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. 1995 Feb;95(2):913–918. doi: 10.1172/JCI117743

Milk-induced eczema is associated with the expansion of T cells expressing cutaneous lymphocyte antigen.

K J Abernathy-Carver 1, H A Sampson 1, L J Picker 1, D Y Leung 1
PMCID: PMC295586  PMID: 7532192

Abstract

The extravasation of T cells at sites of inflammation is critically dependent on the activity of homing receptors (HR) involved in endothelial cell recognition and binding. Two such HR (the cutaneous lymphocyte antigen [CLA] and L-selectin) have been shown to be selectively involved in T cell migration to skin and peripheral lymph nodes, respectively. This study was designed to assess the relationship between the organ specificity of an allergic reaction to food and the expression of HR on T cells activated in vitro by the relevant food allergen. Peripheral blood mononuclear cells were isolated from seven milk allergic children with a history of eczema when exposed to milk. All patients had a positive prick skin test and double-blind placebo-controlled food challenge to milk. 10 children with either allergic eosinophilic gastroenteritis or milk-induced enterocolitis and 8 nonatopic adults served as controls. Five-parameter flow cytometry using monoclonal antibodies was used for detection of the specific HR on freshly isolated T cells versus T cell blasts induced by a 6-d incubation with casein, as compared with Candida albicans. After in vitro stimulation with casein, but not C. albicans, patients with milk allergy and atopic dermatitis had a significantly greater percentage of CLA+ T cells (P < 0.01) than controls with milk-induced enterocolitis, allergic eosinophilic gastroenteritis, or nonatopic healthy controls. In contrast, the percentage of L-selectin-expressing T cells did not differ significantly between these groups. These data suggest that after casein stimulation allergic patients with milk-induced skin disease have an expanded population of CLA+ T cells, as compared with nonatopics or allergic patients without skin involvement. We postulate that heterogeneity in the regulation of HR expression on antigen-specific T cells may play a role in determining sites of involvement in tissue-directed allergic responses.

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  1. Berg E. L., Yoshino T., Rott L. S., Robinson M. K., Warnock R. A., Kishimoto T. K., Picker L. J., Butcher E. C. The cutaneous lymphocyte antigen is a skin lymphocyte homing receptor for the vascular lectin endothelial cell-leukocyte adhesion molecule 1. J Exp Med. 1991 Dec 1;174(6):1461–1466. doi: 10.1084/jem.174.6.1461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berman J. S., Beer D. J., Theodore A. C., Kornfeld H., Bernardo J., Center D. M. Lymphocyte recruitment to the lung. Am Rev Respir Dis. 1990 Jul;142(1):238–257. doi: 10.1164/ajrccm/142.1.238. [DOI] [PubMed] [Google Scholar]
  3. Hamid Q., Boguniewicz M., Leung D. Y. Differential in situ cytokine gene expression in acute versus chronic atopic dermatitis. J Clin Invest. 1994 Aug;94(2):870–876. doi: 10.1172/JCI117408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Jabara H. H., Ackerman S. J., Vercelli D., Yokota T., Arai K., Abrams J., Dvorak A. M., Lavigne M. C., Banchereau J., De Vries J. Induction of interleukin-4-dependent IgE synthesis and interleukin-5-dependent eosinophil differentiation by supernatants of a human helper T-cell clone. J Clin Immunol. 1988 Nov;8(6):437–446. doi: 10.1007/BF00916948. [DOI] [PubMed] [Google Scholar]
  5. Jones S. M., Sampson H. A. The role of allergens in atopic dermatitis. Clin Rev Allergy. 1993 Winter;11(4):471–490. [PubMed] [Google Scholar]
  6. Katz A. J., Twarog F. J., Zeiger R. S., Falchuk Z. M. Milk-sensitive and eosinophilic gastroenteropathy: similar clinical features with contrasting mechanisms and clinical course. J Allergy Clin Immunol. 1984 Jul;74(1):72–78. doi: 10.1016/0091-6749(84)90090-3. [DOI] [PubMed] [Google Scholar]
  7. Kay A. B., Ying S., Varney V., Gaga M., Durham S. R., Moqbel R., Wardlaw A. J., Hamid Q. Messenger RNA expression of the cytokine gene cluster, interleukin 3 (IL-3), IL-4, IL-5, and granulocyte/macrophage colony-stimulating factor, in allergen-induced late-phase cutaneous reactions in atopic subjects. J Exp Med. 1991 Mar 1;173(3):775–778. doi: 10.1084/jem.173.3.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Leung D. Y. Immunopathology of atopic dermatitis. Springer Semin Immunopathol. 1992;13(3-4):427–440. doi: 10.1007/BF00200539. [DOI] [PubMed] [Google Scholar]
  9. May C. D. Objective clinical and laboratory studies of immediate hypersensitivity reactions to foods in asthmatic children. J Allergy Clin Immunol. 1976 Oct;58(4):500–515. doi: 10.1016/0091-6749(76)90194-9. [DOI] [PubMed] [Google Scholar]
  10. Parronchi P., Macchia D., Piccinni M. P., Biswas P., Simonelli C., Maggi E., Ricci M., Ansari A. A., Romagnani S. Allergen- and bacterial antigen-specific T-cell clones established from atopic donors show a different profile of cytokine production. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4538–4542. doi: 10.1073/pnas.88.10.4538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Paul W. E., Seder R. A. Lymphocyte responses and cytokines. Cell. 1994 Jan 28;76(2):241–251. doi: 10.1016/0092-8674(94)90332-8. [DOI] [PubMed] [Google Scholar]
  12. Picker L. J., Butcher E. C. Physiological and molecular mechanisms of lymphocyte homing. Annu Rev Immunol. 1992;10:561–591. doi: 10.1146/annurev.iy.10.040192.003021. [DOI] [PubMed] [Google Scholar]
  13. Picker L. J., Kishimoto T. K., Smith C. W., Warnock R. A., Butcher E. C. ELAM-1 is an adhesion molecule for skin-homing T cells. Nature. 1991 Feb 28;349(6312):796–799. doi: 10.1038/349796a0. [DOI] [PubMed] [Google Scholar]
  14. Picker L. J., Martin R. J., Trumble A., Newman L. S., Collins P. A., Bergstresser P. R., Leung D. Y. Differential expression of lymphocyte homing receptors by human memory/effector T cells in pulmonary versus cutaneous immune effector sites. Eur J Immunol. 1994 Jun;24(6):1269–1277. doi: 10.1002/eji.1830240605. [DOI] [PubMed] [Google Scholar]
  15. Picker L. J. Mechanisms of lymphocyte homing. Curr Opin Immunol. 1992 Jun;4(3):277–286. doi: 10.1016/0952-7915(92)90077-r. [DOI] [PubMed] [Google Scholar]
  16. Picker L. J., Michie S. A., Rott L. S., Butcher E. C. A unique phenotype of skin-associated lymphocytes in humans. Preferential expression of the HECA-452 epitope by benign and malignant T cells at cutaneous sites. Am J Pathol. 1990 May;136(5):1053–1068. [PMC free article] [PubMed] [Google Scholar]
  17. Picker L. J., Treer J. R., Ferguson-Darnell B., Collins P. A., Bergstresser P. R., Terstappen L. W. Control of lymphocyte recirculation in man. II. Differential regulation of the cutaneous lymphocyte-associated antigen, a tissue-selective homing receptor for skin-homing T cells. J Immunol. 1993 Feb 1;150(3):1122–1136. [PubMed] [Google Scholar]
  18. Picker L. J., Treer J. R., Ferguson-Darnell B., Collins P. A., Buck D., Terstappen L. W. Control of lymphocyte recirculation in man. I. Differential regulation of the peripheral lymph node homing receptor L-selectin on T cells during the virgin to memory cell transition. J Immunol. 1993 Feb 1;150(3):1105–1121. [PubMed] [Google Scholar]
  19. Powell G. K. Food protein-induced enterocolitis of infancy: differential diagnosis and management. Compr Ther. 1986 Feb;12(2):28–37. [PubMed] [Google Scholar]
  20. 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]
  21. Sampson H. A., Jolie P. L. Increased plasma histamine concentrations after food challenges in children with atopic dermatitis. N Engl J Med. 1984 Aug 9;311(6):372–376. doi: 10.1056/NEJM198408093110605. [DOI] [PubMed] [Google Scholar]
  22. Shimizu Y., Newman W., Tanaka Y., Shaw S. Lymphocyte interactions with endothelial cells. Immunol Today. 1992 Mar;13(3):106–112. doi: 10.1016/0167-5699(92)90151-V. [DOI] [PubMed] [Google Scholar]
  23. Smith D. L., Deshazo R. D. Bronchoalveolar lavage in asthma. An update and perspective. Am Rev Respir Dis. 1993 Aug;148(2):523–532. doi: 10.1164/ajrccm/148.2.523. [DOI] [PubMed] [Google Scholar]
  24. Wierenga E. A., Snoek M., de Groot C., Chrétien I., Bos J. D., Jansen H. M., Kapsenberg M. L. Evidence for compartmentalization of functional subsets of CD2+ T lymphocytes in atopic patients. J Immunol. 1990 Jun 15;144(12):4651–4656. [PubMed] [Google Scholar]
  25. van Reijsen F. C., Bruijnzeel-Koomen C. A., Kalthoff F. S., Maggi E., Romagnani S., Westland J. K., Mudde G. C. Skin-derived aeroallergen-specific T-cell clones of Th2 phenotype in patients with atopic dermatitis. J Allergy Clin Immunol. 1992 Aug;90(2):184–193. doi: 10.1016/0091-6749(92)90070-i. [DOI] [PubMed] [Google Scholar]
  26. van der Heijden F. L., Wierenga E. A., Bos J. D., Kapsenberg M. L. High frequency of IL-4-producing CD4+ allergen-specific T lymphocytes in atopic dermatitis lesional skin. J Invest Dermatol. 1991 Sep;97(3):389–394. doi: 10.1111/1523-1747.ep12480966. [DOI] [PubMed] [Google Scholar]

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