Skip to main content

Advertisement

SpringerLink
Log in

An Overlook to the Characteristics and Roles Played by Eotaxin Network in the Pathophysiology of Food Allergies: Allergic Asthma and Atopic Dermatitis

  • REVIEW
  • Published:
Inflammation Aims and scope Submit manuscript

Abstract

Investigations revealed substantial parts accomplished by chemokines specifically eotaxins and their specific receptors. They are functionally involved in the modulation of the pathologic state of tissue inflammation which is as a result of allergic reactions. Chemokines as small proteins with approximately 8–10 kDa molecular weight are considered and fit in the bigger family of cytokines, containing basic heparin-binding polypeptide mediators. Chemokines actively interfere in the processes of selective, oriented leukocyte (including eosinophil) recruitment. As eminent from their name, more specifically, eotaxins are specialized for eosinophils’ oriented locomotion toward allergic inflamed regions. To date, three members are defined for eotaxin subfamily as follows: eotaxin-1 (CCL11), eotaxin-2 (CCL24), and eotaxin-3 (CCL26), all of them bind to and activate CCR3 but have a low level of homology and appear to exhibit different physiological potentials. Allergy is described as a clinical state in which a pathologic hypersensitivity reaction is always initiated throughout an immunologic mechanism; similar to other immunologic reactions, an allergic reaction could also either be antibody or cell mediated. This type of allergic reactions occurs in all age groups and damages several different organs, having a significant impact on the emotional and social health of patients and their families and relatives. Concerning introductory comments introduced above, the authors of the present review attempted to collect and provide the latest evidences and information regarding the correlation between expression of eotaxin family members and allergy, in a wider extent, in two important allergic disorders: atopic asthma (AA) and atopic dermatitis (AD). Overall, concerning the most recent articles published within the database in the life sciences literature regarding the fundamental role(s) played by eotaxins in the pathogenesis of AA and AD, the authors of the current article propose that eotaxins (CCL11, CCL24, and CCL26) play key role(s) during symptomatic inflammatory responses raised in response to allergic crisis of these two clinical states.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Kagan, R.S. 2003. Food allergy: an overview. Environmental Health Perspectives 111: 223.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Patterson, R., P.A. Greenberger, J.M. Halwig, J.L. Liotta, and M. Roberts. 1986. Allergic bronchopulmonary aspergillosis. Natural history and classification of early disease by serologic and roentgenographic studies. Archives of Internal Medicine 146: 916–918.

    Article  CAS  PubMed  Google Scholar 

  3. Husby, S. 1988. Dietary antigens: uptake and humoral immunity in man. Acta Pathologica, Microbiologica et Immunologica Scandinavica, Supplementum 1: 1–40.

    CAS  Google Scholar 

  4. Kondo, N., H. Agata, O. Fukutomi, F. Motoyoshi, and T. Orii. 1990. Lymphocyte responses to food antigens in patients with atopic dermatitis who are sensitive to foods. Journal of Allergy and Clinical Immunology 86: 253–260.

    Article  CAS  PubMed  Google Scholar 

  5. Halstensen, T.S., and P. Brandtzaeg. 1993. Activated T lymphocytes in the celiac lesion: non-proliferative activation (CD25) of CD4+ alpha/beta cells in the lamina propria but proliferation (Ki-67) of alpha/beta and gamma/delta cells in the epithelium. European Journal of Immunology 23: 505–510.

    Article  CAS  PubMed  Google Scholar 

  6. Gerber, B.O., M.P. Zanni, M. Uguccioni, M. Loetscher, C.R. Mackay, W.J. Pichler, et al. 1997. Functional expression of the eotaxin receptor CCR3 in T lymphocytes co-localizing with eosinophils. Current Biology 7: 836–843.

    Article  CAS  PubMed  Google Scholar 

  7. Gonzalo, J.A., C.M. Lloyd, L. Kremer, E. Finger, A.C. Martinez, M.H. Siegelman, et al. 1996. Eosinophil recruitment to the lung in a murine model of allergic inflammation. The role of T cells, chemokines, and adhesion receptors. The Journal of Clinical Investigation 98: 2332–2345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Schroder, J.M., N. Noso, M. Sticherling, and E. Christophers. 1996. Role of eosinophil-chemotactic C-C chemokines in cutaneous inflammation. Journal of Leukocyte Biology 59: 1–5.

    CAS  PubMed  Google Scholar 

  9. Radman, M., G. Hassanshahi, R. Vazirinejad, M.K. Arababadi, M.N. Karimabad, H. Khorramdelazad, et al. 2013. Serum levels of the CC chemokines CCL2, CCL5, and CCL11 in food allergic children with different clinical manifestations. Inflammation 36: 561–566.

    Article  CAS  PubMed  Google Scholar 

  10. Morita, A., K. Shimosako, S. Kikuoka, Y. Taniguchi, M. Kitaura, K. Sasakura, et al. 1999. Development of a sensitive enzyme-linked immunosorbent assay for eotaxin and measurement of its levels in human blood. Journal of Immunological Methods 226: 159–167.

    Article  CAS  PubMed  Google Scholar 

  11. Ponath, P.D., S. Qin, D.J. Ringler, I. Clark-Lewis, J. Wang, N. Kassam, et al. 1996. Cloning of the human eosinophil chemoattractant, eotaxin. Expression, receptor binding, and functional properties suggest a mechanism for the selective recruitment of eosinophils. The Journal of Clinical Investigation 97: 604–612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Uguccioni, M., C.R. Mackay, B. Ochensberger, P. Loetscher, S. Rhis, G.J. LaRosa, et al. 1997. High expression of the chemokine receptor CCR3 in human blood basophils. Role in activation by eotaxin, MCP-4, and other chemokines. The Journal of Clinical Investigation 100: 1137–1143.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 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. The Journal of Experimental Medicine 181: 2153–2159.

    Article  CAS  PubMed  Google Scholar 

  14. Rubbert, A., C. Combadiere, M. Ostrowski, J. Arthos, M. Dybul, E. Machado, et al. 1998. Dendritic cells express multiple chemokine receptors used as coreceptors for HIV entry. The Journal of Immunology 160: 3933–3941.

    CAS  PubMed  Google Scholar 

  15. Bradley, B.L., M. Azzawi, M. Jacobson, B. Assoufi, J.V. Collins, A.M. Irani, et al. 1991. 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. Journal of Allergy and Clinical Immunology 88: 661–674.

    Article  CAS  PubMed  Google Scholar 

  16. 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. Biochemical and Biophysical Research Communications 197: 1167–1172.

    Article  CAS  PubMed  Google Scholar 

  17. Rothenberg, M.E., and S.P. Hogan. 2006. The eosinophil. Annual Review of Immunology 24: 147–174.

    Article  CAS  PubMed  Google Scholar 

  18. Garcia-Zepeda, E.A., M.E. Rothenberg, R.T. Ownbey, J. Celestin, P. Leder, and A.D. Luster. 1996. Human eotaxin is a specific chemoattractant for eosinophil cells and provides a new mechanism to explain tissue eosinophilia. Natue Medicine 2: 449–456.

    Article  CAS  Google Scholar 

  19. Rot, A., M. Krieger, T. Brunner, S.C. Bischoff, T.J. Schall, and C.A. Dahinden. 1992. RANTES and macrophage inflammatory protein 1 alpha induce the migration and activation of normal human eosinophil granulocytes. Journal of Experimental Medicine 176: 1489–1495.

    Article  CAS  PubMed  Google Scholar 

  20. Weber, M., M. Uguccioni, B. Ochensberger, M. Baggiolini, I. Clark-Lewis, and C.A. Dahinden. 1995. Monocyte chemotactic protein MCP-2 activates human basophil and eosinophil leukocytes similar to MCP-3. The Journal of Immunology 154: 4166–4172.

    CAS  PubMed  Google Scholar 

  21. Dahinden, C.A., T. Geiser, T. Brunner, V. von Tscharner, D. Caput, P. Ferrara, et al. 1994. Monocyte chemotactic protein 3 is a most effective basophil- and eosinophil-activating chemokine. Journal of Experimental Medicine 179: 751–756.

    Article  CAS  PubMed  Google Scholar 

  22. Uguccioni, M., P. Loetscher, U. Forssmann, B. Dewald, H. Li, S.H. Lima, et al. 1996. Monocyte chemotactic protein 4 (MCP-4), a novel structural and functional analogue of MCP-3 and eotaxin. Journal of Experimental Medicine 183: 2379–2384.

    Article  CAS  PubMed  Google Scholar 

  23. Baggiolini, M., B. Dewald, and B. Moser. 1994. Interleukin-8 and related chemotactic cytokines—CXC and CC chemokines. Advanced of Immunology 55: 97–179.

    Article  CAS  Google Scholar 

  24. Honda, K., and J. Chihara. 1999. Eosinophil activation by eotaxin—eotaxin primes the production of reactive oxygen species from eosinophils. Allergy 54: 1262–1269.

    Article  CAS  PubMed  Google Scholar 

  25. El-Shazly, A., and T. Ishikawa. 1999. Novel co-operation between eotaxin and substance-P in inducing eosinophil-derived neurotoxin release. Mediators of Inflammation 8: 177–179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Doucet, C., D. Brouty-Boye, C. Pottin-Clemenceau, G.W. Canonica, C. Jasmin, and B. Azzarone. 1998. Interleukin (IL) 4 and IL-13 act on human lung fibroblasts. Implication in asthma. The Journal of Clinical Investigation 101: 2129–2139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Izumi, S., K. Hirai, M. Miyamasu, Y. Takahashi, Y. Misaki, T. Takaishi, et al. 1997. Expression and regulation of monocyte chemoattractant protein-1 by human eosinophils. European Journal of Immunology 27: 816–824.

    Article  CAS  PubMed  Google Scholar 

  28. Heath, H., S. Qin, P. Rao, L. Wu, G. LaRosa, N. Kassam, et al. 1997. Chemokine receptor usage by human eosinophils. The importance of CCR3 demonstrated using an antagonistic monoclonal antibody. The Journal of Clinical Investigation 99: 178–184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jose, P., D. Griffiths-Johnson, P. Collins, D. Walsh, R. Moqbel, N. Totty, et al. 1994. Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. The Journal of Experimental Medicine 179: 881–887.

    Article  CAS  PubMed  Google Scholar 

  30. Rothenberg, M.E., A.D. Luster, and P. Leder. 1995. Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proceedings of the National Academy of Sciences 92: 8960–8964.

    Article  CAS  Google Scholar 

  31. Kitaura, M., T. Nakajima, T. Imai, S. Harada, C. Combadiere, H.L. Tiffany, et al. 1996. Molecular cloning of human eotaxin, an eosinophil-selective CC chemokine, and identification of a specific eosinophil eotaxin receptor, CC chemokine receptor 3. Journal of Biological Chemistry 271: 7725–7730.

    Article  CAS  PubMed  Google Scholar 

  32. Garcia-Zepeda, E.A., M.E. Rothenberg, S. Weremowicz, M.N. Sarafi, C.C. Morton, and A.D. Luster. 1997. Genomic organization, complete sequence, and chromosomal location of the gene for human eotaxin (SCYA11), an eosinophil-specific CC chemokine. Genomics 41: 471–476.

    Article  CAS  PubMed  Google Scholar 

  33. Bartels, J., C. Schlüter, E. Richter, N. Noso, R. Kulke, E. Christophers, et al. 1996. Human dermal fibroblasts express eotaxin: molecular cloning, mRNA expression, and identification of eotaxin sequence variants. Biochemical and Biophysical Research Communications 225: 1045–1051.

    Article  CAS  PubMed  Google Scholar 

  34. Ponath, P.D., S. Qin, T.W. Post, J. Wang, L. Wu, N.P. Gerard, et al. 1996. Molecular cloning and characterization of a human eotaxin receptor expressed selectively on eosinophils. The Journal of Experimental Medicine 183: 2437–2448.

    Article  CAS  PubMed  Google Scholar 

  35. Ying, S., D.S. Robinson, Q. Meng, J. Rottman, R. Kennedy, D.J. Ringler, et al. 1997. Enhanced expression of eotaxin and CCR3 mRNA and protein in atopic asthma. Association with airway hyperresponsiveness and predominant co‐localization of eotaxin mRNA to bronchial epithelial and endothelial cells. European Journal of Immunology 27: 3507–3516.

    Article  CAS  PubMed  Google Scholar 

  36. Ying, S., D.S. Robinson, Q. Meng, L.T. Barata, A.R. McEuen, M.G. Buckley, et al. 1999. CC chemokines in allergen-induced late-phase cutaneous responses in atopic subjects: association of eotaxin with early 6-hour eosinophils, and of eotaxin-2 and monocyte chemoattractant protein-4 with the later 24-hour tissue eosinophilia, and relationship to basophils and other CC chemokines (monocyte chemoattractant protein-3 and RANTES). The Journal of Immunology 163: 3976–3984.

    CAS  PubMed  Google Scholar 

  37. Miyamasu, M., M. Yamaguchi, T. Nakajima, Y. Misaki, Y. Morita, K. Matsushima, et al. 1999. Th1-derived cytokine IFN-γ is a potent inhibitor of eotaxin synthesis in vitro. International Immunology 11: 1001–1004.

    Article  CAS  PubMed  Google Scholar 

  38. Hein, H., C. Schlüter, R. Kulke, E. Christophers, J.-M. Schröder, and J. Bartels. 1997. Genomic organization, sequence, and transcriptional regulation of the human eotaxin gene. Biochemical and Biophysical Research Communications 237: 537–542.

    Article  CAS  PubMed  Google Scholar 

  39. Mochizuki, M., J. Bartels, A.I. Mallet, E. Christophers, and J.-M. Schröder. 1998. IL-4 induces eotaxin: a possible mechanism of selective eosinophil recruitment in helminth infection and atopy. The Journal of Immunology 160: 60–68.

    CAS  PubMed  Google Scholar 

  40. Li, L., Y. Xia, A. Nguyen, Y.H. Lai, L. Feng, T.R. Mosmann, et al. 1999. Effects of Th2 cytokines on chemokine expression in the lung: IL-13 potently induces eotaxin expression by airway epithelial cells. The Journal of Immunology 162: 2477–2487.

    CAS  PubMed  Google Scholar 

  41. Matsukura, S., C. Stellato, J.R. Plitt, C. Bickel, K. Miura, S.N. Georas, et al. 1999. Activation of eotaxin gene transcription by NF-κB and STAT6 in human airway epithelial cells. The Journal of Immunology 163: 6876–6883.

    CAS  PubMed  Google Scholar 

  42. Amerio, P., A. Frezzolini, C. Feliciani, R. Verdolini, P. Teofoli, O. Pit, et al. 2003. Eotaxins and CCR3 receptor in inflammatory and allergic skin diseases: therapeutical implications. Current Drug Targets-Inflammation & Allergy 2: 81–94.

    Article  CAS  Google Scholar 

  43. Sallusto, F., C.R. Mackay, and A. Lanzavecchia. 1997. Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science 277: 2005–2007.

    Article  CAS  PubMed  Google Scholar 

  44. Romagnani, P., A. De Paulis, C. Beltrame, F. Annunziato, V. Dente, E. Maggi, et al. 1999. Tryptase-chymase double-positive human mast cells express the eotaxin receptor CCR3 and are attracted by CCR3-binding chemokines. The American Journal of Pathology 155: 1195–1204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Palframan, R.T., P.D. Collins, T.J. Williams, and S.M. Rankin. 1998. Eotaxin induces a rapid release of eosinophils and their progenitors from the bone marrow. Blood 91: 2240–2248.

    CAS  PubMed  Google Scholar 

  46. Taha, R.A., E.M. Minshall, D.Y. Leung, M. Boguniewicz, A. Luster, S. Muro, et al. 2000. Evidence for increased expression of eotaxin and monocyte chemotactic protein-4 in atopic dermatitis. Journal of Allergy and Clinical Immunology 105: 1002–1007.

    Article  CAS  PubMed  Google Scholar 

  47. Kitayama, J., R.C. Fuhlbrigge, K.D. Puri, and T.A. Springer. 1997. P-selectin, L-selectin, and alpha 4 integrin have distinct roles in eosinophil tethering and arrest on vascular endothelial cells under physiological flow conditions. The Journal of Immunology 159: 3929–3939.

    CAS  PubMed  Google Scholar 

  48. Hohki, G., N. Terada, N. Hamano, M. Kitaura, T. Nakajima, O. Yoshie, et al. 1997. The effects of eotaxin on the surface adhesion molecules of endothelial cells and on eosinophil adhesion to microvascular endothelial cells. Biochemical and Biophysical Research Communications 241: 136–141.

    Article  CAS  PubMed  Google Scholar 

  49. Sabroe, I., D.M. Conroy, N.P. Gerard, Y. Li, P.D. Collins, T.W. Post, et al. 1998. Cloning and characterization of the guinea pig eosinophil eotaxin receptor, CC chemokine receptor-3: blockade using a monoclonal antibody in vivo. The Journal of Immunology 161: 6139–6147.

    CAS  PubMed  Google Scholar 

  50. Jia, G.-Q., J.-A. Gonzalo, A. Hidalgo, D. Wagner, M. Cybulsky, and J.C. Gutierrez-Ramos. 1999. Selective eosinophil transendothelial migration triggered by eotaxin via modulation of Mac-1/ICAM-1 and VLA-4/VCAM-1 interactions. International Immunology 11: 1–10.

    Article  CAS  PubMed  Google Scholar 

  51. Gutierrez-Ramos, J.C., C. Lloyd, and J.A. Gonzalo. 1999. Eotaxin: from an eosinophilic chemokine to a major regulator of allergic reactions. Immunology Today 20: 500–504.

    Article  CAS  PubMed  Google Scholar 

  52. Petering, H., C. Kluthe, Y. Dulkys, P. Kiehl, P.D. Ponath, A. Kapp, et al. 2001. Characterization of the CC chemokine receptor 3 on human keratinocytes. Journal of Investigative Dermatology 116: 549–555.

    Article  CAS  PubMed  Google Scholar 

  53. Salcedo, R., H.A. Young, M.L. Ponce, J.M. Ward, H.K. Kleinman, W.J. Murphy, et al. 2001. Eotaxin (CCL11) induces in vivo angiogenic responses by human CCR3+ endothelial cells. The Journal of Immunology 166: 7571–7578.

    Article  CAS  PubMed  Google Scholar 

  54. Nomiyama, H., L. Osborne, T. Imai, J. Kusuda, R. Miura, L.-C. Tsui, et al. 1998. Assignment of the human CC chemokine MPIF-2/eotaxin-2 (SCYA24) to chromosome 7q11.23. Genomics 49: 339–340.

    Article  CAS  PubMed  Google Scholar 

  55. Jahnsen, F.L., R. Haye, E. Gran, P. Brandtzaeg, and F.-E. Johansen. 1999. Glucocorticosteroids inhibit mRNA expression for eotaxin, eotaxin-2, and monocyte-chemotactic protein-4 in human airway inflammation with eosinophilia. The Journal of Immunology 163: 1545–1551.

    CAS  PubMed  Google Scholar 

  56. Dulkys, Y., G. Schramm, D. Kimmig, S. Knöß, A. Weyergraf, A. Kapp, et al. 2001. Detection of mRNA for eotaxin-2 and eotaxin-3 in human dermal fibroblasts and their distinct activation profile on human eosinophils. Journal of Investigative Dermatology 116: 498–505.

    Article  CAS  PubMed  Google Scholar 

  57. Shahabuddin, S., P. Ponath, and R.P. Schleimer. 2000. Migration of eosinophils across endothelial cell monolayers: interactions among IL-5, endothelial-activating cytokines, and CC chemokines. The Journal of Immunology 164: 3847–3854.

    Article  CAS  PubMed  Google Scholar 

  58. Patel, V.P., B.L. Kreider, Y. Li, H. Li, K. Leung, T. Salcedo, et al. 1997. Molecular and functional characterization of two novel human CC chemokines as inhibitors of two distinct classes of myeloid progenitors. The Journal of Experimental Medicine 185: 1163–1172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Heinemann, A., A. Hartnell, V.E. Stubbs, K. Murakami, D. Soler, G. LaRosa, et al. 2000. Basophil responses to chemokines are regulated by both sequential and cooperative receptor signaling. The Journal of Immunology 165: 7224–7233.

    Article  CAS  PubMed  Google Scholar 

  60. Maune, S., and J. Meyer. 2002. The role of CC chemokines in chronic sinusitis. Oto-Rhino-Laryngologia Nova 12: 63–70.

    Article  Google Scholar 

  61. Hoeck, J., and M. Woisetschläger. 2001. Activation of eotaxin-3/CCL26 gene expression in human dermal fibroblasts is mediated by STAT6. The Journal of Immunology 167: 3216–3222.

    Article  CAS  PubMed  Google Scholar 

  62. Shinkai, A., H. Yoshisue, M. Koike, E. Shoji, S. Nakagawa, A. Saito, et al. 1999. A novel human CC chemokine, eotaxin-3, which is expressed in IL-4-stimulated vascular endothelial cells, exhibits potent activity toward eosinophils. The Journal of Immunology 163: 1602–1610.

    CAS  PubMed  Google Scholar 

  63. Teran, L.M. 2000. CCL chemokines and asthma. Immunology Today 21: 235–242.

    Article  CAS  PubMed  Google Scholar 

  64. Kitaura, M., N. Suzuki, T. Imai, S. Takagi, R. Suzuki, T. Nakajima, et al. 1999. Molecular cloning of a novel human CC chemokine (eotaxin-3) that is a functional ligand of CC chemokine receptor 3. Journal of Biological Chemistry 274: 27975–27980.

    Article  CAS  PubMed  Google Scholar 

  65. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annual Review of Immunology 17: 255–281.

    Article  CAS  PubMed  Google Scholar 

  66. Maddox, L., and D.A. Schwartz. 2002. The pathophysiology of asthma. Annual Review of Medicine 53: 477–498.

    Article  CAS  PubMed  Google Scholar 

  67. Hatae, T., M. Wada, C. Yokoyama, M. Shimonishi, and T. Tanabe. 2001. Prostacyclin-dependent apoptosis mediated by PPAR delta. The Journal of Biological Chemistry 276: 46260–46267.

    Article  CAS  PubMed  Google Scholar 

  68. Daynes, R.A., and D.C. Jones. 2002. Emerging roles of PPARs in inflammation and immunity. Nature Reviews Immunology 2: 748–759.

    Article  CAS  PubMed  Google Scholar 

  69. Clark, R.B., D. Bishop-Bailey, T. Estrada-Hernandez, T. Hla, L. Puddington, and S.J. Padula. 2000. The nuclear receptor PPAR gamma and immunoregulation: PPAR gamma mediates inhibition of helper T cell responses. The Journal of Immunology 164: 1364–1371.

    Article  CAS  PubMed  Google Scholar 

  70. Chinetti, G., S. Griglio, M. Antonucci, I.P. Torra, P. Delerive, Z. Majd, et al. 1998. Activation of proliferator-activated receptors alpha and gamma induces apoptosis of human monocyte-derived macrophages. The Journal of Biological Chemistry 273: 25573–25580.

    Article  CAS  PubMed  Google Scholar 

  71. Ricote, M., A.C. Li, T.M. Willson, C.J. Kelly, and C.K. Glass. 1998. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 391: 79–82.

    Article  CAS  PubMed  Google Scholar 

  72. Devchand, P.R., H. Keller, J.M. Peters, M. Vazquez, F.J. Gonzalez, and W. Wahli. 1996. The PPARalpha-leukotriene B4 pathway to inflammation control. Nature 384: 39–43.

    Article  CAS  PubMed  Google Scholar 

  73. Fujisawa, T., Y. Kato, H. Nagase, J. Atsuta, A. Terada, K. Iguchi, et al. 2000. Chemokines induce eosinophil degranulation through CCR-3. Journal of Allergy and Clinical Immunology 106: 507–513.

    Article  CAS  PubMed  Google Scholar 

  74. Han, S.J., J.H. Kim, Y.J. Noh, H.S. Chang, C.S. Kim, K.S. Kim, et al. 1999. Interleukin (IL)-5 downregulates tumor necrosis factor (TNF)-induced eotaxin messenger RNA (mRNA) expression in eosinophils. Induction of eotaxin mRNA by TNF and IL-5 in eosinophils. American Journal of Respiratory Cell and Molecular Biology 21: 303–310.

    Article  CAS  PubMed  Google Scholar 

  75. Zhou, X., H. Hu, S. Balzar, J.B. Trudeau, and S.E. Wenzel. 2012. MAPK regulation of IL-4/IL-13 receptors contributes to the synergistic increase in CCL11/eotaxin-1 in response to TGF-beta1 and IL-13 in human airway fibroblasts. The Journal of Immunology 188: 6046–6054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Wenzel, S.E., J.B. Trudeau, S. Barnes, X. Zhou, M. Cundall, J.Y. Westcott, et al. 2002. TGF-beta and IL-13 synergistically increase eotaxin-1 production in human airway fibroblasts. The Journal of Immunology 169: 4613–4619.

    Article  CAS  PubMed  Google Scholar 

  77. Hoeck, J., and M. Woisetschlager. 2001. STAT6 mediates eotaxin-1 expression in IL-4 or TNF-alpha-induced fibroblasts. The Journal of Immunology 166: 4507–4515.

    Article  CAS  PubMed  Google Scholar 

  78. Matsukura, S., M. Odaka, M. Kurokawa, H. Kuga, T. Homma, H. Takeuchi, et al. 2010. Transforming growth factor-beta stimulates the expression of eotaxin/CC chemokine ligand 11 and its promoter activity through binding site for nuclear factor-kappabeta in airway smooth muscle cells. Clinical & Experimental Allergy 40: 763–771.

    CAS  Google Scholar 

  79. Kumagai, N., K. Fukuda, Y. Ishimura, and T. Nishida. 2000. Synergistic induction of eotaxin expression in human keratocytes by TNF-alpha and IL-4 or IL-13. Investigative Ophthalmology & Visual Science 41: 1448–1453.

    CAS  Google Scholar 

  80. Liu, Y., C. Meyer, A. Muller, F. Herweck, Q. Li, R. Mullenbach, et al. 2011. IL-13 induces connective tissue growth factor in rat hepatic stellate cells via TGF-beta-independent Smad signaling. The Journal of Immunology 187: 2814–2823.

    Article  CAS  PubMed  Google Scholar 

  81. Zheng, T., Z. Zhu, W. Liu, C.G. Lee, Q. Chen, R.J. Homer, et al. 2003. Cytokine regulation of IL-13Ralpha2 and IL-13Ralpha1 in vivo and in vitro. Journal of Allergy and Clinical Immunology 111: 720–728.

    Article  CAS  PubMed  Google Scholar 

  82. Hirst, S.J., M.P. Hallsworth, Q. Peng, and T.H. Lee. 2002. Selective induction of eotaxin release by interleukin-13 or interleukin-4 in human airway smooth muscle cells is synergistic with interleukin-1beta and is mediated by the interleukin-4 receptor alpha-chain. American Journal of Respiratory Cell and Molecular Biology 165: 1161–1171.

    Google Scholar 

  83. Baggiolini, M., and C.A. Dahinden. 1994. CC chemokines in allergic inflammation. Immunology Today 15: 127–133.

    Article  CAS  PubMed  Google Scholar 

  84. Aceves, S.S., R.O. Newbury, R. Dohil, J.F. Bastian, and D.H. Broide. 2007. Esophageal remodeling in pediatric eosinophilic esophagitis. Journal of Allergy and Clinical Immunology 119: 206–212.

    Article  CAS  PubMed  Google Scholar 

  85. Kephart, G.M., J.A. Alexander, A.S. Arora, Y. Romero, T.C. Smyrk, N.J. Talley, et al. 2010. Marked deposition of eosinophil-derived neurotoxin in adult patients with eosinophilic esophagitis. The American Journal of Gastroenterology 105: 298–307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Cheng, E., R.F. Souza, and S.J. Spechler. 2012. Tissue remodeling in eosinophilic esophagitis. American Journal of Physiology-Gastrointestinal and Liver Physiology 303: G1175–G1187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Abonia, J.P., J.P. Franciosi, and M.E. Rothenberg. 2010. TGFβ1: mediator of a feedback loop in eosinophilic esophagitis… or should we really say mastocytic esophagitis? The Journal of Allergy and Clinical Immunology 126: 1205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Hogan, S.P., and M.E. Rothenberg. 2006. Eosinophil function in eosinophil-associated gastrointestinal disorders. Current Allergy and Asthma Reports 6: 65–71.

    Article  CAS  PubMed  Google Scholar 

  89. Odemuyiwa, S.O., A. Ghahary, Y. Li, L. Puttagunta, J.E. Lee, S. Musat-Marcu, et al. 2004. Cutting edge: human eosinophils regulate T cell subset selection through indoleamine 2,3-dioxygenase. The Journal of Immunology 173: 5909–5913.

    Article  CAS  PubMed  Google Scholar 

  90. Lucendo, A.J., T. Bellón, and B. Lucendo. 2009. The role of mast cells in eosinophilic esophagitis. Pediatric Allergy and Immunology 20: 512–518.

    Article  PubMed  Google Scholar 

  91. Konikoff, M.R., R.J. Noel, C. Blanchard, C. Kirby, S.C. Jameson, B.K. Buckmeier, et al. 2006. A randomized, double-blind, placebo-controlled trial of fluticasone propionate for pediatric eosinophilic esophagitis. Gastroenterology 131: 1381–1391.

    Article  CAS  PubMed  Google Scholar 

  92. Aceves, S., R. Newbury, D. Chen, J. Mueller, R. Dohil, H. Hoffman, et al. 2010. Resolution of remodeling in eosinophilic esophagitis correlates with epithelial response to topical corticosteroids. Allergy 65: 109–116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Chai, O.H., E.-H. Han, H.-K. Lee, and C.H. Song. 2011. Mast cells play a key role in Th2 cytokine-dependent asthma model through production of adhesion molecules by liberation of TNF-α. Experimental & Molecular Medicine 43: 35–43.

    Article  CAS  Google Scholar 

  94. Vicario, M., C. Blanchard, K.F. Stringer, M.H. Collins, M.K. Mingler, A. Ahrens, et al. 2010. Local B cells and IgE production in the oesophageal mucosa in eosinophilic oesophagitis. Gut 59: 12–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Gonsalves, N., G.Y. Yang, B. Doerfler, S. Ritz, A.M. Ditto, and I. Hirano. 2012. Elimination diet effectively treats eosinophilic esophagitis in adults; food reintroduction identifies causative factors. Gastroenterology 142: 1451–1459. e1451.

    Article  PubMed  Google Scholar 

  96. Rajavelu, P., M. Rayapudi, M. Moffitt, A. Mishra, and A. Mishra. 2012. Significance of para-esophageal lymph nodes in food or aeroallergen-induced iNKT cell-mediated experimental eosinophilic esophagitis. American Journal of Physiology-Gastrointestinal and Liver Physiology 302: G645–G654.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Blanchard, C., M.K. Mingler, M. Vicario, J.P. Abonia, Y.Y. Wu, T.X. Lu, et al. 2007. IL-13 involvement in eosinophilic esophagitis: transcriptome analysis and reversibility with glucocorticoids. Journal of Allergy and Clinical Immunology 120: 1292–1300.

    Article  CAS  PubMed  Google Scholar 

  98. Yamazaki, K., J.A. Murray, A.S. Arora, J.A. Alexander, T.C. Smyrk, J.H. Butterfield, et al. 2006. Allergen-specific in vitro cytokine production in adult patients with eosinophilic esophagitis. Digestive Diseases and Sciences 51: 1934–1941.

    Article  CAS  PubMed  Google Scholar 

  99. Otani, I.M., A.A. Anilkumar, R.O. Newbury, M. Bhagat, L.Y. Beppu, R. Dohil, et al. 2013. Anti-IL-5 therapy reduces mast cell and IL-9 cell numbers in pediatric patients with eosinophilic esophagitis. Journal of Allergy and Clinical Immunology 131: 1576–1582. e1572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Umetsu, D.T., J.J. McIntire, O. Akbari, C. Macaubas, and R.H. DeKruyff. 2002. Asthma: an epidemic of dysregulated immunity. Nature Immunology 3: 715–720.

    Article  CAS  PubMed  Google Scholar 

  101. Holt, P.G., C. Macaubas, P.A. Stumbles, and P.D. Sly. 1999. The role of allergy in the development of asthma. Nature 402: B12–17.

    Article  CAS  PubMed  Google Scholar 

  102. Jahnz-Rozyk, K., L.B. Brydak, T. Targowski, M. Machala, and T. Plusa. 2004. Effect of influenza vaccinations on immune response and serum eotaxin level in patients with allergic bronchial asthma. Mediators of Inflammation 13: 195–199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Bousquet, J., P.K. Jeffery, W.W. Busse, M. Johnson, and A.M. Vignola. 2000. Asthma. From bronchoconstriction to airways inflammation and remodeling. American Journal of Respiratory Critical Care Medicine 161: 1720–1745.

    Article  CAS  PubMed  Google Scholar 

  104. Kelly, M., J.M. Hwang, and P. Kubes. 2007. Modulating leukocyte recruitment in inflammation. Journal of Allergy and Clinical Immunology 120: 3–10.

    Article  CAS  PubMed  Google Scholar 

  105. Komiya, A., H. Nagase, H. Yamada, T. Sekiya, M. Yamaguchi, Y. Sano, et al. 2003. Concerted expression of eotaxin-1, eotaxin-2, and eotaxin-3 in human bronchial epithelial cells. Cellular Immunology 225: 91–100.

    Article  CAS  PubMed  Google Scholar 

  106. 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. The Journal of Experimental Medicine 182: 1169–1174.

    Article  CAS  PubMed  Google Scholar 

  107. Humbles, A.A., B. Lu, D.S. Friend, S. Okinaga, J. Lora, A. Al-Garawi, et al. 2002. The murine CCR3 receptor regulates both the role of eosinophils and mast cells in allergen-induced airway inflammation and hyperresponsiveness. Proceeding of the National Academy of Sciences of the United States of America 99: 1479–1484.

    Article  CAS  Google Scholar 

  108. Berkman, N., S. Ohnona, F.K. Chung, and R. Breuer. 2001. Eotaxin-3 but not eotaxin gene expression is upregulated in asthmatics 24 hours after allergen challenge. American Journal of Respiratory Cell and Molecular Biology 24: 682–687.

    Article  CAS  PubMed  Google Scholar 

  109. McElhaney, J.E., C.M. Upshaw, J.W. Hooton, K.E. Lechelt, and G.S. Meneilly. 1998. Responses to influenza vaccination in different T-cell subsets: a comparison of healthy young and older adults. Vaccine 16: 1742–1747.

    Article  CAS  PubMed  Google Scholar 

  110. Wierenga, E.A., M. Snoek, C. de Groot, I. Chretien, J.D. Bos, H.M. Jansen, et al. 1990. Evidence for compartmentalization of functional subsets of CD2+ T lymphocytes in atopic patients. The Journal of Immunology 144: 4651–4656.

    CAS  PubMed  Google Scholar 

  111. Krakauer, T., and C. Russo. 2001. Serum cytokine levels and antibody response to influenza vaccine in the elderly. Immunopharmacology and Immunotoxicology 23: 35–41.

    Article  CAS  PubMed  Google Scholar 

  112. Miyamasu, M., Y. Misaki, M. Yamaguchi, K. Yamamoto, Y. Morita, K. Matsushima, et al. 2000. Regulation of human eotaxin generation by Th1-/Th2-derived cytokines. International of Archives of Allergy and Immunology 122(Suppl 1): 54–58.

    Article  CAS  Google Scholar 

  113. Lilly, C.M., P.G. Woodruff, C.A. Camargo, H. Nakamura, J.M. Drazen, E.S. Nadel, et al. 1999. Elevated plasma eotaxin levels in patients with acute asthma. Journal of Allergy and Clinical Immunology 104: 786–790.

    Article  CAS  PubMed  Google Scholar 

  114. Chu, Y.T., W. Chiang, T.N. Wang, C.H. Hung, Y.J. Jong, and J.R. Wu. 2007. Changes in serum eotaxin and eosinophil cationic protein levels, and eosinophil count during treatment of childhood asthma. Journal of Microbiology, Immunology and Infection 40: 162–167.

    CAS  Google Scholar 

  115. Leung, D.Y. 1995. Atopic dermatitis: the skin as a window into the pathogenesis of chronic allergic diseases. Journal of Allergy and Clinical Immunology 96: 302–318. quiz 319.

    Article  CAS  PubMed  Google Scholar 

  116. Wuthrich, B., and P. Schmid-Grendelmeier. 2003. The atopic eczema/dermatitis syndrome. Epidemiology, natural course, and immunology of the IgE-associated (“extrinsic”) and the nonallergic (“intrinsic”) AEDS. Journal of Investigation Allergology and Clinical Immunology 13: 1–5.

    CAS  Google Scholar 

  117. Hossny, E., M. Aboul-Magd, and S. Bakr. 2001. Increased plasma eotaxin in atopic dermatitis and acute urticaria in infants and children. Allergy 56: 996–1002.

    Article  CAS  PubMed  Google Scholar 

  118. Greiff, L., H. Petersen, E. Mattsson, M. Andersson, J.S. Erjefalt, M. Linden, et al. 2001. Mucosal output of eotaxin in allergic rhinitis and its attenuation by topical glucocorticosteroid treatment. Clinical & Experimental Allergy 31: 1321–1327.

    Article  CAS  Google Scholar 

  119. Lloyd, C.M., T. Delaney, T. Nguyen, J. Tian, A.C. Martinez, A.J. Coyle, et al. 2000. CC chemokine receptor (CCR)3/eotaxin is followed by CCR4/monocyte-derived chemokine in mediating pulmonary T helper lymphocyte type 2 recruitment after serial antigen challenge in vivo. The Journal of Experimental Medicine 191: 265–274.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Kaburagi, Y., Y. Shimada, T. Nagaoka, M. Hasegawa, K. Takehara, and S. Sato. 2001. Enhanced production of CC-chemokines (RANTES, MCP-1, MIP-1alpha, MIP-1beta, and eotaxin) in patients with atopic dermatitis. Archives of Dermatological Research 293: 350–355.

    Article  CAS  PubMed  Google Scholar 

  121. Kagami, S., T. Kakinuma, H. Saeki, Y. Tsunemi, H. Fujita, K. Nakamura, et al. 2003. Significant elevation of serum levels of eotaxin-3/CCL26, but not of eotaxin-2/CCL24, in patients with atopic dermatitis: serum eotaxin-3/CCL26 levels reflect the disease activity of atopic dermatitis. Clinical & Experimental Immunology 134: 309–313.

    Article  CAS  Google Scholar 

  122. Yawalkar, N., M. Uguccioni, J. Scharer, J. Braunwalder, S. Karlen, B. Dewald, et al. 1999. Enhanced expression of eotaxin and CCR3 in atopic dermatitis. Journal of Investigate Dermatology 113: 43–48.

    Article  CAS  Google Scholar 

  123. Yamada, H., K. Hirai, M. Miyamasu, M. Iikura, Y. Misaki, S. Shoji, et al. 1997. Eotaxin is a potent chemotaxin for human basophils. Biochemical Biophysical Research Communications 231: 365–368.

    Article  CAS  PubMed  Google Scholar 

  124. Hatano, Y., K. Katagiri, and S. Takayasu. 1999. Increased levels in vivo of mRNAs for IL-8 and macrophage inflammatory protein-1 alpha (MIP-1 alpha), but not of RANTES mRNA in peripheral blood mononuclear cells of patients with atopic dermatitis (AD). Clinical & Experimental Immunology 117: 237–243.

    Article  CAS  Google Scholar 

  125. Cheng, J.F., N.L. Ott, E.A. Peterson, T.J. George, M.J. Hukee, G.J. Gleich, et al. 1997. Dermal eosinophils in atopic dermatitis undergo cytolytic degeneration. Journal of Allergy and Clinical Immunology 99: 683–692.

    Article  CAS  PubMed  Google Scholar 

  126. Jahnz-Rozyk, K., T. Targowski, E. Paluchowska, W. Owczarek, and A. Kucharczyk. 2005. Serum thymus and activation-regulated chemokine, macrophage-derived chemokine and eotaxin as markers of severity of atopic dermatitis. Allergy 60: 685–688.

    Article  CAS  PubMed  Google Scholar 

  127. Gahr, N., R. Folster-Holst, M. Weichenthal, E. Christophers, J.M. Schroder, and J. Bartels. 2011. Dermal fibroblasts from acute inflamed atopic dermatitis lesions display increased eotaxin/CCL11 responsiveness to interleukin-4 stimulation. British Journal of Dermatology 164: 586–592.

    CAS  PubMed  Google Scholar 

  128. Yang, G.Y., X. Chen, Y.C. Sun, C.L. Ma, and G. Qian. 2013. Chemokine-like factor 1 (CLFK1) is over-expressed in patients with atopic dermatitis. International Journal of Biological Sciences 9: 759–765.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

This project was supported by a grant from the Rafsanjan University of Medical Sciences.

Author information

Authors and Affiliations

  1. Molecular Medicine Research Center, Rafsanjan University of Medical Sciences, Rafsanjan, Iran

    Zahra Ahmadi, Gholamhossein Hassanshahi, Hossein Khorramdelazad & Nahid Zainodini

  2. Department of Pediatrics, Tehran University of Medical Sciences, Tehran, Iran

    Leila Koochakzadeh

Authors
  1. Zahra Ahmadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gholamhossein Hassanshahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hossein Khorramdelazad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nahid Zainodini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Leila Koochakzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Leila Koochakzadeh.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmadi, Z., Hassanshahi, G., Khorramdelazad, H. et al. An Overlook to the Characteristics and Roles Played by Eotaxin Network in the Pathophysiology of Food Allergies: Allergic Asthma and Atopic Dermatitis. Inflammation 39, 1253–1267 (2016). https://doi.org/10.1007/s10753-016-0303-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10753-016-0303-9

KEY WORDS

Search

Navigation