Anti-HER3 domain 1 and 3 antibodies reduce tumor growth by hindering HER2/HER3 dimerization and AKT-induced MDM2, XIAP, and fox01 phosphorylation

Neoplasia (United States)

Volumn 15, Issue 3, 2013, Pages 335-347

  Lazrek, Yassamine ^a,b   Dubreuil, Olivier ^b   Garambois, Véronique ^a   Gaborit, Nadège ^a   Larbouret, Christel ^a   le Clorennec, Christophe ^a   Thomas, Gaelle ^a   Leconet, Wilhem ^a   Jarlier, Marta ^c   Pugnière, Martine ^a   Vié, Nadia ^a   Robert, Bruno ^a   Monnet, Céline ^b   Bouayadi, Khalil ^b   Kharrat, Hakim ^b   Mondon, Philippe ^b   Pèlegrin, André ^a   Chardès, Thierry ^a  

^a INSERM   (France)

^b NONE

^c CENTRE VAL D AURELLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; EPITOPE; GLYCOGEN SYNTHASE KINASE 3; PROTEIN KINASE B; PROTEIN MDM2; PROTEIN S6; TRANSCRIPTION FACTOR FKHR; TRASTUZUMAB; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMLA MODEL; APOPTOSIS; ARTICLE; BINDING COMPETITION; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DIMERIZATION; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SURFACE PLASMON RESONANCE; TUMOR GROWTH; TUMOR XENOGRAFT; WESTERN BLOTTING;

EID: 84874616117     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.121960     Document Type: Article

References (52)

1. Yarden Y and Pines G (2012). The ERBB network: at last, cancer therapy meets systems biology. Nat Rev Cancer 12, 553-563.
2. Shi F, Telesco SE, Liu Y, Radhakrishnan R, and Lemmon MA (2010). ErbB3/ HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proc Natl Acad Sci USA 27, 7692-7697.
3. Ben-Kasus T, Schechter B, Lavi S, Yarden Y, and Sela M (2009). Persistent elimination of ErbB-2/HER2-overexpressing tumors using combinations of monoclonal antibodies: relevance of receptor endocytosis. Proc Natl Acad Sci USA 106, 3294-3299.
4. Carraway KL III (2010). E3 ubiquitin ligases in ErbB receptor quantity control. Semin Cell Dev Biol 21, 936-943.
5. Campbell MR, Amin D, and Moasser MM (2010). HER3 comes of age: new insights into its functions and role in signaling, tumor biology, and cancer therapy. Clin Cancer Res 16, 1373-1383.
6. Cook RS, Garrett JT, Sénchez V, Stanford JC, Young C, Chakrabarty A, Dave B, Cook RS, Pao W, McKinely E, et al. (2011). ErbB3 ablation impairs PI3K/ Akt-dependent mammary tumorigenesis. Cancer Res 71, 3941-3951.
7. Friess H, Yamanaka Y, Kobrin MS, Do DA, Büchler MW, and Korc M (1995). Enhanced erbB-3 expression in human pancreatic cancer correlates with tumor progression. Clin Cancer Res 1, 1413-1420.
8. Naidu R, Yadav M, Nair S, and Kutty MK (1998). Expression of c-erbB3 protein in primary breast carcinomas. Br J Cancer 78, 1385-1390.
9. Tanner B, Hasenclever D, Stern K, Schormann W, Bezler M, Hermes M, Brulport M, Bauer A, Schiffer IB, Gebhard S, et al. (2006). ErbB-3 predicts survival in ovarian cancer. J Clin Oncol 24, 4317-4323.
10. Reschke M, Mihic-Probst D, van der Horst EH, Knyazev P, Wild PJ, Hutterer M, Meyer S, Dummer R, Moch H, and Ullrich A (2008). HER3 is a determinant for poor prognosis in melanoma. Clin Cancer Res 14, 5188-5197.
11. Hayashi M, Inokuchi M, Takagi Y, Yamada H, Kojima K, Kumagai J, Kawano T, and Sugihara K (2008). High expression of HER3 is associated with a decreased survival in gastric cancer. Clin Cancer Res 14, 7843-7849.
12. Takikita M, Xie R, Chung JY, Cho H, Ylaya K, Hong SM, Moskaluk CA, and Hewitt SM (2011). Membranous expression of HER3 is associated with a decreased survival in head and neck squamous cell carcinoma. J Transl Med 9, 126-136.
13. Beji A, Horst D, Engel J, Kirchner T, and Ullrich A (2012). Toward the prognostic significance and therapeutic potential of HER3 receptor tyrosine kinase in human colon cancer. Clin Cancer Res 18, 956-968.
14. Ho-Pun-Cheung A, Assenat E, Bascoul-Mollevi C, Bibeau F, Boissière-Michot F, Cellier D, Azria D, Rouanet P, Senesse P, Ychou M, et al. (2011). EGFR and HER3 mRNA expression levels predict distant metastases in locally advanced rectal cancer. Int J Cancer 128, 2938-2946.
15. Narayan M, Wilken JA, Harris LN, Baron AT, Kimbler KD, and Maihle NJ (2009). Trastuzumab-induced HER reprogramming in "resistant" breast carcinoma cells. Cancer Res 69, 2191-2194.
16. Wheeler DL, Huang S, Kruser TJ, Nechrebecki MM, Armstrong EA, Benavente S, Gondi V, Hsu KT, and Harari PM (2008). Mechanisms of acquired resistance to cetuximab: role of HER (ErbB) family members. Oncogene 27, 3944-3956.
17. Yonesaka K, Zejnullahu K, Okamoto I, Satoh T, Cappuzzo F, Souglakos J, Ercan D, Rogers A, Roncalli M, Takeda M, et al. (2011). Activation of ERBB2 signaling causes resistance to the EGFR-directed therapeutic antibody cetuximab. Sci Transl Med 3, 99-86.
18. Arnoletti JP, Buchsbaum DJ, Huang ZQ, Hawkins AE, Khazaeli MB, Kraus MH, and Vickers SM (2004). Mechanisms of resistance to Erbitux (anti-epidermal growth factor receptor) combination therapy in pancreatic adenocarcinoma cells. J Gastrointest Surg 8, 960-969.
19. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, Lindeman N, Gale CM, Zhao X, Christensen J, et al. (2007). MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316, 1039-1043.
20. Garrett JT, Olivares MG, Rinehart C, Granja-Ingram ND, Sénchez V, Chakrabarty A, Dave B, Cook RS, Pao W, McKinely E, et al. (2011). Transcriptional and posttranslational up-regulation of HER3 (ErbB3) compensates for inhibition of the HER2 tyrosine kinase. Proc Natl Acad Sci USA 108, 5021-5026.
21. Chakrabarty A, Sénchez V, Kuba MG, Rinehart C, and Arteaga CL (2011). Feedback upregulation of HER3 (ErbB3) expression and activity attenuates antitumor effect of PI3K inhibitors. Proc Natl Acad Sci USA 109, 2718-2723.
22. Desbois-Mouthon C, Baron A, Blivet-Van Eggelpoël MJ, Fartoux L, Venot C, Bladt F, Housset C, and Rosmorduc O (2009). Insulin-like growth factor-1 receptor inhibition induces a resistance mechanism via the epidermal growth factor receptor/HER3/AKT signaling pathway: rational basis for cotargeting insulin-like growth factor-1 receptor and epidermal growth factor receptor in hepatocellular carcinoma. Clin Cancer Res 15, 5445-5456.
23. Kruser TJ and Wheeler DL (2010). Mechanisms of resistance to HER family targeting antibodies. Exp Cell Res 316, 1083-1100.
24. van der Horst EH, Murgia M, Treder M, and 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.
25. Schoeberl B, Faber AC, Li D, Liang MC, Crosby K, Onsum M, Burenkova O, Pace E, Walton Z, Nie L, et al. (2010). An ErbB3 antibody, MM-121, is active in cancers with ligand-dependent activation. Cancer Res 70, 2485-2494.
26. Sala G, Traini S, D'Egidio M, Vianale G, Rossi C, Piccolo E, Lattanzio R, Piantelli M, Tinari N, Natali PG, 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.
27. Schaefer G, Haber L, Crocker LM, Shia S, Shao L, Dowbenko D, Totpal K, Wong A, Lee CV, Stawicki S, 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.
28. Aurisicchio L, Marra E, Luberto L, Carlomosti F, De Vitis C, Noto A, Gunes Z, Roscilli G, Mesiti G, Mancini R, et al. (2012). Novel anti-ErbB3 monoclonal antibodies show therapeutic efficacy in xenografted and spontaneous mouse tumors. J Cell Physiol 227, 3381-3388.
29. Blackburn E, Zona S, Murphy ML, Brown IR, Chan SK, and Gullick WJ (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 Res Treat 134, 53-59.
30. Sheng Q, Liu X, Fleming E, Yuan K, Piao H, Chen J, Moustafa Z, Thomas RK, Greulich H, Schinzel A, et al. (2010). An activated ErbB3/NRG1 autocrine loop supports in vivo proliferation in ovarian cancer cells. Cancer Cell 17, 298-310.
31. Schmiedel J, Blaukat A, Li S, Knöchel T, and Ferguson KM (2008). Matuzumab binding to EGFR prevents the conformational rearrangement required for dimerization. Cancer Cell 13, 365-373.
32. Gaborit N, Larbouret C, Vallaghe J, Peyrusson F, Bascoul-Mollevi C, Crapez E, Azria D, Chardès T, Poul MA, Mathis G, et al. (2011). Time-resolved fluorescence resonance energy transfer (TR-FRET) to analyze the disruption of EGFR/ HER2 dimers: a new method to evaluate the efficiency of targeted therapy using monoclonal antibodies. J Biol Chem 286, 11337-11345.
33. Mondon P, Souyris N, Douchy L, Crozet F, Bouayadi K, and Kharrat H (2007). Method for generation of human hyperdiversified antibody fragment library. Biotechnol J 2, 76-82.
34. Talavera A, Friemann R, Gómez-Puerta S, Martinez-Fleites C, Garrido G, Rabasa A, López-Requena A, Pupo A, Johansen RF, Sénchez O, et al. (2009). Nimotuzumab, an antitumor antibody that targets the epidermal growth factor receptor, blocks ligand binding while permitting the active receptor conformation. Cancer Res 69, 5851-5859.
35. Li S, Schmitz KR, Jeffrey PD, Wiltzius JJ, Kussie P, and Ferguson KM (2005). Structural basis for inhibition of the epidermal growth factor receptor by cetuximab. Cancer Cell 7, 301-311.
36. Larbouret C, Robert B, Navarro-Teulon I, Thèzenas S, Ladjemi MZ, Morisseau S, Campigna E, Bibeau F, Mach JP, Pèlegrin A, et al. (2007). In vivo therapeutic synergism of anti-epidermal growth factor receptor and anti-HER2 monoclonal antibodies against pancreatic carcinomas. Clin Cancer Res 13, 3356-3362.
37. Zhou BB, Peyton M, He B, Liu C, Girard L, Caudler E, Lo Y, Baribaud F, Mikami I, Reguart N, et al. (2006). Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell 10, 39-50.
38. Farhan H, Schuster C, Klinger M, Weisz E, Waxenecke G, Schuster M, Sexl V, Mudde GC, Freissmuth M, and Kircheis R (2006). Inhibition of xenograft tumor growth and down-regulation of ErbB receptors by an antibody directed against Lewis Y antigen. J Pharmacol Exp Ther 319, 1459-1466.
39. Nakamura H, Takamori S, Fujii T, Ono M, Yamana H, Kuwano M, and Shirouzu K (2005). Cooperative cell-growth inhibition by combination treatment with ZD1839 (Iressa) and trastuzumab (Herceptin) in non-small-cell lung cancer. Cancer Lett 230, 33-46.
40. McDonagh CF, Huhalov A, Harms BD, Adams S, Paragas V, Oyama S, Zhang B, Luus L, Overland R, Nguyen S, et al. (2012). Antitumor activity of a novel bispecific antibody that targets the ErbB2/ErbB3 oncogenic unit and inhibits heregulin-induced activation of ErbB3. Mol Cancer Ther 11, 582-593.
41. Huang SM, Li C, Armstrong EA, Peet CR, Saker J, Amler LC, Sliwkowski MX, and Harari P (2012). Dual targeting of EGFR and HER3 with MEHD7945A overcomes acquired resistance to EGFR inhibitors and radiation. Cancer Res 73, 824-833.
42. Zhang Q, Park E, Kani K, and Landgraf R (2012). Functional isolation of activated and unilaterally phosphorylated heterodimers of ERBB2 and ERBB3 as scaffolds in ligand-dependent signaling. Proc Natl Acad Sci USA 109, 13237-13242.
43. Cho HS and Leahy DJ (2002). Structure of the extracellular region of HER3 reveals an interdomain tether. Science 297, 1330-1333.
44. Aird KM, Ding X, Baras A, Wei J, Morse MA, Clay T, Lyerly HK, and Devi GR (2008). Trastuzumab signaling in ErbB2-overexpressing inflammatory breast cancer correlates with X-linked inhibitor of apoptosis protein expression. Mol Cancer Ther 7, 38-47.
45. Yang JY, Zong CS, Xia W, Yamaguchi H, Ding Q, Xie X, Lang JY, Lai CC, Chang CJ, Huang WC, et al. (2008). ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 10, 138-148.
46. Wu Y, Shang X, Sarkissyan M, Slamon D, and Vadgama JV (2010). FOXO1A is a target for HER2-overexpressing breast tumors. Cancer Res 70, 5475-5485.
47. Chandarlapaty S, Sawai A, Scaltriti M, Rodrik-Outmezgui V, Grbovic-Huezo O, Serra V, Majumder PK, Baselga J, and Rosen N (2011). AKT inhibition relieves feedback suppression of receptor tyrosine kinase expression and activity. Cancer Cell 19, 58-71.
48. Fu W, Ma Q, Chen L, Li P, Zhang M, Ramamoorthy S, Nawaz Z, Shimojima T, Wang H, Yang Y, et al. (2009). MDM2 acts downstream of p53 as an E3 ligase to promote FOXO ubiquitination and degradation. J Biol Chem 284, 13987-14000.
49. Eckelman BP, Salvesen GS, and Scott FL (2006). Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 7, 988-994.
50. Huang S, Benavente S, Armstrong EA, Li C, Wheeler DL, and Harari PM (2011). p53 modulates acquired resistance to EGFR inhibitors and radiation. Cancer Res 71, 7071-7079.
51. Cao Z, Wu X, Yen L, Sweeney C, and Carraway KL III (2007). Neuregulininduced ErbB3 downregulation is mediated by a protein stability cascade involving the E3 ubiquitin ligase Nrdp1. Mol Cell Biol 27, 2180-2188.
52. Qiu XB and Goldberg AL (2002). Nrdp1/FLRF is a ubiquitin ligase promoting ubiquitination and degradation of the epidermal growth factor receptor family member, ErbB3. Proc Natl Acad Sci USA 99, 14843-14848.