Glioma revisited: From neurogenesis and cancer stem cells to the epigenetic regulation of the niche

Journal of Oncology

Volumn , Issue , 2012, Pages

  De Almeida Sassi, Felipe ^a,b   Lunardi Brunetto, Algemir ^a,c   Schwartsmann, Gilberto ^a,b,c   Roesler, Rafael ^a,b,c   Abujamra, Ana Lucia ^a,b,c  

^a HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^c National Institute for Translational Medicine INCT TM   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER CELL; CANCER GENETICS; CANCER GROWTH; CANCER STEM CELL; CARCINOGENESIS; CELL HETEROGENEITY; CELL HYPOXIA; EPIGENETICS; GENETIC REGULATION; GLIOBLASTOMA; GLIOMA; HUMAN; NONHUMAN; PRIMORDIAL GERM CELL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL NICHE; SUBVENTRICULAR ZONE; TUMOR MICROENVIRONMENT;

EID: 84867008591     PISSN: 16878450     EISSN: 16878469     Source Type: Journal    
DOI: 10.1155/2012/537861     Document Type: Review

References (153)

1. Eriksson P. S., Perfilieva E., Björk-Eriksson T., Alborn A. M., Nordborg C., Peterson D. A., Gage F. H., Neurogenesis in the adult human hippocampus. Nature Medicine 1998 4 11 1313 1317 2-s2.0-0031789814 10.1038/3305 (Pubitemid 28512114)
2. Quiones-Hinojosa A., Chaichana K., The human subventricular zone: a source of new cells and a potential source of brain tumors. Experimental Neurology 2007 205 2 313 324 2-s2.0-34248581586 10.1016/j.expneurol.2007.03.016 (Pubitemid 46755774)
3. Doetsch F., Caille I., Lim D. A., Garcia-Verdugo J. M., Alvarez-Buylla A., Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999 97 6 703 716 2-s2.0-0033040497 10.1016/S0092-8674(00)80783-7 (Pubitemid 29278045)
4. Lois C., Alvarez-Buylla A., Long-distance neuronal migration in the adult mammalian brain. Science 1994 264 5162 1145 1148 2-s2.0-0028361594 (Pubitemid 24210676)
5. Ahn S., Joyner A. L., In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 2005 437 7060 894 897 2-s2.0-27144487469 10.1038/nature03994 (Pubitemid 41486765)
6. Riquelme P. A., Drapeau E., Doetsch F., Brain micro-ecologies: neural stem cell niches in the adult mammalian brain. Philosophical Transactions of the Royal Society B 2008 363 1489 123 137 2-s2.0-36448982477 10.1098/rstb.2006.2016 (Pubitemid 350174578)
7. Mirzadeh Z., Merkle F. T., Soriano-Navarro M., Garcia-Verdugo J. M., Alvarez-Buylla A., Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008 3 3 265 278 2-s2.0-50849113768 10.1016/j.stem.2008.07.004
8. Bouab M., Paliouras G. N., Aumont A., Forest-Bérard K., Fernandes K. J. L., Aging of the subventricular zone neural stem cell niche: evidence for quiescence-associated changes between early and mid-adulthood. Neuroscience 2011 173 135 149 2-s2.0-78650679757 10.1016/j.neuroscience.2010.11.032
9. Sanai H., Tramontin A. D., Quiones-Hinojosa A., Barbaro N. M., Gupta H., Kunwar S., Lawton M. T., McDermott M. W., Parsa A. T., Verdugo J. M. G., Berger M. S., Alvarez-Buylla A., Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004 427 6976 740 744 2-s2.0-1442354188 10.1038/nature02301 (Pubitemid 38294593)
10. Chaichana K., Zamora-Berridi G., Camara-Quintana J., Quiones-Hinojosa A., Neurosphere assays: growth factors and hormone differences in tumor and nontumor studies. Stem Cells 2006 24 12 2851 2857 2-s2.0-33845988686 10.1634/stemcells.2006-0399 (Pubitemid 46053021)
11. Kukekov V. G., Laywell E. D., Suslov O., Davies K., Scheffler B., Thomas L. B., O'Brien T. F., Kusakabe M., Steindler D. A., Multipotent stem/progenitor cells with similar properties arise from neurogenic regions of adult human brain. Experimental Neurology 1999 156 2 333 344 2-s2.0-0032909852 10.1006/exnr.1999.7028 (Pubitemid 29205008)
12. Quiones-Hinojosa A., Sanai N., Soriano-Navarro M., Gonzalez-Perez O., Mirzadeh Z., Gil-Perotin S., Romero-Rodriguez R., Berger M. S., Garcia-Verdugo J. M., Alvarez-Buylla A., Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. Journal of Comparative Neurology 2006 494 3 415 434 2-s2.0-29144483551 10.1002/cne.20798 (Pubitemid 41794059)
13. Gates M. A., Thomas L. B., Howard E. M., Laywell E. D., Sajin B., Faissner A., Gotz B., Silver J., Steindler D. A., Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. Journal of Comparative Neurology 1995 361 2 249 266 2-s2.0-0028808672 10.1002/cne.903610205
14. Capela A., Temple S., LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002 35 5 865 875 2-s2.0-0037194887 10.1016/S0896-6273(02)00835-8
15. Kuhn H. G., Dickinson-Anson H., Gage F. H., Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. Journal of Neuroscience 1996 16 6 2027 2033 2-s2.0-0029863342 (Pubitemid 26144015)
16. Cameron H. A., Mckay R. D. G., Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. Journal of Comparative Neurology 2001 435 4 406 417 2-s2.0-0035833068 10.1002/cne.1040 (Pubitemid 32574293)
17. Bull N. D., Bartlett P. F., The adult mouse hippocampal progenitor is neurogenic but not a stem cell. Journal of Neuroscience 2005 25 47 10815 10821 2-s2.0-28044445073 10.1523/JNEUROSCI.3249-05.2005 (Pubitemid 41692611)
18. Seaberg R. M., Van der Kooy D., Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. Journal of Neuroscience 2002 22 5 1784 1793 2-s2.0-0036522968 (Pubitemid 35386296)
19. Vukovic J., Blackmore D. G., Jhaveri D., Bartlett P. F., Activation of neural precursors in the adult neurogenic niches. Neurochemistry International 2011 59 3 341 346 2-s2.0-79959678532 10.1016/j.neuint.2011.04.003
20. Bruel-Jungerman E., Davis S., Rampon C., Laroche S., Long-term potentiation enhances neurogenesis in the adult dentate gyrus. Journal of Neuroscience 2006 26 22 5888 5893 2-s2.0-33745276538 10.1523/JNEUROSCI.0782-06. 2006 (Pubitemid 44318353)
21. Chun S. K., Sun W., Park J. J., Jung M. W., Enhanced proliferation of progenitor cells following long-term potentiation induction in the rat dentate gyrus. Neurobiology of Learning and Memory 2006 86 3 322 329 2-s2.0-33748945385 10.1016/j.nlm.2006.05.005 (Pubitemid 44436977)
22. Bath K. G., Lee F. S., Neurotrophic factor control of adult SVZ neurogenesis. Developmental Neurobiology 2010 70 5 339 349 2-s2.0-77949747257 10.1002/dneu.20781
23. Linnarsson S., Willson C. A., Ernfors P., Cell death in regenerating populations of neurons in BDNF mutant mice. Molecular Brain Research 2000 75 1 61 69 2-s2.0-0033954760 10.1016/S0169-328X(99)00295-8 (Pubitemid 30058326)
24. Giuliani A., D'Intino G., Paradisi M., Giardino L., Calzà L., p75NTR-Immunoreactivity in the subventricular zone of adult male rats: expression by cycling cells. Journal of Molecular Histology 2004 35 8-9 749 758 2-s2.0-16644374997 10.1007/s10735-004-9609-2 (Pubitemid 41404620)
25. Ip N. Y., McClain J., Barrezueta N. X., Aldrich T. H., Pan L., Li Y., Wiegand S. J., Friedman B., Davis S., Yancopoulos G. D., The α component of the CNTF receptor is required for signaling and defines potential CNTF targets in the adult and during development. Neuron 1993 10 1 89 102 2-s2.0-0027403260 10.1016/0896-6273(93)90245-M (Pubitemid 23045429)
26. Lee J., Kotliarova S., Kotliarov Y., Li A., Su Q., Donin N. M., Pastorino S., Purow B. W., Christopher N., Zhang W., Park J. K., Fine H. A., Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006 9 5 391 403 2-s2.0-33646358694 10.1016/j.ccr.2006.03.030 (Pubitemid 43668737)
27. Morshead C. M., Garcia A. D., Sofroniew M. V., Van Der Kooy D., The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. European Journal of Neuroscience 2003 18 1 76 84 2-s2.0-0043169430 10.1046/j.1460-9568.2003.02727.x (Pubitemid 36920847)
28. Pincus D. W., Keyoung H. M., Harrison-Restelli C., Goodman R. R., Fraser R. A. R., Edgar M., Sakakibara S. I., Okano H., Nedergaard M., Goldman S. A., Fibroblast growth factor-2/brain-derived neurotrophic factor-associated maturation of new neurons generated from adult human subependymal cells. Annals of Neurology 1998 43 5 576 585 2-s2.0-15644372867 10.1002/ana.410430505 (Pubitemid 28225548)
29. Sun Y., Jin K., Childs J. T., Xie L., Mao X. O., Greenberg D. A., Vascular endothelial growth factor-B (VEGFB) stimulates neurogenesis: evidence from knockout mice and growth factor administration. Developmental Biology 2006 289 2 329 335 2-s2.0-30044451865 10.1016/j.ydbio.2005.10.016 (Pubitemid 43049936)
30. Tropepe V., Craig C. G., Morshead C. M., Van Kooy D. D., Transforming growth factor- α null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. Journal of Neuroscience 1997 17 20 7850 7859 2-s2.0-0030826603 (Pubitemid 27426222)
31. Wittko I. M., Schänzer A., Kuzmichev A., Schneider F. T., Shibuya M., Raab S., Plate K. H., VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream In vivo. Journal of Neuroscience 2009 29 27 8704 8714 2-s2.0-67650487559 10.1523/JNEUROSCI.5527-08.2009
32. Jackson E. L., Garcia-Verdugo J. M., Gil-Perotin S., Roy M., Quinones-Hinojosa A., VandenBerg S., Alvarez-Buylla A., PDGFR α -positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006 51 2 187 199 2-s2.0-33745880884 10.1016/j.neuron.2006.06.012 (Pubitemid 44063617)
33. Jackson E. L., Alvarez-Buylla A., Characterization of adult neural stem cells and their relation to brain tumors. Cells Tissues Organs 2008 188 1-2 212 224 2-s2.0-46949108513 10.1159/000114541 (Pubitemid 351962244)
34. Erlandsson A., Brännvall K., Gustafsdottir S., Westermark B., Forsberg-Nilsson K., Autocrine/paracrine platelet-derived growth factor regulates proliferation of neural progenitor cells. Cancer Research 2006 66 16 8042 8048 2-s2.0-33748041449 10.1158/0008-5472.CAN-06-0900 (Pubitemid 44299169)
35. Goldberg J. S., Hirschi K. K., Diverse roles of the vasculature within the neural stem cell niche. Regenerative Medicine 2009 4 6 879 897 2-s2.0-75649144081 10.2217/rme.09.61
36. Sun Y., Hu J., Zhou L., Pollard S. M., Smith A., Interplay between FGF2 and BMP controls the self-renewal, dormancy and differentiation of rat neural stem cells. Journal of Cell Science 2011 124 11 1867 1877 2-s2.0-79958195179 10.1242/jcs.085506
37. Nam H. S., Benezra R., High levels of Id1 expression define B1 type adult neural stem cells. Cell Stem Cell 2009 5 5 515 526 2-s2.0-70350494493 10.1016/j.stem.2009.08.017
38. Hanahan D., Weinberg R. A., Hallmarks of cancer: the next generation. Cell 2011 144 5 646 674 2-s2.0-79952284127 10.1016/j.cell.2011.02.013
39. Van Meir E. G., Kikuchi T., Tada M., Li H., Diserens A. C., Wojcik B. E., Huang H. J. S., Friedmann T., De Tribolet N., Cavenee W. K., Analysis of the p53 gene and its expression in human glioblastoma cells. Cancer Research 1994 54 3 649 652 2-s2.0-0028117269 (Pubitemid 24068319)
40. Ricci-Vitiani L., Pallini R., Biffoni M., Todaro M., Invernici G., Cenci T., Maira G., Parati E. A., Stassi G., Larocca L. M., De Maria R., Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010 468 7325 824 830 2-s2.0-78650153633 10.1038/nature09557
41. Wurmser A. E., Nakashima K., Summers R. G., Toni N., D'Amour K. A., Lie D. C., Cage F. H., Cell fusion-independent differentiation of neural stem cells to the endothelial lineage. Nature 2004 430 6997 350 356 2-s2.0-3142753475 10.1038/nature02604 (Pubitemid 38937742)
42. Clevers H., The cancer stem cell: premises, promises and challenges. Nature Medicine 2011 17 3 313 319 2-s2.0-79952370202 10.1038/nm.2304
43. Gage F. H., Neurogenesis in the adult brain. Journal of Neuroscience 2002 22 3 612 613 2-s2.0-0036469896 (Pubitemid 34141738)
44. Siebzehnrubl F. A., Reynolds B. A., Vescovi A., Steindler D. A., Deleyrolle L. P., The origins of glioma: E Pluribus Unum? GLIA 2011 59 8 1135 1147 2-s2.0-79957922064 10.1002/glia.21143
45. Barami K., Sloan A. E., Rojiani A., Schell M. J., Staller A., Brem S., Relationship of gliomas to the ventricular walls. Journal of Clinical Neuroscience 2009 16 2 195 201 2-s2.0-58149200892 10.1016/j.jocn.2008.03.006
46. Canoll P., Goldman J. E., The interface between glial progenitors and gliomas. Acta Neuropathologica 2008 116 5 465 477 2-s2.0-54149085908 10.1007/s00401-008-0432-9
47. Bohman L. E., Swanson K. R., Moore J. L., Rockne R., Mandigo C., Hankinson T., Assanah M., Canoll P., Bruce J. N., Magnetic resonance imaging characteristics of glioblastoma multiforme: implications for understanding glioma ontogeny. Neurosurgery 2010 67 5 1319 1327 2-s2.0-77958515020 10.1227/NEU.0b013e3181f556ab
48. Alcantara Llaguno S., Chen J., Kwon C. H., Jackson E. L., Li Y., Burns D. K., Alvarez-Buylla A., Parada L. F., Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 2009 15 1 45 56 2-s2.0-57849109837 10.1016/j.ccr.2008.12.006
49. van den Berge S. A., Middeldorp J., Eleana Zhang C., Curtis M. A., Leonard B. W., Mastroeni D., Voorn P., van de Berg W. D. J., Huitinga I., Hol E. M., Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP- δ Aging Cell 2010 9 3 313 326 2-s2.0-77955271817 10.1111/j.1474-9726.2010.00556.x
50. Foroni C., Galli R., Cipelletti B., Caumo A., Alberti S., Fiocco R., Vescovi A., Resilience to transformation and inherent genetic and functional stability of adult neural stem cells ex vivo. Cancer Research 2007 67 8 3725 3733 2-s2.0-34248595985 10.1158/0008-5472.CAN-06-4577 (Pubitemid 46762158)
51. Jiang Y., Uhrbom L., On the origin of glioma. Upsala Journal of Medical Sciences 2012 117 2 113 121 2-s2.0-84859903751 10.3109/03009734.2012.658976
52. Furnari F. B., Fenton T., Bachoo R. M., Mukasa A., Stommel J. M., Stegh A., Hahn W. C., Ligon K. L., Louis D. N., Brennan C., Chin L., DePinho R. A., Cavenee W. K., Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes and Development 2007 21 21 2683 2710 2-s2.0-35949002429 10.1101/gad.1596707 (Pubitemid 350070717)
53. Lee J.-S., Lee H. J., Moon B.-H., Song S.-H., Lee M.-O., Shim S. H., Kim H. S., Lee M. C., Kwon J. T., Fornace Jr. A. J., Kim S. U., Cha H. J., Generation of cancerous neural stem cells forming glial tumor by oncogenic stimulation. Stem Cell Reviews and Reports 2012 8 2 532 545 2-s2.0-84861714815 10.1007/s12015-011-9280-4
54. Liu C., Sage J. C., Miller M. R., Verhaak R. G. W., Hippenmeyer S., Vogel H., Foreman O., Bronson R. T., Nishiyama A., Luo L., Zong H., Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 2011 146 2 209 221 2-s2.0-79960809488 10.1016/j.cell.2011.06.014
55. Sukhdeo K., Hambardzumyan D., Rich J. N., Glioma development: where did it all go wrong? Cell 2011 146 2 187 188 2-s2.0-79960774446 10.1016/j.cell.2011. 06.047
56. Assanah M., Lochhead R., Ogden A., Bruce J., Goldman J., Canoll P., Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. Journal of Neuroscience 2006 26 25 6781 6790 2-s2.0-33745778950 10.1523/JNEUROSCI.0514-06.2006 (Pubitemid 44315239)
57. Graeber M. B., Scheithauer B. W., Kreutzberg G. W., Microglia in brain tumors. GLIA 2002 40 2 252 259 2-s2.0-0036850131 10.1002/glia.10147 (Pubitemid 35337382)
58. Charles N. A., Holland E. C., Gilbertson R., Glass R., Kettenmann H., The brain tumor microenvironment. GLIA 2012 60 3 502 514 2-s2.0-84856226955 10.1002/glia.21264
59. Naganuma H., Sasaki A., Satoh E., Nagasaka M., Nakano S., Isoe S., Nukui H., Modulation of transforming growth factor- β secretion from malignant glioma cells by interleukin-1 β Neurologia Medico-Chirurgica 1996 36 3 145 150 2-s2.0-0029964163 (Pubitemid 26098220)
60. Letterio J. J., Roberts A. B., Regulation of immune responses by TGF- β Annual Review of Immunology 1998 16 137 161 2-s2.0-0031944290 10.1146/annurev.immunol.16.1.137 (Pubitemid 28183362)
61. Watters J. J., Schartner J. M., Badie B., Microglia function in brain tumors. Journal of Neuroscience Research 2005 81 3 447 455 2-s2.0-25444488717 10.1002/jnr.20485 (Pubitemid 41359299)
62. Li H., Fan X., Houghton J., Tumor microenvironment: the role of the tumor stroma in cancer. Journal of Cellular Biochemistry 2007 101 4 805 815 2-s2.0-34447276000 10.1002/jcb.21159 (Pubitemid 47040863)
63. Carmeliet P., VEGF as a key mediator of angiogenesis in cancer. Oncology 2005 69 3 4 10 2-s2.0-27944473690 10.1159/000088478 (Pubitemid 41680947)
64. Hoelzinger D. B., Demuth T., Berens M. E., Autocrine factors that sustain glioma invasion and paracrine biology in the brain microenvironment. Journal of the National Cancer Institute 2007 99 21 1583 1593 2-s2.0-36048994736 10.1093/jnci/djm187 (Pubitemid 351767231)
65. Teicher B. A., Fricker S. P., CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clinical Cancer Research 2010 16 11 2927 2931 2-s2.0-77953090345 10.1158/1078-0432.CCR-09-2329
66. Wiesenhofer B., Stockhammer G., Kostron H., Maier H., Hinterhuber H., Humpel C., Glial cell line-derived neurotrophic factor (GDNF) and its receptor (GFR- α 1) are strongly expressed in human gliomas. Acta Neuropathologica 2000 99 2 131 137 2-s2.0-0033952634 (Pubitemid 30093419)
67. Lee J., Lund-Smith C., Borboa A., Gonzalez A. M., Baird A., Eliceiri B. P., Glioma-induced remodeling of the neurovascular unit. Brain Research 2009 1288 125 134 2-s2.0-69049106309 10.1016/j.brainres.2009.06.095
68. Kokovay E., Goderie S., Wang Y., Lotz S., Lin G., Sun Y., Roysam B., Shen Q., Temple S., Adult svz lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell 2010 7 2 163 173 2-s2.0-77956241246 10.1016/j.stem.2010.05.019
69. Walzlein J. H., Synowitz M., Engels B., Markovic D. S., Gabrusiewicz K., Nikolaev E., Yoshikawa K., Kaminska B., Kempermann G., Uckert W., Kaczmarek L., Kettenmann H., Glass R., The antitumorigenic response of neural precursors depends on subventricular proliferation and age. Stem Cells 2008 26 11 2945 2954 2-s2.0-56249093493 10.1634/stemcells.2008-0307
70. Chirasani S. R., Sternjak A., Wend P., Momma S., Campos B., Herrmann I. M., Graf D., Mitsiadis T., Herold-Mende C., Besser D., Synowitz M., Kettenmann H., Glass R., Bone morphogenetic protein-7 release from endogenous neural precursor cells suppresses the tumourigenicity of stem-like glioblastoma cells. Brain 2010 133 7 1961 1972 2-s2.0-77954368572 10.1093/brain/awq128
71. Binello E., Germano I. M., Stem cells as therapeutic vehicles for the treatment of high-grade gliomas. Neuro-Oncology 2012 14 3 256 265 2-s2.0-84859526994 10.1093/neuonc/nor204
72. Bellail A. C., Hunter S. B., Brat D. J., Tan C., Van Meir E. G., Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion. International Journal of Biochemistry and Cell Biology 2004 36 6 1046 1069 2-s2.0-13444275480 10.1016/j.biocel.2004.01.013 (Pubitemid 38501557)
73. Singh S. K., Clarke I. D., Terasaki M., Bonn V. E., Hawkins C., Squire J., Dirks P. B., Identification of a cancer stem cell in human brain tumors. Cancer Research 2003 63 18 5821 5828 2-s2.0-0141842674 (Pubitemid 37187480)
74. Yin A. H., Miraglia S., Zanjani E. D., Almeida-Porada G., Ogawa M., Leary A. G., Olweus J., Kearney J., Buck D. W., AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997 90 12 5002 5012 2-s2.0-0031453534 (Pubitemid 28007217)
75. Salven P., Mustjoki S., Alitalo R., Alitalo K., Rafii S., VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells. Blood 2003 101 1 168 172 2-s2.0-0037222688 10.1182/blood-2002-03-0755 (Pubitemid 36025904)
76. Uchida N., Buck D. W., He D., Reitsma M. J., Masek M., Phan T. V., Tsukamoto A. S., Gage F. H., Weissman I. L., Direct isolation of human central nervous system stem cells. Proceedings of the National Academy of Sciences of the United States of America 2000 97 26 14720 14725 2-s2.0-0034687840 10.1073/pnas.97.26.14720 (Pubitemid 32016642)
77. Zeppernick F., Ahmadi R., Campos B., Dictus C., Helmke B. M., Becker N., Lichter P., Unterberg A., Radlwimmer B., Herold-Mende C. C., Stem cell marker CD133 affects clinical outcome in glioma patients. Clinical Cancer Research 2008 14 1 123 129 2-s2.0-40749155451 10.1158/1078-0432.CCR-07-0932 (Pubitemid 351377986)
78. Bao S., Wu Q., McLendon R. E., Hao Y., Shi Q., Hjelmeland A. B., Dewhirst M. W., Bigner D. D., Rich J. N., Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006 444 7120 756 760 2-s2.0-33845317573 10.1038/nature05236 (Pubitemid 44949604)
79. Lathia J. D., Hitomi M., Gallagher J., Gadani S. P., Adkins J., Vasanji A., Liu L., Eyler C. E., Heddleston J. M., Wu Q., Minhas S., Soeda A., Hoeppner D. J., Ravin R., McKay R. D. G., McLendon R. E., Corbeil D., Chenn A., Hjelmeland A. B., Park D. M., Rich J. N., Distribution of CD133 reveals glioma stem cells self-renew through symmetric and asymmetric cell divisions. Cell Death and Disease 2011 2 9 e200 2-s2.0-80053430963 10.1038/cddis.2011.80
80. Li. Z. Z., Wang H., Eyler C. E., Hjelmeland A. B., Rich J. N., Turning cancer stem cells inside out: an exploration of glioma stem cells signalling pathways. Journal of Biological Chemistry 2009 284 25 16705 16709 2-s2.0-67649118749 10.1074/jbc.R900013200
81. Kondo T., Brain cancer stem-like cells. European Journal of Cancer 2006 42 9 1237 1242 2-s2.0-33646916614 10.1016/j.ejca.2006.01.038 (Pubitemid 43795099)
82. Radtke F., Raj K., The role of Notch in tumorigenesis: oncogene or tumour suppressor. Nature Reviews Cancer 2003 3 10 756 767 2-s2.0-0142259346 (Pubitemid 37328814)
83. Purow B. W., Haque R. M., Noel M. W., Su Q., Burdick M. J., Lee J., Sundaresan T., Pastorino S., Park J. K., Mikolaenko I., Maric D., Eberhart C. G., Fine H. A., Expression of Notch-1 and its ligands, Delta-like-1 and Jagged=1, is critical for glioma cell survival and proliferation. Cancer Research 2005 65 6 2353 2363 2-s2.0-20144387679 10.1158/0008-5472.CAN-04-1890 (Pubitemid 40490146)
84. Di Magliano M. P., Hebrok M., Hedgehog signalling in cancer formation and maintenance. Nature Reviews Cancer 2003 3 12 903 911 2-s2.0-0345059765 (Pubitemid 37500175)
85. Ruiz i Altaba A., Sánchez P., Dahmane N., Gli and hedgehog in cancer: tumours, embryos and stem cells. Nature Reviews Cancer 2002 2 5 361 372 2-s2.0-0036559186 (Pubitemid 37328949)
86. Bar E. E., Chaudhry A., Lin A., Fan X., Schreck K., Matsui W., Piccirillo S., Vescovi A. L., DiMeco F., Olivi A., Eberhart C. G., Cyclopamine-mediated Hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 2007 25 10 2524 2533 2-s2.0-35348837163 10.1634/stemcells.2007-0166 (Pubitemid 47582744)
87. Ulasov I. V., Nandi S., Dey M., Sonabend A. M., Lesniak M. S., Inhibition of sonic hedgehog and notch pathways enhances sensitivity of cd133+ glioma stem cells to temozolomide therapy. Molecular Medicine 2011 17 1-2 103 112 2-s2.0-78751640633 10.2119/molmed.2010.00062
88. Logan C. Y., Nusse R., The Wnt signaling pathway in development and disease. Annual Review of Cell and Developmental Biology 2004 20 781 810 2-s2.0-8444251784 10.1146/annurev.cellbio.20.010403.113126 (Pubitemid 39488658)
89. Chenn A., Walsh C. A., Increased neuronal production, enlarged forebrains and cytoarchitectural distortions in β -catenin overexpressing transgenic mice. Cerebral Cortex 2003 13 6 599 606 2-s2.0-0038662778 10.1093/cercor/13.6. 599 (Pubitemid 36613167)
90. Marino S., Medulloblastoma: developmental mechanisms out of control. Trends in Molecular Medicine 2005 11 1 17 22 2-s2.0-11844301282 10.1016/j.molmed.2004.11.008 (Pubitemid 40092670)
91. Konnikova L., Kotecki M., Kruger M. M., Cochran B. H., Knockdown of STAT3 expression by RNAi induces apoptosis in astrocytoma cells. BMC Cancer 2003 3, article 23 2-s2.0-3042748279 10.1186/1471-2407-3-23 (Pubitemid 38851326)
92. Bromberg J., Stat proteins and oncogenesis. Journal of Clinical Investigation 2002 109 9 1139 1142 2-s2.0-0036251154 10.1172/JCI200215617 (Pubitemid 34496590)
93. Sherry M. M., Reeves A., Wu J. K., Cochran B. H., STAT3 is required for proliferation and maintenance of multipotency in glioblastoma stem cells. Stem Cells 2009 27 10 2383 2392 2-s2.0-70350212976 10.1002/stem.185
94. Eyler C. E., Foo W. C., LaFiura K. M., McLendon R. E., Hjelmeland A. B., Rich J. N., Brain cancer stem cells display preferential sensitivity to Akt inhibition. Stem Cells 2008 26 12 3027 3036 2-s2.0-58049198191 10.1634/stemcells.2007-1073
95. Panchision D. M., McKay R. D. G., The control of neural stem cells by morphogenic signals. Current Opinion in Genetics and Development 2002 12 4 478 487 2-s2.0-0036668287 10.1016/S0959-437X(02)00329-5 (Pubitemid 34722930)
96. Piccirillo S. G. M., Reynolds B. A., Zanetti N., Lamorte G., Binda E., Broggi G., Brem H., Olivi A., Dimeco F., Vescovi A. L., Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 2006 444 7120 761 765 2-s2.0-33845610993 10.1038/nature05349 (Pubitemid 44949605)
97. Hope K. J., Jin L., Dick J. E., Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nature Immunology 2004 5 7 738 743 2-s2.0-3242754448 10.1038/ni1080 (Pubitemid 39023306)
98. Denysenko T., Gennero L., Roos M. A., Melcarne A., Juenemann C., Faccani G., Morra I., Cavallo G., Reguzzi S., Pescarmona G., Ponzetto A., Glioblastoma cancer stem cells: heterogeneity, microenvironment and related therapeutic strategies. Cell Biochemistry and Function 2010 28 5 343 351 2-s2.0-77956812631 10.1002/cbf.1666
99. Heddleston J. M., Hitomi M., Venere M., Flavahan W. A., Yang K., Kim Y., Minhas S., Rich J. N., Hjelmeland A. B., Glioma stem cell maintenance: the role of the microenvironment. Current Pharmaceutical Design 2011 17 23 2386 2401 2-s2.0-80053515159 10.2174/138161211797249260
100. Yuan X., Curtin J., Xiong Y., Liu G., Waschsmann-Hogiu S., Farkas D. L., Black K. L., Yu J. S., Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 2004 23 58 9392 9400 2-s2.0-11244293572 10.1038/sj.onc.1208311 (Pubitemid 40069671)
101. Yu S. C., Ping Y. F., Yi L., Zhou Z. H., Chen J. H., Yao X. H., Gao L., Wang J. M., Bian X. W., Isolation and characterization of cancer stem cells from a human glioblastoma cell line U87. Cancer Letters 2008 265 1 124 134 2-s2.0-43649086456 10.1016/j.canlet.2008.02.010
102. Ledur P. F., Villodre E. S., Paulus R., Cruz L. A., Flores D. G., Lenz G., Extracellular ATP reduces tumor sphere growth and cancer stem cell population in glioblastoma cells. Purinergic Signalling 2012 8 1 39 48 2-s2.0-84857674630 10.1007/s11302-011-9252-9
103. Barrett L. E., Granot Z., Coker C., Iavarone A., Hambardzumyan D., Holland E. C., Nam H.-S., Benezra R., Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma. Cancer Cell 2012 21 1 11 24 2-s2.0-84855932131 10.1016/j.ccr.2011.11.025
104. Folkerth R. D., Histologic measures of angiogenesis in human primary brain tumors. Cancer Treatment and Research 2004 117 79 95 2-s2.0-2342442123
105. Calabrese C., Poppleton H., Kocak M., Hogg T. L., Fuller C., Hamner B., Oh E. Y., Gaber M. W., Finklestein D., Allen M., Frank A., Bayazitov I. T., Zakharenko S. S., Gajjar A., Davidoff A., Gilbertson R. J., A perivascular niche for brain tumor stem cells. Cancer Cell 2007 11 1 69 82 2-s2.0-33846029123 10.1016/j.ccr.2006.11.020 (Pubitemid 46054518)
106. He H., Li M. W., Niu C. S., The pathological characteristics of glioma stem cell niches. Journal of Clinical Neuroscience 2012 19 1 121 127 2-s2.0-84855187212 10.1016/j.jocn.2011.07.026
107. Lathia J. D., Heddleston J. M., Venere M., Rich J. N., Deadly teamwork: neural cancer stem cells and the tumor microenvironment. Cell Stem Cell 2011 8 5 482 485 2-s2.0-79955702339 10.1016/j.stem.2011.04.013
108. Bao S., Wu Q., Sathornsumetee S., Hao Y., Li Z., Hjelmeland A. B., Shi Q., McLendon R. E., Bigner D. D., Rich J. N., Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Research 2006 66 16 7843 7848 2-s2.0-33748051406 10.1158/0008-5472.CAN-06-1010 (Pubitemid 44299144)
109. Charles N., Ozawa T., Squatrito M., Bleau A. M., Brennan C. W., Hambardzumyan D., Holland E. C., Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 2010 6 2 141 152 2-s2.0-75349091751 10.1016/j.stem.2010.01.001
110. Kioi M., Vogel H., Schultz G., Hoffman R. M., Harsh G. R., Brown J. M., Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. Journal of Clinical Investigation 2010 120 3 694 705 2-s2.0-77949697909 10.1172/JCI40283
111. Wang R., Chadalavada K., Wilshire J., Kowalik U., Hovinga K. E., Geber A., Fligelman B., Leversha M., Brennan C., Tabar V., Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010 468 7325 829 835 2-s2.0-78650098659 10.1038/nature09624
112. Lathia J. D., Gallagher J., Myers J. T., Li M., Vasanji A., McLendon R. E., Hjelmeland A. B., Huang A. Y., Rich J. N., Direct In vivo evidence for tumor propagation by glioblastoma cancer stem cells. PLoS ONE 2011 6 9 e24807 2-s2.0-80053058993 10.1371/journal.pone.0024807
113. Vaupel P., Hypoxia in neoplastic tissue. Microvascular Research 1977 13 3 399 408 2-s2.0-0017645626 (Pubitemid 8135801)
114. Vaupel P. W., Frinak S., Bicher H. I., Heterogeneous oxygen partial pressure and pH distributition in C3H mouse mammary adenocarcinoma. Cancer Research 1981 41 5 2008 2013 2-s2.0-0019461848 (Pubitemid 11114612)
115. Kallinowski F., Schlenger K. H., Runkel S., Kloes M., Stohrer M., Okunieff P., Vaupel P., Blood flow, metabolism, cellular microenvironment, and growth rate of human tumor xenografts. Cancer Research 1989 49 14 3759 3764 2-s2.0-0024311944 (Pubitemid 19197393)
116. Adair T. H., Gay W. J., Montani J. P., Growth regulation of the vascular system: evidence for a metabolic hypothesis. American Journal of Physiology 1990 259 3 R393 R404 2-s2.0-0025080230 (Pubitemid 20307558)
117. Shweiki D., Itin A., Soffer D., Keshet E., Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992 359 6398 843 845 2-s2.0-0026485002 10.1038/359843a0
118. Wang G. L., Semenza G. L., General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proceedings of the National Academy of Sciences of the United States of America 1993 90 9 4304 4308 2-s2.0-0027210562 (Pubitemid 23134215)
119. Evans S. M., Judy K. D., Dunphy I., Timothy Jenkins W., Hwang W. T., Nelson P. T., Lustig R. A., Jenkins K., Magarelli D. P., Hahn S. M., Collins R. A., Grady S., Koch C. J., Hypoxia is important in the biology and aggression of human glial brain tumors. Clinical Cancer Research 2004 10 24 8177 8184 2-s2.0-19944426500 10.1158/1078-0432.CCR-04-1081 (Pubitemid 40053376)
120. Rankin E. B., Giaccia A. J., The role of hypoxia-inducible factors in tumorigenesis. Cell Death and Differentiation 2008 15 4 678 685 2-s2.0-40949142209 10.1038/cdd.2008.21 (Pubitemid 351405072)
121. Parmar K., Mauch P., Vergilio J. A., Sackstein R., Down J. D., Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proceedings of the National Academy of Sciences of the United States of America 2007 104 13 5431 5436 2-s2.0-34248359065 10.1073/pnas. 0701152104 (Pubitemid 47175697)
122. Heddleston J. M., Li Z., McLendon R. E., Hjelmeland A. B., Rich J. N., The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009 8 20 3274 3284 2-s2.0-70350225829
123. Takahashi K., Yamanaka S., Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006 126 4 663 676 2-s2.0-33747195353 10.1016/j.cell.2006.07.024 (Pubitemid 44233629)
124. Seidel S., Garvalov B. K., Wirta V., Von Stechow L., Schänzer A., Meletis K., Wolter M., Sommerlad D., Henze A. T., Nistér M., Reifenberger G., Lundeberg J., Frisén J., Acker T., A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 α Brain 2010 133 4 983 995 2-s2.0-77950838848 10.1093/brain/awq042
125. Rapisarda A., Hollingshead M., Uranchimeg B., Bonomi C. A., Borgel S. D., Carter J. P., Gehrs B., Raffeld M., Kinders R. J., Parchment R., Anver M. R., Shoemaker R. H., Melillo G., Increased antitumor activity of bevacizumab in combination with hypoxia inducible factor-1 inhibition. Molecular Cancer Therapeutics 2009 8 7 1867 1877 2-s2.0-67651166780 10.1158/1535-7163.MCT-09-0274
126. Chamberlain M. C., Bevacizumab for the treatment of recurrent glioblastoma. Clinical Medicine Insights 2011 5 117 129 2-s2.0-79958031331 10.4137/CMO.S7232
127. National Cancer Institute
128. Kunkel P., Ulbricht U., Bohlen P., Brockmann M. A., Fillbrandt R., Stavrou D., Westphal M., Lamszus K., Inhibition of glioma angiogenesis and growth In vivo by systemic treatment with a monoclonal antibody against vascular endothelial growth factor receptor-2. Cancer Research 2001 61 18 6624 6628 2-s2.0-0035884609 (Pubitemid 32896475)
129. Nakabayashi H., Yawata T., Shimizu K., Anti-invasive and antiangiogenic effects of MMI-166 on malignant glioma cells. BMC Cancer 2010 10, article 339 2-s2.0-77953922891 10.1186/1471-2407-10-339
130. De Boüard S., Herlin P., Christensen J. G., Lemoisson E., Gauduchon P., Raymond E., Guillamo J. S., Antiangiogenic and anti-invasive effects of sunitinib on experimental human glioblastoma. Neuro-Oncology 2007 9 4 412 423 2-s2.0-38449097166 10.1215/15228517-2007-024
131. Conley S. J., Gheordunescu E., Kakarala P., Newman B., Korkaya H., Heath A. N., Clouthier S. G., Wicha M. S., Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proceedings of the National Academy of Sciences of the United States of America 2012 109 8 2784 2789 2-s2.0-84857407549 10.1073/pnas.1018866109
132. Cavalli G., Chromatin and epigenetics in development: blending cellular memory with cell fate plasticity. Development 2006 133 11 2089 2094 2-s2.0-33745612032 10.1242/dev.02402 (Pubitemid 43986119)
133. Hu M., Yao J., Cai L., Bachman K. E., Van Den Brûle F., Velculescu V., Polyak K., Distinct epigenetic changes in the stromal cells of breast cancers. Nature Genetics 2005 37 8 899 905 2-s2.0-23044499067 10.1038/ng1596 (Pubitemid 41077119)
134. Li E., Chromatin modification and epigenetic reprogramming in mammalian development. Nature Reviews Genetics 2002 3 9 662 673 2-s2.0-0036733675 10.1038/nrg887 (Pubitemid 34984255)
135. Hsieh J., Gage F. H., Epigenetic control of neural stem cell fate. Current Opinion in Genetics and Development 2004 14 5 461 469 2-s2.0-5444244267 10.1016/j.gde.2004.07.006 (Pubitemid 39360292)
136. Strahl B. D., Allis C. D., The language of covalent histone modifications. Nature 2000 403 6765 41 45 2-s2.0-0034610814 10.1038/47412 (Pubitemid 30038513)
137. Szutorisz H., Dillon N., The epigenetic basis for embryonic stem cell pluripotency. BioEssays 2005 27 12 1286 1293 2-s2.0-30444440701 10.1002/bies.20330 (Pubitemid 43076172)
138. Dey P., Epigenetic changes in tumor microenvironment. Indian Journal of Cancer 2011 48 4 507 512 2-s2.0-84856862426 10.4103/0019-509X.92246
139. Ducasse M.,.Brown M. A, Epigenetic aberrations and cancer. Molecular Cancer 2006 5 60 10.1186/1476-4598-5-60 (Pubitemid 44848505)
140. Hegi M. E., Diserens A. C., Gorlia T., Hamou M. F., De Tribolet N., Weller M., Kros J. M., Hainfellner J. A., Mason W., Mariani L., Bromberg J. E. C., Hau P., Mirimanoff R. O., Cairncross J. G., Janzer R. C., Stupp R., MGMT gene silencing and benefit from temozolomide in glioblastoma. New England Journal of Medicine 2005 352 10 997 1003 2-s2.0-20044372154 10.1056/NEJMoa043331 (Pubitemid 40349502)
141. Rajendran G., Shanmuganandam K., Bendre A., Mujumdar D., Goel A., Shiras A., Epigenetic regulation of DNA methyltransferases: DNMT1 and DNMT3B in gliomas. Journal of Neuro-Oncology 2011 104 2 483 494 2-s2.0-78651089974 10.1007/s11060-010-0520-2
142. Wiencke J. K., Zheng S., Jelluma N., Tihan T., Vandenberg S., Tamgüney T., Baumber R., Parsons R., Lamborn K. R., Berger M. S., Wrensch M. R., Haas-Kogan D. A., Stokoe D., Methylation of the PTEN promoter defines low-grade gliomas and secondary glioblastoma. Neuro-Oncology 2007 9 3 271 279 2-s2.0-34547432233 10.1215/15228517-2007-003 (Pubitemid 47169659)
143. Huangfu D., Osafune K., Maehr R., Guo W., Eijkelenboom A., Chen S., Muhlestein W., Melton D. A., Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nature Biotechnology 2008 26 11 1269 1275 2-s2.0-55749104227 10.1038/nbt.1502
144. Bapat S. A., Jin V., Berry N., Balch C., Sharma N., Kurrey N., Zhang S., Fang F., Lan X., Li M., Kennedy B., Bigsby R. M., Huang T. H., Nephew K. P., Multivalent epigenetic marks confer microenvironment-responsive epigenetic plasticity to ovarian cancer cells. Epigenetics 2010 5 8 716 729 2-s2.0-79952457504
145. Hsieh J., Nakashima K., Kuwabara T., Mejia E., Gage F. H., Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proceedings of the National Academy of Sciences of the United States of America 2004 101 47 16659 16664 2-s2.0-9344252804 10.1073/pnas.0407643101 (Pubitemid 39557769)
146. Postovit L. M., Margaryan N. V., Seftor E. A., Kirschmann D. A., Lipavsky A., Wheaton W. W., Abbott D. E., Seftor R. E. B., Hendrix M. J. C., Human embryonic stem cell microenvironment suppresses the tumorigenic phenotype of aggressive cancer cells. Proceedings of the National Academy of Sciences of the United States of America 2008 105 11 4329 4334 2-s2.0-41949142373 10.1073/pnas.0800467105 (Pubitemid 351754380)
147. Hendrix M. J. C., Seftor E. A., Seftor R. E. B., Kasemeier-Kulesa J., Kulesa P. M., Postovit L. M., Reprogramming metastatic tumour cells with embryonic microenvironments. Nature Reviews Cancer 2007 7 4 246 255 2-s2.0-33947583623 10.1038/nrc2108 (Pubitemid 46480969)
148. Minucci S., Pelicci P. G., Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nature Reviews Cancer 2006 6 1 38 51 2-s2.0-30344477367 10.1038/nrc1779 (Pubitemid 43054973)
149. Lee M. J., Kim Y. S., Kummar S., Giaccone G., Trepel J. B., Histone deacetylase inhibitors in cancer therapy. Current Opinion in Oncology 2008 20 6 639 649 2-s2.0-55749101363 10.1097/CCO.0b013e3283127095
150. Sang N., Chen S., Histone deacetylase inhibitors: the epigenetic therapeutics that repress hypoxia-inducible factors. Journal of Biomedicine and Biotechnology 2011 2011 14 2-s2.0-79251576774 10.1155/2011/197946 197946
151. Shahrzad S., Bertrand K., Minhas K., Coomber B. L., Induction of DNA hypomethylation by tumor hypoxia. Epigenetics 2007 2 2 119 125 2-s2.0-38449086370 (Pubitemid 351682006)
152. Kim M. S., Kwon H. J., Lee Y. M., Baek J. H., Jang J. E., Lee S. W., Moon E. J., Kim H. S., Lee S. K., Chung H. Y., Kim C. W., Kim K. W., Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nature Medicine 2001 7 4 437 443 2-s2.0-0035048449 10.1038/86507 (Pubitemid 32298546)
153. Jeong J. W., Bae M. K., Ahn M. Y., Kim S. H., Sohn T. K., Bae M. H., Yoo M. A., Song E. J., Lee K. J., Kim K. W., Regulation and destabilization of HIF-1 α by ARD1-mediated acetylation. Cell 2002 111 5 709 720 2-s2.0-18744375998 10.1016/S0092-8674(02)01085-1 (Pubitemid 35441252)