Eosinophil recruitment to the lung in a murine model of allergic inflammation. The role of T cells, chemokines, and adhesion receptors (original) (raw)

Abstract

Eosinophil accumulation is a distinctive feature of lung allergic inflammation. Here, we have used a mouse model of OVA (ovalbumin)-induced pulmonary eosinophilia to study the cellular and molecular mechanisms for this selective recruitment of eosinophils to the airways. In this model there was an early accumulation of infiltrating monocytes/macrophages in the lung during the OVA treatment, whereas the increase in infiltrating T-lymphocytes paralleled the accumulation of eosinophils. The kinetics of accumulation of these three leukocyte subtypes correlated with the levels of mRNA expression of the chemokines monocyte chemotactic peptide-1/JE, eotaxin, and RANTES (regulated upon activation in normal T cells expressed and secreted), suggesting their involvement in the recruitment of these leukocytes. Furthermore, blockade of eotaxin with specific antibodies in vivo reduced the accumulation of eosinophils in the lung in response to OVA by half. Mature CD4+ T-lymphocytes were absolutely required for OVA-induced eosinophil accumulation since lung eosinophilia was prevented in CD4+-deficient mice. However, these cells were neither the main producers of the major eosinophilic chemokines eotaxin, RANTES, or MIP-1alpha, nor did they regulate the expression of these chemokines. Rather, the presence of CD4+ T cells was necessary for enhancement of VCAM-1 (vascular cell adhesion molecule-1) expression in the lung during allergic inflammation induced by the OVA treatment. In support of this, mice genetically deficient for VCAM-1 and intercellular adhesion molecule-1 failed to develop pulmonary eosinophilia. Selective eosinophilic recruitment during lung allergic inflammation results from a sequential accumulation of certain leukocyte types, particularly T cells, and relies on the presence of both eosinophilic chemoattractants and adhesion receptors.

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Selected References

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  1. Basten A., Beeson P. B. Mechanism of eosinophilia. II. Role of the lymphocyte. J Exp Med. 1970 Jun 1;131(6):1288–1305. doi: 10.1084/jem.131.6.1288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Begg S. K., Radley J. M., Pollard J. W., Chisholm O. T., Stanley E. R., Bertoncello I. Delayed hematopoietic development in osteopetrotic (op/op) mice. J Exp Med. 1993 Jan 1;177(1):237–242. doi: 10.1084/jem.177.1.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bentley A. M., Maestrelli P., Saetta M., Fabbri L. M., Robinson D. S., Bradley B. L., Jeffery P. K., Durham S. R., Kay A. B. Activated T-lymphocytes and eosinophils in the bronchial mucosa in isocyanate-induced asthma. J Allergy Clin Immunol. 1992 Apr;89(4):821–829. doi: 10.1016/0091-6749(92)90437-7. [DOI] [PubMed] [Google Scholar]
  4. Bousquet J., Chanez P., Lacoste J. Y., Barnéon G., Ghavanian N., Enander I., Venge P., Ahlstedt S., Simony-Lafontaine J., Godard P. Eosinophilic inflammation in asthma. N Engl J Med. 1990 Oct 11;323(15):1033–1039. doi: 10.1056/NEJM199010113231505. [DOI] [PubMed] [Google Scholar]
  5. Bradley B. L., Azzawi M., Jacobson M., Assoufi B., Collins J. V., Irani A. M., Schwartz L. B., Durham S. R., Jeffery P. K., Kay A. B. 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. doi: 10.1016/0091-6749(91)90160-p. [DOI] [PubMed] [Google Scholar]
  6. Briscoe D. M., Cotran R. S., Pober J. S. Effects of tumor necrosis factor, lipopolysaccharide, and IL-4 on the expression of vascular cell adhesion molecule-1 in vivo. Correlation with CD3+ T cell infiltration. J Immunol. 1992 Nov 1;149(9):2954–2960. [PubMed] [Google Scholar]
  7. Burd P. R., Freeman G. J., Wilson S. D., Berman M., DeKruyff R., Billings P. R., Dorf M. E. Cloning and characterization of a novel T cell activation gene. J Immunol. 1987 Nov 1;139(9):3126–3131. [PubMed] [Google Scholar]
  8. 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]
  9. Carlos T. M., Harlan J. M. Leukocyte-endothelial adhesion molecules. Blood. 1994 Oct 1;84(7):2068–2101. [PubMed] [Google Scholar]
  10. Chervenick P. A., LoBuglio A. F. Human blood monocytes: stimulators of granulocyte and mononuclear colony formation in vitro. Science. 1972 Oct 13;178(4057):164–166. doi: 10.1126/science.178.4057.164. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Chuluyan H. E., Osborn L., Lobb R., Issekutz A. C. Domains 1 and 4 of vascular cell adhesion molecule-1 (CD106) both support very late activation antigen-4 (CD49d/CD29)-dependent monocyte transendothelial migration. J Immunol. 1995 Sep 15;155(6):3135–3134. [PubMed] [Google Scholar]
  13. 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]
  14. Corry D. B., Folkesson H. G., Warnock M. L., Erle D. J., Matthay M. A., Wiener-Kronish J. P., Locksley R. M. Interleukin 4, but not interleukin 5 or eosinophils, is required in a murine model of acute airway hyperreactivity. J Exp Med. 1996 Jan 1;183(1):109–117. doi: 10.1084/jem.183.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Davatelis G., Tekamp-Olson P., Wolpe S. D., Hermsen K., Luedke C., Gallegos C., Coit D., Merryweather J., Cerami A. Cloning and characterization of a cDNA for murine macrophage inflammatory protein (MIP), a novel monokine with inflammatory and chemokinetic properties. J Exp Med. 1988 Jun 1;167(6):1939–1944. doi: 10.1084/jem.167.6.1939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. De Monchy J. G., Kauffman H. F., Venge P., Koëter G. H., Jansen H. M., Sluiter H. J., De Vries K. Bronchoalveolar eosinophilia during allergen-induced late asthmatic reactions. Am Rev Respir Dis. 1985 Mar;131(3):373–376. doi: 10.1164/arrd.1985.131.3.373. [DOI] [PubMed] [Google Scholar]
  18. Del Prete G., Maggi E., Parronchi P., Chrétien I., Tiri A., Macchia D., Ricci M., Banchereau J., De Vries J., Romagnani S. IL-4 is an essential factor for the IgE synthesis induced in vitro by human T cell clones and their supernatants. J Immunol. 1988 Jun 15;140(12):4193–4198. [PubMed] [Google Scholar]
  19. Drazen J. M., Arm J. P., Austen K. F. Sorting out the cytokines of asthma. J Exp Med. 1996 Jan 1;183(1):1–5. doi: 10.1084/jem.183.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ebisawa M., Bochner B. S., Georas S. N., Schleimer R. P. Eosinophil transendothelial migration induced by cytokines. I. Role of endothelial and eosinophil adhesion molecules in IL-1 beta-induced transendothelial migration. J Immunol. 1992 Dec 15;149(12):4021–4028. [PubMed] [Google Scholar]
  21. Elias J. A., Schreiber A. D., Gustilo K., Chien P., Rossman M. D., Lammie P. J., Daniele R. P. Differential interleukin 1 elaboration by unfractionated and density fractionated human alveolar macrophages and blood monocytes: relationship to cell maturity. J Immunol. 1985 Nov;135(5):3198–3204. [PubMed] [Google Scholar]
  22. Ernst C. A., Zhang Y. J., Hancock P. R., Rutledge B. J., Corless C. L., Rollins B. J. Biochemical and biologic characterization of murine monocyte chemoattractant protein-1. Identification of two functional domains. J Immunol. 1994 Apr 1;152(7):3541–3549. [PubMed] [Google Scholar]
  23. Fels A. O., Pawlowski N. A., Cramer E. B., King T. K., Cohn Z. A., Scott W. A. Human alveolar macrophages produce leukotriene B4. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7866–7870. doi: 10.1073/pnas.79.24.7866. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Foster P. S., Hogan S. P., Ramsay A. J., Matthaei K. I., Young I. G. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J Exp Med. 1996 Jan 1;183(1):195–201. doi: 10.1084/jem.183.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Fung-Leung W. P., Schilham M. W., Rahemtulla A., Kündig T. M., Vollenweider M., Potter J., van Ewijk W., Mak T. W. CD8 is needed for development of cytotoxic T cells but not helper T cells. Cell. 1991 May 3;65(3):443–449. doi: 10.1016/0092-8674(91)90462-8. [DOI] [PubMed] [Google Scholar]
  26. Ganzalo J. A., Jia G. Q., Aguirre V., Friend D., Coyle A. J., Jenkins N. A., Lin G. S., Katz H., Lichtman A., Copeland N. Mouse Eotaxin expression parallels eosinophil accumulation during lung allergic inflammation but it is not restricted to a Th2-type response. Immunity. 1996 Jan;4(1):1–14. doi: 10.1016/s1074-7613(00)80293-9. [DOI] [PubMed] [Google Scholar]
  27. Gavett S. H., Chen X., Finkelman F., Wills-Karp M. Depletion of murine CD4+ T lymphocytes prevents antigen-induced airway hyperreactivity and pulmonary eosinophilia. Am J Respir Cell Mol Biol. 1994 Jun;10(6):587–593. doi: 10.1165/ajrcmb.10.6.8003337. [DOI] [PubMed] [Google Scholar]
  28. Gavett S. H., O'Hearn D. J., Li X., Huang S. K., Finkelman F. D., Wills-Karp M. Interleukin 12 inhibits antigen-induced airway hyperresponsiveness, inflammation, and Th2 cytokine expression in mice. J Exp Med. 1995 Nov 1;182(5):1527–1536. doi: 10.1084/jem.182.5.1527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gleich G. J. The eosinophil and bronchial asthma: current understanding. J Allergy Clin Immunol. 1990 Feb;85(2):422–436. doi: 10.1016/0091-6749(90)90151-s. [DOI] [PubMed] [Google Scholar]
  30. Gleich G. J. The eosinophil and bronchial asthma: current understanding. J Allergy Clin Immunol. 1990 Feb;85(2):422–436. doi: 10.1016/0091-6749(90)90151-s. [DOI] [PubMed] [Google Scholar]
  31. Gordon J. R., Galli S. J. Mast cells as a source of both preformed and immunologically inducible TNF-alpha/cachectin. Nature. 1990 Jul 19;346(6281):274–276. doi: 10.1038/346274a0. [DOI] [PubMed] [Google Scholar]
  32. Gurtner G. C., Davis V., Li H., McCoy M. J., Sharpe A., Cybulsky M. I. Targeted disruption of the murine VCAM1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev. 1995 Jan 1;9(1):1–14. doi: 10.1101/gad.9.1.1. [DOI] [PubMed] [Google Scholar]
  33. Hamelmann E., Oshiba A., Paluh J., Bradley K., Loader J., Potter T. A., Larsen G. L., Gelfand E. W. Requirement for CD8+ T cells in the development of airway hyperresponsiveness in a marine model of airway sensitization. J Exp Med. 1996 Apr 1;183(4):1719–1729. doi: 10.1084/jem.183.4.1719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Heeger P., Wolf G., Meyers C., Sun M. J., O'Farrell S. C., Krensky A. M., Neilson E. G. Isolation and characterization of cDNA from renal tubular epithelium encoding murine Rantes. Kidney Int. 1992 Jan;41(1):220–225. doi: 10.1038/ki.1992.31. [DOI] [PubMed] [Google Scholar]
  35. Jia G. Q., Gonzalo J. A., Lloyd C., Kremer L., Lu L., Martinez-A C., Wershil B. K., Gutierrez-Ramos J. C. Distinct expression and function of the novel mouse chemokine monocyte chemotactic protein-5 in lung allergic inflammation. J Exp Med. 1996 Nov 1;184(5):1939–1951. doi: 10.1084/jem.184.5.1939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Lamas A. M., Mulroney C. M., Schleimer R. P. Studies on the adhesive interaction between purified human eosinophils and cultured vascular endothelial cells. J Immunol. 1988 Mar 1;140(5):1500–1505. [PubMed] [Google Scholar]
  38. Lasky L. A. Selectins: interpreters of cell-specific carbohydrate information during inflammation. Science. 1992 Nov 6;258(5084):964–969. doi: 10.1126/science.1439808. [DOI] [PubMed] [Google Scholar]
  39. Lewinsohn D. M., Bargatze R. F., Butcher E. C. Leukocyte-endothelial cell recognition: evidence of a common molecular mechanism shared by neutrophils, lymphocytes, and other leukocytes. J Immunol. 1987 Jun 15;138(12):4313–4321. [PubMed] [Google Scholar]
  40. Lieschke G. J., Stanley E., Grail D., Hodgson G., Sinickas V., Gall J. A., Sinclair R. A., Dunn A. R. Mice lacking both macrophage- and granulocyte-macrophage colony-stimulating factor have macrophages and coexistent osteopetrosis and severe lung disease. Blood. 1994 Jul 1;84(1):27–35. [PubMed] [Google Scholar]
  41. Lin G., Finger E., Gutierrez-Ramos J. C. Expression of CD34 in endothelial cells, hematopoietic progenitors and nervous cells in fetal and adult mouse tissues. Eur J Immunol. 1995 Jun;25(6):1508–1516. doi: 10.1002/eji.1830250606. [DOI] [PubMed] [Google Scholar]
  42. Lopez A. F., Williamson D. J., Gamble J. R., Begley C. G., Harlan J. M., Klebanoff S. J., Waltersdorph A., Wong G., Clark S. C., Vadas M. A. Recombinant human granulocyte-macrophage colony-stimulating factor stimulates in vitro mature human neutrophil and eosinophil function, surface receptor expression, and survival. J Clin Invest. 1986 Nov;78(5):1220–1228. doi: 10.1172/JCI112705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Luo Y., Laning J., Devi S., Mak J., Schall T. J., Dorf M. E. Biologic activities of the murine beta-chemokine TCA3. J Immunol. 1994 Nov 15;153(10):4616–4624. [PubMed] [Google Scholar]
  44. Mombaerts P., Iacomini J., Johnson R. S., Herrup K., Tonegawa S., Papaioannou V. E. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 1992 Mar 6;68(5):869–877. doi: 10.1016/0092-8674(92)90030-g. [DOI] [PubMed] [Google Scholar]
  45. Nakajima H., Iwamoto I., Tomoe S., Matsumura R., Tomioka H., Takatsu K., Yoshida S. CD4+ T-lymphocytes and interleukin-5 mediate antigen-induced eosinophil infiltration into the mouse trachea. Am Rev Respir Dis. 1992 Aug;146(2):374–377. doi: 10.1164/ajrccm/146.2.374. [DOI] [PubMed] [Google Scholar]
  46. Nakajima H., Sano H., Nishimura T., Yoshida S., Iwamoto I. Role of vascular cell adhesion molecule 1/very late activation antigen 4 and intercellular adhesion molecule 1/lymphocyte function-associated antigen 1 interactions in antigen-induced eosinophil and T cell recruitment into the tissue. J Exp Med. 1994 Apr 1;179(4):1145–1154. doi: 10.1084/jem.179.4.1145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Pober J. S., Gimbrone M. A., Jr, Lapierre L. A., Mendrick D. L., Fiers W., Rothlein R., Springer T. A. Overlapping patterns of activation of human endothelial cells by interleukin 1, tumor necrosis factor, and immune interferon. J Immunol. 1986 Sep 15;137(6):1893–1896. [PubMed] [Google Scholar]
  48. 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]
  49. 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]
  50. Post T. W., Bozic C. R., Rothenberg M. E., Luster A. D., Gerard N., Gerard C. Molecular characterization of two murine eosinophil beta chemokine receptors. J Immunol. 1995 Dec 1;155(11):5299–5305. [PubMed] [Google Scholar]
  51. Rahemtulla A., Fung-Leung W. P., Schilham M. W., Kündig T. M., Sambhara S. R., Narendran A., Arabian A., Wakeham A., Paige C. J., Zinkernagel R. M. Normal development and function of CD8+ cells but markedly decreased helper cell activity in mice lacking CD4. Nature. 1991 Sep 12;353(6340):180–184. doi: 10.1038/353180a0. [DOI] [PubMed] [Google Scholar]
  52. Resnick M. B., Weller P. F. Mechanisms of eosinophil recruitment. Am J Respir Cell Mol Biol. 1993 Apr;8(4):349–355. doi: 10.1165/ajrcmb/8.4.349. [DOI] [PubMed] [Google Scholar]
  53. Robinson D. S., Hamid Q., Ying S., Tsicopoulos A., Barkans J., Bentley A. M., Corrigan C., Durham S. R., Kay A. B. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N Engl J Med. 1992 Jan 30;326(5):298–304. doi: 10.1056/NEJM199201303260504. [DOI] [PubMed] [Google Scholar]
  54. Rollins B. J., Morrison E. D., Stiles C. D. 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. doi: 10.1073/pnas.85.11.3738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. 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]
  56. Rothenberg M. E., Luster A. D., Leder P. Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8960–8964. doi: 10.1073/pnas.92.19.8960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. 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]
  58. Sanderson C. J. Interleukin-5, eosinophils, and disease. Blood. 1992 Jun 15;79(12):3101–3109. [PubMed] [Google Scholar]
  59. Sanderson C. J., Warren D. J., Strath M. Identification of a lymphokine that stimulates eosinophil differentiation in vitro. Its relationship to interleukin 3, and functional properties of eosinophils produced in cultures. J Exp Med. 1985 Jul 1;162(1):60–74. doi: 10.1084/jem.162.1.60. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. 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]
  61. Schall T. J., Jongstra J., Dyer B. J., Jorgensen J., Clayberger C., Davis M. M., Krensky A. M. A human T cell-specific molecule is a member of a new gene family. J Immunol. 1988 Aug 1;141(3):1018–1025. [PubMed] [Google Scholar]
  62. 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]
  63. Schweighoffer T., Shaw S. Adhesion cascades: diversity through combinatorial strategies. Curr Opin Cell Biol. 1992 Oct;4(5):824–829. doi: 10.1016/0955-0674(92)90106-m. [DOI] [PubMed] [Google Scholar]
  64. Springer T. A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994 Jan 28;76(2):301–314. doi: 10.1016/0092-8674(94)90337-9. [DOI] [PubMed] [Google Scholar]
  65. Spry C. J. Mechanism of eosinophilia. V. Kinetics of normal and accelerated eosinopoiesis. Cell Tissue Kinet. 1971 Jul;4(4):351–364. [PubMed] [Google Scholar]
  66. Van Rooijen N. The liposome-mediated macrophage 'suicide' technique. J Immunol Methods. 1989 Nov 13;124(1):1–6. doi: 10.1016/0022-1759(89)90178-6. [DOI] [PubMed] [Google Scholar]
  67. Van Vliet E., Melis M., Van Ewijk W. Monoclonal antibodies to stromal cell types of the mouse thymus. Eur J Immunol. 1984 Jun;14(6):524–529. doi: 10.1002/eji.1830140608. [DOI] [PubMed] [Google Scholar]
  68. Walker C., Bode E., Boer L., Hansel T. T., Blaser K., Virchow J. C., Jr Allergic and nonallergic asthmatics have distinct patterns of T-cell activation and cytokine production in peripheral blood and bronchoalveolar lavage. Am Rev Respir Dis. 1992 Jul;146(1):109–115. doi: 10.1164/ajrccm/146.1.109. [DOI] [PubMed] [Google Scholar]
  69. Walker C., Virchow J. C., Jr, Bruijnzeel P. L., Blaser K. T cell subsets and their soluble products regulate eosinophilia in allergic and nonallergic asthma. J Immunol. 1991 Mar 15;146(6):1829–1835. [PubMed] [Google Scholar]
  70. Walsh G. M., Mermod J. J., Hartnell A., Kay A. B., Wardlaw A. J. Human eosinophil, but not neutrophil, adherence to IL-1-stimulated human umbilical vascular endothelial cells is alpha 4 beta 1 (very late antigen-4) dependent. J Immunol. 1991 May 15;146(10):3419–3423. [PubMed] [Google Scholar]
  71. Walsh G. M., Wardlaw A. J., Hartnell A., Sanderson C. J., Kay A. B. Interleukin-5 enhances the in vitro adhesion of human eosinophils, but not neutrophils, in a leucocyte integrin (CD11/18)-dependent manner. Int Arch Allergy Appl Immunol. 1991;94(1-4):174–178. doi: 10.1159/000235355. [DOI] [PubMed] [Google Scholar]
  72. Wang B., Biron C., She J., Higgins K., Sunshine M. J., Lacy E., Lonberg N., Terhorst C. A block in both early T lymphocyte and natural killer cell development in transgenic mice with high-copy numbers of the human CD3E gene. Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9402–9406. doi: 10.1073/pnas.91.20.9402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Wegner C. D., Gundel R. H., Reilly P., Haynes N., Letts L. G., Rothlein R. Intercellular adhesion molecule-1 (ICAM-1) in the pathogenesis of asthma. Science. 1990 Jan 26;247(4941):456–459. doi: 10.1126/science.1967851. [DOI] [PubMed] [Google Scholar]
  74. 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]
  75. Widmer U., Yang Z., van Deventer S., Manogue K. R., Sherry B., Cerami A. Genomic structure of murine macrophage inflammatory protein-1 alpha and conservation of potential regulatory sequences with a human homolog, LD78. J Immunol. 1991 Jun 1;146(11):4031–4040. [PubMed] [Google Scholar]
  76. Xu H., Gonzalo J. A., St Pierre Y., Williams I. R., Kupper T. S., Cotran R. S., Springer T. A., Gutierrez-Ramos J. C. Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J Exp Med. 1994 Jul 1;180(1):95–109. doi: 10.1084/jem.180.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]