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. 1994 Apr 1;179(4):1331–1336. doi: 10.1084/jem.179.4.1331

Rapid dendritic cell recruitment is a hallmark of the acute inflammatory response at mucosal surfaces

PMCID: PMC2191461  PMID: 8145044

Abstract

Immunohistochemical analysis of challenge sites such as skin and the peritoneal cavity has identified neutrophils as virtually the sole cellular participants in acute bacterial inflammation, peak influx occurring 24-48 h in advance of mononuclear cell populations associated with adaptive immunity. This study challenges the general applicability of this paradigm. We demonstrate here that the earliest detectable cellular response after inhalation of Moraxella catarrhalis organisms is the recruitment of putative class II major histocompatibility complex-bearing dendritic cell (DC) precursors into the airway epithelium, the initial wave arriving in advance of the neutrophil influx. Unlike the neutrophils which rapidly transit into the airway lumen, the DC precursors remain within the epithelium during the acute inflammatory response where they differentiate, and develop the dendriform morphology typical of resident DC found in the normal epithelium. During the ensuing 48-h period, these cells then migrate to the regional lymph nodes. No comparable DC response was observed after epidermal or intraperitoneal challenge, and it may be that mucosal surfaces are unique in their requirement for rapid DC responses during acute inflammation. We hypothesize that the role of the DC influx during acute inflammation may be surveillance for opportunistic viruses, and that this covert protective mechanism is operative at a restricted number of mucosal tissue sites.

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Selected References

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

  1. Boog C. J., Boes J., Melief C. J. Role of dendritic cells in the regulation of class I restricted cytotoxic T lymphocyte responses. J Immunol. 1988 May 15;140(10):3331–3337. [PubMed] [Google Scholar]
  2. Damoiseaux J. G., Döpp E. A., Neefjes J. J., Beelen R. H., Dijkstra C. D. Heterogeneity of macrophages in the rat evidenced by variability in determinants: two new anti-rat macrophage antibodies against a heterodimer of 160 and 95 kd (CD11/CD18). J Leukoc Biol. 1989 Dec;46(6):556–564. doi: 10.1002/jlb.46.6.556. [DOI] [PubMed] [Google Scholar]
  3. Holt P. G., Degebrodt A., O'Leary C., Krska K., Plozza T. T cell activation by antigen-presenting cells from lung tissue digests: suppression by endogenous macrophages. Clin Exp Immunol. 1985 Dec;62(3):586–593. [PMC free article] [PubMed] [Google Scholar]
  4. Holt P. G., Oliver J., Bilyk N., McMenamin C., McMenamin P. G., Kraal G., Thepen T. Downregulation of the antigen presenting cell function(s) of pulmonary dendritic cells in vivo by resident alveolar macrophages. J Exp Med. 1993 Feb 1;177(2):397–407. doi: 10.1084/jem.177.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Holt P. G., Oliver J., McMenamin C., Schon-Hegrad M. A. Studies on the surface phenotype and functions of dendritic cells in parenchymal lung tissue of the rat. Immunology. 1992 Apr;75(4):582–587. [PMC free article] [PubMed] [Google Scholar]
  6. Holt P. G., Schon-Hegrad M. A., Oliver J., Holt B. J., McMenamin P. G. A contiguous network of dendritic antigen-presenting cells within the respiratory epithelium. Int Arch Allergy Appl Immunol. 1990;91(2):155–159. doi: 10.1159/000235107. [DOI] [PubMed] [Google Scholar]
  7. Holt P. G., Schon-Hegrad M. A., Oliver J. MHC class II antigen-bearing dendritic cells in pulmonary tissues of the rat. Regulation of antigen presentation activity by endogenous macrophage populations. J Exp Med. 1988 Feb 1;167(2):262–274. doi: 10.1084/jem.167.2.262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Holt P. G., Schon-Hegrad M. A., Phillips M. J., McMenamin P. G. Ia-positive dendritic cells form a tightly meshed network within the human airway epithelium. Clin Exp Allergy. 1989 Nov;19(6):597–601. doi: 10.1111/j.1365-2222.1989.tb02752.x. [DOI] [PubMed] [Google Scholar]
  9. Janeway C. A., Jr The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol Today. 1992 Jan;13(1):11–16. doi: 10.1016/0167-5699(92)90198-G. [DOI] [PubMed] [Google Scholar]
  10. Kips J. C., Tavernier J., Pauwels R. A. Tumor necrosis factor causes bronchial hyperresponsiveness in rats. Am Rev Respir Dis. 1992 Feb;145(2 Pt 1):332–336. doi: 10.1164/ajrccm/145.2_Pt_1.332. [DOI] [PubMed] [Google Scholar]
  11. MacPherson G. G. Properties of lymph-borne (veiled) dendritic cells in culture. I. Modulation of phenotype, survival and function: partial dependence on GM-CSF. Immunology. 1989 Sep;68(1):102–107. [PMC free article] [PubMed] [Google Scholar]
  12. Mason D. W., Arthur R. P., Dallman M. J., Green J. R., Spickett G. P., Thomas M. L. Functions of rat T-lymphocyte subsets isolated by means of monoclonal antibodies. Immunol Rev. 1983;74:57–82. doi: 10.1111/j.1600-065x.1983.tb01084.x. [DOI] [PubMed] [Google Scholar]
  13. Mayrhofer G., Holt P. G., Papadimitriou J. M. Functional characteristics of the veiled cells in afferent lymph from the rat intestine. Immunology. 1986 Jul;58(3):379–387. [PMC free article] [PubMed] [Google Scholar]
  14. Nonacs R., Humborg C., Tam J. P., Steinman R. M. Mechanisms of mouse spleen dendritic cell function in the generation of influenza-specific, cytolytic T lymphocytes. J Exp Med. 1992 Aug 1;176(2):519–529. doi: 10.1084/jem.176.2.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Robinson A. P., White T. M., Mason D. W. Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology. 1986 Feb;57(2):239–247. [PMC free article] [PubMed] [Google Scholar]
  16. Schon-Hegrad M. A., Oliver J., McMenamin P. G., Holt P. G. Studies on the density, distribution, and surface phenotype of intraepithelial class II major histocompatibility complex antigen (Ia)-bearing dendritic cells (DC) in the conducting airways. J Exp Med. 1991 Jun 1;173(6):1345–1356. doi: 10.1084/jem.173.6.1345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Steinman R. M. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol. 1991;9:271–296. doi: 10.1146/annurev.iy.09.040191.001415. [DOI] [PubMed] [Google Scholar]

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