Combined treatment of Nimotuzumab and rapamycin is effective against temozolomide-resistant human gliomas regardless of the EGFR mutation status

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Chong, Dawn Q ^a   Toh, Xin Y ^a   Ho, Ivy A W ^a   Sia, Kian C ^a   Newman, Jennifer P ^a   Yulyana, Yulyana ^a   Ng, Wai Hoe ^b   Lai, Siang H ^c   Ho, Mac M F ^a   Dinesh, Nivedh ^f   Tham, Chee K ^a   Lam, Paula Y P ^a,d,e  

^a DIVISION OF MEDICAL ONCOLOGY   (Singapore)

^b NATIONAL NEUROSCIENCE INSTITUTE   (Singapore)

^c SINGAPORE GENERAL HOSPITAL   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e DUKE NUS MEDICAL SCHOOL   (Singapore)

^f NATIONAL UNIVERSITY HOSPITAL   (Singapore)

Author keywords

EGFR; EGFRvIII; GBM; Nimotuzumab; Rapamycin

Indexed keywords

ANTINEOPLASTIC AGENT; DACARBAZINE; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; MONOCLONAL ANTIBODY; NIMOTUZUMAB; RAPAMYCIN; TEMOZOLOMIDE;

ANALOGS AND DERIVATIVES; APOPTOSIS; BRAIN NEOPLASMS; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; GLIOBLASTOMA; HUMAN; MUTATION; PATHOLOGY; TUMOR CELL LINE;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DACARBAZINE; DRUG RESISTANCE, NEOPLASM; GLIOBLASTOMA; HUMANS; MUTATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIROLIMUS;

EID: 84928530835     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1191-3     Document Type: Article

References (46)

1. Smith JS, Tachibana I, Passe SM, Huntley BK, Borell TJ, Iturria N, et al. PTEN mutation, EGFR amplification, and outcome in patients with anaplastic astrocytoma and glioblastoma multiforme. J Natl Cancer Inst. 2001;93(16):1246-56.
2. Heimberger AB, Suki D, Yang D, Shi W, Aldape K. The natural history of EGFR and EGFRvIII in glioblastoma patients. J Transl Med. 2005;3:38.
3. Heimberger AB, Hlatky R, Suki D, Yang D, Weinberg J, Gilbert M, et al. Prognostic effect of epidermal growth factor receptor and EGFRvIII in glioblastoma multiforme patients. Clin Cancer Res. 2005;11(4):1462-6.
4. Viana-Pereira M, Lopes JM, Little S, Milanezi F, Basto D, Pardal F, et al. Analysis of EGFR overexpression, EGFR gene amplification and the EGFRvIII mutation in Portuguese high-grade gliomas. Anticancer Res. 2008;28(2A):913-20.
5. Pines G, Kostler WJ, Yarden Y. Oncogenic mutant forms of EGFR: lessons in signal transduction and targets for cancer therapy. FEBS Lett. 2010;584(12):2699-706.
6. Talavera A, Friemann R, Gomez-Puerta S, Martinez-Fleites C, Garrido G, Rabasa A, et al. Nimotuzumab, an antitumor antibody that targets the epidermal growth factor receptor, blocks ligand binding while permitting the active receptor conformation. Cancer Res. 2009;69(14):5851-9.
7. Zhao L, Li QQ, Zhang R, Xi M, Liao YJ, Qian D, et al. The overexpression of IGFBP-3 is involved in the chemosensitivity of esophageal squamous cell carcinoma cells to nimotuzumab combined with cisplatin. Tumour Biol. 2012;33(4):1115-23.
8. Strumberg D, Schultheis B, Scheulen ME, Hilger RA, Krauss J, Marschner N, et al. Phase II study of nimotuzumab, a humanized monoclonal anti-epidermal growth factor receptor (EGFR) antibody, in patients with locally advanced or metastatic pancreatic cancer. Invest New Drugs. 2012;30(3):1138-43.
9. Casaco A, Lopez G, Garcia I, Rodriguez JA, Fernandez R, Figueredo J, et al. Phase I single-dose study of intracavitary-administered Nimotuzumab labeled with 188 Re in adult recurrent high-grade glioma. Cancer Biol Ther. 2008;7(3):333-9.
10. 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 radiarion and chemotherapy with Temozolomide versus standard radiation and Temozolomide. In: American Society of Clinical Oncology Annual Meeting 2012. 2012. J Clin Oncol; 2012: (suppl; abstr 2033).
11. Akashi Y, Okamoto I, Iwasa T, Yoshida T, Suzuki M, Hatashita E, 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(4):749-55.
12. Hong J, Peng Y, Liao Y, Jiang W, Wei R, Huo L, 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(1):151-7.
13. Dowling RJ, Topisirovic I, Fonseca BD, Sonenberg N. Dissecting the role of mTOR: lessons from mTOR inhibitors. Biochim Biophys Acta. 2010;1804(3):433-9.
14. Sami A, Karsy M. Targeting the PI3K/AKT/mTOR signaling pathway in glioblastoma: novel therapeutic agents and advances in understanding. Tumour Biol. 2013;34(4):1991-2002.
15. Guertin DA, Sabatini DM. Defining the role of mTOR in cancer. Cancer Cell. 2007;12(1):9-22.
16. Benjamin D, Colombi M, Moroni C, Hall MN. Rapamycin passes the torch: a new generation of mTOR inhibitors. Nat Rev Drug Discov. 2011;10(11):868-80.
17. Dibble CC, Manning BD. Signal integration by mTORC1 coordinates nutrient input with biosynthetic output. Nat Cell Biol. 2013;15(6):555-64.
18. Heimberger AB, Wang E, McGary EC, Hess KR, Henry VK, Shono T, et al. Mechanisms of action of rapamycin in gliomas. Neuro Oncol. 2005;7(1):1-11.
19. Reardon DA, Quinn JA, Vredenburgh JJ, Gururangan S, Friedman AH, Desjardins A, et al. Phase 1 trial of gefitinib plus sirolimus in adults with recurrent malignant glioma. Clin Cancer Res. 2006;12(3 Pt 1):860-8.
20. Doherty L, Gigas DC, Kesari S, Drappatz J, Kim R, Zimmerman J, et al. Pilot study of the combination of EGFR and mTOR inhibitors in recurrent malignant gliomas. Neurology. 2006;67(1):156-8.
21. James R, Vishwakarma S, Chivukula IV, Basavaraj C, Melarkode R, Montero E, et al. EGFR targeting monoclonal antibody combines with an mTOR inhibitor and potentiates tumor inhibition by acting on complementary signaling hubs. Cancer Med. 2012;1(2):114-27.
22. Fan QW, Cheng CK, Gustafson WC, Charron E, Zipper P, Wong RA, et al. EGFR phosphorylates tumor-derived EGFRvIII driving STAT3/5 and progression in glioblastoma. Cancer Cell. 2013;24(4):438-49.
23. Sarkaria JN, Carlson BL, Schroeder MA, Grogan P, Brown PD, Giannini C, et al. Use of an orthotopic xenograft model for assessing the effect of epidermal growth factor receptor amplification on glioblastoma radiation response. Clin Cancer Res. 2006;12(7 Pt 1):2264-71.
24. Lee WH, Yeh MY, Tu YC, Han SH, Wang YC. Establishment and characterization of a malignant glioma cell line, GBM8401/TSGH. NDMC J Surg Oncol. 1988;38(3):173-81.
25. Lee WH, Tu YC. Scanning electron microscopic study of three glioblastoma multiforme (GBM) cell lines of the Chinese brain in vitro and in vivo. Zhonghua Yi Xue Za Zhi (Taipei). 1991;48(3):177-84.
26. Das A, Tan WL, Teo J, Smith DR. Glioblastoma multiforme in an Asian population: evidence for a distinct genetic pathway. J Neurooncol. 2002;60(2):117-25.
27. Ekstrand AJ, James CD, Cavenee WK, Seliger B, Pettersson RF, Collins VP. Genes for epidermal growth factor receptor, transforming growth factor alpha, and epidermal growth factor and their expression in human gliomas in vivo. Cancer Res. 1991;51(8):2164-72.
28. Huang HS, Nagane M, Klingbeil CK, Lin H, Nishikawa R, Ji XD, et al. The enhanced tumorigenic activity of a mutant epidermal growth factor receptor common in human cancers is mediated by threshold levels of constitutive tyrosine phosphorylation and unattenuated signaling. J Biol Chem. 1997;272(5):2927-35.
29. Hatanpaa KJ, Burma S, Zhao D, Habib AA. Epidermal growth factor receptor in glioma: signal transduction, neuropathology, imaging, and radioresistance. Neoplasia. 2010;12(9):675-84.
30. Johnson H, Del Rosario AM, Bryson BD, Schroeder MA, Sarkaria JN, White FM. Molecular characterization of EGFR and EGFRvIII signaling networks in human glioblastoma tumor xenografts. Mol Cell Proteomics. 2012;11(12):1724-40.
31. Sarkaria JN, Yang L, Grogan PT, Kitange GJ, Carlson BL, Schroeder MA, et al. Identification of molecular characteristics correlated with glioblastoma sensitivity to EGFR kinase inhibition through use of an intracranial xenograft test panel. Mol Cancer Ther. 2007;6(3):1167-74.
32. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, 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):459-66.
33. Tham CK, See SJ, Tan SH, Lim KH, Ng WH, Thomas J, et al. Combined temozolomide and radiation as an initial treatment for anaplastic glioma. Asia Pac J Clin Oncol. 2013;9(3):220-5.
34. Chen P, Aldape K, Wiencke JK, Kelsey KT, Miike R, Davis RL, et al. Ethnicity delineates different genetic pathways in malignant glioma. Cancer Res. 2001;61(10):3949-54.
35. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell. 2006;9(3):157-73.
36. Yan W, Zhang W, You G, Zhang J, Han L, Bao Z, et al. Molecular classification of gliomas based on whole genome gene expression: a systematic report of 225 samples from the Chinese Glioma Cooperative Group. Neuro Oncol. 2012;14(12):1432-40.
37. Dai B, Pieper RO, Li D, Wei P, Liu M, Woo SY, et al. FoxM1B regulates NEDD4-1 expression, leading to cellular transformation and full malignant phenotype in immortalized human astrocytes. Cancer Res. 2010;70(7):2951-61.
38. Boland WK, Bebb G. Nimotuzumab: a novel anti-EGFR monoclonal antibody that retains anti-EGFR activity while minimizing skin toxicity. Expert Opin Biol Ther. 2009;9(9):1199-206.
39. Crombet T, Osorio M, Cruz T, Roca C, del Castillo R, Mon R, 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(9):1646-54.
40. Garrido G, Tikhomirov IA, Rabasa A, Yang E, Gracia E, Iznaga N, et al. Bivalent binding by intermediate affinity of nimotuzumab: a contribution to explain antibody clinical profile. Cancer Biol Ther. 2011;11(4):373-82.
41. Jaramillo M, Grothe S, Basrdsnes J, Banville M, Paul-Roc B, Tikhomirov I, et al. Nimotuzumab, a humanized antiepidermal growth factor receptor antibody, interacts with EGFRvIII. In: AACR 101st Annual Meeting: 2010. Washington, D.C: Cancer Research; 2010. 2010: 70(78 Suppl).
42. Takeda M, Okamoto I, Nishimura Y, Nakagawa K. Nimotuzumab, a novel monoclonal antibody to the epidermal growth factor receptor, in the treatment of non-small cell lung cancer. Lung Cancer: Targets and Therapy. 2011;2:59-67.
43. Oyama TM, Oyama K, Oyama TB, Ishida S, Okano Y, Oyama Y. Zinc at clinically-relevant concentrations potentiates the cytotoxicity of polysorbate 80, a non-ionic surfactant. Toxicol In Vitro. 2010;24(3):737-44.
44. Grandal MV, Zandi R, Pedersen MW, Willumsen BM, van Deurs B, Poulsen HS. EGFRvIII escapes down-regulation due to impaired internalization and sorting to lysosomes. Carcinogenesis. 2007;28(7):1408-17.
45. Hu J, Jo M, Cavenee WK, Furnari F, VandenBerg SR, Gonias SL. Crosstalk between the urokinase-type plasminogen activator receptor and EGF receptor variant III supports survival and growth of glioblastoma cells. Proc Natl Acad Sci U S A. 2011;108(38):15984-9.
46. Qu YY, Hu SL, Xu XY, Wang RZ, Yu HY, Xu JY, et al. Nimotuzumab enhances the radiosensitivity of cancer cells in vitro by inhibiting radiation-induced DNA damage repair. PLoS One. 2013;8(8):e70727.