Germline STAT3 gain-of-function mutations in primary immunodeficiency: Impact on the cellular and clinical phenotype

Biomedical Journal - Tập 44 - Trang 412-421 - 2021
Laura Faletti1, Stephan Ehl1, Maximilian Heeg1
1Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center, Faculty of Medicine, University of Freiburg, Freiburg, Germany

Tài liệu tham khảo

Fisher, 1995, Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome, Cell, 81, 935, 10.1016/0092-8674(95)90013-6 Flanagan, 2014, Activating germline mutations in STAT3 cause early-onset multi-organ autoimmune disease, Nat Genet, 46, 812, 10.1038/ng.3040 Haapaniemi, 2015, Autoimmunity, hypogammaglobulinemia, lymphoproliferation, and mycobacterial disease in patients with activating mutations in STAT3, Blood, 125, 639, 10.1182/blood-2014-04-570101 Milner, 2015, Early-onset lymphoproliferation and autoimmunity caused by germline STAT3 gain-of-function mutations, Blood, 125, 591, 10.1182/blood-2014-09-602763 Morris, 2018, The molecular details of cytokine signaling via the JAK/STAT pathway, Protein Sci, 27, 1984, 10.1002/pro.3519 Silva, 2004, Role of STATs as downstream signal transducers in Src family kinase-mediated tumorigenesis, Oncogene, 23, 8017, 10.1038/sj.onc.1208159 Igaz, 2001, Biological and clinical significance of the JAK-STAT pathway; lessons from knockout mice, Inflamm Res, 50, 435, 10.1007/PL00000267 Ihle, 1997, Jaks and Stats in cytokine signaling, Stem Cell, 15, 105, 10.1002/stem.5530150814 O'Shea, 1997, Jaks, STATs, cytokine signal transduction, and immunoregulation: are we there yet?, Immunity, 7, 1, 10.1016/S1074-7613(00)80505-1 Takeda, 1997, Targeted disruption of the mouse Stat 3 gene leads to early embryonic lethality, Proc Natl Acad Sci USA, 94, 3801, 10.1073/pnas.94.8.3801 Hillmer, 2016, STAT3 signaling in immunity, Cytokine Growth Factor Rev, 31, 1, 10.1016/j.cytogfr.2016.05.001 Holland, 2007, STAT3 mutations in the hyper-IgE syndrome, N Engl J Med, 357, 1608, 10.1056/NEJMoa073687 Minegishi, 2007, Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome, Nature, 448, 1058, 10.1038/nature06096 Fabre, 2019, Clinical aspects of STAT3 gain-of-function germline mutations: a systematic review, J Allergy Clin Immunol Pract, 7, 1958, 10.1016/j.jaip.2019.02.018 Jägle, 2020, Distinct molecular response patterns of activating STAT3 mutations associate with penetrance of lymphoproliferation and autoimmunity, Clin Immunol, 210, 108316, 10.1016/j.clim.2019.108316 Tanita, 2021, Clinical and immunological heterogeneity in Japanese patients with gain-of-function variants in STAT3, J Clin Immunol, 41, 780, 10.1007/s10875-021-00975-y Fabre, 2018, STAT3 gain of function: a new kid on the block in interstitial lung diseases, Am J Respir Crit Care Med, 197, e22, 10.1164/rccm.201707-1500IM Mauracher, 2020, Erythropoiesis defect observed in STAT3 GOF patients with severe anemia, J Allergy Clin Immunol, 145, 1297, 10.1016/j.jaci.2019.11.042 Velayos, 2017, An activating mutation in STAT3 results in neonatal diabetes through reduced insulin synthesis, Diabetes, 66, 1022, 10.2337/db16-0867 Sediva, 2017, Short Stature in a Boy with Multiple Early-Onset Autoimmune Conditions due to a STAT3 Activating Mutation: Could Intracellular Growth Hormone Signalling Be Compromised?, Horm Res Paediatr, 88, 160, 10.1159/000456544 Shah, 2018, T-cell receptor αβ+ and CD19+ cell-depleted haploidentical and mismatched hematopoietic stem cell transplantation in primary immune deficiency, J Allergy Clin Immunol, 141, 1417, 10.1016/j.jaci.2017.07.008 Parlato, 2019, Efficacy of ruxolitinib therapy in a patient with severe enterocolitis associated with a STAT3 gain-of-function mutation, Gastroenterology, 156, 1206, 10.1053/j.gastro.2018.11.065 Todaro, 2019, Multisystem autoimmune disease caused by increased STAT3 phosphorylation and dysregulated gene expression, Haematologica, 104, e322, 10.3324/haematol.2018.202374 Gonzalez-Mancera, 2020, STAT3 gain-of-function mutation in a patient with pulmonary Mycobacterium abscessus infection, Respir Med Case Rep, 30, 101125 Terry, 2020, Prenatal autoimmune disease, multisystem, infantile onset-like phenotype and proximal renal tubular dysplasia associated with STAT3 mutation, Pediatr Dev Pathol, 23, 306, 10.1177/1093526619890734 Silva-Carmona, 2020, Successful treatment of interstitial lung disease in STAT3 gain-of-function using JAK inhibitors, Am J Respir Crit Care Med, 202, 893, 10.1164/rccm.201906-1204LE Sarfati, 2021, Life-saving, dose-adjusted, targeted therapy in a patient with a STAT3 gain-of-function mutation, J Clin Immunol, 41, 807, 10.1007/s10875-020-00914-3 Maccari, 2018, Disease evolution and response to rapamycin in activated phosphoinositide 3-kinase δ syndrome: the European society for immunodeficiencies-activated phosphoinositide 3-kinase δ syndrome registry, Front Immunol, 9, 543, 10.3389/fimmu.2018.00543 Schwab, 2018, Phenotype, penetrance, and treatment of 133 cytotoxic T-lymphocyte antigen 4-insufficient subjects, J Allergy Clin Immunol, 142, 1932, 10.1016/j.jaci.2018.02.055 Lorenzini, 2020, Characterization of the clinical and immunologic phenotype and management of 157 individuals with 56 distinct heterozygous NFKB1 mutations, J Allergy Clin Immunol, 146, 901, 10.1016/j.jaci.2019.11.051 Velichko, 2002, STAT3 activation by type I interferons is dependent on specific tyrosines located in the cytoplasmic domain of interferon receptor chain 2c. Activation of multiple STATS proceeds through the redundant usage of two tyrosine residues, J Biol Chem, 277, 35635, 10.1074/jbc.M204578200 Kwon, 2009, Analysis of interleukin-21-induced Prdm1 gene regulation reveals functional cooperation of STAT3 and IRF4 transcription factors, Immunity, 31, 941, 10.1016/j.immuni.2009.10.008 Vallania, 2009, Genome-wide discovery of functional transcription factor binding sites by comparative genomics: the case of Stat 3, Proc Natl Acad Sci USA, 106, 5117, 10.1073/pnas.0900473106 Wen, 1995, Maximal activation of transcription by Stat 1 and Stat 3 requires both tyrosine and serine phosphorylation, Cell, 82, 241, 10.1016/0092-8674(95)90311-9 Wingelhofer, 2018, Implications of STAT3 and STAT5 signaling on gene regulation and chromatin remodeling in hematopoietic cancer, Leukemia, 32, 1713, 10.1038/s41375-018-0117-x Carow, 2014, SOCS3, a major regulator of infection and inflammation, Front Immunol, 5, 58, 10.3389/fimmu.2014.00058 Chung, 1997, Specific inhibition of Stat 3 signal transduction by PIAS3, Science, 278, 1803, 10.1126/science.278.5344.1803 Roca Suarez, 2018, Viral manipulation of STAT3: evade, exploit, and injure, PLoS Pathog, 14, 10.1371/journal.ppat.1006839 Cheon, 2011, The functions of signal transducers and activators of transcriptions 1 and 3 as cytokine-inducible proteins, J Interferon Cytokine Res, 31, 33, 10.1089/jir.2010.0100 Huynh, 2019, Therapeutically exploiting STAT3 activity in cancer - using tissue repair as a road map, Nat Rev Canc, 19, 82, 10.1038/s41568-018-0090-8 Wegrzyn, 2009, Function of mitochondrial Stat 3 in cellular respiration, Science, 323, 793, 10.1126/science.1164551 Gough, 2009, Mitochondrial STAT3 supports Ras-dependent oncogenic transformation, Science, 324, 1713, 10.1126/science.1171721 Jerez, 2012, STAT3 mutations unify the pathogenesis of chronic lymphoproliferative disorders of NK cells and T-cell large granular lymphocyte leukemia, Blood, 120, 3048, 10.1182/blood-2012-06-435297 Veitia, 2018, Mechanisms of mendelian dominance, Clin Genet, 93, 419, 10.1111/cge.13107 Vogel, 2015, The ying and yang of STAT3 in human disease, J Clin Immunol, 35, 615, 10.1007/s10875-015-0187-8 Wan, 2015, Opposing roles of STAT1 and STAT3 in IL-21 function in CD4+ T cells, Proc Natl Acad Sci USA, 112, 9394, 10.1073/pnas.1511711112 Sadreev, 2018, The competitive nature of signal transducer and activator of transcription complex formation drives phenotype switching of T cells, Immunology, 153, 488, 10.1111/imm.12851 Novak, 1996, Formation of STAT5-containing DNA binding complexes in response to colony-stimulating factor-1 and platelet-derived growth factor, J Biol Chem, 271, 18350, 10.1074/jbc.271.31.18350 Kanai, 2012, The stat5b pathway defect and autoimmunity, Front Immunol, 3, 234, 10.3389/fimmu.2012.00234 Gutiérrez, 2018, Partial growth hormone insensitivity and dysregulatory immune disease associated with de novo germline activating STAT3 mutations, Mol Cell Endocrinol, 473, 166, 10.1016/j.mce.2018.01.016 Rawlings, 2004, The JAK/STAT signaling pathway, J Cell Sci, 117, 1281, 10.1242/jcs.00963 Zhang, 2013, Mitochondrial localized Stat 3 promotes breast cancer growth via phosphorylation of serine 727, J Biol Chem, 288, 31280, 10.1074/jbc.M113.505057 Raja, 2020, Clin Cancer Res Zhang, 2014, STAT3 in cancer-friend or foe?, Cancers, 6, 1408, 10.3390/cancers6031408 Deenick, 2018, Signal transducer and activator of transcription 3 control of human T and B cell responses, Front Immunol, 9, 168, 10.3389/fimmu.2018.00168 Yang, 2007, STAT3 regulates cytokine-mediated generation of inflammatory helper T cells, J Biol Chem, 282, 9358, 10.1074/jbc.C600321200 Wu, 2016, Stat 3 is important for follicular regulatory T cell differentiation, PLoS One, 11 Yang, 2008, Molecular antagonism and plasticity of regulatory and inflammatory T cell programs, Immunity, 29, 44, 10.1016/j.immuni.2008.05.007 Fornek, 2006, Critical role for Stat 3 in T-dependent terminal differentiation of IgG B cells, Blood, 107, 1085, 10.1182/blood-2005-07-2871 Nabhani, 2017, STAT3 gain-of-function mutations associated with autoimmune lymphoproliferative syndrome like disease deregulate lymphocyte apoptosis and can be targeted by BH3 mimetic compounds, Clin Immunol, 181, 32, 10.1016/j.clim.2017.05.021 Kimura, 2004, SOCS3 is a physiological negative regulator for granulopoiesis and granulocyte colony-stimulating factor receptor signaling, J Biol Chem, 279, 6905, 10.1074/jbc.C300496200 Owen, 2017, STAT5 and CD4 + T cell immunity, F1000Res, 6, 32, 10.12688/f1000research.9838.1 Pillemer, 2007, Deficient SOCS3 expression in CD4+CD25+FoxP3+ regulatory T cells and SOCS3-mediated suppression of Treg function, Eur J Immunol, 37, 2082, 10.1002/eji.200737193 Carpenter, 2014, STAT3 target genes relevant to human cancers, Cancers, 6, 897, 10.3390/cancers6020897 Turkson, 2000, STAT proteins: novel molecular targets for cancer drug discovery, Oncogene, 19, 6613, 10.1038/sj.onc.1204086 Xiong, 2014, Transcription factor STAT3 as a novel molecular target for cancer prevention, Cancers, 6, 926, 10.3390/cancers6020926 Segatto, 2018, STAT3 in breast cancer onset and progression: a matter of time and context, Int J Mol Sci, 19, 9, 10.3390/ijms19092818 Koskela, 2012, Somatic STAT3 mutations in large granular lymphocytic leukemia, N Engl J Med, 366, 1905, 10.1056/NEJMoa1114885 Andersson, 2013, Novel somatic mutations in large granular lymphocytic leukemia affecting the STAT-pathway and T-cell activation, Blood Canc J, 3, e168, 10.1038/bcj.2013.65 Jerez, 2013, STAT3 mutations indicate the presence of subclinical T-cell clones in a subset of aplastic anemia and myelodysplastic syndrome patients, Blood, 122, 2453, 10.1182/blood-2013-04-494930 Rajala, 2014, Uncovering the pathogenesis of large granular lymphocytic leukemia-novel STAT3 and STAT5b mutations, Ann Med, 46, 114, 10.3109/07853890.2014.882105 Lamy, 1998, Dysregulation of CD95/CD95 ligand-apoptotic pathway in CD3(+) large granular lymphocyte leukemia, Blood, 92, 4771, 10.1182/blood.V92.12.4771 Epling-Burnette, 2001, Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression, J Clin Invest, 107, 351, 10.1172/JCI9940 Shah, 2008, Molecular profiling of LGL leukemia reveals role of sphingolipid signaling in survival of cytotoxic lymphocytes, Blood, 112, 770, 10.1182/blood-2007-11-121871 Gutiérrez, 2020, Activating mutations of STAT3: impact on human growth, Mol Cell Endocrinol, 518, 110979, 10.1016/j.mce.2020.110979 Ray, 2013, The IL-6 trans-signaling-STAT3 pathway mediates ECM and cellular proliferation in fibroblasts from hypertrophic scar, J Invest Dermatol, 133, 1212, 10.1038/jid.2012.499 Papaioannou, 2018, STAT3 controls COL1A2 enhancer activation cooperatively with JunB, regulates type I collagen synthesis posttranscriptionally, and is essential for lung myofibroblast differentiation, Mol Biol Cell, 29, 84, 10.1091/mbc.E17-06-0342 Pechkovsky, 2012, STAT3-mediated signaling dysregulates lung fibroblast-myofibroblast activation and differentiation in UIP/IPF, Am J Pathol, 180, 1398, 10.1016/j.ajpath.2011.12.022 Knight, 2011, STAT3 in tissue fibrosis: is there a role in the lung?, Pulm Pharmacol Therapeut, 24, 193, 10.1016/j.pupt.2010.10.005 Prêle, 2012, STAT3: a central mediator of pulmonary fibrosis?, Proc Am Thorac Soc, 9, 177, 10.1513/pats.201201-007AW Kasembeli, 2018, Contribution of STAT3 to inflammatory and fibrotic diseases and prospects for its targeting for treatment, Int J Mol Sci, 19, 2299, 10.3390/ijms19082299 Dees, 2020, TGF-β-induced epigenetic deregulation of SOCS3 facilitates STAT3 signaling to promote fibrosis, J Clin Invest, 130, 2347, 10.1172/JCI122462 Tangye, 2017, Low IgE is insufficiently sensitive to guide genetic testing of STAT3 gain-of-function mutations, Clin Chem, 63, 1539, 10.1373/clinchem.2017.273458 Fusaro, 2021, Improving the diagnostic efficiency of primary immunodeficiencies with targeted next-generation sequencing, J Allergy Clin Immunol, 147, 734, 10.1016/j.jaci.2020.05.046 Maffucci, 2016, Genetic diagnosis using whole exome sequencing in common variable immunodeficiency, Front Immunol, 7, 220, 10.3389/fimmu.2016.00220 Forbes, 2018, Jakinibs for the treatment of immune dysregulation in patients with gain-of-function signal transducer and activator of transcription 1 (STAT1) or STAT3 mutations, J Allergy Clin Immunol, 142, 1665, 10.1016/j.jaci.2018.07.020 Russell, 2018, A novel de novo activating mutation in STAT3 identified in a patient with common variable immunodeficiency (CVID), Clin Immunol, 187, 132, 10.1016/j.clim.2017.11.007 Wienke, 2015, A novel human STAT3 mutation presents with autoimmunity involving Th17 hyperactivation, Oncotarget, 6, 20037, 10.18632/oncotarget.5042 Weinreich, 2017, Up, down, and all around: diagnosis and treatment of novel STAT3 variant, Front Pediatr, 5, 49, 10.3389/fped.2017.00049 Besnard, 2018, Pediatric-onset Evans syndrome: heterogeneous presentation and high frequency of monogenic disorders including LRBA and CTLA4 mutations, Clin Immunol, 188, 52, 10.1016/j.clim.2017.12.009 Giovannini-Chami, 2019, STAT3 gain of function: a new aetiology of severe rheumatic disease, Rheumatology, 58, 365, 10.1093/rheumatology/key308 Khoury, 2017, Tocilizumab promotes regulatory T-cell alleviation in STAT3 gain-of-function-associated multi-organ autoimmune syndrome, Clin Therapeut, 39, 444, 10.1016/j.clinthera.2017.01.004 Bakhtiar, 2019, Allogeneic hematopoietic stem cell transplantation for congenital immune dysregulatory disorders, Front Pediatr, 7, 461, 10.3389/fped.2019.00461 Hadjadj, 2020, Early-onset autoimmunity associated with SOCS1 haploinsufficiency, Nat Commun, 11, 5341, 10.1038/s41467-020-18925-4 Walker, 2016, Identification of a gain-of-function STAT3 mutation (p.Y640F) in lymphocytic variant hypereosinophilic syndrome, Blood, 127, 948, 10.1182/blood-2015-06-654277 Fernandez-Pol, 2021, Two cases with features of lymphocyte variant hypereosinophilic syndrome with STAT3 SH2 domain mutations, Am J Surg Pathol, 45, 193, 10.1097/PAS.0000000000001604