Evaluating the Serum Levels of CCL17, CCL22, and CCL28 Chemokines and the Gene Expression of α4β1 and α4β7 Integrins in Patients With Allergic Rhinitis
-
Razieh Rezaeianpour
,
Ramin Lotfi
,
Seyed Hamidreza Mortazavi
,
Ali Gorgin Karaji
,
Alireza Rezaiemanesh
,
Farhad Salari
Abstract
Allergic rhinitis (AR) is a chronic inflammatory disease involving the nasal mucosa. Leukocytes recruitment to the inflammation sites is controlled by chemokines, cytokines, and adhesion molecules. Retinoic acid (RA), a vitamin A metabolite, plays an essential role in mucosal immunity and the production of inflammatory cytokines and chemokines. This study intended to evaluate the serum levels of RA, CCL17, CCL22, CCL28, and the mRNA expression levels of α4, β1, and β7 integrins in AR patients compared to healthy subjects. Peripheral blood was collected from 37 patients with AR and 30 age- and gender-matched healthy individuals. Serum levels of RA, CCL17, CCL22, and CCL28 were measured by the enzyme-linked immunosorbent assay (ELISA) technique, and the mRNA expression levels for α4, β1, and β7 integrins were assessed using the quantitative real-time PCR method. Our results showed that the serum levels of CCL22 and CCL28 chemokines are significantly higher in the AR group compared to the healthy controls (P<0.01). However, the gene expression of the β1 integrin in the AR group was significantly lower than that of the control group (P<0.001). Besides, there was a positive association between serum RA and CCL17 levels in patients (P<0.0001, r=0.6). In conclusion, increased serum levels of CCL22 and CCL28 chemokines, as well as decreased gene expression of β1 integrin in AR patients, may contribute to the pathogenesis and/or exacerbation of AR.
1. Bellanti JA, Wallerstedt DB. Allergic rhinitis update: epidemiology and natural history. Allergy Asthma Proc 2000;21:367-70.
2. Seaton A, Godden DJ, Brown K. Increase in asthma: a more toxic environment or a more susceptible population? Thorax 1994;49:171-4.
3. Patel S, Murray C, Woodcock A, Simpson A, Custovic A. Dietary antioxidant intake, allergic sensitization and allergic diseases in young children. Allergy 2009;64:1766-72.
4. Mora JR, Iwata M, Von Andrian UH. Vitamin effects on the immune system: vitamins A and D take centre stage. Nat Rev Immunol 2008;8:685-98.
5. Erkelens MN, Mebius RE. Retinoic Acid and Immune Homeostasis: A Balancing Act. Trends Immunol 2017;38:168-80.
6. Hoag KA, Nashold FE, Goverman J, Hayes CE. Retinoic acid enhances the T helper 2 cell development that is essential for robust antibody responses through its action on antigen-presenting cells. J Nutr 2002;132:3736-9.
7. Tokuyama H, Tokuyama Y, Nakanishi K. Retinoids inhibit IL-4-dependent IgE and IgG1 production by LPS-stimulated murine splenic B cells. Cell Immunol 1995;162:153-8.
8. Grenningloh R, Gho A, Di Lucia P, Klaus M, Bollag W, Ho I-C, et al. Cutting Edge: Inhibition of the retinoid X receptor (RXR) blocks T helper 2 differentiation and prevents allergic lung inflammation. J Immunol 2006;176:5161-6.
9. Matheu V, Berggård K, Barrios Y, Barrios Y, Arnau MR, Zubeldia JM, et al. Impact on allergic immune response after treatment with vitamin A. Nutr Metab (Lond) 2009;6:44.
10. Nakano H, Free ME, Whitehead G, Maruoka S, Wilson R, Nakano K, et al. Pulmonary CD103+ dendritic cells prime Th2 responses to inhaled allergens. Mucosal Immunol 2012;5:53-65.
11. Butcher EC, Picker LJ. Lymphocyte homing and homeostasis. Science 1996;272:60-6.
12. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000;18:217-42.
13. Rot A, Von Andrian UH. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol 2004;22:891-928.
14. Schuh JM, Blease K, Hogaboam CMJ. CXCR2 is necessary for the development and persistence of chronic fungal asthma in mice. J Immunol 2002;168:1447-56.
15. Penna G, Vulcano M, Roncari A, Facchetti F, Sozzani S, Adorini L. Cutting edge: differential chemokine production by myeloid and plasmacytoid dendritic cells. J Immunol 2002;169:6673-6.
16. Ezzat M, Shaheen K. Serum mucosa-associated epithelial chemokine in atopic dermatitis: a specific marker for severity. Indian J Dermatol 2009;54:229-36.
17. Wang W, Soto H, Oldham ER, Buchanan ME, Homey B, Catron D, et al. Identification of a novel chemokine (CCL28), which binds CCR10 (GPR2). J Biol Chem 2000;275:22313-23.
18. Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992;69:11-25.
19. Hood JD, Cheresh DA. Role of integrins in cell invasion and migration. Nat Rev Cancer 2002;2:91-100.
20. Giancotti FG, Ruoslahti E. Integrin signaling. Science 1999;285:1028-33.
21. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002;110:673-87.
22. Schweighoffer T, Tanaka Y, Tidswell M, Erle D, Horgan K, Luce G, et al. Selective expression of integrin alpha 4 beta 7 on a subset of human CD4+ memory T cells with Hallmarks of gut-trophism. J Immunol 1993;151:717-29.
23. Erle DJ, Briskin MJ, Butcher EC, Garcia-Pardo A, Lazarovits AI, Tidswell M. Expression and function of the MAdCAM-1 receptor, integrin alpha 4 beta 7, on human leukocytes. J Immunol 1994;153:517-28.
24. Rott LS, Briskin MJ, Andrew DP, Berg EL, Butcher EC. A fundamental subdivision of circulating lymphocytes defined by adhesion to mucosal addressin cell adhesion molecule-1. Comparison with vascular cell adhesion molecule-1 and correlation with beta 7 integrins and memory differentiation. J Immunol 1996;156:3727-36.
25. von Andrian UH, Mackay CR. T-cell function and migration. Two sides of the same coin. N Engl J Med 2000;343:1020-34.
26. DeNucci CC, Pagán AJ, Mitchell JS, Shimizu Y. Control of α4β7 integrin expression and CD4 T cell homing by the β1 integrin subunit. J Immunol 2010;184:2458-67.
27. Komoriya A, Green L, Mervic M, Yamada S, Yamada K, Humphries M. The minimal essential sequence for a major cell type-specific adhesion site (CS1) within the alternatively spliced type III connecting segment domain of fibronectin is leucine-aspartic acid-valine. J Biol Chem 1991;266:15075-9.
28. Shyjan AM, Bertagnolli M, Kenney CJ, Briskin MJ. Human mucosal addressin cell adhesion molecule-1 (MAdCAM-1) demonstrates structural and functional similarities to the alpha 4 beta 7-integrin binding domains of murine MAdCAM-1, but extreme divergence of mucin-like sequences. J Immunol 1996;156:2851-7.
29. Rivera-Nieves J, Olson T, Bamias G, Bruce A, Solga M, Knight RF, et al. L-selectin, α4β1, and α4β7 integrins participate in CD4+ T cell recruitment to chronically inflamed small intestine. J Immunol 2005;174:2343-52.
30. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45.
31. Sly RM. Changing prevalence of allergic rhinitis and asthma. Ann Allergy Asthma Immunol 1999;82:233-48.
32. Cortijo J, Sanz MJ, Iranzo A, Montesinos JL, Nabah YNA, Alfón J, et al. A small molecule, orally active, α4β1/α4β7 dual antagonist reduces leukocyte infiltration and airway hyper‐responsiveness in an experimental model of allergic asthma in Brown Norway rats. Br J Pharmacol 2006;147:661-70.
33. Godiska R, Chantry D, Raport CJ, Sozzani S, Allavena P, Leviten D, et al. Human macrophage–derived chemokine (MDC), a novel chemoattractant for monocytes, monocyte-derived dendritic cells, and natural killer cells. J Exp Med 1997;185:1595-604.
34. Vermaelen K, Pauwels R. Pulmonary dendritic cells. Am J Respir Crit Care Med 2005;172:530-51.
35. Hijnen D, de Bruin-Weller M, Oosting B, Lebre C, de Jong E, Bruijnzeel-Koomen C, et al. Serum thymus and activation-regulated chemokine (TARC) and cutaneous T cell–attracting chemokine (CTACK) levels in allergic diseases: TARC and CTACK are disease-specific markers for atopic dermatitis. J Allergy Clin Immunol 2004;113:334-40.
36. Vijayanand P, Durkin K, Hartmann G, Morjaria J, Seumois G, Staples KJ, et al. Chemokine receptor 4 plays a key role in T cell recruitment into the airways of asthmatic patients. J Immunol 2010;184:4568-74.
37. Wågsäter D, Dienus O, Löfgren S, Hugander A, Dimberg J. Quantification of the chemokines CCL17 and CCL22 in human colorectal adenocarcinomas. Mol Med Rep 2008;1:211-7.
38. Cheung DS, Ehlenbach SJ, Kitchens T, Riley DA, Grayson MH. Development of atopy by severe paramyxoviral infection in a mouse model. Ann Allergy Asthma Immunol 2010;105:437-43.e1.
39. Khan SH, Park SS, Sirajuddin IA, Grayson MH. Respiratory virus and asthma: the role of immunoglobulin E. Clin Ther 2008;30:1017-24.
40. John AE, Thomas MS, Berlin AA, Lukacs NW. Temporal production of CCL28 corresponds to eosinophil accumulation and airway hyperreactivity in allergic airway inflammation. Am J Pathol 2005;166:345-53.
41. Hieshima K, Ohtani H, Shibano M, Izawa D, Nakayama T, Kawasaki Y, et al. CCL28 has dual roles in mucosal immunity as a chemokine with broad-spectrum antimicrobial activity. J Immunol 2003;170:1452-61.
42. Hanamoto H, Nakayama T, Miyazato H, Takegawa S, Hieshima K, Tatsumi Y, et al. Expression of CCL28 by Reed-Sternberg cells defines a major subtype of classical Hodgkin's disease with frequent infiltration of eosinophils and/or plasma cells. Am J Pathol 2004;164:997-1006.
43. Danilova E, Skrindo I, Gran E, Hales B, Smith W, Jahnsen J, et al. A role for CCL28–CCR3 in T-cell homing to the human upper airway mucosa. Mucosal Immunol 2015;8:107-14.
44. Pan J, Kunkel EJ, Gosslar U, Lazarus N, Langdon P, Broadwell K, et al. Cutting edge: a novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J Immunol 2000;165:2943-9.
45. Nagakubo D, Yoshie O, Hirata T. Upregulated CCL28 expression in the nasal mucosa in experimental allergic rhinitis: Implication for CD4+ memory T cell recruitment. Cell Immunol 2016;302:58-62.
46. Hiroi T, Iwatani K, Iijima H, Kodama S, Yanagita M, Kiyono H. Nasal immune system: distinctive Th0 and Th1/Th2 type environments in murine nasal‐associated lymphoid tissues and nasal passage, respectively. Eur J Immunol 1998;28:3346-53.
47. Cassani B, Villablanca EJ, De Calisto J, Wang S, Mora JR. Vitamin A and immune regulation: role of retinoic acid in gut-associated dendritic cell education, immune protection and tolerance. Mol Aspects Med 2012;33:63-76.
48. Yokota-Nakatsuma A, Takeuchi H, Ohoka Y, Kato C, Song S, Hoshino T, et al. Retinoic acid prevents mesenteric lymph node dendritic cells from inducing IL-13-producing inflammatory Th2 cells. Mucosal Immunol 2014;7:786-801.
49. Mucida D, Park Y, Kim G, Turovskaya O, Scott I, Kronenberg M, et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007;317:256-60.
50. Wu J, Zhang Y, Liu Q, Zhong W, Xia Z. All-trans retinoic acid attenuates airway inflammation by inhibiting Th2 and Th17 response in experimental allergic asthma. BMC Immunol 2013;14:28.
51. Mielke LA, Jones SA, Raverdeau M, Higgs R, Stefanska A, Groom JR, et al. Retinoic acid expression associates with enhanced IL-22 production by γδ T cells and innate lymphoid cells and attenuation of intestinal inflammation. J Exp Med 2013;210:1117-24.
52. Terada N, Nomura T, Kim W, Otsuka Y, Takahashi R, Kishi H, et al. Expression of C–C chemokine TARC in human nasal mucosa and its regulation by cytokines. Clin Exp Allergy 2001;31:1923-31.
53. Berin MC, Eckmann L, Broide DH, Kagnoff MF. Regulated production of the T helper 2–type T-cell chemoattractant TARC by human bronchial epithelial cells in vitro and in human lung xenografts. Am J Respir Cell Mol Biol 2001;24:382-9.
54. Manabe K, Nishioka Y, Kishi J, Inayama M, Aono Y, Nakamura Y, et al. Elevation of macrophage-derived chemokine in eosinophilic pneumonia: a role of alveolar macrophages. J Med Invest 2005;52:85-92.
55. Pilette C, Francis J, Till S, Durham S. CCR4 ligands are up-regulated in the airways of atopic asthmatics after segmental allergen challenge. Eur Respir J 2004;23:876-84.
56. Herter J, Zarbock A. Integrin regulation during leukocyte recruitment. J Immunol 2013;190:4451-7.
57. Hemler ME, Elices MJ, Parker C, Takada Y. Structure of the integrin VLA‐4 and its cell‐cell and cell‐matrix adhesion functions. Immunol Rev 1990;114:45-65.
58. Berlin C, Berg EL, Briskin MJ, Andrew DP, Kilshaw PJ, Holzmann B, et al. α4β7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell 1993;74:185-95.
59. Bourges D, Chevaleyre C, Wang C, Berri M, Zhang X, Nicaise L, et al. Differential expression of adhesion molecules and chemokines between nasal and small intestinal mucosae: implications for T‐and sIgA+ B‐lymphocyte recruitment. Immunology 2007;122:551-61.
60. Johansson MW, Mosher DF. Integrin activation states and eosinophil recruitment in asthma. Front Pharmacol 2013;4:33.
61. Seminario MC, Bochner BS. Expression and function of beta 1 integrins on human eosinophils. Mem Inst Oswaldo Cruz 1997;92 Suppl 2:157-64.
62. Yao L, Pan J, Setiadi H, Patel KD, McEver RP. Interleukin 4 or oncostatin M induces a prolonged increase in P-selectin mRNA and protein in human endothelial cells. J Exp Med 1996;184:81-92.
63. Sanz MJ, Marinova-Mutafchieva L, Green P, Lobb RR, Feldmann M, Nourshargh S. IL-4-induced eosinophil accumulation in rat skin is dependent on endogenous TNF-α and α4 integrin/VCAM-1 adhesion pathways. J Immunol 1998;160:5637-45.
64. Hickey MJ, Granger DN, Kubes P. Molecular mechanisms underlying IL-4-induced leukocyte recruitment in vivo: a critical role for the α4 integrin. J Immunol 1999;163:3441-8.
65. Xu B, Aoyama K, Kusumoto M, Matsuzawa A, Butcher EC, Michie SA, et al. Lack of lymphoid chemokines CCL19 and CCL21 enhances allergic airway inflammation in mice. Int Immunol 2007;19:775-84.
2. Seaton A, Godden DJ, Brown K. Increase in asthma: a more toxic environment or a more susceptible population? Thorax 1994;49:171-4.
3. Patel S, Murray C, Woodcock A, Simpson A, Custovic A. Dietary antioxidant intake, allergic sensitization and allergic diseases in young children. Allergy 2009;64:1766-72.
4. Mora JR, Iwata M, Von Andrian UH. Vitamin effects on the immune system: vitamins A and D take centre stage. Nat Rev Immunol 2008;8:685-98.
5. Erkelens MN, Mebius RE. Retinoic Acid and Immune Homeostasis: A Balancing Act. Trends Immunol 2017;38:168-80.
6. Hoag KA, Nashold FE, Goverman J, Hayes CE. Retinoic acid enhances the T helper 2 cell development that is essential for robust antibody responses through its action on antigen-presenting cells. J Nutr 2002;132:3736-9.
7. Tokuyama H, Tokuyama Y, Nakanishi K. Retinoids inhibit IL-4-dependent IgE and IgG1 production by LPS-stimulated murine splenic B cells. Cell Immunol 1995;162:153-8.
8. Grenningloh R, Gho A, Di Lucia P, Klaus M, Bollag W, Ho I-C, et al. Cutting Edge: Inhibition of the retinoid X receptor (RXR) blocks T helper 2 differentiation and prevents allergic lung inflammation. J Immunol 2006;176:5161-6.
9. Matheu V, Berggård K, Barrios Y, Barrios Y, Arnau MR, Zubeldia JM, et al. Impact on allergic immune response after treatment with vitamin A. Nutr Metab (Lond) 2009;6:44.
10. Nakano H, Free ME, Whitehead G, Maruoka S, Wilson R, Nakano K, et al. Pulmonary CD103+ dendritic cells prime Th2 responses to inhaled allergens. Mucosal Immunol 2012;5:53-65.
11. Butcher EC, Picker LJ. Lymphocyte homing and homeostasis. Science 1996;272:60-6.
12. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000;18:217-42.
13. Rot A, Von Andrian UH. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol 2004;22:891-928.
14. Schuh JM, Blease K, Hogaboam CMJ. CXCR2 is necessary for the development and persistence of chronic fungal asthma in mice. J Immunol 2002;168:1447-56.
15. Penna G, Vulcano M, Roncari A, Facchetti F, Sozzani S, Adorini L. Cutting edge: differential chemokine production by myeloid and plasmacytoid dendritic cells. J Immunol 2002;169:6673-6.
16. Ezzat M, Shaheen K. Serum mucosa-associated epithelial chemokine in atopic dermatitis: a specific marker for severity. Indian J Dermatol 2009;54:229-36.
17. Wang W, Soto H, Oldham ER, Buchanan ME, Homey B, Catron D, et al. Identification of a novel chemokine (CCL28), which binds CCR10 (GPR2). J Biol Chem 2000;275:22313-23.
18. Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992;69:11-25.
19. Hood JD, Cheresh DA. Role of integrins in cell invasion and migration. Nat Rev Cancer 2002;2:91-100.
20. Giancotti FG, Ruoslahti E. Integrin signaling. Science 1999;285:1028-33.
21. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002;110:673-87.
22. Schweighoffer T, Tanaka Y, Tidswell M, Erle D, Horgan K, Luce G, et al. Selective expression of integrin alpha 4 beta 7 on a subset of human CD4+ memory T cells with Hallmarks of gut-trophism. J Immunol 1993;151:717-29.
23. Erle DJ, Briskin MJ, Butcher EC, Garcia-Pardo A, Lazarovits AI, Tidswell M. Expression and function of the MAdCAM-1 receptor, integrin alpha 4 beta 7, on human leukocytes. J Immunol 1994;153:517-28.
24. Rott LS, Briskin MJ, Andrew DP, Berg EL, Butcher EC. A fundamental subdivision of circulating lymphocytes defined by adhesion to mucosal addressin cell adhesion molecule-1. Comparison with vascular cell adhesion molecule-1 and correlation with beta 7 integrins and memory differentiation. J Immunol 1996;156:3727-36.
25. von Andrian UH, Mackay CR. T-cell function and migration. Two sides of the same coin. N Engl J Med 2000;343:1020-34.
26. DeNucci CC, Pagán AJ, Mitchell JS, Shimizu Y. Control of α4β7 integrin expression and CD4 T cell homing by the β1 integrin subunit. J Immunol 2010;184:2458-67.
27. Komoriya A, Green L, Mervic M, Yamada S, Yamada K, Humphries M. The minimal essential sequence for a major cell type-specific adhesion site (CS1) within the alternatively spliced type III connecting segment domain of fibronectin is leucine-aspartic acid-valine. J Biol Chem 1991;266:15075-9.
28. Shyjan AM, Bertagnolli M, Kenney CJ, Briskin MJ. Human mucosal addressin cell adhesion molecule-1 (MAdCAM-1) demonstrates structural and functional similarities to the alpha 4 beta 7-integrin binding domains of murine MAdCAM-1, but extreme divergence of mucin-like sequences. J Immunol 1996;156:2851-7.
29. Rivera-Nieves J, Olson T, Bamias G, Bruce A, Solga M, Knight RF, et al. L-selectin, α4β1, and α4β7 integrins participate in CD4+ T cell recruitment to chronically inflamed small intestine. J Immunol 2005;174:2343-52.
30. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45.
31. Sly RM. Changing prevalence of allergic rhinitis and asthma. Ann Allergy Asthma Immunol 1999;82:233-48.
32. Cortijo J, Sanz MJ, Iranzo A, Montesinos JL, Nabah YNA, Alfón J, et al. A small molecule, orally active, α4β1/α4β7 dual antagonist reduces leukocyte infiltration and airway hyper‐responsiveness in an experimental model of allergic asthma in Brown Norway rats. Br J Pharmacol 2006;147:661-70.
33. Godiska R, Chantry D, Raport CJ, Sozzani S, Allavena P, Leviten D, et al. Human macrophage–derived chemokine (MDC), a novel chemoattractant for monocytes, monocyte-derived dendritic cells, and natural killer cells. J Exp Med 1997;185:1595-604.
34. Vermaelen K, Pauwels R. Pulmonary dendritic cells. Am J Respir Crit Care Med 2005;172:530-51.
35. Hijnen D, de Bruin-Weller M, Oosting B, Lebre C, de Jong E, Bruijnzeel-Koomen C, et al. Serum thymus and activation-regulated chemokine (TARC) and cutaneous T cell–attracting chemokine (CTACK) levels in allergic diseases: TARC and CTACK are disease-specific markers for atopic dermatitis. J Allergy Clin Immunol 2004;113:334-40.
36. Vijayanand P, Durkin K, Hartmann G, Morjaria J, Seumois G, Staples KJ, et al. Chemokine receptor 4 plays a key role in T cell recruitment into the airways of asthmatic patients. J Immunol 2010;184:4568-74.
37. Wågsäter D, Dienus O, Löfgren S, Hugander A, Dimberg J. Quantification of the chemokines CCL17 and CCL22 in human colorectal adenocarcinomas. Mol Med Rep 2008;1:211-7.
38. Cheung DS, Ehlenbach SJ, Kitchens T, Riley DA, Grayson MH. Development of atopy by severe paramyxoviral infection in a mouse model. Ann Allergy Asthma Immunol 2010;105:437-43.e1.
39. Khan SH, Park SS, Sirajuddin IA, Grayson MH. Respiratory virus and asthma: the role of immunoglobulin E. Clin Ther 2008;30:1017-24.
40. John AE, Thomas MS, Berlin AA, Lukacs NW. Temporal production of CCL28 corresponds to eosinophil accumulation and airway hyperreactivity in allergic airway inflammation. Am J Pathol 2005;166:345-53.
41. Hieshima K, Ohtani H, Shibano M, Izawa D, Nakayama T, Kawasaki Y, et al. CCL28 has dual roles in mucosal immunity as a chemokine with broad-spectrum antimicrobial activity. J Immunol 2003;170:1452-61.
42. Hanamoto H, Nakayama T, Miyazato H, Takegawa S, Hieshima K, Tatsumi Y, et al. Expression of CCL28 by Reed-Sternberg cells defines a major subtype of classical Hodgkin's disease with frequent infiltration of eosinophils and/or plasma cells. Am J Pathol 2004;164:997-1006.
43. Danilova E, Skrindo I, Gran E, Hales B, Smith W, Jahnsen J, et al. A role for CCL28–CCR3 in T-cell homing to the human upper airway mucosa. Mucosal Immunol 2015;8:107-14.
44. Pan J, Kunkel EJ, Gosslar U, Lazarus N, Langdon P, Broadwell K, et al. Cutting edge: a novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J Immunol 2000;165:2943-9.
45. Nagakubo D, Yoshie O, Hirata T. Upregulated CCL28 expression in the nasal mucosa in experimental allergic rhinitis: Implication for CD4+ memory T cell recruitment. Cell Immunol 2016;302:58-62.
46. Hiroi T, Iwatani K, Iijima H, Kodama S, Yanagita M, Kiyono H. Nasal immune system: distinctive Th0 and Th1/Th2 type environments in murine nasal‐associated lymphoid tissues and nasal passage, respectively. Eur J Immunol 1998;28:3346-53.
47. Cassani B, Villablanca EJ, De Calisto J, Wang S, Mora JR. Vitamin A and immune regulation: role of retinoic acid in gut-associated dendritic cell education, immune protection and tolerance. Mol Aspects Med 2012;33:63-76.
48. Yokota-Nakatsuma A, Takeuchi H, Ohoka Y, Kato C, Song S, Hoshino T, et al. Retinoic acid prevents mesenteric lymph node dendritic cells from inducing IL-13-producing inflammatory Th2 cells. Mucosal Immunol 2014;7:786-801.
49. Mucida D, Park Y, Kim G, Turovskaya O, Scott I, Kronenberg M, et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007;317:256-60.
50. Wu J, Zhang Y, Liu Q, Zhong W, Xia Z. All-trans retinoic acid attenuates airway inflammation by inhibiting Th2 and Th17 response in experimental allergic asthma. BMC Immunol 2013;14:28.
51. Mielke LA, Jones SA, Raverdeau M, Higgs R, Stefanska A, Groom JR, et al. Retinoic acid expression associates with enhanced IL-22 production by γδ T cells and innate lymphoid cells and attenuation of intestinal inflammation. J Exp Med 2013;210:1117-24.
52. Terada N, Nomura T, Kim W, Otsuka Y, Takahashi R, Kishi H, et al. Expression of C–C chemokine TARC in human nasal mucosa and its regulation by cytokines. Clin Exp Allergy 2001;31:1923-31.
53. Berin MC, Eckmann L, Broide DH, Kagnoff MF. Regulated production of the T helper 2–type T-cell chemoattractant TARC by human bronchial epithelial cells in vitro and in human lung xenografts. Am J Respir Cell Mol Biol 2001;24:382-9.
54. Manabe K, Nishioka Y, Kishi J, Inayama M, Aono Y, Nakamura Y, et al. Elevation of macrophage-derived chemokine in eosinophilic pneumonia: a role of alveolar macrophages. J Med Invest 2005;52:85-92.
55. Pilette C, Francis J, Till S, Durham S. CCR4 ligands are up-regulated in the airways of atopic asthmatics after segmental allergen challenge. Eur Respir J 2004;23:876-84.
56. Herter J, Zarbock A. Integrin regulation during leukocyte recruitment. J Immunol 2013;190:4451-7.
57. Hemler ME, Elices MJ, Parker C, Takada Y. Structure of the integrin VLA‐4 and its cell‐cell and cell‐matrix adhesion functions. Immunol Rev 1990;114:45-65.
58. Berlin C, Berg EL, Briskin MJ, Andrew DP, Kilshaw PJ, Holzmann B, et al. α4β7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell 1993;74:185-95.
59. Bourges D, Chevaleyre C, Wang C, Berri M, Zhang X, Nicaise L, et al. Differential expression of adhesion molecules and chemokines between nasal and small intestinal mucosae: implications for T‐and sIgA+ B‐lymphocyte recruitment. Immunology 2007;122:551-61.
60. Johansson MW, Mosher DF. Integrin activation states and eosinophil recruitment in asthma. Front Pharmacol 2013;4:33.
61. Seminario MC, Bochner BS. Expression and function of beta 1 integrins on human eosinophils. Mem Inst Oswaldo Cruz 1997;92 Suppl 2:157-64.
62. Yao L, Pan J, Setiadi H, Patel KD, McEver RP. Interleukin 4 or oncostatin M induces a prolonged increase in P-selectin mRNA and protein in human endothelial cells. J Exp Med 1996;184:81-92.
63. Sanz MJ, Marinova-Mutafchieva L, Green P, Lobb RR, Feldmann M, Nourshargh S. IL-4-induced eosinophil accumulation in rat skin is dependent on endogenous TNF-α and α4 integrin/VCAM-1 adhesion pathways. J Immunol 1998;160:5637-45.
64. Hickey MJ, Granger DN, Kubes P. Molecular mechanisms underlying IL-4-induced leukocyte recruitment in vivo: a critical role for the α4 integrin. J Immunol 1999;163:3441-8.
65. Xu B, Aoyama K, Kusumoto M, Matsuzawa A, Butcher EC, Michie SA, et al. Lack of lymphoid chemokines CCL19 and CCL21 enhances allergic airway inflammation in mice. Int Immunol 2007;19:775-84.
| Files | ||
| Issue | Vol 61 No 8 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/acta.v61i8.14903 | |
| Keywords | ||
| Allergic rhinitis Retinoic acid Chemokine (C-C Motif) ligand 17 (CCL17) α4β1 α4β7 | ||
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How to Cite
1.
Rezaeianpour R, Lotfi R, Mortazavi SH, Gorgin Karaji A, Rezaiemanesh A, Salari F. Evaluating the Serum Levels of CCL17, CCL22, and CCL28 Chemokines and the Gene Expression of α4β1 and α4β7 Integrins in Patients With Allergic Rhinitis. Acta Med Iran. 2024;61(8):459-467.
