The Role of ErbB3 and its binding partners in breast cancer progression and resistance to hormone and tyrosine kinase directed therapies

Journal of Mammary Gland Biology and Neoplasia

Volumn 13, Issue 2, 2008, Pages 225-233

  Hamburger, Anne W ^a  

^a UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

Author keywords

Ebp1; ErbB3; Gefitinib; Nrdp1; Tamoxifen

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ANTIESTROGEN; CANERTINIB; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 3 BINDING PROTEIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; ESTROGEN RECEPTOR; GEFITINIB; LAPATINIB; MEMBRANE PROTEIN; NEU DIFFERENTIATION FACTOR; NEUREGULIN RECEPTOR DEGRADATION PROTEIN 1; PROTEIN KINASE B; PROTEIN LRIG1; PROTEIN TYROSINE KINASE INHIBITOR; RING FINGER PROTEIN; TAMOXIFEN; TRASTUZUMAB;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER HORMONE THERAPY; CANCER INHIBITION; CANCER RESISTANCE; CLINICAL TRIAL; DRUG SENSITIVITY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; NONHUMAN; PROGNOSIS; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; PROTEIN TARGETING; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BREAST NEOPLASMS; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; ESTROGEN ANTAGONISTS; FEMALE; HUMANS; MEMBRANE GLYCOPROTEINS; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, ERBB-3; RNA-BINDING PROTEINS; TAMOXIFEN; UBIQUITIN-PROTEIN LIGASES;

EID: 44149128380     PISSN: 10833021     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10911-008-9077-5     Document Type: Article

References (81)

1. Holbro T, Civenni G, Hynes NE. The ErbB receptors and their role in cancer progression. Exp Cell Res. 2003;284(1):99-110.
2. Yarden Y. The EGFR family and its ligands in human cancer, signalling mechanisms and therapeutic opportunities. Eur J Cancer. 2001;37(Suppl 4):S3-S8.
3. Kraus MH, Issing W, Miki T, Popescu NC, Aaronson SA. Isolation and characterization of ERBB3, a third member of the ERBB/epidermal growth factor receptor family: Evidence for overexpression in a subset of human mammary tumors. Proc Natl Acad Sci USA. 1989;86(23):9193-7.
4. Fedi P, Pierce JH, di Fiore PP, Kraus MH. Efficient coupling with phosphatidylinositol 3-kinase, but not phospholipase C gamma or GTPase-activating protein, distinguishes ErbB-3 signaling from that of other ErbB/EGFR family members. Mol Cell Biol. 1994;14(1):492-500.
5. Hellyer NJ, Cheng K, Koland JG. ErbB3 (HER3) interaction with the p85 regulatory subunit of phosphoinositide 3-kinase. Biochem J. 1998;333(Pt 3):757-63.
6. Soltoff SP, Carraway KL III, Prigent SA, Gullick WG, Cantley LC. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol Cell Biol. 1994;14(6):3550-8.
7. Schulze WX, Deng L, Mann M. Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol Syst Biol. 2005;1:2005.
8. Luo J, Manning BD, Cantley LC. Targeting the PI3K-Akt pathway in human cancer: Rationale and promise. Cancer Cell. 2003;4(4):257-62.
9. Hynes NE, Lane HA. ERBB receptors and cancer: The complexity of targeted inhibitors. Nat Rev Cancer. 2005;5(5):341-54.
10. Lemoine NR, Barnes DM, Hollywood DP, Hughes CM, Smith P, Dublin E, et al. Expression of the ERBB3 gene product in breast cancer. Br J Cancer. 1992;66(6):1116-21.
11. Naidu R, Yadav M, Nair S, Kutty MK. Expression of c-erbB3 protein in primary breast carcinomas. Br J Cancer. 1998;78(10):1385-90.
12. Travis A, Pinder SE, Robertson JF, Bell JA, Wencyk P, Gullick WJ, et al. C-erbB-3 in human breast carcinoma: Expression and relation to prognosis and established prognostic indicators. Br J Cancer. 1996;74(2):229-33.
13. Gasparini G, Gullick WJ, Maluta S, Dalla PP, Caffo O, Leonardi E, et al. c-erbB-3 and c-erbB-2 protein expression in node-negative breast carcinoma - an immunocytochemical study. Eur J Cancer. 1994;30A(1):16-22.
14. Bieche I, Onody P, Tozlu S, Driouch K, Vidaud M, Lidereau R. Prognostic value of ERBB family mRNA expression in breast carcinomas. Int J Cancer. 2003;106(5):758-65.
15. Pawlowski V, Revillion F, Hebbar M, Hornez L, Peyrat JP. Prognostic value of the type I growth factor receptors in a large series of human primary breast cancers quantified with a real-time reverse transcription-polymerase chain reaction assay. Clin Cancer Res. 2000;6(11):4217-25.
16. Barnes NL, Khavari S, Boland GP, Cramer A, Knox WF, Bundred NJ. Absence of HER4 expression predicts recurrence of ductal carcinoma in situ of the breast. Clin Cancer Res. 2005;11(6):2163-8.
17. Quinn CM, Ostrowski JL, Lane SA, Loney DP, Teasdale J, Benson FA. c-erbB-3 protein expression in human breast cancer: Comparison with other tumour variables and survival. Histopathology. 1994;25(3):247-52.
18. Witton CJ, Reeves JR, Going JJ, Cooke TG, Bartlett JM. Expression of the HER1-4 family of receptor tyrosine kinases in breast cancer. J Pathol. 2003;200(3):290-7.
19. Wiseman SM, Makretsov N, Nielsen TO, Gilks B, Yorida E, Cheang M, et al. Coexpression of the type 1 growth factor receptor family members HER-1, HER-2, and HER-3 has a synergistic negative prognostic effect on breast carcinoma survival. Cancer. 2005;103(9):1770-7.
20. Kim HH, Vijapurkar U, Hellyer NJ, Bravo D, Koland JG. Signal transduction by epidermal growth factor and heregulin via the kinase-deficient ErbB3 protein. Biochem J. 1998;334(Pt 1):189-95.
21. Pinkas-Kramarski R, Soussan L, Waterman H, Levkowitz G, Alroy I, Klapper L, et al. Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. EMBO J. 1996;15(10):2452-67.
22. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF III, Hynes NE. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci USA. 2003;100(15):8933-8.
23. van der Horst EH, Murgia M, Treder M, Ullrich A. Anti-HER-3 MAbs inhibit HER-3-mediated signaling in breast cancer cell lines resistant to anti-HER-2 antibodies. Int J Cancer. 2005;115(4):519-27.
24. Chen CH, Chernis GA, Hoang VQ, Landgraf R. Inhibition of heregulin signaling by an aptamer that preferentially binds to the oligomeric form of human epidermal growth factor receptor-3. Proc Natl Acad Sci USA. 2003;100(16):9226-31.
25. Lund CV, Popkov M, Magnenat L, Barbas CF III. Zinc finger transcription factors designed for bispecific coregulation of ErbB2 and ErbB3 receptors: Insights into ErbB receptor biology. Mol Cell Biol. 2005;25(20):9082-91.
26. Scott GK, Goga A, Bhaumik D, Berger CE, Sullivan CS, Benz CC. Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem. 2007;282(2):1479-86.
27. Clarke R, Leonessa F, Welch JN, Skaar TC. Cellular and molecular pharmacology of antiestrogen action and resistance. Pharmacol Rev. 2001;53(1):25-71.
28. Mouridsen HT, Rose C, Brodie AH, Smith IE. Challenges in the endocrine management of breast cancer. Breast. 2003;12(Suppl 2):S2-19.
29. Newby JC, Johnston SR, Smith IE, Dowsett M. Expression of epidermal growth factor receptor and c-erbB2 during the development of tamoxifen resistance in human breast cancer. Clin Cancer Res. 1997;3(9):1643-51.
30. Shou J, Massarweh S, Osborne CK, Wakeling AE, Ali S, Weiss H, et al. Mechanisms of tamoxifen resistance: Increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J Natl Cancer Inst. 2004;96(12):926-35.
31. Pietras RJ, Arboleda J, Reese DM, Wongvipat N, Pegram MD, Ramos L, et al. HER-2 tyrosine kinase pathway targets estrogen receptor and promotes hormone-independent growth in human breast cancer cells. Oncogene. 1995;10(12):2435-46.
32. Tang CK, Perez C, Grunt T, Waibel C, Cho C, Lupu R. Involvement of heregulin-beta2 in the acquisition of the hormone-independent phenotype of breast cancer cells. Cancer Res. 1996;56(14):3350-8.
33. Benz CC, Scott GK, Sarup JC, Johnson RM, Tripathy D, Coronado E, et al. Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu. Breast Cancer Res Treat. 1992;24(2):85-95.
34. Tovey S, Dunne B, Witton CJ, Forsyth A, Cooke TG, Bartlett JM. Can molecular markers predict when to implement treatment with aromatase inhibitors in invasive breast cancer? Clin Cancer Res. 2005;11(13):4835-42.
35. Liu B, Ordonez-Ercan D, Fan Z, Edgerton SM, Yang X, Thor AD. Downregulation of erbB3 abrogates erbB2-mediated tamoxifen resistance in breast cancer cells. Int J Cancer. 2007;120(9):1874-82.
36. deGraffenried LA, Friedrichs WE, Russell DH, Donzis EJ, Middleton AK, Silva JM, et al. Inhibition of mTOR activity restores tamoxifen response in breast cancer cells with aberrant Akt Activity. Clin Cancer Res. 2004;10(23):8059-67.
37. Jordan NJ, Gee JM, Barrow D, Wakeling AE, Nicholson RI. Increased constitutive activity of PKB/Akt in tamoxifen resistant breast cancer MCF-7 cells. Breast Cancer Res Treat. 2004;87(2):167-80.
38. Clark AS, West K, Streicher S, Dennis PA. Constitutive and inducible Akt activity promotes resistance to chemotherapy, trastuzumab, or tamoxifen in breast cancer cells. Mol Cancer Ther. 2002;1(9):707-17.
39. Agrawal A, Gutteridge E, Gee JM, Nicholson RI, Robertson JF. Overview of tyrosine kinase inhibitors in clinical breast cancer. Endocr Relat Cancer. 2005;12(Suppl 1):S135-S144.
40. Sergina NV, Rausch M, Wang D, Blair J, Hann B, Shokat KM, et al. Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature. 2007;445(7126):437-41.
41. Menendez JA, Lupu R. Transphosphorylation of kinase-dead HER3 and breast cancer progression: A new standpoint or an old concept revisited? Breast Cancer Res. 2007;9(5):111.
42. Hsieh AC, Moasser MM. Targeting HER proteins in cancer therapy and the role of the non-target HER3. Br J Cancer. 2007;97(4):453-7.
43. Motoyama AB, Hynes NE, Lane HA. The efficacy of ErbB receptor-targeted anticancer therapeutics is influenced by the availability of epidermal growth factor-related peptides. Cancer Res. 2002;62(11):3151-8.
44. Hutcheson IR, Knowlden JM, Hiscox SE, Barrow D, Gee JM, Robertson JF, et al. Heregulin beta1 drives gefitinib-resistant growth and invasion in tamoxifen-resistant MCF-7 breast cancer cells. Breast Cancer Res. 2007;9(4):R50.
45. Ferrer-Soler L, Vazquez-Martin A, Brunet J, Menendez JA, De LR, Colomer R. An update of the mechanisms of resistance to EGFR-tyrosine kinase inhibitors in breast cancer: Gefitinib (Iressa) -induced changes in the expression and nucleo-cytoplasmic trafficking of HER-ligands (Review). Int J Mol Med. 2007;20(1):3-10.
46. Offterdinger M, Schofer C, Weipoltshammer K, Grunt TW. c-erbB-3: A nuclear protein in mammary epithelial cells. J Cell Biol. 2002;157(6):929-39.
47. Arteaga CL. Can trastuzumab be effective against tumors with low HER2/ Neu (ErbB2) receptors? J Clin Oncol. 2006;24(23):3722-5.
48. Diamonti AJ, Guy PM, Ivanof C, Wong K, Sweeney C, Carraway KL III. An RBCC protein implicated in maintenance of steady-state neuregulin receptor levels. Proc Natl Acad Sci USA. 2002;99(5):2866-71.
49. Qiu XB, Goldberg AL. Nrdp1/FLRF is a ubiquitin ligase promoting ubiquitination and degradation of the epidermal growth factor receptor family member, ErbB3. Proc Natl Acad Sci USA. 2002;99(23):14843-8.
50. Bouyain S, Leahy DJ. Structure-based mutagenesis of the substrate-recognition domain of Nrdp1/FLRF identifies the binding site for the receptor tyrosine kinase ErbB3. Protein Sci. 2007;16(4):654-61.
51. Wu X, Yen L, Irwin L, Sweeney C, Carraway KL III. Stabilization of the E3 ubiquitin ligase Nrdp1 by the deubiquitinating enzyme USP8. Mol Cell Biol. 2004;24(17):7748-57.
52. Cao Z, Wu X, Yen L, Sweeney C, Carraway KL III. Neuregulin-induced ErbB3 downregulation is mediated by a protein stability cascade involving the E3 ubiquitin ligase Nrdp1. Mol Cell Biol. 2007;27(6):2180-8.
53. Yen L, Cao Z, Wu X, Ingalla ER, Baron C, Young LJ, et al. Loss of Nrdp1 enhances ErbB2/ErbB3-dependent breast tumor cell growth. Cancer Res. 2006;66(23):11279-86.
54. Maitra A, Wistuba II, Washington C, Virmani AK, Ashfaq R, Milchgrub S, et al. High-resolution chromosome 3p allelotyping of breast carcinomas and precursor lesions demonstrates frequent loss of heterozygosity and a discontinuous pattern of allele loss. Am J Pathol. 2001;159(1):119-30.
55. Sweeney C, Miller JK, Shattuck DL, Carraway KL III. ErbB receptor negative regulatory mechanisms: Implications in cancer. J Mammary Gland Biol Neoplasia. 2006;11(1):89-99.
56. Ljuslinder I, Malmer B, Golovleva I, Thomasson M, Grankvist K, Hockenstrom T, et al. Increased copy number at 3p14 in breast cancer. Breast Cancer Res. 2005;7(5):R719-R727.
57. Laederich MB, Funes-Duran M, Yen L, Ingalla E, Wu X, Carraway KL III, et al. The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases. J Biol Chem. 2004;279(45):47050-6.
58. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 2007;316(5827):1039-43.
59. Shattuck DL, Miller JK, Laederich M, Funes M, Petersen H, Carraway KL III, et al. LRIG1 is a novel negative regulator of the Met receptor and opposes Met and Her2 synergy. Mol Cell Biol. 2007;27(5):1934-46.
60. Yoo JY, Wang XW, Rishi AK, Lessor T, Xia XM, Gustafson TA, et al. Interaction of the PA2G4 (EBP1) protein with ErbB-3 and regulation of this binding by heregulin. Br J Cancer. 2000;82(3):683-90.
61. Radomski N, Jost E. Molecular cloning of a murine cDNA encoding a novel protein, p38-2G4, which varies with the cell cycle. Exp Cell Res. 1995;220(2):434-45.
62. Xia X, Lessor TJ, Zhang Y, Woodford N, Hamburger AW. Analysis of the expression pattern of Ebp1, an ErbB-3-binding protein. Biochem Biophys Res Commun. 2001;289(1):240-4.
63. Horvath BM, Magyar Z, Zhang Y, Hamburger AW, Bako L, Visser RG, et al. EBP1 regulates organ size through cell growth and proliferation in plants. EMBO J. 2006;25(20):4909-20.
64. Lessor TJ, Yoo JY, Xia X, Woodford N, Hamburger AW. Ectopic expression of the ErbB-3 binding protein ebp1 inhibits growth and induces differentiation of human breast cancer cell lines. J Cell Physiol. 2000;183(3):321-9.
65. Lessor TJ, Hamburger AW. Regulation of the ErbB3 binding protein Ebp1 by protein kinase C. Mol Cell Endocrinol. 2001;175(1-2):185-91.
66. Liu Z, Ahn JY, Liu X, Ye K. Ebp1 isoforms distinctively regulate cell survival and differentiation. Proc Natl Acad Sci USA. 2006;103(29):10917-22.
67. Xia X, Cheng A, Lessor T, Zhang Y, Hamburger AW. Ebp1, an ErbB-3 binding protein, interacts with Rb and affects Rb transcriptional regulation. J Cell Physiol. 2001;187(2):209-17.
68. Zhang YX, Woodford N, Xia XM, Hamburger AW. Repression of E2F1-mediated transcription by the ErbB3 binding protein Ebp1 involves histone deacetylases. Nucleic Acids Res. 2003;31(8):2168-77.
69. Zhang Y, Akinmade D, Hamburger AW. The ErbB3 binding protein Ebp1 interacts with Sin3A to repress E2F1 and AR-mediated transcription. Nucleic Acids Res. 2005;33(18):6024-33.
70. Zhang Y, Hamburger AW. Heregulin regulates the ability of the ErbB3-binding protein Ebp1 to bind E2F promoter elements and repress E2F-mediated transcription. J Biol Chem. 2004;279(25):26126-33.
71. Akinmade D, Lee M, Zhang Y, Hamburger AW. Ebp1-mediated inhibition of cell growth requires serine 363 phosphorylation. Int J Oncol. 2007;31(4):851-8.
72. Squatrito M, Mancino M, Donzelli M, Areces LB, Draetta GF. EBP1 is a nucleolar growth-regulating protein that is part of pre-ribosomal ribonucleoprotein complexes. Oncogene 2004;23(25):4454-65.
73. Squatrito M, Mancino M, Sala L, Draetta GF. Ebp1 is a dsRNA-binding protein associated with ribosomes that modulates eIF2alpha phosphorylation. Biochem Biophys Res Commun. 2006;344(3):859-68.
74. Monie TP, Perrin AJ, Birtley JR, Sweeney TR, Karakasiliotis I, Chaudhry Y, et al. Structural insights into the transcriptional and translational roles of Ebp1. EMBO J 2007;26:3936-44.
75. Kowalinski E, Bange G, Bradatsch B, Hurt E, Wild K, Sinning I. The crystal structure of Ebp1 reveals a methionine aminopeptidase fold as binding platform for multiple interactions. FEBS Lett. 2007;581(23):4450-4.
76. Vadlamudi RK, Adam L, Wang RA, Mandal M, Nguyen D, Sahin A, et al. Regulatable expression of p21-activated kinase-1 promotes anchorage-independent growth and abnormal organization of mitotic spindles in human epithelial breast cancer cells. J Biol Chem. 2000;275(46):36238-44.
77. Rayala SK, Talukder AH, Balasenthil S, Tharakan R, Barnes CJ, Wang RA, et al. P21-activated kinase 1 regulation of estrogen receptor-alpha activation involves serine 305 activation linked with serine 118 phosphorylation. Cancer Res. 2006;66(3):1694-701.
78. Holm C, Rayala S, Jirstrom K, Stal O, Kumar R, Landberg G. Association between Pak1 expression and subcellular localization and tamoxifen resistance in breast cancer patients. J Natl Cancer Inst. 2006;98(10):671-80.
79. Akinmade D, Talukder AH, Zhang Y, Luo WM, Kumar R, Hamburger AW. Phosphorylation of the ErbB3 binding protein Ebp1 by p21-activated kinase 1 in breast cancer cells. Br J Cancer 2008, in press.
80. Ou K, Kesuma D, Ganesan K, Yu K, Soon SY, Lee SY, et al. Quantitative profiling of drug-associated proteomic alterations by combined 2-nitrobenzenesulfenyl chloride (NBS) isotope labeling and 2DE/MS identification. J Proteome Res. 2006;5(9):2194-206.
81. Kumar R, Gururaj AE, Barnes CJ. p21-activated kinases in cancer. Nat Rev Cancer. 2006;6(6):459-71.