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Published in: Cancer Cell International 1/2018

Open Access 01-12-2018 | Primary research

In situ characterization of stem cells-like biomarkers in meningiomas

Authors: Hanin Alamir, Mona Alomari, Abdulla Ahmed A. Salwati, Mohamad Saka, Mohammed Bangash, Saleh Baeesa, Fahad Alghamdi, Angel Carracedo, Hans-Juergen Schulten, Adeel Chaudhary, Adel Abuzenadah, Deema Hussein

Published in: Cancer Cell International | Issue 1/2018

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Abstract

Background

Meningioma cancer stem cells (MCSCs) contribute to tumor aggressiveness and drug resistance. Successful therapies developed for inoperable, recurrent, or metastatic tumors must target these cells and restrict their contribution to tumor progression. Unfortunately, the identity of MCSCs remains elusive, and MSCSs’ in situ spatial distribution, heterogeneity, and relationship with tumor grade, remain unclear.

Methods

Seven tumors classified as grade II or grade III, including one case of metastatic grade III, and eight grade I meningioma tumors, were analyzed for combinations of ten stem cell (SC)-related markers using immunofluorescence of consecutive sections. The correlation of expression for all markers were investigated. Three dimensional spatial distribution of markers were qualitatively analyzed using a grid, designed as a repository of information for positive staining. All statistical analyses were completed using Statistical Analysis Software Package.

Results

The patterns of expression for SC-related markers were determined in the context of two dimensional distribution and cellular features. All markers could be detected in all tumors, however, Frizzled 9 and GFAP had differential expression in grade II/III compared with grade I meningioma tissues. Correlation analysis showed significant relationships between the expression of GFAP and CD133 as well as SSEA4 and Vimentin. Data from three dimensional analysis showed a complex distribution of SC markers, with increased gene hetero-expression being associated with grade II/III tumors. Sub regions that showed multiple co-staining of markers including CD133, Frizzled 9, GFAP, Vimentin, and SSEA4, but not necessarily the proliferation marker Ki67, were highly associated with grade II/III meningiomas.

Conclusion

The distribution and level of expression of CSCs markers in meningiomas are variable and show hetero-expression patterns that have a complex spatial nature, particularly in grade II/III meningiomas. Thus, results strongly support the notion of heterogeneous populations of CSCs, even in grade I meningiomas, and call for the use of multiple markers for the accurate identification of individual CSC subgroups. Such identification will lead to practical clinical diagnostic protocols that can quantitate CSCs, predict tumor recurrence, assist in guiding treatment selection for inoperable tumors, and improve follow up of therapy.
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Literature
1.
go back to reference Lym RL, Ostrom QT, Kruchko C, Couce M, Brat DJ, Louis DN, Barnholtz-Sloan JS. Completeness and concordancy of WHO grade assignment for brain and central nervous system tumors in the United States, 2004–2011. J Neurooncol. 2015;123(1):43–51.PubMedPubMedCentralCrossRef Lym RL, Ostrom QT, Kruchko C, Couce M, Brat DJ, Louis DN, Barnholtz-Sloan JS. Completeness and concordancy of WHO grade assignment for brain and central nervous system tumors in the United States, 2004–2011. J Neurooncol. 2015;123(1):43–51.PubMedPubMedCentralCrossRef
2.
go back to reference Khan I, Bangash M, Baeesa S, Jamal A, Carracedo A, Alghamdi F, Qashqari H, Abuzenadah A, AlQahtani M, Damanhouri G, et al. Epidemiological trends of histopathologically WHO classified CNS tumors in developing countries: systematic review. Asian Pac J Cancer Prev. 2015;16(1):205–16.PubMedCrossRef Khan I, Bangash M, Baeesa S, Jamal A, Carracedo A, Alghamdi F, Qashqari H, Abuzenadah A, AlQahtani M, Damanhouri G, et al. Epidemiological trends of histopathologically WHO classified CNS tumors in developing countries: systematic review. Asian Pac J Cancer Prev. 2015;16(1):205–16.PubMedCrossRef
3.
go back to reference Preusser M, Brastianos PK, Mawrin C. Advances in meningioma genetics: novel therapeutic opportunities. Nat Rev Neurol. 2018;14(2):106–15.PubMedCrossRef Preusser M, Brastianos PK, Mawrin C. Advances in meningioma genetics: novel therapeutic opportunities. Nat Rev Neurol. 2018;14(2):106–15.PubMedCrossRef
4.
go back to reference Brastianos PK, Horowitz PM, Santagata S, Jones RT, McKenna A, Getz G, Ligon KL, Palescandolo E, Van Hummelen P, Ducar MD, et al. Genomic sequencing of meningiomas identifies oncogenic SMO and AKT1 mutations. Nat Genet. 2013;45(3):285–9.PubMedPubMedCentralCrossRef Brastianos PK, Horowitz PM, Santagata S, Jones RT, McKenna A, Getz G, Ligon KL, Palescandolo E, Van Hummelen P, Ducar MD, et al. Genomic sequencing of meningiomas identifies oncogenic SMO and AKT1 mutations. Nat Genet. 2013;45(3):285–9.PubMedPubMedCentralCrossRef
5.
go back to reference Clark VE, Erson-Omay EZ, Serin A, Yin J, Cotney J, Ozduman K, Avsar T, Li J, Murray PB, Henegariu O, et al. Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science. 2013;339(6123):1077–80.PubMedPubMedCentralCrossRef Clark VE, Erson-Omay EZ, Serin A, Yin J, Cotney J, Ozduman K, Avsar T, Li J, Murray PB, Henegariu O, et al. Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science. 2013;339(6123):1077–80.PubMedPubMedCentralCrossRef
6.
go back to reference Abedalthagafi M, Bi WL, Aizer AA, Merrill PH, Brewster R, Agarwalla PK, Listewnik ML, Dias-Santagata D, Thorner AR, Van Hummelen P, et al. Oncogenic PI3K mutations are as common as AKT1 and SMO mutations in meningioma. Neuro Oncol. 2016;18(5):649–55.PubMedPubMedCentralCrossRef Abedalthagafi M, Bi WL, Aizer AA, Merrill PH, Brewster R, Agarwalla PK, Listewnik ML, Dias-Santagata D, Thorner AR, Van Hummelen P, et al. Oncogenic PI3K mutations are as common as AKT1 and SMO mutations in meningioma. Neuro Oncol. 2016;18(5):649–55.PubMedPubMedCentralCrossRef
8.
go back to reference Linsler S, Kraemer D, Driess C, Oertel J, Kammers K, Rahnenfuhrer J, Ketter R, Urbschat S. Molecular biological determinations of meningioma progression and recurrence. PLoS ONE. 2014;9(4):e94987.PubMedPubMedCentralCrossRef Linsler S, Kraemer D, Driess C, Oertel J, Kammers K, Rahnenfuhrer J, Ketter R, Urbschat S. Molecular biological determinations of meningioma progression and recurrence. PLoS ONE. 2014;9(4):e94987.PubMedPubMedCentralCrossRef
9.
go back to reference Shivapathasundram G, Wickremesekera AC, Tan ST, Itinteang T. Tumour stem cells in meningioma: a review. J Clin Neurosci. 2018;47:66–71.PubMedCrossRef Shivapathasundram G, Wickremesekera AC, Tan ST, Itinteang T. Tumour stem cells in meningioma: a review. J Clin Neurosci. 2018;47:66–71.PubMedCrossRef
10.
go back to reference Hu D, Wang X, Mao Y, Zhou L. Identification of CD105 (endoglin)-positive stem-like cells in rhabdoid meningioma. J Neurooncol. 2012;106(3):505–17.PubMedCrossRef Hu D, Wang X, Mao Y, Zhou L. Identification of CD105 (endoglin)-positive stem-like cells in rhabdoid meningioma. J Neurooncol. 2012;106(3):505–17.PubMedCrossRef
11.
go back to reference Lim HY, Kim KM, Kim BK, Shim JK, Lee JH, Huh YM, Kim SH, Kim EH, Park EK, Shim KW, et al. Isolation of mesenchymal stem-like cells in meningioma specimens. Int J Oncol. 2013;43(4):1260–8.PubMedCrossRef Lim HY, Kim KM, Kim BK, Shim JK, Lee JH, Huh YM, Kim SH, Kim EH, Park EK, Shim KW, et al. Isolation of mesenchymal stem-like cells in meningioma specimens. Int J Oncol. 2013;43(4):1260–8.PubMedCrossRef
12.
go back to reference Rath P, Miller DC, Litofsky NS, Anthony DC, Feng Q, Franklin C, Pei L, Free A, Liu J, Ren M, et al. Isolation and characterization of a population of stem-like progenitor cells from an atypical meningioma. Exp Mol Pathol. 2011;90(2):179–88.PubMedCrossRef Rath P, Miller DC, Litofsky NS, Anthony DC, Feng Q, Franklin C, Pei L, Free A, Liu J, Ren M, et al. Isolation and characterization of a population of stem-like progenitor cells from an atypical meningioma. Exp Mol Pathol. 2011;90(2):179–88.PubMedCrossRef
13.
go back to reference Tang H, Gong Y, Mao Y, Xie Q, Zheng M, Wang D, Zhu H, Wang X, Chen H, Chen X, et al. CD133-positive cells might be responsible for efficient proliferation of human meningioma cells. Int J Mol Sci. 2012;13(5):6424–39.PubMedPubMedCentralCrossRef Tang H, Gong Y, Mao Y, Xie Q, Zheng M, Wang D, Zhu H, Wang X, Chen H, Chen X, et al. CD133-positive cells might be responsible for efficient proliferation of human meningioma cells. Int J Mol Sci. 2012;13(5):6424–39.PubMedPubMedCentralCrossRef
14.
go back to reference Freitag D, McLean AL, Simon M, Koch A, Grube S, Walter J, Kalff R, Ewald C. NANOG overexpression and its correlation with stem cell and differentiation markers in meningiomas of different WHO grades. Mol Carcinog. 2017;56(8):1953–64.PubMedCrossRef Freitag D, McLean AL, Simon M, Koch A, Grube S, Walter J, Kalff R, Ewald C. NANOG overexpression and its correlation with stem cell and differentiation markers in meningiomas of different WHO grades. Mol Carcinog. 2017;56(8):1953–64.PubMedCrossRef
17.
go back to reference Taieb N, Maresca M, Guo XJ, Garmy N, Fantini J, Yahi N. The first extracellular domain of the tumour stem cell marker CD133 contains an antigenic ganglioside-binding motif. Cancer Lett. 2009;278(2):164–73.PubMedCrossRef Taieb N, Maresca M, Guo XJ, Garmy N, Fantini J, Yahi N. The first extracellular domain of the tumour stem cell marker CD133 contains an antigenic ganglioside-binding motif. Cancer Lett. 2009;278(2):164–73.PubMedCrossRef
18.
go back to reference Wu X, Wu F, Xu D, Zhang T. Prognostic significance of stem cell marker CD133 determined by promoter methylation but not by immunohistochemical expression in malignant gliomas. J Neurooncol. 2016;127(2):221–32.PubMedPubMedCentralCrossRef Wu X, Wu F, Xu D, Zhang T. Prognostic significance of stem cell marker CD133 determined by promoter methylation but not by immunohistochemical expression in malignant gliomas. J Neurooncol. 2016;127(2):221–32.PubMedPubMedCentralCrossRef
19.
go back to reference Yan X, Ma L, Yi D, Yoon JG, Diercks A, Foltz G, Price ND, Hood LE, Tian Q. A CD133-related gene expression signature identifies an aggressive glioblastoma subtype with excessive mutations. Proc Natl Acad Sci USA. 2011;108(4):1591–6.PubMedPubMedCentralCrossRef Yan X, Ma L, Yi D, Yoon JG, Diercks A, Foltz G, Price ND, Hood LE, Tian Q. A CD133-related gene expression signature identifies an aggressive glioblastoma subtype with excessive mutations. Proc Natl Acad Sci USA. 2011;108(4):1591–6.PubMedPubMedCentralCrossRef
20.
go back to reference Metellus P, Nanni-Metellus I, Delfino C, Colin C, Tchogandjian A, Coulibaly B, Fina F, Loundou A, Barrie M, Chinot O, et al. Prognostic impact of CD133 mRNA expression in 48 glioblastoma patients treated with concomitant radiochemotherapy: a prospective patient cohort at a single institution. Ann Surg Oncol. 2011;18(10):2937–45.PubMedCrossRef Metellus P, Nanni-Metellus I, Delfino C, Colin C, Tchogandjian A, Coulibaly B, Fina F, Loundou A, Barrie M, Chinot O, et al. Prognostic impact of CD133 mRNA expression in 48 glioblastoma patients treated with concomitant radiochemotherapy: a prospective patient cohort at a single institution. Ann Surg Oncol. 2011;18(10):2937–45.PubMedCrossRef
21.
go back to reference Wu B, Sun C, Feng F, Ge M, Xia L. Do relevant markers of cancer stem cells CD133 and Nestin indicate a poor prognosis in glioma patients? A systematic review and meta-analysis. J Exp Clin Cancer Res. 2015;34:44–55.PubMedPubMedCentralCrossRef Wu B, Sun C, Feng F, Ge M, Xia L. Do relevant markers of cancer stem cells CD133 and Nestin indicate a poor prognosis in glioma patients? A systematic review and meta-analysis. J Exp Clin Cancer Res. 2015;34:44–55.PubMedPubMedCentralCrossRef
22.
go back to reference Khan I, Baeesa S, Bangash M, Schulten HJ, Alghamdi F, Qashqari H, Madkhali N, Carracedo A, Saka M, Jamal A, et al. Pleomorphism and drug resistant cancer stem cells are characteristic of aggressive primary meningioma cell lines. Cancer Cell Int. 2017;17:72–85.PubMedPubMedCentralCrossRef Khan I, Baeesa S, Bangash M, Schulten HJ, Alghamdi F, Qashqari H, Madkhali N, Carracedo A, Saka M, Jamal A, et al. Pleomorphism and drug resistant cancer stem cells are characteristic of aggressive primary meningioma cell lines. Cancer Cell Int. 2017;17:72–85.PubMedPubMedCentralCrossRef
23.
go back to reference Prieto-Vila M, Takahashi RU, Usuba W, Kohama I, Ochiya T. Drug resistance driven by cancer stem cells and their niche. Int J Mol Sci. 2017;18(12):E2574.PubMedCrossRef Prieto-Vila M, Takahashi RU, Usuba W, Kohama I, Ochiya T. Drug resistance driven by cancer stem cells and their niche. Int J Mol Sci. 2017;18(12):E2574.PubMedCrossRef
24.
go back to reference Ishiwata T, Teduka K, Yamamoto T, Kawahara K, Matsuda Y, Naito Z. Neuroepithelial stem cell marker nestin regulates the migration, invasion and growth of human gliomas. Oncol Rep. 2011;26(1):91–9.PubMed Ishiwata T, Teduka K, Yamamoto T, Kawahara K, Matsuda Y, Naito Z. Neuroepithelial stem cell marker nestin regulates the migration, invasion and growth of human gliomas. Oncol Rep. 2011;26(1):91–9.PubMed
25.
go back to reference Liu J, Reeves C, Jacques T, McEvoy A, Miserocchi A, Thompson P, Sisodiya S, Thom M. Nestin-expressing cell types in the temporal lobe and hippocampus: morphology, differentiation, and proliferative capacity. Glia. 2018;66(1):62–77.PubMedCrossRef Liu J, Reeves C, Jacques T, McEvoy A, Miserocchi A, Thompson P, Sisodiya S, Thom M. Nestin-expressing cell types in the temporal lobe and hippocampus: morphology, differentiation, and proliferative capacity. Glia. 2018;66(1):62–77.PubMedCrossRef
27.
go back to reference Reimer R, Helmbold H, Szalay B, Hagel C, Hohenberg H, Deppert W, Bohn W. Nestin modulates glucocorticoid receptor function by cytoplasmic anchoring. PLoS ONE. 2009;4(6):e6084.PubMedPubMedCentralCrossRef Reimer R, Helmbold H, Szalay B, Hagel C, Hohenberg H, Deppert W, Bohn W. Nestin modulates glucocorticoid receptor function by cytoplasmic anchoring. PLoS ONE. 2009;4(6):e6084.PubMedPubMedCentralCrossRef
28.
go back to reference Galani V, Alexiou GA, Miliaras G, Dimitriadis E, Triantafyllou E, Galani A, Goussia A, Kanavaros P, Trangas T. Expression of stem cell marker nestin and microRNA-21 in meningiomas. Turk Neurosurg. 2015;25(4):574–7.PubMed Galani V, Alexiou GA, Miliaras G, Dimitriadis E, Triantafyllou E, Galani A, Goussia A, Kanavaros P, Trangas T. Expression of stem cell marker nestin and microRNA-21 in meningiomas. Turk Neurosurg. 2015;25(4):574–7.PubMed
30.
go back to reference Annovazzi L, Mellai M, Caldera V, Valente G, Schiffer D. SOX2 expression and amplification in gliomas and glioma cell lines. Cancer Genomics Proteomics. 2011;8(3):139–47.PubMed Annovazzi L, Mellai M, Caldera V, Valente G, Schiffer D. SOX2 expression and amplification in gliomas and glioma cell lines. Cancer Genomics Proteomics. 2011;8(3):139–47.PubMed
31.
go back to reference Alonso MM, Diez-Valle R, Manterola L, Rubio A, Liu D, Cortes-Santiago N, Urquiza L, Jauregi P, Lopez de Munain A, Sampron N, et al. Genetic and epigenetic modifications of Sox2 contribute to the invasive phenotype of malignant gliomas. PLoS ONE. 2011;6(11):e26740.PubMedPubMedCentralCrossRef Alonso MM, Diez-Valle R, Manterola L, Rubio A, Liu D, Cortes-Santiago N, Urquiza L, Jauregi P, Lopez de Munain A, Sampron N, et al. Genetic and epigenetic modifications of Sox2 contribute to the invasive phenotype of malignant gliomas. PLoS ONE. 2011;6(11):e26740.PubMedPubMedCentralCrossRef
32.
go back to reference Favaro R, Appolloni I, Pellegatta S, Sanga AB, Pagella P, Gambini E, Pisati F, Ottolenghi S, Foti M, Finocchiaro G, et al. Sox2 is required to maintain cancer stem cells in a mouse model of high-grade oligodendroglioma. Cancer Res. 2014;74(6):1833–44.PubMedCrossRef Favaro R, Appolloni I, Pellegatta S, Sanga AB, Pagella P, Gambini E, Pisati F, Ottolenghi S, Foti M, Finocchiaro G, et al. Sox2 is required to maintain cancer stem cells in a mouse model of high-grade oligodendroglioma. Cancer Res. 2014;74(6):1833–44.PubMedCrossRef
33.
go back to reference Gangemi RM, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P, Ravetti GL, Zona GL, Daga A, Corte G. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells. 2009;27(1):40–8.PubMedCrossRef Gangemi RM, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P, Ravetti GL, Zona GL, Daga A, Corte G. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells. 2009;27(1):40–8.PubMedCrossRef
34.
go back to reference Song WS, Yang YP, Huang CS, Lu KH, Liu WH, Wu WW, Lee YY, Lo WL, Lee SD, Chen YW, et al. Sox2, a stemness gene, regulates tumor-initiating and drug-resistant properties in CD133-positive glioblastoma stem cells. J Chin Med Assoc. 2016;79(10):538–45.PubMedCrossRef Song WS, Yang YP, Huang CS, Lu KH, Liu WH, Wu WW, Lee YY, Lo WL, Lee SD, Chen YW, et al. Sox2, a stemness gene, regulates tumor-initiating and drug-resistant properties in CD133-positive glioblastoma stem cells. J Chin Med Assoc. 2016;79(10):538–45.PubMedCrossRef
35.
go back to reference Simonetti M, Agarwal N, Stosser S, Bali KK, Karaulanov E, Kamble R, Pospisilova B, Kurejova M, Birchmeier W, Niehrs C, et al. Wnt-Fzd signaling sensitizes peripheral sensory neurons via distinct noncanonical pathways. Neuron. 2014;83(1):104–21.PubMedCrossRef Simonetti M, Agarwal N, Stosser S, Bali KK, Karaulanov E, Kamble R, Pospisilova B, Kurejova M, Birchmeier W, Niehrs C, et al. Wnt-Fzd signaling sensitizes peripheral sensory neurons via distinct noncanonical pathways. Neuron. 2014;83(1):104–21.PubMedCrossRef
36.
go back to reference Schenkelaars Q, Fierro-Constain L, Renard E, Hill AL, Borchiellini C. Insights into Frizzled evolution and new perspectives. Evol Dev. 2015;17(2):160–9.PubMedCrossRef Schenkelaars Q, Fierro-Constain L, Renard E, Hill AL, Borchiellini C. Insights into Frizzled evolution and new perspectives. Evol Dev. 2015;17(2):160–9.PubMedCrossRef
37.
go back to reference Pecina-Slaus N, Kafka A, Varosanec AM, Markovic L, Krsnik Z, Njiric N, Mrak G. Expression patterns of Wnt signaling component, secreted frizzledrelated protein 3 in astrocytoma and glioblastoma. Mol Med Rep. 2016;13(5):4245–51.PubMedPubMedCentralCrossRef Pecina-Slaus N, Kafka A, Varosanec AM, Markovic L, Krsnik Z, Njiric N, Mrak G. Expression patterns of Wnt signaling component, secreted frizzledrelated protein 3 in astrocytoma and glioblastoma. Mol Med Rep. 2016;13(5):4245–51.PubMedPubMedCentralCrossRef
38.
go back to reference Generoso SF, Giustiniano M, La Regina G, Bottone S, Passacantilli S, Di Maro S, Cassese H, Bruno A, Mallardo M, Dentice M, et al. Pharmacological folding chaperones act as allosteric ligands of Frizzled4. Nat Chem Biol. 2015;11(4):280–6.PubMedCrossRef Generoso SF, Giustiniano M, La Regina G, Bottone S, Passacantilli S, Di Maro S, Cassese H, Bruno A, Mallardo M, Dentice M, et al. Pharmacological folding chaperones act as allosteric ligands of Frizzled4. Nat Chem Biol. 2015;11(4):280–6.PubMedCrossRef
39.
go back to reference Tondeur S, Assou S, Nadal L, Hamamah S, De Vos J. Biology and potential of human embryonic stem cells. Ann Biol Clin (Paris). 2008;66(3):241–7.PubMed Tondeur S, Assou S, Nadal L, Hamamah S, De Vos J. Biology and potential of human embryonic stem cells. Ann Biol Clin (Paris). 2008;66(3):241–7.PubMed
40.
go back to reference Harichandan A, Sivasubramaniyan K, Hennenlotter J, Schwentner C, Stenzl A, Buhring HJ. Isolation of adult human spermatogonial progenitors using novel markers. J Mol Cell Biol. 2013;5(5):351–3.PubMedCrossRef Harichandan A, Sivasubramaniyan K, Hennenlotter J, Schwentner C, Stenzl A, Buhring HJ. Isolation of adult human spermatogonial progenitors using novel markers. J Mol Cell Biol. 2013;5(5):351–3.PubMedCrossRef
41.
go back to reference Virant-Klun I, Skutella T, Hren M, Gruden K, Cvjeticanin B, Vogler A, Sinkovec J. Isolation of small SSEA-4-positive putative stem cells from the ovarian surface epithelium of adult human ovaries by two different methods. Biomed Res Int. 2013;2013:690415.PubMedPubMedCentral Virant-Klun I, Skutella T, Hren M, Gruden K, Cvjeticanin B, Vogler A, Sinkovec J. Isolation of small SSEA-4-positive putative stem cells from the ovarian surface epithelium of adult human ovaries by two different methods. Biomed Res Int. 2013;2013:690415.PubMedPubMedCentral
42.
go back to reference Lou YW, Wang PY, Yeh SC, Chuang PK, Li ST, Wu CY, Khoo KH, Hsiao M, Hsu TL, Wong CH. Stage-specific embryonic antigen-4 as a potential therapeutic target in glioblastoma multiforme and other cancers. Proc Natl Acad Sci USA. 2014;111(7):2482–7.PubMedPubMedCentralCrossRef Lou YW, Wang PY, Yeh SC, Chuang PK, Li ST, Wu CY, Khoo KH, Hsiao M, Hsu TL, Wong CH. Stage-specific embryonic antigen-4 as a potential therapeutic target in glioblastoma multiforme and other cancers. Proc Natl Acad Sci USA. 2014;111(7):2482–7.PubMedPubMedCentralCrossRef
43.
go back to reference Noto Z, Yoshida T, Okabe M, Koike C, Fathy M, Tsuno H, Tomihara K, Arai N, Noguchi M, Nikaido T. CD44 and SSEA-4 positive cells in an oral cancer cell line HSC-4 possess cancer stem-like cell characteristics. Oral Oncol. 2013;49(8):787–95.PubMedCrossRef Noto Z, Yoshida T, Okabe M, Koike C, Fathy M, Tsuno H, Tomihara K, Arai N, Noguchi M, Nikaido T. CD44 and SSEA-4 positive cells in an oral cancer cell line HSC-4 possess cancer stem-like cell characteristics. Oral Oncol. 2013;49(8):787–95.PubMedCrossRef
44.
go back to reference Gottschling S, Jensen K, Warth A, Herth FJ, Thomas M, Schnabel PA, Herpel E. Stage-specific embryonic antigen-4 is expressed in basaloid lung cancer and associated with poor prognosis. Eur Respir J. 2013;41(3):656–63.PubMedCrossRef Gottschling S, Jensen K, Warth A, Herth FJ, Thomas M, Schnabel PA, Herpel E. Stage-specific embryonic antigen-4 is expressed in basaloid lung cancer and associated with poor prognosis. Eur Respir J. 2013;41(3):656–63.PubMedCrossRef
45.
go back to reference Kavitha CV, Jain AK, Agarwal C, Pierce A, Keating A, Huber KM, Serkova NJ, Wempe MF, Agarwal R, Deep G. Asiatic acid induces endoplasmic reticulum stress and apoptotic death in glioblastoma multiforme cells both in vitro and in vivo. Mol Carcinog. 2015;54(11):1417–29.PubMedCrossRef Kavitha CV, Jain AK, Agarwal C, Pierce A, Keating A, Huber KM, Serkova NJ, Wempe MF, Agarwal R, Deep G. Asiatic acid induces endoplasmic reticulum stress and apoptotic death in glioblastoma multiforme cells both in vitro and in vivo. Mol Carcinog. 2015;54(11):1417–29.PubMedCrossRef
46.
go back to reference Aloia A, Petrova E, Tomiuk S, Bissels U, Deas O, Saini M, Zickgraf FM, Wagner S, Spaich S, Sutterlin M, et al. The sialyl-glycolipid stage-specific embryonic antigen 4 marks a subpopulation of chemotherapy-resistant breast cancer cells with mesenchymal features. Breast Cancer Res. 2015;17(1):146–62.PubMedPubMedCentralCrossRef Aloia A, Petrova E, Tomiuk S, Bissels U, Deas O, Saini M, Zickgraf FM, Wagner S, Spaich S, Sutterlin M, et al. The sialyl-glycolipid stage-specific embryonic antigen 4 marks a subpopulation of chemotherapy-resistant breast cancer cells with mesenchymal features. Breast Cancer Res. 2015;17(1):146–62.PubMedPubMedCentralCrossRef
47.
go back to reference Sivasubramaniyan K, Harichandan A, Schilbach K, Mack AF, Bedke J, Stenzl A, Kanz L, Niederfellner G, Buhring HJ. Expression of stage-specific embryonic antigen-4 (SSEA-4) defines spontaneous loss of epithelial phenotype in human solid tumor cells. Glycobiology. 2015;25(8):902–17.PubMedPubMedCentralCrossRef Sivasubramaniyan K, Harichandan A, Schilbach K, Mack AF, Bedke J, Stenzl A, Kanz L, Niederfellner G, Buhring HJ. Expression of stage-specific embryonic antigen-4 (SSEA-4) defines spontaneous loss of epithelial phenotype in human solid tumor cells. Glycobiology. 2015;25(8):902–17.PubMedPubMedCentralCrossRef
48.
go back to reference Meijer DH, Kane MF, Mehta S, Liu H, Harrington E, Taylor CM, Stiles CD, Rowitch DH. Separated at birth? The functional and molecular divergence of OLIG1 and OLIG2. Nat Rev Neurosci. 2012;13(12):819–31.PubMedPubMedCentralCrossRef Meijer DH, Kane MF, Mehta S, Liu H, Harrington E, Taylor CM, Stiles CD, Rowitch DH. Separated at birth? The functional and molecular divergence of OLIG1 and OLIG2. Nat Rev Neurosci. 2012;13(12):819–31.PubMedPubMedCentralCrossRef
49.
50.
go back to reference Mateo JL, van den Berg DL, Haeussler M, Drechsel D, Gaber ZB, Castro DS, Robson P, Lu QR, Crawford GE, Flicek P, et al. Characterization of the neural stem cell gene regulatory network identifies OLIG2 as a multifunctional regulator of self-renewal. Genome Res. 2015;25(1):41–56.PubMedPubMedCentralCrossRef Mateo JL, van den Berg DL, Haeussler M, Drechsel D, Gaber ZB, Castro DS, Robson P, Lu QR, Crawford GE, Flicek P, et al. Characterization of the neural stem cell gene regulatory network identifies OLIG2 as a multifunctional regulator of self-renewal. Genome Res. 2015;25(1):41–56.PubMedPubMedCentralCrossRef
51.
go back to reference Motomura K, Natsume A, Watanabe R, Ito I, Kato Y, Momota H, Nishikawa R, Mishima K, Nakasu Y, Abe T, et al. Immunohistochemical analysis-based proteomic subclassification of newly diagnosed glioblastomas. Cancer Sci. 2012;103(10):1871–9.PubMedCrossRef Motomura K, Natsume A, Watanabe R, Ito I, Kato Y, Momota H, Nishikawa R, Mishima K, Nakasu Y, Abe T, et al. Immunohistochemical analysis-based proteomic subclassification of newly diagnosed glioblastomas. Cancer Sci. 2012;103(10):1871–9.PubMedCrossRef
52.
go back to reference Nevo I, Woolard K, Cam M, Li A, Webster JD, Kotliarov Y, Kim HS, Ahn S, Walling J, Kotliarova S, et al. Identification of molecular pathways facilitating glioma cell invasion in situ. PLoS ONE. 2014;9(11):e111783.PubMedPubMedCentralCrossRef Nevo I, Woolard K, Cam M, Li A, Webster JD, Kotliarov Y, Kim HS, Ahn S, Walling J, Kotliarova S, et al. Identification of molecular pathways facilitating glioma cell invasion in situ. PLoS ONE. 2014;9(11):e111783.PubMedPubMedCentralCrossRef
53.
go back to reference Matsumoto S, Banine F, Feistel K, Foster S, Xing R, Struve J, Sherman LS. Brg1 directly regulates Olig2 transcription and is required for oligodendrocyte progenitor cell specification. Dev Biol. 2016;413(2):173–87.PubMedPubMedCentralCrossRef Matsumoto S, Banine F, Feistel K, Foster S, Xing R, Struve J, Sherman LS. Brg1 directly regulates Olig2 transcription and is required for oligodendrocyte progenitor cell specification. Dev Biol. 2016;413(2):173–87.PubMedPubMedCentralCrossRef
54.
go back to reference Hol EM, Capetanaki Y. Type III intermediate filaments desmin, glial fibrillary acidic protein (GFAP), vimentin, and peripherin. Cold Spring Harb Perspect Biol. 2017;9(12):a021642.PubMedCrossRef Hol EM, Capetanaki Y. Type III intermediate filaments desmin, glial fibrillary acidic protein (GFAP), vimentin, and peripherin. Cold Spring Harb Perspect Biol. 2017;9(12):a021642.PubMedCrossRef
55.
go back to reference Bouamrani A, Ramus C, Gay E, Pelletier L, Cubizolles M, Brugiere S, Wion D, Berger F, Issartel JP. Increased phosphorylation of vimentin in noninfiltrative meningiomas. PLoS ONE. 2010;5(2):e9238.PubMedPubMedCentralCrossRef Bouamrani A, Ramus C, Gay E, Pelletier L, Cubizolles M, Brugiere S, Wion D, Berger F, Issartel JP. Increased phosphorylation of vimentin in noninfiltrative meningiomas. PLoS ONE. 2010;5(2):e9238.PubMedPubMedCentralCrossRef
56.
go back to reference van den Berge SA, Middeldorp J, Zhang CE, Curtis MA, Leonard BW, Mastroeni D, Voorn P, van de Berg WD, Huitinga I, Hol EM. Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP-delta. Aging Cell. 2010;9(3):313–26.PubMedCrossRef van den Berge SA, Middeldorp J, Zhang CE, Curtis MA, Leonard BW, Mastroeni D, Voorn P, van de Berg WD, Huitinga I, Hol EM. Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP-delta. Aging Cell. 2010;9(3):313–26.PubMedCrossRef
57.
go back to reference Brehar FM, Arsene D, Brinduse LA, Gorgan MR. Immunohistochemical analysis of GFAP-delta and nestin in cerebral astrocytomas. Brain Tumor Pathol. 2015;32(2):90–8.PubMedCrossRef Brehar FM, Arsene D, Brinduse LA, Gorgan MR. Immunohistochemical analysis of GFAP-delta and nestin in cerebral astrocytomas. Brain Tumor Pathol. 2015;32(2):90–8.PubMedCrossRef
58.
go back to reference Mariani M, Karki R, Spennato M, Pandya D, He S, Andreoli M, Fiedler P, Ferlini C. Class III beta-tubulin in normal and cancer tissues. Gene. 2015;563(2):109–14.PubMedCrossRef Mariani M, Karki R, Spennato M, Pandya D, He S, Andreoli M, Fiedler P, Ferlini C. Class III beta-tubulin in normal and cancer tissues. Gene. 2015;563(2):109–14.PubMedCrossRef
59.
go back to reference Max N, Hu C, Kreylos O, Crivelli S. BuildBeta–a system for automatically constructing beta sheets. Proteins. 2010;78(3):559–74.PubMed Max N, Hu C, Kreylos O, Crivelli S. BuildBeta–a system for automatically constructing beta sheets. Proteins. 2010;78(3):559–74.PubMed
60.
go back to reference Person F, Wilczak W, Hube-Magg C, Burdelski C, Moller-Koop C, Simon R, Noriega M, Sauter G, Steurer S, Burdak-Rothkamm S, et al. Prevalence of betaIII-tubulin (TUBB3) expression in human normal tissues and cancers. Tumour Biol. 2017;39(10):1010428317712166.PubMedCrossRef Person F, Wilczak W, Hube-Magg C, Burdelski C, Moller-Koop C, Simon R, Noriega M, Sauter G, Steurer S, Burdak-Rothkamm S, et al. Prevalence of betaIII-tubulin (TUBB3) expression in human normal tissues and cancers. Tumour Biol. 2017;39(10):1010428317712166.PubMedCrossRef
62.
go back to reference Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM, Wakimoto H, Cahill DP, Nahed BV, Curry WT, Martuza RL, et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science. 2014;344(6190):1396–401.PubMedPubMedCentralCrossRef Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM, Wakimoto H, Cahill DP, Nahed BV, Curry WT, Martuza RL, et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science. 2014;344(6190):1396–401.PubMedPubMedCentralCrossRef
63.
go back to reference Malta TM, Sokolov A, Gentles AJ, Burzykowski T, Poisson L, Weinstein JN, Kaminska B, Huelsken J, Omberg L, Gevaert O, et al. Machine learning identifies stemness features associated with oncogenic dedifferentiation. Cell. 2018;173(2):338–54.PubMedCrossRef Malta TM, Sokolov A, Gentles AJ, Burzykowski T, Poisson L, Weinstein JN, Kaminska B, Huelsken J, Omberg L, Gevaert O, et al. Machine learning identifies stemness features associated with oncogenic dedifferentiation. Cell. 2018;173(2):338–54.PubMedCrossRef
64.
go back to reference Schulten HJ, Hussein D, Al-Adwani F, Karim S, Al-Maghrabi J, Al-Sharif M, Jamal A, Al-Ghamdi F, Baeesa SS, Bangash M, et al. Microarray expression data identify DCC as a candidate gene for early meningioma progression. PLoS ONE. 2016;11(4):e0153681.PubMedPubMedCentralCrossRef Schulten HJ, Hussein D, Al-Adwani F, Karim S, Al-Maghrabi J, Al-Sharif M, Jamal A, Al-Ghamdi F, Baeesa SS, Bangash M, et al. Microarray expression data identify DCC as a candidate gene for early meningioma progression. PLoS ONE. 2016;11(4):e0153681.PubMedPubMedCentralCrossRef
65.
go back to reference Schulten HJ, Bangash M, Karim S, Dallol A, Hussein D, Merdad A, Al-Thoubaity FK, Al-Maghrabi J, Jamal A, Al-Ghamdi F, et al. Comprehensive molecular biomarker identification in breast cancer brain metastases. J Transl Med. 2017;15(1):269–88.PubMedPubMedCentralCrossRef Schulten HJ, Bangash M, Karim S, Dallol A, Hussein D, Merdad A, Al-Thoubaity FK, Al-Maghrabi J, Jamal A, Al-Ghamdi F, et al. Comprehensive molecular biomarker identification in breast cancer brain metastases. J Transl Med. 2017;15(1):269–88.PubMedPubMedCentralCrossRef
66.
go back to reference Bailey MH, Tokheim C, Porta-Pardo E, Sengupta S, Bertrand D, Weerasinghe A, Colaprico A, Wendl MC, Kim J, Reardon B, et al. Comprehensive characterization of cancer driver genes and mutations. Cell. 2018;173(2):371–85.PubMedCrossRef Bailey MH, Tokheim C, Porta-Pardo E, Sengupta S, Bertrand D, Weerasinghe A, Colaprico A, Wendl MC, Kim J, Reardon B, et al. Comprehensive characterization of cancer driver genes and mutations. Cell. 2018;173(2):371–85.PubMedCrossRef
67.
go back to reference Zhang M, Song T, Yang L, Chen R, Wu L, Yang Z, Fang J. Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients. J Exp Clin Cancer Res. 2008;27:85–91.PubMedPubMedCentralCrossRef Zhang M, Song T, Yang L, Chen R, Wu L, Yang Z, Fang J. Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients. J Exp Clin Cancer Res. 2008;27:85–91.PubMedPubMedCentralCrossRef
68.
go back to reference Wang B, Li M, Wu Z, Li X, Li YU, Shi X, Cheng W. Associations between SOX2 and miR-200b expression with the clinicopathological characteristics and prognosis of patients with glioma. Exp Ther Med. 2015;10(1):88–96.PubMedPubMedCentralCrossRef Wang B, Li M, Wu Z, Li X, Li YU, Shi X, Cheng W. Associations between SOX2 and miR-200b expression with the clinicopathological characteristics and prognosis of patients with glioma. Exp Ther Med. 2015;10(1):88–96.PubMedPubMedCentralCrossRef
69.
go back to reference Pavelin S, Becic K, Forempoher G, Mrklic I, Pogorelic Z, Titlic M, Andelinovic S. Expression of Ki-67 and p53 in meningiomas. Neoplasma. 2013;60(5):480–5.PubMedCrossRef Pavelin S, Becic K, Forempoher G, Mrklic I, Pogorelic Z, Titlic M, Andelinovic S. Expression of Ki-67 and p53 in meningiomas. Neoplasma. 2013;60(5):480–5.PubMedCrossRef
70.
71.
go back to reference Shah SM, Kang YJ, Christensen BL, Feng AS, Kollmar R. Expression of Wnt receptors in adult spiral ganglion neurons: frizzled 9 localization at growth cones of regenerating neurites. Neuroscience. 2009;164(2):478–87.PubMedPubMedCentralCrossRef Shah SM, Kang YJ, Christensen BL, Feng AS, Kollmar R. Expression of Wnt receptors in adult spiral ganglion neurons: frizzled 9 localization at growth cones of regenerating neurites. Neuroscience. 2009;164(2):478–87.PubMedPubMedCentralCrossRef
72.
go back to reference Otero JJ, Rowitch D, Vandenberg S. OLIG2 is differentially expressed in pediatric astrocytic and in ependymal neoplasms. J Neurooncol. 2011;104(2):423–38.PubMedCrossRef Otero JJ, Rowitch D, Vandenberg S. OLIG2 is differentially expressed in pediatric astrocytic and in ependymal neoplasms. J Neurooncol. 2011;104(2):423–38.PubMedCrossRef
73.
go back to reference Roque DM, Buza N, Glasgow M, Bellone S, Bortolomai I, Gasparrini S, Cocco E, Ratner E, Silasi DA, Azodi M, et al. Class III beta-tubulin overexpression within the tumor microenvironment is a prognostic biomarker for poor overall survival in ovarian cancer patients treated with neoadjuvant carboplatin/paclitaxel. Clin Exp Metastasis. 2014;31(1):101–10.PubMedCrossRef Roque DM, Buza N, Glasgow M, Bellone S, Bortolomai I, Gasparrini S, Cocco E, Ratner E, Silasi DA, Azodi M, et al. Class III beta-tubulin overexpression within the tumor microenvironment is a prognostic biomarker for poor overall survival in ovarian cancer patients treated with neoadjuvant carboplatin/paclitaxel. Clin Exp Metastasis. 2014;31(1):101–10.PubMedCrossRef
74.
go back to reference Yu Y, Chen Y, Kim B, Wang H, Zhao C, He X, Liu L, Liu W, Wu LM, Mao M, et al. Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell. 2013;152(1–2):248–61.PubMedPubMedCentralCrossRef Yu Y, Chen Y, Kim B, Wang H, Zhao C, He X, Liu L, Liu W, Wu LM, Mao M, et al. Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell. 2013;152(1–2):248–61.PubMedPubMedCentralCrossRef
75.
go back to reference Boulagnon-Rombi C, Fleury C, Fichel C, Lefour S, Marchal Bressenot A, Gauchotte G. Immunohistochemical approach to the differential diagnosis of meningiomas and their mimics. J Neuropathol Exp Neurol. 2017;76(4):289–98.PubMedCrossRef Boulagnon-Rombi C, Fleury C, Fichel C, Lefour S, Marchal Bressenot A, Gauchotte G. Immunohistochemical approach to the differential diagnosis of meningiomas and their mimics. J Neuropathol Exp Neurol. 2017;76(4):289–98.PubMedCrossRef
76.
go back to reference Hermansen SK, Christensen KG, Jensen SS, Kristensen BW. Inconsistent immunohistochemical expression patterns of four different CD133 antibody clones in glioblastoma. J Histochem Cytochem. 2011;59(4):391–407.PubMedPubMedCentralCrossRef Hermansen SK, Christensen KG, Jensen SS, Kristensen BW. Inconsistent immunohistochemical expression patterns of four different CD133 antibody clones in glioblastoma. J Histochem Cytochem. 2011;59(4):391–407.PubMedPubMedCentralCrossRef
77.
go back to reference Albayrak BS, Ismailoglu O, Tanriover G, Cetinalp EN, Demir N. The double immunostaining of CD133 and Ki-67 favours a significant co-localization pattern in fibroblastic subtype of meningiomas. Neurol Neurochir Pol. 2011;45(5):467–73.PubMed Albayrak BS, Ismailoglu O, Tanriover G, Cetinalp EN, Demir N. The double immunostaining of CD133 and Ki-67 favours a significant co-localization pattern in fibroblastic subtype of meningiomas. Neurol Neurochir Pol. 2011;45(5):467–73.PubMed
78.
go back to reference Petricevic J, Forempoher G, Ostojic L, Mardesic-Brakus S, Andjelinovic S, Vukojevic K, Saraga-Babic M. Expression of nestin, mesothelin and epithelial membrane antigen (EMA) in developing and adult human meninges and meningiomas. Acta Histochem. 2011;113(7):703–11.PubMedCrossRef Petricevic J, Forempoher G, Ostojic L, Mardesic-Brakus S, Andjelinovic S, Vukojevic K, Saraga-Babic M. Expression of nestin, mesothelin and epithelial membrane antigen (EMA) in developing and adult human meninges and meningiomas. Acta Histochem. 2011;113(7):703–11.PubMedCrossRef
79.
go back to reference Brown DV, Filiz G, Daniel PM, Hollande F, Dworkin S, Amiridis S, Kountouri N, Ng W, Morokoff AP, Mantamadiotis T. Expression of CD133 and CD44 in glioblastoma stem cells correlates with cell proliferation, phenotype stability and intra-tumor heterogeneity. PLoS ONE. 2017;12(2):e0172791.PubMedPubMedCentralCrossRef Brown DV, Filiz G, Daniel PM, Hollande F, Dworkin S, Amiridis S, Kountouri N, Ng W, Morokoff AP, Mantamadiotis T. Expression of CD133 and CD44 in glioblastoma stem cells correlates with cell proliferation, phenotype stability and intra-tumor heterogeneity. PLoS ONE. 2017;12(2):e0172791.PubMedPubMedCentralCrossRef
80.
go back to reference Liu Y, Shi J, Chen M, Cao YF, Liu YW, Pan J, Qi ST. Periostin: a novel prognostic predictor for meningiomas. J Neurooncol. 2015;121(3):505–12.PubMedCrossRef Liu Y, Shi J, Chen M, Cao YF, Liu YW, Pan J, Qi ST. Periostin: a novel prognostic predictor for meningiomas. J Neurooncol. 2015;121(3):505–12.PubMedCrossRef
81.
go back to reference Gerdes MJ, Gökmen-Polar Y, Sui Y, Pang AS, LaPlante N, Harris AL, Tan P-H, Ginty F, Badve SS. Single-cell heterogeneity in ductal carcinoma in situ of breast. Mod Pathol. 2017;31(3):406–17.PubMedCrossRefPubMedCentral Gerdes MJ, Gökmen-Polar Y, Sui Y, Pang AS, LaPlante N, Harris AL, Tan P-H, Ginty F, Badve SS. Single-cell heterogeneity in ductal carcinoma in situ of breast. Mod Pathol. 2017;31(3):406–17.PubMedCrossRefPubMedCentral
82.
go back to reference Huang L, Liang J, Geng Y, Tsang WM, Yao X, Jhanji V, Zhang M, Cheung HS, Pang CP, Yam GH. Directing adult human periodontal ligament-derived stem cells to retinal fate. Invest Ophthalmol Vis Sci. 2013;54(6):3965–74.PubMedCrossRef Huang L, Liang J, Geng Y, Tsang WM, Yao X, Jhanji V, Zhang M, Cheung HS, Pang CP, Yam GH. Directing adult human periodontal ligament-derived stem cells to retinal fate. Invest Ophthalmol Vis Sci. 2013;54(6):3965–74.PubMedCrossRef
83.
go back to reference Phi JH, Park SH, Chung CK, Wang KC, Cho BK, Kim SK. Atypical cell clusters expressing both neuronal and oligodendrocytic markers: novel histological pattern of glioneuronal tumors? Pathol Int. 2009;59(10):735–43.PubMedCrossRef Phi JH, Park SH, Chung CK, Wang KC, Cho BK, Kim SK. Atypical cell clusters expressing both neuronal and oligodendrocytic markers: novel histological pattern of glioneuronal tumors? Pathol Int. 2009;59(10):735–43.PubMedCrossRef
84.
go back to reference Rieske P, Golanska E, Zakrzewska M, Piaskowski S, Hulas-Bigoszewska K, Wolanczyk M, Szybka M, Witusik-Perkowska M, Jaskolski DJ, Zakrzewski K, et al. Arrested neural and advanced mesenchymal differentiation of glioblastoma cells-comparative study with neural progenitors. BMC Cancer. 2009;9:54–68.PubMedPubMedCentralCrossRef Rieske P, Golanska E, Zakrzewska M, Piaskowski S, Hulas-Bigoszewska K, Wolanczyk M, Szybka M, Witusik-Perkowska M, Jaskolski DJ, Zakrzewski K, et al. Arrested neural and advanced mesenchymal differentiation of glioblastoma cells-comparative study with neural progenitors. BMC Cancer. 2009;9:54–68.PubMedPubMedCentralCrossRef
85.
go back to reference Mamber C, Kozareva DA, Kamphuis W, Hol EM. Shades of gray: the delineation of marker expression within the adult rodent subventricular zone. Prog Neurobiol. 2013;111:1–16.PubMedCrossRef Mamber C, Kozareva DA, Kamphuis W, Hol EM. Shades of gray: the delineation of marker expression within the adult rodent subventricular zone. Prog Neurobiol. 2013;111:1–16.PubMedCrossRef
86.
go back to reference Platel JC, Bordey A. The multifaceted subventricular zone astrocyte: from a metabolic and pro-neurogenic role to acting as a neural stem cell. Neuroscience. 2016;323:20–8.PubMedCrossRef Platel JC, Bordey A. The multifaceted subventricular zone astrocyte: from a metabolic and pro-neurogenic role to acting as a neural stem cell. Neuroscience. 2016;323:20–8.PubMedCrossRef
87.
go back to reference Shaikh A, Nagvenkar P, Pethe P, Hinduja I, Bhartiya D. Molecular and phenotypic characterization of CD133 and SSEA4 enriched very small embryonic-like stem cells in human cord blood. Leukemia. 2015;29(9):1909–17.PubMedCrossRef Shaikh A, Nagvenkar P, Pethe P, Hinduja I, Bhartiya D. Molecular and phenotypic characterization of CD133 and SSEA4 enriched very small embryonic-like stem cells in human cord blood. Leukemia. 2015;29(9):1909–17.PubMedCrossRef
88.
go back to reference Matsuoka Y, Nakatsuka R, Sumide K, Kawamura H, Takahashi M, Fujioka T, Uemura Y, Asano H, Sasaki Y, Inoue M, et al. Prospectively isolated human bone marrow cell-derived MSCs support primitive human CD34-negative hematopoietic stem cells. Stem Cells. 2015;33(5):1554–65.PubMedCrossRef Matsuoka Y, Nakatsuka R, Sumide K, Kawamura H, Takahashi M, Fujioka T, Uemura Y, Asano H, Sasaki Y, Inoue M, et al. Prospectively isolated human bone marrow cell-derived MSCs support primitive human CD34-negative hematopoietic stem cells. Stem Cells. 2015;33(5):1554–65.PubMedCrossRef
89.
go back to reference Chailangkarn T, Trujillo CA, Freitas BC, Hrvoj-Mihic B, Herai RH, Yu DX, Brown TT, Marchetto MC, Bardy C, McHenry L, et al. A human neurodevelopmental model for Williams syndrome. Nature. 2016;536(7616):338–43.PubMedPubMedCentralCrossRef Chailangkarn T, Trujillo CA, Freitas BC, Hrvoj-Mihic B, Herai RH, Yu DX, Brown TT, Marchetto MC, Bardy C, McHenry L, et al. A human neurodevelopmental model for Williams syndrome. Nature. 2016;536(7616):338–43.PubMedPubMedCentralCrossRef
90.
go back to reference Du J, Li B, Fang Y, Liu Y, Wang Y, Li J, Zhou W, Wang X. Overexpression of class III beta-tubulin, Sox2, and nuclear Survivin is predictive of taxane resistance in patients with stage III ovarian epithelial cancer. BMC Cancer. 2015;15:536–46.PubMedPubMedCentralCrossRef Du J, Li B, Fang Y, Liu Y, Wang Y, Li J, Zhou W, Wang X. Overexpression of class III beta-tubulin, Sox2, and nuclear Survivin is predictive of taxane resistance in patients with stage III ovarian epithelial cancer. BMC Cancer. 2015;15:536–46.PubMedPubMedCentralCrossRef
91.
go back to reference Qu J, Rizak JD, Fan Y, Guo X, Li J, Huma T, Ma Y. Establishment and partial characterization of a human tumor cell line, GBM-HSF, from a glioblastoma multiforme. Hum Cell. 2014;27(3):129–36.PubMedCrossRef Qu J, Rizak JD, Fan Y, Guo X, Li J, Huma T, Ma Y. Establishment and partial characterization of a human tumor cell line, GBM-HSF, from a glioblastoma multiforme. Hum Cell. 2014;27(3):129–36.PubMedCrossRef
92.
go back to reference Hsieh JJ, Manley BJ, Khan N, Gao J, Carlo MI, Cheng EH. Overcome tumor heterogeneity-imposed therapeutic barriers through convergent genomic biomarker discovery: a braided cancer river model of kidney cancer. Semin Cell Dev Biol. 2017;64:98–106.PubMedCrossRef Hsieh JJ, Manley BJ, Khan N, Gao J, Carlo MI, Cheng EH. Overcome tumor heterogeneity-imposed therapeutic barriers through convergent genomic biomarker discovery: a braided cancer river model of kidney cancer. Semin Cell Dev Biol. 2017;64:98–106.PubMedCrossRef
93.
go back to reference Azar S, Leventoux N, Ripoll C, Rigau V, Goze C, Lorcy F, Bauchet L, Duffau H, Guichet PO, Rothhut B, et al. Cellular and molecular characterization of IDH1-mutated diffuse low grade gliomas reveals tumor heterogeneity and absence of EGFR/PDGFRalpha activation. Glia. 2018;66(2):239–55.PubMedCrossRef Azar S, Leventoux N, Ripoll C, Rigau V, Goze C, Lorcy F, Bauchet L, Duffau H, Guichet PO, Rothhut B, et al. Cellular and molecular characterization of IDH1-mutated diffuse low grade gliomas reveals tumor heterogeneity and absence of EGFR/PDGFRalpha activation. Glia. 2018;66(2):239–55.PubMedCrossRef
94.
go back to reference Irvin DM, McNeill RS, Bash RE, Miller CR. Intrinsic astrocyte heterogeneity influences tumor growth in glioma mouse models. Brain Pathol. 2017;27(1):36–50.PubMedCrossRef Irvin DM, McNeill RS, Bash RE, Miller CR. Intrinsic astrocyte heterogeneity influences tumor growth in glioma mouse models. Brain Pathol. 2017;27(1):36–50.PubMedCrossRef
95.
go back to reference McGranahan N, Swanton C. Clonal heterogeneity and tumor evolution: past, present, and the future. Cell. 2017;168(4):613–28.PubMedCrossRef McGranahan N, Swanton C. Clonal heterogeneity and tumor evolution: past, present, and the future. Cell. 2017;168(4):613–28.PubMedCrossRef
96.
go back to reference Welker AM, Jaros BD, An M, Beattie CE. Changes in tumor cell heterogeneity after chemotherapy treatment in a xenograft model of glioblastoma. Neuroscience. 2017;356:35–43.PubMedCrossRefPubMedCentral Welker AM, Jaros BD, An M, Beattie CE. Changes in tumor cell heterogeneity after chemotherapy treatment in a xenograft model of glioblastoma. Neuroscience. 2017;356:35–43.PubMedCrossRefPubMedCentral
97.
go back to reference Rosenberg S, Verreault M, Schmitt C, Guegan J, Guehennec J, Levasseur C, Marie Y, Bielle F, Mokhtari K, Hoang-Xuan K, et al. Multi-omics analysis of primary glioblastoma cell lines shows recapitulation of pivotal molecular features of parental tumors. Neuro Oncol. 2017;19(2):219–28.PubMed Rosenberg S, Verreault M, Schmitt C, Guegan J, Guehennec J, Levasseur C, Marie Y, Bielle F, Mokhtari K, Hoang-Xuan K, et al. Multi-omics analysis of primary glioblastoma cell lines shows recapitulation of pivotal molecular features of parental tumors. Neuro Oncol. 2017;19(2):219–28.PubMed
98.
go back to reference Bolognesi MM, Manzoni M, Scalia CR, Zannella S, Bosisio FM, Faretta M, Cattoretti G. Multiplex staining by sequential immunostaining and antibody removal on routine tissue sections. J Histochem Cytochem. 2017;65(8):431–44.PubMedCrossRefPubMedCentral Bolognesi MM, Manzoni M, Scalia CR, Zannella S, Bosisio FM, Faretta M, Cattoretti G. Multiplex staining by sequential immunostaining and antibody removal on routine tissue sections. J Histochem Cytochem. 2017;65(8):431–44.PubMedCrossRefPubMedCentral
99.
go back to reference Simmons AJ, Lau KS. Deciphering tumor heterogeneity from FFPE tissues: its promise and challenges. Mol Cell Oncol. 2017;4(1):e1260191.PubMedCrossRef Simmons AJ, Lau KS. Deciphering tumor heterogeneity from FFPE tissues: its promise and challenges. Mol Cell Oncol. 2017;4(1):e1260191.PubMedCrossRef
101.
go back to reference Correnti M, Raggi C. Stem-like plasticity and heterogeneity of circulating tumor cells: current status and prospect challenges in liver cancer. Oncotarget. 2017;8(4):7094–115.PubMedCrossRef Correnti M, Raggi C. Stem-like plasticity and heterogeneity of circulating tumor cells: current status and prospect challenges in liver cancer. Oncotarget. 2017;8(4):7094–115.PubMedCrossRef
Metadata
Title
In situ characterization of stem cells-like biomarkers in meningiomas
Authors
Hanin Alamir
Mona Alomari
Abdulla Ahmed A. Salwati
Mohamad Saka
Mohammed Bangash
Saleh Baeesa
Fahad Alghamdi
Angel Carracedo
Hans-Juergen Schulten
Adeel Chaudhary
Adel Abuzenadah
Deema Hussein
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2018
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-018-0571-6

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