IL-13 downregulates PPAR-γ/heme oxygenase-1 via ER stress-stimulated calpain activation: Aggravation of activated microglia death

Cellular and Molecular Life Sciences

Volumn 67, Issue 9, 2010, Pages 1465-1476

  Liu, Shing Hwa ^a   Yang, Cheng Ning ^b   Pan, Hung Chuan ^c,d   Sung, Yen Jen ^b   Liao, Ko Kaung ^e   Chen, Wen Bao ^d   Lin, Wen Zheng ^d   Sheu, Meei Ling ^c,d  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^d NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^e CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Calpain; Heme oxygenase 1; Interleukin 13; Microglia; PPAR

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CALPAIN 2; CALPASTATIN; CASPASE 12; DNA; HEME OXYGENASE 1; INTERLEUKIN 13; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA ANTAGONIST; RECOMBINANT ENZYME; SMALL INTERFERING RNA; CALPAIN; ISOENZYME; LIPOPOLYSACCHARIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; MICROGLIA; NERVE CELL NECROSIS; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; ANIMAL; CELL CULTURE; CELL DEATH; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENDOPLASMIC RETICULUM; GENETICS; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CALPAIN; CELL DEATH; CELLS, CULTURED; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; HEME OXYGENASE-1; INTERLEUKIN-13; ISOENZYMES; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; PPAR GAMMA; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; STRESS, PHYSIOLOGICAL;

EID: 77952299922     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-009-0255-4     Document Type: Article

References (53)

1. ML Block JS Hong 2005 Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism Prog Neurobiol 76 77 98 10.1016/j.pneurobio.2005.06.004 1:CAS:528:DC%2BD2MXpvFemu7o%3D 16081203 (Pubitemid 41242883)
2. ST Dheen C Kaur EA Ling 2007 Microglial activation and its implications in the brain diseases Curr Med Chem 14 1189 1197 10.2174/092986707780597961 1:CAS:528:DC%2BD2sXltFejsro%3D 17504139 (Pubitemid 46739320)
3. L Minghetti MA Ajmone-Cat MA De Berardinis SR De 2005 Microglial activation in chronic neurodegenerative diseases: roles of apoptotic neurons and chronic stimulation Brain Res Rev 48 251 256 10.1016/j.brainresrev.2004.12.015 1:CAS:528:DC%2BD2MXjs1Cmu74%3D 15850664 (Pubitemid 40585756)
4. NP Whitney TM Eidem H Peng Y Huang JC Zheng 2009 Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders J Neurochem 108 1343 1359 10.1111/j.1471-4159. 2009.05886.x 1:CAS:528:DC%2BD1MXjsFWgs7k%3D 19154336
5. WH Shin DY Lee KW Park SU Kim MS Yang EH Joe BK Jin 2004 Microglia expressing interleukin-13 undergo cell death and contribute to neuronal survival in vivo Glia 46 142 152 10.1002/glia.10357 15042582 (Pubitemid 38596180)
6. MS Yang KA Ji SB Jeon BK Jin SU Kim I Jou E Joe 2006 Interleukin-13 enhances cyclooxygenase-2 expression in activated rat brain microglia: implications for death of activated microglia J Immunol 177 1323 1329 1:CAS:528:DC%2BD28XmsVaku7o%3D 16818793
7. L Zhao SL Ackerman 2006 Endoplasmic reticulum stress in health and disease Curr Opin Cell Biol 18 444 452 10.1016/j.ceb.2006.06.005 1:CAS:528:DC%2BD28Xmslyqt7k%3D 16781856 (Pubitemid 44026518)
8. H Yoshida 2007 ER stress and diseases FEBS J 274 630 658 10.1111/j.1742-4658.2007.05639.x 1:CAS:528:DC%2BD2sXitVOhtLo%3D 17288551 (Pubitemid 46150855)
9. D Lindholm H Wootz L Korhonen 2006 ER stress and neurodegenerative diseases Cell Death Differ 13 385 392 10.1038/sj.cdd.4401778 1:CAS:528:DC%2BD28Xhtl2mt7o%3D 16397584
10. C Culmsee S Landshamer 2006 Molecular insights into mechanisms of the cell death program: role in the progression of neurodegenerative disorders Curr Alzheimer Res 3 269 283 10.2174/156720506778249461 1:CAS:528: DC%2BD28Xos1Kjsro%3D 17017859 (Pubitemid 44351472)
11. S Kyuhou N Kato H Gemba 2006 Emergence of endoplasmic reticulum stress and activated microglia in Purkinje cell degeneration mice Neurosci Lett 396 91 96 10.1016/j.neulet.2005.11.023 1:CAS:528:DC%2BD28XhvVWkur4%3D 16356646 (Pubitemid 43276419)
12. GM Murphy Jr L Yang B Cordell 1998 Macrophage colony-stimulating factor augments beta-amyloid-induced interleukin-1, interleukin-6, and nitric oxide production by microglial cells J Biol Chem 273 20967 20971 10.1074/jbc.273.33. 20967 1:CAS:528:DyaK1cXlsFOrs7w%3D 9694846 (Pubitemid 28385379)
13. WR Markesbery 1997 Oxidative stress hypothesis in Alzheimer's disease Free Radic Biol Med 23 134 147 10.1016/S0891-5849(96)00629-6 1:CAS:528:DyaK2sXjtlaqs7o%3D 9165306 (Pubitemid 27217017)
14. HM Schipper 2000 Heme oxygenase-1: role in brain aging and neurodegeneration Exp Gerontol 35 821 830 10.1016/S0531-5565(00)00148-0 1:CAS:528:DC%2BD3cXot1Wqtrk%3D 11053673
15. A Takeda Y Itoyama T Kimpara X Zhu J Avila BE Dwyer G Perry MA Smith 2004 Heme catabolism and heme oxygenase in neurodegenerative disease Antioxid Redox Signal 6 888 894 1:CAS:528:DC%2BD2cXntFCgsL4%3D 15345149
16. HM Schipper 2004 Heme oxygenase expression in human central nervous system disorders Free Radic Biol Med 37 1995 2011 10.1016/j.freeradbiomed.2004. 09.015 1:CAS:528:DC%2BD2cXpslyju7c%3D 15544918 (Pubitemid 39491319)
17. Y Lin HJ Vreman RJ Wong T Tjoa T Yamauchi LJ Noble-Haeusslein 2007 Heme oxygenase-1 stabilizes the blood-spinal cord barrier and limits oxidative stress and white matter damage in the acutely injured murine spinal cord J Cereb Blood Flow Metab 27 1010 1021 1:CAS:528:DC%2BD2sXlvVSkt70%3D 17047682
18. NG Innamorato AI Rojo AJ Garcia-Yague M Yamamoto ML de Ceballos A Cuadrado 2008 The transcription factor Nrf2 is a therapeutic target against brain inflammation J Immunol 181 680 689 1:CAS:528:DC%2BD1cXnsVGitL0%3D 18566435
19. T Kielian MM Syed S Liu NK Phulwani N Phillips G Wagoner PD Drew N Esen 2008 The synthetic peroxisome proliferator-activated receptor-gamma agonist ciglitazone attenuates neuroinflammation and accelerates encapsulation in bacterial brain abscesses J Immunol 180 5004 5016 1:CAS:528:DC%2BD1cXjsVKqtb4%3D 18354226
20. SR Lee HY Kim JS Hong WK Baek JW Park 2009 PPARgamma agonist pioglitazone reduces matrix metalloproteinase-9 activity and neuronal damage after focal cerebral ischemia Biochem Biophys Res Commun 380 17 21 10.1016/j.bbrc.2008.12. 181 1:CAS:528:DC%2BD1MXitVygsr4%3D 19135426
21. M Sobrado MP Pereira I Ballesteros O Hurtado D Fernandez-Lopez JM Pradillo JR Caso J Vivancos F Nombela J Serena I Lizasoain MA Moro 2009 Synthesis of lipoxin A4 by 5-lipoxygenase mediates PPARgamma-dependent, neuroprotective effects of rosiglitazone in experimental stroke J Neurosci 29 3875 3884 10.1523/JNEUROSCI.5529-08.2009 1:CAS:528:DC%2BD1MXktVSqtbo%3D 19321784
22. G Kronke A Kadl E Ikonomu S Bluml A Furnkranz IJ Sarembock VN Bochkov M Exner BR Binder N Leitinger 2007 Expression of heme oxygenase-1 in human vascular cells is regulated by peroxisome proliferator-activated receptors Arterioscler Thromb Vasc Biol 27 1276 1282 10.1161/ATVBAHA.107.142638 17413033 (Pubitemid 46809415)
23. MS Yang EJ Park S Sohn HJ Kwon WH Shin HK Pyo B Jin KS Choi I Jou EH Joe 2002 Interleukin-13 and-4 induce death of activated microglia Glia 38 273 280 10.1002/glia.10057 12007140
24. ML Sheu FM Ho KF Chao ML Kuo SH Liu 2004 Activation of phosphoinositide 3-kinase in response to high glucose leads to regulation of reactive oxygen species-related nuclear factor-kappaB activation and cyclooxygenase-2 expression in mesangial cells Mol Pharmacol 66 187 196 10.1124/mol.66.1.187 1:CAS:528:DC%2BD2cXlsVOisr4%3D 15213311 (Pubitemid 38822102)
25. ML Sheu FM Ho RS Yang KF Chao WW Lin SY Lin-Shiau SH Liu 2005 High glucose induces human endothelial cell apoptosis through a phosphoinositide 3-kinase-regulated cyclooxygenase-2 pathway Arterioscler Thromb Vasc Biol 25 539 545 10.1161/01.ATV.0000155462.24263.e4 1:CAS:528:DC%2BD2MXhtl2ku7w%3D 15653566 (Pubitemid 40315675)
26. ML Sheu SH Liu KH Lan 2007 Honokiol induces calpain-mediated glucose-regulated protein-94 cleavage and apoptosis in human gastric cancer cells and reduces tumor growth PLoS One 2 e1096 10.1371/journal.pone.0001096 17971859 (Pubitemid 351586224)
27. T Nakagawa H Zhu N Morishima E Li J Xu BA Yankner J Yuan 2000 Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta Nature 403 98 103 10.1038/47513 1:CAS:528:DC%2BD3cXlvVSqsg%3D%3D 10638761 (Pubitemid 30038529)
28. T Nakagawa J Yuan 2000 Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis J Cell Biol 150 887 894 10.1083/jcb.150.4.887 1:CAS:528:DC%2BD3cXmtVelsrs%3D 10953012 (Pubitemid 30663424)
29. R Siman DG Flood G Thinakaran RW Neumar 2001 Endoplasmic reticulum stress-induced cysteine protease activation in cortical neurons: effect of an Alzheimer's disease-linked presenilin-1 knock-in mutation J Biol Chem 276 44736 44743 10.1074/jbc.M104092200 1:CAS:528:DC%2BD3MXovFegtLg%3D 11574534
30. JD Malhotra RJ Kaufman 2007 Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9 2277 2293 10.1089/ars.2007.1782 1:CAS:528:DC%2BD2sXht1GrsLzL 17979528 (Pubitemid 350059010)
31. T Uehara 2007 Accumulation of misfolded protein through nitrosative stress linked to neurodegenerative disorders Antioxid Redox Signal 9 597 601 10.1089/ars.2006.1517 1:CAS:528:DC%2BD2sXktFCit7o%3D 17465882 (Pubitemid 46598257)
32. I Kim W Xu JC Reed 2008 Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities Nat Rev Drug Discov 7 1013 1030 10.1038/nrd2755 1:CAS:528:DC%2BD1cXhsVenu7%2FM 19043451
33. AM Szczepanik S Funes W Petko GE Ringheim 2001 IL-4, IL-10 and IL-13 modulate A beta(1-42)-induced cytokine and chemokine production in primary murine microglia and a human monocyte cell line J Neuroimmunol 113 49 62 10.1016/S0165-5728(00)00404-5 1:CAS:528:DC%2BD3MXhsVSrtr0%3D 11137576 (Pubitemid 32008670)
34. AE Kelly-Welch EM Hanson MR Boothby AD Keegan 2003 Interleukin-4 and interleukin-13 signaling connections maps Science 300 1527 1528 10.1126/science.1085458 1:CAS:528:DC%2BD3sXktlKru7o%3D 12791978 (Pubitemid 36686713)
35. SL LaPorte ZS Juo J Vaclavikova LA Colf X Qi NM Heller AD Keegan KC Garcia 2008 Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system Cell 132 259 272 10.1016/j.cell.2007.12.030 1:CAS:528:DC%2BD1cXhvVSrtbo%3D 18243101 (Pubitemid 351172435)
36. GS Habicht LI Katona JL Benach 1991 Cytokines and the pathogenesis of neuroborreliosis: borrelia burgdorferi induces glioma cells to secrete interleukin-6 J Infect Dis 164 568 574 1:CAS:528:DyaK3MXmslOltr8%3D 1908002
37. MG Netea BJ Kullberg LA Joosten T Sprong I Verschueren OC Boerman F Amiot WB van den Berg JW Van der Meer 2001 Lethal Escherichia coli and Salmonella typhimurium endotoxemia is mediated through different pathways Eur J Immunol 31 2529 2538 10.1002/1521-4141(200109)31:9<2529::AID-IMMU2529>3.0.CO;2-B 1:CAS:528:DC%2BD3MXntFSqu78%3D 11536150 (Pubitemid 32898719)
38. H Nakanishi 2003 Microglial functions and proteases Mol Neurobiol 27 163 176 10.1385/MN:27:2:163 1:CAS:528:DC%2BD3sXltFams74%3D 12777686 (Pubitemid 36724519)
39. SK Ray NL Banik 2003 Calpain and its involvement in the pathophysiology of CNS injuries and diseases: therapeutic potential of calpain inhibitors for prevention of neurodegeneration Curr Drug Targets CNS Neurol Disord 2 173 189 10.2174/1568007033482887 1:CAS:528:DC%2BD3sXks1GmsL0%3D 12769798
40. P Glynn 2000 Neural development and neurodegeneration: two faces of neuropathy target esterase Prog Neurobiol 61 61 74 10.1016/S0301-0082(99)00043-X 1:CAS:528:DC%2BD3cXisValurY%3D 10759065 (Pubitemid 30100403)
41. SJ Crocker PD Smith V Jackson-Lewis WR Lamba SP Hayley E Grimm SM Callaghan RS Slack E Melloni S Przedborski GS Robertson H Anisman Z Merali DS Park 2003 Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of Parkinson's disease J Neurosci 23 4081 4091 1:CAS:528:DC%2BD3sXktFKgurw%3D 12764095
42. SJ Franco MA Rodgers BJ Perrin J Han DA Bennin DR Critchley A Huttenlocher 2004 Calpain-mediated proteolysis of talin regulates adhesion dynamics Nat Cell Biol 6 977 983 10.1038/ncb1175 1:CAS:528:DC%2BD2cXnvFGqs7Y%3D 15448700 (Pubitemid 39359850)
43. Y Tan N Dourdin C Wu TD Veyra JS Elce PA Greer 2006 Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress-induced apoptosis J Biol Chem 281 16016 16024 10.1074/jbc.M601299200 1:CAS:528:DC%2BD28Xlt1CkurY%3D 16597616 (Pubitemid 43848495)
44. PJ Syapin 2008 Regulation of haeme oxygenase-1 for treatment of neuroinflammation and brain disorders Br J Pharmacol 155 623 640 10.1038/bjp.2008.342 1:CAS:528:DC%2BD1cXht12lsrjI 18794892
45. J Wang S Dore 2007 Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage Brain 130 1643 1652 10.1093/brain/awm095 17525142 (Pubitemid 47355932)
46. XM Liu KJ Peyton D Ensenat H Wang AI Schafer J Alam W Durante 2005 Endoplasmic reticulum stress stimulates heme oxygenase-1 gene expression in vascular smooth muscle. Role in cell survival J Biol Chem 280 872 877 10.1074/jbc.M410413200 1:CAS:528:DC%2BD2MXitFGjtQ%3D%3D 15546873
47. GH Lee HK Kim SW Chae DS Kim KC Ha M Cuddy C Kress JC Reed HR Kim HJ Chae 2007 Bax inhibitor-1 regulates endoplasmic reticulum stress-associated reactive oxygen species and heme oxygenase-1 expression J Biol Chem 282 21618 21628 10.1074/jbc.M700053200 1:CAS:528:DC%2BD2sXotVGmtr8%3D 17526500 (Pubitemid 47195775)
48. AO Rosa J Egea A Martinez AG Garcia MG Lopez 2008 Neuroprotective effect of the new thiadiazolidinone NP00111 against oxygen-glucose deprivation in rat hippocampal slices: implication of ERK1/2 and PPARgamma receptors Exp Neurol 212 93 99 10.1016/j.expneurol.2008.03.008 1:CAS:528:DC%2BD1cXnt1OmtrY%3D 18471812
49. A Contestabile 2009 Benefits of caloric restriction on brain aging and related pathological states: understanding mechanisms to devise novel therapies Curr Med Chem 16 350 361 10.2174/092986709787002637 1:CAS:528: DC%2BD1MXjsFGqs7Y%3D 19149582
50. R Kapadia JH Yi R Vemuganti 2008 Mechanisms of anti-inflammatory and neuroprotective actions of PPAR-gamma agonists Front Biosci 13 1813 1826 10.2741/2802 1:CAS:528:DC%2BD1cXhs1Cgtr8%3D 17981670 (Pubitemid 351599735)
51. N Schintu L Frau M Ibba P Caboni A Garau E Carboni AR Carta 2009 PPAR-γ-mediated neuroprotection in a chronic mouse model of Parkinson's disease Eur J Neurosci 29 954 963 10.1111/j.1460-9568.2009.06657.x 19245367
52. X Yu XG Shao H Sun YN Li J Yang YC Deng YG Huang 2008 Activation of cerebral peroxisome proliferator-activated receptors gamma exerts neuroprotection by inhibiting oxidative stress following pilocarpine-induced status epilepticus Brain Res 1200 146 158 10.1016/j.brainres.2008.01.047 1:CAS:528:DC%2BD1cXjtlWktr8%3D 18289512
53. TN Lin WM Cheung JS Wu JJ Chen H Lin JJ Chen JY Liou SK Shyue KK Wu 2006 15d-Prostaglandin J2 protects brain from ischemia-reperfusion injury Arterioscler Thromb Vasc Biol 26 481 487 10.1161/01.ATV.0000201933.53964.5b 1:CAS:528:DC%2BD28XisFarsr8%3D 16385084