Journal of Neuroimmunology
Volume 218, Issue 1 , Pages 36-47 , 25 January 2010

Peroxisome proliferator-activated receptor-γ agonists suppress iNOS expression induced by LPS in rat primary Schwann cells

  • Fupeng Zhang

      Affiliations

    • Department of Microbiology and Immunology, Medical College, Nantong 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • Both authors contributed equally to this work.
    • ,
  • Fen Liu

      Affiliations

    • Laboratory of Cellular and Molecular Tumor Immunology, Cyrus Tang Hematology Center, Medical College of Soochow University, Suzhou, 215123, China
    • Both authors contributed equally to this work.
    • ,
  • Meijuan Yan

      Affiliations

    • Jiangsu Province Key Laboratory of Neuroregeneration, Nantong University, 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • ,
  • Huoyan Ji

      Affiliations

    • Department of Microbiology and Immunology, Medical College, Nantong 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • ,
  • Ling Hu

      Affiliations

    • Department of Microbiology and Immunology, Medical College, Nantong 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • ,
  • Xiaohong Li

      Affiliations

    • Department of Microbiology and Immunology, Medical College, Nantong 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • ,
  • Ji Qian

      Affiliations

    • Department of Microbiology and Immunology, Medical College, Nantong 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • ,
  • Xingxin He

      Affiliations

    • Department of Microbiology and Immunology, Medical College, Nantong 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • ,
  • Li Zhang

      Affiliations

    • Department of Microbiology and Immunology, Medical College, Nantong 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • ,
  • Aiguo Shen

      Affiliations

    • Jiangsu Province Key Laboratory of Neuroregeneration, Nantong University, 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • Corresponding Author InformationCorresponding authors. Shen is to be contacted at Jiangsu Province Key Laboratory of Neuroregeneration, Nantong University, 19 Qixiu Road, Nantong, Jiangsu, China, 226001. Tel./fax: +86 513 85051999. Cheng, Department of Microbiology and Immunology, Medical College, Nantong University, 19 Qixiu Road, Nantong, Jiangsu, China, 226001. Tel./fax: +86 513 85051999.
    • ,
  • Chun Cheng

      Affiliations

    • Department of Microbiology and Immunology, Medical College, Nantong 19 Qixiu Road, Nantong, Jiangsu, 226001, China
    • Corresponding Author InformationCorresponding authors. Shen is to be contacted at Jiangsu Province Key Laboratory of Neuroregeneration, Nantong University, 19 Qixiu Road, Nantong, Jiangsu, China, 226001. Tel./fax: +86 513 85051999. Cheng, Department of Microbiology and Immunology, Medical College, Nantong University, 19 Qixiu Road, Nantong, Jiangsu, China, 226001. Tel./fax: +86 513 85051999.

Received 2 June 2009 ,Revised 6 October 2009 ,Accepted 22 October 2009.

References 

  1. Akahori T, Sho M, Hamada K, Suzaki Y, Kuzumoto Y, Nomi T, et al. Importance of peroxisome proliferator-activated receptor-gamma in hepatic ischemia/reperfusion injury in mice. J. Hepatol. 2007;47:784–792
  2. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124:783–801
  3. Anon, 1999. A unified nomenclature system for the nuclear receptor superfamily. Cell 97, 161–163.
  4. Aouadi M, Laurent K, Prot M, Le Marchand-Brustel Y, Binetruy B, Bost F. Inhibition of p38MAPK increases adipogenesis from embryonic to adult stages. Diabetes. 2006;55:281–289
  5. Armati PJ, Pollard JD. Immunology of the Schwann cell. Baillieres Clin. Neurol. 1996;5:47–64
  6. Bae JH, Jang BC, Suh SI, Ha E, Baik HH, Kim SS, et al. Manganese induces inducible nitric oxide synthase (iNOS) expression via activation of both MAP kinase and PI3K/Akt pathways in BV2 microglial cells. Neurosci. Lett. 2006;398:151–154
  7. Belvisi MG, Hele DJ. Peroxisome proliferator-activated receptors as novel targets in lung disease. Chest. 2008;134:152–157
  8. Berger J, Patel HV, Woods J, Hayes NS, Parent SA, Clemas J, et al. A PPARgamma mutant serves as a dominant negative inhibitor of PPAR signaling and is localized in the nucleus. Mol. Cell. Endocrinol. 2000;162:57–67
  9. Beutler B, Hoebe K, Du X, Ulevitch RJ. How we detect microbes and respond to them: the Toll-like receptors and their transducers. J Leukoc Biol. 2003;74:479–485
  10. Bhatheja K, Field J. Schwann cells: origins and role in axonal maintenance and regeneration. Int. J. Biochem. Cell Biol. 2006;38:1995–1999
  11. Brockes JP, Fields KL, Raff MC. Studies on cultured rat Schwann cells. I. Establishment of purified populations from cultures of peripheral nerve. Brain Res. 1979;165:105–118
  12. Burgermeister E, Seger R. MAPK kinases as nucleo-cytoplasmic shuttles for PPARgamma. Cell Cycle. 2007;6:1539–1548
  13. Burgermeister E, Chuderland D, Hanoch T, Meyer M, Liscovitch M, Seger R. Interaction with MEK causes nuclear export and downregulation of peroxisome proliferator-activated receptor gamma. Mol. Cell. Biol. 2007;27:803–817
  14. Cary SP, Winger JA, Derbyshire ER, Marletta MA. Nitric oxide signaling: no longer simply on or off. Trends Biochem. Sci. 2006;31:231–239
  15. Cheng C, Qin Y, Shao X, Wang H, Gao Y, Cheng M, et al. Induction of TNF-alpha by LPS in Schwann cell is regulated by MAPK activation signals. Cell. Mol. Neurobiol. 2007;27:909–921
  16. 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
  17. Constantin G, Piccio L, Bussini S, Pizzuti A, Scarpini E, Baron P, et al. Induction of adhesion molecules on human schwann cells by proinflammatory cytokines, an immunofluorescence study. J. Neurol. Sci. 1999;170:124–130
  18. Conti G, Rostami A, Scarpini E, Baron P, Galimberti D, Bresolin N, et al. Inducible nitric oxide synthase (iNOS) in immune-mediated demyelination and Wallerian degeneration of the rat peripheral nervous system. Exp. Neurol. 2004;187:350–358
  19. Czlonkowska A, Ciesielska A, Gromadzka G, Kurkowska-Jastrzebska I. Estrogen and cytokines production — the possible cause of gender differences in neurological diseases. Curr. Pharm. Des. 2005;11:1017–1030
  20. Da Silva J, Pierrat B, Mary JL, Lesslauer W. Blockade of p38 mitogen-activated protein kinase pathway inhibits inducible nitric-oxide synthase expression in mouse astrocytes. J. Biol. Chem. 1997;272:28373–28380
  21. Diradourian C, Girard J, Pegorier JP. Phosphorylation of PPARs: from molecular characterization to physiological relevance. Biochimie. 2005;87:33–38
  22. Escher P, Wahli W. Peroxisome proliferator-activated receptors: insight into multiple cellular functions. Mutat. Res. 2000;448:121–138
  23. Fahmi H, Di Battista JA, Pelletier JP, Mineau F, Ranger P, Martel-Pelletier J. Peroxisome proliferator-activated receptor gamma activators inhibit interleukin-1beta-induced nitric oxide and matrix metalloproteinase 13 production in human chondrocytes. Arthritis Rheum. 2001;44:595–607
  24. Feige JN, Gelman L, Michalik L, Desvergne B, Wahli W. From molecular action to physiological outputs: peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions. Prog. Lipid Res. 2006;45:120–159
  25. Gold R, Zielasek J, Kiefer R, Toyka KV, Hartung HP. Secretion of nitrite by Schwann cells and its effect on T-cell activation in vitro. Cell. Immunol. 1996;168:69–77
  26. Gurnell M. PPARgamma and metabolism: insights from the study of human genetic variants. Clin Endocrinol (Oxf). 2003;59:267–277
  27. Gurnell M, Wentworth JM, Agostini M, Adams M, Collingwood TN, Provenzano C, et al. A dominant-negative peroxisome proliferator-activated receptor gamma (PPARgamma) mutant is a constitutive repressor and inhibits PPARgamma-mediated adipogenesis. J. Biol. Chem. 2000;275:5754–5759
  28. 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
  29. Hoefen RJ, Berk BC. The role of MAP kinases in endothelial activation. Vascul. Pharmacol. 2002;38:271–273
  30. Houseknecht KL, Cole BM, Steele PJ. Peroxisome proliferator-activated receptor gamma (PPARgamma) and its ligands: a review. Domest. Anim. Endocrinol. 2002;22:1–23
  31. Ji Y, Liu J, Wang Z, Liu N, Gou W. PPARgamma agonist, rosiglitazone, regulates angiotensin II-induced vascular inflammation through the TLR4-dependent signaling pathway. Lab. Invest. 2009;89:887–902
  32. Jiang C, Ting AT, Seed B. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature. 1998;391:82–86
  33. Jiang Z, Georgel P, Du X, Shamel L, Sovath S, Mudd S, et al. CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 2005;6:565–570
  34. Kaisho T, Akira S. Pleiotropic function of Toll-like receptors. Microbes. Infect. 2004;6:1388–1394
  35. Kampa M, Castanas E. Membrane steroid receptor signaling in normal and neoplastic cells. Mol. Cell. Endocrinol. 2006;246:76–82
  36. Kielian T, McMahon M, Bearden ED, Baldwin AC, Drew PD, Esen N. S. aureus-dependent microglial activation is selectively attenuated by the cyclopentenone prostaglandin 15-deoxy-Delta12, 14-prostaglandin J2 (15d-PGJ2). J. Neurochem. 2004;90:1163–1172
  37. Kim SH, Kim J, Sharma RP. Inhibition of p38 and ERK MAP kinases blocks endotoxin-induced nitric oxide production and differentially modulates cytokine expression. Pharmacol. Res. 2004;49:433–439
  38. Kitamura Y, Shimohama S, Koike H, Kakimura J, Matsuoka Y, Nomura Y, et al. Increased expression of cyclooxygenases and peroxisome proliferator-activated receptor-gamma in Alzheimer's disease brains. Biochem. Biophys. Res. Commun. 1999;254:582–586
  39. Konukoglu D, Serin O, Turhan MS. Plasma leptin and its relationship with lipid peroxidation and nitric oxide in obese female patients with or without hypertension. Arch. Med. Res. 2006;37:602–606
  40. Levy D, Hoke A, Zochodne DW. Local expression of inducible nitric oxide synthase in an animal model of neuropathic pain. Neurosci. Lett. 1999;260:207–209
  41. Lisak RP, Skundric D, Bealmear B, Ragheb S. The role of cytokines in Schwann cell damage, protection, and repair. J. Infect. Dis. 1997;176(Suppl 2):S173–S179
  42. Luo G, Peng D, Zheng J, Chen X, Wu J, Elster E, et al. The role of NO in macrophage dysfunction at early stage after burn injury. Burns. 2005;31:138–144
  43. Maeda T, Kiguchi N, Kobayashi Y, Ozaki M, Kishioka S. Pioglitazone attenuates tactile allodynia and thermal hyperalgesia in mice subjected to peripheral nerve injury. J Pharmacol Sci. 2008;108:341–347
  44. Marriott HM, Ali F, Read RC, Mitchell TJ, Whyte MK, Dockrell DH. Nitric oxide levels regulate macrophage commitment to apoptosis or necrosis during pneumococcal infection. FASEB J. 2004;18:1126–1128
  45. Morrison SG, Morrison RP. A predominant role for antibody in acquired immunity to chlamydial genital tract reinfection. J. Immunol. 2005;175:7536–7542
  46. Nagai H, Kumamoto H, Fukuda M, Takahashi T. Inducible nitric oxide synthase and apoptosis-related factors in the synovial tissues of temporomandibular joints with internal derangement and osteoarthritis. J. Oral Maxillofac. Surg. 2003;61:801–807
  47. Nagareddy PR, Xia Z, MacLeod KM, McNeill JH. N-acetylcysteine prevents nitrosative stress-associated depression of blood pressure and heart rate in streptozotocin diabetic rats. J. Cardiovasc. Pharmacol. 2006;47:513–520
  48. Orlikowski D, Chazaud B, Plonquet A, Poron F, Sharshar T, Maison P, et al. Monocyte chemoattractant protein 1 and chemokine receptor CCR2 productions in Guillain–Barre syndrome and experimental autoimmune neuritis. J. Neuroimmunol. 2003;134:118–127
  49. Pacurari M, Yin XJ, Zhao J, Ding M, Leonard SS, Schwegler-Berry D, et al. Raw single-wall carbon nanotubes induce oxidative stress and activate MAPKs, AP-1, NF-kappaB, and Akt in normal and malignant human mesothelial cells. Environ. Health Perspect. 2008;116:1211–1217
  50. Pershadsingh HA, Heneka MT, Saini R, Amin NM, Broeske DJ, Feinstein DL. Effect of pioglitazone treatment in a patient with secondary multiple sclerosis. J. Neuroinflammation. 2004;1:3
  51. 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. USA. 1999;96:4668–4673
  52. Phulwani NK, Feinstein DL, Gavrilyuk V, Akar C, Kielian T. 15-deoxy-Delta12, 14-prostaglandin J2 (15d-PGJ2) and ciglitazone modulate Staphylococcus aureus-dependent astrocyte activation primarily through a PPAR-gamma-independent pathway. J. Neurochem. 2006;99:1389–1402
  53. Qin Y, Cheng C, Wang H, Shao X, Gao Y, Shen A. TNF-alpha as an autocrine mediator and its role in the activation of Schwann cells. Neurochem. Res. 2008;33:1077–1084
  54. 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
  55. Rochette-Egly C. Nuclear receptors: integration of multiple signalling pathways through phosphorylation. Cell. Signal. 2003;15:355–366
  56. Saraiva RM, Hare JM. Nitric oxide signaling in the cardiovascular system: implications for heart failure. Curr. Opin. Cardiol. 2006;21:221–228
  57. Shen A, Yang J, Gu Y, Zhou D, Sun L, Qin Y, et al. Lipopolysaccharide-evoked activation of p38 and JNK leads to an increase in ICAM-1 expression in Schwann cells of sciatic nerves. FEBS J. 2008;275:4343–4353
  58. Shibuya A, Wada K, Nakajima A, Saeki M, Katayama K, Mayumi T, et al. Nitration of PPARgamma inhibits ligand-dependent translocation into the nucleus in a macrophage-like cell line, RAW 264. FEBS Lett. 2002;525:43–47
  59. Storling J, Binzer J, Andersson AK, Zullig RA, Tonnesen M, Lehmann R, et al. Nitric oxide contributes to cytokine-induced apoptosis in pancreatic beta cells via potentiation of JNK activity and inhibition of Akt. Diabetologia. 2005;48:2039–2050
  60. Sung B, Park S, Yu BP, Chung HY. Modulation of PPAR in aging, inflammation, and calorie restriction. J. Gerontol. A Biol. Sci. Med. Sci. 2004;59:997–1006
  61. Tinker AC, Wallace AV. Selective inhibitors of inducible nitric oxide synthase: potential agents for the treatment of inflammatory diseases?. Curr. Top Med. Chem. 2006;6:77–92
  62. Tofaris GK, Patterson PH, Jessen KR, Mirsky R. Denervated Schwann cells attract macrophages by secretion of leukemia inhibitory factor (LIF) and monocyte chemoattractant protein-1 in a process regulated by interleukin-6 and LIF. J. Neurosci. 2002;22:6696–6703
  63. Tureyen K, Kapadia R, Bowen KK, Satriotomo I, Liang J, Feinstein DL, et al. Peroxisome proliferator-activated receptor-gamma agonists induce neuroprotection following transient focal ischemia in normotensive, normoglycemic as well as hypertensive and type-2 diabetic rodents. J. Neurochem. 2007;101:41–56
  64. Ulett GC, Adderson EE. Nitric oxide is a key determinant of group B streptococcus-induced murine macrophage apoptosis. J. Infect. Dis. 2005;191:1761–1770
  65. Vidal-Puig A, Jimenez-Linan M, Lowell BB, Hamann A, Hu E, Spiegelman B, et al. Regulation of PPAR gamma gene expression by nutrition and obesity in rodents. J. Clin. Invest. 1996;97:2553–2561
  66. Vougioukas VI, Roeske S, Bruck W. Involvement of intercellular adhesion molecule-1 in myelin recognition by macrophages. Acta Neuropathol. 2000;99:673–679
  67. Vunta H, Davis F, Palempalli UD, Bhat D, Arner RJ, Thompson JT, et al. The anti-inflammatory effects of selenium are mediated through 15-deoxy-Delta12, 14-prostaglandin J2 in macrophages. J. Biol. Chem. 2007;282:17964–17973
  68. Wang H, Cheng C, Qin Y, Niu S, Gao S, Li X, et al. Role of mitogen-activated protein kinase cascades in inducible nitric oxide synthase expression by lipopolysaccharide in a rat schwann cell line. Neurochem. Res. 2009;34:430–437
  69. Xu J, Drew PD. Peroxisome proliferator-activated receptor-gamma agonists suppress the production of IL-12 family cytokines by activated glia. J. Immunol. 2007;178:1904–1913
  70. Xu Z, Wang BR, Wang X, Kuang F, Duan XL, Jiao XY, et al. ERK1/2 and p38 mitogen-activated protein kinase mediate iNOS-induced spinal neuron degeneration after acute traumatic spinal cord injury. Life Sci. 2006;79:1895–1905
  71. Yamagishi S, Ogasawara S, Mizukami H, Yajima N, Wada R, Sugawara A, et al. Correction of protein kinase C activity and macrophage migration in peripheral nerve by pioglitazone, peroxisome proliferator activated-gamma-ligand, in insulin-deficient diabetic rats. J. Neurochem. 2008;104:491–499
  72. Zhao Y, Fei M, Wang Y, Lu M, Cheng C, Shen A. Expression of Foxo3a in non-Hodgkin's lymphomas is correlated with cell cycle inhibitor p27. Eur. J. Haematol. 2008;81:83–93

PII: S0165-5728(09)00431-7

doi: 10.1016/j.jneuroim.2009.10.016

Journal of Neuroimmunology
Volume 218, Issue 1 , Pages 36-47 , 25 January 2010

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