Cooperative interactions between c-Src, estrogen receptors and receptor tyrosine Kinases in breast cancer

Advances in Rapid Sex-Steroid Action: New Challenges and New Chances in Breast and Prostate Cancers

Volumn 9781461417644, Issue , 2012, Pages 31-59

  Parsons, Sarah J ^a   Pritchard, Jessica E ^a   Fox, Emily M ^b   Shupnik, Margaret A ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

Androgen receptor; c Src; Estrogen receptor; HER family receptors; Progesterone receptor; Therapeutic resistance

Indexed keywords

EID: 84921736328     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-1764-4_3     Document Type: Chapter

References (180)

1. Clemons M, Goss P (2010) Mechanisms of Disease: estrogen and the risk of breast cancer. N Engl J Med 344:276-285
2. Gompel A, Plu-Bureau G (2010) Is the decrease in breast cancer incidence related to a decrease in postmenopausal hormone therapy? Ann N Y Acad Sci 1205:268-276
3. Brisken C, O?Malley B (2010) Hormone action in the mammary gland. Cold Spring Harb Perspect Biol 2:a003178
4. Fox EM, Davis RJ, Shupnik MA (2008) ERbeta in breast cancer-onlooker, passive player, or active protector? Steroids 73:1039-1051
5. Clarke RB, Howell A, Potten CS, Anderson E (1997) Dissociation between steroid receptor expression and cell proliferation in the human breast. Cancer Res 57:4987-4991
6. Fox EM, Bernaciak TM, Wen J, Weaver AM, Shupnik MA, Silva CM (2008) Signal transducer and activator of transcription 5b, c-Src, and epidermal growth factor receptor signaling play integral roles in estrogen-stimulated proliferation of estrogen receptorpositive breast cancer cells. Mol Endocrinol 22:1781-1796
7. Herynk MH, Fuqua SA (2004) Estrogen receptor mutations in human disease. Endocr Rev 25:869-898
8. Biscardi JS, Ishizawar RC, Silva CM, Parsons SJ (2000) Tyrosine kinase signalling in breast cancer: epidermal growth factor receptor and c-Src interactions in breast cancer. Breast Cancer Res 2:203-210
9. Silva CM, Shupnik MA (2007) Integration of steroid and growth factor pathways in breast cancer: focus on signal transducers and activators of transcription and their potential role in resistance. Mol Endocrinol 21:1499-1512
10. Nilsson S, Makela S, Treuter E et al (2001) Mechanisms of estrogen action. Physiol Rev 81:1535-1565
11. Shupnik MA (2004) Crosstalk between steroid receptors and the c-Src-receptor tyrosine kinase pathways: implications for cell proliferation. Oncogene 23:7979-7989
12. Levin ER (2003) Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol Endocrinol 17:309-317
13. Hammes SR, Levin ER (2007) Extranuclear steroid receptors: nature and actions. Endocr Rev 28:726-741
14. Prossnitz ER, Oprea TI, Sklar LA, Arterburn JB (2008) The ins and outs of GPR30: a transmembrane estrogen receptor. J Steroid Biochem Mol Biol 109:350-353
15. Song RX, McPherson RA, Adam L et al (2002) Linkage of rapid estrogen action to MAPK activation by ERalpha-Shc association and Shc pathway activation. Mol Endocrinol 16:116-127
16. Song RX, Barnes CJ, Zhang Z, Bao Y, Kumar R, Santen RJ (2004) The role of Shc and insulin-like growth factor 1 receptor in mediating the translocation of estrogen receptor alpha to the plasma membrane. Proc Natl Acad Sci U S A 101:2076-2081
17. Pedram A, Razandi M, Levin ER (2006) Nature of functional estrogen receptor at the plasma membrane. Mol Endocrinol 20:1996-2009
18. Ahola TM, Alkio N, Manninen T, Ylikomi T (2002) Progestin and G protein-coupled receptor 30 inhibit mitogen-activated protein kinase activity in MCF-7 breast cancer cells. Endocrinology 143:4620-4626
19. Bjornstrom L, Sjoberg M (2005) Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol 19:833-842
20. Fox EM, Andrade J, Shupnik MA (2009) Novel actions of estrogen to promote proliferation: integration of cytoplasmic and nuclear pathways. Steroids 74:622-627
21. Cabodi S, Moro L, Baj G et al (2004) p130Cas interacts with estrogen receptor alpha and modulates non-genomic estrogen signaling in breast cancer cells. J Cell Sci 117:1603-1611
22. Barletta F, Wong CW, McNally C, Komm BS, Katzenellenbogen B, Cheskis BJ (2004) Characterization of the interactions of estrogen receptor and MNAR in the activation of cSrc. Mol Endocrinol 18:1096-1108
23. Edwards DP, Boonyaratanakornkit V (2003) Rapid extranuclear signaling by the estrogen receptor (ER): MNAR couples ER and Src to the MAP kinase signaling pathway. Mol Interv 3:12-315
24. Summy JM, Gallick GE (2003) Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev 22:337-358
25. Thomas SM, Brugge JS (1997) Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513-609
26. Brown MT, Cooper JA (1996) Regulation, substrates and functions of src. Biochim Biophys Acta 1287:121-149
27. Arnold SF, Obourn JD, Jaffe H, Notides AC (1995) Phosphorylation of the human estrogen receptor on tyrosine 537 in vivo and by src family tyrosine kinases in vitro. Mol Endocrinol 9:24-33
28. Castoria G, Migliaccio A, Bilancio A et al (2001) PI3-kinase in concert with Src promotes the S-phase entry of oestradiol-stimulated MCF-7 cells. EMBO J 20:6050-6059
29. Kraus S, Gioeli D, Vomastek T, Gordon V, Weber MJ (2006) Receptor for activated C kinase 1 (RACK1) and Src regulate the tyrosine phosphorylation and function of the androgen receptor. Cancer Res 66:11047-11054
30. Cheng CY, Kuo CT, Lin CC, Hsieh HL, Yang CM (2010) IL-1beta induces expression of matrix metalloproteinase-9 and cell migration via a c-Src-dependent, growth factor receptor transactivation in A549 cells. Br J Pharmacol 160:1595-1610
31. Lee CW, Lin CC, Lin WN et al (2007) TNF-alpha induces MMP-9 expression via activation of Src/EGFR, PDGFR/PI3K/Akt cascade and promotion of NF-kappaB/p300 binding in human tracheal smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 292:L799-812
32. Wu CY, Hsieh HL, Sun CC, Tseng CP, Yang CM (2008) IL-1 beta induces proMMP-9 expression via c-Src-dependent PDGFR/PI3K/Akt/p300 cascade in rat brain astrocytes. J Neurochem 105:1499-1512
33. Migliaccio A, Di Domenico M, Castoria G et al (1996) Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J 15:1292-1300
34. Kumar P, Wu Q, Chambliss KL et al (2007) Direct Interactions with G alpha i and G betagamma mediate nongenomic signaling by estrogen receptor alpha. Mol Endocrinol 21:1370-1380
35. Migliaccio A, Piccolo D, Castoria G et al (1998) Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J 17:2008-2018
36. Arnold SF, Vorojeikina DP, Notides AC (1995) Phosphorylation of tyrosine 537 on the human estrogen receptor is required for binding to an estrogen response element. J Biol Chem 270:30205-30212
37. Yudt MR, Vorojeikina D, Zhong L et al (1999) Function of estrogen receptor tyrosine 537 in hormone binding, DNA binding, and transactivation. Biochemistry 38:14146-14156
38. Wong CW, McNally C, Nickbarg E, Komm BS, Cheskis BJ (2002) Estrogen receptorinteracting protein that modulates its nongenomic activity-crosstalk with Src/Erk phosphorylation cascade. Proc Natl Acad Sci U S A 99:14783-14788
39. Cheskis BJ, Greger J, Cooch N et al (2008) MNAR plays an important role in ERa activation of Src/MAPK and PI3K/Akt signaling pathways. Steroids 73:901-905
40. Vadlamudi RK, Wang RA, Mazumdar A et al (2001) Molecular cloning and characterization of PELP1, a novel human coregulator of estrogen receptor alpha. J Biol Chem 276:38272-38279
41. Riggins RB, Thomas KS, Ta HQ et al (2006) Physical and functional interactions between Cas and c-Src induce tamoxifen resistance of breast cancer cells through pathways involving epidermal growth factor receptor and signal transducer and activator of transcription 5b. Cancer Res 66:7007-7015
42. Chen Y, Alvarez EA, Azzam D et al (2010) Combined Src and ER blockade impairs human breast cancer proliferation in vitro and in vivo. Breast Cancer Res Treat
43. Manavathi B, Acconcia F, Rayala SK, Kumar R (2006) An inherent role of microtubule network in the action of nuclear receptor. Proc Natl Acad Sci U S A 103:15981-15986
44. Wang X, Yang Z, Zhang H et al (2008) The estrogen receptor-interacting protein HPIP increases estrogen-responsive gene expression through activation of MAPK and AKT. Biochim Biophys Acta 1783:1220-1228
45. Alam SM, Rajendran M, Ouyang S, Veeramani S, Zhang L, Lin MF (2009) A novel role of Shc adaptor proteins in steroid hormone-regulated cancers. Endocr Relat Cancer 16:1-16
46. Kousteni S, Bellido T, Plotkin LI et al (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104:719-730
47. Migliaccio A, Di Domenico M, Castoria G et al (2005) Steroid receptor regulation of epidermal growth factor signaling through Src in breast and prostate cancer cells: steroid antagonist action. Cancer Res 65:10585-10593
48. Wells A (1999) EGF receptor. Int J Biochem Cell Biol 31:637-643
49. Normanno N, De Luca A, Bianco C et al (2006) Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 366:2-16
50. Zhang H, Berezov A, Wang Q et al (2007) ErbB receptors: from oncogenes to targeted cancer therapies. J Clin Invest 117:2051-2058
51. Bogdan S, Klambt C (2001) Epidermal growth factor receptor signaling. Curr Biol 11:R292-295
52. Mendelsohn J (2002) Targeting the epidermal growth factor receptor for cancer therapy. J Clin Oncol 20:1S-13S
53. Nicholson RI, Gee JM, Harper ME (2001) EGFR and cancer prognosis. Eur J Cancer 37 Suppl 4:S9-15
54. Velu TJ, Beguinot L, Vass WC et al (1987) Epidermal-growth-factor-dependent transformation by a human EGF receptor proto-oncogene. Science 238:1408-1410
55. Jorissen RN, Walker F, Pouliot N, Garrett TP, Ward CW, Burgess AW (2003) Epidermal growth factor receptor: mechanisms of activation and signalling. Exp Cell Res 284:31-53
56. Ren W, Korchin B, Zhu QS et al (2008) Epidermal growth factor receptor blockade in combination with conventional chemotherapy inhibits soft tissue sarcoma cell growth in vitro and in vivo. Clin Cancer Res 14:2785-2795
57. Lopez JP, Wang-Rodriguez J, Chang C et al (2007) Gefitinib inhibition of drug resistance to doxorubicin by inactivating ABCG2 in thyroid cancer cell lines. Arch Otolaryngol Head Neck Surg 133:1022-1027
58. Harari D, Yarden Y (2000) Molecular mechanisms underlying ErbB2/HER2 action in breast cancer. Oncogene 19:6102-6114
59. Schiffer IB, Gebhard S, Heimerdinger CK et al (2003) Switching off HER-2/neu in a tetracycline-controlled mouse tumor model leads to apoptosis and tumor-size-dependent remission. Cancer Res 63:7221-7231
60. Piccart-Gebhart MJ, Procter M, Leyland-Jones B et al (2005) Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 353:1659-1672
61. Vogel CL, Cobleigh MA, Tripathy D et al (2002) Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 20:719-726
62. Tiezzi DG, Andrade JM, Ribeiro-Silva A, Zola FE, Marana HR, Tiezzi MG (2007) HER-2, p53, p21 and hormonal receptors proteins expression as predictive factors of response and prognosis in locally advanced breast cancer treated with neoadjuvant docetaxel plus epirubicin combination. BMC Cancer 7:36
63. Pritchard KI, Shepherd LE, O?Malley FP et al (2006) HER2 and responsiveness of breast cancer to adjuvant chemotherapy. N Engl J Med 354:2103-2111
64. Tubbs R, Barlow WE, Budd GT et al (2009) Outcome of patients with early-stage breast cancer treated with doxorubicin-based adjuvant chemotherapy as a function of HER2 and TOP2A status. J Clin Oncol 27:3881-3886
65. Del Mastro L, Bruzzi P, Nicolo G et al (2005) HER2 expression and efficacy of dose-dense anthracycline-containing adjuvant chemotherapy in breast cancer patients. Br J Cancer 93:7-14
66. Gilcrease MZ, Woodward WA, Nicolas MM et al (2009) Even low-level HER2 expression may be associated with worse outcome in node-positive breast cancer. Am J Surg Pathol 33:759-767
67. Witton CJ, Reeves JR, Going JJ, Cooke TG, Bartlett JM (2003) Expression of the HER1-4 family of receptor tyrosine kinases in breast cancer. J Pathol 200:290-297
68. Frogne T, Laenkholm AV, Lyng MB, Henriksen KL, Lykkesfeldt AE (2009) Determination of HER2 phosphorylation at tyrosine 1221/1222 improves prediction of poor survival for breast cancer patients with hormone receptor-positive tumors. Breast Cancer Res 11:R11
69. Petit T, Wilt M, Velten M et al (2010) Semi-quantitative evaluation of estrogen receptor expression is a strong predictive factor of pathological complete response after anthracycline-based neo-adjuvant chemotherapy in hormonal-sensitive breast cancer. Breast Cancer Res Treat 124:387-391
70. Huober J, von Minckwitz G, Denkert C et al (2010) Effect of neoadjuvant anthracyclinetaxane-based chemotherapy in different biological breast cancer phenotypes: overall results from the GeparTrio study. Breast Cancer Res Treat 124:133-140
71. Darb-Esfahani S, Loibl S, Muller BM et al (2009) Identification of biology-based breast cancer types with distinct predictive and prognostic features: role of steroid hormone and HER2 receptor expression in patients treated with neoadjuvant anthracycline/taxane-based chemotherapy. Breast Cancer Res 11:R69
72. Andre F, Mazouni C, Liedtke C et al (2008) HER2 expression and efficacy of preoperative paclitaxel/FAC chemotherapy in breast cancer. Breast Cancer Res Treat 108:183-190
73. Stoica GE, Franke TF, Moroni M et al (2003) Effect of estradiol on estrogen receptor-alpha gene expression and activity can be modulated by the ErbB2/PI 3-K/Akt pathway. Oncogene 22:7998-8011
74. Oh AS, Lorant LA, Holloway JN, Miller DL, Kern FG, El-Ashry D (2001) Hyperactivation of MAPK induces loss of ERalpha expression in breast cancer cells. Mol Endocrinol 15:1344-1359
75. Zhu Y, Sullivan LL, Nair SS et al (2006) Coregulation of estrogen receptor by ERBB4/ HER4 establishes a growth-promoting autocrine signal in breast tumor cells. Cancer Res 66:7991-7998
76. Mendez P, Azcoitia I, Garcia-Segura LM (2003) Estrogen receptor alpha forms estrogendependent multimolecular complexes with insulin-like growth factor receptor and phosphatidylinositol 3-kinase in the adult rat brain. Brain Res Mol Brain Res 112:170-176
77. Santen RJ, Fan P, Zhang Z, Bao Y, Song RX, Yue W (2009) Estrogen signals via an extranuclear pathway involving IGF-1R and EGFR in tamoxifen-sensitive and -resistant breast cancer cells. Steroids 74:586-594
78. Song RX, Zhang Z, Chen Y, Bao Y, Santen RJ (2007) Estrogen signaling via a linear pathway involving insulin-like growth factor I receptor, matrix metalloproteinases, and epidermal growth factor receptor to activate mitogen-activated protein kinase in MCF-7 breast cancer cells. Endocrinology 148:4091-4101
79. Song RX, Chen Y, Zhang Z et al (2010) Estrogen utilization of IGF-1-R and EGF-R to signal in breast cancer cells. J Steroid Biochem Mol Biol 118:219-230
80. Hewitt SC, Li Y, Li L, Korach KS (2010) Estrogen-mediated regulation of Igf1 transcription and uterine growth involves direct binding of estrogen receptor alpha to estrogen-responsive elements. J Biol Chem 285:2676-2685
81. Madeo A, MaggioliniM(2010) Nuclear alternate estrogen receptor GPR30 mediates 17betaestradiol-induced gene expression and migration in breast cancer-associated fibroblasts. Cancer Res 70:6036-6046
82. Filardo EJ (2002) Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J Steroid Biochem Mol Biol 80:231-238
83. Filardo EJ, Quinn JA, Bland KI, Frackelton AR Jr (2000) Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol 14:1649-1660
84. Vivacqua A, Lappano R, De Marco P et al (2009) G protein-coupled receptor 30 expression is up-regulated by EGF and TGF alpha in estrogen receptor alpha-positive cancer cells. Mol Endocrinol 23:1815-1826
85. Naresh A, Thor AD, Edgerton SM, Torkko KC, Kumar R, Jones FE (2008) The HER4/4ICD estrogen receptor coactivator and BH3-only protein is an effector of tamoxifen-induced apoptosis. Cancer Res 68:6387-6395
86. Chen JQ, Delannoy M, Cooke C, Yager JD (2004) Mitochondrial localization of ERalpha and ERbeta in human MCF7 cells. Am J Physiol Endocrinol Metab 286:E1011-1022
87. Vidal GA, Naresh A, Marrero L, Jones FE (2005) Presenilin-dependent gamma-secretase processing regulates multiple ERBB4/HER4 activities. J Biol Chem 280:19777-19783
88. Naresh A, Long W, Vidal GA et al (2006) The ERBB4/HER4 intracellular domain 4ICD is a BH3-only protein promoting apoptosis of breast cancer cells. Cancer Res 66:6412-6420
89. Kato S, Endoh H, Masuhiro Y et al (1995) Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270:1491-1494
90. Bunone G, Briand PA, Miksicek RJ, Picard D (1996) Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. Embo J 15:2174-2183
91. Marquez DC, Lee J, Lin T, Pietras RJ (2001) Epidermal growth factor receptor and tyrosine phosphorylation of estrogen receptor. Endocrine 16:73-81
92. Curtis SW, Washburn T, Sewall C et al (1996) Physiological coupling of growth factor and steroid receptor signaling pathways: estrogen receptor knockout mice lack estrogen-like response to epidermal growth factor. Proc Natl Acad Sci U S A 93:12626-12630
93. Vignon F, Bouton MM, Rochefort H (1987) Antiestrogens inhibit the mitogenic effect of growth factors on breast cancer cells in the total absence of estrogens. Biochem Biophys Res Commun 146:1502-1508
94. Montero JC, Rodriguez-Barrueco R, Ocana A, Diaz-Rodriguez E, Esparis-Ogando A, Pandiella A (2008) Neuregulins and cancer. Clin Cancer Res 14:3237-3241
95. Loi S, Sotiriou C, Haibe-Kains B et al (2009) Gene expression profiling identifies activated growth factor signaling in poor prognosis (Luminal-B) estrogen receptor positive breast cancer. BMC Med Genomics 2:37
96. St-Laurent V, Sanchez M, Charbonneau C, Tremblay A (2005) Selective hormonedependent repression of estrogen receptor beta by a p38-activated ErbB2/ErbB3 pathway. J Steroid Biochem Mol Biol 94:23-37
97. Lindberg K, Helguero LA, Omoto Y, Gustafsson JA, Haldosen LA (2011) EstrogenEstrogen receptor beta represses Akt signaling in breast cancer cells via downregulation of HER2/ HER3 and upregulation of PTEN - implications for tamoxifen sensitivity. Breast Cancer Res 13:R43
98. Ballare C, Uhrig M, Bechtold T et al (2003) Two domains of the progesterone receptor interact with the estrogen receptor and are required for progesterone activation of the c-Src/Erk pathway in mammalian cells. Mol Cell Biol 23:1994-2008
99. Novaro V, Roskelley CD, Bissell MJ (2003) Collagen-IV and laminin-1 regulate estrogen receptor alpha expression and function in mouse mammary epithelial cells. J Cell Sci 116: 2975-2986
100. Sisci D, Aquila S, Middea E et al (2004) Fibronectin and type IV collagen activate ERalpha AF-1 by c-Src pathway: effect on breast cancer cell motility. Oncogene 23:8920-8930
101. Biscardi JS, Tice DA, Parsons SJ (1999) c-Src, receptor tyrosine kinases, and human cancer. Adv Cancer Res 76:61-119
102. Ishizawar R, Parsons SJ (2004) c-Src and cooperating partners in human cancer. Cancer Cell 6:209-214
103. Boerner JL, Biscardi JS, Silva CM, Parsons SJ (2005) Transactivating agonists of the EGF receptor require Tyr 845 phosphorylation for induction of DNA synthesis. Mol Carcinog 44:262-273
104. Weaver AM, Silva CM (2007) Signal transducer and activator of transcription 5b: a new target of breast tumor kinase/protein tyrosine kinase 6. Breast Cancer Res 9:R79
105. Boerner JL, Demory ML, Silva C, Parsons SJ (2004) Phosphorylation of Y845 on the epidermal growth factor receptor mediates binding to the mitochondrial protein cytochrome c oxidase subunit II. Mol Cell Biol 24:7059-7071
106. Demory ML, Boerner JL, Davidson R et al (2009) Epidermal growth factor receptor translocation to the mitochondria: regulation and effect. J Biol Chem 284:36592-6604
107. Cao X, Zhu H, Ali-Osman F, Lo HW (2011) EGFR and EGFRvIII undergo stress- and EGFR kinase inhibitor-induced mitochondrial translocalization: a potential mechanism of EGFR-driven antagonism of apoptosis. Mol Cancer 10:26
108. Garcia R, Bowman TL, Niu G et al (2001) Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20:2499-2513
109. Bernaciak TM, Zareno J, Parsons JT, Silva CM (2009) A novel role for signal transducer and activator of transcription 5b (STAT5b) in beta1-integrin-mediated human breast cancer cell migration. Breast Cancer Res 11:R52
110. Miyake T, Parsons SJ (2011) Functional interactions link choline kinase to EGFR and c-Src in breast cancer cell proliferation. Oncogene (Epub ahead of print)
111. Al-Saffar NM, Jackson LE, Raynaud FI et al (2010) The phosphoinositide 3-kinase inhibitor PI-103 downregulates choline kinase alpha leading to phosphocholine and total choline decrease detected by magnetic resonance spectroscopy. Cancer Res 70:5507-5517
112. Cuadrado A, Carnero A, Dolfi F, Jimenez B, Lacal JC (1993) Phosphorycholine: a novel second messenger essential for mitogenic activity of growth factors. Oncogene 8:2959-2968
113. Parsons SJ, Parsons JT (2004) Src family kinases, key regulators of signal transduction. Oncogene 23:7906-7909
114. Bromann PA, Korkaya H, Courtneidge SA (2004) The interplay between Src family kinases and receptor tyrosine kinases. Oncogene 23:7957-7968
115. Reynolds AB, Roczniak-Ferguson A (2004) Emerging roles for p120-catenin in cell adhesion and cancer. Oncogene 23:7947-7956
116. Ischenko I, Camaj P, Seeliger H et al (2008) Inhibition of Src tyrosine kinase reverts chemoresistance toward 5-fluorouracil in human pancreatic carcinoma cells: an involvement of epidermal growth factor receptor signaling. Oncogene 27:7212-7222
117. Lurje G, Lenz HJ (2009) EGFR signaling and drug discovery. Oncology 77:400-410
118. Belsches-Jablonski AP, Biscardi JS, Peavy DR, Tice DA, Romney DA, Parsons SJ (2001) Src family kinases and HER2 interactions in human breast cancer cell growth and survival. Oncogene 20:1465-1475
119. Ishizawar RC, Miyake T, Parsons SJ (2007) c-Src modulates ErbB2 and ErbB3 heterocomplex formation and function. Oncogene 26:3503-3510
120. Cabioglu N, Summy J, Miller C et al (2005) CXCL-12/stromal cell-derived factor-1alpha transactivates HER2-neu in breast cancer cells by a novel pathway involving Src kinase activation. Cancer Res 65:6493-6497
121. Wang SE, Xiang B, Zent R, Quaranta V, Pozzi A, Arteaga CL (2009) Transforming growth factor beta induces clustering of HER2 and integrins by activating Src-focal adhesion kinase and receptor association to the cytoskeleton. Cancer Res 69:475-482
122. Peters AA, Buchanan G, Ricciardelli C et al (2009) Androgen receptor inhibits estrogen receptor-alpha activity and is prognostic in breast cancer. Cancer Res 69:6131-6140
123. Castellano I, Allia E, Accortanzo V et al (2010) Androgen receptor expression is a significant prognostic factor in estrogen receptor positive breast cancers. Breast Cancer Res Treat 124:607-617
124. Hu R, Dawood S, Holmes MD et al (2011) Androgen receptor expression and breast cancer survival in postmenopausal women. Clin Cancer Res
125. Migliaccio A, Castoria G, Di Domenico M et al (2000) Steroid-induced androgen receptoroestradiol receptor beta-Src complex triggers prostate cancer cell proliferation. Embo J 19:5406-5417
126. Hamzeh M, Robaire B (2011) Androgens activate mitogen-activated protein kinase via epidermal growth factor receptor/insulin-like growth factor 1 receptor in the mouse PC-1 cell line. J Endocrinol 209:55-64
127. Migliaccio A, Varricchio L, De Falco A et al (2007) Inhibition of the SH3 domain-mediated binding of Src to the androgen receptor and its effect on tumor growth. Oncogene 26: 6619-6629
128. Zhou J, Hernandez G, Tu SW et al (2005) Synergistic induction of DOC-2/DAB2 gene expression in transitional cell carcinoma in the presence of GATA6 and histone deacetylase inhibitor. Cancer Res 65:6089-6096
129. Cops EJ, Bianco-Miotto T, Moore NL et al (2008) Antiproliferative actions of the synthetic androgen, mibolerone, in breast cancer cells are mediated by both androgen and progesterone receptors. J Steroid Biochem Mol Biol 110:236-243
130. Birrell SN, Butler LM, Harris JM, Buchanan G, Tilley WD (2007) Disruption of androgen receptor signaling by synthetic progestins may increase risk of developing breast cancer. Faseb J 21:2285-2293
131. Sanga S, Broom BM, Cristini V, Edgerton ME (2009) Gene expression meta-analysis supports existence of molecular apocrine breast cancer with a role for androgen receptor and implies interactions with ErbB family. BMC Med Genomics 2:59
132. Naderi A, Chia KM, Liu J (2011) Synergy between inhibitors of androgen receptor and MEK has therapeutic implications in estrogen receptor-negative breast cancer. Breast Cancer Res 13:R36
133. Lange CA (2004) Making sense of cross-talk between steroid hormone receptors and intracellular signaling pathways: who will have the last word? Mol Endocrinol 18:269-278
134. Richer JK, Jacobsen BM, Manning NG, Abel MG, Wolf DM, Horwitz KB (2002) Differential gene regulation by the two progesterone receptor isoforms in human breast cancer cells. J Biol Chem 277:5209-5218
135. Ward RD, Weigel NL (2009) Steroid receptor phosphorylation: Assigning function to sitespecific phosphorylation. Biofactors 35:528-536
136. Faivre EJ, Daniel AR, Hillard CJ, Lange CA (2008) Progesterone receptor rapid signaling mediates serine 345 phosphorylation and tethering to specificity protein 1 transcription factors. Mol Endocrinol 22:823-837
137. Daniel AR, Qiu M, Faivre EJ, Ostrander JH, Skildum A, Lange CA (2007) Linkage of progestin and epidermal growth factor signaling: phosphorylation of progesterone receptors mediates transcriptional hypersensitivity and increased ligand-independent breast cancer cell growth. Steroids 72:188-201
138. Abdel-Hafiz H, Dudevoir ML, Horwitz KB (2009) Mechanisms underlying the control of progesterone receptor transcriptional activity by SUMOylation. J Biol Chem 284: 9099-9108
139. Daniel AR, Lange CA (2009) Protein kinases mediate ligand-independent derepression of sumoylated progesterone receptors in breast cancer cells. Proc Natl Acad Sci U S A 106:14287-14292
140. Boonyaratanakornkit V, McGowan E, Sherman L, Mancini MA, Cheskis BJ, Edwards DP (2007) The role of extranuclear signaling actions of progesterone receptor in mediating progesterone regulation of gene expression and the cell cycle. Mol Endocrinol 21:359-375
141. Boonyaratanakornkit V, Scott MP, Ribon V et al (2001) Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Mol Cell 8:269-280
142. Skildum A, Faivre E, Lange CA (2005) Progesterone receptors induce cell cycle progression via activation of mitogen-activated protein kinases. Mol Endocrinol 19: 327-339
143. Hagan CR, Faivre EJ, Lange CA (2009) Scaffolding actions of membrane-associated progesterone receptors. Steroids 74:568-572
144. Kabat GC, Etgen AM, Rohan TE (2010) Do steroid hormones play a role in the etiology of glioma? Cancer Epidemiol Biomarkers Prev 19:2421-2427
145. Rashid F, Khan RN, Iftikhar SY (2010) Probing the link between oestrogen receptors and oesophageal cancer. World J Surg Oncol 8:9
146. Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, Baylin SB (1994) Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet 7:536-540
147. Grodstein F, Newcomb PA, Stampfer MJ (1999) Postmenopausal hormone therapy and the risk of colorectal cancer: a review and meta-analysis. Am J Med 106:574-582
148. Li LC, Chui R, Nakajima K, Oh BR, Au HC, Dahiya R (2000) Frequent methylation of estrogen receptor in prostate cancer: correlation with tumor progression. Cancer Res 60:702-706
149. Tanaka Y, Sasaki M, Kaneuchi M, Shiina H, Igawa M, Dahiya R (2003) Polymorphisms of estrogen receptor alpha in prostate cancer. Mol Carcinog 37:202-208
150. Kavanagh DO, McIlroy M, Myers E et al (2010) The role of oestrogen receptor alpha in human thyroid cancer: contributions from coregulatory proteins and the tyrosine kinase receptor HER2. Endocr Relat Cancer 17:255-264
151. Konduri S, Schwarz RE (2007) Estrogen receptor beta/alpha ratio predicts response of pancreatic cancer cells to estrogens and phytoestrogens. J Surg Res 140:55-66
152. Kawai H, Ishii A, Washiya K et al (2005) Estrogen receptor alpha and beta are prognostic factors in non-small cell lung cancer. Clin Cancer Res 11:5084-5089
153. Jacobs C, Rubsamen H (1983) Expression of pp60c-src protein kinase in adult and fetal human tissue: high activities in some sarcomas and mammary carcinomas. Cancer Res 43:1696-1702
154. Ottenhoff-Kalff AE, Rijksen G, van Beurden EA, Hennipman A, Michels AA, Staal GE (1992) Characterization of protein tyrosine kinases from human breast cancer: involvement of the c-src oncogene product. Cancer Res 52:4773-4778
155. Vallabhaneni S, Nair BC, Cortez V et al (2010) Significance of ER-Src axis in hormonal therapy resistance. Breast Cancer Res Treat
156. Duxbury MS, Ito H, Zinner MJ, Ashley SW, Whang EE (2004) Inhibition of SRC tyrosine kinase impairs inherent and acquired gemcitabine resistance in human pancreatic adenocarcinoma cells. Clin Cancer Res 10:2307-2318
157. George JA, Chen T, Taylor CC (2005) SRC tyrosine kinase and multidrug resistance protein-1 inhibitions act independently but cooperatively to restore paclitaxel sensitivity to paclitaxel-resistant ovarian cancer cells. Cancer Res 65:10381-10388
158. Kopetz S, Lesslie DP, Dallas NA et al (2009) Synergistic activity of the SRC family kinase inhibitor dasatinib and oxaliplatin in colon carcinoma cells is mediated by oxidative stress. Cancer Res 69:3842-3849
159. Ta HQ, Thomas KS, Schrecengost RS, Bouton AH (2008) A novel association between p130Cas and resistance to the chemotherapeutic drug adriamycin in human breast cancer cells. Cancer Res 68:8796-8804
160. Pritchard JE, Conaway MR, Silva CM, Parsons SJ (2011) A mechanistic study of the effect of doxorubicin/adriamycin on the estrogen response in a breast cancer model. Submitted
161. Rhee J, Han SW, Cha Y et al (2010) High serum TGF-alpha predicts poor response to lapatinib and capecitabine in HER2-positive breast cancer. Breast Cancer Res Treat 125:107-114
162. Li X, Lewis MT, Huang J et al (2008) Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 100:672-679
163. Mueller KL, Yang ZQ, Haddad R, Ethier SP, Boerner JL (2010) EGFR/Met association regulates EGFR TKI resistance in breast cancer. J Mol Signal 5:8
164. Balzer EM, Whipple RA, Thompson K et al (2010) c-Src differentially regulates the functions of microtentacles and invadopodia. Oncogene 29:6402-6408
165. Zhang S, Huang WC, Li P et al (2011) Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nat Med 17:461-469
166. Rexer BN, Ham AJ, Rinehart C et al (2011) Phosphoproteomic mass spectrometry profiling links Src family kinases to escape from HER2 tyrosine kinase inhibition. Oncogene
167. Mayer EL, Krop IE (2010) Advances in targeting SRC in the treatment of breast cancer and other solid malignancies. Clin Cancer Res 16:3526-3532
168. Puls LN, Eadens M, Messersmith W (2011) Current status of SRC inhibitors in solid tumor malignancies. Oncologist 16:566-578
169. Hudis CA (2007) Trastuzumab-mechanism of action and use in clinical practice. N Engl J Med 357:39-51
170. Boschelli F, Arndt K, Gambacorti-Passerini C (2010) Bosutinib: a review of preclinical studies in chronic myelogenous leukaemia. Eur J Cancer 46:1781-1789
171. Araujo J, Logothetis C (2010) Dasatinib: a potent SRC inhibitor in clinical development for the treatment of solid tumors. Cancer Treat Rev 36:492-500
172. Somlo G, Atzori F, Strauss L et al (2009) Dasatinib plus capecitabine (Cap) for progressive advanced breast cancer(ABC): Phase I study CA180004. J Clin Oncol 27:43s
173. Mayer E, Baurain J, Sparano J et al (2009) Dasatinib in advanced HER2/neu amplified and ER/PR-positive breast cancer: Phase II study CA180088. J Clin Oncol 27:43s
174. NCI (2011) Clinical Trials Database. National Cancer Institute
175. Green TP, Fennell M, Whittaker R et al (2009) Preclinical anticancer activity of the potent, oral Src inhibitor AZD0530. Mol Oncol
176. Moon C, Chae YK, Lee J (2010) Targeting epidermal growth factor receptor in head and neck cancer: lessons learned from cetuximab. Exp Biol Med (Maywood) 235:907-920
177. NCI (2011) Cancer Drug Information. National Cancer Institute
178. Buzdar AU (2009) Role of biologic therapy and chemotherapy in hormone receptor- and HER2-positive breast cancer. Ann Oncol 20:993-999
179. Cleator SJ, Ahamed E, Coombes RC, Palmieri C (2009) A 2009 update on the treatment of patients with hormone receptor-positive breast cancer. Clin Breast Cancer 9 Suppl 1:S6-S17
180. Lin SX, Chen J, Mazumdar M et al (2010) Molecular therapy of breast cancer: progress and future directions. Nat Rev Endocrinol 6:485-493