Laminin-γ1 chain and stress inducible protein 1 synergistically mediate PrPC-dependent axonal growth via Ca2+ mobilization in dorsal root ganglia neurons

Journal of Neurochemistry

Volumn 124, Issue 2, 2013, Pages 210-223

  Santos, Tiago G ^a,b   Beraldo, Flavio H ^c   Hajj, Glaucia N M ^a,b   Lopes, Marilene H ^d   Roffe, Martin ^a   Lupinacci, Fernanda C S ^a,b   Ostapchenko, Valeriy G ^c   Prado, Vania F ^c   Prado, Marco A M ^c   Martins, Vilma R ^a  

^a A C CAMARGO CANCER CENTER   (Brazil)

^b National Institute for Translational Neuroscience (CNPq/MCT/FAPESP)   (Brazil)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

axonogenesis; co chaperones; laminin; neuro transmitters; prion protein; trophic signals

Indexed keywords

BUNGAROTOXIN RECEPTOR; HEAT SHOCK PROTEIN; LAMININ GAMMA1; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; PHOSPHOLIPASE C; PRION PROTEIN; STRESS INDUCIBLE PROTEIN 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; LIGAND BINDING; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; NULL ALLELE; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPINAL GANGLION; WILD TYPE;

ANIMALS; AXONS; CALCIUM SIGNALING; CELL SURVIVAL; EXTRACELLULAR FLUID; GANGLIA, SPINAL; HEAT-SHOCK PROTEINS; INTRACELLULAR FLUID; LAMININ; MICE; MICE, KNOCKOUT; PRIMARY CELL CULTURE; PROTEIN BINDING; PRPC PROTEINS; RECEPTOR CROSS-TALK; SENSORY RECEPTOR CELLS; UP-REGULATION;

MUS;

EID: 84871623904     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12091     Document Type: Article

References (90)

1. Achyuta A. K., Cieri R., Unger K., and, Murthy S. K., (2009) Synergistic effect of immobilized laminin and nerve growth factor on PC12 neurite outgrowth. Biotechnol. Prog. 25, 227-234.
2. Aguzzi A., Baumann F., and, Bremer J., (2008) The prion's elusive reason for being. Annu. Rev. Neurosci. 31, 439-477.
3. Albert A. P., (2011) Gating mechanisms of canonical transient receptor potential channel proteins: role of phosphoinositols and diacylglycerol. Adv. Exp. Med. Biol. 704, 391-411.
4. Alessandri-Haber N., Dina O. A., Chen X., and, Levine J. D., (2009) TRPC1 and TRPC6 channels cooperate with TRPV4 to mediate mechanical hyperalgesia and nociceptor sensitization. J. Neurosci. 29, 6217-6228.
5. Alvarez F. J., Villalba R. M., Carr P. A., Grandes P., and, Somohano P. M., (2000) Differential distribution of metabotropic glutamate receptors 1a, 1b, and 5 in the rat spinal cord. J. Comp. Neurol. 422, 464-487.
6. Arantes C., Nomizo R., Lopes M. H., Hajj G. N., Lima F. R., and, Martins V. R., (2009) Prion protein and its ligand stress inducible protein 1 regulate astrocyte development. Glia.
7. Belkin A. M., and, Stepp M. A., (2000) Integrins as receptors for laminins. Microsc. Res. Tech. 51, 280-301.
8. Beraldo F. H., Arantes C. P., Santos T. G., Queiroz N. G., Young K., Rylett R. J., Markus R. P., Prado M. A., and, Martins V. R., (2010) Role of alpha7 nicotinic acetylcholine receptor in calcium signaling induced by prion protein interaction with stress-inducible protein 1. J. Biol. Chem. 285, 36542-36550.
9. Beraldo F. H., Arantes C. P., Santos T. G., et al,. (2011) Metabotropic glutamate receptors transduce signals for neurite outgrowth after binding of the prion protein to laminin gamma1 chain. FASEB J. 25, 265-279.
10. Biasini E., Turnbaugh J. A., Unterberger U., and, Harris D. A., (2012) Prion protein at the crossroads of physiology and disease. Trends Neurosci. 35, 92-103.
11. Bremer J., Baumann F., Tiberi C., et al,. (2010) Axonal prion protein is required for peripheral myelin maintenance. Nat. Neurosci. 13, 310-318.
12. 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.
13. 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.
14. Caetano F. A., Lopes M. H., Hajj G. N., et al,. (2008) Endocytosis of prion protein is required for ERK1/2 signaling induced by stress-inducible protein 1. J. Neurosci. 28, 6691-6702.
15. Carlton S. M., and, Hargett G. L., (2007) Colocalization of metabotropic glutamate receptors in rat dorsal root ganglion cells. J. Comp. Neurol. 501, 780-789.
16. Caughey B., and, Baron G. S., (2006) Prions and their partners in crime. Nature 443, 803-810.
17. Chao M. V., (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 4, 299-309.
18. Chen Z. L., and, Strickland S., (2003) Laminin gamma1 is critical for Schwann cell differentiation, axon myelination, and regeneration in the peripheral nerve. J. Cell Biol. 163, 889-899.
19. 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.
20. 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.
21. Ciobanu C., Reid G., and, Babes A., (2009) Acute and chronic effects of neurotrophic factors BDNF and GDNF on responses mediated by thermo-sensitive TRP channels in cultured rat dorsal root ganglion neurons. Brain Res. 1284, 54-67.
22. Coitinho A. S., Freitas A. R., Lopes M. H., et al,. (2006) The interaction between prion protein and laminin modulates memory consolidation. Eur. J. Neurosci. 24, 3255-3264.
23. Colling S. B., Collinge J., and, Jefferys J. G., (1996) Hippocampal slices from prion protein null mice: disrupted Ca(2 +)-activated K+ currents. Neurosci. Lett. 209, 49-52.
24. Collinge J., Whittington M. A., Sidle K. C., Smith C. J., Palmer M. S., Clarke A. R., and, Jefferys J. G., (1994) Prion protein is necessary for normal synaptic function. Nature 370, 295-297.
25. Crawford J. H., Wainwright A., Heavens R., Pollock J., Martin D. J., Scott R. H., and, Seabrook G. R., (2000) Mobilisation of intracellular Ca2 + by mGluR5 metabotropic glutamate receptor activation in neonatal rat cultured dorsal root ganglia neurones. Neuropharmacology 39, 621-630.
26. Devanathan V., Jakovcevski I., Santuccione A., Li S., Lee H. J., Peles E., Leshchyns'ka I., Sytnyk V., and, Schachner M., (2010) Cellular form of prion protein inhibits Reelin-mediated shedding of Caspr from the neuronal cell surface to potentiate Caspr-mediated inhibition of neurite outgrowth. J. Neurosci. 30, 9292-9305.
27. Erlich R. B., Kahn S. A., Lima F. R., Muras A. G., Martins R. A., Linden R., Chiarini L. B., Martins V. R., Moura N., and, V, (2007) STI1 promotes glioma proliferation through MAPK and PI3K pathways. Glia 55, 1690-1698.
28. Eustace B. K., and, Jay D. G., (2004) Extracellular roles for the molecular chaperone, hsp90. Cell Cycle 3, 1098-1100.
29. Fischer M. J., (2010) Amine coupling through EDC/NHS: a practical approach. Methods Mol. Biol. 627, 55-73.
30. Fuhrmann M., Bittner T., Mitteregger G., Haider N., Moosmang S., Kretzschmar H., and, Herms J., (2006) Loss of the cellular prion protein affects the Ca2 + homeostasis in hippocampal CA1 neurons. J. Neurochem. 98, 1876-1885.
31. Gauczynski S., Peyrin J. M., Haik S., et al,. (2001) The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein. EMBO J. 20, 5863-5875.
32. Graner E., Mercadante A. F., Zanata S. M., et al,. (2000a) Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res. Mol. Brain Res. 76, 85-92.
33. Graner E., Mercadante A. F., Zanata S. M., Martins V. R., Jay D. G., and, Brentani R. R., (2000b) Laminin-induced PC-12 cell differentiation is inhibited following laser inactivation of cellular prion protein. FEBS Lett. 482, 257-260.
34. Hajj G. N., Lopes M. H., Mercadante A. F., et al,. (2007) Cellular prion protein interaction with vitronectin supports axonal growth and is compensated by integrins. J. Cell Sci. 120, 1915-1926.
35. Hajj G. N., Santos T. G., Cook Z. S., and, Martins V. R., (2009) Developmental expression of prion protein and its ligands stress-inducible protein 1 and vitronectin. J. Comp. Neurol. 517, 371-384.
36. Hajj G. N., Santos T. G., Landemberger M. C., and, Lopes M. H., (2012) Transmissible spongiform encephalopathies, in Brain Damage-Bridging Between Basic Research and Clinics (, Gonzales-Quevedo A., ed.), pp. 187-220. INTECHOPEN, Rijeka.
37. Herms J. W., Korte S., Gall S., Schneider I., Dunker S., and, Kretzschmar H. A., (2000) Altered intracellular calcium homeostasis in cerebellar granule cells of prion protein-deficient mice. J. Neurochem. 75, 1487-1492.
38. Hofmann H. A., Siegling A., Denzer D., Spreyer P., and, De V. J., (2001) Metabotropic glutamate mGlu1 receptor mRNA expression in dorsal root ganglia of rats after peripheral nerve injury. Eur. J. Pharmacol. 429, 135-138.
39. Jia Y., Zhou J., Tai Y., and, Wang Y., (2007) TRPC channels promote cerebellar granule neuron survival. Nat. Neurosci. 10, 559-567.
40. Khosravani H., Zhang Y., Tsutsui S., et al,. (2008) Prion protein attenuates excitotoxicity by inhibiting NMDA receptors. J. Gen. Physiol. 131, i5.
41. Krieglstein K., (2004) Factors promoting survival of mesencephalic dopaminergic neurons. Cell Tissue Res. 318, 73-80.
42. 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.
43. Li D. P., and, Pan H. L., (2010) Increased group I metabotropic glutamate receptor activity in paraventricular nucleus supports elevated sympathetic vasomotor tone in hypertension. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R552-R561.
44. Li Y., Jia Y. C., Cui K., Li N., Zheng Z. Y., Wang Y. Z., and, Yuan X. B., (2005) Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 434, 894-898.
45. Li A., Christensen H. M., Stewart L. R., Roth K. A., Chiesa R., and, Harris D. A., (2007) Neonatal lethality in transgenic mice expressing prion protein with a deletion of residues 105-125. EMBO J. 26, 548-558.
46. Liebkind R., Laatikainen T., and, Liesi P., (2003) Is the soluble KDI domain of gamma1 laminin a regeneration factor for the mammalian central nervous system? J. Neurosci. Res. 73, 637-643.
47. 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.
48. Lima F. R., Arantes C. P., Muras A. G., Nomizo R., Brentani R. R., and, Martins V. R., (2007) Cellular prion protein expression in astrocytes modulates neuronal survival and differentiation. J. Neurochem. 103, 2164-2176.
49. 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.
50. Linden R., Cordeiro Y., and, Lima L. M., (2012) Allosteric function and dysfunction of the prion protein. Cell. Mol. Life Sci. 69, 1105-1124.
51. 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.
52. Loubet D., Dakowski C., Pietri M., et al,. (2012) Neuritogenesis: the prion protein controls beta1 integrin signaling activity. FASEB J. 26, 678-690.
53. Malaga-Trillo E., Solis G. P., Schrock Y., Geiss C., Luncz L., Thomanetz V., and, Stuermer C. A., (2009) Regulation of embryonic cell adhesion by the prion protein. PLoS Biol. 7, e55.
54. Mallucci G. R., Ratte S., Asante E. A., Linehan J., Gowland I., Jefferys J. G., and, Collinge J., (2002) Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBO J. 21, 202-210.
55. Martins V. R., Graner E., Garcia-Abreu J., de Souza S. J., Mercadante A. F., Veiga S. S., Zanata S. M., Neto V. M., and, Brentani R. R., (1997) Complementary hydropathy identifies a cellular prion protein receptor. Nat. Med. 3, 1376-1382.
56. Martins V. R., Beraldo F. H., Hajj G. N., Lopes M. H., Lee K. S., Prado M. M., and, Linden R., (2010) Prion protein: orchestrating neurotrophic activities. Curr. Issues Mol. Biol. 12, 63-86.
57. Moore R. A., Taubner L. M., and, Priola S. A., (2009) Prion protein misfolding and disease. Curr. Opin. Struct. Biol. 19, 14-22.
58. Nelson J., McFerran N. V., Pivato G., Chambers E., Doherty C., Steele D., and, Timson D. J., (2008) The 67 kDa laminin receptor: structure, function and role in disease. Biosci. Rep. 28, 33-48.
59. Neugebauer V., and, Carlton S. M., (2002) Peripheral metabotropic glutamate receptors as drug targets for pain relief. Expert Opin. Ther. Targets 6, 349-361.
60. Nicolet C. M., and, Craig E. A., (1989) Isolation and characterization of STI1, a stress-inducible gene from Saccharomyces cerevisiae. Mol. Cell. Biol. 9, 3638-3646.
61. Nilius B., and, Owsianik G., (2011) The transient receptor potential family of ion channels. Genome Biol. 12, 218.
62. Ostapchenko V. G., Makarava N., Savtchenko R., and, Baskakov I. V., (2008) The polybasic N-terminal region of the prion protein controls the physical properties of both the cellular and fibrillar forms of PrP. J. Mol. Biol. 383, 1210-1224.
63. Patapoutian A., (2005) TRP channels and thermosensation. Chem. Senses 30 (Suppl 1), i193-i194.
64. Paulsson M., Aumailley M., Deutzmann R., Timpl R., Beck K., and, Engel J., (1987) Laminin-nidogen complex. Extraction with chelating agents and structural characterization. Eur. J. Biochem. 166, 11-19.
65. Rieger R., Edenhofer F., Lasmezas C. I., and, Weiss S., (1997) The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells. Nat. Med. 3, 1383-1388.
66. Roffe M., Beraldo F. H., Bester R., et al,. (2010) Prion protein interaction with stress-inducible protein 1 enhances neuronal protein synthesis via mTOR. Proc. Natl Acad. Sci. USA 107, 13147-13152.
67. Santoni G., and, Farfariello V., (2011) TRP channels and cancer: new targets for diagnosis and chemotherapy. Endocr. Metab. Immune Disord. Drug Targets 11, 54-67.
68. Santos T. G., Silva I. R., Costa-Silva B., Lepique A. P., Martins V. R., and, Lopes M. H., (2011) Enhanced neural progenitor/stem cells self-renewal via the interaction of stress-inducible protein 1 with the prion protein. Stem Cells 29, 1126-1136.
69. 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.
70. Schmitt-Ulms G., Legname G., Baldwin M. A., et al,. (2001) Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J. Mol. Biol. 314, 1209-1225.
71. 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.
72. Sharma H. S., (2007) Neurotrophic factors in combination: a possible new therapeutic strategy to influence pathophysiology of spinal cord injury and repair mechanisms. Curr. Pharm. Des. 13, 1841-1874.
73. Shmerling D., Hegyi I., Fischer M., Blattler T., Brandner S., Gotz J., Rulicke T., Flechsig E., Cozzio A., and, von M. C., Hangartner C., Aguzzi A., and, Weissmann C., (1998) Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell 93, 203-214.
74. Sorgato M. C., and, Bertoli A., (2009) From cell protection to death: may Ca2 + signals explain the chameleonic attributes of the mammalian prion protein? Biochem. Biophys. Res. Commun. 379, 171-174.
75. Tu P., Kunert-Keil C., Lucke S., Brinkmeier H., and, Bouron A., (2009) Diacylglycerol analogues activate second messenger-operated calcium channels exhibiting TRPC-like properties in cortical neurons. J. Neurochem. 108, 126-138.
76. Tucker B. A., Rahimtula M., and, Mearow K. M., (2005) Integrin activation and neurotrophin signaling cooperate to enhance neurite outgrowth in sensory neurons. J. Comp. Neurol. 486, 267-280.
77. 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.
78. Venstrom K. A., and, Reichardt L. F., (1993) Extracellular matrix. 2: role of extracellular matrix molecules and their receptors in the nervous system. FASEB J. 7, 996-1003.
79. Walsh N., Larkin A., Swan N., Conlon K., Dowling P., McDermott R., and, Clynes M., (2011) RNAi knockdown of Hop (Hsp70/Hsp90 organising protein) decreases invasion via MMP-2 down regulation. Cancer Lett. 306, 180-189.
80. Walz R., Amaral O. B., Rockenbach I. C., Roesler R., Izquierdo I., Cavalheiro E. A., Martins V. R., and, Brentani R. R., (1999) Increased sensitivity to seizures in mice lacking cellular prion protein. Epilepsia 40, 1679-1682.
81. Wang T. H., Chao A., Tsai C. L., et al,. (2010) Stress-induced phosphoprotein 1 as a secreted biomarker for human ovarian cancer promotes cancer cell proliferation. Mol. Cell. Proteomics 9, 1873-1884.
82. Weissmann C., and, Flechsig E., (2003) PrP knock-out and PrP transgenic mice in prion research. Br. Med. Bull. 66, 43-60.
83. 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.
84. Wiksten M., Vaananen A., Liebkind R., Rauhala P., and, Liesi P., (2004a) Soluble KDI domain of gamma1 laminin protects adult hippocampus from excitotoxicity of kainic acid. J. Neurosci. Res. 78, 411-419.
85. Wiksten M., Vaananen A. J., Liebkind R., and, Liesi P., (2004b) Regeneration of adult rat spinal cord is promoted by the soluble KDI domain of gamma1 laminin. J. Neurosci. Res. 78, 403-410.
86. Wiksten M., Vaananen A., and, Liesi P., (2007) Selective overexpression of gamma1 laminin in astrocytes in amyotrophic lateral sclerosis indicates an involvement in ALS pathology. J. Neurosci. Res. 85, 2045-2058.
87. Wong K., Qiu Y., Hyun W., Nixon R., VanCleff J., Sanchez-Salazar J., Prusiner S. B., and, DeArmond S. J., (1996) Decreased receptor-mediated calcium response in prion-infected cells correlates with decreased membrane fluidity and IP3 release. Neurology 47, 741-750.
88. Yamamoto S., Wajima T., Hara Y., Nishida M., and, Mori Y., (2007) Transient receptor potential channels in Alzheimer's disease. Biochim. Biophys. Acta 1772, 958-967.
89. Zanata S. M., Lopes M. H., Mercadante A. F., et al,. (2002) Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J. 21, 3307-3316.
90. Zhou S., Komak S., Du J., and, Carlton S. M., (2001) Metabotropic glutamate 1alpha receptors on peripheral primary afferent fibers: their role in nociception. Brain Res. 913, 18-26.