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Clinical and Developmental Immunology
Volume 2012, Article ID 480429, 15 pages
http://dx.doi.org/10.1155/2012/480429
Review Article

Toxin-Based Targeted Therapy for Malignant Brain Tumors

1Department of Pathology, Duke University Medical Center, Durham, NC 27710, USA
2Department of Surgery, Duke University Medical Center, Durham, NC 27710, USA
3Laboratory of Molecular Biology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA

Received 28 September 2011; Accepted 3 November 2011

Academic Editor: Michael H. Kershaw

Copyright © 2012 Vidyalakshmi Chandramohan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. N. Louis and J. F. Gusella, “A tiger behind many doors: multiple genetic pathways to malignant glioma,” Trends in Genetics, vol. 11, no. 10, pp. 412–415, 1995. View at Publisher · View at Google Scholar · View at Scopus
  2. G. E. Keles, B. Anderson, and M. S. Berger, “The effect of extent of resection on time to tumor progression and survival in patients with glioblastoma multiforme of the cerebral hemisphere,” Surgical Neurology, vol. 52, no. 4, pp. 371–379, 1999. View at Publisher · View at Google Scholar · View at Scopus
  3. S. A. Leibel, C. B. Scott, and J. S. Loeffler, “Contemporary approaches to the treatment of malignant gliomas with radiation therapy,” Seminars in Oncology, vol. 21, no. 2, pp. 198–219, 1994. View at Google Scholar · View at Scopus
  4. G. J. Lesser and S. Grossman, “The chemotherapy of high-grade astrocytomas,” Seminars in Oncology, vol. 21, no. 2, pp. 220–235, 1994. View at Google Scholar · View at Scopus
  5. 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 randomised phase III study: 5-year analysis of the EORTC-NCIC trial,” The Lancet Oncology, vol. 10, no. 5, pp. 459–466, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. D. A. Reardon, A. Desjardins, K. B. Peters et al., “Phase 2 study of carboplatin, irinotecan, and bevacizumab for recurrent glioblastoma after progression on bevacizumab therapy,” Cancer, vol. 117, no. 23, pp. 5351–5358, 2011. View at Google Scholar
  7. L. S. Constine, P. D. Woolf, D. Cann et al., “Hypothalamic-pituitary dysfunction after radiation for brain tumors,” The New England Journal of Medicine, vol. 328, no. 2, pp. 87–94, 1993. View at Publisher · View at Google Scholar · View at Scopus
  8. J. P. Imperato, N. A. Paleologos, and N. A. Vick, “Effects of treatment on long-term survivors with malignant astrocytomas,” Annals of Neurology, vol. 28, no. 6, pp. 818–822, 1990. View at Publisher · View at Google Scholar · View at Scopus
  9. F. B. Furnari, T. Fenton, R. M. Bachoo et al., “Malignant astrocytic glioma: genetics, biology, and paths to treatment,” Genes and Development, vol. 21, no. 21, pp. 2683–2710, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Sathornsumetee, D. A. Reardon, A. Desjardins, J. A. Quinn, J. J. Vredenburgh, and J. N. Rich, “Molecularly targeted therapy for malignant glioma,” Cancer, vol. 110, no. 1, pp. 12–24, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Herlyn, A. Menrad, and H. Koprowski, “Structure, function, and clinical significance of human tumor antigens,” Journal of the National Cancer Institute, vol. 82, no. 24, pp. 1883–1889, 1990. View at Google Scholar · View at Scopus
  12. C. B. Siegall, “Targeted toxins as anticancer agents,” Cancer, vol. 74, no. 3, pp. 1006–1012, 1994. View at Google Scholar · View at Scopus
  13. F. L. Moolten and S. R. Cooperband, “Selective destruction of target cells by diphtheria toxin conjugated to antibody directed against antigens on the cells,” Science, vol. 169, no. 3940, pp. 68–70, 1970. View at Google Scholar · View at Scopus
  14. I. Pastan, R. Hassan, D. J. FitzGerald, and R. J. Kreitman, “Immunotoxin treatment of cancer,” Annual Review of Medicine, vol. 58, pp. 221–237, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Olsnes, K. Refsnes, and A. Pihl, “Mechanism of action of the toxic lectins abrin and ricin,” Nature, vol. 249, no. 5468, pp. 627–631, 1974. View at Google Scholar · View at Scopus
  16. J. E. Weldon and I. Pastan, “A guide to taming a toxin—recombinant immunotoxins constructed from pseudomonas exotoxin a for the treatment of cancer,” FEBS Journal, vol. 278, no. 23, pp. 4683–4700, 2011. View at Google Scholar
  17. L. Carrasco, C. Fernandez Puentes, and D. Vazquez, “Effects of ricin on the ribosomal sites involved in the interaction of the elongation factors,” European Journal of Biochemistry, vol. 54, no. 2, pp. 499–503, 1975. View at Google Scholar · View at Scopus
  18. M. Yamaizumi, E. Mekada, T. Uchida, and Y. Okada, “One molecule of diphtheria toxin fragment A introduced into a cell can kill the cell,” Cell, vol. 15, no. 1, pp. 245–250, 1978. View at Google Scholar · View at Scopus
  19. K. Eiklid, S. Olsnes, and A. Pihl, “Entry of lethal doses of abrin, ricin and modeccin into the cytosol of HeLa cells,” Experimental Cell Research, vol. 126, no. 2, pp. 321–326, 1980. View at Google Scholar · View at Scopus
  20. V. S. Allured, R. J. Collier, S. F. Carroll, and D. B. McKay, “Structure of exotoxin A of Pseudomonas aeruginosa at 3.0-Angstrom resolution,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 5, pp. 1320–1324, 1986. View at Google Scholar · View at Scopus
  21. J. Hwang, D. J. Fitzgerald, S. Adhya, and I. Pastan, “Functional domains of pseudomonas exotoxin identified by deletion analysis of the gene expressed in E. coli,” Cell, vol. 48, no. 1, pp. 129–136, 1987. View at Google Scholar · View at Scopus
  22. M. Z. Kounnas, R. E. Morris, M. R. Thompson, D. J. FitzGerald, D. K. Strickland, and C. B. Saelinger, “The α2-macroglobulin receptor/low density lipoprotein receptor-related protein binds and internalizes Pseudomonas exotoxin A,” Journal of Biological Chemistry, vol. 267, no. 18, pp. 12420–12423, 1992. View at Google Scholar · View at Scopus
  23. D. V. Pastrana, A. J. Hanson, J. Knisely, G. Bu, and D. J. FitzGerald, “LRP1B functions as a receptor for Pseudomonas exotoxin,” Biochimica et Biophysica Acta, vol. 1741, no. 3, pp. 234–239, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. C. B. Siegall, V. K. Chaudhary, D. J. FitzGerald, and I. Pastan, “Functional analysis of domains II, Ib, and III of Pseudomonas exotoxin,” Journal of Biological Chemistry, vol. 264, no. 24, pp. 14256–14261, 1989. View at Google Scholar · View at Scopus
  25. D. J. P. FitzGerald, I. S. Trowbridge, I. Pastan, and M. C. Willingham, “Enhancement of toxicity of antitransferrin receptor antibody-Pseudomonas exotoxin conjugates by adenovirus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 80, no. 13 I, pp. 4134–4138, 1983. View at Google Scholar · View at Scopus
  26. L. Greenfield, M. J. Bjorn, G. Horn et al., “Nucleotide sequence of the structural gene for diphtheria toxin carried by corynebacteriophage ß,” Proceedings of the National Academy of Sciences of the United States of America, vol. 80, no. 22, pp. 6853–6857, 1983. View at Google Scholar · View at Scopus
  27. J. G. Naglich, J. E. Metherall, D. W. Russell, and L. Eidels, “Expression cloning of a Diphtheria toxin receptor: identity with a heparin-binding EGF-like growth factor precursor,” Cell, vol. 69, no. 6, pp. 1051–1061, 1992. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Tsuneoka, K. Nakayama, K. Hatsuzawa, M. Komada, N. Kitamura, and E. Mekada, “Evidence for involvement of furin in cleavage and activation of diphtheria toxin,” Journal of Biological Chemistry, vol. 268, no. 35, pp. 26461–26465, 1993. View at Google Scholar · View at Scopus
  29. K. Sandvig and S. Olsnes, “Diphtheria toxin entry into cells is facilitated by low pH,” Journal of Cell Biology, vol. 87, no. 3, pp. 828–832, 1980. View at Google Scholar · View at Scopus
  30. R. J. Collier and A. M. Pappenheimer Jr., “Studies on the mode of action of diphtheria toxin. II. Effect of toxin on amino acid incorporation in cell-free systems,” Journal of Experimental Medicine, vol. 120, pp. 1019–1039, 1964. View at Google Scholar
  31. T. Honjo, Y. Nishizuka, and O. Hayaishi, “Diphtheria toxin-dependent adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis,” Journal of Biological Chemistry, vol. 243, no. 12, pp. 3553–3555, 1968. View at Google Scholar · View at Scopus
  32. B. G. Van Ness, J. B. Howard, and J. W. Bodley, “ADP-ribosylation of elongation factor 2 by diphtheria toxin. Isolation and properties of the novel ribosyl-amino acid and its hydrolysis products,” Journal of Biological Chemistry, vol. 255, no. 22, pp. 10717–10720, 1980. View at Google Scholar · View at Scopus
  33. F. I. Lamb, L. M. Roberts, and J. M. Lord, “Nucleotide sequence of cloned cDNA coding for preproricin,” European Journal of Biochemistry, vol. 148, no. 2, pp. 265–270, 1985. View at Google Scholar · View at Scopus
  34. S. Olsnes and A. Pihl, “Different biological properties of the two constituent peptide chains of ricin, a toxic protein inhibiting protein synthesis,” Biochemistry, vol. 12, no. 16, pp. 3121–3126, 1973. View at Google Scholar · View at Scopus
  35. D. L. Newton, R. Wales, P. T. Richardson et al., “Cell surface and intracellular functions for ricin galactose binding,” Journal of Biological Chemistry, vol. 267, no. 17, pp. 11917–11922, 1992. View at Google Scholar · View at Scopus
  36. S. Sperti, L. Montanaro, A. Mattioli, and F. Stirpe, “Inhibition by ricin of protein synthesis in vitro: 60 S ribosomal subunit as the target of the toxin,” Biochemical Journal, vol. 136, no. 3, pp. 813–815, 1973. View at Google Scholar · View at Scopus
  37. Y. Endo, K. Mitsui, M. Motizuki, and K. Tsurugi, “The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. The site and the characteristics of the modification in 28 S ribosomal RNA caused by the toxins,” Journal of Biological Chemistry, vol. 262, no. 12, pp. 5908–5912, 1987. View at Google Scholar · View at Scopus
  38. D. W. Laske, R. J. Youle, and E. H. Oldfield, “Tumor regression with regional distribution of the targeted toxin TF- CRM107 in patients with malignant brain tumors,” Nature Medicine, vol. 3, no. 12, pp. 1362–1368, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Weaver and D. W. Laske, “Transferrin receptor ligand-targeted toxin conjugate (Tf-CRM107) therapy of malignant gliomas,” Journal of Neuro-Oncology, vol. 65, no. 1, pp. 3–13, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. D. W. Laske, K. M. Muraszko, E. H. Oldfield et al., “Intraventricular immunotoxin therapy for leptomeningeal neoplasia,” Neurosurgery, vol. 41, no. 5, pp. 1039–1051, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. R. W. Rand, R. J. Kreitman, N. Patronas, F. Varricchio, I. Pastan, and R. K. Puri, “Intratumoral administration of recombinant circularly permuted interleukin-4-Pseudomonas exotoxin in patients with high-grade glioma,” Clinical Cancer Research, vol. 6, no. 6, pp. 2157–2165, 2000. View at Google Scholar · View at Scopus
  42. F. Weber, A. Asher, R. Bucholz et al., “Safety, tolerability, and tumor response of IL4-Pseudomonas exotoxin (NBI-3001) in patients with recurrent malignant glioma,” Journal of Neuro-Oncology, vol. 64, no. 1-2, pp. 125–137, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. F. W. Weber, F. Floeth, A. Asher et al., “Local convection enhanced, delivery of IL4-Pseudomonas exotoxin (NBI-3001) for treatment of patients with recurrent malignant glioma,” Acta Neurochirurgica, Supplementum, no. 88, pp. 93–103, 2003. View at Google Scholar · View at Scopus
  44. N. G. Rainov, K. Gorbatyuk, and V. Heidecke, “Clinical trials with intracerebral convection-enhanced delivery of targeted toxins in malignant glioma,” Reviews on Recent Clinical Trials, vol. 3, no. 1, pp. 2–9, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Kunwar, M. D. Prados, S. M. Chang et al., “Direct intracerebral delivery of cintredekin besudotox (IL13-PE38QQR) in recurrent malignant glioma: a report by the cintredekin besudotox intraparenchymal study group,” Journal of Clinical Oncology, vol. 25, no. 7, pp. 837–844, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Kunwar, S. Chang, M. Westphal et al., “Phase III randomized trial of CED of IL13-PE38QQR vs Gliadel wafers for recurrent glioblastoma,” Neuro-Oncology, vol. 12, no. 8, pp. 871–881, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. T. F. Liu, P. D. Hall, K. A. Cohen et al., “Interstitial diphtheria toxin-epidermal growth factor fusion protein therapy produces regressions of subcutaneous human glioblastoma multiforme tumors in athymic nude mice,” Clinical Cancer Research, vol. 11, no. 1, pp. 329–334, 2005. View at Google Scholar · View at Scopus
  48. J. H. Sampson, G. Akabani, G. E. Archer et al., “Progress report of a Phase I study of the intracerebral microinfusion of a recombinant chimeric protein composed of transforming growth factor (TGF)-α and a mutated form of the Pseudomonas exotoxin termed PE-38 (TP-38) for the treatment of malignant brain tumors,” Journal of Neuro-Oncology, vol. 65, no. 1, pp. 27–35, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. J. H. Sampson, G. Akabani, G. E. Archer et al., “Intracerebral infusion of an EGFR-targeted toxin in recurrent malignant brain tumors,” Neuro-Oncology, vol. 10, no. 3, pp. 320–329, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. D. E. Bullard and D. D. Bigner, “Applications of monoclonal antibodies in the diagnosis and treatment of primary brain tumors,” Journal of Neurosurgery, vol. 63, no. 1, pp. 2–16, 1985. View at Google Scholar · View at Scopus
  51. I. S. Trowbridge, R. A. Newman, D. L. Domingo, and C. Sauvage, “Transferrin receptors: structure and function,” Biochemical Pharmacology, vol. 33, no. 6, pp. 925–932, 1984. View at Publisher · View at Google Scholar · View at Scopus
  52. K. C. Gatter, G. Brown, I. S. Trowbridge, R. E. Woolston, and D. Y. Mason, “Transferrin receptors in human tissues: their distribution and possible clinical relevance,” Journal of Clinical Pathology, vol. 36, no. 5, pp. 539–545, 1983. View at Google Scholar
  53. I. S. Trowbridge and D. L. Domingo, “Anti-transferrin receptor monoclonal antibody and toxin-antibody conjugates affect growth of human tumour cells,” Nature, vol. 294, no. 5837, pp. 171–173, 1981. View at Google Scholar · View at Scopus
  54. L. D. Recht, T. W. Griffin, V. Raso, and A. R. Salimi, “Potent cytotoxicity of an antihuman transferrin receptor-ricin A-chain immunotoxin on human glioma cells in vitro,” Cancer Research, vol. 50, no. 20, pp. 6696–6700, 1990. View at Google Scholar · View at Scopus
  55. J. Zovickian, V. G. Johnson, and R. J. Youle, “Potent and specific killing of human malignant brain tumor cells by an anti-transferrin receptor antibody-ricin immunotoxin,” Journal of Neurosurgery, vol. 66, no. 6, pp. 850–861, 1987. View at Google Scholar · View at Scopus
  56. L. Greenfield, V. G. Johnson, and R. J. Youle, “Mutations in diphtheria toxin separate binding from entry and amplify immunotoxin selectivity,” Science, vol. 238, no. 4826, pp. 536–539, 1987. View at Google Scholar · View at Scopus
  57. D. W. Laske, O. Ilercil, A. Akbasak, R. J. Youle, and E. H. Oldfield, “Efficacy of direct intratumoral therapy with targeted protein toxins for solid human gliomas in nude mice,” Journal of Neurosurgery, vol. 80, no. 3, pp. 520–526, 1994. View at Google Scholar · View at Scopus
  58. L. A. Martell, A. Agrawal, D. A. Ross, and K. M. Muraszko, “Efficacy of transferrin receptor-targeted immunotoxins in brain tumor cell lines and pediatric brain tumors,” Cancer Research, vol. 53, no. 6, pp. 1348–1353, 1993. View at Google Scholar · View at Scopus
  59. V. G. Johnson, C. Wrobel, D. Wilson et al., “Improved tumor-specific immunotoxins in the treatment of CNS and leptomeningeal neoplasia,” Journal of Neurosurgery, vol. 70, no. 2, pp. 240–248, 1989. View at Google Scholar · View at Scopus
  60. L. Giannone, F. A. Greco, and J. D. Hainsworth, “Combination intraventricular chemotherapy for meningeal neoplasia,” Journal of Clinical Oncology, vol. 4, no. 1, pp. 68–73, 1986. View at Google Scholar · View at Scopus
  61. D. J. Yoon, D. S. Chu, C. W. Ng et al., “Genetically engineering transferrin to improve its in vitro ability to deliver cytotoxins,” Journal of Controlled Release, vol. 133, no. 3, pp. 178–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Nelms, A. D. Keegan, J. Zamorano, J. J. Ryan, and W. E. Paul, “The IL-4 receptor: signaling mechanisms and biologic functions,” Annual Review of Immunology, vol. 17, pp. 701–738, 1999. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Kondo, T. Takeshita, N. Ishii et al., “Sharing of the interleukin-2 (IL-2) receptor γ chain between receptors for IL-2 and IL-4,” Science, vol. 262, no. 5141, pp. 1874–1877, 1993. View at Google Scholar · View at Scopus
  64. S. M. Russell, A. D. Keegan, N. Harada et al., “Interleukin-2 receptor γ chain: a functional component of the interleukin-4 receptor,” Science, vol. 262, no. 5141, pp. 1880–1883, 1993. View at Google Scholar · View at Scopus
  65. N. I. Obiri, W. Debinski, W. J. Leonard, and R. K. Puri, “Receptor for interleukin 13. Interaction with interleukin 4 by a mechanism that does not involve the common γ chain shared by receptors for interleukins 2, 4, 7, 9, and 15,” Journal of Biological Chemistry, vol. 270, no. 15, pp. 8797–8804, 1995. View at Publisher · View at Google Scholar · View at Scopus
  66. N. I. Obiri, P. Leland, T. Murata, W. Debinski, and R. K. Puri, “The IL-13 receptor structure differs on various cell types and may share more than one component with il-4 receptor,” Journal of Immunology, vol. 158, no. 2, pp. 756–764, 1997. View at Google Scholar · View at Scopus
  67. N. I. Obiri, G. G. Hillman, G. P. Haas, S. Sud, and R. K. Puri, “Expression of high affinity interleukin-4 receptors on human renal cell carcinoma cells and inhibition of tumor cell growth in vitro by interleukin- 4,” Journal of Clinical Investigation, vol. 91, no. 1, pp. 88–93, 1993. View at Google Scholar · View at Scopus
  68. N. I. Obiri, J. P. Siegel, F. Varricchio, and R. K. Puri, “Expression of high-affinity IL-4 receptors on human melanoma, ovarian and breast carcinoma cells,” Clinical and Experimental Immunology, vol. 95, no. 1, pp. 148–155, 1994. View at Google Scholar · View at Scopus
  69. W. Debinski, R. K. Puri, R. J. Kreitman, and I. Pastan, “A wide range of human cancers express interleukin 4 (IL4) receptors that can be targeted with chimeric toxin composed of IL4 and Pseudomonas exotoxin,” Journal of Biological Chemistry, vol. 268, no. 19, pp. 14065–14070, 1993. View at Google Scholar · View at Scopus
  70. R. K. Puri, W. Debinski, N. Obiri, R. Kreitman, and I. Pastan, “Human renal cell carcinoma cells are sensitive to the cytotoxic effect of a chimeric protein composed of human interleukin-4 and Pseudomonas exotoxin,” Cellular Immunology, vol. 154, no. 2, pp. 369–379, 1994. View at Publisher · View at Google Scholar · View at Scopus
  71. R. K. Puri, P. Leland, R. J. Kreitman, and I. Pastan, “Human neurological cancer cells express interleukin-4 (IL-4) receptors which are targets for the toxic effects of IL4-Pseudomonas exotoxin chimeric protein,” International Journal of Cancer, vol. 58, no. 4, pp. 574–581, 1994. View at Google Scholar · View at Scopus
  72. R. J. Kreitman, R. K. Puri, and I. Pastan, “A circularly permuted recombinant interleukin 4 toxin with increased activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 15, pp. 6889–6893, 1994. View at Publisher · View at Google Scholar · View at Scopus
  73. R. J. Kreitman, R. K. Puri, and I. Pastan, “Increased antitumor activity of a circularly permuted interleukin 4-toxin in mice with interleukin 4 receptor-bearing human carcinoma,” Cancer Research, vol. 55, no. 15, pp. 3357–3363, 1995. View at Google Scholar · View at Scopus
  74. B. H. Joshi, P. Leland, A. Asher, R. A. Prayson, F. Varricchio, and R. K. Puri, “In situ expression of interleukin-4 (IL-4) receptors in human brain tumors and cytotoxicity of a recombinant IL-4 cytotoxin in primary glioblastoma cell cultures,” Cancer Research, vol. 61, no. 22, pp. 8058–8061, 2001. View at Google Scholar · View at Scopus
  75. R. K. Puri, D. S. Hoon, P. Leland et al., “Preclinical development of a recombinant toxin containing circularly permuted interleukin 4 and truncated Pseudomonas exotoxin for therapy of malignant astrocytoma,” Cancer Research, vol. 56, no. 24, pp. 5631–5637, 1996. View at Google Scholar · View at Scopus
  76. S. R. Husain, N. Behari, R. J. Kreitman, I. Pastan, and R. K. Puri, “Complete regression of established human glioblastoma tumor xenograft by interleukin-4 toxin therapy,” Cancer Research, vol. 58, no. 16, pp. 3649–3653, 1998. View at Google Scholar · View at Scopus
  77. T. Shimamura, S. R. Husain, and R. K. Puri, “The IL-4 and IL-13 pseudomonas exotoxins: new hope for brain tumor therapy,” Neurosurgical Focus, vol. 20, no. 4, p. E11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Mintz, D. M. Gibo, B. Slagle-Webb, N. D. Christensen, and W. Debinski, “IL-13Rα2 is a glioma-restricted receptor for interleukin-13,” Neoplasia, vol. 4, no. 5, pp. 388–399, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. 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. View at Publisher · View at Google Scholar · View at Scopus
  80. 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. View at Google Scholar · View at Scopus
  81. S. R. Husain, N. I. Obiri, P. Gill et al., “Receptor for interleukin 13 on AIDS-associated Kaposi's sarcoma cells serves as a new target for a potent Pseudomonas exotoxin-based chimeric toxin protein,” Clinical Cancer Research, vol. 3, no. 2, pp. 151–156, 1997. View at Google Scholar · View at Scopus
  82. B. H. Joshi, P. Leland, and R. K. Puri, “Identification and characterization of interleukin-13 receptor in human medulloblastoma and targeting these receptors with interleukin-13-pseudomonas exotoxin fusion protein,” Croatian Medical Journal, vol. 44, no. 4, pp. 455–462, 2003. View at Google Scholar · View at Scopus
  83. K. Kawakami, M. Kawakami, B. H. Joshi, and R. K. Puri, “Interleukin-13 receptor-targeted cancer therapy in an immunodeficient animal model of human head and neck cancer,” Cancer Research, vol. 61, no. 16, pp. 6194–6200, 2001. View at Google Scholar · View at Scopus
  84. 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. View at Google Scholar · View at Scopus
  85. C. Li, W. A. Hall, N. Jin, D. A. Todhunter, A. Panoskaltsis-Mortari, and D. A. Vallera, “Targeting glioblastoma multiforme with an IL-13/diphtheria toxin fusion protein in vitro and in vivo in nude mice,” Protein Engineering, vol. 15, no. 5, pp. 419–427, 2002. View at Google Scholar · View at Scopus
  86. E. Rustamzadeh, W. A. Hall, D. A. Todhunter et al., “Intracranial therapy of glioblastoma with the fusion protein DTIL13 in immunodeficient mice,” International Journal of Cancer, vol. 118, no. 10, pp. 2594–2601, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. 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 Cancer Therapeutics, vol. 7, no. 6, pp. 1579–1587, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. J. S. Jarboe, K. R. Johnson, Y. Choi, R. R. Lonser, and J. K. Park, “Expression of interleukin-13 receptor α2 in glioblastoma multiforme: implications for targeted therapies,” Cancer Research, vol. 67, no. 17, pp. 7983–7986, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. J. Massague, “Epidermal growth factor-like transforming growth factor. II. Interaction with epidermal growth factor receptors in human placenta membranes and A431 cells,” Journal of Biological Chemistry, vol. 258, no. 22, pp. 13614–13620, 1983. View at Google Scholar · View at Scopus
  90. L. J. Pike, H. Marquardt, G. J. Todaro et al., “Transforming growth factor and epidermal growth factor stimulate the phosphorylation of a synthetic, tyrosine-containing peptide in a similar manner,” Journal of Biological Chemistry, vol. 257, no. 24, pp. 14628–14631, 1982. View at Google Scholar · View at Scopus
  91. R. Derynck, A. B. Roberts, M. E. Winkler, E. Y. Chen, and D. V. Goeddel, “Human transforming growth factor-α: precursor structure and expression in E. coli,” Cell, vol. 38, no. 1, pp. 287–297, 1984. View at Google Scholar · View at Scopus
  92. G. Carpenter and S. Cohen, “Epidermal Growth Factor,” Annual Review of Biochemistry, vol. 48, pp. 193–216, 1979. View at Google Scholar
  93. H. Ushiro and S. Cohen, “Identification of phosphotyrosine as a product of epidermal growth factor-activated protein kinase in A-431 cell membranes,” Journal of Biological Chemistry, vol. 255, no. 18, pp. 8363–8365, 1980. View at Google Scholar · View at Scopus
  94. J. G. M. Klijn, P. M. J. J. Berns, P. I. M. Schmitz, and J. A. Foekens, “The clinical significance of epidermal growth factor receptor (EGF-R) in human breast cancer: a review on 5232 patients,” Endocrine Reviews, vol. 13, no. 1, pp. 3–17, 1992. View at Publisher · View at Google Scholar · View at Scopus
  95. K. Pavelic, Z. Banjac, J. Pavelic, and S. Spaventi, “Evidence for a role of EGF receptor in the progression of human lung carcinoma,” Anticancer Research, vol. 13, no. 4, pp. 1133–1137, 1993. View at Google Scholar · View at Scopus
  96. J. Rubin Grandis, M. F. Melhem, E. L. Barnes, and D. J. Tweardy, “Quantitative immunohistochemical analysis of transforming growth factor-α and epidermal growth factor receptor in patients with squamous cell carcinoma of the head and neck,” Cancer, vol. 78, no. 6, pp. 1284–1292, 1996. View at Publisher · View at Google Scholar · View at Scopus
  97. S. B. Fox, R. A. Persad, N. Coleman, C. A. Day, P. B. Silcocks, and C. C. Collins, “Prognostic value of c-erbB-2 and epidermal growth factor receptor in stage A1 (T1a) prostatic adenocarcinoma,” The British Journal of Urology, vol. 74, no. 2, pp. 214–220, 1994. View at Google Scholar · View at Scopus
  98. N. H. Chow, S. H. Chan, T. S. Tzai, C. L. Ho, and H. S. Liu, “Expression profiles of ErbB family receptors and prognosis in primary transitional cell carcinoma of the urinary bladder,” Clinical Cancer Research, vol. 7, no. 7, pp. 1957–1962, 2001. View at Google Scholar · View at Scopus
  99. W. Yasui, H. Sumiyoshi, J. Hata et al., “Expression of epidermal growth factor receptor in human gastric and colonic carcinomas,” Cancer Research, vol. 48, no. 1, pp. 137–141, 1988. View at Google Scholar · View at Scopus
  100. J. M. Bartlett, S. P. Langdon, B. J. B. Simpson et al., “The prognostic value of epidermal growth factor receptor mRNA expression in primary ovarian cancer,” The British Journal of Cancer, vol. 73, no. 3, pp. 301–306, 1996. View at Google Scholar · View at Scopus
  101. N. Arita, T. Hayakawa, S. Izumoto et al., “Epidermal growth factor receptor in human glioma,” Journal of Neurosurgery, vol. 70, no. 6, pp. 916–919, 1989. View at Google Scholar · View at Scopus
  102. T. A. Libermann, N. Razon, A. D. Bartal et al., “Expression of epidermal growth factor receptors in human brain tumors,” Cancer Research, vol. 44, no. 2, pp. 753–760, 1984. View at Google Scholar
  103. T. A. Libermann, H. R. Nusbaum, N. Razon et al., “Amplification, enhanced expression and possible rearrangement of EGF receptor gene in primary human brain tumours of glial origin,” Nature, vol. 313, no. 5998, pp. 144–147, 1985. View at Google Scholar · View at Scopus
  104. G. N. Fuller and S. H. Bigner, “Amplified cellular oncogenes in neoplasms of the human central nervous system,” Mutation Research, vol. 276, no. 3, pp. 299–306, 1992. View at Publisher · View at Google Scholar · View at Scopus
  105. M. Chaffanet, C. Chauvin, M. Laine et al., “EGF receptor amplification and expression in human brain tumours,” European Journal of Cancer, vol. 28, no. 1, pp. 11–17, 1992. View at Google Scholar · View at Scopus
  106. S. M. Huang and P. M. Harari, “Epidermal growth factor receptor inhibition in cancer therapy: biology, rationale and preliminary clinical results,” Investigational New Drugs, vol. 17, no. 3, pp. 259–269, 1999. View at Publisher · View at Google Scholar · View at Scopus
  107. S. Kunwar, L. H. Pai, and I. Pastan, “Cytotoxicity and antitumor effects of growth factor-toxin fusion proteins on human glioblastoma multiforme cells,” Journal of Neurosurgery, vol. 79, no. 4, pp. 569–576, 1993. View at Google Scholar · View at Scopus
  108. P. C. Phillips, C. Levow, M. Catterall, O. M. Colvin, I. Pastan, and H. Brem, “Transforming growth factor-α-Pseudomonas exotoxin fusion protein (TGF-α-PE38) treatment of subcutaneous and intracranial human glioma and medulloblastoma xenografts in athymic mice,” Cancer Research, vol. 54, no. 4, pp. 1008–1015, 1994. View at Google Scholar · View at Scopus
  109. O. Engebraaten, G. O. Hjortland, S. Juell, H. Hirschberg, and Ø. Fodstad, “Intratumoral immunotoxin treatment of human malignant brain tumors in immunodeficient animals,” International Journal of Cancer, vol. 97, no. 6, pp. 846–852, 2002. View at Publisher · View at Google Scholar · View at Scopus
  110. T. F. Liu, K. A. Cohen, J. G. Ramage, M. C. Willingham, A. M. Thorburn, and A. E. Frankel, “A diphtheria toxin-epidermal growth factor fusion protein is cytotoxic to human glioblastoma multiforme cells,” Cancer Research, vol. 63, no. 8, pp. 1834–1837, 2003. View at Google Scholar · View at Scopus
  111. C. J. Wikstrand, C. J. Reist, G. E. Archer, M. R. Zalutsky, and D. D. Bigner, “The class III variant of the epidermal growth factor receptor (EGFRvIII): characterization and utilization as an immunotherapeutic target,” Journal of NeuroVirology, vol. 4, no. 2, pp. 148–158, 1998. View at Google Scholar · View at Scopus
  112. N. Sugawa, A. J. Ekstrand, C. D. James, and V. P. Collins, “Identical splicing of aberrant epidermal growth factor receptor transcripts from amplified rearranged genes in human glioblastomas,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 21, pp. 8602–8606, 1990. View at Google Scholar · View at Scopus
  113. S. K. Batra, S. Castelino-Prabhu, C. J. Wikstrand et al., “Epidermal growth factor ligand-independent, unregulated, cell-transforming potential of a naturally occurring human mutant EGFRvIII gene,” Cell Growth and Differentiation, vol. 6, no. 10, pp. 1251–1259, 1995. View at Google Scholar · View at Scopus
  114. P. A. Humphrey, A. J. Wong, B. Vogelstein et al., “Anti-synthetic peptide antibody reacting at the fusion junction of deletion-mutant epidermal growth factor receptors in human glioblastoma,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 11, pp. 4207–4211, 1990. View at Publisher · View at Google Scholar · View at Scopus
  115. J. C. Sok, F. M. Coppelli, S. M. Thomas et al., “Mutant epidermal growth factor receptor (EGFRvIII) contributes to head and neck cancer growth and resistance to EGFR targeting,” Clinical Cancer Research, vol. 12, no. 17, pp. 5064–5073, 2006. View at Publisher · View at Google Scholar · View at Scopus
  116. C. J. Wikstrand, L. P. Hale, S. K. Batra et al., “Monoclonal antibodies against EGFRvIII are tumor specific and react with breast and lung carcinomas and malignant gliomas,” Cancer Research, vol. 55, no. 14, pp. 3140–3148, 1995. View at Google Scholar · View at Scopus
  117. M. Nagane, A. Levitzki, A. Gazit, W. K. Cavenee, and H. J. S. Huang, “Drug resistance of human glioblastoma cells conferred by a tumor-specific mutant epidermal growth factor receptor through modulation of Bcl-XL and caspase-3-like proteases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 10, pp. 5724–5729, 1998. View at Google Scholar · View at Scopus
  118. I. A. J. Lorimer, C. J. Wikstrand, S. K. Batra, D. D. Bigner, and I. Pastan, “Immunotoxins that target an oncogenic mutant epidermal growth factor receptor expressed in human tumors,” Clinical Cancer Research, vol. 1, no. 8, pp. 859–864, 1995. View at Google Scholar · View at Scopus
  119. I. A. J. Lorimer, A. Keppler-Hafkemeyer, R. A. Beers, C. N. Pegram, D. D. Bigner, and I. Pastan, “Recombinant immunotoxins specific for a mutant epidermal growth factor receptor: targeting with a single chain antibody variable domain isolated by phage display,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 25, pp. 14815–14820, 1996. View at Publisher · View at Google Scholar · View at Scopus
  120. G. E. Archer, J. H. Sampson, I. A. J. Lorimer et al., “Regional treatment of epidermal growth factor receptor vIII-expressing neoplastic meningitis with a single-chain immunotoxin, MR-1,” Clinical Cancer Research, vol. 5, no. 9, pp. 2646–2652, 1999. View at Google Scholar · View at Scopus
  121. R. Beers, P. Chowdhury, D. Bigner, and I. Pastan, “Immunotoxins with increased activity against epidermal growth factor receptor vIII-expressing cells produced by antibody phage display,” Clinical Cancer Research, vol. 6, no. 7, pp. 2835–2843, 2000. View at Google Scholar · View at Scopus
  122. J. H. Sampson, M. Brady, R. Raghavan et al., “Colocalization of gadolinium-diethylene triamine pentaacetic acid with high-molecular-weight molecules after intracerebral convection-enhanced delivery in humans,” Neurosurgery, vol. 69, no. 3, pp. 668–676, 2011. View at Publisher · View at Google Scholar
  123. W. T. Loging, A. Lal, I. M. Siu et al., “Identifying potential tumor markers and antigens by database mining and rapid expression screening,” Genome Research, vol. 10, no. 9, pp. 1393–1402, 2000. View at Publisher · View at Google Scholar · View at Scopus
  124. C. T. Kuan, K. Wakiya, J. M. Dowell et al., “Glycoprotein nonmetastatic melanoma protein B, a potential molecular therapeutic target in patients with glioblastoma multiforme,” Clinical Cancer Research, vol. 12, no. 7, pp. 1970–1982, 2006. View at Publisher · View at Google Scholar · View at Scopus
  125. C.T. Kuan, K. Wakiya, S.T. Keir et al., “Affinity-matured anti-glycoprotein nmb recombinant immunotoxins targeting malignant gliomas and melanomas,” International Journal of Cancer, vol. 129, pp. 111–121, 2011. View at Google Scholar
  126. G. Pluschke, M. Vanek, A. Evans et al., “Molecular cloning of a human melanoma-associated chondroitin sulfate proteoglycan,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 18, pp. 9710–9715, 1996. View at Publisher · View at Google Scholar · View at Scopus
  127. M. Schrappe, F. G. Klier, R. C. Spiro, T. A. Waltz, R. A. Reisfeld, and C. L. Gladson, “Correlation of chondroitin sulfate proteoglycan expression on proliferating brain capillary endothelial cells with the malignant phenotype of astroglial cells,” Cancer Research, vol. 51, no. 18, pp. 4986–4993, 1991. View at Google Scholar · View at Scopus
  128. G. O. Hjortland, S. S. Garman-Vik, S. Juell et al., “Immunotoxin treatment targeted to the high-molecular-weight melanoma-associated antigen prolonging the survival of immunodeficient rats with invasive intracranial human glioblastoma multiforme,” Journal of Neurosurgery, vol. 100, no. 2, pp. 320–327, 2004. View at Google Scholar · View at Scopus
  129. S. Carrel, R. S. Accolla, A. L. Carmagnola, and J. P. Mach, “Common human melanoma-associated antigen(s) detected by monoclonal antibodies,” Cancer Research, vol. 40, no. 7, pp. 2523–2528, 1980. View at Google Scholar · View at Scopus
  130. S. N. Kurpad, X. G. Zhao, C. J. Wikstrand, S. K. Batra, R. E. McLendon, and D. D. Bigner, “Tumor antigens in astrocytic gliomas,” Glia, vol. 15, no. 3, pp. 244–256, 1995. View at Google Scholar · View at Scopus
  131. D. D. Bigner, M. Brown, R. E. Coleman et al., “Phase I studies of treatment of malignant gliomas and neoplastic meningitis with 131I-radiolabeled monoclonal antibodies anti-tenascin 81C6 and anti-chondroitin proteoglycan sulfate Me1-14 F(ab')2—a preliminary report,” Journal of Neuro-Oncology, vol. 24, no. 1, pp. 109–122, 1995. View at Publisher · View at Google Scholar · View at Scopus
  132. I. Cokgor, G. Akabani, H. S. Friedman et al., “Long term response in a patient with neoplastic meningitis secondary to melanoma treated with 131I-radiolabeled antichondroitin proteoglycan sulfate Mel-14 F(ab′)2: a case study,” Cancer, vol. 91, no. 9, pp. 1809–1813, 2001. View at Publisher · View at Google Scholar
  133. J. Ayriss, R. Reisfeld, C. T. Kuan, S. Keir, I. Pastan, and D. D. Bigner, “Mel-14 and 9.2.27 immunotoxins: promising therapeutics for pediatric glioma,” in Proceedings of the Pediatric Neuro-Oncology Basic and Translational Research Conference, New Orleans, LA, USA, May 2011.
  134. Eph Nomenclature Committee, “Unified nomenclature for eph family receptors and their ligands, the ephrins,” Cell, vol. 90, pp. 403–404, 1997. View at Google Scholar
  135. K. Kullander and R. Klein, “Mechanisms and functions of Eph and ephrin signalling,” Nature Reviews Molecular Cell Biology, vol. 3, no. 7, pp. 475–486, 2002. View at Publisher · View at Google Scholar · View at Scopus
  136. J. Wykosky, D. M. Gibo, and W. Debinski, “A novel, potent, and specific ephrinA1-based cytotoxin against EphA2 receptor-expressing tumor cells,” Molecular Cancer Therapeutics, vol. 6, no. 12, pp. 3208–3218, 2007. View at Publisher · View at Google Scholar · View at Scopus
  137. J. Wykosky, D. M. Gibo, C. Stanton, and W. Debinski, “EphA2 as a novel molecular marker and target in glioblastoma multiforme,” Molecular Cancer Research, vol. 3, no. 10, pp. 541–551, 2005. View at Publisher · View at Google Scholar · View at Scopus
  138. H. W. Smith and C. J. Marshall, “Regulation of cell signalling by uPAR,” Nature Reviews Molecular Cell Biology, vol. 11, no. 1, pp. 23–36, 2010. View at Publisher · View at Google Scholar · View at Scopus
  139. D. A. Vallera, C. Li, N. Jin, A. Panoskaltsis-Mortari, and W. A. Hall, “Targeting urokinase-type plasminogen activator receptor on human glioblastoma tumors with diphtheria toxin fusion protein DTAT,” Journal of the National Cancer Institute, vol. 94, no. 8, pp. 597–606, 2002. View at Google Scholar · View at Scopus
  140. B. J. Stish, S. Oh, and D. A. Vallera, “Anti-glioblastoma effect of a recombinant bispecific cytotoxin cotargeting human IL-13 and EGF receptors in a mouse xenograft model,” Journal of Neuro-Oncology, vol. 87, no. 1, pp. 51–61, 2008. View at Publisher · View at Google Scholar · View at Scopus
  141. S. Oh, A. K. Tsai, J. R. Ohlfest, A. Panoskaltsis-Mortari, and D. A. Vallera, “Evaluation of a bispecific biological drug designed to simultaneously target glioblastoma and its neovasculature in the brain: laboratory investigation,” Journal of Neurosurgery, vol. 114, no. 6, pp. 1662–1671, 2011. View at Publisher · View at Google Scholar
  142. D. A. Todhunter, W. A. Hall, E. Rustamzadeh, Y. Shu, S. O. Doumbia, and D. A. Vallera, “A bispecific immunotoxin (DTAT13) targeting human IL-13 receptor (IL-13R) and urokinase-type plasminogen activator receptor (uPAR) in a mouse xenograft model,” Protein Engineering, Design and Selection, vol. 17, no. 2, pp. 157–164, 2004. View at Publisher · View at Google Scholar · View at Scopus
  143. W. A. Vandergrift, S. J. Patel, J. S. Nicholas, and A. K. Varma, “Convection-enhanced delivery of immunotoxins and radioisotopes for treatment of malignant gliomas,” Neurosurgical Focus, vol. 20, no. 4, p. E13, 2006. View at Publisher · View at Google Scholar · View at Scopus
  144. M. Onda, R. Beers, L. Xiang, S. Nagata, Q. C. Wang, and I. Pastan, “An immunotoxin with greatly reduced immunogenicity by identification and removal of B cell epitopes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 32, pp. 11311–11316, 2008. View at Publisher · View at Google Scholar · View at Scopus
  145. M. R. Zalutsky, “Current status of therapy of solid tumors: brain tumor therapy,” Journal of Nuclear Medicine, vol. 46, no. 1, pp. 151S–156S, 2005. View at Google Scholar · View at Scopus
  146. M. R. Zalutsky, A. Boskovitz, C. T. Kuan et al., “Radioimmunotargeting of malignant glioma by monoclonal antibody D2C7 reactive against both wild-type and variant III mutant epidermal growth factor receptors,” Nuclear Medicine and Biology, vol. 39, no. 1, pp. 23–34, 2012. View at Google Scholar
  147. Y. Kato, G. Vaidyanathan, M. K. Kaneko et al., “Evaluation of anti-podoplanin rat monoclonal antibody NZ-1 for targeting malignant gliomas,” Nuclear Medicine and Biology, vol. 37, no. 7, pp. 785–794, 2010. View at Publisher · View at Google Scholar · View at Scopus