Nimotuzumab as a radiosensitizing agent in the treatment of high grade glioma: Challenges and opportunities

OncoTargets and Therapy

Volumn 6, Issue , 2013, Pages 931-942

  Diaz Miqueli, Arlhee ^a   Martinez, Giselle Saurez ^a  

^a CENTER OF MOLECULAR IMMUNOLOGY   (Cuba)

Author keywords

High grade gliomas; Nimotuzumab; Radiation

Indexed keywords

CD133 ANTIGEN; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; NAVELBINE; NIMOTUZUMAB; PLACEBO; TEMOZOLOMIDE; VASCULOTROPIN;

ACNE; ADVANCED CANCER; ANOREXIA; ANTIANGIOGENIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APHASIA; BLOOD TOXICITY; CANCER COMBINATION CHEMOTHERAPY; CANCER GRADING; CANCER RADIOTHERAPY; CANCER STEM CELL; CANCER SURGERY; CANCER SURVIVAL; CELL CYCLE REGULATION; CHEMORADIOTHERAPY; CHEMOTHERAPY INDUCED EMESIS; CHILL; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG FEVER; DRUG INDUCED HEADACHE; DRUG MECHANISM; ESOPHAGUS CARCINOMA; FATIGUE; FEVER; GASTROINTESTINAL CARCINOMA; GLIOBLASTOMA; GLIOMA; HEAD AND NECK CANCER; HUMAN; HYPERTRANSAMINASEMIA; LUNG NON SMALL CELL CANCER; MUCOSA INFLAMMATION; MULTIPLE CYCLE TREATMENT; NAUSEA; NONHUMAN; OLIGODENDROGLIOMA; OVERALL SURVIVAL; PONTINE GLIOMA; PROTEIN EXPRESSION; PROTEIN TARGETING; RADIATION SICKNESS; RADIOSENSITIZATION; REVIEW; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; SURVIVAL TIME; THROMBOCYTOPENIA; TREMOR;

EID: 84880849129     PISSN: 11786930     EISSN: None     Source Type: Journal    
DOI: 10.2147/OTT.S33532     Document Type: Review

References (86)

1. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007;114:97-109.
2. Laperriere N, Zuraw L, Cairncross G. Radiotherapy for newly diagnosed malignant glioma in adults: a systematic review. Radiother Oncol. 2002;64:259-273.
3. Hart MG, Grant R, Garside R, Rogers G, Somerville M, Stein K. Temozolomide for high grade glioma [review]. Cochrane Database Syst Rev. 2008:CD007415.
4. Koshy M, Villano JL, Dolecek TA, et al. Improved survival time trends for glioblastoma using the SEER 17 population-based registries. J Neurooncol. 2012;107:207-212.
5. Nazzaro JM, Neuwelt EA. The role of surgery in the management of supratentorial intermediate and high-grade astrocytomas in adults. J Neurosurg. 1990;73:331-344.
6. Lorenzoni J, Torrico A, Villanueva P, Gederlini A, Torrealba G. Surgery for high-grade gliomas in a developing country: survival estimation using a simple stratification system. Surg Neurol. 2008;70:591-597; discussion 7.
7. Wolff JE, Driever PH, Erdlenbruch B, et al. Intensive chemotherapy improves survival in pediatric high-grade glioma after gross total resection: results of the HIT-GBM-C protocol. Cancer. 2010;116:705-712.
8. Oszvald A, Guresir E, Setzer M, et al. Glioblastoma therapy in the elderly and the importance of the extent of resection regardless of age. J Neurosurg. 2012;116:357-364.
9. Wild-Bode C, Weller M, Rimner A, Dichgans J, Wick W. Sublethal irradiation promotes migration and invasiveness of glioma cells: implications for radiotherapy of human glioblastoma. Cancer Res. 2001;61:2744-2750.
10. Garden AS, Maor MH, Yung WK, et al. Outcome and patterns of failure following limited-volume irradiation for malignant astrocytomas. Radiother Oncol. 1991;20:99-110.
11. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756-760.
12. Ciardiello F, Tortora G. EGFR antagonists in cancer treatment. N Engl J Med. 2008;358:1160-1174.
13. Hennequin C, Quero L, Favaudon V. Determinants and predictive factors of tumour radiosensitivity. Cancer Radiother. 2008;12:3-13.
14. Stupp R, Mason WP, van den Bent MJ, et al; European Organization for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups, National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987-996.
15. Weller M, Stupp R, Reifenberger G, et al. MGMT promoter methylation in malignant gliomas: ready for personalized medicine? Nat Rev Neurol. 2010;6:39-51.
16. Yabroff KR, Harlan L, Zeruto C, Abrams J, Mann B. Patterns of care and survival for patients with glioblastoma multiforme diagnosed during 2006. Neuro Oncol. 2012;14:351-359.
17. Zawlik I, Vaccarella S, Kita D, Mittelbronn M, Franceschi S, Ohgaki H. Promoter methylation and polymorphisms of the MGMT gene in glioblastomas: a population-based study. Neuroepidemiology. 2009;32:21-29.
18. Stupp R, Mayer M, Kann R, et al. Neoadjuvant chemotherapy and radiotherapy followed by surgery in selected patients with stage IIIB non-small-cell lung cancer: a multicentre phase II trial. Lancet Oncol. 2009;10:785-793.
19. Sartor CI. Mechanisms of disease: Radiosensitization by epidermal growth factor receptor inhibitors. Nat Clin Pract Oncol. 2004;1:80-87.
20. Viana-Pereira M, Lopes JM, Little S, et al. Analysis of EGFR overexpression, EGFR gene amplification and the EGFRvIII mutation in Portuguese high-grade gliomas. Anticancer Res. 2008;28:913-920.
21. Jarvela S, Helin H, Haapasalo J, et al. Amplification of the epidermal growth factor receptor in astrocytic tumours by chromogenic in situ hybridization: association with clinicopathological features and patient survival. Neuropathol Appl Neurobiol. 2006;32:441-450.
22. Bredel M, Pollack IF, Hamilton RL, James CD. Epidermal growth factor receptor expression and gene amplification in high-grade non-brainstem gliomas of childhood. Clin Cancer Res. 1999;5:1786-1792.
23. Mellinghoff IK, Wang MY, Vivanco I, et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med. 2005;353:2012-2024.
24. Fedrigo CA, Grivicich I, Schunemann DP, et al. Radioresistance of human glioma spheroids and expression of HSP70, p53 and EGFr. Radiat Oncol. 2011;6:156.
25. Gilbertson RJ, Hill DA, Hernan R, et al. ERBB1 is amplified and overexpressed in high-grade diffusely infiltrative pediatric brain stem glioma. Clin Cancer Res. 2003;9:3620-3624.
26. Yarden Y, Pines G. The ERBB network: at last, cancer therapy meets systems biology. Nat Rev Cancer. 2012;12:553-563.
27. Mateo C, Moreno E, Amour K, Lombardero J. Humanization of a mouse monoclonal antibody that blocks the epidermal growth factor receptor: recovery of antagonistic activity. Immunotechnology. 1997;3:71-81.
28. Diaz Miqueli A, Blanco R, Garcia B, et al. Biological activity in vitro of anti-epidermal growth factor receptor monoclonal antibodies with different affinities. Hybridoma (Larchmt). 2007;26:423-431.
29. Spicer J, Harper P. Targeted therapies for non-small cell lung cancer. Int J Clin Pract. 2005;59:1055-1062.
30. Crombet-Ramos T, Rak J, Perez R, Viloria-Petit A. Antiproliferative, antiangiogenic and proapoptotic activity of h-R3: A humanized anti-EGFR antibody. Int J Cancer. 2002;101:567-575.
31. Viloria-Petit A, Crombet T, Jothy S, et al. Acquired resistance to the antitumor effect of epidermal growth factor receptor-blocking antibodies in vivo: a role for altered tumor angiogenesis. Cancer Res. 2001;61:5090-5101.
32. Crombet T, Osorio M, Cruz T, et al. Use of the humanized anti-epidermal growth factor receptor monoclonal antibody h-R3 in combination with radiotherapy in the treatment of locally advanced head and neck cancer patients. J Clin Oncol. 2004;22:1646-1654.
33. Rodriguez MO, Rivero TC, del Castillo Bahi R, et al. Nimotuzumab plus radiotherapy for unresectable squamous-cell carcinoma of the head and neck. Cancer Biol Ther. 2010;9:343-349.
34. Ramos TC, Figueredo J, Catala M, et al. Treatment of high-grade glioma patients with the humanized anti-epidermal growth factor receptor (EGFR) antibody h-R3: report from a phase I/II trial. Cancer Biol Ther. 2006;5:375-379.
35. Massimino M, Bode U, Biassoni V, Fleischhack G. Nimotuzumab for pediatric diffuse intrinsic pontine gliomas. Expert Opin Biol Ther. 2011;11:247-256.
36. Ramos-Suzarte M, Lorenzo-Luaces P, Lazo NG, et al. Treatment of malignant, non-resectable, epithelial origin esophageal tumours with the humanized anti-epidermal growth factor antibody nimotuzumab combined with radiation therapy and chemotherapy. Cancer Biol Ther. 2012;13:600-605.
37. Diaz Miqueli A, Rolff J, Lemm M, Fichtner I, Perez R, Montero E. Radiosensitisation of U87MG brain tumours by anti-epidermal growth factor receptor monoclonal antibodies. Br J Cancer. 2009;100:950-958.
38. Cancer Therapy Evaluation Program. Common Terminology Criteria for Adverse Events v3.0 (CTCAE). Available from: http://ctep.cancer.gov/protocolDevelopment/electronic_applications/docs/ctcaev3.pdf. Accessed July 5, 2013.
39. Solomon MT, Selva JC, Figueredo J, et al. Radiotherapy plus the anti-EGFR mAb nimotuzumab or placebo for the treatment of high-grade glioma patients. ASCO Annual Meeting; June 1-5, 2012; Chicago, IL, USA. J Clin Oncol. 30(Suppl):Abstr 2515.
40. Hong J, Peng Y, Liao Y, et al. Nimotuzumab prolongs survival in patients with malignant gliomas: A phase I/II clinical study of concomitant radiochemotherapy with or without nimotuzumab. Exp Ther Med. 2012;4:151-157.
41. Westphal M, Bach F. Final results of a randomized phase III trial of nimotuzumab for the treatment of newly diagnosed glioblastoma in addition to standard radiation and chemotherapy with temozolomide versus standard radiation and temoziolamide. ASCO Annual Meeting; June 1-5, 2012; Chicago, IL, USA. J Clin Oncol. 30(Suppl):Abstr 2033.
42. Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352:997-1003.
43. Fleischhack G, Siegler S, Warmuth-Metz M, et al. Final results of a phase III study consisting of nimotuzumab and concomitant standard radiotherapy for the treatment of newly diagnosed diffuse intrinsic pontine gliomas. Pediatr Blood Cancer. 2009;Suppl:755.
44. Crombet T, Cabanas R, Alert J, et al. Nimotuzumab and radiotherapy in children and adolescents with brain stem glioma: preliminary results from a phase II study. Eur J Cancer. 2009;7(2):497.
45. Akashi Y, Okamoto I, Iwasa T, et al. Enhancement of the antitumor activity of ionising radiation by nimotuzumab, a humanised monoclonal antibody to the epidermal growth factor receptor, in non-small cell lung cancer cell lines of differing epidermal growth factor receptor status. Br J Cancer. 2008;98:749-755.
46. Gonzalez JE, Barquinero JF, Lee M, Garcia O, Casaco A. Radiosensitization induced by the anti-epidermal growth factor receptor monoclonal antibodies cetuximab and nimotuzumab in A431 cells. Cancer Biol Ther. 2012;13:71-76.
47. Perez R, Moreno E, Garrido G, Crombet T. EGFR-Targeting as a Biological Therapy: Understanding Nimotuzumab's Clinical Effects. Cancers. 2011;3:2014-2031.
48. Schmidt-Ullrich RK, Contessa JN, Lammering G, Amorino G, Lin PS. ERBB receptor tyrosine kinases and cellular radiation responses. Oncogene. 2003;22:5855-5865.
49. Huang SM, Bock JM, Harari PM. Epidermal growth factor receptor blockade with C225 modulates proliferation, apoptosis, and radiosensitivity in squamous cell carcinomas of the head and neck. Cancer Res. 1999;59:1935-1940.
50. Dent P, Reardon DB, Park JS, et al. Radiation-induced release of transforming growth factor alpha activates the epidermal growth factor receptor and mitogen-activated protein kinase pathway in carcinoma cells, leading to increased proliferation and protection from radiation-induced cell death. Mol Biol Cell. 1999;10:2493-2506.
51. Clarke MF, Dick JE, Dirks PB, et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66:9339-9344.
52. Hemmati HD, Nakano I, Lazareff JA, et al. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A. 2003;100:15178-15183.
53. Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821-5828.
54. Singh SK, Clarke ID, Hide T, Dirks PB. Cancer stem cells in nervous system tumors. Oncogene. 2004;23:7267-7273.
55. Bao S, Wu Q, Sathornsumetee S, et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 2006;66:7843-7848.
56. Eramo A, Ricci-Vitiani L, Zeuner A, et al. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ. 2006;13:1238-1241.
57. 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.
58. Mazzoleni S, Politi LS, Pala M, et al. Epidermal growth factor receptor expression identifies functionally and molecularly distinct tumor-initiating cells in human glioblastoma multiforme and is required for gliomagenesis. Cancer Res. 2012;70:7500-7513.
59. Ayuso-Sacido A, Moliterno JA, Kratovac S, et al. Activated EGFR signaling increases proliferation, survival, and migration and blocks neuronal differentiation in post-natal neural stem cells. J Neurooncol. 2010;97:323-337.
60. Sato A, Sunayama J, Matsuda K, et al. Regulation of neural stem/progenitor cell maintenance by PI3K and mTOR. Neurosci Lett. 2010;470:115-120.
61. Calabrese C, Poppleton H, Kocak M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11:69-82.
62. Shintani S, Li C, Mihara M, et al. Enhancement of tumor radioresponse by combined treatment with gefitinib (Iressa, ZD1839), an epidermal growth factor receptor tyrosine kinase inhibitor, is accompanied by inhibition of DNA damage repair and cell growth in oral cancer. Int J Cancer. 2003;107:1030-1037.
63. Iliakis G, Wang Y, Guan J, Wang H. DNA damage checkpoint control in cells exposed to ionizing radiation. Oncogene. 2003;22:5834-5847.
64. Harari PM, Huang SM. Head and neck cancer as a clinical model for molecular targeting of therapy: combining EGFR blockade with radiation. Int J Radiat Oncol Biol Phys. 2001;49:427-433.
65. Nyati MK, Maheshwari D, Hanasoge S, et al. Radiosensitization by pan ErbB inhibitor CI-1033 in vitro and in vivo. Clin Cancer Res. 2004;10:691-700.
66. Herbst RS, Johnson DH, Mininberg E, et al. Phase I/II trial evaluating the anti-vascular endothelial growth factor monoclonal antibody bevacizumab in combination with the HER-1/epidermal growth factor receptor tyrosine kinase inhibitor erlotinib for patients with recurrent non-small-cell lung cancer. J Clin Oncol. 2005;23:2544-2555.
67. Tabernero J. The role of VEGF and EGFR inhibition: implications for combining anti-VEGF and anti-EGFR agents. Mol Cancer Res. 2007;5:203-220.
68. Niu G, Wright KL, Huang M, et al. Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene. 2002;21:2000-2008.
69. Milas L, Mason K, Hunter N, et al. In vivo enhancement of tumor radioresponse by C225 antiepidermal growth factor receptor antibody. Clin Cancer Res. 2000;6:701-708.
70. Schmidt-Ullrich RK, Mikkelsen RB, Dent P, et al. Radiation-induced proliferation of the human A431 squamous carcinoma cells is dependent on EGFR tyrosine phosphorylation. Oncogene. 1997;15:1191-1197.
71. Schmidt-Ullrich RK, Valerie K, Fogleman PB, Walters J. Radiation-induced autophosphorylation of epidermal growth factor receptor in human malignant mammary and squamous epithelial cells. Radiat Res. 1996;145:81-85.
72. Ramakrishnan MS, Eswaraiah A, Crombet T, et al. Nimotuzumab, a promising therapeutic monoclonal for treatment of tumors of epithelial origin. MAbs. 2009;1:41-48.
73. Bebb G, Smith C, Rorke S, et al. Phase I clinical trial of the anti-EGFR monoclonal antibody nimotuzumab with concurrent external thoracic radiotherapy in Canadian patients diagnosed with stage IIb, III or IV non-small cell lung cancer unsuitable for radical therapy. Cancer Chemother Pharmacol. 2011;67:837-845.
74. Choi HJ, Sohn JH, Lee CG, et al. A phase I study of nimotuzumab in combination with radiotherapy in stages IIB-IV non-small cell lung cancer unsuitable for radical therapy: Korean results. Lung Cancer. 2011;71:55-59.
75. Ling Y, Chen J, Tao M, Chu X, Zhang X. A pilot study of nimotuzumab combined with cisplatin and 5-FU in patients with advanced esophageal squamous cell carcinoma. J Thorac Dis. 2012;4:58-62.
76. Kim YH, Sasaki Y, Lee KH, et al. Randomized phase II study of nimotuzumab, an anti-EGFR antibody, plus irinotecan in patients with 5-fluorouracil-based regimen-refractory advanced or recurrent gastric cancer in Korea and Japan: Preliminary results. 2011 Gastrointestinal Cancers Symposium; January 20-22, 2011; San Francisco, CA, USA. J Clin Oncol. 2011;29(Suppl 4):Abstr 87.
77. Zhao KL, Hu XC, Wu XH, Fu XL, Fan M, Jiang GL. A phase I dose escalation study of Nimotuzumab in combination with concurrent chemoradiation for patients with locally advanced squamous cell carcinoma of esophagus. Invest New Drugs. 2012;30:1585-1590.
78. Bebb G, Boland W, Melosky B. Don't jump to rash conclusions. Cancer Biol Ther. 2011;11:639-641.
79. Cabanas R, Saurez G, Rios M, et al. Treatment of children with high grade glioma with nimotuzumab: A 5-y institutional experience. MAbs. 2013;5(2):202-207.
80. Fortin D. The blood-brain barrier: its influence in the treatment of brain tumors metastases. Curr Cancer Drug Targets. 2012;12:247-259.
81. Rojo F, Gracias E, Villena N, et al. Pharmacodynamic trial of nimotuzumab in unresectable squamous cell carcinoma of the head and neck: a SENDO Foundation study. Clin Cancer Res. 2010;16:2474-2482.
82. Garrido G, Tikhomirov IA, Rabasa A, et al. Bivalent binding by intermediate affinity of nimotuzumab: a contribution to explain antibody clinical profile. Cancer Biol Ther. 2011;11:373-382.
83. Zarghooni M, Bartels U, Lee E, et al. Whole-genome profiling of pediatric diffuse intrinsic pontine gliomas highlights platelet-derived growth factor receptor alpha and poly (ADP-ribose) polymerase as potential therapeutic targets. J Clin Oncol. 2010;28:1337-1344.
84. Verhaak RG, Hoadley KA, Purdom E, et al; Cancer Genome Atlas Research Network. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17:98-110.
85. Basavaraj C, Sierra P, Shivu J, Melarkode R, Montero E, Nair P. Nimotuzumab with chemoradiation confers survival advantage in treatment naive head and neck tumors overexpressing EGFR. Cancer Biol Ther. 2010;10(7):673-681.
86. Bode U, Massimino M, Bach F, et al. Nimotuzumab treatment of malignant gliomas. Expert Opin Biol Ther. 2012;12(12):1649-1659.