STAT3 is essential for the maintenance of neurosphere-initiating tumor cells in patients with glioblastomas: A potential for targeted therapy?

International Journal of Cancer

Volumn 128, Issue 4, 2011, Pages 826-838

  Villalva, Claire ^a,b   Martin Lannerée, Severine ^c,d   Cortes, Ulrich ^a,b   Dkhissi, Fatima ^a,e   Wager, Michel ^a   Le Corf, Amélie ^a,b   Tourani, Jean Marc ^a   Dusanter Fourt, Isabelle ^c,d   Turhan, Ali G ^a,b   Karayan Tapon, Lucie ^a,b  

^a UNIVERSITÉ DE POITIERS   (France)

^b POITIERS UNIVERSITY HOSPITAL   (France)

^c INSTITUT COCHIN   (France)

^d INSERM   (France)

^e Université Sorbonne Paris Cité   (France)

Author keywords

glioblastomas; neurospheres; STAT3; stem like cells

Indexed keywords

ANTINEOPLASTIC AGENT; MESSENGER RNA; SMALL INTERFERING RNA; STAT3 PROTEIN; STATTIC; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; CELL PROLIFERATION; CELL RENEWAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA METHYLATION; DNA REPAIR; GLIOBLASTOMA; GROWTH INHIBITION; HUMAN; HUMAN CELL; IC 50; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR CELL;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CYCLIC S-OXIDES; DACARBAZINE; DRUG SYNERGISM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GLIOBLASTOMA; HUMANS; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; NEURAL STEM CELLS; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; STAT3 TRANSCRIPTION FACTOR; TUMOR CELLS, CULTURED;

EID: 78649876801     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25416     Document Type: Article

References (58)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, et al. Radiotherapy plus concomitant and adjuvant Temozolomide for glioblastoma. N Engl J Med 2005; 352: 987-96.
2. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavanee WK, DePinho RA,. Malignant glioma: genetics and biology of a grave matter. Genes Dev 2001; 15: 1311-33.
3. Stewart LA,. Chemotherapy in adult high-grade glioma: a systematic review and meta-analysis of individual patient data from 12 randomised trials. Lancet 2002; 359: 1011-18.
4. Singh SK, Clarke ID, Terasaki M, Bonn WE, Hawkins C, Squire J, Dirks PB,. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-8.
5. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB,. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401.
6. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, de Vitis 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: 7011-7021.
7. Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, Yu JS,. Isolation of cancer stem cell from adult glioblastoma multiforme. Oncogene 2004; 23: 9392-400.
8. Kang SK, Park JB, Cha SH,. Multipotent, dedifferentiated cancer stem-like cells from brain gliomas. Stem Cells Dev 2006; 15: 423-35.
9. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF,. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-8. (Pubitemid 36418143)
10. Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier CP,. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 2007; 67: 4010-15.
11. Ogden AT, Waziri AE, Lochhead RA, Fusco D, Lopez K, Ellis JA, Kang J, Assanah M, McKahnn GM, Sisti MB, McCormick PC, Canoll P, et al. Identification of A2B5+CD133- tumor-initiating cells in adult human gliomas. Neurosurgery 2008; 62: 505-15.
12. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS,. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006; 5: 67.
13. Beier D, Röhrl S, Pillai DR, Schwarz S, Kunz-Schughart LA, Leukel P, Proescholdt M, Brawanski A, Bogdahn U, Trampe-Kieslich A, Giebel B, Wischusen J, et al. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 2008; 68: 5706-15.
14. Kang MK, Kang SK,. Tumorigenesis of chemotherapeutic drug-resistant cancer stem-like cells in brain glioma. Stem Cells Dev 2007; 16: 837-47.
15. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN,. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 456-60.
16. Kalani MY, Cheshier SH, Cord BJ, Bababeygy SR, Vogel H, Weissman IL, Palmer TD, Nusse R,. Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci USA 2008; 105: 16970-5.
17. Cui H, Ma J, Ding J, Li T, Alam G, Ding HF,. Bmi-1 regulates the differentiation and clonogenic self-renewal of I-type neuroblastoma cells in a concentration-dependent manner. J Biol Chem 2006; 281: 34696-704.
18. Bar EE, Chaudhry A, Lin A, Fan X, Schreck K, Matsui W, Piccirillo S, Vescovi AL, DiMeco F, Olivi A, Eberhart CG,. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells 2007; 25: 2524-33.
19. Niwa H, Burdon T, Chambers I, Smith A,. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 1999; 12: 2048-60.
20. Matsuda T, Nakamura T, Nakao K, Arai T, Katsuki M, Heike T, Yokota T,. STAT3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells. EMBO J 1999; 18: 4261-9.
21. Levy DE, Lee CK,. What does Stat3 do? J Clin Invest 2002; 109: 1143-8.
22. Yu H, Jove R,. The STATs of cancer-new molecular targets come of age. Nat Rev Cancer 2004; 4: 97-105.
23. Wang H, Wang H, Zhang W, Huang HJ, Liao WS, Fuller GN,. Analysis of the activation status of Akt, NFkappaB and Stat3 in human diffuse glioma. Lab Invest 2004; 84: 941-51.
24. Weissenberger J, Loeffler S, Kappeler A, Kopf M, Lukes A, Afanasieva TA, Aguzzi A, Weis J,. IL-6 is required for glioma development in a mouse model. Oncogene 2004; 23: 3308-16.
25. Abou-Ghazal M, Yang DS, Qiao W, Reina-Ortiz C, Wei J, Kong LY, Fuller GN, Hiraoka N, Priebe W, Sawaya R, Heimberger AB,. The incidence, correlation with tumor-infiltrating inflammation, and prognosis of phosphorylated STAT3 expression in human gliomas. Clin Cancer Res 2008; 14: 8228-35.
26. Rahaman SO, Vogelbaum MA, Haque SJ,. Aberrant Stat3 signaling by interleukin-4 in malignant glioma cells: involvement of IL13Ralpha-2. Cancer Res 2005; 65: 2956-63.
27. Li GH, Wei H, Chen Z, Lv SQ, Yin CL, Wang DL,. STAT3 silencing with lentivirus inhibits growth and induces apoptosis and differentiation of U251 cells. J Neurooncol 2009; 91: 165-74.
28. Rahaman SO, Harbor PC, Chernova O, Barnett GH, Vogelbaum MA, Haque SJ,. Inhibition of constitutively active Stat3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells. Oncogene 2002; 21: 8404-13.
29. Konnikova L, Kotecki M, Kruger MM, Cochran BH,. Knockdown of STAT3 expression by RNAi induces apoptosis in astrocytoma cells. BMC Cancer 2003; 3: 23.
30. Lo HW, Cao X, Zhu H, Ali-Osman F,. Constitutively activated STAT3 frequently coexpresses with epidermal growth factor receptor in high-grade gliomas and targeting STAT3 sensitizes them to Iressa and alkylators. Clin Cancer Res 2008; 14: 6042-54.
31. Shen J, Li R, Li G,. Inhibitory effects of decoy-ODN targeting activated STAT3 on human glioma growth in vivo. In Vivo 2009; 23: 237-43.
32. Gu J, Li G, Sun T,. Blockage of the STAT3 signaling pathway with a decoy oligonucleotide suppresses growth of human malignant glioma cells. J Neurooncol 2008; 89: 9-17.
33. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der Kooy D,. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 1999; 208: 166-88.
34. Brunet de la Grange P, Armstrong F, Duval V, Rouyez MC, Goardon N, Romeo PH, Pflumio F,. Low SCL/TAL1 expression reveals its major role in adult hematopoietic myeloid progenitors and stem cells. Blood 2006; 108: 2998-3004.
35. Sirven A, Ravet E, Charneau P, Zennou V, Coulombel L, Guétard D, Pflumio F, Dubart-Kupperschmitt A,. Enhanced transgene expression in cord blood CD34(+)-derived hematopoietic cells, including developing T cells and NOD/SCID mouse repopulating cells, following transduction with modified trip lentiviral vectors. Mol Ther 2001; 3: 438-48.
36. Schust J, Sperl B, Hollis A, Mayer TU, Berg T,. Stattic: a small-molecule inhibitor of STAT3 activation and dimerization. Chem Biol 2006; 13: 1235-42.
37. Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, Baylin SB, Herman JG,. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 2000; 343: 1350-54.
38. Hegi ME, Diserens AC, Godard S, Dietrich PY, Regli L, Ostermann S, Otten P, van Melle G, de Tribolet N, Stupp R,. Clinical trial substantiates the predictive value of O-6-methylguanine-DNA methyltransferase promoter methylation in glioblastoma patients treated with temozolomide. Clin Cancer Res 2004; 10: 1871-4.
39. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005; 352: 997-1003.
40. Singec I, Knoth R, Meyer RP, Maciaczyk J, Volk B, Nikkhah G, Frotscher M, Snyder EY,. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat Methods 2006; 3: 801-6.
41. Coles-Takabe BL, Brain I, Purpura KA, Karpowicz P, Zandstra PW, Morshead CM, van der Kooy D,. Don't look: growing clonal versus nonclonal neural stem cell colonies. Stem Cells 2008; 26: 2938-44.
42. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ,. Efficient tumor formation by single human melanoma cells. Nature 2008; 456: 593-8.
43. Fuh B, Sobo M, Cen L, Josiah D, Hutzen B, Cisek K, Bhasin D, Regan N, Lin L, Chan C, Caldas H, de Angelis S, et al. LLL-3 inhibits STAT3 activity, suppresses glioblastoma cell growth and prolongs survival in a mouse glioblastoma model. Br J Cancer 2009; 13: 106-12.
44. Dasgupta A, Raychaudhuri B, Haqqi T, Haqqi T, Prayson R, van Meir EG, Vogelbaum M, Haque SJ,. Stat3 activation is required for the growth of U87 cell-derived tumours in mice. Eur J Cancer 2009; 45: 677-84.
45. Brantley EC, Nabors LB, Gillespie GY, Choi YH, Palmer CA, Harrison K, Roarty K, Benveniste EN,. Loss of protein inhibitors of activated STAT-3 expression in glioblastoma multiforme tumors: implications for STAT-3 activation and gene expression. Clin Cancer Res 2008; 14: 4694-704.
46. Su Y, Li G, Zhang X, Gu J, Zhang C, Tian Z, Zhang J,. JSI-124 inhibits glioblastoma multiforme cell proliferation through G(2)/M cell cycle arrest and apoptosis augment. Cancer Biol Ther 2008; 7: 1243-9.
47. Sherry M, Reeves A, Wu JK, Cochran BH,. STAT3 is required for proliferation and maintenance of multipotency in glioblatoma stem cells. Stem Cells 2009; 27: 2383-92.
48. D'Archivio M, Santangelo C, Scazzocchio B, Scazzocchio B, Varì R, Filesi C, Masella R, Giovannini C,. Modulatory effects of polyphenols on apoptosis induction: relevance for cancer prevention. Int J Mol Sci 2008; 9: 213-28.
49. Boehm AL, Sen M, Seethala R, Gooding WE, Freilino M, Wong SM, Wang S, Johnson DE, Grandis JR,. Combined targeting of epidermal growth factor receptor, signal transducer and activator of transcription-3, and Bcl-X(L) enhances antitumor effects in squamous cell carcinoma of the head and neck. Mol Pharmacol 2008; 73: 1632-42.
50. Sinibaldi D, Wharton W, Turkson J, Bowman T, Pledger WJ, Jove R,. Induction of p21WAF1/CIP1 and cyclin D1 expression by the Src oncoprotein in mouse fibroblasts: role of activated STAT3 signaling. Oncogene 2000; 19: 5419-27.
51. Germain D, Frank DA,. Targeting the cytoplasmic and nuclear functions of signal transducers and activators of transcription 3 for cancer therapy. Clin Cancer Res 2007; 13: 5665-9.
52. Yang J, Liao X, Agarwal MK,. Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFkappaB. Genes Dev 2007; 21: 1396-408.
53. Wegrzyn J, Potla R, Chwae YJ, Sepuri NB, Zhang Q, Koeck T, Derecka M, Szczepanek K, Szelag M, Gornicka A, Moh A, Mogghadas M, et al. Function of mitochondrial Stat3 in cellular respiration. Science 2009; 323: 793-7.
54. Brown S, Zeidler MP,. Unphosphorylated STATs go nuclear. Curr Opin Genet Dev 2008; 18: 455-60.
55. Wen Z, Zhong Z, Darnell JE, Jr,. Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 1995; 82: 241-50.
56. Zhang X, Blenis J, Li HC, Schindler C, Chen-Kiang S,. Requirement of serine phosphorylation for formation of STAT-promoter complexes. Science 1995; 267: 1990-4.
57. Gough DJ, Corlett A, Schlessinger K, Wegrzyn J, Larner AC, Levy DE,. Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 2009; 324: 1713-6.
58. Harir N, Pecquet C, Kerenyi M, Sonneck K, Kovacic B, Nyga R, Brevet M, Dhennin I, Gouilleux-Gruart V, Beug H, Valent P, Lassoued K, et al. Constitutive activation of Stat5 promotes its cytoplasmic localization and association with PI3-kinase in myeloid leukemias. Blood 2007; 109: 1678-86.