increased oxygen radicals generated by the neutrophils . J Clin Immunol 1983;3:228-240.Crossref 6. Sacks T, Moldow CF, Craddock PR, et al: Oxygen radicals mediate endothelial cell damage by complement-stimulated granulocytes . J Clin Invest 1978;62:1161-1167.Crossref 7. Klebanoff SJ: Antimicrobial mechanisms in neutrophilic polymorphonuclear leukocytes . Semin Hematol 1975;12:117-142. 8. Niwa Y, Sohmiya K: Enhanced neutrophilic functions in mucocutaneous lymph node syndrome (MCLS): With special reference to the possible role of increased oxygen intermediate generation in the pathogenesis of coronary thromboarteritis . J Pediatr 1984;104:56-60.Crossref 9. Boxer LA, Oliver JM, Spielberg SP, et al: Protection of granulocytes by vitamin E in glutathione synthetase deficiency . N Engl J Med 1979;301:901-905.Crossref 10. Spielberg SP, Boxer LA, Corash LM: Improved erythrocyte survival with high-dose vitamin E chronic hemolyzing G6PD and glutathione synthetase deficiencies . Ann Intern Med 1979;90:53-54.Crossref 11. Necheles TF, Maldonado N, Barquet-Chediak H: Homozygous erythrocyte glutathione-peroxidase deficiency: Clinical and biochemical studies . Blood 1969;33:164-169. 12. Skosey JL, Chow DC, Musinow S, et al: Effect of oxygen tension on human peripheral blood leukocytes . J Cell Biol 1981;88:358-363.Crossref 13. Metzger Z, Hoffeld JT, Oppenheim JJ: Macrophage-mediated suppression . J Immunol 1980;124:983-988. 14. Nishida H, Tanimoto K, Akaoka H: Effect of free radicals on the lymphocytes . Clin Immunol Immunopathol 1981;19:319-324.Crossref 15. Murray HW, Cohn ZA: Macrophage oxygen-department antimicrobial activity: I. Susceptibility of toxoplasma gondii to oxygen intermediates . J Exp Med 1979;150:938-949.Crossref 16. Murray HW, Juangbhnich CW, Nathan CF, et al: Macrophage oxygen-department antimicrobial activity: II. The role of oxygen intermediates . J Exp Med 1979;150:950-964.Crossref 17. Babior MB: Oxygen-dependent microbial killing by phagocytes . N Engl J Med 1978;298:659-668.Crossref 18. Takayama K, Noguchi T, Nakano M, et al: Reactivities of diphenylfuran (a singlet oxygen trap) with singlet oxygen and hydroxyl radical in aqueous systems . Biochem Biophys 1977;75:1052-1058.Crossref 19. Heikkila RE, Cabbat FS: Chemiluminescence from autooxidizing 6-hydroxydopamine: The involvement of activated forms of oxygen . Photochem Photobiol 1978;28:677-680.Crossref 20. Ushijima Y, Nakano M: No or little production of singlet molecular oxygen in HOCl or HOCl/H2O2. A model system for myeloperoxidase/H2O2/Cl- . Biochem Biophys 1980;93:1232-1237.Crossref 21. Chorzelski TP, Jablonska S, Beutner EH: Linear IgA bullous dermatosis , in Beutner EH, Chorzelski TP, Bean SF (eds): Immunopathology of the Skin , ed 2. New York, John Wiley & Sons Inc, 1979, pp 315-323. 22. Stendahl O, Molin L, Dahlgren C: The inhibition of polymorphonuclear leukocyte cytotoxicity by dapsone . J Clin Invest 1978;62:214-220.Crossref 23. Cornbleet T: Sulfoxone (diasone) sodium for dermatitis herpetiformis . Arch Dermatol 1951;64:684-687.Crossref 24. Sheddon IB, Wilkinson DS: Subcorneal pustular dermatosis . Br J Dermatol 1956;68:385-394.Crossref 25. MacMillan AL, Champion RH: Generalized pustular psoriasis treated with dapsone . Br J Dermatol 1973;88:183-185.Crossref 26. Winkelmann RK, Ditto WB: Cutaneous and visceral symptoms of necrotizing or `allergic' angiitis: A study of 38 cases . Medicine 1964;43:59-89.Crossref 27. Williams K, Capstick RB, Lewis DA, et al: Anti-inflammatory actions of dapsone and its related biochemistry . J Pharm Pharmacol 1976;28:555-558.Crossref 28. Ward M, McManns JPA: Dapsone in Crohn's disease . Lancet 1975;1:1236-1237.Crossref 29. Niwa Y, Sakane T, Miyachi Y: Dissociation of the inhibitory effect of dapsone on the generation of oxygen intermediates: In comparison with that of colchicine and various scavengers . Biochem Pharmacol 1984;35:2355-2360.Crossref 30. Miyachi Y, Niwa Y: Effect of potassium iodide, colchicine and dapsone on the generation of polymorphonuclear leukocytederived oxygen intermediates . Br J Dermatol 1982;107:209-214.Crossref 31. Ikai M, Imamura S: Pemphygus-like antibodies in dermatitis herpetiformis . Dermatologica 1976;152:302-308.Crossref 32. Miller DR, Kaplan HG: Decreased nitroblue tetrazolium dye reduction in the phagocytes of patients receiving prednisone . Pediatrics 1970;45:861-865. 33. Oyanagui Y: Inhibition of superoxide anion production in macrophages by anti-inflammatory drugs . Biochem Pharmacol 1976;25:1473-1480.Crossref 34. Skosey JL, Chow DC, Damgaard E, et al: Effect of cytochalasin B on the response of human polymorphonuclear leukocytes to zymosan . J Cell Biol 1973;57:237-240.Crossref 35. Skosey JL, Damgaard E, Chow DC, et al: Modification of zymosan-induced release of lysosomal enzymes from human polymorphonuclear leukocytes by cytochalasin B . J Cell Biol 1974;62:625-634.Crossref 36. Cohen PP: Suspending media for normal tissues , in Umbreit WW (ed): Monometric Techniques and Tissues Metabolism . Minneapolis, Burgess Publishing Co, 1957, pp 149-150. 37. Jaffe EA, Nachman RL, Becker CG, et al: Culture of human endothelial cells derived from umbilical veins . J Clin Invest 1973;52:2745-2756.Crossref 38. Maciag T, Hoover GA, Stemerman MB, et al: Serial propagation of human endothelial cells in vitro . J Cell Biol 1981;91:420-426.Crossref 39. Johnson AR, Erdos G: Metabolism of vasoactive peptides by human endothelial cells in culture . J Clin Invest 1977;59:684-695.Crossref 40. Hoyer LW, Santos RP, Hoyer JR: Antihemophilic factor antigen: Localization in endothelial cells by immunofluorescence microscopy . J Clin Invest 1976;52:2737-2744.Crossref 41. Jaffe EA: Endothelial cells and biology of the factor 8 . N Engl J Med 1976;296:377-383. 42. Cochrane CG: Mechanisms involved in the deposition of immune complexes in tissues . J Exp Med 1971;134( (suppl) ):75s-89s.Crossref 43. Kniker WT, Cochrane CG: The localization of immune complexes in experimental serum sickness: The role of vasoactive amines and hydrodynamic forces . J Exp Med 1968;127:119-136.Crossref 44. Weissman G, Znrier RB, Spieler PJ, et al: Mechanisms of lysosomal enzyme release from leukocytes exposed to immune complexes and other particles . J Exp Med 1971;134( (suppl) ):149s-165s. 45. Michelson AM: Oxygen radicals , in Parnham MJ, Winkelmann J (eds): Agents and Actions . Basel, Switzerland, Birkhäuser Verlag, 1982, vol 11 ( (suppl) ), pp 179-201. 46. Emerit I, Michelson AM: Mechanism of photosensitivity in systemic lupus erythematosus patients . Proc Natl Acad Sci USA 1981;78:2537-2540.Crossref 47. Cochrane CG: Immunologic tissue injury mediated by neutrophilic leukocytes . Adv Immunol 1968;9:97-162. 48. Weissman G: Lysosomal mechanisms of tissue injury in arthritis . N Engl J Med 1972;286:141-147.Crossref 49. Janoff A: At least three human neutrophil lysosomal proteases are capable of degrading joint connective tissues . Ann NY Acad Sci 1975;256:402-408.Crossref 50. Cochrane CG, Unanue ER, Dixon FJ: A role of polymorphonuclear leukocytes and complement in nephrotoxic nephritis . J Exp Med 1965;122:99-116.Crossref 51. Katz SI, Strober W: The pathogenesis of dermatitis herpetiformis . J Invest Dermatol 1978;70:63-75.Crossref

Journal

Archives of DermatologyAmerican Medical Association

Published: Jan 1, 1985

References