LINGO-1 protein interacts with the p75 neurotrophin receptor in intracellular membrane compartments

Journal of Biological Chemistry

Volumn 290, Issue 15, 2015, Pages 9511-9520

  Meabon, James S ^a,c   De Laat, Rian ^d   Ieguchi, Katsuaki ^e   Wiley, Jesse C ^b   Hudson, Mark P ^b   Bothwell, Mark ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d Mental Illness Research Education and Clinical Center Veterans Affairs Medical Center ^*  (United States)

^e TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

University of washington

Indexed keywords

CELL MEMBRANES; COBALT COMPOUNDS; GLYCOPROTEINS;

CO-IMMUNOPRECIPITATION EXPERIMENTS; INTRACELLULAR LOCALIZATION; INTRACELLULAR MEMBRANES; INTRACELLULAR RETENTION; MYELIN BASIC PROTEIN; NOGO-66 RECEPTORS; P75 NEUROTROPHIN RECEPTOR; UNIVERSITY OF WASHINGTON;

PROTEINS;

EARLY ENDOSOME ANTIGEN 1; LEUCINE RICH REPEAT IG DOMAIN CONTAINING NOGO INTERACTING PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MEMBRANE PROTEIN; NEUROTROPHIN RECEPTOR P75; NOGO 66 RECEPTOR; RAB11 PROTEIN; RAB7 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; LINGO1 PROTEIN, HUMAN; MYELIN PROTEIN; NERVE GROWTH FACTOR RECEPTOR; NERVE PROTEIN; NGFR PROTEIN, HUMAN; POLYSACCHARIDE; PROTEIN BINDING; RTN4R PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BIOTINYLATION; BRAIN CORTEX; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CELLULAR DISTRIBUTION; CEREBELLUM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOSOME; GEL ELECTROPHORESIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; INTRACELLULAR MEMBRANE; MITOCHONDRION; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; ANIMAL; BINDING COMPETITION; BRAIN; C57BL MOUSE; CELL MEMBRANE; CYTOLOGY; GENETICS; HEK293 CELL LINE; METABOLISM; MUTATION; NERVE CELL; NEWBORN;

ANIMALS; ANIMALS, NEWBORN; BINDING, COMPETITIVE; BRAIN; CELL MEMBRANE; GPI-LINKED PROTEINS; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MUTATION; MYELIN PROTEINS; NERVE TISSUE PROTEINS; NEURONS; POLYSACCHARIDES; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RECEPTORS, NERVE GROWTH FACTOR;

EID: 84927130665     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.608018     Document Type: Article

References (33)

1. Mi, S., Lee, X., Shao, Z., Thill, G., Ji, B., Relton, J., Levesque, M., Allaire, N., Perrin, S., Sands, B., Crowell, T., Cate, R. L., McCoy, J. M., and Pepinsky, R. B. (2004) LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 7, 221-228
2. Fournier, A. E., GrandPré, T., and Strittmatter, S. M. (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409, 341-346
3. Liu, B. P., Fournier, A., GrandPré, T., and Strittmatter, S. M. (2002) My-elin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 297, 1190-1193
4. Shao, Z., Browning, J. L., Lee, X., Scott, M. L., Shulga-Morskaya, S., Allaire, N., Thill, G., Levesque, M., Sah, D., McCoy, J. M., Murray, B., Jung, V., Pepinsky, R. B., and Mi, S. (2005) TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 45, 353-359
5. Mi, S., Miller, R. H., Lee, X., Scott, M. L., Shulag-Morskaya, S., Shao, Z., Chang, J., Thill, G., Levesque, M., Zhang, M., Hession, C., Sah, D., Trapp, B., He, Z., Jung, V., McCoy, J. M., and Pepinsky, R. B. (2005) LINGO-1 negatively regulates myelination by oligodendrocytes. Nat. Neurosci. 8, 745-751
6. Lee, X., Yang, Z., Shao, Z., Rosenberg, S. S., Levesque, M., Pepinsky, R. B., Qiu, M., Miller, R. H., Chan, J. R., and Mi, S. (2007) NGF regulates the expression of axonal LINGO-1 to inhibit oligodendrocyte differentiation and myelination. J. Neurosci. 27, 220-225
7. Jepson, S., Vought, B., Gross, C. H., Gan, L., Austen, D., Frantz, J. D., Zwahlen, J., Lowe, D., Markland, W., and Krauss, R. (2012) LINGO-1, a transmembrane signaling protein, inhibits oligodendrocyte differentiation and myelination through intercellular self-interactions. J. Biol. Chem. 287, 22184-22195
8. Inoue, H., Lin, L., Lee, X., Shao, Z., Mendes, S., Snodgrass-Belt, P., Sweigard, H., Engber, T., Pepinsky, B., Yang, L., Beal, M. F., Mi, S., and Isacson, O. (2007) Inhibition of the leucine-rich repeat protein LINGO-1 enhances survival, structure, and function of dopaminergic neurons in Parkinson's disease models. Proc. Natl. Acad. Sci. U.S.A. 104, 14430-14435
9. Lööv, C., Fernqvist, M., Walmsley, A., Marklund, N., and Erlandsson, A. (2012) Neutralization of LINGO-1 during in vitro differentiation of neural stem cells results in proliferation of immature neurons. PLoS ONE 7, e29771
10. Bai, Y., Markham, K., Chen, F., Weerasekera, R., Watts, J., Horne, P., Wakutani, Y., Bagshaw, R., Mathews, P. M., Fraser, P. E., Westaway, D., St George-Hyslop, P., and Schmitt-Ulms, G. (2008) The in vivo brain interactome of the amyloid precursor protein. Mol. Cell. Proteomics 7, 15-34
11. Zhong, X., Pocas, J., Liu, Y., Wu, P. W., Mosyak, L., Somers, W., and Kriz, R. (2009) Swift residue-screening identifies key N-glycosylated asparagines sufficient for surface expression of neuroglycoprotein Lingo-1. FEBS Lett. 583, 1034-1038
12. Kanning, K. C., Hudson, M., Amieux, P. S., Wiley, J. C., Bothwell, M., and Schecterson, L. C. (2003) Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability. J. Neurosci. 23, 5425-5436
13. Wong, S. T., Henley, J. R., Kanning, K. C., Huang, K. H., Bothwell, M., and Poo, M. M. (2002) A p75NTR and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci. 5, 1302-1308
14. Dilly, K. W., Rossow, C. F., Votaw, V. S., Meabon, J. S., Cabarrus, J. L., and Santana, L. F. (2006) Mechanisms underlying variations in excitationcontraction coupling across the mouse left ventricular free wall. J. Physiol. 572, 227-241
15. Carim-Todd, L., Escarceller, M., Estivill, X., and Sumoy, L. (2003) LRRN6A/LERN1 (leucine-rich repeat neuronal protein 1), a novel gene with enriched expression in limbic system and neocortex. Eur. J. Neurosci. 18, 3167-3182
16. Mosyak, L., Wood, A., Dwyer, B., Buddha, M., Johnson, M., Aulabaugh, A., Zhong, X., Presman, E., Benard, S., Kelleher, K., Wilhelm, J., Stahl, M. L., Kriz, R., Gao, Y., Cao, Z., Ling, H. P., Pangalos, M. N., Walsh, F. S., and Somers, W. S. (2006) The structure of the Lingo-1 ectodomain, a module implicated in central nervous system repair inhibition. J. Biol. Chem. 281, 36378-36390
17. Mandai, K., Guo, T., St Hillaire, C., Meabon, J. S., Kanning, K. C., Bothwell, M., and Ginty, D. D. (2009) LIG family receptor tyrosine kinase-associated proteins modulate growth factor signals during neural development. Neuron 63, 614-627
18. Rubin, C., Gur, G., and Yarden, Y. (2005) Negative regulation of receptor tyrosine kinases: unexpected links to c-Cbl and receptor ubiquitylation. Cell Res. 15, 66-71
19. Bandtlow, C., and Dechant, G. (2004) From cell death to neuronal regeneration, effects of the p75 neurotrophin receptor depend on interactions with partner subunits. Sci. STKE 2004, pe24
20. Park, J. B., Yiu, G., Kaneko, S., Wang, J., Chang, J., He, X. L., Garcia, K. C., and He, Z. (2005) A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 45, 345-351
21. Gonzalez, A., and Rodriguez-Boulan, E. (2009) Clathrin and AP1B: key roles in basolateral trafficking through trans-endosomal routes. FEBS Lett. 583, 3784-3795
22. Domeniconi, M., Zampieri, N., Spencer, T., Hilaire, M., Mellado, W., Chao, M. V., and Filbin, M. T. (2005) MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth. Neuron 46, 849-855
23. Urra, S., Escudero, C. A., Ramos, P., Lisbona, F., Allende, E., Covarrubias, P., Parraguez, J. I., Zampieri, N., Chao, M. V., Annaert, W., and Bronfman, F. C. (2007) TrkA receptor activation by nerve growth factor induces shedding of the p75 neurotrophin receptor followed by endosomal γ-secretase-mediated release of the p75 intracellular domain. J. Biol. Chem. 282, 7606-7615
24. Escudero, C. A., Lazo, O. M., Galleguillos, C., Parraguez, J. I., Lopez-Verrilli, M. A., Cabeza, C., Leon, L., Saeed, U., Retamal, C., Gonzalez, A., Marzolo, M. P., Carter, B. D., Court, F. A., and Bronfman, F. C. (2014) The p75 neurotrophin receptor evades the endolysosomal route in neuronal cells, favouring multivesicular bodies specialised for exosomal release. J. Cell Sci. 127, 1966-1979
25. Zhang, Z., Xu, X., Zhang, Y., Zhou, J., Yu, Z., and He, C. (2009) LINGO-1 interacts with WNK1 to regulate Nogo-induced inhibition of neurite extension. J. Biol. Chem. 284, 15717-15728
26. Lee, B. H., Min, X., Heise, C. J., Xu, B. E., Chen, S., Shu, H., Luby-Phelps, K., Goldsmith, E. J., and Cobb, M. H. (2004) WNK1 phosphorylates synaptotagmin 2 and modulates its membrane binding. Mol. Cell 15, 741-751
27. Fu, Y., Subramanya, A., Rozansky, D., and Cohen, D. M. (2006) WNK kinases influence TRPV4 channel function and localization. Am. J. Physiol. Renal Physiol. 290, F1305-F1314
28. Golbang, A. P., Cope, G., Hamad, A., Murthy, M., Liu, C. H., Cuthbert, A. W., and O'Shaughnessy, K. M. (2006) Regulation of the expression of the Na/Cl cotransporter by WNK4 and WNK1: evidence that accelerated dynamin-dependent endocytosis is not involved. Am. J. Physiol. Renal Physiol. 291, F1369-F1376
29. Cope, G., Murthy, M., Golbang, A. P., Hamad, A., Liu, C. H., Cuthbert, A. W., and O'Shaughnessy, K. M. (2006) WNK1 affects surface expression of the ROMK potassium channel independent of WNK4. J. Am. Soc. Nephrol. 17, 1867-1874
30. Jiang, Y., Cong, P., Williams, S. R., Zhang, W., Na, T., Ma, H. P., and Peng, J. B. (2008) WNK4 regulates the secretory pathway via which TRPV5 is targeted to the plasma membrane. Biochem. Biophys. Res. Commun. 375, 225-229
31. Subramanya, A. R., Liu, J., Ellison, D. H., Wade, J. B., and Welling, P. A. (2009) WNK4 diverts the thiazide-sensitive NaCl cotransporter to the lysosome and stimulates AP-3 interaction. J. Biol. Chem. 284, 18471-18480
32. Fang, L., Garuti, R., Kim, B. Y., Wade, J. B., and Welling, P. A. (2009) The ARH adaptor protein regulates endocytosis of the ROMK potassium secretory channel in mouse kidney. J. Clin. Invest. 119, 3278-3289
33. Wiedemann, U., Boisguerin, P., Leben, R., Leitner, D., Krause, G., Moelling, K., Volkmer-Engert, R., and Oschkinat, H. (2004) Quantification of PDZ domain specificity, prediction of ligand affinity and rational design of super-binding peptides. J. Mol. Biol. 343, 703-718