The peptide NAP promotes neuronal growth and differentiation through extracellular signal-regulated protein kinase and Akt pathways, and protects neurons co-cultured with astrocytes damaged by ethanol

Journal of Neurochemistry

Volumn 103, Issue 2, 2007, Pages 557-568

  Pascual, Maria ^a   Guerri, Consuelo ^a  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

Activity dependent neuroprotective protein; Brain development; Ethanol; MAPK ERK; PI 3K Akt

Indexed keywords

ALCOHOL; CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; NAP PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN KINASE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BRAIN CORTEX; COCULTURE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENZYME ACTIVATION; ENZYME REGULATION; FEMALE; FETUS; MALE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE CELL LESION; NERVE CELL PLASTICITY; NERVE GROWTH; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECRETION; RAT; SIGNAL TRANSDUCTION; SYNAPSE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELL DIVISION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM DEPRESSANTS; COCULTURE TECHNIQUES; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENZYME ACTIVATION; ETHANOL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HOMEODOMAIN PROTEINS; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NEURITES; NEURONS; NEUROPROTECTIVE AGENTS; OLIGOPEPTIDES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 34848928509     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04761.x     Document Type: Article

References (57)

1. Bassan M., Zamostiano R., Davidson A. et al. (1999) Complete sequence of a novel protein containing a femtomolar-activity-dependent neuroprotective peptide. J. Neurochem. 72, 1283 1293.
2. Bonni A., Brunet A., West A. E., Datta S. R., Takasu M. A. Greenberg M. E. (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286, 1358 1362.
3. Brenneman D. E., Hauser J., Spong C. Y., Phillips T. M., Pert C. B. Ruff M. (1999) VIP and D-ala-peptide T-amide release chemokines which prevent HIV-1 GP120-induced neuronal death. Brain Res. 838, 27 36.
4. Chen Y. Swanson R. A. (2003) Astrocytes and brain injury. J. Cereb. Blood Flow Metab. 23, 137 149.
5. Climent E., Sancho-Tello M., Miñana R., Barettino D. Guerri C. (2000) Astrocytes in culture express the full-length Trk-B receptor and respond to brain derived neurotrophic factor by changing intracellular calcium levels: effect of ethanol exposure in rats. Neurosci. Lett. 288, 53 56.
6. Divinski I., Mittelman L. Gozes I. (2004) A femtomolar acting octapeptide interacts with tubulin and protects astrocytes against zinc intoxication. J. Biol. Chem. 279, 28531 28538.
7. Divinski I., Holtser-Cochav M., Vulih-Schultzman I., Steingart R. A. Gozes I. (2006) Peptide neuroprotection through specific interaction with brain tubulin. J. Neurochem. 98, 973 984.
8. Furman S., Steingart R. A., Mandel S., Hauser J. M., Brenneman D. E. Gozes I. (2004) Subcellular localization and secretion of activity-dependent neuroprotective protein in astrocytes. Neuron Glia Biol. 1, 193 199.
9. Guerri C. (2002) Mechanisms involved in central nervous system dysfunctions induced by prenatal ethanol exposure. Neurotox. Res. 4, 327 335.
10. Guerri C., Pascual M. Renau-Piqueras J. (2001) Glia and fetal alcohol syndrome. Neurotoxicology 22, 593 599.
11. Guerri C., Rubert G. Pascual M. (2006) Glial targets of developmental exposure to ethanol, in Brain Development: normal processes and the effects of alcohol and nicotine (Miller M. W., ed Vol. 18. pp. 295 312. Oxford University Press, New York.
12. Han B. H. Holtzman D. M. (2000) BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J. Neurosci. 20, 5775 5781.
13. Horne M. M. Guadagno T. M. (2003) A requirement for MAP kinase in the assembly and maintenance of the mitotic spindle. J. Cell Biol. 161, 1021 1028.
14. Hoshi M., Ohta K., Gotoh Y., Mori A., Murofushi H., Sakai H. Nishida E. (1992) Mitogen-activated-protein-kinase-catalyzed phosphorylation of microtubule-associated proteins, microtubule-associated protein 2 and microtubule-associated protein 4, induces an alteration in their function. Eur. J. Biochem. 203, 43 52.
15. Huang E. J. Reichardt L. F. (2001) Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677 736.
16. Ibata Y., Toya S. Kohsaka S. (1991) Effects of astroglia on the development of cultured neurons from embryonic rat cerebral cortex. Comp. Biochem. Physiol. C. 98, 139 146.
17. Ishida N., Hara T., Kamura T., Yoshida M., Nakayama K. Nakayama K. I. (2002) Phosphorylation of p27Kip1 on serine 10 is required for its binding to CRM1 and nuclear export. J. Biol. Chem. 277, 14355 14358.
18. Kilic E., Kilic U., Soliz J., Bassetti C. L., Gassmann M. Hermann D. M. (2005) Brain-derived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB J. 19, 2026 2028.
19. Kilic U., Kilic E., Jarve A. et al. (2006) Human vascular endothelial growth factor protects axotomized retinal ganglion cells in vivo by activating ERK-1/2 and Akt pathways. J. Neurosci. 26, 12439 12446.
20. Kumral A., Yesilirmak D. C., Sonmez U. et al. (2006) Neuroprotective effect of the peptides ADNF-9 and NAP on hypoxic-ischemic brain injury in neonatal rats. Brain Res. 1115, 169 178.
21. Leker R. R., Teichner A., Grigoriadis N., Ovadia H., Brenneman D. E., Fridkin M., Giladi E., Romano J. Gozes I. (2002) NAP, a femtomolar-acting peptide, protects the brain against ischemic injury by reducing apoptotic death. Stroke 33, 1085 1092.
22. Lieber C. S. De Carli L. M. (1994) Animal models of chronic ethanol toxicity. Methods Enzymol. 233, 585 594.
23. Mandel S., Rechavi G. Gozes I. (2007) Activity-dependent neuroprotective protein (ADNP) differentially interacts with chromatin to regulate genes essential for embryogenesis. Dev. Biol. 303, 814 824.
24. Mannella P. Brinton R. D. (2006) Estrogen receptor protein interaction with phosphatidylinositol 3-kinase leads to activation of phosphorylated Akt and extracellular signal-regulated kinase 1/2 in the same population of cortical neurons: a unified mechanism of estrogen action. J. Neurosci. 26, 9439 9447.
25. Marshall C. J. (1994) MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev. 4, 82 89.
26. Martinez R. Gomes F. C. (2005) Proliferation of cerebellar neurons induced by astrocytes treated with thyroid hormone is mediated by a cooperation between cell contact and soluble factors and involves the epidermal growth factor-protein kinase a pathway. J. Neurosci. Res. 80, 341 349.
27. Minana R., Duran J. M., Tomas M., Renau-Piqueras J. Guerri C. (2001) Neural cell adhesion molecule is endocytosed via a clathrin-dependent pathway. Eur. J. Neurosci. 13, 749 756.
28. Morishima-Kawashima M. Kosik K. S. (1996) The pool of map kinase associated with microtubules is small but constitutively active. Mol. Biol. Cell. 7, 893 905.
29. Newman E. A. (2004) New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 26, 536 542.
30. Parpura V., Basarsky T. A., Liu F., Jeftinija K., Jeftinija S. Haydon P. G. (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744 747.
31. Pinhasov A., Mandel S., Torchinsky A., Giladi E., Pittel Z., Goldsweig A. M., Servoss S. J., Brenneman D. E. Gozes I. (2003) Activity-dependent neuroprotective protein: a novel gene essential for brain formation. Brain Res. Dev. Brain Res. 144, 83 90.
32. Poggi S. H., Vink J., Goodwin K., Hill J. M., Brenneman D. E., Pinhasov A., Gozes I. Spong C. Y. (2002) Differential expression of embryonic and maternal activity-dependent neuroprotective protein during mouse development. Am. J. Obstet. Gynecol. 187, 973 976.
33. Poggi S. H., Goodwin K., Hill J. M., Brenneman D. E., Tendi E., Schinelli S., Abebe D. Spong C. Y. (2003) The role of activity-dependent neuroprotective protein in a mouse model of fetal alcohol syndrome. Am. J. Obstet. Gynecol. 189, 790 793.
34. Quintana F. J., Zaltzman R., Fernandez-Montesinos R., Herrera J. L., Gozes I., Cohen I. R. Pozo D. (2006) NAP, a peptide derived from the activity-dependent neuroprotective protein, modulates macrophage function. Ann. NY Acad. Sci. 1070, 500 506.
35. Ray J., Peterson D. A., Schinstine M. Gage F. H. (1993) Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc. Natl Acad. Sci. USA 90, 3602 3606.
36. Renau-Piqueras J., Zaragoza R., De Paz P., Baguena-Cervellera R., Megias L. Guerri C. (1989) Effects of prolonged ethanol exposure on the glial fibrillary acidic protein-containing intermediate filaments of astrocytes in primary culture: a quantitative immunofluorescence and immunogold electron microscopic study. J. Histochem. Cytochem. 37, 229 240.
37. Reszka A. A., Seger R., Diltz C. D., Krebs E. G. Fischer E. H. (1995) Association of mitogen-activated protein kinase with the microtubule cytoskeleton. Proc. Natl Acad. Sci. USA 92, 8881 8885.
38. Romano J., Beni-Adani L., Nissenbaum O. L., Brenneman D. E., Shohami E. Gozes I. (2002) A single administration of the peptide NAP induces long-term protective changes against the consequences of head injury: gene Atlas array analysis. J. Mol. Neurosci. 18, 37 345.
39. Rubert G., Minana R., Pascual M. Guerri C. (2006) Ethanol exposure during embryogenesis decreases the radial glial progenitorpool and affects the generation of neurons and astrocytes. J. Neurosci. Res. 84, 483 496.
40. Saez R., Burgal M., Renau-Piqueras J., Marques A. Guerri C. (1991) Evolution of several cytoskeletal proteins of astrocytes in primary culture: effect of prenatal alcohol exposure. Neurochem. Res. 16, 737 747.
41. Sanchis R., Sancho-Tello M. Guerri C. (1986) The effects of chronic alcohol consumption on pregnant rats and their offspring. Alcohol Alcohol. 21, 295 305.
42. Smith-Swintosky V. L., Gozes I., Brenneman D. E., D'Andrea M. R. Plata-Salaman C. R. (2005) Activity-dependent neurotrophic factor-9 and NAP promote neurite outgrowth in rat hippocampal and cortical cultures. J. Mol. Neurosci. 25, 225 238.
43. Spong C. Y., Abebe D. T., Gozes I., Brenneman D. E. Hill J. M. (2001) Prevention of fetal demise and growth restriction in a mouse model of fetal alcohol syndrome. J. Pharmacol. Exp. Ther. 297, 774 779.
44. Steingart R. A. Gozes I. (2006) Recombinant activity-dependent neuroprotective protein protects cells against oxidative stress. Mol. Cell Endocrinol. 252, 148 153.
45. Sutherland R. J., McDonald R. J. Savage D. D. (1997) Prenatal exposure to moderate levels of ethanol can have long-lasting effects on hippocampal synaptic plasticity in adult offspring. Hippocampus 7, 232 238.
46. Sweatt J. D. (2001) Protooncogenes subserve memory formation in the adult CNS. Neuron 31, 671 674.
47. Thoenen H. (2000) Neurotrophins and activity-dependent plasticity. Prog. Brain Res. 128, 183 191.
48. Valles S., Lindo L., Montoliu C., Renau-Piqueras J. Guerri C. (1994) Prenatal exposure to ethanol induces changes in the nerve growth factor and its receptor in proliferating astrocytes in primary culture. Brain Res. 656, 281 286.
49. Valles S., Pitarch J., Renau-Piqueras J. Guerri C. (1997) Ethanol exposure affects glial fibrillary acidic protein gene expression and transcription during rat brain development. J. Neurochem. 69, 2484 2493.
50. Visochek L., Steingart R. A., Vulih-Shultzman I., Klein R., Priel E., Gozes I. Cohen-Armon M. (2005) PolyADP-ribosylation is involved in neurotrophic activity. J. Neurosci. 25, 7420 7428.
51. Wang X. F. Cynader M. S. (1999) Effects of astrocytes on neuronal attachment and survival shown in a serum-free co-culture system. Brain Res. Brain Res. Protoc. 4, 209 216.
52. White D. M., Walker S., Brenneman D. E. Gozes I. (2000) CREB contributes to the increased neurite outgrowth of sensory neurons induced by vasoactive intestinal polypeptide and activity-dependent neurotrophic factor. Brain Res. 868, 31 38.
53. Wilkemeyer M. F., Chen S. Y., Menkari C. E., Brenneman D. E., Sulik K. K. Charness M. E. (2003) Differential effects of ethanol antagonism and neuroprotection in peptide fragment NAPVSIPQ prevention of ethanol-induced developmental toxicity. Proc. Natl Acad. Sci. USA 100, 8543 8548.
54. Zaltzman R., Alexandrovich A., Beni S. M., Trembovler V., Shohami E. Gozes I. (2004) Brain injury-dependent expression of activity-dependent neuroprotective protein. J. Mol. Neurosci. 24, 181 187.
55. Zamostiano R., Pinhasov A., Gelber E. et al. (2001) Cloning and characterization of the human activity-dependent neuroprotective protein. J. Biol. Chem. 276, 708 714.
56. Zemlyak I., Furman S., Brenneman D. E. Gozes I. (2000) A novel peptide prevents death in enriched neuronal cultures. Regul. Pept. 96, 39 43.
57. Zusev M. Gozes I. (2004) Differential regulation of activity-dependent neuroprotective protein in rat astrocytes by VIP and PACAP. Regul. Pept. 123, 33 41.