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SMARCB1 – Schwannomatosis

SMARCB1 encodes the INI1/BAF47 core subunit of the SWI/SNF chromatin-remodeling complex. Heterozygous germline variants in SMARCB1 predispose to an autosomal dominant tumor syndrome characterized by multiple non-vestibular schwannomas, clinically defined as schwannomatosis, with incomplete penetrance and variable expressivity (PMID:17357086). Patients typically present in adulthood with painful or asymptomatic nerve sheath tumors without vestibular nerve involvement.

Genetic studies of familial schwannomatosis cohorts have identified SMARCB1 germline variants in approximately 45% of familial probands and 9% of sporadic cases, encompassing missense, splice-site, and truncating alleles distributed across the gene (PMID:24933152). Hotspots include the 5′ untranslated region variant c.*82C>T and the exon 1 missense change c.41C>A (p.Pro14His). The recurrent exon 1 variant c.92A>T (p.Glu31Val) segregates with multiple schwannomas and meningiomas in a kindred, confirmed by absence of mutant allele mRNA and loss of INI1 expression in tumors (PMID:19582488).

Segregation analysis and tumor studies support a four-hit model involving SMARCB1 and NF2. In a series of 19 families, eight distinct germline splice or missense SMARCB1 variants segregated with disease in 13 affected relatives, and associated tumors exhibited somatic LOH or second-hit NF2 mutations (PMID:18647326; PMID:22949514). Mosaic retention of INI1 protein in schwannomas suggests hypomorphic or alternatively spliced transcripts contribute to schwannoma development.

Functional assays demonstrate that truncating SMARCB1 variants unmask a nuclear export signal, leading to CRM1-dependent cytoplasmic mislocalization and loss of tumor suppressor activity; nuclear retention by mutation of the NES or inhibition of exportin-1 restores cell cycle arrest and senescence in SMARCB1-deficient cells (PMID:11782423; PMID:12548550). RNA-based studies confirm aberrant splicing for deep-intronic and splice-site variants, with consequent nonsense-mediated decay or altered isoform expression (PMID:22752724; PMID:24740647).

A small number of studies failed to identify SMARCB1 variants in patients with multiple meningiomas unrelated to NF2, indicating that SMARCB1 is not a major predisposition gene in that context (PMID:20472658). No conflicting evidence disputes the SMARCB1–schwannomatosis association, which remains well supported by genetic, segregation, and functional data.

Together, the evidence places the SMARCB1–schwannomatosis association in the Strong category: germline variants segregate in autosomal dominant families, tumors demonstrate second-hit SMARCB1 and NF2 alterations, and functional studies concordantly show loss of nuclear tumor suppressor function. Additional rare phenotypes (e.g., meningiomas, leiomyosarcoma) expand the clinical spectrum beyond the scoring scope. Key take-home: germline SMARCB1 testing is essential for accurate diagnosis, risk assessment, and surveillance in schwannomatosis.

References

  • American Journal of Human Genetics • 2007 • Germline mutation of INI1/SMARCB1 in familial schwannomatosis PMID:17357086
  • Clinical Genetics • 2008 • Alterations in the SMARCB1 (INI1) tumor suppressor gene in familial schwannomatosis PMID:18647326
  • Cancer Genetics • 2014 • SMARCB1 mutations in schwannomatosis and genotype correlations with rhabdoid tumors PMID:24933152
  • Neurogenetics • 2010 • Schwannomatosis associated with multiple meningiomas due to a familial SMARCB1 mutation PMID:19582488
  • Human Molecular Genetics • 2012 • Expression of SMARCB1 (INI1) mutations in familial schwannomatosis PMID:22949514
  • Acta Neuropathologica • 2014 • Premature termination of SMARCB1 translation may be followed by reinitiation in schwannomatosis-associated schwannomas PMID:24740647
  • The EMBO Journal • 2002 • A masked NES in INI1/hSNF5 mediates hCRM1-dependent nuclear export PMID:11782423
  • Journal of Cellular Physiology • 2003 • INI1 expression induces cell cycle arrest and markers of senescence in malignant rhabdoid tumor cells PMID:12548550
  • Neurogenetics • 2012 • RNA-based analysis of two SMARCB1 mutations associated with familial schwannomatosis with meningiomas PMID:22752724
  • Journal of Medical Genetics • 2010 • SMARCB1 mutations are not a common cause of multiple meningiomas PMID:20472658

Evidence Based Scoring (AI generated)

Gene–Disease Association

Strong

Multiple independent families (n=8) with germline SMARCB1 variants and 13 segregating relatives; concordant LOH and somatic NF2 second hits

Genetic Evidence

Strong

SMARCB1 germline variants in ~45% of familial and ~9% of sporadic schwannomatosis probands, including missense, splice, and truncating changes

Functional Evidence

Moderate

Truncating variants unmask a CRM1-dependent NES abrogating nuclear tumor suppressor function; rescue by export inhibition and reexpression induces senescence