In vitro effects and ex vivo binding of an EGFR-specific immunotoxin on rhabdomyosarcoma cells

Journal of Cancer Research and Clinical Oncology

Volumn 141, Issue 6, 2015, Pages 1049-1061

  Niesen, Judith ^b   Brehm, Hannes ^a   Stein, Christoph ^a,b   Berges, Nina ^a   Pardo, Alessa ^a   Fischer, Rainer ^b,c   ten Haaf, Andre ^d   Gattenlöhner, Stefan ^d   Tur, Mehmet K ^d   Barth, Stefan ^a,b  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

EGFR; Immunotoxin; Pseudomonas exotoxin A; Rhabdomyosarcoma; scFv

Indexed keywords

EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOTOXIN; RECOMBINANT PROTEIN;

APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; IMMUNOTHERAPY; IN VITRO STUDY; METABOLISM; PATHOLOGY; PROCEDURES; RHABDOMYOSARCOMA; RHABDOMYOSARCOMA, ALVEOLAR; RHABDOMYOSARCOMA, EMBRYONAL; TREATMENT OUTCOME; TUMOR CELL LINE; UPREGULATION;

APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; IMMUNOTOXINS; IN VITRO TECHNIQUES; MICROSCOPY, CONFOCAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT PROTEINS; RHABDOMYOSARCOMA; RHABDOMYOSARCOMA, ALVEOLAR; RHABDOMYOSARCOMA, EMBRYONAL; TREATMENT OUTCOME; UP-REGULATION;

EID: 84937965492     PISSN: 01715216     EISSN: 14321335     Source Type: Journal    
DOI: 10.1007/s00432-014-1884-z     Document Type: Article

References (78)

1. Abraham J et al (2011) Preclinical testing of erlotinib in a transgenic alveolar rhabdomyosarcoma mouse model. Sarcoma 2011:130484. doi:10.1155/2011/130484
2. Ahmad ZA, Yeap SK, Ali AM, Ho WY, Alitheen NB, Hamid M (2012) scFv antibody: principles and clinical application. Clin Dev Immunol 2012:980250. doi:10.1155/2012/980250
3. Allen TM (2002) Ligand-targeted therapeutics in anticancer therapy. Nat Rev Cancer 2:750–763. doi:10.1038/nrc903
4. Amoury M et al (2013) SNAP-tag based agents for preclinical in vitro imaging in malignant diseases. Curr Pharm Des 19:5429–5436
5. Antignani A, Fitzgerald D (2013) Immunotoxins: the role of the toxin. Toxins 5:1486–1502. doi:10.3390/toxins5081486
6. Armistead PM et al (2007) Expression of receptor tyrosine kinases and apoptotic molecules in rhabdomyosarcoma: correlation with overall survival in 105 patients. Cancer 110:2293–2303. doi:10.1002/cncr.23038
7. Azemar M et al (2000) Recombinant antibody toxins specific for ErbB2 and EGF receptor inhibit the in vitro growth of human head and neck cancer cells and cause rapid tumor regression in vivo International journal of cancer. J Int Cancer 86:269–275
8. Bachran D et al (2010) Epidermal growth factor receptor expression affects the efficacy of the combined application of saponin and a targeted toxin on human cervical carcinoma cells. Int J Cancer 127:1453–1461. doi:10.1002/ijc.25123
9. Barth S (2002) Technology evaluation: BL22. NCI current opinion in molecular therapeutics 4:72–75
10. Barth S, Huhn M, Matthey B, Klimka A, Galinski EA, Engert A (2000) Compatible-solute-supported periplasmic expression of functional recombinant proteins under stress conditions. Appl Environ Microbiol 66:1572–1579
11. Becker N, Benhar I (2012) Antibody-based immunotoxins for the treatment of cancer. Antibodies 1:39–69. doi:10.3390/antib1010039
12. Biberacher V et al (2012) The cytotoxicity of anti-CD22 immunotoxin is enhanced by bryostatin 1 in B-cell lymphomas through CD22 upregulation and PKC-betaII depletion. Haematologica 97:771–779. doi:10.3324/haematol.2011.049155
13. Bisogno G et al (2012) Rhabdomyosarcoma in adolescents: a report from the AIEOP soft tissue sarcoma committee. Cancer 118:821–827. doi:10.1002/cncr.26355
14. Brehm H et al (2014) A CSPG4-specific immunotoxin kills rhabdomyosarcoma cells and binds to primary tumor tissues Cancer Lett. doi:10.1016/j.canlet.2014.07.006
15. Bruell D et al (2003) The recombinant anti-EGF receptor immunotoxin 425(scFv)-ETA′ suppresses growth of a highly metastatic pancreatic carcinoma cell line. Int J Oncol 23:1179–1186
16. Bruell D et al (2005) Recombinant anti-EGFR immunotoxin 425(scFv)-ETA′ demonstrates anti-tumor activity against disseminated human pancreatic cancer in nude mice. Int J Mol Med 15:305–313
17. Camp ER, Summy J, Bauer TW, Liu W, Gallick GE, Ellis LM (2005) Molecular mechanisms of resistance to therapies targeting the epidermal growth factor receptor. Clin Cancer Res 11:397–405
18. Cen L et al (2007) Phosphorylation profiles of protein kinases in alveolar and embryonal rhabdomyosarcoma. Mod Pathol 20:936–946. doi:10.1038/modpathol.3800834
19. Chandramohan V, Bigner D (2013) A novel recombinant immunotoxin-based therapy targeting wild-type and mutant EGFR improves survival in murine models of glioblastoma. OncoImmunology 2(12):e26852
20. Chong CR, Janne PA (2013) The quest to overcome resistance to EGFR-targeted therapies in cancer. Nat Med 19:1389–1400. doi:10.1038/nm.3388
21. Cizeau J, Grenkow DM, Brown JG, Entwistle J, MacDonald GC (2009) Engineering and biological characterization of VB6-845, an anti-EpCAM immunotoxin containing a T-cell epitope-depleted variant of the plant toxin bouganin. J Immunother 32:574–584. doi:10.1097/CJI.0b013e3181a6981c
22. Colcher D, Pavlinkova G, Beresford G, Booth BJ, Choudhury A, Batra SK (1998) Pharmacokinetics and biodistribution of genetically-engineered antibodies. Q J Nucl Med 42:225–241
23. Davicioni E et al (2009) Molecular classification of rhabdomyosarcoma–genotypic and phenotypic determinants of diagnosis: a report from the Children’s Oncology Group. Am J Pathol 174:550–564. doi:10.2353/ajpath.2009.080631
24. De Giovanni C et al (1996) Antisense epidermal growth factor receptor transfection impairs the proliferative ability of human rhabdomyosarcoma cells. Cancer Res 56:3898–3901
25. Dittmann K, Mayer C, Fehrenbacher B, Schaller M, Kehlbach R, Rodemann HP (2010) Nuclear EGFR shuttling induced by ionizing radiation is regulated by phosphorylation at residue Thr654. FEBS Lett 584:3878–3884. doi:10.1016/j.febslet.2010.08.005
26. Ganti R et al (2006) Expression and genomic status of EGFR and ErbB-2 in alveolar and embryonal rhabdomyosarcoma. Mod Pathol 19:1213–1220. doi:10.1038/modpathol.3800636
27. Gattenlohner S et al (2010) A human recombinant autoantibody-based immunotoxin specific for the fetal acetylcholine receptor inhibits rhabdomyosarcoma growth in vitro and in a murine transplantation model. J Biomed Biotechnol 2010:187621. doi:10.1155/2010/187621
28. Ghetie MA, Tucker K, Richardson J, Uhr JW, Vitetta ES (1994) Eradication of minimal disease in severe combined immunodeficient mice with disseminated Daudi lymphoma using chemotherapy and an immunotoxin cocktail. Blood 84:702–707
29. Green MR, Sambrook J (2012) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
30. Hawkins DS, Gupta AA, Rudzinski ER (2014) What is new in the biology and treatment of pediatric rhabdomyosarcoma? Curr Opin Pediatr 26:50–56. doi:10.1097/MOP.0000000000000041
31. Hristodorov D et al (2013) Microtubule-associated protein tau facilitates the targeted killing of proliferating cancer cells in vitro and in a xenograft mouse tumour model in vivo. Br J Cancer 109:1570–1578. doi:10.1038/bjc.2013.457
32. Hussain AF, Amoury M, Barth S (2013) SNAP-tag technology: a powerful tool for site specific conjugation of therapeutic and imaging agents. Curr Pharm Des 19:5437–5442
33. Jain S, Xu R, Prieto VG, Lee P (2010) Molecular classification of soft tissue sarcomas and its clinical applications Int J. Clin Exp Pathol 3:416–428
34. Kamat V et al (2008) Enhanced EGFR inhibition and distinct epitope recognition by EGFR antagonistic mAbs C225 and 425. Cancer Biol Ther 7:726–733
35. Kampmeier F, Ribbert M, Nachreiner T, Dembski S, Beaufils F, Brecht A, Barth S (2009) Site-specific, covalent labeling of recombinant antibody fragments via fusion to an engineered version of 6-O-alkylguanine DNA alkyltransferase. Bioconjug Chem 20:1010–1015. doi:10.1021/bc9000257
36. Kampmeier F et al (2010) Rapid optical imaging of EGF receptor expression with a single-chain antibody SNAP-tag fusion protein. Eur J Nucl Med Mol Imaging 37:1926–1934. doi:10.1007/s00259-010-1482-5
37. Koefoed K et al (2011) Rational identification of an optimal antibody mixture for targeting the epidermal growth factor receptor. mAbs 3:584–595. doi:10.4161/mabs.3.6.17955
38. Kreitman RJ (2006) Immunotoxins for targeted cancer therapy. AAPS j 8:E532–E551. doi:10.1208/aapsj080363
39. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
40. Mazzoleni S et al (2010) Epidermal growth factor receptor expression identifies functionally and molecularly distinct tumor-initiating cells in human glioblastoma multiforme and is required for gliomagenesis. Cancer Res 70:7500–7513. doi:10.1158/0008-5472.can-10-2353
41. Mendelsohn J (2002) Targeting the epidermal growth factor receptor for cancer therapy. J Clin Oncol 20:1s–13s
42. Missiaglia E et al (2012) PAX3/FOXO1 fusion gene status is the key prognostic molecular marker in rhabdomyosarcoma and significantly improves current risk stratification. J Clin Oncol 30:1670–1677. doi:10.1200/jco.2011.38.5591
43. Muller KM, Arndt KM, Strittmatter W, Pluckthun A (1998) The first constant domain (C(H)1 and C(L)) of an antibody used as heterodimerization domain for bispecific miniantibodies. FEBS Lett 422:259–264
44. Murthy U, Basu A, Rodeck U, Herlyn M, Ross AH, Das M (1987) Binding of an antagonistic monoclonal antibody to an intact and fragmented EGF-receptor polypeptide. Arch Biochem Biophys 252:549–560
45. Pardo A, Stocker M, Kampmeier F, Melmer G, Fischer R, Thepen T, Barth S (2012) In vivo imaging of immunotoxin treatment using Katushka-transfected A-431 cells in a murine xenograft tumour model. Cancer Immunol Immunother 61:1617–1626. doi:10.1007/s00262-012-1219-3
46. Pastan I, FitzGerald D (1991) Recombinant toxins for cancer treatment. Science 254:1173–1177
47. Pastan I, Chaudhary V, FitzGerald DJ (1992) Recombinant toxins as novel therapeutic agents. Annu Rev Biochem 61:331–354. doi:10.1146/annurev.bi.61.070192.001555
48. Pastan I, Hassan R, FitzGerald DJ, Kreitman RJ (2007) Immunotoxin treatment of cancer. Annu Rev Med 58:221–237. doi:10.1146/annurev.med.58.070605.115320
49. Pedersen MW, Jacobsen HJ, Koefoed K, Hey A, Pyke C, Haurum JS, Kragh M (2010) Sym004: a novel synergistic anti-epidermal growth factor receptor antibody mixture with superior anticancer efficacy. Cancer Res 70:588–597. doi:10.1158/0008-5472.CAN-09-1417
50. Ratti M, Tomasello G (2014) Emerging combination therapies to overcome resistance in EGFR-driven tumors. Anticancer Drugs 25:127–139. doi:10.1097/cad.0000000000000035
51. Ray A, Huh WW (2012) Current state-of-the-art systemic therapy for pediatric soft tissue sarcomas. Curr Oncol Rep 14:311–319. doi:10.1007/s11912-012-0243-y
52. Ricci C et al (2002) HER/erbB receptors as therapeutic targets of immunotoxins in human rhabdomyosarcoma cells. J Immunother 25:314–323
53. Schiffer S et al (2013) Species-dependent functionality of the human cytolytic fusion proteins granzyme B-H22(scFv) and H22(scFv)-angiogenin in macrophages. Antibodies 2:9–18. doi:10.3390/antib2010009
54. Sequist LV, Lynch TJ (2008) EGFR tyrosine kinase inhibitors in lung cancer: an evolving story. Annu Rev Med 59:429–442. doi:10.1146/annurev.med.59.090506.202405
55. Simon-Keller K, Barth S, Vincent A, Marx A (2013) Targeting the fetal acetylcholine receptor in rhabdomyosarcoma. Expert Opin Ther Targets 17:127–138. doi:10.1517/14728222.2013.734500
56. Singh R, Samant U, Hyland S, Chaudhari PR, Wels WS, Bandyopadhyay D (2007) Target-specific cytotoxic activity of recombinant immunotoxin scFv(MUC1)-ETA on breast carcinoma cells and primary breast tumors. Mol Cancer Ther 6:562–569. doi:10.1158/1535-7163.MCT-06-0604
57. Singh R, Zhang Y, Pastan I, Kreitman RJ (2012) Synergistic antitumor activity of anti-CD25 recombinant immunotoxin LMB-2 with chemotherapy. Clin Cancer Res 18:152–160. doi:10.1158/1078-0432.ccr-11-1839
58. Stahnke B et al (2008) Granzyme B-H22(scFv), a human immunotoxin targeting CD64 in acute myeloid leukemia of monocytic subtypes. Mol Cancer Ther 7:2924–2932. doi:10.1158/1535-7163.MCT-08-0554
59. Stocker M, Tur MK, Sasse S, Krussmann A, Barth S, Engert A (2003) Secretion of functional anti-CD30-angiogenin immunotoxins into the supernatant of transfected 293T-cells. Protein Expr Purif 28:211–219
60. Sumegi J, Streblow R, Frayer RW, Dal Cin P, Rosenberg A, Meloni-Ehrig A, Bridge JA (2010) Recurrent t(2;2) and t(2;8) translocations in rhabdomyosarcoma without the canonical PAX-FOXO1 fuse PAX3 to members of the nuclear receptor transcriptional coactivator family. Genes Chromosom Cancer 49:224–236. doi:10.1002/gcc.20731
61. Tebbutt N, Pedersen MW, Johns TG (2013) Targeting the ERBB family in cancer: couples therapy. Nat Rev Cancer 13:663–673. doi:10.1038/nrc3559
62. Thorpe SJ, Turner C, Heath A, Feavers I, Vatn I, Natvig JB, Thompson KM (2003) Clonal analysis of a human antimouse antibody (HAMA) response. Scand J Immunol 57:85–92
63. Tur MK et al (2003) Recombinant CD64-specific single chain immunotoxin exhibits specific cytotoxicity against acute myeloid leukemia cells. Cancer Res 63:8414–8419
64. Wachtel M et al (2006) Subtype and prognostic classification of rhabdomyosarcoma by immunohistochemistry. J Clin Oncol 24:816–822. doi:10.1200/jco.2005.03.4934
65. Walter D et al (2011) CD133 positive embryonal rhabdomyosarcoma stem-like cell population is enriched in rhabdospheres. PLoS ONE 6:e19506. doi:10.1371/journal.pone.0019506
66. Wayne AS, Fitzgerald DJ, Kreitman RJ, Pastan I (2014) Immunotoxins for leukemia. Blood 123:2470–2477. doi:10.1182/blood-2014-01-492256
67. Wei BR, Ghetie MA, Vitetta ES (2000) The combined use of an immunotoxin and a radioimmunoconjugate to treat disseminated human B-cell lymphoma in immunodeficient mice. Clin Cancer Res 6:631–642
68. Weidle UH, Tiefenthaler G, Schiller C, Weiss EH, Georges G, Brinkmann U (2014) Prospects of bacterial and plant protein-based immunotoxins for treatment of cancer. Cancer Genomics Proteomics 11:25–38
69. Weiss A, Gill J, Goldberg J, Lagmay J, Spraker-Perlman H, Venkatramani R, Reed D (2014) Advances in therapy for pediatric sarcomas. Curr Oncol Rep 16:395. doi:10.1007/s11912-014-0395-z
70. Weldon JE, Pastan I (2011) A guide to taming a toxin–recombinant immunotoxins constructed from Pseudomonas exotoxin A for the treatment of cancer. FEBS J 278:4683–4700. doi:10.1111/j.1742-4658.2011.08182.x
71. Wels W et al (2004) Recombinant immunotoxins and retargeted killer cells: employing engineered antibody fragments for tumor-specific targeting of cytotoxic effectors. Cancer Immunol Immunother 53:217–226. doi:10.1007/s00262-003-0482-8
72. Williamson D et al (2010) Fusion gene-negative alveolar rhabdomyosarcoma is clinically and molecularly indistinguishable from embryonal rhabdomyosarcoma. J Clin Oncol 28:2151–2158. doi:10.1200/jco.2009.26.3814
73. Yamamoto Y et al (2013) Cetuximab promotes anticancer drug toxicity in rhabdomyosarcomas with EGFR amplification in vitro. Oncol Rep 30:1081–1086. doi:10.3892/or.2013.2588
74. Yewale C, Baradia D, Vhora I, Patil S, Misra A (2013) Epidermal growth factor receptor targeting in cancer: a review of trends and strategies. Biomaterials 34:8690–8707. doi:10.1016/j.biomaterials.2013.07.100
75. Yip WL, Weyergang A, Berg K, Tonnesen HH, Selbo PK (2007) Targeted delivery and enhanced cytotoxicity of cetuximab-saporin by photochemical internalization in EGFR-positive cancer cells. Mol Pharm 4:241–251. doi:10.1021/mp060105u
76. Yokota T, Milenic DE, Whitlow M, Schlom J (1992) Rapid tumor penetration of a single-chain Fv and comparison with other immunoglobulin forms. Cancer Res 52:3402–3408
77. Yun CH et al (2008) The T790 M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci USA 105:2070–2075. doi:10.1073/pnas.0709662105
78. Zanola A, Rossi S, Faggi F, Monti E, Fanzani A (2012) Rhabdomyosarcomas: an overview on the experimental animal models. J Cell Mol Med 16:1377–1391. doi:10.1111/j.1582-4934.2011.01518.x