An antibody to amphiregulin, an abundant growth factor in patients' fluids, inhibits ovarian tumors

Oncogene

Volumn 35, Issue 4, 2016, Pages 438-447

  Carvalho, S ^a   Lindzen, M ^a   Lauriola, M ^a,e   Shirazi, N ^a   Sinha, S ^a   Abdul Hai, A ^b   Levanon, K ^c   Korach, J ^c   Barshack, I ^c   Cohen, Y ^c   Onn, A ^c   Mills, G ^d   Yarden, Y ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b KAPLAN MEDICAL CENTER   (Israel)

^c SHEBA MEDICAL CENTER   (Israel)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIREGULIN; CISPLATIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GROWTH FACTOR; LIGAND; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY AR30; NEU DIFFERENTIATION FACTOR; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; AREG PROTEIN, HUMAN; CONDITIONED MEDIUM; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR DERIVATIVE; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER PATIENT; CANCER RESISTANCE; CONTROLLED STUDY; DRUG EFFICACY; DRUG TARGETING; FEMALE; HUMAN; HUMAN CELL; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN SECRETION; TUMOR GROWTH; TUMOR XENOGRAFT; UPREGULATION; ANALYSIS; ANIMAL; CONDITIONED MEDIUM; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULARLY TARGETED THERAPY; NUDE MOUSE; OVARIAN NEOPLASMS; PATHOLOGY; PROCEDURES; TUMOR CELL CULTURE; UBIQUITINATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; CULTURE MEDIA, CONDITIONED; EGF FAMILY OF PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE, NUDE; MOLECULAR TARGETED THERAPY; OVARIAN NEOPLASMS; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFORMING GROWTH FACTOR ALPHA; TUMOR CELLS, CULTURED; UBIQUITINATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84955752970     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.93     Document Type: Article

References (52)

1. Witsch E, Sela M, Yarden Y. Roles for growth factors in cancer progression. Physiology (Bethesda) 2010; 25: 85-101.
2. Burgess AW. EGFR family: structure physiology signalling and therapeutic targets. Growth Factors 2008; 26: 263-274.
3. Hynes NE, MacDonald G. ErbB receptors and signaling pathways in cancer. Curr Opin Cell Biol 2009; 21: 177-184.
4. Jones JT, Akita RW, Sliwkowski MX. Binding specificities and affinities of egf domains for ErbB receptors. FEBS Lett 1999; 447: 227-231.
5. Kochupurakkal BS, Harari D, Di-Segni A, Maik-Rachline G, Lyass L, Gur G et al. Epigen, the last ligand of ErbB receptors, reveals intricate relationships between affinity and mitogenicity. J Biol Chem 2005; 280: 8503-8512.
6. Amit I, Citri A, Shay T, Lu Y, Katz M, Zhang F et al. A module of negative feedback regulators defines growth factor signaling. Nat Genet 2007; 39: 503-512.
7. Lazzara MJ, Lauffenburger DA. Quantitative modeling perspectives on the ErbB system of cell regulatory processes. Exp Cell Res 2009; 315: 717-725.
8. Reddy CC, Niyogi SK, Wells A, Wiley HS, Lauffenburger DA. Engineering epidermal growth factor for enhanced mitogenic potency. Nat Biotechnol 1996; 14:1696-1699.
9. Tzahar E, Moyer JD, Waterman H, Barbacci EG, Bao J, Levkowitz G et al. Pathogenic poxviruses reveal viral strategies to exploit the ErbB signaling network. EMBO J 1998; 17: 5948-5963.
10. Wilson KJ, Mill C, Lambert S, Buchman J, Wilson TR, Hernandez-Gordillo V et al. EGFR ligands exhibit functional differences in models of paracrine and autocrine signaling. Growth factors (Chur, Switzerland) 2012; 30: 107-116.
11. Berasain C, Avila MA. Amphiregulin. Semin Cell Dev Biol 2014; 28C: 31-41.
12. Willmarth NE, Ethier SP. Autocrine and juxtacrine effects of amphiregulin on the proliferative, invasive, and migratory properties of normal and neoplastic human mammary epithelial cells. J Biol Chem 2006; 281: 37728-37737.
13. Higginbotham JN, Demory Beckler M, Gephart JD, Franklin JL, Bogatcheva G, Kremers GJ et al. Amphiregulin exosomes increase cancer cell invasion. Curr Biol 2011; 21: 779-786.
14. Sternlicht MD, Sunnarborg SW, Kouros-Mehr H, Yu Y, Lee DC, Werb Z. Mammary ductal morphogenesis requires paracrine activation of stromal EGFR via ADAM17-dependent shedding of epithelial amphiregulin. Development 2005; 132: 3923-3933.
15. Shoyab M, Plowman GD, McDonald VL, Bradley JG, Todaro GJ. Structure and function of human amphiregulin: a member of the epidermal growth factor family. Science 1989; 243: 1074-1076.
16. DeWittA, Iida T, Lam HY, Hill V, Wiley HS, Lauffenburger DA. Affinity regulates spatial range of EGF receptor autocrine ligand binding. Dev Biol 2002; 250: 305-316.
17. Ebner R, Derynck R. Epidermal growth factor and transforming growth factor-alpha: differential intracellular routing and processing of ligand-receptor complexes. Cell Regul 1991; 2: 599-612.
18. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, Langdon WY et al. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev 1998; 12: 3663-3674.
19. Stern KA, Place TL, Lill NL. EGF and amphiregulin differentially regulate Cbl recruitment to endosomes and EGF receptor fate. Biochem J 2008; 410: 585-594.
20. Baldys A, Gooz M, Morinelli TA, Lee MH, Raymond JR Jr, Luttrell LM et al. Essential role of c-Cbl in amphiregulin-induced recycling and signaling of the endogenous epidermal growth factor receptor. Biochemistry 2009; 48: 1462-1473.
21. Roepstorff K, Grandal MV, Henriksen L, Knudsen SL, Lerdrup M, Grovdal L et al. Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic 2009; 10: 1115-1127.
22. Zwang Y, Yarden Y. Systems biology of growth factor-induced receptor endocytosis. Traffic 2009; 10: 349-363.
23. Frosi Y, Anastasi S, Ballaro C, Varsano G, Castellani L, Maspero E et al. A two-tiered mechanism of EGFR inhibition by RALT/MIG6 via kinase suppression and receptor degradation. J Cell Biol 2010; 189: 557-571.
24. Keyse SM. Dual-specificity MAP kinase phosphatases (MKPs) and cancer. Cancer Metastasis Rev 2008; 27: 253-261.
25. Lopez J, Banerjee S, Kaye SB. New developments in the treatment of ovarian cancer - future perspectives. Ann Oncol 2013; 24: x69-x76.
26. Eckstein N, Servan K, Girard L, Cai D, von Jonquieres G, Jaehde U et al. Epidermal growth factor receptor pathway analysis identifies amphiregulin as a key factor for cisplatin resistance of human breast cancer cells. J Biol Chem 2008; 283: 739-750.
27. Arteaga CL, Sliwkowski MX, Osborne CK, Perez EA, Puglisi F, Gianni L. Treatment of HER2-positive breast cancer: current status and future perspectives. Nat Rev Clin Oncol 2012; 9: 16-32.
28. Yarden Y, Pines G. The ERBB network: at last, cancer therapy meets systems biology. Nat Rev Cancer 2012; 12: 553-563.
29. Sheng Q, Liu X, Fleming E, Yuan K, Piao H, Chen J et al. An activated ErbB3/NRG1 autocrine loop supports in vivo proliferation in ovarian cancer cells. Cancer Cell 2010; 17: 298-310.
30. Gui T, Shen K. The epidermal growth factor receptor as a therapeutic target in epithelial ovarian cancer. Cancer Epidemiol 2012; 36: 490-496.
31. Siwak DR, Carey M, Hennessy BT, Nguyen CT, McGahren Murray MJ, Nolden L et al. Targeting the epidermal growth factor receptor in epithelial ovarian cancer: current knowledge and future challenges. J Oncol 2010; 2010: 568938.
32. Murphy M, Stordal B. Erlotinib or gefitinib for the treatment of relapsed platinum pretreated non-small cell lung cancer and ovarian cancer: a systematic review. Drug Resist Updat 2011; 14: 177-190.
33. Lassus H, Sihto H, Leminen A, Joensuu H, Isola J, Nupponen NN et al. Gene amplification, mutation, and protein expression of EGFR and mutations of ERBB2 in serous ovarian carcinoma. J Mol Med (Berl) 2006; 84: 671-681.
34. Brustmann H. Epidermal growth factor receptor expression in serous ovarian carcinoma: an immunohistochemical study with galectin-3 and cyclin D1 and outcome. Int J Gynecol Pathol 2008; 27: 380-389.
35. Lindzen M, Lavi S, Leitner O, Yarden Y. Tailored cancer immunotherapy using combinations of chemotherapy and a mixture of antibodies against EGF-receptor ligands. Proc Natl Acad Sci USA 2010; 107: 12559-12563.
36. Van Zoelen EJ, Stortelers C, Lenferink AE, Van de Poll ML. The EGF domain: requirements for binding to receptors of the ErbB family. Vitam Horm 2000; 59: 99-131.
37. Sato S, Drake AW, Tsuji I, Fan J. A potent anti-HB-EGF monoclonal antibody inhibits cancer cell proliferation and multiple angiogenic activities of HB-EGF. PLoS ONE 2012; 7: e51964.
38. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
39. Sporn MB, Todaro GJ. Autocrine secretion and malignant transformation of cells. N Engl J Med 1980; 303: 878-880.
40. Normanno N, Bianco C, Strizzi L, Mancino M, Maiello MR, De Luca A et al. The ErbB receptors and their ligands in cancer: an overview. Curr Drug Targets 2005; 6: 243-257.
41. Esposito CL, Passaro D, Longobardo I, Condorelli G, Marotta P, Affuso A et al. A neutralizing RNA aptamer against EGFR causes selective apoptotic cell death. PLoS ONE 2011; 6: e24071.
42. Pedersen MW, Jacobsen HJ, Koefoed K, Hey A, Pyke C, Haurum JS et al. Sym004: a novel synergistic anti-epidermal growth factor receptor antibody mixture with superior anticancer efficacy. Cancer Res 2010; 70: 588-597.
43. Friedman LM, Rinon A, Schechter B, Lyass L, Lavi S, Bacus SS et al. Synergistic down-regulation of receptor tyrosine kinases by combinations of mAbs: implications for cancer immunotherapy. Proc Natl Acad Sci USA 2005; 102: 1915-1920.
44. Lindzen M, Carvalho S, Starr A, Ben-Chetrit N, Pradeep CR, Kostler WJ et al. A recombinant decoy comprising EGFR and ErbB-4 inhibits tumor growth and metastasis. Oncogene 2012; 31: 3505-3515.
45. Khambata-Ford S, Garrett CR, Meropol NJ, Basik M, Harbison CT, Wu S et al. Expression of epiregulin and amphiregulin and K-ras mutation status predict disease control in metastatic colorectal cancer patients treated with cetuximab. J Clin Oncol 2007; 25: 3230-3237.
46. Yonesaka K, Zejnullahu K, Lindeman N, Homes AJ, Jackman DM, Zhao F et al. Autocrine production of amphiregulin predicts sensitivity to both gefitinib and cetuximab in EGFR wild-type cancers. Clin Cancer Res 2008; 14: 6963-6973.
47. Ciarloni L, Mallepell S, Brisken C. Amphiregulin is an essential mediator of estrogen receptor alpha function in mammary gland development. Proc Natl Acad Sci USA 2007; 104: 5455-5460.
48. Hsu D, Fukata M, Hernandez YG, Sotolongo JP, Goo T, Maki J et al. Toll-like receptor 4 differentially regulates epidermal growth factor-related growth factors in response to intestinal mucosal injury. Lab Invest 2010; 90: 1295-1305.
49. Panupinthu N, Yu S, Zhang D, Zhang F, Gagea M, Lu Y et al. Self-reinforcing loop of amphiregulin and Y-box binding protein-1 contributes to poor outcomes in ovarian cancer. Oncogene 2013; 33: 2846-2856.
50. Sauer L, Gitenay D, Vo C, Baron VT. Mutant p53 initiates a feedback loop that involves Egr-1/EGF receptor/ERK in prostate cancer cells. Oncogene 2010; 29: 2628-2637.
51. Bast RC Jr., Hennessy B, Mills GB. The biology of ovarian cancer: new opportunities for translation. Nat Rev Cancer 2009; 9: 415-428.
52. Blivet-Van Eggelpoel M-J, Chettouh H, Fartoux L, Aoudjehane L, Barbu V, Rey C et al. Epidermal growth factor receptor and HER-3 restrict cell response to sorafenib in hepatocellular carcinoma cells. J Hepatol 2012; 57: 108-115.