The G Protein-Coupled Estrogen Receptor-1, GPER-1, Promotes Fibrillogenesis via a Shc-Dependent Pathway Resulting in Anchorage-Independent Growth

Hormones and Cancer

Volumn 5, Issue 6, 2014, Pages 390-404

  Magruder, Hilary T ^a   Quinn, Jeffrey A ^a   Schwartzbauer, Jean E ^b   Reichner, Jonathan ^a   Huang, Allan ^a   Filardo, Edward J ^a,c  

^a BROWN UNIVERSITY   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c Radix BioSolutions   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ACTIN; BENZHYDRYL DERIVATIVE; EPIDERMAL GROWTH FACTOR; ESTRADIOL; ESTROGEN RECEPTOR; FIBRONECTIN; FULVESTRANT; G PROTEIN COUPLED RECEPTOR; GPER PROTEIN, HUMAN; GPR30 PROTEIN, MOUSE; PHENOL DERIVATIVE; PROTEIN SHC; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ANALOGS AND DERIVATIVES; ANIMAL; BREAST TUMOR; CELL ADHESION; CELL GROWTH; DRUG EFFECTS; FEMALE; FOCAL ADHESION; GENETICS; HUMAN; METABOLISM; MOUSE; MUTATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STRESS FIBER; TUMOR CELL LINE;

ACTINS; ANIMALS; BENZHYDRYL COMPOUNDS; BREAST NEOPLASMS; CELL ADHESION; CELL GROWTH PROCESSES; CELL LINE, TUMOR; EPIDERMAL GROWTH FACTOR; ESTRADIOL; ESTROGEN RECEPTOR MODULATORS; FEMALE; FIBRONECTINS; FOCAL ADHESIONS; HUMANS; MICE; MUTATION; PHENOLS; PHOSPHORYLATION; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; STRESS FIBERS;

EID: 84930027452     PISSN: 18688497     EISSN: 18688500     Source Type: Journal    
DOI: 10.1007/s12672-014-0195-9     Document Type: Article

References (79)

1. Stoffels JM, Zhao C, Baron W (2013) Fibronectin in tissue regeneration: timely disassembly of the scaffold is necessary to complete the build. Cell Mol Life Sci 70:4243–4253
2. Astrof S, Hynes RO (2009) Fibronectins in vascular morphogenesis. Angiol 12:165–175
3. Francis SE, Goh KL, Hodivala-Dilke K, Bader BL, Stark M, Davidson D, Hynes RO (2002) Central roles of α5β1 integrin and fibronectin in vascular development in mouse embryos and embryoid bodies. Arterioscler Thromb Vasc Biol 22:927–933
4. Faraldo MM, Deugnier MA, Thiery JP, Glukhova MA (2001) Growth defects induced by perturbation of B1-integrin function in the mammary gland epithelium result from a lack of MAPK activation via the Shc and Akt pathways. EMBO Rep 2:431–437
5. Williams CM, Engler AJ, Slone RD, Galante LL, Schwarzbauer JE (2008) Fibronectin expression modulates mammary epithelial cell proliferation during acinar differentiation. Cancer Res 68:3185–3192
6. Faull RJ, Kovach NL, Harlan JM, Ginsberg MH (1993) Affinity modulation of integrin α5β1: regulation of the functional response by soluble fibronectin. J Cell Biol 121:155–162
7. Hocking DC, Sottile J, Langenbach KJ (2000) Stimulation of integrin-mediated cell contractility by fibronectin polymerization. J Biol Chem 275:10673–10682
8. Ingham KC, Brew SA, Huff S, Litvinovich SV (1997) Cryptic self-association sites in type III modules of fibronectin. J Biol Chem 272:1718–1724
9. Klotzsch E, Smith ML, Kubow KE, Muntwyler S, Little WC, Beyeler F, Gourdon D, Nelson BJ, Vogel V (2009) Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites. Proc Natl Acad Sci U S A 106:18267–18272
10. Valenick LV, Hsia HC, Schwarzbauer JE (2005) Fibronectin fragmentation promotes alpha4beta1 integrin-mediated contraction of a fibrin-fibronectin provisional matrix. Exp Cell Res 309:48–55
11. Woodward TL, Mienaltowski AS, Modi RR, Bennett JM, Haslam SZ (2001) Fibronectin and the α5β1 integrin are under developmental and ovarian steroid regulation in the normal mouse mammary gland. Endocrinol 142:3214–3222
12. Faraldo MM, Deugnier MA, Tlouzeau S, Thiery JP, Glukhova MA (2002) Perturbation of beta 1-integrin function in involuting mammary gland results in premature dedifferentiation of secretory epithelial cells. Mol Biol Cell 13(10):3521–3531
13. Price JE (1996) Metastasis from human breast cancer cell lines. Breast Cancer Res Treat 39:93–102
14. Saulnier R, Bhardwaj B, Klassen J, Leopold D, Rahimi N, Tremblay E, Mosher D, Elliott B (1996) Fibronectin fibrils and growth factors stimulate anchorage-independent growth of murine mammary carcinoma. Exp Cell Res 222:360–369
15. Qiao H, Saulnier R, Patryzkat A, Rahimi N, Raptis L, Rossiter J, Tremblay E, Elliott B (2000) Cooperative effect of hepatocyte growth factor and fibronectin in anchorage-independent survival of mammary carcinoma cells: requirement for phosphatidulinositol 3-kinase activity. Cell Growth Differ 11:123–133
16. Discher DM, Noy D, Strazalka J, Ye S, Moser CC, Lear JD, Blasie JK, Dutton PL (2005) Design of amphiphilic protein maquettes: controlling assembly, membrane insertion, and cofactor interactions. Biochemistry 44(37):12329–12343
17. Frisch SM, Francis H (1994) Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124(4):619–626
18. Frisch SM, Vuori K, Ruoslahti E, Chan-Hui PY (1996) Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 134:793–799
19. Martin SW, Butcher AJ, Berrow NS, Richards MW, Paddon RE, Turner DJ, Dolphin AC, Sihra TS, Fitzgerald EM (2006) Phosphorylation sites on calcium channel alpha 1 and beta subunits regulate ERK-dependent modulation of neuronal N-type calcium channels. Call Calcium 39(3):275–292
20. Green JA, Berrier AL, Pankov R, Yamada KM (2009) beta1 integrin cytoplasmic domain residues selectively modulate fibronectin matrix assembly and cell spreading through talin and Akt-1. J Biol Chem 284:8148–8159
21. Ridley AJ, Hall A (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389–399
22. Sottile J, Hocking DC, Swiatek PJ (1998) Fibronectin matrix assembly enhances adhesion-dependent cell growth. J Cell Sci 111:2933–2943
23. Wierzbicka-Patynowski I, Schwarzbauer JE (2002) Regulatory role for SRC and phosphatidylinositol 3-kinase in initiation of fibronectin matrix assembly. J Biol Chem 277:19703–19708
24. Wierzbicka-Patynowski I, Mao Y, Schwarzbauer JE (2007) Continuous requirement for pp 60-Src and phospho-paxillin during fibronectin matrix assembly by transformed cells. J Cell Physiol 210:750–756
25. Mao Y, Schwarzbauer JE (2005) Stimulatory effects of a three-dimensional microenvironment on cell mediated fibronectin fibrillogenesis. J Cell Sci 118:4427–4436
26. Accornero P, Miretti S, Cucuzza LS, Martignani E, Baratta M (2010) Epidermal growth factor and hepatocyte growth factor cooperate to enhance cell proliferation, scatter, and invasion in murine mammary epithelial cells. J Mol Endocrinol 44:115–125
27. Ravichandran KS (2001) Signaling via Shc family adapter proteins. Oncogene 20:6322–6330
28. Wary KK, Mariotti A, Zurzolo C, Gianeotti FG (1998) A requirement of caveolin-1 and associated kinase Fyn in intergrin signaling and anchorage-dependent cell growth. Cell 94(5):625–634
29. Ma Z, Myers DP, Wu RF, Nwariaku FE, Terada LS (2007) p66Shc mediates anoikis through RhoA. J Cell Biol 179:23–31
30. Migliaccio E, Mele S, Salcini AE, Pelicci G, Lai KM, Superti-Furga G, Pawson T, Di Fiore PP, Lanfrancone L, Pelicci PG (1997) Opposite effects of the p52shc/p46shc and p66shc splicing isoforms on the EGF receptor-MAP kinase-fos signalling pathway. EMBO J 16:706–716
31. Bonati A, Carlo-Stella C, Lunghi P, Albertini R, Pinelli S, Migliaccio E, Sammarelli G, Savoldo B, Tabilio A, Dall'Aglio PP, Pelicci PG (2000) Selective expression and constitutive phosphorylation of SHC proteins [corrected] in the CD34+ fraction of chronic myelogenous leukemias. Cancer Res 60:728–732
32. Zhang L, Lorenz U, Ravichandran KS (2003) Role of Shc in T-cell development and function. Immunol Rev 191:183–195
33. Giles AJ, Bender TP, Ravichandran KS (2009) The adaptor protein Shc plays a key role during early B cell development. J Immunol 183:5468–5476
34. Ma Z, Liu Z, Wu RF, Terada LS (2010) p66(Shc) restrains Ras hyperactivation and suppresses metastatic behavior. Oncogene 29:5559–5567
35. Frackelton AR Jr, Lu L, Davol PA, Bagdasaryan R, Hafer LJ, Sgroi DC (2006) p66 Shc and tyrosine-phosphorylated Shc in primary breast tumors identify patients likely to relapse despite tamoxifen therapy. Breast Cancer Res 8:R73
36. Grossman SR, Lyle S, Resnick MB, Sabo E, Lis RT, Rosinha E, Liu Q, Hsieh CC, Bhat G, Frackelton AR Jr, Hafer LJ (2007) p66 Shc tumor levels show a strong prognostic correlation with disease outcome in stage IIA colon cancer. Clin Cancer Res 13:5798–5804
37. Lee CS, Hall RE, Alexander IE, Koga M, Shine J, Sutherland RL (1990) Inverse relationship between estrogen receptor and epidermal growth factor receptor mRNA levels in human breast cancer cell lines. Growth Factors 3(2):97–103
38. Filardo EJ, Graeber CT, Quinn JA, Resnick MB, Giri D, DeLellis RA, Steinhoff MM, Sabo E (2006) Distribution of GPR30, a seven-membrane-spanning estrogen receptor, in primary breast cancer and its association with clinicopathological determinants of tumor progression. Clin Cancer Res 12:6359–6366
39. Arias-Pulido H, Royce M, Gong Y, Joste N, Lomo L, Lee SJ, Chaher N, Verschraegen C, Lara J, Prossnitz ER, Cristofanilli M (2010) GPR30 and estrogen receptor expression: new insights into hormone dependence of inflammatory breast cancer. Breast Cancer Res Treat 123:51–58
40. Ignatov A, Ignatov T, Weissenborn C, Eggemann H, Bischoff J, Semczuk A, Roessner A, Costa SD, Kalinski T (2011) G-protein-coupled estrogen receptor GPR30 and tamoxifen resistance in breast cancer. Breast Cancer Res Treat 128:457–466
41. Steiman J, Peralta EA, Louis S, Kamel O (2013) Biology of the estrogen receptor, GPR30, in triple negative breast cancer. Am J Surg 206:698–703
42. Filardo EJ, Quinn JA, Frackelton AR, Bland KI (2002) Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol 16:70–84
43. Filardo EJ, Quinn JA, Bland KI, Frackelton AR (2000) Estrogen-induced activation of Erk-1 and Erk-2 requires the G-protein coupled receptor homolog, GPR30, and occurs via the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol 14:1649–1660
44. Quinn JA, Graeber T, Frackelton R, Kim M, Schwarzbauer JE, Filardo EJ (2009) Coordinate regulation of estrogen-mediated fibronectin matrix assembly and epidermal growth factor receptor transactivation by the G protein-coupled receptor, GPR30. Mol Endocrinol 23:1052–1064
45. Sechler JL, Takada Y, Schwarzbauer JE (1996) Altered rate of fibronectin matrix assembly by deletion of the first type III repeats. J Cell Biol 134:573–583
46. Filardo EJ, Brooks PC, Deming SL, Damsky C, Cheresh DA (1995) Requirement of the NPXY motif in the integrin β3 subunit cytoplasmic tail for melanoma cell migration in vitro and in vivo. J Cell Biol 130:441–450
47. Pierschbacher MD, Hayman EG, Ruoslahti E (1981) Location of the cell-attachment site in fibronectin with monoclonal antibodies and proteolytic fragments of the molecule. Cell 26(2):259–267
48. Foty R (2011) A simple hanging drop cell culture protocol for generation of 3D spheroids. J Vis Exp 6(51)
49. Bartosh TJ, Ylostalo JH (2014) Preparation of anti-inflammatory mesenchymal stem/precursor cells (MSCs) through sphere formation using hanging-drop culture technique. Curr Protoc Stem Cell Biol 6(28)
50. Archacka K, Pozzobon M, Repele A, Rossi CA, Campanella M, De Coppi P (2014) Culturing muscle fibres in hanging drop: a novel approach to solve an old problem. Biol Cell 106(2):72–82
51. Tsai C, Wu H, Lin C, Lin Y, Chao A, Wang T, Hsueh S, Lai C, Wang H (2013) Estradiol and tamoxifen induce cell migration through GPR30 and activation of focal adhesion kinase (FAK) in endometrial cancers with low or without nuclear estrogen receptor α (ERα). PLoS ONE 8(9):e72999
52. Pupo M, Pisano A, Lappano R, Santolla MF, De Francesco EM, Abonante S, Rosano C, Maggiolini M (2012) Bisphenol A induces gene expression changes and proliferative effects through GPER in breast cancer cells and cancer-associated fibroblasts. Enviorn Health Perspect 120(8):1177–1182
53. Ginsberg MH, Partridge A, Shattil SJ (2005) Integrin regulation. Curr Opin Cell Biol 17(5):509–516
54. Luo BH, Carman CV, Springer TA (2007) Structural basis of integrin regulation and signaling. Annu Rev Immunol 25:619–647
55. O’Toole TE, Loftus JC, Plow EF, Glass AA, Harper JR, Ginsberg MH (1989) Efficient surface expressin of platelet GPIIb-IIIa requires both subunits. Blood 74(1):14–18
56. Price J (1996) Metastasis from human breast cancer cell lines. Breast Cancer Res Treat 39(1):93–102
57. Acconcia F, Barnes CJ, Kumar R (2006) Estrogen and tamoxifen induce cytoskeletal remodeling and migration in endometrial cells. Endocrinol 147:1203–1212
58. Azios NG, Krishnamoorthy L, Harris M, Cubano LA, Cammer M, Dharmawardhane SF (2007) Estrogen and resveratrol regulate Rac and Cdc42 signaling to the actin cytoskeleton of metastatic breast cancer cells. Neoplasia 9(2):147–158
59. Sapino A, Pietribiasi F, Bussolati G, Marchisio PC (1986) Estrogen- and tamoxifen-induced rearrangement of cytoskeletal and adhesion structures in breast cancer MCF-7 cells. Cancer Res 46:2526–2531
60. Ehlers EM, Schubert C (1999) Differences in morphology and cytoskeleton of MCF-7 and MX-1 cells after therapy with OH-tamoxifen and the pure estrogen antagonist ZM 182780. An immunofluorescence and scanning electron microscopic study. Ann Anat 181:231–236
61. Dong S, Terasaka S, Kiyama R (2011) Bisphenol A induces a rapid activation of Erk1/2 through GPR30 in human breast cancer cells. Environ Pollut 159(1):212–218
62. Cosemans JMEM, Iserbyt BF, Deckmyn H, Heemskerk JMW (2008) Multiple ways to switch platelet integrins on and off. J Thromb Haemost 6(8):1253–1261
63. Oberyszyn T, Conti C, Ross M, Oberyszyn A, Tober K, Rackoff A, Robertson F (1998) β2 integrin/ICAM-1 adhesion molecule interactions in cutaneous inflammation and tumor promotion. Carcinogenesis 19(3):445–455
64. Philips DR, Prasad KS, Manganello J, Bao M, Nannizzi-Alaimo L (2001) Integrin tyrosine phosphorylation in platelet signaling. Curr Opin Cell Biol 13(5):541–554
65. Cowan KJ, Law DA, Phillips DR (2000) Identification of Shc as the primary protein binding to the tyrosine-phosphorylated beta3 subunit of alpha iibbeta3 during outside-in integrin platelet signaling. J Biol Chem 275:36423–36429
66. Sweet DT, Chen Z, Wiley DM, Bautch VL, Tzima E (2012) The adaptor protein Shc integrates growth factor and ECM signaling during postnatal angiogenesis. Blood 119:1946–1955
67. Barberis L, Wary KK, Fiucci G, Liu F, Hirsch E, Brancaccio M, Altruda F, Tarone G, Giancotti FG (2000) Distinct roles of adaptor protein Shc and focal adhesion kinase in integrin signaling to ERK. J Biol Chem 275:36532–36540
68. Wary K, Mainiero F, Isakoff SJ, Marcantonio EE, Giancotti FG (1996) The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87:733–743
69. Habib T, Herrera R, Decker SJ (1994) Activators of protein kinase C stimulate association of Shc and the PEST tyrosine phosphatase. J Biol Chem 269(41):25243–25246
70. Deshmukh L, Gorbatyuk V, Vinogradova O (2010) Integrin β3 phosphoylation dictates its complex with the Sch phosphotyrosine-binding (PTB) domain. J Biol Chem 285:34875–34884
71. Angers-Loustau A, Cote JF, Charest A, Dowbenko D, Spencer S, Laskv LA, Tremblay (1999) Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J Cell Biol 144(5):1019–1031
72. Debnath J (2010) p66Shc and Ras: controlling anoikis from the inside-out. Oncogene 29:5556–5558
73. Charest A, Wagner J, Jacob S, McGlade CJ, Tremblay ML (1996) Phosphotyrosine-independent binding of Shc to the NPLH sequence of murine protein-tyrosine phosphatase-PEST. Evidence for extended phosphotyrosine binding/phosphotyrosine interaction domain recognition specificity. J Biol Chem 271(14):8424–2429
74. Sachdev S, Bu Y, Gelman IH (2009) Paxillin-Y118 phosphorylation contributes to the control of Src-induced anchorage-independent growth by FAK and adhesion. BMC Cancer 9(12)
75. Petita B, Thierya JP (2000) Focal adhesions: structure and dynamics. Biol Cell 92:477–494
76. Arregui CO, Balsamo J, Lilien J (1998) Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant-negative mutant PTP1B. J Cell Biol 143(3):861–873
77. Yu DH, Qu CK, Henegariu O, Lu X, Feng GS (1998) Protein-tyrosine phosphatase Shp-2 regulates cell spreading, migration, and focal adhesion. J Biol Chem 273(33):21125–21131
78. Zheng Y, Lu Z (2013) Regulation of tumor cell migration by protein tyrosine phosphatase (PTP)-proline-, glutamate-, serine-, and threonine-rich sequence (PEST). Chin J Cancer 32(2):75–83
79. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, Huang Y, Hu X, Su F, Lieberman J, Song E (2007) Let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131:1109–1123