Targeting IKK2 by pharmacological inhibitor AS602868 prevents excitotoxic injury to neurons and oligodendrocytes

Journal of Neural Transmission

Volumn 115, Issue 5, 2008, Pages 693-701

  Sarnico, I ^a   Boroni, F ^a   Benarese, M ^a   Alghisi, M ^a   Valerio, A ^a   Battistin, L ^b   Spano, P ^a,b   Pizzi, M ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

^b IRCCS SAN CAMILLO HOSPITAL   (Italy)

Author keywords

Anilinopyrimidine; AS602868; Glutamate; Hippocampal slices; IKK2; NF B

Indexed keywords

1 [5 HYDROXY 2 (2 THIENYL) 4 QUINAZOLINYLAMINO] 3 METHYL 2,5 PYRROLEDIONE; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN SLICE; CELL ACTIVITY; CELL DEATH; CELL DEGENERATION; CONTROLLED STUDY; DEMYELINATION; EXCITOTOXICITY; HIPPOCAMPUS; NERVE CELL; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; TRAUMATIC BRAIN INJURY;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EXCITATORY AMINO ACID AGONISTS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; I-KAPPA B KINASE; MYELIN BASIC PROTEINS; N-METHYLASPARTATE; NEURONS; NEUROPROTECTIVE AGENTS; OLIGODENDROGLIA; PYRIMIDINES; RATS; RATS, WISTAR; TIME FACTORS;

EID: 44749091716     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-007-0016-1     Document Type: Article

References (54)

1. Akassoglou K, Douni E, Bauer J, Lassmann H, Kollias G, Probert L (2003) Exclusive tumor necrosis factor (TNF) signaling by the p75TNF receptor triggers inflammatory ischemia in the CNS of transgenic mice. Proc Natl Acad Sci USA 100:709-714
2. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973
3. Bachis A, Colangelo AM, Vicini S, Doe PP, De Bernardi MA, Brooker G, Mocchetti I (2001) Interleukin-10 prevents glutamate-mediated cerebellar granule cell death by blocking caspase-3-like activity. J Neurosci 21:3104-3112
4. Bahr BA (1995) Long-term hippocampal slices: a model system for investigating synaptic mechanisms and pathologic processes. J Neurosci Res 42:294-305
5. Beattie MS, Hermann GE, Rogers RC, Bresnhan JC (2002) Cell death in models of spinal cord injury. Prog Brain Res 137:37-47
6. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A 92:7162-6
7. Chen LF, Greene WC (2004) Shaping the nuclear action of NF-κB. Nat Rev Mol Cell Biol 5:392-401
8. Cherng JM, Lin HJ, Hung MS, Lin YR, Chan MH, Lin JC (2006) Inhibition of nuclear factor kappaB is associated with neuroprotective effects of glycyrrhizic acid on glutamate-induced excitotoxicity in primary neurons. Eur J Pharmacol 547:10-21
9. Cho S, Liu D, Fairman D, Li P, Jenkins L, McGonigle P, Wood A (2004) Spatiotemporal evidence of apoptosis-mediated ischemic injury in organotypic hippocampal slice cultures. Neurochem Int 45:117-27
10. Clemens JA, Stephenson DT, Smalstig EB, Dixon EP, Little SP (1997) Global ischemia activates nuclear factor-kappa B in forebrain neurons of rats. Stroke 28:1073-1080
11. Frelin C, Imbert V, Griessinger E, Loubat A, Dreano M, Peyron JF (2003) AS602868, a pharmacological inhibitor of IKK2, reveals the apoptotic potential of TNF-alpha in Jurkat leukemic cells. Oncogene 22:8187-8194
12. Frelin C, Imbert V, Griessinger E, Peyron AC, Rochet N, Philip P, Dageville C, Sirvent A, Hummelsberger M, berard E, Dreano M, Sirvent N, Peyron JF (2005) Targeting NF-kappaB activation via pharmacologic inhibition of IKK2-induced apoptosis of human acute myeloid leukemia cells. Blood 105:804-811
13. Gao Z, Hwang D, Bataille F, Lefevre M, York D, Quon MJ, Ye J (2002) Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex. J Biol Chem 277:48115-48121
14. Goffi F, Boroni F, Benarese M, Sarnico I, Benetti A, Spano PF, Pizzi M (2005) The inhibitor of I kappa B alpha phosphorylation BAY 11-7082 prevents NMDA neurotoxicity in mouse hippocampal slices. Neurosci Lett 377:147-151
15. Grilli M, Pizzi M, Memo M, Spano P (1996) Neuroprotection by aspirin and sodium salicylate through blockade of NF-kappaB activation. Science 274:1383-1385
16. Hayden MS, Ghosh S (2004) Signaling to NF-kappaB. Genes Dev 18:2195-2224
17. Heckmann A, Waltzinger C, Paul Jolicoeur P, Dreano M, Kosco-Vilbois MH, Sagot Y (2004) IKK2 inhibitor alleviates kidney and wasting diseases in a murine model of human AIDS. Am J Pathol 164:1253-1262
18. Herrmann O, Baumann B, de Lorenzi R, Muhammad S, Zhang W, Kleesiek J, Malfertheiner M, Köhrmann M, Potrovita I, Maegele I, Beyer C, Burke JR, Hasan MT, Bujard H, Wirth T, Pasparakis M, Schwaninger M (2005) IKK mediates ischemia-induced neuronal death. Nat Med 11:1322-1329
19. Hu MC, Lee DF, Xia W, Golfman LS, Ou-Yang F, Yang JY, Zou Y, Bao S, Hanada N, Saso H, Kobayashi R, Hung MC (2004) IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 117:225-237
20. Inta I, Paxian S, Maegele I, Zhang W, Pizzi M, Spano PF, Sarnico I, Muhammad S, Herrmann O, Inta D, Baumann B, Liou HC, Schmid RM, Schwaninger M (2006) Bim and Noxa are candidates to mediate the deleterious effect of the NF-kappa B subunit RelA in cerebral ischemia. J Neurosci 26:12896-12903
21. Jourdan M, Moreaux J, Vos JD, Hose D, Mahtouk K, Abouladze M, Robert N, Baudard M, Rème T, Romanelli A, Goldschmidt H, Rossi JF, Dreano M, Klein B (2007) Targeting NF-kappaB pathway with an IKK2 inhibitor induces inhibition of multiple myeloma cell growth. Br J Haematol 138:160-168
22. Kaltschmidt B, Uherek M, Volk B, Baeuerle PA, Kaltschmidt C (1997) Transcription factor NF-κB is activated in primary neurons by amyloid β peptides and in neurons surrounding early plaques from patients with Alzheimer's disease. Proc Natl Acad Sci USA 94:2642-2647
23. Karin M, Yamamoto Y, Wang QM (2004) The IKK NF-kappa B system: a treasure trove for drug development. Nat Rev Drug Discov 3:17-26
24. Khoshnan A, Ko J, Watkin EE, Paige LA, Reinhart PH, Patterson PH (2004) Activation of the IkappaB kinase complex and nuclear factor-kappaB contributes to mutant huntingtin neurotoxicity. J Neurosci 24:7999-8008
25. Lamberti C, Lin KM, Yamamoto Y, Verma U, Verma IM, Byers S, Gaynor RB (2001) Regulation of beta-catenin function by the IkappaB kinases. J Biol Chem 276:42276-42286
26. Li S, Mealing GA, Morley P, Stys PK (1999) Novel injury mechanism in anoxia and trauma of spinal cord white matter: glutamate release via reverse Na+-dependent glutamate transport. J Neurosci 19:RC16
27. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, Dong HX, Wu YJ, Fan GS, Jacquin MF, Hsu CY, Choi DW (1997) Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 17:5395-406
28. Liu Y, Wong TP, Aarts M, Rooyakkers A, Liu L, Lai TW, Wu DC, Lu J, Tymianski M, Craig AM, Wang YT (2007) NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J Neurosci 27:2846-2857
29. Luedde T, Assmus U, Wüstefeld T, Meyer zu Vilsendorf A, Roskams T, Schmidt-Supprian M, Rajewsky K, Brenner DA, Manns MP, Pasparakis M, Trautwein C (2005) Deletion of IKK2 in hepatocytes does not sensitize these cells to TNF-induced apoptosis but protects from ischemia/reperfusion injury. J Clin Invest 115:849-859
30. Mandai K, Matsumoto M, Kitagawa K, Matsushita K, Ohtsuki T, Mabuchi T, Colman DR, Kamada T, Yanagihara T (1997) Ischemic damage and subsequent proliferation of oligodendrocytes in focal cerebral ischemia. Neuroscience 77:849-861
31. Matute C, Alberdi E, Domercq M, Pérez-Cerdà F, Pérez-Samartìn A, Sànchez-Gòmez MV (2001) The link between excitotoxic oligodendroglial death and demyelinating diseases. Trends Neurosci 24:224-230
32. McDonald JW, Althomsons SP, Hyrc KL, Choi DW, Goldberg MP (1998) Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat Med 4:291-297
33. Nurmi A, Lindsberg PJ, Koistinaho M, Zhang W, Juettler E, Karjalainen-Lindsberg ML, Weih F, Frank N, Schwaninger M, Koistinaho J (2004) Nuclear factor-kappaB contributes to infarction after permanent focal ischemia. Stroke 35:987-991
34. + current enhancement by neurotoxic beta-amyloid peptides in nerve growth factor-differentiated PC-12 cells and hippocampal neurones. J Neurochem 94:572-586
35. Pitt D, Werner P, Raine CS (2000) Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6:67-70
36. Pizzi M, Fallacara C, Arrighi V, Memo M, Spano PF (1993) Attenuation of excitatory amino acid toxicity by metabotropic glutamate receptor agonists and aniracetam in primary cultures of cerebellar granule cells. J Neurochem 61:683-689
37. 2+ concentration and excitotoxicity in cultured cerebellar granule cells: pivotal role of protein kinase C. Mol Pharmacol 49:586-594
38. Pizzi M, Goffi F, Boroni F, Benarese M, Perkins SE, Liou HC, Spano P (2002) Opposing roles for NF-kappa B/Rel factors p65 and c-Rel in the modulation of neuron survival elicited by glutamate and interleukin-1beta. J Biol Chem 277:20717-20723
39. Pizzi M, Sarnico I, Boroni F, Benarese M, Dreano M, Garotta G, Valerio A, Spano P (2004) Prevention of neuron and oligodendrocyte degeneration by interleukin-6 (IL-6) and IL-6 receptor/IL-6 fusion protein in organotypic hippocampal slices. Mol Cell Neurosci 25:301-311
40. Pizzi M, Sarnico I, Boroni F, Benarese M, Steimberg N, Mazzoleni G, Dietz GP, Bahr M, Liou HC, Spano PF (2005a) NF-kappaB factor c-Rel mediates neuroprotection elicited by mGlu5 receptor agonists against amyloid beta-peptide toxicity. Cell Death Differ 12:761-772
41. Pizzi M, Sarnico I, Boroni F, Benetti A, Benarese M, Spano PF (2005b) Inhibition of IκBα phosphorylation prevents glutamate-induced NF-κB activation and neuronal cell death. Acta Neurochirurgia Suppl 93:59-63
42. Potrovita I, Zhang W, Burkly L, Hahm K, Lincecum JZ, Wang MZ, Maurer MH, Rossner M, Schneider A, Schwaninger M (2004) Tumor necrosis factor-like weak inducer of apoptosis-induced neurodegeneration. J Neurosci 24:8237-8244
43. Qin ZH, Chen RW, Wang Y, Nakai M, Chuang DM, Chase TN (1999) Nuclear factor kappaB nuclear translocation upregulates c-Myc and p53 expression during NMDA receptor-mediated apoptosis in rat striatum. J Neurosci 19:4023-4033
44. Rothman SM, Olney JW (1986) Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann Neurol 19:105-11
45. Sakhi S, Bruce A, Sun N, Tocco G, Baudry M, Schreiber SS (1997) Induction of tumor suppressor p53 and DNA fragmentation in organotypic hippocampal cultures following excitotoxin treatment. Exp Neurol 145:81-8
46. Sakurai H, Suzuki S, Kawasaki N, Nakano H, Okazaki T, Chino A, Doi T, Saiki I (2003) Tumor necrosis factor-alpha-induced IKK phosphorylation of NF-kappaB p65 on serine 536 is mediated through the TRAF2, TRAF5, and TAK1 signaling pathway. J Biol Chem 278:36916-36923
47. Schneider A, Martin-Villalba A, Weih F, Vogel J, Wirth T, Schwaninger M (1999) NF-kappaB is activated and promotes cell death in focal cerebral ischemia. Nat Med 5:554-559
48. Smith T, Groom A, Zhu B, Turski L (2000) Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat Med 6:62-66
49. Ueno T, Sawa Y, Kitagawa-Sakakida S, Nishimura M, Morishita R, Kaneda Y, Kohmura E, Yoshimine T, Matsuda H (2001) Nuclear factor-kappa B decoy attenuates neuronal damage after global brain ischemia: a future strategy for brain protection during circulatory arrest. J Thorac Cardiovasc Surg 122:720-727
50. Valerio A, Boroni F, Benarese M, Sarnico I, Ghisi V, Bresciani LG, Ferrario M, Borsani G, Spano P, Pizzi M (2006) NF-kappaB pathway: a target for preventing beta-amyloid (Abeta)-induced neuronal damage and Abeta42 production. Eur J Neurosci 23:1711-1720
51. Vollgraf U, Wegner M, Richter-Landsberg C (1999) Activation of AP-1 and nuclear factor-kappaB transcription factors is involved in hydrogen peroxide-induced apoptotic cell death of oligodendrocytes. J Neurochem 73:2501-2509
52. Werner P, Pitt D, Raine CS (2001) Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann Neurol 50:169-180
53. Yin K, Juurlink BH (2000) Regulation of expression of nuclear factor kappa B RelA in oligodendrocytes: effect of hypoxia. Neuroreport 11:1877-1881
54. Zhang W, Potrovita I, Tarabin V, Herrmann O, Beer V, Weih F, Schneider A, Schwaninger M (2005) Neuronal activation of NF-kappaB contributes to cell death in cerebral ischemia. J Cereb Blood Flow Metab 25:30-40