EGR1 and the ERK-ERF axis drive mammary cell migration in response to EGF

FASEB Journal

Volumn 26, Issue 4, 2012, Pages 1582-1592

  Tarcic, Gabi ^a   Avraham, Roi ^a   Pines, Gur ^a   Amit, Ido ^a,g   Shay, Tal ^a,g   Lu, Yiling ^b   Zwang, Yaara ^a,h   Katz, Menachem ^a,i   Ben Chetrit, Nir ^a   Jacob Hirsch, Jasmine ^c,d   Virgilio, Laura ^e,f   Rechavi, Gideon ^c,d   Mavrothalassitis, George ^e,f   Mills, Gordon B ^b   Domany, Eytan ^a   Yarden, Yosef ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF TEXAS   (United States)

^c SHEBA MEDICAL CENTER   (Israel)

^d TEL AVIV UNIVERSITY   (Israel)

^e UNIVERSITY OF CRETE   (Greece)

^f INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^g BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^h DANA FARBER CANCER INSTITUTE   (United States)

ⁱ ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Growth factor; Negative feedback; Phosphorylation; Transcription

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; EPIDERMAL GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN C FOS; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR FOSB;

ARTICLE; BREAST CELL; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOMICS;

CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; EARLY GROWTH RESPONSE PROTEIN 1; EPIDERMAL GROWTH FACTOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MAMMARY GLANDS, HUMAN; MICROARRAY ANALYSIS; MICRORNAS; PROTEOME; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84860899357     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-194654     Document Type: Article

References (55)

1. Kholodenko, B. N., Hancock, J. F., and Kolch, W. (2010) Signalling ballet in space and time. Nat. Rev. Mol. Cell. Biol. 11, 414-426
2. Avraham, R., and Yarden, Y. (2011) Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat. Rev. Mol. Cell. Biol. 12, 104-117
3. Hynes, N. E., and MacDonald, G. (2009) ErbB receptors and signaling pathways in cancer. Curr. Opin. Cell Biol. 21, 177-184
4. Yarden, Y., and Sliwkowski, M. X. (2001) Untangling the ErbB signalling network. Nat. Rev. Mol. Cell. Biol. 2, 127-137 (Pubitemid 33674041)
5. Yuan, T. L., and Cantley, L. C. (2008) PI3K pathway alterations in cancer: variations on a theme. Oncogene 27, 5497-5510
6. Katz, M., Amit, I., and Yarden, Y. (2007) Regulation of MAPKs by growth factors and receptor tyrosine kinases. Biochim. Biophys. Acta 1773, 1161-1176 (Pubitemid 47125978)
7. Von Kriegsheim, A., Baiocchi, D., Birtwistle, M., Sumpton, D., Bienvenut, W., Morrice, N., Yamada, K., Lamond, A., Kalna, G., Orton, R., Gilbert, D., and Kolch, W. (2009) Cell fate decisions are specified by the dynamic ERK interactome. Nat. Cell Biol. 11, 1458-1464
8. Le Gallic, L., Sgouras, D., Beal, G., Jr., and Mavrothalassitis, G. (1999) Transcriptional repressor ERF is a Ras/mitogen-activated protein kinase target that regulates cellular proliferation. Mol. Cell. Biol. 19, 4121-4133 (Pubitemid 29241986)
9. Chou, Y. T., Lin, H. H., Lien, Y. C., Wang, Y. H., Hong, C. F., Kao, Y. R., Lin, S. C., Chang, Y. C., Lin, S. Y., Chen, S. J., Chen, H. C., Yeh, S. D., and Wu, C. W. (2010) EGFR promotes lung tumorigenesis by activating miR-7 through a Ras/ERK/Myc pathway that targets the Ets2 transcriptional repressor ERF. Cancer Res. 70, 8822-8831
10. Herschman, H. R. (1991) Primary response genes induced by growth factors and tumor promoters. Annu. Rev. Biochem. 60, 281-319
11. Amit, I., Citri, A., Shay, T., Lu, Y., Katz, M., Zhang, F., Tarcic, G., Siwak, D., Lahad, J., Jacob-Hirsch, J., Amariglio, N., Vaisman, N., Segal, E., Rechavi, G., Alon, U., Mills, G. B., Domany, E., and Yarden, Y. (2007) A module of negative feedback regulators defines growth factor signaling. Nat. Genet. 39, 503-512 (Pubitemid 46514770)
12. Yilmaz, M., and Christofori, G. (2009) EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis. Rev. 28, 15-33
13. Nieman, M. T., Prudoff, R. S., Johnson, K. R., and Wheelock, M. J. (1999) N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J. Cell Biol. 147, 631-644
14. Katz, M., Amit, I., Citri, A., Shay, T., Carvalho, S., Lavi, S., Milanezi, F., Lyass, L., Amariglio, N., Jacob-Hirsch, J., Ben-Chetrit, N., Tarcic, G., Lindzen, M., Avraham, R., Liao, Y. C., Trusk, P., Lyass, A., Rechavi, G., Spector, N. L., Lo, S. H., Schmitt, F., Bacus, S. S., and Yarden, Y. (2007) A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration. Nat. Cell Biol. 9, 961-969 (Pubitemid 47190451)
15. Bauer, J., Margolis, M., Schreiner, C., Edgell, C. J., Azizkhan, J., Lazarowski, E., and Juliano, R. L. (1992) In vitro model of angiogenesis using a human endothelium-derived permanent cell line: contributions of induced gene expression, G-proteins, and integrins. J. Cell. Physiol. 153, 437-449
16. Grotegut, S., von Schweinitz, D., Christofori, G., and Lehembre, F. (2006) Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J. 25, 3534-3545 (Pubitemid 44264864)
17. McCawley, L. J., O'Brien, P., and Hudson, L. G. (1997) Overexpression of the epidermal growth factor receptor contributes to enhanced ligand-mediated motility in keratinocyte cell lines. Endocrinology 138, 121-127 (Pubitemid 27009414)
18. Fitzgerald, J. S., Busch, S., Wengenmayer, T., Foerster, K., de la Motte, T., Poehlmann, T. G., and Markert, U. R. (2005) Signal transduction in trophoblast invasion. Chem. Immunol. Allergy 88, 181-199 (Pubitemid 43094385)
19. Xian, C. J., and Zhou, X. F. (2004) EGF family of growth factors: essential roles and functional redundancy in the nerve system. Front. Biosci. 9, 85-92 (Pubitemid 38925441)
20. Schlegel, J., Stumm, G., Brandle, K., Merdes, A., Mechtersheimer, G., Hynes, N. E., and Kiessling, M. (1994) Amplification and differential expression of members of the erbB-gene family in human glioblastoma. J. Neurooncol. 22, 201-207
21. Morishige, M., Hashimoto, S., Ogawa, E., Toda, Y., Kotani, H., Hirose, M., Wei, S., Hashimoto, A., Yamada, A., Yano, H., Mazaki, Y., Kodama, H., Nio, Y., Manabe, T., Wada, H., Kobayashi, H., and Sabe, H. (2008) GEP100 links epidermal growth factor receptor signalling to Arf6 activation to induce breast cancer invasion. Nat. Cell Biol. 10, 85-92
22. Avraham, R., Sas-Chen, A., Manor, O., Steinfeld, I., Shalgi, R., Tarcic, G., Bossel, N., Zeisel, A., Amit, I., Zwang, Y., Enerly, E., Russnes, H. G., Biagioni, F., Mottolese, M., Strano, S., Blandino, G., Borresen-Dale, A. L., Pilpel, Y., Yakhini, Z., Segal, E., and Yarden, Y. (2010) EGF decreases the abundance of microRNAs that restrain oncogenic transcription factors. Sci. Signal. 3, ra43
23. Tait, L., Soule, H. D., and Russo, J. (1990) Ultrastructural and immunocytochemical characterization of an immortalized human breast epithelial cell line, MCF-10. Cancer Res. 50, 6087-6094 (Pubitemid 20331425)
24. Gilles, C., Polette, M., Zahm, J. M., Tournier, J. M., Volders, L., Foidart, J. M., and Birembaut, P. (1999) Vimentin contributes to human mammary epithelial cell migration. J. Cell Sci. 112, 4615-4625 (Pubitemid 30034810)
25. Irie, H. Y., Pearline, R. V., Grueneberg, D., Hsia, M., Ravichandran, P., Kothari, N., Natesan, S., and Brugge, J. S. (2005) Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition. J. Cell Biol. 171, 1023-1034 (Pubitemid 41815834)
26. Sheehan, K. M., Calvert, V. S., Kay, E. W., Lu, Y., Fishman, D., Espina, V., Aquino, J., Speer, R., Araujo, R., Mills, G. B., Liotta, L. A., Petricoin, E. F., 3rd, and Wulfkuhle, J. D. (2005) Use of reverse phase protein microarrays and reference standard development for molecular network analysis of metastatic ovarian carcinoma. Mol Cell Proteomics 4, 346-355 (Pubitemid 40590555)
27. Wells, A., Gupta, K., Chang, P., Swindle, S., Glading, A., and Shiraha, H. (1998) Epidermal growth factor receptor-mediated motility in fibroblasts. Microsc. Res. Tech. 43, 395-411 (Pubitemid 28565787)
28. Klemke, R. L., Cai, S., Giannini, A. L., Gallagher, P. J., de Lanerolle, P., and Cheresh, D. A. (1997) Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137, 481-492 (Pubitemid 27181299)
29. Potempa, S., and Ridley, A. J. (1998) Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/scatter factor-induced adherens junction disassembly. Mol. Biol. Cell 9, 2185-2200 (Pubitemid 28373633)
30. Moelling, K., Schad, K., Bosse, M., Zimmermann, S., and Schweneker, M. (2002) Regulation of Raf-Akt Cross-talk. J. Biol. Chem. 277, 31099-31106 (Pubitemid 34970815)
31. Murphy, L. O., Smith, S., Chen, R. H., Fingar, D. C., and Blenis, J. (2002) Molecular interpretation of ERK signal duration by immediate early gene products. Nat. Cell Biol. 4, 556-564
32. Sharrocks, A. D. (2001) The ETS-domain transcription factor family. Nat. Rev. Mol. Cell. Biol. 2, 827-837
33. Conacci-Sorrell, M., Ngouenet, C., and Eisenman, R. N. (2010) Myc-nick: a cytoplasmic cleavage product of Myc that promotes alpha-tubulin acetylation and cell differentiation. Cell 142, 480-493
34. Kasneci, A., Kemeny-Suss, N. M., Komarova, S. V., and Chalifour, L. E. (2009) Egr-1 negatively regulates calsequestrin expression and calcium dynamics in ventricular cells. Cardiovasc. Res. 81, 695-702
35. Collins, S., Lutz, M. A., Zarek, P. E., Anders, R. A., Kersh, G. J., and Powell, J. D. (2008) Opposing regulation of T cell function by Egr-1/NAB2 and Egr-2/Egr-3. Eur. J. Immunol. 38, 528-536
36. Owens, D. M., and Keyse, S. M. (2007) Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 26, 3203-3213 (Pubitemid 46763015)
37. Honma, S., Kawamoto, T., Takagi, Y., Fujimoto, K., Sato, F., Noshiro, M., Kato, Y., and Honma, K. (2002) Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature 419, 841-844 (Pubitemid 35238570)
38. Weisz, L., Zalcenstein, A., Stambolsky, P., Cohen, Y., Goldfinger, N., Oren, M., and Rotter, V. (2004) Transactivation of the EGR1 gene contributes to mutant p53 gain of function. Cancer Res. 64, 8318-8327 (Pubitemid 39491770)
39. Santos, S. D., Verveer, P. J., and Bastiaens, P. I. (2007) Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat. Cell Biol. 9, 324-330 (Pubitemid 46344612)
40. Zwang, Y., Sas-Chen, A., Drier, Y., Shay, T., Avraham, R., Lauriola, M., Shema, E., Lidor-Nili, E., Jacob-Hirsch, J., Amariglio, N., Lu, Y., Mills, G. B., Rechavi, G., Oren, M., Domany, E., and Yarden, Y. (2011) Two phases of mitogenic signaling unveil roles for p53 and EGR1 in elimination of inconsistent growth signals. Mol. Cell 42, 524-535
41. Lawson, M. A., Tsutsumi, R., Zhang, H., Talukdar, I., Butler, B. K., Santos, S. J., Mellon, P. L., and Webster, N. J. (2007) Pulse sensitivity of the luteinizing hormone beta promoter is determined by a negative feedback loop Involving early growth response-1 and Ngfi-A binding protein 1 and 2. Mol. Endocrinol. 21, 1175-1191 (Pubitemid 46984767)
42. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (Pubitemid 44647421)
43. Cohen-Saidon, C., Cohen, A. A., Sigal, A., Liron, Y., and Alon, U. (2009) Dynamics and variability of ERK2 response to EGF in individual living cells. Mol. Cell. 36, 885-893
44. Tang, C., Shi, X., Wang, W., Zhou, D., Tu, J., Xie, X., Ge, Q., Xiao, P. F., Sun, X., and Lu, Z. (2010) Global analysis of in vivo EGR1-binding sites in erythroleukemia cell using chromatin immunoprecipitation and massively parallel sequencing. Electrophoresis 31, 2936-2943
45. Damm, S., Koefinger, P., Stefan, M., Wels, C., Mehes, G., Richtig, E., Kerl, H., Otte, M., and Schaider, H. (2010) HGFpromoted motility in primary human melanocytes depends on CD44v6 regulated via NF-B, Egr-1, and C/EBP-beta. J. Invest. Dermatol. 130, 1893-1903
46. Cermak, V., Kosla, J., Plachy, J., Trejbalova, K., Hejnar, J., and Dvorak, M. (2010) The transcription factor EGR1 regulates metastatic potential of v-src transformed sarcoma cells. Cell. Mol. Life Sci. 67, 3557-3568
47. Baron, V., Adamson, E. D., Calogero, A., Ragona, G., and Mercola, D. (2006) The transcription factor Egr1 is a direct regulator of multiple tumor suppressors including TGFβ1, PTEN, p53, and fibronectin. Cancer Gene Ther. 13, 115-124 (Pubitemid 43113412)
48. de Mestre, A. M., Rao, S., Hornby, J. R., Soe-Htwe, T., Khachigian, L. M., and Hulett, M. D. (2005) Early growth response gene 1 (EGR1) regulates heparanase gene transcription in tumor cells. J. Biol. Chem. 280, 35136-35147 (Pubitemid 41532700)
49. Laufs, S., Schumacher, J., and Allgayer, H. (2006) Urokinasereceptor (u-PAR): an essential player in multiple games of cancer: a review on its role in tumor progression, invasion, metastasis, proliferation/dormancy, clinical outcome and minimal residual disease. Cell Cycle 5, 1760-1771
50. Salah, Z., Maoz, M., Pizov, G., and Bar-Shavit, R. (2007) Transcriptional regulation of human protease-activated receptor 1: a role for the early growth response-1 protein in prostate cancer. Cancer Res. 67, 9835-9843 (Pubitemid 47621231)
51. Kakonen, S. M., Selander, K. S., Chirgwin, J. M., Yin, J. J., Burns, S., Rankin, W. A., Grubbs, B. G., Dallas, M., Cui, Y., and Guise, T. A. (2002) Transforming growth factor-beta stimulates parathyroid hormone-related protein and osteolytic metastases via Smad and mitogen-activated protein kinase signaling pathways. J. Biol. Chem. 277, 24571-24578 (Pubitemid 34951984)
52. Sauer, L., Gitenay, D., Vo, C., and Baron, V. T. (2010) Mutant p53 initiates a feedback loop that involves Egr-1/EGF receptor/ERK in prostate cancer cells. Oncogene 29, 2628-2637
53. Scharnhorst, V., Menke, A. L., Attema, J., Haneveld, J. K., Riteco, N., van Steenbrugge, G. J., van der Eb, A. J., and Jochemsen, A. G. (2000) EGR-1 enhances tumor growth and modulates the effect of the Wilms' tumor 1 gene products on tumorigenicity. Oncogene 19, 791-800 (Pubitemid 30107710)
54. Abdulkadir, S. A., Qu, Z., Garabedian, E., Song, S. K., Peters, T. J., Svaren, J., Carbone, J. M., Naughton, C. K., Catalona, W. J., Ackerman, J. J., Gordon, J. I., Humphrey, P. A., and Milbrandt, J. (2001) Impaired prostate tumorigenesis in Egr1-deficient mice. Nat. Med. 7, 101-107 (Pubitemid 32095648)
55. Oda, K., Matsuoka, Y., Funahashi, A., and Kitano, H. (2005) A comprehensive pathway map of epidermal growth factor receptor signaling. Mol. Syst. Biol. 1, 0010