Significance of interleukin-13 receptor alpha 2-targeted Glioblastoma therapy

Neuro-Oncology

Volumn 16, Issue 10, 2014, Pages 1304-1312

  Thaci, Bart ^b   Brown, Christine E ^c   Binello, Emanuela ^b   Werbaneth, Katherine ^b   Sampath, Prakash ^a,b   Sengupta, Sadhak ^a,b  

^a ROGER WILLIAMS MEDICAL CENTER   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Glioblastoma; Glioma; IL13R 2; Immunotherapy; Toxin

Indexed keywords

CINTREDEKIN BESUDOTOX; HYBRID PROTEIN; INTERLEUKIN 13 RECEPTOR ALPHA2; LIPOSOME; T LYMPHOCYTE RECEPTOR; TUMOR ANTIGEN; EXOTOXIN; IL13-PE38QQR; INTERLEUKIN 13;

ADVERSE OUTCOME; ARTICLE; AUTOTRANSPLANTATION; CANCER IMMUNOTHERAPY; CARCINOGENESIS; CD8+ T LYMPHOCYTE; CLINICAL EFFECTIVENESS; CLINICAL STUDY; CONFUSION; DENDRITIC CELL; DRUG EFFICACY; DRUG MECHANISM; FATIGUE; GAIT DISORDER; GLIOBLASTOMA; HEADACHE; HEMIPARESIS; HUMAN; LUNG EMBOLISM; NONHUMAN; NYSTAGMUS; OVERALL SURVIVAL; PARESTHESIA; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SEIZURE; SPEECH DISORDER; STRUCTURE ANALYSIS; ANIMAL; BRAIN NEOPLASMS; CLINICAL TRIAL (TOPIC); DISEASE MODEL; IMMUNOLOGY; MOLECULARLY TARGETED THERAPY; MOUSE; PROCEDURES; TREATMENT OUTCOME;

ANIMALS; BRAIN NEOPLASMS; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; EXOTOXINS; GLIOBLASTOMA; HUMANS; INTERLEUKIN-13; INTERLEUKIN-13 RECEPTOR ALPHA2 SUBUNIT; LIPOSOMES; MICE; MOLECULAR TARGETED THERAPY; TREATMENT OUTCOME;

EID: 84935912627     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nou045     Document Type: Article

References (87)

1. Stupp R, Hegi ME, Mason WP, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459-466.
2. Van Meir EG, Hadjipanayis CG, Norden AD, et al. Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J Clin. 2010;60(3):166-193.
3. Wainwright DA, Nigam P, Thaci B, et al. Recent developments on immunotherapy for brain cancer. Expert Opin Emerg Drugs. 2012;17(2):181-202.
4. Porter DL, Levine BL, Kalos M, et al. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365(8):725-733.
5. Kochenderfer JN, Dudley ME, Feldman SA, et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood. 2012;119(12):2709-2720.
6. Brentjens RJ, Riviere I, Park JH, et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood. 2011;118(18):4817-4828.
7. Verma S, Miles D, Gianni L, et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med. 2012;367(19):1783-1791.
8. Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711-723.
9. Debinski W, Gibo DM, Hulet SW, et al. Receptor for interleukin 13 is a marker and therapeutic target for human high-grade gliomas. Clin Cancer Res. 1999;5(5):985-990.
10. Minty A, Chalon P, Derocq JM, et al. Interleukin-13 is a new human lymphokine regulating inflammatory and immune responses. Nature. 1993;362(6417):248-250.
11. Terabe M, Matsui S, Noben-Trauth N, et al. NKT cell-mediated repression of tumor immunosurveillance by IL-13 and the IL-4R-STAT6 pathway. Nat Immunol. 2000;1(6):515-520.
12. Fichtner-Feigl S, Strober W, Kawakami K, et al. IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat Med. 2006;12(1):99-106.
13. Arima K, Sato K, Tanaka G, et al. Characterization of the interaction between interleukin-13 and interleukin-13 receptors. J Biol Chem. 2005;280(26):24915-24922.
14. Debinski W, Gibo DM. Molecular expression analysis of restrictive receptor for interleukin 13, a brain tumor-associated cancer/testis antigen. Mol Med. 2000;6(5):440-449.
15. Andrews AL, Nasir T, Bucchieri F, et al. IL-13 receptor alpha 2: a regulator of IL-13 and IL-4 signal transduction in primary human fibroblasts. J Allergy Clin Immunol. 2006;118(4):858-865.
16. Tabata Y, Khurana Hershey GK. IL-13 receptor isoforms: breaking through the complexity. Curr Allergy Asthma Rep. 2007;7(5):338-345.
17. DebinskiW, Obiri NI, Powers SK, et al. Human glioma cells overexpress receptors for interleukin 13 and are extremely sensitive to a novel chimeric protein composed of interleukin 13 and pseudomonas exotoxin. Clin Cancer Res. 1995;1(11):1253-1258.
18. Rahaman SO, Sharma P, Harbor PC, et al. IL-13R (alpha) 2, a decoy receptor for IL-13 acts as an inhibitor of IL-4-dependent signal transduction in glioblastoma cells. Cancer Res. 2002;62(4):1103-1109.
19. Hsi LC, Kundu S, Palomo J, et al. Silencing IL-13Ralpha2 promotes glioblastoma cell death via endogenous signaling. Mol Cancer Ther. 2011;10(7):1149-1160.
20. Viita H, Pacholska A, Ahmad F, et al. 15-Lipoxygenase-1 induces lipid peroxidation and apoptosis, and improves survival in rat malignant glioma. In Vivo. 2012;26(1):1-8.
21. Hilton DJ, Zhang JG, Metcalf D, et al. Cloning and characterization of a binding subunit of the interleukin 13 receptor that is also a component of the interleukin 4 receptor. Proc Natl Acad Sci U S A. 1996;93(1):497-501.
22. Aman MJ, Tayebi N, Obiri NI, et al. cDNA cloning and characterization of the human interleukin 13 receptor alpha chain. J Biol Chem. 1996;271(46):29265-29270.
23. Zurawski SM, Vega F Jr., Huyghe B, et al. Receptors for interleukin-13 and interleukin-4 are complex and share a novel component that functions in signal transduction. EMBO J. 1993;12(7):2663-2670.
24. DebinskiW, Gibo DM, Obiri NI, et al. Novel anti-brain tumor cytotoxins specific for cancer cells. Nat Biotechnol. 1998;16(5):449-453.
25. Debinski W, Thompson JP. Retargeting interleukin 13 for radioimmunodetection and radioimmunotherapy of human highgrade gliomas. Clin Cancer Res. 1999;5(10 Suppl):3143s-3147s.
26. Kahlon KS, Brown C, Cooper LJ, et al. Specific recognition and killing of glioblastoma multiforme by interleukin 13-zetakine redirected cytolytic T cells. Cancer Res. 2004;64(24):9160-9166.
27. Madhankumar AB, Mintz A, Debinski W. Interleukin 13 mutants of enhanced avidity toward the glioma-associated receptor, IL13Ralpha2. Neoplasia. 2004;6(1):15-22.
28. Kong S, Sengupta S, Tyler B, et al. Suppression of human glioma xenografts with second-generation IL13R-specific chimeric antigen receptor-modified T cells. Clin Cancer Res. 2012;18(21):5949-5960.
29. Brown CE, Warden CD, Starr R, et al. Glioma IL13Ralpha2 is associated with mesenchymal signature gene expression and poor patient prognosis. PLoS One. 2013;8(10):e77769.
30. Liu H, Jacobs BS, Liu J, et al. Interleukin-13 sensitivity and receptor phenotypes of human glial cell lines: non-neoplastic glia and low-grade astrocytoma differ from malignant glioma. Cancer Immunol Immunother. 2000;49(6):319-324.
31. Rahaman SO, Vogelbaum MA, Haque SJ. Aberrant Stat3 signaling by interleukin-4 in malignant glioma cells: involvement of IL-13Ralpha2. Cancer Res. 2005;65(7):2956-2963.
32. Fujisawa T, Joshi B, Nakajima A, et al. A novel role of interleukin-13 receptor alpha2 in pancreatic cancer invasion and metastasis. Cancer Res. 2009;69(22):8678-8685.
33. Fujisawa T, Joshi BH, Puri RK. IL-13 regulates cancer invasion and metastasis through IL-13Ralpha2 via ERK/AP-1 pathway in mouse model of human ovarian cancer. Int J Cancer. 2012;131(2):344-356.
34. Fichtner-Feigl S, Terabe M, Kitani A, et al. Restoration of tumor immunosurveillance via targeting of interleukin-13 receptor-alpha 2. Cancer Res. 2008;68(9):3467-3475.
35. Mintz A, Gibo DM, Slagle-Webb B, et al. IL-13Ralpha2 is a gliomarestricted receptor for interleukin-13. Neoplasia. 2002;4(5):388-399.
36. Barth S. hIL-13-PE38QQR. NeoPharm. Curr Opin Investig Drugs. 2001;2(9):1309-1313.
37. Liu TF, Cai J, Gibo DM, et al. Reoxygenation of hypoxic glioblastoma multiforme cells potentiates the killing effect of an interleukin-13-based cytotoxin. Clin Cancer Res. 2009;15(1):160-168.
38. Stish BJ, Oh S, Vallera DA. Anti-glioblastoma effect of a recombinant bispecific cytotoxin cotargeting human IL-13 and EGF receptors in a mouse xenograft model. J Neurooncol. 2008;87(1):51-61.
39. Rustamzadeh E, Vallera DA, Todhunter DA, et al. Immunotoxin pharmacokinetics: a comparison of the anti-glioblastoma bispecific fusion protein (DTAT13) to DTAT and DTIL13. J Neurooncol. 2006;77(3):257-266.
40. Zhou G, Ye GJ, Debinski W, et al. Engineered herpes simplex virus 1 is dependent on IL13Ralpha 2 receptor for cell entry and independent of glycoprotein D receptor interaction. Proc Natl Acad Sci U S A. 2002;99(23):15124-15129.
41. Ulasov IV, Tyler MA, Han Y, et al. Novel recombinant adenoviral vector that targets the interleukin-13 receptor alpha2 chain permits effective gene transfer to malignant glioma. Hum Gene Ther. 2007;18(2):118-129.
42. Ou W, Marino MP, Suzuki A, et al. Specific targeting of human IL-13 receptor alpha2-positive cells with lentiviral vectors displaying IL-13 [published online ahead of print]. Hum Gene Ther Methods. 2012.
43. Allen C, Paraskevakou G, Iankov I, et al. Interleukin-13 displaying retargeted oncolytic measles virus strains have significant activity against gliomas with improved specificity. Mol Ther. 2008;16(9):1556-1564.
44. Kunwar S, Prados MD, Chang SM, et al. Direct intracerebral delivery of cintredekin besudotox (IL13-PE38QQR) in recurrent malignant glioma: a report by the Cintredekin Besudotox Intraparenchymal Study Group. J Clin Oncol. 2007;25(7):837-844.
45. Liu H, Prayson RA, Estes ML, et al. In vivo expression of the interleukin 4 receptor alpha by astrocytes in epilepsy cerebral cortex. Cytokine. 2000;12(11):1656-1661.
46. Candolfi M, Xiong W, Yagiz K, et al. Gene therapy-mediated delivery of targeted cytotoxins for glioma therapeutics. Proc Natl Acad Sci U S A. 2010;107(46):20021-20026.
47. Madhankumar AB, Slagle-Webb B, Mintz A, et al. Interleukin-13 receptor-targeted nanovesicles are a potential therapy for glioblastoma multiforme. Mol Cancer Ther. 2006;5(12):3162-3169.
48. Madhankumar AB, Slagle-Webb B, Wang X, et al. Efficacy of interleukin-13 receptor-targeted liposomal doxorubicin in the intracranial brain tumor model. Mol Cancer Ther. 2009;8(3):648-654.
49. Kioi M, Seetharam S, Puri RK. Targeting IL-13Ralpha2-positive cancer with a novel recombinant immunotoxin composed of a single-chain antibody and mutated Pseudomonas exotoxin. Mol Cancer Ther. 2008;7(6):1579-1587.
50. Balyasnikova IV, Wainwright DA, Solomaha E, et al. Characterization and immunotherapeutic implications for a novel antibody targeting interleukin (IL)-13 receptor alpha2. J Biol Chem. 2012;287(36):30215-30227.
51. Pandya H, Gibo DM, Garg S, et al. An interleukin 13 receptor alpha 2-specific peptide homes to human Glioblastoma multiforme xenografts. Neuro Oncol. 2012;14(1):6-18.
52. Rozhkova EA, Ulasov I, Lai B, et al. A high-performance nanobio photocatalyst for targeted brain cancer therapy. Nano Lett. 2009;9(9):3337-3342.
53. Kim DH, Rozhkova EA, Ulasov IV, et al. Biofunctionalized magneticvortex microdiscs for targeted cancer-cell destruction. Nat Mater. 2010;9(2):165-171.
54. Fadul CE, Fisher JL, Hampton TH, et al. Immune response in patients with newly diagnosed glioblastoma multiforme treated with intranodal autologous tumor lysate-dendritic cell vaccination after radiation chemotherapy. J Immunother. 2011;34(4):382-389.
55. Shimato S, Natsume A, Wakabayashi T, et al. Identification of a human leukocyte antigen-A24-restricted T-cell epitope derived from interleukin-13 receptor alpha2 chain, a glioma-associated antigen. J Neurosurg. 2008;109(1):117-122.
56. ∗02 allele. Cytotherapy. 2012;14(6):733-742.
57. Saikali S, Avril T, Collet B, et al. Expression of nine tumour antigens in a series of human glioblastoma multiforme: interest of EGFRvIII, IL-13Ralpha2, gp100 and TRP-2 for immunotherapy. J Neurooncol. 2007;81(2):139-148.
58. Okada H, Kalinski P, Ueda R, et al. Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J Clin Oncol. 2011;29(3):330-336.
59. A Study of ICT-107 Immunotherapy in Glioblastoma Multiforme (GBM). Available at: http://clinicaltrials.gov/show/NCT01280552. Accessed January 23, 2014.
60. Okada H, Butterfield L, Hamilton R, et al. Robust inductions of type-1 CD8+ T-cell responses in WHO grade II low-grade glioma patients receiving peptide-based vaccines in combination with poly-ICLC [abstract]. Neuro Oncol. 2013;15:iii71.
61. Emtage PC, Lo AS, Gomes EM, et al. Second-generation anticarcinoembryonic antigen designer T cells resist activation-induced cell death, proliferate on tumor contact, secrete cytokines, and exhibit superior antitumor activity in vivo: a preclinical evaluation. Clin Cancer Res. 2008;14(24):8112-8122.
62. Brown CE, Starr R, Aguilar B, et al. Stem-like tumor-initiating cells isolated from IL13Ralpha2 expressing gliomas are targeted and killed by IL13-zetakine-redirected T cells. Clin Cancer Res. 2012;18(8):2199-2209.
63. Chang L, Chang WC, McNamara G, et al. Transgene-enforced costimulation of CD4+ T cells leads to enhanced and sustained anti-tumor effector functioning. Cytotherapy. 2007;9(8):771-784.
64. Kunwar S. Convection enhanced delivery of IL13-PE38QQR for treatment of recurrent malignant glioma: presentation of interim findings from ongoing phase 1 studies. Acta Neurochir Suppl. 2003;88:105-111.
65. Kunwar S, Chang SM, Prados MD, et al. Safety of intraparenchymal convection-enhanced delivery of cintredekin besudotox in early-phase studies. Neurosurg Focus. 2006;20(4):E15.
66. Vogelbaum MA, Sampson JH, Kunwar S, et al. Convection-enhanced delivery of cintredekin besudotox (interleukin-13-PE38QQR) followed by radiation therapy with and without temozolomide in newly diagnosed malignant gliomas: phase 1 study of final safety results. Neurosurgery. 2007;61(5):1031-1037; discussion 1037-1038.
67. Kunwar S, Chang S, Westphal M, et al. Phase III randomized trial of CED of IL13-PE38QQR vs Gliadel wafers for recurrent glioblastoma. Neuro Oncol. 2010;12(8):871-881.
68. Jarboe JS, Johnson KR, Choi Y, et al. Expression of interleukin-13 receptor alpha2 in glioblastoma multiforme: implications for targeted therapies. Cancer Res. 2007;67(17):7983-7986.
69. Bozinov O, Kalk JM, Krayenbuhl N, et al. Decreasing expression of the interleukin-13 receptor IL-13Ralpha2 in treated recurrent malignant gliomas. Neurol Med Chir (Tokyo). 2010;50(8):617-621.
70. 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(1):98-110.
71. Engler JR, Robinson AE, Smirnov I, et al. Increased microglia/macrophage gene expression in a subset of adult and pediatric astrocytomas. PLoS One. 2012;7(8):e43339.
72. Vandergrift WA, Patel SJ, Nicholas JS, et al. Convection-enhanced delivery of immunotoxins and radioisotopes for treatment of malignant gliomas. Neurosurg Focus. 2006;20(4):E13.
73. Mueller S, Polley MY, Lee B, et al. Effect of imaging and catheter characteristics on clinical outcome for patients in the PRECISE study. J Neurooncol. 2011;101(2):267-277.
74. Sampson JH, Archer G, Pedain C, et al. Poor drug distribution as a possible explanation for the results of the PRECISE trial. J Neurosurg. 2010;113(2):301-309.
75. 18F-FHBG PET in a patient with glioma. Nat Clin Pract Oncol. 2009;6(1):53-58.
76. Berger C, Jensen MC, Lansdorp PM, et al. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest. 2008;118(1):294-305.
77. Wang X, Berger C, Wong CW, et al. Engraftment of human central memory-derived effector CD8+ T cells in immunodeficient mice. Blood. 2011;117(6):1888-1898.
78. Kawakami M, Kawakami K, Takahashi S, et al. Analysis of interleukin-13 receptor alpha2 expression in human pediatric brain tumors. Cancer. 2004;101(5):1036-1042.
79. Debinski W, Gibo DM, Slagle B, et al. Receptor for interleukin 13 is abundantly and specifically over-expressed in patients with glioblastoma multiforme. Int J Oncol. 1999;15(3):481-486.
80. Joshi BH, Plautz GE, Puri RK. Interleukin-13 receptor alpha chain: a novel tumor-associated transmembrane protein in primary explants of human malignant gliomas. Cancer Res. 2000;60(5):1168-1172.
81. Nguyen V, Conyers JM, Zhu D, et al. IL-13Ralpha2-targeted therapy escapees: biologic and therapeutic implications. Transl Oncol. 2011;4(6):390-400.
82. Buonerba C, Di Lorenzo G, Marinelli A, et al. A comprehensive outlook on intracerebral therapy of malignant gliomas. Crit Rev Oncol Hematol. 2011;80(1):54-68.
83. Nash KT, Thompson JP, DebinskiW. Molecular targeting of malignant gliomas with novel multiply-mutated interleukin 13-based cytotoxins. Crit Rev Oncol Hematol. 2001;39(1-2):87-98.
84. Kioi M, Kawakami K, Puri RK. Analysis of antitumor activity of an interleukin-13 (IL-13) receptor-targeted cytotoxin composed of IL-13 antagonist and Pseudomonas exotoxin. Clin Cancer Res. 2004;10(18 Pt 1):6231-6238.
85. Li YM, Vallera DA, Hall WA. Diphtheria toxin-based targeted toxin therapy for brain tumors. J Neurooncol. 2013;114(2):155-164.
86. Rustamzadeh E, HallWA, Todhunter DA, et al. Intracranial therapy of glioblastoma with the fusion protein DTIL13 in immunodeficient mice. Int J Cancer. 2006;118(10):2594-2601.
87. Ou W, Marino MP, Suzuki A, et al. Specific targeting of human interleukin (IL)-13 receptor alpha2-positive cells with lentiviral vectors displaying IL-13. Hum Gene Ther Methods. 2012;23(2):137-147.