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Identification of a Progenitor Cell of Origin Capable of Generating Oncogene (2011) 30, 2333–2344 & 2011 Macmillan Publishers Limited All rights reserved 0950-9232/11 www.nature.com/onc ORIGINAL ARTICLE Identification of a progenitor cell of origin capable of generating diverse meningioma histological subtypes M Kalamarides1,2,3, AO Stemmer-Rachamimov4, M Niwa-Kawakita1,2, F Chareyre1,2, E Taranchon1,2, Z-Y Han1,2, C Martinelli1,2, EA Lusis5, B Hegedus6,8, DH Gutmann6 and M Giovannini1,2,7 1Inserm, U674, Paris, France; 2Universite´ Paris 7—Denis Diderot, Institut Universitaire d’He´matologie, Paris, France; 3AP-HP, Hoˆpital Beaujon, Service de Neurochirurgie, Clichy, France; 4Molecular Neuro-Oncology and Pathology Department, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; 5Department of Neurosurgery, Washington University School of Medicine, St Louis, MO, USA; 6Department of Neurology, Washington University School of Medicine, St Louis, MO, USA and 7Center for Neural Tumor Research, House Ear Institute, Los Angeles, CA, USA Meningiomas are among the most common primary affect older adults, particularly women, and are often central nervous system tumours in adults. Studies focused associated with significant morbidity (Louis et al., 2000). on the molecular basis for meningioma development are Histologically, these tumours exhibit a wide range of hampered by a lack of information with regard to the cell of histological appearances, with meningothelial, fibroblas- origin for these brain tumours. Herein, we identify a tic and transitional meningiomas comprising the most prostaglandin D synthase-positive meningeal precursor as common World Health Organization subtypes. the cell of origin for murine meningioma, and show that Compared with adult gliomas, relatively less is known neurofibromatosis type 2 (Nf2) inactivation in prostaglandin about the cell of origin of these tumours or the critical D2 synthase (PGDS) ( þ ) primordial meningeal cells, genetic changes that drive tumourigenesis. Insights into before the formation of the three meningeal layers, accounts the genetic aetiology of meningioma have derived from for the heterogeneity of meningioma histological subtypes. the study of individuals with the inherited cancer Using a unique PGDSCre strain, we define a critical predisposition syndrome neurofibromatosis type 2 embryonic and early postnatal developmental window in (NF2), in which 50% of affected individuals develop which biallelic Nf2 inactivation in PGDS ( þ )progenitor meningioma (Evans et al., 1992). The central role of the cells results in meningioma formation. Moreover, we identify NF2 gene in regulating leptomeningeal cell proliferation differentially expressed markers that characterize the two is underscored by the finding of biallelic NF2 gene major histological meningioma subtypes both in human and inactivation in 50–80% of sporadic meningiomas mouse tumours. Collectively, these findings establish the cell (Ruttledge et al., 1994; Gutmann et al., 1997). In oforiginforthesecommonbraintumoursaswellasa particular, NF2 loss is most frequently observed in the susceptible developmental period in which signature genetic fibroblastic histological subtype (Hartmann et al., 2006). mutations culminate in meningioma formation. Previously, we showed that biallelic Nf2 gene in- Oncogene (2011) 30, 2333–2344; doi:10.1038/onc.2010.609; activation in leptomeningeal cells of genetically engi- published online 17 January 2011 neered mice (GEM) is sufficient for meningioma development. Nf2 inactivation in leptomeningeal cells Keywords: neurofibromatosis type 2; arachnoid; brain of newborn Nf2 conditional knockout mice (Nf2flox2/flox2) tumours was accomplished by non-selective cellular targeting with intrathecal adenoviral Cre recombinase delivery (Kalamarides et al., 2002). Many of these mice devel- Introduction oped meningiomas, firmly establishing the critical role of the Nf2 gene in meningioma pathogenesis. However, Meningiomas account for approximately one-third of all several important questions remained unaddressed. primary central nervous system tumours and constitute First, it is unclear which cell type(s) during development the most common brain tumour in adults over 35 years and differentiation of the arachnoidal cell lineage of age. These leptomeningeal neoplasms usually represents the cellular target for Nf2 gene inactivation. Second, it is not known how Nf2 loss in these Correspondence: Current address: Dr M Giovannini, Center for leptomeningeal cells results in the development of the Neural Tumor Research, House Ear Institute, 2100W Third Street, distinct meningioma histological subtypes (Kros et al., Los Angeles, CA 90057, USA. 2001; Lee et al., 2006). Third, is there a specific time E-mail: [email protected] window during mouse development when Nf2 inactiva- 8Current address: Department of Thoracic Surgery, Medical tion results in meningioma formation? University of Vienna, Vienna, Austria Received 6 May 2010; revised 9 November 2010; accepted 27 November The purpose of this study was to generate a novel 2010; published online 17 January 2011 GEM strain to define the cell of origin of meningioma Heterogeneity of meningioma histological subtypes M Kalamarides et al 2334 and to explain the spectrum of histological subtypes. These are the first recognizable cells of the developing Herein, we identified the prostaglandin D2 synthase mesoderm-derived meningeal layer (Kamiryo et al., (PGDS) gene as a specific marker of arachnoidal cells of 1990). At E15.5, the extracellular space became enlarged rats, mice and human beings (Urade et al., 1993; around the brain, showing a reticular structure that Yamashima et al., 1997; Kawashima et al., 2001). We resembled the subarachnoid space (Figures 1e–g) leveraged this marker to develop a new transgenic Cre (McLone and Bondareff, 1975). At this stage of strain to target Nf2 inactivation to PGDS-expressing development, neural crest-derived undifferentiated cra- cells and showed that they are the meningioma cell of nial mesenchyme rostral to the Rathke’s pouch (tele- origin capable of giving rise to both fibroblastic and ncephalic meninges) showed no PGDS immunostaining meningothelial histological subtypes. Moreover, we (Figure 1e). Starting at E18.5, PGDS immunostaining show that biallelic Nf2 inactivation in PGDS ( þ ) progressed in a caudal to rostral direction along the meningeal progenitor cells must occur during a defined telencephalic meninges and was complete by postnatal developmental window, such that Nf2 inactivation in day 5 (PN5) (Figures 1d, h), when all arachnoidal cells PGDS ( þ ) meningeal cells after this period does not were PGDS ( þ ) irrespective of their embryological result in meningioma development. Finally, we used origin or location. In contrast, dura mater cells were several human microarray data sets to identify tran- negative for PGDS expression (Figure 1h). scripts differentially expressed in fibroblastic and Next, we characterized the pattern of PGDSCre meningiothelial meningioma subtypes, and validated a expression and activity using a LacZ reporter strain subset of these markers at the protein level in both (ACZL), in which the chicken b-actin promoter and human and mouse meningioma tumours. Collectively, loxP-flanked CAT gene are upstream of the LacZ gene these findings establish a PGDS ( þ ) meningeal cell as (Akagi et al., 1997). In the resulting PGDSCre;ACZL the cell of origin for the two major meningioma mice, meningeal progenitor cells and all their progeny histological subtypes, and define a susceptible develop- are identified by LacZ expression and positive X-gal mental window during which Nf2 inactivation leads to staining. We isolated embryos from these crosses and meningioma formation. scored the brain and spinal cord after staining the sections with X-gal. Between E15.5 and E17.0, the primitive interface zone between the dura mater (outer Results zone) and the arachnoid (inner zone) is formed (Angelov and Vasilev, 1989). At E18.5, blue cells were observed in PGDSCre is expressed at E12.5 in the mouse primordial both outer (dural border cells, DBCs) and inner (ABCs) meningeal cells that give rise to the multiple meningeal zones, whereas only the internal layer was positive for layers PGDS expression (Figures 2a and b). These findings In the adult arachnoid, PGDS is expressed by arachnoid indicate that both zones derive from PGDS ( þ ) barrier cells (ABCs), whereas its expression is negligible primordial meningeal cells. In PN3 pups, X-gal ( þ ) in arachnoid trabeculae and pia mater (Beuckmann cells were also found in the arachnoid at the skull base. et al., 2000). Similar to previous studies on human By PN5, PGDS ( þ ) cells were observed in the meningiomas (Kalamarides et al., 2008), we found that meningeal convexity, a structure that originates from both human and mouse meningiomas exhibit intense the neural crest (Le Lievre and Le Douarin, 1975) PGDS immunoreactivity (Supplementary Figure S1), (Figure 1h). In adult mice, arachnoidal cells were both suggesting that PGDS is a marker of normal and Cre immunopositive and X-gal positive. In addition, neoplastic arachnoidal cells. some oligodendrocytes and choroid plexus cells were To determine whether early Nf2 inactivation, before positive for both Cre and LacZ (Figures 2c, e and f). the separation of the primordial meninges into the three To test whether these PGDS ( þ ) meningeal convexity terminally differentiated layers, might result in menin- arachnoidal cells derive from the neural crest, we gioma formation in vivo, we generated mice in which
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