Neurobiology of Aging
Volume 30, Issue 6 , Pages 920-931 , June 2009

Interleukin-4 mediates the neuroprotective effects of rosiglitazone in the aged brain

Received 16 May 2007 ,Revised 4 September 2007 ,Accepted 5 September 2007.

References 

  1. Akiyama TE, Sakai S, Lambert G, Nicol CJ, Matsusue K, Pimprale S, et al. Conditional disruption of the peroxisome proliferator-activated receptor gamma gene in mice results in lowered expression of ABCA1, ABCG1, and apoE in macrophages and reduced cholesterol efflux. Mol. Cell. Biol. 2002;22:2607–2619
  2. Allahtavakoli M, Shabanzadeh AP, Sadr SS, Parviz M, Djahanguiri B. Rosiglitazone, a peroxisome proliferator-activated receptor-gamma ligand, reduces infarction volume and neurological deficits in an embolic model of stroke. Clin. Exp. Pharmacol. Physiol. 2006;33:1052–1058
  3. Bake S, Sohrabji F. 17Beta-estradiol differentially regulates blood–brain barrier permeability in young and aging female rats. Endocrinology. 2004;145:5471–5475
  4. Barry CE, Nolan Y, Clarke RM, Lynch A, Lynch MA. Activation of c-Jun-N-terminal kinase is critical in mediating lipopolysaccharide-induced changes in the rat hippocampus. J. Neurochem. 2005;93:221–231
  5. Berger J, Moller DE. The mechanisms of action of PPARs. Annu. Rev. Med. 2002;53:409–435
  6. Bernardo A, Minghetti L. PPAR-gamma agonists as regulators of microglial activation and brain inflammation. Curr. Pharm. Des. 2006;12:93–109
  7. Bernardo A, Levi G, Minghetti L. Role of the peroxisome proliferator-activated receptor-gamma (PPAR-gamma) and its natural ligand 15-deoxy-Delta12,14-prostaglandin J2 in the regulation of microglial functions. Eur. J. Neurosci. 2000;12:2215–2223
  8. Bernardo A, Ajmone-Cat MA, Levi G, Minghetti L. 15-Deoxy-delta12,14-prostaglandin J2 regulates the functional state and the survival of microglial cells through multiple molecular mechanisms. J. Neurochem. 2003;87:742–751
  9. Bernardo A, Gasparini L, Ongini E, Minghetti L. Dynamic regulation of microglial functions by the non-steroidal anti-inflammatory drug NCX 2216 implications for chronic treatments of neurodegenerative diseases. Neurobiol. Dis. 2006;22:25–32
  10. Bogacka I, Xie H, Bray GA, Smith SR. The effect of pioglitazone on peroxisome proliferator-activated receptor-gamma target genes related to lipid storage in vivo. Diabates Care. 2004;27:1660–1667
  11. Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S. MAPK CREB and zif268 are all required for the consolidation of recognition memory. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2003;358:805–814
  12. Chawla A, Barak Y, Nagy L, Liao D, Tontonoz P, Evans RM. PPAR-gamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat. Med. 2001;7:48–52
  13. Clarke RM, O’Connell F, Lyons A, Lynch MA. The HMG-CoA reductase inhibitor, atorvastatin, attenuates the effects of acute administration of amyloid-beta1-42 in the rat hippocampus in vivo. Neuropharmacology. 2007;52:136–145
  14. Combs CK, Johnson DE, Karlo JC, Cannady SB, Landreth GE. Inflammatory mechanisms in Alzheimer's disease: inhibition of beta-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARgamma agonists. J. Neurosci. 2000;20:558–567
  15. Combs CK, Bates P, Karlo JC, Landreth GE. Regulation of beta-amyloid stimulated proinflammatory responses by peroxisome proliferator-activated receptor alpha. Neurochem. Int. 2001;39:449–457
  16. Costello DA, O’Leary DM, Herron CE. Agonists of peroxisome proliferator-activated receptor-gamma attenuate the Abeta-mediated impairment of LTP in the hippocampus in vitro. Neuropharmacology. 2005;49:359–366
  17. Cristiano L, Bernardo A, Ceru MP. Peroxisome proliferator-activated receptors (PPARs) and peroxisomes in rat cortical and cerebellar astrocytes. J. Neurocytol. 2001;30:671–683
  18. Davies CA, Loddick SA, Toulmond S, Stroemer RP, Hunt J, Rothwell NJ. The progression and topographic distribution of interleukin-1beta expression after permanent middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 1999;19:87–98
  19. Feinstein DL, Galea E, Gavrilyuk V, Brosnan CF, Whitacre CC, Dumitrescu-Ozimek L, et al. Peroxisome proliferator-activated receptor-gamma agonists prevent experimental autoimmune encephalomyelitis. Ann. Neurol. 2002;51:694–702
  20. Gelinas DS, Lambermon MH, McLaurin J. Ciglitazone increases basal cytokine expression in the central nervous system of adult rats. Brain Res. 2005;1034:139–146
  21. Gooney M, Lynch MA. Long-term potentiation in the dentate gyrus of the rat hippocampus is accompanied by brain-derived neurotrophic factor-induced activation of TrkB. J. Neurochem. 2001;77:1198–1207
  22. Griffin R, Nally R, Nolan Y, McCartney Y, Linden J, Lynch MA. The age-related attenuation in long-term potentiation is associated with microglial activation. J. Neurochem. 2006;99:1263–1272
  23. Hafezi-Moghadam A, Thomas KL, Wagner DD. ApoE-deficiency leads to a progressive age-dependent blood–brain barrier leakage. Am. J. Physiol. Cell Physiol. 2007;292:C1256–C1262
  24. Hasegawa H, Takano H, Zou Y, Qin Y, Hizukuri K, Odaka K, et al. Pioglitazone, a peroxisome proliferator-activated receptor gamma activator, ameliorates experimental autoimmune myocarditis by modulating Th1/Th2 balance. J. Mol. Cell. Cardiol. 2005;38:257–265
  25. Heneka MT, Klockgether T, Feinstein DL. Peroxisome proliferator-activated receptor-gamma ligands reduce neuronal inducible nitric oxide synthase expression and cell death in vivo. J. Neurosci. 2000;20:6862–6867
  26. Heneka MT, Sastre M, Dumitrescu-Ozimek L, Hanke A, Dewachter I, Kuiperi C, et al. Acute treatment with the PPARgamma agonist pioglitazone and ibuprofen reduces glial inflammation and Abeta1-42 levels in APPV717I transgenic mice. Brain. 2005;128:1442–1453
  27. Hodgkinson CP, Ye S. Microarray analysis of peroxisome proliferator-activated receptor-gamma induced changes in gene expression in macrophages. Biochem. Biophys. Res. Commun. 2003;308:505–510
  28. Inestrosa NC, Godoy JA, Quintanilla RA, Koenig CS, Bronfman M. Peroxisome proliferator-activated receptor gamma is expressed in hippocampal neurons and its activation prevents beta-amyloid neurodegeneration: role of Wnt signaling. Exp. Cell Res. 2005;304:91–104
  29. Kageyama H, Hirano T, Okada K, Ebara T, Kageyama A, Murakami T, et al. Lipoprotein lipase mRNA in white adipose tissue but not in skeletal muscle is increased by pioglitazone through PPAR-gamma. Biochem. Biophys. Res. Commun. 2003;305:22–27
  30. Kainu T, Wikstrom AC, Gustafsson JA, Pelto-Huikko M. Localization of the peroxisome proliferator-activated receptor in the brain. Neuroreport. 1994;5:2481–2485
  31. Kelly A, Vereker E, Nolan Y, Brady M, Barry C, Loscher CE, et al. Activation of p38 plays a pivotal role in the inhibitory effect of lipopolysaccharide and interleukin-1 beta on long-term potentiation in rat dentate gyrus. J. Biol. Chem. 2003;278:19453–19462
  32. Khandoudi N, Delerive P, Berrebi-Bertrand I, Buckingham RE, Staels B, Bril A. Rosiglitazone, a peroxisome proliferator-activated receptor-gamma, inhibits the Jun NH(2)-terminal kinase/activating protein 1 pathway and protects the heart from ischemia/reperfusion injury. Diabetes. 2002;51:1507–1514
  33. Kim EJ, Kwon KJ, Park JY, Lee SH, Moon CH, Baik EJ. Effects of peroxisome proliferator-activated receptor agonists on LPS-induced neuronal death in mixed cortical neurons: associated with iNOS and COX-2.. Brain Res. 2002;941:1–10
  34. Kliewer SA, Lehmann JM, Milburn MV, Willson TM. The PPARs and PXRs: nuclear xenobiotic receptors that define novel hormone signaling pathways. Recent Prog. Horm. Res. 1999;54:345-L367;(Discussion 67–68)
  35. Kuhn R, Rajewsky K, Muller W. Generation and analysis of interleukin-4 deficient mice. Science. 1991;254:707–710
  36. Lennon AM, Ramauge M, Dessouroux A, Pierre M. MAP kinase cascades are activated in astrocytes and preadipocytes by 15-deoxy-Delta(12-14)-prostaglandin J(2) and the thiazolidinedione ciglitazone through peroxisome proliferator activator receptor gamma-independent mechanisms involving reactive oxygenated species. J. Biol. Chem. 2002;277:29681–29685
  37. Li AJ, Katafuchi T, Oda S, Hori T, Oomura Y. Interleukin-6 inhibits long-term potentiation in rat hippocampal slices. Brain Res. 1997;748:30–38
  38. Lonergan PE, Martin DS, Horrobin DF, Lynch MA. Neuroprotective actions of eicosapentaenoic acid on lipopolysaccharide-induced dysfunction in rat hippocampus. J. Neurochem. 2004;91:20–29
  39. Luna-Medina R, Cortes-Canteli M, Alonso M, Santos A, Martinez A, Perez-Castillo A. Regulation of inflammatory response in neural cells in vitro by thiadiazolidinones derivatives through peroxisome proliferator-activated receptor gamma activation. J. Biol. Chem. 2005;280:21453–21462
  40. Luo Y, Yin W, Signore AP, Zhang F, Hong Z, Wang S, et al. Neuroprotection against focal ischemic brain injury by the peroxisome proliferator-activated receptor-gamma agonist rosiglitazone. J. Neurochem. 2006;97:435–448
  41. Lynch AM, Lynch MA. The age-related increase in IL-1 type I receptor in rat hippocampus is coupled with an increase in caspase-3 activation. Eur. J. Neurosci. 2002;15:1779–1788
  42. Lynch AM, Moore M, Craig S, Lonergan PE, Martin DS, Lynch MA. Analysis of interleukin-1 beta-induced cell signaling activation in rat hippocampus following exposure to gamma irradiation. Protective effect of eicosapentaenoic acid. J. Biol. Chem. 2003;278:51075–51084
  43. Lynch AM, Loane DJ, Minogue AM, Clarke RM, Kilroy D, Nally RE, et al. Eicosapentaenoic acid confers neuroprotection in the amyloid-beta challenged aged hippocampus. Neurobiol. Aging. 2007;28:845–855
  44. Maher FO, Nolan Y, Lynch MA. Down-regulation of IL-4-induced signalling in hippocampus contributes to deficits in LTP in the aged rat. Neurobiol. Aging. 2005;26:717–728
  45. Martin DS, Lonergan PE, Boland B, Fogarty MP, Brady M, Horrobin DF, et al. Apoptotic changes in the aged brain are triggered by interleukin-1beta-induced activation of p38 and reversed by treatment with eicosapentaenoic acid. J. Biol. Chem. 2002;277:34239–34246
  46. McGahon B, Maguire C, Kelly A, Lynch MA. Activation of p42 mitogen-activated protein kinase by arachidonic acid and trans-1-amino-cyclopentyl-1,3-dicarboxylate impacts on long-term potentiation in the dentate gyrus in the rat: analysis of age-related changes. Neuroscience. 1999;90:1167–1175
  47. Minogue AM, Schmid AW, Fogarty MP, Moore AC, Campbell VA, Herron CE, et al. Activation of the c-Jun N-terminal kinase signaling cascade mediates the effect of amyloid-beta on long-term potentiation and cell death in hippocampus: a role for interleukin-1beta?. J. Biol. Chem. 2003;278:27971–27980
  48. Minogue, A.M., Lynch, A.M., Loane, D.J., Herron, C.E., Lynch, M.A., 2007. Modulation of amyloid-beta-induced and age associated changes in rat hippocampus by eicosapentaenoic acid. J. Neurochem., in press.
  49. Moreno S, Farioli-Vecchioli S, Ceru MP. Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS. Neuroscience. 2004;123:131–145
  50. Nolan Y, Maher FO, Martin DS, Clarke RM, Brady MT, Bolton AE, et al. Role of interleukin-4 in regulation of age-related inflammatory changes in the hippocampus. J. Biol. Chem. 2005;280:9354–9362
  51. Park EJ, Park SY, Joe EH, Jou I. 15d-PGJ2 and rosiglitazone suppress Janus kinase-STAT inflammatory signaling through induction of suppressor of cytokine signaling 1 (SOCS1) and SOCS3 in glia. J. Biol. Chem. 2003;278:14747–14752
  52. Park KS, Lee RD, Kang SK, Han SY, Park KL, Yang KH, et al. Neuronal differentiation of embryonic midbrain cells by upregulation of peroxisome proliferator-activated receptor-gamma via the JNK-dependent pathway. Exp. Cell Res. 2004;297:424–433
  53. Pedersen WA, McMillan PJ, Kulstad JJ, Leverenz JB, Craft S, Haynatzki GR. Rosiglitazone attenuates learning and memory deficits in Tg2576 Alzheimer mice. Exp. Neurol. 2006;199:265–273
  54. Petrova TV, Akama KT, Van Eldik LJ. Cyclopentenone prostaglandins suppress activation of microglia: down-regulation of inducible nitric-oxide synthase by 15-deoxy-Delta12,14-prostaglandin J2. Proc. Natl. Acad. Sci. U.S.A. 1999;96:4668–4673
  55. Ricote M, Li AC, Willson TM, Kelly CJ, Glass CK. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature. 1998;391:79–82
  56. Risner ME, Saunders AM, Altman JF, Ormandy GC, Craft S, Foley IM, et al. Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer's disease. Pharmacogenom. J. 2006;6:246–254
  57. Smith P, Dunne DW, Fallon PG. Defective in vivo induction of functional type 2 cytokine responses in aged mice. Eur. J. Immunol. 2001;31:1495–1502
  58. Strum JC, Shehee R, Virley D, Richardson J, Mattie M, Selley P, et al. Rosiglitazone induces mitochondrial biogenesis in mouse brain. J. Alzheimer's Dis. 2007;11:45–51
  59. Sundararajan S, Gamboa JL, Victor NA, Wanderi EW, Lust WD, Landreth GE. Peroxisome proliferator-activated receptor-gamma ligands reduce inflammation and infarction size in transient focal ischemia. Neuroscience. 2005;130:685–696
  60. Ujiie M, Dickstein DL, Carlow DA, Jefferies WA. Blood–brain barrier permeability precedes senile plaque formation in an Alzheimer disease model. Microcirculation. 2003;10:463–470
  61. Wada K, Nakajima A, Katayama K, Kudo C, Shibuya A, Kubota N, et al. Peroxisome proliferator-activated receptor gamma-mediated regulation of neural stem cell proliferation and differentiation. J. Biol. Chem. 2006;281:12673–12681
  62. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ, Anwyl R. Block of long-term potentiation by naturally secreted and synthetic amyloid beta-peptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase, cyclin-dependent kinase 5, and p38 mitogen-activated protein kinase as well as metabotropic glutamate receptor type 5. J. Neurosci. 2004;24:3370–3378
  63. Watson GS, Cholerton BA, Reger MA, Baker LD, Plymate SR, Asthana S, et al. Preserved cognition in patients with early Alzheimer's disease and amnestic mild cognitive impairment during treatment with rosiglitazone: a preliminary study. Am. J. Geriatr. Psychiatry. 2005;13:950–958
  64. Zhao Y, Patzer A, Herdegen T, Gohlke P, Culman J. Activation of cerebral peroxisome proliferator-activated receptors gamma promotes neuroprotection by attenuation of neuronal cyclooxygenase-2 overexpression after focal cerebral ischemia in rats. FASEB J. 2006;20:1162–1175

PII: S0197-4580(07)00371-5

doi: 10.1016/j.neurobiolaging.2007.09.001

Neurobiology of Aging
Volume 30, Issue 6 , Pages 920-931 , June 2009

Article Tools

* Image Usage & Resolution