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Annual Review of Genomics and Human Genetics

Volume 24, 2023

The SWI/SNF Complex in Neural Crest Cell Development and Disease

Abstract

While the neural crest cell population gives rise to an extraordinary array of derivatives, including elements of the craniofacial skeleton, skin pigmentation, and peripheral nervous system, it is today increasingly recognized that Schwann cell precursors are also multipotent. Two mammalian paralogs of the SWI/SNF (tch/ucrose onermentable) chromatin-remodeling complexes, BAF (Brg1-associated factors) and PBAF (polybromo-associated BAF), are critical for neural crest specification during normal mammalian development. There is increasing evidence that pathogenic variants in components of the BAF and PBAF complexes play central roles in the pathogenesis of neural crest–derived tumors. Transgenic mouse models demonstrate a temporal window early in development where pathogenic variants in result in the formation of aggressive, poorly differentiated tumors, such as rhabdoid tumors. By contrast, later in development, homozygous inactivation of requires additional pathogenic variants in tumor suppressor genes to drive the development of differentiated adult neoplasms derived from the neural crest, which have a comparatively good prognosis in humans.

Keyword(s): NF2, rhabdoid, Schwann cell precursors, schwannoma, Smarcb1, SWI/SNF
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2023-08-25
2024-04-29
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Literature Cited

  1. 1.
    Adameyko I, Lallemend F, Aquino JB, Pereira JA, Topilko P et al. 2009. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139:366–79
     [Google Scholar]
  2. 2.
    Akhmametyeva EM, Mihaylova MM, Luo H, Kharzai S, Welling DB, Chang L-S. 2006. Regulation of the Neurofibromatosis 2 gene promoter expression during embryonic development. Dev. Dyn. 235:2771–85
     [Google Scholar]
  3. 3.
    Alaidarous A, Parfait B, Ferkal S, Cohen J, Wolkenstein P, Mazereeuw-Hautier J. 2019. Segmental schwannomatosis: characteristics in 12 patients. Orphanet J. Rare Dis. 14:207
     [Google Scholar]
  4. 4.
    Asthagiri AR, Parry DM, Butman JA, Kim HJ, Tsilou ET et al. 2009. Neurofibromatosis type 2. Lancet 373:1974–86
     [Google Scholar]
  5. 5.
    Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y et al. 2010. CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463:958–62
     [Google Scholar]
  6. 6.
    Baser ME, Kuramoto L, Woods R, Joe H, Friedman JM et al. 2005. The location of constitutional neurofibromatosis 2 (NF2) splice site mutations is associated with the severity of NF2. J. Med. Genet. 42:540–46
     [Google Scholar]
  7. 7.
    Behling F, Fodi C, Skardelly M, Paulsen F, Tabatabai G et al. 2022. The prognostic role of the immunohistochemical expression of S100 in meningiomas. J. Cancer Res. Clin. Oncol. https://doi.org/10.1007/s00432-022-04186-9
    [Crossref] [Google Scholar]
  8. 8.
    Betancur P, Bronner-Fraser M, Sauka-Spengler T. 2010. Assembling neural crest regulatory circuits into a gene regulatory network. Annu. Rev. Cell Dev. Biol. 26:581–603
     [Google Scholar]
  9. 9.
    Biegel JA. 2006. Molecular genetics of atypical teratoid/rhabdoid tumor. Neurosurg. Focus 20:E11
     [Google Scholar]
  10. 10.
    Bi-Lin KW, Seshachalam PV, Tuoc T, Stoykova A, Ghosh S, Singh MK. 2021. Critical role of the BAF chromatin remodeling complex during murine neural crest development. PLOS Genet. 17:e1009446
     [Google Scholar]
  11. 11.
    Boetto J, Apra C, Bielle F, Peyre M, Kalamarides M. 2018. Selective vulnerability of the primitive meningeal layer to prenatal Smo activation for skull base meningothelial meningioma formation. Oncogene 37:4955–63
     [Google Scholar]
  12. 12.
    Boetto J, Peyre M, Kalamarides M. 2021. Meningiomas from a developmental perspective: exploring the crossroads between meningeal embryology and tumorigenesis. Acta Neurochir. 163:57–66
     [Google Scholar]
  13. 13.
    Bolande RP. 1974. The neurocristopathies: a unifying concept of disease arising in neural crest maldevelopment. Hum. Pathol. 5:409–29
     [Google Scholar]
  14. 14.
    Bracken AP, Brien GL, Verrijzer CP. 2019. Dangerous liaisons: interplay between SWI/SNF, NuRD, and Polycomb in chromatin regulation and cancer. Genes Dev. 33:936
     [Google Scholar]
  15. 15.
    Bronner ME, LeDouarin NM. 2012. Development and evolution of the neural crest: an overview. Dev. Biol. 366:2–9
     [Google Scholar]
  16. 16.
    Bronner ME, Simões-Costa M. 2016. The neural crest migrating into the twenty-first century. Current Topics in Developmental Biology, Vol. 116 PM Wassarman 115–34. San Diego, CA: Academic
     [Google Scholar]
  17. 17.
    Bultman S, Gebuhr T, Yee D, la Mantia C, Nicholson J et al. 2000. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6:1287–95
     [Google Scholar]
  18. 18.
    Burnside RD. 2015. 22q11.21 Deletion syndromes: a review of proximal, central, and distal deletions and their associated features. Cytogenet. Genome Res. 146:89–99
     [Google Scholar]
  19. 19.
    Buscariollo DL, Park HS, Roberts KB, Yu JB. 2012. Survival outcomes in atypical teratoid rhabdoid tumor for patients undergoing radiotherapy in a Surveillance, Epidemiology, and End Results analysis. Cancer 118:4212–19
     [Google Scholar]
  20. 20.
    Caltabiano R, Magro G, Polizzi A, Praticó AD, Ortensi A et al. 2017. A mosaic pattern of INI1/SMARCB1 protein expression distinguishes schwannomatosis and NF2-associated peripheral schwannomas from solitary peripheral schwannomas and NF2-associated vestibular schwannomas. Child's Nervous Syst. 33:933–40
     [Google Scholar]
  21. 21.
    Carter JM, O'Hara C, Dundas G, Gilchrist D, Collins MS et al. 2012. Epithelioid malignant peripheral nerve sheath tumor arising in a schwannoma, in a patient with “neuroblastoma-like” schwannomatosis and a novel germline SMARCB1 mutation. Am. J. Surg. Pathol. 36:154–60
     [Google Scholar]
  22. 22.
    Cenik BK, Shilatifard A. 2021. COMPASS and SWI/SNF complexes in development and disease. Nat. Rev. Genet. 22:38–58
     [Google Scholar]
  23. 23.
    Christiaans I, Kenter SB, Brink HC, van Os TAM, Baas F et al. 2011. Germline SMARCB1 mutation and somatic NF2 mutations in familial multiple meningiomas. J. Med. Genet. 48:93–97
     [Google Scholar]
  24. 24.
    Chun HJE, Johann PD, Milne K, Zapatka M, Buellesbach A et al. 2019. Identification and analyses of extra-cranial and cranial rhabdoid tumor molecular subgroups reveal tumors with cytotoxic T cell infiltration. Cell Rep. 29:2338–54.e7
     [Google Scholar]
  25. 25.
    Chun HJE, Lim EL, Heravi-Moussavi A, Saberi S, Mungall KL et al. 2016. Genome-wide profiles of extra-cranial malignant rhabdoid tumors reveal heterogeneity and dysregulated developmental pathways. Cancer Cell 29:394–406
     [Google Scholar]
  26. 26.
    Collord G, Tarpey P, Kurbatova N, Martincorena I, Moran S et al. 2018. An integrated genomic analysis of anaplastic meningioma identifies prognostic molecular signatures. Sci. Rep. 8:13537
     [Google Scholar]
  27. 27.
    Custers L, Khabirova E, Coorens THH, Oliver TRW, Calandrini C et al. 2021. Somatic mutations and single-cell transcriptomes reveal the root of malignant rhabdoid tumours. Nat. Commun. 12:1407
     [Google Scholar]
  28. 28.
    Dasgupta K, Jeong J. 2019. Developmental biology of the meninges. Genesis 57:e23288
     [Google Scholar]
  29. 29.
    del Savio E, Maestro R. 2022. Beyond SMARCB1 loss: recent insights into the pathobiology of epithelioid sarcoma. Cells 11:2626
     [Google Scholar]
  30. 30.
    Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T et al. 1992. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 359:162–65
     [Google Scholar]
  31. 31.
    Dyachuk V, Furlan A, Shahidi MK, Giovenco M, Kaukua N et al. 2014. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors. Science 345:82–87
     [Google Scholar]
  32. 32.
    Eaton KW, Tooke LS, Wainwright LM, Judkins AR, Biegel JA. 2011. Spectrum of SMARCB1/INI1 mutations in familial and sporadic rhabdoid tumors. Pediatr. Blood Cancer 56:7–15
     [Google Scholar]
  33. 33.
    Eroglu B, Wang G, Tu N, Sun X, Mivechi NF. 2006. Critical role of Brg1 member of the SWI/SNF chromatin remodeling complex during neurogenesis and neural crest induction in zebrafish. Dev. Dyn. 235:2722–35
     [Google Scholar]
  34. 34.
    Espinosa-Medina I, Outin E, Picard CA, Chettouh Z, Dymecki S et al. 2014. Parasympathetic ganglia derive from Schwann cell precursors. Science 345:87–90
     [Google Scholar]
  35. 35.
    Evans DG, Hartley CL, Smith PT, King AT, Bowers NL et al. 2020. Incidence of mosaicism in 1055 de novo NF2 cases: much higher than previous estimates with high utility of next-generation sequencing. Genet. Med. 22:53–59
     [Google Scholar]
  36. 36.
    Evans DG, Messiaen LM, Foulkes WD, Irving REA, Murray AJ et al. 2021. Typical 22q11.2 deletion syndrome appears to confer a reduced risk of schwannoma. Genet. Med. 23:1779–82
     [Google Scholar]
  37. 37.
    Evans DGR, Huson SM, Birch JM. 2012. Malignant peripheral nerve sheath tumours in inherited disease. Clin. Sarcoma Res. 2:17
     [Google Scholar]
  38. 38.
    Evans DGR, Huson SM, Donnai D, Neary W, Blair V et al. 1992. A clinical study of type 2 neurofibromatosis. Q. J. Med. 84:603–18
     [Google Scholar]
  39. 39.
    Evans DGR, Sainio M, Baser ME. 2000. Neurofibromatosis type 2. J. Med. Genet. 37:897–904
     [Google Scholar]
  40. 40.
    Foulkes WD, Kamihara J, Evans DGR, Brugières L, Bourdeaut F et al. 2017. Cancer surveillance in Gorlin syndrome and rhabdoid tumor predisposition syndrome. Clin. Cancer Res. 23:e62–67
     [Google Scholar]
  41. 41.
    Fountain DM, Smith MJ, O'Leary C, Pathmanaban ON, Roncaroli F et al. 2021. The spatial phenotype of genotypically distinct meningiomas demonstrate potential implications of the embryology of the meninges. Oncogene 40:875–84
     [Google Scholar]
  42. 42.
    Furlan A, Adameyko I. 2018. Schwann cell precursor: a neural crest cell in disguise?. Dev. Biol. 444:S25–35
     [Google Scholar]
  43. 43.
    Furlan A, Dyachuk V, Kastriti ME, Calvo-Enrique L, Abdo H et al. 2017. Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla. Science 357:eaal3753
     [Google Scholar]
  44. 44.
    Gill CM, Loewenstern J, Rutland JW, Arib H, Pain M et al. 2021. SWI/SNF chromatin remodeling complex alterations in meningioma. J. Cancer Res. Clin. Oncol. 147:3431–40
     [Google Scholar]
  45. 45.
    Giovannini M, Robanus-Maandag E, Niwa-Kawakita M, van der Valk M, Woodruff JM et al. 1999. Schwann cell hyperplasia and tumors in transgenic mice expressing a naturally occurring mutant NF2 protein. Genes Dev. 13:978–86
     [Google Scholar]
  46. 46.
    Giovannini M, Robanus-Maandag E, van der Valk M, Niwa-Kawakita M, Abramowski V et al. 2000. Conditional biallelic Nf2 mutation in the mouse promotes manifestations of human neurofibromatosis type 2. Genes Dev. 14:1617–30
     [Google Scholar]
  47. 47.
    Graf M, Interlandi M, Moreno N, Holdhof D, Göbel C et al. 2022. Single-cell transcriptomics identifies potential cells of origin of MYC rhabdoid tumors. Nat. Commun. 13:1544
     [Google Scholar]
  48. 48.
    Grünewald TGP, Cidre-Aranaz F, Surdez D, Tomazou EM, de Álava E et al. 2018. Ewing sarcoma. Nat. Rev. Disease Primers 4:5
     [Google Scholar]
  49. 49.
    Guidi CJ, Sands AT, Zambrowicz BP, Turner TK, Demers DA et al. 2001. Disruption of Ini1 leads to peri-implantation lethality and tumorigenesis in mice. Mol. Cell Biol. 21:3598–603
     [Google Scholar]
  50. 50.
    Halliday D, Emmanouil B, Pretorius P, MacKeith S, Painter S et al. 2017. Genetic Severity Score predicts clinical phenotype in NF2. J. Med. Genet. 54:657–64
     [Google Scholar]
  51. 51.
    Han ZY, Richer W, Fréneaux P, Chauvin C, Lucchesi C et al. 2016. The occurrence of intracranial rhabdoid tumours in mice depends on temporal control of Smarcb1 inactivation. Nat. Commun. 7:10421
     [Google Scholar]
  52. 52.
    Hannan CJ, Lewis D, O'Leary C, Donofrio CA, Evans DG et al. 2020. The inflammatory microenvironment in vestibular schwannoma. Neuro-Oncol. Adv. 2:vdaa023
     [Google Scholar]
  53. 53.
    Hargreaves DC, Crabtree GR. 2011. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21:396–420
     [Google Scholar]
  54. 54.
    Hasselblatt M, Nagel I, Oyen F, Bartelheim K, Russell RB et al. 2014. SMARCA4-mutated atypical teratoid/rhabdoid tumors are associated with inherited germline alterations and poor prognosis. Acta Neuropathol. 128:453–56
     [Google Scholar]
  55. 55.
    Hasselblatt M, Oyen F, Gesk S, Kordes U, Wrede B et al. 2009. Cribriform neuroepithelial tumor (CRINET): a nonrhabdoid ventricular tumor with INI1 loss and relatively favorable prognosis. J. Neuropathol. Exp. Neurol. 68:1249–55
     [Google Scholar]
  56. 56.
    Heatley N, Kolson Kokohaare E, Strauss DC, Hallin M, Jones RL et al. 2020. Epithelioid malignant peripheral nerve sheath tumor arising in schwannoma. Rare Tumors 12:2036361320950862
     [Google Scholar]
  57. 57.
    Hexter A, Jones A, Joe H, Heap L, Smith MJ et al. 2015. Clinical and molecular predictors of mortality in neurofibromatosis 2: a UK national analysis of 1192 patients. J. Med. Genet. 52:699–705
     [Google Scholar]
  58. 58.
    Ho B, Johann PD, Grabovska Y, De Dieu Andrianteranagna MJ, Yao F et al. 2020. Molecular subgrouping of atypical teratoid/rhabdoid tumors—a reinvestigation and current consensus. Neuro-Oncology 22:613–24
     [Google Scholar]
  59. 59.
    Holdhof D, Johann PD, Spohn M, Bockmayr M, Safaei S et al. 2021. Atypical teratoid/rhabdoid tumors (ATRTs) with SMARCA4 mutation are molecularly distinct from SMARCB1-deficient cases. Acta Neuropathol. 141:291–301
     [Google Scholar]
  60. 60.
    Holsten T, Bens S, Oyen F, Nemes K, Hasselblatt M et al. 2018. Germline variants in SMARCB1 and other members of the BAF chromatin-remodeling complex across human disease entities: a meta-analysis. Eur. J. Hum. Genet. 26:1083–93
     [Google Scholar]
  61. 61.
    Hutter S, Piro RM, Reuss DE, Hovestadt V, Sahm F et al. 2014. Whole exome sequencing reveals that the majority of schwannomatosis cases remain unexplained after excluding SMARCB1 and LZTR1 germline variants. Acta Neuropathol. 128:449–52
     [Google Scholar]
  62. 62.
    Ibrahim GM, Huang A, Halliday W, Dirks PB, Malkin D et al. 2011. Cribriform neuroepithelial tumour: novel clinicopathological, ultrastructural and cytogenetic findings. Acta Neuropathol. 122:511–14
     [Google Scholar]
  63. 63.
    Jessen KR, Mirsky R. 2005. The origin and development of glial cells in peripheral nerves. Nat. Rev. Neurosci. 6:671–82
     [Google Scholar]
  64. 64.
    Jessen KR, Mirsky R. 2019. Schwann cell precursors; multipotent glial cells in embryonic nerves. Front. Mol. Neurosci. 12:69
     [Google Scholar]
  65. 65.
    Johann PD, Erkek S, Zapatka M, Kerl K, Buchhalter I et al. 2016. Atypical teratoid/rhabdoid tumors are comprised of three epigenetic subgroups with distinct enhancer landscapes. Cancer Cell 29:379–93
     [Google Scholar]
  66. 66.
    Johann PD, Hovestadt V, Thomas C, Jeibmann A, Heß K et al. 2017. Cribriform neuroepithelial tumor: molecular characterization of a SMARCB1-deficient non-rhabdoid tumor with favorable long-term outcome. Brain Pathol. 27:411–18
     [Google Scholar]
  67. 67.
    Joseph NM, Mukouyama YS, Mosher JT, Jaegle M, Crone SA et al. 2004. Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneurial fibroblasts in addition to Schwann cells. Development 131:5599–612
     [Google Scholar]
  68. 68.
    Kadoch C, Crabtree GR. 2013. Reversible disruption of mSWI/SNF (BAF) complexes by the SS18-SSX oncogenic fusion in synovial sarcoma. Cell 153:71–85
     [Google Scholar]
  69. 69.
    Kadoch C, Williams RT, Calarco JP, Miller EL, Weber CM et al. 2016. Dynamics of BAF-Polycomb complex opposition on heterochromatin in normal and oncogenic states. Nat. Genet. 49:213–22
     [Google Scholar]
  70. 70.
    Kalamarides M, Niwa-Kawakita M, Leblois H, Abramowski V, Perricaudet M et al. 2002. Nf2 gene inactivation in arachnoidal cells is rate-limiting for meningioma development in the mouse. Genes Dev. 16:1060–65
     [Google Scholar]
  71. 71.
    Kalamarides M, Stemmer-Rachamimov AO, Niwa-Kawakita M, Chareyre F, Taranchon E et al. 2011. Identification of a progenitor cell of origin capable of generating diverse meningioma histological subtypes. Oncogene 30:2333–44
     [Google Scholar]
  72. 72.
    Kastriti ME, Faure L, von Ahsen D, Bouderlique TG, Boström J et al. 2022. Schwann cell precursors represent a neural crest-like state with biased multipotency. EMBO J. 41:e108780
     [Google Scholar]
  73. 73.
    Kaukua N, Shahidi MK, Konstantinidou C, Dyachuk V, Kaucka M et al. 2014. Glial origin of mesenchymal stem cells in a tooth model system. Nature 513:551–54
     [Google Scholar]
  74. 74.
    Khavari PA, Peterson CL, Tamkun JW, Mendel DB, Crabtree GR. 1993. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366:170–74
     [Google Scholar]
  75. 75.
    Klochendler-Yeivin A, Fiette L, Barra J, Muchardt C, Babinet C, Yaniv M. 2000. The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. EMBO Rep. 1:500–6
     [Google Scholar]
  76. 76.
    le Loarer F, Zhang L, Fletcher CD, Ribeiro A, Singer S et al. 2014. Consistent SMARCB1 homozygous deletions in epithelioid sarcoma and in a subset of myoepithelial carcinomas can be reliably detected by FISH in archival material. Genes Chromosomes Cancer 53:475
     [Google Scholar]
  77. 77.
    Li W, Xiong Y, Shang C, Twu KY, Hang CT et al. 2013. Brg1 governs distinct pathways to direct multiple aspects of mammalian neural crest cell development. PNAS 110:1738–43
     [Google Scholar]
  78. 78.
    Ling ITC, Sauka-Spengler T. 2019. Early chromatin shaping predetermines multipotent vagal neural crest into neural, neuronal and mesenchymal lineages. Nat. Cell Biol. 21:1504–17
     [Google Scholar]
  79. 79.
    Lousado L, Prazeres PHDM, Andreotti JP, Paiva AE, Azevedo PO et al. 2017. Schwann cell precursors as a source for adrenal gland chromaffin cells. Cell Death Disease 8:e3072
     [Google Scholar]
  80. 80.
    Makoto I, Lee SMK, Johnson JE, McMahon AP, Takada S. 1997. Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389:966–70
     [Google Scholar]
  81. 81.
    Mashtalir N, Suzuki H, Farrell DP, Sankar A, Luo J et al. 2020. A structural model of the endogenous human BAF complex informs disease mechanisms. Cell 183:802–17.e24
     [Google Scholar]
  82. 82.
    McBride MJ, Pulice JL, Beird HC, Ingram DR, D'Avino AR et al. 2018. The SS18-SSX fusion oncoprotein hijacks BAF complex targeting and function to drive synovial sarcoma. Cancer Cell 33:1128–41.e7
     [Google Scholar]
  83. 83.
    McClatchey AI, Saotome I, Mercer K, Crowley D, Gusella JF et al. 1998. Mice heterozygous for a mutation at the Nf2 tumor suppressor locus develop a range of highly metastatic tumors. Genes Dev. 12:1121–33
     [Google Scholar]
  84. 84.
    McClatchey AI, Saotome I, Ramesh V, Gusella JF, Jacks T 1997. The Nf2 tumor suppressor gene product is essential for extraembryonic development immediately prior to gastrulation. Genes Dev. 11:1253–65
     [Google Scholar]
  85. 85.
    McDonald-McGinn DM, Sullivan KE, Marino B, Philip N, Swillen A et al. 2015. 22q11.2 deletion syndrome. Nat. Rev. Dis. Primers 1:15071
     [Google Scholar]
  86. 86.
    Meulemans D, Bronner-Fraser M. 2004. Gene-regulatory interactions in neural crest evolution and development. Dev. Cell 7:291–99
     [Google Scholar]
  87. 87.
    Michel BC, D'Avino AR, Cassel SH, Mashtalir N, McKenzie ZM et al. 2018. A non-canonical SWI/SNF complex is a synthetic lethal target in cancers driven by BAF complex perturbation. Nat. Cell Biol. 20:1410–20
     [Google Scholar]
  88. 88.
    Möller E, Praz V, Rajendran S, Dong R, Cauderay A et al. 2022. EWSR1-ATF1 dependent 3D connectivity regulates oncogenic and differentiation programs in Clear Cell Sarcoma. Nat. Commun. 13:2267
     [Google Scholar]
  89. 89.
    Morgan KM, Siow VS, Strotmeyer S, Gow KW, Malek MM. 2022. Characteristics and outcomes in pediatric non-central nervous system malignant rhabdoid tumors: a report from the National Cancer Database. Ann. Surg. Oncol. 29:671–78
     [Google Scholar]
  90. 90.
    Murisier F, Guichard S, Beermann F. 2007. The tyrosinase enhancer is activated by Sox10 and Mitf in mouse melanocytes. Pigment Cell Res. 20:173–84
     [Google Scholar]
  91. 91.
    Nehila T, Ferguson JW, Atit RP. 2020. Polycomb Repressive Complex 2: a dimmer switch of gene regulation in calvarial bone development. Curr. Osteoporos. Rep. 18:378–87
     [Google Scholar]
  92. 92.
    Neiswender H, Navarre S, Kozlowski DJ, LeMosy EK. 2017. Early craniofacial defects in zebrafish that have reduced function of a Wnt-interacting extracellular matrix protein, Tinagl1. Cleft Palate-Craniofac. J. 54:381–90
     [Google Scholar]
  93. 93.
    Ng JMY, Martinez D, Marsh ED, Zhang Z, Rappaport E et al. 2015. Generation of a mouse model of atypical teratoid/rhabdoid tumor of the central nervous system through combined deletion of Snf5 and p53. Cancer Res. 75:4629–39
     [Google Scholar]
  94. 94.
    Ostrom QT, Patil N, Cioffi G, Waite K, Kruchko C, Barnholtz-Sloan JS. 2020. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the united states in 2013–2017. Neuro-Oncology 22:Suppl. 1iv1–96. Correction 2022. Neuro-Oncology 24:1214
     [Google Scholar]
  95. 95.
    Pagliaroli L, Porazzi P, Curtis AT, Scopa C, Mikkers HMM et al. 2021. Inability to switch from ARID1A-BAF to ARID1B-BAF impairs exit from pluripotency and commitment towards neural crest formation in ARID1B-related neurodevelopmental disorders. Nat. Commun. 12:6469
     [Google Scholar]
  96. 96.
    Piotrowski A, Xie J, Liu YF, Poplawski AB, Gomes AR et al. 2013. Germline loss-of-function mutations in LZTR1 predispose to an inherited disorder of multiple schwannomas. Nat. Genet. 46:182–87
     [Google Scholar]
  97. 97.
    Plotkin SR, Messiaen L, Legius E, Pancza P, Avery RA et al. 2022. Updated diagnostic criteria and nomenclature for neurofibromatosis type 2 and schwannomatosis: an international consensus recommendation. Genet. Med. 24:1967–77
     [Google Scholar]
  98. 98.
    Ramadhan DA, Gautami W, Rahmartani LD, Rafli A, Gunawan K et al. 2022. ATRT-21. Contribution of germline mosaic alterations of SMARCB1 in rhabdoid tumor predisposition syndrome. Neuro-Oncology 24:Suppl. 1i7–8
     [Google Scholar]
  99. 99.
    Randazzo FM, Khavari P, Crabtree G, Tamkun J, Rossant J. 1994. brg1: a putative murine homologue of the Drosophila brahma gene, a homeotic gene regulator. Dev. Biol. 161:229–42
     [Google Scholar]
  100. 100.
    Roberts CWM, Galusha SA, McMenamin ME, Fletcher CDM, Orkin SH. 2000. Haploinsufficiency of Snf5 (integrase interactor 1) predisposes to malignant rhabdoid tumors in mice. PNAS 97:13796–800
     [Google Scholar]
  101. 101.
    Roberts CWM, Leroux MM, Fleming MD, Orkin SH. 2002. Highly penetrant, rapid tumorigenesis through conditional inversion of the tumor suppressor gene Snf5. Cancer Cell 2:415–25
     [Google Scholar]
  102. 102.
    Rouleau GA, Merel P, Lutchman M, Sanson M, Zucman J et al. 1993. Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature 363:515–21
     [Google Scholar]
  103. 103.
    Rousseau G, Noguchi T, Bourdon V, Sobol H, Olschwang S. 2011. SMARCB1/INI1 germline mutations contribute to 10% of sporadic schwannomatosis. BMC Neurol. 11:9
     [Google Scholar]
  104. 104.
    Sánchez-Molina S, Figuerola-Bou E, Blanco E, Sánchez-Jiménez M, Táboas P et al. 2020. RING1B recruits EWSR1-FLI1 and cooperates in the remodeling of chromatin necessary for Ewing sarcoma tumorigenesis. Sci. Adv. 6:eaba3058
     [Google Scholar]
  105. 105.
    Sauka-Spengler T, Bronner-Fraser M. 2008. A gene regulatory network orchestrates neural crest formation. Nat. Rev. Mol. Cell Biol. 9:557–68
     [Google Scholar]
  106. 106.
    Schuettengruber B, Bourbon HM, di Croce L, Cavalli G. 2017. Genome regulation by Polycomb and Trithorax: 70 years and counting. Cell 171:34–57
     [Google Scholar]
  107. 107.
    Schwarz D, Varum S, Zemke M, Schöler A, Baggiolini A et al. 2014. Ezh2 is required for neural crest-derived cartilage and bone formation. Development 141:867–77
     [Google Scholar]
  108. 108.
    Simões-Costa M, Bronner ME. 2015. Establishing neural crest identity: a gene regulatory recipe. Development 142:242–57
     [Google Scholar]
  109. 109.
    Smith CL, Tallquist MD. 2010. PDGF function in diverse neural crest cell populations. Cell Adh. Migr. 4:561
     [Google Scholar]
  110. 110.
    Smith MJ, Higgs JE, Bowers NL, Halliday D, Paterson J et al. 2011. Cranial meningiomas in 411 neurofibromatosis type 2 (NF2) patients with proven gene mutations: clear positional effect of mutations, but absence of female severity effect on age at onset. J. Med. Genet. 48:261–65
     [Google Scholar]
  111. 111.
    Smith MJ, Isidor B, Beetz C, Williams SG, Bhaskar SS et al. 2015. Mutations in LZTR1 add to the complex heterogeneity of schwannomatosis. Neurology 84:141–47
     [Google Scholar]
  112. 112.
    Smith MJ, O'Sullivan J, Bhaskar SS, Hadfield KD, Poke G et al. 2013. Loss-of-function mutations in SMARCE1 cause an inherited disorder of multiple spinal meningiomas. Nat. Genet. 45:295–98
     [Google Scholar]
  113. 113.
    Smith MJ, Wallace AJ, Bowers NL, Eaton H, Evans DGR. 2014. SMARCB1 mutations in schwannomatosis and genotype correlations with rhabdoid tumors. Cancer Genet. 207:373–78
     [Google Scholar]
  114. 114.
    Smith MJ, Wallace AJ, Bowers NL, Rustad CF, Woods CG et al. 2012. Frequency of SMARCB1 mutations in familial and sporadic schwannomatosis. Neurogenetics 13:141–45
     [Google Scholar]
  115. 115.
    Soldatov R, Kaucka M, Kastriti ME, Petersen J, Chontorotzea T et al. 2019. Spatiotemporal structure of cell fate decisions in murine neural crest. Science 364:eaas9536
     [Google Scholar]
  116. 116.
    Staege MS, Hutter C, Neumann I, Foja S, Hattenhorst UE et al. 2004. DNA microarrays reveal relationship of Ewing family tumors to both endothelial and fetal neural crest-derived cells and define novel targets. Cancer Res. 64:8213–21
     [Google Scholar]
  117. 117.
    Teranishi Y, Miyawaki S, Hongo H, Dofuku S, Okano A et al. 2021. Targeted deep sequencing of DNA from multiple tissue types improves the diagnostic rate and reveals a highly diverse phenotype of mosaic neurofibromatosis type 2. J. Med. Genet. 58:701–11
     [Google Scholar]
  118. 118.
    Torchia J, Golbourn B, Feng S, Ho KC, Sin-Chan P et al. 2016. Integrated (epi)-genomic analyses identify subgroup-specific therapeutic targets in CNS rhabdoid tumors. Cancer Cell 30:891–908
     [Google Scholar]
  119. 119.
    Torchia J, Picard D, Lafay-Cousin L, Hawkins CE, Kim SK et al. 2015. Molecular subgroups of atypical teratoid rhabdoid tumours in children: an integrated genomic and clinicopathological analysis. Lancet Oncol. 16:569–82
     [Google Scholar]
  120. 120.
    Trofatter JA, MacCollin MM, Rutter JL, Murreil JR, Duyao MP et al. 1993. A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 72:791–800
     [Google Scholar]
  121. 121.
    Tsurusaki Y, Okamoto N, Ohashi H, Kosho T, Imai Y et al. 2012. Mutations affecting components of the SWI/SNF complex cause Coffin-Siris syndrome. Nat. Genet. 44:376–78
     [Google Scholar]
  122. 122.
    van den Munckhof P, Christiaans I, Kenter SB, Baas F, Hulsebos TJM. 2012. Germline SMARCB1 mutation predisposes to multiple meningiomas and schwannomas with preferential location of cranial meningiomas at the falx cerebri. Neurogenetics 13:1–7
     [Google Scholar]
  123. 123.
    Versteege I, Sévenet N, Lange J, Rousseau-Merck MF, Ambros P et al. 1998. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 394:203–6
     [Google Scholar]
  124. 124.
    Vitte J, Gao F, Coppola G, Judkins AR, Giovannini M. 2017. Timing of Smarcb1 and Nf2 inactivation determines schwannoma versus rhabdoid tumor development. Nat. Commun. 8:300
     [Google Scholar]
  125. 125.
    Wang W, Côté J, Xue Y, Zhou S, Khavari PA et al. 1996. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 15:5370–82
     [Google Scholar]
  126. 126.
    Wang W, Xue Y, Zhou S, Kuo A, Cairns BR, Crabtree GR. 1996. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev. 10:2117–30
     [Google Scholar]
  127. 127.
    Weider M, Küspert M, Bischof M, Vogl MR, Hornig J et al. 2012. Chromatin-remodeling factor Brg1 is required for Schwann cell differentiation and myelination. Dev. Cell 23:193–201
     [Google Scholar]
  128. 128.
    Wilson BG, Wang X, Shen X, McKenna ES, Lemieux ME et al. 2010. Epigenetic antagonism between Polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 18:316–28
     [Google Scholar]
  129. 129.
    World Health Organ. (WHO) Classif. Tumours Ed. Board, eds. 2022. Central Nervous System Tumours WHO Classif. Tumours Vol. 6 Geneva: WHO. , 5th ed..
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The SWI/SNF Complex in Neural Crest Cell Development and Disease
Annual Review of Genomics and Human Genetics 24, 203 (2023); https://doi.org/10.1146/annurev-genom-011723-082913
/content/journals/10.1146/annurev-genom-011723-082913
/content/journals/10.1146/annurev-genom-011723-082913
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