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. 1997 Mar 1;99(5):926–936. doi: 10.1172/JCI119257

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

C Stellato 1, P Collins 1, P D Ponath 1, D Soler 1, W Newman 1, G La Rosa 1, H Li 1, J White 1, L M Schwiebert 1, C Bickel 1, M Liu 1, B S Bochner 1, T Williams 1, R P Schleimer 1
PMCID: PMC507900  PMID: 9062350

Abstract

Monocyte chemotactic protein-4 (MCP-4) is a newly identified C-C chemokine with potent eosinophil chemoattractant properties. We describe studies of its biological activity in vitro to induce chemotaxis of peripheral blood eosinophils and to induce histamine release from IL-3-primed peripheral blood basophils. MCP-4 and eotaxin caused a similar rise in eosinophil intracytoplasmic Ca2+ and complete cross-desensitization. MCP-4 also abolished the eosinophil Ca2+ response to MCP-3 and partially desensitized the response to macrophage inflammatory protein-1alpha. MCP-4 activated cell migration via either CCR2b or CCR3 in mouse lymphoma cells transfected with these chemokine receptors. MCP-4 inhibited binding of 125I-eotaxin to eosinophils and CCR3-transfected cells and inhibited 125I-MCP-1 binding to CCR2b-transfectants. MCP-4 mRNA was found in cells collected in bronchoalveolar lavage of asthmatic and nonasthmatic subjects and was prominently expressed in human lung and heart. MCP-4 mRNA was expressed in several human bronchial epithelial cell lines after cytokine stimulation. Pretreatment of BEAS-2B epithelial cells with the glucocorticoid budesonide inhibited MCP-4 mRNA expression. These features make MCP-4 a candidate for playing a role in eosinophil recruitment during allergic respiratory diseases.

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Selected References

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  1. Baggiolini M., Dahinden C. A. CC chemokines in allergic inflammation. Immunol Today. 1994 Mar;15(3):127–133. doi: 10.1016/0167-5699(94)90156-2. [DOI] [PubMed] [Google Scholar]
  2. Becker S., Quay J., Koren H. S., Haskill J. S. Constitutive and stimulated MCP-1, GRO alpha, beta, and gamma expression in human airway epithelium and bronchoalveolar macrophages. Am J Physiol. 1994 Mar;266(3 Pt 1):L278–L286. doi: 10.1152/ajplung.1994.266.3.L278. [DOI] [PubMed] [Google Scholar]
  3. Bischoff S. C., Krieger M., Brunner T., Rot A., von Tscharner V., Baggiolini M., Dahinden C. A. RANTES and related chemokines activate human basophil granulocytes through different G protein-coupled receptors. Eur J Immunol. 1993 Mar;23(3):761–767. doi: 10.1002/eji.1830230329. [DOI] [PubMed] [Google Scholar]
  4. Bochner B. S., Klunk D. A., Sterbinsky S. A., Coffman R. L., Schleimer R. P. IL-13 selectively induces vascular cell adhesion molecule-1 expression in human endothelial cells. J Immunol. 1995 Jan 15;154(2):799–803. [PubMed] [Google Scholar]
  5. Bochner B. S., Luscinskas F. W., Gimbrone M. A., Jr, Newman W., Sterbinsky S. A., Derse-Anthony C. P., Klunk D., Schleimer R. P. Adhesion of human basophils, eosinophils, and neutrophils to interleukin 1-activated human vascular endothelial cells: contributions of endothelial cell adhesion molecules. J Exp Med. 1991 Jun 1;173(6):1553–1557. doi: 10.1084/jem.173.6.1553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bochner B. S., Schleimer R. P. The role of adhesion molecules in human eosinophil and basophil recruitment. J Allergy Clin Immunol. 1994 Sep;94(3 Pt 1):427–439. doi: 10.1016/0091-6749(94)90195-3. [DOI] [PubMed] [Google Scholar]
  7. Charo I. F., Myers S. J., Herman A., Franci C., Connolly A. J., Coughlin S. R. Molecular cloning and functional expression of two monocyte chemoattractant protein 1 receptors reveals alternative splicing of the carboxyl-terminal tails. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2752–2756. doi: 10.1073/pnas.91.7.2752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chaudhuri A., Zbrzezna V., Polyakova J., Pogo A. O., Hesselgesser J., Horuk R. Expression of the Duffy antigen in K562 cells. Evidence that it is the human erythrocyte chemokine receptor. J Biol Chem. 1994 Mar 18;269(11):7835–7838. [PubMed] [Google Scholar]
  9. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  10. Clark-Lewis I., Moser B., Walz A., Baggiolini M., Scott G. J., Aebersold R. Chemical synthesis, purification, and characterization of two inflammatory proteins, neutrophil activating peptide 1 (interleukin-8) and neutrophil activating peptide. Biochemistry. 1991 Mar 26;30(12):3128–3135. doi: 10.1021/bi00226a021. [DOI] [PubMed] [Google Scholar]
  11. Collins P. D., Marleau S., Griffiths-Johnson D. A., Jose P. J., Williams T. J. Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J Exp Med. 1995 Oct 1;182(4):1169–1174. doi: 10.1084/jem.182.4.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Combadiere C., Ahuja S. K., Murphy P. M. Cloning and functional expression of a human eosinophil CC chemokine receptor. J Biol Chem. 1995 Jul 14;270(28):16491–16494. doi: 10.1074/jbc.270.28.16491. [DOI] [PubMed] [Google Scholar]
  13. Combadiere C., Ahuja S. K., Tiffany H. L., Murphy P. M. Cloning and functional expression of CC CKR5, a human monocyte CC chemokine receptor selective for MIP-1(alpha), MIP-1(beta), and RANTES. J Leukoc Biol. 1996 Jul;60(1):147–152. doi: 10.1002/jlb.60.1.147. [DOI] [PubMed] [Google Scholar]
  14. Dahinden C. A., Geiser T., Brunner T., von Tscharner V., Caput D., Ferrara P., Minty A., Baggiolini M. Monocyte chemotactic protein 3 is a most effective basophil- and eosinophil-activating chemokine. J Exp Med. 1994 Feb 1;179(2):751–756. doi: 10.1084/jem.179.2.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dobrina A., Menegazzi R., Carlos T. M., Nardon E., Cramer R., Zacchi T., Harlan J. M., Patriarca P. Mechanisms of eosinophil adherence to cultured vascular endothelial cells. Eosinophils bind to the cytokine-induced ligand vascular cell adhesion molecule-1 via the very late activation antigen-4 integrin receptor. J Clin Invest. 1991 Jul;88(1):20–26. doi: 10.1172/JCI115278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ebisawa M., Liu M. C., Yamada T., Kato M., Lichtenstein L. M., Bochner B. S., Schleimer R. P. Eosinophil transendothelial migration induced by cytokines. II. Potentiation of eosinophil transendothelial migration by eosinophil-active cytokines. J Immunol. 1994 May 1;152(9):4590–4596. [PubMed] [Google Scholar]
  17. Franci C., Wong L. M., Van Damme J., Proost P., Charo I. F. Monocyte chemoattractant protein-3, but not monocyte chemoattractant protein-2, is a functional ligand of the human monocyte chemoattractant protein-1 receptor. J Immunol. 1995 Jun 15;154(12):6511–6517. [PubMed] [Google Scholar]
  18. Fujisawa T., Abu-Ghazaleh R., Kita H., Sanderson C. J., Gleich G. J. Regulatory effect of cytokines on eosinophil degranulation. J Immunol. 1990 Jan 15;144(2):642–646. [PubMed] [Google Scholar]
  19. Garcia-Zepeda E. A., Rothenberg M. E., Ownbey R. T., Celestin J., Leder P., Luster A. D. Human eotaxin is a specific chemoattractant for eosinophil cells and provides a new mechanism to explain tissue eosinophilia. Nat Med. 1996 Apr;2(4):449–456. doi: 10.1038/nm0496-449. [DOI] [PubMed] [Google Scholar]
  20. Gilbert H. S., Ornstein L. Basophil counting with a new staining method using alcian blue. Blood. 1975 Aug;46(2):279–286. [PubMed] [Google Scholar]
  21. Griffiths-Johnson D. A., Collins P. D., Rossi A. G., Jose P. J., Williams T. J. The chemokine, eotaxin, activates guinea-pig eosinophils in vitro and causes their accumulation into the lung in vivo. Biochem Biophys Res Commun. 1993 Dec 30;197(3):1167–1172. doi: 10.1006/bbrc.1993.2599. [DOI] [PubMed] [Google Scholar]
  22. Hadley T. J., Lu Z. H., Wasniowska K., Martin A. W., Peiper S. C., Hesselgesser J., Horuk R. 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. 1994 Sep;94(3):985–991. doi: 10.1172/JCI117465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hansel T. T., De Vries I. J., Iff T., Rihs S., Wandzilak M., Betz S., Blaser K., Walker C. An improved immunomagnetic procedure for the isolation of highly purified human blood eosinophils. J Immunol Methods. 1991 Dec 15;145(1-2):105–110. doi: 10.1016/0022-1759(91)90315-7. [DOI] [PubMed] [Google Scholar]
  24. Jose P. J., Adcock I. M., Griffiths-Johnson D. A., Berkman N., Wells T. N., Williams T. J., Power C. A. Eotaxin: cloning of an eosinophil chemoattractant cytokine and increased mRNA expression in allergen-challenged guinea-pig lungs. Biochem Biophys Res Commun. 1994 Nov 30;205(1):788–794. doi: 10.1006/bbrc.1994.2734. [DOI] [PubMed] [Google Scholar]
  25. Jose P. J., Griffiths-Johnson D. A., Collins P. D., Walsh D. T., Moqbel R., Totty N. F., Truong O., Hsuan J. J., Williams T. J. Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. J Exp Med. 1994 Mar 1;179(3):881–887. doi: 10.1084/jem.179.3.881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Kwon O. J., Jose P. J., Robbins R. A., Schall T. J., Williams T. J., Barnes P. J. Glucocorticoid inhibition of RANTES expression in human lung epithelial cells. Am J Respir Cell Mol Biol. 1995 May;12(5):488–496. doi: 10.1165/ajrcmb.12.5.7537968. [DOI] [PubMed] [Google Scholar]
  28. LICHTENSTEIN L. M., OSLER A. G. STUDIES ON THE MECHANISMS OF HYPERSENSITIVITY PHENOMENA. IX. HISTAMINE RELEASE FROM HUMAN LEUKOCYTES BY RAGWEED POLLEN ANTIGEN. J Exp Med. 1964 Oct 1;120:507–530. doi: 10.1084/jem.120.4.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Liu M. C., Bleecker E. R., Lichtenstein L. M., Kagey-Sobotka A., Niv Y., McLemore T. L., Permutt S., Proud D., Hubbard W. C. Evidence for elevated levels of histamine, prostaglandin D2, and other bronchoconstricting prostaglandins in the airways of subjects with mild asthma. Am Rev Respir Dis. 1990 Jul;142(1):126–132. doi: 10.1164/ajrccm/142.1.126. [DOI] [PubMed] [Google Scholar]
  30. Mackay C. R. Chemokine receptors and T cell chemotaxis. J Exp Med. 1996 Sep 1;184(3):799–802. doi: 10.1084/jem.184.3.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Meurer R., Van Riper G., Feeney W., Cunningham P., Hora D., Jr, Springer M. S., MacIntyre D. E., Rosen H. 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. J Exp Med. 1993 Dec 1;178(6):1913–1921. doi: 10.1084/jem.178.6.1913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Murphy P. M. Chemokine receptors: structure, function and role in microbial pathogenesis. Cytokine Growth Factor Rev. 1996 Jun;7(1):47–64. doi: 10.1016/1359-6101(96)00009-3. [DOI] [PubMed] [Google Scholar]
  33. Myers S. J., Wong L. M., Charo I. F. Signal transduction and ligand specificity of the human monocyte chemoattractant protein-1 receptor in transfected embryonic kidney cells. J Biol Chem. 1995 Mar 17;270(11):5786–5792. doi: 10.1074/jbc.270.11.5786. [DOI] [PubMed] [Google Scholar]
  34. Nakamura H., Yoshimura K., Jaffe H. A., Crystal R. G. Interleukin-8 gene expression in human bronchial epithelial cells. J Biol Chem. 1991 Oct 15;266(29):19611–19617. [PubMed] [Google Scholar]
  35. 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]
  36. Neote K., Mak J. Y., Kolakowski L. F., Jr, Schall T. J. Functional and biochemical analysis of the cloned Duffy antigen: identity with the red blood cell chemokine receptor. Blood. 1994 Jul 1;84(1):44–52. [PubMed] [Google Scholar]
  37. 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]
  38. Peiper S. C., Wang Z. X., Neote K., Martin A. W., Showell H. J., Conklyn M. J., Ogborne K., Hadley T. J., Lu Z. H., Hesselgesser J. The Duffy antigen/receptor for chemokines (DARC) is expressed in endothelial cells of Duffy negative individuals who lack the erythrocyte receptor. J Exp Med. 1995 Apr 1;181(4):1311–1317. doi: 10.1084/jem.181.4.1311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ponath P. D., Qin S., Post T. W., Wang J., Wu L., Gerard N. P., Newman W., Gerard C., Mackay C. R. Molecular cloning and characterization of a human eotaxin receptor expressed selectively on eosinophils. J Exp Med. 1996 Jun 1;183(6):2437–2448. doi: 10.1084/jem.183.6.2437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Ponath P. D., Qin S., Ringler D. J., Clark-Lewis I., Wang J., Kassam N., Smith H., Shi X., Gonzalo J. A., Newman W. Cloning of the human eosinophil chemoattractant, eotaxin. Expression, receptor binding, and functional properties suggest a mechanism for the selective recruitment of eosinophils. J Clin Invest. 1996 Feb 1;97(3):604–612. doi: 10.1172/JCI118456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Power C. A., Meyer A., Nemeth K., Bacon K. B., Hoogewerf A. J., Proudfoot A. E., Wells T. N. Molecular cloning and functional expression of a novel CC chemokine receptor cDNA from a human basophilic cell line. J Biol Chem. 1995 Aug 18;270(33):19495–19500. doi: 10.1074/jbc.270.33.19495. [DOI] [PubMed] [Google Scholar]
  42. Reddel R. R., Ke Y., Gerwin B. I., McMenamin M. G., Lechner J. F., Su R. T., Brash D. E., Park J. B., Rhim J. S., Harris C. C. Transformation of human bronchial epithelial cells by infection with SV40 or adenovirus-12 SV40 hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes. Cancer Res. 1988 Apr 1;48(7):1904–1909. [PubMed] [Google Scholar]
  43. 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]
  44. Rothenberg M. E., Luster A. D., Lilly C. M., Drazen J. M., Leder P. Constitutive and allergen-induced expression of eotaxin mRNA in the guinea pig lung. J Exp Med. 1995 Mar 1;181(3):1211–1216. doi: 10.1084/jem.181.3.1211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Saiki R. K., Bugawan T. L., Horn G. T., Mullis K. B., Erlich H. A. Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes. Nature. 1986 Nov 13;324(6093):163–166. doi: 10.1038/324163a0. [DOI] [PubMed] [Google Scholar]
  46. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Schleimer R. P., Freeland H. S., Peters S. P., Brown K. E., Derse C. P. An assessment of the effects of glucocorticoids on degranulation, chemotaxis, binding to vascular endothelium and formation of leukotriene B4 by purified human neutrophils. J Pharmacol Exp Ther. 1989 Aug;250(2):598–605. [PubMed] [Google Scholar]
  49. Schleimer R. P., Rutledge B. K. Cultured human vascular endothelial cells acquire adhesiveness for neutrophils after stimulation with interleukin 1, endotoxin, and tumor-promoting phorbol diesters. J Immunol. 1986 Jan;136(2):649–654. [PubMed] [Google Scholar]
  50. Schleimer R. P., Sterbinsky S. A., Kaiser J., Bickel C. A., Klunk D. A., Tomioka K., Newman W., Luscinskas F. W., Gimbrone M. A., Jr, McIntyre B. W. IL-4 induces adherence of human eosinophils and basophils but not neutrophils to endothelium. Association with expression of VCAM-1. J Immunol. 1992 Feb 15;148(4):1086–1092. [PubMed] [Google Scholar]
  51. Schuler G. D., Boguski M. S., Stewart E. A., Stein L. D., Gyapay G., Rice K., White R. E., Rodriguez-Tomé P., Aggarwal A., Bajorek E. A gene map of the human genome. Science. 1996 Oct 25;274(5287):540–546. [PubMed] [Google Scholar]
  52. Schwiebert L. M., Beck L. A., Stellato C., Bickel C. A., Bochner B. S., Schleimer R. P., Schwiebert L. A. Glucocorticosteroid inhibition of cytokine production: relevance to antiallergic actions. J Allergy Clin Immunol. 1996 Jan;97(1 Pt 2):143–152. doi: 10.1016/s0091-6749(96)80214-4. [DOI] [PubMed] [Google Scholar]
  53. Sehmi R., Wardlaw A. J., Cromwell O., Kurihara K., Waltmann P., Kay A. B. Interleukin-5 selectively enhances the chemotactic response of eosinophils obtained from normal but not eosinophilic subjects. Blood. 1992 Jun 1;79(11):2952–2959. [PubMed] [Google Scholar]
  54. Siraganian R. P. An automated continuous-flow system for the extraction and fluorometric analysis of histamine. Anal Biochem. 1974 Feb;57(2):383–394. doi: 10.1016/0003-2697(74)90093-1. [DOI] [PubMed] [Google Scholar]
  55. Stellato C., Beck L. A., Gorgone G. A., Proud D., Schall T. J., Ono S. J., Lichtenstein L. M., Schleimer R. P. Expression of the chemokine RANTES by a human bronchial epithelial cell line. Modulation by cytokines and glucocorticoids. J Immunol. 1995 Jul 1;155(1):410–418. [PubMed] [Google Scholar]
  56. Taub D. D., Oppenheim J. J. Chemokines, inflammation and the immune system. Ther Immunol. 1994 Aug;1(4):229–246. [PubMed] [Google Scholar]
  57. Teran L. M., Noso N., Carroll M., Davies D. E., Holgate S., Schröder J. M. Eosinophil recruitment following allergen challenge is associated with the release of the chemokine RANTES into asthmatic airways. J Immunol. 1996 Aug 15;157(4):1806–1812. [PubMed] [Google Scholar]
  58. Uguccioni M., Loetscher P., Forssmann U., Dewald B., Li H., Lima S. H., Li Y., Kreider B., Garotta G., Thelen M. Monocyte chemotactic protein 4 (MCP-4), a novel structural and functional analogue of MCP-3 and eotaxin. J Exp Med. 1996 May 1;183(5):2379–2384. doi: 10.1084/jem.183.5.2379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Walsh G. M., Hartnell A., Wardlaw A. J., Kurihara K., Sanderson C. J., Kay A. B. IL-5 enhances the in vitro adhesion of human eosinophils, but not neutrophils, in a leucocyte integrin (CD11/18)-dependent manner. Immunology. 1990 Oct;71(2):258–265. [PMC free article] [PubMed] [Google Scholar]
  60. Warner J. A., Reshef A., MacGlashan D. W., Jr A rapid Percoll technique for the purification of human basophils. J Immunol Methods. 1987 Dec 4;105(1):107–110. doi: 10.1016/0022-1759(87)90419-4. [DOI] [PubMed] [Google Scholar]
  61. 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]
  62. Weller P. F. The immunobiology of eosinophils. N Engl J Med. 1991 Apr 18;324(16):1110–1118. doi: 10.1056/NEJM199104183241607. [DOI] [PubMed] [Google Scholar]
  63. Wolpe S. D., Davatelis G., Sherry B., Beutler B., Hesse D. G., Nguyen H. T., Moldawer L. L., Nathan C. F., Lowry S. F., Cerami A. Macrophages secrete a novel heparin-binding protein with inflammatory and neutrophil chemokinetic properties. J Exp Med. 1988 Feb 1;167(2):570–581. doi: 10.1084/jem.167.2.570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Ying S., Taborda-Barata L., Meng Q., Humbert M., Kay A. B. 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. 1995 Jun 1;181(6):2153–2159. doi: 10.1084/jem.181.6.2153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Zeitlin P. L., Lu L., Rhim J., Cutting G., Stetten G., Kieffer K. A., Craig R., Guggino W. B. A cystic fibrosis bronchial epithelial cell line: immortalization by adeno-12-SV40 infection. Am J Respir Cell Mol Biol. 1991 Apr;4(4):313–319. doi: 10.1165/ajrcmb/4.4.313. [DOI] [PubMed] [Google Scholar]

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