Structure and axon outgrowth inhibitor binding of the Nogo-66 receptor and related proteins

EMBO Journal

Volumn 22, Issue 13, 2003, Pages 3291-3302

  Barton, William A ^a   Liu, Betty P ^b   Tzvetkova, Dorothea ^a   Jeffrey, Philip D ^a   Fournier, Alyson E ^b   Sah, Dinah ^c   Cate, Richard ^c   Strittmatter, Stephen M ^b   Nikolov, Dimitar B ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BIOGEN   (United States)

Author keywords

Axon outgrowth; Leucine rich repeats; Ligand binding; Nogo 66 receptor

Indexed keywords

CELL SURFACE PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; LEUCINE; MAG PROTEIN; MYELIN; NGR PROTEIN; NGR2 PROTEIN; NGR3 PROTEIN; NOGO 66 RECEPTOR; OMGP PROTEIN; PROTEIN; PROTEIN NOGO; RECEPTOR; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; BRAIN INJURY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EMBRYO; GENE DELETION; HUMAN; HUMAN CELL; LEUCINE RICH REPEAT; LIGAND BINDING; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SURFACE PROPERTY;

AMINO ACID SEQUENCE; ANIMALS; AXONS; CRYSTALLIZATION; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYELIN PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, CELL SURFACE; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA;

EID: 0038263895     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg325     Document Type: Article

References (53)

1. Bandtlow, C., Zachleder, T. and Schwab, M.E. (1990) Oligodendrocytes arrest neurite growth by contact inhibition. J. Neurosci., 10, 3837-3848.
2. Bartsch, U. et al. (1995) Lack of evidence that myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS. Neuron, 15, 1375-1381.
3. Brunger, A.T. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D, 54, 905-921.
4. CCP4 (1994) The CCP4 suite: programs for X-ray crystallography. Acta Crystallogr. D, 50, 760-763.
5. David, S. and Aguayo, A.J. (1981) Axonal elongation into peripheral nervous system 'bridges' after central nervous system injury in adult rats. Science, 214, 931-933.
6. Davies, S.J., Fitch, M.T., Memberg, S.P., Hall, A.K., Raisman, G. and Silver, J. (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature, 390, 680-683.
7. NTR: novel functions and implications for diseases of the nervous system. Nat. Neurosci., 5, 1131-1136.
8. Domeniconi, M. et al. (2002) Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron, 35, 283-290.
9. Dou, C.L. and Levine, J.M. (1994) Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J. Neurosci., 14, 7616-7628.
10. Evdokimov, A.G., Anderson, D.E., Routzahn, K.M. and Waugh, D.S. (2001) Unusual molecular architecture of thee Yersinia pestis cytotoxin M: a leucine rich repeat protein with the shortest repeating unit. J. Mol. Biol., 312, 807-821.
11. Fournier, A.E., GrandPre, T. and Strittmatter, S.M. (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature, 409, 341-346.
12. Fournier, A.E., Gould, G.C., Liu, B.P. and Strittmatter, S.M. (2002) Truncated soluble Nogo receptor binds Nogo-66 and blocks inhibition of axon growth by myelin. J. Neurosci., 22, 8876-8883.
13. Fournier, A.E., Takizawa, B.T. and Strittmatter, S.M. (2003) Rho kinase inhibition enhances axonal regeneration in the injured CNS. J. Neurosci., 23, 1416-1423.
14. GrandPre, T., Nakamura, F., Vartanian, T. and Strittmatter, S.M. (2000) Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature, 403, 439-444.
15. GrandPre, T., Li, S. and Strittmatter, S.M. (2002) Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature, 417, 547-551.
16. He, X.L., Bazan, J.F., McDermott, G., Park, J.B., Wang, K., Tessier-Lavigne, M., He, Z. and Garcia, K.C. (2003) Structure of the nogo receptor ectodomain. A recognition module implicated in myelin inhibition. Neuron, 38, 177-185.
17. Hendrickson, W.A. (1991) Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science, 254, 51-58.
18. Heras, B., Edeling, M.A., Byriel, K.A., Jones, A., Raina, S. and Martin, J.L. (2003) Dehydration converts DsbG crystal diffraction from low to high resolution. Structure, 11, 139-145.
19. Holm, L. and Sander, C. (1998) Touring protein fold space with DALI/FSSP. Nucleic Acids Res., 26, 316-319.
20. Huber, A.B. and Schwab, M.E. (2000) Nogo-A, a potent inhibitor of neurite outgrowth and regeneration. Biol. Chem., 381, 407-419.
21. Huizinga, E.G., Tsuji, S., Romijn, R.A.P., Schiphorst, M.E., de Groot, P.G., Sixma, J.J. and Gros, P. (2002) Structures of the glycoprotein Ibα and its complex with von Willebrand factor A1 domain. Science, 297, 1176-1179.
22. Jones, T.A., Zou, J.Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A, 47, 110-119.
23. Kim, J.E., Bonilla, I.E., Qiu, D. and Strittmatter, S.M. (2003a) Nogo-C is sufficient to delay nerve regeneration. Mol. Cell. Neurosci., in press.
24. Kim, J.E., Li, S., GrandPre, T., Qiu, D. and Strittmatter, S.M. (2003b) Axon regeneration in young adult mice lacking Nogo-A/B. Neuron, 38, 187-199.
25. Kobe, B. and Deisenhofer, J. (1993) Crystal structure of porcine ribonuclease inhibitor; a protein with leucine rich repeats. Nature, 366, 751-756.
26. Kobe, B. and Deisenhofer, J. (1995) A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature, 374, 183-186.
27. Kobe, B. and Kajava, A.V. (2001) The leucine rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol., 11, 725-732.
28. Kraulis, P.J. (1991) Molscript: A program to produce both detailed and schematic plots of portein structures. J. Appl. Cryst., 24, 946-950.
29. Li, S. and Strittmatter, S.M. (2003) Delayed systemic nogo-66 receptor antagonist promotes recovery from spinal cord injury. J. Neurosci., 23, 4219-4127.
30. Liu, B.P., Fournier, A., GrandPre, T. and Strittmatter, S.M. (2002) Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science, 297, 1190-1193.
31. Marino, M., Braun, L., Cossart, P. and Ghosh, P. (1999) Structure of the InlB leucine rich repeats, a domain that triggers host cell invasion by the pathogen L.monocytogenes. Mol. Cell, 4, 1063-1072.
32. McGee, A.W. and Strittmatter, S.M. (2003) The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci., 26, 193-198.
33. McKerracher, L., David, S., Jackson, D.L., Kottis, V., Dunn, R.J. and Braun, P.E. (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron, 13, 805-811.
34. Merrit, E.A. and Bacon, D.J. (1997) Raster3D Version 2: Photorealistic molecular graphics. Methods Enzymol., 277, 505-524.
35. Mukhopadhyay, G., Doherty, P., Walsh, F.S., Crocker, P.R. and Filbin, M.T. (1994) A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron, 13, 757-767.
36. Nicholls, A., Sharp, K. and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins, 11, 281-296.
37. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326.
38. Papageorgiou, A.C., Shapiro, R. and Acharya, K.R. (1997) Molecular recognition of human angiogenin by placental ribonuclease inhibitor - an x-ray crystallographic study at 2.0 Å resolution. EMBO J., 16, 5162-5177.
39. Pignot, V. et al. (2003) Characterization of two novel proteins, NgRH1 and NgRH2, structurally and biochemically homologous to the Nogo-66 receptor. J. Neurochem., 85, 717-728.
40. Pot, C. et al. (2002) Nogo-A expressed in Schwann cells impairs axonal regeneration after peripheral nerve injury. J. Cell Biol., 159, 29-35.
41. Prinjha, R., Moore, S.E., Vinson, M., Blake, S., Morrow, R., Christie, G., Michalovich, D., Simmons, D.L. and Walsh, F. S. (2000) Inhibitor of neurite outgrowth in humans. Nature, 403, 383-384.
42. Raineteau, O., Z'Graggen, W.J., Thallmair, M. and Schwab, M. E. (1999) Sprouting and regeneration after pyramidotomy and blockade of the myelin-associated neurite growth inhibitors NI 35/250 in adult rats. Eur. J. Neurosci., 11, 1486-1490.
43. Richardson, P.M., McGuinness, U.M. and Aguayo, A.J. (1980) Axons from CNS neurons regenerate into PNS grafts. Nature, 284, 264-265.
44. Roux, P.P. and Barker, P.A. (2002) Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol., 67, 203-233.
45. Savio, T. and Schwab, M.E. (1989) Rat CNS white matter, but not gray matter, is nonpermissive for neuronal cell adhesion and fiber outgrowth. J. Neurosci., 9, 1126-1133.
46. Schafer, M., Fruttiger, M., Montag, D., Schachner, M. and Martini, R. (1996) Disruption of the gene for the myelin-associated glycoprotein improves axonal regrowth along myelin in C57BL/Wlds mice. Neuron, 16, 1107-1113.
47. Schnell, L. and Schwab, M.E. (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature, 343, 269-272.
48. Schwab, M.E. and Caroni, P. (1988) Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. J. Neurosci., 8, 2381-2393.
49. Snow, D. M., Lemmon, V., Carrino, D.A., Caplan, A.I. and Silver, J. (1990) Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol., 109, 111-130.
50. Thallmair, M., Metz, G.A., Z'Graggen, W.J., Raineteau, O., Kartje, G.L. and Schwab, M.E. (1998) Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat. Neurosci., 1, 124-131.
51. Wang, K.C., Koprivica, V., Kim, J.A., Sivasankaran, R., Guo, Y., Neve, R.L. and He, Z. (2002a) Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature, 417, 941-944.
52. Wang, K.C., Kim, J.A., Sivasankaran, R., Segal, R. and He, Z. (2002b) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature, 420, 74-78.
53. NTR and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci., 5. 1302-1308.