Inhibition of HER3 activation and tumor growth with a human antibody binding to a conserved epitope formed by domain III and IV

mAbs

Volumn 9, Issue 5, 2017, Pages 831-843

  Schmitt, Lisa C ^a   Rau, Alexander ^a   Seifert, Oliver ^a   Honer, Jonas ^a   Hutt, Meike ^a   Schmid, Simone ^a   Zantow, Jonas ^b   Hust, Michael ^b   Dübel, Stefan ^b   Olayioye, Monilola A ^a   Kontermann, Roland E ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Cancer therapy; ErbB3; HER3; heregulin; internalization; phage display; receptor tyrosine kinase; therapeutic antibody

Indexed keywords

CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G3 43; NEU DIFFERENTIATION FACTOR; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; UNCLASSIFIED DRUG; CANCER ANTIBODY; EPITOPE; ERBB3 PROTEIN, HUMAN; IMMUNOGLOBULIN G; NRG1 PROTEIN, HUMAN;

AFFINITY CHROMATOGRAPHY; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN BINDING; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOCHEMICAL ANALYSIS; CANCER THERAPY; CELL PROLIFERATION; CELL SURVIVAL; COLONY FORMATION; COMPETITIVE INHIBITION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIMERIZATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOGLOBULIN DOMAIN; INTERNALIZATION; LIGAND BINDING; MOUSE; MTT ASSAY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIZE EXCLUSION CHROMATOGRAPHY; TUMOR GROWTH; TUMOR VOLUME; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; EXPERIMENTAL NEOPLASM; IMMUNOLOGY; MCF-7 CELL LINE; PATHOLOGY; SIGNAL TRANSDUCTION;

ANTIBODIES, NEOPLASM; EPITOPES; HUMANS; IMMUNOGLOBULIN G; MCF-7 CELLS; NEOPLASMS, EXPERIMENTAL; NEUREGULIN-1; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85020301573     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.1080/19420862.2017.1319023     Document Type: Article

References (44)

1. Wieduwilt MJ, Moasser MM. The epidermal growth factor receptor family:Biology driving targeted therapeutics. Cell Mol Life Sci 2008; 65:1566-84; PMID:18259690 PMCID; https://doi.org/10.1007/s00018-008-7440-8.
2. Kol A, Terwisscha van Scheltinga AG, Timmer-Bosscha H, Lamberts LE, Bensch F, de Vries EG, Schröder CP. HER3, a serious partner in crime:Therapeutic approaches and potential biomarkers for effect of HER3-targeting. Pharmacol Ther 2014; 143:1-11; PMID:24513440; https://doi.org/10.1016/j.pharmthera.2014.01.005.
3. Baselga J, Swain SM. Novel anticancer targets:Revisiting ErbB2 and discovering ErbB3. Nat Rev Cancer 2009; 9:463-75; PMID:19536107; https://doi.org/10.1038/nrc2656.
4. Aurisicchio L, Marra E, Roscilli G, Mancini R, Ciliberto G. The promise of anti-ErbB3 monoclonals as new cancer therapeutics. Oncotarget 2012; 3:744-58; PMID:22889873; https://doi.org/10.18632/oncotarget.550
5. Ocana A, Vera-Badillo F, Seruga B, Templeton A, Pandiella A, Amir E. HER3 overexpression and survival in solid tumors:A meta-analysis. J Natl Cancer Inst 2012; 105:266-73; PMID:23221996; https://doi.org/10.1093/jnci/djs501.
6. Amin DN, Cambell MR, Moasser MM. The role of HER3, the unpretentious member of the HER family, in cancer biology and cancer therapeutics. Semin Cell Dev Biol 2010; 21:944-50; PMID:20816829; https://doi.org/10.1016/j.semcdb.2010.08.007.
7. Kruser TJ, Wheeler DL. Mechanisms of resistance to HER family targeting antibodies. Exp Cell Res 2010; 316:1083-100; PMID:20064507; https://doi.org/10.1016/j.yexcr.2010.01.009.
8. Roskoski Jr R. The ErbB/HER family of protein-tyrosine kinases and cancer. Pharmacol Res 2014; 79:34-74; PMID:24269963; https://doi.org/10.1016/j.phrs.2013.11.002.
9. Breuleux M. Role of heregulin in human cancer. Cell Mol Life Sci 2007; 64:2358-77; PMID:17530167; https://doi.org/10.1007/s00018-007-7120-0.
10. Cho HS, Leahy DJ. Structure of the extracellular region of HER3 reveals an interdomain tether. Science 2002; 297:1330-33; PMID:12154198; https://doi.org/10.1126/science.1074611.
11. Schmitz KR, Ferguson KM. 2009 Interaction of antibodies with ErbB receptor extracellular regions. Exp Cell Res 2007; 315:659-70; PMID:18992239; https://doi.org/10.1016/j.yexcr.2008.10.008.
12. Yarden Y, Sliwkowski MX. Untangeling the ErbB signalling network. Nat Rev Mol Cell Biol 2001; 2:127-37; PMID:11252954; https://doi.org/10.1038/35052073.
13. Gaborit N, Lindzen M, Yarden Y. Emerging anti-cancer antibodies and combination therapies targeting HER3/ErbB3. Human Vaccin Immunother 2015; 12:576-92; PMID:26529100; https://doi.org/10.1080/21645515.2015.1102809.
14. Sierke SL, Cheng K, Kim HH, Koland JG. Biochemical characterization of the protein tyrosine kinase homology domain of the ErbB3 (HER3) receptor protein. Biochem J 1997; 322:757-63; PMID:9148746.
15. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 1997; 16:1647-55; PMID:9130710; https://doi.org/10.1093/emboj/16.7.1647.
16. Tanizaki J, Okamoto I, Sakai K, Nakagawa K. Differential roles of trans-phosphorylated EGFR, HER2, HER3, and RET as heterodimerisation partners of MET in lung cancer with MET amplification. B J Cancer 2011; 105:807-13; PMID:21847121; https://doi.org/10.1038/bjc.2011.322.
17. Mujoo K, Choi BK, Huang Z, Zhang N, An Z. Regulation of ErbB3/HER3 signaling in cancer. Oncotarget 2014; 5:10222-36; PMID:25400118; https://doi.org/10.18632/oncotarget.2655.
18. Wu X, Cheng Y, Li G, Xia L, Gu R, Wen X, Ming X, Chen H. Her3 is associated with poor survival of gastric adenocarcinoma:Her3 promotes proliferation, survival and migration of human gastric cancer mediated by PI3K/AKT signaling pathway. Med Oncol 2014; 31:903; PMID:24623015; https://doi.org/10.1007/s12032-014-0903-x.
19. Shi F, Telesco SE, Radhakrishnan R, Lemmon MA. ErbB3/HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Prot Natl Acad Sci USA 2010; 107:7692-97; PMID:20351256; https://doi.org/10.1073/pnas.1002753107.
20. Steinkamp MP, Low-Nam ST, Yang S, Lidke KA, Lidke DS, Wilson BS. ErbB3 is an active tyrosine kinase capable of homo- and heterointeractions. Mol Cell Biol 2014; 34:965-77; PMID:24379439; https://doi.org/10.1128/MCB.01605-13.
21. Jaiswal BS, Kljavin NM, Stawiski EW, Chan E, Parikh C, Durinck S, Chaudhuri S, Pujara K, Guillory J, Edgar KA, et al. Oncogenic ErbB3 mutations in human cancers. Cancer Cell 2013; 23:603-17; PMID:23680147; https://doi.org/10.1016/j.ccr.2013.04.012.
22. Malm M, Frejd FY, Stahl S, Löfblom J. Targeting HER3 using mono- and bispecific antibodies or alternative scaffolds. MAbs 2016; 8:1195-209; PMID:27532938; https://doi.org/10.1080/19420862.2016.1212147.
23. Zhang N, Chang Y, Rios A, An Z. HER3/ErbB3, an emerging cancer therapeutic target. Acta Biochim Biophys Sin 2016; 48:39-48; PMID:26496898; https://doi.org/10.1093/abbs/gmv103.
24. Garner AP, Bialucha CU, Spraque ER, Garrett JT, Sheng Q, Li S, Sineshchekova O, Saxena P, Sutton CR, Chen D, et al. An antibody that locks HER3 in the inactive conformation inhibits tumor growth driven by HER2 or Neuregulin. Cancer Res 2013; 73:6024-35; PMID:23928993; https://doi.org/10.1158/0008-5472.CAN-13-1198.
25. Lee S, Greenlee EB, Amick JR, Ligon GF, Lillquist JS, Natoli Jr EJ, Hadari Y, Alvarado D, Schlessinger J. Inhibition of ErbB3 by a monoclonal antibody that locks the extracellular domain in an inactive configuration. Proc Natl Acad Sci USA 2015; 112:13225-30; PMID:26460020; https://doi.org/10.1073/pnas.1518361112.
26. Horton HM, Bernett MJ, Pong E, Peipp M, Karki S, Chu SY, Richards JO, Vostiar I, Joyce PF, Repp R, et al. Potent in vitro and in vivo activity of an Fc engineered anti-CD19 monoclonal antibody against lymphoma and leukemia. Cancer Res 2008; 68:8049-57; PMID:18829563; https://doi.org/10.1158/0008-5472.CAN-08-2268.
27. Liu JF, RayCoqiard O, Selle F, Poveda AM, Cibula D, Hirte H, Hilpert F, Raspagliesi F, Gladieff L, Harter P, et al. Randomized Phase II trial of Seribantumab in combination with paclitaxel in patients with advanced Platinum-Resistant or -Refractory ovarian cancer. J Clin Oncol 2016; 34:4345-53; PMID:27998236; https://doi.org/10.1200/JCO.2016.67.1891.
28. Meneses-Lorente G, Friess T, Kolm I, Hölzlwimmer G, Bader S, Meille C, Thomas M, Bossenmaier B. Preclinical pharmacokinetics, pharmacodynamcis, and efficacy of RG7116:A novel humanized, glycoengineered anti-HER3 antibody. Cancer Chemother Pharmacol 2015; 75:837-50; PMID:25702049; https://doi.org/10.1007/s00280-015-2697-8.
29. Zhou Y, Goenaga AL, Harms BD, Zhou H, Lou J, Conrad F, Adams GP, Schoeberl B, Nielsen UB, Marks JD. Impact of intrinsic affinity on functional binding and biological activity of EGFR antibodies. Mol Cancer Ther 2012; 11:1467-76; PMID:22564724; https://doi.org/10.1158/1535-7163.MCT-11-1038.
30. Lemmon MA. Ligand-induced Erbb receptor dimerization. Exp Cell Res 2009; 315:638-48; PMID:19038249; https://doi.org/10.1016/j.yexcr.2008.10.024.
31. Hu S, Sun Y, Meng Y, Wang X, Yang W, Fu W, Guo H, Qian W, Hou S, Li B, et al. Molecular architecture of the ErbB2 extracellular domain homodimer. Oncotarget 2015; 6:1695-706; PMID:25633808; https://doi.org/10.18632/oncotarget.2713.
32. Huang Z, Choi BK, Mujoo K, Fan X, Fa M, Mukherjee S, Owiti N, Zhang N, An Z. The E3 ubiquitin ligase NEDD4 negatively regulates HER3/ErbB3 level and signaling. Oncogene 2015; 34:1105-15; PMID:24662824; https://doi.org/10.1038/onc.2014.56.
33. Le Clorennec C, Lazrek Y, Dubreuil O, Larbouret C, Poul M-A, Mondon P, Melino G, Pèlegrin A, Chardès T. The anti-HER (ErbB3) therapeutic antibody 9F7-F11 induces HER3 ubiquitination and degradation in tumors through JNK1/2-dependent ITCH/AIP4 activation. Oncotarget 2016; 7:37013-29; PMID:27203743; https://doi.org/10.18632/oncotarget.9455.
34. Lazrek Y, Dubreuil O, Garambois V, Gaborit N, Larbouret C, Le Clorennec C, Thomas G, Leconet W, Jarlier M, Pugnière M, et al. Anti-HER3 domain 1 and 3 antibodies reduce tumor growth by hindering HER2/HER3 dimerization and AKT-induced MDM2, XIAP, and FoxO1 phosphorylation. Neoplasia 2013; 15:335-47; PMID:23479511.
35. Wang S, Huang J, Lyu H, Cai B, Yang X, Li F, Tan J, Edgerton SM, Thor AD, Lee CK, et al. Therapeutic targeting of erbB3 with MM-121/SAR256212 enhances antitumor activity of paclitaxel against erbB2-overexpressing breast cancer. Breast Cancer Res 2013; 15:R101; PMID:24168763; https://doi.org/10.1186/bcr3563.
36. Mischberger C, Schiller CB, Schräml M, Dimoudis N, Friess T, Gerdes CA, Reiff U, Lifke V, Hoelzlwimmer G, Kolm I, et al. RG7116, a therapeutic antibody that binds to inactive HER3 receptor and is optimized for immune effector activation. Cancer Res 2013; 73:5183-94; PMID:23780344; https://doi.org/10.1158/0008-5472.CAN-13-0099.
37. 2 fragments of a mixture of three monoclonal anti-HER-2 antibodies. Clin Cancer Res 2004; 10:3542-51; PMID:15161714; https://doi.org/10.1158/1078-0432.CCR-03-0549.
38. Crombet-Ramos T, Rak J, Pérez R, Viloria-Petit A. Antiproliferative, antiangiogenic and proapoptotic activity of h-R3:A humanized anti-EGFR antibody. Int J Cancer 2002; 101:567-75; PMID:12237899; https://doi.org/10.1002/ijc.10647.
39. Yu J, Li Q, Xu Q, Liu L, Jiang B. MiR-148a inhibits angiogenesis by targeting ErbB3. J Biomed Res 2011; 25:170-7; PMID:23554686; https://doi.org/10.1016/S1674-8301(11)60022-5.
40. Schoeberl B, Faber AC, Li D, Liang MC, Crosby K, Onsum M, Burenkova O, Pace E, Walton Z, Nie L, et al. An ErbB3 antibody, M121, is active in cancers with ligand-dependent activation. Cancer Res 2010; 70:2485-94; PMID:20215504; https://doi.org/10.1158/0008-5472.CAN-09-3145.
41. Müller D, Trunk G, Sichelstiel A, Zettlitz KA, Quintanilla M, Kontermann RE. Murine endoglin-specific single-chain Fv fragments for the analysis of vascular targeting strategies in mice. J Immunol Methods 2008; 339:90-8; PMID:18790696; https://doi.org/10.1016/j.jim.2008.08.008.
42. Frenzel A, Kügler J, Wilke S, Schirrmann T, Hust M. Construction of human antibody gene libraries and selection of antibodies by phage display. Methods Mol Biol 2014; 1060:215-43; PMID:24037844; https://doi.org/10.1007/978-1-62703-586-6_12.
43. Rondot S, Koch J, Breitling F, Dübel S. A helper phage to improve single-chain antibody presentation in phage display. Nat Biotechnol 2001; 19:75-8; PMID:11135557; https://doi.org/10.1038/83567.
44. Hust M, Meyer T, Voedisch B, Rülker T, Thie H, El-Ghezal A, Kirsch MI, Schütte M, Helmsing S, Meier D, et al. A human scFv antibody generation pipeline for proteome research. J Biotechnol 2011; 152:159-70; PMID:20883731; https://doi.org/10.1016/j.jbiotec.2010.09.945.