Metabotropic glutamate receptors transduce signals for neurite outgrowth after binding of the prion protein to laminin γ1 chain

FASEB Journal

Volumn 25, Issue 1, 2011, Pages 265-279

  Beraldo, Flavio H ^a,e   Arantes, Camila P ^a,b   Santos, Tiago G ^a,c   Machado, Cleiton F ^a,c   Roffe, Martin ^d   Hajj, Gláucia N ^a   Lee, Kil S ^a   Magalhães, Ana C ^e   Caetano, Fabiana A ^e,g   Mancini, Gabriel L ^a   Lopes, Marilene H ^a   Américo, Tatiana A ^h   Magdesian, Margaret H ^h   Ferguson, Stephen S G ^e   Linden, Rafael ^h   Prado, Marco A M ^e,f   Martins, Vilma R ^a  

^a HOSPITAL ALEMÃO OSWALDO CRUZ   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c A C CAMARGO CANCER CENTER   (Brazil)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^e ROBARTS RESEARCH INSTITUTE   (Canada)

^f UNIVERSITY OF WESTERN ONTARIO   (Canada)

^g FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^h FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

G coupled protein receptors; GPI anchored proteins; Multiprotein complexes; Neurotrophic signals; Signal transduction

Indexed keywords

G PROTEIN COUPLED RECEPTOR; LAMININ GAMMA1; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; MITOGEN ACTIVATED PROTEIN KINASE 1; MULTIPROTEIN COMPLEX; PHOSPHOLIPASE C; PRION PROTEIN; PROTEIN KINASE C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CELL ACTIVATION; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROPHYSIOLOGY; NONHUMAN; PHAGE DISPLAY; PRION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; BENZOATES; CALCIUM; CELLS, CULTURED; FEMALE; GLYCINE; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; LAMININ; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURITES; NEURONS; PROTEIN BINDING; PRPC PROTEINS; PYRIDINES; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; TYPE C PHOSPHOLIPASES;

MUS;

EID: 79251552792     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-161653     Document Type: Article

References (64)

1. Weissmann, C. (2004) The state of the prion. Nat. Rev. Microbiol. 2, 861-871
2. Linden, R., Martins, V. R., Prado, M. A., Cammarota, M., Izquierdo, I., and Brentani, R. R. (2008) Physiology of the prion protein. Physiol. Rev. 88, 673-728
3. Parkin, E. T., Watt, N. T., Hussain, I., Eckman, E. A., Eckman, C. B., Manson, J. C., Baybutt, H. N., Turner, A. J., and Hooper, N. M. (2007) Cellular prion protein regulates beta-secretase cleavage of the Alzheimer's amyloid precursor protein. Proc. Natl. Acad. Sci. U. S. A. 104, 11062-11067
4. Lauren, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W., and Strittmatter, S. M. (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457, 1128-1132
5. Gimbel, D. A., Nygaard, H. B., Coffey, E. E., Gunther, E. C., Lauren, J., Gimbel, Z. A., and Strittmatter, S. M. (2010) Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J. Neurosci. 30, 6367-6374
6. Balducci, C., Beeg, M., Stravalaci, M., Bastone, A., Sclip, A., Biasini, E., Tapella, L., Colombo, L., Manzoni, C., Borsello, T., Chiesa, R., Gobbi, M., Salmona, M., and Forloni, G. (2010) Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein. Proc. Natl. Acad. Sci. U. S. A. 107, 2295-2300
7. Calella, A. M., Farinelli, M., Nuvolone, M., Mirante, O., Moos, R., Falsig, J., Mansuy, I. M., and Aguzzi, A. (2010) Prion protein and Abeta-related synaptic toxicity impairment. EMBO Mol. Med. 2, 306-314
8. Kessels, H. W., Nguyen, L. N., Nabavi, S., and Malinow, R. (2010) The prion protein as a receptor for amyloid-beta. Nature 466, E3-E4
9. Zanata, S. M., Lopes, M. H., Mercadante, A. F., Hajj, G. N., Chiarini, L. B., Nomizo, R., Freitas, A. R., Cabral, A. L., Lee, K. S., Juliano, M. A., de Oliveira, E., Jachieri, S. G., Burlingame, A., Huang, L., Linden, R., Brentani, R. R., and Martins, V. R. (2002) Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J. 21, 3307-3316
10. Chiarini, L. B., Freitas, A. R., Zanata, S. M., Brentani, R. R., Martins, V. R., and Linden, R. (2002) Cellular prion protein transduces neuroprotective signals. EMBO J. 21, 3317-3326
11. Lopes, M. H., Hajj, G. N., Muras, A. G., Mancini, G. L., Castro, R. M., Ribeiro, K. C., Brentani, R. R., Linden, R., and Martins, V. R. (2005) Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signaling pathways. J. Neurosci. 25, 11330-11339
12. Santuccione, A., Sytnyk, V., Leshchyns'ka, I., and Schachner, M. (2005) Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J. Cell Biol. 169, 341-354
13. Graner, E., Mercadante, A. F., Zanata, S. M., Forlenza, O. V., Cabral, A. L., Veiga, S. S., Juliano, M. A., Roesler, R., Walz, R., Minetti, A., Izquierdo, I., Martins, V. R., and Brentani, R. R. (2000) Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res. Mol. Brain Res. 76, 85-92
14. Coitinho, A. S., Freitas, A. R., Lopes, M. H., Hajj, G. N., Roesler, R., Walz, R., Rossato, J. I., Cammarota, M., Izquierdo, I., Martins, V. R., and Brentani, R. R. (2006) The interaction between prion protein and laminin modulates memory consolidation. Eur. J. Neurosci. 24, 3255-3264
15. Hager, G., Pawelzik, H., Kreutzberg, G. W., and Zieglgansberger, W. (1998) A peptide derived from a neurite outgrowth-promoting domain on the gamma 1 chain of laminin modulates the electrical properties of neocortical neurons. Neuroscience 86, 1145-1154 (Pubitemid 28318540)
16. Liesi, P., Narvanen, A., Soos, J., Sariola, H., and Snounou, G. (1989) Identification of a neurite outgrowth-promoting domain of laminin using synthetic peptides. FEBS Lett. 244, 141-148 (Pubitemid 19050499)
17. Liesi, P., Laatikainen, T., and Wright, J. M. (2001) Biologically active sequence (KDI) mediates the neurite outgrowth function of the gamma-1 chain of laminin-1. J. Neurosci. Res. 66, 1047-1053
18. Chen, Z. L., Haegeli, V., Yu, H., and Strickland, S. (2009) Cortical deficiency of laminin gamma1 impairs the AKT/GSK-3beta signaling pathway and leads to defects in neurite outgrowth and neuronal migration. Dev. Biol. 327, 158-168
19. Bueler, H., Fischer, M., Lang, Y., Bluethmann, H., Lipp, H. P., DeArmond, S. J., Prusiner, S. B., Aguet, M., and Weissmann, C. (1992) Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577-582
20. Manson, J. C., Clarke, A. R., Hooper, M. L., Aitchison, L., McConnell, I., and Hope, J. (1994) 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol. Neurobiol. 8, 121-127
21. Caetano, F. A., Lopes, M. H., Hajj, G. N., Machado, C. F., Pinto, A. C., Magalhaes, A. C., Vieira, M. P., Americo, T. A., Massensini, A. R., Priola, S. A., Vorberg, I., Gomez, M. V., Linden, R., Prado, V. F., Martins, V. R., and Prado, M. A. (2008) Endocytosis of prion protein is required for ERK1/2 signaling induced by stress-inducible protein 1. J. Neurosci. 28, 6691-6702
22. Sunyach, C., Jen, A., Deng, J., Fitzgerald, K. T., Frobert, Y., Grassi, J., McCaffrey, M. W., and Morris, R. (2003) The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein. EMBO J. 22, 3591-3601
23. Anborgh, P. H., Godin, C., Pampillo, M., Dhami, G. K., Dale, L. B., Cregan, S. P., Truant, R., and Ferguson, S. S. (2005) Inhibition of metabotropic glutamate receptor signaling by the huntingtin-binding protein optineurin. J. Biol. Chem. 280, 34840-34848
24. Dale, L. B., Babwah, A. V., Bhattacharya, M., Kelvin, D. J., and Ferguson, S. S. (2001) Spatial-temporal patterning of metabotropic glutamate receptor-mediated inositol 1,4,5-triphosphate, calcium, and protein kinase C oscillations: protein kinase C-dependent receptor phosphorylation is not required. J. Biol. Chem. 276, 35900-35908
25. Policha, A., Daneshtalab, N., Chen, L., Dale, L. B., Altier, C., Khosravani, H., Thomas, W. G., Zamponi, G. W., and Ferguson, S. S. (2006) Role of angiotensin II type 1A receptor phosphorylation, phospholipase D, and extracellular calcium in isoformspecific protein kinase C membrane translocation responses. J. Biol. Chem. 281, 26340-26349
26. 2+-binding protein caldendrin: gene structure, splice isoforms, and expression in the rat central nervous system. Mol. Cell. Neurosci. 19, 459-475
27. Ferraguti, F., Crepaldi, L., and Nicoletti, F. (2008) Metabotropic glutamate 1 receptor: current concepts and perspectives. Pharmacol. Rev. 60, 536-581
28. Putney, J. W., Jr., Broad, L. M., Braun, F. J., Lievremont, J. P., and Bird, G. S. (2001) Mechanisms of capacitative calcium entry. J. Cell Sci. 114, 2223-2229
29. Romano, C., Yang, W. L., and O'Malley, K. L. (1996) Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J. Biol. Chem. 271, 28612-28616
30. Babwah, A. V., Dale, L. B., and Ferguson, S. S. (2003) Protein kinase C isoform-specific differences in the spatial-temporal regulation and decoding of metabotropic glutamate receptor1a-stimulated second messenger responses. J. Biol. Chem. 278, 5419-5426
31. Kingston, A. E., Griffey, K., Johnson, M. P., Chamberlain, M. J., Kelly, G., Tomlinson, R., Wright, R. A., Johnson, B. G., Schoepp, D. D., Harris, J. R., Clark, B. P., Baker, R. S., and Tizzano, J. T. (2002) Inhibition of group I metabotropic glutamate receptor responses in vivo in rats by a new generation of carboxyphenylglycine-like amino acid antagonists. Neurosci. Lett. 330, 127-130
32. Gasparini, F., Lingenhohl, K., Stoehr, N., Flor, P. J., Heinrich, M., Vranesic, I., Biollaz, M., Allgeier, H., Heckendorn, R., Urwyler, S., Varney, M. A., Johnson, E. C., Hess, S. D., Rao, S. P., Sacaan, A. I., Santori, E. M., Velicelebi, G., and Kuhn, R. (1999) 2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist. Neuropharmacology 38, 1493-1503
33. Martins, V. R., Linden, R., Prado, M. A., Walz, R., Sakamoto, A. C., Izquierdo, I., and Brentani, R. R. (2002) Cellular prion protein: on the road for functions. FEBS Lett. 512, 25-28
34. Martins, V. R., Beraldo, F. H., Hajj, G. N., Lopes, M. H., Lee, K. S., Prado, M. M., and Linden, R. (2009) Prion protein: orchestrating neurotrophic activities. Curr. Issues Mol. Biol. 12, 63-86
35. Rauch, U. (2004) Extracellular matrix components associated with remodeling processes in brain. Cell. Mol. Life Sci. 61, 2031-2045
36. Hagg, T., Portera-Cailliau, C., Jucker, M., and Engvall, E. (1997) Laminins of the adult mammalian CNS; laminin-alpha2 (merosin M-) chain immunoreactivity is associated with neuronal processes. Brain Res. 764, 17-27
37. Luckenbill-Edds, L. (1997) Laminin and the mechanism of neuronal outgrowth. Brain Res. Brain Res. Rev. 23, 1-27
38. Mitchell, K. J., Pinson, K. I., Kelly, O. G., Brennan, J., Zupicich, J., Scherz, P., Leighton, P. A., Goodrich, L. V., Lu, X., Avery, B. J., Tate, P., Dill, K., Pangilinan, E., Wakenight, P., Tessier-Lavigne, M., and Skarnes, W. C. (2001) Functional analysis of secreted and transmembrane proteins critical to mouse development. Nat. Genet. 28, 241-249
39. Ido, H., Ito, S., Taniguchi, Y., Hayashi, M., Sato-Nishiuchi, R., Sanzen, N., Hayashi, Y., Futaki, S., and Sekiguchi, K. (2008) Laminin isoforms containing the gamma3 chain are unable to bind to integrins due to the absence of the glutamic acid residue conserved in the C-terminal regions of the gamma1 and gamma2 chains. J. Biol. Chem. 283, 28149-28157
40. Schrock, Y., Solis, G. P., and Stuermer, C. A. (2009) Regulation of focal adhesion formation and filopodia extension by the cellular prion protein (PrPC). FEBS Lett. 583, 389-393
41. Hajj, G. N., Lopes, M. H., Mercadante, A. F., Veiga, S. S., da Silveira, R. B., Santos, T. G., Ribeiro, K. C., Juliano, M. A., Jacchieri, S. G., Zanata, S. M., and Martins, V. R. (2007) Cellular prion protein interaction with vitronectin supports axonal growth and is compensated by integrins. J. Cell Sci. 120, 1915-1926
42. Yamada, Y., and Kleinman, H. K. (1992) Functional domains of cell adhesion molecules. Curr. Opin. Cell Biol. 4, 819-823
43. Malinda, K. M., Nomizu, M., Chung, M., Delgado, M., Kuratomi, Y., Yamada, Y., Kleinman, H. K., and Ponce, M. L. (1999) Identification of laminin alpha1 and beta1 chain peptides active for endothelial cell adhesion, tube formation, and aortic sprouting. FASEB J. 13, 53-62
44. Liesi, P. (1985) Do neurons in the vertebrate CNS migrate on laminin? EMBO J. 4, 1163-1170
45. Wiksten, M., Liebkind, R., Laatikainen, T., and Liesi, P. (2003) Gamma 1 laminin and its biologically active KDI-domain may guide axons in the floor plate of human embryonic spinal cord. J. Neurosci. Res. 71, 338-352
46. Wiksten, M., Vaananen, A., Liebkind, R., Rauhala, P., and Liesi, P. (2004) Soluble KDI domain of gamma1 laminin protects adult hippocampus from excitotoxicity of kainic acid. J. Neurosci. Res. 78, 411-419
47. Vaananen, A. J., Rauhala, P., Tuominen, R. K., and Liesi, P. (2006) KDI tripeptide of gamma1 laminin protects rat dopaminergic neurons from 6-OHDA induced toxicity. J. Neurosci. Res. 84, 655-665
48. Krebs, B., Wiebelitz, A., Balitzki-Korte, B., Vassallo, N., Paluch, S., Mitteregger, G., Onodera, T., Kretzschmar, H. A., and Herms, J. (2007) Cellular prion protein modulates the intracellular calcium response to hydrogen peroxide. J. Neurochem. 100, 358-367 (Pubitemid 46010997)
49. Brini, M., Miuzzo, M., Pierobon, N., Negro, A., and Sorgato, M. C. (2005) The prion protein and its paralogue Doppel affect calcium signaling in Chinese hamster ovary cells. Mol. Biol. Cell 16, 2799-2808
50. 2+ homeostasis in hippocampal CA1 neurons. J. Neurochem. 98, 1876-1885
51. Kristensson, K., Feuerstein, B., Taraboulos, A., Hyun, W. C., Prusiner, S. B., and DeArmond, S. J. (1993) Scrapie prions alter receptor-mediated calcium responses in cultured cells. Neurology 43, 2335-2341 (Pubitemid 23346972)
52. Bruno, V., Battaglia, G., Copani, A., D'Onofrio, M., Di Iorio, P., De Blasi, A., Melchiorri, D., Flor, P. J., and Nicoletti, F. (2001) Metabotropic glutamate receptor subtypes as targets for neuroprotective drugs. J. Cereb. Blood Flow Metab. 21, 1013-1033
53. Maiese, K., Chong, Z. Z., and Li, F. (2005) Driving cellular plasticity and survival through the signal transduction pathways of metabotropic glutamate receptors. Curr. Neurovasc. Res. 2, 425-446
54. Ribeiro, F. M., Ferreira, L. T., Paquet, M., Cregan, T., Ding, Q., Gros, R., and Ferguson, S. S. (2009) Phosphorylation-independent regulation of metabotropic glutamate receptor 5 desensitization and internalization by G protein-coupled receptor kinase 2 in neurons. J. Biol. Chem. 284, 23444-23453
55. Brugger, B., Graham, C., Leibrecht, I., Mombelli, E., Jen, A., Wieland, F., and Morris, R. (2004) The membrane domains occupied by glycosylphosphatidylinositol-anchored prion protein and Thy-1 differ in lipid composition. J. Biol. Chem. 279, 7530-7536
56. Mouillet-Richard, S., Ermonval, M., Chebassier, C., Laplanche, J. L., Lehmann, S., Launay, J. M., and Kellermann, O. (2000) Signal transduction through prion protein. Science 289, 1925-1928
57. Jen, A., Parkyn, C. J., Mootoosamy, R. C., Ford, M. J., Warley, A., Liu, Q., Bu, G., Baskakov, I. V., Moestrup, S., McGuinness, L., Emptage, N., and Morris, R. J. (2010) Neuronal low-density lipoprotein receptor-related protein 1 binds and endocytoses prion fibrils via receptor cluster 4. J. Cell Sci. 123, 246-255
58. Magalhaes, A. C., Silva, J. A., Lee, K. S., Martins, V. R., Prado, V. F., Ferguson, S. S., Gomez, M. V., Brentani, R. R., and Prado, M. A. (2002) Endocytic intermediates involved with the intracellular trafficking of a fluorescent cellular prion protein. J. Biol. Chem. 277, 33311-33318
59. Francesconi, A., Kumari, R., and Zukin, R. S. (2009) Regulation of group I metabotropic glutamate receptor trafficking and signaling by the caveolar/lipid raft pathway. J. Neurosci. 29, 3590-3602
60. Romano, S. A., Cordeiro, Y., Lima, L. M., Lopes, M. H., Silva, J. L., Foguel, D., and Linden, R. (2009) Reciprocal remodeling upon binding of the prion protein to its signaling partner hop/STI1. FASEB J. 23, 4308-4316
61. Hannan, A. J., Blakemore, C., Katsnelson, A., Vitalis, T., Huber, K. M., Bear, M., Roder, J., Kim, D., Shin, H. S., and Kind, P. C. (2001) PLC-beta1, activated via mGluRs, mediates activity-dependent differentiation in cerebral cortex. Nat. Neurosci. 4, 282-288
62. Huber, K. M., Roder, J. C., and Bear, M. F. (2001) Chemical induction of mGluR5- and protein synthesis-dependent longterm depression in hippocampal area CA1. J. Neurophysiol. 86, 321-325
63. Castiglione, M., Calafiore, M., Costa, L., Sortino, M. A., Nicoletti, F., and Copani, A. (2008) Group I metabotropic glutamate receptors control proliferation, survival and differentiation of cultured neural progenitor cells isolated from the subventricular zone of adult mice. Neuropharmacology 55, 560-567
64. Renner, M., Lacor, P. N., Velasco, P. T., Xu, J., Contractor, A., Klein, W. L., and Triller, A. (2010) Deleterious effects of amyloid beta oligomers acting as an extracellular scaffold for mGluR5. Neuron 66, 739-754