Interleukin-13 Receptor Alpha 2-Targeted Glioblastoma Immunotherapy

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Sengupta, Sadhak ^a,b   Thaci, Bart ^b   Crawford, Andrew C ^c   Sampath, Prakash ^a,b  

^a ROGER WILLIAMS MEDICAL CENTER   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CHIMERIC ANTIGEN RECEPTOR; CORTICOSTEROID; DENDRITIC CELL VACCINE; DEXAMETHASONE; IMMUNOMODULATING AGENT; INTERLEUKIN 13 ANTIBODY; INTERLEUKIN 13 RECEPTOR ALPHA2; INTERLEUKIN 13 ZETAKINE; MOLECULAR THERAPY AGENT; MONOCLONAL ANTIBODY; SYNTHETIC PEPTIDE; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIGEN EXPRESSION; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL THERAPY; CLINICAL TRIAL (TOPIC); DENDRITIC CELL; GENETIC MANIPULATION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; IMMUNE EVASION; IMMUNE RESPONSE; MOLECULARLY TARGETED THERAPY; NONHUMAN; PHAGE DISPLAY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROGRESSION FREE SURVIVAL; REVIEW; T LYMPHOCYTE; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN NEOPLASMS; EVIDENCE BASED MEDICINE; IMMUNOLOGY; IMMUNOTHERAPY; PROCEDURES; TREATMENT OUTCOME;

ANIMALS; ANTIBODIES, MONOCLONAL; BRAIN NEOPLASMS; EVIDENCE-BASED MEDICINE; GLIOBLASTOMA; HUMANS; IMMUNOTHERAPY; INTERLEUKIN-13 RECEPTOR ALPHA2 SUBUNIT; MOLECULAR TARGETED THERAPY; TREATMENT OUTCOME;

EID: 84930904260     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/952128     Document Type: Review

References (79)

1. C. E. Rolle, S. Sengupta, and M. S. Lesniak, "Challenges in clinical design of immunotherapy trials for malignant glioma, " Neurosurgery Clinics ofNorth America, vol. 21, no. 1, pp. 201-214, 2010.
2. L. S. Ashby and T. C. Ryken, "Management of malignant glioma: steady progress with multimodal approaches, " Neurosurgical focus, vol. 20, no. 4, p. E3, 2006.
3. R. Stupp, M. E. Hegi, W. P. Mason et al., "Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a rand omised phase III study: 5-year analysis of the EORTC-NCIC trial, " The Lancet Oncology, vol. 10, no. 5, pp. 459-466, 2009.
4. A. Omuro and L. M. DeAngelis, "Glioblastoma and other malignant gliomas: a clinical review, " JAMA, vol. 310, no. 17, pp. 1842-1850, 2013.
5. C. E. Rolle, S. Sengupta, and M. S. Lesniak, "Mechanisms of immune evasion by gliomas, " Advances in Experimental Medicine and Biology, vol. 746, pp. 53-76, 2012.
6. S. Bao, Q. Wu, R. E. McLendon et al., "Glioma stem cells promote radioresistance by preferential activation of the DNA damage response, " Nature, vol. 444, no. 7120, pp. 756-760, 2006.
7. G. Frosina, "DNA repair and resistance of gliomas to chemotherapy and radiotherapy, " Molecular Cancer Research, vol. 7, no. 7, pp. 989-999, 2009.
8. A. F. Carpentier and Y. Meng, "Recent advances in immunotherapy for human glioma, " Current Opinion in Oncology, vol. 18, no. 6, pp. 631-636, 2006.
9. D. A. Wainwright, P. Nigam, B. Thaci, M. Dey, and M. S. Lesniak, "Recent developments on immunotherapy for brain cancer, " Expert Opinion on Emerging Drugs, vol. 17, no. 2, pp. 181-202, 2012.
10. D. L. Porter, B. L. Levine, M. Kalos, A. Bagg, and C. H. June, "Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia, "The New England Journal of Medicine, vol. 365, no. 8, pp. 725-733, 2011.
11. B. Thaci, C. E. Brown, E. Binello, K. Werbaneth, P. Sampath, and S. Sengupta, "Significance of interleukin-13 receptor alpha 2-targeted glioblastoma therapy, " Neuro-Oncology, 2014.
12. K. Arima, K. Sato, G. Tanaka et al., "Characterization of the interaction between interleukin-13 and interleukin-13 receptors, " Journal of Biological Chemistry, vol. 280, no. 26, pp. 24915-24922, 2005.
13. C. E. Brown, C. D. Warden, R. Starr et al., "Glioma IL13Rα2 is associated with mesenchymal signature gene expression and poor patient prognosis, " PLoS ONE, vol. 8, no. 10, Article ID e77769, 2013.
14. W. Debinski, D. M. Gibo, S. W. Hulet, J. R. Connor, and G. Y. Gillespie, "Receptor for interleukin 13 is a marker and therapeutic target for human high-grade gliomas, " Clinical Cancer Research, vol. 5, no. 5, pp. 985-990, 1999.
15. W. Debinski, N. I. Obiri, S. K. Powers, I. Pastan, and R. K. Puri, "Human glioma cells overexpress receptors for interleukin 13 and are extremely sensitive to a novel chimeric protein composed of interleukin 13 and Pseudomonas exotoxin, " Clinical Cancer Research, vol. 1, no. 11, pp. 1253-1258, 1995.
16. A. B. Madhankumar, B. Slagle-Webb, A. Mintz, J. M. Sheehan, and J. R. Connor, "Interleukin-13 receptor-targeted nanovesicles are a potential therapy for glioblastoma multiforme, "Molecular Cancer Therapeutics, vol. 5, no. 12, pp. 3162-3169, 2006.
17. A. B. Madhankumar, B. Slagle-Webb, X. Wang et al., "Efficacy of interleukin-13 receptor-targeted liposomal doxorubicin in the intracranial brain tumor model, " Molecular Cancer Therapeutics, vol. 8, no. 3, pp. 648-654, 2009.
18. M. Candolfi, W. Xiong, K. Yagiz et al., "Gene therapy-mediated delivery of targeted cytotoxins for glioma therapeutics, " Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 46, pp. 20021-20026, 2010.
19. I. V. Ulasov, M. A. Tyler, Y. Han, J. N. Glasgow, and M. S. Lesniak, "Novel recombinant adenoviral vector that targets the interleukin-13 receptor α2 chain permits effective gene transfer to malignant glioma, " Human Gene Therapy, vol. 18, no. 2, pp. 118-129, 2007.
20. I. V. Balyasnikova, D. A. Wainwright, E. Solomaha et al., "Characterization and immunotherapeutic implications for a novel antibody targeting interleukin (IL)-13 Receptor α2, " The Journal of Biological Chemistry, vol. 287, no. 36, pp. 30215-30227, 2012.
21. H. Okada, P. Kalinski, R. Ueda et al., "Induction of CD8+ Tcell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with α-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma, " Journal of Clinical Oncology, vol. 29, no. 3, pp. 330-336, 2011.
22. K. S. Kahlon, C. Brown, L. J. N. Cooper, A. Raubitschek, S. J. Forman, and M. C. Jensen, "Specific recognition and killing of glioblastoma multiforme by interleukin 13-zetakine redirected cytolytic T cells, " Cancer Research, vol. 64, no. 24, pp. 9160-9166, 2004.
23. S. Kong, S. Sengupta, B. Tyler et al., "Suppression of human glioma xenografts with second-generation IL13R-specific chimeric antigen receptor-modified T cells, " Clinical Cancer Research, vol. 18, no. 21, pp. 5949-5960, 2012.
24. M. Kioi, S. Seetharam, and R. K. Puri, "Targeting IL-13RA2- positive cancer with a novel recombinant immunotoxin composed of a single-chain antibody and mutated Pseudomonas exotoxin, "Molecular CancerTherapeutics, vol. 7, no. 6, pp. 1579-1587, 2008.
25. C. E. Fadul, J. L. Fisher, T. H. Hampton et al., "Immune response in patients with newly diagnosed glioblastoma multiforme treated with intranodal autologous tumor lysatedendritic cell vaccination after radiation chemotherapy, " Journal of Immunotherapy, vol. 34, no. 4, pp. 382-389, 2011.
26. S. Shimato, A. Natsume, T. Wakabayashi et al., "Identification of a human leukocyte antigen-A24-restricted T-cell epitope derived from interleukin-13 receptor α2 chain, a gliomaassociated antigen: laboratory investigation, " Journal of Neurosurgery, vol. 109, no. 1, pp. 117-122, 2008.
27. K. Iwami, S. Shimato, M. Ohno et al., "Peptide-pulsed dendritic cell vaccination targeting interleukin-13 receptor alpha2 chain in recurrent malignant glioma patients with HLA-A?24/A?02 allele, " Cytotherapy, vol. 14, no. 6, pp. 733-742, 2012.
28. A Study of ICT-107 Immunotherapy in Glioblastoma Multiforme (GBM), 2012, http://clinicaltrials.gov/show/NCT01280552.
29. S. Saikali, T. Avril, B. Collet et al., "Expression of nine tumour antigens in a series of human glioblastoma multiforme: interest of EGFRvIII, IL-13Rα2, gp100 and TRP-2 for immunotherapy, " Journal of Neuro-Oncology, vol. 81, no. 2, pp. 139-148, 2007.
30. H. Okada, L. Butterfield, R. Hamilton 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, " Neuro-Oncology, vol. 15, p. iii71, 2013.
31. Q. Ma, R. M. Gonzalo-Daganzo, and R. P. Junghans, "Genetically engineered T cells as adoptive immunotherapy of cancer, " Cancer Chemotherapy and Biological Response Modifiers, vol. 20, pp. 315-341, 2002.
32. M. C. Jensen and S. R. Riddell, "Design and implementation of adoptive therapy with chimeric antigen receptor-modified T cells, " Immunological Reviews, vol. 257, no. 1, pp. 127-144, 2014.
33. S. Krebs, T. G. Rodriguez-Cruz, and C. Derenzo, "Genetically modified T cells to target glioblastoma, " Frontiers in Oncology, vol. 3, article 322, 2013.
34. R. H. Vonderheide and C. H. June, "Engineering T cells for cancer: our synthetic future, " Immunological Reviews, vol. 257, no. 1, pp. 7-13, 2014.
35. T. S. Park, S. A. Rosenberg, and R. A. Morgan, "Treating cancer with genetically engineered T cells, " Trends in Biotechnology, vol. 29, no. 11, pp. 550-557, 2011.
36. P. C. R. Emtage, A. S. Y. Lo, E. M. Gomes, D. L. Liu, R. M. Gonzalo-Daganzo, and R. P. Junghans, "Second-generation anti-carcinoembryonic 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, " Clinical Cancer Research, vol. 14, no. 24, pp. 8112-8122, 2008.
37. Cellular Adoptive Immunotherapy Using Genetically Modified T-Lymphocytes in Treating Patients With Recurrent or Refractory High-Grade Malignant Glioma, 2011, http://clinicaltrials.gov/ct2/show/NCT00730613.
38. Phase I Study of Cellular Immunotherapy for Recurrent/Refractory Malignant Glioma Using Intratumoral Infusions of GRm13Z40-2, An Allogeneic CD8+ Cytolitic T-Cell Line Genetically Modified to Express the IL 13-Zetakine and HyTK and to be Resistant to Glucocorticoids, in Combination With Interleukin-2, 2013, http://www.clinicaltrials.gov/ct2/show/NCT01082926.
39. M. Hegde, A. Corder, K. K. Chow et al., "Combinational targeting offsets antigen escape and enhances effector functions of adoptively transferred T cells in glioblastoma, " Molecular Therapy, vol. 21, no. 11, pp. 2087-2101, 2013.
40. S. Krebs, K. K. Chow, Z. Yi et al., "T cells redirected to interleukin-13Ralpha2 with interleukin-13 mutein-chimeric antigen receptors have anti-glioma activity but also recognize interleukin-13Ralpha1, " Cytotherapy, vol. 16, no. 8, pp. 1121-1131, 2014.
41. C. E. Brown, R. Starr, B. Aguilar et al., "Stem-like tumorinitiating cells isolated from IL13Rα2 expressing gliomas are targeted and killed by IL13-zetakine-redirected T cells, " Clinical Cancer Research, vol. 18, no. 8, pp. 2199-2209, 2012.
42. S. S. Yaghoubi, M. C. Jensen, N. Satyamurthy et al., "Noninvasive detection of therapeutic cytolytic T cells with 18 F-FHBG PET inapatientwithglioma, "Nature Clinical Practice Oncology, vol. 6, no. 1, pp. 53-58, 2009.
43. G. Z. Jian, J. Eguchi, C. A. Kruse et al., "Antigenic profiling of glioma cells to generate allogeneic vaccines or dendritic cellbased therapeutics, " Clinical Cancer Research, vol. 13, no. 2, part 1, pp. 566-575, 2007.
44. Y. Liang, M. Diehn, N. Watson et al., "Gene expression profiling reveals molecularly and clinically distinct subtypes of glioblastoma multiforme, " Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 16, pp. 5814-5819, 2005.
45. J. A. Cowan and B. G. Thompson, "Chapter 36. Neurosurgery, " in CURRENT Diagnosis & Treatment: Surgery, 13e, G. M. Doherty, Ed., The McGraw-Hill, New York, NY, USA, 2010.
46. Z. Fan, T. Sehm, M. Rauh et al., "Dexamethasone alleviates tumor-associated brain damage and angiogenesis, " PLoS ONE, vol. 9, no. 4, Article IDe93264, 2014.
47. L. Bavaresco, A. Bernardi, E. Braganhol, M. R. Wink, and A. M. O. Battastini, "Dexamethasone inhibits proliferation and stimulates ecto-5 ′-nucleotidase/CD73 activity in C6 rat glioma cell line, " Journal of Neuro-Oncology, vol. 84, no. 1, pp. 1-8, 2007.
48. S. C. Higgins and G. J. Pelkington, "The in vitro effects of tricyclic drugs and dexamethasone on cellular respiration of malignant glioma, " Anticancer Research, vol. 30, no. 2, pp. 391-397, 2010.
49. L. A. Nafe, J. R. Dodam, and C. R. Reinero, "In-vitro immunosuppression of canine T-lymphocyte-specific proliferation with dexamethasone, cyclosporine, and the active metabolites of azathioprine and leflunomide in a flow-cytometric assay, " Canadian Journal of Veterinary Research, vol. 78, no. 3, pp. 168-175, 2014.
50. M. Löwenberg, A. P. Verhaar, G. R. van den Brink, and D. W. Hommes, "Glucocorticoid signaling: a nongenomic mechanism for T-cell immunosuppression, " Trends in Molecular Medicine, vol. 13, no. 4, pp. 158-163, 2007.
51. J. Liao, X. Wang, Y. Bi et al., "Dexamethasone potentiates myeloid-derived suppressor cell function in prolonging allograft survival through nitric oxide, " Journal of Leukocyte Biology, 2014.
52. P. R. Kumaresan, P. R. Manuri, N. D. Albert et al., "Bioengineering T cells to target carbohydrate to treat opportunistic fungal infection, " Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 29, pp. 10660-10665, 2014.
53. M. D. Mazur, V. Nguyen, and D. W. Fults, "Glioblastoma presenting with steroid-induced pseudoregression of contrast enhancement on magnetic resonance imaging, " Case Reports in Neurological Medicine, vol. 2012, Article ID 816873, 6 pages, 2012.
54. FDA Approval for Temozolomide, http://www.cancer.gov/cancertopics/druginfo/fda-temozolomide.
55. S. Sengupta, J. Marrinan, C. Frishman, and P. Sampath, "Impact of temozolomide on immune response during malignant glioma chemotherapy, " Clinical and Developmental Immunology, vol. 2012, Article ID 831090, 7 pages, 2012.
56. C. S. Brock, E. S. Newland s, S. R. Wedge et al., "Phase I trial of temozolomide using an extended continuous oral schedule, " Cancer Research, vol. 58, no. 19, pp. 4363-4367, 1998.
57. A. B. Heimberger, W. Sun, S. F. Hussain et al., "Immunological responses in a patient with glioblastoma multiforme treated with sequential courses of temozolomide and immunotherapy: case study, " Neuro-Oncology, vol. 10, no. 1, pp. 98-103, 2008.
58. M. Gand er, S. Leyvraz, L. Decosterd et al., "Sequential administration of temozolomide and fotemustine: depletion of O6- alkyl guanine-DNA transferase in blood lymphocytes and in tumours, " Annals of Oncology, vol. 10, no. 7, pp. 831-838, 1999.
59. M. C. Kizilarslanoglu, S. Aksoy, N. O. Yildirim, E. Ararat, I. Sahin, and K. Altundag, "Temozolomide-related infections: review of the literature, " Journal of B. U. ON., vol. 16, no. 3, pp. 547-550, 2011.
60. M. Briegert, A. H. Enk, and B. Kaina, "Change in expression of MGMT during maturation of human monocytes into dendritic cells, " DNA Repair, vol. 6, no. 9, pp. 1255-1263, 2007.
61. M. Briegert and B. Kaina, "Humanmonocytes, but not dendritic cells derived fromthem, are defective in base excision repair and hypersensitive to methylating agents, " Cancer Research, vol. 67, no. 1, pp. 26-31, 2007.
62. N. Sawai, S. Zhou, E. F. Vanin, P. Houghton, T. P. Brent, and B. P. Sorrentino, "Protection and in vivo selection of hematopoietic stem cells using temozolomide, O6-benzylguanine, and an alkyltransferase-expressing retroviral vector, " Molecular Therapy, vol. 3, no. 1, pp. 78-87, 2001.
63. W. Debinski, D. M. Gibo, B. Slagle, S. K. Powers, and G. Y. Gillespie, "Receptor for interleukin 13 is abundantly and specifically over-expressed in patients with glioblastoma multiforme, " International Journal of Oncology, vol. 15, no. 3, pp. 481-486, 1999.
64. B. H. Joshi, G. E. Plautz, and R. K. Puri, "Interleukin-13 receptor chain: a novel tumor-associated transmembrane protein in primary explants of human malignant gliomas, " Cancer Research, vol. 60, no. 5, pp. 1168-1172, 2000.
65. M. Kawakami, K. Kawakami, S. Takahashi, M. Abe, and R. K. Puri, "Analysis of interleukin-13 receptor α2 expression in human pediatric brain tumors, " Cancer, vol. 101, no. 5, pp. 1036-1042, 2004.
66. H. Pandya, D. M. Gibo, S. Garg, S. Kridel, and W. Debinski, "An interleukin 13 receptor α2-specific peptide homes to human Glioblastoma multiforme xenografts, " Neuro-Oncology, vol. 14, no. 1, pp. 6-18, 2012.
67. C. J. Wheeler and K. L. Black, "DCVax-brain and DC vaccines in the treatment of GBM, "Expert Opinion on Investigational Drugs, vol. 18, no. 4, pp. 509-519, 2009.
68. S. S. Bullain, A. Sahin, O. Szentirmai et al., "Genetically engineered T cells to target EGFRvIII expressing glioblastoma, " Journal of Neuro-Oncology, vol. 94, no. 3, pp. 373-382, 2009.
69. B. D. Choi, C. M. Suryadevara, P. C. Gedeon et al., "Intracerebral delivery of a third generation EGFRvIII-specific chimeric antigen receptor is efficacious against human glioma, " Journal of Clinical Neuroscience, vol. 21, no. 1, pp. 189-190, 2014.
70. R. A. Morgan, L. A. Johnson, J. L. Davis et al., "Recognition of glioma stem cells by genetically modified T cells targeting EGFRvIII and development of adoptive cell therapy for glioma, " Human Gene Therapy, vol. 23, no. 10, pp. 1043-1053, 2012.
71. White Blood Cells With Anti-EGFR-III for Malignant Gliomas, 2014, http://www.clinicaltrials.gov/ct2/show/NCT01454596.
72. K. K. Chow, S. Naik, S. Kakarla et al., "T cells redirected to EphA2 for the immunotherapy of glioblastoma, " Molecular Therapy, vol. 21, no. 3, pp. 629-637, 2013.
73. N. Ahmed, V. S. Salsman, Y. Kew et al., "HER2-specific T cells target primary glioblastoma stemcells and induce regression of autologous experimental tumors, " Clinical Cancer Research, vol. 16, no. 2, pp. 474-485, 2010.
74. CMV-specific Cytotoxic T Lymphocytes Expressing CAR Targeting HER2 in Patients with GBM (HERT-GBM), 2014, http://www.clinicaltrials.gov/ct2/show/NCT01109095.
75. M. Kalos, B. L. Levine, D. L. Porter et al., "T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia, " Science Translational Medicine, vol. 3, no. 95, Article ID95ra73, 2011.
76. D. L. Porter, M. Kalos, Z. Zheng, B. Levine, and C. June, "Chimeric antigen receptor therapy for B-cell malignancies, " Journal of Cancer, vol. 2, no. 1, pp. 331-332, 2011.
77. S. A. Grupp, M. Kalos, D. Barrett et al., "Chimeric antigen receptor-modified T cells for acute lymphoid leukemia, " New England Journal of Medicine, vol. 368, no. 16, pp. 1509-1518, 2013.
78. J. Maher, "Immunotherapy of malignant disease using chimeric antigen receptor engrafted T cells, " ISRN Oncology, vol. 2012, Article ID 278093, 23 pages, 2012.
79. M. Sadelain, R. Brentjens, and I. Rivière, "The basic principles of chimeric antigen receptor design, " Cancer Discovery, vol. 3, no. 4, pp. 388-398, 2013.