Angiogenesis and hypoxia in glioblastoma: A focus on cancer stem cells

CNS and Neurological Disorders - Drug Targets

Volumn 11, Issue 7, 2012, Pages 878-883

  Mongiardi, Maria Patrizia ^a  

^a CNR   (Italy)

Author keywords

Angiogenesis; Cancer stem cells; Glioblastoma multiforme; Hypoxia; Microenvironment; Stem cell niche

Indexed keywords

CD31 ANTIGEN; CD34 ANTIGEN; HYPOXIA INDUCIBLE FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; CANCER RECURRENCE; CANCER STEM CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL INTERACTION; ENDOTHELIAL PROGENITOR CELL; GLIOBLASTOMA; HUMAN; HYPOXIA; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OXIDATIVE STRESS; REVIEW; STEM CELL NICHE; TUMOR MICROENVIRONMENT; TUMOR MODEL;

ANIMALS; BRAIN NEOPLASMS; CELL HYPOXIA; GLIOBLASTOMA; HUMANS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; STEM CELL NICHE;

EID: 84873139483     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/1871527311201070878     Document Type: Review

References (57)

1. Stupp, R.; Hegi, M.E.; Mason, W.P.; van den Bent, M.J.; Taphoorn, M.J.; Janzer, R.C.; Ludwin, S.K.; Allgeier, A.; Fisher, B.; Belanger, K.; Hau, P.; Brandes, A.A.; Gijtenbeek, J.; Marosi, C.; Vecht, C.J.; Mokhtari, K.; Wesseling, P.; Villa, S.; Eisenhauer, E.; Gorlia, T.; Weller, M.; Lacombe, D.; Cairncross, J.G.; Mirimanoff, R.O. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol., 2009, 10(5), 459-466.
2. Charles, N.A.; Holland, E.C.; Gilbertson, R.; Glass, R.; Kettenmann, H. The brain tumor microenvironment. Glia, 2011, 59(8), 1169-1180.
3. 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), 829-833.
4. Ricci-Vitiani, L.; Pallini, R.; Biffoni, M.; Todaro, M.; Invernici, G.; Cenci, T.; Maira, G.; Parati, E.A.; Stassi, G.; Larocca, L.M.; De, M.R. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature, 2010, 468(7325), 824-828.
5. Clarke, M.F.; Dick, J.E.; Dirks, P.B.; Eaves, C.J.; Jamieson, C.H.; Jones, D.L.; Visvader, J.; Weissman, I.L.; Wahl, G.M. Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res., 2006, 66(19), 9339-9344.
6. Chen, J.; McKay, R.M.; Parada, L.F. Malignant glioma: lessons from genomics, mouse models, and stem cells. Cell, 2012, 149(1), 36-47.
7. 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.
8. Onder, T.T.; Kara, N.; Cherry, A.; Sinha, A.U.; Zhu, N.; Bernt, K.M.; Cahan, P.; Marcarci, B.O.; Unternaehrer, J.; Gupta, P.B.; Lander, E.S.; Armstrong, S.A.; Daley, G.Q. Chromatin-modifying enzymes as modulators of reprogramming. Nature, 2012, 483(7391), 598-602.
9. Sugiarto, S.; Persson, A.I.; Munoz, E.G.; Waldhuber, M.; Lamagna, C.; Andor, N.; Hanecker, P.; Ayers-Ringler, J.; Phillips, J.; Siu, J.; Lim, D.A.; Vandenberg, S.; Stallcup, W.; Berger, M.S.; Bergers, G.; Weiss, W.A.; Petritsch, C. Asymmetry-defective oligodendrocyte progenitors are glioma precursors. Cancer Cell, 2011, 20(3), 328-340.
10. Heddleston, J.M.; Li, Z.; Lathia, J.D.; Bao, S.; Hjelmeland, A.B.; Rich, J.N. Hypoxia inducible factors in cancer stem cells. Br. J. Cancer, 2010, 102(5), 789-795.
11. Lapidot, T.; Sirard, C.; Vormoor, J.; Murdoch, B.; Hoang, T.; Caceres-Cortes, J.; Minden, M.; Paterson, B.; Caligiuri, M.A.; Dick, J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature, 1994, 367(6464), 645-648.
12. Bonnet, D.; Dick, J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med., 1997, 3(7), 730-737.
13. Al-Hajj, M.; Wicha, M.S.; Benito-Hernandez, A.; Morrison, S.J.; Clarke, M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA, 2003, 100(7), 3983-3988.
14. Ignatova, T.N.; Kukekov, V.G.; Laywell, E.D.; Suslov, O.N.; Vrionis, F.D.; Steindler, D.A. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia, 2002, 39(3), 193-206.
15. Singh, S.K.; Hawkins, C.; Clarke, I.D.; Squire, J.A.; Bayani, J.; Hide, T.; Henkelman, R.M.; Cusimano, M.D.; Dirks, P.B. Identification of human brain tumour initiating cells. Nature, 2004, 432(7015), 396-401.
16. Galli, R.; Binda, E.; Orfanelli, U.; Cipelletti, B.; Gritti, A.; De, V.S.; Fiocco, R.; Foroni, C.; Dimeco, F.; Vescovi, A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res., 2004, 64(19), 7011-7021.
17. 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.
18. 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.
19. Diehn, M.; Cho, R.W.; Lobo, N.A.; Kalisky, T.; Dorie, M.J.; Kulp, A.N.; Qian, D.; Lam, J.S.; Ailles, L.E.; Wong, M.; Joshua, B.; Kaplan, M.J.; Wapnir, I.; Dirbas, F.M.; Somlo, G.; Garberoglio, C.; Paz, B.; Shen, J.; Lau, S.K.; Quake, S.R.; Brown, J.M.; Weissman, I.L.; Clarke, M.F. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature, 2009, 458(7239), 780-783.
20. Bleau, A.M.; Hambardzumyan, D.; Ozawa, T.; Fomchenko, E.I.; Huse, J.T.; Brennan, C.W.; Holland, E.C. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell, 2009, 4(3), 226-235.
21. Donnenberg, V.S.; Donnenberg, A.D. Multiple drug resistance in cancer revisited: the cancer stem cell hypothesis. J. Clin. Pharmacol., 2005, 45(8), 872-877.
22. Shapiro, J.R.; Yung, W.K.; Shapiro, W.R. Isolation, karyotype, and clonal growth of heterogeneous subpopulations of human malignant gliomas. Cancer Res., 1981, 41(6), 2349-2359.
23. Wikstrand, C.J.; Bigner, S.H.; Bigner, D.D. Demonstration of complex antigenic heterogeneity in a human glioma cell line and eight derived clones by specific monoclonal antibodies. Cancer Res., 1983, 43(7), 3327-3334.
24. Jung, V.; Romeike, B.F.; Henn, W.; Feiden, W.; Moringlane, J.R.; Zang, K.D.; Urbschat, S. Evidence of focal genetic microheterogeneity in glioblastoma multiforme by area-specific CGH on microdissected tumor cells. J. Neuropathol. Exp. Neurol., 1999, 58(9), 993-999.
25. Huang, H.S.; Nagane, M.; Klingbeil, C.K.; Lin, H.; Nishikawa, R.; Ji, X.D.; Huang, C.M.; Gill, G.N.; Wiley, H.S.; Cavenee, W.K. The enhanced tumorigenic activity of a mutant epidermal growth factor receptor common in human cancers is mediated by threshold levels of constitutive tyrosine phosphorylation and unattenuated signaling. J. Biol. Chem., 1997, 272(5), 2927-2935.
26. Nishikawa, R.; Sugiyama, T.; Narita, Y.; Furnari, F.; Cavenee, W.K.; Matsutani, M. Immunohistochemical analysis of the mutant epidermal growth factor, deltaEGFR, in glioblastoma. Brain Tumor Pathol., 2004, 21(2), 53-56.
27. Fiorenzo, P.; Mongiardi, M.P.; Dimitri, D.; Cozzolino, M.; Ferri, A.; Montano, N.; Trevisi, G.; Maira, G.; Battistini, L.; Falchetti, M.L.; Levi, A.; Pallini, R. HIF1-positive and HIF1-negative glioblastoma cells compete in vitro but cooperate in tumor growth in vivo. Int. J. Oncol., 2010, 36(4), 785-791.
28. Kim, Y.; Kim, E.; Wu, Q.; Guryanova, O.; Hitomi, M.; Lathia, J.D.; Serwanski, D.; Sloan, A.E.; Weil, R.J.; Lee, J.; Nishiyama, A.; Bao, S.; Hjelmeland, A.B.; Rich, J.N. Platelet-derived growth factor receptors differentially inform intertumoral and intratumoral heterogeneity. Genes Dev., 2012, 26(11), 1247-1262.
29. Bonavia, R.; Inda, M.M.; Cavenee, W.K.; Furnari, F.B. Heterogeneity maintenance in glioblastoma: a social network. Cancer Res., 2011, 71(12), 4055-4060.
30. Bergers, G.; Hanahan, D. Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer, 2008, 8(8), 592-603.
31. Lu, K.V.; Chang, J.P.; Parachoniak, C.A.; Pandika, M.M.; Aghi, M.K.; Meyronet, D.; Isachenko, N.; Fouse, S.D.; Phillips, J.J.; Cheresh, D.A.; Park, M.; Bergers, G. VEGF Inhibits Tumor Cell Invasion and Mesenchymal Transition through a MET/VEGFR2 Complex. Cancer Cell, 2012, 22(1), 21-35.
32. St, C.B.; Rago, C.; Velculescu, V.; Traverso, G.; Romans, K.E.; Montgomery, E.; Lal, A.; Riggins, G.J.; Lengauer, C.; Vogelstein, B.; Kinzler, K.W. Genes expressed in human tumor endothelium. Science, 2000, 289(5482), 1197-1202.
33. Carson-Walter, E.B.; Watkins, D.N.; Nanda, A.; Vogelstein, B.; Kinzler, K.W.; St, C.B. Cell surface tumor endothelial markers are conserved in mice and humans. Cancer Res., 2001, 61(18), 6649-6655.
34. Bussolati, B.; Deambrosis, I.; Russo, S.; Deregibus, M.C.; Camussi, G. Altered angiogenesis and survival in human tumorderived endothelial cells. FASEB J., 2003, 17(9), 1159-1161.
35. Falchetti, M.L.; Pierconti, F.; Casalbore, P.; Maggiano, N.; Levi, A.; Larocca, L.M.; Pallini, R. Glioblastoma induces vascular endothelial cells to express telomerase in vitro. Cancer Res., 2003, 63(13), 3750-3754.
36. Falchetti, M.L.; Mongiardi, M.P.; Fiorenzo, P.; Petrucci, G.; Pierconti, F.; D'Agnano, I.; D'Alessandris, G.; Alessandri, G.; Gelati, M.; Ricci-Vitiani, L.; Maira, G.; Larocca, L.M.; Levi, A.; Pallini, R. Inhibition of telomerase in the endothelial cells disrupts tumor angiogenesis in glioblastoma xenografts. Int. J. Cancer, 2008, 122(6), 1236-1242.
37. 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 celllike glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res., 2006, 66(16), 7843-7848.
38. Folkins, C.; Shaked, Y.; Man, S.; Tang, T.; Lee, C.R.; Zhu, Z.; Hoffman, R.M.; Kerbel, R.S. Glioma tumor stem-like cells promote tumor angiogenesis and vasculogenesis via vascular endothelial growth factor and stromal-derived factor 1. Cancer Res., 2009, 69(18), 7243-7251.
39. Maniotis, A.J.; Folberg, R.; Hess, A.; Seftor, E.A.; Gardner, L.M.; Pe'er, J.; Trent, J.M.; Meltzer, P.S.; Hendrix, M.J. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am. J. Pathol., 1999, 155(3), 739-752.
40. Hendrix, M.J.; Seftor, E.A.; Hess, A.R.; Seftor, R.E. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat. Rev. Cancer, 2003, 3(6), 411-421.
41. Dome, B.; Hendrix, M.J.; Paku, S.; Tovari, J.; Timar, J. Alternative vascularization mechanisms in cancer: Pathology and therapeutic implications. Am. J. Pathol., 2007, 170(1), 1-15.
42. Zhao, Y.; Dong, J.; Huang, Q.; Lou, M.; Wang, A.; Lan, Q. Endothelial cell transdifferentiation of human glioma stem progenitor cells in vitro. Brain Res. Bull., 2010, 82(5-6), 308-312.
43. El, H.S.; Boisselier, B.; Peglion, F.; Rousseau, A.; Colin, C.; Idbaih, A.; Marie, Y.; Mokhtari, K.; Thomas, J.L.; Eichmann, A.; Delattre, J.Y.; Maniotis, A.J.; Sanson, M. A new alternative mechanism in glioblastoma vascularization: tubular vasculogenic mimicry. Brain, 2010, 133(Pt 4), 973-982.
44. Ivan, M.; Kondo, K.; Yang, H.; Kim, W.; Valiando, J.; Ohh, M.; Salic, A.; Asara, J.M.; Lane, W.S.; Kaelin, W.G., Jr. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science, 2001, 292(5516), 464-468.
45. Huang, L.E.; Arany, Z.; Livingston, D.M.; Bunn, H.F. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J. Biol. Chem., 1996, 271(50), 32253-32259.
46. Maxwell, P.H.; Ratcliffe, P.J. Oxygen sensors and angiogenesis. Semin. Cell Dev. Biol., 2002, 13(1), 29-37.
47. Covello, K.L.; Simon, M.C. HIFs, hypoxia, and vascular development. Curr. Top. Dev. Biol., 2004, 62, 37-54.
48. Liu, Y.V.; Baek, J.H.; Zhang, H.; Diez, R.; Cole, R.N.; Semenza, G.L. RACK1 competes with HSP90 for binding to HIF-1alpha and is required for O(2)-independent and HSP90 inhibitor-induced degradation of HIF-1alpha. Mol. Cell, 2007, 25(2), 207-217.
49. Cam, H.; Easton, J.B.; High, A.; Houghton, P.J. mTORC1 signaling under hypoxic conditions is controlled by ATMdependent phosphorylation of HIF-1alpha. Mol. Cell, 2010, 40(4), 509-520.
50. Mongiardi, M.P.; Stagni, V.; Natoli, M.; Giaccari, D.; D'Agnano, I.; Falchetti, M.L.; Barila, D.; Levi, A. Oxygen sensing is impaired in ATM-defective cells. Cell Cycle, 2011, 10(24), 4311-4320.
51. Pistollato, F.; Rampazzo, E.; Abbadi, S.; Della, P.A.; Scienza, R.; d'Avella, D.; Denaro, L.; Te, K.G.; Panchision, D.M.; Basso, G. Molecular mechanisms of HIF-1alpha modulation induced by oxygen tension and BMP2 in glioblastoma derived cells. PLoS One, 2009, 4(7), e6206.
52. Gustafsson, M.V.; Zheng, X.; Pereira, T.; Gradin, K.; Jin, S.; Lundkvist, J.; Ruas, J.L.; Poellinger, L.; Lendahl, U.; Bondesson, M. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell, 2005, 9(5), 617-628.
53. Bray, S.J. Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol., 2006, 7(9), 678-689.
54. 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.
55. Bar, E.E. Glioblastoma, cancer stem cells and hypoxia. Brain Pathol., 2011, 21(2), 119-129.
56. Mazumdar, J.; O'Brien, W.T.; Johnson, R.S.; LaManna, J.C.; Chavez, J.C.; Klein, P.S.; Simon, M.C. O2 regulates stem cells through Wnt/beta-catenin signalling. Nat. Cell Biol., 2010, 12(10), 1007-1013.
57. De, P.M.; Hanahan, D. The biology of personalized cancer medicine: facing individual complexities underlying hallmark capabilities. Mol. Oncol., 2012, 6(2), 111-127.