Enhanced expression of integrin ανβ3 induced by TGF-β is required for the enhancing effect of fibroblast growth factor 1 (FGF1) in TGF-β-induced epithelial-mesenchymal transition (EMT) in mammary epithelial cells

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Mori, Seiji ^a   Kodaira, Moe ^a   Ito, Ayano ^a   Okazaki, Mika ^a   Kawaguchi, Naomasa ^a   Hamada, Yoshinosuke ^a   Takada, Yoshikazu ^b,c   Matsuura, Nariaki ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; MUTANT PROTEIN; TRANSFORMING GROWTH FACTOR BETA; VITRONECTIN RECEPTOR; FGFR1 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR RECEPTOR 1;

ARTICLE; BREAST EPITHELIUM; CELL ASSAY; CELL CULTURE; CELL INVASION ASSAY; CELL LINE; EPITHELIAL MESENCHYMAL TRANSITION; FLOW CYTOMETRY; GENE AMPLIFICATION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MCF10A CELL LINE; MCF12A CELL LINE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; WOUND HEALING ASSAY; ZYMOGRAPHY; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; EPITHELIUM CELL; MAMMARY GLAND; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLAST GROWTH FACTOR 1; HUMANS; INTEGRIN ALPHAVBETA3; MAMMARY GLANDS, HUMAN; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84947442283     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137486     Document Type: Article

References (50)

1. Xu J, Lamouille S, Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res. 2009; 19(2):156-72. doi: 10.1038/cr.2009.5 PMID: 19153598.
2. Moustakas A, Heldin CH. Induction of epithelial-mesenchymal transition by transforming growth factor beta. Semin Cancer Biol. 2012; 22(5-6):446-54. doi: 10.1016/j.semcancer.2012.04.002 PMID: 22548724.
3. Katsuno Y, Lamouille S, Derynck R. TGF-beta signaling and epithelial-mesenchymal transition in cancer progression. Curr Opin Oncol. 2013; 25(1):76-84. doi: 10.1097/CCO.0b013e32835b6371 PMID: 23197193.
4. Lanner F, Rossant J. The role of FGF/Erk signaling in pluripotent cells. Development. 2010; 137 (20):3351-60. Epub 2010/09/30. doi: 137/20/3351 [pii] doi: 10.1242/dev.050146 PMID: 20876656.
5. Guillemot F, Zimmer C. From cradle to grave: the multiple roles of fibroblast growth factors in neural development. Neuron. 2011; 71(4):574-88. Epub 2011/08/27. doi: S0896-6273(11)00678-7 [pii] doi: 10.1016/j.neuron.2011.08.002 PMID: 21867876.
6. Ciruna B, Rossant J. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev Cell. 2001; 1(1):37-49. PMID: 11703922.
7. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009; 139(5):871-90. doi: 10.1016/j.cell.2009.11.007 PMID: 19945376.
8. Wesche J, Haglund K, Haugsten EM. Fibroblast growth factors and their receptors in cancer. Biochem J. 2011; 437(2):199-213. doi: 10.1042/BJ20101603 PMID: 21711248.
9. Turner C, Kohandel M. Investigating the link between epithelial-mesenchymal transition and the cancer stem cell phenotype: A mathematical approach. J Theor Biol. 2010; 265(3):329-35. doi: 10.1016/j.jtbi. 2010.05.024 PMID: 20648969.
10. Beenken A, Mohammadi M. The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discov. 2009; 8(3):235-53. doi: 10.1038/nrd2792 PMID: 19247306; PubMed Central PMCID: PMC3684054.
11. Billottet C, Elkhatib N, Thiery JP, Jouanneau J. Targets of fibroblast growth factor 1 (FGF-1) and FGF-2 signaling involved in the invasive and tumorigenic behavior of carcinoma cells. Mol Biol Cell. 2004; 15 (10):4725-34. doi: 10.1091/mbc.E04-04-0336 PMID: 15282342; PubMed Central PMCID: PMC519162.
12. Billottet C, Tuefferd M, Gentien D, Rapinat A, Thiery JP, Broet P, et al. Modulation of several waves of gene expression during FGF-1 induced epithelial-mesenchymal transition of carcinoma cells. J Cell Biochem. 2008; 104(3):826-39. doi: 10.1002/jcb.21667 PMID: 18189245.
13. Ramos C, Becerril C, Montano M, Garcia-De-Alba C, Ramirez R, Checa M, et al. FGF-1 reverts epithelial- mesenchymal transition induced by TGF-{beta}1 through MAPK/ERK kinase pathway. Am J Physiol Lung Cell Mol Physiol. 2010; 299(2):L222-31. doi: 10.1152/ajplung.00070.2010 PMID: 20495078.
14. Takada Y, Ye X, Simon S. The integrins. Genome Biol. 2007; 8(5):215. doi: 10.1186/gb-2007-8-5-215 PMID: 17543136; PubMed Central PMCID: PMC1929136.
15. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002; 110(6):673-87. PMID: 12297042.
16. Streuli CH, Akhtar N. Signal co-operation between integrins and other receptor systems. Biochem J. 2009; 418(3):491-506. doi: 10.1042/BJ20081948 PMID: 19228122.
17. Ivaska J, Heino J. Interplay between cell adhesion and growth factor receptors: from the plasma membrane to the endosomes. Cell Tissue Res. 2010; 339(1):111-20. doi: 10.1007/s00441-009-0857-z PMID: 19722108; PubMed Central PMCID: PMC2784865.
18. Mamuya FA, Duncan MK. aV integrins and TGF-beta-induced EMT: a circle of regulation. J Cell Mol Med. 2012; 16(3):445-55. doi: 10.1111/j.1582-4934.2011.01419.x PMID: 21883891; PubMed Central PMCID: PMC3290750.
19. Margadant C, Sonnenberg A. Integrin-TGF-beta crosstalk in fibrosis, cancer and wound healing. EMBO Rep. 2010; 11(2):97-105. doi: 10.1038/embor.2009.276 PMID: 20075988; PubMed Central PMCID: PMC2828749.
20. Mori S, Wu CY, Yamaji S, Saegusa J, Shi B, Ma Z, et al. Direct binding of integrin alphavbeta3 to FGF1 plays a role in FGF1 signaling. J Biol Chem. 2008; 283(26):18066-75. doi: 10.1074/jbc.M801213200 PMID: 18441324; PubMed Central PMCID: PMC2440593.
21. Yamaji S, Saegusa J, Ieguchi K, Fujita M, Mori S, Takada YK, et al. A novel fibroblast growth factor-1 (FGF1) mutant that acts as an FGF antagonist. PLoS One. 2010; 5(4):e10273. doi: 10.1371/journal. pone.0010273 PMID: 20422052; PubMed Central PMCID: PMC2858075.
22. Mori S, Tran V, Nishikawa K, Kaneda T, Hamada Y, Kawaguchi N, et al. A dominant-negative FGF1 mutant (the R50E mutant) suppresses tumorigenesis and angiogenesis. PLoS One. 2013; 8(2): e57927. doi: 10.1371/journal.pone.0057927 PMID: 23469107; PubMed Central PMCID: PMC3585250.
23. Pechkovsky DV, Scaffidi AK, Hackett TL, Ballard J, Shaheen F, Thompson PJ, et al. Transforming growth factor beta1 induces alphavbeta3 integrin expression in human lung fibroblasts via a beta3 integrin-, c-Src-, and p38 MAPK-dependent pathway. J Biol Chem. 2008; 283(19):12898-908. doi: 10. 1074/jbc.M708226200 PMID: 18353785.
24. Scaffidi AK, Petrovic N, Moodley YP, Fogel-Petrovic M, Kroeger KM, Seeber RM, et al. alpha(v)beta(3) Integrin interacts with the transforming growth factor beta (TGFbeta) type II receptor to potentiate the proliferative effects of TGFbeta1 in living human lung fibroblasts. J Biol Chem. 2004; 279(36):37726-33. doi: 10.1074/jbc.M403010200 PMID: 15187087.
25. Galliher AJ, Schiemann WP. Beta3 integrin and Src facilitate transforming growth factor-beta mediated induction of epithelial-mesenchymal transition in mammary epithelial cells. Breast Cancer Res. 2006; 8 (4):R42. doi: 10.1186/bcr1524 PMID: 16859511; PubMed Central PMCID: PMC1779461.
26. Feng XX, Liu M, Yan W, Zhou ZZ, Xia YJ, Tu W, et al. beta3 integrin promotes TGF-beta1/H2O2/HOClmediated induction of metastatic phenotype of hepatocellular carcinoma cells by enhancing TGF-beta1 signaling. PLoS One. 2013; 8(11):e79857. doi: 10.1371/journal.pone.0079857 PMID: 24260309; PubMed Central PMCID: PMC3832483.
27. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods. 2003; 30(3):256-68. PMID: 12798140.
28. Blatchford DR, Quarrie LH, Tonner E, McCarthy C, Flint DJ, Wilde CJ. Influence of microenvironment on mammary epithelial cell survival in primary culture. J Cell Physiol. 1999; 181(2):304-11. doi: 10. 1002/(SICI)1097-4652(199911)181:2<304::AID-JCP12>3.0.CO;2-5 PMID: 10497309.
29. Weaver VM, Lelievre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, et al. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell. 2002; 2(3):205-16. PMID: 12242153; PubMed Central PMCID: PMC2788997.
30. Hollestelle A, Peeters JK, Smid M, Timmermans M, Verhoog LC, Westenend PJ, et al. Loss of E-cadherin is not a necessity for epithelial to mesenchymal transition in human breast cancer. Breast Cancer Res Treat. 2013; 138(1):47-57. doi: 10.1007/s10549-013-2415-3 PMID: 23338761.
31. Brown KA, Aakre ME, Gorska AE, Price JO, Eltom SE, Pietenpol JA, et al. Induction by transforming growth factor-beta1 of epithelial to mesenchymal transition is a rare event in vitro. Breast Cancer Res. 2004; 6(3):R215-31. doi: 10.1186/bcr778 PMID: 15084245; PubMed Central PMCID: PMC400675.
32. Tran DD, Corsa CA, Biswas H, Aft RL, Longmore GD. Temporal and spatial cooperation of Snail1 and Twist1 during epithelial-mesenchymal transition predicts for human breast cancer recurrence. Mol Cancer Res. 2011; 9(12):1644-57. doi: 10.1158/1541-7786.MCR-11-0371 PMID: 22006115.
33. Mulder KM. Role of Ras and Mapks in TGFbeta signaling. Cytokine Growth Factor Rev. 2000; 11(1- 2):23-35. PMID: 10708950.
34. Kang JS, Liu C, Derynck R. New regulatory mechanisms of TGF-beta receptor function. Trends Cell Biol. 2009; 19(8):385-94. doi: 10.1016/j.tcb.2009.05.008 PMID: 19648010.
35. Gotzmann J, Mikula M, Eger A, Schulte-Hermann R, Foisner R, Beug H, et al. Molecular aspects of epithelial cell plasticity: implications for local tumor invasion and metastasis. Mutat Res. 2004; 566(1):9-20. PMID: 14706509.
36. Debnath J, Brugge JS. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer. 2005; 5(9):675-88. doi: 10.1038/nrc1695 PMID: 16148884.
37. Shirakihara T, Horiguchi K, Miyazawa K, Ehata S, Shibata T, Morita I, et al. TGF-beta regulates isoform switching of FGF receptors and epithelial-mesenchymal transition. EMBO J. 2011; 30(4):783-95. doi: 10.1038/emboj.2010.351 PMID: 21224849; PubMed Central PMCID: PMC3041949.
38. Schwartz MA, Ginsberg MH. Networks and crosstalk: integrin signalling spreads. Nat Cell Biol. 2002; 4 (4):E65-8. Epub 2002/04/11. doi: 10.1038/ncb0402-e65 ncb0402-e65 [pii]. PMID: 11944032.
39. Legate KR, Wickstrom SA, Fassler R. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev. 2009; 23(4):397-418. Epub 2009/02/26. doi: 23/4/397 [pii] doi: 10.1101/gad.1758709 PMID: 19240129.
40. Uttamsingh S, Bao X, Nguyen KT, Bhanot M, Gong J, Chan JL, et al. Synergistic effect between EGF and TGF-beta1 in inducing oncogenic properties of intestinal epithelial cells. Oncogene. 2008; 27 (18):2626-34. doi: 10.1038/sj.onc.1210915 PMID: 17982486.
41. Finlay GA, Thannickal VJ, Fanburg BL, Paulson KE. Transforming growth factor-beta 1-induced activation of the ERK pathway/activator protein-1 in human lung fibroblasts requires the autocrine induction of basic fibroblast growth factor. J Biol Chem. 2000; 275(36):27650-6. doi: 10.1074/jbc.M000893200 PMID: 10862759.
42. Gotzmann J, Fischer AN, Zojer M, Mikula M, Proell V, Huber H, et al. A crucial function of PDGF in TGF-beta-mediated cancer progression of hepatocytes. Oncogene. 2006; 25(22):3170-85. doi: 10. 1038/sj.onc.1209083 PMID: 16607286.
43. Fischer AN, Fuchs E, Mikula M, Huber H, Beug H, Mikulits W. PDGF essentially links TGF-beta signaling to nuclear beta-catenin accumulation in hepatocellular carcinoma progression. Oncogene. 2007; 26 (23):3395-405. doi: 10.1038/sj.onc.1210121 PMID: 17130832.
44. Fujita M, Ieguchi K, Cedano-Prieto DM, Fong A, Wilkerson C, Chen JQ, et al. An Integrin Binding-defective Mutant of Insulin-like Growth Factor-1 (R36E/R37E IGF1) Acts as a Dominant-negative Antagonist of the IGF1 Receptor (IGF1R) and Suppresses Tumorigenesis but Still Binds to IGF1R. J Biol Chem. 2013; 288(27):19593-603. doi: 10.1074/jbc.M113.470872 PMID: 23696648; PubMed Central PMCID: PMC3707660.
45. Fujita M, Ieguchi K, Davari P, Yamaji S, Taniguchi Y, Sekiguchi K, et al. Cross-talk between integrin alpha6beta4 and insulin-like growth factor-1 receptor (IGF1R) through direct alpha6beta4 binding to IGF1 and subsequent alpha6beta4-IGF1-IGF1R ternary complex formation in anchorage-independent conditions. J Biol Chem. 2012; 287(15):12491-500. Epub 2012/02/22. doi: 10.1074/jbc.M111.304170 PMID: 22351760; PubMed Central PMCID: PMC3320998.
46. Fujita M, Takada YK, Takada Y. Insulin-like Growth Factor (IGF) Signaling Requires alphavbeta3- IGF1-IGF Type 1 Receptor (IGF1R) Ternary Complex Formation in Anchorage Independence, and the Complex Formation Does Not Require IGF1R and Src Activation. J Biol Chem. 2013; 288(5):3059-69. Epub 2012/12/18. doi: 10.1074/jbc.M112.412536 PMID: 23243309; PubMed Central PMCID: PMC3561530.
47. Saegusa J, Yamaji S, Ieguchi K, Wu CY, Lam KS, Liu FT, et al. The direct binding of insulin-like growth factor-1 (IGF-1) to integrin alphavbeta3 is involved in IGF-1 signaling. J Biol Chem. 2009; 284 (36):24106-14. Epub 2009/07/07. doi: M109.013201 [pii] doi: 10.1074/jbc.M109.013201 PMID: 19578119.
48. Hong JP, Li XM, Li MX, Zheng FL. VEGF suppresses epithelial-mesenchymal transition by inhibiting the expression of Smad3 and miR192, a Smad3-dependent microRNA. Int J Mol Med. 2013; 31 (6):1436-42. doi: 10.3892/ijmm.2013.1337 PMID: 23588932.
49. Ramos C, Montano M, Becerril C, Cisneros-Lira J, Barrera L, Ruiz V, et al. Acidic fibroblast growth factor decreases alpha-smooth muscle actin expression and induces apoptosis in human normal lung fibroblasts. Am J Physiol Lung Cell Mol Physiol. 2006; 291(5):L871-9. doi: 10.1152/ajplung.00019. 2006 PMID: 16766579.
50. Shukla MN, Rose JL, Ray R, Lathrop KL, Ray A, Ray P. Hepatocyte growth factor inhibits epithelial to myofibroblast transition in lung cells via Smad7. Am J Respir Cell Mol Biol. 2009; 40(6):643-53. doi: 10. 1165/rcmb.2008-0217OC PMID: 18988920; PubMed Central PMCID: PMC2689916.