Glioblastoma cancer-initiating cells inhibit T-cell proliferation and effector responses by the signal transducers and activators of transcription 3 pathway

Molecular Cancer Therapeutics

Volumn 9, Issue 1, 2010, Pages 67-78

  Wei, Jun ^a   Barr, Jason ^a   Kong, Ling Yuan ^a   Wang, Yongtao ^a   Wu, Adam ^a   Sharma, Amit K ^a   Gumin, Joy ^a   Henry, Verlene ^a   Colman, Howard ^a   Priebe, Waldemar ^a   Sawaya, Raymond ^a   Lang, Frederick F ^a   Heimberger, Amy B ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; B7 ANTIGEN; CD133 ANTIGEN; CD34 ANTIGEN; CD40 ANTIGEN; CD45 ANTIGEN; CD86 ANTIGEN; GALECTIN 3; INTERLEUKIN 2; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCYTE CHEMOTACTIC PROTEIN 1; PROSTAGLANDIN E2; PROTEIN INHIBITOR; SMALL INTERFERING RNA; STAT3 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN; WP 1066;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CLONING; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GLIOBLASTOMA; GLIOMA ASSOCIATED CANCER INITIATING CELL; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; T LYMPHOCYTE ACTIVATION; TUMOR XENOGRAFT;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SEPARATION; CHEMOKINES; GLIOBLASTOMA; HUMANS; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; PHOSPHOPROTEINS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 73949096430     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-09-0734     Document Type: Article

References (62)

1. Kurpad SN, Zhao XG, Wikstrand CJ, Batra SK, McLendon RE, Bigner DD. Tumor antigens in astrocytic gliomas [Review]. Glia 1995;15: 244-56.
2. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004;10:909-15.
3. Dey M, Hussain SF, Heimberger AB. The role of glioma microenvironment in immune modulation: potential targets for intervention. Lett Drug Des Discov 2006;3:443-51.
4. Hickey WF, Hsu BL, Kimura H. T-lymphocyte entry into the central nervous system. J Neurosci Res 1991;28:254-60.
5. Morford LA, Elliott LH, Carlson SL, Brooks WH, Roszman TL. T cell receptor-mediated signaling is defective in T cells obtained from patients with primary intracranial tumors. J Immunol 1997;159:4415-25.
6. Fontana A, Hengartner H, de Tribolet N, Weber E. Glioblastoma cells release interleukin 1 and factors inhibiting interleukin 2-mediated effects. J Immunol 1984;132:1837-44.
7. Elliott LH, Brooks WH, Roszman TL. Cytokinetic basis for the impaired activation of lymphocytes from patients with primary intracranial tumors. J Immunol 1984;132:1208-15.
8. Miescher S, Whiteside TL, de Tribolet N, von Fliedner V. In situ characterization, clonogenic potential, and antitumor cytolytic activity of T lymphocytes infiltrating human brain cancers. J Neurosurg 1988; 68:438-48.
9. Ashkenazi E, Deutsch M, Tirosh R, Weinreb A, Tsukerman A, Brodie C. A selective impairment of the IL-2 system in lymphocytes of patients with glioblastomas: increased level of soluble IL-2R and reduced protein tyrosine phosphorylation. Neuroimmunomodulation 1997;4:49-56.
10. Sanai N, Alvarez-Buylla A, Berger MS. Neural stem cells and the origin of gliomas. N Engl J Med 2005;353:811-22.
11. Liu G, Yuan X, Zeng Z, et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006;5:67-79.
12. Sun Y, Kong W, Falk A, et al. CD133 (Prominin) negative human neural stem cells are clonogenic and tripotent. PLoS One 2009;4:e5498.
13. Shmelkov SV, Butler JM, Hooper AT, et al. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest 2008;118:2111-20.
14. Bleau AM, Hambardzumyan D, Ozawa T, et al. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009;4: 226-35.
15. 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; 27:2897-909.
16. Galli R, Binda E, Orfanelli U, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004;64:7011-21.
17. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radio-resistance by preferential activation of the DNA damage response. Nature 2006;444:756-60.
18. Murat A, Migliavacca E, Gorlia T, et al. Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol 2008;26:3015-24.
19. Lang R, Patel D, Morris JJ, Rutschman RL, Murray PJ. Shaping gene expression in activated and resting primary macrophages by IL-10. J Immunol 2002;169:2253-63.
20. O'Farrell AM, Liu Y, Moore KW, Mui AL. IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: evidence for Stat3-dependent and -independent pathways. EMBO J 1998;17:1006-18.
21. Kortylewski M, Kujawski M, Wang T, et al. Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat Med 2005;11:1314-21.
22. Hussain SF, Kong L-Y, Jordan J, et al. A novel small molecule inhibitor of signal transducers and activators of transcription 3 reverses immune tolerance in malignant glioma patients. Cancer Res 2007; 67:9630-6.
23. Brantley EC, Nabors LB, Y GG, et al. 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.
24. Abou-Ghazal M, Yang DS, Qiao W, et al. The incidence, correlation with tumor-infiltrating inflammation, and prognosis of phosphorylated STAT3 expression in human gliomas. Clin Cancer Res 2008;14: 8228-35.
25. Yu H, Jove R. The STATs of cancer-new molecular targets come of age. Nat Rev Cancer 2004;4:97-105.
26. Yu H, Kortylewski M, Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol 2007;7:41-51.
27. Steinbrink K, Wolfl M, Jonuleit H, Knop J, Enk AH. Induction of tolerance by IL-10-treated dendritic cells. J Immunol 1997;159: 4772-80.
28. Williams L, Bradley L, Smith A, Foxwell B. Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J Immunol 2004;172: 567-76.
29. DiMeo D, Tian J, Zhang J, Narushima S, Berg DJ. Increased interleukin-10 production and Th2 skewing in the absence of 5-lipoxygenase. Immunology 2008;123:250-62.
30. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 1999;190: 995-1004.
31. Niu G, Bowman T, Huang M, et al. Roles of activated Src and Stat3 signaling in melanoma tumor cell growth. Oncogene 2002; 21:7001-10.
32. Gabrilovich DI, Chen HL, Girgis KR, et al. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells [erratum appears in Nat Med 1996 Nov;2: 1267]. Nat Med 1996;2:1096-103.
33. Rummel C, Sachot C, Poole S, Luheshi GN. Circulating interleukin-6 induces fever through a STAT3-linked activation of COX-2 in the brain. Am J Physiol Regul Integr Comp Physiol 2006;291: R1316-26.
34. Boniface K, Bak-Jensen KS, Li Y, et al. Prostaglandin E2 regulates Th17 cell differentiation and function through cyclic AMP and EP2/ EP4 receptor signaling. J Exp Med 2009;206:535-48.
35. Kinjyo I, Inoue H, Hamano S, et al. Loss of SOCS3 in T helper cells resulted in reduced immune responses and hyperproduction of interleukin 10 and transforming growth factor-β1. J Exp Med 2006;203: 1021-31.
36. Heimberger AB, Bigner DD, Sampson JJ. Biological principles of brain tumor immunotherapy. In: Liau LM, Becker DP, Cloughesy TF, Bigner DD, editors. Brain Tumor Immunotherapy. Totowa (NJ): Humana Press Inc.; 2000, p. 101-30.
37. Ferrajoli A, Faderl S, Van Q, et al. WP1066 disrupts Janus kinase-2 and induces caspase-dependent apoptosis in acute myelogenous leukemia cells. Cancer Res 2007;67:11291-9.
38. Sherry MM, Reeves A, Wu JK, Cochran BH. STAT3 is required for proliferation and maintenance of multipotency in glioblastoma stem cells. Stem Cells 2009;27:2383-92.
39. Iwamaru A, Szymanski S, Iwado E, et al. A novel inhibitor of the STAT3 pathway induces apoptosis in malignant glioma cells both in vitro and in vivo. Oncogene 2007;26:2435-44.
40. Kong LY, Abou-Ghazal MK, Wei J, et al. A novel inhibitor of signal transducers and activators of transcription 3 activation is efficacious against established central nervous system melanoma and inhibits regulatory T cells. Clin Cancer Res 2008;14:5759-68.
41. Kong L-K, Wei J, Sharma AK, et al. A novel phosphorylated STAT3 inhibitor enhances T cell cytotoxicity against melanoma through inhibition of regulatory T cells. Cancer Immunol Immunother 2008;58: 1023-32.
42. Heimberger AB, Priebe W. Small molecular inhibitors of p-STAT3: novel agents for treatment of primary and metastatic CNS cancers. Recent Patents CNS Drug Discov 2008;3:179-88.
43. Heimberger AB, Crotty LE, Archer GE, et al. Epidermal growth factor receptor VIII peptide vaccination is efficacious against established intracerebral tumors. Clin Cancer Res 2003;9:4247-54.
44. Lee A, Kessler JD, Read TA, et al. Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 2005;8:723-9.
45. Parant O, Dubernard G, Challier JC, et al. CD34+ cells in maternal placental blood are mainly fetal in origin and express endothelial markers. Lab Invest 2009;89:915-23.
46. Gomez GG, Kruse CA. Mechanisms of malignant glioma immune resistance and sources of immunosuppression. Gene Ther Mol Biol 2006;10a:133-46.
47. Parsa AT, Waldron JS, Panner A, et al. Loss of tumor suppressor PTEN function increases B7-1 expression and immunoresistance in glioma. Nat Med 2007;1:84-8.
48. Dong H, Strome SE, Salomao DR, et al. Tumor-associated B7-1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002;8:793-800.
49. Fecci PE, Mitchell DA, Whitesides JF, et al. Increased regulatory T-cell fraction amidst a diminished CD4 compartment explains cellular immune defects in patients with malignant glioma. Cancer Res 2006; 66:3294-302.
50. Heimberger AB, Reina-Ortiz C, Yang DS, et al. Incidence and prognostic impact of FoxP3+ regulatory T cells in human gliomas. Clin Cancer Res 2008;14:5166-72.
51. Jacobs JF, Idema AJ, Bol KF, et al. Regulatory T cells and the PD-L1/ PD-1 pathway mediate immune suppression in malignant human brain tumors. Neuro Oncol 2009;11:394-402.
52. Wei J, Duramad O, Perng OA, Reiner SL, Liu YJ, Qin FX. Antagonistic nature of T helper 1/2 developmental programs in opposing peripheral induction of Foxp3+ regulatory T cells. Proc Natl Acad Sci U S A 2007;104:18169-74.
53. Wang L, Yi T, Kortylewski M, Pardoll DM, Zeng D, Yu H. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med 2009;206:1457-64.
54. Sawa S, Kamimura D, Jin GH, et al. Autoimmune arthritis associated with mutated interleukin (IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+ T cells. J Exp Med 2006;203:1459-70.
55. Ghods AJ, Irvin D, Liu G, et al. Spheres isolated from 9L gliosarcoma rat cell line possess chemoresistant and aggressive cancer stem-like cells. Stem Cells 2007;25:1645-53.
56. Kang SK, Park JB, Cha SH. Multipotent, dedifferentiated cancer stem-like cells from brain gliomas. Stem Cells Dev 2006;15:423-35.
57. Zorn E, Nelson EA, Mohseni M, et al. IL-2 regulates FOXP3 expression in human CD4+CD25+ regulatory T cells through a STAT-dependent mechanism and induces the expansion of these cells in vivo. Blood 2006;108:1571-9.
58. Peng W, Wang HY, Miyahara Y, Peng G, Wang RF. Tumor-associated galectin-3 modulates the function of tumor-reactive T cells. Cancer Res 2008;68:7228-36.
59. Kuklinski S, Pesheva P, Heimann C, et al. Expression pattern of galectin-3 in neural tumor cell lines. J Neurosci Res 2000;60:45-57.
60. Strik HM, Schmidt K, Lingor P, et al. Galectin-1 expression in human glioma cells: modulation by ionizing radiation and effects on tumor cell proliferation and migration. Oncol Rep 2007;18:483-8.
61. Turkson J, Jove R. STAT proteins: novel molecular targets for cancer drug discovery. Oncogene 2000;19:6613-26.
62. Lin L, Amin R, Gallicano GI, et al. The STAT3 inhibitor NSC 74859 is effective in hepatocellular cancers with disrupted TGF-β signaling. Oncogene 2009;28:961-72.