A novel gain-of-function STAT1 mutation resulting in basal phosphorylation of STAT1 and increased distal IFN-γ-mediated responses in chronic mucocutaneous candidiasis

Molecular Immunology

Volumn 68, Issue 2, 2015, Pages 597-605

  Martinez Martinez, Laura ^a   Martinez Saavedra, Maria Teresa ^b   Fuentes Prior, Pablo ^c   Barnadas, Maria ^a   Rubiales, Maria Victoria ^a   Noda, Judith ^b   Badell, Isabel ^a   Rodríguez Gallego, Carlos ^d,e   de la Calle Martin, Oscar ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b HOSPITAL UNIVERSITARIO DE GRAN CANARIA DR NEGRÍN   (Spain)

^c HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^d HOSPITAL UNIVERSITARIO SON ESPASES   (Spain)

^e HEALTH RESEARCH INSTITUTE OF THE BALEARIC ISLANDS IDISBA   (Spain)

Author keywords

Chronic mucocutaneous candidiasis; Coiled coil domain; Gain of function mutation; IFN ; IL 17 producing T cells; STAT1

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; STAT1 PROTEIN; IL17A PROTEIN, HUMAN; STAT1 PROTEIN, HUMAN;

ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; CYTOKINE PRODUCTION; GAIN OF FUNCTION MUTATION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; MALE; MUCOCUTANEOUS CANDIDIASIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYCLONAL ACTIVATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE; ADULT; CASE REPORT; CD4+ T LYMPHOCYTE; CHILD; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; METABOLISM; MUTATION; PEDIGREE; PHOSPHORYLATION; T LYMPHOCYTE SUBPOPULATION;

ADULT; CANDIDIASIS, CHRONIC MUCOCUTANEOUS; CD4-POSITIVE T-LYMPHOCYTES; CHILD; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-17; MALE; MUTATION; PEDIGREE; PHOSPHORYLATION; STAT1 TRANSCRIPTION FACTOR; T-LYMPHOCYTE SUBSETS;

EID: 84949213854     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2015.09.014     Document Type: Article

References (37)

1. Basu R., Hatton R.D., Weaver C.T. The Th17 family: flexibility follows function. Immunol. Rev. 2013, 252:89-103. 10.1111/imr.12035.
2. Boisson B., Wang C., Pedergnana V., Wu L., Cypowyj S., Rybojad M., Belkadi A., Picard C., Abel L., Fieschi C., Puel A., Li X., Casanova J.L. An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronic mucocutaneous candidiasis. Immunity 2013, 39:676-686. 10.1016/j.immuni.2013.09.002.
3. Boisson-Dupuis S., Kong X.F., Okada S., Cypowyj S., Puel A., Abel L., Casanova J.L. Inborn errors of human STAT1: allelic heterogeneity governs the diversity of immunological and infectious phenotypes. Curr. Opin. Immunol. 2012, 10.1016/j.coi.2012.04.011.
4. Cheon H., Stark G.R. Unphosphorylated STAT1 prolongs the expression of interferon-induced immune regulatory genes. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9373-9378. 10.1073/pnas.0903487106.
5. Cypowyj S., Picard C., Maródi L., Casanova J.L., Puel A. Immunity to infection in IL-17-deficient mice and humans. Eur. J. Immunol. 2012, 10.1002/eji.201242605.
6. Dupuis S., Dargemont C., Fieschi C., Thomassin N., Rosenzweig S., Harris J., Holland S.M., Schreiber R.D., Casanova J.L. Impairment of mycobacterial but not viral immunity by a germline human STAT1 mutation. Science 2001, 293:300-303. 10.1126/science.1061154.
7. Dupuis S., Jouanguy E., Al-Hajjar S., Fieschi C., Al-Mohsen I.Z., Al-Jumaah S., Yang K., Chapgier A., Eidenschenk C., Eid P., Al Ghonaium A., Tufenkeji H., Frayha H., Al-Gazlan S., Al-Rayes H., Schreiber R.D., Gresser I., Casanova J.-L. Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat. Genet. 2003, 10.1038/ng1097.
8. Engelhardt K.R., Grimbacher B. Mendelian traits causing susceptibility to mucocutaneous fungal infections in human subjects. J. Allergy Clin. Immunol. 2012, 10.1016/j.jaci.2011.12.966.
9. Frans G., Moens L., Schaballie H., Van Eyck L., Borgers H., Wuyts M., Dillaerts D., Vermeulen E., Dooley J., Grimbacher B., Cant A., Declerck D., Peumans M., Renard M., De Boeck K., Hoffman I., François I., Liston A., Claessens F., Bossuyt X., Meyts I. Gain-of-function mutations in signal transducer and activator of transcription 1 (STAT1): chronic mucocutaneous candidiasis accompanied by enamel defects and delayed dental shedding. J. Allergy Clin. Immunol. 2014, 134:1209-1213. e6. 10.1016/j.jaci.2014.05.044.
10. Glocker E.-O., Hennigs A., Nabavi M., Schäffer A.A., Woellner C., Salzer U., Pfeifer D., Veelken H., Warnatz K., Tahami F., Jamal S., Manguiat A., Rezaei N., Amirzargar A.A., Plebani A., Hannesschläger N., Gross O., Ruland J., Grimbacher B. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N. Engl. J. Med. 2009, 361:1727-1735. 10.1056/NEJMoa0810719.
11. Guarda G., Braun M., Staehli F., Tardivel A., Mattmann C., Förster I., Farlik M., Decker T., Du Pasquier R.A., Romero P., Tschopp J. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011, 34:213-223. 10.1016/j.immuni.2011.02.006.
12. Hori T., Ohnishi H., Teramoto T., Tsubouchi K., Naiki T., Hirose Y., Ohara O., Seishima M., Kaneko H., Fukao T., Kondo N. Autosomal-dominant chronic mucocutaneous candidiasis with stat1-mutation can be complicated with chronic active hepatitis and hypothyroidism. J. Clin. Immunol. 2012, 32:1213-1220. 10.1007/s10875-012-9744-6.
13. Kisand K., Bøe Wolff A.S., Podkrajsek K.T., Tserel L., Link M., Kisand K.V., Ersvaer E., Perheentupa J., Erichsen M.M., Bratanic N., Meloni A., Cetani F., Perniola R., Ergun-Longmire B., Maclaren N., Krohn K.J.E., Pura M., Schalke B., Ströbel P., Leite M.I., Battelino T., Husebye E.S., Peterson P., Willcox N., Meager A. Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th 17-associated cytokines. J. Exp. Med. 2010, 10.1084/jem.20091669.
14. Kumar N., Hanks M.E., Chandrasekaran P., Davis B.C., Hsu A.P., Van Wagoner N.J., Merlin J.S., Spalding C., La Hoz R.M., Holland S.M., Zerbe C.S., Sampaio E.P. Gain-of-function signal transducer and activator of transcription 1 (STAT1) mutation-related primary immunodeficiency is associated with disseminated mucormycosis. J. Allergy Clin. Immunol. 2014, 134:236-239. 10.1016/j.jaci.2014.02.037.
15. Lasiglie D., Traggiai E., Federici S., Alessio M., Buoncompagni A., Accogli A., Penco F., Martini A., Gattomo M. Role of IL-1beta in the development of human TH17 cells: lesson from patients carrying NLPR3 gene mutations. Clin. Exp. Rheumatol. 2011, 29:381-382.
16. Liu L., Okada S., Kong X.-F., Kreins A.Y., Cypowyj S., Abhyankar A., Toubiana J., Itan Y., Audry M., Nitschke P., Masson C., Toth B., Flatot J., Migaud M., Chrabieh M., Kochetkov T., Bolze A., Borghesi A., Toulon A., Hiller J., Eyerich S., Eyerich K., Gulácsy V., Chernyshova L., Chernyshov V., Bondarenko A., Grimaldo R.M.C., Blancas-Galicia L., Beas I.M.M., Roesler J., Magdorf K., Engelhard D., Thumerelle C., Burgel P.-R., Hoernes M., Drexel B., Seger R., Kusuma T., Jansson A.F., Sawalle-Belohradsky J., Belohradsky B., Jouanguy E., Bustamante J., Bué M., Karin N., Wildbaum G., Bodemer C., Lortholary O., Fischer A., Blanche S., Al-Muhsen S., Reichenbach J., Kobayashi M., Rosales F.E., Lozano C.T., Kilic S.S., Oleastro M., Etzioni A., Traidl-Hoffmann C., Renner E.D., Abel L., Picard C., Maródi L., Boisson-Dupuis S., Puel A., Casanova J.-L. Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis. J. Exp. Med. 2011, 208:1635-1648. 10.1084/jem.20110958.
17. Maggi L., Santarlasci V., Capone M., Rossi M.C., Querci V., Mazzoni A., Cimaz R., De Palma R., Liotta F., Maggi E., Romagnani S., Cosmi L., Annunziato F. Distinctive features of classic and nonclassic (Th17 derived) human Th1 cells. Eur. J. Immunol. 2012, 42:3180-3188. 10.1002/eji.201242648.
18. Mills K.H.G., Dungan L.S., Jones S.a., Harris J. The role of inflammasome-derived IL-1 in driving IL-17 responses. J. Leukoc. Biol. 2013, 93:489-497. 10.1189/jlb.1012543.
19. Minegishi Y. Hyper-IgE syndrome. Curr. Opin. Immunol. 2009, 10.1016/j.coi.2009.07.013.
20. Puel A., Cypowyj S., Bustamante J., Wright J.F., Liu L., Lim H.K., Migaud M., Israel L., Chrabieh M., Audry M., Gumbleton M., Toulon A., Bodemer C., El-Baghdadi J., Whitters M., Paradis T., Brooks J., Collins M., Wolfman N.M., Al-Muhsen S., Galicchio M., Abel L., Picard C., Casanova J.-L. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science (New York, N.Y.) 2011, 10.1542/peds.2011-2107CCCC.
21. Puel A., Döffinger R., Natividad A., Chrabieh M., Barcenas-Morales G., Picard C., Cobat A., Ouachée-Chardin M., Toulon A., Bustamante J., Al-Muhsen S., Al-Owain M., Arkwright P.D., Costigan C., McConnell V., Cant A.J., Abinun M., Polak M., Bougnères P.-F., Kumararatne D., Marodi L., Nahum A., Roifman C., Blanche S., Fischer A., Bodemer C., Abel L., Lilic D., Casanova J.-L. Autoantibodies against IL-17A, IL-17F, and IL-22 in patients with chronic mucocutaneous candidiasis and autoimmune polyendocrine syndrome type I. J. Exp. Med. 2010, 207:291-297. 10.1084/jem.20091983.
22. Puel A., Picard C., Cypowyj S., Lilic D., Abel L., Casanova J.L. Inborn errors of mucocutaneous immunity to Candida albicans in humans: a role for IL-17 cytokines?. Curr. Opin. Immunol. 2010, 10.1016/j.coi.2010.06.009.
23. Rautemaa R., Hietanen J., Niissalo S., Pirinen S., Perheentupa J. Oral and oesophageal squamous cell carcinoma-a complication or component of autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED, APS-I). Oral Oncol. 2007, 43:607-613. 10.1016/j.oraloncology.2006.07.005.
24. Rosa D.D., Pasqualotto A.C., Denning D.W. Chronic mucocutaneous candidiasis and oesophageal cancer. Med. Mycol. 2008, 10.1080/13693780701616023.
25. Sampaio E.P., Hsu A.P., Pechacek J., Bax H.I., Dias D.L., Paulson M.L., Chandrasekaran P., Rosen L.B., Carvalho D.S., Ding L., Vinh D.C., Browne S.K., Datta S., Milner J.D., Kuhns D.B., Long Priel D.A., Sadat M.A., Shiloh M., De Marco B., Alvares M., Gillman J.W., Ramarathnam V., De La Morena M., Bezrodnik L., Moreira I., Uzel G., Johnson D., Spalding C., Zerbe C.S., Wiley H., Greenberg D.E., Hoover S.E., Rosenzweig S.D., Galgiani J.N., Holland S.M. Signal transducer and activator of transcription 1 (STAT1) gain-of-function mutations and disseminated coccidioidomycosis and histoplasmosis. J. Allergy Clin. Immunol. 2013, 131. 10.1016/j.jaci.2013.01.052.
26. Smeekens S.P., Plantinga T.S., van de Veerdonk F.L., Heinhuis B., Hoischen A., Joosten L.A.B., Arkwright P.D., Gennery A., Kullberg B.J., Veltman J.A., Lilic D., van der Meer J.W.M., Netea M.G. STAT1 hyperphosphorylation and defective IL12r/IL23r signaling underlie defective immunity in autosomal dominant chronic mucocutaneous candidiasis. PLoS One 2011, 6. 10.1371/journal.pone.0029248.
27. Sohn S.-Y., Hearing P. Adenovirus sequesters phosphorylated STAT1 at viral replication centers and inhibits STAT dephosphorylation. J. Virol. 2011, 85:7555-7562. 10.1128/JVI.00513-11.
28. Sologuren I., Boisson-Dupuis S., Pestano J., Vincent Q.B., Fernández-Pérez L., Chapgier A., Cárdenes M., Feinberg J., García-Laorden M.I., Picard C., Santiago E., Kong X., Jannière L., Colino E., Herrera-Ramos E., Francés A., Navarrete C., Blanche S., Faria E., Remiszewski P., Cordeiro A., Freeman A., Holland S., Abarca K., Valerón-Lemaur M., Gonçalo-Marques J., Silveira L., García-Castellano J.M., Caminero J., Pérez-Arellano J.L., Bustamante J.L.A., Abel L., Casanova J.L., Rodríguez-Gallego C. Partial recessive IFN-(R1 deficiency: genetic, immunological and clinical features of 14 patients from 11 kindreds. Hum. Mol. Genet. 2011, 20:1509-1523. 10.1093/hmg/ddr029.
29. Soltész B., Tóth B., Shabashova N., Bondarenko A., Okada S., Cypowyj S., Abhyankar A., Csorba G., Taskó S., Sarkadi A.K., Méhes L., Rozsíval P., Neumann D., Chernyshova L., Tulassay Z., Puel A., Casanova J.-L., Sediva A., Litzman J., Maródi L. New and recurrent gain-of-function STAT1 mutations in patients with chronic mucocutaneous candidiasis from Eastern and Central Europe. J. Med. Genet. 2013, 50:567-578. 10.1136/jmedgenet-2013-101570.
30. Takezaki S., Yamada M., Kato M., Park M.-J., Maruyama K., Yamazaki Y., Chida N., Ohara O., Kobayashi I., Ariga T. Chronic mucocutaneous candidiasis caused by a gain-of-function mutation in the STAT1 DNA-binding domain. J. Immunol. 2012, 189:1521-1526. 10.4049/jimmunol.1200926.
31. Tóth B., Méhes L., Taskó S., Szalai Z., Tulassay Z., Cypowyj S., Casanova J.L., Puel A., Maródi L. Herpes in STAT1 deficiency. Lancet 2012, 379:2500. 10.1016/s0140-6736(12)60,365-1.
32. Uzel G., Sampaio E.P., Lawrence M.G., Hsu A.P., Hackett M., Dorsey M.J., Noel R.J., Verbsky J.W., Freeman A.F., Janssen E., Bonilla F.A., Pechacek J., Chandrasekaran P., Browne S.K., Agharahimi A., Gharib A.M., Mannurita S.C., Yim J.J., Gambineri E., Torgerson T., Tran D.Q., Milner J.D., Holland S.M. Dominant gain-of-function STAT1 mutations in FOXP3 wild-type immune dysregulation-polyendocrinopathy-enteropathy-X-linked-like syndrome. J. Allergy Clin. Immunol. 2013, 131. 10.1016/j.jaci.2012.11.054.
33. Van de Veerdonk F.L., Joosten L.A.B., Shaw P.J., Smeekens S.P., Malireddi R.K.S., van der Meer J.W.M., Kullberg B.J., Netea M.G., Kanneganti T.D. The inflammasome drives protective Th1 and Th17 cellular responses in disseminated candidiasis. Eur. J. Immunol. 2011, 41:2260-2268. 10.1002/eji.201041226.
34. Van de Veerdonk F.L., Plantinga T.S., Hoischen A., Smeekens S.P., Joosten L.A.B., Gilissen C., Arts P., Rosentul D.C., Carmichael A.J., Smits-van der Graaf C.A.A., Kullberg B.J., van der Meer J.W.M., Lilic D., Veltman J.A., Netea M.G. STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. N. Engl. J. Med. 2011, 365:54-61. 10.1056/NEJMoa1100102.
35. Yamane H., Paul W.E. Early signaling events that underlie fate decisions of naive CD4+ T cells toward distinct T-helper cell subsets. Immunol. Rev. 2013, 252:12-23. 10.1111/imr.12032.
36. Yamazaki Y., Yamada M., Kawai T., Morio T., Onodera M., Ueki M., Watanabe N., Takada H., Takezaki S., Chida N., Kobayashi I., Ariga T. Two novel gain-of-function mutations of STAT1 responsible for chronic mucocutaneous candidiasis disease: impaired production of IL-17A and IL-22, and the presence of Anti-IL-17F autoantibody. J. Immunol. 2014, 193:4880-4887. 10.4049/jimmunol.1401467.
37. Zielinski C.E., Mele F., Aschenbrenner D., Jarrossay D., Ronchi F., Gattorno M., Monticelli S., Lanzavecchia A., Sallusto F. Pathogen-induced human TH17 cells produce IFN-[ggr] or IL-10 and are regulated by IL-1[bgr]. Nature 2012, 484:514-518.