Role of erbB3 receptors in cancer therapeutic resistance

Acta Biochimica et Biophysica Sinica

Volumn 46, Issue 3, 2014, Pages 190-198

  Lee, Youngseok ^a,b   Ma, Jian ^c   Lyu, Hui ^a   Huang, Jingcao ^a   Kim, Aeree ^b   Liu, Bolin ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Korea University College of Medicine   (South Korea)

^c CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

cancer; cell signaling; erbB3; receptor tyrosine kinase; resistance

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; PROTEIN TYROSINE KINASE;

BIOLOGICAL MODEL; CELL SIGNALING; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; ERBB3; HUMAN; METABOLISM; METHODOLOGY; MOLECULARLY TARGETED THERAPY; NEOPLASM; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; RESISTANCE; REVIEW; SIGNAL TRANSDUCTION;

CANCER; CELL SIGNALING; ERBB3; RECEPTOR TYROSINE KINASE; RESISTANCE;

DRUG RESISTANCE, NEOPLASM; HUMANS; MODELS, BIOLOGICAL; MOLECULAR TARGETED THERAPY; NEOPLASMS; PHOSPHORYLATION; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION;

EID: 84897743013     PISSN: 16729145     EISSN: 17457270     Source Type: Journal    
DOI: 10.1093/abbs/gmt150     Document Type: Review

References (114)

1. Baselga J and Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer 2009, 9: 463-475.
2. Hynes NE and MacDonald G. ErbB receptors and signaling pathways in cancer. Curr Opin Cell Biol 2009, 21: 177-184.
3. Hynes NE and Lane HA. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 2005, 5: 341-354.
4. DeFazio A, Chiew YE, Sini RL, Janes PW and Sutherland RL. Expression of c-erbB receptors, heregulin and oestrogen receptor in human breast cell lines. Int J Cancer 2000, 87: 487-498.
5. Olayioye MA, Neve RM, Lane HA and Hynes NE. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J 2000, 19: 3159.
6. Ogiso H, Ishitani R, Nureki O, Fukai S, Yamanaka M, Kim JH and Saito K, et al. Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains. Cell 2002, 110: 775-787.
7. Ferguson KM, Berger MB, Mendrola JM, Cho HS, Leahy DJ and Lemmon MA. EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol Cell 2003, 11: 507-517.
8. Burgess AW, Cho HS, Eigenbrot C, Ferguson KM, Garrett TP, Leahy DJ and Lemmon MA, et al. An open-And-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol Cell 2003, 12: 541-552.
9. Cho HS and Leahy DJ. Structure of the extracellular region of HER3 reveals an interdomain tether. Science 2002, 297: 1330-1333.
10. Graus-Porta D, Beerli RR, Daly JM and Hynes NE. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 1997, 16: 1647-1655.
11. Mendelsohn J and Baselga J. Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol 2003, 21: 2787-2799.
12. Boudeau J, Miranda-Saavedra D, Barton GJ and Alessi DR. Emerging roles of pseudokinases. Trends Cell Biol 2006, 16: 443-452.
13. Citri A, Skaria KB and Yarden Y. The deaf and the dumb: the biology of ErbB-2 and ErbB-3. Exp Cell Res 2003, 284: 54-65.
14. Shi F, Telesco SE, Liu Y, Radhakrishnan R and Lemmon MA. ErbB3/ HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proc Natl Acad Sci USA 2010, 107: 7692-7697.
15. Schulze WX, Deng L and Mann M. Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol Syst Biol 2005, 1: 2005.0008.
16. Amin DN, Campbell MR and 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: 944-950.
17. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF, III and 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: 8933-8938.
18. Lee-Hoeflich ST, Crocker L, Yao E, Pham T, Munroe X, Hoeflich KP and Sliwkowski MX, et al. A central role for HER3 in HER2-Amplified breast cancer: implications for targeted therapy. Cancer Res 2008, 68: 5878-5887.
19. Jathal MK, Chen L, Mudryj M and Ghosh PM. Targeting ErbB3: the new RTK(id) on the prostate cancer block. Immunol Endocr Metab Agents Med Chem 2011, 11: 131-149.
20. Mills GB and Yarden Y. The rebirth of a phoenix: ovarian cancers are addicted to ErbB-3. Cancer Cell 2010, 17: 217-218.
21. Sheng Q, Liu X, Fleming E, Yuan K, Piao H, Chen J and Moustafa Z, et al. An activated ErbB3/NRG1 autocrine loop supports in vivo proliferation in ovarian cancer cells. Cancer Cell 2010, 17: 298-310.
22. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO and Lindeman N, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007, 316: 1039-1043.
23. Huang S, Li C, Armstrong EA, Peet CR, Saker J, Amler LC and Sliwkowski MX, et al. Dual targeting of EGFR and HER3 with MEHD7945A overcomes acquired resistance to EGFR inhibitors and radiation. Cancer Res 2013, 73: 824-833.
24. Aurisicchio L, Marra E, Luberto L, Carlomosti F, De Vitis C, Noto A and Gunes Z, et al. Novel anti-ErbB3 monoclonal antibodies show therapeutic efficacy in xenografted and spontaneous mouse tumors. J Cell Physiol 2012, 227: 3381-3388.
25. Aurisicchio L, Marra E, Roscilli G, Mancini R and Ciliberto G. The promise of anti-ErbB3 monoclonals as new cancer therapeutics. Oncotarget 2012, 3: 744-758.
26. Jiang N, Saba NF and Chen ZG. Advances in targeting HER3 as an anticancer therapy. Chemother Res Pract 2012, 2012: 817304.
27. Berger MB, Mendrola JM and Lemmon MA. ErbB3/HER3 does not homodimerize upon neuregulin binding at the cell surface. FEBS Lett 2004, 569: 332-336.
28. Plowman GD, Whitney GS, Neubauer MG, Green JM, McDonald VL, Todaro GJ and Shoyab M. Molecular cloning and expression of an additional epidermal growth factor receptor-related gene. Proc Natl Acad Sci USA 1990, 87: 4905-4909.
29. Alimandi M, Romano A, CuriaMC, Muraro R, Fedi P, Aaronson SA and Di Fiore PP, et al. Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas. Oncogene 1995, 10: 1813.
30. Hsieh A and Moasser M. Targeting HER proteins in cancer therapy and the role of the non-Target HER3. Br J Cancer 2007, 97: 453-457.
31. Wallasch C, Weiss F, Niederfellner G, Jallal B, Issing W and Ullrich A. Heregulin-dependent regulation of HER2/neu oncogenic signaling by heterodimerization with HER3. EMBO J 1995, 14: 4267-4275.
32. Chakrabarty A, Rexer BN, Wang SE, Cook RS, Engelman JA and Arteaga C. H1047R phosphatidylinositol 3-kinase mutant enhances HER2-mediated transformation by heregulin production and activation of HER3. Oncogene 2010, 29: 5193-5203.
33. Liu B, Ordonez-Ercan D, Fan Z, Edgerton SM, Yang X and Thor AD. Downregulation of erbB3 abrogates erbB2-mediated tamoxifen resistance in breast cancer cells. Int J Cancer 2007, 120: 1874-1882.
34. Liu B, Ordonez-Ercan D, Fan Z, Huang X, Edgerton SM, Yang X and Thor AD. Estrogenic promotion of ErbB2 tyrosine kinase activity in mammary tumor cells requires activation of ErbB3 signaling. Mol Cancer Res 2009, 7: 1882-1892.
35. Beji A, Horst D, Engel J, Kirchner T and Ullrich A. Toward the prognostic significance and therapeutic potential of HER3 receptor tyrosine kinase in human colon cancer. Clin Cancer Res 2012, 18: 956-968.
36. Maurer CA, Friess H, Kretschmann B, Zimmermann A, Stauffer A, Baer HU and Korc M, et al. Increased expression of erbB3 in colorectal cancer is associated with concomitant increase in the level of erbB2. Hum Pathol 1998, 29: 771-777.
37. Jaiswal BS, Kljavin NM, Stawiski EW, Chan E, Parikh C, Durinck S and Chaudhuri S, et al. Oncogenic ERBB3 mutations in human cancers. Cancer Cell 2013, 23: 603-617.
38. Grupka NL, Lear-Kaul KC, Kleinschmidt-DeMasters BK and Singh M. Epidermal growth factor receptor status in breast cancer metastases to the central nervous system. Comparison with HER-2/neu status. Arch Pathol Lab Med 2004, 128: 974-979.
39. Bieche I, Onody P, Tozlu S, Driouch K, Vidaud M and Lidereau R. Prognostic value of ERBB family mRNA expression in breast carcinomas. Int J Cancer 2003, 106: 758-765.
40. deFazio A, Chiew YE, Sini RL, Janes PW and Sutherland RL. Expression of c-erbB receptors, heregulin and oestrogen receptor in human breast cell lines. Int J Cancer 2000, 87: 487-498.
41. Kim A, Liu B, Ordonez-Ercan D, Alvarez KM, Jones LD, McKimmey C and Edgerton SM, et al. Functional interaction between mouse erbB3 and wild-Type rat c-neu in transgenic mouse mammary tumor cells. Breast Cancer Res 2005, 7: R708-R718.
42. Siegel PM, Ryan ED, Cardiff RD and Muller WJ. Elevated expression of activated forms of Neu/ErbB-2 and ErbB-3 are involved in the induction of mammary tumors in transgenic mice: implications for human breast cancer. EMBO J 1999, 18: 2149-2164.
43. Liles JS, Arnoletti JP, Tzeng CW, Howard JH, Kossenkov AV, Kulesza P and Heslin MJ, et al. ErbB3 expression promotes tumorigenesis in pancreatic adenocarcinoma. Cancer Biol Ther 2010, 10: 555-563.
44. Reschke M, Mihic-Probst D, van der Horst EH, Knyazev P, Wild PJ, Hutterer M and Meyer S, et al. HER3 is a determinant for poor prognosis in melanoma. Clin Cancer Res 2008, 14: 5188-5197.
45. Barnes NL, Khavari S, Boland GP, Cramer A, Knox WF and Bundred NJ. Absence of HER4 expression predicts recurrence of ductal carcinoma in situ of the breast. Clin Cancer Res 2005, 11: 2163-2168.
46. Naidu R, Yadav M, Nair S and Kutty M. Expression of c-erbB3 protein in primary breast carcinomas. Br J Cancer 1998, 78: 1385-1390.
47. Quinn C, Ostrowski J, Lane S, Loney D, Teasdale J and Benson E. c-erbB-3 protein expression in human breast cancer: comparison with other tumour variables and survival. Histopathology 1994, 25: 247-252.
48. Lemoine N, Barnes D, Hollywood D, Hughes C, Smith P, Dublin E and Prigent S, et al. Expression of the ERBB3 gene product in breast cancer. Br J Cancer 1992, 66: 1116-1121.
49. Travis A, Pinder S, Robertson J, Bell J, Wencyk P, Gullick W and Nicholson R, et al. C-erbB-3 in human breast carcinoma: expression and relation to prognosis and established prognostic indicators. Br J Cancer 1996, 74: 229-233.
50. Gasparini G, Pozza F, Bevilacqua P, Gullick W, Lemoine N, Maluta S and Palma P, et al. c-erbB-3 and c-erbB-2 protein expression in node-negative breast carcinoma-An immunocytochemical study. Eur J Cancer 1994, 30: 16-22.
51. Pawlowski V, Revillion F, Hebbar M, Hornez L and 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 transcriptionpolymerase chain reaction assay. Clin Cancer Res 2000, 6: 4217-4225.
52. Witton CJ, Reeves JR, Going JJ, Cooke TG and Bartlett J. Expression of the HER1-4 family of receptor tyrosine kinases in breast cancer. J Pathol 2003, 200: 290-297.
53. Sassen A, Rochon J, Wild P, Hartmann A, Hofstaedter F, Schwarz S and Brockhoff G. Cytogenetic analysis of HER1/EGFR, HER2, HER3 and HER4 in 278 breast cancer patients. Breast Cancer Res 2008, 10: R2. .
54. Bieche I, Onody P, Tozlu S, Driouch K, Vidaud M and Lidereau R. Prognostic value of ERBB family mRNA expression in breast carcinomas. Int J Cancer 2003, 106: 758-765.
55. Lee Y, Cho S, Seo JH, Shin BK, Kim HK, Kim I and Kim A. Correlated expression of erbB-3 with hormone receptor expression and favorable clinical outcome in invasive ductal carcinomas of the breast. Am J Clin Pathol 2007, 128: 1041-1049.
56. Koutras A, Kalogeras K, Dimopoulos M, Wirtz R, Dafni U, Briasoulis E and Pectasides D, et al. Evaluation of the prognostic and predictive value of HER family mRNA expression in high-risk early breast cancer: A Hellenic Cooperative Oncology Group (HeCOG) study. Br J Cancer 2008, 99: 1775-1785.
57. Lee H, Akita RW, Sliwkowski MX and Maihle NJ. A naturally occurring secreted human ErbB3 receptor isoform inhibits heregulinstimulated activation of ErbB2, ErbB3, and ErbB4. Cancer Res 2001, 61: 4467-4473.
58. Offterdinger M, Schöfer C, Weipoltshammer K and Grunt TW. c-erbB-3 a nuclear protein in mammary epithelial cells. J Cell Biol 2002, 157: 929-940.
59. Chiu CG, Masoudi H, Leung S, Voduc DK, Gilks B, Huntsman DG and Wiseman SM. HER-3 overexpression is prognostic of reduced breast cancer survival: A study of 4046 patients. Ann Surg 2010, 251: 1107-1116.
60. Ocana A, Vera-Badillo F, Seruga B, Templeton A, Pandiella A and Amir E. HER3 overexpression and survival in solid tumors: A meta-Analysis. J Natl Cancer Inst 2013, 105: 266-273.
61. Tanizaki J, Okamoto I, Okabe T, Sakai K, Tanaka K, Hayashi H and Kaneda H, et al. Activation of HER family signaling as a mechanism of acquired resistance to ALK inhibitors in EML4-ALK-positive non-small cell lung cancer. Clin Cancer Res 2012, 18: 6219-6226.
62. Contessa JN, Abell A, Mikkelsen RB, Valerie K and Schmidt-Ullrich RK. Compensatory ErbB3/c-Src signaling enhances carcinoma cell survival to ionizing radiation. Breast Cancer Res Treat 2006, 95: 17-27.
63. Vlacich G and Coffey RJ. Resistance to EGFR-Targeted therapy: A family affair. Cancer Cell 2011, 20: 423-425.
64. Kirouac DC, Du JY, Lahdenranta J, Overland R, Yarar D, Paragas V and Pace E, et al. Computational modeling of ERBB2-Amplified breast cancer identifies combined ErbB2/3 blockade as superior to the combination of MEK and AKT inhibitors. Sci Signal 2013, 6: ra68.
65. Campbell MR, Amin D and Moasser MM. HER3 comes of age: new insights into its functions and role in signaling, tumor biology, and cancer therapy. Clin Cancer Res 2010, 16: 1373-1383.
66. Mattoon D, Lamothe B, Lax I and Schlessinger J. The docking protein Gab1 is the primary mediator of EGF-stimulated activation of the PI-3K/ Akt cell survival pathway. BMC Biol 2004, 2: 24.
67. Suenaga A, Takada N, Hatakeyama M, Ichikawa M, Yu X, Tomii K and Okimoto N, et al. Novel mechanism of interaction of p85 subunit of phosphatidylinositol 3-kinase and ErbB3 receptor-derived phosphotyrosyl peptides. J Biol Chem 2005, 280: 1321-1326.
68. Hemi R, Paz K, Wertheim N, Karasik A, Zick Y and Kanety H. Transactivation of ErbB2 and ErbB3 by tumor necrosis factor-A and anisomycin leads to impaired insulin signaling through serine/threonine phosphorylation of IRS proteins. J Biol Chem 2002, 277: 8961-8969.
69. Vivanco I and Sawyers CL. The phosphatidylinositol-3-kinase-AKT pathway in human cancer. Nat Rev Cancer 2002, 2: 489-501.
70. Knuefermann C, Lu Y, Liu B, Jin W, Liang K, Wu L and Schmidt M, et al. HER2/PI-3K/Akt activation leads to a multidrug resistance in human breast adenocarcinoma cells. Oncogene 2003, 22: 3205-3212.
71. Clarke R, Leonessa F, Welch JN and Skaar TC. Cellular and molecular pharmacology of antiestrogen action and resistance. Pharmacol Rev 2001, 53: 25-72.
72. Mouridsen HT, Rose C, Brodie AH and Smith IE. Challenges in the endocrine management of breast cancer. Breast 2003, 12: S2-S19.
73. Newby JC, Johnston S, Smith IE and 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: 1643-1651.
74. Shou J, Massarweh S, Osborne CK, Wakeling AE, Ali S, Weiss H and Schiff R. Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-Talk in ER/HER2-positive breast cancer. J Natl Cancer Inst 2004, 96: 926-935.
75. Benz CC, Scott GK, Sarup JC, Johnson RM, Tripathy D, Coronado E and Shepard HM, et al. Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu. Breast Cancer Res Treat 1992, 24: 85-95.
76. Pietras RJ, Arboleda J, Reese DM, Wongvipat N, Pegram MD, Ramos L and Gorman CM, et al. HER-2 tyrosine kinase pathway targets estrogen receptor and promotes hormone-independent growth in human breast cancer cells. Oncogene 1995, 10: 2435-2446.
77. Tang CK, Perez C, Grunt T,Waibel C, Cho C and Lupu R. Involvement of heregulin-b2 in the acquisition of the hormone-independent phenotype of breast cancer cells. Cancer Res 1996, 56: 3350-3358.
78. Tovey S, Dunne B, Witton CJ, Forsyth A, Cooke TG and Bartlett JM. Can molecular markers predict when to implement treatment with aromatase inhibitors in invasive breast cancer? Clin Cancer Res 2005, 11: 4835-4842.
79. Clark AS, West K, Streicher S and Dennis PA. Constitutive and inducible Akt activity promotes resistance to chemotherapy, trastuzumab, or tamoxifen in breast cancer cells. Mol Cancer Ther 2002, 1: 707-717.
80. Friedrichs WE, Russell DH, Donzis EJ, Middleton AK, Silva JM, Roth RA and Hidalgo M. Inhibition of mTOR activity restores tamoxifen response in breast cancer cells with aberrant Akt activity. Clin Cancer Res 2004, 10: 8059-8067.
81. Jordan NJ, Gee JM, Barrow D, Wakeling AE and Nicholson RI. Increased constitutive activity of PKB/Akt in tamoxifen resistant breast cancer MCF-7 cells. Breast Cancer Res Treat 2004, 87: 167-180.
82. Seruga B and Tannock IF. Chemotherapy-based treatment for castrationresistant prostate cancer. J Clin Oncol 2011, 29: 3686-3694.
83. Kruser TJ and Wheeler DL. Mechanisms of resistance to HER family targeting antibodies. Exp Cell Res 2010, 316: 1083-1100.
84. Yonesaka K, Zejnullahu K, Okamoto I, Satoh T, Cappuzzo F, Souglakos J and Ercan D, et al. Activation of ERBB2 signaling causes resistance to the EGFR-directed therapeutic antibody cetuximab. Sci Transl Med 2011, 3: 99ra86.
85. Incorvati JA, Shah S, Mu Y and Lu J. Targeted therapy for HER2 positive breast cancer. J Hematol Oncol 2013, 6: 38.
86. Nielsen DL, Kumler I, Palshof JA and Andersson M. Efficacy of HER2-Targeted therapy in metastatic breast cancer. Monoclonal antibodies and tyrosine kinase inhibitors. Breast 2013, 22: 1-12.
87. Hurvitz SA, Hu Y, O'Brien N and Finn RS. Current approaches and future directions in the treatment of HER2-positive breast cancer. Cancer Treat Rev 2013, 39: 219-229.
88. Rexer BN and Arteaga CL. Intrinsic and acquired resistance to HER2-Targeted therapies in HER2 gene-Amplified breast cancer: mechanisms and clinical implications. Crit Rev Oncog 2012, 17: 1-16.
89. Stern HM. Improving treatment of HER2-positive cancers: opportunities and challenges. Sci Transl Med 2012, 4: 127rv122.
90. Berns K, Horlings HM, Hennessy BT, Madiredjo M, Hijmans EM, Beelen K and Linn SC, et al. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 2007, 12: 395-402.
91. Zhang S, Huang WC, Li P, Guo H, Poh SB, Brady SW and Xiong Y, et al. Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nat Med 2011, 17: 461-469.
92. Agus DB, Akita RW, Fox WD, Lewis GD, Higgins B, Pisacane PI and Lofgren JA, et al. Targeting ligand-Activated ErbB2 signaling inhibits breast and prostate tumor growth. Cancer Cell 2002, 2: 127-137.
93. Lu Y, Zi X, Zhao Y, Mascarenhas D and Pollak M. Insulin-like growth factor-I receptor signaling and resistance to trastuzumab (herceptin). J Natl Cancer Inst 2001, 93: 1852-1857.
94. Nahta R, Yuan LX, Zhang B, Kobayashi R and Esteva FJ. Insulin-like growth factor-I receptor/human epidermal growth factor receptor 2 heterodimerization contributes to trastuzumab resistance of breast cancer cells. Cancer Res 2005, 65: 11118-11128.
95. Huang X, Gao L, Wang S, McManaman JL, Thor AD, Yang X and Esteva FJ, et al. Heterotrimerization of the growth factor receptors erbB2, erbB3, and insulin-like growth factor-i receptor in breast cancer cells resistant to herceptin. Cancer Res 2010, 70: 1204-1214.
96. Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T and Jagiello-Gruszfeld A, et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 2006, 355: 2733-2743.
97. Chen FL, Xia W and Spector NL. Acquired resistance to small molecule ErbB2 tyrosine kinase inhibitors. Clin Cancer Res 2008, 14: 6730-6734.
98. McArthur H. An overview of HER-Targeted therapy with lapatinib in breast cancer. Adv Ther 2009, 26: 263-271.
99. Eichhorn PJ, Gili M, Scaltriti M, Serra V, Guzman M, Nijkamp W and Beijersbergen RL, et al. Phosphatidylinositol 3-kinase hyperactivation results in lapatinib resistance that is reversed by the mTOR/ phosphatidylinositol 3-kinase inhibitor NVP-BEZ235. Cancer Res 2008, 68: 9221-9230.
100. Rexer BN, Ham AJ, Rinehart C, Hill S, Granja-Ingram Nde M, Gonzalez-Angulo AM and Mills GB, et al. Phosphoproteomic mass spectrometry profiling links Src family kinases to escape from HER2 tyrosine kinase inhibition. Oncogene 2011, 30: 4163-4174.
101. Zhang S, Huang WC, Zhang L, Zhang C, Lowery FJ, Ding Z and Guo H, et al. SRC family kinases as novel therapeutic targets to treat breast cancer brain metastases. Cancer Res 2013, 73: 5764-5774.
102. Abel EV, Basile KJ, Kugel CH, III, Witkiewicz AK, Le K, Amaravadi RK and Karakousis GC, et al. Melanoma adapts to RAF/MEK inhibitors through FOXD3-mediated upregulation of ERBB3. J Clin Invest 2013, 123: 2155-2168.
103. Montero-Conde C, Ruiz-Llorente S, Dominguez JM, Knauf JA, Viale A, Sherman EJ and Ryder M, et al. Relief of feedback inhibition of HER3 transcription by RAF and MEK inhibitors attenuates their antitumor effects in BRAF-mutant thyroid carcinomas. Cancer Discov 2013, 3: 520-533.
104. Sartor AO. Progression of metastatic castrate-resistant prostate cancer: impact of therapeutic intervention in the post-docetaxel space. J Hematol Oncol 2011, 4: 18.
105. Bezler M, Hengstler JG and Ullrich A. Inhibition of doxorubicin-induced HER3-PI3K-AKT signalling enhances apoptosis of ovarian cancer cells. Mol Oncol 2012, 6: 516-529.
106. Wang S, Huang X, Lee CK and Liu B. Elevated expression of erbB3 confers paclitaxel resistance in erbB2-overexpressing breast cancer cells via upregulation of survivin. Oncogene 2010, 29: 4225-4236.
107. Church DN and Talbot DC. Survivin in solid tumors: rationale for development of inhibitors. Curr Oncol Rep 2012, 14: 120-128.
108. Kanwar JR, Kamalapuram SK and Kanwar RK. Targeting survivin in cancer: the cell-signalling perspective. Drug Discov Today 2011, 16: 485-494.
109. Kelly RJ, Lopez-Chavez A, Citrin D, Janik JE and Morris JC. Impacting tumor cell-fate by targeting the inhibitor of apoptosis protein survivin. Mol Cancer 2011, 10: 35.
110. Katso R, Okkenhaug K, Ahmadi K, White S, Timms J and Waterfield MD. Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu Rev Cell Dev Biol 2001, 17: 615-675.
111. Reddy KB, Nabha SM and Atanaskova N. Role of MAP kinase in tumor progression and invasion. Cancer Metastasis Rev 2003, 22: 395-403.
112. Summy JM and Gallick GE. Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev 2003, 22: 337-358.
113. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT and Horwitz AF. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 2004, 6: 154-161.
114. Xue C, Liang F, Mahmood R, Vuolo M, Wyckoff J, Qian H and Tsai KL, et al. ErbB3-dependent motility and intravasation in breast cancer metastasis. Cancer Res 2006, 66: 1418-1426.