The oral antidiabetic pioglitazone protects from neurodegeneration and amyotrophic lateral sclerosis-like symptoms in superoxide dismutase-G93A transgenic mice

Journal of Neuroscience

Volumn 25, Issue 34, 2005, Pages 7805-7812

  Schütz, Burkhard ^a,d   Reimann, Jens ^a   Dumitrescu Ozimek, Lucia ^a   Kappes Horn, Karin ^a   Landreth, Gary E ^b   Schürmann, Britta ^a   Zimmer, Andreas ^a   Heneka, Michael T ^a,c  

^a UNIVERSITY OF BONN   (Germany)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Degeneration; Glia; Microglia; Motor neurons; Neuroinflammation; Peroxisome proliferator activated receptor

Indexed keywords

CYCLOOXYGENASE 2; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; ORAL ANTIDIABETIC AGENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MICROGLIA; MOTOR NEURON DISEASE; MUSCLE ATROPHY; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; SYMPTOMATOLOGY; TRANSGENIC MOUSE;

ADMINISTRATION, ORAL; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; HUMANS; HYPOGLYCEMIC AGENTS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; SUPEROXIDE DISMUTASE; THIAZOLIDINEDIONES;

EID: 23944490153     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2038-05.2005     Document Type: Article

References (50)

1. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, et al. (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421.
2. Almer G, Vukosavic S, Romero N, Przedborski S (1999) Inducible nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 72:2415-2425.
3. Almer G, Guegan C, Teismann P, Naini A, Rosoklija G, Hays AP, Chen C, Przedborski S (2001) Increased expression of the pro-inflammatory enzyme cyclooxygenase-2 in amyotrophic lateral sclerosis. Ann Neurol 49:176-185.
4. Azari MF, Profyris C, Le Grande MR, Lopes EC, Hirst J, Petratos S, Cheema SS (2005) Effects of intraperitoneal injection of Rofecoxib in a mouse model of ALS. Eur J Neurol 12:357-364.
5. Barbeito LH, Pehar M, Cassina P, Vargas MR, Peluffo H, Viera L, Estevez AG, Beckman JS (2004) A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res Brain Res Rev 47:263-274.
6. Berger J, Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53:409-435.
7. Blanquart C, Barbier O, Fruchart JC, Staels B, Glineur C (2003) Peroxisome proliferator-activated receptors: regulation of transcriptional activities and roles in inflammation. J Steroid Biochem Mol Biol 85:267-273.
8. Breidert T, Callebert J, Heneka MT, Landreth G, Launay JM, Hirsch EC (2002) Protective action of the peroxisome proliferator-activated receptor-gamma agonist pioglitazone in a mouse model of Parkinson's disease. J Neurochem 82:615-624.
9. Brooke MH, Engel WK (1969) The histographic analysis of human muscle biopsies with regard to fiber types. 2. Diseases of the upper and lower motor neuron. Neurology 19:378-393.
10. Combs CK, Johnson DE, Karlo JC, Cannady SB, Landreth GE (2000) Inflammatory mechanisms in Alzheimer's disease: inhibition of β-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARγ agonists. J Neurosci 20:558-567.
11. Daynes RA, Jones DC (2002) Emerging roles of PPARs in inflammation and immunity. Nat Rev Immunol 2:748-759.
12. Drachman DB, Frank K, Dykes-Hoberg M, Teismann P, Almer G, Przedborski S, Rothstein JD (2002) Cyclooxygenase 2 inhibition protects motor neurons and prolongs survival in a transgenic mouse model of ALS. Ann Neurol 52:771-778.
13. Feinstein DL (2003) Therapeutic potential of peroxisome proliferator-activated receptor agonists for neurological disease. Diabetes Technol Ther 5:67-73.
14. Feinstein DL, Galea E, Gavrilyuk V, Brosnan CF, Whitacre CC, Dumitrescu-Ozimek L, Landreth GE, Pershadsingh HA, Weinberg G, Heneka MT (2002) Peroxisome proliferator-activated receptor-gamma agonists prevent experimental autoimmune encephalomyelitis. Ann Neurol 51:694-702.
15. Grommes C, Landreth GE, Heneka MT (2004) Antineoplastic effects of peroxisome proliferator-activated receptor gamma agonists. Lancet Oncol 5:419-429.
16. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264:1772-1775.
17. Heiman-Patterson TD, Deitch JS, Blankenhorn E, Erwin K, Perreault MJ, Alexander B, Alexander GM (2003) Background and gender effects on survival in the SOD1 (G93A) transgenic mouse model of ALS. Amyotroph Lateral Scler Other Motor Neuron Disord 4 [Suppl 1]:118.
18. Heneka MT, Feinstein DL, Galea E, Gleichmann M, Wullner U, Klockgether T (1999) Peroxisome proliferator-activated receptor gamma agonists protect cerebellar granule cells from cytokine-induced apoptotic cell death by inhibition of inducible nitric oxide synthase. J Neuroimmunol 100:156-168.
19. Heneka MT, Klockgether T, Feinstein DL (2000) Peroxisome proliferator-activated receptor-γ ligands reduce neuronal inducible nitric oxide synthase expression and cell death in vivo. J Neurosci 20:6862-6867.
20. Hensley K, Floyd RA, Gordon B, Mou S, Pye QN, Stewart C, West M, Williamson K (2002) Temporal patterns of cytokine and apoptosis-related gene expression in spinal cords of the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. J Neurochem 82:365-374.
21. In t'Veld BA, Ruitenberg A, Hofman A, Launer LJ, van Duijn CM, Stijnen T, Breteler MM, Stricker BH (2001) Nonsteroidal antiinflammatory drugs and the risk of Alzheimer's disease. N Engl J Med 345:1515-1521.
22. Kunst CB (2004) Complex genetics of amyotrophic lateral sclerosis. Am J Hum Genet 75:933-947.
23. Landreth GE, Heneka MT (2001) Anti-inflammatory actions of peroxisome proliferator-activated receptor gamma agonists in Alzheimer's disease. Neurobiol Aging 22:937-944.
24. Lim GP, Yang F, Chu T, Chen P, Beech W, Teter B, Tran T, Ubeda O, Ashe KH, Frautschy SA, Cole GM (2000) Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J Neurosci 20:5709-5714.
25. Maeshiba Y, Kiyota Y, Yamashita K, Yoshimura Y, Motohashi M, Tanayama S (1997) Disposition of the new antidiabetic agent pioglitazone in rats, dogs, and monkeys. Arzneimittelforschung 47:29-35.
26. McGeer PL, McGeer EG (2002) Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 26:459-470.
27. Natarajan C, Muthian G, Barak Y, Evans RM, Bright JJ (2003) Peroxisome proliferator-activated receptor-gamma-deficient heterozygous mice develop an exacerbated neural antigen-induced Th1 response and experimental allergic encephalomyelitis. J Immunol 171:5743-5750.
28. Nathan C, Xie QW (1994) Regulation of biosynthesis of nitric oxide. J Biol Chem 269:13725-13728.
29. Niino M, Iwabuchi K, Kikuchi S, Ato M, Morohashi T, Ogata A, Tashiro K, Onoe K (2001) Amelioration of experimental autoimmune encephalomyelitis in C57BL/6 mice by an agonist of peroxisome proliferator-activated receptor-gamma. J Neuroimmunol 116:40-48.
30. Nogawa S, Forster C, Zhang F, Nagayama M, Ross ME, Iadecola C (1998) Interaction between inducible nitric oxide synthase and cyclooxygenase-2 after cerebral ischemia. Proc Natl Acad Sci USA 95:10966-10971.
31. O'Banion MK (1999) Cyclooxygenase-2: molecular biology, pharmacology, and neurobiology. Crit Rev Neurobiol 13:45-82.
32. Park EJ, Park SY, Joe EH, Jou I (2003) 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 278:14747-14752.
33. Patsouris D, Muller M, Kersten S (2004) Peroxisome proliferator activated receptor ligands for the treatment of insulin resistance. Curr Opin Investig Drugs 5:1045-1050.
34. Phul RK, Shaw PJ, Ince PG, Smith ME (2000) Expression of nitric oxide synthase isoforms in spinal cord in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:259-267.
35. Pompl PN, Ho L, Bianchi M, McManus T, Qin W, Pasinetti GM (2003) A therapeutic role for cyclooxygenase-2 inhibitors in a transgenic mouse model of amyotrophic lateral sclerosis. FASEB J 17:725-727.
36. Sasaki S, Warita H, Abe K, Iwata M (2001) Inducible nitric oxide synthase (iNOS) and nitrotyrosine immunoreactivity in the spinal cords of transgenic mice with a G93A mutant SOD1 gene. J Neuropathol Exp Neurol 60:839-846.
37. Schutz B, Mauer D, Salmon AM, Changeux JP, Zimmer A (2004) Analysis of the cellular expression pattern of beta-CGRP in alpha-CGRP-deficient mice. J Comp Neurol 476:32-43.
38. Shimazu T, Inoue I, Araki N, Asano Y, Sawada M, Furuya D, Nagoya H, Greenberg JH (2005) A peroxisome proliferator-activated receptor-gamma agonist reduces infarct size in transient but not in permanent ischemia. Stroke 36:353-359.
39. Shiomi T, Tsutsui H, Hayashidani S, Suematsu N, Ikeuchi M, Wen J, Ishibashi M, Kubota T, Egashira K, Takeshita A (2002) Pioglitazone, a peroxisome proliferator-activated receptor-gamma agonist, attenuates left ventricular remodeling and failure after experimental myocardial infarction. Circulation 106:3126-3132.
40. Shouda T, Yoshida T, Hanada T, Wakioka T, Oishi M, Miyoshi K, Komiya S, Kosai K, Hanakawa Y, Hashimoto K, Nagata K, Yoshimura A (2001) Induction of the cytokine signal regulator SOCS3/CIS3 as a therapeutic strategy for treating inflammatory arthritis. J Clin Invest 108:1781-1788.
41. Sundararajan S, Gamboa JL, Victor NA, Wanderi EW, Lust WD, Landreth GE (2005) Peroxisome proliferator-activated receptor-gamma ligands reduce inflammation and infarction size in transient focal ischemia. Neuroscience 130:685-696.
42. Suzuki A, Hanada T, Mitsuyama K, Yoshida T, Kamizono S, Hoshino T, Kubo M, Yamashita A, Okabe M, Takeda K, Akira S, Matsumoto S, Toyonaga A, Sata M, Yoshimura A (2001) CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J Exp Med 193:471-481.
43. Talbot K (2002) Motor neurone disease. Postgrad Med J 78:513-519.
44. Watson GS, Craft S (2003) The role of insulin resistance in the pathogenesis of Alzheimer's disease: implications for treatment. CNS Drugs 17:27-45.
45. Weydt P, Weiss MD, Moller T, Carter GT (2002) Neuro-inflammation as a therapeutic target in amyotrophic lateral sclerosis. Curr Opin Investig Drugs 3:1720-1724.
46. Weydt P, Hong SY, Kliot M, Moller T (2003) Assessing disease onset and progression in the SOD1 mouse model of ALS. NeuroReport 14:1051-1054.
47. Xie W, Merrill JR, Bradshaw WS, Simmons DL (1993) Structural determination and promoter analysis of the chicken mitogen-inducible prostaglandin G/H synthase gene and genetic mapping of the murine homolog. Arch Biochem Biophys 300:247-252.
48. Yasojima K, Tourtellotte WW, McGeer EG, McGeer PL (2001) Marked increase in cyclooxygenase-2 in ALS spinal cord: implications for therapy. Neurology 57:952-956.
49. Yki-Jarvinen H (2004) Thiazolidinediones. N Engl J Med 351:1106-1118.
50. Yoshihara T, Ishigaki S, Yamamoto M, Liang Y, Niwa J, Takeuchi H, Doyu M, Sobue G (2002) Differential expression of inflammation- and apoptosis-related genes in spinal cords of a mutant SOD1 transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 80:158-167.