γ-Enolase C-terminal peptide promotes cell survival and neurite outgrowth by activation of the PI3K/Akt and MAPK/ERK signalling pathways

Biochemical Journal

Volumn 443, Issue 2, 2012, Pages 439-450

  Hafner, Anja ^a   Obermajer, Natasǎ ^b   Kos, Janko ^a,b  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

enolase; Actin remodelling; Extracellular signalregulated kinase (ERK); Neurotrophic effect; Phosphoinositide 3 kinase (PI3K); RhoA

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ACTIN; C PEPTIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEURON SPECIFIC ENOLASE; NEUROTROPHIC FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RHO KINASE; WORTMANNIN;

ACTIN POLYMERIZATION; ARTICLE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOSKELETON; ENZYME INHIBITION; HUMAN; HUMAN CELL; NERVE FIBER GROWTH; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL SURVIVAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; NEURITES; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPYRUVATE HYDRATASE; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84859478188     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111351     Document Type: Article

References (53)

1. Nagtegaal, I. D., Lakke, E. A. and Marani, E. (1998) Trophic and tropic factors in the development of the central nervous system. Arch. Physiol. Biochem. 106, 161-202 (Pubitemid 29147030)
2. Jin, E., Nosaka, K. and Sano, M. (2007) NGF-dependent formation of ruffles in PC12D cells requires a different pathway from that for neurite outgrowth. Neurochem. Int. 51, 216-226 (Pubitemid 47176703)
3. Nikolic, M. (2002) The role of Rho GTPases and associated kinases in regulating neurite outgrowth. Int. J. Biochem. Cell Biol. 34, 731-745
4. Luo, L. (2002) Actin cytoskeleton regulation inneuronal morphogenesis and structural plasticity. Annu. Rev. Cell Dev. Biol. 18, 601-635
5. Hattori, T., Ohsawa, K., Mizuno, Y., Kato, K. and Kohsaka, S. (1994) Synthetic peptide corresponding to30 amino acids of the C-terminal of neuron-specific enolase promotes survival of neocortical neurons in culture. Biochem. Biophys. Res. Commun. 202, 25-30 (Pubitemid 24252560)
6. Hattori, T., Takei, N., Mizuno, Y., Kato, K. and Kohsaka, S. (1995) Neurotrophic and neuroprotective effects of neuron-specific enolase on cultured neurons from embryonic rat brain. Neurosci. Res. 21, 191-198
7. Rider, C. C. and Taylor, C. B. (1974) Enolase isoenzymes inrat tissues. Biochim. Biophys. Acta 365, 285-300
8. Fletcher, L., Rider, C. C. and Taylor, C. B. (1976) Enolase isoenzymes. III. Chromatography and immunological characteristic of rat brain enolase. Biochim. Biophys. Acta 452, 245-252
9. Schmechel, D. E., Marangos, P. J., Martin, B. M., Winfield, S., Burkhart, D. S., Roses, A. D. and Ginns, E. I. (1987) Localization of neuron-specific enolase (NSE) mRNA in human brain. Neurosci. Lett. 76, 233-238 (Pubitemid 17067820)
10. Takei, N., Kondo, J., Nagaike, K., Ohsawa, K., Kato, K. and Kohsaka, S. (1991) Neuronal survival factor from bovine brain is identical to neuron-specific enolase. J. Neurochem. 57, 1178-1184 (Pubitemid 21922739)
11. Obermajer, N., Doljak, B., Jamnik, P., Fonovič, U. P. and Kos, J. (2009) Cathepsin Xcleaves the C-terminal dipeptide of α- and γ -enolase and impairs survival and neuriotegenesis of neuronal cells. Int. J. Biochem. Cell Biol. 41, 1685-1696
12. Hafner, A., Obermajer, N. and Kos, J. (2010) γ 1-Syntrophin mediates trafficking of γ -enolase towards the plasma membrane and enhances its neurotrophic activity. Neurosignals 18, 246-258
13. Vaudry, D., Stork, P. J., Lazarovici, P. and Eiden, L. E. (2002) Signaling pathways for PC12 cell differentiation: making the right connections. Science 296, 1648-1649 (Pubitemid 34579153)
14. Frebel, K. and Wiese, S. (2006) Signalling molecules essential for neuronal survival and differentiation. Biochem. Soc. Trans. 34, 1287-1290 (Pubitemid 46769039)
15. Segal, R. A. and Greenberg, M. E. (1996) Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19, 463-489 (Pubitemid 26080836)
16. Kaplan, D. R. and Miller, F. D. (1997) Signal transduction by the neurotrophin receptors. Curr. Opin. Cell. Biol. 9, 213-221 (Pubitemid 27135989)
17. Encinas, M., Iglesias, M., Llecha, N. and Comella, J. X. (1999) Extracellular-regulated kinases and phosphatidylinositol 3-kinase are involved in brain-derived neurotrophic factor-mediated survival and neuritogenesis of the neuroblastoma cell line SH-SY5Y. J. Neurochem. 73, 1409-1421 (Pubitemid 29440140)
18. Kim, Y., Seger, R., Suresh Babu, C. V., Hwang, S. Y. and Yoo, Y. S. (2004) A positive role of the PI3-K/Akt signaling pathway in PC12 cell differentiation. Mol. Cells 18, 353-359 (Pubitemid 40298032)
19. Kuruvilla, R., Ye, H. and Ginty, D. D. (2000) Spatially and functionally distinct roles of the PI3-K effector pathway during NGF signaling in sympathetic neurons. Neuron 27, 499-512
20. Ming, G., Song, H., Berninger, B., Inagaki, N., Tessier-Lavigne, M. and Poo, M. (1999) Phospholipase C-γ and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidance. Neuron 23, 139-148 (Pubitemid 29262471)
21. Luo, L (2000) Rho GTPases inneuronal morphogenesis. Nat. Rev. Neurosci. 1, 173-180
22. Etienne-Manneville, S. and Hall, A. (2002) Rho GTPases incell biology. Nature 420, 629-635
23. Jeon, C. Y., Kim, H. J., Lee, J. Y., Kim, J., Kim, S. C. and Park, J. B. (2010) p190RhoGAP and Rap-dependent RhoGAP (ARAP3) inactivate RhoA in response to nerve growth factor leading to neurite outgrowth from PC12 cells. Exp. Mol. Med. 42, 335-344
24. Tornieri, K., Welshhans, K., Geddis, M. S. and Rehder, V. (2006) Control of neurite outgrowth and growth cone motility by phosphatidylinositol-3-kinase. Cell Motil. Cytoskeleton 63, 173-192
25. Pang, L., Sawada, T., Decker, S. J. and Saltiel, A. R. (1995) Inhibition of MAP kinase kinase block the differentiation of PC-12 cells induced by nerve growth factor. J. Biol. Chem. 270, 13585-13588
26. Reffas, S. and Schlegel, W. (2000) Compartment-specific regulation of extracellular signal-regulated kinase (ERK) and c-Jun N-terminal kinase (JNK) mitogen-activated protein kinases (MAPKs) by ERK-dependent and non-ERK-dependent inductions of MAPK phosphatase (MKP)-3 and MKP-1 in differentiating P19 cells. Biochem. J. 352, 701-708 (Pubitemid 32015025)
27. Miloso, M., Scuteri, A., Foudah, D. and Tredici, G. (2008) MAPKs asmediators of cell fate determination: an approach to neurodegenerative diseases. Curr. Med. Chem. 15, 538-548 (Pubitemid 351516810)
28. Marshall, C. J. (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 899-912
29. Vaillancourt, R. R., Gardner, A. M. and Johnson, G. L. (1994) B-Raf-dependent regulation of the MEK-1/mitogen-activated protein kinase pathway in PC12 cells and regulation by cyclic AMP. Mol. Cell. Biol. 14, 6522-6530 (Pubitemid 24299721)
30. York, R. D., Molliver, D. C., Grewal, S. S., Stenberg, P. E., McCleskey, E. W. and Stork, P. J. S. (2000) Role of phosphoinositide 3-kinase and endocytosis in nerve growth factor-induced extracellular signal-regulated kinase activation via Ras and Rap1. Mol. Cell. Biol. 20, 8069-8083
31. Nusser, N., Gosmanova, E., Zheng, Y. and Tigyi, G. (2002) Nerve growth factor signals through TrkA, phosphatidylinositol 3-kinase, and Rac1 to inactivate RhoA during the initiation of neuronal differentiation of PC12 cells. J. Biol. Chem. 277, 35840-35846
32. Klippel, A., Kavanaugh, W. M., Pot, D. and Williams, L. T. (1997) A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol. 17, 338-344 (Pubitemid 26425623)
33. Crowder, R. J. and Freeman, R. S. (1998) Phosphatidylinositol 3-kinase and Akt protein kinase are necessary and sufficient for the survival of nerve growth factor-dependent sympathetic neurons. J. Neurosci. 18, 2933-2943 (Pubitemid 28163223)
34. Jin, E., Nosaka, K. and Sano, M. (2007) NGF-dependent formation of ruffles in PC12D cells required a different pathway from that for neurite outgrowth. Neurochem. Int. 51, 216-226 (Pubitemid 47176703)
35. Jaiswal, R. K., Moodie, S. A., Wolfman, A. and Landreth, G. E. (1994) The mitogen-activated protein kinase cascade is activated by B-Raf in response to nerve growth factor through interaction with p21ras. Mol. Cell. Biol. 14, 6944-6953
36. Orike, N., Middleton, G., Borthwick, E., Buchman, V., Cowen, T. and Davies, A. M. (2001) Role of PI 3-kinase, Akt and Bcl-2-related proteins in sustaining the survival of neurotrophic factor-independent adult sympathetic neurons. J. Cell Biol. 154, 995-1005 (Pubitemid 34286179)
37. Lavenius, E., Parrow, V., Nånberg, E. and Påhlman, S. (1994) Basic FGF and IGF-I promote differentiation of human SH-SY5Y neuroblastoma cells in culture. Growth Factors 10, 29-39 (Pubitemid 24060285)
38. Sebök, A., Nusser, N., Debreceni, B., Guo, Z., Santos, M. F., Szeberenyi, J. and Tigyi, G. (1999) Different roles for RhoA during neurite initiation, elongation, and regeneration in PC12 cells. J. Neurochem. 73, 949-960 (Pubitemid 29395451)
39. Noguchi, Y., Nakamura, S., Yasuda, T., Kitagawa, M., Kohn, L. D., Saito, Y. and Hirai, A. (1988) Newly synthesized Rho A, not Ras, is isoprenylated and translocated to membranes coincident with progression of the G1 to S phase of growth-stimulated rat FRTL-5 cells. J. Biol. Chem. 273, 3649-3653
40. Yamaguchi, Y., Katoh, H., Yasui, H., Mori, K. and Negishi, M. (2001) RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J. Biol. Chem. 276, 18977-18983
41. Rueda, D., Gaide, O., Ho, L., Lewkowicz, E., Niedergang, F., Hailfinger, S., Rebeaud, F., Guzzardi, M., Conne, B., Thelen, M. et al. (2007) Bcl10 controls TCR- and Fcγ R-induced actin polymerization. J. Immunol. 178, 4373-4384 (Pubitemid 46492388)
42. Rudkin, B. B., Lazarovici, P., Levi, B. Z., Abe, Y., Fujita, K. and Guroff, G. (1989) Cell cycle-specific action of nerve growth factor in PC12 cells: differentiation without proliferation. EMBO J. 8, 3319-3325 (Pubitemid 19273559)
43. Urdiales, J. L., Becker, E., Andrieu, M., Thomas, A., Jullien, J., van Grunsven, L. A., Menut, S., Evan, G. I., Martín-Zanca, D. and Rudkin, B. B. (1998) Cell cycle phase-specific surface expression of nerve growth factor receptors TrkA and p75NTR. J. Neurosci. 18, 6767-6775 (Pubitemid 28388008)
44. Favata, M. F., Horiuchi, K. Y., Manos, E. J., Daulerio, A. J., Stradley, D. A., Feeser, W. S., Van Dyk, D. E., Pitts, W. J., Earl, R. A., Hobbs, F. et al. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273, 18623-18632 (Pubitemid 28334795)
45. Roux, P. P. and Blenis, J. (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68, 320-344 (Pubitemid 38756868)
46. Kim, B., Leventhal, P. S., Saltiel, A. R. and Feldman, E. L. (1997) Insulin-like growth factor-I-mediated neurite outgrowth in vitro requires mitogen-activated protein kinase activation. J. Biol. Chem. 272, 21268-21273 (Pubitemid 27373992)
47. van Lookeren Campagne, M., Dotti, C. G., Verkleij, A. J., Gispen, W. H. and Oestreicher, A. B. (1992) Redistribution of B-50/growth-associated protein 43 during differentiation and maturation of rat hippocampal neurons in vitro. Neuroscience 51, 601-619
48. 2+-dependent interaction of the growth-associated protein GAP-43 with the synaptic core complex. Biochem. J. 325, 455-463
49. Cao, X., Kambe, F., Yamauchi, M. and Seo, H. (2009) Thyroid-hormone- dependent activation of the phosphoinositide 3-kinase/Akt cascade requires Src and enhances neuronal survival. Biochem. J. 424, 201-209
50. Fuenzalida, K., Quintanilla, R., Ramos, P., Piderit, D., Fuentealba, R. A., Martinez, G., Inestrosa, N. C. and Bronfman, M. (2007) Peroxisome proliferator-activated receptor γ up-regulates the Bcl-2 anti-apoptotic protein in neurons and induces mitochondrial stabilization and protection against oxidative stress and apoptosis. J. Biol. Chem. 282, 37006-37015
51. Spero, D. A. and Roisen, F. J. (1985) Neuro-2a neuroblastoma cells form neurites in the presence of taxol and cytochalasin D. Brain Res. 355, 155-159 (Pubitemid 16209592)
52. Bradke, F. and Dotti, C. G. (1999) The role of local actin instability in axon formation. Science 283, 1931-1934
53. Loudon, R. P., Silver, L. D., Yee, Jr, H. F. and Gallo, G. (2006) RhoA-kinase and myosin IIare required for the maintenance of growth cone polarity and guidance by nerve growth factor. J. Neurobiol. 66, 847-867 (Pubitemid 44025538)