Hyperimmunoglobulinemia E and hereditary immune deficiencies

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Ilham Fadil
Fatima Ailal
Vivien Beziat
Jean Laurent Casanova
Bertrand Boisson
Ahmed Aziz Bousfiha

Abstract

The detection of a high serum immunoglobulin E (IgE) level is first suggestive of allergy, atopy or parasitosis. However, some very high values can be a sign of more severe diseases. We propose a diagnostic strategy based on clinical and biological data to identify the various hereditary immune diseases that also present with abnormally high serum IgE levels.

Keywords:

Hyperimmunoglobulinemia E , Hereditary immune deficiencies , HyperIgE syndromes , Primary immune deficiencies.

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References

  1. Ishizaka K, Ishizaka T. Identification of IgE. Journal of Allergy and Clinical Immunology. 2016 Jun;137(6):1646–50.
  2. Johansson SGO. The discovery of IgE. Journal of Allergy and Clinical Immunology. 2016 Jun;137(6):1671–3.
  3. Lindberg R, Arroyave C. Levels of IgE in serum from normal children and allergic children as measured by an enzyme immunoassay. Journal of Allergy and Clinical Immunology. 1986 Oct;78(4):614–8.
  4. Saarinen UM, Juntunen K, Kajosaari M, Björkstén F. SERUM IMMUNOGLOBULIN E IN ATOPIC AND NON-ATOPIC CHILDREN AGED 6 MONTHS TO 5 YEARS.: A Follow-up Study. Acta Paediatrica. 1982 May;71(3):489–94.
  5. Stone KD, Prussin C, Metcalfe DD. IgE, mast cells, basophils, and eosinophils. Journal of Allergy and Clinical Immunology. 2010 Feb;125(2):S73–80.
  6. Hamilton RG, Adkinson NF. 23. Clinical laboratory assessment of IgE-dependent hypersensitivity. Journal of Allergy and Clinical Immunology. 2003 Feb;111(2):S687–701.
  7. Zellweger F, Eggel A. IgE‐associated allergic disorders: recent advances in etiology, diagnosis, and treatment. Allergy. 2016 Dec 1;71(12):1652–61.
  8. Wittig HJ, Belloit J, De Fillippi I, Royal G. Age-related serum immunoglobulin E levels in healthy subjects and in patients with allergic disease. Journal of Allergy and Clinical Immunology. 1980 Oct;66(4):305–13.
  9. Garcia G, Humbert M. Infection et réponse à IgE. Revue Française d’Allergologie et d’Immunologie Clinique. 1998 Jan;38(4):241–6.
  10. Grimbacher B, Belohradsky BH, Holland SM. Immunoglobulin E in primary immunodeficiency diseases. Allergy. 2002 Nov;57(11):995–1007.
  11. Zhang Q, Boisson B, Béziat V, Puel A, Casanova JL. Human hyper-IgE syndrome: singular or plural? Mamm Genome. 2018 Aug;29(7–8):603–17.
  12. Allaoui A, Mokhantar K, Jeddane L, Ailal F, Elkabli H, Bousfiha AA, et al. Quand faut-il suspecter un déficit immunitaire chez l’adulte? When to suspect an immune deficiency in adults? Tunis Med. 2022; 100(8-9):585-591
  13. Bousfiha A, Moundir A, Tangye SG, Picard C, Jeddane L, Al-Herz W, et al. The 2022 Update of IUIS Phenotypical Classification for Human Inborn Errors of Immunity. J Clin Immunol. 2022 Oct;42(7):1508–20.
  14. Tangye SG, Al-Herz W, Bousfiha A, Cunningham-Rundles C, Franco JL, Holland SM, et al. Human Inborn Errors of Immunity: 2022 Update on the Classification from the International Union of Immunological Societies Expert Committee. J Clin Immunol. 2022 Oct;42(7):1473–507.
  15. Alyasin S, Esmaeilzadeh H, Ebrahimi N, Nabavizadeh SH, Kashef S, Esmaeilzadeh E, et al. Phenotyping and long-term follow up of patients with hyper IgE syndrome. Allergologia et Immunopathologia. 2019 Mar;47(2):152–8.
  16. Al-Shaikhly T, Ochs HD. Hyper IgE Syndromes, Clinical & Molecular Characteristics. Immunology and Cell Biology [Internet]. 2018 Sep 28 [cited 2018 Oct 2]; Available from: http://doi.wiley.com/10.1111/imcb.12209
  17. Zhang Q, Boisson B, Béziat V, Puel A, Casanova JL. Human hyper-IgE syndrome: singular or plural? Mammalian Genome [Internet]. 2018 Aug 9 [cited 2018 Aug 13]; Available from: http://link.springer.com/10.1007/s00335-018-9767-2
  18. Fadil I, Ben-Ali M, Jeddane L, Barbouche MR, Bousfiha AA. The Seven STAT3-Related Hyper-IgE Syndromes. J Clin Immunol. 2021 Aug;41(6):1384–9.
  19. Grimbacher B, Schäffer AA, Holland SM, Davis J, Gallin JI, Malech HL, et al. Genetic linkage of hyper-IgE syndrome to chromosome 4. Am J Hum Genet. 1999 Sep;65(3):735–44.
  20. Davis S, Schaller J, Wedgwood R, Harvard MD. JOB’S SYNDROME: Recurrent, " Cold ", Staphylococcal Abscesses. The Lancet. 1966 May 7;287(7445):1013–5.
  21. Buckley RH, Wray BB, Belmaker EZ. Extreme hyperimmunoglobulinemia E and undue susceptibility to infection. Pathologica. 1972 Jan 1;49(1):59–70.
  22. Borges WG, Hensley T, Carey JC, Petrak BA, Hill HR. The face of Job. The Journal of Pediatrics. 1998 Aug;133(2):303–5.
  23. Grimbacher B, Holland SM, Gallin JI, Greenberg F, Hill SC, Malech HL, et al. Hyper-IgE syndrome with recurrent infections--an autosomal dominant multisystem disorder. N Engl J Med. 1999 Mar 4;340(9):692–702.
  24. Vogel TP, Milner JD, Cooper MA. The Ying and Yang of STAT3 in Human Disease. J Clin Immunol. 2015 Oct;35(7):615–23.
  25. Chamlin SL, McCalmont TH, Cunningham BB, Esterly NB, Lai CH, Mallory SB, et al. Cutaneous manifestations of hyper-IgE syndrome in infants and children. The Journal of Pediatrics. 2002 Oct;141(4):572–5.
  26. Eberting CLD, Davis J, Puck JM, Holland SM, Turner ML. Dermatitis and the Newborn Rash of Hyper-IgE Syndrome. Arch Dermatol. 2004 Sep 1;140(9):1119–25.
  27. Woellner C, Gertz EM, Schäffer AA, Lagos M, Perro M, Glocker EO, et al. Mutations in STAT3 and diagnostic guidelines for hyper-IgE syndrome. Journal of Allergy and Clinical Immunology. 2010 Feb;125(2):424-432.e8.
  28. Béziat V, Fieschi C, Momenilandi M, Migaud M, Belaid B, Djidjik R, et al. Inherited human ZNF341 deficiency. Current Opinion in Immunology. 2023 Jun;82:102326.
  29. Béziat V, Li J, Lin JX, Ma CS, Li P, Bousfiha A, et al. A recessive form of hyper-IgE syndrome by disruption of ZNF341-dependent STAT3 transcription and activity. Science Immunology. 2018 Jun 15;3(24):eaat4956.
  30. Frey-Jakobs S, Hartberger JM, Fliegauf M, Bossen C, Wehmeyer ML, Neubauer JC, et al. ZNF341 controls STAT3 expression and thereby immunocompetence. Sci Immunol. 2018 Jun 15;3(24):eaat4941.
  31. Schwerd T, Twigg SRF, Aschenbrenner D, Manrique S, Miller KA, Taylor IB, et al. A biallelic mutation in IL6ST encoding the GP130 co-receptor causes immunodeficiency and craniosynostosis. J Exp Med. 2017 Sep 4;214(9):2547–62.
  32. Shahin T, Aschenbrenner D, Cagdas D, Köstel Bal S, Domínguez Conde C, Garncarz W, et al. Selective loss of function variants in IL6ST cause Hyper-IgE Syndrome with distinct impairments of T cell phenotype and function. Haematologica. 2018 Oct 11;haematol.2018.194233.
  33. Nieminen P, Morgan NV, Fenwick AL, Parmanen S, Veistinen L, Mikkola ML, et al. Inactivation of IL11 Signaling Causes Craniosynostosis, Delayed Tooth Eruption, and Supernumerary Teeth. The American Journal of Human Genetics. 2011 Jul;89(1):67–81.
  34. Spencer S, Köstel Bal S, Egner W, Lango Allen H, Raza SI, Ma CA, et al. Loss of the interleukin-6 receptor causes immunodeficiency, atopy, and abnormal inflammatory responses. J Exp Med. 2019 Sep 2;216(9):1986–98.
  35. Puel A, Bastard P, Bustamante J, Casanova JL. Human autoantibodies underlying infectious diseases. J Exp Med. 2022 Mar 23;219(4):e20211387.
  36. Béziat V, Tavernier SJ, Chen YH, Ma CS, Materna M, Laurence A, et al. Dominant-negative mutations in human IL6ST underlie hyper-IgE syndrome. Journal of Experimental Medicine. 2020 Jun 1;217(6):e20191804.
  37. Felgentreff K, Siepe M, Kotthoff S, von Kodolitsch Y, Schachtrup K, Notarangelo LD, et al. Severe eczema and Hyper-IgE in Loeys–Dietz-syndrome — Contribution to new findings of immune dysregulation in connective tissue disorders. Clinical Immunology. 2014 Jan;150(1):43–50.
  38. RESERVES IUTD. Orphanet: Syndrome de Loeys Dietz [Internet]. [cited 2021 Aug 17]. Available from: https://www.orpha.net/consor/cgi-bin/OC_Exp.php?Lng=FR&Expert=60030
  39. Dorjbal B, Stinson JR, Ma CA, Weinreich MA, Miraghazadeh B, Hartberger JM, et al. Hypomorphic caspase activation and recruitment domain 11 (CARD11) mutations associated with diverse immunologic phenotypes with or without atopic disease. Journal of Allergy and Clinical Immunology. 2019 Apr;143(4):1482–95.
  40. Lyons JJ, Liu Y, Ma CA, Yu X, O’Connell MP, Lawrence MG, et al. ERBIN deficiency links STAT3 and TGF-β pathway defects with atopy in humans. J Exp Med. 2017 Jan 26;jem.20161435.
  41. Hannula-Jouppi K, Laasanen SL, Ilander M, Furio L, Tuomiranta M, Marttila R, et al. Intrafamily and Interfamilial Phenotype Variation and Immature Immunity in Patients With Netherton Syndrome and Finnish SPINK5 Founder Mutation. JAMA Dermatol. 2016 Apr 1;152(4):435–42.
  42. Laroussinie A, Hainaut E, Barbarot S, Drui D, Pierre P, Sonnet E, et al. Syndrome de Netherton : évaluation des axes antéhypophysaires – étude REHYNE. Annales d’Endocrinologie. 2016 Sep;77(4):277.
  43. Yang L, Fliegauf M, Grimbacher B. Hyper-IgE syndromes: reviewing PGM3 deficiency. Current Opinion in Pediatrics. 2014 Dec;26(6):697–703.
  44. Zhang Y, Yu X, Ichikawa M, Lyons JJ, Datta S, Lamborn IT, et al. Autosomal recessive PGM3 mutations link glycosylation defects to atopy, immune deficiency, autoimmunity, and neurocognitive impairment. J Allergy Clin Immunol. 2014 May;133(5):1400-1409.e5.
  45. Ben-Ali M, Ben-Khemis L, Mekki N, Yaakoubi R, Ouni R, Benabdessalem C, et al. Defective glycosylation leads to defective gp130-dependent STAT3 signaling in PGM3-deficient patients. J Allergy Clin Immunol. 2019 Apr;143(4):1638-1640.e2. doi: 10.1016/j.jaci.2018.12.987.
  46. Buchbinder D, Nugent DJ, Fillipovich AH. Wiskott–Aldrich syndrome: diagnosis, current management, and emerging treatments. Appl Clin Genet. 2014 Apr 3;7:55–66.
  47. Schwinger W, Urban C, Ulreich R, Sperl D, Karastaneva A, Strenger V, et al. The Phenotype and Treatment of WIP Deficiency: Literature Synopsis and Review of a Patient With Pre-transplant Serial Donor Lymphocyte Infusions to Eliminate CMV. Front Immunol. 2018 Nov 2;9:2554.
  48. Al-Mousa H, Hawwari A, Al-Ghonaium A, Al-Saud B, Al-Dhekri H, Al-Muhsen S, et al. Hematopoietic stem cell transplantation corrects WIP deficiency. Journal of Allergy and Clinical Immunology. 2017 Mar;139(3):1039-1040.e4.
  49. Hsu CC, Lee JYY, Chao SC. Omenn syndrome: a case report and review of literature. Dermatologica Sinica. 2011 Jun;29(2):50–4.
  50. Michaelovsky E, Frisch A, Carmel M, Patya M, Zarchi O, Green T, et al. Genotype-phenotype correlation in 22q11.2 deletion syndrome. BMC Med Genet. 2012 Dec;13(1):122.
  51. Chen CB, Tahboub F, Plesec T, Kay M, Radhakrishnan K. A Review of Autoimmune Enteropathy and Its Associated Syndromes. Dig Dis Sci. 2020 Nov;65(11):3079–90.
  52. Barzaghi F, Hernandez LCA, Neven B, Ricci S, Kucuk ZY, Bleesing JJ, et al. Long-term follow-up of IPEX syndrome patients after different therapeutic strategies: An international multicenter retrospective study. J Allergy Clin Immunol. 2018 Mar;141(3):1036-1049.e5.
  53. Kahr WHA, Pluthero FG, Elkadri A, Warner N, Drobac M, Chen CH, et al. Loss of the Arp2/3 complex component ARPC1B causes platelet abnormalities and predisposes to inflammatory disease. Nature Communications. 2017 Apr 3;8:14816.
  54. Brigida I, Zoccolillo M, Cicalese MP, Pfajfer L, Barzaghi F, Scala S, et al. T-cell defects in patients with ARPC1B germline mutations account for combined immunodeficiency. Blood. 2018 Nov 29;132(22):2362–74.
  55. Volpi S, Cicalese MP, Tuijnenburg P, Tool ATJ, Cuadrado E, Abu-Halaweh M, et al. A combined immunodeficiency with severe infections, inflammation, and allergy caused by ARPC1B deficiency. Journal of Allergy and Clinical Immunology. 2019 Jun;143(6):2296–9.
  56. Su HC. DOCK8 (Dedicator of cytokinesis 8) deficiency. Curr Opin Allergy Clin Immunol. 2010 Dec;10(6):515–20.
  57. Koskenvuo M, Kainulainen L, Vanto T, Lukkarinen H, Lähteenmäki P, Ruuskanen O. [Severe atopy and allergy--rare hyper-IgE syndrome caused by the DOCK8 mutation as underlying condition]. Duodecim. 2015;131(6):541–4.
  58. Jabara HH, Ohsumi T, Chou J, Massaad MJ, Benson H, Megarbane A, et al. A homozygous mucosa-associated lymphoid tissue 1 (MALT1) mutation in a family with combined immunodeficiency. Journal of Allergy and Clinical Immunology. 2013 Jul;132(1):151–8.
  59. McKinnon ML, Rozmus J, Fung SY, Hirschfeld AF, Del Bel KL, Thomas L, et al. Combined immunodeficiency associated with homozygous MALT1 mutations. Journal of Allergy and Clinical Immunology. 2014 May;133(5):1458-1462.e7.
  60. Hwa V. Human growth disorders associated with impaired GH action: Defects in STAT5B and JAK2. Molecular and Cellular Endocrinology. 2021 Jan;519:111063.
  61. Hwa V, Nadeau K, Wit JM, Rosenfeld RG. STAT5b deficiency: Lessons from STAT5b gene mutations. Best Practice & Research Clinical Endocrinology & Metabolism. 2011 Feb;25(1):61–75.
  62. Nadeau K, Hwa V, Rosenfeld RG. STAT5b Deficiency: An Unsuspected Cause of Growth Failure, Immunodeficiency, and Severe Pulmonary Disease. The Journal of Pediatrics. 2011 May;158(5):701–8.
  63. Abdollahpour H, Appaswamy G, Kotlarz D, Diestelhorst J, Beier R, Schäffer AA, et al. The phenotype of human STK4 deficiency. Blood. 2012 Apr 12;119(15):3450–7.
  64. Orange JS, Chinen J, editors. Encyclopedia of Medical Immunology: Immunodeficiency Diseases [Internet]. New York, NY: Springer New York; 2020 [cited 2021 Aug 28]. Available from: http://link.springer.com/10.1007/978-1-4614-8678-7
  65. Wang Y, Ma CS, Ling Y, Bousfiha A, Camcioglu Y, Jacquot S, et al. Dual T cell– and B cell–intrinsic deficiency in humans with biallelic RLTPR mutations. J Exp Med. 2016 Oct 17;213(11):2413–35.
  66. Lévy R, Gothe F, Momenilandi M, Magg T, Materna M, Peters P, et al. Human CARMIL2 deficiency underlies a broader immunological and clinical phenotype than CD28 deficiency. J Exp Med. 2023 Feb 6;220(2):e20220275.
  67. Kotlarz D, Ziętara N, Milner JD, Klein C. Human IL-21 and IL-21R deficiencies: two novel entities of primary immunodeficiency. Current Opinion in Pediatrics. 2014 Dec;26(6):704–12.
  68. Salzer E, Kansu A, Sic H, Májek P, Ikincioğullari A, Dogu FE, et al. Early-onset inflammatory bowel disease and common variable immunodeficiency–like disease caused by IL-21 deficiency. Journal of Allergy and Clinical Immunology. 2014 Jun;133(6):1651-1659.e12.