Molecular analysis of ex-vivo CD133+ GBM cells revealed a common invasive and angiogenic profile but different proliferative signatures among high grade gliomas

BMC Cancer

Volumn 10, Issue , 2010, Pages

  Garcia, Juan L ^a,b   Perez Caro, Maria ^c   Gomez Moreta, Juan A ^d   Gonzalez, Francisco ^c   Ortiz, Javier ^d   Blanco, Oscar ^d   Sancho, Magdalena ^d   Hernandez Rivas, Jesus M ^b,d   Gonzalez Sarmiento, Rogelio ^b,e   Sanchez Martin, Manuel ^e  

^a Instituto de Estudios de Salud de Castilla y León IESCyL   (Spain)

^b CSIC   (Spain)

^c OncoStem Pharma SL ^*  (Spain)

^d HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

^e UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD133 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; TEMOZOLOMIDE; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; MESSENGER RNA; PEPTIDE; TUMOR MARKER;

ADULT; AGED; ARTICLE; BIOTINYLATION; CELL POPULATION; CELL VIABILITY; CLINICAL ARTICLE; COMPARATIVE GENOMIC HYBRIDIZATION; DOWN REGULATION; EX VIVO STUDY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; GENE AMPLIFICATION; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENETIC ANALYSIS; GLIOBLASTOMA; GLIOMA; HUMAN; MALE; NUCLEOTIDE SEQUENCE; PROTEIN METHYLATION; UPREGULATION; BRAIN TUMOR; DNA MICROARRAY; FLOW CYTOMETRY; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AGED; ANTIGENS, CD; BRAIN NEOPLASMS; COMPARATIVE GENOMIC HYBRIDIZATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GLIOBLASTOMA; GLYCOPROTEINS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR MARKERS, BIOLOGICAL;

EID: 77955821735     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-10-454     Document Type: Article

References (66)

1. Sanchez-Martin M. Brain tumour stem cells: implications for cancer therapy and regenerative medicine. Curr Stem Cell Res Ther 2008, 3(3):197-207. 18782002, 10.2174/157488808785740370.
2. Perez-Losada J, Gutierrez-Cianca N, Sanchez-Garcia I. Philadelphia-positive B-cell acute lymphoblastic leukemia is initiated in an uncommitted progenitor cell. Leuk Lymphoma 2001, 42(4):569-576. 10.3109/10428190109099316, 11697484.
3. Perez-Caro M, Gutierrez-Cianca N, Gonzalez-Herrero I, Lopez-Hernandez I, Flores T, Orfao A, Sanchez-Martin M, Gutierrez-Adan A, Pintado B, Sanchez-Garcia I. Sustained leukaemic phenotype after inactivation of BCR-ABLp190 in mice. Oncogene 2007, 26(12):1702-1713. 10.1038/sj.onc.1209968, 16983340.
4. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100(7):3983-3988. 10.1073/pnas.0530291100, 153034, 12629218.
5. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer research 2003, 63(18):5821-5828.
6. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature 2004, 432(7015):396-401. 10.1038/nature03128, 15549107.
7. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer research 2004, 64(19):7011-7021. 10.1158/0008-5472.CAN-04-1364, 15466194.
8. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney A, Huang EH, Simeone DM, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 2007, 104(24):10158-10163. 10.1073/pnas.0703478104, 1891215, 17548814.
9. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445(7123):106-110. 10.1038/nature05372, 17122772.
10. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445(7123):111-115. 10.1038/nature05384, 17122771.
11. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, Weissman IL, Clarke MF, Ailles LE. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007, 104(3):973-978. 10.1073/pnas.0610117104, 1783424, 17210912.
12. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM. Identification of pancreatic cancer stem cells. Cancer research 2007, 67(3):1030-1037. 10.1158/0008-5472.CAN-06-2030, 17283135.
13. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol (Berl) 2007, 114(2):97-109.
14. Li A, Walling J, Ahn S, Kotliarov Y, Su Q, Quezado M, Oberholtzer JC, Park J, Zenklusen JC, Fine HA. Unsupervised analysis of transcriptomic profiles reveals six glioma subtypes. Cancer research 2009, 69(5):2091-2099. 10.1158/0008-5472.CAN-08-2100, 2845963, 19244127.
15. Miller CR, Perry A. Glioblastoma. Arch Pathol Lab Med 2007, 131(3):397-406.
16. Tate MC, Aghi MK. Biology of Angiogenesis and Invasion in Glioma. Neurotherapeutics 2009, 6(3):447-457. 10.1016/j.nurt.2009.04.001, 19560735.
17. Gilbertson RJ, Rich JN. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer 2007, 7(10):733-736. 10.1038/nrc2246, 17882276.
18. Reynolds BA, Rietze RL. Neural stem cells and neurospheres--re-evaluating the relationship. Nat Methods 2005, 2(5):333-336. 10.1038/nmeth758, 15846359.
19. Pevny L, Rao MS. The stem-cell menagerie. Trends in neurosciences 2003, 26(7):351-359. 10.1016/S0166-2236(03)00169-3, 12850431.
20. Morrison SJ, White PM, Zock C, Anderson DJ. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 1999, 96(5):737-749. 10.1016/S0092-8674(00)80583-8, 10089888.
21. Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 2000, 97(26):14720-14725. 10.1073/pnas.97.26.14720, 18985, 11121071.
22. Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997, 90(12):5002-5012.
23. Fricker RA, Carpenter MK, Winkler C, Greco C, Gates MA, Bjorklund A. Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J Neurosci 1999, 19(14):5990-6005.
24. Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier CP. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer research 2007, 67(9):4010-4015. 10.1158/0008-5472.CAN-06-4180, 17483311.
25. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic acids research 2002, 30(1):207-210. 10.1093/nar/30.1.207, 99122, 11752295.
26. Herrero J, Al-Shahrour F, Diaz-Uriarte R, Mateos A, Vaquerizas JM, Santoyo J, Dopazo J. GEPAS: A web-based resource for microarray gene expression data analysis. Nucleic acids research 2003, 31(13):3461-3467. 10.1093/nar/gkg591, 168997, 12824345.
27. Sebat J, Lakshmi B, Troge J, Alexander J, Young J, Lundin P, Maner S, Massa H, Walker M, Chi M, et al. Large-scale copy number polymorphism in the human genome. Science 2004, 305(5683):525-528. New York, NY, 15273396, 10.1126/science.1098918.
28. Iafrate AJ, Feuk L, Rivera MN, Listewnik ML, Donahoe PK, Qi Y, Scherer SW, Lee C. Detection of large-scale variation in the human genome. Nat Genet 2004, 36(9):949-951. 10.1038/ng1416, 15286789.
29. Olshen AB, Venkatraman ES, Lucito R, Wigler M. Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics 2004, 5(4):557-572. 10.1093/biostatistics/kxh008, 15475419.
30. Hernandez JM, Schoenmakers EF, Dal Cin P, Michaux L, Van de Ven WJ, Van den Berghe H. Molecular delineation of the commonly deleted segment in mature B-cell lymphoid neoplasias with deletion of 7q. Genes Chromosomes Cancer 1997, 18(2):147-150. 9115965, 10.1002/(SICI)1098-2264(199702)18:2<147::AID-GCC10>3.0.CO;2-H.
31. Ivanov AI, Pero RS, Scheck AC, Romanovsky AA. Prostaglandin E(2)-synthesizing enzymes in fever: differential transcriptional regulation. American journal of physiology 2002, 283(5):R1104-1117.
32. Jeuken JW, Cornelissen SJ, Vriezen M, Dekkers MM, Errami A, Sijben A, Boots-Sprenger SH, Wesseling P. MS-MLPA: an attractive alternative laboratory assay for robust, reliable, and semiquantitative detection of MGMT promoter hypermethylation in gliomas. Laboratory investigation; a journal of technical methods and pathology 2007, 87(10):1055-1065. 10.1038/labinvest.3700664, 17700563.
33. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006, 5:67. 10.1186/1476-4598-5-67, 1697823, 17140455.
34. Kang MK, Kang SK. Tumorigenesis of chemotherapeutic drug-resistant cancer stem-like cells in brain glioma. Stem cells and development 2007, 16(5):837-847. 10.1089/scd.2007.0006, 17999604.
35. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444(7120):756-760. 10.1038/nature05236, 17051156.
36. Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier CP. CD133+ and CD133- Glioblastoma-Derived Cancer Stem Cells Show Differential Growth Characteristics and Molecular Profiles. Cancer research 2007, 67(9):4010-4015. 10.1158/0008-5472.CAN-06-4180, 17483311.
37. Hoelzinger DB, Mariani L, Weis J, Woyke T, Berens TJ, McDonough WS, Sloan A, Coons SW, Berens ME. Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets. Neoplasia 2005, 7(1):7-16. New York, NY, 15720813, PMC1490313, 10.1593/neo.04535.
38. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 2001, 7(5):575-583. 10.1038/87904, 11329059.
39. Jackson CJ, Jenkins KL. Type I collagen fibrils promote rapid vascular tube formation upon contact with the apical side of cultured endothelium. Experimental Cell Research 1991, 192(1):319-323. 10.1016/0014-4827(91)90194-Y, 1701729.
40. Ramirez F, Di Liberto M. Complex and diversified regulatory programs control the expression of vertebrate collagen genes. FASEB J 1990, 4(6):1616-1623.
41. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A. Isolation and Characterization of Tumorigenic, Stem-like Neural Precursors from Human Glioblastoma. Cancer research 2004, 64(19):7011-7021. 10.1158/0008-5472.CAN-04-1364, 15466194.
42. Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS. Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 2004, 23:9392-9400. 10.1038/sj.onc.1208311, 15558011.
43. Ma C, Rong Y, Radiloff DR, Datto MB, Centeno B, Bao S, Cheng AW, Lin F, Jiang S, Yeatman TJ, et al. Extracellular matrix protein betaig-h3/TGFBI promotes metastasis of colon cancer by enhancing cell extravasation. Genes & development 2008, 22(3):308-321. 2216691, 18245446, 10.1101/gad.1632008.
44. Christensen K, Schroder HD, Kristensen BW. CD133 identifies perivascular niches in grade II-IV astrocytomas. Journal of neuro-oncology 2008, 90(2):157-170. 10.1007/s11060-008-9648-8, 18612800.
45. Palmer T, Willhoite A, Gage F. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000, 425(4):479-494. 10.1002/1096-9861(20001002)425:4<479::AID-CNE2>3.0.CO;2-3, 10975875.
46. Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C, Ferron SR, Aroca-Aguilar JD, Sanchez P, Mira H, Escribano J, Farinas I. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci 2006, 9(3):331-339. 10.1038/nn1657, 16491078.
47. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, et al. A Perivascular Niche for Brain Tumor Stem Cells. Cancer Cell 2007, 11(1):69-82. 10.1016/j.ccr.2006.11.020, 17222791.
48. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, McLendon RE, Bigner DD, Rich JN. Stem Cell-like Glioma Cells Promote Tumor Angiogenesis through Vascular Endothelial Growth Factor. Cancer research 2006, 66(16):7843-7848. 10.1158/0008-5472.CAN-06-1010, 16912155.
49. Rikiyama T, Curtis J, Oikawa M, Zimonjic DB, Popescu N, Murphy BA, Wilson MA, Johnson AC. GCF2: expression and molecular analysis of repression. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression 2003, 1629(1-3):15-25.
50. Elahi A, Zhang L, Yeatman TJ, Gery S, Sebti S, Shibata D. HPP1-mediated tumor suppression requires activation of STAT1 pathways. International journal of cancer 2008, 122(7):1567-1572.
51. Besson A, Wilson TL, Yong VW. The anchoring protein RACK1 links protein kinase Cepsilon to integrin beta chains. Requirements for adhesion and motility. The Journal of biological chemistry 2002, 277(24):22073-22084. 10.1074/jbc.M111644200, 11934885.
52. Fukata Y, Itoh TJ, Kimura T, Menager C, Nishimura T, Shiromizu T, Watanabe H, Inagaki N, Iwamatsu A, Hotani H, et al. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 2002, 4(8):583-591.
53. Poirier K, Keays D, Francis F, Saillour Y, Bahi N, Manouvrier S, Fallet-Bianco C, Pasquier L, Toutain A, Tuy F, et al. Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A). Hum Mutat 2007, 28(11):1055-1064. 10.1002/humu.20572, 17584854.
54. Bellenchi GC, Gurniak CB, Perlas E, Middei S, Ammassari-Teule M, Witke W. N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes Dev 2007, 21(18):2347-2357. PMC1973148, 17875668, 10.1101/gad.434307.
55. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 2004, 304(5671):743-746. New York, NY, 15118165, 10.1126/science.1094561.
56. Harris AL. Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2002, 2(1):38-47. 10.1038/nrc704, 11902584.
57. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, et al. IDH1 and IDH2 mutations in gliomas. The New England journal of medicine 2009, 360(8):765-773. 10.1056/NEJMoa0808710, 2820383, 19228619.
58. Balss J, Meyer J, Mueller W, Korshunov A, Hartmann C, von Deimling A. Analysis of the IDH1 codon 132 mutation in brain tumors. Acta neuropathologica 2008, 116(6):597-602. 10.1007/s00401-008-0455-2, 18985363.
59. Mor-Vaknin N, Punturieri A, Sitwala K, Markovitz DM. Vimentin is secreted by activated macrophages. Nat Cell Biol 2003, 5(1):59-63. 10.1038/ncb898, 12483219.
60. Nieminen M, Henttinen T, Merinen M, Marttila-Ichihara F, Eriksson JE, Jalkanen S. Vimentin function in lymphocyte adhesion and transcellular migration. Nat Cell Biol 2006, 8(2):156-162. 10.1038/ncb1355, 16429129.
61. Confalonieri S, Quarto M, Goisis G, Nuciforo P, Donzelli M, Jodice G, Pelosi G, Viale G, Pece S, Di Fiore PP. Alterations of ubiquitin ligases in human cancer and their association with the natural history of the tumor. Oncogene 2009, 28(33):2959-2968. 10.1038/onc.2009.156, 19543318.
62. D'Arca D, Zhao X, Xu W, Ramirez-Martinez NC, Iavarone A, Lasorella A. Huwe1 ubiquitin ligase is essential to synchronize neuronal and glial differentiation in the developing cerebellum. PNAS 2010, 107(13):5875-5880. 10.1073/pnas.0912874107, 2851916, 20231446.
63. Haberle J, Gorg B, Rutsch F, Schmidt E, Toutain A, Benoist JF, Gelot A, Suc AL, Hohne W, Schliess F, et al. Congenital glutamine deficiency with glutamine synthetase mutations. The New England journal of medicine 2005, 353(18):1926-1933. 10.1056/NEJMoa050456, 16267323.
64. Golsteyn RM, Mundt KE, Fry AM, Nigg EA. Cell cycle regulation of the activity and subcellular localization of Plk1, a human protein kinase implicated in mitotic spindle function. The Journal of cell biology 1995, 129(6):1617-1628. 10.1083/jcb.129.6.1617, 2291169, 7790358.
65. Degenhardt Y, Lampkin T. Targeting Polo-like Kinase in Cancer Therapy. Clin Cancer Res 2010, 16(2):384-389. 10.1158/1078-0432.CCR-09-1380, 20068088.
66. Toyoshima-Morimoto F, Taniguchi E, Shinya N, Iwamatsu A, Nishida E. Polo-like kinase 1 phosphorylates cyclin B1 and targets it to the nucleus during prophase. Nature 2001, 410(6825):215-220. 10.1038/35065617, 11242082.