Skip to main content
Top
Published in: Journal of Neuro-Oncology 1/2008

01-01-2008 | Lab investigation - human/animal tissue

Expression of stem cell markers in human astrocytomas of different WHO grades

Authors: Yue-Hui Ma, Rolf Mentlein, Friederike Knerlich, Marie-Luise Kruse, H. Maximilian Mehdorn, Janka Held-Feindt

Published in: Journal of Neuro-Oncology | Issue 1/2008

Login to get access

Abstract

According to new hypotheses astrocytomas/gliomas either arise from or attract neural stem cells. Biological markers, particularly antigenic markers, have played a significant role for the characterization of these tumour stem cells (TSCc). Because these studies have been performed with single experimental samples mostly from gliomas, we investigated the expression of the stem cell markers CD133/Prominin, Nestin, Sox-2, Musashi-1, CXCR4, Flt-4/VEGFR-3 and CD105/Endoglin in 72 astrocytomas of different WHO-grades and compared it to normal adult human brain. Expression of their mRNA was quantified by quantitative RT-PCR, of their protein by counting immunopositive cells. In contrast to normal brain, tumour samples showed a high variability for the expression of all markers. However, their mean expression was significantly increased in astrocytomas, but this depended on the WHO grade only for CD133, Nestin, Sox-2 and Musashi-1. Confocal microscopy revealed that these markers mostly could be co-stained with glial fibrillary acidic protein, a marker for astoglial cells, but less frequently with the proliferation marker Ki-67/MIB-1. These markers sometimes, but not necessarily could be co-stained with each other in complex patterns. Our results show that most astrocytomas contain considerable portions of cells expressing stem cell markers. It appears that some of these cells originate from tumour genesis (supporting the stem cell hypothesis) while others are attracted by the tumours. Further functional markers are required to differentiate these TSC-types.
Literature
1.
go back to reference Mahaley MS Jr, Mettlin C, Natarajan N, Laws ER Jr, Peace B (1989) National survey of patterns of care for brain-tumour patients. J Neurosurg 71:826–836PubMedCrossRef Mahaley MS Jr, Mettlin C, Natarajan N, Laws ER Jr, Peace B (1989) National survey of patterns of care for brain-tumour patients. J Neurosurg 71:826–836PubMedCrossRef
2.
go back to reference Kleihues P, Soylemezoglu F, Schauble B, Scheithauer BW, Burger PC (1995) Histopathology, classification, and grading of gliomas. Glia 15:211–221PubMedCrossRef Kleihues P, Soylemezoglu F, Schauble B, Scheithauer BW, Burger PC (1995) Histopathology, classification, and grading of gliomas. Glia 15:211–221PubMedCrossRef
3.
go back to reference Nozaki M, Tada M, Kobayashi H, Zhang CL, Sawamura Y, Abe H, Ishii N, Van Meir EG (1999) Roles of the functional loss of p53 and other genes in astrocytoma tumourigenesis and progression. Neuro-Oncol 1:124–137PubMed Nozaki M, Tada M, Kobayashi H, Zhang CL, Sawamura Y, Abe H, Ishii N, Van Meir EG (1999) Roles of the functional loss of p53 and other genes in astrocytoma tumourigenesis and progression. Neuro-Oncol 1:124–137PubMed
4.
go back to reference von Deimling A, Louis DN, Wiestler OD (1995) Molecular pathways in the formation of gliomas. Glia 15:328–338CrossRef von Deimling A, Louis DN, Wiestler OD (1995) Molecular pathways in the formation of gliomas. Glia 15:328–338CrossRef
5.
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 tumours. 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 tumours. Cancer Res 63:5821–5828PubMed
6.
go back to reference Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum H (2003) Cancerous stem cells can arise from pediatric brain tumours. Proc Natl Acad Sci USA 100:15178–15183PubMedCrossRef Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum H (2003) Cancerous stem cells can arise from pediatric brain tumours. Proc Natl Acad Sci USA 100:15178–15183PubMedCrossRef
7.
go back to reference Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A (2004) Isolation and characterization of tumourigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64:7011–7021PubMedCrossRef Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A (2004) Isolation and characterization of tumourigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64:7011–7021PubMedCrossRef
8.
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
9.
go back to reference Dahmane N, Sanchez P, Gitton Y, Palma V, Sun T, Beyna M, Weiner H, Ruiz i Altaba A (2001) The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumourigenesis. Development 128:5201–5212PubMed Dahmane N, Sanchez P, Gitton Y, Palma V, Sun T, Beyna M, Weiner H, Ruiz i Altaba A (2001) The Sonic Hedgehog-Gli pathway regulates dorsal brain growth and tumourigenesis. Development 128:5201–5212PubMed
10.
go back to reference Ruiz i Altaba A, Sanchez P, Dahmane N (2002) Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat Rev Cancer 2:361–372PubMedCrossRef Ruiz i Altaba A, Sanchez P, Dahmane N (2002) Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat Rev Cancer 2:361–372PubMedCrossRef
11.
go back to reference Pardal R, Clarke MF, Morrison SJ (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3:895–902PubMedCrossRef Pardal R, Clarke MF, Morrison SJ (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3:895–902PubMedCrossRef
12.
go back to reference Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105–111PubMedCrossRef Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105–111PubMedCrossRef
13.
go back to reference Zhu Y, Guignard F, Zhao D, Liu L, Burns DK, Mason RP, Messing A, Parada LF (2005) Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell 8:119–130PubMedCrossRef Zhu Y, Guignard F, Zhao D, Liu L, Burns DK, Mason RP, Messing A, Parada LF (2005) Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell 8:119–130PubMedCrossRef
14.
go back to reference You H, Kim YI, Im SY, Suh-Kim H, Paek SH, Park SH, Kim DG, Jung HW (2005) Immunohistochemical study of central neurocytoma, subependymoma, and subependymal giant cell astrocytoma. J Neuro-Oncol 74:1–8CrossRef You H, Kim YI, Im SY, Suh-Kim H, Paek SH, Park SH, Kim DG, Jung HW (2005) Immunohistochemical study of central neurocytoma, subependymoma, and subependymal giant cell astrocytoma. J Neuro-Oncol 74:1–8CrossRef
15.
go back to reference Rao G, Pedone CA, Coffin CM, Holland EC, Fults DW (2003) c-Myc enhances sonic hedgehog-induced medulloblastoma formation from nestin-expressing neural progenitors in mice. Neoplasia 5:198–204PubMed Rao G, Pedone CA, Coffin CM, Holland EC, Fults DW (2003) c-Myc enhances sonic hedgehog-induced medulloblastoma formation from nestin-expressing neural progenitors in mice. Neoplasia 5:198–204PubMed
16.
go back to reference Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN (2000) Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet 25:55–57PubMedCrossRef Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN (2000) Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet 25:55–57PubMedCrossRef
17.
go back to reference Uhrbom L, Dai C, Celestino JC, Rosenblum MK, Fuller GN, Holland EC (2002) Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated Akt. Cancer Res 62:5551–5558PubMed Uhrbom L, Dai C, Celestino JC, Rosenblum MK, Fuller GN, Holland EC (2002) Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated Akt. Cancer Res 62:5551–5558PubMed
18.
go back to reference Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumourigenic prostate cancer stem cells. Cancer Res 65:10946–10951PubMedCrossRef Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumourigenic prostate cancer stem cells. Cancer Res 65:10946–10951PubMedCrossRef
19.
go back to reference Taylor MD, Poppleton H, Fuller C, Su X, Liu Y, Jensen P, Magdaleno S, Dalton J, Calabrese C, Board J, Macdonald T, Rutka J, Guha A, Gajjar A, Curran T, Gilbertson RJ (2005) Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 8:323–335PubMedCrossRef Taylor MD, Poppleton H, Fuller C, Su X, Liu Y, Jensen P, Magdaleno S, Dalton J, Calabrese C, Board J, Macdonald T, Rutka J, Guha A, Gajjar A, Curran T, Gilbertson RJ (2005) Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 8:323–335PubMedCrossRef
20.
go back to reference Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumourigenic breast cancer cells. Proc Natl Acad Sci USA 100:3983–3988PubMedCrossRef Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumourigenic breast cancer cells. Proc Natl Acad Sci USA 100:3983–3988PubMedCrossRef
21.
go back to reference Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz S, Van Belle PA, Xu X, Elder DE, Herlyn M (2005) A tumourigenic subpopulation with stem cell properties in melanomas. Cancer Res 65:9328–9337PubMedCrossRef Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz S, Van Belle PA, Xu X, Elder DE, Herlyn M (2005) A tumourigenic subpopulation with stem cell properties in melanomas. Cancer Res 65:9328–9337PubMedCrossRef
22.
go back to reference Nilsson L, Astrand-Grundstrom I, Arvidsson I, Jacobsson B, Hellstrom-Lindberg E, Hast R, Jacobsen SE (2000) Isolation and characterization of hematopoietic progenitor/stem cells in 5q-deleted myelodysplastic syndromes: evidence for involvement at the hematopoietic stem cell level. Blood 96:2012–2021PubMed Nilsson L, Astrand-Grundstrom I, Arvidsson I, Jacobsson B, Hellstrom-Lindberg E, Hast R, Jacobsen SE (2000) Isolation and characterization of hematopoietic progenitor/stem cells in 5q-deleted myelodysplastic syndromes: evidence for involvement at the hematopoietic stem cell level. Blood 96:2012–2021PubMed
23.
go back to reference Seigel GM, Campbell LM, Narayan M, Gonzalez-Fernandez F (2005) Cancer stem cell characteristics in retinoblastoma. Mol Vis 11:729–737PubMed Seigel GM, Campbell LM, Narayan M, Gonzalez-Fernandez F (2005) Cancer stem cell characteristics in retinoblastoma. Mol Vis 11:729–737PubMed
24.
go back to reference Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, Goodell MA, Brenner MK (2004) A distinct “side population” of cells with high drug efflux capacity in human tumour cells. Proc Natl Acad Sci USA 101:14228–14233PubMedCrossRef Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, Goodell MA, Brenner MK (2004) A distinct “side population” of cells with high drug efflux capacity in human tumour cells. Proc Natl Acad Sci USA 101:14228–14233PubMedCrossRef
25.
go back to reference Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, Crowley D, Bronson RT, Jacks T (2005) Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121:823–835PubMedCrossRef Kim CF, Jackson EL, Woolfenden AE, Lawrence S, Babar I, Vogel S, Crowley D, Bronson RT, Jacks T (2005) Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121:823–835PubMedCrossRef
26.
go back to reference Reiss K, Mentlein R, Sievers J, Hartmann D (2002) Stromal cell-derived factor 1 is secreted by meningeal cells and acts as chemotactic factor on neuronal stem cells of the cerebellar external granular layer. Neuroscience 115:295–305PubMedCrossRef Reiss K, Mentlein R, Sievers J, Hartmann D (2002) Stromal cell-derived factor 1 is secreted by meningeal cells and acts as chemotactic factor on neuronal stem cells of the cerebellar external granular layer. Neuroscience 115:295–305PubMedCrossRef
27.
go back to reference Le Bras B, Barallobre MJ, Homman-Ludiye J, Ny A, Wyns S, Tammela T, Haiko P, Karkkainen MJ, Yuan L, Muriel MP, Chatzopoulou E, Breant C, Zalc B, Carmeliet P, Alitalo K, Eichmann A, Thomas JL (2006) VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain. Nat Neurosci 9:340–348PubMedCrossRef Le Bras B, Barallobre MJ, Homman-Ludiye J, Ny A, Wyns S, Tammela T, Haiko P, Karkkainen MJ, Yuan L, Muriel MP, Chatzopoulou E, Breant C, Zalc B, Carmeliet P, Alitalo K, Eichmann A, Thomas JL (2006) VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain. Nat Neurosci 9:340–348PubMedCrossRef
28.
go back to reference Henriksen R, Gobl A, Wilander E, Oberg K, Miyazono K, Funa K (1995) Expression and prognostic significance of TGF-beta isotypes, latent TGF-beta 1 binding protein, TGF-beta type I and type II receptors, and endoglin in normal ovary and ovarian neoplasms. Lab Invest 73:213–220PubMed Henriksen R, Gobl A, Wilander E, Oberg K, Miyazono K, Funa K (1995) Expression and prognostic significance of TGF-beta isotypes, latent TGF-beta 1 binding protein, TGF-beta type I and type II receptors, and endoglin in normal ovary and ovarian neoplasms. Lab Invest 73:213–220PubMed
29.
go back to reference Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS (2004) Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 23:9392–9400PubMedCrossRef Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS (2004) Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 23:9392–9400PubMedCrossRef
30.
go back to reference Ignatova TN, Kukekov VG, Laywell ED, Suslov ON, Vrionis FD, Steindler DA (2002) Human cortical glial tumours contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 39:193–206PubMedCrossRef Ignatova TN, Kukekov VG, Laywell ED, Suslov ON, Vrionis FD, Steindler DA (2002) Human cortical glial tumours contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 39:193–206PubMedCrossRef
31.
go back to reference Salmaggi A, Boiardi A, Gelati M, Russo A, Calatozzolo C, Ciusani E, Sciacca FL, Ottolina A, Parati EA, La Porta C, Alessandri G, Marras C, Croci D, De Rossi M (2006) Glioblastoma-derived tumourspheres identify a population of tumour stem-like cells with angiogenic potential and enhanced multidrug resistence phenotype. Glia 54:850–860PubMedCrossRef Salmaggi A, Boiardi A, Gelati M, Russo A, Calatozzolo C, Ciusani E, Sciacca FL, Ottolina A, Parati EA, La Porta C, Alessandri G, Marras C, Croci D, De Rossi M (2006) Glioblastoma-derived tumourspheres identify a population of tumour stem-like cells with angiogenic potential and enhanced multidrug resistence phenotype. Glia 54:850–860PubMedCrossRef
32.
go back to reference Weigmann A, Corbeil D, Hellwig A, Huttner WB (1997) Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci USA 94:12425–12430PubMedCrossRef Weigmann A, Corbeil D, Hellwig A, Huttner WB (1997) Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci USA 94:12425–12430PubMedCrossRef
33.
go back to reference Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW (1997) AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90:5002–5012PubMed Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW (1997) AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90:5002–5012PubMed
34.
go back to reference Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL (2000) Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 97:14720–14725PubMedCrossRef Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL (2000) Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 97:14720–14725PubMedCrossRef
35.
go back to reference Cattaneo E, McKay R (1990) Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 347:762–765PubMedCrossRef Cattaneo E, McKay R (1990) Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 347:762–765PubMedCrossRef
36.
go back to reference Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585–595PubMedCrossRef Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585–595PubMedCrossRef
37.
go back to reference Kondo T, Setoguchi T, Taga T (2004) Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA 101:781–786PubMedCrossRef Kondo T, Setoguchi T, Taga T (2004) Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA 101:781–786PubMedCrossRef
38.
go back to reference Almqvist PM, Mah R, Lendahl U, Jacobsson B, Hendson G (2002) Immunohistochemical detection of nestin in pediatric brain tumours. J Histochem Cytochem 50:147–158PubMed Almqvist PM, Mah R, Lendahl U, Jacobsson B, Hendson G (2002) Immunohistochemical detection of nestin in pediatric brain tumours. J Histochem Cytochem 50:147–158PubMed
39.
go back to reference Tohyama T, Lee VM, Rorke LB, Marvin M, McKay RD, Trojanowski JQ (1992) Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumour cells. Lab Invest 66:303–313PubMed Tohyama T, Lee VM, Rorke LB, Marvin M, McKay RD, Trojanowski JQ (1992) Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumour cells. Lab Invest 66:303–313PubMed
40.
go back to reference Hockfield S, McKay RD (1985) Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310–3328PubMed Hockfield S, McKay RD (1985) Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310–3328PubMed
41.
go back to reference Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25–34PubMedCrossRef Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25–34PubMedCrossRef
42.
go back to reference Gu H, Wang S, Messam CA, Yao Z (2002) Distribution of nestin immunoreactivity in the normal adult human forebrain. Brain Res 943:174–180PubMedCrossRef Gu H, Wang S, Messam CA, Yao Z (2002) Distribution of nestin immunoreactivity in the normal adult human forebrain. Brain Res 943:174–180PubMedCrossRef
43.
go back to reference Lu G, Kwong WH, Li Q, Wang X, Feng Z, Yew DT (2005) bcl2, bax, and nestin in the brains of patients with neurodegeneration and those of normal aging. J Mol Neurosci 27:167–174PubMedCrossRef Lu G, Kwong WH, Li Q, Wang X, Feng Z, Yew DT (2005) bcl2, bax, and nestin in the brains of patients with neurodegeneration and those of normal aging. J Mol Neurosci 27:167–174PubMedCrossRef
44.
go back to reference Wei LC, Shi M, Chen LW, Cao R, Zhang P, Chan YS (2002) Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Brain Res Dev Brain Res 139:9–17PubMedCrossRef Wei LC, Shi M, Chen LW, Cao R, Zhang P, Chan YS (2002) Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Brain Res Dev Brain Res 139:9–17PubMedCrossRef
45.
go back to reference Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469:311–324PubMedCrossRef Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469:311–324PubMedCrossRef
46.
go back to reference Holmin S, Almqvist P, Lendahl U, Mathiesen T (1997) Adult nestin-expressing subependymal cells differentiate to astrocytes in response to brain injury. Eur J Neurosci 9:65–75PubMedCrossRef Holmin S, Almqvist P, Lendahl U, Mathiesen T (1997) Adult nestin-expressing subependymal cells differentiate to astrocytes in response to brain injury. Eur J Neurosci 9:65–75PubMedCrossRef
47.
go back to reference Krum JM, Rosenstein JM (1999) Transient coexpression of nestin, GFAP, and vascular endothelial growth factor in mature reactive astroglia following neural grafting or brain wounds. Exp Neurol 160:348–360PubMedCrossRef Krum JM, Rosenstein JM (1999) Transient coexpression of nestin, GFAP, and vascular endothelial growth factor in mature reactive astroglia following neural grafting or brain wounds. Exp Neurol 160:348–360PubMedCrossRef
48.
go back to reference Lin RC, Matesic DF, Marvin M, McKay RD, Brustle O (1995) Re-expression of the intermediate filament nestin in reactive astrocytes. Neurobiol Dis 2:79–85PubMedCrossRef Lin RC, Matesic DF, Marvin M, McKay RD, Brustle O (1995) Re-expression of the intermediate filament nestin in reactive astrocytes. Neurobiol Dis 2:79–85PubMedCrossRef
49.
go back to reference Li Y, Chopp M (1999) Temporal profile of nestin expression after focal cerebral ischemia in adult rat. Brain Res 838:1–10PubMedCrossRef Li Y, Chopp M (1999) Temporal profile of nestin expression after focal cerebral ischemia in adult rat. Brain Res 838:1–10PubMedCrossRef
50.
go back to reference Yoo YM, Lee U, Kim YJ (2005) Apoptosis and nestin expression in the cortex and cultured astrocytes following 6-OHDA administration. Neurosci Lett 382:88–92PubMedCrossRef Yoo YM, Lee U, Kim YJ (2005) Apoptosis and nestin expression in the cortex and cultured astrocytes following 6-OHDA administration. Neurosci Lett 382:88–92PubMedCrossRef
51.
go back to reference Schmidt-Kastner R, Humpel C (2002) Nestin expression persists in astrocytes of organotypic slice cultures from rat cortex. Int J Dev Neurosci 20:29–38PubMedCrossRef Schmidt-Kastner R, Humpel C (2002) Nestin expression persists in astrocytes of organotypic slice cultures from rat cortex. Int J Dev Neurosci 20:29–38PubMedCrossRef
52.
go back to reference Kawaguchi A, Miyata T, Sawamoto K, Takashita N, Murayama A, Akamatsu W, Ogawa M, Okabe M, Tano Y, Goldman SA, Okano H (2001) Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci 17:259–273PubMedCrossRef Kawaguchi A, Miyata T, Sawamoto K, Takashita N, Murayama A, Akamatsu W, Ogawa M, Okabe M, Tano Y, Goldman SA, Okano H (2001) Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci 17:259–273PubMedCrossRef
53.
go back to reference van de Wetering M, Oosterwegel M, van Norren K, Clevers H (1993) Sox-4, an Sry-like HMG box protein, is a transcriptional activator in lymphocytes. EMBO J 12:3847–3854PubMed van de Wetering M, Oosterwegel M, van Norren K, Clevers H (1993) Sox-4, an Sry-like HMG box protein, is a transcriptional activator in lymphocytes. EMBO J 12:3847–3854PubMed
54.
go back to reference Yuan H, Corbi N, Basilico C, Dailey L (1995) Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev 9:2635–2645PubMedCrossRef Yuan H, Corbi N, Basilico C, Dailey L (1995) Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev 9:2635–2645PubMedCrossRef
55.
go back to reference Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17:126–140PubMedCrossRef Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17:126–140PubMedCrossRef
56.
go back to reference Brazel CY, Limke TL, Osborne JK, Miura T, Cai J, Pevny L, Rao MS (2005) Sox2 expression defines a heterogeneous population of neurosphere-forming cells in the adult murine brain. Aging Cell 4:197–207PubMedCrossRef Brazel CY, Limke TL, Osborne JK, Miura T, Cai J, Pevny L, Rao MS (2005) Sox2 expression defines a heterogeneous population of neurosphere-forming cells in the adult murine brain. Aging Cell 4:197–207PubMedCrossRef
57.
go back to reference Kanemura Y, Mori K, Sakakibara S, Fujikawa H, Hayashi H, Nakano A, Matsumoto T, Tamura K, Imai T, Ohnishi T, Fushiki S, Nakamura Y, Yamasaki M, Okano H, Arita N (2001) Musashi1, an evolutionarily conserved neural RNA-binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation 68:141–152PubMedCrossRef Kanemura Y, Mori K, Sakakibara S, Fujikawa H, Hayashi H, Nakano A, Matsumoto T, Tamura K, Imai T, Ohnishi T, Fushiki S, Nakamura Y, Yamasaki M, Okano H, Arita N (2001) Musashi1, an evolutionarily conserved neural RNA-binding protein, is a versatile marker of human glioma cells in determining their cellular origin, malignancy, and proliferative activity. Differentiation 68:141–152PubMedCrossRef
58.
go back to reference Sakakibara S, Imai T, Hamaguchi K, Okabe M, Aruga J, Nakajima K, Yasutomi D, Nagata T, Kurihara Y, Uesugi S, Miyata T, Ogawa M, Mikoshiba K, Okano H (1996) Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 176:230–242PubMedCrossRef Sakakibara S, Imai T, Hamaguchi K, Okabe M, Aruga J, Nakajima K, Yasutomi D, Nagata T, Kurihara Y, Uesugi S, Miyata T, Ogawa M, Mikoshiba K, Okano H (1996) Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 176:230–242PubMedCrossRef
59.
go back to reference Sakakibara S, Okano H (1997) Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J Neurosci 17:8300–8312PubMed Sakakibara S, Okano H (1997) Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J Neurosci 17:8300–8312PubMed
60.
go back to reference Shu HJ, Saito T, Watanabe H, Ito JI, Takeda H, Okano H, Kawata S (2002) Expression of the Musashi1 gene encoding the RNA-binding protein in human hepatoma cell lines. Biochem Biophys Res Commun 293:150–154PubMedCrossRef Shu HJ, Saito T, Watanabe H, Ito JI, Takeda H, Okano H, Kawata S (2002) Expression of the Musashi1 gene encoding the RNA-binding protein in human hepatoma cell lines. Biochem Biophys Res Commun 293:150–154PubMedCrossRef
61.
go back to reference Corti S, Locatelli F, Papadimitriou D, Donadoni C, Del Bo R, Fortunato F, Strazzer S, Salani S, Bresolin N, Comi GP (2005) Multipotentiality, homing properties, and pyramidal neurogenesis of CNS-derived LeX (ssea-1)+/CXCR4+ stem cells. FASEB J 19:1860–1862PubMed Corti S, Locatelli F, Papadimitriou D, Donadoni C, Del Bo R, Fortunato F, Strazzer S, Salani S, Bresolin N, Comi GP (2005) Multipotentiality, homing properties, and pyramidal neurogenesis of CNS-derived LeX (ssea-1)+/CXCR4+ stem cells. FASEB J 19:1860–1862PubMed
62.
go back to reference Kaipainen A, Korhonen J, Mustonen T, van Hinsbergh VW, Fang GH, Dumont D., Breitman M, Alitalo K (1995) Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Natl Acad Sci USA 92:3566–35670PubMedCrossRef Kaipainen A, Korhonen J, Mustonen T, van Hinsbergh VW, Fang GH, Dumont D., Breitman M, Alitalo K (1995) Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Natl Acad Sci USA 92:3566–35670PubMedCrossRef
63.
go back to reference Salven P, Mustjoki S, Alitalo R, Alitalo K, Rafii S (2003) VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells. Blood 101:168–172PubMedCrossRef Salven P, Mustjoki S, Alitalo R, Alitalo K, Rafii S (2003) VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells. Blood 101:168–172PubMedCrossRef
64.
go back to reference Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague J, Letarte M (1992) Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J Biol Chem 267:19027–19030PubMed Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague J, Letarte M (1992) Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J Biol Chem 267:19027–19030PubMed
65.
go back to reference Chen CZ, Li L, Li M, Lodish HF (2003) The endoglin (positive) sca-1 (positive) rhodamine (low) phenotype defines a near-homogeneous population of long-term repopulating hematopoietic stem cells. Immunity 19:525–533PubMedCrossRef Chen CZ, Li L, Li M, Lodish HF (2003) The endoglin (positive) sca-1 (positive) rhodamine (low) phenotype defines a near-homogeneous population of long-term repopulating hematopoietic stem cells. Immunity 19:525–533PubMedCrossRef
66.
go back to reference Chen CZ, Li M, de Graaf D, Monti S, Gottgens B, Sanchez MJ, Lander ES, Golub TR, Green AR, Lodish HF (2002) Identification of endoglin as a functional marker that defines long-term repopulating hematopoietic stem cells. Proc Natl Acad Sci USA 99:15468–15473PubMedCrossRef Chen CZ, Li M, de Graaf D, Monti S, Gottgens B, Sanchez MJ, Lander ES, Golub TR, Green AR, Lodish HF (2002) Identification of endoglin as a functional marker that defines long-term repopulating hematopoietic stem cells. Proc Natl Acad Sci USA 99:15468–15473PubMedCrossRef
67.
go back to reference Pierelli L, Bonanno G, Rutella S, Marone M, Scambia G, Leone G (2001) CD105 (endoglin) expression on hematopoietic stem/progenitor cells. Leuk Lymphoma 42:1195–1206PubMedCrossRef Pierelli L, Bonanno G, Rutella S, Marone M, Scambia G, Leone G (2001) CD105 (endoglin) expression on hematopoietic stem/progenitor cells. Leuk Lymphoma 42:1195–1206PubMedCrossRef
68.
go back to reference Toda M, Iizuka Y, Yu W, Imai T, Ikeda E, Yoshida K, Kawase T, Kawakami Y, Okano H, Uyemura K (2001) Expression of the neural RNA-binding protein Musashi1 in human gliomas. Glia 34:1–7PubMedCrossRef Toda M, Iizuka Y, Yu W, Imai T, Ikeda E, Yoshida K, Kawase T, Kawakami Y, Okano H, Uyemura K (2001) Expression of the neural RNA-binding protein Musashi1 in human gliomas. Glia 34:1–7PubMedCrossRef
69.
go back to reference Wilson JM, Sato K, Chernoff EA, Belecky-Adams TL (2007) Expression patterns of chick Musashi-1 in the developing nervous system. Gene Expr Patterns Apr 21, Epub ahead of print Wilson JM, Sato K, Chernoff EA, Belecky-Adams TL (2007) Expression patterns of chick Musashi-1 in the developing nervous system. Gene Expr Patterns Apr 21, Epub ahead of print
70.
go back to reference Akasaka Y, Saikawa Y, Fujita K, Kubota T, Ishikawa Y, Fujimoto A, Ishii T, Okano H, Kitajima M (2005) Expression of a candidate marker for progenitor cells, Musashi-1, in the proliferative regions of human antrum and its decreased expression in intestinal metaplasia. Histopathology 47:348–356PubMedCrossRef Akasaka Y, Saikawa Y, Fujita K, Kubota T, Ishikawa Y, Fujimoto A, Ishii T, Okano H, Kitajima M (2005) Expression of a candidate marker for progenitor cells, Musashi-1, in the proliferative regions of human antrum and its decreased expression in intestinal metaplasia. Histopathology 47:348–356PubMedCrossRef
Metadata
Title
Expression of stem cell markers in human astrocytomas of different WHO grades
Authors
Yue-Hui Ma
Rolf Mentlein
Friederike Knerlich
Marie-Luise Kruse
H. Maximilian Mehdorn
Janka Held-Feindt
Publication date
01-01-2008
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 1/2008
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-007-9439-7

Other articles of this Issue 1/2008

Journal of Neuro-Oncology 1/2008 Go to the issue