Production of the novel C-C chemokine MCP-4 by airway cells and comparison of its biological activity to other C-C chemokines

Journal of Clinical Investigation

Volumn 99, Issue 5, 1997, Pages 926-936

  Stellato, Cristiana ^d   Collins, Paul ^a   Ponath, Paul D ^b   Soler, Dulce ^b   Newman, Walter ^b   La Rosa, Greg ^b   Li, Haodong ^c   White, John ^e   Schwiebert, Lisa M ^d   Bickel, Carol ^d   Liu, Mark ^d   Bochner, Bruce S ^d   Williams, Timothy ^a   Schleimer, Robert P ^d  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b MILLENNIUM PHARMACEUTICALS INC   (United States)

^c GLAXOSMITHKLINE   (United States)

^d JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

^e GLAXOSMITHKLINE   (United Kingdom)

Author keywords

allergy; chemokines; eosinophils; glucocorticoids; inflammation

Indexed keywords

BUDESONIDE; CALCIUM ION; CHEMOKINE RECEPTOR; HISTAMINE; INTERLEUKIN 3; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 3;

ANIMAL CELL; ARTICLE; ASTHMA; BASOPHIL; CALCIUM CELL LEVEL; CELL MIGRATION; CHEMOTAXIS; CONTROLLED STUDY; DESENSITIZATION; EOSINOPHIL; HISTAMINE RELEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG LAVAGE; LYMPHOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM;

EID: 17544401008     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119257     Document Type: Article

References (68)

1. Weller, P.F. 1991. The immunobiology of eosinophils. N. Engl. J. Med. 324:1110-1118.
2. Sur, S., C.R. Adolphson, and G.J. Gleich. 1993. Eosinophils: biochemical and cellular aspects. In Allergy Principles and Practice. 4th Ed. E. Middleton, C.E. Reed, E.F. Ellis, J.N.F. Adkinson, J.W. Yunginger, and W. Busse, editors. Mosby, St. Louis, MO. 169-200.
3. Bochner, B.S., and R.P. Schleimer. 1994. The role of adhesion molecules in human eosinophil and basophil recruitment. J. Allergy Clin. Immunol. 94: 427-438.
4. Bochner, B.S., F.W. Luscinskas, M.A. Gimbrone, Jr., W. Newman, S.A. Sterbinsky, C. Derse-Anthony, D. Klunk, and R.P. Schleimer. 1991. Adhesion of human basophils, eosinophils, and neutrophils to IL-1-activaled human vascular endothelial cells. Contributions of endothelial cell adhesion molecules. J. Exp. Med. 173:1553-1557.
5. Weller, P.F., T.H. Rand, S.E. Goelz, G. Chi-Rosso, and R.R. Lobb. 1991. 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. USA. 88:7430-7433.
6. Dobrina, A., R. Menegazzi, T.M. Carlos, E. Nardon, R. Cramer, T. Zacchi, J.M. Harlan, and P. Patriarca. 1991. Mechanisms of eosinophil adherence to cultured vascular endothelial cells. Eosinophils bind to the cytokine-induced endothelial ligand vascular cell adhesion molecule-1 via the very late activation antigen-4 integrin receptor. J. Clin. Invest. 88:20-26.
7. Bochner, B.S., D.A. Klunk, S.A. Sterbinsky, R.L. Coffman, and R.P. Schleimer. 1995. Interleukin-13 selectively induces vascular cell adhesion molecule-1 (VCAM-1) expression in human endothelial cells. J. Immunol. 154:799-803.
8. Fujisawa, T., R. Abu-Ghazaleh, H. Kita, C.J. Sanderson, and G.J. Gleich. 1990. Regulatory effect of cytokines on eosinophil degranulation. J. Immunol. 144:642-646.
9. Sehmi, R., A.J. Wardlaw, O. Cromwell, K. Kurihara, P. Waltmann, and A.B. Kay. 1992. Interleukin-5 selectively enhances the chemotactic response of eosinophils obtained from normal but not eosinophilic subjects. Blood. 79: 2952-2959.
10. Ebisawa, M., M.C. Liu, T. Yamada, M. Kato, L.M. Lichtenstein, B.S. Bochner, and R.P. Schleimer. 1994. Eosinophil transendothelial migration induced by cytokines. II. The potentiation of eosinophil transendothelial migration by eosinophil-active cytokines. J. Immunol. 152:4590-4597.
11. Walsh, G.M., A. Hartnell, A.J. Wardlaw, K. Kurihara, C.J. Sanderson, and A.B. Kay. 1990. IL-5 enhances the in vitro adhesion of human eosinophils. but not neutrophils, in a leukocyte integrin (CD11/18)-dependent manner. Immunology. 71:258-265.
12. Oppenheim, J.J., C.O.C. Zachariae, N. Mukaida, and K. Matsushima. 1991. Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu. Rev. Immunol. 9:617-648.
13. Schall, T.J. 1991. Biology of the RANTES/SIS cytokine family. Cytokine. 3:165-183.
14. Baggiolini, M., and C.A. Dahinden. 1994. CC chemokines in allergic inflammation. Immunol. Today. 15:127-133.
15. Taub, D.D., and J.J. Oppenheim. 1994. Chemokines, inflammation and the immune system. Ther. Immunol. 1:229-246.
16. Ponath, P.D., S. Qin, D.J. Ringler, I. Clark-Lewis, J. Wang, N. Kassam, H. Smith, J.-A. Bonzalo, W. Newman, J.-C. Gutierrez-Ramos, and C.R. MacKay. 1996. Cloning of the human eosinophil chemoattractant, eotaxin. Expression, receptor binding and function properties provide a mechanism for the selective recruitment of eosinophils. J. Clin. Invest. 97:604-612.
17. Garcia-Zepeda, E.A., M.E. Rothenberg, R.T. Ownbey, J. Celestin, P. Leder, and A. Luster. 1996. Human eotaxin is a specific chemoattractant for eosinophil cells and provides new mechanism to explain tissue eosinophilia. Nat. Med. 4:449-456.
18. Kameyoshi, Y., A. Dorschner, A.I. Mallet, E. Christophers, and J.M. Schroder. 1992. Cytokine RANTES released by thrombin-stimulated platelets is a potent attractant for human eosinophils. J. Exp. Med. 176:587-592.
19. Dahinden, C.A., T. Geiser, T. Brunner, V. von Tscharner, D. Caput, P. Ferrara, A. Minty, and M. Baggiolini. 1994. Monocyte chemotactic protein 3 is a most effective basophil-and eosinophil-activating chemokine. J. Exp. Med. 179:751-756.
20. Jose, P.J., D.A. Griffiths-Johnson, P.D. Collins, D.T. Walsh, R. Moqbel, N.F. Totty, O. Truong, J.J. Hsuan, and T.J. Williams. 1994. Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. J. Exp. Med. 179:881-887.
21. Rot, A., M. Krieger, T. Brunner, S.C. Bischoff, T.J. Schall, and C.A. Dahinden. 1992. RANTES and macrophage inflammatory protein 1α induce the migration and activation of normal human eosinophil granulocytes. J. Exp. Med. 176:1489-1495.
22. Bischoff, S.C., M. Krieger, T. Brunner, A. Rot, V. Vontscharner, M. Baggiolini, and C.A. Dahinden. 1993. RANTES and related chemokines activate human basophil granulocytes through different G-protein-coupled receptors. Eur. J. Immunol. 23:761-767.
23. Ying, S., L. Taborda-Barata, Q. Meng, M. Humbert, and A.B. Kay. 1995. The kinetics of allergen-induced transcription of messenger RNA for monocyte chemotactic protein-3 and RANTES in the skin of human atopic subjects. Relationship to eosinophil, T cell, and macrophage recruitment. J. Exp. Med. 181:2153-2159.
24. Rothenberg, M.E., A.D. Luster, C.M. Lilly, J.M. Drazen, and P. Leder. 1995. Constitutive and allergen-induced expression of eotaxin mRNA in the guinea pig lung. J. Exp. Med. 181:1211-1216.
25. Jose, P.J., I.M. Adcock, D.A. Giffiths-Johnson, N. Berkman, T.N. Wells, T.J. Williams, and C.A. Power. 1994. Eotaxin: cloning of an eosinophil chemoattractant cytokine and increased mRNA expression in allergen-challenge guinea pig lungs. Biochem. Biophys. Res. Commun. 205:788-794.
26. Teran, L.M., N. Noso, M. Carroll, D.E. Davies, S. Holgate, and J.-M. Schröder. 1996. Eosinophil recruitment following allergen challenge is associated with the release of the chemokine RANTES into asthmatic airways. J. Immunol. 157:1806-1812.
27. Meurer, R., G. Van Riper, W. Feeney, P. Cunningham, D. Hora, Jr., M.S. Springer, D.E. MacIntyre, and H. Rosen. 1993. 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 1α, or human interleukin 8. J. Exp. Med. 178: 1913-1921.
28. Beck, L., C. Bickel, S. Sterbinsky, C. Stellato, R. Hamilton, H. Rosen, B. Bochner, and R. Schleimer. 1995. Injection of human subjects with RANTES causes dermal infiltration of eosinophils (EOS) and mononuclear cells (MNC). FASEB (Fed. Am. Soc. Exp. Biol.) J. 9:804a. (Abstr.)
29. Griffiths-Johnson, D.A., P.D. Collins, A.G. Rossi, P.J. Jose, and T.J. Williams. 1993. The chemokine, eotaxin, activates guinea-pig eosinophils in vitro and causes their accumulation into the lung in vivo. Biochem. Biophys. Res. Commun. 197:1167-1172.
30. Collins, P.D., S. Marleau, D.A. Griffiths-Johnson, P.J. Jose, and T.J. Williams. 1995. Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J. Exp. Med. 182:1169-1174.
31. Murphy, P.M. 1996. Chemokine receptors: structure, function and role in microbial pathogenesis. Cytokine and Growth Factors Reviews. 7:47-58.
32. Mackay, C.R. 1996. Chemokine receptors and T cell chemotaxis. J. Exp. Med. 184:799-802.
33. Neote, K., D. DiGregorio, J.Y. Mak, R. Horuk, and T.J. Schall. 1993. Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor. Cell. 72:415-425.
34. Combadiere, C., S.K. Ahuja, and P.M. Murphy. 1995. Cloning and functional expression of a human eosinophil CC chemokine receptor. J. Biol. Chem. 270:16491-16494.
35. Power, C.A., A. Meyer, K. Nemeth, K.B. Bacon, A.J. Hoogewerf, A.E. Proudfoot, and T.N. Wells. 1995. Molecular cloning and functional expression of a novel CC chemokine receptor cDNA from a human basophilic cell line. J. Biol. Chem. 270:19495-19500.
36. Chaudhuri, A., V. Zbrzezna, J. Polyakova, A.O. Pogo, J. Hesselgesser, and R. Horuk. 1994. Expression of the Duffy antigen in K562 cells. Evidence that it is the human erythrocyte chemokine receptor. J. Biol. Chem. 269:7835-7838.
37. Ponath, P.D., S. Qin, T.W. Post, J. Wang, L. Wu, N.P. Gerard, W. Neuman, C. Gerard, and C. R. Mackay. 1996. Molecular cloning and characterization of a human eotaxin receptor expressed selectively on eosinophils. J. Exp. Med. 183:2437-2448.
38. Combadiere, C., S. Ahuja, H.L. Tiffany, and P.M. Murphy. 1996. Cloning and functional expression of CC CKR5, a human monocyte CC chemokine receptor selective for MIP-1α, MIP-1β, and RANTES. J. Leuk. Biol. 60:147-152.
39. Peiper, S.C., Z.X. Wang, K. Neote, A.W. Martin, H.J. Showell, M.J. Conklyn, K. Ogborne, T.J. Hadley, Z.H. Lu, and J. Hesselgesser. 1995. The duffy antigen/receptor for chemokines (DARC) is expressed in endothelial cells of Duffy negative individuals who lack the erythrocyte receptor. J. Exp. Med. 181:1311-1317.
40. Hadley, T.J., Z. Lu, K. Wasniowska, A.W. Martin, S.C. Peiper, J. Hesselgesser, and R. Horuk. 1994. Postcapillary venule endothelial cells in kidney express a multispecific chemokine receptor that is structurally and functionally identical to the erythroid isoform, which is the duffy blood group antigen. J. Clin. Invest. 94:985-991.
41. Neote, K., J.Y. Mak, L.F. Kolakowski, and T.J. Schall. 1994. Functional and biochemical analysis of the cloned Duffy antigen: identity with the red blood cell chemokine receptor. Blood. 84:44-52.
42. Stellato, C., L. Beck, L. Schweibert, H. Li, J. White, and R.P. Schleimer. 1996. A novel C-C chemokine. CKβ10, is expressed in airway epithelial cells and is a potent eosinophil chemoattractant. J. Allergy Clin. Immunol. 97:304.
43. Uguccioni, M., P. Loetscher, U. Forssmann, B. Dewald, H. Li, S.H. Lima, H. Li, B. Kreider, G. Barotta, M. Thelen, and M. Baggiolini. 1996. Monocyte chemotactic protein 4 (MCP-4), a novel structural and functional analogue of MCP-3 and eotaxin. J. Exp. Med 183:2379-2384.
44. Clark-Lewis, I., B. Moser, A. Walz, M. Baggiolini, G.J. Scott, and R. Aebersold. 1991. Chemical synthesis, purification, and characterization of two inflammatory proteins, neutrophil activating peptide 1 (interleukin 8) and neutrophil activating peptide. Biochemistry. 30:3128-3135.
45. Reddel, R.R., Y. Ke, B.I. Gerwin, M.G. McMenamin, J.F. Lechner, R. T. Su, D.E. Brash, P.-B. Park, J.S. Rhim, and C.C. Harris. 1988. Transformation of human bronchial epithelial cells by infection with SV40 or adenovirus-12 SV4-hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes. Cancer Res. 48:1904-1909.
46. Zeitlin, P.L., L. Lu, J. Rhim, G. Cutting, G. Stretten, K.A. Keiffer, R. Craig, and W.B. Guggino. 1991. A cystic fibrosis bronchial epithelial cell line: immortalization by adenovirus 12-SV40 infection. Am. J. Respir. Cell Mol. Biol. 4:313-317.
47. 2, and other bronchoconstricting substances in the airways of mild asthmatic subjects. Am. Rev. Respir. Dis. 142: 126-132.
48. Warner, J.A., A. Reshef, and D.W. MacGlashan, Jr. 1987. A rapid Percoll technique for the purification of basophils. J. Immunol. Methods. 105:107-110.
49. Gilbert, H.S., and L. Ornstein. 1975. Basophil counting with a new staining method using Alcian blue. Blood. 46:279-286.
50. Hansel, T.T., I.J.M.D. Vries, T. Iff, S. Rihs, M. Wandzilak, S. Betz, K. Blaser, and C. Walker. 1991. An improved immunomagnetic procedure for the isolation of highly purified human blood eosinophils. J. Immunol. Methods. 145: 105-110.
51. Schleimer, R.P., and B.K. Rutledge. 1986. Cultured human vascular endothelial cells acquire adhesiveness for leukocytes following stimulation with interleukin-1, endotoxin, and tumor-promoting phorbol esters. J. Immunol. 136:649-654.
52. Schleimer, R.P., S.A. Sterbinsky, J. Kaiser, C.A. Bickel, D.A. Klunk, K. Tomioka, W. Newman, F.W. Luscinskas, M.A. Gimbrone, Jr., B.W. McIntyre, and B.S. Bochner. 1992. Interleukin-4 induces adherence of human eosinophils and basophils but not neutrophils to endothelium: association with expression of VCAM-1. J. Immunol. 148:1086-1092.
53. Schleimer, R.P., H.S. Freeland, S.P. Peters, K.E. Brown, and C.P. Derse. 1989. An assessment of the effects of glucocorticoids on degranulation, chemotaxis, binding to vascular endothelial cells and formation of leukotriene B4 by purified human neutrophils. J. Pharmacol. Exp. Ther. 250:598-605.
54. Lichtenstein, L.M., and A.G. Osler. 1964. Studies on the mechanisms of hypersensitivity phenomena. J. Exp. Med. 120:507-530.
55. Siraganian, R.P. 1974. An automated continuous-flow system for the extraction and fluorometric analysis of histamine. Anal. Biochem. 57:383-391.
56. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
57. Saiki, R.K., T.L. Bugawan, G.T. Horn, K.B. Mullis, and H.A. Erlich. 1986. Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes. Nature (Lond.). 324:163-166.
58. Sanger, F., S. Nieklen, and A.R. Couson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5463-5469.
59. Schuler, G.D., M.S. Boguski, E.A. Stewart, L.D. Stein, G. Gyapay, K. Rice, R.E. White, P. Rodriguez-Tomé, A. Aggarwal, E. Bajorek, et al. 1996. A gene map of the human genome. Science (Wash. DC). 274:540-546.
60. Charo, I.F., S.J. Myers, A. Herman, C. Franci, A.J. Connolly, and S.R. Coughlin. 1994. Molecular cloning and functional expression of two monocyte chemoattractant protein 1 receptors reveals alternative splicing of the carboxyterminal tails. Proc. Natl. Acad. Sci. USA. 91:2752-2758.
61. Franci, C., L.M. Wong, J. Van Damme, P. Proost, and I.F. Charo. 1995. Monocyte chemoattractant protein-3, but not monocyte chemoattractant protein-2, is a functional ligand of the human monocyte chemoattractant protein-1 receptor. J. Immunol. 154:6511-6517.
62. Myers, S.J., L.M. Wong, and I.F. Charo. 1995. Signal transduction and ligand specificity of the human MCP-1 (monocyte chemoattractant protein-1) receptor in transfected embryonic kidney cells. J. Biol. Chem. 270:5786-5791.
63. Nakamura, H., K. Yoshimura, H.A. Jaffe, and R.G. Crystal. 1991. Interleukin-8 gene expression in human bronchial epithelial cells. J. Biol. Chem. 266: 19611-19617.
64. Becker, S., J. Quay, H.S. Koren, and J.S. Haskill. 1994. Constitutive and stimulated MCP-1, GRO alpha, beta, and gamma expression in human airway epithelium and bronchoalveolar macrophages. Am. J. Physiol. 266:L278-L286.
65. Kwon, O.J., P.J. Jose, R.A. Robbins, T.J. Schall, T.J. Williams, and P.J. Barnes. 1996. Glucocorticoid inhibition of RANTES expression in human lung epithelial cells. Am. J. Respir. Cell. Mol. Biol. 12:488-496.
66. Stellato, C., L.A. Beck, G.A. Gorgone, D. Proud, T.J. Schall, S.J. Ono, L.M. Lichtenstein, and R.P. Schleimer. 1995. Expression of the chemokine RANTES by a human bronchial epithelial cell line: modulation by cytokines and glucocorticoids. J. Immunol. 155:410-418.
67. Wolpe, S.D., G. Davatelis, B. Sherry, B. Beutler, D.G. Hesse, H.T. Nguyen, L.L. Moldawer, C.F. Nathan, S.F. Lowry, and A. Cerami. 1988. Macrophages secrete a novel heparin-binding protein with inflammatory and neutrophil chemokinetic properties. J. Exp. Med. 167:570-581.
68. Schwiebert, L.M., L.A. Beck, C. Stellato, C.A. Bickel, B.S. Bochner, and R.P. Schleimer. 1996. Glucocorticosteroid inhibition of cytokine production: relevance to antiallergic actions. J. Allergy Clin. Immunol. 97:143-152.