Eicosanoid receptor subtype-mediated opposing regulation of TLR-stimulated expression of astrocyte glial-derived neurotrophic factor

FASEB Journal

Volumn 26, Issue 7, 2012, Pages 3075-3083

  Li, Xianwu ^a   Cudaback, Eiron ^a   Breyer, Richard M ^b   Montine, Kathleen S ^a   Keene, C Dirk ^a   Montine, Thomas J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

EP1; FP; Parkinson's disease; PGE2; TP

Indexed keywords

CYCLOOXYGENASE 2; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; IBUPROFEN; ICOSANOID; MITOGEN ACTIVATED PROTEIN KINASE KINASE; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; PROSTAGLANDIN E RECEPTOR; RECEPTOR; RECEPTOR SUBTYPE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ASSAY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; HYPOTHESIS; INNATE IMMUNITY; MOUSE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; REGULATORY MECHANISM; WILD TYPE;

ANIMALS; ASTROCYTES; BASE SEQUENCE; CELLS, CULTURED; DNA PRIMERS; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; IMMUNITY, INNATE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; RECEPTORS, EICOSANOID; RECEPTORS, PROSTAGLANDIN E, EP1 SUBTYPE; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 9; TOLL-LIKE RECEPTORS;

MURINAE; MUS;

EID: 84863219648     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-200279     Document Type: Article

References (60)

1. Beraud, D., Twomey, M., Bloom, B., Mittereder, A., Ton, V., Neitzke, K., Chasovskikh, S., Mhyre, T. R. Mhyre, and Maguire-Zeiss, K. A. (2011) α-Synuclein alters Toll-like receptor expression. Front. Neurosci. 5, 80
2. Bsibsi, M., Bajramovic, J. J., Vogt, M. H., van Duijvenvoorden, E., Baghat, A., Persoon-Deen, C., Tielen, F., Verbeek, R., Huitinga, I., Ryffel, B., Kros, A., Gerritsen, W.H., Amor, S., and van Noort, J. M. (2010) The microtubule regulator stathmin is an endogenous protein agonist for TLR3. J. Immunol. 184, 6929-6937
3. Shiose, S., Chen, Y., Okano, K., Roy, S., Kohno, H., Tang, J., Pearlman, E., Maeda, T., Palczewski, K., and Maeda, A. (2011) Toll-like receptor 3 is required for development of retinopathy caused by impaired all-trans-retinal clearance in mice. J. Biol. Chem. 286, 15543-15555
4. Lim, J. E., Kou, J., Song, M., Pattanayak, A., Jin, J., Lalonde, R., and Fukuchi, K. (2011) MyD88 deficiency ameliorates β-amyloidosis in an animal model of Alzheimer's disease. Am. J. Pathol. 179, 1095-1103
5. Roodveldt, C., Labrador-Garrido, A., Gonzalez-Rey, E., Fernandez-Montesinos, R., Caro, M., Lachaud C. C., Waudby, C.A., Delgado, M., Dobson, C.M., and Pozo, D. (2010) Glial innate immunity generated by non-aggregated alpha-synuclein in mouse: differences between wild-type and Parkinson's disease-linked mutants. PLoS One 5, e13481
6. Stefanova, N., Fellner, L., Reindl, M., Masliah, E., Poewe, W., and Wenning, G. K. (2011) Toll-like receptor 4 promotes α-synuclein clearance and survival of nigral dopaminergic neurons. Am. J. Pathol. 179, 954-963
7. Stone, D. K., Reynolds, A. D., Mosley, R. L., and Gendelman, H. E. (2009) Innate and adaptive immunity for the pathobiology of Parkinson's disease. Antioxid. Redox Signal. 11, 2151-2166
8. Ros-Bernal, F., Hunot, S., Herrero, M. T., Parnadeau, S., Corvol, J. C., Lu, L., Alvarez-Fischer, D., Carrillo-de Sauvage, M.A., Saurini, F., Coussieu, C., Kinagawa, K., Prigent, A., Höglinger, G., Hamon, M., Tronche, F., Hirsch, E. C., and Vyas, S. (2011) Microglial glucocorticoid receptors play a pivotal role in regulating dopaminergic neurodegeneration in parkinsonism. Proc. Natl. Acad. Sci. U. S. A. 108, 6632-6637
9. Fuxe, K. G., Tarakanov, A. O., Goncharova, L. B., and Agnati, L. F. (2008) A new road to neuroinflammation in Parkinson's disease? Brain Res. Rev. 58, 453-458
10. Shie, F. S., Montine, K. S., Breyer, R. M., and Montine, T. J. (2005) Microglial EP2 is critical to neurotoxicity from activated cerebral innate immunity. Glia 52, 70-77 (Pubitemid 41532139)
11. Bsibsi, M., Persoon-Deen, C., Verwer, R. W., Meeuwsen, S., Ravid, R., and van Noort, J. M. (2006) Toll-like receptor 3 on adult human astrocytes triggers production of neuroprotective mediators. Glia 53, 688-695
12. Tanaka, T., Oh-Hashi, K., Shitara, H., Hirata, Y., and Kiuchi, K. (2008) NF-κB independent signaling pathway is responsible for LPS-induced GDNF gene expression in primary rat glial cultures. Neurosci. Lett. 431, 262-267
13. Li, X. Z., Bai, L. M., Yang, Y. P., Luo, W. F., Hu, W. D., Chen, J., Mao, C., and Liu, C. (2009) Effects of IL-6 secreted from astrocytes on the survival of dopaminergic neurons in lipopolysaccharide-induced inflammation. Neurosci. Res. 65, 252-258
14. Verity, A. N., Wyatt, T. L., Lee, W., Hajos, B., Baecker, P. A., Eglen, R. M., and Johnson, R. M. (1999) Differential regulation of glial cell line-derived neurotrophic factor (GDNF) expression in human neuroblastoma and glioblastoma cell lines. J. Neurosci. Res. 55, 187-197 (Pubitemid 29056959)
15. Verity, A. N., Wyatt, T. L., Hajos, B., Eglen, R. M., Baecker, P. A., and Johnson, R. M. (1998) Regulation of glial cell line-derived neurotrophic factor release from rat C6 glioblastoma cells. J. Neurochem. 70, 531-539 (Pubitemid 28079342)
16. Lin, L. F., Doherty, D. H., Lile, J. D., Bektesh, S., and Collins, F. (1993) GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260, 1130-1132 (Pubitemid 23186789)
17. Granholm, A. C., Reyland, M., Albeck, D., Sanders, L., Gerhardt, G., Hoernig, G. Shen, L., Westphal, H., and Hoffer, B. (2000) Glial cell line-derived neurotrophic factor is essential for postnatal survival of midbrain dopamine neurons. J. Neurosci. 20, 3182-3190 (Pubitemid 30263135)
18. Pascual, A., Hidalgo-Figueroa, M., Piruat, J. I., Pintado, C. O., Gómez-Diaz, R., and López-Barneo, J. (2008) Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat. Neurosci. 11, 755-761 (Pubitemid 351896676)
19. Kearns, C. M., and Gash, D. M. (1995) GDNF protects nigral dopamine neurons against 6-hydroxydopamine in vivo. Brain Res. 672, 104-111
20. Kordower, J. H., Emborg, M. E., Bloch, J., Ma, S. Y., Chu, Y., Leventhal, L., McBride, J., Chen, E. Y., Palfi, S., Roitberg, B. Z., Brown, W. D., Holden, J. E., Pyzalski, R., Taylor, M. D., Carvey, P., Ling, Z., Trono, D., Hantraye, P., Déglon, N., and Aebischer, P. (2000) Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson's disease. Science 290, 767-773
21. Grondin, R., Cass, W. A., Zhang, Z., Stanford, J. A., Gash, D. M., and Gerhardt, G. A. (2003) Glial cell line-derived neurotrophic factor increases stimulus-evoked dopamine release and motor speed in aged rhesus monkeys. J. Neurosci. 23, 1974-1980 (Pubitemid 36314753)
22. Maswood, N., Grondin, R., Zhang, Z., Stanford, J. A., Surgener, S. P., Gash, D. A., and Gerhardt, G. A. (2002) Effects of chronic intraputamenal infusion of glial cell line-derived neurotrophic factor (GDNF) in aged rhesus monkeys. Neurobiol. Aging 23, 881-889 (Pubitemid 35217713)
23. Tomac, A., Lindqvist, E., Lin, L. F., Ogren, S. O., Young, D., Hopper, B. J., and Olson, L. (1995) Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 373, 335-339
24. Nutt, J. G., Burchiel, K. J., Comella, C. L., Jankovic, J., Lang, A. E., Laws, E. R., Jr., Lozano, A. M., Penn, R. D., Simpson, R. K., Jr., Stacy, M., Wooten, G.F., and ICV GDNF Study Group. (2003) Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 60, 69-73 (Pubitemid 36070646)
25. Lang, A. E., Gill, S., Patel, N. K., Lozano, A., Nutt, J. G., Penn, R., Brooks, D. J., Hotton, G., Moro, E., Heywood, P., Brodsky, M. A., Burchiel, K., Kelly, P., Dalvi, A., Scott, B., Stacy, M., Turner, D., Wooten, V. G., Elias, W. J., Laws, E. R., Dhawan, V., Stoessl, A. J., Matcham. J., Coffey, R. J., and Traub, M. (2006) Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Ann. Neurol. 59, 459-466 (Pubitemid 43358066)
26. Slevin, J. T., Gash, D. M., Smith, C. D., Gerhardt, G. A., Kryscio, R., Chebrolu, H., Walton, A., Wagner, R., and Young, A. B. (2007) Unilateral intraputamenal glial cell line-derived neurotrophic factor in patients with Parkinson disease: response to 1 year of treatment and 1 year of withdrawal. J. Neurosurg. 106, 614-620 (Pubitemid 46536457)
27. Gill, S. S., Patel, N. K., Hotton, G. R., O'Sullivan, K., McCarter, R., Bunnage, M., Brooks, D. J., Svendsen, C. N., and Heywood, P. (2003) Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat. Med. 9, 589-595 (Pubitemid 36597106)
28. Hovland, D. N., Jr., Boyd, R. B., Butt, M. T., Engelhardt, J. A., Moxness, M. S., Ma, M. H., Emery, M. G., Ernst, N. B., Reed, R. P., Zeller, J. R., Gash, D. M., Masterman, D. M., Potter, B. M., Cosenza, M. E., and Lightfoot, R. M. (2007) Six-month continuous intraputamenal infusion toxicity study of recombinant methionyl human glial cell line-derived neurotrophic factor (r-metHuGDNF in rhesus monkeys. Toxicol. Pathol. 35, 1013-1029
29. Su, X., Kells, A. P., Huang, E. J., Lee, H. S., Hadaczek, P., Beyer, J., Bringas, J., Pivirotto, P., Penticuff, J., Eberling, J., Federoff, H. J., Forsayeth, J., and Bankiewicz, K. S. (2009) Safety evaluation of AAV2-GDNF gene transfer into the dopaminergic nigrostriatal pathway in aged and parkinsonian rhesus monkeys. Hum. Gene Ther. 20, 1627-1640
30. Lau, Y. S., Patki, G., Das-Panja, K., Le, W. D., and Ahmad, S. O. (2011) Neuroprotective effects and mechanisms of exercise in a chronic mouse model of Parkinson's disease with moderate neurodegeneration. Eur. J. Neurosci. 33, 1264-1274
31. Zigmond, M. J., Cameron, J. L., Leak, R. K., Mirnics, K., Russell, V. A., Smeyne, R. J., and Smith, A. D. (2009) Triggering endogenous neuroprotective processes through exercise in models of dopamine deficiency. Parkinsonism Relat. Disord. 15(Suppl. 3), S42-S45
32. Tajiri, N., Yasuhara, T., Shingo, T., Kondo, A., Yuan, W., Kadota, T., Wang, F., Baba, T., Tayra, J. T., Morimoto, T., Jing, M., Kikuchi, Y., Kuramoto, S., Agari, T., Miyoshi, Y., Fujino, H., Obata, F., Takeda, I., Furuta, T., and Date, I. (2010) Exercise exerts neuroprotective effects on Parkinson's disease model of rats. Brain Res. 1310, 200-207
33. Biju, K., Zhou, Q., Li, G., Imam, S. Z., Roberts, J. L., Morgan, W. W., Clark, R. A., and Li, S. (2010) Macrophage-mediated GDNF delivery protects against dopaminergic neurodegeneration: a therapeutic strategy for Parkinson's disease. Mol. Ther. 18, 1536-1544
34. Wu, J., Yu, W., Chen, Y., Su, Y., Ding, Z., Ren, H, Jiang, Y., and Wang, J. (2010) Intrastriatal transplantation of GDNF-engineered BMSCs and its neuroprotection in lactacystin-induced Parkinsonian rat model. Neurochem. Res. 35, 495-502
35. Thompson, L. H., Grealish, S., Kirik, D., and Bjorklund, A. (2009) Reconstruction of the nigrostriatal dopamine pathway in the adult mouse brain. Eur. J. Neurosci. 30, 625-638
36. Yang, X., Mertens, B., Lehtonen, E., Vercammen, L., Bockstael, O., Chtarto, A., Levivier, M., Brotchi, J., Michotte, Y., Baekelandt, V., Sarre, S., and Tenenbaum, L. (2009) Reversible neurochemical changes mediated by delayed intrastriatal glial cell line-derived neurotrophic factor gene delivery in a partial Parkinson's disease rat model. J. Gene Med. 11, 899-912
37. Eberling, J. L., Kells, A. P., Pivirotto, P., Beyer, J., Bringas, J., Federoff, H. J., Forsayeth, J., and Bankiewicz, K. S. (2009) Functional effects of AAV2-GDNF on the dopaminergic nigrostriatal pathway in parkinsonian rhesus monkeys. Hum. Gene Ther. 20, 511-518
38. Garbayo, E., Montero-Menei, C. N., Ansorena, E., Lanciego, J. L., Aymerich, M. S., and Blanco - Prieto, M. J. (2009) Effective GDNF brain delivery using microspheres-a promising strategy for Parkinson's disease. J. Control. Release 135, 119-126
39. Hong, M., Mukhida, K., and Mendez, I. (2008) GDNF therapy for Parkinson's disease. Expert Rev. Neurother. 8, 1125-1139 (Pubitemid 351962079)
40. Emborg, M. E., Ebert, A. D., Moirano, J., Peng, S., Suzuki, M., Capowski, E., Joers, V., Roitberg, B. Z., Aebischer, P., and Svendsen, C. N. (2008) GDNF-secreting human neural progenitor cells increase tyrosine hydroxylase and VMAT2 expression in MPTP-treated cynomolgus monkeys. Cell Transplant. 17, 383-395 (Pubitemid 351717341)
41. Lindvall, O., and Wahlberg, L. U. (2008) Encapsulated cell biodelivery of GDNF: a novel clinical strategy for neuroprotection and neuroregeneration in Parkinson's disease? Exp. Neurol. 209, 82-88
42. Guan, Y., Zhang, Y., Wu, J., Qi, Z., Yang, G., Dou, D., Gao, Y., Chen, L., Zhang, X., Davis, L. S, Wei, M., Fan, X., Carmosino, M., Hao, C., Imig, J. D, Breyer, R. M, and Breyer, M. D. (2007) Antihypertensive effects of selective prostaglandin E2 receptor subtype 1 targeting. J. Clin. Invest. 117, 2496-2505 (Pubitemid 47494351)
43. Li, X., Cudaback, E., Keene, C. D., Breyer, R. M., and Montine, T. J. (2011) Suppressed microglial E prostanoid receptor 1 signaling selectively reduces tumor necrosis factor α and interleukin 6 secretion from Toll-like receptor 3 activation. Glia 59, 569-576
44. Okun, E., Griffioen, K. J., Lathia, J. D., Tang, S. C., Mattson, M. P., and Arumugam, T. V. (2009) Toll-like receptors in neurodegeneration. Brain Res. Rev. 59, 278-292
45. Carpentier, P. A., Begolka, W. S., Olson, J. K., Elhofy, A., Karpus, W. J., and Miller, S. D. (2005) Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 49, 360-374 (Pubitemid 40222914)
46. Soeda, S., Koyanagi, S., Kuramoto, Y., Kimura, M., Oda, M., Kozako, T., Hayashida, S., and Shimeno, H. (2008) Anti-apoptotic roles of plasminogen activator inhibitor-1 as a neurotrophic factor in the central nervous system. Thromb. Haemost. 100, 1014-1020
47. Kariko, K., Ni, H., Capodici, J., Lamphier, M., and Weissman, D. (2004) mRNA is an endogenous ligand for Toll-like receptor 3. J. Biol. Chem. 279, 12542-12550 (Pubitemid 38445825)
48. Ginsberg, S. D., Galvin, J. E., Chiu, T. S., Lee, V. M., Masliah, E., and Trojanowski, J. Q. (1998) RNA sequestration to pathological lesions of neurodegenerative diseases. Acta Neuropathol. 96, 487-494 (Pubitemid 28474756)
49. Saito, T., and Gale, M., Jr. (2008) Differential recognition of double-stranded RNA by RIG-I-like receptors in antiviral immunity. J. Exp. Med. 205, 1523-1527 (Pubitemid 351962014)
50. Teismann, P., Tieu, K., Choi, D. K., Wu, D. C., Naini, A., Hunot, S., Vila, M., Jackson-Lewis, V., and Przedborski, S. (2003) Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 100, 5473-5478 (Pubitemid 36542729)
51. Mattammal, M. B., Strong, R., Lakshmi, V. M., Chung, H. D., and Stephenson, A. H. (1995) Prostaglandin H synthetase-mediated metabolism of dopamine: implication for Parkinson's disease. J. Neurochem. 64, 1645-1654
52. Chen, H., Jacobs, E., Schwarzschild, M. A., McCullough, M. L., Calle, E. E., Thun, M. J., and Ascherio, A. (2005) Nonsteroidal antiinflammatory drug use and the risk for Parkinson's disease. Ann. Neurol. 58, 963-967 (Pubitemid 41746889)
53. Gagne, J. J., and Power, M. C. (2010) Anti-inflammatory drugs and risk of Parkinson disease: a meta-analysis. Neurology 74, 995-1002
54. Gao, X., Chen, H., Schwarzschild, M. A., and Ascherio, A. (2011) Use of ibuprofen and risk of Parkinson disease. Neurology 76, 863-869
55. Becker, C., Jick, S. S., and Meier, C. R. (2011) NSAID use and risk of Parkinson disease: a population-based case-control study. Eur. J. Neurol. 18, 1336-1342
56. Driver, J. A., Logroscino, G., Lu, L., Gaziano, J. M., and Kurth, T. (2011) Use of non-steroidal anti-inflammatory drugs and risk of Parkinson's disease: nested case-control study. BMJ 342, d198
57. Bornebroek, M., de Lau, L. M., Haag, M. D., Koudstaal, P. J., Hofman, A., Stricker, B. H., and Breteler, M. M. (2007) Nonsteroidal anti-inflammatory drugs and the risk of Parkinson disease. Neuroepidemiology 28, 193-196 (Pubitemid 47573713)
58. Furuyashiki, T., and Narumiya, S. (2011) Stress responses: the contribution of prostaglandin E2 and its receptors. Nat. Rev. Endocrinol. 7, 163-175
59. 2 acts on EP1 receptor and amplifies both dopamine D1 and D2 receptor signaling in the striatum. J. Neurosci. 27, 12900-12907
60. Tanaka, Y., Furuyashiki, T., Momiyama, T., Namba, H., Mizoguchi, A., Mitsumori, T., Kayahara, T., Shichi, H., Kimura, K., Matsuoka, T., Nawa, H., Narumiya, S. (2009) Prostaglandin E receptor EP1 enhances GABA-mediated inhibition of dopaminergic neurons in the substantia nigra pars compacta and regulates dopamine level in the dorsal striatum. Eur. J. Neurosci. 30, 2338-2346