Skip to main content
Erschienen 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

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

Erschienen in: Journal of Neuro-Oncology | Ausgabe 1/2008

Einloggen, um Zugang zu erhalten

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.
Literatur
1.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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
Metadaten
Titel
Expression of stem cell markers in human astrocytomas of different WHO grades
verfasst von
Yue-Hui Ma
Rolf Mentlein
Friederike Knerlich
Marie-Luise Kruse
H. Maximilian Mehdorn
Janka Held-Feindt
Publikationsdatum
01.01.2008
Verlag
Springer US
Erschienen in
Journal of Neuro-Oncology / Ausgabe 1/2008
Print ISSN: 0167-594X
Elektronische ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-007-9439-7

Weitere Artikel der Ausgabe 1/2008

Journal of Neuro-Oncology 1/2008 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Hirnblutung unter DOAK und VKA ähnlich bedrohlich

17.05.2024 Direkte orale Antikoagulanzien Nachrichten

Kommt es zu einer nichttraumatischen Hirnblutung, spielt es keine große Rolle, ob die Betroffenen zuvor direkt wirksame orale Antikoagulanzien oder Marcumar bekommen haben: Die Prognose ist ähnlich schlecht.

Thrombektomie auch bei großen Infarkten von Vorteil

16.05.2024 Ischämischer Schlaganfall Nachrichten

Auch ein sehr ausgedehnter ischämischer Schlaganfall scheint an sich kein Grund zu sein, von einer mechanischen Thrombektomie abzusehen. Dafür spricht die LASTE-Studie, an der Patienten und Patientinnen mit einem ASPECTS von maximal 5 beteiligt waren.

Schwindelursache: Massagepistole lässt Otholiten tanzen

14.05.2024 Benigner Lagerungsschwindel Nachrichten

Wenn jüngere Menschen über ständig rezidivierenden Lagerungsschwindel klagen, könnte eine Massagepistole der Auslöser sein. In JAMA Otolaryngology warnt ein Team vor der Anwendung hochpotenter Geräte im Bereich des Nackens.

Schützt Olivenöl vor dem Tod durch Demenz?

10.05.2024 Morbus Alzheimer Nachrichten

Konsumieren Menschen täglich 7 Gramm Olivenöl, ist ihr Risiko, an einer Demenz zu sterben, um mehr als ein Viertel reduziert – und dies weitgehend unabhängig von ihrer sonstigen Ernährung. Dafür sprechen Auswertungen zweier großer US-Studien.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.