Impaired RASGRF1/ERK-mediated GM-CSF response characterizes CARD9 deficiency in French-Canadians

Journal of Allergy and Clinical Immunology

Volumn 137, Issue 4, 2016, Pages 1178-1188.e7

  Gavino, Christina ^a   Hamel, Nancy ^a,b   Zeng, Ji Bin ^a   Legault, Catherine ^b   Guiot, Marie Christine ^b   Chankowsky, Jeffrey ^b   Lejtenyi, Duncan ^b   Lemire, Martine ^b   Alarie, Isabelle ^c   Dufresne, Simon ^d   Boursiquot, Jean Nicolas ^e   McIntosh, Fiona ^a   Langelier, Mélanie ^a   Behr, Marcel A ^a,b   Sheppard, Donald C ^b   Foulkes, William D ^a,b   Vinh, Donald C ^a,b  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c CENTRE HOSPITALIER UNIVERSITAIRE DE SHERBROOKE   (Canada)

^d MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^e LAVAL UNIVERSITY   (Canada)

Author keywords

candidiasis; Caspase recruitment domain containing protein 9; CSF2; extracellular signal regulated kinase; GM CSF; Ras protein specific guanine nucleotide releasing factor 1; spontaneous central nervous system candidiasis

Indexed keywords

CASPASE RECRUITMENT DOMAIN CONTAINING PROTEIN 9; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PEPTIDES AND PROTEINS; PROTEIN BCL 10; RAS PROTEIN SPECIFIC GUANINE NUCLEOTIDE RELEASING FACTOR 1; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CARD9 PROTEIN, HUMAN; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; GENETIC MARKER; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RASGRF1 PROTEIN, HUMAN;

ADULT; ALLELIC IMBALANCE; ARTICLE; CANADIAN; CANDIDA ALBICANS; CASE REPORT; CONTROLLED STUDY; DISEASE PREDISPOSITION; FOUNDER EFFECT; GENE EXPRESSION; GENE MUTATION; HUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; YOUNG ADULT; CANDIDIASIS, INVASIVE; CENTRAL NERVOUS SYSTEM FUNGAL INFECTIONS; COHORT ANALYSIS; DEFICIENCY; FEMALE; GENETIC MARKER; GENETICS; IMMUNOLOGIC DEFICIENCY SYNDROMES; IMMUNOLOGY; MALE; METABOLISM; MICROBIOLOGY; POINT MUTATION; QUEBEC; REAL TIME POLYMERASE CHAIN REACTION;

ADULT; BIOMARKERS; CANDIDIASIS, INVASIVE; CARD SIGNALING ADAPTOR PROTEINS; CENTRAL NERVOUS SYSTEM FUNGAL INFECTIONS; COHORT STUDIES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENETIC MARKERS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMUNOLOGIC DEFICIENCY SYNDROMES; MALE; POINT MUTATION; QUEBEC; RAS-GRF1; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84951320697     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.09.016     Document Type: Article

References (42)

1. E.O. Glocker, A. Hennigs, M. Nabavi, A.A. Schäffer, C. Woellner, U. Salzer, and et al. A homozygous CARD9 mutation in a family with susceptibility to fungal infections N Engl J Med 361 2009 1727 1735
2. A. Drewniak, R.P. Gazendam, A.T. Tool, M. van Houdt, M.H. Jansen, J.L. van Hamme, and et al. Invasive fungal infection and impaired neutrophil killing in human CARD9 deficiency Blood 121 2013 2385 2392
3. F. Lanternier, S. Pathan, Q.B. Vincent, L. Liu, S. Cypowyj, C. Prando, and et al. Deep dermatophytosis and inherited CARD9 deficiency N Engl J Med 369 2013 1704 1714
4. X. Wang, W. Wang, Z. Lin, X. Wang, T. Li, J. Yu, and et al. CARD9 mutations linked to subcutaneous phaeohyphomycosis and TH17 cell deficiencies J Allergy Clin Immunol 133 2014 905 908.e3
5. F. Lanternier, E. Barbati, U. Meinzer, L. Liu, V. Pedergnana, M. Migaud, and et al. Inherited CARD9 deficiency in 2 unrelated patients with invasive Exophiala infection J Infect Dis 211 2015 1241 1250
6. C. Gavino, A. Cotter, D. Lichtenstein, D. Lejtenyi, C. Fortin, C. Legault, and et al. CARD9 deficiency and spontaneous central nervous system candidiasis: complete clinical remission with GM-CSF therapy Clin Infect Dis 59 2014 81 84
7. M. Herbst, R. Gazendam, D. Reimnitz, J. Sawalle-Belohradsky, A. Groll, P.G. Schlegel, and et al. Chronic Candida albicans meningitis in a 4-year-old girl with a homozygous mutation in the CARD9 gene (Q295X) Pediatr Infect Dis J 34 2015 999 1002
8. F. Lanternier, S.A. Mahdaviani, E. Barbati, H. Chaussade, Y. Koumar, R. Levy, and et al. Inherited CARD9 deficiency in otherwise healthy children and adults with Candida species-induced meningoencephalitis, colitis, or both J Allergy Clin Immunol 135 2015 1558 1568.e2
9. D.C. Vinh, B. Schwartz, A.P. Hsu, D.J. Miranda, P.A. Valdez, D. Fink, and et al. Interleukin-12 receptor beta1 deficiency predisposing to disseminated coccidioidomycosis Clin Infect Dis 52 2011 e99 e102
10. B.H. Segal, W. Han, J.J. Bushey, M. Joo, Z. Bhatti, J. Feminella, and et al. NADPH oxidase limits innate immune responses in the lungs in mice PLoS One 5 2010 e9631
11. E.D. Renner, S. Rylaarsdam, S. Anover-Sombke, A.L. Rack, J. Reichenbach, J.C. Carey, and 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 122 2008 181 187
12. A. Kozomara, and S. Griffiths-Jones miRBase: annotating high confidence microRNAs using deep sequencing data Nucleic Acids Res 42 Database issue 2014 D68 D73
13. N. Wong, and X. Wang miRDB: an online resource for microRNA target prediction and functional annotations Nucleic Acids Res 43 Database issue 2015 D146 D152
14. A.A. Morris, G.G. Kalz, and E.S. Lotspeich Ependymitis and meningitis due to Candida (Monilia) albicans Arch Neurol Psychiatry 54 1945 361 366
15. G. Belisle, W. Lachance, and G. Leblanc [Meningitis caused by Candida albicans. Report of a case and discussion] Union Med Can 97 1968 710 715
16. J.T. Black Cerebral candidiasis: case report of brain abscess secondary to Candida albicans, and review of literature J Neurol Neurosurg Psychiatry 33 1970 864 870
17. M. Germain, M. Gourdeau, and J. Hebert Case report: familial chronic mucocutaneous candidiasis complicated by deep candida infection Am J Med Sci 307 1994 282 283
18. N. Hamel, B.J. Feng, L. Foretova, D. Stoppa-Lyonnet, S.A. Narod, E. Imyanitov, and et al. On the origin and diffusion of BRCA1 c.5266dupC (5382insC) in European populations Eur J Hum Genet 19 2011 300 306
19. O. Gross, A. Gewies, K. Finger, M. Schäfer, T. Sparwasser, C. Peschel, and et al. Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity Nature 442 2006 651 656
20. S. Esnault, and J.S. Malter Extracellular signal-regulated kinase mediates granulocyte-macrophage colony-stimulating factor messenger RNA stabilization in tumor necrosis factor-alpha plus fibronectin-activated peripheral blood eosinophils Blood 99 2002 4048 4052
21. K.K. Meja, P.M. Seldon, Y. Nasuhara, K. Ito, P.J. Barnes, M.A. Lindsay, and et al. p38 MAP kinase and MKK-1 co-operate in the generation of GM-CSF from LPS-stimulated human monocytes by an NF-kappa B-independent mechanism Br J Pharmacol 131 2000 1143 1153
22. P.H. Anborgh, X. Qian, A.G. Papageorge, W.C. Vass, J.E. DeClue, and D.R. Lowy Ras-specific exchange factor GRF: oligomerization through its Dbl homology domain and calcium-dependent activation of Raf Mol Cell Biol 19 1999 4611 4622
23. X.M. Jia, B. Tang, L.L. Zhu, Y.H. Liu, X.Q. Zhao, S. Gorjestani, and et al. CARD9 mediates Dectin-1-induced ERK activation by linking Ras-GRF1 to H-Ras for antifungal immunity J Exp Med 211 2014 2307 2321
24. S.P. Smeekens, A. Ng, V. Kumar, M.D. Johnson, T.S. Plantinga, C. van Diemen, and et al. Functional genomics identifies type I interferon pathway as central for host defense against Candida albicans Nat Commun 4 2013 1342
25. D. Duffy, V. Rouilly, V. Libri, M. Hasan, B. Beitz, M. David, and et al. Functional analysis via standardized whole-blood stimulation systems defines the boundaries of a healthy immune response to complex stimuli Immunity 40 2014 436 450
26. A. Francisco-Cruz, M. Aguilar-Santelises, O. Ramos-Espinosa, D. Mata-Espinosa, B. Marquina-Castillo, J. Barrios-Payan, and et al. Granulocyte-macrophage colony-stimulating factor: not just another haematopoietic growth factor Med Oncol 31 2014 774
27. M.J. McGeachy GM-CSF: the secret weapon in the T(H)17 arsenal Nat Immunol 12 2011 521 522
28. F. Lanternier, S. Cypowyj, C. Picard, J. Bustamante, O. Lortholary, J.L. Casanova, and et al. Primary immunodeficiencies underlying fungal infections Curr Opin Pediatr 25 2013 736 747
29. H.S. Goodridge, T. Shimada, A.J. Wolf, Y.M. Hsu, C.A. Becker, X. Lin, and et al. Differential use of CARD9 by dectin-1 in macrophages and dendritic cells J Immunol 182 2009 1146 1154
30. J. Yang, L. Chai, C. Gao, T.C. Fowles, Z. Alipio, H. Dang, and et al. SALL4 is a key regulator of survival and apoptosis in human leukemic cells Blood 112 2008 805 813
31. C.R. Scriver Human genetics: lessons from Quebec populations Annu Rev Genomics Hum Genet 2 2001 69 101
32. A. Borha, J.J. Parienti, E. Emery, O. Coskun, S. Khouri, and J.M. Derlon [Candida albicans cerebral granuloma in an immunocompetent patient. A case report] Neurochirurgie 55 2009 57 62
33. C. Carra Dalliere, E. Thouvenot, G. Baptista, V. Le Moing, and M. Charif [Meningomyeloradiculitis in an immunocompetent patient] Rev Neurol (Paris) 166 2010 741 744
34. G. Hoarau, O. Kerdraon, M. Lagree, M. Vinchon, N. François, F. Dubos, and et al. Detection of (1,3)-beta-D-glucans in situ in a Candida albicans brain granuloma J Infect 67 2013 622 624
35. J.M. Torres, R. Martinez-Barricarte, S. García-Gómez, M.S. Mazariegos, Y. Itan, B. Boisson, and et al. Inherited BCL10 deficiency impairs hematopoietic and nonhematopoietic immunity J Clin Invest 124 2014 5239 5248
36. H.H. Jabara, T. Ohsumi, J. Chou, M.J. Massaad, H. Benson, A. Megarbane, and et al. A homozygous mucosa-associated lymphoid tissue 1 (MALT1) mutation in a family with combined immunodeficiency J Allergy Clin Immunol 132 2013 151 158
37. M.L. McKinnon, J. Rozmus, S.Y. Fung, A.F. Hirschfeld, K.L. Del Bel, L. Thomas, and et al. Combined immunodeficiency associated with homozygous MALT1 mutations J Allergy Clin Immunol 133 2014 1458 1462 e1-7
38. D. Punwani, H. Wang, A.Y. Chan, M.J. Cowan, J. Mallott, U. Sunderam, and et al. Combined immunodeficiency due to MALT1 mutations, treated by hematopoietic cell transplantation J Clin Immunol 35 2015 135 146
39. M.J. Ruping, J.J. Vehreschild, A. Groll, C. Lass-Flörl, H. Ostermann, M. Ruhnke, and et al. Current issues in the clinical management of invasive aspergillosis - the AGIHO, DMykG, OGMM and PEG web-based survey and expert consensus conference 2009 Mycoses 54 2011 e557 e568
40. P. Liang, X. Wang, R. Wang, Z. Wan, W. Han, and R. Li CARD9 deficiencies linked to impaired neutrophil functions against Phialophora verrucosa Mycopathologia 179 2015 347 357
41. A.S. Grumach, F. de Queiroz-Telles, M. Migaud, F. Lanternier, N.R. Filho, S.M. Palma, and et al. A homozygous CARD9 mutation in a Brazilian patient with deep dermatophytosis J Clin Immunol 35 2015 486 490
42. C. Guerrero, J.M. Rojas, M. Chedid, L.M. Esteban, D.B. Zimonjic, N.C. Popescu, and et al. Expression of alternative forms of Ras exchange factors GRF and SOS1 in different human tissues and cell lines Oncogene 12 1996 1097 1107