Signaling mechanism of the netrin-1 receptor DCC in axon guidance

Progress in Biophysics and Molecular Biology

Volumn 118, Issue 3, 2015, Pages 153-160

  Finci, L ^a,b   Zhang, Y ^a   Meijers, R ^c   Wang, J H ^a,b  

^a PEKING UNIVERSITY   (China)

^b HARVARD MEDICAL SCHOOL   (United States)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Axon guidance; DCC; Netrin 1; Structure; UNC5

Indexed keywords

CELL SURFACE RECEPTOR; DCC PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL; AXON; CHEMISTRY; CYTOPLASM; HUMAN; METABOLISM; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CYTOPLASM; HUMANS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84952631661     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2015.04.001     Document Type: Review

References (48)

1. Ahmed G., Shinmyo Y., Ohta K., Islam S.M., Hossain M., Naser I.B., Riyadh M.A., Su Y., Zhang S., Tessier-Lavigne M., Tanaka H. Draxin inhibits axonal outgrowth through the netrin receptor DCC. J. Neurosci. 2011, 31:14018-14023.
2. Arakawa H. Netrin-1 and its receptors in tumorigenesis. Nat. Rev. Cancer 2004, 4:978-987.
3. Bredesen D.E., Mehlen P., Rabizadeh S. Receptors that mediate cellular dependence. Cell death Differ. 2005, 12:1031-1043.
4. Castets M., Broutier L., Molin Y., Brevet M., Chazot G., Gadot N., Paquet A., Mazelin L., Jarrosson-Wuilleme L., Scoazec J.Y., Bernet A., Mehlen P. DCC constrains tumour progression via its dependence receptor activity. Nature 2012, 482:534-537.
5. 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.
6. Chen Q., Sun X., Zhou X.H., Liu J.H., Wu J., Zhang Y., Wang J.H. N-terminal horseshoe conformation of DCC is functionally required for axon guidance and might be shared by other neural receptors. J. Cell. Sci. 2013, 126:186-195.
7. Cirulli V., Yebra M. Netrins: beyond the brain. Nat. Rev. Mol. Cell. Biol. 2007, 8:296-306.
8. Dickson B.J. Molecular mechanisms of axon guidance. Science 2002, 298:1959-1964.
9. Dyson H.J., Wright P.E. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell. Biol. 2005, 6:197-208.
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., Simons J., Bronson R.T., Gordon J.I., Tessier-Lavigne M., Weinberg R.A. 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. Finci L.I., Kruger N., Sun X., Zhang J., Chegkazi M., Wu Y., Schenk G., Mertens H.D., Svergun D.I., Zhang Y., Wang J.H., Meijers R. The crystal structure of netrin-1 in complex with DCC reveals the bifunctionality of netrin-1 as a guidance cue. Neuron 2014, 83:839-849.
13. Freigang J., Proba K., Leder L., Diederichs K., Sonderegger P., Welte W. The crystal structure of the ligand binding module of axonin-1/TAG-1 suggests a zipper mechanism for neural cell adhesion. Cell 2000, 101:425-433.
14. Geisbrecht B.V., Dowd K.A., Barfield R.W., Longo P.A., Leahy D.J. Netrin binds discrete subdomains of DCC and UNC5 and mediates interactions between DCC and heparin. J. Biol. Chem. 2003, 278:32561-32568.
15. Goldschneider D., Mehlen P. Dependence receptors: a new paradigm in cell signaling and cancer therapy. Oncogene 2010, 29:1865-1882.
16. Haddick P.C., Tom I., Luis E., Quinones G., Wranik B.J., Ramani S.R., Stephan J.P., Tessier-Lavigne M., Gonzalez L.C. Defining the ligand specificity of the deleted in colorectal cancer (DCC) receptor. PLoS ONE 2014, 9:e84823.
17. 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.
18. Islam S.M., Shinmyo Y., Okafuji T., Su Y., Naser I.B., Ahmed G., Zhang S., Chen S., Ohta K., Kiyonari H., Abe T., Tanaka S., Nishinakamura R., Terashima T., Kitamura T., Tanaka H. Draxin, a repulsive guidance protein for spinal cord and forebrain commissures. Science 2009, 323:388-393.
19. 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.
20. Kennedy T.E., Serafini T., de la Torre J.R., Tessier-Lavigne M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 1994, 78:425-435.
21. Keynes R., Cook G.M. Axon guidance molecules. Cell 1995, 83:161-169.
22. Kidd T., Russell C., Goodman C.S., Tear G. Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 1998, 20:25-33.
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. Krimpenfort P., Song J.Y., Proost N., Zevenhoven J., Jonkers J., Berns A. Deleted in colorectal carcinoma suppresses metastasis in p53-deficient mammary tumours. Nature 2012, 482:538-541.
25. Kruger R.P., Lee J., Li W., Guan K.L. Mapping netrin receptor binding reveals domains of Unc5 regulating its tyrosine phosphorylation. J. Neurosci. 2004, 24:10826-10834.
26. Lee J.S., Chien C.B. When sugars guide axons: insights from heparan sulphate proteoglycan mutants. Nat. Rev. Genet. 2004, 5:923-935.
27. 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.
28. Leung-Hagesteijn C., Spence A.M., Stern B.D., Zhou Y., Su M.W., Hedgecock E.M., Culotti J.G. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 1992, 71:289-299.
29. 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.
30. 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.
31. Ma W., Shang Y., Wei Z., Wen W., Wang W., Zhang M. Phosphorylation of DCC by ERK2 is facilitated by direct docking of the receptor P1 domain to the kinase. Structure 2010, 18:1502-1511.
32. Mehlen P., Furne C. Netrin-1: when a neuronal guidance cue turns out to be a regulator of tumorigenesis. Cell. Mol. Life Sci. 2005, 62:2599-2616.
33. Meijers R., Puettmann-Holgado R., Skiniotis G., Liu J.H., Walz T., Wang J.H., Schmucker D. Structural basis of Dscam isoform specificity. Nature 2007, 449:487-491.
34. Meyerhardt J.A., Look A.T., Bigner S.H., Fearon E.R. Identification and characterization of neogenin, a DCC-related gene. Oncogene 1997, 14:1129-1136.
35. Rigato C., Buckinx R., Le-Corronc H., Rigo J.M., Legendre P. Pattern of invasion of the embryonic mouse spinal cord by microglial cells at the time of the onset of functional neuronal networks. Glia 2011, 59:675-695.
36. Sawaya M.R., Wojtowicz W.M., Andre I., Qian B., Wu W., Baker D., Eisenberg D., Zipursky S.L. A double S shape provides the structural basis for the extraordinary binding specificity of Dscam isoforms. Cell 2008, 134:1007-1018.
37. Serafini T., Colamarino S.A., Leonardo E.D., Wang H., Beddington R., Skarnes W.C., Tessier-Lavigne M. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 1996, 87:1001-1014.
38. Serafini T., Kennedy T.E., Galko M.J., Mirzayan C., Jessell T.M., Tessier-Lavigne M. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 1994, 78:409-424.
39. Shipp E.L., Hsieh-Wilson L.C. Profiling the sulfation specificities of glycosaminoglycan interactions with growth factors and chemotactic proteins using microarrays. Chem. Biol. 2007, 14:195-208.
40. Stein E., Zou Y., Poo M., Tessier-Lavigne M. Binding of DCC by netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation. Science 2001, 291:1976-1982.
41. Su X.D., Gastinel L.N., Vaughn D.E., Faye I., Poon P., Bjorkman P.J. Crystal structure of hemolin: a horseshoe shape with implications for homophilic adhesion. Science 1998, 281:991-995.
42. Tessier-Lavigne M. Wiring the brain: the logic and molecular mechanisms of axon guidance and regeneration. Harvey Lect. 2002, 98:103-143.
43. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science 1996, 274:1123-1133.
44. Tong J., Killeen M., Steven R., Binns K.L., Culotti J., Pawson T. Netrin stimulates tyrosine phosphorylation of the UNC-5 family of netrin receptors and induces Shp2 binding to the RCM cytodomain. J. Biol. Chem. 2001, 276:40917-40925.
45. Wang J.-H., Springer T.A. Structural specializations of immunoglobulin superfamily members for adhesion to integrins and viruses. Immunol. Rev. 1998, 163:197-215.
46. Wei Z., Yan J., Lu Q., Pan L., Zhang M. Cargo recognition mechanism of myosin X revealed by the structure of its tail MyTH4-FERM tandem in complex with the DCC P3 domain. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3572-3577.
47. Xu K., Wu Z., Renier N., Antipenko A., Tzvetkova-Robev D., Xu Y., Minchenko M., Nardi-Dei V., Rajashankar K.R., Himanen J., Tessier-Lavigne M., Nikolov D.B. Neural migration. Structures of netrin-1 bound to two receptors provide insight into its axon guidance mechanism. Science 2014, 344:1275-1279.
48. 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.