An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronic mucocutaneous candidiasis

Immunity

Volumn 39, Issue 4, 2013, Pages 676-686

  Boisson, Bertrand ^a   Wang, Chenhui ^b   Pedergnana, Vincent ^c,f   Wu, Ling ^b   Cypowyj, Sophie ^a   Rybojad, Michel ^d   Belkadi, Aziz ^c,f   Picard, Capucine ^c,e,f   Abel, Laurent ^c,e,f   Fieschi, Claire ^d,f   Puel, Anne ^c,f   Li, Xiaoxia ^b   Casanova, Jean Laurent ^a,c,e,f  

^a ROCKEFELLER UNIVERSITY   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c IMAGINE INSTITUTE   (France)

^d SAINT LOUIS HOSPITAL   (France)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 17FA; INTERLEUKIN 25; PROTEIN; PROTEIN ACT1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR; UNCLASSIFIED DRUG;

ACT1 GENE; ARTICLE; CYTOKINE PRODUCTION; FIBROBLAST; GENE; GENE MUTATION; HOMOZYGOSITY; HOST RESISTANCE; HUMAN; HUMAN CELL; MISSENSE MUTATION; MUCOCUTANEOUS CANDIDIASIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PSORIASIS;

ADULT; AMINO ACID SEQUENCE; ANTIGENS, CD40; CANDIDIASIS, CHRONIC MUCOCUTANEOUS; FEMALE; FIBROBLASTS; HEAT-SHOCK PROTEINS; HOMOZYGOTE; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INTERLEUKIN-17; MALE; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PEDIGREE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, INTERLEUKIN-17; SIBLINGS; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED PEPTIDES AND PROTEINS;

EID: 84885865938     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.09.002     Document Type: Article

References (75)

1. Abecasis G.R., Cherny S.S., Cookson W.O., Cardon L.R. Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat. Genet. 2002, 30:97-101.
2. Adzhubei I., Jordan D.M., Sunyaev S.R. Predicting Functional Effect of Human Missense Mutations Using PolyPhen-2. Curr. Protoc. Hum. Genet. 2013, Chapter 7. Unit7 20.
3. Alcais A., Quintana-Murci L., Thaler D.S., Schurr E., Abel L., Casanova J.L. Life-threatening infectious diseases of childhood: single-gene inborn errors of immunity?. Ann N Y Acad Sci 2010, 1214:18-33.
4. Atkinson T.P., Schäffer A.A., Grimbacher B., Schroeder H.W., Woellner C., Zerbe C.S., Puck J.M. An immune defect causing dominant chronic mucocutaneous candidiasis and thyroid disease maps to chromosome 2p in a single family. Am. J. Hum. Genet. 2001, 69:791-803.
5. Bieber T. Atopic dermatitis. N.Engl. J. Med. 2008, 358:1483-1494.
6. Bogunovic D., Byun M., Durfee L.A., Abhyankar A., Sanal O., Mansouri D., Salem S., Radovanovic I., Grant A.V., Adimi P., et al. Mycobacterial Disease and Impaired IFN-gamma Immunity in Humans with Inherited ISG15 Deficiency. Science 2012, 337:1684-1688.
7. Boisson B., Laplantine E., Prando C., Giliani S., Israelsson E., Xu Z., Abhyankar A., Israël L., Trevejo-Nunez G., Bogunovic D., et al. Immunodeficiency, autoinflammation and amylopectinosis in humans with inherited HOIL-1 and LUBAC deficiency. Nat. Immunol. 2012, 13:1178-1186.
8. Bolze A., Byun M., McDonald D., Morgan N.V., Abhyankar A., Premkumar L., Puel A., Bacon C.M., Rieux-Laucat F., Pang K., et al. Whole-exome-sequencing-based discovery of human FADD deficiency. Am. J. Hum. Genet. 2010, 87:873-881.
9. Byun M., Abhyankar A., Lelarge V., Plancoulaine S., Palanduz A., Telhan L., Boisson B., Picard C., Dewell S., Zhao C., et al. Whole-exome sequencing-based discovery of STIM1 deficiency in a child with fatal classic Kaposi sarcoma. J.Exp. Med. 2010, 207:2307-2312.
10. Canales L., Middlemas R.O., Louro J.M., South M.A. Immunological observations in chronic mucocutaneous candidiasis. Lancet 1969, 2:567-571.
11. Casanova J.-L., Abel L. The Genetic Theory of Infectious Diseases: A Brief History and Selected Illustrations. Annual Review of Genomics and Human Genetics 2013, 14:215-243.
12. Chandesris M.O., Melki I., Natividad A., Puel A., Fieschi C., Yun L., Thumerelle C., Oksenhendler E., Boutboul D., Thomas C., et al. Autosomal dominant STAT3 deficiency and hyper-IgE syndrome: molecular, cellular, and clinical features from a French national survey. Medicine (Baltimore) 2012, 91:e1-e19.
13. Chang S.H., Park H., Dong C. Act1 adaptor protein is an immediate and essential signaling component of interleukin-17 receptor. J.Biol. Chem. 2006, 281:35603-35607.
14. Chang S.H., Reynolds J.M., Pappu B.P., Chen G., Martinez G.J., Dong C. Interleukin-17C promotes Th17 cell responses and autoimmune disease via interleukin-17 receptor E. Immunity 2011, 35:611-621.
15. Claudio E., Sønder S.U., Saret S., Carvalho G., Ramalingam T.R., Wynn T.A., Chariot A., Garcia-Perganeda A., Leonardi A., Paun A., et al. The adaptor protein CIKS/Act1 is essential for IL-25-mediated allergic airway inflammation. J.Immunol. 2009, 182:1617-1630.
16. de Beaucoudrey L., Puel A., Filipe-Santos O., Cobat A., Ghandil P., Chrabieh M., Feinberg J., von Bernuth H., Samarina A., Jannière L., et al. Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing Tcells. J.Exp. Med. 2008, 205:1543-1550.
17. de Beaucoudrey L., Samarina A., Bustamante J., Cobat A., Boisson-Dupuis S., Feinberg J., Al-Muhsen S., Jannière L., Rose Y., de Suremain M., et al. Revisiting human IL-12Rβ1 deficiency: a survey of 141 patients from 30countries. Medicine (Baltimore) 2010, 89:381-402.
18. Drewniak A., Gazendam R.P., Tool A.T., van Houdt M., Jansen M.H., van Hamme J.L., van Leeuwen E.M., Roos D., Scalais E., de Beaufort C., et al. Invasive fungal infection and impaired neutrophil killing in human CARD9 deficiency. Blood 2013, 121:2385-2392.
19. Ellinghaus E., Ellinghaus D., Stuart P.E., Nair R.P., Debrus S., Raelson J.V., Belouchi M., Fournier H., Reinhard C., Ding J., et al. Genome-wide association study identifies a psoriasis susceptibility locus at TRAF3IP2. Nat. Genet. 2010, 42:991-995.
20. Fallon P.G., Ballantyne S.J., Mangan N.E., Barlow J.L., Dasvarma A., Hewett D.R., McIlgorm A., Jolin H.E., McKenzie A.N. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J.Exp. Med. 2006, 203:1105-1116.
21. Gaffen S.L. Structure and signalling in the IL-17 receptor family. Nat. Rev. Immunol. 2009, 9:556-567.
22. Glocker E., Grimbacher B. Chronic mucocutaneous candidiasis and congenital susceptibility to Candida. Curr. Opin. Allergy Clin. Immunol. 2010, 10:542-550.
23. Glocker E.O., Hennigs A., Nabavi M., Schäffer A.A., Woellner C., Salzer U., Pfeifer D., Veelken H., Warnatz K., Tahami F., et al. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N.Engl. J. Med. 2009, 361:1727-1735.
24. 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.
25. Hüffmeier U., Uebe S., Ekici A.B., Bowes J., Giardina E., Korendowych E., Juneblad K., Apel M., McManus R., Ho P., et al. Common variants at TRAF3IP2 are associated with susceptibility to psoriatic arthritis and psoriasis. Nat. Genet. 2010, 42:996-999.
26. Kalliomäki M., Salminen S., Arvilommi H., Kero P., Koskinen P., Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 2001, 357:1076-1079.
27. Kang Z., Swaidani S., Yin W., Wang C., Barlow J.L., Gulen M.F., Bulek K., Do J.S., Aronica M., McKenzie A.N., et al. Epithelial cell-specific Act1 adaptor mediates interleukin-25-dependent helminth expulsion through expansion of Lin(-)c-Kit(+) innate cell population. Immunity 2012, 36:821-833.
28. Kirkpatrick C.H., Rich R.R., Graw R.G., Smith T.K., Mickenberg I., Rogentine G.N. Treatment of chronic mucocutaneous moniliasis by immunologic reconstitution. Clin. Exp. Immunol. 1971, 9:733-748.
29. 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., et al. Chronic mucocutaneous candidiasis in APECED or thymoma patients correlates with autoimmunity to Th17-associated cytokines. J.Exp. Med. 2010, 207:299-308.
30. Leroy D., Dompmartin A., Houtteville J.P., Theron J. Aneurysm associated with chronic mucocutaneous candidiasis during long-term therapy with ketoconazole. Dermatologica 1989, 178:43-46.
31. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
32. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 1000 Genome Project Data Processing Subgroup.
33. Lilic D. Unravelling fungal immunity through primary immune deficiencies. Curr. Opin. Microbiol. 2012, 15:420-426.
34. Liu C., Swaidani S., Qian W., Kang Z., Sun P., Han Y., Wang C., Gulen M.F., Yin W., Zhang C., et al. A CC' loop decoy peptide blocks the interaction between Act1 and IL-17RA to attenuate IL-17- and IL-25-induced inflammation. Sci. Signal. 2011, 4:ra72.
35. Liu L., Okada S., Kong X.F., Kreins A.Y., Cypowyj S., Abhyankar A., Toubiana J., Itan Y., Audry M., Nitschke P., et al. Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis. J.Exp. Med. 2011, 208:1635-1648.
36. Ma C.S., Chew G.Y., Simpson N., Priyadarshi A., Wong M., Grimbacher B., Fulcher D.A., Tangye S.G., Cook M.C. Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J.Exp. Med. 2008, 205:1551-1557.
37. Maitra A., Shen F., Hanel W., Mossman K., Tocker J., Swart D., Gaffen S.L. Distinct functional motifs within the IL-17 receptor regulate signal transduction and target gene expression. Proc. Natl. Acad. Sci. USA 2007, 104:7506-7511.
38. Matsushima Y., Kikkawa Y., Takada T., Matsuoka K., Seki Y., Yoshida H., Minegishi Y., Karasuyama H., Yonekawa H. An atopic dermatitis-like skin disease with hyper-IgE-emia develops in mice carrying a spontaneous recessive point mutation in the Traf3ip2 (Act1/CIKS) gene. J.Immunol. 2010, 185:2340-2349.
39. Mauro C., Vito P., Mellone S., Pacifico F., Chariot A., Formisano S., Leonardi A. Role of the adaptor protein CIKS in the activation of the IKK complex. Biochem. Biophys. Res. Commun. 2003, 309:84-90.
40. McKenna A., Hanna M., Banks E., Sivachenko A., Cibulskis K., Kernytsky A., Garimella K., Altshuler D., Gabriel S., Daly M., DePristo M.A. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010, 20:1297-1303.
41. Mellett M., Atzei P., Horgan A., Hams E., Floss T., Wurst W., Fallon P.G., Moynagh P.N. Orphan receptor IL-17RD tunes IL-17A signalling and is required for neutrophilia. Nat Commun 2012, 3:1119.
42. Milner J.D., Brenchley J.M., Laurence A., Freeman A.F., Hill B.J., Elias K.M., Kanno Y., Spalding C., Elloumi H.Z., Paulson M.L., et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 2008, 452:773-776.
43. Minegishi Y., Saito M., Nagasawa M., Takada H., Hara T., Tsuchiya S., Agematsu K., Yamada M., Kawamura N., Ariga T., et al. Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J.Exp. Med. 2009, 206:1291-1301.
44. Ng P.C., Henikoff S. SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res. 2003, 31:3812-3814.
45. Nograles K.E., Zaba L.C., Shemer A., Fuentes-Duculan J., Cardinale I., Kikuchi T., Ramon M., Bergman R., Krueger J.G., Guttman-Yassky E. IL-22-producing "T22" Tcells account for upregulated IL-22 in atopic dermatitis despite reduced IL-17-producing TH17 Tcells. J Allergy Clin. Immunol. 2009, 123:1244-1252. e1242.
46. Novatchkova M., Leibbrandt A., Werzowa J., Neubüser A., Eisenhaber F. The STIR-domain superfamily in signal transduction, development and immunity. Trends Biochem. Sci. 2003, 28:226-229.
47. Onishi R.M., Gaffen S.L. Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology 2010, 129:311-321.
48. Owyang A.M., Zaph C., Wilson E.H., Guild K.J., McClanahan T., Miller H.R., Cua D.J., Goldschmidt M., Hunter C.A., Kastelein R.A., Artis D. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J.Exp. Med. 2006, 203:843-849.
49. 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, 92:109-122.
50. Puel A., Döffinger R., Natividad A., Chrabieh M., Barcenas-Morales G., Picard C., Cobat A., Ouachée-Chardin M., Toulon A., Bustamante J., et al. 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.
51. Puel A., Cypowyj S., Bustamante J., Wright J.F., Liu L., Lim H.K., Migaud M., Israel L., Chrabieh M., Audry M., et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011, 332:65-68.
52. Puel A., Cypowyj S., Maródi L., Abel L., Picard C., Casanova J.L. Inborn errors of human IL-17 immunity underlie chronic mucocutaneous candidiasis. Curr. Opin. Allergy Clin. Immunol. 2012, 12:616-622.
53. Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M.A., Bender D., Maller J., Sklar P., de Bakker P.I., Daly M.J., Sham P.C. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 2007, 81:559-575.
54. Qian Y., Qin J., Cui G., Naramura M., Snow E.C., Ware C.F., Fairchild R.L., Omori S.A., Rickert R.C., Scott M., et al. Act1, a negative regulator in CD40- and BAFF-mediated B cell survival. Immunity 2004, 21:575-587.
55. Qian Y., Liu C., Hartupee J., Altuntas C.Z., Gulen M.F., Jane-Wit D., Xiao J., Lu Y., Giltiay N., Liu J., et al. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat. Immunol. 2007, 8:247-256.
56. Qian Y., Giltiay N., Xiao J., Wang Y., Tian J., Han S., Scott M., Carter R., Jorgensen T.N., Li X. Deficiency of Act1, a critical modulator of B cell function, leads to development of Sjögren's syndrome. Eur. J. Immunol. 2008, 38:2219-2228.
57. Ramirez-Carrozzi V., Sambandam A., Luis E., Lin Z., Jeet S., Lesch J., Hackney J., Kim J., Zhou M., Lai J., et al. IL-17C regulates the innate immune function of epithelial cells in an autocrine manner. Nat. Immunol. 2011, 12:1159-1166.
58. Renner E.D., Rylaarsdam S., Anover-Sombke S., Rack A.L., Reichenbach J., Carey J.C., Zhu Q., Jansson A.F., Barboza J., Schimke L.F., et al. Novel signal transducer and activator of transcription 3 (STAT3) mutations, reduced T(H)17 cell numbers, and variably defective STAT3 phosphorylation in hyper-IgE syndrome. J.Allergy Clin. Immunol. 2008, 122:181-187.
59. Rickel E.A., Siegel L.A., Yoon B.R., Rottman J.B., Kugler D.G., Swart D.A., Anders P.M., Tocker J.E., Comeau M.R., Budelsky A.L. Identification of functional roles for both IL-17RB and IL-17RA in mediating IL-25-induced activities. J.Immunol. 2008, 181:4299-4310.
60. Romberg N., Morbach H., Lawrence M.G., Kim S., Kang I., Holland S.M., Milner J.D., Meffre E. Gain-of-function STAT1 mutations are associated with PD-L1 overexpression and a defect in B-cell survival. J.Allergy Clin. Immunol. 2013, 131:1691-1693.
61. 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., et al. Signal transducer and activator of transcription 1 (STAT1) gain-of-function mutations and disseminated coccidioidomycosis and histoplasmosis. J Allergy Clin. Immunol. 2013, 131:1624-1634. e1617.
62. Shi Y., Ullrich S.J., Zhang J., Connolly K., Grzegorzewski K.J., Barber M.C., Wang W., Wathen K., Hodge V., Fisher C.L., et al. A novel cytokine receptor-ligand pair. Identification, molecular characterization, and invivo immunomodulatory activity. J.Biol. Chem. 2000, 275:19167-19176.
63. Smeekens S.P., Plantinga T.S., van de Veerdonk F.L., Heinhuis B., Hoischen A., Joosten L.A., Arkwright P.D., Gennery A., Kullberg B.J., Veltman J.A., et al. STAT1 hyperphosphorylation and defective IL12R/IL23R signaling underlie defective immunity in autosomal dominant chronic mucocutaneous candidiasis. PLoS ONE 2011, 6:e29248.
64. Song X., Zhu S., Shi P., Liu Y., Shi Y., Levin S.D., Qian Y. IL-17RE is the functional receptor for IL-17C and mediates mucosal immunity to infection with intestinal pathogens. Nat. Immunol. 2011, 12:1151-1158.
65. Sun D., Novotny M., Bulek K., Liu C., Li X., Hamilton T. Treatment with IL-17 prolongs the half-life of chemokine CXCL1 mRNA via the adaptor TRAF5 and the splicing-regulatory factor SF2 (ASF). Nat. Immunol. 2011, 12:853-860.
66. 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.
67. 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., et al. Dominant gain-of-function STAT1 mutations in FOXP3 wild-type immune dysregulation-polyendocrinopathy-enteropathy-X-linked-like syndrome. J Allergy Clin. Immunol. 2013, 131:1611-1623. e1613.
68. van de Veerdonk F.L., Plantinga T.S., Hoischen A., Smeekens S.P., Joosten L.A., Gilissen C., Arts P., Rosentul D.C., Carmichael A.J., Smits-van der Graaf C.A., et al. STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. N.Engl. J. Med. 2011, 365:54-61.
69. Wang C., Wu L., Bulek K., Martin B.N., Zepp J.A., Kang Z., Liu C., Herjan T., Misra S., Carman J.A., et al. The psoriasis-associated D10N variant of the adaptor Act1 with impaired regulation by the molecular chaperone hsp90. Nat. Immunol. 2013, 14:72-81.
70. Wang X., Lin Z., Gao L., Wang A., Wan Z., Chen W., Yang Y., Li R. Exome sequencing reveals a signal transducer and activator of transcription 1 (STAT1) mutation in a child with recalcitrant cutaneous fusariosis. J.Allergy Clin. Immunol. 2013, 131:1242-1243.
71. Wells R.S. Chronic oral candidiasis (autosomal recessive inheritance) (three cases). Proc. R. Soc. Med. 1970, 63:890-891.
72. Wells R.S., Higgs J.M., Macdonald A., Valdimarsson H., Holt P.J. Familial chronic muco-cutaneous candidiasis. J.Med. Genet. 1972, 9:302-310.
73. Williamson D.M. Chronic hyperplastic candidiasis and squamous carcinoma. Br. J. Dermatol. 1969, 81:125-127.
74. Zhang B., Liu C., Qian W., Han Y., Li X., Deng J. Crystal Structure of IL-17 Receptor B SEFIR Domain. J Immunol. 2013, 190:2320-2326.
75. Zhao A., Urban J.F., Sun R., Stiltz J., Morimoto M., Notari L., Madden K.B., Yang Z., Grinchuk V., Ramalingam T.R., et al. Critical role of IL-25 in nematode infection-induced alterations in intestinal function. J.Immunol. 2010, 185:6921-6929.