Notch1 stimulation induces a vascularization switch with pericyte-like cell differentiation of glioblastoma stem cells

Stem Cells

Volumn 33, Issue 1, 2015, Pages 21-34

  Guichet, Pierre Olivier ^a   Guelfi, Sophie ^a   Teigell, Marisa ^a   Hoppe, Liesa ^a   Bakalara, Norbert ^a,b   Bauchet, Luc ^a,b   Duffau, Hugues ^a   Lamszus, Katrin ^c   Rothhut, Bernard ^a   Hugnot, Jean Philippe ^a,d  

^a HÔPITAL SAINT ELOI   (France)

^b MONTPELLIER UNIVERSITY HOSPITAL   (France)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UNIV MONTPELLIER   (France)

Author keywords

Glioblastoma; Glioma; Notch; Vascularization

Indexed keywords

ALPHA INTEGRIN; ALPHA SMOOTH MUSCLE ACTIN; CELL MARKER; CYTOKINE; EPIDERMAL GROWTH FACTOR; INTEGRIN ALPHA 9; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 8; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 9; NOTCH1 RECEPTOR; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PLACENTAL GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; NOTCH1 PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN PERICYTE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL GROWTH; CELL MIGRATION; CELL STIMULATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; GLIOBLASTOMA; GROWTH RATE; HUMAN; HUMAN CELL; MOUSE; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; STEM CELL; STEM CELL CULTURE; UPREGULATION; VASCULARIZATION; XENOTRANSPLANTATION; ANIMAL; BRAIN TUMOR; GENETIC TRANSFECTION; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; PATHOLOGY; PERICYTE; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; BRAIN NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; GLIOBLASTOMA; HETEROGRAFTS; HUMANS; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; PERICYTES; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84919459280     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1767     Document Type: Article

References (61)

1. Ricard D, Idbaih A, Ducray F, et al. Primary brain tumours in adults. Lancet 2012; 379: 1984-1996.
2. Plate KH, Scholz A, Dumont DJ,. Tumor angiogenesis and anti-angiogenic therapy in malignant gliomas revisited. Acta Neuropathol 2012; 124: 763-775.
3. Venere M, Fine HA, Dirks PB, et al. Cancer stem cells in gliomas: Identifying and understanding the apex cell in cancer's hierarchy. Glia 2011; 59: 1148-1154.
4. Hardee ME, Zagzag D,. Mechanisms of glioma-associated neovascularization. Am J Pathol 2012; 181: 1126-1141.
5. Hjelmeland AB, Rich JN,. The quest for self-identity: Not all cancer stem cells are the same. Clin Cancer Res 2012; 18: 3495-3498.
6. Sakariassen PO, Prestegarden L, Wang J, et al. Angiogenesis-independent tumor growth mediated by stem-like cancer cells. Proc Natl Acad Sci U S A 2006; 103: 16466-16471.
7. Hjelmeland AB, Lathia JD, Sathornsumetee S, et al. Twisted tango: Brain tumor neurovascular interactions. Nat Neurosci 2011; 14: 1375-1381.
8. Guruharsha KG, Kankel MW, Artavanis-Tsakonas S,. The Notch signalling system: Recent insights into the complexity of a conserved pathway. Nat Rev Genet 2012; 13: 654-666.
9. Phng LK, Gerhardt H,. Angiogenesis: A team effort coordinated by notch. Dev Cell 2009; 16: 196-208.
10. Noguera-Troise I, Daly C, Papadopoulos NJ, et al. Blockade of DLL4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 2006; 444: 1032-1037.
11. Liu J, Sato C, Cerletti M, et al. Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr Top Dev Biol 2010; 92: 367-409.
12. Stockhausen MT, Kristoffersen K, Poulsen HS,. Notch signaling and brain tumors. Adv Exp Med Biol 2012; 727: 289-304.
13. Wang J, Sullenger BA, Rich JN,. Notch signaling in cancer stem cells. Adv Exp Med Biol 2012; 727: 174-185.
14. Guichet PO, Bieche I, Teigell M, et al. Cell death and neuronal differentiation of glioblastoma stem-like cells induced by neurogenic transcription factors. Glia 2013; 61: 225-239.
15. Engin F, Yao Z, Yang T, et al. Dimorphic effects of Notch signaling in bone homeostasis. Nat Med 2008; 14: 299-305.
16. Salmon P, Trono D,. Production and titration of lentiviral vectors. Curr Prot Hum Genet 2007;Chapter 12:Unit 12.10.
17. Purow BW, Haque RM, Noel MW, et al. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res 2005; 65: 2353-2363.
18. Mizutani K, Yoon K, Dang L, et al. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 2007; 449: 351-355.
19. Tanigaki K, Nogaki F, Takahashi J, et al. Notch1 and Notch3 instructively restrict bFGF-responsive multipotent neural progenitor cells to an astroglial fate. Neuron 2001; 29: 45-55.
20. Gridley T,. Notch signaling in vascular development and physiology. Development 2007; 134: 2709-2718.
21. Klein T, Bischoff R,. Physiology and pathophysiology of matrix metalloproteases. Amino Acids 2011; 41: 271-290.
22. Gunther HS, Schmidt NO, Phillips HS, et al. Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene 2008; 27: 2897-2909.
23. Kanamori M, Kawaguchi T, Nigro JM, et al. Contribution of Notch signaling activation to human glioblastoma multiforme. J Neurosurg 2007; 106: 417-427.
24. Fan X, Khaki L, Zhu TS, et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 2010; 28: 5-16.
25. Kristoffersen K, Villingshoj M, Poulsen HS, et al. Level of Notch activation determines the effect on growth and stem cell-like features in glioblastoma multiforme neurosphere cultures. Cancer Biol Ther 2013; 14: 625-637.
26. Zheng Y, Lin L, Zheng Z,. TGF-alpha induces upregulation and nuclear translocation of Hes1 in glioma cell. Cell Biochem Funct 2008; 26: 692-700.
27. Gulino A, Di Marcotullio L, Screpanti I,. The multiple functions of Numb. Exp Cell Res 2010; 316: 900-906.
28. Chi Z, Zhang J, Tokunaga A, et al. Botch promotes neurogenesis by antagonizing Notch. Dev Cell 2012; 22: 707-720.
29. Zhang XP, Zheng G, Zou L, et al. Notch activation promotes cell proliferation and the formation of neural stem cell-like colonies in human glioma cells. Mol Cell Biochem 2008; 307: 101-108.
30. Wang J, Wang C, Meng Q, et al. siRNA targeting Notch-1 decreases glioma stem cell proliferation and tumor growth. Mol Biol Rep 2012; 39: 2497-2503.
31. Saito N, Fu J, Zheng S, et al. A high Notch pathway activation predicts response to gamma secretase inhibitors in proneural subtype of glioma tumor initiating cells. Stem Cells 2014; 32: 301-312.
32. Verhaak RG, Hoadley KA, Purdom E, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010; 17: 98-110.
33. Beier CP, Beier D,. CD133 negative cancer stem cells in glioblastoma. Front Biosci 2011; 3: 701-710.
34. Schulte A, Gunther HS, Phillips HS, et al. A distinct subset of glioma cell lines with stem cell-like properties reflects the transcriptional phenotype of glioblastomas and overexpresses CXCR4 as therapeutic target. Glia 2011; 59: 590-602.
35. Lobry C, Oh P, Aifantis I,. Oncogenic and tumor suppressor functions of Notch in cancer: It's NOTCH what you think. J Exp Med 2011; 208: 1931-1935.
36. Gangemi RM, Griffero F, Marubbi D, et al. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 2009; 27: 40-48.
37. Ligon KL, Huillard E, Mehta S, et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 2007; 53: 503-517.
38. Valdez JM, Zhang L, Su Q, et al. Notch and TGFbeta form a reciprocal positive regulatory loop that suppresses murine prostate basal stem/progenitor cell activity. Cell Stem Cell 2012; 11: 676-688.
39. Mourikis P, Sambasivan R, Castel D, et al. A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 2012; 30: 243-252.
40. Bjornson CR, Cheung TH, Liu L, et al. Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 2012; 30: 232-242.
41. Goel S, Duda DG, Xu L, et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev 2011; 91: 1071-1121.
42. Hedlund EM, Hosaka K, Zhong Z, et al. Malignant cell-derived PlGF promotes normalization and remodeling of the tumor vasculature. Proc Natl Acad Sci U S A 2009; 106: 17505-17510.
43. Brat DJ, Bellail AC, Van Meir EG,. The role of interleukin-8 and its receptors in gliomagenesis and tumoral angiogenesis. Neurooncol 2005; 7: 122-133.
44. Ongusaha PP, Kwak JC, Zwible AJ, et al. HB-EGF is a potent inducer of tumor growth and angiogenesis. Cancer Res 2004; 64: 5283-5290.
45. Mishima K, Higashiyama S, Asai A, et al. Heparin-binding epidermal growth factor-like growth factor stimulates mitogenic signaling and is highly expressed in human malignant gliomas. Acta Neuropathol 1998; 96: 322-328.
46. Digtyar AV, Pozdnyakova NV, Feldman NB, et al. Endostatin: Current concepts about its biological role and mechanisms of action. Biochemistry 2007; 72: 235-246.
47. Kume T,. Ligand-dependent Notch signaling in vascular formation. Adv Exp Med Biol 2012; 727: 210-222.
48. Ridgway J, Zhang G, Wu Y, et al. Inhibition of DLL4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 2006; 444: 1083-1087.
49. Patel NS, Dobbie MS, Rochester M, et al. Up-regulation of endothelial delta-like 4 expression correlates with vessel maturation in bladder cancer. Clin Cancer Res 2006; 12: 4836-4844.
50. Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000; 2: 737-744.
51. Labrie M, St-Pierre Y,. Epigenetic regulation of mmp-9 gene expression. Cell Mol Life Sci 2013; 70: 3109-3124.
52. Wang Z, Banerjee S, Li Y, et al. Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res 2006; 66: 2778-2784.
53. Funahashi Y, Shawber CJ, Sharma A, et al. Notch modulates VEGF action in endothelial cells by inducing matrix metalloprotease activity. Vasc Cell 2011; 3: 2.
54. Hensel T, Amberger VR, Schwab ME,. A metalloprotease activity from C6 glioma cells inactivates the myelin-associated neurite growth inhibitors and can be neutralized by antibodies. Br J Cancer 1998; 78: 1564-1572.
55. Du R, Petritsch C, Lu K, et al. Matrix metalloproteinase-2 regulates vascular patterning and growth affecting tumor cell survival and invasion in GBM. Neurooncol 2008; 10: 254-264.
56. Goldberg JS, Hirschi KK,. Diverse roles of the vasculature within the neural stem cell niche. Regen Med 2009; 4: 879-897.
57. Calabrese C, Poppleton H, Kocak M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007; 11: 69-82.
58. Zhu TS, Costello MA, Talsma CE, et al. Endothelial cells create a stem cell niche in glioblastoma by providing NOTCH ligands that nurture self-renewal of cancer stem-like cells. Cancer Res 2011; 71: 6061-6072.
59. Cheng L, Huang Z, Zhou W, et al. Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 2013; 153: 139-152.
60. Kluppel M, Wrana JL,. Turning it up a Notch: Cross-talk between TGF beta and Notch signaling. Bioessays 2005; 27: 115-118.
61. Dahlqvist C, Blokzijl A, Chapman G, et al. Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 2003; 130: 6089-6099.