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CARD9Predisposition to Invasive Fungal Disease due to CARD9 Deficiency

CARD9 encodes an intracellular adaptor protein critical for antifungal immunity via C-type lectin receptor signaling. Autosomal recessive loss-of-function variants in CARD9 abrogate NF-κB and MAPK activation downstream of dectin-1, impairing GM-CSF and proinflammatory cytokine responses in monocytes and neutrophils. First described in a consanguineous kindred with chronic mucocutaneous candidiasis and fatal central nervous system infection, CARD9 deficiency has since been reported in diverse ethnicities and across multiple fungal pathogens (PMID:19864672).

Genetic evidence includes over 35 affected individuals from more than 15 unrelated families harboring biallelic nonsense, frameshift, and splice-site CARD9 variants. Segregation analyses in a five-generation pedigree revealed four additional affected relatives with the recurrent p.Gln295Ter variant segregating in trans with private alleles (PMID:19864672; PMID:29307770). Compound heterozygous LoF alleles, such as c.865C>T (p.Gln289Ter) and c.23_29del (p.Asp8AlafsTer10), were identified in a Colombian child with phaeohyphomycosis, with absent CARD9 protein expression in PBMCs (PMID:30264381).

The variant spectrum comprises recurrent nonsense mutations (e.g., c.883C>T (p.Gln295Ter)), frameshift indels, and splice-site changes (e.g., c.184G>A (p.Gly62Ser), c.288C>T (p.Gly96=)), as well as hypomorphic missense alleles (c.271T>C (p.Tyr91His)) enriched via founder effects in French-Canadians. A heterozygous dominant-negative splice variant, c.1434+1G>C, generates truncated transcripts reducing BCL10/MALT1 recruitment and conferring variable penetrance of hypogammaglobulinemia and candidal esophagitis (PMID:34791587).

Functional studies demonstrate that CARD9 deficiency disrupts dectin-1–CARD9–BCL10–MALT1 signalosome assembly, leading to abrogated NF-κB p65 activation and impaired ERK-mediated GM-CSF production in monocytes. Knockout and knock-in murine models recapitulate invasive fungal phenotypes and confirm rescue by exogenous GM-CSF. Structural analyses of CARD9 variants (e.g., R70W) further elucidate filament formation defects underlying loss of function (PMID:26488816; PMID:30429846).

Clinically, CARD9-deficient patients present with spontaneous central nervous system candidiasis, deep dermatophytosis, phaeohyphomycosis (e.g., Corynespora cassiicola), invasive Saprochaete capitata, Exophiala dermatitidis infections, and allergic bronchopulmonary aspergillosis–like syndromes. Common manifestations include headache (HP:0002315), vomiting (HP:0002013), osteomyelitis (HP:0002754), and recurrent fever (HP:0001954).

Key Take-home

CARD9 deficiency is a definitive autosomal recessive immunodeficiency with broad susceptibility to invasive fungal disease, diagnosable via genetic testing for biallelic LoF variants and confirmed by functional assays; early recognition enables targeted immunomodulation and antifungal prophylaxis.

References

  • The New England Journal of Medicine • 2009 • A homozygous CARD9 mutation in a family with susceptibility to fungal infections. PMID:19864672
  • Clinical Immunology (Orlando, Fla.) • 2018 • A young girl with severe cerebral fungal infection due to CARD9 deficiency. PMID:29307770
  • Journal of Clinical Immunology • 2018 • Early-Onset Invasive Infection Due to Corynespora cassiicola Associated with Compound Heterozygous CARD9 Mutations in a Colombian Patient. PMID:30264381
  • Mycoses • 2018 • Novel bi-allelic splice mutations in CARD9 causing adult-onset Candida endophthalmitis. PMID:28984994
  • The Journal of Allergy and Clinical Immunology • 2016 • Impaired RASGRF1/ERK-mediated GM-CSF response characterizes CARD9 deficiency in French-Canadians. PMID:26521038
  • Immunity • 2015 • Ubiquitin Ligase TRIM62 Regulates CARD9-Mediated Anti-fungal Immunity and Intestinal Inflammation. PMID:26488816
  • Frontiers in Immunology • 2018 • A CARD9 Founder Mutation Disrupts NF-κB Signaling by Inhibiting BCL10 and MALT1 Recruitment and Signalosome Formation. PMID:30429846

Evidence Based Scoring (AI generated)

Gene–Disease Association

Definitive

Over 35 affected individuals from >15 unrelated families; extensive segregation and functional concordance

Genetic Evidence

Strong

Biallelic loss-of-function CARD9 variants in over 30 probands with familial segregation and reaching the genetic cap

Functional Evidence

Strong

Multiple in vitro and in vivo studies demonstrating impaired NF-κB/GM-CSF signaling and rescue in murine models