Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions

Journal of Neuroscience

Volumn 23, Issue 13, 2003, Pages 5393-5406

  Oertle, Thomas ^a   Van der Haar, Marjan E ^a   Bandtlow, Christine E ^b   Robeva, Anna ^c   Burfeind, Patricia ^c   Buss, Armin ^a   Huber, Andrea B ^a,e   Simonen, Mario ^a,d   Schnell, Lisa ^a   Brösamle, Christian ^a,f   Kaupmann, Klemens ^d   Vallon, Rüdiger ^c   Schwab, Martin E ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF INNSBRUCK   (Austria)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^d NOVARTIS PHARMA AG   (Switzerland)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f GEOPHYSICAL LABORATORY   (United States)

Author keywords

Active sites; Inhibitory regions; Membrane topology; Neurite outgrowth; Nogo; Reticulon

Indexed keywords

BIOTIN; EPITOPE; GENE PRODUCT; PROTEIN NOGO A; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL SPREADING; CELL SURFACE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FIBROBLAST; GROWTH CONE; IMMUNOFLUORESCENCE; MEMBRANE STRUCTURE; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT;

EID: 0038384089     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-13-05393.2003     Document Type: Article

References (74)

1. Amberger VR, Hensel T, Ogata N, Schwab ME (1998) Spreading and migration of human glioma and rat C6 cells on central nervous system myelin in vitro is correlated with tumor malignancy and involves a metalloproteolytic activity. Cancer Res 58:149-158.
2. Bandtlow CE, Löschinger J (1997) Developmental changes in neuronal responsiveness to the CNS myelin-associated neurite growth inhibitor NI-35/250. Eur J Neurosci 9:2743-2752.
3. Bandtlow CE, Zachleder T, Schwab ME (1990) Oligodendrocytes arrest neurite growth by contact inhibition. J Neurosci 10:3837-3848.
4. Bandtlow CE, Schmidt MF, Hassinger TD, Schwab ME, Kater SB (1993) Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones. Science 259:80-83.
5. Behar O, Mizuno K, Neumann S, Woolf CJ (2000) Putting the spinal cord together again. Neuron 26:291-293.
6. Belien ATJ, Paganetti PA, Schwab ME (1999) Membrane-type 1 matrix metalloprotease (MTI-MMP) enables invasive migration of glioma cells in central nervous system white matter. J Cell Biol 144:373-383.
7. Bradbury NA (1999) Intracellular CFTR: localization and function. Physiol Rev 79:175-191.
8. Buffo A, Zagrebelsky M, Huber AB, Skerra A, Schwab ME, Strata P, Rossi F (2000) Application of neutralizing antibodies against NI-35/250 myelin-associated neurite growth inhibitory proteins to the adult rat cerebellum induces sprouting of uninjured Purkinje cell axons. J Neurosci 20:2275-2286.
9. Bush KT, Stuart RO, Li SH, Moura LA, Sharp AH, Ross CA, Nigam SK (1994) Epithelial inositol 1,4,5-trisphosphate receptors. Multiplicity of localization, solubility, and isoforms. J Biol Chem 269:23694-23699.
10. Caroni P, Schwab ME (1988) Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J Cell Biol 106:1281-1288.
11. Chen MS, Schnell L, van der Haar ME, Oertle T, Schwab ME (1999) Inhibitory activity and domain(s) of the myelin protein Nogo-A. Soc Neurosci Abstr 25:2030.
12. Chen MS, Huber AB, van der Haar ME, Frank M, Schnell L, Spillmann AA, Christ F, Schwab ME (2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403:434-439.
13. Cocquerel L, Op dB, Lambot M, Roussel J, Delgrange D, Pillez A, Wychowski C, Penin F, Dubuisson J (2002) Topological changes in the transmembrane domains of hepatitis C virus envelope glycoproteins. EMBO J 21:2893-2902.
14. Croul S, Mezitis SG, Stieber A, Chen YJ, Gonatas JO, Goud B, Gonatas NK (1990) Immunocytochemical visualization of the Golgi apparatus in several species, including human, and tissues with an antiserum against MG-160, a sialoglycoprotein of rat Golgi apparatus. J Histochem Cytochem 38:957-963.
15. Cunningham AM, Ryugo DK, Sharp AH, Reed RR, Snyder SH, Ronnett GV (1993) Neuronal inositol 1,4,5-trisphosphate receptor localized to the plasma membrane of olfactory cilia. Neuroscience 57:339-352.
16. De Strooper B, Beullens M, Contreras B, Levesque L, Craessaerts K, Cordell B, Moechars D, Bollen M, Fraser P, George-Hyslop PS, Van Leuven F (1997) Phosphorylation, subcellular localization, and membrane orientation of the Alzheimer's disease-associated presenilins. J Biol Chem 272:3590-3598.
17. Domeniconi M, Cao Z, Spencer T, Sivasankaran R, Wang KC, Nikulina E, Kimura N, Cai H, Deng K, Gao Y, He Z, Filbin MT (2002) Myelin-associated glycoprotein interacts with the Nogo66 receptor to inhibit neurite outgrowth. Neuron 35:283-290.
18. Donato R (1999) Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1450:191-231.
19. Fernandez C, Adeishvili K, Wuthrich K (2001) Transverse relaxation-optimized NMR spectroscopy with the outer membrane protein OmpX in dihexanoyl phosphatidylcholine micelles. Proc Natl Acad Sci USA 98:2358-2363.
20. Flanagan JG, Leder P (1990) The kit ligand: a cell surface molecule altered in steel mutant fibroblasts. Cell 63:185-194.
21. Fournier AE, GrandPre T, Strittmatter SM (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409:341-346.
22. Fritsche J, Reber BFX, Schindelholz B, Bandtlow CE (1999) Differential cytoskeletal changes during growth cone collapse in response to hSemalll and thrombin. Mol Cell Neurosci 14:398-418.
23. Goder V, Spiess M (2001) Topogenesis of membrane proteins: determinants and dynamics. FEBS Lett 504:87-93.
24. Goldberg JL, Barres BA (2000) Nogo in nerve regeneration. Nature 403:369-370.
25. Gonatas JO, Mezitis SG, Stieber A, Fleischer B, Gonatas NK (1989) MG-160. A novel sialoglycoprotein of the medial cisternae of the Golgi apparatus. J Biol Chem 264:646-653.
26. Gonatas JO, Mourelatos Z, Stieber A, Lane WS, Brosius J, Gonatas NK (1995) MG-160, a membrane sialoglycoprotein of the medial cisternae of the rat Golgi apparatus, binds basic fibroblast growth factor and exhibits a high level of sequence identity to a chicken fibroblast growth factor receptor. J Cell Sci 108:457-467.
27. GrandPré T, Nakamura F, Vartanian T, Strittmatter SM (2000) Identification of the Nogo inhibitor of axon regeneration as a reticulon protein. Nature 403:439-444.
28. Hegde RS, Mastrianni JA, Scott MR, DeFea KA, Tremblay P, Torchia M, DeArmond SJ, Prusiner SB, Lingappa VR (1998) A transmembrane form of the prion protein in neurodegenerative disease. Science 279:827-834.
29. Huber AB, Weinmann O, Brosamle C, Oertle T, Schwab ME (2002) Patterns of nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J Neurosci 22:3553-3567.
30. Kaupmann K, Huggel K, Heid J, Flor PJ, Bischoff S, Mickel SJ, McMaster G, Angst C, Bittiger H, Froestl W, Bettler B (1997) Expression cloning of GABA(B) receptors uncovers similarity to metabotropic glutamate receptors. Nature 386:239-246.
31. Kelleher DJ, Kreibich G, Gilmore R (1992) Oligosaccharyltransferase activity is associated with a protein complex composed of ribophorins I and II and a 48 kd protein. Cell 69:55-65.
32. Lee FS, Kim AH, Khursigara G, Chao MV (2001) The uniqueness of being a neurotrophin receptor. Curr Opin Neurobiol 11:281-286.
33. Levy D (1996) Membrane proteins which exhibit multiple topological orientations. Essays Biochem 31:49-60.
34. Li X, Saint CP, Aktories K, Lamarche-Vane N (2002) Rac1 and Cdc42 but not RhoA or Rho kinase activities are required for neurite outgrowth induced by the Netrin-1 receptor DCC (deleted in colorectal cancer) in N1E-115 neuroblastoma cells. J Biol Chem 277:15207-15214.
35. Liu BP, Fournier A, GrandPre T, Strittmatter SM (2002) Myelin-associated glycoprotein as a functional ligand for the nogo-66 receptor. Science 297:1190-1193.
36. Loschinger J, Bandtlow CE, Jung J, Klostermann S, Schwab ME, Bonhoeffer F, Kater SB (1997) Retinal axon growth cone responses to different environmental cues are mediated by different second-messenger systems. J Neurobiol 33:825-834.
37. Lu Y, Xiong X, Helm A, Kimani K, Bragin A, Skach WR (1998) Co- and posttranslational translocation mechanisms direct cystic fibrosis transmembrane conductance regulator N terminus transmembrane assembly. J Biol Chem 273:568-576.
38. Mayrleitner M, Schafer R, Fleischer S (1995) IP3 receptor purified from liver plasma membrane is an (1,4,5)IP3 activated and (1,3,4,5)IP4 inhibited calcium permeable ion channel. Cell Calcium 17:141-153.
39. Merril CR, Dunau ML, Goldman D (1981) A rapid sensitive silver stain for polypeptides in polyacrylamide gels. Anal Biochem 110:201-207.
40. Monne M, Gafvelin G, Nilsson R, von Heijne G (1999) N-tail translocation in a eukaryotic polytopic membrane protein: synergy between neighboring transmembrane segments. Eur J Biochem 263:264-269.
41. Moreira EF, Jaworski CJ, Rodriguez IR (1999) Cloning of a novel member of the reticulon gene family (RTN3): gene structure and chromosomal localization to 11q13. Genomics 58:73-81.
42. Morris NJ, Ross SA, Neveu JM, Lane WS, Lienhard GE (1999) Cloning and characterization of a 22 kDa protein from rat adipocytes: a new member of the reticulon family. Biochim Biophys Acta 1450:68-76.
43. Niederöst B, Zimmermann DR, Schwab ME, Bandtlow CE (1999) Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycan. J Neurosci 19:8979-8989.
44. Niederost B, Oertle T, Fritsche J, McKinney RA, Bandtlow CE (2002) Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Racl. J Neurosci 22:10368-10376.
45. Nilsson I, Witt S, Kiefer H, Mingarro I, von Heijne G (2000) Distant downstream sequence determinants can control N-tail translocation during protein insertion into the endoplasmic reticulum membrane. J Biol Chem 275:6207-6213.
46. Oertle T, Bandtlow CE, Schwab ME (2000) Characterization of the gene structure and the inhibitory regions of Nogo-RTN4. Soc Neurosci Abstr 26:573.
47. Oertle T, Merkler D, Schwab ME (2003a) Do cancer cells die because of Nogo-B? Oncogene 22:1390-1399.
48. Oertle T, Huber C, van der Putten H, Schwab ME (2003b) Genomic structure and functional characterisation of the promoters of human and mouse Nogo/Rtn-4. J Mol Biol 325:299-323.
49. Oertle T, Klinger M, Stuermer CAO, Schwab ME (2003c) A reticular rhapsody: phylogenic evolution and nomenclature of the RTN/Nogo gene family. FASEB J, in press.
50. Olpe HR, Karlsson G, Pozza MF, Brugger F, Steinmann M, Van Riezen H, Fagg G, Hall RG, Froestl W, Bittiger H (1990) CGP 35348: a centrally active blocker of GABAB receptors. Eur J Pharmacol 187:27-38.
51. Ostapchuk P, Hearing P, Ganem D (1994) A dramatic shift in the transmembrane topology of a viral envelope glycoprotein accompanies hepatitis B viral morphogenesis. EMBO J 13:1048-1057.
52. Prinjha R, Moore SE, Vinson M, Blake S, Morrow R, Christie G, Michalovich D, Simmons DL, Walsh FS (2000) Inhibitor of neurite outgrowth in humans. Nature 403:383-384.
53. Quinton TM, Dean WL (1996) Multiple inositol 1,4,5-trisphosphate receptor isoforms are present in platelets. Biochem Biophys Res Commun 224:740-746.
54. Roebroek AJM, van de Velde HJK, Van Bokhoven A, Broers JLV, Ramaekers FCS, Van de Ven WJM (1994) Cloning and expression of alternative transcripts of a novel neuroendocrine-specific gene and identification of its 135-kDa translational product. J Biol Chem 268:13439-13447.
55. Roebroek AJ, Contreras B, Pauli IG, Van de Ven WJ (1998) cDNA cloning, genomic organization, and expression of the human RTN2 gene, a member of a gene family encoding reticulons. Genomics 51:98-106.
56. Rubin BP, Spillmann AA, Bandtlow CE, Keller F, Schwab ME (1995) Inhibition of PC12 cell attachment and neurite outgrowth by detergent solubilized CNS myelin proteins. Eur J Neurosci 7:2524-2529.
57. Schmalfeldt M, Bandtlow CE, Dours-Zimmermann MT, Winterhalter KH, Zimmermann DR (2000) Brain derived versican V2 is a potent inhibitor of axonal growth. J Cell Sci 113:807-816.
58. Schwab ME, Bartholdi D (1996) Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 76:319-370.
59. Schwab ME, Caroni P (1988) Oligodendrocytes and CNS myelin are non-permissive substrates for neurite growth and fibroblast spreading in vitro. J Neurosci 8:2381-2393.
60. Spillmann AA, Bandtlow CE, Lottspeich F, Keller F, Schwab ME (1998) Identification and characterization of a bovine neurite growth inhibitor (bNI-220). J Biol Chem 273:19283-19293.
61. Tagami S, Eguchi Y, Kinoshita M, Takeda M, Tsujimoto Y (2000) A novel protein, RTN-XS, interacts with both Bcl-XL and Bcl-2 on endoplasmic reticulum and reduces their anti-apoptotic activity. Oncogene 19:5736-5746.
62. Tamagnone L, Artigiani S, Chen H, He Z, Ming G, Song H, Chedotal A, Winberg ML, Goodman CS, Poo M-M, Tessier-Lavigne M, Comoglio PM (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99:71-80.
63. Tanimura A, Tojyo Y, Turner RJ (2000) Evidence that type I, II, and III inositol 1,4,5-trisphosphate receptors can occur as integral plasma membrane proteins. J Biol Chem 275:27488-27493.
64. Ughrin YM, Chen ZJ, Levine JM (2003) Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J Neurosci 23:175-186.
65. van de Velde HJK, Roebroek AJ, Senden NH, Ramaekers FC, Van de Ven WJ (1994) NSP-encoded reticulons, neuroendocrine proteins of a novel gene family associated with membranes of the endoplasmic reticulum. J Cell Sci 107:2403-2416.
66. van der Haar ME, Visser HW, de Vries H, Hoekstra D (1998) Transport of proteolipid protein to the plasma membrane does not depend on glycosphingolipid cotransport in oligodendrocyte cultures. J Neurosci Res 51:371-381.
67. Vielmetter J, Stolze B, Bonhoeffer F, Stuermer CA (1990) In vitro assay to test differential substrate affinities of growing axons and migratory cells. Exp Brain Res 81:283-287.
68. Vyas AA, Patel HV, Fromholt SE, Heffer-Lauc M, Vyas KA, Dang J, Schachner M, Schnaar RL (2002) Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration. Proc Natl Acad Sci USA 99:8412-8417.
69. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, He Z (2002a) Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417:941-944.
70. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z (2002b) p75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420:74-78.
71. Wang X, Chun SJ, Treloar H, Vartanian T, Greer CA, Strittmatter SM (2002c) Localization of nogo-a and nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J Neurosci 22:5505-5515.
72. Wiessner C, Bareyre FM, Allegrini PR, Mir AK, Frentzel S, Zurini M, Schnell L, Oertle T, Schwab ME (2003) Anti Nogo-A antibody infusion 24 hours after experimental stroke improved behavioral outcome and corticospinal plasticity in normotensive and spontaneously hypertensive rats. J Cereb Blood Flow Metab 23:154-165.
73. Winton MJ, Dubreuil CI, Lasko D, Leclerc N, McKerracher L (2002) Characterization of new cell permeable C3-like proteins that inactivate Rho and stimulate neurite outgrowth on inhibitory substrates. J Biol Chem 277:32820-32829.
74. Yamashita T, Higuchi H, Tohyama M (2002) The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J Cell Biol 157:565-570.