Endothelial cells promote stem-like phenotype of glioma cells through activating the Hedgehog pathway

Journal of Pathology

Volumn 234, Issue 1, 2014, Pages 11-22

  Yan, Guang Ning ^a   Yang, Lang ^a   Lv, Yang Fan ^a   Shi, Yu ^a   Shen, Li Li ^a   Yao, Xiao Hong ^a   Guo, Qiao Nan ^a   Zhang, Peng ^a   Cui, You Hong ^a   Zhang, Xia ^a   Bian, Xiu Wu ^a   Guo, De Yu ^a  

^a SOUTHWEST HOSPITAL   (China)

Author keywords

endothelial cell; glioma stem cell; hedgehog pathway; niche

Indexed keywords

BMI1 PROTEIN; CD133 ANTIGEN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR SOX2; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE; SHH PROTEIN, HUMAN;

ARTICLE; CANCER STEM CELL; CANCER SURVIVAL; CARCINOGENESIS; CARCINOGENICITY; COCULTURE; ENDOTHELIUM CELL; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; IN VITRO STUDY; MAJOR CLINICAL STUDY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR MICROENVIRONMENT; ALLOGRAFT; ANIMAL; BRAIN TUMOR; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GLIOMA; MALE; METABOLISM; MIDDLE AGED; MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION; STEM CELL NICHE; TUMOR CELL LINE;

ALLOGRAFTS; ANIMALS; ANTIGENS, CD; BRAIN NEOPLASMS; CELL LINE, TUMOR; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; GLIOMA; GLYCOPROTEINS; HEDGEHOG PROTEINS; HUMANS; MALE; MICE; MIDDLE AGED; NEOPLASTIC STEM CELLS; PEPTIDES; PHENOTYPE; SIGNAL TRANSDUCTION; STEM CELL NICHE; TUMOR MICROENVIRONMENT;

EID: 84905914556     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4349     Document Type: Article

References (63)

1. Li J, Di C, Mattox AK, et al., The future role of personalized medicine in the treatment of glioblastoma multiforme. Pharmgenom Pers Med 2010; 3: 111-127.
2. Welte Y, Adjaye J, Lehrach HR, et al., Cancer stem cells in solid tumors: elusive or illusive? Cell Commun Signal 2010; 8 (1): 6.
3. Rapp UR, Ceteci F, and, Schreck R,. Oncogene-induced plasticity and cancer stem cells. Cell Cycle 2008; 7 (1): 45-51.
4. Heddleston JM, Li Z, McLendon RE, et al., The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009; 8 (20): 3274-3284.
5. Moore KA,. Stem cells and their niches. Science 2006; 311: 1880-1885.
6. Ghajar CM, Peinado H, Mori H, et al., The perivascular niche regulates breast tumour dormancy. Nat Cell Biol 2013; 15 (7): 807-817.
7. Ritchie KE, Nör JE,. Perivascular stem cell niche in head and neck cancer. Cancer Lett 2012; 338 (1): 41-46.
8. Seidel S, Garvalov BK, Wirta V, et al., A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2. Brain 2010; 133 (4): 983-995.
9. Sleeman JP,. The metastatic niche and stromal progression. Cancer Metast Rev 2012; 31 (3-4): 429-440.
10. Pienta KJ, Robertson B, Coffey D, et al., The cancer diaspora: metastasis beyond the seed and soil hypothesis. Clin Cancer Res 2013; 19 (21): 5849-5855.
11. Borovski T, De Sousa E, Melo F, et al., Cancer stem cell niche: the place to be. Cancer Res 2011; 71 (3): 634-639.
12. Ping YF, Yao XH, Jiang JY, et al., The chemokine CXCL12 and its receptor CXCR4 promote glioma stem cell-mediated VEGF production and tumour angiogenesis via PI3K-AKT signalling. J Pathol 2011; 224 (3): 344-354.
13. Calabrese C, Poppleton H, Kocak M, et al., A perivascular niche for brain tumor stem cells. Cancer Cell 2007; 11 (1): 69-82.
14. Chen MH, Wilson CW, Chuang PT,. Snapshot: hedgehog signaling pathway. Cell 2007; 130 (2): 386.
15. Suling L, Gabriela D, Ilia DM, et al., Hedgehog signaling and bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res 2006; 66 (12): 6063-6071.
16. Shahi MH, Afzal M, Sinha S, et al., Regulation of sonic hedgehog-GLI1 downstream target genes PTCH1, Cyclin D2, Plakoglobin, PAX6 and NKX2.2 and their epigenetic status in medulloblastoma and astrocytoma. BMC Cancer 2010; 10 (1): 614.
17. O'Brien CA, Kreso A, Jamieson CHM,. Cancer stem cells and self-renewal. Clin Cancer Res 2010; 16 (12): 3113-3120.
18. Wang X, Venugopal C, Manoranjan B, et al., Sonic hedgehog regulates Bmi1 in human medulloblastoma brain tumor-initiating cells. Oncogene 2011; 31 (2): 187-199.
19. Yan GN, Lv YF, Yang L, et al., Glioma stem cells enhance endothelial cell migration and proliferation via the Hedgehog pathway. Oncol Lett 2013; 6 (5): 1524-1530.
20. Rota LM, Lazzarino DA, Ziegler AN, et al., Determining mammosphere-forming potential: application of the limiting dilution analysis. J Mamm Gland Biol Neoplasia 2012; 17 (2): 119-123.
21. Setti M, Savalli N, Osti D, et al., Functional role of CLIC1 ion channel in glioblastoma-derived stem/progenitor cells. J Natl Cancer Inst 2013; 105 (21): 1644-1655.
22. Naito S, von Eschenbach AC, Giavazzi R, et al., Growth and metastasis of tumor cells isolated from a human renal cell carcinoma implanted into different organs of nude mice. Cancer Res 1986; 46 (8): 4109-4115.
23. Wang H, Zhang D, Wu W, et al., Overexpression and gender-specific differences of SRC-3 (SRC-3/AIB1) immunoreactivity in human non-small cell lung cancer: an in vivo study. J Histochem Cytochem 2010; 58 (12): 1121-1127.
24. Korkolopoulou P, Konstantinidou AE, Kavantzas N, et al., Morphometric microvascular characteristics predict prognosis in superficial and invasive bladder cancer. Virchows Arch 2001; 438 (6): 603-611.
25. Kenney AM, Cole MD, Rowitch DH., Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 2003; 130 (1): 15-28.
26. Oliver TG, Grasfeder LL, Carroll AL, et al., Transcriptional profiling of the Sonic hedgehog response: a critical role for N-myc in proliferation of neuronal precursors. Proc Natl Acad Sci USA 2003; 100 (12): 7331-7336.
27. 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 (4): 503-517.
28. Nagata S, Hirano K, Kanemori M, et al., Self-renewal and pluripotency acquired through somatic reprogramming to human cancer stem cells. PLoS One 2012; 7 (11): e48699.
29. Takezaki T, Hide T, Takanaga H, et al., Essential role of the Hedgehog signaling pathway in human glioma-initiating cells. Cancer Sci 2011; 102 (7): 1306-1312.
30. Hu YY, Zheng MH, Cheng G, et al., Notch signaling contributes to the maintenance of both normal neural stem cells and patient-derived glioma stem cells. BMC Cancer 2011; 11 (1): 82.
31. Nager M, Bhardwaj D, Cantí C, et al., β-catenin signalling in glioblastoma multiforme and glioma-initiating cells. Chemother Res Pract 2012; 2012: 1-7.
32. Santisteban M, Reiman JM, Asiedu MK, et al., Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res 2009; 69 (7): 2887-2895.
33. Gupta PB, Chaffer CL, Weinberg RA,. Cancer stem cells: mirage or reality? Nat Med 2009; 15 (9): 1010-1012.
34. Iwasaki H, Suda T,. Cancer stem cells and their niche. Cancer Sci 2009; 100 (7): 1166-1172.
35. Barami K., Relationship of neural stem cells with their vascular niche: implications in the malignant progression of gliomas. J Clin Neurosci 2008; 15 (11): 1193-1197.
36. + niches and single cells in glioblastoma have different phenotypes. J Neurooncol 2010; 104 (1): 129-143.
37. Charles N, Ozawa T, Squatrito M, et al., Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells. Cell Stem Cell 2010; 6 (2): 141-152.
38. Butler JM, Kobayashi H, Rafii S,. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer 2010; 10 (2): 138-146.
39. Charalambous C, Virrey J, Kardosh A, et al., Glioma-associated endothelial cells show evidence of replicative senescence. Exp Cell Res 2007; 313 (6): 1192-1202.
40. Charalambous C, Chen TC, Hofman FM., Characteristics of tumor-associated endothelial cells derived from glioblastoma multiforme. Neurosurg Focus 2006; 20 (4): E22.
41. Hovinga KE, Shimizu F, Wang R, et al., Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate. Stem Cells 2010; 28 (6): 1019-1029.
42. 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 (18): 6061-6072.
43. Lu J, Ye XC, Fan F, et al., Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 2013; 23 (2): 171-185.
44. Hambardzumyan D, Becher OJ, Rosenblum MK, et al., PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev 2008; 22 (4): 436-448.
45. Xu Q, Yuan XP, Liu GT, et al., Hedgehog signaling regulates brain tumor-initiating cell proliferation and portends shorter survival for patients with PTEN-coexpressing glioblastomas. Stem Cells 2008; 26 (12): 3018-3026.
46. Kool M, Korshunov A, Remke M, et al., Molecular subgroups of medulloblastoma: an international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, Group 3, and Group 4 medulloblastomas. Acta Neuropathol 2012; 123 (4): 473-484.
47. Pugh TJ, Weeraratne SD, Archer TC, et al., Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 2012; 488 (7409): 106-110.
48. Goodrich LV, Milenkovic L, Higgins KM, et al., Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997; 277 (5329): 1109-1113.
49. Michael LE, Westerman BA, Ermilov AN, et al., Bmi1 is required for hedgehog pathway-driven medulloblastoma expansion. Neoplasia 2008; 10 (12): 1343-1349.
50. Gerardo Valadez J, Grover VK, Carter MD, et al., Identification of Hedgehog pathway responsive glioblastomas by isocitrate dehydrogenase mutation. Cancer Lett 2013; 328 (2): 297-306.
51. Clement V, Sanchez P, de Tribolet N, et al., HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 2007; 17 (2): 165-172.
52. Sarangi A, Valadez JG, Rush S, et al., Targeted inhibition of the Hedgehog pathway in established malignant glioma xenografts enhances survival. Oncogene 2009; 28 (39): 3468-3476.
53. Bar EE, Chaudhry A, Lin A, et al., Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 2007; 25 (10): 2524-2533.
54. Yauch RL, Gould SE, Scales SJ, et al., A paracrine requirement for hedgehog signalling in cancer. Nature 2008; 455 (7211): 406-410.
55. Ehtesham M, Sarangi A, Valadez JG, et al., Ligand-dependent activation of the hedgehog pathway in glioma progenitor cells. Oncogene 2007; 26 (39): 5752-5761.
56. Becher OJ, Hambardzumyan D, Fomchenko EI, et al., Gli activity correlates with tumor grade in platelet-derived growth factor-induced gliomas. Cancer Res 2008; 68 (7): 2241-2249.
57. Kasperczyk H, Baumann B, Debatin KM, et al., Characterization of sonic hedgehog as a novel NF-κB target gene that promotes NF-κB-mediated apoptosis resistance and tumor growth in vivo. FASEB J 2009; 23 (1): 21-33.
58. Singh AP, Arora S, Bhardwaj A, et al., CXCL12/CXCR4 protein signaling axis induces sonic hedgehog expression in pancreatic cancer cells via extracellular regulated kinase- and Akt kinase-mediated activation of nuclear factor B: implications for bidirectional tumor-stromal interactions. J Biol Chem 2012; 287 (46): 39115-391
59. Moran CM, Myers CT, Lewis CM, et al., Hedgehog regulates angiogenesis of intersegmental vessels through the VEGF signaling pathway. Dev Dyn 2012; 241 (6): 1034-1042.
60. Folkins C, Shaked Y, Man S, et al., 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.
61. Kenig S, Alonso MB, Mueller MM, et al., Glioblastoma and endothelial cells cross-talk, mediated by SDF-1, enhances tumour invasion and endothelial proliferation by increasing expression of cathepsins B, S, and MMP-9. Cancer Lett 2010; 289 (1): 53-61.
62. Robles Irizarry L, Hambardzumyan D, Nakano I, et al., Therapeutic targeting of VEGF in the treatment of glioblastoma. Expert Opin Ther Targets 2012; 16 (10): 973-984.
63. Huang Z, Cheng L, Guryanova OA, et al., Cancer stem cells in glioblastoma-molecular signaling and therapeutic targeting. Protein Cell 2010; 1 (7): 638-655.