Novel roles for ERK5 and cofilin as critical mediators linking ERα-driven transcription, actin reorganization, and invasiveness in breast cancer

Molecular Cancer Research

Volumn 12, Issue 5, 2014, Pages 714-727

  Madak Erdogan, Zeynep ^a   Ventrella, Rosa ^a   Petry, Luke ^a   Katzenellenbogen, Benita S ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CELL NUCLEUS RECEPTOR; COFILIN; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 7; CFL1 PROTEIN, HUMAN; CHROMATIN; COFILIN 1; ESTRADIOL; ESTROGEN RECEPTOR ALPHA, HUMAN; MAP2K5 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 5;

ACTIN FILAMENT; ARTICLE; BREAST CANCER; CANCER CELL; CARCINOGENICITY; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHROMATIN; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROGNOSIS; REGULATORY MECHANISM; TUMOR INVASION; BREAST TUMOR; CELL GROWTH; CELL NUCLEUS; FEMALE; GENETICS; MCF 7 CELL LINE; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; TUMOR CELL LINE;

ACTINS; BREAST NEOPLASMS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CELL NUCLEUS; CHROMATIN; COFILIN 1; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; MAP KINASE KINASE 5; MAP KINASE SIGNALING SYSTEM; MCF-7 CELLS; MITOGEN-ACTIVATED PROTEIN KINASE 7; NEOPLASM INVASIVENESS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 84900464485     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-13-0588     Document Type: Article

References (51)

1. Katzenellenbogen BS, Frasor J. Therapeutic targeting in the estrogen receptor hormonal pathway. Semin Oncol 2004;31:28-38.
2. Frasor J, Danes JM, Komm B, Chang KC, Lyttle CR, Katzenellenbogen BS. Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 2003;144:4562-74.
3. Frasor J, Stossi F, Danes JM, Komm B, Lyttle CR, Katzenellenbogen BS. Selective estrogen receptor modulators: discrimination of agonistic versus antagonistic activities by gene expression profiling in breast cancer cells. Cancer Res 2004;64:1522-33.
4. Hah N, Danko CG, Core L, Waterfall JJ, Siepel A, Lis JT, et al. A rapid, extensive, and transient transcriptional response to estrogen signaling in breast cancer cells. Cell 2011;145:622-34.
5. Ross-Innes CS, Stark R, Teschendorff AE, Holmes KA, Ali HR, Dunning MJ, et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature 2012;481: 389-93.
6. Soulez M, Parker MG. Identification of novel oestrogen receptor target genes in human ZR75-1 breast cancer cells by expression profiling. J Mol Endocrinol 2001;27:259-74.
7. Bergamaschi A, Christensen BL, Katzenellenbogen BS. Reversal of endocrine resistance in breast cancer: interrelationships among 14-3-3zeta, FOXM1, and a gene signature associated with mitosis. Breast Cancer Res 2011;13:R70.
8. Creighton CJ, Hilger AM, Murthy S, Rae JM, Chinnaiyan AM, El-Ashry D. Activation of mitogen-activated protein kinase in estrogen receptor alpha-positive breast cancer cells in vitro induces an in vivo molecular phenotype of estrogen receptor alpha-negative human breast tumors. Cancer Res 2006;66:3903-11.
9. Osborne CK, Schiff R. Mechanisms of endocrine resistance in breast cancer. Annu Rev Med 2011;62:233-47.
10. Schiff R, Massarweh S, Shou J, Osborne CK. Breast cancer endocrine resistance: how growth factor signaling and estrogen receptor coregulators modulate response. Clin Cancer Res 2003;9:447S-54S.
11. Shou J, Massarweh S, Osborne CK, Wakeling AE, Ali S, Weiss H, et al. Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J Natl Cancer Inst 2004;96:926-35.
12. Madak-Erdogan Z, Lupien M, Stossi F, Brown M, Katzenellenbogen BS. Genomic collaboration of estrogen receptor alpha and extracellular signal-regulated kinase 2 in regulating gene and proliferation programs. Mol Cell Biol 2011;31:226-36.
13. Bravo-Cordero JJ, Magalhaes MA, Eddy RJ, Hodgson L, Condeelis J. Functions of cofilin in cell locomotion and invasion. Nat Rev Mol Cell Biol 2013;14:405-15.
14. Stossi F, Madak-Erdogan Z, Katzenellenbogen BS. Macrophage-elicited loss of estrogen receptor-alpha in breast cancer cells via involvement of MAPK and c-Jun at the ESR1 genomic locus. Oncogene 2012;31:1825-34.
15. Madak-Erdogan Z, Charn TH, Jiang Y, Liu ET, Katzenellenbogen JA, Katzenellenbogen BS. Integrative genomics of gene and metabolic regulation by estrogen receptors alpha and beta, and their coregulators. Mol Syst Biol 2013;9:676.
16. Madak-Erdogan Z, Katzenellenbogen BS. Aryl hydrocarbon receptor modulation of estrogen receptor alpha-mediated gene regulation by a multimeric chromatin complex involving the two receptors and the coregulator RIP140. Toxicol Sci 2012;125:401-11.
17. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9:357-9.
18. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008;9: R137.
19. Ye T, Krebs AR, Choukrallah MA, Keime C, Plewniak F, Davidson I, et al. seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res 2011;39:e35.
20. Liu T, Ortiz JA, Taing L, Meyer CA, Lee B, Zhang Y, et al. Cistrome: an integrative platform for transcriptional regulation studies. Genome Biol 2011;12:R83.
21. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, et al. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 2010;28:495-501.
22. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012;9:676-82.
23. Kim K, Madak-Erdogan Z, Ventrella R, Katzenellenbogen BS. A Micro-RNA196a2* and TP63 circuit regulated by estrogen receptor-alpha and ERK2 that controls breast cancer proliferation and invasiveness properties. Horm Cancer 2013;4:78-91.
24. Klein AM, Zaganjor E, Cobb MH. Chromatin-tethered MAPKs. Curr Opin Cell Biol 2013;25:272-7.
25. Turjanski AG, Vaque JP, Gutkind JS. MAP kinases and the control of nuclear events. Oncogene 2007;26:3240-53.
26. Barsyte-Lovejoy D, Galanis A, Clancy A, Sharrocks AD. ERK5 is targeted to myocyte enhancer factor 2A (MEF2A) through a MAPK docking motif. Biochem J 2004;381:693-9.
27. Yang Q, Deng X, Lu B, Cameron M, Fearns C, Patricelli MP, et al. Pharmacological inhibition ofBMK1suppresses tumor growth through promyelocytic leukemia protein. Cancer Cell 2010;18:258-67.
28. Hu Y, Plutz M, Belmont AS. Hsp70 gene association with nuclear speckles is Hsp70 promoter specific. J Cell Biol 2010;191:711-9.
29. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 2006;3:995-1000.
30. Chan AY, Bailly M, Zebda N, Segall JE, Condeelis JS. Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J Cell Biol 2000;148:531-42.
31. Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, Symons M, et al.Molecular mechanisms of invadopodium formation: the role of the NWASP-Arp2/3 complex pathway and cofilin. J Cell Biol 2005;168:441-52.
32. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 2004;304:743-6.
33. Meira M, Masson R, Stagljar I, Lienhard S, Maurer F, Boulay A, et al. Memo is a cofilin-interacting protein that influences PLCgamma1 and cofilin activities, and is essential for maintaining directionality during ErbB2-induced tumor-cell migration. J Cell Sci 2009;122:787-97.
34. Wang W, Eddy R, Condeelis J. The cofilin pathway in breast cancer invasion and metastasis. Nat Rev Cancer 2007;7:429-40.
35. Montero JC, Ocana A, Abad M, Ortiz-Ruiz MJ, Pandiella A, Esparis-Ogando A. Expression of Erk5 in early stage breast cancer and association with disease free survival identifies this kinase as a potential therapeutic target. PLoS ONE 2009;4:e5565.
36. Kim KY, Levin DE. Mpk1 MAPK association with the Paf1 complex blocks Sen1-mediated premature transcription termination. Cell 2011;144:745-56.
37. Wang W, Mouneimne G, Sidani M, Wyckoff J, Chen X, Makris A, et al. The activity status of cofilin is directly related to invasion, intravasation, and metastasis of mammary tumors. J Cell Biol 2006; 173:395-404.
38. Vitolo MI, Boggs AE, Whipple RA, Yoon JR, Thompson K, Matrone MA, et al. Loss of PTEN induces microtentacles through PI3K-independent activation of cofilin. Oncogene 2013;32:2200-10.
39. Muller CB, de Barros RL, Castro MA, Lopes FM, Meurer RT, Roehe A, et al. Validation of cofilin-1 as a biomarker in non-small cell lung cancer: application of quantitative method in a retrospective cohort. J Cancer Res Clin Oncol 2011;137:1309-16.
40. Pastor MD, Nogal A, Molina-Pinelo S, Melendez R, Salinas A, Gonzalez De la Pena M, et al. Identification of proteomic signatures associated with lung cancer and COPD. J Proteomics 2013;89:227-37.
41. Peng XC, Gong FM, Zhao YW, Zhou LX, Xie YW, Liao HL, et al. Comparative proteomic approach identifies PKM2 and cofilin-1 as potential diagnostic, prognostic and therapeutic targets for pulmonary adenocarcinoma. PLoS ONE 2011;6:e27309.
42. Yang ZL, Miao X, Xiong L, Zou Q, Yuan Y, Li J, et al. CFL1 and Arp3 are biomarkers for metastasis and poor prognosis of squamous cell/adenosquamous carcinomas and adenocarcinomas of gallbladder. Cancer Invest 2013;31:132-9.
43. Medjkane S, Perez-Sanchez C, Gaggioli C, Sahai E, Treisman R. Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat Cell Biol 2009;11:257-68.
44. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 2003;113:329-42.
45. Vartiainen MK, Guettler S, Larijani B, Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 2007;316:1749-52.
46. Zuchero JB, Belin B, Mullins RD. Actin binding to WH2 domains regulates nuclear import of the multifunctional actin regulator JMY. Mol Biol Cell 2012;23:853-63.
47. Hu Q, Kwon YS, Nunez E, Cardamone MD, Hutt KR, Ohgi KA, et al. Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1-dependent gene networking in interchromatin granules. Proc Natl Acad Sci U S A 2008;105:19199-204.
48. Huang W, Ghisletti S, Saijo K, Gandhi M, Aouadi M, Tesz GJ, et al. Coronin 2A mediates actin-dependent de-repression of inflammatory response genes. Nature 2011;470:414-8.
49. Madak-Erdogan Z, Kieser KJ, Kim SH, Komm B, Katzenellenbogen JA, Katzenellenbogen BS. Nuclear and extranuclear pathway inputs in the regulation of global gene expression by estrogen receptors. Mol Endocrinol 2008;22:2116-27.
50. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012;486:346-52.
51. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, et al. Gene-expression profiles to predict distant metastasis of lymph-nodenegative primary breast cancer. Lancet 2005;365:671-9.