Phosphorylation of DCC by ERK2 Is Facilitated by Direct Docking of the Receptor P1 Domain to the Kinase

Structure

Volumn 18, Issue 11, 2010, Pages 1502-1511

  Ma, Wenfu ^a   Shang, Yuan ^b   Wei, Zhiyi ^b   Wen, Wenyu ^a   Wang, Wenning ^a   Zhang, Mingjie ^a,b  

^a FUDAN UNIVERSITY   (China)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN DCC; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

EID: 78149425640     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2010.08.011     Document Type: Article

References (46)

1. Akella R., Moon T.M., Goldsmith E.J. Unique MAP kinase binding sites. Biochim. Biophys. Acta 2008, 1784:48-55.
2. Arakawa H. Netrin-1 and its receptors in tumorigenesis. Nat. Rev. Cancer 2004, 4:978-987.
3. Campbell D.S., Holt C.E. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 2003, 37:939-952.
4. Canagarajah B.J., Khokhlatchev A., Cobb M.H., Goldsmith E.J. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 1997, 90:859-869.
5. Carvalho A.L., Chuang A., Jiang W.W., Lee J., Begum S., Poeta L., Zhao M., Jeronimo C., Henrique R., Nayak C.S., et al. Deleted in colorectal cancer is a putative conditional tumor-suppressor gene inactivated by promoter hypermethylation in head and neck squamous cell carcinoma. Cancer Res. 2006, 66:9401-9407.
6. Chan S.S., Zheng H., Su M.W., Wilk R., Killeen M.T., Hedgecock E.M., Culotti J.G. UNC-40, a C. elegans homolog of DCC (deleted in colorectal cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 1996, 87:187-195.
7. Chang C.I., Xu B.E., Akella R., Cobb M.H., Goldsmith E.J. Crystal structures of MAP kinase p38 complexed to the docking sites on its nuclear substrate MEF2A and activator MKK3b. Mol. Cell 2002, 9:1241-1249.
8. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 2003, 3:11-22.
9. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
10. Fazeli A., Dickinson S.L., Hermiston M.L., Tighe R.V., Steen R.G., Small C.G., Stoeckli E.T., Keino-Masu K., Masu M., Rayburn H., et al. Phenotype of mice lacking functional deleted in colorectal cancer (Dcc) gene. Nature 1997, 386:796-804.
11. Fearon E.R., Cho K.R., Nigro J.M., Kern S.E., Simons J.W., Ruppert J.M., Hamilton S.R., Preisinger A.C., Thomas G., Kinzler K.W., et al. Identification of a chromosome 18q gene that is altered in colorectal cancers. Science 1990, 247:49-56.
12. Fitamant J., Guenebeaud C., Coissieux M.-M., Guix C., Treilleux I., Scoazec J.-Y., Bachelot T., Bernet A., Mehlen P. Netrin-1 expression confers a selective advantage for tumor cell survival in metastatic breast cancer. Proc. Natl. Acad. Sci. USA 2008, 105:4850-4855.
13. Forcet C., Stein E., Pays L., Corset V., Llambi F., Tessier-Lavigne M., Mehlen P. Netrin-1-mediated axon outgrowth requires deleted in colorectal cancer-dependent MAPK activation. Nature 2002, 417:443-447.
14. Goldschneider D., Mehlen P. Dependence receptors: a new paradigm in cell signaling and cancer therapy. Oncogene 2010, 29:1865-1882.
15. Goldsmith E.J., Cobb M.H., Chang C.I. Structure of MAPKs. Methods Mol. Biol. 2004, 250:127-144.
16. Goldsmith E.J., Akella R., Min X., Zhou T., Humphreys J.M. Substrate and docking interactions in serine/threonine protein kinases. Chem. Rev. 2007, 107:5065-5081.
17. Heise C.J., Cobb M.H. Expression and characterization of MAP kinases in bacteria. Methods 2006, 40:209-212.
18. Herbert T.P., Tee A.R., Proud C.G. The extracellular signal-regulated kinase pathway regulates the phosphorylation of 4E-BP1 at multiple sites. J. Biol. Chem. 2002, 277:11591-11596.
19. Hong K., Hinck L., Nishiyama M., Poo M.M., Tessier-Lavigne M., Stein E. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 1999, 97:927-941.
20. Hoshino R., Chatani Y., Yamori T., Tsuruo T., Oka H., Yoshida O., Shimada Y., Ari-i S., Wada H., Fujimoto J., Kohno M. Constitutive activation of the 41-/43-kDa mitogen-activated protein kinase signaling pathway in human tumors. Oncogene 1999, 18:813-822.
21. Keino-Masu K., Masu M., Hinck L., Leonardo E.D., Chan S.S., Culotti J.G., Tessier-Lavigne M. Deleted in colorectal cancer (DCC) encodes a netrin receptor. Cell 1996, 87:175-185.
22. Keleman K., Dickson B.J. Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 2001, 32:605-617.
23. Kolodziej P.A., Timpe L.C., Mitchell K.J., Fried S.R., Goodman C.S., Jan L.Y., Jan Y.N. frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 1996, 87:197-204.
24. Laskowski R.A., Moss D.S., Thornton J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 1993, 231:1049-1067.
25. Leonardo E.D., Hinck L., Masu M., Keino-Masu K., Ackerman S.L., Tessier-Lavigne M. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 1997, 386:833-838.
26. Li X., Meriane M., Triki I., Shekarabi M., Kennedy T.E., Larose L., Lamarche-Vane N. The adaptor protein Nck-1 couples the netrin-1 receptor DCC (deleted in colorectal cancer) to the activation of the small GTPase Rac1 through an atypical mechanism. J. Biol. Chem. 2002, 277:37788-37797.
27. Li W., Lee J., Vikis H.G., Lee S.H., Liu G., Aurandt J., Shen T.L., Fearon E.R., Guan J.L., Han M., et al. Activation of FAK and Src are receptor-proximal events required for netrin signaling. Nat. Neurosci. 2004, 7:1213-1221.
28. Li X., Gao X., Liu G., Xiong W., Wu J., Rao Y. Netrin signal transduction and the guanine nucleotide exchange factor DOCK180 in attractive signaling. Nat. Neurosci. 2008, 11:28-35.
29. Liu G., Beggs H., Jurgensen C., Park H.T., Tang H., Gorski J., Jones K.R., Reichardt L.F., Wu J., Rao Y. Netrin requires focal adhesion kinase and Src family kinases for axon outgrowth and attraction. Nat. Neurosci. 2004, 7:1222-1232.
30. Llambi F., Causeret F., Bloch-Gallego E., Mehlen P. Netrin-1 acts as a survival factor via its receptors UNC5H and DCC. EMBO J. 2001, 20:2715-2722.
31. Mazelin L., Bernet A., Bonod-Bidaud C., Pays L., Arnaud S., Gespach C., Bredesen D.E., Scoazec J.Y., Mehlen P. Netrin-1 controls colorectal tumorigenesis by regulating apoptosis. Nature 2004, 431:80-84.
32. Monick M.M., Powers L.S., Gross T.J., Flaherty D.M., Barrett C.W., Hunninghake G.W. Active ERK contributes to protein translation by preventing JNK-dependent inhibition of protein phosphatase 1. J. Immunol. 2006, 177:1636-1645.
33. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 1997, 53:240-255.
34. Park H.H., Lo Y.-C., Lin S.-C., Wang L., Yang J.K., Wu H. The Death Domain Superfamily in Intracellular Signaling of Apoptosis and Inflammation. Annu. Rev. Immunol. 2007, 25:561-586.
35. Rajasekharan S., Baker K.A., Horn K.E., Jarjour A.A., Antel J.P., Kennedy T.E. Netrin 1 and Dcc regulate oligodendrocyte process branching and membrane extension via Fyn and RhoA. Development 2009, 136:415-426.
36. Remenyi A., Good M.C., Bhattacharyya R.P., Lim W.A. The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol. Cell 2005, 20:951-962.
37. Ren X.R., Ming G.L., Xie Y., Hong Y., Sun D.M., Zhao Z.Q., Feng Z., Wang Q., Shim S., Chen Z.F., et al. Focal adhesion kinase in netrin-1 signaling. Nat. Neurosci. 2004, 7:1204-1212.
38. Storoni L.C., McCoy A.J., Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:432-438.
39. Tcherkezian J., Brittis P.A., Thomas F., Roux P.P., Flanagan J.G. Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 2010, 141:632-644.
40. Thiebault K., Mazelin L., Pays L., Llambi F., Joly M.O., Scoazec J.Y., Saurin J.C., Romeo G., Mehlen P. The netrin-1 receptors UNC5H are putative tumor suppressors controlling cell death commitment. Proc. Natl. Acad. Sci. USA 2003, 100:4173-4178.
41. Xie Y., Ding Y.Q., Hong Y., Feng Z., Navarre S., Xi C.X., Zhu X.J., Wang C.L., Ackerman S.L., Kozlowski D., et al. Phosphatidylinositol transfer protein-alpha in netrin-1-induced PLC signalling and neurite outgrowth. Nat. Cell Biol. 2005, 7:1124-1132.
42. Yang Y., Zou L., Wang Y., Xu K.S., Zhang J.X., Zhang J.H. Axon guidance cue Netrin-1 has dual function in angiogenesis. Cancer Biol. Ther. 2007, 6:743-748.
43. Yang L., Garbe D.S., Bashaw G.J. A frazzled/DCC-dependent transcriptional switch regulates midline axon guidance. Science 2009, 324:944-947.
44. Zhang F., Strand A., Robbins D., Cobb M.H., Goldsmith E.J. Atomic structure of the MAP kinase ERK2 at 2.3 A resolution. Nature 1994, 367:704-711.
45. Zhou T., Sun L., Humphreys J., Goldsmith E.J. Docking interactions induce exposure of activation loop in the MAP kinase ERK2. Structure 2006, 14:1011-1019.
46. Zhu X.J., Wang C.Z., Dai P.G., Xie Y., Song N.N., Liu Y., Du Q.S., Mei L., Ding Y.Q., Xiong W.C. Myosin X regulates netrin receptors and functions in axonal path-finding. Nat. Cell Biol. 2007, 9:184-192.