Association between Two Single Nucleotide Polymorphisms of Thymic Stromal Lymphopoietin (TSLP) Gene and Asthma in Iranian Population
-
Maral Ranjbar
,
Mojdeh Matloubi
,
Mohammad-Ali Assarehzadegan
,
Morteza Fallahpour
,
Fatemeh Sadeghi
,
Saeed Soleyman-Jahi
,
Leila Janani
Abstract
Thymic stromal lymphopoietin (TSLP) is a cytokine similar to IL-7, which is released by airway epithelial cells in response to injury and inflammation. Current literature is contradictory about the association between different single nucleotide polymorphisms (SNPs) of the TSLP gene and asthma development in different countries.
We aimed to evaluate the association between two common TSLP SNPs (rs2289276 and rs2289278) and the risk of asthma in the Iranian population. Genotyping of the TSLP gene was performed in 126 adult asthmatic patients and 300 controls; using the TaqMan genotyping assay. Moreover, total serum IgE level and eosinophil count were assessed.
The results indicated that the TT genotype of rs2289276 was inversely associated with the risk of asthma (p=0.002). A similar inverse association was detected in subgroups of atopic (p=0.001) and non-atopic (p=0.005) asthma. Moreover, the TT genotype of this SNP was more prevalent in severe and late-onset categories of asthma. In subgroup analysis, a significant sex-specific association between rs2290276 and asthma was observed in women (p=0.004). The prevalence of rs2289276 was extremely low, which made it infeasible to perform any further analysis.
Overall, our findings indicated that rs2290276 SNP of the TSLP gene has a protective phenotype against asthma development in the Iranian population.
1. Mukherjee AB, Zhang Z. Allergic asthma: influence of genetic and environmental factors. J Biol Chem. 2011;286(38):32883-9.
2. Braman, SS. The global burden of asthma. Chest. 2006;130(1 Suppl):4s-12s.
3. Fazlollahi MR, Najmi M, Fallahnezhad M, Sabetkish N, Kazemnejad A, Bidad K, et al. The prevalence of asthma in Iranian adults: The first national survey and the most recent updates. Clin Respir J. 2018;12(5):1872-81.
4. Liu YJ. TSLP in epithelial cell and dendritic cell cross talk. Adv Immunol. 2009;101:1-25.
5. Tsilingiri K, Fornasa G, Rescigno M. Thymic Stromal Lymphopoietin: To Cut a Long Story Short. Cell Mol Gastroenterol Hepatol. 2017;3(2):174-82.
6. Wong CK, Hu S, Cheung PF, Lam CW. Thymic stromal lymphopoietin induces chemotactic and prosurvival effects in eosinophils: implications in allergic inflammation. Am J Respir Cell Mol Biol. 2010;43(3):305-15.
7. Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B, et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol. 2002;3(7):673-80.
8. Birben E, Sahiner UM, Karaaslan C, Yavuz TS, Cosgun E, Kalayci O, et al. The Genetic Variants of Thymic Stromal Lymphopoietin Protein in Children with Asthma and Allergic Rhinitis. Int Arch Allergy Immunol. 2014;163(3):185-92.
9. Elmaraghy MA, Hodieb MM, Khattab RAER, Abdelgalel MN. Association between TSLP gene polymorphism and bronchial asthma in children in Beni Suef Governorate in Egypt. Comp Clin Path. 2018;27(3):565-70.
10. Hunninghake GM, Soto-Quiros ME, Avila L, Kim HP, Lasky-Su J, Rafaels N, et al. TSLP polymorphisms are associated with asthma in a sex-specific fashion. Allergy. 2010;65(12):1566-75.
11. Harada M, Hirota T, Jodo AI, Hitomi Y, Sakashita M, Tsunoda T, et al. Thymic stromal lymphopoietin gene promoter polymorphisms are associated with susceptibility to bronchial asthma. Am J Respir Cell Mol Biol. 2011;44(6):787-93.
12. Liu M, Rogers L, Cheng Q, Shao Y, Fernandez-Beros ME, Hirschhorn JN, et al. Genetic variants of TSLP and asthma in an admixed urban population. PLoS ONE. 2011;6(9):e25099.
13. Liu W, Xu LS, Liu QJ, Dong FZ, Qiu RF, Wen MC, et al. Two single nucleotide polymorphisms in TSLP gene are associated with asthma susceptibility in Chinese Han population. Exp Lung Res. 2012;38(8):375-82.
14. Saba N, Raja GK, Yusuf O, Rehman S, Munir S, Mansoor A. Impacts of different cytokine and chemokine polymorphisms in Pakistani asthmatics a case control study. COPD Research and Practice. 2017;3(1):8.
15. Weber WW. Populations and genetic polymorphisms. Mol Diagn. 1999;4(4):299-307.
16. Mete F, Ozkaya E, Aras S, Koksal V, Etlik O, Baris I. Association between gene polymorphisms in TIM1, TSLP, IL18R1 and childhood asthma in Turkish population. Int J Clin Exp Med. 2014;7(4):1071-7.
17. Heinrich J, Richter K, Frye C, Meyer I, Wölke G, Wjst M, et al. European Community Respiratory Health Survey (ECRHS). Pneumologie. 2002;56(5):297-303.
18. Matloubi M, Ranjbar M, Assarehzadegan MA, Fallahpour M, Sadeghi F, Soleiman-Jahi S, et al. The Impact of Interleukin (IL)-33 Gene Polymorphisms and Environmental Factors on Risk of Asthma in the Iranian Population. Lung. 2020;198(1):105-112.
19. Le Moual N, Zock J-P, Dumas O, Lytras T, Andersson E, Lillienberg L, et al. Update of an occupational asthma-specific job exposure matrix to assess exposure to 30 specific agents. Occup Environ Med. 2018;75(7):507-14.
20. Moffatt MF, Gut IG, Demenais F, Strachan DP, Bouzigon E, Heath S, et al. A Large-Scale, Consortium-Based Genomewide Association Study of Asthma. N Engl J Med. 2010;363(13):1211-21.
21. Heinzerling L, Mari A, Bergmann K-C, Bresciani M, Burbach G, Darsow U, et al. The skin prick test – European standards. Clin Transl Allergy. 2013;3(1):3.
22. Assarehzadegan MA SH, Amini A. Sensitization to Common Aeroallergens among Asthmatic Patients in a Tropical Region Affected by Dust Storm. J Med Sci. 2013;13(7):592-7.
23. Standardization of Spirometry, 1994 Update. American Thoracic Society. Am J Respir Crit Care Med. 1995;152(3):1107-36.
24. Bateman ED, Hurd SS, Barnes PJ, Bousquet J, Drazen JM, FitzGerald M, et al. Global strategy for asthma management and prevention: GINA executive summary. Eur Respir J. 2008;31(1):143-78.
25. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16(3):1215.
26. Harada M, Hirota T, Jodo A, Doi S, Kameda M, Fujita K, et al. Functional analysis of the thymic stromal lymphopoietin variants in human bronchial epithelial cells. Am J Respir Cell Mol Biol. 2009;40(3):368-74.
27. Williams T, Admon A, Luscher B, Tjian R. Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements. Genes Dev. 1988;2(12a):1557-69.
28. Keselman, A, Heller N. Estrogen Signaling Modulates Allergic Inflammation and Contributes to Sex Differences in Asthma. Front Immunol. 2015;6:568.
29. Yung JA, Fuseini H, Newcomb DC. Hormones, sex, and asthma. Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology. 2018;120(5):488-94.
30. Cook EB, Stahl JL, Schwantes EA, Fox KE, Mathur SK. IL-3 and TNFα increase Thymic Stromal Lymphopoietin Receptor (TSLPR) expression on eosinophils and enhance TSLP-stimulated degranulation. Clin Mol Allergy. 2012;10(1):8.
2. Braman, SS. The global burden of asthma. Chest. 2006;130(1 Suppl):4s-12s.
3. Fazlollahi MR, Najmi M, Fallahnezhad M, Sabetkish N, Kazemnejad A, Bidad K, et al. The prevalence of asthma in Iranian adults: The first national survey and the most recent updates. Clin Respir J. 2018;12(5):1872-81.
4. Liu YJ. TSLP in epithelial cell and dendritic cell cross talk. Adv Immunol. 2009;101:1-25.
5. Tsilingiri K, Fornasa G, Rescigno M. Thymic Stromal Lymphopoietin: To Cut a Long Story Short. Cell Mol Gastroenterol Hepatol. 2017;3(2):174-82.
6. Wong CK, Hu S, Cheung PF, Lam CW. Thymic stromal lymphopoietin induces chemotactic and prosurvival effects in eosinophils: implications in allergic inflammation. Am J Respir Cell Mol Biol. 2010;43(3):305-15.
7. Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B, et al. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol. 2002;3(7):673-80.
8. Birben E, Sahiner UM, Karaaslan C, Yavuz TS, Cosgun E, Kalayci O, et al. The Genetic Variants of Thymic Stromal Lymphopoietin Protein in Children with Asthma and Allergic Rhinitis. Int Arch Allergy Immunol. 2014;163(3):185-92.
9. Elmaraghy MA, Hodieb MM, Khattab RAER, Abdelgalel MN. Association between TSLP gene polymorphism and bronchial asthma in children in Beni Suef Governorate in Egypt. Comp Clin Path. 2018;27(3):565-70.
10. Hunninghake GM, Soto-Quiros ME, Avila L, Kim HP, Lasky-Su J, Rafaels N, et al. TSLP polymorphisms are associated with asthma in a sex-specific fashion. Allergy. 2010;65(12):1566-75.
11. Harada M, Hirota T, Jodo AI, Hitomi Y, Sakashita M, Tsunoda T, et al. Thymic stromal lymphopoietin gene promoter polymorphisms are associated with susceptibility to bronchial asthma. Am J Respir Cell Mol Biol. 2011;44(6):787-93.
12. Liu M, Rogers L, Cheng Q, Shao Y, Fernandez-Beros ME, Hirschhorn JN, et al. Genetic variants of TSLP and asthma in an admixed urban population. PLoS ONE. 2011;6(9):e25099.
13. Liu W, Xu LS, Liu QJ, Dong FZ, Qiu RF, Wen MC, et al. Two single nucleotide polymorphisms in TSLP gene are associated with asthma susceptibility in Chinese Han population. Exp Lung Res. 2012;38(8):375-82.
14. Saba N, Raja GK, Yusuf O, Rehman S, Munir S, Mansoor A. Impacts of different cytokine and chemokine polymorphisms in Pakistani asthmatics a case control study. COPD Research and Practice. 2017;3(1):8.
15. Weber WW. Populations and genetic polymorphisms. Mol Diagn. 1999;4(4):299-307.
16. Mete F, Ozkaya E, Aras S, Koksal V, Etlik O, Baris I. Association between gene polymorphisms in TIM1, TSLP, IL18R1 and childhood asthma in Turkish population. Int J Clin Exp Med. 2014;7(4):1071-7.
17. Heinrich J, Richter K, Frye C, Meyer I, Wölke G, Wjst M, et al. European Community Respiratory Health Survey (ECRHS). Pneumologie. 2002;56(5):297-303.
18. Matloubi M, Ranjbar M, Assarehzadegan MA, Fallahpour M, Sadeghi F, Soleiman-Jahi S, et al. The Impact of Interleukin (IL)-33 Gene Polymorphisms and Environmental Factors on Risk of Asthma in the Iranian Population. Lung. 2020;198(1):105-112.
19. Le Moual N, Zock J-P, Dumas O, Lytras T, Andersson E, Lillienberg L, et al. Update of an occupational asthma-specific job exposure matrix to assess exposure to 30 specific agents. Occup Environ Med. 2018;75(7):507-14.
20. Moffatt MF, Gut IG, Demenais F, Strachan DP, Bouzigon E, Heath S, et al. A Large-Scale, Consortium-Based Genomewide Association Study of Asthma. N Engl J Med. 2010;363(13):1211-21.
21. Heinzerling L, Mari A, Bergmann K-C, Bresciani M, Burbach G, Darsow U, et al. The skin prick test – European standards. Clin Transl Allergy. 2013;3(1):3.
22. Assarehzadegan MA SH, Amini A. Sensitization to Common Aeroallergens among Asthmatic Patients in a Tropical Region Affected by Dust Storm. J Med Sci. 2013;13(7):592-7.
23. Standardization of Spirometry, 1994 Update. American Thoracic Society. Am J Respir Crit Care Med. 1995;152(3):1107-36.
24. Bateman ED, Hurd SS, Barnes PJ, Bousquet J, Drazen JM, FitzGerald M, et al. Global strategy for asthma management and prevention: GINA executive summary. Eur Respir J. 2008;31(1):143-78.
25. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16(3):1215.
26. Harada M, Hirota T, Jodo A, Doi S, Kameda M, Fujita K, et al. Functional analysis of the thymic stromal lymphopoietin variants in human bronchial epithelial cells. Am J Respir Cell Mol Biol. 2009;40(3):368-74.
27. Williams T, Admon A, Luscher B, Tjian R. Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements. Genes Dev. 1988;2(12a):1557-69.
28. Keselman, A, Heller N. Estrogen Signaling Modulates Allergic Inflammation and Contributes to Sex Differences in Asthma. Front Immunol. 2015;6:568.
29. Yung JA, Fuseini H, Newcomb DC. Hormones, sex, and asthma. Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology. 2018;120(5):488-94.
30. Cook EB, Stahl JL, Schwantes EA, Fox KE, Mathur SK. IL-3 and TNFα increase Thymic Stromal Lymphopoietin Receptor (TSLPR) expression on eosinophils and enhance TSLP-stimulated degranulation. Clin Mol Allergy. 2012;10(1):8.
| Files | ||
| Issue | Vol 19 No 4 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v19i4.4111 | |
| PMID | 33463103 | |
| Keywords | ||
| Ashthma Atopic Single nucleotide polymorphism Thymic stromal lymphopoietin | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Ranjbar M, Matloubi M, Assarehzadegan M-A, Fallahpour M, Sadeghi F, Soleyman-Jahi S, Janani L. Association between Two Single Nucleotide Polymorphisms of Thymic Stromal Lymphopoietin (TSLP) Gene and Asthma in Iranian Population. Iran J Allergy Asthma Immunol. 2020;19(4):362-372.
