CD133 + niches and single cells in glioblastoma have different phenotypes

Journal of Neuro-Oncology

Volumn 104, Issue 1, 2011, Pages 129-143

  Christensen, Karina ^a   Schrøder, Henrik Daa ^a   Kristensen, Bjarne Winther ^a  

^a ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

CD133; Glioblastoma; Niche; Tumor stem cells

Indexed keywords

BMI1 PROTEIN; CD133 ANTIGEN; CD31 ANTIGEN; CD34 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; KI 67 ANTIGEN; NESTIN; PODOPLANIN; TRANSCRIPTION FACTOR SOX2; VON WILLEBRAND FACTOR;

ADULT; AGED; ARTICLE; BLOOD VESSEL; CANCER STEM CELL; CELL COUNT; CELL DIFFERENTIATION; CELL LABELING; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; MALE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ADULT; AGED; ANALYSIS OF VARIANCE; ANTIGENS, CD; ANTIGENS, CD31; BLOOD VESSELS; BRAIN NEOPLASMS; CELL COUNT; FEMALE; GLIOBLASTOMA; GLYCOPROTEINS; HUMANS; KI-67 ANTIGEN; MALE; MIDDLE AGED; NEOPLASTIC STEM CELLS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEPTIDES; PHENOTYPE; PLATELET MEMBRANE GLYCOPROTEINS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; STEM CELL NICHE;

EID: 80052526409     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-010-0488-y     Document Type: Article

References (87)

1. RJ Gilbertson JN Rich 2007 Making a tumour's bed: glioblastoma stem cells and the vascular niche Nat Rev Cancer 7 733 736 17882276 10.1038/nrc2246 1:CAS:528:DC%2BD2sXhtVOnsrzM (Pubitemid 47463683)
2. L Li T Xie 2005 Stem cell niche: structure and function Annu Rev Cell Dev Biol 21 605 631 16212509 10.1146/annurev.cellbio.21.012704.131525 1:CAS:528:DC%2BD2MXhtlektbvE (Pubitemid 41740648)
3. H Chen YC Tung B Li K Iqbal I Grundke-Iqbal 2007 Trophic factors counteract elevated FGF-2-induced inhibition of adult neurogenesis Neurobiol Aging 28 1148 1162 16859812 10.1016/j.neurobiolaging.2006.05.036 1:CAS:528:DC%2BD2sXmtVahsrY%3D (Pubitemid 46810057)
4. L Li WB Neaves 2006 Normal stem cells and cancer stem cells: the niche matters Cancer Res 66 4553 4557 16651403 10.1158/0008-5472.CAN-05-3986 1:CAS:528:DC%2BD28XjvF2ks7c%3D
5. LE Ailles IL Weissman 2007 Cancer stem cells in solid tumors Curr Opin Biotechnol 18 460 466 18023337 10.1016/j.copbio.2007.10.007 1:CAS:528: DC%2BD2sXhtlGhu73N (Pubitemid 350116595)
6. A Veeravagu SR Bababeygy MS Kalani L Hou V Tse 2008 The cancer stem cell-vascular niche complex in brain tumor formation Stem Cells Dev 17 859 867 18429673 10.1089/scd.2008.0047
7. K Christensen HD Schrøder BW Kristensen 2008 CD133 identifies perivascular niches in grade II-IV astrocytomas J Neurooncol 90 157 170 18612800 10.1007/s11060-008-9648-8
8. SK Singh C Hawkins ID Clarke JA Squire J Bayani T Hide RM Henkelman MD Cusimano PB Dirks 2004 Identification of human brain tumour initiating cells Nature 432 396 401 15549107 10.1038/nature03128 1:CAS:528:DC%2BD2cXpvVCjtbY%3D (Pubitemid 39551674)
9. N Thon K Damianoff J Hegermann S Grau B Krebs O Schnell JC Tonn R Goldbrunner 2008 Presence of pluripotent CD133(+) cells correlates with malignancy of gliomas Mol Cell Neurosci 43 51 59 10.1016/j.mcn.2008.07.022 18761091 10.1016/j.mcn.2008.07.022
10. F Zeppernick R Ahmadi B Campos C Dictus BM Helmke N Becker P Lichter A Unterberg B Radlwimmer CC Herold-Mende 2008 Stem cell marker CD133 affects clinical outcome in glioma patients Clin Cancer Res 14 123 129 18172261 10.1158/1078-0432.CCR-07-0932 1:CAS:528:DC%2BD1cXoslCg (Pubitemid 351377986)
11. HD Hemmati I Nakano JA Lazareff M Masterman Smith DH Geschwind M Bronner Fraser HI Kornblum 2003 Cancerous stem cells can arise from pediatric brain tumors Proc Natl Acad Sci USA 100 15178 15183 14645703 10.1073/pnas.2036535100 1:CAS:528:DC%2BD3sXpvFaqu70%3D (Pubitemid 37518036)
12. J Lessard G Sauvageau 2003 Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells Nature 423 255 260 12714970 10.1038/nature01572 1:CAS:528:DC%2BD3sXjs1yntbg%3D (Pubitemid 40852690)
13. AV Molofsky R Pardal T Iwashita IK Park MF Clarke SJ Morrison 2003 Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation Nature 425 962 967 14574365 10.1038/nature02060 1:CAS:528:DC%2BD3sXosVOht7w%3D (Pubitemid 37376927)
14. IK Park D Qian M Kiel MW Becker M Pihalja IL Weissman SJ Morrison MF Clarke 2003 Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells Nature 423 302 305 12714971 10.1038/nature01587 1:CAS:528:DC%2BD3sXjs1ynur4%3D (Pubitemid 40852701)
15. S Hockfield RD McKay 1985 Identification of major cell classes in the developing mammalian nervous system J Neurosci 5 3310 3328 4078630 1:STN:280:DyaL28%2FovVSqsA%3D%3D (Pubitemid 16182611)
16. CB Johansson S Momma DL Clarke M Risling U Lendahl J Frisen 1999 Identification of a neural stem cell in the adult mammalian central nervous system Cell 96 25 34 9989494 10.1016/S0092-8674(00)80956-3 1:CAS:528: DyaK1MXmslagsw%3D%3D (Pubitemid 29044150)
17. Mazzoleni S, Politi LS, Pala M et al. (2010) Epidermal growth factor receptor expression identifies functionally and molecularly distinct tumor-initiating cells in human glioblastoma multiforme and is required for gliomagenesis. Cancer Res 70:7500-7513
18. Sulman EP, Goodman LD, Le TT et al. (2008) A novel marker of glioma stem cells that is prognostic for treatment response and patient outcome. Proceedings of the 99th Annual Meeting of the American Association for Cancer Research. Abstract no. 3777
19. KL Ligon E Huillard S Mehta S Kesari H Liu JA Alberta RM Bachoo M Kane DN Louis RA DePinho DJ Anderson CD Stiles DH Rowitch 2007 Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma Neuron 53 503 517 17296553 10.1016/j.neuron.2007.01.009 1:CAS:528:DC%2BD2sXis1altLk%3D (Pubitemid 46216748)
20. YH Ma R Mentlein F Knerlich ML Kruse HM Mehdorn J Held-Feindt 2008 Expression of stem cell markers in human astrocytomas of different WHO grades J Neurooncol 86 31 45 17611714 10.1007/s11060-007-9439-7 (Pubitemid 350263430)
21. R Pallini L Ricci-Vitiani GL Banna M Signore D Lombardi M Todaro G Stassi M Martini G Maira LM Larocca MR De 2008 Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme Clin Cancer Res 14 8205 8212 19088037 10.1158/1078-0432.CCR-08-0644 1:CAS:528:DC%2BD1cXhsV2it7jN
22. SK Singh ID Clarke M Terasaki VE Bonn C Hawkins J Squire PB Dirks 2003 Identification of a cancer stem cell in human brain tumors Cancer Res 63 5821 5828 14522905 1:CAS:528:DC%2BD3sXnvVSjtbc%3D (Pubitemid 37187480)
23. E Fuchs T Tumbar G Guasch 2004 Socializing with the neighbors: stem cells and their niche Cell 116 769 778 15035980 10.1016/S0092-8674(04)00255-7 1:CAS:528:DC%2BD2cXivVyks7s%3D (Pubitemid 38410723)
24. TD Palmer AR Willhoite FH Gage 2000 Vascular niche for adult hippocampal neurogenesis J Comp Neurol 425 479 494 10975875 10.1002/1096-9861(20001002)425: 4<479::AID-CNE2>3.0.CO;2-3 1:STN:280:DC%2BD3cvlvVOmtw%3D%3D
25. N Sanai AD Tramontin A Quinones-Hinojosa NM Barbaro N Gupta S Kunwar MT Lawton MW McDermott AT Parsa VJ Manuel-Garcia MS Berger A Alvarez-Buylla 2004 Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration Nature 427 740 744 14973487 10.1038/nature02301 1:CAS:528:DC%2BD2cXhtlajsr0%3D (Pubitemid 38294593)
26. Q Shen SK Goderie L Jin N Karanth Y Sun N Abramova P Vincent K Pumiglia S Temple 2004 Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells Science 304 1338 1340 15060285 10.1126/science.1095505 1:CAS:528:DC%2BD2cXkt1Gnsrw%3D (Pubitemid 38697433)
27. Q Shen Y Wang E Kokovay G Lin SM Chuang SK Goderie B Roysam S Temple 2008 Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions Cell Stem Cell 3 289 300 18786416 10.1016/j.stem.2008.07. 026 1:CAS:528:DC%2BD1cXhtF2jtr%2FN
28. M Tavazoie DV Van V Silva-Vargas M Louissaint L Colonna B Zaidi JM Garcia-Verdugo F Doetsch 2008 A specialized vascular niche for adult neural stem cells Cell Stem Cell 3 279 288 18786415 10.1016/j.stem.2008.07.025 1:CAS:528:DC%2BD1cXhtF2jtr%2FM
29. S Bao Q Wu S Sathornsumetee Y Hao Z Li AB Hjelmeland Q Shi RE McLendon DD Bigner JN Rich 2006 Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor Cancer Res 66 7843 7848 16912155 10.1158/0008-5472.CAN-06-1010 1:CAS:528:DC%2BD28XotFWqsb8%3D (Pubitemid 44299144)
30. TN Kreisl L Kim K Moore P Duic C Royce I Stroud N Garren M Mackey JA Butman K Camphausen J Park PS Albert HA Fine 2008 Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma J Clin Oncol 27 740 745 19114704 10.1200/JCO.2008.16.3055
31. JJ Vredenburgh A Desjardins JE Herndon JM Dowell DA Reardon JA Quinn JN Rich S Sathornsumetee S Gururangan M Wagner DD Bigner AH Friedman HS Friedman 2007 Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma Clin Cancer Res 13 1253 1259 17317837 10.1158/1078-0432.CCR-06-2309 1:CAS:528:DC%2BD2sXhvF2htr8%3D (Pubitemid 46424067)
32. C Calabrese H Poppleton M Kocak TL Hogg C Fuller B Hamner EY Oh MW Gaber D Finklestein M Allen A Frank IT Bayazitov SS Zakharenko A Gajjar A Davidoff RJ Gilbertson 2007 A perivascular niche for brain tumor stem cells Cancer Cell 11 69 82 17222791 10.1016/j.ccr.2006.11.020 1:CAS:528:DC%2BD2sXhtFClsLY%3D (Pubitemid 46054518)
33. T Borovski JJ Verhoeff CR Ten K Cameron NA de Vries TO van DJ Richel WR van Furth JP Medema MR Sprick 2009 Tumor microvasculature supports proliferation and expansion of glioma-propagating cells Int J Cancer 125 1222 1230 19431144 10.1002/ijc.24408 1:CAS:528:DC%2BD1MXovVers7Y%3D
34. C Folkins S Man P Xu Y Shaked DJ Hicklin RS Kerbel 2007 Anticancer therapies combining antiangiogenic and tumor cell cytotoxic effects reduce the tumor stem-like cell fraction in glioma xenograft tumors Cancer Res 67 3560 3564 17440065 10.1158/0008-5472.CAN-06-4238 1:CAS:528:DC%2BD2sXkt1Kju70%3D (Pubitemid 46762138)
35. MJ Hendrix EA Seftor PS Meltzer LM Gardner AR Hess DA Kirschmann GC Schatteman RE Seftor 2001 Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in vasculogenic mimicry Proc Natl Acad Sci USA 98 8018 8023 11416160 10.1073/pnas.131209798 1:CAS:528: DC%2BD3MXlt1Kntbs%3D (Pubitemid 32642679)
36. Graham DI, Lantos PL (2002) Tumours of the nervous system. In: Graham DI, Lantos PL (eds) Greenfield's neuropathology Volume 2, 7th edn. Arnold, London, pp 768-1052
37. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (eds) (2007) WHO classification of tumours of the central nervous system. International Agency for Research on Cancer, Lyon
38. K Neckelmann BW Kristensen HD Schrøder 2004 Improved histopathological evaluation of gliomas using tissue fragments obtained by ultrasonic aspiration Clin-Neuropathol 23 47 52 15074577 1:STN:280: DC%2BD2c7nvFymtA%3D%3D (Pubitemid 38372548)
39. V Malhotra R Malik R Gondal PC Beohar B Parkash 1986 Evaluation of histological appearance of tissues removed by cavitron ultrasonic surgical aspirator (CUSA) Acta Neurochir 81 132 134 10.1007/BF01401235 1:STN:280:DyaL28zhvFCmuw%3D%3D (Pubitemid 16007442)
40. JF Silverman FD Jones M Unverferth L Berns 1989 Cytopathology of neoplasms of the central nervous system in specimens obtained by the cavitron ultrasonic surgical aspirator Acta Cytol 33 576 582 2476903 1:STN:280: DyaL1MzovFKqsQ%3D%3D (Pubitemid 19246114)
41. SR Shi C Liu L Pootrakul L Tang A Young R Chen RJ Cote CR Taylor 2008 Evaluation of the value of frozen tissue section used as "gold standard" for immunohistochemistry Am J Clin Pathol 129 358 366 18285257 10.1309/7CXUYXT23E5AL8KQ 1:CAS:528:DC%2BD1cXjvF2js7k%3D (Pubitemid 352029287)
42. HJ Gundersen 1992 Stereology: the fast lane between neuroanatomy and brain function-or still only a tightrope? Acta Neurol Scand Suppl 137 8 13 1357908 10.1111/j.1600-0404.1992.tb05032.x 1:STN:280:DyaK3s%2FjsVWmtQ%3D%3D
43. HJ Gundersen TF Bendtsen L Korbo N Marcussen A Moller K Nielsen JR Nyengaard B Pakkenberg FB Sorensen A Vesterby 1988 Some new, simple and efficient stereological methods and their use in pathological research and diagnosis APMIS 96 379 394 3288247 10.1111/j.1699-0463.1988.tb05320.x 1:STN:280:DyaL1c3ktVOjsQ%3D%3D
44. HJ Gundersen EB Jensen 1987 The efficiency of systematic sampling in stereology and its prediction J Microsc 147 229 263 3430576 10.1111/j.1365-2818. 1987.tb02837.x 1:STN:280:DyaL1c7hvVyltA%3D%3D
45. Y Mao L Zhou W Zhu X Wang G Yang L Xie X Mao K Jin 2007 Proliferative status of tumor stem cells may be correlated with malignancy grade of human astrocytomas Front Biosci 12 2252 2259 17127461 10.2741/2227 1:CAS:528:DC%2BD28Xht1WgsbfN
46. M Schmitz A Temme V Senner R Ebner S Schwind S Stevanovic R Wehner G Schackert HK Schackert M Fussel M Bachmann EP Rieber B Weigle 2007 Identification of SOX2 as a novel glioma-associated antigen and potential target for T cell-based immunotherapy Br J Cancer 96 1293 1301 17375044 10.1038/sj.bjc.6603696 1:CAS:528:DC%2BD2sXkt1GqtrY%3D (Pubitemid 46625072)
47. CV Pfenninger T Roschupkina F Hertwig D Kottwitz E Englund J Bengzon SE Jacobsen UA Nuber 2007 CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells Cancer Res 67 5727 5736 17575139 10.1158/0008-5472.CAN- 07-0183 1:CAS:528:DC%2BD2sXmsFCqsb4%3D (Pubitemid 46985005)
48. SW Bruggeman D Hulsman E Tanger T Buckle M Blom J Zevenhoven TO van LM van 2007 Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma Cancer Cell 12 328 341 17936558 10.1016/j.ccr.2007.08. 032 1:CAS:528:DC%2BD2sXht1ais7zO (Pubitemid 47539307)
49. G Liu X Yuan Z Zeng P Tunici H Ng IR Abdulkadir L Lu D Irvin KL Black JS Yu 2006 Analysis of gene expression and chemoresistance of CD133 + cancer stem cells in glioblastoma Mol Cancer 5 67 79 17140455 10.1186/1476-4598-5-67 (Pubitemid 44942887)
50. RJ Schrot JH Ma CM Greco AD Arias JM Angelastro 2007 Organotypic distribution of stem cell markers in formalin-fixed brain harboring glioblastoma multiforme J Neurooncol 85 149 157 17516028 10.1007/s11060-007-9401-8 (Pubitemid 47629396)
51. A Murat E Migliavacca T Gorlia WL Lambiv T Shay MF Hamou TN de L Regli W Wick MC Kouwenhoven JA Hainfellner FL Heppner PY Dietrich Y Zimmer JG Cairncross RC Janzer E Domany M Delorenzi R Stupp ME Hegi 2008 Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma J Clin Oncol 26 3015 3024 18565887 10.1200/JCO.2007.15.7164 1:CAS:528:DC%2BD1cXoslOqsLs%3D
52. S Bao Q Wu RE McLendon Y Hao Q Shi AB Hjelmeland MW Dewhirst DD Bigner JN Rich 2006 Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature 444 756 760 17051156 10.1038/nature05236 1:CAS:528:DC%2BD28Xht1OntbzP (Pubitemid 44949604)
53. A Eramo L Ricci-Vitiani A Zeuner R Pallini F Lotti G Sette E Pilozzi LM Larocca C Peschle MR De 2006 Chemotherapy resistance of glioblastoma stem cells Cell Death Differ 13 1238 1241 16456578 10.1038/sj.cdd.4401872 1:CAS:528:DC%2BD28Xls1Khtrs%3D (Pubitemid 43905604)
54. MK Kang SK Kang 2007 Tumorigenesis of chemotherapeutic drug-resistant cancer stem-like cells in brain glioma Stem Cells Dev 16 837 848 17999604 10.1089/scd.2007.0006 1:CAS:528:DC%2BD2sXht1ykurjN (Pubitemid 350125223)
55. K Mishima Y Kato MK Kaneko R Nishikawa T Hirose M Matsutani 2006 Increased expression of podoplanin in malignant astrocytic tumors as a novel molecular marker of malignant progression Acta Neuropathol 111 483 488 16596424 10.1007/s00401-006-0063-y 1:CAS:528:DC%2BD28XktFSqt78%3D
56. Y Nakamura Y Kanemura T Yamada Y Sugita K Higaki M Yamamoto M Takahashi M Yamasaki 2006 D2-40 antibody immunoreactivity in developing human brain, brain tumors and cultured neural cells Mod Pathol 19 974 985 16648867 10.1038/modpathol.3800616
57. J Shibahara T Kashima Y Kikuchi A Kunita M Fukayama 2006 Podoplanin is expressed in subsets of tumors of the central nervous system Virchows Arch 448 493 499 16411134 10.1007/s00428-005-0133-x 1:CAS:528:DC%2BD28XjtFamsL8%3D
58. M Zhang T Song L Yang R Chen L Wu J Fang 2008 Nestin and CD133: valuable stem cell-specific markers for determining clinical outcome of glioma patients J Exp Clin Cancer Res 27 85 100 19108713 10.1186/1756-9966-27-85 1:CAS:528:DC%2BD1cXhtlKitbjL
59. J Haapasalo A Mennander P Helen H Haapasalo J Isola 2005 Ultrarapid Ki-67 immunostaining in frozen section interpretation of gliomas J Clin Pathol 58 263 268 15735157 10.1136/jcp.2004.018606 1:STN:280:DC%2BD2M7gsVahtw%3D%3D (Pubitemid 40380320)
60. E Jaros RH Perry L Adam PJ Kelly PJ Crawford RM Kalbag AD Mendelow RP Sengupta AD Pearson 1992 Prognostic implications of p53 protein, epidermal growth factor receptor, and Ki-67 labelling in brain tumours Br J Cancer 66 373 385 1503912 10.1038/bjc.1992.273 1:STN:280:DyaK38zmvVyltA%3D%3D
61. JF Reavey-Cantwell RI Haroun M Zahurak RE Clatterbuck RJ Parker R Mehta JP Fruehauf H Brem 2001 The prognostic value of tumor markers in patients with glioblastoma multiforme: analysis of 32 patients and review of the literature J Neurooncol 55 195 204 11859975 10.1023/A:1013845004294 1:STN:280: DC%2BD387isFGhsg%3D%3D (Pubitemid 34134044)
62. UM Gehling S Ergun U Schumacher C Wagener K Pantel M Otte G Schuch P Schafhausen T Mende N Kilic K Kluge B Schafer DK Hossfeld W Fiedler 2000 In vitro differentiation of endothelial cells from AC133-positive progenitor cells Blood 95 3106 3112 10807776 1:CAS:528:DC%2BD3cXjt1equ7k%3D (Pubitemid 30321161)
63. W Hilbe S Dirnhofer F Oberwasserlechner T Schmid E Gunsilius G Hilbe E Woll CM Kahler 2004 CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer J Clin Pathol 57 965 969 15333659 10.1136/jcp.2004.016444 1:STN:280:DC%2BD2cvivVCgtA%3D%3D (Pubitemid 39208249)
64. M Peichev AJ Naiyer D Pereira Z Zhu WJ Lane M Williams MC Oz DJ Hicklin L Witte MA Moore S Rafii 2000 Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors Blood 95 952 958 10648408 1:CAS:528:DC%2BD3cXotV2gsA%3D%3D (Pubitemid 30062717)
65. P Salven S Mustjoki R Alitalo K Alitalo S Rafii 2003 VEGFR-3 and CD133 identify a population of CD34+lymphatic/vascular endothelial precursor cells Blood 101 168 172 12393704 10.1182/blood-2002-03-0755 1:CAS:528: DC%2BD3sXhtFWjuw%3D%3D (Pubitemid 36025904)
66. HR Zhang FL Chen CP Xu YF Ping QL Wang ZQ Liang JM Wang XW Bian 2008 Incorporation of endothelial progenitor cells into the neovasculature of malignant glioma xenograft J Neurooncol 93 165 174 10.1007/s11060-008-9757-4 19052696 10.1007/s11060-008-9757-4
67. J Rebetz D Tian A Persson B Widegren LG Salford E Englund D Gisselsson X Fan 2008 Glial progenitor-like phenotype in low-grade glioma and enhanced CD133-expression and neuronal lineage differentiation potential in high-grade glioma PLoS ONE 3 e1936 e1948 18398462 10.1371/journal.pone.0001936 (Pubitemid 351984112)
68. D Beier J Wischhusen W Dietmaier P Hau M Proescholdt A Brawanski U Bogdahn CP Beier 2008 CD133 expression and cancer stem cells predict prognosis in high-grade oligodendroglial tumors Brain Pathol 18 370 377 18371181 10.1111/j.1750-3639.2008.00130.x (Pubitemid 351782845)
69. PO Sakariassen H Immervoll M Chekenya 2007 Cancer stem cells as mediators of treatment resistance in brain tumors: status and controversies Neoplasia 9 882 892 18030356 10.1593/neo.07658 1:CAS:528:DC%2BD2sXhtl2rtrrK (Pubitemid 350086444)
70. PP Zheng WC Hop TM Luider PA Sillevis Smitt JM Kros 2007 Increased levels of circulating endothelial progenitor cells and circulating endothelial nitric oxide synthase in patients with gliomas Ann Neurol 62 40 48 17503506 10.1002/ana.21151 1:CAS:528:DC%2BD2sXhtVajsrrM (Pubitemid 47235279)
71. CM Baum IL Weissman AS Tsukamoto AM Buckle B Peault 1992 Isolation of a candidate human hematopoietic stem-cell population Proc Natl Acad Sci USA 89 2804 2808 1372992 10.1073/pnas.89.7.2804 1:STN:280:DyaK383ht12iug%3D%3D
72. VM Udani JG Santarelli YC Yung AJ Wagers SH Cheshier IL Weissman V Tse 2005 Hematopoietic stem cells give rise to perivascular endothelial-like cells during brain tumor angiogenesis Stem Cells Dev 14 478 486 16305333 10.1089/scd.2005.14.478 1:CAS:528:DC%2BD2MXht1GisLnF (Pubitemid 41780800)
73. Dong J, Zhao Y, Huang Q, Fei X, Diao Y, Shen Y, Xiao H, Zhang T, Lan Q, Gu X (2010) Glioma stem/progenitor cells contribute to neovascularization via transdifferentiation. Stem Cell Rev. doi: 10.1007/s12015-010-9169-7
74. Y Zhao J Dong Q Huang M Lou A Wang Q Lan 2010 Endothelial cell transdifferentiation of human glioma stem progenitor cells in vitro Brain Res Bull 82 308 312 20599593 10.1016/j.brainresbull.2010.06.006 1:CAS:528: DC%2BC3cXpt12nur4%3D
75. MS Ahluwalia CL Gladson 2010 Progress on antiangiogenic therapy for patients with malignant glioma J Oncol 2010 689018 20379377
76. MC Tate MK Aghi 2009 Biology of angiogenesis and invasion in glioma Neurotherapeutics 6 447 457 19560735 10.1016/j.nurt.2009.04.001 1:CAS:528:DC%2BD1MXhsFent7bN
77. CE Griguer CR Oliva E Gobin P Marcorelles DJ Benos JR Lancaster Jr GY Gillespie 2008 CD133 is a marker of bioenergetic stress in human glioma PLoS ONE 3 e3655 18985161 10.1371/journal.pone.0003655
78. S Seidel BK Garvalov V Wirta SL Von A Schanzer K Meletis M Wolter D Sommerlad AT Henze M Nister G Reifenberger J Lundeberg J Frisen T Acker 2010 A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha Brain 133 983 995 20375133 10.1093/brain/awq042
79. M Sanchez-Beato E Sanchez J Gonzalez-Carrero M Morente A Diez L Sanchez-Verde MC Martin JC Cigudosa M Vidal MA Piris 2006 Variability in the expression of polycomb proteins in different normal and tumoral tissues. A pilot study using tissue microarrays Mod Pathol 19 684 694 16528373 10.1038/modpathol.3800577 1:CAS:528:DC%2BD28Xjs1agtbY%3D
80. G Kania D Corbeil J Fuchs KV Tarasov P Blyszczuk WB Huttner KR Boheler AM Wobus 2005 Somatic stem cell marker prominin-1/CD133 is expressed in embryonic stem cell-derived progenitors Stem Cells 23 791 804 15917475 10.1634/stemcells.2004-0232 1:CAS:528:DC%2BD2MXlslCltbw%3D (Pubitemid 40791794)
81. M Florek M Haase AM Marzesco D Freund G Ehninger WB Huttner D Corbeil 2005 Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer Cell Tissue Res 319 15 26 15558321 10.1007/s00441-004-1018-z 1:CAS:528: DC%2BD2cXhtVGgtLjE (Pubitemid 40104635)
82. F Aroca W Renaud C Bartoli C Bouvier-Labit D Figarella-Branger 1999 Expression of PECAM-1/CD31 isoforms in human brain gliomas J Neurooncol 43 19 25 10448867 10.1023/A:1006233816724 1:STN:280:DyaK1Mzns1SqtQ%3D%3D (Pubitemid 29351973)
83. ZS Tuncer GL Vegh V Fulop DR Genest SC Mok RS Berkowitz 2000 Expression of epidermal growth factor receptor-related family products in gestational trophoblastic diseases and normal placenta and its relationship with development of postmolar tumor Gynecol Oncol 77 389 393 10831347 10.1006/gyno.2000.5777 1:CAS:528:DC%2BD3cXjs1Wgt7g%3D (Pubitemid 30368555)
84. J Dahlstrand VP Collins U Lendahl 1992 Expression of the class VI intermediate filament nestin in human central nervous system tumors Cancer Res 52 5334 5341 1382841 1:CAS:528:DyaK38XmtlWhurw%3D
85. HJ Kahn D Bailey A Marks 2002 Monoclonal antibody D2-40, a new marker of lymphatic endothelium, reacts with Kaposi's sarcoma and a subset of angiosarcomas Mod Pathol 15 434 440 11950918 10.1038/modpathol.3880543 (Pubitemid 34326952)
86. AL Ferri M Cavallaro D Braida CA Di A Canta A Vezzani S Ottolenghi PP Pandolfi M Sala S DeBiasi SK Nicolis 2004 Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain Development 131 3805 3819 15240551 10.1242/dev.01204 1:CAS:528:DC%2BD2cXnt1eltLg%3D (Pubitemid 39199387)
87. LE Stuhr A Raa AM Oyan KH Kalland PO Sakariassen K Petersen R Bjerkvig RK Reed 2007 Hyperoxia retards growth and induces apoptosis, changes in vascular density and gene expression in transplanted gliomas in nude rats J Neurooncol. 82 191 202 10.1007/s11060-007-9407-2 (Pubitemid 47629400)