Cell density-dependent inhibition of epidermal growth factor receptor signaling by p38α mitogen-activated protein kinase via sprouty2 downregulation

Molecular and Cellular Biology

Volumn 29, Issue 12, 2009, Pages 3332-3343

  Swat, Aneta ^a   Dolado, Ignacio ^a   Rojas, Jose Maria ^b   Nebreda, Angel R ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; ENZYME INHIBITOR; ENZYME INHIBITOR SPRY2; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 14; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE SIAH2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL CYCLE ARREST; CELL DENSITY; CELL GROWTH; CELL PROLIFERATION; CONTACT INHIBITION; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MITOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; UPREGULATION;

ANIMALS; BASE SEQUENCE; CELL COUNT; CELL CYCLE; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CONTACT INHIBITION; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DNA PRIMERS; DOWN-REGULATION; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 14; MODELS, BIOLOGICAL; NIH 3T3 CELLS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 67649211582     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01955-08     Document Type: Article

References (46)

1. Abercrombie, M. 1979. Contact inhibition and malignancy. Nature 281:259-262. (Pubitemid 10225333)
2. Alfonso, P., I. Dolado, A. Swat, A. Nunez, A. Cuadrado, A. R. Nebreda, and J. I. Casal. 2006. Proteomic analysis of p38alpha mitogen-activated protein kinase-regulated changes in membrane fractions of RAS-transformed fibroblasts. Proteomics 6(Suppl. 1):S262-S271.
3. Alonso, G., C. Ambrosino, M. Jones, and A. R. Nebreda. 2000. Differential activation of p38 mitogen-activated protein kinase isoforms depending on signal strength. J. Biol. Chem. 275:40641-40648.
4. Ambrosino, C., G. Mace, S. Galban, C. Fritsch, K. Vintersten, E. Black, M. Gorospe, and A. R. Nebreda. 2003. Negative feedback regulation of MKK6 mRNA stability by p38α mitogen-activated protein kinase. Mol. Cell. Biol. 23:370-381.
5. Balmanno, K., and S. J. Cook. 1999. Sustained MAP kinase activation is required for the expression of cyclin D1, p21Cip1 and a subset of AP-1 proteins in CCL39 cells. Oncogene 18:3085-3097. (Pubitemid 29261229)
6. Besson, A., S. F. Dowdy, and J. M. Roberts. 2008. CDK inhibitors: cell cycle regulators and beyond. Dev. Cell 14:159-169. (Pubitemid 351189186)
7. Bloom, J., and M. Pagano. 2003. Deregulated degradation of the cdk inhibitor p27 and malignant transformation. Semin. Cancer Biol. 13:41-47.
8. Bulavin, D. V., and A. J. Fornace, Jr. 2004. p38 MAP kinase's emerging role as a tumor suppressor. Adv. Cancer Res. 92:95-118.
9. Carter, S. B. 1968. Tissue homeostasis and the biological basis of cancer. Nature 220:970-974.
10. Cho, Y. S., J. M. Bae, Y. S. Chun, J. H. Chung, Y. K. Jeon, I. S. Kim, M. S. Kim, and J. W. Park. 2008. HIF-1alpha controls keratinocyte proliferation by up-regulating p21(WAF1/Cip1). Biochim. Biophys. Acta 1783:323-333.
11. Chu, I., J. Sun, A. Arnaout, H. Kahn, W. Hanna, S. Narod, P. Sun, C. K. Tan, L. Hengst, and J. Slingerland. 2007. p27 phosphorylation by Src regulates inhibition of cyclin E-Cdk2. Cell 128:281-294. (Pubitemid 46123510)
12. Curto, M., and A. I. McClatchey. 2008. Nf2/Merlin: a coordinator of receptor signalling and intercellular contact. Br J. Cancer 98:256-262. (Pubitemid 351161230)
13. Dolado, I., A. Swat, N. Ajenjo, G. De Vita, A. Cuadrado, and A. R. Nebreda. 2007. p38alpha MAP kinase as a sensor of reactive oxygen species in tumorigenesis. Cancer Cell 11:191-205. (Pubitemid 46209847)
14. Faust, D., I. Dolado, A. Cuadrado, F. Oesch, C. Weiss, A. R. Nebreda, and C. Dietrich. 2005. p38alpha MAPK is required for contact inhibition. Oncogene 24:7941-7945. (Pubitemid 41715200)
15. Frey, M. R., R. S. Dise, K. L. Edelblum, and D. B. Polk. 2006. p38 kinase regulates epidermal growth factor receptor downregulation and cellular migration. EMBO J. 25:5683-5692. (Pubitemid 44967752)
16. Fuse, T., M. Tanikawa, M. Nakanishi, K. Ikeda, T. Tada, H. Inagaki, K. Asai, T. Kato, and K. Yamada. 2000. p27Kip1 expression by contact inhibition as a prognostic index of human glioma. J. Neurochem. 74:1393-1399. (Pubitemid 30163958)
17. Grimmler, M., Y. Wang, T. Mund, Z. Cilensek, E. M. Keidel, M. B. Waddell, H. Jakel, M. Kullmann, R. W. Kriwacki, and L. Hengst. 2007. Cdk-inhibitory activity and stability of p27Kip1 are directly regulated by oncogenic tyrosine kinases. Cell 128:269-280. (Pubitemid 46123508)
18. Grovdal, L. M., E. Stang, A. Sorkin, and I. H. Madshus. 2004. Direct interaction of Cbl with pTyr 1045 of the EGF receptor (EGFR) is required to sort the EGFR to lysosomes for degradation. Exp. Cell Res. 300:388-395.
19. Hall, A. B., N. Jura, J. DaSilva, Y. J. Jang, D. Gong, and D. Bar-Sagi. 2003. hSpry2 is targeted to the ubiquitin-dependent proteasome pathway by c-Cbl. Curr. Biol. 13:308-314.
20. Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100:57-70. (Pubitemid 30046295)
21. Ishida, N., M. Kitagawa, S. Hatakeyama, and K. Nakayama. 2000. Phosphorylation at serine 10, a major phosphorylation site of p27(Kip1), increases its protein stability. J. Biol. Chem. 275:25146-25154.
22. Jozic, D., N. Cardenes, Y. L. Deribe, G. Moncalian, D. Hoeller, Y. Groemping, I. Dikic, K. Rittinger, and J. Bravo. 2005. Cbl promotes clustering of endocytic adaptor proteins. Nat. Struct. Mol. Biol. 12:972-979.
23. Khurana, A., K. Nakayama, S. Williams, R. J. Davis, T. Mustelin, and Z. Ronai. 2006. Regulation of the ring finger E3 ligase Siah2 by p38 MAPK. J. Biol. Chem. 281:35316-35326.
24. Kiyokawa, H., R. D. Kineman, K. O. Manova-Todorova, V. C. Soares, E. S. Hoffman, M. Ono, D. Khanam, A. C. Hayday, L. A. Frohman, and A. Koff. 1996. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 85:721-732. (Pubitemid 126334352)
25. Levenberg, S., A. Yarden, Z. Kam, and B. Geiger. 1999. p27 is involved in N-cadherin-mediated contact inhibition of cell growth and S-phase entry. Oncogene 18:869-876. (Pubitemid 29086263)
26. Levine, E. M., Y. Becker, C. W. Boone, and H. Eagle. 1965. Contact inhibition, macromolecular synthesis, and polyribosomes in cultured human diploid fibroblasts. Proc. Natl. Acad. Sci. USA 53:350-356.
27. Levkowitz, G., H. Waterman, E. Zamir, Z. Kam, S. Oved, W. Y. Langdon, L. Beguinot, B. Geiger, and Y. Yarden. 1998. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12:3663-3674. (Pubitemid 29019647)
28. Lito, P., B. D. Mets, S. Kleff, S. O'Reilly, V. M. Maher, and J. J. McCormick. 2008. Evidence that sprouty 2 is necessary for sarcoma formation by H-Ras oncogene-transformed human fibroblasts. J. Biol. Chem. 283:2002-2009.
29. Martin, A., J. Odajima, S. L. Hunt, P. Dubus, S. Ortega, M. Malumbres, and M. Barbacid. 2005. Cdk2 is dispensable for cell cycle inhibition and tumor suppression mediated by p27(Kip1) and p21(Cip1). Cancer Cell 7:591-598. (Pubitemid 40799251)
30. Martinez, N., C. A. Garcia-Dominguez, B. Domingo, J. L. Oliva, N. Zarich, A. Sanchez, S. Gutierrez-Eisman, J. Llopis, and J. M. Rojas. 2007. Sprouty2 binds Grb2 at two different proline-rich regions, and the mechanism of ERK inhibition is independent of this interaction. Cell Signal. 19:2277-2285. (Pubitemid 47371084)
31. Mason, J. M., D. J. Morrison, B. Bassit, M. Dimri, H. Band, J. D. Licht, and I. Gross. 2004. Tyrosine phosphorylation of Sprouty proteins regulates their ability to inhibit growth factor signaling: a dual feedback loop. Mol. Biol. Cell 15:2176-2188.
32. Nadeau, R. J., J. L. Toher, X. Yang, D. Kovalenko, and R. Friesel. 2007. Regulation of Sprouty2 stability by mammalian Seven-in-Absentia homolog 2. J. Cell Biochem. 100:151-160. (Pubitemid 44958186)
33. Polyak, K., J. Y. Kato, M. J. Solomon, C. J. Sherr, J. Massague, J. M. Roberts, and A. Koff. 1994. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev. 8:9-22. (Pubitemid 2042846)
34. Schmidt, M. H., and I. Dikic. 2005. The Cbl interactome and its functions. Nat. Rev. Mol. Cell Biol. 6:907-918.
35. Shtiegman, K., B. S. Kochupurakkal, Y. Zwang, G. Pines, A. Starr, A. Vexler, A. Citri, M. Katz, S. Lavi, Y. Ben-Basat, S. Benjamin, S. Corso, J. Gan, R. B. Yosef, S. Giordano, and Y. Yarden. 2007. Defective ubiquitinylation of EGFR mutants of lung cancer confers prolonged signaling. Oncogene 26:6968-6978. (Pubitemid 350014608)
36. Sibilia, M., A. Fleischmann, A. Behrens, L. Stingl, J. Carroll, F. M. Watt, J. Schlessinger, and E. F. Wagner. 2000. The EGF receptor provides an essential survival signal for SOS-dependent skin tumor development. Cell 102:211-220.
37. Tsvetkov, L. M., K. H. Yeh, S. J. Lee, H. Sun, and H. Zhang. 1999. p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. Curr. Biol. 9:661-664.
38. Ventura, J. J., S. Tenbaum, E. Perdiguero, M. Huth, C. Guerra, M. Barbacid, M. Pasparakis, and A. R. Nebreda. 2007. p38alpha MAP kinase is essential in lung stem and progenitor cell proliferation and differentiation. Nat. Genet. 39:750-758.
39. Vergarajauregui, S., A. San Miguel, and R. Puertollano. 2006. Activation of p38 mitogen-activated protein kinase promotes epidermal growth factor receptor internalization. Traffic 7:686-698. (Pubitemid 43676977)
40. Weber, J. D., D. M. Raben, P. J. Phillips, and J. J. Baldassare. 1997. Sustained activation of extracellular-signal-regulated kinase 1 (ERK1) is required for the continued expression of cyclin D1 in G1 phase. Biochem. J. 326(Pt. 1):61-68. (Pubitemid 27386918)
41. Wieser, R. J., D. Faust, C. Dietrich, and F. Oesch. 1999. p16INK4 mediates contact-inhibition of growth. Oncogene 18:277-281. (Pubitemid 29060603)
42. Wong, E. S., C. W. Fong, J. Lim, P. Yusoff, B. C. Low, W. Y. Langdon, and G. R. Guy. 2002. Sprouty2 attenuates epidermal growth factor receptor ubiquitylation and endocytosis, and consequently enhances Ras/ERK signalling. EMBO J. 21:4796-4808.
43. Yanagisawa, K., A. Kosaka, H. Iwahana, M. Nakanishi, and S. Tominaga. 1999. Opposite regulation of the expression of cyclin-dependent kinase inhibitors during contact inhibition. J. Biochem. 125:36-40. (Pubitemid 29085959)
44. Zeng, Q., and W. Hong. 2008. The emerging role of the hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 13:188-192. (Pubitemid 351318373)
45. Zhao, B., X. Wei, W. Li, R. S. Udan, Q. Yang, J. Kim, J. Xie, T. Ikenoue, J. Yu, L. Li, P. Zheng, K. Ye, A. Chinnaiyan, G. Halder, Z. C. Lai, and K. L. Guan. 2007. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21:2747-2761. (Pubitemid 350070721)
46. Zwang, Y., and Y. Yarden. 2006. p38 MAP kinase mediates stress-induced internalization of EGFR: implications for cancer chemotherapy. EMBO J. 25:4195-4206. (Pubitemid 44435217)