Skip to main content
Top
Published in: Journal of Neuro-Oncology 1/2011

01-08-2011 | Laboratory Investigation - Human/Animal Tissue

Isolation and characterization of tumor stem-like cells from human meningiomas

Published in: Journal of Neuro-Oncology | Issue 1/2011

Login to get access

Abstract

Recent advances in research have found that tumor stem-like cells are resistant to surgery, radiotherapy, and chemotherapy. Tumor stem-like cells play critical roles in tumor recurrence, angiogenesis, and invasion in malignant brain tumors. However, the identification of tumor stem-like cells in meningiomas has not been clarified. In this study, we identified the stem-like features of sphere-forming cells in human meningiomas. The results showed that meningioma stem-like cells possess the ability to form spheres in identical stem cell culture condition. These meningioma sphere cells (MgSCs) expressed progenitor cell marker, CD133, but not differentiated cell marker, epithelial membrane antigen (EMA) on immunofluorescence staining. Importantly, the mRNA expression of ABCG, and CD133 was higher in MgSCs than daughter meningioma adherent cells (MgACs). In addition, cells displayed chemotherapeutic resistance to vincristine more in MgSCs than MgACs. This phenomenon was also found in single cell form from dissociated spheres than MgACs. Moreover, MgSCs are more resistant to irradiation treatment than MgACs. Furthermore, MgSCs revealed high tumorigenicity in vivo following orthotopic inoculation into the brains of immunodeficient mice. The corresponding immunohistochemical (IHC) staining found that MgSCs are positive for EMA, vimentin, and CD133, consistent with IHC of primary human meningiomas. These findings have provided better understanding of meningioma cell biology and suggested that meningioma stem-like cells may serve as a novel target in therapeutic resistant meningiomas.
Literature
1.
go back to reference Marosi C, Hassler M, Roessler K, Reni M, Sant M, Mazza E, Vecht C (2008) Meningioma. Crit Rev Oncol Hematol 67:153–171PubMedCrossRef Marosi C, Hassler M, Roessler K, Reni M, Sant M, Mazza E, Vecht C (2008) Meningioma. Crit Rev Oncol Hematol 67:153–171PubMedCrossRef
2.
go back to reference Perez-Bacete MJ, Cerda-Nicolas M, Piquer J, Peydro-Olaya A (1989) Differential immunohistochemical characteristics of meningiomas and other neoplasms of the central nervous system. Arch Neurobiol (Madr) 52:265–272 Perez-Bacete MJ, Cerda-Nicolas M, Piquer J, Peydro-Olaya A (1989) Differential immunohistochemical characteristics of meningiomas and other neoplasms of the central nervous system. Arch Neurobiol (Madr) 52:265–272
3.
go back to reference Meis JM, Ordonez NG, Bruner JM (1986) Meningiomas. An immunohistochemical study of 50 cases. Arch Pathol Lab Med 110:934–937PubMed Meis JM, Ordonez NG, Bruner JM (1986) Meningiomas. An immunohistochemical study of 50 cases. Arch Pathol Lab Med 110:934–937PubMed
4.
go back to reference Barresi V, Cerasoli S, Vitarelli E, Tuccari G (2007) Density of microvessels positive for CD105 (endoglin) is related to prognosis in meningiomas. Acta Neuropathol 114:147–156PubMedCrossRef Barresi V, Cerasoli S, Vitarelli E, Tuccari G (2007) Density of microvessels positive for CD105 (endoglin) is related to prognosis in meningiomas. Acta Neuropathol 114:147–156PubMedCrossRef
5.
go back to reference Aghi MK, Carter BS, Cosgrove GR, Ojemann RG, Amin-Hanjani S, Martuza RL, Curry WT Jr, Barker FG II (2009) Long-term recurrence rates of atypical meningiomas after gross total resection with or without postoperative adjuvant radiation. Neurosurgery 64:56–60 (discussion 60)PubMedCrossRef Aghi MK, Carter BS, Cosgrove GR, Ojemann RG, Amin-Hanjani S, Martuza RL, Curry WT Jr, Barker FG II (2009) Long-term recurrence rates of atypical meningiomas after gross total resection with or without postoperative adjuvant radiation. Neurosurgery 64:56–60 (discussion 60)PubMedCrossRef
6.
go back to reference Yoo-Jin K, Kim Y, Bochem N, Ketter R, Henn W, Feiden W (2008) Meningiomas: multiparametric approach for risk stratification and grading. Pathologe 29:428–433PubMedCrossRef Yoo-Jin K, Kim Y, Bochem N, Ketter R, Henn W, Feiden W (2008) Meningiomas: multiparametric approach for risk stratification and grading. Pathologe 29:428–433PubMedCrossRef
7.
go back to reference Tseng KY, Chung MH, Sytwu HK, Lee HM, Chen KY, Chang C, Lin CK, Yen CH, Chen JH, Lin GJ, Ma HI, Yeh YS, Ju DT, Liu MY, Hueng DY (2010) Osteopontin expression is a valuable marker for prediction of short-term recurrence in WHO grade I benign meningiomas. J Neurooncol 100:217–223. doi:10.1007/s11060-010-0164-2 PubMedCrossRef Tseng KY, Chung MH, Sytwu HK, Lee HM, Chen KY, Chang C, Lin CK, Yen CH, Chen JH, Lin GJ, Ma HI, Yeh YS, Ju DT, Liu MY, Hueng DY (2010) Osteopontin expression is a valuable marker for prediction of short-term recurrence in WHO grade I benign meningiomas. J Neurooncol 100:217–223. doi:10.​1007/​s11060-010-0164-2 PubMedCrossRef
8.
go back to reference Kunishio K, Kobayashi K, Kagawa M, Makabe T, Matsumoto A, Matsumoto Y (2007) A case of malignant meningioma treated by individual adjuvant chemotherapy based on the mRNA expression of drug-resistance gene. Gan To Kagaku Ryoho 34:265–268PubMed Kunishio K, Kobayashi K, Kagawa M, Makabe T, Matsumoto A, Matsumoto Y (2007) A case of malignant meningioma treated by individual adjuvant chemotherapy based on the mRNA expression of drug-resistance gene. Gan To Kagaku Ryoho 34:265–268PubMed
9.
go back to reference Demeule M, Shedid D, Beaulieu E, Del Maestro RF, Moghrabi A, Ghosn PB, Moumdjian R, Berthelet F, Beliveau R (2001) Expression of multidrug-resistance P-glycoprotein (MDR1) in human brain tumors. Int J Cancer 93:62–66. doi:10.1002/ijc.1306[pii] PubMedCrossRef Demeule M, Shedid D, Beaulieu E, Del Maestro RF, Moghrabi A, Ghosn PB, Moumdjian R, Berthelet F, Beliveau R (2001) Expression of multidrug-resistance P-glycoprotein (MDR1) in human brain tumors. Int J Cancer 93:62–66. doi:10.​1002/​ijc.​1306[pii] PubMedCrossRef
11.
go back to reference Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H, Sorrentino BP (2001) The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 7:1028–1034PubMedCrossRef Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H, Sorrentino BP (2001) The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 7:1028–1034PubMedCrossRef
12.
go back to reference Zabierowski SE, Herlyn M (2008) Learning the ABCs of melanoma-initiating cells. Cancer Cell 13:185–187PubMedCrossRef Zabierowski SE, Herlyn M (2008) Learning the ABCs of melanoma-initiating cells. Cancer Cell 13:185–187PubMedCrossRef
13.
go back to reference Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, Nephew KP (2008) Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 68:4311–4320PubMedCrossRef Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, Nephew KP (2008) Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 68:4311–4320PubMedCrossRef
14.
go back to reference Capper D, Gaiser T, Hartmann C, Habel A, Mueller W, Herold-Mende C, von Deimling A, Siegelin MD (2009) Stem-cell-like glioma cells are resistant to TRAIL/Apo2L and exhibit down-regulation of caspase-8 by promoter methylation. Acta Neuropathol 117:445–456PubMedCrossRef Capper D, Gaiser T, Hartmann C, Habel A, Mueller W, Herold-Mende C, von Deimling A, Siegelin MD (2009) Stem-cell-like glioma cells are resistant to TRAIL/Apo2L and exhibit down-regulation of caspase-8 by promoter methylation. Acta Neuropathol 117:445–456PubMedCrossRef
15.
go back to reference Ma HI, Kao CL, Lee YY, Chiou GY, Tai LK, Lu KH, Huang CS, Chen YW, Chiou SH, Cheng IC, Wong TT (2009) Differential expression profiling between atypical teratoid/rhabdoid and medulloblastoma tumor in vitro and in vivo using microarray analysis. Childs Nerv Syst 26:293–303PubMedCrossRef Ma HI, Kao CL, Lee YY, Chiou GY, Tai LK, Lu KH, Huang CS, Chen YW, Chiou SH, Cheng IC, Wong TT (2009) Differential expression profiling between atypical teratoid/rhabdoid and medulloblastoma tumor in vitro and in vivo using microarray analysis. Childs Nerv Syst 26:293–303PubMedCrossRef
16.
go back to reference Kao CL, Huang PI, Tsai PH, Tsai ML, Lo JF, Lee YY, Chen YJ, Chen YW, Chiou SH (2009) Resveratrol-induced apoptosis and increased radiosensitivity in CD133-positive cells derived from atypical teratoid/rhabdoid tumor. Int J Radiat Oncol Biol Phys 74:219–228PubMedCrossRef Kao CL, Huang PI, Tsai PH, Tsai ML, Lo JF, Lee YY, Chen YJ, Chen YW, Chiou SH (2009) Resveratrol-induced apoptosis and increased radiosensitivity in CD133-positive cells derived from atypical teratoid/rhabdoid tumor. Int J Radiat Oncol Biol Phys 74:219–228PubMedCrossRef
18.
go back to reference Altaner C (2008) Glioblastoma and stem cells. Neoplasma 55:369–374PubMed Altaner C (2008) Glioblastoma and stem cells. Neoplasma 55:369–374PubMed
19.
go back to reference Chiou SH, Kao CL, Chen YW, Chien CS, Hung SC, Lo JF, Chen YJ, Ku HH, Hsu MT, Wong TT (2008) Identification of CD133-positive radioresistant cells in atypical teratoid/rhabdoid tumor. PLoS One 3:e2090PubMedCrossRef Chiou SH, Kao CL, Chen YW, Chien CS, Hung SC, Lo JF, Chen YJ, Ku HH, Hsu MT, Wong TT (2008) Identification of CD133-positive radioresistant cells in atypical teratoid/rhabdoid tumor. PLoS One 3:e2090PubMedCrossRef
20.
go back to reference Ma HI, Chiou SH, Hueng DY, Tai KL, Huang PI, Kao CL, Chen YW, Sytwu HK (2010) Celecoxib and radioresistant glioblastoma-derived CD133+ cells: improvement in radiotherapeutic effects. J Neurosurg. doi:10.3171/2009.11.JNS091396 Ma HI, Chiou SH, Hueng DY, Tai KL, Huang PI, Kao CL, Chen YW, Sytwu HK (2010) Celecoxib and radioresistant glioblastoma-derived CD133+ cells: improvement in radiotherapeutic effects. J Neurosurg. doi:10.​3171/​2009.​11.​JNS091396
21.
go back to reference Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432:396–401PubMedCrossRef Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432:396–401PubMedCrossRef
22.
go back to reference Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821–5828PubMed Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821–5828PubMed
23.
go back to reference Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65:10946–10951PubMedCrossRef Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65:10946–10951PubMedCrossRef
24.
go back to reference Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, Collins AT (2004) CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 117:3539–3545PubMedCrossRef Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, Collins AT (2004) CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 117:3539–3545PubMedCrossRef
25.
26.
go back to reference O’Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445:106–110PubMedCrossRef O’Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445:106–110PubMedCrossRef
28.
go back to reference Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, Fuhlbrigge RC, Kupper TS, Sayegh MH, Frank MH (2008) Identification of cells initiating human melanomas. Nature 451:345–349PubMedCrossRef Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, Fuhlbrigge RC, Kupper TS, Sayegh MH, Frank MH (2008) Identification of cells initiating human melanomas. Nature 451:345–349PubMedCrossRef
29.
go back to reference Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, Pratesi G, Fabbri A, Andriani F, Tinelli S, Roz E, Caserini R, Lo Vullo S, Camerini T, Mariani L, Delia D, Calabro E, Pastorino U, Sozzi G (2009) Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 106:16281–16286PubMedCrossRef Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, Pratesi G, Fabbri A, Andriani F, Tinelli S, Roz E, Caserini R, Lo Vullo S, Camerini T, Mariani L, Delia D, Calabro E, Pastorino U, Sozzi G (2009) Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 106:16281–16286PubMedCrossRef
30.
go back to reference Chang CJ, Hsu CC, Yung MC, Chen KY, Tzao C, Wu WF, Chou HY, Lee YY, Lu KH, Chiou SH, Ma HI (2009) Enhanced radiosensitivity and radiation-induced apoptosis in glioma CD133-positive cells by knockdown of SirT1 expression. Biochem Biophys Res Commun 380:236–242PubMedCrossRef Chang CJ, Hsu CC, Yung MC, Chen KY, Tzao C, Wu WF, Chou HY, Lee YY, Lu KH, Chiou SH, Ma HI (2009) Enhanced radiosensitivity and radiation-induced apoptosis in glioma CD133-positive cells by knockdown of SirT1 expression. Biochem Biophys Res Commun 380:236–242PubMedCrossRef
31.
go back to reference Blazek ER, Foutch JL, Maki G (2007) Daoy medulloblastoma cells that express CD133 are radioresistant relative to CD133− cells, and the CD133+ sector is enlarged by hypoxia. Int J Radiat Oncol Biol Phys 67:1–5PubMedCrossRef Blazek ER, Foutch JL, Maki G (2007) Daoy medulloblastoma cells that express CD133 are radioresistant relative to CD133− cells, and the CD133+ sector is enlarged by hypoxia. Int J Radiat Oncol Biol Phys 67:1–5PubMedCrossRef
32.
go back to reference Lasky JL III, Choe M, Nakano I (2009) Cancer stem cells in pediatric brain tumors. Curr Stem Cell Res Ther 4:298–305PubMedCrossRef Lasky JL III, Choe M, Nakano I (2009) Cancer stem cells in pediatric brain tumors. Curr Stem Cell Res Ther 4:298–305PubMedCrossRef
34.
go back to reference Xu Q, Yuan X, Tunici P, Liu G, Fan X, Xu M, Hu J, Hwang JY, Farkas DL, Black KL, Yu JS (2009) Isolation of tumour stem-like cells from benign tumours. Br J Cancer 101:303–311PubMedCrossRef Xu Q, Yuan X, Tunici P, Liu G, Fan X, Xu M, Hu J, Hwang JY, Farkas DL, Black KL, Yu JS (2009) Isolation of tumour stem-like cells from benign tumours. Br J Cancer 101:303–311PubMedCrossRef
35.
go back to reference Lee CC, Jan HJ, Lai JH, Ma HI, Hueng DY, Lee YC, Cheng YY, Liu LW, Wei HW, Lee HM (2010) Nodal promotes growth and invasion in human gliomas. Oncogene 29:3110–3123PubMedCrossRef Lee CC, Jan HJ, Lai JH, Ma HI, Hueng DY, Lee YC, Cheng YY, Liu LW, Wei HW, Lee HM (2010) Nodal promotes growth and invasion in human gliomas. Oncogene 29:3110–3123PubMedCrossRef
36.
go back to reference Jan HJ, Lee CC, Shih YL, Hueng DY, Ma HI, Lai JH, Wei HW, Lee HM (2010) Osteopontin regulates human glioma cell invasiveness and tumor growth in mice. Neuro Oncol 12:58–70PubMed Jan HJ, Lee CC, Shih YL, Hueng DY, Ma HI, Lai JH, Wei HW, Lee HM (2010) Osteopontin regulates human glioma cell invasiveness and tumor growth in mice. Neuro Oncol 12:58–70PubMed
37.
go back to reference Lin GJ, Huang SH, Chen YW, Hueng DY, Chien MW, Chia WT, Chang DM, Sytwu HK (2009) Melatonin prolongs islet graft survival in diabetic NOD mice. J Pineal Res 47:284–292PubMedCrossRef Lin GJ, Huang SH, Chen YW, Hueng DY, Chien MW, Chia WT, Chang DM, Sytwu HK (2009) Melatonin prolongs islet graft survival in diabetic NOD mice. J Pineal Res 47:284–292PubMedCrossRef
38.
go back to reference Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760PubMedCrossRef Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760PubMedCrossRef
39.
go back to reference Hu W, Shen F, Chen G, Shen G, Liu W, Zhou J (2009) Possible involvement of brain tumour stem cells in the emergence of a fast-growing malignant meningioma after surgical resection and radiotherapy of high-grade astrocytoma: case report and preliminary laboratory investigation. J Int Med Res 37:240–246PubMed Hu W, Shen F, Chen G, Shen G, Liu W, Zhou J (2009) Possible involvement of brain tumour stem cells in the emergence of a fast-growing malignant meningioma after surgical resection and radiotherapy of high-grade astrocytoma: case report and preliminary laboratory investigation. J Int Med Res 37:240–246PubMed
40.
go back to reference Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN, Sullenger BA (2010) Notch promotes radioresistance of glioma stem cells. Stem Cells 28:17–28PubMedCrossRef Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN, Sullenger BA (2010) Notch promotes radioresistance of glioma stem cells. Stem Cells 28:17–28PubMedCrossRef
42.
go back to reference 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 16:262–270PubMedCrossRef 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 16:262–270PubMedCrossRef
43.
go back to reference Bellahcene A, Castronovo V, Ogbureke KU, Fisher LW, Fedarko NS (2008) Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nat Rev Cancer 8:212–226PubMedCrossRef Bellahcene A, Castronovo V, Ogbureke KU, Fisher LW, Fedarko NS (2008) Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nat Rev Cancer 8:212–226PubMedCrossRef
45.
go back to reference Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, Lichter P, Unterberg A, Radlwimmer B, Herold-Mende CC (2008) Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res 14:123–129PubMedCrossRef Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, Lichter P, Unterberg A, Radlwimmer B, Herold-Mende CC (2008) Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res 14:123–129PubMedCrossRef
46.
go back to reference Fatoo A, Nanaszko MJ, Allen BB, Mok CL, Bukanova EN, Beyene R, Moliterno JA, Boockvar JA (2010) Understanding the role of tumor stem cells in glioblastoma multiforme: a review article. J Neurooncol. doi:10.1007/s11060-010-0406-3 Fatoo A, Nanaszko MJ, Allen BB, Mok CL, Bukanova EN, Beyene R, Moliterno JA, Boockvar JA (2010) Understanding the role of tumor stem cells in glioblastoma multiforme: a review article. J Neurooncol. doi:10.​1007/​s11060-010-0406-3
Metadata
Title
Isolation and characterization of tumor stem-like cells from human meningiomas
Publication date
01-08-2011
Published in
Journal of Neuro-Oncology / Issue 1/2011
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-010-0469-1

Other articles of this Issue 1/2011

Journal of Neuro-Oncology 1/2011 Go to the issue