16
Views
20
CrossRef citations to date
0
Altmetric
Article

Establishment of Extracellular Signal-Regulated Kinase 1/2 Bistability and Sustained Activation through Sprouty 2 and Its Relevance for Epithelial Function

, , , , , , , , & show all
Pages 1783-1799 | Received 29 Jul 2009, Accepted 19 Jan 2010, Published online: 20 Mar 2023

REFERENCES

  • Bashor, C. J., N. C. Helman, S. Yan, and W. A. Lim. 2008. Using engineered scaffold interactions to reshape MAP kinase pathway signaling dynamics. Science 319:1539–1543.
  • Bhattacharya, M., N. Ojha, S. Solanki, C. K. Mukhopadhyay, R. Madan, N. Patel, G. Krishnamurthy, S. Kumar, S. K. Basu, and A. Mukhopadhyay. 2006. IL-6 and IL-12 specifically regulate the expression of Rab5 and Rab7 via distinct signaling pathways. EMBO J. 25:2878–2888.
  • Casci, T., J. Vinós, and M. Freeman. 1999. Sprouty, an intracellular inhibitor of Ras signaling. Cell 96:655–665.
  • Chandramouli, S., C. Y. Yu, P. Yusoff, D. H. Lao, H. F. Leong, K. Mizuno, and G. R. Guy. 2008. Tesk1 interacts with Spry2 to abrogate its inhibition of ERK phosphorylation downstream of receptor tyrosine kinase signaling. J. Biol. Chem. 283:1679–1691.
  • Das, J., M. Ho, J. Zikherman, C. Govern, M. Yang, A. Weiss, A. K. Chakraborty, and J. P. Roose. 2009. Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell 136:337–351.
  • DaSilva, J., L. Xu, H. J. Kim, W. T. Miller, and D. Bar-Sagi. 2006. Regulation of sprouty stability by Mnk1-dependent phosphorylation. Mol. Cell. Biol. 26:1898–1907.
  • Day, C. L., H. Puthalakath, G. Skea, A. Strasser, I. Barsukov, L. Y. Lian, D. C. Huang, and M. G. Hinds. 2004. Localization of dynein light chains 1 and 2 and their pro-apoptotic ligands. Biochem. J. 377:597–605.
  • Edwin, F., R. Singh, R. Endersby, S. J. Baker, and T. B. Patel. 2006. The tumor suppressor PTEN is necessary for human Sprouty 2-mediated inhibition of cell proliferation. J. Biol. Chem. 281:4816–4822.
  • Egan, J. E., A. B. Hall, B. A. Yatsula, and D. Bar-Sagi. 2002. The bimodal regulation of epidermal growth factor signaling by human Sprouty proteins. Proc. Natl. Acad. Sci. U. S. A. 99:6041–6046.
  • Ferrell, J. E., and W. Xiong. 2001. Bistability in cell signaling: how to make continuous processes discontinuous, and reversible processes irreversible. Chaos 11:227–236.
  • Fixman, E. D., A. Stewart, and J. G. Martin. 2007. Basic mechanisms of development of airway structural changes in asthma. Eur. Respir. J. 29:379–389.
  • Formstecher, E., J. W. Ramos, M. Fauquet, D. A. Calderwood, J. C. Hsieh, B. Canton, X. T. Nguyen, J. V. Barnier, J. Camonis, M. H. Ginsberg, and H. Chneiweiss. 2001. PEA-15 mediates cytoplasmic sequestration of ERK MAP kinase. Dev. Cell 1:239–250.
  • Goplen, N., M. Z. Karim, Q. Liang, M. M. Gorska, S. Rozario, L. Guo, and R. Alam. 2009. Combined sensitization of mice to extracts of dust mite, ragweed, and Aspergillus species breaks through tolerance and establishes chronic features of asthma. J. Allergy Clin. Immunol. 123:925–932.e11.
  • Gorska, M. M., S. J. Stafford, O. Cen, S. Sur, and R. Alam. 2004. Unc119, a novel activator of Lck/Fyn, is essential for T cell activation. J. Exp. Med. 199:369–379.
  • Hacohen, N., S. Kramer, D. Sutherland, Y. Hiromi, and M. A. Krasnow. 1998. Sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92:253–263.
  • 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.
  • Hanafusa, H., S. Torii, T. Yasunaga, and E. Nishida. 2002. Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 4:850–858.
  • Hervagault, J. F., and S. Canu. 1987. Bistability and irreversible transitions in a simple substrate cycle. J. Theor. Biol. 127:439–449.
  • Impagnatiello, M. A., S. Weitzer, G. Gannon, A. Compagni, M. Cotten, and G. Christofori. 2001. Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J. Cell Biol. 152:1087–1098.
  • Inder, K., A. Harding, S. J. Plowman, M. R. Philips, R. G. Parton, and J. F. Hancock. 2008. Activation of the MAPK module from different spatial locations generates distinct system outputs. Mol. Biol. Cell 19:4776–4784.
  • Jacquier, A., E. Buhler, M. K. Schäfer, D. Bohl, S. Blanchard, C. Beclin, and G. Haase. 2006. Alsin/Rac1 signaling controls survival and growth of spinal motoneurons. Ann. Neurol. 60:105–117.
  • Kangaspeska, S., B. Stride, R. Métivier, M. Polycarpou-Schwarz, D. Ibberson, R. P. Carmouche, V. Benes, F. Gannon, and G. Reid. 2008. Transient cyclical methylation of promoter DNA. Nature 452:112–115.
  • Kim, H. J., L. J. Taylor, and D. Bar-Sagi. 2007. Spatial regulation of EGFR signaling by Sprouty2. Curr. Biol. 17:455–461.
  • Klein, O. D., G. Minowada, R. Peterkova, A. Kangas, B. D. Yu, H. Lesot, M. Peterka, J. Jernvall, and G. R. Martin. 2006. Sprouty genes control diastema tooth development via bidirectional antagonism of epithelial-mesenchymal FGF signaling. Dev. Cell 11:181–190.
  • Kramer, S., M. Okabe, N. Hacohen, M. A. Krasnow, and Y. Hiromi. 1999. Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 126:2515–2525.
  • Lao, D. H., S. Chandramouli, P. Yusoff, C. W. Fong, T. Y. Saw, L. P. Tai, C. Y. Yu, H. F. Leong, and G. R. Guy. 2006. A Src homology 3-binding sequence on the C terminus of Sprouty2 is necessary for inhibition of the Ras/ERK pathway downstream of fibroblast growth factor receptor stimulation. J. Biol. Chem. 281:29993–30000.
  • Lee, P. J., X. Zhang, P. Shan, B. Ma, C. G. Lee, R. J. Homer, Z. Zhu, M. Rincon, B. T. Mossman, and J. A. Elias. 2006. ERK1/2 mitogen-activated protein kinase selectively mediates IL-13-induced lung inflammation and remodeling in vivo. J. Clin. Invest. 116:163–173.
  • Lin, J., A. Harding, E. Giurisato, and A. S. Shaw. 2009. KSR1 modulates the sensitivity of mitogen-activated protein kinase pathway activation in T cells without altering fundamental system outputs. Mol. Cell. Biol. 29:2082–2091.
  • Lisman, J. E. 1985. A mechanism for memory storage insensitive to molecular turnover: a bistable autophosphorylating kinase. Proc. Natl. Acad. Sci. U. S. A. 82:3055–3057.
  • Liu, W., Q. Liang, S. Balzar, S. Wenzel, M. Gorska, and R. Alam. 2008. Cell-specific activation profile of extracellular signal-regulated kinase 1/2, Jun N-terminal kinase, and p38 mitogen-activated protein kinases in asthmatic airways. J. Allergy Clin. Immunol. 121:893–902.e2.
  • Lu, A., F. Tebar, B. Alvarez-Moya, C. López-Alcalá, M. Calvo, C. Enrich, N. Agell, T. Nakamura, M. Matsuda, and O. Bachs. 2009. A clathrin-dependent pathway leads to KRas signaling on late endosomes en route to lysosomes. J. Cell Biol. 184:863–879.
  • Macia, J., S. Regot, T. Peeters, N. Conde, R. Solé, and F. Posas. 2009. Dynamic signaling in the Hog1 MAPK pathway relies on high basal signal transduction. Sci. Signal. 2(63):ra13.
  • Markevich, N. I., J. B. Hoek, and B. N. Kholodenko. 2004. Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades. J. Cell Biol. 164:353–359.
  • Métivier, R., G. Penot, M. R. Hübner, G. Reid, H. Brand, M. Kos, and F. Gannon. 2003. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115:751–763.
  • Moarefi, I., M. LaFevre-Bernt, F. Sicheri, M. Huse, C. H. Lee, J. Kuriyan, and W. T. Miller. 1997. Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature 385:650–653.
  • 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.
  • Nechamen, C. A., R. M. Thomas, and J. A. Dias. 2007. APPL1, APPL2, Akt2 and FOXO1a interact with FSHR in a potential signaling complex. Mol. Cell. Endocrinol. 260-262:93–99.
  • Qui, M., and S. Green. 1992. PC12 cell neuronal differentiation is associated with prolonged p21ras activity and consequent prolonged ERK activity. Neuron 9:705–717.
  • Rao, N., I. Dodge, and H. Band. 2002. The Cbl family of ubiquitin ligases: critical negative regulators of tyrosine kinase signaling in the immune system. J. Leukoc. Biol. 71:753–763.
  • Romero Rosales, K., E. R. Peralta, G. G. Guenther, S. Y. Wong, and A. L. Edinger. 2009. Rab7 activation by growth factor withdrawal contributes to the induction of apoptosis. Mol. Biol. Cell 20:2831–2840.
  • Rubin, C., V. Litvak, H. Medvedovsky, Y. Zwang, S. Lev, and Y. Yarden. 2003. Sprouty fine-tunes EGF signaling through interlinked positive and negative feedback loops. Curr. Biol. 13:297–307.
  • Rubin, C., Y. Zwang, N. Vaisman, D. Ron, and Y. Yarden. 2005. Phosphorylation of carboxyl-terminal tyrosines modulates the specificity of Sprouty-2 inhibition of different signaling pathways. J. Biol. Chem. 280:9735–9744.
  • Schenck, A., L. Goto-Silva, C. Collinet, M. Rhinn, A. Giner, B. Habermann, M. Brand, and M. Zerial. 2008. The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133:486–497.
  • Tefft, D., M. Lee, S. Smith, D. L. Crowe, S. Bellusci, and D. Warburton. 2002. mSprouty2 inhibits FGF10-activated MAP kinase by differentially binding to upstream target proteins. Am. J. Physiol. Lung Cell. Mol. Physiol. 283:L700–L706.
  • Tian, T., A. Harding, K. Inder, S. Plowman, R. G. Parton, and J. F. Hancock. 2007. Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat. Cell Biol. 9:905–914.
  • Topp, J. D., N. W. Gray, R. D. Gerard, and B. F. Horazdovsky. 2004. Alsin is a Rab5 and Rac1 guanine nucleotide exchange factor. J. Biol. Chem. 279:24612–24623.
  • Traverse, S., N. Gomez, H. Paterson, C. Marshall, and P. Cohen. 1992. Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288:351–355.
  • Tresini, M., A. Lorenzini, C. Torres, and V. J. Cristofalo. 2007. Modulation of replicative senescence of diploid human cells by nuclear ERK signaling. J. Biol. Chem. 282:4136–4151.
  • Valdembri, D., P. T. Caswell, K. I. Anderson, J. P. Schwarz, I. König, E. Astanina, F. Caccavari, J. C. Norman, M. J. Humphries, F. Bussolino, and G. Serini. 2009. Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol. 7:e25.
  • Wang, J., W. H. Shen, Y. J. Jin, P. W. Brandt-Rauf, and Y. Yin. 2007. A molecular link between E2F-1 and the MAPK cascade. J. Biol. Chem. 282:18521–18531.
  • Wills-Karp, M., and F. D. Finkelman. 2008. Untangling the complex web of IL-4- and IL-13-mediated signaling pathways. Sci. Signal. 1:pe55.
  • 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.
  • Xiong, W., and J. E. Ferrell Jr. 2003. A positive-feedback-based bistable ‘memory module’ that governs a cell fate decision. Nature 426:460–465.
  • Yigzaw, Y., H. M. Poppleton, N. Sreejayan, A. Hassid, and T. B. Patel. 2003. Protein-tyrosine phosphatase-1B (PTP1B) mediates the anti-migratory actions of Sprouty. J. Biol. Chem. 278:284–288.
  • Yildirim, N., M. Santillan, D. Horike, and M. C. Mackey. 2004. Dynamics and bistability in a reduced model of the lac operon. Chaos 14:279–292.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.