A combined gene signature of hypoxia and Notch pathway in human glioblastoma and its prognostic relevance

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Irshad, Khushboo ^a   Mohapatra, Saroj Kant ^b   Srivastava, Chitrangda ^a   Garg, Harshit ^a   Mishra, Seema ^c   Dikshit, Bhawana ^a   Sarkar, Chitra ^a   Gupta, Deepak ^a   Chandra, Poodipedi Sarat ^a   Chattopadhyay, Parthaprasad ^a   Sinha, Subrata ^d   Chosdol, Kunzang ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^b NATIONAL INSTITUTE OF BIOMEDICAL GENOMICS   (India)

^c UNIVERSITY OF HYDERABAD   (India)

^d NATIONAL BRAIN RESEARCH CENTRE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONATE DEHYDRATASE IX; DLL1 PROTEIN; DLL3 PROTEIN; DLL4 PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; JAGGED1; JAGGED2; MEMBRANE PROTEIN; MESSENGER RNA; NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; NOTCH4 RECEPTOR; OSTEOPONTIN; OXYGEN; PHOSPHOGLYCERATE KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR HES 2; TRANSCRIPTION FACTOR HES 5; TRANSCRIPTION FACTOR HES 6; TRANSCRIPTION FACTOR HEY 1; TRANSCRIPTION FACTOR HEY 2; UNCLASSIFIED DRUG; VASCULOTROPIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HES1 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; PGK1 PROTEIN, HUMAN;

ARTICLE; BRAIN SURGERY; CANCER PROGNOSIS; CANCER SURVIVAL; CLINICAL ARTICLE; CLUSTER ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DIAGNOSTIC TEST ACCURACY STUDY; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IN VITRO STUDY; MALE; MONOLAYER CULTURE; POLYMERASE CHAIN REACTION; PREDICTION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SENSITIVITY AND SPECIFICITY; STATISTICAL ANALYSIS; UPREGULATION; BRAIN NEOPLASMS; CELL HYPOXIA; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MORTALITY; PATHOLOGY; PRINCIPAL COMPONENT ANALYSIS; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN NEOPLASMS; CELL HYPOXIA; CLUSTER ANALYSIS; GLIOBLASTOMA; HOMEODOMAIN PROTEINS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KAPLAN-MEIER ESTIMATE; OSTEOPONTIN; PHOSPHOGLYCERATE KINASE; PRINCIPAL COMPONENT ANALYSIS; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR HES-1; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 84928902768     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118201     Document Type: Article

References (56)

1. Kesari S (2011) Understanding glioblastoma tumor biology: the potential to improve current diagnosis and treatments. Semin Oncol 38 Suppl 4: S2-10. doi: 10.1053/j.seminoncol.2011.09.005 PMID: 22078644
2. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, et al. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352: 987-996. PMID: 15758009
3. Grossman SA, Ye X, Piantadosi S, Desideri S, Nabors LB, et al. (2010) Survival of patients with newly diagnosed glioblastoma treated with radiation and temozolomide in research studies in the United States. Clin Cancer Res 16: 2443-2449. doi: 10.1158/1078-0432.CCR-09-3106 PMID: 20371685
4. Gravendeel LA, Kouwenhoven MC, Gevaert O, de Rooi JJ, Stubbs AP, et al. (2009) Intrinsic gene expression profiles of gliomas are a better predictor of survival than histology. Cancer Res 69: 9065-9072. doi: 10.1158/0008-5472.CAN-09-2307 PMID: 19920198
5. Ruano Y, Mollejo M, Camacho FI, Rodriguez de Lope A, Fiano C, et al. (2008) Identification of survival-related genes of the phosphatidylinositol 30′-kinase signaling pathway in glioblastoma multiforme. Cancer 112: 1575-1584. doi: 10.1002/cncr.23338 PMID: 18260157
6. Wong DJ, Nuyten DS, Regev A, Lin M, Adler AS, et al. (2008) Revealing targeted therapy for human cancer by gene module maps. Cancer Res 68: 369-378. doi: 10.1158/0008-5472.CAN-07-0382 PMID: 18199530
7. Persano L, Rampazzo E, Della Puppa A, Pistollato F, Basso G (2011) The three-layer concentric model of glioblastoma: cancer stem cells, microenvironmental regulation, and therapeutic implications. ScientificWorldJournal 11: 1829-1841. doi: 10.1100/2011/736480 PMID: 22125441
8. Rapisarda A, Melillo G (2012) Overcoming disappointing results with antiangiogenic therapy by targeting hypoxia. Nat Rev Clin Oncol 9: 378-390. doi: 10.1038/nrclinonc.2012.64 PMID: 22525710
9. Semenza GL (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732. PMID: 13130303
10. Wilson WR, Hay MP (2011) Targeting hypoxia in cancer therapy. Nat Rev Cancer 11: 393-410. doi: 10.1038/nrc3064 PMID: 21606941
11. Said HM, Hagemann C, Staab A, Stojic J, Kuhnel S, et al. (2007) Expression patterns of the hypoxia-related genes osteopontin, CA9, erythropoietin, VEGF and HIF-1alpha in human glioma in vitro and in vivo. Radiother Oncol 83: 398-405. PMID: 17524506
12. Zhu Y, Denhardt DT, Cao H, Sutphin PD, Koong AC, et al. (2005) Hypoxia upregulates osteopontin expression in NIH-3T3 cells via a Ras-activated enhancer. Oncogene 24: 6555-6563. PMID: 16007184
13. Flynn JR, Wang L, Gillespie DL, Stoddard GJ, Reid JK, et al. (2008) Hypoxia-regulated protein expression, patient characteristics, and preoperative imaging as predictors of survival in adults with glioblastoma multiforme. Cancer 113: 1032-1042. doi: 10.1002/cncr.23678 PMID: 18618497
14. Lino MM, Merlo A, Boulay JL (2010) Notch signaling in glioblastoma: a developmental drug target? BMC Med 8: 72. doi: 10.1186/1741-7015-8-72 PMID: 21078177
15. Koch U, Radtke F (2007) Notch and cancer: a double-edged sword. Cell Mol Life Sci 64: 2746-2762. PMID: 17687513
16. Lobry C, Oh P, Aifantis I (2011) Oncogenic and tumor suppressor functions of Notch in cancer: it's NOTCH what you think. J Exp Med 208: 1931-1935. doi: 10.1084/jem.20111855 PMID: 21948802
17. Xing F, Okuda H, Watabe M, Kobayashi A, Pai SK, et al. (2011) Hypoxia-induced Jagged2 promotes breast cancer metastasis and self-renewal of cancer stem-like cells. Oncogene 30: 4075-4086. doi: 10.1038/onc.2011.122 PMID: 21499308
18. Purow BW, Haque RM, Noel MW, Su Q, Burdick MJ, et al. (2005) Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res 65: 2353-2363. PMID: 15781650
19. Main H, Lee KL, Yang H, Haapa-Paananen S, Edgren H, et al. (2010) Interactions between Notch- and hypoxia-induced transcriptomes in embryonic stem cells. Exp Cell Res 316: 1610-1624. doi: 10.1016/j.yexcr.2009.12.012 PMID: 20034489
20. Diez H, Fischer A, Winkler A, Hu CJ, Hatzopoulos AK, et al. (2007) Hypoxia-mediated activation of Dll4-Notch-Hey2 signaling in endothelial progenitor cells and adoption of arterial cell fate. Exp Cell Res 313: 1-9. PMID: 17045587
21. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, et al. (2005) Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9: 617-628. PMID: 16256737
22. Zheng X, Linke S, Dias JM, Gradin K, Wallis TP, et al. (2008) Interaction with factor inhibiting HIF-1 defines an additional mode of cross-coupling between the Notch and hypoxia signaling pathways. Proc Natl Acad Sci U S A 105: 3368-3373. doi: 10.1073/pnas.0711591105 PMID: 18299578
23. Chen J, Imanaka N, Griffin JD (2010) Hypoxia potentiates Notch signaling in breast cancer leading to decreased E-cadherin expression and increased cell migration and invasion. Br J Cancer 102: 351-360. doi: 10.1038/sj.bjc.6605486 PMID: 20010940
24. Mimeault M, Batra SK (2013) Hypoxia-inducing factors as master regulators of stemness properties and altered metabolism of cancer- and metastasis-initiating cells. J Cell Mol Med.
25. Liang D, Ma Y, Liu J, Trope CG, Holm R, et al. (2012) The hypoxic microenvironment upgrades stem-like properties of ovarian cancer cells. BMC Cancer 12: 201. doi: 10.1186/1471-2407-12-201 PMID: 22642602
26. Sharma A, Paranjape AN, Rangarajan A, Dighe RR (2012) A monoclonal antibody against human Notch1 ligand-binding domain depletes subpopulation of putative breast cancer stem-like cells. Mol Cancer Ther 11: 77-86. doi: 10.1158/1535-7163.MCT-11-0508 PMID: 22075160
27. Hu YY, Zheng MH, Cheng G, Li L, Liang L, et al. (2011) Notch signaling contributes to the maintenance of both normal neural stem cells and patient-derived glioma stem cells. BMC Cancer 11: 82. doi: 10.1186/1471-2407-11-82 PMID: 21342503
28. Bar EE, Lin A, Mahairaki V, Matsui W, Eberhart CG (2010) Hypoxia increases the expression of stemcell markers and promotes clonogenicity in glioblastoma neurospheres. Am J Pathol 177: 1491-1502. doi: 10.2353/ajpath.2010.091021 PMID: 20671264
29. Pistollato F, Rampazzo E, Persano L, Abbadi S, Frasson C, et al. (2010) Interaction of hypoxia-inducible factor-1alpha and Notch signaling regulates medulloblastoma precursor proliferation and fate. Stem Cells 28: 1918-1929. doi: 10.1002/stem.518 PMID: 20827750
30. Seidel S, Garvalov BK, Wirta V, von Stechow L, Schanzer A, et al. (2010) A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha. Brain 133: 983-995. doi: 10.1093/brain/awq042 PMID: 20375133
31. Qiang L, Wu T, Zhang HW, Lu N, Hu R, et al. (2012) HIF-1alpha is critical for hypoxia-mediated maintenance of glioblastoma stem cells by activating Notch signaling pathway. Cell Death Differ 19: 284-294. doi: 10.1038/cdd.2011.95 PMID: 21818118
32. Kanamori M, Kawaguchi T, Nigro JM, Feuerstein BG, Berger MS, et al. (2007) Contribution of Notch signaling activation to human glioblastoma multiforme. J Neurosurg 106: 417-427. PMID: 17367064
33. Li Z, Wang J, Gong L, Wen Z, Xu C, et al. (2011) Correlation of Delta-like ligand 4 (DLL4) with VEGF and HIF-1alpha expression in human glioma. Asian Pac J Cancer Prev 12: 215-218. PMID: 21517260
34. Chigurupati S, Venkataraman R, Barrera D, Naganathan A, Madan M, et al. (2010) Receptor channel TRPC6 is a key mediator of Notch-driven glioblastoma growth and invasiveness. Cancer Res 70: 418-427. doi: 10.1158/0008-5472.CAN-09-2654 PMID: 20028870
35. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U (2008) Notch signaling mediates hypoxiainduced tumor cell migration and invasion. Proc Natl Acad Sci U S A 105: 6392-6397. doi: 10.1073/pnas.0802047105 PMID: 18427106
36. Huang XD, Wang ZF, Dai LM, Li ZQ (2012) Microarray analysis of the hypoxia-induced gene expression profile in malignant C6 glioma cells. Asian Pac J Cancer Prev 13: 4793-4799. PMID: 23167422
37. Phung YT, Barbone D, Broaddus VC, Ho M (2011) Rapid generation of in vitro multicellular spheroids for the study of monoclonal antibody therapy. J Cancer 2: 507-514. PMID: 22043235
38. Palanichamy JK, Mehndiratta M, Bhagat M, Ramalingam P, Das B, et al. (2010) Silencing of integrated human papillomavirus-16 oncogenes by small interfering RNA-mediated heterochromatization. Mol Cancer Ther 9: 2114-2122. doi: 10.1158/1535-7163.MCT-09-0977 PMID: 20587668
39. Shahi MH, Afzal M, Sinha S, Eberhart CG, Rey JA, et al. (2010) 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 10: 614. doi: 10.1186/1471-2407-10-614 PMID: 21059263
40. Datta K, Babbar P, Srivastava T, Sinha S, Chattopadhyay P (2002) p53 dependent apoptosis in glioma cell lines in response to hydrogen peroxide induced oxidative stress. Int J Biochem Cell Biol 34: 148-157. PMID: 11809417
41. Sermeus A, Michiels C (2011) Reciprocal influence of the p53 and the hypoxic pathways. Cell Death Dis 2: e164. doi: 10.1038/cddis.2011.48 PMID: 21614094
42. Kamat CD, Green DE, Warnke L, Thorpe JE, Ceriello A, et al. (2007) Mutant p53 facilitates pro-angiogenic, hyperproliferative phenotype in response to chronic relative hypoxia. Cancer Lett 249: 209-219. PMID: 16997458
43. Choy MK, Movassagh M, Bennett MR, Foo RS (2010) PKB/Akt activation inhibits p53-mediated HIF1A degradation that is independent of MDM2. J Cell Physiol 222: 635-639. doi: 10.1002/jcp.21980 PMID: 19950214
44. Mendez O, Zavadil J, Esencay M, Lukyanov Y, Santovasi D, et al. (2010) Knock down of HIF-1alpha in glioma cells reduces migration in vitro and invasion in vivo and impairs their ability to form tumor spheres. Mol Cancer 9: 133. doi: 10.1186/1476-4598-9-133 PMID: 20515450
45. Zagzag D, Zhong H, Scalzitti JM, Laughner E, Simons JW, et al. (2000) Expression of hypoxia-inducible factor 1alpha in brain tumors: association with angiogenesis, invasion, and progression. Cancer 88: 2606-2618. PMID: 10861440
46. Martinez-Gonzalez A, Calvo GF, Perez Romasanta LA, Perez-Garcia VM (2012) Hypoxic cell waves around necrotic cores in glioblastoma: a biomathematical model and its therapeutic implications. Bull Math Biol 74: 2875-2896. doi: 10.1007/s11538-012-9786-1 PMID: 23151957
47. Chung FY, Huang MY, Yeh CS, Chang HJ, Cheng TL, et al. (2009) GLUT1 gene is a potential hypoxic marker in colorectal cancer patients. BMC Cancer 9: 241. doi: 10.1186/1471-2407-9-241 PMID: 19619276
48. Zheng Y, Ni Y, Huang X, Wang Z, Han W (2013) Overexpression of HIF-1alpha indicates a poor prognosis in tongue carcinoma and may be associated with tumour metastasis. Oncol Lett 5: 1285-1289. PMID: 23599780
49. Wos J, Brys M, Lewy-Trenda I, Stasikowska O, Papiez P, et al. (2011) Analysis of HIF-1alpha and COX-2 expression in tumor stroma and correlation with the degree of neoplasm invasiveness in laryngeal cancer - preliminary study. Otolaryngol Pol 65: 102-108. PMID: 22000259
50. Nakajima T, Anayama T, Koike T, Shingyoji M, Castle L, et al. (2012) Endobronchial ultrasound doppler image features correlate with mRNA expression of HIF1-alpha and VEGF-C in patients with non-smallcell lung cancer. J Thorac Oncol 7: 1661-1667. doi: 10.1097/JTO.0b013e318265b4df PMID: 23059773
51. Dai CX, Gao Q, Qiu SJ, Ju MJ, Cai MY, et al. (2009) Hypoxia-inducible factor-1 alpha, in association with inflammation, angiogenesis and MYC, is a critical prognostic factor in patients with HCC after surgery. BMC Cancer 9: 418. doi: 10.1186/1471-2407-9-418 PMID: 19948069
52. Colman H, Zhang L, Sulman EP, McDonald JM, Shooshtari NL, et al. (2010) A multigene predictor of outcome in glioblastoma. Neuro Oncol 12: 49-57. doi: 10.1093/neuonc/nop007 PMID: 20150367
53. Cornero A, Acquaviva M, Fardin P, Versteeg R, Schramm A, et al. (2012) Design of a multi-signature ensemble classifier predicting neuroblastoma patients' outcome. BMC Bioinformatics 13 Suppl 4: S13. doi: 10.1186/1471-2105-13-S4-S13 PMID: 22536959
54. Li A, Walling J, Kotliarov Y, Center A, Steed ME, et al. (2008) Genomic changes and gene expression profiles reveal that established glioma cell lines are poorly representative of primary human gliomas. Mol Cancer Res 6: 21-30. doi: 10.1158/1541-7786.MCR-07-0280 PMID: 18184972
55. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, et al. (2006) 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 9: 391-403. PMID: 16697959
56. Iacopino F, Angelucci C, Piacentini R, Biamonte F, Mangiola A, et al. (2014) Isolation of cancer stem cells from three human glioblastoma cell lines: characterization of two selected clones. PLoS One 9: e105166. doi: 10.1371/journal.pone.0105166 PMID: 25121761