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Association of HLA-DQ and IL13 gene variants with challenge-proven shrimp allergy in West Bengal, India

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Abstract

Little is known about genetic factors and mechanisms underlying shrimp allergy. Genome-wide association studies identified HLA class-II and IL13 genes as highly plausible candidates for shrimp allergy. The present study was designed to investigate potential associations of HLA-DQ rs9275596, IL13 rs20541, and IL13 rs1800925 polymorphisms with challenge-proven shrimp allergy using the data from 532 people of West Bengal, India; selected on basis of positive skin prick test, elevated specific IgE and medical history. Risk genotypes, i.e., HLA-DQ rs9275596 CC, IL13 rs20541 AA, and IL13 rs1800925 TT, were found to be significantly associated with challenge positive shrimp allergy (P = 0.04, 0.01, and 0.03, respectively). Distribution of genotypes for HLA-DQ and IL13 polymorphisms in allergic and control subjects showed significant difference between younger (20–40 years) and older (> 40 years) age group (P = 0.006). Risk genotypes significantly associated with elevated shrimp-specific IgE. IL13 TA haplotype significantly associated with shrimp allergy and elevated specific IgE (P = 0.02). Synergistic effect of IL13 TA haplotype–HLA-DQ rs9275596 CC genotype interaction significantly elevated specific IgE (P = 0.03). The present study suggests that HLA-DQ and IL13 polymorphisms pose major risk for shrimp allergic patients in West Bengal, India and thus could be helpful for early target-specific therapeutic intervention in near future.

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Data availability

The datasets generated and/or analyzed during the current study are not publicly available due to consent requirements to protect subjects’ privacy but are available from the corresponding author on reasonable request.

References

  • Arima K, Umeshita-Suyama R, Sakata Y et al (2002) Upregulation of IL-13 concentration in vivo by the IL13 variant associated with bronchial asthma. J Allergy Clin Immunol 109(6):980–7

    CAS  PubMed  Google Scholar 

  • Ashley SE, Tan HTT, Peters R et al (2017) Genetic variation at the Th2 immune gene IL13 is associated with IgE-mediated paediatric food allergy. Clin Exp Allergy 47(8):1032–1037

    CAS  PubMed  Google Scholar 

  • Cameron L, Webster RB, Strempel JM et al (2006) Th2 cell-selective enhancement of human IL13 transcription by IL13 -1112C>T, a polymorphism associated with allergic inflammation. J Immunol 177(12):8633–42

    CAS  PubMed  Google Scholar 

  • Carnes J, Ferrer A, Huertas AJ et al (2007) The use of raw or boiled crustacean extracts for the diagnosis of seafood allergic individuals. Ann Allergy Asthma Immunol 98(4):349–354

    CAS  PubMed  Google Scholar 

  • Chen W, Ericksen MB, Levin LS et al (2004) Functional effect of the R110Q IL13 genetic variant alone and in combination with IL4RA genetic variants. J Allergy Clin Immunol 114:553–60

    CAS  PubMed  Google Scholar 

  • Daly MJ, Rioux JD, Schaffner SF et al (2001) High-resolution haplotype structure in the human genome. Nat Genet 29:229–232

    CAS  PubMed  Google Scholar 

  • Dey D, Ghosh N, Pandey N et al (2014) A hospital-based survey on food allergy in the population of Kolkata, India. Int Arch Allergy Immunol 164:218–21

    CAS  PubMed  Google Scholar 

  • Dimitrov I, Doytchinova I (2016) Associations between milk and egg allergens and the HLA-DRB1/DQ polymorphism: a bioinformatics approach. Int Arch Allergy Immunol 169:33–39

    CAS  PubMed  Google Scholar 

  • Ebisawa M, Ito K, Fujisawa T (2017) Committee for Japanese Pediatric Guideline for Food Allergy, The Japanese Society of Pediatric Allergy and Clinical Immunology, The Japanese Society of Allergology Japanese guidelines for food allergy 2017. Allergol Int 66:248–264

  • Gabriel SB, Schaffner SF, Nguyen H et al (2002) The structure of haplotype blocks in the human genome. Science 296(5576):2225–9

    CAS  PubMed  Google Scholar 

  • Graves PE, Kabesch M, Halonen M et al (2000) A cluster of seven tightly linked polymorphisms in the IL-13 gene is associated with total serum IgE levels in three populations of white children. J Allergy Clin Immunol 105(3):506–13

    CAS  PubMed  Google Scholar 

  • Gupta R, Holdford D, Bilaver L et al (2013) The economic impact of childhood food allergy in the United States. JAMA Pediatr 134(Suppl 3):S149–S150

    Google Scholar 

  • Hoffjan S, Nicolae D, Ober C (2003) Association studies for asthma and atopic diseases: a comprehensive review of the literature. Respir Res 4(1):14

    PubMed  PubMed Central  Google Scholar 

  • Hong X, Tsai HJ, Wang X (2009) Genetics of food allergy. Curr Opin Pediatr 21:770–776

    PubMed  PubMed Central  Google Scholar 

  • Hong X, Hao K, Ladd-Acosta C et al (2015) Genome-wide association study identifies peanut allergy-specific loci and evidence of epigenetic mediation in US children. Nat Commun 6:6304

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kazemi S, Vaisi-Raygani A, Keramat F et al (2019) Evaluation of the relationship between IL12, IL-13 and TNF-α gene polymorphisms with the susceptibility to brucellosis: a case control study. BMC Infect Dis 19:1036

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khor SS, Morino R, Nakazono K et al (2018) Genome-wide association study of self-reported food reactions in Japanese identifies shrimp and peach specific loci in the HLA-DR/DQ gene region. Sci Rep 8(1):1069

    PubMed  PubMed Central  Google Scholar 

  • Kodgule RR, Singh V, Dhar R et al (2014) Reference values for peak expiratory flow in Indian adult population using a European Union scale peak flow meter. J Postgrad Med 60(2):123–9

    CAS  PubMed  Google Scholar 

  • Kumar R, Kumari D, Srivastava P et al (2010) Identification of IgE-mediated food allergy and allergens in older children and adults with asthma and allergic rhinitis. Indian J Chest Dis Allied Sci 52(4):217–24

    PubMed  Google Scholar 

  • Laha A, Ghosh A, Moitra S et al (2020) Association of STAT6 rs3024974 (C/T) polymorphism with IgE mediated food sensitization among West Bengal population. India. Int Arch Allergy Immunol 181(3):200–210

    CAS  PubMed  Google Scholar 

  • Lertnawapan R, Maek-a-nantawat W (2011) Anaphylaxis and biphasic phase in Thailand: 4-year observation. Allergol Int 60:283–289

    PubMed  Google Scholar 

  • Liu X, Nickel R, Beyer K et al (2000) An IL13 coding region variant is associated with a high total serum IgE level and atopic dermatitis in the German multicenter atopy study (MAS-90). J Allergy Clin Immunol 106:167–70

    CAS  PubMed  Google Scholar 

  • Liu X, Beaty TH, Deindl P et al (2004) Associations between specific serum IgE response and 6 variants within the genes IL4, IL13, and IL4RA in German children: the German Multicenter Atopy Study. J Allergy Clin Immunol 113(3):489–495

    CAS  PubMed  Google Scholar 

  • Long X, Chen Q, Zhao J et al (2015) An IL-13 promoter polymorphism associated with Liver Fibrosis in patients with Schistosoma japonicum. PLoS ONE 10(8):e0135360

    PubMed  PubMed Central  Google Scholar 

  • Madore AM, Vaillancourt VT, Asai Y et al (2013) HLA-DQB1*02 and DQB1*06:03P are associated with peanut allergy. Eur J Hum Genet 21(10):1181–4

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mandal J, Das M, Roy I et al (2009) Immediate hypersensitivity to common food allergens: an investigation on food sensitization in respiratory allergic patients of Calcutta, India. World Allergy Organ J 2:9–12

    PubMed  PubMed Central  Google Scholar 

  • Martino D, Joo JE, Sexton-Oates A et al (2014) Epigenome-wide association study reveals longitudinally stable DNA methylation differences in CD4+ T cells from children with IgE-mediated food allergy. Epigenetics 9(7):998–1006

    PubMed  PubMed Central  Google Scholar 

  • Martino DJ, Ashley S, Koplin J et al (2017) Genome-wide association study of peanut allergy reproduces association with amino acid polymorphisms in HLA-DRB1. Clin Exp Allergy 47(2):217–223

    CAS  PubMed  Google Scholar 

  • Moonesinghe H, Mackenzie H, Venter C et al (2016) Prevalence of fish and shellfish allergy: a systematic review. Ann Allergy Asthma Immunol 117(3):264–272

    PubMed  Google Scholar 

  • Muraro A, Werfel T, Hoffmann-Sommergruber K et al (2014) EAACI food allergy and anaphylaxis guidelines: diagnosis and management of food allergy. Allergy 69(8):1008–25

    PubMed  Google Scholar 

  • Ravkov EV, Pavlov IY, Martins TB et al (2013) Identification and validation of shrimp-tropomyosin specific CD4 T cell epitopes. Hum Immunol 74(12):1542–9

    CAS  PubMed  Google Scholar 

  • Rosenbaum D, Hawkins G, Zhu L et al (2014) The rare IL-13 R105Q variant, strongly enhances IL-13 protein activity (HYP6P. 268). J Immunol 192(Suppl 1):118.13.

  • Ruethers T, Taki AC, Johnston EB et al (2018) Seafood allergy: a comprehensive review of fish and shellfish allergens. Mol Immunol 100:28–57

    CAS  PubMed  Google Scholar 

  • Sampson HA, van Wijk RG, Bindslev-Jensen C et al (2012) Standardizing double-blind, placebo-controlled oral food challenges: American academy of allergy, asthma & immunology-European academy of allergy and clinical immunology PRACTALL consensus report. J Allergy Clin Immunol 130(6):1260–74

    PubMed  Google Scholar 

  • Sicherer SH, Sampson HA (2010) Food allergy. J Allergy Clin Immunol 125(2 Suppl 2):S116-125

    PubMed  Google Scholar 

  • Smit DV, Cameron PA, Rainer TH (2005) Anaphylaxis presentations to an emergency department in Hong Kong: incidence and predictors of biphasic reactions. J Emerg Med 28:381–388

    PubMed  Google Scholar 

  • Techapornroong M, Akrawinthawong K, Cheungpasitporn W et al (2010) Anaphylaxis: a ten years inpatient retrospective study. Asian Pac J Allergy Immunol 28:262–269

    PubMed  Google Scholar 

  • Tejedor-Alonso MA, Moro-Moro M, Mugica-Garcia MV (2015) Epidemiology of anaphylaxis: contributions from the last 10 years. J Investig Allergol Clin Immunol 25(3):163–75

    CAS  Google Scholar 

  • Thong BY, Cheng YK, Leong KP et al (2005) Anaphylaxis in adults referred to a clinical immunology/allergy centre in Singapore. Singapore Med J 46:529–534

    CAS  PubMed  Google Scholar 

  • Tsai HJ, Kumar R, Pongracic J et al (2009) Familial aggregation of food allergy and sensitization to food allergens: a family-based study. Clin Exp Allergy 39(1):101–9

    CAS  PubMed  Google Scholar 

  • Vladich FD, Brazille SM, Stern D et al (2005) IL-13 R130Q, a common variant associated with allergy and asthma, enhances effector mechanisms essential for human allergic inflammation. J Clin Invest 115:747–754

    CAS  PubMed  PubMed Central  Google Scholar 

  • Woo CK, Bahna SL (2011) Not all shellfish “allergy” is allergy! Clin Transl Allergy 1:3

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav A, Govindasamy GK, Naidu R (2012) Polymorphic variants of interleukin-13 R130Q, interleukin-4 T589C, interleukin-4RA I50V, and interleukin-4RA Q576R in allergic rhinitis: a pilot study. Allergy Rhinol (Providence) 3(1):e35-40

    Google Scholar 

  • Zotova V, Clarke AE, Chan ES et al (2019) Low resolution rates of seafood allergy. J Allergy Clin Immunol Pract 7(2):690–692

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors convey thanks to the patients who voluntarily participated in our study. We are also grateful to the lab professionals of the Allergy and Asthma Research Center, Kolkata, for their technical help. We are also thankful to the Principal, Barasat Govt. College for providing infrastructure facilities for this study.

Funding

Was provided by Council of Scientific and Industrial Research, Govt. of India (Sanction no. 08/606(0004)/2017-EMR-I dated 14/11/2017) and Department of Science and Technology, Govt. of West Bengal (Sanction No. 1170(Sanc.)/ST/P/S&T/1G-4/2016, dated 02.03.16).

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Authors

Contributions

All the authors have made substantial contributions. Arghya Laha contributed to data compilation and wrote first draft of the manuscript. Amlan Ghosh designed the genotyping protocol for HLA-DQ rs9275596 and helps in LD analysis. Saibal Moitra diagnosed the disease, provided the sample, and supervised the oral food challenge. Himani Biswas helped in data collection. Srijit Bhattacharya did the statistical analysis. Nimai Chandra Saha, Goutam Kumar Saha, and Sanjoy Podder conceived the study design. Sanjoy Podder supervised the work, critically revised the manuscript, and made the final draft. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sanjoy Podder.

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The authors declare that they have no competing interests.

Ethics approval and consent to participate

The study protocol was approved by the Clinical Research Ethics Committee, Allergy and Asthma Research Center, West Bengal, India (CREC-AARC Ref: 004/17). All the procedures performed in the present study involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Written informed consent was obtained from all included subjects and patient anonymity was preserved using methods approved by the Ethics Committee.

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Laha, A., Ghosh, A., Moitra, S. et al. Association of HLA-DQ and IL13 gene variants with challenge-proven shrimp allergy in West Bengal, India. Immunogenetics 72, 489–498 (2020). https://doi.org/10.1007/s00251-020-01185-3

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  • DOI: https://doi.org/10.1007/s00251-020-01185-3

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