Intracranial therapy of glioblastoma with the fusion protein DTAT in immunodeficient mice

International Journal of Cancer

Volumn 120, Issue 2, 2007, Pages 411-419

  Rustamzadeh, Edward ^a   Hall, Walter A ^a   Todhunter, Deborah A ^a   Vallera, Vincent D ^a   Low, Walter C ^a   Liu, Haiying ^a   Panoskaltsis Mortari, Angela ^a   Vallera, Daniel A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Brain tumor; Diphtheria toxin; Fusion protein; Glioblastoma; Immunotoxin; uPA; uPAR

Indexed keywords

AMINO ACID; DIPHTHERIA TOXIN; HYBRID PROTEIN; PROTEIN DTAT; UROKINASE;

ADOLESCENT; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL INJURY; CANCER GROWTH; CANCER SURVIVAL; CONTINUOUS INFUSION; CONTROLLED STUDY; DRUG EFFICACY; DRUG SPECIFICITY; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; MAXIMUM TOLERATED DOSE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUDE MOUSE; PRIORITY JOURNAL; RNA SPLICING; THERMODYNAMICS; TUMOR VOLUME;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; GLIOBLASTOMA; HUMANS; INJECTIONS; KIDNEY; LIVER; MAGNETIC RESONANCE IMAGING; MICE; MICE, NUDE; RECOMBINANT FUSION PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 33845601313     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22278     Document Type: Article

References (64)

1. Rustamzadeh E, Low WC, Vallera DA, Hall WA. Immunotoxin therapy for CNS tumor. J Neurooncol 2003;64:101-16.
2. Yamamoto M, Sawaya R, Mohanam S, Rao VH, Bruner JM, Nicolson GL, Rao JS. Expression and localization of urokinase-type plasminogen activator receptor in a human gliomas. Cancer Res 1994;54:5016-20.
3. Mori T, Abe T, Wakabayashi Y, Hikawa T, Matsuo K, Yamada Y, Kuwano M, Hori S. Up-regulation of urokinase-type plasminogen activator and its receptor correlates with enhanced invasion activity of human glioma cells mediated by transforming growth factor-α or basic fibroblast growth factor. J Neurooncol 2000;46:115-23.
4. Grondahl-Hansen J, Peters HA, van Putten WL, Look MP, Pappot H, Ronne E, Dano K, Klijn JG, Brunner N, Foekens JA. Prognostic significance of the receptor for urokinase plasminogen activator in breast cancer. Clin Cancer Res 1995;1:1079-87.
5. Verspaget HW, Sier CF, Ganesh S, Griffioen G, Lamers CB. Prognostic value of plasminogen activators and their inhibitors in colorectal cancer. Eur J Cancer 1995;31:1105-9.
6. Prager GW, Breuss JM, Steurer S, Mihaly J, Binder BR. Vascular endothelial growth factor (VEGF) induces rapid prourokinase (pro-uPA) activation on the surface of endothelial cells. Blood 2004;103:955-62.
7. Choong PF, Nadesapillai AP. Urokinase plasminogen activator system: a multifunctional role in tumor progression and metastasis. Clin Orthop Relat Res 2003;415(Suppl.):S46-58.
8. Roldan AL, Cubellis MV, Masucci MT, Behrendt N, Lund LR, Dano K, Appella E, Blasi F. Cloning and expression of the receptor for human urokinase plasminogen activator, a central molecule in cell surface, plasmin dependent proteolysis. EMBO J 1990;9:467-74.
9. 2-terminal amino acid sequence and glycosylation variants. J Biol Chem 1990;265:6543-60.
10. Cubellis MV, Nolli ML, Cassani G, Blasi F. Binding of single-chain prourokinase to the urokinase receptor of human U937 cells. J Biol Chem 1986;261:15819-22.
11. Ellis V, Behrendt N, Dano K. Plasminogen activation by receptor-bound urokinase. J Biol Chem 1991;266:12752-8.
12. Ronne E, Behrendt N, Ellis V. Cell-induced potentiation of the plasminogen activation system is abolished by a monoclonal antibody that recognizes the NH-terminal domain of the urokinase receptor. FEBS Lett 1991;288:233-6.
13. Vallera DA, Li C, Jin N, Panoskaltsis-Mortari A, Hall WA. Targeting urokinase-type plasminogen activator receptor on human glioblastoma tumors with diphtheria toxin fusion protein DTAT. J Nat Cancer Inst 2002;94:597-605.
14. Parsa AT, Chakrabarti I, Hurley PT, Chi JH, Hall JS, Kaiser MG, Bruce JN. Limitations of C6/Wistart rat intracerebral glioma model: implications for evaluating immunotherapy. Neurosurgery 2000;47:993-9.
15. Vitetta ES. Immuntoxin and vascular leak syndrome. Cancer 2000;6:5218-24.
16. Baluna R, Vitetta ES. An in vivo model to study of immuntoxin-induced vascular leak syndrome in human tissue. J Immunother 1999;22:41-7.
17. Kreitman RJ. Toxin-labeled monoclonal antibodies. Curr Pharm Biotechnol 2001;2:313-25.
18. Baluna R, Vitetta ES. Vascular leak syndrome: a side effect of immunotherapy. Immunopharmacology 1997;37:117-32.
19. Li C, Hall WA, Jin N, Todhunter DA, Panoskaltsis-Mortari A, Vallera DA. Targeting glioblastoma multiforme with an IL-13/diphtheria toxin fusion protein in vitro and in vivo in nude mice. Protein Eng 2002;15:419-27.
20. Chan CH, Blazar BR, Eide CR, Kreitman RJ, Vallera DA. A murine cytokine fusion toxin specifically targeting the murine granulocyte-macrophage colony-stimulating factor (GM-CSF) receptor on normal committed bone marrow progenitor cells and GM-CSF-dependent tumor cells. Blood 1995;86:2732-40.
21. 390-mIL-3), with bone marrow progenitor cells. Blood 1996;88:1445-56.
22. 390 anti-CD3sFv, a potential new recombinant anti-GVHD immunotoxin. Protein Eng 1997;10:1071-6.
23. Rustamzadeh E, Hall WA, Todhunter DA, Low WC, Liu H, Panoskaltsis-Mortari A, Vallera DA. Intracranial therapy of glioblastoma with the fusion protein DTIL13 in immunodeficient mice. Int J Cancer 2006;118:2594-601.
24. Souweidane MM, Occhiogrosso G, Mark EB, Edgar MA. Interstitial infusion of IL-13-PE38QQR in the rat brain stem. J Neurooncol 2004;67:287-93.
25. Myklebust AT, Godal A, Fodstad O. Targeted therapy with immunotoxins in a nude rat model for leptomeningeal growth of human small cell lung cancer. Cancer Res 1994;54:2146-50.
26. Engebraaten O, Hjortland GO, Juell S, Hirschberg H, Fodstad O. Intratumoral immunotoxin treatment of human malignant brain tumors in immunodeficient animals Int J Cancer 2002;97:846-52.
27. Hjortland GO, Garman-Vik SS, Juell S, Olsen OE, Hirschberg H, Fodstad O, Engebraaten O. Immunotoxin treatment targeted to the high-molecular weight melanoma-associated antigen prolonging the survival of immunodeficient rats with invasive intracranial human glioblastoma multiforme. J Neurosurg 2004;100:320-7.
28. Kawakami K, Kawakami M, Kioi M, Husain SR, Puri RK. Distribution kinetics of targeted cytotoxin in glioma by bolus or convection-enhanced delivery in murine model. J Neurosurg 2004;101:1004-11.
29. Sung C, Dedrick RL, Hall WA, Johnson PA, Youle RJ. The spatial distribution of immunotoxins in solid tumors: assessment by quantitative autoradiography. Cancer Res 1993;53:2092-9.
30. Jain RK. Vascular and interstitial barriers to delivery of therapeutic agents in tumors. Cancer Metastasis Rev 1990;9:253-66.
31. Juweid M, Neumann R, Paik C, Perez-Bacete MJ, Sato J, van Osdol W, Weinstein JN. Micropharmacology of monoclonal antibodies in solid tumors: direct experimental evidence for binding site barrier. Cancer Res 1992;52:5144-53.
32. Adams GP, Schier R, McCall AM, Simmons HH, Horak EM, Alpaugh RK, Marks JD, Weiner LM. High affinity restricts the localization and tumor penetration of single-chain fv antibody molecules. Cancer Res 2001;61:4750-55.
33. Saga T, Neumann RD, Heya T, Sato J, Kinuya S, Le N, Paik CH, Weinstein JN. Targeting cancer micrometastases with monoclonal antibodies: a binding-site barrier. Proc Natl Acad Sci USA 1995;92:8999-9003.
34. Kroll RA, Pagel MA, Muldoon LL, Roman-Goldstein S, Neuwelt EA. Increasing volume of distribution to the brain with interstitial infusion: dose, rather than convection, might be the most important factor. Neurosurgery 1996;38:746-52.
35. Laske DW, Ilercil O, Akbasak A, Youle RJ, Oldfield EH. Efficacy of direct intratumoral therapy with targeted protein toxins for solid human gliomas in nude mice. J Neurosurg 1994;80:520-6.
36. Rustamzadeh E, Vallera DA, Todhunter DA, Low WC, Panoskaltsis-Mortari A, Hall WA. Immunotoxin pharmacokinetics: a comparison of the anti-glioblastoma bi-specific fusion proteins (DTAT13) to DTAT and DTIL13. J Neurooncol 2006;77:257-66.
37. Estreicher A, Wohlwend A, Belin D, Schleuning WD, Vassalli JD. Characterization of the cellular binding site for the urokinase-type plasminogen activator. J Biol Chem 1989;264:1180-9.
38. Wiesner SM, Freese A, Ohlfest JR. Emerging concepts in glioma biology: implications for clinical protocols and rational treatment strategies. Neurosurg Focus 2005;19:E3.
39. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005;308:1314-18.
40. Gehrmann J, Matsumoto Y, Kreutzberg GW. Microglia: intrinsic immunoeffector cell of the brain. Brain Res 1995;20:269-87.
41. Streit WJ. The role of microglia in brain injury. Neurotoxicology 1996;17:671-8.
42. Rossner S, Hartig W, Schliebs R, Bruckner G, Brauer K, Perez-Polo JR, Wiley RG, Bigl V. 192IgG-saporin immunotoxin-induced loss of cholingeric cells differentially activates microglia in rat basal forebrain nuclei. Neurosci Res 1995;41:335-46.
43. Gu Z, Yu J, Perez-Polo JR. Responses in the aged rat brain after total immunolesion. J Neurosci Res 1998;54:7-16.
44. Book AA, Wiley RG, Schweitzer JB. 192 IgG-saporin. 2. Neuropathology in the rat brain. Acta Neuropathol 1995;89:519-26.
45. Liau LM, Prins RM, Kiertscher SM, Odesa SK, Kremen TJ, Giovannone AJ, Lin JW, Chute DJ, Mischel PS, Cloughesy TF, Roth MD. Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin Cancer Res 2005;11:5515-25.
46. Yajima N, Yamanaka R, Mine T, Tsuchiya N, Homma J, Sano M, Kuramoto T, Obata Y, Komatsu N, Arima Y, Yamada A, Shigemori M, et al. Immunologic evaluation of personalized peptide vaccination for patients with advanced malignant glioma. Clin Cancer Res 2005;11:5900-11.
47. Conese M, Olson D, Blasi F. Protease nexin-1-urokinase complexes are internalized and degraded through a mechanism that requires both urokinase receptor and α2-macroglobulin receptor. J Biol Chem 1994;269:17886-92.
48. Cubellis MV, Wun TC, Blasi F. Receptor-mediated internalization and degradation of urokinase is caused by its specific inhibitor PAI-1. EMBO J 1990;9:1079-85.
49. Estreicher A, Muhlhauser J, Carpentier JL, Orci L, Vassalli JD. The receptor for urokinase type plasminogen activator polarizes expression of the protease to the leading edge of migrating monocytes and promotes degradation of enzyme inhibitor complexes. J Cell Biol 1990;111:783-92.
50. Nykjaer A, Conese M, Christensen EI, Olson D, Cremona O, Gliemann J, Blasi F. Recycling of the urokinase receptor upon internalization of the uPA: serpin complexes. EMBO J 1997;16:2610-20.
51. Rajagopal V, Kreitman RJ. Recombinant toxins that bind to the urokinase receptor are cytotoxic without requiring binding to the α(2)-macroglobulin receptor. J Biol Chem 2000;11:7566-73.
52. Fabbrini MS, Carpani D, Bello-Rivero I, Soria MR. The amino-terminal fragment of human urokinase directs a recombinant chimeric toxin to target cells: internalization is toxin mediated. FASEB J 1997;11:1169-76.
53. Ippoliti R, Lendaro E, Benedetti PA, Torrisi MR, Belleudi F, Carpani D, Soria MR, Fabbrini MS. Endocytosis of a chimera between human pro-urokinase and plant toxin saporin: an unusual internalization mechanism. FASEB J 2000;4:1335-44.
54. Rustamzadeh E, Low WC, Vallera DA, Hall WA. Immunotoxin therapy for CNS tumors. J Neurooncol 2003;64:101-16.
55. Hagihara N, Walbridge S, Olson AW, Oldfield EH, Youle RJ. Vascular protection by chloroquine during brain tumor therapy with Tf-CRM107. Cancer Res 2000;60:230-4.
56. Hall WA, Myklebust A, Godal A, Nesland JM, Fodstad O. In vivo efficacy of intrathecal transferrin-Pseudomonas exotoxin A immunotoxin against LOX melanoma. Neurosurgery 1994;34:649-56.
57. Solberg H, Ploug M, Hoyer-Hansen G, Nielsen BS, Lund LR. The murine receptor for urokinase-type plasminogen activator is primarily expressed in tissues actively undergoing remodeling. J Histochem Cytochem 2001;49:237-46.
58. Bacharach E, Itin A, Keshet E. In vivo patterns of expression of urokinase and its inhibitor PAI-1 suggest a concerted role in regulating physiological angiogenesis. Proc Natl Acad Sci USA 1992;89:10686-90.
59. Pepper MS, Sappino AP, Stocklin R, Montesano R, Orci L, Vassalli JD. Upregulation of urokinase receptor expression on migrating endothelial cells. J Cell Biol 1993;673-84.
60. Almus-Jacobs F, Varki N, Sawdey MS, Lostutoff DJ. Endotoxin stimulates expression of the murine urokinase receptor gene in vivo. Am J Pathol 1995;147:688-98.
61. Kioi M, Husain SR, Croteau D, Kunwar S, Puri RK. Convection-enhanced delivery of interleukin-13 receptor-directed cytotoxin for malignant glioma therapy. Technol Cancer Res Treat 2006;5:239-50.
62. Todhunter DA, Hall WA, Rustamzadeh E, Shu Y, Doumbia SO, Vallera DA. A bispecific immunotoxin (DTAT13) targeting human IL-13 receptor (IL-13R) and urokinase-type plasminogen activator receptor (uPAR) in a mouse xenograft model. Prot Eng Des Sel 2004;17:157-64.
63. Debinksi W, Obiri NI, Powers SK, Pastan I, Puri RK. Human glioma cells overexpressed receptors for interleukin 13 and are extremely sensitive to a novel chimeric protein composed of interleukin 13 and pseudomonas exotoxin. Clin Cancer Res 1995;1:1253-8.
64. Debinski W. An immune regulatory cytokine receptor and glioblastoma multiforme: an unexpected link. Crit Rev Oncog 1998;9:255-68.