Chondroitin sulfate reduces cell death of rat hippocampal slices subjected to oxygen and glucose deprivation by inhibiting p38, NFκB and iNOS

Neurochemistry International

Volumn 58, Issue 6, 2011, Pages 676-683

  Martín De Saavedra, María Dolores ^a,b   Del Barrio, Laura ^a,b   Cañas, Noelia ^a,b   Egea, Javier ^a,b,c   Lorrio, Silvia ^a,b,c   Montell, Eullia ^d   Vergés, Josep ^d   García, Antonio G ^a,b,e   López, Manuela G ^a,b,c  

^a INSTITUTO TEÓFILO HERNANDO   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^d BIOIBERICA SA   (Spain)

^e HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

Author keywords

Chondroitin sulfate; Hippocampal slice; iNOS; Neuroprotection; NF B; Nitric oxide; Oxygen glucose deprivation; p38; p65

Indexed keywords

CHONDROITIN SULFATE; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; OXYGEN; SYNAPTOPHYSIN; SYNAPTOTAGMIN I;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN OXYGEN CONSUMPTION; CELL DEATH; CELL NUCLEUS; CONTROLLED STUDY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME RELEASE; HIPPOCAMPUS; IMMUNE RESPONSE; INTRACELLULAR SIGNALING; MALE; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; RAT; REOXYGENATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

RATTUS;

EID: 79953718336     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.02.006     Document Type: Article

References (59)

1. H. Arai, S. Kashiwagi, Y. Nagasaka, K. Uchida, Y. Hoshii, and K. Nakamura Oxidative modification of apolipoprotein E in human very-low-density lipoprotein and its inhibition by glycosaminoglycans Arch. Biochem. Biophys. 367 1999 1 8 (Pubitemid 29394186)
2. M. Asada, M. Shinomiya, M. Suzuki, E. Honda, R. Sugimoto, M. Ikekita, and T. Imamura Glycosaminoglycan affinity of the complete fibroblast growth factor family Biochim. Biophys. Acta 1790 2009 40 48
3. F.C. Barone, E.A. Irving, A.M. Ray, J.C. Lee, S. Kassis, S. Kumar, A.M. Badger, R.F. White, M.J. McVey, J.J. Legos, J.A. Erhardt, A.H. Nelson, E.H. Ohlstein, A.J. Hunter, K. Ward, B.R. Smith, J.L. Adams, and A.A. Parsons SB 239063, a second-generation p38 mitogen-activated protein kinase inhibitor, reduces brain injury and neurological deficits in cerebral focal ischemia J. Pharmacol. Exp. Ther. 296 2001 312 321 (Pubitemid 32112455)
4. 2) in human fibroblast cultures Glycoconj. J. 20 2004 133 141 (Pubitemid 38402431)
5. G.M. Campo, A. Avenoso, S. Campo, A. D'Ascola, P. Traina, and A. Calatroni Chondroitin-4-sulphate inhibits NF-kB translocation and caspase activation in collagen-induced arthritis in mice Osteoarthritis Cartilage 16 2008 1474 1483
6. G.M. Campo, A. Avenoso, S. Campo, A. D'Ascola, P. Traina, D. Sama, and A. Calatroni Glycosaminoglycans modulate inflammation and apoptosis in LPS-treated chondrocytes J. Cell. Biochem. 106 2009 83 92
7. N. Canas, T. Valero, M. Villarroya, E. Montell, J. Verges, A.G. Garcia, and M.G. Lopez Chondroitin sulfate protects SH-SY5Y cells from oxidative stress by inducing heme oxygenase-1 via phosphatidylinositol 3-kinase/Akt J. Pharmacol. Exp. Ther. 323 2007 946 953 (Pubitemid 350146070)
8. N. Canas, R. Gorina, A.M. Planas, J. Verges, E. Montell, A.G. Garcia, and M.G. Lopez Chondroitin sulfate inhibits lipopolysaccharide-induced inflammation in rat astrocytes by preventing nuclear factor kappa B activation Neuroscience 167 2010 872 879
9. C.C. Chan, C.R. Roberts, J.D. Steeves, and W. Tetzlaff Aggrecan components differentially modulate nerve growth factor-responsive and neurotrophin-3-responsive dorsal root ganglion neurite growth J. Neurosci. Res. 86 2008 581 592 (Pubitemid 351204471)
10. O. Chechneva, K. Dinkel, F. Cavaliere, M. Martinez-Sanchez, and K.G. Reymann Anti-inflammatory treatment in oxygen-glucose-deprived hippocampal slice cultures is neuroprotective and associated with reduced cell proliferation and intact neurogenesis Neurobiol. Dis. 23 2006 247 259 (Pubitemid 44080836)
11. P.S. Cohen, H. Schmidtmayerova, J. Dennis, L. Dubrovsky, B. Sherry, H. Wang, M. Bukrinsky, and K.J. Tracey The critical role of p38 MAP kinase in T cell HIV-1 replication Mol. Med. 3 1997 339 346 (Pubitemid 27295104)
12. C. Dell'Orbo, G. De Luca, L. Gioglio, D. Quacci, and C. Soldi The role of proteoglycans in maintaining collagen fibril morphology Histol. Histopathol. 10 1995 583 588
13. P. du Souich, A.G. Garcia, J. Verges, and E. Montell Immunomodulatory and anti-inflammatory effects of chondroitin sulphate J. Cell. Mol. Med. 13 2009 1451 1463
14. J. Egea, A.O. Rosa, M. Sobrado, L. Gandia, M.G. Lopez, and A.G. Garcia Neuroprotection afforded by nicotine against oxygen and glucose deprivation in hippocampal slices is lost in alpha7 nicotinic receptor knockout mice Neuroscience 145 2007 866 872 (Pubitemid 46441652)
15. J. Egea, A.G. Garcia, J. Verges, E. Montell, and M.G. Lopez Antioxidant, antiinflammatory and neuroprotective actions of chondroitin sulfate and proteoglycans Osteoarthritis Cartilage 2010
16. R. Garcia-Olivas, S. Vilaro, M. Reina, and S. Castel PDGF-stimulated cell proliferation and migration of human arterial smooth muscle cells Colocalization of PDGF isoforms with glycosaminoglycans Int. J. Biochem. Cell Biol. 39 2007 1915 1929 (Pubitemid 47321351)
17. S. Ghatan, S. Larner, Y. Kinoshita, M. Hetman, L. Patel, Z. Xia, R.J. Youle, and R.S. Morrison p38 MAP kinase mediates bax translocation in nitric oxide-induced apoptosis in neurons J. Cell Biol. 150 2000 335 347 (Pubitemid 30491357)
18. G. Gloire, E. Dejardin, and J. Piette Extending the nuclear roles of IkappaB kinase subunits Biochem. Pharmacol. 72 2006 1081 1089 (Pubitemid 44465842)
19. G. Gloire, S. Legrand-Poels, and J. Piette NF-kappaB activation by reactive oxygen species: fifteen years later Biochem. Pharmacol. 72 2006 1493 1505 (Pubitemid 44666727)
20. M. Grandati, C. Verrecchia, M.L. Revaud, M. Allix, R.G. Boulu, and M. Plotkine Calcium-independent NO-synthase activity and nitrites/nitrates production in transient focal cerebral ischaemia in mice Br. J. Pharmacol. 122 1997 625 630 (Pubitemid 27453086)
21. R. Hernanz, A.M. Briones, A. Martin, A.E. Beltran, T. Tejerina, M. Salaices, and M.J. Alonso Ouabain treatment increases nitric oxide bioavailability and decreases superoxide anion production in cerebral vessels J. Hypertens. 26 2008 1944 1954
22. M. Hetman, K. Kanning, J.E. Cavanaugh, and Z. Xia Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase J. Biol. Chem. 274 1999 22569 22580
23. G.K. Hunter, K.S. Wong, and J.J. Kim Binding of calcium to glycosaminoglycans: an equilibrium dialysis study Arch. Biochem. Biophys. 260 1988 161 167 (Pubitemid 18049993)
24. C. Iadecola, F. Zhang, S. Xu, R. Casey, and M.E. Ross Inducible nitric oxide synthase gene expression in brain following cerebral ischemia J. Cereb. Blood Flow Metab. 15 1995 378 384
25. C. Jomphe, M. Gabriac, T.M. Hale, L. Heroux, L.E. Trudeau, D. Deblois, E. Montell, J. Verges, and P. du Souich Chondroitin sulfate inhibits the nuclear translocation of nuclear factor-kappaB in interleukin-1beta-stimulated chondrocytes Basic Clin. Pharmacol. Toxicol. 102 2008 59 65 (Pubitemid 350301907)
26. B. Kaltschmidt, T. Sparna, and C. Kaltschmidt Activation of NF-kappa B by reactive oxygen intermediates in the nervous system Antioxid. Redox Signal. 1 1999 129 144 (Pubitemid 129619770)
27. G. Lisignoli, F. Grassi, N. Zini, S. Toneguzzi, A. Piacentini, D. Guidolin, C. Bevilacqua, and A. Facchini Anti-Fas-induced apoptosis in chondrocytes reduced by hyaluronan: evidence for CD44 and CD54 (intercellular adhesion molecule 1) involvement Arthritis Rheum. 44 2001 1800 1807 (Pubitemid 32758227)
28. J. Martel-Pelletier, F. Mineau, D. Jovanovic, J.A. Di Battista, and J.P. Pelletier Mitogen-activated protein kinase and nuclear factor kappaB together regulate interleukin-17-induced nitric oxide production in human osteoarthritic chondrocytes: possible role of transactivating factor mitogen-activated protein kinase-activated protein kinase (MAPKAPK) Arthritis Rheum. 42 1999 2399 2409 (Pubitemid 30333421)
29. E. Martin-Blanco p38 MAPK signalling cascades: ancient roles and new functions Bioessays 22 2000 637 645 (Pubitemid 30457955)
30. V. Mary, F. Wahl, A. Uzan, and J.M. Stutzmann Enoxaparin in experimental stroke: neuroprotection and therapeutic window of opportunity Stroke 32 2001 993 999 (Pubitemid 32285173)
31. A. Matsuzawa, K. Saegusa, T. Noguchi, C. Sadamitsu, H. Nishitoh, S. Nagai, S. Koyasu, K. Matsumoto, K. Takeda, and H. Ichijo ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity Nat. Immunol. 6 2005 587 592 (Pubitemid 41710729)
32. M.P. Mattson, and M.K. Meffert Roles for NF-kappaB in nerve cell survival, plasticity, and disease Cell Death Differ. 13 2006 852 860
33. M.P. Mattson, C. Culmsee, Z. Yu, and S. Camandola Roles of nuclear factor kappaB in neuronal survival and plasticity J. Neurochem. 74 2000 443 456 (Pubitemid 30053716)
34. J. Mocco, C.E. Shelton, P. Sergot, A.F. Ducruet, R.J. Komotar, M.L. Otten, S.A. Sosunov, R.B. Macarthur, T.P. Kennedy, and E.S. Connolly Jr. O-desulfated heparin improves outcome after rat cerebral ischemia/reperfusion injury Neurosurgery 61 2007 1297 1303 discussion 1303-1294
35. M. Morawski, M.K. Bruckner, P. Riederer, G. Bruckner, and T. Arendt Perineuronal nets potentially protect against oxidative stress Exp. Neurol. 188 2004 309 315 (Pubitemid 38891592)
36. M.A. Moro, A. Cardenas, O. Hurtado, J.C. Leza, and I. Lizasoain Role of nitric oxide after brain ischaemia Cell Calcium 36 2004 265 275 (Pubitemid 38992352)
37. A. Nurmi, P.J. Lindsberg, M. Koistinaho, W. Zhang, E. Juettler, M.L. Karjalainen-Lindsberg, F. Weih, N. Frank, M. Schwaninger, and J. Koistinaho Nuclear factor-kappaB contributes to infarction after permanent focal ischemia Stroke 35 2004 987 991 (Pubitemid 38419815)
38. E.P. Reeves, M. Williamson, B. Byrne, D.A. Bergin, S.G. Smith, P. Greally, R. O'Kennedy, S.J. O'Neill, and N.G. McElvaney IL-8 dictates glycosaminoglycan binding and stability of IL-18 in cystic fibrosis J. Immunol. 184 2010 1642 1652
39. A.I. Rojo, M. Salina, M. Salazar, S. Takahashi, G. Suske, V. Calvo, M.R. de Sagarra, and A. Cuadrado Regulation of heme oxygenase-1 gene expression through the phosphatidylinositol 3-kinase/PKC-zeta pathway and Sp1 Free Radic. Biol. Med. 41 2006 247 261 (Pubitemid 43928500)
40. A. Rolls, H. Avidan, L. Cahalon, H. Schori, S. Bakalash, V. Litvak, S. Lev, O. Lider, and M. Schwartz A disaccharide derived from chondroitin sulphate proteoglycan promotes central nervous system repair in rats and mice Eur. J. Neurosci. 20 2004 1973 1983 (Pubitemid 39331117)
41. A. Rolls, L. Cahalon, S. Bakalash, H. Avidan, O. Lider, and M. Schwartz A sulfated disaccharide derived from chondroitin sulfate proteoglycan protects against inflammation-associated neurodegeneration Faseb J. 20 2006 547 549 (Pubitemid 46671245)
42. F. Ronca, L. Palmieri, P. Panicucci, and G. Ronca Anti-inflammatory activity of chondroitin sulfate Osteoarthritis Cartilage 6 Suppl. A 1998 14 21 (Pubitemid 28255099)
43. M. Santra, M. Katakowski, R.L. Zhang, Z.G. Zhang, H. Meng, F. Jiang, and M. Chopp Protection of adult mouse progenitor cells and human glioma cells by de novo decorin expression in an oxygen- and glucose-deprived cell culture model system J. Cereb. Blood Flow Metab. 26 2006 1311 1322 (Pubitemid 44435245)
44. R. Saravanan, and A. Shanmugam Preventive effect of low molecular weight glycosaminoglycan from Amussium pleuronectus (Linne) on oxidative injury and cellular abnormalities in isoproterenol-induced cardiotoxicity in Wistar rats Appl. Biochem. Biotechnol. 162 2009 43 51
45. A. Schneider, A. Martin-Villalba, F. Weih, J. Vogel, T. Wirth, and M. Schwaninger NF-kappaB is activated and promotes cell death in focal cerebral ischemia Nat. Med. 5 1999 554 559 (Pubitemid 29220215)
46. G. Sethi, B. Sung, and B.B. Aggarwal Nuclear factor-kappaB activation: from bench to bedside Exp. Biol. Med. (Maywood) 233 2008 21 31
47. I.M. Shah, I.M. Macrae, and M. Di Napoli Neuroinflammation and neuroprotective strategies in acute ischaemic stroke - from bench to bedside Curr. Mol. Med. 9 2009 336 354
48. P.A. Singleton, T. Mirzapoiazova, Y. Guo, S. Sammani, N. Mambetsariev, F.E. Lennon, L. Moreno-Vinasco, and J.G. Garcia High-molecular-weight hyaluronan is a novel inhibitor of pulmonary vascular leakiness Am. J. Physiol. Lung Cell Mol. Physiol. 299 2010 L639 L651
49. M. Sobrado, J.M. Roda, M.G. Lopez, J. Egea, and A.G. Garcia Galantamine and memantine produce different degrees of neuroprotection in rat hippocampal slices subjected to oxygen-glucose deprivation Neurosci. Lett. 365 2004 132 136 (Pubitemid 38881640)
50. M. Strassburger, H. Braun, and K.G. Reymann Anti-inflammatory treatment with the p38 mitogen-activated protein kinase inhibitor SB239063 is neuroprotective, decreases the number of activated microglia and facilitates neurogenesis in oxygen-glucose-deprived hippocampal slice cultures Eur. J. Pharmacol. 592 2008 55 61
51. 2+-induced p38 MAP kinase activation EMBO Rep. 5 2004 161 166 (Pubitemid 38401195)
52. P.W. Tsai, S.G. Shiah, M.T. Lin, C.W. Wu, and M.L. Kuo Up-regulation of vascular endothelial growth factor C in breast cancer cells by heregulin-beta 1. A critical role of p38/nuclear factor-kappa B signaling pathway J. Biol. Chem. 278 2003 5750 5759
53. S.E. Tully, M. Rawat, and L.C. Hsieh-Wilson Discovery of a TNF-alpha antagonist using chondroitin sulfate microarrays J. Am. Chem. Soc. 128 2006 7740 7741 (Pubitemid 43945708)
54. N. Volpi Oral absorption and bioavailability of ichthyic origin chondroitin sulfate in healthy male volunteers Osteoarthritis Cartilage 11 2003 433 441 (Pubitemid 36722657)
55. K.W. Ward, J.W. Prokscht, L.M. Azzaranot, J.A. Mumawa, T.J. Roethke, G.J. Stelman, M.J. Walsh, K.S. Zeigler, J.E. McSurdy-Freed, J.R. Kehlert, J. Chokshi, M.A. Levy, and B.R. Smith Preclinical pharmacokinetics of SB-203580, a potent inhibitor of p38 mitogen-activated protein kinase Xenobiotica 31 2001 783 797 (Pubitemid 33116451)
56. Z. Xia, M. Dickens, J. Raingeaud, R.J. Davis, and M.E. Greenberg Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis Science 270 1995 1326 1331
57. Z.G. Zhang, T.S. Lu, and H.Y. Yuan Neuroprotective effects of ultra-low-molecular-weight heparin in vitro and vivo models of ischemic injury Fundam. Clin. Pharmacol. 2010
58. B.Q. Zhao, Y. Suzuki, K. Kondo, Y. Ikeda, and K. Umemura Combination of a free radical scavenger and heparin reduces cerebral hemorrhage after heparin treatment in a rabbit middle cerebral artery occlusion model Stroke 32 2001 2157 2163 (Pubitemid 32868116)
59. M. Zhou, R. Dominguez, and M. Baudry Superoxide dismutase/catalase mimetics but not MAP kinase inhibitors are neuroprotective against oxygen/glucose deprivation-induced neuronal death in hippocampus J. Neurochem. 103 2007 2212 2223 (Pubitemid 350173556)