Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation (original) (raw)

J Exp Med. 1994 Mar 1; 179(3): 881–887.

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Abstract

Eosinophil accumulation is a prominent feature of allergic inflammatory reactions, such as those occurring in the lung of the allergic asthmatic, but the endogenous chemoattractants involved have not been identified. We have investigated this in an established model of allergic inflammation, using in vivo systems both to generate and assay relevant activity. Bronchoalveolar lavage (BAL) fluid was taken from sensitized guinea pigs at intervals after aerosol challenge with ovalbumin. BAL fluid was injected intradermally in unsensitized assay guinea pigs and the accumulation of intravenously injected 111In- eosinophils was measured. Activity was detected at 30 min after allergen challenge, peaking from 3 to 6 h and declining to low levels by 24 h. 3-h BAL fluid was purified using high performance liquid chromatography techniques in conjunction with the skin assay. Microsequencing revealed a novel protein from the C-C branch of the platelet factor 4 superfamily of chemotactic cytokines. The protein, "eotaxin," exhibits homology of 53% with human MCP-1, 44% with guinea pig MCP-1, 31% with human MIP-1 alpha, and 26% with human RANTES. Laser desorption time of flight mass analysis gave four different signals (8.15, 8.38, 8.81, and 9.03 kD), probably reflecting differential O- glycosylation. Eotaxin was highly potent, inducing substantial 111In- eosinophil accumulation at a 1-2 pmol dose in the skin, but did not induce significant 111In-neutrophil accumulation. Eotaxin was a potent stimulator of both guinea pig and human eosinophils in vitro. Human recombinant RANTES, MIP-1 alpha, and MCP-1 were all inactive in inducing 111In-eosinophil accumulation in guinea pig skin; however, evidence was obtained that eotaxin shares a binding site with RANTES on guinea pig eosinophils. This is the first description of a potent eosinophil chemoattractant cytokine generated in vivo and suggests the possibility that similar molecules may be important in the human asthmatic lung.

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De Monchy JG, Kauffman HF, Venge P, Koëter GH, Jansen HM, Sluiter HJ, De Vries K. Bronchoalveolar eosinophilia during allergen-induced late asthmatic reactions. Am Rev Respir Dis. 1985 Mar;131(3):373–376. [PubMed] [Google Scholar]
Bousquet J, Chanez P, Lacoste JY, Barnéon G, Ghavanian N, Enander I, Venge P, Ahlstedt S, Simony-Lafontaine J, Godard P, et al. Eosinophilic inflammation in asthma. N Engl J Med. 1990 Oct 11;323(15):1033–1039. [PubMed] [Google Scholar]
Bradley BL, Azzawi M, Jacobson M, Assoufi B, Collins JV, Irani AM, Schwartz LB, Durham SR, Jeffery PK, Kay AB. Eosinophils, T-lymphocytes, mast cells, neutrophils, and macrophages in bronchial biopsy specimens from atopic subjects with asthma: comparison with biopsy specimens from atopic subjects without asthma and normal control subjects and relationship to bronchial hyperresponsiveness. J Allergy Clin Immunol. 1991 Oct;88(4):661–674. [PubMed] [Google Scholar]
Wegner CD, Gundel RH, Reilly P, Haynes N, Letts LG, Rothlein R. Intercellular adhesion molecule-1 (ICAM-1) in the pathogenesis of asthma. Science. 1990 Jan 26;247(4941):456–459. [PubMed] [Google Scholar]
Dunn CJ, Elliott GA, Oostveen JA, Richards IM. Development of a prolonged eosinophil-rich inflammatory leukocyte infiltration in the guinea-pig asthmatic response to ovalbumin inhalation. Am Rev Respir Dis. 1988 Mar;137(3):541–547. [PubMed] [Google Scholar]
Sanjar S, Aoki S, Kristersson A, Smith D, Morley J. Antigen challenge induces pulmonary airway eosinophil accumulation and airway hyperreactivity in sensitized guinea-pigs: the effect of anti-asthma drugs. Br J Pharmacol. 1990 Apr;99(4):679–686. [PMC free article] [PubMed] [Google Scholar]
Griffiths-Johnson DA, Karol MH. Validation of a non-invasive technique to assess development of airway hyperreactivity in an animal model of immunologic pulmonary hypersensitivity. Toxicology. 1991 Jan;65(3):283–294. [PubMed] [Google Scholar]
Campos MG, Church MK. How useful are guinea-pig models of asthma? Clin Exp Allergy. 1992 Jul;22(7):665–666. [PubMed] [Google Scholar]
Collins PD, Jose PJ, Williams TJ. The sequential generation of neutrophil chemoattractant proteins in acute inflammation in the rabbit in vivo. Relationship between C5a and proteins with the characteristics of IL-8/neutrophil-activating protein 1. J Immunol. 1991 Jan 15;146(2):677–684. [PubMed] [Google Scholar]
Jose PJ, Collins PD, Perkins JA, Beaubien BC, Totty NF, Waterfield MD, Hsuan J, Williams TJ. Identification of a second neutrophil-chemoattractant cytokine generated during an inflammatory reaction in the rabbit peritoneal cavity in vivo. Purification, partial amino acid sequence and structural relationship to melanoma-growth-stimulatory activity. Biochem J. 1991 Sep 1;278(Pt 2):493–497. [PMC free article] [PubMed] [Google Scholar]
Faccioli LH, Nourshargh S, Moqbel R, Williams FM, Sehmi R, Kay AB, Williams TJ. The accumulation of 111In-eosinophils induced by inflammatory mediators, in vivo. Immunology. 1991 Jun;73(2):222–227. [PMC free article] [PubMed] [Google Scholar]
Weg VB, Williams TJ, Lobb RR, Nourshargh S. A monoclonal antibody recognizing very late activation antigen-4 inhibits eosinophil accumulation in vivo. J Exp Med. 1993 Feb 1;177(2):561–566. [PMC free article] [PubMed] [Google Scholar]
Totty NF, Waterfield MD, Hsuan JJ. Accelerated high-sensitivity microsequencing of proteins and peptides using a miniature reaction cartridge. Protein Sci. 1992 Sep;1(9):1215–1224. [PMC free article] [PubMed] [Google Scholar]
Brune DC. Alkylation of cysteine with acrylamide for protein sequence analysis. Anal Biochem. 1992 Dec;207(2):285–290. [PubMed] [Google Scholar]
Darbonne WC, Rice GC, Mohler MA, Apple T, Hébert CA, Valente AJ, Baker JB. Red blood cells are a sink for interleukin 8, a leukocyte chemotaxin. J Clin Invest. 1991 Oct;88(4):1362–1369. [PMC free article] [PubMed] [Google Scholar]
Anwar AR, Moqbel R, Walsh GM, Kay AB, Wardlaw AJ. Adhesion to fibronectin prolongs eosinophil survival. J Exp Med. 1993 Mar 1;177(3):839–843. [PMC free article] [PubMed] [Google Scholar]
Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
Frigas E, Gleich GJ. The eosinophil and the pathophysiology of asthma. J Allergy Clin Immunol. 1986 Apr;77(4):527–537. [PubMed] [Google Scholar]
Yoshimura T, Yuhki N, Moore SK, Appella E, Lerman MI, Leonard EJ. Human monocyte chemoattractant protein-1 (MCP-1). Full-length cDNA cloning, expression in mitogen-stimulated blood mononuclear leukocytes, and sequence similarity to mouse competence gene JE. FEBS Lett. 1989 Feb 27;244(2):487–493. [PubMed] [Google Scholar]
Furutani Y, Nomura H, Notake M, Oyamada Y, Fukui T, Yamada M, Larsen CG, Oppenheim JJ, Matsushima K. Cloning and sequencing of the cDNA for human monocyte chemotactic and activating factor (MCAF). Biochem Biophys Res Commun. 1989 Feb 28;159(1):249–255. [PubMed] [Google Scholar]
Rollins BJ, Morrison ED, Stiles CD. Cloning and expression of JE, a gene inducible by platelet-derived growth factor and whose product has cytokine-like properties. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3738–3742. [PMC free article] [PubMed] [Google Scholar]
Jiang Y, Valente AJ, Williamson MJ, Zhang L, Graves DT. Post-translational modification of a monocyte-specific chemoattractant synthesized by glioma, osteosarcoma, and vascular smooth muscle cells. J Biol Chem. 1990 Oct 25;265(30):18318–18321. [PubMed] [Google Scholar]
Oppenheim JJ, Zachariae CO, Mukaida N, Matsushima K. Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu Rev Immunol. 1991;9:617–648. [PubMed] [Google Scholar]
Van Damme J, Proost P, Lenaerts JP, Opdenakker G. Structural and functional identification of two human, tumor-derived monocyte chemotactic proteins (MCP-2 and MCP-3) belonging to the chemokine family. J Exp Med. 1992 Jul 1;176(1):59–65. [PMC free article] [PubMed] [Google Scholar]
Leonard EJ, Yoshimura T. Human monocyte chemoattractant protein-1 (MCP-1). Immunol Today. 1990 Mar;11(3):97–101. [PubMed] [Google Scholar]
Rot A, Krieger M, Brunner T, Bischoff SC, Schall TJ, Dahinden CA. 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. [PMC free article] [PubMed] [Google Scholar]
Kameyoshi Y, Dörschner A, Mallet AI, Christophers E, Schröder JM. Cytokine RANTES released by thrombin-stimulated platelets is a potent attractant for human eosinophils. J Exp Med. 1992 Aug 1;176(2):587–592. [PMC free article] [PubMed] [Google Scholar]
Alam R, Stafford S, Forsythe P, Harrison R, Faubion D, Lett-Brown MA, Grant JA. RANTES is a chemotactic and activating factor for human eosinophils. J Immunol. 1993 Apr 15;150(8 Pt 1):3442–3448. [PubMed] [Google Scholar]
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]
Kulmburg PA, Huber NE, Scheer BJ, Wrann M, Baumruker T. Immunoglobulin E plus antigen challenge induces a novel intercrine/chemokine in mouse mast cells. J Exp Med. 1992 Dec 1;176(6):1773–1778. [PMC free article] [PubMed] [Google Scholar]
Neote K, DiGregorio D, Mak JY, Horuk R, Schall TJ. Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor. Cell. 1993 Feb 12;72(3):415–425. [PubMed] [Google Scholar]
Sozzani S, Molino M, Locati M, Luini W, Cerletti C, Vecchi A, Mantovani A. Receptor-activated calcium influx in human monocytes exposed to monocyte chemotactic protein-1 and related cytokines. J Immunol. 1993 Feb 15;150(4):1544–1553. [PubMed] [Google Scholar]
Van Riper G, Siciliano S, Fischer PA, Meurer R, Springer MS, 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. [PMC free article] [PubMed] [Google Scholar]
Wang JM, McVicar DW, Oppenheim JJ, Kelvin DJ. 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. [PMC free article] [PubMed] [Google Scholar]
Gao JL, Kuhns DB, Tiffany HL, McDermott D, Li X, Francke U, Murphy PM. Structure and functional expression of the human macrophage inflammatory protein 1 alpha/RANTES receptor. J Exp Med. 1993 May 1;177(5):1421–1427. [PMC free article] [PubMed] [Google Scholar]
Lellouch-Tubiana A, Lefort J, Simon MT, Pfister A, Vargaftig BB. Eosinophil recruitment into guinea pig lungs after PAF-acether and allergen administration. Modulation by prostacyclin, platelet depletion, and selective antagonists. Am Rev Respir Dis. 1988 Apr;137(4):948–954. [PubMed] [Google Scholar]
Coyle AJ, Page CP, Atkinson L, Flanagan R, Metzger WJ. The requirement for platelets in allergen-induced late asthmatic airway obstruction. Eosinophil infiltration and heightened airway responsiveness in allergic rabbits. Am Rev Respir Dis. 1990 Sep;142(3):587–593. [PubMed] [Google Scholar]
e Silva PM, Martins MA, Faria Neto HC, Cordeiro RS, Vargaftig BB. Generation of an eosinophilotactic activity in the pleural cavity of platelet-activating factor-injected rats. J Pharmacol Exp Ther. 1991 Jun;257(3):1039–1044. [PubMed] [Google Scholar]
Cochran BH, Reffel AC, Stiles CD. Molecular cloning of gene sequences regulated by platelet-derived growth factor. Cell. 1983 Jul;33(3):939–947. [PubMed] [Google Scholar]

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