A Novel Homozygous Mutation Causing Complete TYK2 Deficiency, with Severe Respiratory Viral Infections, EBV-Driven Lymphoma, and Jamestown Canyon Viral Encephalitis.
EBV lymphoma
Inborn error of immunity
Jamestown Canyon virus
TYK2
viral encephalitis
Journal
Journal of clinical immunology
ISSN: 1573-2592
Titre abrégé: J Clin Immunol
Pays: Netherlands
ID NLM: 8102137
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
received:
17
04
2023
accepted:
30
08
2023
medline:
27
11
2023
pubmed:
11
9
2023
entrez:
11
9
2023
Statut:
ppublish
Résumé
Autosomal recessive tyrosine kinase 2 (TYK2) deficiency is characterized by susceptibility to mycobacterial and viral infections. Here, we report a 4-year-old female with severe respiratory viral infections, EBV-driven Burkitt-like lymphoma, and infection with the neurotropic Jamestown Canyon virus. A novel, homozygous c.745C > T (p.R249*) variant was found in TYK2. The deleterious effects of the TYK2 lesion were confirmed by immunoblotting; by evaluating functional responses to IFN-α/β, IL-10, and IL-23; and by assessing its scaffolding effect on the cell surface expression of cytokine receptor subunits. The effects of the mutation could not be pharmacologically circumvented in vitro, suggesting that alternative modalities, such as hematopoietic stem cell transplantation or gene therapy, may be needed. We characterize the first patient from Canada with a novel homozygous mutation in TYK2.
Identifiants
pubmed: 37695435
doi: 10.1007/s10875-023-01580-x
pii: 10.1007/s10875-023-01580-x
doi:
Substances chimiques
TYK2 Kinase
EC 2.7.10.2
TYK2 protein, human
EC 2.7.10.2
Types de publication
Case Reports
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2011-2021Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Minegishi Y, Saito M, Morio T, Watanabe K, Agematsu K, Tsuchiya S, Takada H, Hara T, Kawamura N, Ariga T, et al. Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity. 2006;25(5):745–55.
doi: 10.1016/j.immuni.2006.09.009
pubmed: 17088085
Kreins AY, Ciancanelli MJ, Okada S, Kong XF, Ramírez-Alejo N, Kilic SS, El Baghdadi J, Nonoyama S, Mahdaviani SA, Ailal F, et al. Human TYK2 deficiency: mycobacterial and viral infections without hyper-IgE syndrome. J Exp Med. 2015;212(10):1641–62.
doi: 10.1084/jem.20140280
pubmed: 26304966
pmcid: 4577846
Ogishi M, Arias AA, Yang R, Han JE, Zhang P, Rinchai D, Halpern J, Mulwa J, Keating N, Chrabieh M, et al. Impaired IL-23-dependent induction of IFN-γ underlies mycobacterial disease in patients with inherited TYK2 deficiency. J Exp Med. 2022;219(10):e20220094.
doi: 10.1084/jem.20220094
pubmed: 36094518
pmcid: 9472563
Nemoto M, Hattori H, Maeda N, Akita N, Muramatsu H, Moritani S, Kawasaki T, Maejima M, Ode H, Hachiya A, et al. Compound heterozygous TYK2 mutations underlie primary immunodeficiency with T-cell lymphopenia. Sci Rep. 2018;8(1):6956.
doi: 10.1038/s41598-018-25260-8
pubmed: 29725107
pmcid: 5934390
Vinh DC, Schwartz B, Hsu AP, Miranda DJ, Valdez PA, Fink D, Lau KP, Long-Priel D, Kuhns DB, Uzel G, et al. Interleukin-12 receptor beta1 deficiency predisposing to disseminated Coccidioidomycosis. Clin Infect Dis. 2011;52(4):e99–102.
doi: 10.1093/cid/ciq215
pubmed: 21258095
pmcid: 3060907
Gavino C, Cotter A, Lichtenstein D, Lejtenyi D, Fortin C, Legault C, Alirezaie N, Majewski J, Sheppard DC, Behr MA, et al. CARD9 deficiency and spontaneous central nervous system candidiasis: complete clinical remission with GM-CSF therapy. Clin Infect Dis. 2014;59(1):81–4.
doi: 10.1093/cid/ciu215
pubmed: 24704721
pmcid: 4305130
Gavino C, Hamel N, Zeng JB, Legault C, Guiot MC, Chankowsky J, Lejtenyi D, Lemire M, Alarie I, Dufresne S, et al. Impaired RASGRF1/ERK-mediated GM-CSF response characterizes CARD9 deficiency in French-Canadians. J Allergy Clin Immunol. 2016;137(4):1178-1188.e7.
doi: 10.1016/j.jaci.2015.09.016
pubmed: 26521038
Gavino C, Landekic M, Zeng J, Wu N, Jung S, Zhong MC, Cohen-Blanchet A, Langelier M, Neyret O, Lejtenyi D, et al. Morpholino-based correction of hypomorphic ZAP70 mutation in an adult with combined immunodeficiency. J Allergy Clin Immunol. 2017;139(5):1688-1692 e10.
doi: 10.1016/j.jaci.2017.02.002
pubmed: 28216435
pmcid: 7126384
Ghoreschi K, Laurence A, O’Shea JJ. Janus kinases in immune cell signaling. Immunol Rev. 2009;228(1):273–87.
doi: 10.1111/j.1600-065X.2008.00754.x
pubmed: 19290934
pmcid: 2782696
Wöss K, Simonović N, Strobl B, Macho-Maschler S, Müller M. TYK2: an upstream kinase of STATs in cancer. Cancers (Basel). 2019;11(11):1728–46.
doi: 10.3390/cancers11111728
pubmed: 31694222
Ragimbeau J, Dondi E, Alcover A, Eid P, Uzé G, Pellegrini S. The tyrosine kinase Tyk2 controls IFNAR1 cell surface expression. Embo j. 2003;22(3):537–47.
doi: 10.1093/emboj/cdg038
pubmed: 12554654
pmcid: 140723
Li Z, Rotival M, Patin E, Michel F, Pellegrini S. Two common disease-associated TYK2 variants impact exon splicing and TYK2 dosage. PLoS ONE. 2020;15(1):e0225289.
doi: 10.1371/journal.pone.0225289
pubmed: 31961910
pmcid: 6974145
Levin D, Harari D, Schreiber G. Stochastic receptor expression determines cell fate upon interferon treatment. Mol Cell Biol. 2011;31(16):3252–66.
doi: 10.1128/MCB.05251-11
pubmed: 21690295
pmcid: 3147786
Schreiber G. The molecular basis for differential type I interferon signaling. J Biol Chem. 2017;292(18):7285–94.
doi: 10.1074/jbc.R116.774562
pubmed: 28289098
pmcid: 5418031
Azimov R, Abuladze N, Sassani P, Newman D, Kao L, Liu W, Orozco N, Ruchala P, Pushkin A, Kurtz I. G418-mediated ribosomal read-through of a nonsense mutation causing autosomal recessive proximal renal tubular acidosis. Am J Physiol Renal Physiol. 2008;295(3):F633–41.
doi: 10.1152/ajprenal.00015.2008
pubmed: 18614622
pmcid: 2653109
Frew J, Baradaran-Heravi A, Balgi AD, Wu X, Yan TD, Arns S, Shidmoossavee FS, Tan J, Jaquith JB, Jansen-West KR, et al. Premature termination codon readthrough upregulates progranulin expression and improves lysosomal function in preclinical models of GRN deficiency. Mol Neurodegener. 2020;15(1):21.
doi: 10.1186/s13024-020-00369-5
pubmed: 32178712
pmcid: 7075020
Keeling KM, Xue X, Gunn G, Bedwell DM. Therapeutics based on stop codon readthrough. Annu Rev Genomics Hum Genet. 2014;15:371–94.
doi: 10.1146/annurev-genom-091212-153527
pubmed: 24773318
pmcid: 5304456
Rubenstein RC, Zeitlin PL. A pilot clinical trial of oral sodium 4-phenylbutyrate (Buphenyl) in deltaF508-homozygous cystic fibrosis patients: partial restoration of nasal epithelial CFTR function. Am J Respir Crit Care Med. 1998;157(2):484–90.
doi: 10.1164/ajrccm.157.2.9706088
pubmed: 9476862
Pignani S, Todaro A, Ferrarese M, Marchi S, Lombardi S, Balestra D, Pinton P, Bernardi F, Pinotti M, Branchini A. The chaperone-like sodium phenylbutyrate improves factor IX intracellular trafficking and activity impaired by the frequent p.R294Q mutation. J Thromb Haemost. 2018;16(10):2035–43.
doi: 10.1111/jth.14236
pubmed: 29993188
Pomozi V, Brampton C, Szeri F, Dedinszki D, Kozák E, van de Wetering K, Hopkins H, Martin L, Váradi A, Le Saux O. Functional rescue of ABCC6 deficiency by 4-phenylbutyrate therapy reduces dystrophic calcification in Abcc6
doi: 10.1016/j.jid.2016.10.035
pubmed: 27826008
Zhang Q, Matuozzo D, Le Pen J, Lee D, Moens L, Asano T, Bohlen J, Liu Z, Moncada-Velez M, Kendir-Demirkol Y, et al. Recessive inborn errors of type I IFN immunity in children with COVID-19 pneumonia. J Exp Med. 2022;219(8):e20220131.
doi: 10.1084/jem.20220131
pubmed: 35708626
pmcid: 9206114
Drebot MA. Emerging mosquito-borne bunyaviruses in Canada. Can Commun Dis Rep. 2015;41(6):117–23.
doi: 10.14745/ccdr.v41i06a01
pubmed: 29769943
pmcid: 5864308
Pastula DM, Hoang Johnson DK, White JL, Dupuis AP 2nd, Fischer M, Staples JE. Jamestown Canyon virus disease in the United States-2000-2013. Am J Trop Med Hyg. 2015;93(2):384–9.
doi: 10.4269/ajtmh.15-0196
pubmed: 26033022
pmcid: 4530766
Matkovic E, Hoang Johnson DK, Staples JE, Mora-Pinzon MC, Elbadawi LI, Osborn RA, Warshauer DM, Wegner MV, Davis JP. Enhanced arboviral surveillance to increase detection of Jamestown Canyon virus infections, Wisconsin, 2011–2016. Am J Trop Med Hyg. 2019;100(2):445–51.
doi: 10.4269/ajtmh.18-0575
pubmed: 30526745
Fuchs S, Kaiser-Labusch P, Bank J, Ammann S, Kolb-Kokocinski A, Edelbusch C, Omran H, Ehl S. Tyrosine kinase 2 is not limiting human antiviral type III interferon responses. Eur J Immunol. 2016;46(11):2639–49.
doi: 10.1002/eji.201646519
pubmed: 27615517
Meyts I, Casanova JL. Viral infections in humans and mice with genetic deficiencies of the type I IFN response pathway. Eur J Immunol. 2021;51(5):1039–61.
doi: 10.1002/eji.202048793
pubmed: 33729549
pmcid: 8900014
Stertz S, Hale BG. Interferon system deficiencies exacerbating severe pandemic virus infections. Trends Microbiol. 2021;29(11):973–82.
doi: 10.1016/j.tim.2021.03.001
pubmed: 33757684
pmcid: 7980109
Geiger TR, Martin JM. The Epstein-Barr virus-encoded LMP-1 oncoprotein negatively affects Tyk2 phosphorylation and interferon signaling in human B cells. J Virol. 2006;80(23):11638–50.
doi: 10.1128/JVI.01570-06
pubmed: 16987978
pmcid: 1642610
Philippot Q, Ogishi M, Bohlen J, Puchan J, Arias AA, Nguyen T, Martin-Fernandez M, Conil C, Rinchai D, Momenilandi M, et al. Human IL-23 is essential for IFN-γ-dependent immunity to mycobacteria. Sci Immunol. 2023;8(80):eabq5204.
doi: 10.1126/sciimmunol.abq5204
pubmed: 36763636
pmcid: 10069949
van de Vosse E, Haverkamp MH, Ramirez-Alejo N, Martinez-Gallo M, Blancas-Galicia L, Metin A, Garty BZ, Sun-Tan Ç, Broides A, de Paus RA, et al. IL-12Rβ1 deficiency: mutation update and description of the IL12RB1 variation database. Hum Mutat. 2013;34(10):1329–39.
doi: 10.1002/humu.22380
pubmed: 23864330
pmcid: 4104692
Prando C, Samarina A, Bustamante J, Boisson-Dupuis S, Cobat A, Picard C, AlSum Z, Al-Jumaah S, Al-Hajjar S, Frayha H, et al. Inherited IL-12p40 deficiency: genetic, immunologic, and clinical features of 49 patients from 30 kindreds. Medicine (Baltimore). 2013;92(2):109–22.
doi: 10.1097/MD.0b013e31828a01f9
Bustamante J, Boisson-Dupuis S, Abel L, Casanova JL. Mendelian susceptibility to mycobacterial disease: genetic, immunological, and clinical features of inborn errors of IFN-γ immunity. Semin Immunol. 2014;26(6):454–70.
doi: 10.1016/j.smim.2014.09.008
pubmed: 25453225
pmcid: 4357480
Vinh DC. Insights into human antifungal immunity from primary immunodeficiencies. Lancet Infect Dis. 2011;11(10):780–92.
doi: 10.1016/S1473-3099(11)70217-1
Vinh DC. The molecular immunology of human susceptibility to fungal diseases: lessons from single gene defects of immunity. Expert Rev Clin Immunol. 2019;15(5):461–86.
doi: 10.1080/1744666X.2019.1584038
pubmed: 30773066
Yan H, Piazza F, Krishnan K, Pine R, Krolewski JJ. Definition of the interferon-alpha receptor-binding domain on the TYK2 kinase. J Biol Chem. 1998;273(7):4046–51.
doi: 10.1074/jbc.273.7.4046
pubmed: 9461596
Richter MF, Duménil G, Uzé G, Fellous M, Pellegrini S. Specific contribution of Tyk2 JH regions to the binding and the expression of the interferon alpha/beta receptor component IFNAR1. J Biol Chem. 1998;273(38):24723–9.
doi: 10.1074/jbc.273.38.24723
pubmed: 9733772
Kotenko SV, Krause CD, Izotova LS, Pollack BP, Wu W, Pestka S. Identification and functional characterization of a second chain of the interleukin-10 receptor complex. Embo j. 1997;16(19):5894–903.
doi: 10.1093/emboj/16.19.5894
pubmed: 9312047
Walter MR. The molecular basis of IL-10 function: from receptor structure to the onset of signaling. Curr Top Microbiol Immunol. 2014;380:191–212.
pubmed: 25004819
pmcid: 4489423
Robinson RT. IL12Rβ1: the cytokine receptor that we used to know. Cytokine. 2015;71(2):348–59.
doi: 10.1016/j.cyto.2014.11.018
pubmed: 25516297