Meningiomas from a developmental perspective: exploring the crossroads between meningeal embryology and tumorigenesis.
Embryological development
Meningioma
Journal
Acta neurochirurgica
ISSN: 0942-0940
Titre abrégé: Acta Neurochir (Wien)
Pays: Austria
ID NLM: 0151000
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
12
10
2020
accepted:
12
11
2020
pubmed:
21
11
2020
medline:
18
5
2021
entrez:
20
11
2020
Statut:
ppublish
Résumé
Meningiomas are tumors arising from the meninges and represent the most frequent central nervous system tumors in adults. Recent large-scale genetic studies and preclinical meningioma mouse modelling led to a better comprehension of meningioma development and suggested evidences of close relationships between meningeal embryology and tumorigenesis. In this non-systematic review, we summarize the current knowledge on meningeal embryology and developmental biology, and illustrate how meningioma tumorigenesis is deeply related to meningeal embryology, concerning the potential cell of origin, the role of reactivation of embryonic stem cells, the influence of the embryonic tissue of origin, and the parallelism between topography-dependant molecular pathways involved in normal meninges and in meningioma development. Our study emphasizes why future studies on meningeal embryology are mandatory to affine our comprehension of mechanisms underlying meningioma initiation and development.
Identifiants
pubmed: 33216210
doi: 10.1007/s00701-020-04650-w
pii: 10.1007/s00701-020-04650-w
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
57-66Références
Aavikko M, Li S-P, Saarinen S et al (2012) Loss of SUFU function in familial multiple meningioma. Am J Hum Genet 91(3):520–526
pubmed: 22958902
pmcid: 3511996
Adeeb N, Mortazavi MM, Tubbs RS, Cohen-Gadol AA (2012) The cranial dura mater: a review of its history, embryology, and anatomy. Childs Nerv Syst 28(6):827–837
pubmed: 22526439
Angelov DN, Vasilev VA (1989) Morphogenesis of rat cranial meninges. Cell Tissue Res 257(1):207–216
pubmed: 2752410
Aszterbaum M, Rothman A, Johnson RL, Fisher M, Xie J, Bonifas JM, Zhang X, Scott MP, Epstein EH (1998) Identification of mutations in the human PATCHED gene in sporadic basal cell carcinomas and in patients with the basal cell nevus syndrome. J Invest Dermatol 110(6):885–888
pubmed: 9620294
Barshes N, Demopoulos A, Engelhard HH (2005) Anatomy and physiology of the leptomeninges and CSF space. Cancer Treat Res 125:1–16
pubmed: 16211880
Beltrami S, Kim R, Gordon J (2013) Neurofibromatosis type 2 protein, NF2: an uncoventional cell cycle regulator. Anticancer Res 33(1):1–11
pubmed: 23267122
pmcid: 3725758
Beuckmann CT, Lazarus M, Gerashchenko D et al (2000) Cellular localization of lipocalin-type prostaglandin D synthase (beta-trace) in the central nervous system of the adult rat. J Comp Neurol 428(1):62–78
pubmed: 11058225
Boetto J, Bielle F, Sanson M, Peyre M, Kalamarides M (2017) SMO mutation status defines a distinct and frequent molecular subgroup in olfactory groove meningiomas. Neuro-oncology 19(3):345–351
pubmed: 28082415
pmcid: 5464306
Brastianos PK, Horowitz PM, Santagata S et al (2013) Genomic sequencing of meningiomas identifies oncogenic SMO and AKT1 mutations. Nat Genet 45(3):285–289
pubmed: 23334667
pmcid: 3739288
Catala M (1998) Embryonic and fetal development of structures associated with the cerebro-spinal fluid in man and other species. Part I: the ventricular system, meninges and choroid plexuses. Arch Anat Cytol Pathol 46(3):153–169
pubmed: 9754371
Choe Y, Siegenthaler JA, Pleasure SJ (2012) A cascade of morphogenic signaling initiated by the meninges controls corpus callosum formation. Neuron 73(4):698–712
pubmed: 22365545
pmcid: 3292762
Choe Y, Zarbalis KS, Pleasure SJ (2014) Neural crest-derived mesenchymal cells require Wnt signaling for their development and drive invagination of the telencephalic midline. PLoS One 9(2):e86025
pubmed: 24516524
pmcid: 3916303
Clark VE, Erson-Omay EZ, Serin A et al (2013) Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science 339(6123):1077–1080
pubmed: 23348505
pmcid: 4808587
Clark VE, Harmancı AS, Bai H et al (2016) Recurrent somatic mutations in POLR2A define a distinct subset of meningiomas. Nat Genet 48(10):1253–1259
pubmed: 27548314
pmcid: 5114141
Couly GF, Le Douarin NM (1987) Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds: implications for the genesis of cephalic human congenital abnormalities. Dev Biol 120(1):198–214
pubmed: 3817289
Dasgupta K, Chung JU, Asam K, Jeong J (2019) Molecular patterning of the embryonic cranial mesenchyme revealed by genome-wide transcriptional profiling. Dev Biol 455(2):434–448
pubmed: 31351040
pmcid: 6842427
Decimo I, Fumagalli G, Berton V, Krampera M, Bifari F (2012) Meninges: from protective membrane to stem cell niche. Am J Stem Cells 1(2):92–105
pubmed: 23671802
pmcid: 3636743
Diamand KEM, Barratt KS, Arkell RM (2018) Overview of Rodent Zic genes. Adv Exp Med Biol 1046:179–207
pubmed: 29442323
Evans DG, Oudit D, Smith MJ, Rutkowski D, Allan E, Newman WG, Lear JT (2017) First evidence of genotype-phenotype correlations in Gorlin syndrome. J Med Genet 54(8):530–536
pubmed: 28596197
Gilbert-Barness E, Cohen MM, Opitz JM (2000) Multiple meningiomas, craniofacial hyperostosis and retinal abnormalities in Proteus syndrome. Am J Med Genet 93(3):234–240
pubmed: 10925389
Gorlin RJ, Goltz RW (1960) Multiple nevoid basal-cell epithelioma, jaw cysts and bifid rib. A syndrome. N Engl J Med 262:908–912
pubmed: 13851319
Goutagny S, Yang HW, Zucman-Rossi J, Chan J, Dreyfuss JM, Park PJ, Black PM, Giovannini M, Carroll RS, Kalamarides M (2010) Genomic profiling reveals alternative genetic pathways of meningioma malignant progression dependent on the underlying NF2 status. Clin Cancer Res 16(16):4155–4164
pubmed: 20682713
Hahn H, Christiansen J, Wicking C et al (1996) A mammalian patched homolog is expressed in target tissues of sonic hedgehog and maps to a region associated with developmental abnormalities. J Biol Chem 271(21):12125–12128
pubmed: 8647801
Haines DE (1991) The meninges. Meningiomas, O. Al Mefty, pp 9–25
Haines DE, Harkey HL, Al-Mefty O (1993) The “subdural” space: a new look at an outdated concept. Neurosurgery 32(1):111–120
pubmed: 8421539
Hindley CJ, Condurat AL, Menon V, Thomas R, Azmitia LM, Davis JA, Pruszak J (2016) The Hippo pathway member YAP enhances human neural crest cell fate and migration. Sci Rep 6:23208
pubmed: 26980066
pmcid: 4793290
Huang MC (2011) Anatomy and biology of the leptomeninges. Al-Mefty’s Meningioma, Second. Thieme, pp 25–34
Hutchings M, Weller RO (1986) Anatomical relationships of the pia mater to cerebral blood vessels in man. J Neurosurg 65(3):316–325
pubmed: 3734882
Inoue T, Ogawa M, Mikoshiba K, Aruga J (2008) Zic deficiency in the cortical marginal zone and meninges results in cortical lamination defects resembling those in type II lissencephaly. J Neurosci 28(18):4712–4725
pubmed: 18448648
pmcid: 6670431
Jeong J, Mao J, Tenzen T, Kottmann AH, McMahon AP (2004) Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev 18(8):937–951
pubmed: 15107405
pmcid: 395852
Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM (2002) Tissue origins and interactions in the mammalian skull vault. Dev Biol 241(1):106–116
pubmed: 11784098
Kalamarides M, Stemmer-Rachamimov AO, Takahashi M, Han Z-Y, Chareyre F, Niwa-Kawakita M, Black PM, Carroll RS, Giovannini M (2008) Natural history of meningioma development in mice reveals: a synergy of Nf2 and p16(Ink4a) mutations. Brain Pathol 18(1):62–70
pubmed: 17924978
pmcid: 2253711
Kalamarides M, Peyre M, Giovannini M (2010) Meningioma mouse models. J Neurooncol 99(3):325–331
pubmed: 20734219
Kalamarides M, Stemmer-Rachamimov AO, Niwa-Kawakita M et al (2011) Identification of a progenitor cell of origin capable of generating diverse meningioma histological subtypes. Oncogene 30(20):2333–2344
pubmed: 21242963
Kawashima M, Suzuki SO, Yamashima T, Fukui M, Iwaki T (2001) Prostaglandin D synthase (beta-trace) in meningeal hemangiopericytoma. Mod Pathol 14(3):197–201
pubmed: 11266526
Keppler-Noreuil KM, Baker EH, Sapp JC, Lindhurst MJ, Biesecker LG (2016) Somatic AKT1 mutations cause meningiomas colocalizing with a characteristic pattern of cranial hyperostosis. Am J Med Genet A 170(10):2605–2610
pubmed: 27550858
pmcid: 5580816
Ketter R, Rahnenführer J, Henn W, Kim Y-J, Feiden W, Steudel W-I, Zang KD, Urbschat S (2008) Correspondence of tumor localization with tumor recurrence and cytogenetic progression in meningiomas. Neurosurgery 62(1):61–69 discussion 69-70
pubmed: 18300892
Kida S, Yamashima T, Kubota T, Ito H, Yamamoto S (1988) A light and electron microscopic and immunohistochemical study of human arachnoid villi. J Neurosurg 69(3):429–435
pubmed: 3404241
Kimonis VE, Goldstein AM, Pastakia B, Yang ML, Kase R, DiGiovanna JJ, Bale AE, Bale SJ (1997) Clinical manifestations in 105 persons with nevoid basal cell carcinoma syndrome. Am J Med Genet 69(3):299–308
pubmed: 9096761
Kros J, de Greve K, van Tilborg A, Hop W, Pieterman H, Avezaat C, Lekanne Dit Deprez R, Zwarthoff E (2001) NF2 status of meningiomas is associated with tumour localization and histology. J Pathol 194(3):367–372
pubmed: 11439370
Kume T, Deng KY, Winfrey V, Gould DB, Walter MA, Hogan BL (1998) The forkhead/winged helix gene Mf1 is disrupted in the pleiotropic mouse mutation congenital hydrocephalus. Cell 93(6):985–996
pubmed: 9635428
Langer LF, Ward JM, Archer TK (2019) Tumor suppressor SMARCB1 suppresses super-enhancers to govern hESC lineage determination. Elife. https://doi.org/10.7554/eLife.45672
Laurendeau I, Ferrer M, Garrido D, D’Haene N, Ciavarelli P, Basso A, Vidaud M, Bieche I, Salmon I, Szijan I (2010) Gene expression profiling of the hedgehog signaling pathway in human meningiomas. Mol Med 16(7–8):262–270
pubmed: 20386868
pmcid: 2896461
Le Lièvre CS, Le Douarin NM (1975) Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J Embryol Exp Morphol 34(1):125–154
pubmed: 1185098
Lee JH, Sade B, Choi E, Golubic M, Prayson R (2006) Meningothelioma as the predominant histological subtype of midline skull base and spinal meningioma. J Neurosurg 105(1):60–64
pubmed: 16871881
Lindhurst MJ, Sapp JC, Teer JK et al (2011) A mosaic activating mutation in AKT1 associated with the Proteus syndrome. N Engl J Med 365(7):611–619
pubmed: 21793738
pmcid: 3170413
Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131(6):803–820
pubmed: 27157931
Marshall GM, Carter DR, Cheung BB, Liu T, Mateos MK, Meyerowitz JG, Weiss WA (2014) The prenatal origins of cancer. Nat Rev Cancer 14(4):277–289
pubmed: 24599217
pmcid: 4041218
Mawrin C, Perry A (2010) Pathological classification and molecular genetics of meningiomas. J Neurooncol 99(3):379–391
pubmed: 20809251
McBratney-Owen B, Iseki S, Bamforth SD, Olsen BR, Morriss-Kay GM (2008) Development and tissue origins of the mammalian cranial base. Dev Biol 322(1):121–132
pubmed: 18680740
pmcid: 2847450
Mishra S, Choe Y, Pleasure SJ, Siegenthaler JA (2016) Cerebrovascular defects in Foxc1 mutants correlate with aberrant WNT and VEGF-A pathways downstream of retinoic acid from the meninges. Dev Biol 420(1):148–165
pubmed: 27671872
pmcid: 5124406
Mota M, Shevde LA (2020) Merlin regulates signaling events at the nexus of development and cancer. Cell Commun Signal 18(1):63
pubmed: 32299434
pmcid: 7164249
Narang A, Maheshwari C, Aggarwal V, Bansal P, Singh P (2020) Gorlin-Goltz syndrome with intracranial meningioma: case report and review of literature. World Neurosurg 133:324–330
pubmed: 31605858
Noden DM, Trainor PA (2005) Relations and interactions between cranial mesoderm and neural crest populations. J Anat 207(5):575–601
pubmed: 16313393
pmcid: 1571569
O’Rahilly R, Müller F (1986) The meninges in human development. J Neuropathol Exp Neurol 45(5):588–608
pubmed: 3746345
Ostrom QT, Gittleman H, Truitt G, Boscia A, Kruchko C, Barnholtz-Sloan JS (2018) CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2011-2015. Neuro Oncol 20(suppl_4):iv1–iv86
pubmed: 30445539
pmcid: 6129949
Patel AJ, Wan Y-W, Al-Ouran R et al (2019) Molecular profiling predicts meningioma recurrence and reveals loss of DREAM complex repression in aggressive tumors. Proc Natl Acad Sci U S A 116(43):21715–21726
pubmed: 31591222
pmcid: 6815170
Porta C, Paglino C, Mosca A (2014) Targeting PI3K/Akt/mTOR signaling in cancer. Front Oncol 4:64
pubmed: 24782981
pmcid: 3995050
Preusser M, Brastianos PK, Mawrin C (2018) Advances in meningioma genetics: novel therapeutic opportunities. Nat Rev Neurol 14(2):106–115
pubmed: 29302064
Rimkus TK, Carpenter RL, Qasem S, Chan M, Lo H-W (2016) Targeting the Sonic Hedgehog signaling pathway: review of smoothened and GLI inhibitors. Cancers (Basel). https://doi.org/10.3390/cancers8020022
Roessler E, Belloni E, Gaudenz K, Jay P, Berta P, Scherer SW, Tsui LC, Muenke M (1996) Mutations in the human Sonic Hedgehog gene cause holoprosencephaly. Nat Genet 14(3):357–360
pubmed: 8896572
Rogers L, Barani I, Chamberlain M, Kaley TJ, McDermott M, Raizer J, Schiff D, Weber DC, Wen PY, Vogelbaum MA (2015) Meningiomas: knowledge base, treatment outcomes, and uncertainties. A RANO review. J Neurosurg 122(1):4–23
pubmed: 25343186
pmcid: 5062955
Sahm F, Schrimpf D, Stichel D et al (2017) DNA methylation-based classification and grading system for meningioma: a multicentre, retrospective analysis. Lancet Oncol 18(5):682–694
pubmed: 28314689
Saxton RA, Sabatini DM (2017) mTOR signaling in growth, metabolism, and disease. Cell 168(6):960–976
pubmed: 28283069
pmcid: 5394987
Shankar GM, Abedalthagafi M, Vaubel RA et al (2017) Germline and somatic BAP1 mutations in high-grade rhabdoid meningiomas. Neuro Oncol 19(4):535–545
pubmed: 28170043
Siegenthaler JA, Pleasure SJ (2011) We have got you “covered”: how the meninges control brain development. Curr Opin Genet Dev 21(3):249–255
pubmed: 21251809
pmcid: 3105186
Smith MJ, Higgs JE, Bowers NL 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(4):261–265
pubmed: 21278391
Smith MJ, O’Sullivan J, Bhaskar SS et al (2013) Loss-of-function mutations in SMARCE1 cause an inherited disorder of multiple spinal meningiomas. Nat Genet 45(3):295–298
pubmed: 23377182
Tischfield MA, Robson CD, Gilette NM et al (2017) Cerebral vein malformations result from loss of Twist1 expression and BMP signaling from skull progenitor cells and dura. Dev Cell 42(5):445–461.e5
pubmed: 28844842
pmcid: 5595652
Urade Y, Kitahama K, Ohishi H, Kaneko T, Mizuno N, Hayaishi O (1993) Dominant expression of mRNA for prostaglandin D synthase in leptomeninges, choroid plexus, and oligodendrocytes of the adult rat brain. Proc Natl Acad Sci USA 90(19):9070–9074
pubmed: 8415655
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):1–7
pubmed: 22038540
Vasudevan HN, Braunstein SE, Phillips JJ et al (2018) Comprehensive molecular profiling identifies FOXM1 as a key transcription factor for meningioma proliferation. Cell Rep 22(13):3672–3683
pubmed: 29590631
Vivatbutsiri P, Ichinose S, Hytönen M, Sainio K, Eto K, Iseki S (2008) Impaired meningeal development in association with apical expansion of calvarial bone osteogenesis in the Foxc1 mutant. J Anat 212(5):603–611
pubmed: 18422524
pmcid: 2409093
Weller RO, Sharp MM, Christodoulides M, Carare RO, Møllgård K (2018) The meninges as barriers and facilitators for the movement of fluid, cells and pathogens related to the rodent and human CNS. Acta Neuropathol 135(3):363–385
pubmed: 29368214
Xavier GM, Seppala M, Barrell W, Birjandi AA, Geoghegan F, Cobourne MT (2016) Hedgehog receptor function during craniofacial development. Dev Biol 415(2):198–215
pubmed: 26875496
Yamashima T, Sakuda K, Tohma Y et al (1997) Prostaglandin D synthase (beta-trace) in human arachnoid and meningioma cells: roles as a cell marker or in cerebrospinal fluid absorption, tumorigenesis, and calcification process. J Neurosci 17(7):2376–2382
pubmed: 9065498
pmcid: 6573504
Yoshida T, Vivatbutsiri P, Morriss-Kay G, Saga Y, Iseki S (2008) Cell lineage in mammalian craniofacial mesenchyme. Mech Dev 125(9–10):797–808
pubmed: 18617001
Youngblood MW, Duran D, Montejo JD et al (2019) Correlations between genomic subgroup and clinical features in a cohort of more than 3000 meningiomas. J Neurosurg :1–10. https://doi.org/10.3171/2019.8.JNS191266
Zador Z, Landry AP, Balas M, Cusimano MD (2020) Landscape of immune cell gene expression is unique in predominantly WHO grade 1 skull base meningiomas when compared to convexity. Sci Rep 10(1):9065
pubmed: 32493984
pmcid: 7270140
Zang KD (2001) Meningioma: a cytogenetic model of a complex benign human tumor, including data on 394 karyotyped cases. Cytogenet Cell Genet 93(3–4):207–220
pubmed: 11528114
Zarbalis K, Siegenthaler JA, Choe Y, May SR, Peterson AS, Pleasure SJ (2007) Cortical dysplasia and skull defects in mice with a Foxc1 allele reveal the role of meningeal differentiation in regulating cortical development. Proc Natl Acad Sci USA 104(35):14002–14007
pubmed: 17715063
Zhang N, Bai H, David KK, Dong J, Zheng Y, Cai J, Giovannini M, Liu P, Anders RA, Pan D (2010) The Merlin/NF2 tumor suppressor functions through the YAP oncoprotein to regulate tissue homeostasis in mammals. Dev Cell 19(1):27–38
pubmed: 20643348
pmcid: 2925178