PET imaging of epidermal growth factor receptor expression in tumours using 89Zr-labelled ZEGFR:2377 affibody molecules

International Journal of Oncology

Volumn 48, Issue 4, 2016, Pages 1325-1332

  Garousi, Javad ^a   Andersson, Ken G ^b   Mitran, Bogdan ^a   Pichl, Marie Louise ^a   Stahl, Stefan ^b   Orlova, Anna ^a   Löfblom, John ^b   Tolmachev, Vladimir ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

affibody molecules; epidermal growth factor receptor; positron emission tomography; radionuclide imaging; xenografts; zirconium 89

Indexed keywords

DEFEROXAMINE CETUXIMAB ZR 89; DEFEROXAMINE ZEGFR:2377 ZR 89; EPIDERMAL GROWTH FACTOR RECEPTOR; TRACER; UNCLASSIFIED DRUG; EGFR PROTEIN, HUMAN; MONOCLONAL ANTIBODY; ZIRCONIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG CONJUGATION; DRUG DISTRIBUTION; DRUG TUMOR LEVEL; FEMALE; IN VIVO STUDY; ISOTOPE LABELING; MOUSE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CHEMISTRY; DIAGNOSTIC IMAGING; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MOLECULAR IMAGING; NON SMALL CELL LUNG CANCER; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MOLECULAR IMAGING; POSITRON-EMISSION TOMOGRAPHY; RECEPTOR, EPIDERMAL GROWTH FACTOR; XENOGRAFT MODEL ANTITUMOR ASSAYS; ZIRCONIUM;

EID: 84959020465     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2016.3369     Document Type: Article

References (54)

1. Mendelsohn J, and Baselga J. Epidermal growth factor receptor targeting in cancer. Semin Oncol. 33: 369-385, 2006.
2. Scaltriti M, and Baselga J. The epidermal growth factor receptor pathway: A model for targeted therapy. Clin Cancer Res. 12: 5268-5272, 2006.
3. Goffin JR, and Zbuk K. Epidermal growth factor receptor: Pathway, therapies and pipeline. Clin Ther. 35: 1282-1303, 2013.
4. Ang KK, Andratschke NH, and Milas L. Epidermal growth factor receptor, and response of head-And-neck carcinoma to therapy. Int J Radiat Oncol Biol Phys. 58: 959-965, 2004.
5. Tsutsui S, Kataoka A, Ohno S, Murakami S, Kinoshita J, and Hachitanda Y. Prognostic, and predictive value of epidermal growth factor receptor in recurrent breast cancer. Clin Cancer Res. 8: 3454-3460, 2002.
6. Selvaggi G, Novello S, Torri V, Leonardo E, De Giuli P, Borasio P, Mossetti C, Ardissone F, Lausi P, and Scagliotti GV. Epidermal growth factor receptor overexpression correlates with a poor prognosis in completely resected non-small-cell lung cancer. Ann Oncol. 15: 28-32, 2004.
7. Humbert O, Riedinger JM, Charon-Barra C, Berriolo-Riedinger A, Desmoulins I, Lorgis V, Kanoun S, Coutant C, Fumoleau P, Cochet A, and Brunotte F. Identification of biomarkers including 18FDG-PET/CT for early prediction of response to neoadjuvant chemotherapy in triple negative breast cancer. Clin Cancer Res. 21: 5460-5468, 2015.
8. Ang KK, Berkey BA, Tu X, Zhang HZ, Katz R, Hammond EH, Fu KK, and Milas L. Impact of epidermal growth factor receptor expression on survival, and pattern of relapse in patients with advanced head, and neck carcinoma. Cancer Res. 62: 7350-7356, 2002.
9. Cappuzzo F, Hirsch FR, Rossi E, Bartolini S, Ceresoli GL, Bemis L, Haney J, Witta S, Danenberg K, Domenichini I, et al. Epidermal growth factor receptor gene, and protein, and gefitinib sensitivity in non-small-cell lung cancer. J Natl Cancer Inst. 97: 643-655, 2005.
10. Hirsch FR, Varella-Garcia M, Bunn PA Jr, Franklin WA, Dziadziuszko R, Thatcher N, Chang A, Parikh P, Pereira JR, Ciuleanu T, et al. Molecular predictors of outcome with gefitinib in a phase III placebo-controlled study in advanced non-smallcell lung cancer. J Clin Oncol. 24: 5034-5042, 2006.
11. Pirker R, Pereira JR, von Pawel J, Krzakowski M, Ramlau R, Park K, de Marinis F, Eberhardt WE, Paz-Ares L, Störkel S, et al. EGFR expression as a predictor of survival for first-line chemotherapy plus cetuximab in patients with advanced nonsmall-cell lung cancer: Analysis of data from the phase 3 FLEX study. Lancet Oncol. 13: 33-42, 2012.
12. Bradley JD, Paulus R, Komaki R, Masters G, Blumenschein G, Schild S, Bogart J, Hu C, Forster K, Magliocco A, et al. Standarddose versus high-dose conformal radiotherapy with concurrent, and consolidation carboplatin plus paclitaxel with or without cetuximab for patients with stage IIIA or IIIB non-small-cell lung cancer (RTOG 0617): A randomised, two-by-Two factorial phase 3 study. Lancet Oncol. 16: 187-199, 2015.
13. Bentzen SM, Atasoy BM, Daley FM, Dische S, Richman PI, Saunders MI, Trott KR, and Wilson GD. Epidermal growth factor receptor expression in pretreatment biopsies from head, and neck squamous cell carcinoma as a predictive factor for a benefit from accelerated radiation therapy in a randomized controlled trial. J Clin Oncol. 23: 5560-5567, 2005.
14. Vignot S, Besse B, André F, Spano JP, and Soria JC. Discrepancies between primary tumor, and metastasis: A literature review on clinically established biomarkers. Crit Rev Oncol Hematol. 84: 301-313, 2012.
15. Yarom N, Marginean C, Moyana T, Gorn-Hondermann I, Birnboim HC, Marginean H, Auer RC, Vickers M, Asmis TR, Maroun J, et al. EGFR expression variance in paired colorectal cancer primary, and metastatic tumors. Cancer Biol Ther. 10: 416-421, 2010.
16. Wei Q, Shui Y, Zheng S, Wester K, Nordgren H, Nygren P, Glimelius B, and Carlsson J. EGFR, HER2, and HER3 expression in primary colorectal carcinomas, and corresponding metastases: Implications for targeted radionuclide therapy. Oncol Rep. 25: 3-11, 2011.
17. Gomez-Roca C, Raynaud CM, Penault-Llorca F, Mercier O, Commo F, Morat L, Sabatier L, Dartevelle P, Taranchon E, Besse B, et al. Differential expression of biomarkers in primary non-small cell lung cancer, and metastatic sites. J Thorac Oncol. 4: 1212-1220, 2009.
18. Italiano A, Vandenbos FB, Otto J, Mouroux J, Fontaine D, Marcy PY, Cardot N, Thyss A, and Pedeutour F. Comparison of the epidermal growth factor receptor gene, and protein in primary non-small-cell-lung cancer, and metastatic sites: Implications for treatment with EGFR-inhibitors. Ann Oncol. 17: 981-985, 2006.
19. Goldenberg A, Masui H, Divgi C, Kamrath H, Pentlow K, and Mendelsohn J. Imaging of human tumor xenografts with an indium-111-labeled anti-epidermal growth factor receptor monoclonal antibody. J Natl Cancer Inst. 81: 1616-1625, 1989.
20. Divgi CR, Welt S, Kris M, Real FX, Yeh SD, Gralla R, Merchant B, Schweighart S, Unger M, Larson SM, et al. Phase I, and imaging trial of indium 111-labeled anti-epidermal growth factor receptor monoclonal antibody 225 in patients with squamous cell lung carcinoma. J Natl Cancer Inst. 83: 97-104, 1991.
21. Cai W, Chen K, He L, Cao Q, Koong A, and Chen X. Quantitative PET of EGFR expression in xenograft-bearing mice using 64Cu-labeled cetuximab, a chimeric anti-EGFR monoclonal antibody. Eur J Nucl Med Mol Imaging. 34: 850-858, 2007.
22. Ping Li W, Meyer LA, Capretto DA, Sherman CD, and Anderson CJ. Receptor-binding, biodistribution and metabolism studies of 64Cu-DOTA-cetuximab, a PET-imaging agent for epidermal growth-factor receptor-positive tumors. Cancer Biother Radiopharm. 23: 158-171, 2008.
23. Nayak TK, Garmestani K, Baidoo KE, Milenic DE, and Brechbiel MW. Preparation, biological evaluation and pharmacokinetics of the human anti-HER1 monoclonal antibody panitumumab labeled with 86Y for quantitative PET of carcinoma. J Nucl Med. 51: 942-950, 2010.
24. Nayak TK, Garmestani K, Milenic DE, and Brechbiel MW. PET, and MRI of metastatic peritoneal, and pulmonary colorectal cancer in mice with human epidermal growth factor receptor 1-Targeted 89Zr-labeled panitumumab. J Nucl Med. 53: 113-120, 2012.
25. Aerts HJ, Dubois L, Perk L, Vermaelen P, van Dongen GA, Wouters BG, and Lambin P. Disparity between in vivo EGFR expression, and 89Zr-labeled cetuximab uptake assessed with PET. J Nucl Med. 50: 123-131, 2009.
26. Chang AJ, De Silva RA, and Lapi SE. Development, and characterization of 89Zr-labeled panitumumab for immuno-positron emission tomographic imaging of the epidermal growth factor receptor. Mol Imaging. 12: 17-27, 2013.
27. Cuartero-Plaza A, Martínez-Miralles E, Rosell R, Vadell-Nadal C, Farré M, and Real FX. Radiolocalization of squamous lung carcinoma with 131I-labeled epidermal growth factor. Clin Cancer Res. 2: 13-20, 1996.
28. Reilly RM, Kiarash R, Sandhu J, Lee YW, Cameron RG, Hendler A, Vallis K, and Gariépy J. A comparison of EGF, and MAb 528 labeled with 111In for imaging human breast cancer. J Nucl Med. 41: 903-911, 2000.
29. Velikyan I, Sundberg AL, Lindhe O, Höglund AU, Eriksson O, Werner E, Carlsson J, Bergström M, Långström B, and Tolmachev V : Preparation, and evaluation of 68Ga-DOTA-hEGF for visualization of EGFR expression in malignant tumors. J Nucl Med. 46: 1881-1888, 2005.
30. Li W, Niu G, Lang L, Guo N, Ma Y, Kiesewetter DO, Backer JM, Shen B, and Chen X. PET imaging of EGF receptors using [18F] FBEM-EGF in a head, and neck squamous cell carcinoma model. Eur J Nucl Med Mol Imaging. 39: 300-308, 2012.
31. Löfblom J, Feldwisch J, Tolmachev V, Carlsson J, Ståhl S, and Frejd FY. Affibody molecules: Engineered proteins for therapeutic, diagnostic, and biotechnological applications. FEBS Lett. 584: 2670-2680, 2010.
32. Nygren PA. Alternative binding proteins: Affibody binding proteins developed from a small three-helix bundle scaffold. FEBS J. 275: 2668-2676, 2008.
33. Ahlgren S, and Tolmachev V. Radionuclide molecular imaging using Affibody molecules. Curr Pharm Biotechnol. 11: 581-589, 2010.
34. Feldwisch J, and Tolmachev V. Engineering of affibody molecules for therapy, and diagnostics. Methods Mol Biol. 899: 103-126, 2012.
35. Sörensen J, Sandberg D, Sandström M, Wennborg A, Feldwisch J, Tolmachev V, Åström G, Lubberink M, Garske-Román U, Carlsson J, et al. First-in-human molecular imaging of HER2 expression in breast cancer metastases using the 111In-ABY-025 affibody molecule. J Nucl Med. 55: 730-735, 2014.
36. Friedman M, Orlova A, Johansson E, Eriksson TL, Höidén-Guthenberg I, Tolmachev V, Nilsson FY, and Ståhl S. Directed evolution to low nanomolar affinity of a tumor-Targeting epidermal growth factor receptor-binding affibody molecule. J Mol Biol. 376: 1388-1402, 2008.
37. Tolmachev V, Friedman M, Sandström M, Eriksson TL, Rosik D, Hodik M, Ståhl S, Frejd FY, and Orlova A. Affibody molecules for epidermal growth factor receptor targeting in vivo: Aspects of dimerization, and labeling chemistry. J Nucl Med. 50: 274-283, 2009.
38. Tolmachev V, Rosik D, Wållberg H, Sjöberg A, Sandström M, Hansson M, Wennborg A, and Orlova A. Imaging of EGFR expression in murine xenografts using site-specifically labelled anti-EGFR 111In-DOTA-ZEGFR:2377 Affibody molecule: aspect of the injected tracer amount. Eur J Nucl Med Mol Imaging. 37: 613-622, 2010.
39. Vosjan MJ, Perk LR, Visser GW, Budde M, Jurek P, Kiefer GE, and van Dongen GA. Conjugation, and radiolabeling of monoclonal antibodies with zirconium-89 for PET imaging using the bifunctional chelate p-isothiocyanatobenzyl-desferrioxamine. Nat Protoc. 5: 739-743, 2010.
40. Malmberg J, Tolmachev V, and Orlova A. Imaging agents for in vivo molecular profiling of disseminated prostate cancer-Targeting EGFR receptors in prostate cancer: comparison of cellular processing of [111In]-labeled affibody molecule ZEGFR:2377, and cetuximab. Int J Oncol. 38: 1137-1143, 2011.
41. Barta P, Malmberg J, Melicharova L, Strandgård J, Orlova A, Tolmachev V, Laznicek M, and Andersson K. Protein interactions with HER-family receptors can have different characteristics depending on the hosting cell line. Int J Oncol. 40: 1677-1682, 2012.
42. Tolmachev V, and Stone-Elander S. Radiolabelled proteins for positron emission tomography: Pros, and cons of labelling methods. Biochim Biophys Acta 1800: 487-510, 2010.
43. Altai M, Strand J, Rosik D, Selvaraju RK, Eriksson Karlström A, Orlova A, and Tolmachev V. Influence of nuclides, and chelators on imaging using affibody molecules: Comparative evaluation of recombinant affibody molecules site-specifically labeled with 68Ga, and In via maleimido derivatives of DOTA, and NODAGA. Bioconjug Chem. 24: 1102-1109, 2013.
44. Heskamp S, Laverman P, Rosik D, Boschetti F, van der Graaf WT, Oyen WJ, van Laarhoven HW, Tolmachev V, and Boerman OC. Imaging of human epidermal growth factor receptor type 2 expression with 18F-labeled affibody molecule ZHER2:2395 in a mouse model for ovarian cancer. J Nucl Med. 53: 146-153, 2012.
45. Strand J, Varasteh Z, Eriksson O, Abrahmsen L, Orlova A, and Tolmachev V. Gallium-68-labeled affibody molecule for PET imaging of PDGFRβ expression in vivo. Mol Pharm 11:3 957-3964, 2014.
46. Miao Z, Ren G, Liu H, Qi S, Wu S, and Cheng Z. PET of EGFR expression with an 18F-labeled affibody molecule. J Nucl Med. 53: 1110-1118, 2012.
47. Su X, Cheng K, Jeon J, Shen B, Venturin GT, Hu X, Rao J, Chin FT, Wu H, and Cheng Z. Comparison of two site-specifically 18F-labeled affibodies for PET imaging of EGFR positive tumors. Mol Pharm. 11: 3947-3956, 2014.
48. Dijkers EC, Kosterink JG, Rademaker AP, Perk LR, van Dongen GA, Bart J, de Jong JR, de Vries EG, and Lub-de Hooge MN. Development, and characterization of clinical-grade 89Zr-Trastuzumab for HER2/neu immunoPET imaging. J Nucl Med. 50: 974-981, 2009.
49. Terwisscha van Scheltinga AG, Lub-de Hooge MN, Abiraj K, Schröder CP, Pot L, Bossenmaier B, Thomas M, Hölzlwimmer G, Friess T, Kosterink JG, et al. ImmunoPET, and biodistribution with human epidermal growth factor receptor 3 targeting antibody 89Zr-RG7116. MAbs. 6: 1051-1058, 2014.
50. Dijkers EC, Oude Munnink TH, Kosterink JG, Brouwers AH, Jager PL, de Jong JR, van Dongen GA, Schröder CP, Lub-de Hooge MN, and de Vries EG. Biodistribution of 89Zr-Trastuzumab, and PET imaging of HER2-positive lesions in patients with metastatic breast cancer. Clin Pharmacol Ther. 87: 586-592, 2010.
51. Oosting SF, Brouwers AH, van Es SC, Nagengast WB, Oude Munnink TH, Lub-de Hooge MN, Hollema H, de Jong JR, de Jong IJ, de Haas S, et al. 89Zr-bevacizumab PET visualizes heterogeneous tracer accumulation in tumor lesions of renal cell carcinoma patients, and differential effects of antiangiogenic treatment. J Nucl Med. 56: 63-69, 2015.
52. Fischer G, Seibold U, Schirrmacher R, Wängler B, and Wängler C. 89Zr, a radiometal nuclide with high potential for molecular imaging with PET: Chemistry, applications, and remaining challenges. Molecules. 18: 6469-6490, 2013.
53. Vegt E, de Jong M, Wetzels JF, Masereeuw R, Melis M, Oyen WJ, Gotthardt M, and Boerman OC. Renal toxicity of radiolabeled peptides, and antibody fragments: Mechanisms, impact on radionuclide therapy and strategies for prevention. J Nucl Med. 51: 1049-1058, 2010.
54. Ahlgren S, Orlova A, Wållberg H, Hansson M, Sandström M, Lewsley R, Wennborg A, Abrahmsén L, Tolmachev V, and Feldwisch J. Targeting of HER2-expressing tumors using 111In-ABY-025, a second-generation affibody molecule with a fundamentally reengineered scaffold. J Nucl Med. 51: 1131-1138, 2010.