Skip to main content
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1991 Sep;88(3):841–846. doi: 10.1172/JCI115385

Augmentation of reverse arthus reaction by mast cells in mice.

Y Zhang 1, B F Ramos 1, B A Jakschik 1
PMCID: PMC295470  PMID: 1832174

Abstract

Immune complex-induced injury is an important pathogenic factor in antibody-mediated nephritis, systemic lupus erythematosus, rheumatoid arthritis, and other diseases. In this study we investigated the role mast cells in immune complex-mediated injury in mouse skin. Reverse Arthus reaction was induced in mast cell-deficient WBB6F1-W/Wv mice and their congenic controls (WBB6F1(-)+/+). Serial skin sections were evaluated for neutrophil infiltration, edema, and hemorrhage. In WBB6F1-W/Wv mice the neutrophil influx was only 40% and edema 60% of that in congenic controls. Hemorrhage was also significantly reduced in the mast cell-deficient mice. After mast cell reconstitution, the magnitude of the reaction in WBB6F1-W/Wv was equivalent to that in WBB6F1(-)+/+ mice. Mast cell release in reverse Arthus reaction was evaluated by measuring fluorescence intensity after avidin-FITC staining of mast cell granules. There was a 70% decrease in fluorescence intensity. The 5-lipoxygenase inhibitor A-63162 significantly decreased neutrophil accumulation (40%), edema (60%), and hemorrhage in WBB6F1(-)+/+, but not in mast cell-deficient mice. Mast cell reconstitution of WBB6F1-W/Wv mice restored the effect of A-63162. The results indicate that mast cells and their mediators, including leukotrienes, make an important contribution to reverse Arthus reaction.

Full text

PDF
841

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arai K. I., Lee F., Miyajima A., Miyatake S., Arai N., Yokota T. Cytokines: coordinators of immune and inflammatory responses. Annu Rev Biochem. 1990;59:783–836. doi: 10.1146/annurev.bi.59.070190.004031. [DOI] [PubMed] [Google Scholar]
  2. Bergstresser P. R., Tigelaar R. E., Tharp M. D. Conjugated avidin identifies cutaneous rodent and human mast cells. J Invest Dermatol. 1984 Sep;83(3):214–218. doi: 10.1111/1523-1747.ep12263584. [DOI] [PubMed] [Google Scholar]
  3. Bevilacqua M. P., Pober J. S., Mendrick D. L., Cotran R. S., Gimbrone M. A., Jr Identification of an inducible endothelial-leukocyte adhesion molecule. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9238–9242. doi: 10.1073/pnas.84.24.9238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Björk J., Smedegård G. Immune-complex-induced inflammatory reaction studied by intravital microscopy: role of histamine and arachidonic acid metabolites. Inflammation. 1987 Mar;11(1):47–58. doi: 10.1007/BF00917771. [DOI] [PubMed] [Google Scholar]
  5. Björk J., Smedegård G. The microvasculature of the hamster cheek pouch as a model for studying acute immune-complex-induced inflammatory reactions (with 1 color plate). Int Arch Allergy Appl Immunol. 1984;74(2):178–185. doi: 10.1159/000233540. [DOI] [PubMed] [Google Scholar]
  6. Bonney R. J., Naruns P., Davies P., Humes J. L. Antigen-antibody complexes stimulate the synthesis and release of prostaglandins by mouse peritoneal macrophages. Prostaglandins. 1979 Oct;18(4):605–616. doi: 10.1016/0090-6980(79)90027-3. [DOI] [PubMed] [Google Scholar]
  7. Borgeat P., Samuelsson B. Metabolism of arachidonic acid in polymorphonuclear leukocytes. Structural analysis of novel hydroxylated compounds. J Biol Chem. 1979 Aug 25;254(16):7865–7869. [PubMed] [Google Scholar]
  8. Braquet P., Touqui L., Shen T. Y., Vargaftig B. B. Perspectives in platelet-activating factor research. Pharmacol Rev. 1987 Jun;39(2):97–145. [PubMed] [Google Scholar]
  9. Burd P. R., Rogers H. W., Gordon J. R., Martin C. A., Jayaraman S., Wilson S. D., Dvorak A. M., Galli S. J., Dorf M. E. Interleukin 3-dependent and -independent mast cells stimulated with IgE and antigen express multiple cytokines. J Exp Med. 1989 Jul 1;170(1):245–257. doi: 10.1084/jem.170.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chervenick P. A., Boggs D. R. Decreased neutrophils and megakaryocytes in anemic mice of genotype W/W. J Cell Physiol. 1969 Feb;73(1):25–30. doi: 10.1002/jcp.1040730104. [DOI] [PubMed] [Google Scholar]
  11. Claman H. N. On scleroderma. Mast cells, endothelial cells, and fibroblasts. JAMA. 1989 Sep 1;262(9):1206–1209. doi: 10.1001/jama.262.9.1206. [DOI] [PubMed] [Google Scholar]
  12. Dahlén S. E., Björk J., Hedqvist P., Arfors K. E., Hammarström S., Lindgren J. A., Samuelsson B. Leukotrienes promote plasma leakage and leukocyte adhesion in postcapillary venules: in vivo effects with relevance to the acute inflammatory response. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3887–3891. doi: 10.1073/pnas.78.6.3887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Daëron M., Prouvost-Danon A., Voisin G. A. Mast cell membrane antigens and Fc receptors in anaphylaxis. II. Functionally distinct receptors for IgG and for IgE on mouse mast cells. Cell Immunol. 1980 Jan;49(1):178–189. doi: 10.1016/0008-8749(80)90067-2. [DOI] [PubMed] [Google Scholar]
  14. Ebbe S., Phalen E., Stohlman F., Jr Abnormalities of megakaryocytes in W-WV mice. Blood. 1973 Dec;42(6):857–864. [PubMed] [Google Scholar]
  15. Ford-Hutchinson A. W., Bray M. A., Doig M. V., Shipley M. E., Smith M. J. Leukotriene B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes. Nature. 1980 Jul 17;286(5770):264–265. doi: 10.1038/286264a0. [DOI] [PubMed] [Google Scholar]
  16. Fox P. C., Basciano L. K., Siraganian R. P. Mouse mast cell activation and desensitization for immune aggregate-induced histamine release. J Immunol. 1982 Jul;129(1):314–319. [PubMed] [Google Scholar]
  17. Galli S. J., Kitamura Y. Genetically mast-cell-deficient W/Wv and Sl/Sld mice. Their value for the analysis of the roles of mast cells in biologic responses in vivo. Am J Pathol. 1987 Apr;127(1):191–198. [PMC free article] [PubMed] [Google Scholar]
  18. Godfrey H. P., Ilardi C., Engber W., Graziano F. M. Quantitation of human synovial mast cells in rheumatoid arthritis and other rheumatic diseases. Arthritis Rheum. 1984 Aug;27(8):852–856. doi: 10.1002/art.1780270803. [DOI] [PubMed] [Google Scholar]
  19. Hoover R. L., Karnovsky M. J., Austen K. F., Corey E. J., Lewis R. A. Leukotriene B4 action on endothelium mediates augmented neutrophil/endothelial adhesion. Proc Natl Acad Sci U S A. 1984 Apr;81(7):2191–2193. doi: 10.1073/pnas.81.7.2191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jakschik B. A., Rengers T. A., Pinski J. R. Nature of the mast cell-macrophage interaction in immediate hypersensitivity. Adv Prostaglandin Thromboxane Leukot Res. 1987;17A:180–185. [PubMed] [Google Scholar]
  21. Johnson A. R., Hugli T. E., Müller-Eberhard H. J. Release of histamine from rat mast cells by the complement peptides C3a and C5a. Immunology. 1975 Jun;28(6):1067–1080. [PMC free article] [PubMed] [Google Scholar]
  22. Kawanami O., Ferrans V. J., Fulmer J. D., Crystal R. G. Ultrastructure of pulmonary mast cells in patients with fibrotic lung disorders. Lab Invest. 1979 Jun;40(6):717–734. [PubMed] [Google Scholar]
  23. Kitamura Y., Go S., Hatanaka K. Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood. 1978 Aug;52(2):447–452. [PubMed] [Google Scholar]
  24. Klein L. M., Lavker R. M., Matis W. L., Murphy G. F. Degranulation of human mast cells induces an endothelial antigen central to leukocyte adhesion. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8972–8976. doi: 10.1073/pnas.86.22.8972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kuppner M. C., van Meir E., Hamou M. F., de Tribolet N. Cytokine regulation of intercellular adhesion molecule-1 (ICAM-1) expression on human glioblastoma cells. Clin Exp Immunol. 1990 Jul;81(1):142–148. doi: 10.1111/j.1365-2249.1990.tb05305.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Makino H., Ashida Y., Saijo T., Kuriki H., Terao S., Maki Y. Role of leukotrienes in rat reversed passive Arthus pleurisy and the effect of AA-861, a 5-lipoxygenase inhibitor. Int Arch Allergy Appl Immunol. 1986;79(1):38–44. doi: 10.1159/000233939. [DOI] [PubMed] [Google Scholar]
  27. McIntyre T. M., Zimmerman G. A., Prescott S. M. Leukotrienes C4 and D4 stimulate human endothelial cells to synthesize platelet-activating factor and bind neutrophils. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2204–2208. doi: 10.1073/pnas.83.7.2204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nakano T., Sonoda T., Hayashi C., Yamatodani A., Kanayama Y., Yamamura T., Asai H., Yonezawa T., Kitamura Y., Galli S. J. Fate of bone marrow-derived cultured mast cells after intracutaneous, intraperitoneal, and intravenous transfer into genetically mast cell-deficient W/Wv mice. Evidence that cultured mast cells can give rise to both connective tissue type and mucosal mast cells. J Exp Med. 1985 Sep 1;162(3):1025–1043. doi: 10.1084/jem.162.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Plaut M., Pierce J. H., Watson C. J., Hanley-Hyde J., Nordan R. P., Paul W. E. Mast cell lines produce lymphokines in response to cross-linkage of Fc epsilon RI or to calcium ionophores. Nature. 1989 May 4;339(6219):64–67. doi: 10.1038/339064a0. [DOI] [PubMed] [Google Scholar]
  30. Qureshi R., Jakschik B. A. The role of mast cells in thioglycollate-induced inflammation. J Immunol. 1988 Sep 15;141(6):2090–2096. [PubMed] [Google Scholar]
  31. Ramos B. F., Qureshi R., Olsen K. M., Jakschik B. A. The importance of mast cells for the neutrophil influx in immune complex-induced peritonitis in mice. J Immunol. 1990 Sep 15;145(6):1868–1873. [PubMed] [Google Scholar]
  32. Rouzer C. A., Scott W. A., Cohn Z. A., Blackburn P., Manning J. M. Mouse peritoneal macrophages release leukotriene C in response to a phagocytic stimulus. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4928–4932. doi: 10.1073/pnas.77.8.4928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Summers J. B., Gunn B. P., Martin J. G., Mazdiyasni H., Stewart A. O., Young P. R., Goetze A. M., Bouska J. B., Dyer R. D., Brooks D. W. Orally active hydroxamic acid inhibitors of leukotriene biosynthesis. J Med Chem. 1988 Jan;31(1):3–5. doi: 10.1021/jm00396a002. [DOI] [PubMed] [Google Scholar]
  34. Tanaka K., Ueno A., Katori M. Roles of leukotrienes in two rat allergic inflammatory models; IgE-mediated and IgG-antigen complex-induced pleurisies. Prostaglandins. 1986 Jun;31(6):1099–1116. doi: 10.1016/0090-6980(86)90213-3. [DOI] [PubMed] [Google Scholar]
  35. Tharp M. D., Seelig L. L., Jr, Tigelaar R. E., Bergstresser P. R. Conjugated avidin binds to mast cell granules. J Histochem Cytochem. 1985 Jan;33(1):27–32. doi: 10.1177/33.1.2578142. [DOI] [PubMed] [Google Scholar]
  36. Ward P. A., Duque R. E., Sulavik M. C., Johnson K. J. In vitro and in vivo stimulation of rat neutrophils and alveolar macrophages by immune complexes. Production of O-2 and H2O2. Am J Pathol. 1983 Mar;110(3):297–309. [PMC free article] [PubMed] [Google Scholar]
  37. Wei Y. F., Heghinian K., Bell R. L., Jakschik B. A. Contribution of macrophages to immediate hypersensitivity reaction. J Immunol. 1986 Sep 15;137(6):1993–2000. [PubMed] [Google Scholar]
  38. Wei Y. F., Heghinian K., Bell R. L., Jakschik B. A. Contribution of macrophages to immediate hypersensitivity reaction. J Immunol. 1986 Sep 15;137(6):1993–2000. [PubMed] [Google Scholar]
  39. Weichman B. M., Berkenkopf J. W., Cullinan C. A., Sturm R. J. Leukotriene B4 production and pharmacologic regulation of reverse passive Arthus pleurisy: importance of antigen dose. Agents Actions. 1987 Aug;21(3-4):351–354. doi: 10.1007/BF01966513. [DOI] [PubMed] [Google Scholar]
  40. Wershil B. K., Mekori Y. A., Murakami T., Galli S. J. 125I-fibrin deposition in IgE-dependent immediate hypersensitivity reactions in mouse skin. Demonstration of the role of mast cells using genetically mast cell-deficient mice locally reconstituted with cultured mast cells. J Immunol. 1987 Oct 15;139(8):2605–2614. [PubMed] [Google Scholar]
  41. Wershil B. K., Murakami T., Galli S. J. Mast cell-dependent amplification of an immunologically nonspecific inflammatory response. Mast cells are required for the full expression of cutaneous acute inflammation induced by phorbol 12-myristate 13-acetate. J Immunol. 1988 Apr 1;140(7):2356–2360. [PubMed] [Google Scholar]
  42. Yano H., Wershil B. K., Arizono N., Galli S. J. Substance P-induced augmentation of cutaneous vascular permeability and granulocyte infiltration in mice is mast cell dependent. J Clin Invest. 1989 Oct;84(4):1276–1286. doi: 10.1172/JCI114295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Young J. D., Liu C. C., Butler G., Cohn Z. A., Galli S. J. Identification, purification, and characterization of a mast cell-associated cytolytic factor related to tumor necrosis factor. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9175–9179. doi: 10.1073/pnas.84.24.9175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. van den Broek M. F., van den Berg W. B., van de Putte L. B. The role of mast cells in antigen induced arthritis in mice. J Rheumatol. 1988 Apr;15(4):544–551. [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES