Skip to main content
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1993 Dec 1;178(6):1913–1921. doi: 10.1084/jem.178.6.1913

Formation of eosinophilic and monocytic intradermal inflammatory sites in the dog by injection of human RANTES but not human monocyte chemoattractant protein 1, human macrophage inflammatory protein 1 alpha, or human interleukin 8

PMCID: PMC2191290  PMID: 7504053

Abstract

Equilibrium binding studies on canine mononuclear and granulocytic cells allow the identification of a single high affinity receptor for the human C-C chemokine RANTES (dissociation constant, 14 +/- 8 pM), that, in contrast to the human RANTES receptor, has no affinity for human macrophage inflammatory protein 1 alpha (hMIP-1 alpha). A single intradermal injection of hRANTES in dog resulted in eosinophil- and macrophage-rich inflammatory sites within 4 h. Cell infiltration peaked at 16-24 h after hRANTES injection. There was histological evidence of intravascular activation of eosinophils at 4 h, although eosinophils in the vasculature and interstitium contained apparently intact granules. Monocytes were the predominant cells adherent to venular endothelium at 16-24 h. Human MIP-1 alpha elicited no response in canine dermis, whereas monocyte chemoattractant protein 1 caused mild perivascular cuffing with monocytes. In contrast, human interleukin 8 induced a neutrophilic dermal infiltrate that was maximal by 4 h after challenge. This provides the first direct evidence in vivo that RANTES has significant proinflammatory activity and, in addition, could be a mediator in atopic pathologies characterized by eosinophilic and monocytic inflammatory responses.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Arm J. P., Lee T. H. The pathobiology of bronchial asthma. Adv Immunol. 1992;51:323–382. doi: 10.1016/s0065-2776(08)60491-5. [DOI] [PubMed] [Google Scholar]
  2. Ayesh S. K., Azar Y., Babior B. M., Matzner Y. Inactivation of interleukin-8 by the C5a-inactivating protease from serosal fluid. Blood. 1993 Mar 15;81(6):1424–1427. [PubMed] [Google Scholar]
  3. Butcher E. C. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell. 1991 Dec 20;67(6):1033–1036. doi: 10.1016/0092-8674(91)90279-8. [DOI] [PubMed] [Google Scholar]
  4. Corrigan C. J., Kay A. B. T cells and eosinophils in the pathogenesis of asthma. Immunol Today. 1992 Dec;13(12):501–507. doi: 10.1016/0167-5699(92)90026-4. [DOI] [PubMed] [Google Scholar]
  5. Donahue R. E., Seehra J., Metzger M., Lefebvre D., Rock B., Carbone S., Nathan D. G., Garnick M., Sehgal P. K., Laston D. Human IL-3 and GM-CSF act synergistically in stimulating hematopoiesis in primates. Science. 1988 Sep 30;241(4874):1820–1823. doi: 10.1126/science.3051378. [DOI] [PubMed] [Google Scholar]
  6. Dvorak A. M. Ultrastructural evidence for release of major basic protein-containing crystalline cores of eosinophil granules in vivo: cytotoxic potential in Crohn's disease. J Immunol. 1980 Jul;125(1):460–462. [PubMed] [Google Scholar]
  7. Gao J. L., Kuhns D. B., Tiffany H. L., McDermott D., Li X., Francke U., Murphy P. M. Structure and functional expression of the human macrophage inflammatory protein 1 alpha/RANTES receptor. J Exp Med. 1993 May 1;177(5):1421–1427. doi: 10.1084/jem.177.5.1421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gronenborn A. M., Clore G. M. Modeling the three-dimensional structure of the monocyte chemo-attractant and activating protein MCAF/MCP-1 on the basis of the solution structure of interleukin-8. Protein Eng. 1991 Feb;4(3):263–269. doi: 10.1093/protein/4.3.263. [DOI] [PubMed] [Google Scholar]
  9. Henocq E., Vargaftig B. B. Skin eosinophilia in atopic patients. J Allergy Clin Immunol. 1988 Apr;81(4):691–695. doi: 10.1016/0091-6749(88)91040-8. [DOI] [PubMed] [Google Scholar]
  10. Kameyoshi Y., Dörschner A., Mallet A. I., Christophers E., Schröder J. M. Cytokine RANTES released by thrombin-stimulated platelets is a potent attractant for human eosinophils. J Exp Med. 1992 Aug 1;176(2):587–592. doi: 10.1084/jem.176.2.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Neote K., DiGregorio D., Mak J. Y., Horuk R., Schall T. J. Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor. Cell. 1993 Feb 12;72(3):415–425. doi: 10.1016/0092-8674(93)90118-a. [DOI] [PubMed] [Google Scholar]
  12. Nourshargh S., Perkins J. A., Showell H. J., Matsushima K., Williams T. J., Collins P. D. A comparative study of the neutrophil stimulatory activity in vitro and pro-inflammatory properties in vivo of 72 amino acid and 77 amino acid IL-8. J Immunol. 1992 Jan 1;148(1):106–111. [PubMed] [Google Scholar]
  13. Oppenheim J. J., Zachariae C. O., Mukaida N., Matsushima K. Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu Rev Immunol. 1991;9:617–648. doi: 10.1146/annurev.iy.09.040191.003153. [DOI] [PubMed] [Google Scholar]
  14. Rot A., Krieger M., Brunner T., Bischoff S. C., Schall T. J., Dahinden C. A. RANTES and macrophage inflammatory protein 1 alpha induce the migration and activation of normal human eosinophil granulocytes. J Exp Med. 1992 Dec 1;176(6):1489–1495. doi: 10.1084/jem.176.6.1489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Schall T. J., Bacon K., Toy K. J., Goeddel D. V. Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature. 1990 Oct 18;347(6294):669–671. doi: 10.1038/347669a0. [DOI] [PubMed] [Google Scholar]
  16. Schall T. J. Biology of the RANTES/SIS cytokine family. Cytokine. 1991 May;3(3):165–183. doi: 10.1016/1043-4666(91)90013-4. [DOI] [PubMed] [Google Scholar]
  17. Siciliano S. J., Rollins T. E., Springer M. S. Interaction between the C5a receptor and Gi in both the membrane-bound and detergent-solubilized states. J Biol Chem. 1990 Nov 15;265(32):19568–19574. [PubMed] [Google Scholar]
  18. Taub D. D., Conlon K., Lloyd A. R., Oppenheim J. J., Kelvin D. J. Preferential migration of activated CD4+ and CD8+ T cells in response to MIP-1 alpha and MIP-1 beta. Science. 1993 Apr 16;260(5106):355–358. doi: 10.1126/science.7682337. [DOI] [PubMed] [Google Scholar]
  19. Van Riper G., Siciliano S., Fischer P. A., Meurer R., Springer M. S., Rosen H. Characterization and species distribution of high affinity GTP-coupled receptors for human rantes and monocyte chemoattractant protein 1. J Exp Med. 1993 Mar 1;177(3):851–856. doi: 10.1084/jem.177.3.851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Wang J. M., McVicar D. W., Oppenheim J. J., Kelvin D. J. Identification of RANTES receptors on human monocytic cells: competition for binding and desensitization by homologous chemotactic cytokines. J Exp Med. 1993 Mar 1;177(3):699–705. doi: 10.1084/jem.177.3.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Weller P. F., Rand T. H., Goelz S. E., Chi-Rosso G., Lobb R. R. Human eosinophil adherence to vascular endothelium mediated by binding to vascular cell adhesion molecule 1 and endothelial leukocyte adhesion molecule 1. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7430–7433. doi: 10.1073/pnas.88.16.7430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Yamaguchi Y., Hayashi Y., Sugama Y., Miura Y., Kasahara T., Kitamura S., Torisu M., Mita S., Tominaga A., Takatsu K. Highly purified murine interleukin 5 (IL-5) stimulates eosinophil function and prolongs in vitro survival. IL-5 as an eosinophil chemotactic factor. J Exp Med. 1988 May 1;167(5):1737–1742. doi: 10.1084/jem.167.5.1737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Yoshimura T., Yuhki N. Neutrophil attractant/activation protein-1 and monocyte chemoattractant protein-1 in rabbit. cDNA cloning and their expression in spleen cells. J Immunol. 1991 May 15;146(10):3483–3488. [PubMed] [Google Scholar]
  24. Yoshimura T. cDNA cloning of guinea pig monocyte chemoattractant protein-1 and expression of the recombinant protein. J Immunol. 1993 Jun 1;150(11):5025–5032. [PubMed] [Google Scholar]
  25. Zachariae C. O., Anderson A. O., Thompson H. L., Appella E., Mantovani A., Oppenheim J. J., Matsushima K. Properties of monocyte chemotactic and activating factor (MCAF) purified from a human fibrosarcoma cell line. J Exp Med. 1990 Jun 1;171(6):2177–2182. doi: 10.1084/jem.171.6.2177. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES