Combining anti-ERBB3 antibodies specific for domain I and domain III enhances the anti-tumor activity over the individual monoclonal antibodies

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  D'Souza, Jimson W ^a   Reddy, Smitha ^a   Goldsmith, Lisa E ^a   Shchaveleva, Irina ^a   Marks, James D ^b   Litwin, Samuel ^a   Robinson, Matthew K ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; EPITOPE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; MONOCLONAL ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; TRASTUZUMAB; ANTINEOPLASTIC AGENT;

ANTIBODY SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL GROWTH; CELL METABOLISM; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GROWTH RATE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PHAGE DISPLAY; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; CELL SURFACE DISPLAY; CHEMISTRY; DRUG EFFECTS; HEK293 CELL LINE; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASMS; NUDE MOUSE; PROCEDURES; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURFACE DISPLAY TECHNIQUES; HEK293 CELLS; HETEROGRAFTS; HUMANS; IMMUNOGLOBULIN G; IMMUNOTHERAPY; MALE; MICE, NUDE; NEOPLASMS; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION; SINGLE-CHAIN ANTIBODIES;

EID: 84911872833     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112376     Document Type: Article

References (44)

1. Hynes NE, MacDonald G (2009) ErbB receptors and signaling pathways in cancer. Curr Opin Cell Biol 21: 177-184.
2. Yarden Y, Pines G (2012) The ERBB network: at last, cancer therapy meets systems biology. Nat Rev Cancer 12: 553-563.
3. Bellacosa A, Kumar CC, Di Cristofano A, Testa JR (2005) Activation of AKT kinases in cancer: implications for therapeutic targeting. Advances in cancer research 94: 29-86.
4. Robinson MK, Borghaei H, Adams GP, Weiner LM (2011) Pharmacology of Cancer Therapeutics: Monoclonal Antibodies. In: DeVita VT, Lawrence TS, Rosenberg SA, editors. Cancer: Principles and Practice of Oncology. 9th edition ed. Philadelphia: Lippincott Williams & Wilkins. 499-507.
5. Prigent SA, Gullick WJ (1994) Identification of c-erbB-3 binding sites for phosphatidylinositol 3′-kinase and SHC using an EGF receptor/c-erbB-3 chimera. The EMBO journal 13: 2831-2841.
6. Soltoff SP, Carraway KL 3rd, Prigent SA, Gullick WG, Cantley LC (1994) ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Molecular and cellular biology 14: 3550-3558.
7. Zhang K, Sun J, Liu N, Wen D, Chang D, et al. (1996) Transformation of NIH 3T3 cells by HER3 or HER4 receptors requires the presence of HER1 or HER2. J Biol Chem 271: 3884-3890.
8. Alimandi M, Romano A, Curia MC, Muraro R, Fedi P, et al. (1995) Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas. Oncogene 10: 1813-1821.
9. Lee-Hoeflich ST, Crocker L, Yao E, Pham T, Munroe X, et al. (2008) A central role for HER3 in HER2-amplified breast cancer: implications for targeted therapy. Cancer Res 68: 5878-5887.
10. Jaiswal BS, Kljavin NM, Stawiski EW, Chan E, Parikh C, et al. (2013) Oncogenic ERBB3 mutations in human cancers. Cancer Cell 23: 603-617.
11. Hsieh AC, Moasser MM (2007) Targeting HER proteins in cancer therapy and the role of the non-target HER3. Br J Cancer 97: 453-457.
12. van der Horst EH, Murgia M, Treder M, Ullrich A (2005) Anti-HER-3 MAbs inhibit HER-3-mediated signaling in breast cancer cell lines resistant to anti-HER-2 antibodies. Int J Cancer 115: 519-527.
13. Schoeberl B, Faber AC, Li D, Liang MC, Crosby K, et al. (2010) An ErbB3 antibody, MM-121, is active in cancers with ligand-dependent activation. Cancer Res 70: 2485-2494.
14. Blackburn E, Zona S, Murphy ML, Brown IR, Chan SK, et al. (2012) A monoclonal antibody to the human HER3 receptor inhibits Neuregulin 1-beta binding and co-operates with Herceptin in inhibiting the growth of breast cancer derived cell lines. Breast cancer research and treatment 134: 53-59.
15. Sala G, Traini S, D'Egidio M, Vianale G, Rossi C, et al. (2012) An ErbB-3 antibody, MP-RM-1, inhibits tumor growth by blocking ligand-dependent and independent activation of ErbB-3/Akt signaling. Oncogene 31: 1275-1286.
16. Lazrek Y, Dubreuil O, Garambois V, Gaborit N, Larbouret C, et al. (2013) Anti-HER3 domain 1 and 3 antibodies reduce tumor growth by hindering HER2/HER3 dimerization and AKT-induced MDM2, XIAP, and FoxO1 phosphorylation. Neoplasia 15: 335-347.
17. McDonagh CF, Huhalov A, Harms BD, Adams S, Paragas V, et al. (2012) Antitumor activity of a novel bispecific antibody that targets the ErbB2/ErbB3 oncogenic unit and inhibits heregulin-induced activation of ErbB3. Molecular Cancer Therapeutics 11: 582-593.
18. Schaefer G, Haber L, Crocker LM, Shia S, Shao L, et al. (2011) A two-in-one antibody against HER3 and EGFR has superior inhibitory activity compared with monospecific antibodies. Cancer Cell 20: 472-486.
19. 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.
20. 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.
21. Spangler JB, Neil JR, Abramovitch S, Yarden Y, White FM, et al. (2010) Combination antibody treatment down-regulates epidermal growth factor receptor by inhibiting endosomal recycling. Proceedings of the National Academy of Sciences of the United States of America 107: 13252-13257.
22. Ben-Kasus T, Schechter B, Lavi S, Yarden Y, Sela M (2009) Persistent elimination of ErbB-2/HER2-overexpressing tumors using combinations of monoclonal antibodies: relevance of receptor endocytosis. Proceedings of the National Academy of Sciences of the United States of America 106: 3294-3299.
23. Friedman LM, Rinon A, Schechter B, Lyass L, Lavi S, et al. (2005) Synergistic down-regulation of receptor tyrosine kinases by combinations of mAbs: implications for cancer immunotherapy. Proceedings of the National Academy of Sciences of the United States of America 102: 1915-1920.
24. Baselga J, Cortes J, Kim SB, Im SA, Hegg R, et al. (2012) Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. The New England journal of medicine 366: 109-119.
25. Baselga J, Gelmon KA, Verma S, Wardley A, Conte P, et al. (2010) Phase II Trial of Pertuzumab and Trastuzumab in Patients With Human Epidermal Growth Factor Receptor 2-Positive Metastatic Breast Cancer That Progressed During Prior Trastuzumab Therapy. Journal of clinical oncology 28: 1138-1144.
26. Horak E, Heitner T, Robinson MK, Simmons HH, Garrison J, et al. (2005) Isolation of scFvs to in vitro produced extracellular domains of EGFR family members. Cancer Biother Radiopharm 20: 603-613.
27. Kani K, Park E, Landgraf R (2005) The extracellular domains of ErbB3 retain high ligand binding affinity at endosome pH and in the locked conformation. Biochemistry 44: 15842-15857.
28. Tang Y, Lou J, Alpaugh RK, Robinson MK, Marks JD, et al. (2007) Regulation of antibody-dependent cellular cytotoxicity by IgG intrinsic and apparent affinity for target antigen. J Immunol 179: 2815-2823.
29. 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. Proceedings of the National Academy of Sciences of the United States of America 108: 5021-5026.
30. Campbell MR, Amin D, Moasser MM (2010) HER3 comes of age: new insights into its functions and role in signaling, tumor biology, and cancer therapy. Clinical cancer research: an official journal of the American Association for Cancer Research 16: 1373-1383.
31. Burgess AW, Cho HS, Eigenbrot C, Ferguson KM, Garrett TP, et al. (2003) An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Molecular Cell 12: 541-552.
32. Lemmon MA, Bu Z, Ladbury JE, Zhou M, Pinchasi D, et al. (1997) Two EGF molecules contribute additively to stabilization of the EGFR dimer. The EMBO journal 16: 281-294.
33. Garrett JT, Sutton CR, Kuba MG, Cook RS, Arteaga CL (2013) Dual Blockade of HER2 in HER2-Overexpressing Tumor Cells Does Not Completely Eliminate HER3 Function. Clinical cancer research: an official journal of the American Association for Cancer Research 19: 610-619.
34. Hettmann T (2010) U3-1287 (AMG 888), a fully human mAb directed against HER3. San Diego, CA. IBC Life Sciences.
35. Garrett JT, Sutton CR, Kurupi R, Bialucha CU, Ettenberg SA, et al. (2013) Combination of antibody that inhibits ligand-independent HER3 dimerization and a p110alpha inhibitor potently blocks PI3K signaling and growth of HER2+ breast cancers. Cancer Research.
36. Schmiedel J, Blaukat A, Li S, Knochel T, Ferguson KM (2008) Matuzumab binding to EGFR prevents the conformational rearrangement required for dimerization. Cancer Cell 13: 365-373.
37. 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.
38. Menendez JA, Mehmi I, Lupu R (2006) Trastuzumab in combination with heregulin-activated Her-2 (erbB-2) triggers a receptor-enhanced chemosensitivity effect in the absence of Her-2 overexpression. J Clin Oncol 24: 3735-3746.
39. Motoyama AB, Hynes NE, Lane HA (2002) The efficacy of ErbB receptor-targeted anticancer therapeutics is influenced by the availability of epidermal growth factor-related peptides. Cancer Res 62: 3151-3158.
40. Rudnick SI, Lou J, Shaller CC, Tang Y, Klein-Szanto AJ, et al. (2011) Influence of affinity and antigen internalization on the uptake and penetration of Anti-HER2 antibodies in solid tumors. Cancer Res 71: 2250-2259.
41. Talavera A, Friemann R, Gomez-Puerta S, Martinez-Fleites C, Garrido G, et al. (2009) Nimotuzumab, an antitumor antibody that targets the epidermal growth factor receptor, blocks ligand binding while permitting the active receptor conformation. Cancer Research 69: 5851-5859.
42. Ramakrishnan MS, Eswaraiah A, Crombet T, Piedra P, Saurez G, et al. (2009) Nimotuzumab, a promising therapeutic monoclonal for treatment of tumors of epithelial origin. mAbs 1: 41-48.
43. North B, Lehmann A, Dunbrack RL Jr (2011) A New Clustering of Antibody CDR Loop Conformations. J Mol Biol 406: 228-56.
44. Wakankar AA, Feeney MB, Rivera J, Chen Y, Kim M, et al. (2010) Physicochemical stability of the antibody-drug conjugate Trastuzumab-DM1: changes due to modification and conjugation processes. Bioconjug Chem 21: 1588-1595.