Inhibiting HER3-Mediated Tumor Cell Growth with Affibody Molecules Engineered to Low Picomolar Affinity by Position-Directed Error-Prone PCR-Like Diversification

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Malm, Magdalena ^a   Kronqvist, Nina ^a   Lindberg, Hanna ^a   Gudmundsdotter, Lindvi ^b   Bass, Tarek ^a   Frejd, Fredrik Y ^b,c   Höidén Guthenberg, Ingmarie ^b   Varasteh, Zohreh ^c   Orlova, Anna ^c   Tolmachev, Vladimir ^c   Ståhl, Stefan ^a   Löfblom, John ^a  

^a ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^b Affibody AB   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AFFIBODY MOLECULE; ALANINE; ANTINEOPLASTIC AGENT; HER3 RECEPTOR; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION RESPONSE; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG MEGADOSE; DRUG TARGETING; DRUG UPTAKE; FEMALE; FLOW CYTOMETRY; LOW DRUG DOSE; MALE; MOLECULAR LIBRARY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN REFOLDING; THERMOSTABILITY;

ALANINE; ANIMALS; BIOSENSING TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURFACE DISPLAY TECHNIQUES; CIRCULAR DICHROISM; FEMALE; HUMANS; INHIBITORY CONCENTRATION 50; LIGANDS; MICE; MUTATION; NEOPLASMS; PEPTIDE LIBRARY; PHOSPHORYLATION; PROTEIN BINDING; RECEPTOR, ERBB-3; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 84877609907     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062791     Document Type: Article

References (39)

1. Baselga J, Swain SM, (2009) Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer 9: 463-475.
2. Guy PM, Platko JV, Cantley LC, Cerione RA, Carraway KL 3rd (1994) Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity. Proc Natl Acad Sci U S A 91: 8132-8136.
3. Sierke SL, Cheng K, Kim HH, Koland JG, (1997) Biochemical characterization of the protein tyrosine kinase homology domain of the ErbB3 (HER3) receptor protein. Biochem J 322 (Pt 3): 757-763.
4. Jura N, Shan Y, Cao X, Shaw DE, Kuriyan J, (2009) Structural analysis of the catalytically inactive kinase domain of the human EGF receptor 3. Proc Natl Acad Sci U S A 106: 21608-21613.
5. Citri A, Skaria KB, Yarden Y, (2003) The deaf and the dumb: the biology of ErbB-2 and ErbB-3. Exp Cell Res 284: 54-65.
6. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF 3rd, et al (2003) The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci U S A 100: 8933-8938.
7. Sergina NV, Rausch M, Wang D, Blair J, Hann B, et al. (2007) Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature 445: 437-441.
8. Kong A, Calleja V, Leboucher P, Harris A, Parker PJ, et al. (2008) HER2 oncogenic function escapes EGFR tyrosine kinase inhibitors via activation of alternative HER receptors in breast cancer cells. PLoS One 3: e2881.
9. Garrett JT, Olivares MG, Rinehart C, Granja-Ingram ND, Sanchez V, et al. (2011) Transcriptional and posttranslational up-regulation of HER3 (ErbB3) compensates for inhibition of the HER2 tyrosine kinase. Proc Natl Acad Sci U S A 108: 5021-5026.
10. Sheng Q, Liu X, Fleming E, Yuan K, Piao H, et al. (2010) An activated ErbB3/NRG1 autocrine loop supports in vivo proliferation in ovarian cancer cells. Cancer Cell 17: 298-310.
11. Liu B, Ordonez-Ercan D, Fan Z, Edgerton SM, Yang X, et al. (2007) Downregulation of erbB3 abrogates erbB2-mediated tamoxifen resistance in breast cancer cells. Int J Cancer 120: 1874-1882.
12. Frogne T, Benjaminsen RV, Sonne-Hansen K, Sorensen BS, Nexo E, et al. (2009) Activation of ErbB3, EGFR and Erk is essential for growth of human breast cancer cell lines with acquired resistance to fulvestrant. Breast Cancer Res Treat 114: 263-275.
13. Aurisicchio L, Marra E, Roscilli G, Mancini R, Ciliberto G, (2012) The promise of anti-ErbB3 monoclonals as new cancer therapeutics. Oncotarget 3: 744-758.
14. Kronqvist N, Malm M, Gostring L, Gunneriusson E, Nilsson M, et al. (2011) Combining phage and staphylococcal surface display for generation of ErbB3-specific Affibody molecules. Protein Eng Des Sel 24: 385-396.
15. Gostring L, Malm M, Hoiden-Guthenberg I, Frejd FY, Stahl S, et al. (2012) Cellular effects of HER3-specific affibody molecules. PLoS One 7: e40023.
16. Lofblom J, Feldwisch J, Tolmachev V, Carlsson J, Stahl S, et al. (2010) Affibody molecules: engineered proteins for therapeutic, diagnostic and biotechnological applications. FEBS Lett 584: 2670-2680.
17. Ekerljung L, Wallberg H, Sohrabian A, Andersson K, Friedman M, et al. (2012) Generation and evaluation of bispecific affibody molecules for simultaneous targeting of EGFR and HER2. Bioconjug Chem 23: 1802-1811.
18. Friedman M, Lindstrom S, Ekerljung L, Andersson-Svahn H, Carlsson J, et al. (2009) Engineering and characterization of a bispecific HER2 x EGFR-binding affibody molecule. Biotechnol Appl Biochem 54: 121-131.
19. LaFleur D, Abramyan D, Kanakaraj P, Smith R, Shah R, et al. (2013) Monoclonal antibody therapeutics with up to five specificities: Functional enhancement through fusion of target-specific peptides. mAbs 6: 208-218.
20. Baum RP, Prasad V, Muller D, Schuchardt C, Orlova A, et al. (2010) Molecular imaging of HER2-expressing malignant tumors in breast cancer patients using synthetic 111In- or 68Ga-labeled affibody molecules. J Nucl Med 51: 892-897.
21. Schmidt MM, Wittrup KD, (2009) A modeling analysis of the effects of molecular size and binding affinity on tumor targeting. Mol Cancer Ther 8: 2861-2871.
22. Tolmachev V, Tran TA, Rosik D, Sjoberg A, Abrahmsen L, et al. (2012) Tumor targeting using affibody molecules: interplay of affinity, target expression level, and binding site composition. J Nucl Med 53: 953-960.
23. Aguilar Z, Akita RW, Finn RS, Ramos BL, Pegram MD, et al. (1999) Biologic effects of heregulin/neu differentiation factor on normal and malignant human breast and ovarian epithelial cells. Oncogene 18: 6050-6062.
24. Robinson MK, Hodge KM, Horak E, Sundberg AL, Russeva M, et al. (2008) Targeting ErbB2 and ErbB3 with a bispecific single-chain Fv enhances targeting selectivity and induces a therapeutic effect in vitro. Br J Cancer 99: 1415-1425.
25. Lofblom J, Wernerus H, Stahl S, (2005) Fine affinity discrimination by normalized fluorescence activated cell sorting in staphylococcal surface display. FEMS Microbiol Lett 248: 189-198.
26. Lofblom J, Kronqvist N, Uhlen M, Stahl S, Wernerus H, (2007) Optimization of electroporation-mediated transformation: Staphylococcus carnosus as model organism. J Appl Microbiol 102: 736-747.
27. Feldwisch J, Tolmachev V, Lendel C, Herne N, Sjöberg A, et al. (2010) Design of an optimized scaffold for affibody molecules. J Mol Biol 398: 232-247.
28. Kronqvist N, Lofblom J, Jonsson A, Wernerus H, Stahl S, (2008) A novel affinity protein selection system based on staphylococcal cell surface display and flow cytometry. Protein Eng Des Sel 21: 247-255.
29. Orlova A, Nilsson FY, Wikman M, Widstrom C, Stahl S, et al. (2006) Comparative in vivo evaluation of technetium and iodine labels on an anti-HER2 affibody for single-photon imaging of HER2 expression in tumors. J Nucl Med 47: 512-519.
30. Tolmachev V, Nilsson FY, Widstrom C, Andersson K, Rosik D, et al. (2006) 111In-benzyl-DTPA-ZHER2: 342, an affibody-based conjugate for in vivo imaging of HER2 expression in malignant tumors. J Nucl Med 47: 846-853.
31. Jonsson A, Dogan J, Herne N, Abrahmsén L, Nygren PÅ, (2008) Engineering of a femtomolar affinity binding protein to human serum albumin. Protein Eng Des Sel 21: 515-527.
32. Waibel R, Alberto R, Willuda J, Finnern R, Schibli R, et al. (1999) Stable one-step technetium-99m labeling of His-tagged recombinant proteins with a novel Tc(I)-carbonyl complex. Nat Biotechnol 17: 897-901.
33. de Jong M, Breeman WA, Bernard BF, Rolleman EJ, Hofland LJ, et al. (1995) Evaluation in vitro and in rats of 161Tb-DTPA-octreotide, a somatostatin analogue with potential for intraoperative scanning and radiotherapy. Eur J Nucl Med 22: 608-616.
34. Breeman WA, Kwekkeboom DJ, Kooij PP, Bakker WH, Hofland LJ, et al. (1995) Effect of dose and specific activity on tissue distribution of indium-111-pentetreotide in rats. J Nucl Med 36: 623-627.
35. Hofland LJ, Lamberts SW, van Hagen PM, Reubi JC, Schaeffer J, et al. (2003) Crucial role for somatostatin receptor subtype 2 in determining the uptake of [111In-DTPA-D-Phe1]octreotide in somatostatin receptor-positive organs. J Nucl Med 44: 1315-1321.
36. Tolmachev V, Orlova A, Wei Q, Bruskin A, Carlsson J, et al. (2004) Comparative biodistribution of potential anti-glioblastoma conjugates [111In]DTPA-hEGF and [111In]Bz-DTPA-hEGF in normal mice. Cancer Biother Radiopharm 19: 491-501.
37. Tolmachev V, Stone-Elander S, Orlova A, (2010) Radiolabelled receptor-tyrosine-kinase targeting drugs for patient stratification and monitoring of therapy response: prospects and pitfalls. Lancet Oncol 11: 992-1000.
38. Tolmachev V, Rosik D, Wallberg H, Sjoberg A, Sandstrom M, et al. (2010) Imaging of EGFR expression in murine xenografts using site-specifically labelled anti-EGFR 111In-DOTA-Z EGFR: 2377 Affibody molecule: aspect of the injected tracer amount. Eur J Nucl Med Mol Imaging 37: 613-622.
39. Tolmachev V, Malmberg J, Hofstrom C, Abrahmsen L, Bergman T, et al. (2012) Imaging of insulinlike growth factor type 1 receptor in prostate cancer xenografts using the affibody molecule 111In-DOTA-ZIGF1R: 4551. J Nucl Med 53: 90-97.