Defined spatiotemporal features of RAS-ERK signals dictate cell fate in MCF-7 mammary epithelial cells

Molecular Biology of the Cell

Volumn 27, Issue 12, 2016, Pages 1958-1968

  Herrero, Ana ^a,b   Casar, Berta ^a   Colón Bolea, Paula ^a   Agudo Ibáñez, Lorena ^a   Crespo, Piero ^a  

^a UNIVERSITY OF CANTABRIA   (Spain)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NEU DIFFERENTIATION FACTOR; RAS PROTEIN; EPIDERMAL GROWTH FACTOR; HRAS PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN P21;

ADIPOCYTE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; GOLGI COMPLEX; HUMAN; HUMAN CELL; MCF 7 CELL LINE; ONCOGENE H RAS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPATIOTEMPORAL ANALYSIS; DRUG EFFECTS; MAMMARY GLAND; MAPK SIGNALING; MCF-7 CELL LINE; METABOLISM; ONCOGENE RAS; PHYSIOLOGY;

APOPTOSIS; CELL DIFFERENTIATION; EPIDERMAL GROWTH FACTOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENES, RAS; HUMANS; MAMMARY GLANDS, HUMAN; MAP KINASE SIGNALING SYSTEM; MCF-7 CELLS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEUREGULIN-1; PROTO-ONCOGENE PROTEINS P21(RAS); RAS PROTEINS; SIGNAL TRANSDUCTION; SPATIO-TEMPORAL ANALYSIS;

EID: 84974822301     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-02-0118     Document Type: Article

References (42)

1. Agudo-Ibanez L, Herrero A, Barbacid M, Crespo P (2015). H-ras distribution and signaling in plasma membrane microdomains are regulated by acylation and deacylation events. Mol Cell Biol 35, 1898-1914.
2. Agudo-Ibanez L, Nunez F, Calvo F, Berenjeno IM, Bustelo XR, Crespo P (2007). Transcriptomal profiling of site-specific Ras signals. Cell Signal 19, 2264-2276.
3. Ahearn IM, Haigis K, Bar-Sagi D, Philips MR (2011). Regulating the regulator: post-Translational modification of RAS. Nat Rev Mol Cell Biol 13, 39-51.
4. Ajenjo N, Aaronson DS, Ceballos E, Richard C, Le J, Crespo P (2000). Myeloid leukemia cell growth and differentiation are independent of mitogen-Activated protein kinases ERK1/2 activation. J Biol Chem 275, 7189-7197.
5. Albeck JG, Mills GB, Brugge JS (2013). Frequency-modulated pulses of ERK activity transmit quantitative proliferation signals. Mol Cell 49, 249-261.
6. Arozarena I, Aaronson DS, Matallanas D, Sanz V, Ajenjo N, Tenbaum SP, Teramoto H, Ighishi T, Zabala JC, Gutkind JS, et al. (2000). The Rho family GTPase Cdc42 regulates the activation of Ras/MAP kinase by the exchange factor Ras-GRF. J Biol Chem 275, 26441-26448.
7. Arozarena I, Calvo F, Crespo P (2011). Ras, an actor on many stages: posttranslational modifications, localization, and site-specified events. Genes Cancer 2, 182-194.
8. Arozarena I, Matallanas D, Berciano MT, Sanz-Moreno V, Calvo F, Munoz MT, Egea G, Lafarga M, Crespo P (2004). Activation of H-Ras in the endoplasmic reticulum by the RasGRF family guanine nucleotide exchange factors. Mol Cell Biol 24, 1516-1530.
9. Augsten M, Pusch R, Biskup C, Rennert K, Wittig U, Beyer K, Blume A, Wetzker R, Friedrich K, Rubio I (2006). Live-cell imaging of endogenous Ras-GTP illustrates predominant Ras activation at the plasma membrane. EMBO Rep 7, 46-51.
10. Bivona TG, Perez de Castro I, Ahearn IM, Grana TM, Chiu VK, Lockyer PJ, Cullen PJ, Pellicer A, Cox AD, Philips MR (2003). Phospholipase Cg activates Ras on the Golgi apparatus by means of RasGRP1. Nature 424, 694-698.
11. Caloca MJ, Zugaza JL, Bustelo XR (2003). Exchange factors of the RasGRP family mediate Ras activation in the Golgi. J Biol Chem 278, 33465-33473.
12. Calvo F, Agudo-Ibanez L, Crespo P (2010). The Ras-ERK pathway: understanding site-specific signaling provides hope of new anti-Tumor therapies. Bioessays 32, 412-421.
13. Casar B, Rodriguez J, Gibor G, Seger R, Crespo P (2012). Mxi2 sustains ERK1/2 phosphorylation in the nucleus by preventing ERK1/2 binding to phosphatases. Biochem J 441, 571-578.
14. Casar B, Sanz-Moreno V, Yazicioglu MN, Rodriguez J, Berciano MT, Lafarga M, Cobb MH, Crespo P (2007). Mxi2 promotes stimulus-independent ERK nuclear translocation. EMBO J 26, 635-646.
15. Caunt CJ, Keyse SM (2013). Dual-specificity MAP kinase phosphatases (MKPs): shaping the outcome of MAP kinase signalling. FEBS J 280, 489-504.
16. Chiu VK, Bivona T, Hach A, Sajous JB, Silletti J, Wiener H, Johnson RL, Cox AD, Philips MR (2002). Ras signaling on the endoplasmic reticulum and the golgi. Nat Cell Biol 4, 343-350.
17. Choy E, Chiu VK, Silletti J, Feoktistov M, Morimoto T, Michaelson D, Ivanov IE, Philips MR (1999). Endomembrane trafficking of Ras: The CAAX motif targets proteins to the ER and Golgi. Cell 98, 69-80.
18. Formstecher E, Ramos JW, Fauquet M, Calderwood DA, Hsieh JC, Canton B, Nguyen XT, Barnier JV, Camonis J, Ginsberg MH, et al. (2001). PEA-15 mediates cytoplasmic sequestration of ERK MAP kinase. Dev Cell 1, 239-250.
19. Garant KA, Shmulevitz M, Pan L, Daigle RM, Ahn DG, Gujar SA, Lee PW (2016). Oncolytic reovirus induces intracellular redistribution of Ras to promote apoptosis and progeny virus release. Oncogene 35, 771-782.
20. Giani C, Casalini P, Pupa SM, De Vecchi R, Ardini E, Colnaghi MI, Giordano A, Menard S (1998). Increased expression of c-erbB-2 in hormone-dependent breast cancer cells inhibits cell growth and induces differentiation. Oncogene 17, 425-432.
21. Hatakeyama M, Kimura S, Naka T, Kawasaki T, Yumoto N, Ichikawa M, Kim JH, Saito K, Saeki M, Shirouzu M, et al. (2003). A computational model on the modulation of mitogen-Activated protein kinase (MAPK) and Akt pathways in heregulin-induced ErbB signalling. Biochem J 373, 451-463.
22. Kholodenko BN, Hancock JF, Kolch W (2010). Signalling ballet in space and time. Nat Rev Mol Cell Biol 11, 414-426.
23. Liang CC, Chen HC (2001). Sustained activation of extracellular signal-regulated kinase stimulated by hepatocyte growth factor leads to integrin alpha 2 expression that is involved in cell scattering. J Biol Chem 276, 21146-21152.
24. Lorentzen A, Kinkhabwala A, Rocks O, Vartak N, Bastiaens PI (2010). Regulation of Ras localization by acylation enables a mode of intracellular signal propagation. Sci Signal 3, ra68.
25. Mace PD, Wallez Y, Egger MF, Dobaczewska MK, Robinson H, Pasquale EB, Riedl SJ (2013). Structure of ERK2 bound to PEA-15 reveals a mechanism for rapid release of activated MAPK. Nat Commun 4, 1681.
26. Matallanas D, Sanz-Moreno V, Arozarena I, Calvo F, Agudo-Ibanez L, Santos E, Berciano MT, Crespo P (2006). Distinct utilization of effectors and biological outcomes resulting from site-specific Ras activation: Ras functions in lipid rafts and Golgi complex are dispensable for proliferation and transformation. Mol Cell Biol 26, 100-116.
27. McCawley LJ, Li S, Wattenberg EV, Hudson LG (1999). Sustained activation of the mitogen-Activated protein kinase pathway. A mechanism underlying receptor tyrosine kinase specificity for matrix metalloproteinase-9 induction and cell migration. J Biol Chem 274, 4347-4353.
28. Michailovici I, Harrington HA, Azogui HH, Yahalom-Ronen Y, Plotnikov A, Ching S, Stumpf MP, Klein OD, Seger R, Tzahor E (2014). Nuclear to cytoplasmic shuttling of ERK promotes differentiation of muscle stem/progenitor cells. Development 141, 2611-2620.
29. Nagashima T, Shimodaira H, Ide K, Nakakuki T, Tani Y, Takahashi K, Yumoto N, Hatakeyama M (2007). Quantitative transcriptional control of ErbB receptor signaling undergoes graded to biphasic response for cell differentiation. J Biol Chem 282, 4045-4056.
30. Omerovic J, Hammond DE, Clague MJ, Prior IA (2008). Ras isoform abundance and signalling in human cancer cell lines. Oncogene 27, 2754-2762.
31. Peregrin S, Jurado-Pueyo M, Campos PM, Sanz-Moreno V, Ruiz-Gomez A, Crespo P, Mayor F Jr, Murga C (2006). Phosphorylation of p38 by GRK2 at the docking groove unveils a novel mechanism for inactivating p38MAPK. Curr Biol 16, 2042-2047.
32. Pinilla-Macua I, Watkins SC, Sorkin A (2016). Endocytosis separates EGF receptors from endogenous fluorescently labeled HRas and diminishes receptor signaling to MAP kinases in endosomes. Proc Natl Acad Sci USA 113, 2122-2127.
33. Prior IA, Harding A, Yan J, Sluimer J, Parton RG, Hancock JF (2001). GTPdependent segregation of H-ras from lipid rafts is required for biological activity. Nat Cell Biol 3, 368-375.
34. Robinson MJ, Stippec SA, Goldsmith E, White MA, Cobb MH (1998). A constitutively active and nuclear form of MAP kinase ERK2 is sufficient for neurite outgrowth and cell transformation. Curr Biol 8, 1141-1150.
35. Rodriguez J, Calvo F, Gonzalez JM, Casar B, Andres V, Crespo P (2010). ERK1/2 MAP kinases promote cell cycle entry by rapid, kinase-independent disruption of retinoblastoma-lamin A complexes. J Cell Biol 191, 967-979.
36. Rodriguez-Viciana P, Warne PH, Khwaja A, Marte BM, Pappin D, Das P, Waterfield MD, Ridley A, Downward J (1997). Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell 89, 457-467.
37. Santos SD, Verveer PJ, Bastiaens PI (2007). Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat Cell Biol 9, 324-330.
38. Sanz-Moreno V, Casar B, Crespo P (2003). p38alpha isoform Mxi2 binds to extracellular signal-regulated kinase 1 and 2 mitogen-Activated protein kinase and regulates its nuclear activity by sustaining its phosphorylation levels. Mol Cell Biol 23, 3079-3090.
39. Smith ER, Smedberg JL, Rula ME, Xu XX (2004). Regulation of Ras-MAPK pathway mitogenic activity by restricting nuclear entry of activated MAPK in endoderm differentiation of embryonic carcinoma and stem cells. J Cell Biol 164, 689-699.
40. Song SP, Hennig A, Schubert K, Markwart R, Schmidt P, Prior IA, Bohmer FD, Rubio I (2013). Ras palmitoylation is necessary for N-Ras activation and signal propagation in growth factor signalling. Biochem J 454, 323-332.
41. Traverse SN, Gomez N, Paterson H, Marshall CJ, Cohen P (1992). Sustained activation of the mitogen-Activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Biochem J 288, 351-355.
42. Volinsky N, McCarthy CJ, von Kriegsheim A, Saban N, Okada-Hatakeyama M, Kolch W, Kholodenko BN (2015). Signalling mechanisms regulating phenotypic changes in breast cancer cells. Biosci Rep 35, e00178.