Neurofibromatosis and Schwannomatosis

Scott R. Plotkin; Antje Wick

doi:10.1055/s-0038-1627471

Seminars in Neurology, Table of Contents

Semin Neurol 2018; 38(01): 073-085
DOI: 10.1055/s-0038-1627471

Review Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Neurofibromatosis and Schwannomatosis

Authors

Scott R. Plotkin

¹Department of Neurology and Cancer Center, Massachusetts General Hospital, Boston, Massachusetts
Antje Wick

²Department of Neurology, University Hospital of Heidelberg, Heidelberg, Germany

Abstract

Neurofibromatosis 1, neurofibromatosis 2, and schwannomatosis are a group of related classically inherited but often times sporadic tumor suppressor syndromes. Neuro-oncologists should recognize these syndromes, initiate necessary tests in patients with a clinical suspicion, and support genetic counseling of patients and families. In this review, clinical presentation, diagnostic criteria, day-to-day management including supportive care as well as updates on genetics, and experimental treatment strategies are discussed.

Keywords

neurofibromatosis - schwannomatosis - neurofibroma - schwannoma - meningioma - ependymoma

Full Text

References

References
1 Knudson Jr AG. Mutation and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci U S A 1971; 68 (04) 820-823
2 Friedman JM. Epidemiology of neurofibromatosis type 1. Am J Med Genet 1999; 89 (01) 1-6
3 Lammert M, Friedman JM, Kluwe L, Mautner VF. Prevalence of neurofibromatosis 1 in German children at elementary school enrollment. Arch Dermatol 2005; 141 (01) 71-74
4 Evans DG, Howard E, Giblin C. , et al. Birth incidence and prevalence of tumor-prone syndromes: estimates from a UK family genetic register service. Am J Med Genet A 2010; 152A (02) 327-332
5 Wilding A, Ingham SL, Lalloo F. , et al. Life expectancy in hereditary cancer predisposing diseases: an observational study. J Med Genet 2012; 49 (04) 264-269
6 National Institutes of Health Consensus Development Conference. Neurofibromatosis. Conference statement. Arch Neurol 1988; 45 (05) 575-578
7 Messiaen LM, Callens T, Mortier G. , et al. Exhaustive mutation analysis of the NF1 gene allows identification of 95% of mutations and reveals a high frequency of unusual splicing defects. Hum Mutat 2000; 15 (06) 541-555
8 Cnossen MH, van der Est MN, Breuning MH. , et al. Deletions spanning the neurofibromatosis type 1 gene: implications for genotype-phenotype correlations in neurofibromatosis type 1?. Hum Mutat 1997; 9 (05) 458-464
9 Kehrer-Sawatzki H, Kluwe L, Fünsterer C, Mautner VF. Extensively high load of internal tumors determined by whole body MRI scanning in a patient with neurofibromatosis type 1 and a non-LCR-mediated 2-Mb deletion in 17q11.2. Hum Genet 2005; 116 (06) 466-475
10 Upadhyaya M, Huson SM, Davies M. , et al. An absence of cutaneous neurofibromas associated with a 3-bp inframe deletion in exon 17 of the NF1 gene (c.2970-2972 delAAT): evidence of a clinically significant NF1 genotype-phenotype correlation. Am J Hum Genet 2007; 80 (01) 140-151
11 Brems H, Chmara M, Sahbatou M. , et al. Germline loss-of-function mutations in SPRED1 cause a neurofibromatosis 1-like phenotype. Nat Genet 2007; 39 (09) 1120-1126
12 Messiaen L, Yao S, Brems H. , et al. Clinical and mutational spectrum of neurofibromatosis type 1-like syndrome. JAMA 2009; 302 (19) 2111-2118
13 Wimmer K, Rosenbaum T, Messiaen L. Connections between constitutional mismatch repair deficiency syndrome and neurofibromatosis type 1. Clin Genet 2017; 91 (04) 507-519
14 Rauen KA, Huson SM, Burkitt-Wright E. , et al. Recent developments in neurofibromatoses and RASopathies: management, diagnosis and current and future therapeutic avenues. Am J Med Genet A 2015; 167A (01) 1-10
15 Maertens O, De Schepper S, Vandesompele J. , et al. Molecular dissection of isolated disease features in mosaic neurofibromatosis type 1. Am J Hum Genet 2007; 81 (02) 243-251
16 Ruggieri M, Huson SM. The clinical and diagnostic implications of mosaicism in the neurofibromatoses. Neurology 2001; 56 (11) 1433-1443
17 Serra E, Puig S, Otero D. , et al. Confirmation of a double-hit model for the NF1 gene in benign neurofibromas. Am J Hum Genet 1997; 61 (03) 512-519
18 Gutmann DH, Donahoe J, Brown T, James CD, Perry A. Loss of neurofibromatosis 1 (NF1) gene expression in NF1-associated pilocytic astrocytomas. Neuropathol Appl Neurobiol 2000; 26 (04) 361-367
19 Woodruff JM. Pathology of tumors of the peripheral nerve sheath in type 1 neurofibromatosis. Am J Med Genet 1999; 89 (01) 23-30
20 Zhu Y, Ghosh P, Charnay P, Burns DK, Parada LF. Neurofibromas in NF1: Schwann cell origin and role of tumor environment. Science 2002; 296 (5569): 920-922
21 Serra E, Rosenbaum T, Winner U. , et al. Schwann cells harbor the somatic NF1 mutation in neurofibromas: evidence of two different Schwann cell subpopulations. Hum Mol Genet 2000; 9 (20) 3055-3064
22 DeBella K, Szudek J, Friedman JM. Use of the National Institutes of Health criteria for diagnosis of neurofibromatosis 1 in children. Pediatrics 2000; 105 (3 Pt 1): 608-614
23 Evans DG, Baser ME, McGaughran J, Sharif S, Howard E, Moran A. Malignant peripheral nerve sheath tumours in neurofibromatosis 1. J Med Genet 2002; 39 (05) 311-314
24 Duong TA, Sbidian E, Valeyrie-Allanore L. , et al. Mortality associated with neurofibromatosis 1: a cohort study of 1895 patients in 1980-2006 in France. Orphanet J Rare Dis 2011; 6: 18
25 Evans DG, O'Hara C, Wilding A. , et al. Mortality in neurofibromatosis 1: in North West England: an assessment of actuarial survival in a region of the UK since 1989. Eur J Hum Genet 2011; 19 (11) 1187-1191
26 Thakkar SD, Feigen U, Mautner VF. Spinal tumours in neurofibromatosis type 1: an MRI study of frequency, multiplicity and variety. Neuroradiology 1999; 41 (09) 625-629
27 Prada CE, Rangwala FA, Martin LJ. , et al. Pediatric plexiform neurofibromas: impact on morbidity and mortality in neurofibromatosis type 1. J Pediatr 2012; 160 (03) 461-467
28 Carli M, Ferrari A, Mattke A. , et al. Pediatric malignant peripheral nerve sheath tumor: the Italian and German soft tissue sarcoma cooperative group. J Clin Oncol 2005; 23 (33) 8422-8430
29 Ferner RE, Golding JF, Smith M. , et al. [18F]2-fluoro-2-deoxy-D-glucose positron emission tomography (FDG PET) as a diagnostic tool for neurofibromatosis 1 (NF1) associated malignant peripheral nerve sheath tumours (MPNSTs): a long-term clinical study. Ann Oncol 2008; 19 (02) 390-394
30 Guillamo JS, Créange A, Kalifa C. , et al; Réseau NF France. Prognostic factors of CNS tumours in Neurofibromatosis 1 (NF1): a retrospective study of 104 patients. Brain 2003; 126 (Pt 1): 152-160
31 Listernick R, Ferner RE, Liu GT, Gutmann DH. Optic pathway gliomas in neurofibromatosis-1: controversies and recommendations. Ann Neurol 2007; 61 (03) 189-198
32 Gutmann DH, Rasmussen SA, Wolkenstein P. , et al. Gliomas presenting after age 10 in individuals with neurofibromatosis type 1 (NF1). Neurology 2002; 59 (05) 759-761
33 Huttner AJ, Kieran MW, Yao X. , et al. Clinicopathologic study of glioblastoma in children with neurofibromatosis type 1. Pediatr Blood Cancer 2010; 54 (07) 890-896
34 Tonsgard JH, Kwak SM, Short MP, Dachman AH. CT imaging in adults with neurofibromatosis-1: frequent asymptomatic plexiform lesions. Neurology 1998; 50 (06) 1755-1760
35 Plotkin SR, Bredella MA, Cai W. , et al. Quantitative assessment of whole-body tumor burden in adult patients with neurofibromatosis. PLoS One 2012; 7 (04) e35711
36 Cai W, Kassarjian A, Bredella MA. , et al. Tumor burden in patients with neurofibromatosis types 1 and 2 and schwannomatosis: determination on whole-body MR images. Radiology 2009; 250 (03) 665-673
37 Plotkin SR, Blakeley JO, Dombi E. , et al. Achieving consensus for clinical trials: the REiNS International Collaboration. Neurology 2013; 81 (21) (Suppl. 01) S1-S5
38 Dombi E, Baldwin A, Marcus LJ. , et al. Activity of selumetinib in neurofibromatosis type 1-related plexiform neurofibromas. N Engl J Med 2016; 375 (26) 2550-2560
39 Listernick R, Louis DN, Packer RJ, Gutmann DH. Optic pathway gliomas in children with neurofibromatosis 1: consensus statement from the NF1 Optic Pathway Glioma Task Force. Ann Neurol 1997; 41 (02) 143-149
40 Fisher MJ, Avery RA, Allen JC. , et al; REiNS International Collaboration. Functional outcome measures for NF1-associated optic pathway glioma clinical trials. Neurology 2013; 81 (21) (Suppl. 01) S15-S24
41 Evans DGR, Birch JM, Ramsden RT, Sharif S, Baser ME. Malignant transformation and new primary tumours after therapeutic radiation for benign disease: substantial risks in certain tumour prone syndromes. J Med Genet 2006; 43 (04) 289-294
42 Weiss B, Widemann BC, Wolters P. , et al. Sirolimus for progressive neurofibromatosis type 1-associated plexiform neurofibromas: a neurofibromatosis Clinical Trials Consortium phase II study. Neuro Oncol 2015; 17 (04) 596-603
43 Weiss B, Widemann BC, Wolters P. , et al. Sirolimus for non-progressive NF1-associated plexiform neurofibromas: an NF clinical trials consortium phase II study. Pediatr Blood Cancer 2014; 61 (06) 982-986
44 Ullrich NJ, Robertson R, Kinnamon DD. , et al. Moyamoya following cranial irradiation for primary brain tumors in children. Neurology 2007; 68 (12) 932-938
45 Sharif S, Ferner R, Birch JM. , et al. Second primary tumors in neurofibromatosis 1 patients treated for optic glioma: substantial risks after radiotherapy. J Clin Oncol 2006; 24 (16) 2570-2575
46 Collins VP, Jones DT, Giannini C. Pilocytic astrocytoma: pathology, molecular mechanisms and markers. Acta Neuropathol 2015; 129 (06) 775-788
47 Dasgupta B, Yi Y, Chen DY, Weber JD, Gutmann DH. Proteomic analysis reveals hyperactivation of the mammalian target of rapamycin pathway in neurofibromatosis 1-associated human and mouse brain tumors. Cancer Res 2005; 65 (07) 2755-2760
48 Evans DG, Moran A, King A, Saeed S, Gurusinghe N, Ramsden R. Incidence of vestibular schwannoma and neurofibromatosis 2 in the North West of England over a 10-year period: higher incidence than previously thought. Otol Neurotol 2005; 26 (01) 93-97
49 Wallace AJ, Watson CJ, Oward E, Evans DG, Elles RG. Mutation scanning of the NF2 gene: an improved service based on meta-PCR/sequencing, dosage analysis, and loss of heterozygosity analysis. Genet Test 2004; 8 (04) 368-380
50 Evans DG, Ramsden RT, Shenton A. , et al. Mosaicism in neurofibromatosis type 2: an update of risk based on uni/bilaterality of vestibular schwannoma at presentation and sensitive mutation analysis including multiple ligation-dependent probe amplification. J Med Genet 2007; 44 (07) 424-428
51 Ahronowitz I, Xin W, Kiely R, Sims K, MacCollin M, Nunes FP. Mutational spectrum of the NF2 gene: a meta-analysis of 12 years of research and diagnostic laboratory findings. Hum Mutat 2007; 28 (01) 1-12
52 Baser ME, Kuramoto L, Woods R. , et al. The location of constitutional neurofibromatosis 2 (NF2) splice site mutations is associated with the severity of NF2. J Med Genet 2005; 42 (07) 540-546
53 MacCollin M, Braverman N, Viskochil D. , et al. A point mutation associated with a severe phenotype of neurofibromatosis 2. Ann Neurol 1996; 40 (03) 440-445
54 Ruttledge MH, Andermann AA, Phelan CM. , et al. Type of mutation in the neurofibromatosis type 2 gene (NF2) frequently determines severity of disease. Am J Hum Genet 1996; 59 (02) 331-342
55 Rouleau GA, Merel P, Lutchman M. , et al. Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature 1993; 363 (6429): 515-521
56 Kluwe L, Friedrich RE, Tatagiba M, Mautner VF. Presymptomatic diagnosis for children of sporadic neurofibromatosis 2 patients: a method based on tumor analysis. Genet Med 2002; 4 (01) 27-30
57 Rouleau GA, Wertelecki W, Haines JL. , et al. Genetic linkage of bilateral acoustic neurofibromatosis to a DNA marker on chromosome 22. Nature 1987; 329 (6136): 246-248
58 Wertelecki W, Rouleau GA, Superneau DW. , et al. Neurofibromatosis 2: clinical and DNA linkage studies of a large kindred. N Engl J Med 1988; 319 (05) 278-283
59 Trofatter JA, MacCollin MM, Rutter JL. , et al. A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 1993; 75 (04) 826
60 McClatchey AI, Giovannini M. Membrane organization and tumorigenesis--the NF2 tumor suppressor, Merlin. Genes Dev 2005; 19 (19) 2265-2277
61 Jacoby LB, MacCollin M, Barone R, Ramesh V, Gusella JF. Frequency and distribution of NF2 mutations in schwannomas. Genes Chromosomes Cancer 1996; 17 (01) 45-55
62 Wellenreuther R, Kraus JA, Lenartz D. , et al. Analysis of the neurofibromatosis 2 gene reveals molecular variants of meningioma. Am J Pathol 1995; 146 (04) 827-832
63 Li W, You L, Cooper J. , et al. Merlin/NF2 suppresses tumorigenesis by inhibiting the E3 ubiquitin ligase CRL4(DCAF1) in the nucleus. Cell 2010; 140 (04) 477-490
64 Smith MJ, Higgs JE, Bowers NL. , et al. 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 2011; 48 (04) 261-265
65 Goutagny S, Bah AB, Henin D. , et al. Long-term follow-up of 287 meningiomas in neurofibromatosis type 2 patients: clinical, radiological, and molecular features. Neuro Oncol 2012; 14 (08) 1090-1096
66 Mautner VF, Tatagiba M, Lindenau M. , et al. Spinal tumors in patients with neurofibromatosis type 2: MR imaging study of frequency, multiplicity, and variety. AJR Am J Roentgenol 1995; 165 (04) 951-955
67 Patronas NJ, Courcoutsakis N, Bromley CM, Katzman GL, MacCollin M, Parry DM. Intramedullary and spinal canal tumors in patients with neurofibromatosis 2: MR imaging findings and correlation with genotype. Radiology 2001; 218 (02) 434-442
68 Nunes F, MacCollin M. Neurofibromatosis 2 in the pediatric population. J Child Neurol 2003; 18 (10) 718-724
69 Ruggieri M, Iannetti P, Polizzi A. , et al. Earliest clinical manifestations and natural history of neurofibromatosis type 2 (NF2) in childhood: a study of 24 patients. Neuropediatrics 2005; 36 (01) 21-34
70 Mulvihill JJ, Parry DM, Sherman JL, Pikus A, Kaiser-Kupfer MI, Eldridge R. NIH conference. Neurofibromatosis 1 (Recklinghausen disease) and neurofibromatosis 2 (bilateral acoustic neurofibromatosis). An update. Ann Intern Med 1990; 113 (01) 39-52
71 Baser ME, Friedman JM, Wallace AJ, Ramsden RT, Joe H, Evans DG. Evaluation of clinical diagnostic criteria for neurofibromatosis 2. Neurology 2002; 59 (11) 1759-1765
72 Vakharia KT, Henstrom D, Plotkin SR, Cheney M, Hadlock TA. Facial reanimation of patients with neurofibromatosis type 2. Neurosurgery 2012; 70 (2, Suppl Operative): 237-243
73 Liu R, Fagan P. Facial nerve schwannoma: surgical excision versus conservative management. Ann Otol Rhinol Laryngol 2001; 110 (11) 1025-1029
74 Fuss M, Debus J, Lohr F. , et al. Conventionally fractionated stereotactic radiotherapy (FSRT) for acoustic neuromas. Int J Radiat Oncol Biol Phys 2000; 48 (05) 1381-1387
75 Slattery III WH, Brackmann DE. Results of surgery following stereotactic irradiation for acoustic neuromas. Am J Otol 1995; 16 (03) 315-319 , discussion 319–321
76 Baser ME, Evans DG, Jackler RK, Sujansky E, Rubenstein A. Neurofibromatosis 2, radiosurgery and malignant nervous system tumours. Br J Cancer 2000; 82 (04) 998
77 Thomsen J, Mirz F, Wetke R, Astrup J, Bojsen-Møller M, Nielsen E. Intracranial sarcoma in a patient with neurofibromatosis type 2 treated with gamma knife radiosurgery for vestibular schwannoma. Am J Otol 2000; 21 (03) 364-370
78 Combs SE, Volk S, Schulz-Ertner D, Huber PE, Thilmann C, Debus J. Management of acoustic neuromas with fractionated stereotactic radiotherapy (FSRT): long-term results in 106 patients treated in a single institution. Int J Radiat Oncol Biol Phys 2005; 63 (01) 75-81
79 Plotkin SR, Halpin C, McKenna MJ, Loeffler JS, Batchelor TT, Barker FG. Erlotinib for Progressive Vestibular Schwannoma in Neurofibromatosis 2 Patients. Otol Neurotol 2010; 31 (07) 1135-1143
80 Karajannis MA, Legault G, Hagiwara M. , et al. Phase II trial of lapatinib in adult and pediatric patients with neurofibromatosis type 2 and progressive vestibular schwannomas. Neuro Oncol 2012; 14 (09) 1163-1170
81 Karajannis MA, Legault G, Hagiwara M. , et al. Phase II study of everolimus in children and adults with neurofibromatosis type 2 and progressive vestibular schwannomas. Neuro Oncol 2014; 16 (02) 292-297
82 Plotkin SR, Merker VL, Halpin C. , et al. Bevacizumab for progressive vestibular schwannoma in neurofibromatosis type 2: a retrospective review of 31 patients. Otol Neurotol 2012; 33 (06) 1046-1052
83 Blakeley JO, Ye X, Duda DG. , et al. Efficacy and biomarker study of bevacizumab for hearing loss resulting from neurofibromatosis type 2-associated vestibular schwannomas. J Clin Oncol 2016; 34 (14) 1669-1675
84 Alanin MC, Klausen C, Caye-Thomasen P. , et al. Effect of bevacizumab on intracranial meningiomas in patients with neurofibromatosis type 2 - a retrospective case series. Int J Neurosci 2016; 126 (11) 1002-1006
85 Morris KA, Golding JF, Blesing C. , et al; UK NF2 research group. Toxicity profile of bevacizumab in the UK Neurofibromatosis type 2 cohort. J Neurooncol 2017; 131 (01) 117-124
86 Birckhead B, Sio TT, Pollock BE, Link MJ, Laack NN. Gamma Knife radiosurgery for neurofibromatosis type 2-associated meningiomas: a 22-year patient series. J Neurooncol 2016; 130 (03) 553-560
87 Antinheimo J, Sankila R, Carpén O, Pukkala E, Sainio M, Jääskeläinen J. Population-based analysis of sporadic and type 2 neurofibromatosis-associated meningiomas and schwannomas. Neurology 2000; 54 (01) 71-76
88 Plotkin SR, Blakeley JO, Evans DG. , et al. Update from the 2011 International Schwannomatosis Workshop: from genetics to diagnostic criteria. Am J Med Genet A 2013; 161A (03) 405-416
89 Bruggers CS, Bleyl SB, Pysher T. , et al. Clinicopathologic comparison of familial versus sporadic atypical teratoid/rhabdoid tumors (AT/RT) of the central nervous system. Pediatr Blood Cancer 2011; 56 (07) 1026-1031
90 Boyd C, Smith MJ, Kluwe L, Balogh A, Maccollin M, Plotkin SR. Alterations in the SMARCB1 (INI1) tumor suppressor gene in familial schwannomatosis. Clin Genet 2008; 74 (04) 358-366
91 Hadfield KD, Newman WG, Bowers NL. , et al. Molecular characterisation of SMARCB1 and NF2 in familial and sporadic schwannomatosis. J Med Genet 2008; 45 (06) 332-339
92 Rousseau G, Noguchi T, Bourdon V, Sobol H, Olschwang S. SMARCB1/INI1 germline mutations contribute to 10% of sporadic schwannomatosis. BMC Neurol 2011; 11: 9
93 Smith MJ, Wallace AJ, Bowers NL. , et al. Frequency of SMARCB1 mutations in familial and sporadic schwannomatosis. Neurogenetics 2012; 13 (02) 141-145
94 Piotrowski A, Xie J, Liu YF. , et al. Germline loss-of-function mutations in LZTR1 predispose to an inherited disorder of multiple schwannomas. Nat Genet 2014; 46 (02) 182-187
95 Smith MJ, Isidor B, Beetz C. , et al. Mutations in LZTR1 add to the complex heterogeneity of schwannomatosis. Neurology 2015; 84 (02) 141-147
96 Schneppenheim R, Frühwald MC, Gesk S. , et al. Germline nonsense mutation and somatic inactivation of SMARCA4/BRG1 in a family with rhabdoid tumor predisposition syndrome. Am J Hum Genet 2010; 86 (02) 279-284
97 Martens JA, Winston F. Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr Opin Genet Dev 2003; 13 (02) 136-142
98 Narlikar GJ, Fan HY, Kingston RE. Cooperation between complexes that regulate chromatin structure and transcription. Cell 2002; 108 (04) 475-487
99 Wang W, Côté J, Xue Y. , et al. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J 1996; 15 (19) 5370-5382
100 Wang W, Xue Y, Zhou S, Kuo A, Cairns BR, Crabtree GR. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev 1996; 10 (17) 2117-2130
101 Kalpana GV, Smith ME. Development of targeted therapies for rhabdoid tumors based on the functions of INI1/hSNF5 tumor suppressor. In: Houghton P, Arceci R. , eds. Molecularly Targeted Therapy for Childhood Cancer. New York, NY: Springer Verlag; 2010: 305-330
102 Wilson BG, Roberts CW. SWI/SNF nucleosome remodellers and cancer. Nat Rev Cancer 2011; 11 (07) 481-492
103 Krosl J, Mamo A, Chagraoui J. , et al. A mutant allele of the Swi/Snf member BAF250a determines the pool size of fetal liver hemopoietic stem cell populations. Blood 2010; 116 (10) 1678-1684
104 Yoo AS, Crabtree GR. ATP-dependent chromatin remodeling in neural development. Curr Opin Neurobiol 2009; 19 (02) 120-126
105 Albini S, Puri PL. SWI/SNF complexes, chromatin remodeling and skeletal myogenesis: it's time to exchange!. Exp Cell Res 2010; 316 (18) 3073-3080
106 Caramel J, Medjkane S, Quignon F, Delattre O. The requirement for SNF5/INI1 in adipocyte differentiation highlights new features of malignant rhabdoid tumors. Oncogene 2008; 27 (14) 2035-2044
107 Nowak SJ, Aihara H, Gonzalez K, Nibu Y, Baylies MK. Akirin links twist-regulated transcription with the Brahma chromatin remodeling complex during embryogenesis. PLoS Genet 2012; 8 (03) e1002547
108 Young DW, Pratap J, Javed A. , et al. SWI/SNF chromatin remodeling complex is obligatory for BMP2-induced, Runx2-dependent skeletal gene expression that controls osteoblast differentiation. J Cell Biochem 2005; 94 (04) 720-730
109 Merker VL, Esparza S, Smith MJ, Stemmer-Rachamimov A, Plotkin SR. Clinical features of schwannomatosis: a retrospective analysis of 87 patients. Oncologist 2012; 17 (10) 1317-1322
110 Farschtschi S, Mautner VF, Pham M. , et al. Multifocal nerve lesions and LZTR1 germline mutations in segmental schwannomatosis. Ann Neurol 2016; 80 (04) 625-628
111 Smith MJ, Kulkarni A, Rustad C. , et al. Vestibular schwannomas occur in schwannomatosis and should not be considered an exclusion criterion for clinical diagnosis. Am J Med Genet A 2012; 158A (01) 215-219
112 Gripp KW, Baker L, Kandula V. , et al. Constitutional LZTR1 mutation presenting with a unilateral vestibular schwannoma in a teenager. Clin Genet 2017; 92 (05) 540-543
113 Smith MJ, Bowers NL, Bulman M. , et al. Revisiting neurofibromatosis type 2 diagnostic criteria to exclude LZTR1-related schwannomatosis. Neurology 2017; 88 (01) 87-92
114 van den Munckhof P, Christiaans I, Kenter SB, Baas F, Hulsebos TJ. Germline SMARCB1 mutation predisposes to multiple meningiomas and schwannomas with preferential location of cranial meningiomas at the falx cerebri. Neurogenetics 2012; 13 (01) 1-7
115 Bacci C, Sestini R, Provenzano A. , et al. Schwannomatosis associated with multiple meningiomas due to a familial SMARCB1 mutation. Neurogenetics 2010; 11 (01) 73-80
116 MacCollin M, Chiocca EA, Evans DG. , et al. Diagnostic criteria for schwannomatosis. Neurology 2005; 64 (11) 1838-1845
117 Blakeley J, Schreck KC, Evans DG. , et al. Clinical response to bevacizumab in schwannomatosis. Neurology 2014; 83 (21) 1986-1987