Neuroserpin Attenuates H2O2-Induced Oxidative Stress in Hippocampal Neurons via AKT and BCL-2 Signaling Pathways

Journal of Molecular Neuroscience

Volumn 61, Issue 1, 2017, Pages 123-131

  Cheng, Yong ^a   Loh, Y Peng ^a   Birch, Nigel P ^b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Hippocampal neurons; Neuroprotection; Oxidative stress; Protease inhibitor; Reactive oxygen species

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CASPASE 3; HYDROGEN PEROXIDE; NEUROSERPIN; PROTEIN BCL 2; PROTEIN KINASE B; ANTIOXIDANT; NEUROPEPTIDE; SERINE PROTEINASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; EMBRYO; ENZYME ACTIVATION; FEMALE; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; NERVE CELL; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIOXIDANTS; CASPASE 3; CELLS, CULTURED; HIPPOCAMPUS; HYDROGEN PEROXIDE; NEURONS; NEUROPEPTIDES; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS, SPRAGUE-DAWLEY; SERINE PROTEINASE INHIBITORS; SERPINS; SIGNAL TRANSDUCTION;

EID: 84981249261     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-016-0807-7     Document Type: Article

References (59)

1. Bacskai BJ, Xia MQ, Strickland DK, Rebeck GW, Hyman BT (2000) The endocytic receptor protein LRP also mediates neuronal calcium signaling via N-methyl-D-aspartate receptors. Proc Natl Acad Sci U S A 97:11551–11556.
2. Behl C, Davis JB, Lesley R, Schubert D (1994) Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 77:817–827.
3. Berger P, Kozlov SV, Cinelli P, Kruger SR, Vogt L, Sonderegger P (1999) Neuronal depolarization enhances the transcription of the neuronal serine protease inhibitor neuroserpin. Mol Cell Neurosci 14:455–467.
4. Borges VM, Lee TW, Christie DL, Birch NP (2010) Neuroserpin regulates the density of dendritic protrusions and dendritic spine shape in cultured hippocampal neurons. J Neurosci Res 88:2610–2617.
5. Butterfield DA, Boyd-Kimball D (2004) Amyloid beta-peptide(1-42) contributes to the oxidative stress and neurodegeneration found in Alzheimer disease brain. Brain Pathol 14:426–432.
6. Cheng Y, Cawley NX, Loh YP (2013) Carboxypeptidase E/NFalpha1: a new neurotrophic factor against oxidative stress-induced apoptotic cell death mediated by ERK and PI3-K/AKT pathways. PLoS One 8:e71578.
7. Cheng Y, Rodriguiz RM, Murthy SR, Senatorov V, Thouennon E, Cawley NX, Aryal DK, Ahn S, Lecka-Czernik B, Wetsel WC, Loh YP (2015) Neurotrophic factor-alpha1 prevents stress-induced depression through enhancement of neurogenesis and is activated by rosiglitazone. Mol Psychiatry 20:744–754
8. Choi H, Park HH, Koh SH, Choi NY, Yu HJ, Park J, Lee YJ, Lee KY (2012) Coenzyme Q10 protects against amyloid beta-induced neuronal cell death by inhibiting oxidative stress and activating the P13K pathway. Neurotoxicology 33:85–90.
9. Cinelli P, Madani R, Tsuzuki N, Vallet P, Arras M, Zhao CN, Osterwalder T, Rulicke T, Sonderegger P (2001) Neuroserpin, a neuroprotective factor in focal ischemic stroke. Mol Cell Neurosci 18:443–457
10. de la Monte SM, Wands JR (2006) Molecular indices of oxidative stress and mitochondrial dysfunction occur early and often progress with severity of Alzheimer’s disease. J Alzheimers Dis 9:167–181.
11. Duarte AI, Santos P, Oliveira CR, Santos MS, Rego AC (2008) Insulin neuroprotection against oxidative stress is mediated by Akt and GSK-3beta signaling pathways and changes in protein expression. Biochim Biophys Acta 1783:994–1002.
12. Fabbro S, Schaller K, Seeds NW (2011) Amyloid-beta levels are significantly reduced and spatial memory defects are rescued in a novel neuroserpin-deficient Alzheimer’s disease transgenic mouse model. J Neurochem 118:928–938.
13. Fabbro S, Seeds NW (2009) Plasminogen activator activity is inhibited while neuroserpin is up-regulated in the Alzheimer disease brain. J Neurochem 109:303–315.
14. Gandhi, S., Abramov, A.Y., 2012. Mechanism of oxidative stress in neurodegeneration. Oxidative Medicine and Cellular Longevity, Article ID 428010.
15. Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G (2006) Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13:1423–1433.
16. Gharbi SI, Zvelebil MJ, Shuttleworth SJ, Hancox T, Saghir N, Timms JF, Waterfield MD (2007) Exploring the specificity of the PI3K family inhibitor LY294002. The Biochemical Journal 404:15–21.
17. Hastings GA, Coleman TA, Haudenschild CC, Stefansson S, Smith EP, Barthlow R, Cherry S, Sandkvist M, Lawrence DA (1997) Neuroserpin, a brain-associated inhibitor of tissue plasminogen activator is localized primarily in neurons. Implications for the regulation of motor learning and neuronal survival The Journal of Biological Chemistry 272:33062–33067.
18. Hayashi H, Campenot RB, Vance DE, Vance JE (2007) Apolipoprotein E-containing lipoproteins protect neurons from apoptosis via a signaling pathway involving low-density lipoprotein receptor-related protein-1. J Neurosci 27:1933–1941.
19. Herz J, Strickland DK (2001) LRP: a multifunctional scavenger and signaling receptor. J Clin Invest 108:779–784.
20. Hill RM, Parmar PK, Coates LC, Mezey E, Pearson JF, Birch NP (2000) Neuroserpin is expressed in the pituitary and adrenal glands and induces the extension of neurite-like processes in AtT-20 cells. The Biochemical Journal 345:595–601.
21. Hu K, Yang J, Tanaka S, Gonias SL, Mars WM, Liu Y (2006) Tissue-type plasminogen activator acts as a cytokine that triggers intracellular signal transduction and induces matrix metalloproteinase-9 gene expression. J Biol Chem 281:2120–2127.
22. Joseph JA, Shukitt-Hale B, Casadesus G, Fisher D (2005) Oxidative stress and inflammation in brain aging: nutritional considerations. Neurochem Res 30:927–935.
23. Kinghorn KJ, Crowther DC, Sharp LK, Nerelius C, Davis RL, Chang HT, Green C, Gubb DC, Johansson J, Lomas DA (2006) Neuroserpin binds Abeta and is a neuroprotective component of amyloid plaques in Alzheimer disease. J Biol Chem 281:29268–29277.
24. Krueger SR, Ghisu GP, Cinelli P, Gschwend TP, Osterwalder T, Wolfer DP, Sonderegger P (1997) Expression of neuroserpin, an inhibitor of tissue plasminogen activator, in the developing and adult nervous system of the mouse. J Neurosci 17:8984–8996.
25. Lebeurrier N, Liot G, Lopez-Atalaya JP, Orset C, Fernandez-Monreal M, Sonderegger P, Ali C, Vivien D (2005) The brain-specific tissue-type plasminogen activator inhibitor, neuroserpin, protects neurons against excitotoxicity both in vitro and in vivo. Mol Cell Neurosci 30:552–558.
26. Lee TW, Coates LC, Birch NP (2008) Neuroserpin regulates N-cadherin-mediated cell adhesion independently of its activity as an inhibitor of tissue plasminogen activator. J Neurosci Res 86:1243–1253.
27. Lee TW, Tsang VW, Birch NP (2015) Physiological and pathological roles of tissue plasminogen activator and its inhibitor neuroserpin in the nervous system. Front Cell Neurosci 9:396.
28. Lee YJ, Park KH, Park HH, Kim YJ, Lee KY, Kim SH, Koh SH (2009) Cilnidipine mediates a neuroprotective effect by scavenging free radicals and activating the phosphatidylinositol 3-kinase pathway. J Neurochem 111:90–100.
29. Li J, O W, Li W, Jiang ZG, Ghanbari HA (2013) Oxidative stress and neurodegenerative disorders. Int J Mol Sci 14:24438–24475.
30. Ma J, Tong Y, Yu D, Mao M (2012) Tissue plasminogen activator-independent roles of neuroserpin in the central nervous system. Neural Regeneration Research 7:146–151.
31. Madani R, Kozlov S, Akhmedov A, Cinelli P, Kinter J, Lipp HP, Sonderegger P, Wolfer DP (2003) Impaired explorative behavior and neophobia in genetically modified mice lacking or overexpressing the extracellular serine protease inhibitor neuroserpin. Mol Cell Neurosci 23:473–494.
32. Makarova A, Mikhailenko I, Bugge TH, List K, Lawrence DA, Strickland DK (2003) The low density lipoprotein receptor-related protein modulates protease activity in the brain by mediating the cellular internalization of both neuroserpin and neuroserpin-tissue-type plasminogen activator complexes. J Biol Chem 278:50250–50258.
33. Mancuso C, Scapagini G, Curro D, Giuffrida Stella AM, De Marco C, Butterfield DA, Calabrese V (2007) Mitochondrial dysfunction, free radical generation and cellular stress response in neurodegenerative disorders. Front Biosci 12:1107–1123.
34. Mantuano E, Inoue G, Li X, Takahashi K, Gaultier A, Gonias SL, Campana WM (2008a) The hemopexin domain of matrix metalloproteinase-9 activates cell signaling and promotes migration of Schwann cells by binding to low-density lipoprotein receptor-related protein. J Neurosci 28:11571–11582.
35. Mantuano E, Mukandala G, Li X, Campana WM, Gonias SL (2008b) Molecular dissection of the human alpha2-macroglobulin subunit reveals domains with antagonistic activities in cell signaling. J Biol Chem 283:19904–19911.
36. Melo A, Monteiro L, Lima RM, Oliveira DM, Cerqueira MD, El-Bacha RS (2011) Oxidative stress in neurodegenerative diseases: mechanisms and therapeutic perspectives. Oxidative Med Cell Longev 2011:467180.
37. Miranda E, Lomas DA (2006) Neuroserpin: a serpin to think about. Cell Mol Life Sci 63:709–722.
38. Mohsenifar A, Lotfi AS, Ranjbar B, Allameh A, Zaker F, Hasani L, Kia BE, Hasannia S (2007) A study of the oxidation-induced conformational and functional changes in neuroserpin. Iran Biomed J 11:41–46.
39. Navarro-Yubero C, Cuadrado A, Sonderegger P, Munoz A (2004) Neuroserpin is post-transcriptionally regulated by thyroid hormone. Brain research. Mol Brain Res 123:56–65.
40. Nielsen HM, Minthon L, Londos E, Blennow K, Miranda E, Perez J, Crowther DC, Lomas DA, Janciauskiene SM (2007) Plasma and CSF serpins in Alzheimer disease and dementia with Lewy bodies. Neurology 69:1569–1579.
41. Osterwalder T, Cinelli P, Baici A, Pennella A, Krueger SR, Schrimpf SP, Meins M, Sonderegger P (1998) The axonally secreted serine proteinase inhibitor, neuroserpin, inhibits plasminogen activators and plasmin but not thrombin. J Biol Chem 273:2312–2321.
42. Osterwalder T, Contartese J, Stoeckli ET, Kuhn TB, Sonderegger P (1996) Neuroserpin, an axonally secreted serine protease inhibitor. EMBO J 15:2944–2953.
43. Parmar PK, Coates LC, Pearson JF, Hill RM, Birch NP (2002) Neuroserpin regulates neurite outgrowth in nerve growth factor-treated PC12 cells. J Neurochem 82:1406–1415.
44. Qin XY, Cheng Y, Murthy SR, Selvaraj P, Loh YP (2014) Carboxypeptidase E-DeltaN, a neuroprotein transiently expressed during development protects embryonic neurons against glutamate neurotoxicity. PLoS One 9:e112996.
45. Radi E, Formichi P, Battisti C, Federico A (2014) Apoptosis and oxidative stress in neurodegenerative diseases. J Alzheimers Dis 42(Suppl 3):S125–S152.
46. Robinson SD, Lee TW, Christie DL, Birch NP (2015) Tissue plasminogen activator inhibits NMDA-receptor-mediated increases in calcium levels in cultured hippocampal neurons. Front Cell Neurosci 9:404.
47. Shi Q, Gibson GE (2007) Oxidative stress and transcriptional regulation in Alzheimer disease. Alzheimer Dis Assoc Disord 21:276–291.
48. Shi, Y., Mantuano, E., Inoue, G., Campana, W.M., Gonias, S.L., 2009. Ligand binding to LRP1 transactivates Trk receptors by a Src family kinase-dependent pathway. Science Signaling 2, ra18.
49. Stoeckli ET, Lemkin PF, Kuhn TB, Ruegg MA, Heller M, Sonderegger P (1989) Identification of proteins secreted from axons of embryonic dorsal-root-ganglia neurons. Eur J Biochem 180:249–258.
50. Thomas T, Thomas G, McLendon C, Sutton T, Mullan M (1996) Beta-amyloid-mediated vasoactivity and vascular endothelial damage. Nature 380:168–171.
51. Uranga RM, Katz S, Salvador GA (2013) Enhanced phosphatidylinositol 3-kinase (PI3K)/Akt signaling has pleiotropic targets in hippocampal neurons exposed to iron-induced oxidative stress. J Biol Chem 288:19773–19784.
52. Wang L, Zhang Y, Asakawa T, Ll W, Han S, Ll Q, Xiao B, Namba H, Lu C, Dong Q (2015) Neuroprotective effect of neuroserpin in oxygen-glucose deprivation- and reoxygenation-treated rat astrocytes in vitro. PLoS One 10:1–16
53. Wang S, Chong ZZ, Shang YC, Maiese K (2012) Wnt1 inducible signaling pathway protein 1 (WISP1) blocks neurodegeneration through phosphoinositide 3 kinase/Akt1 and apoptotic mitochondrial signaling involving Bad, Bax, Bim, and Bcl-xL. Curr Neurovasc Res 9:20–31.
54. Wannier-Morino P, Rager G, Sonderegger P, Grabs D (2003) Expression of neuroserpin in the visual cortex of the mouse during the developmental critical period. Eur J Neurosci 17:1853–1860.
55. Wu J, Echeverry R, Guzman J, Yepes M (2010) Neuroserpin protects neurons from ischemia-induced plasmin-mediated cell death independently of tissue-type plasminogen activator inhibition. Am J Pathol 177:2576–2584.
56. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129–1132
57. Yepes M, Sandkvist M, Wong MK, Coleman TA, Smith E, Cohan SL, Lawrence DA (2000) Neuroserpin reduces cerebral infarct volume and protects neurons from ischemia-induced apoptosis. Blood 96:569–576.
58. Zhang Y, Moheban DB, Conway BR, Bhattacharyya A, Segal RA (2000) Cell surface Trk receptors mediate NGF-induced survival while internalized receptors regulate NGF-induced differentiation. J Neurosci 20:5671–5678.
59. Zhang Y, Zhao J, Wang J, Jiao X (2010) Brain-derived neurotrophic factor inhibits phenylalanine-induced neuronal apoptosis by preventing RhoA pathway activation. Neurochem Res 35:480–486