Suppression of microglial activation is neuroprotective in a mouse model of human retinitis pigmentosa

Journal of Neuroscience

Volumn 34, Issue 24, 2014, Pages 8139-8150

  Peng, Bo ^a   Xiao, Jia ^a,c   Wang, Ke ^a   So, Kwok Fai ^a,b   Tipoe, George L ^a   Lin, Bin ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c JINAN UNIVERSITY   (China)

Author keywords

Cx3cr1; Microglia; Minocycline; Photoreceptor degeneration; Rd10 mice

Indexed keywords

5 (4 CHLOROPHENYL) 1 (4 METHOXYPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOLE; CASPASE 3; CASPASE 7; CD11B ANTIGEN; CD45 ANTIGEN; CD68 ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; MINOCYCLINE; PROTEIN BAX; PROTEIN BCL 2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BEHAVIORAL SCIENCE; CELL ACTIVATION; CELL DEATH; CELL FUNCTION; CELL INFILTRATION; CELL SUPPRESSION; CENTRAL NERVOUS SYSTEM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE COURSE; ELECTRORETINOGRAPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; MALE; MICROGLIA; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NICK END LABELING; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA DEVELOPMENT; RETINAL THICKNESS; RETINITIS PIGMENTOSA; SIGNAL TRANSDUCTION;

CX3CR1; MICROGLIA; MINOCYCLINE; PHOTORECEPTOR DEGENERATION; RD10 MICE;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 6; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MINOCYCLINE; MUTATION; NEUROPROTECTIVE AGENTS; PYRAZOLES; RECEPTORS, CHEMOKINE; RETINA; RETINAL DEGENERATION; RETINITIS PIGMENTOSA;

EID: 84902143838     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5200-13.2014     Document Type: Article

References (58)

1. Block ML, Zecca L, Hong JS (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8:57-69. CrossRef Medline
2. Bosco A, Inman DM, Steele MR, Wu G, Soto I, Marsh-Armstrong N, Hubbard WC, Calkins DJ, Horner PJ, Vetter ML (2008) Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci 49:1437-1446. CrossRef Medline
3. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917-924. CrossRef Medline
4. Chen M, Ona VO, Li M, Ferrante RJ, Fink KB, Zhu S, Bian J, Guo L, Farrell LA, Hersch SM, Hobbs W, Vonsattel JP, Cha JH, Friedlander RM (2000) Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med6:797-801. CrossRef Medline
5. Choi SH, Bosetti F (2009) Cyclooxygenase-1 null mice show reduced neuroinflammation in response to beta-amyloid. Aging 1:234-244. Medline
6. Choi SH, Langenbach R, Bosetti F (2008) Genetic deletion or pharmacological inhibition of cyclooxygenase-1 attenuate lipopolysaccharide-induced inflammatory response and brain injury. FASEB J 22:1491-1501. Medline
7. Choi SH, Aid S, Bosetti F (2009) The distinct roles of cyclooxygenase-1 and-2 in neuroinflammation: implications for translational research. Trends Pharmacol Sci 30:174-181. CrossRef Medline
8. Combadière C, Feumi C, Raoul W, Keller N, Rodéro M, Pézard A, Lavalette S, Houssier M, Jonet L, Picard E, Debré P, Sirinyan M, Deterre P, Ferroukhi T, Cohen SY, Chauvaud D, Jeanny JC, Chemtob S, Behar-Cohen F, Sennlaub F (2007) CX3CR1-dependent subretinal microglia cell accumulation is associated with cardinal features of age-related macular degeneration. J Clin Invest 117:2920-2928. CrossRef Medline
9. Ebert S, Weigelt K, Walczak Y, Drobnik W, Mauerer R, Hume DA, Weber BH, Langmann T (2009) Docosahexaenoic acid attenuates microglial activation and delays early retinal degeneration. J Neurochem 110:1863-1875. CrossRef Medline
10. Fan R, Xu F, Previti ML, Davis J, Grande AM, Robinson JK, Van Nostrand WE (2007) Minocycline reduces microglial activation and improves behavioral deficits in a transgenic model of cerebral microvascular amyloid. J Neurosci 27:3057-3063. CrossRef Medline
11. Fuhrmann M, Bittner T, Jung CK, Burgold S, Page RM, Mitteregger G, Haass C, La Ferla FM, Kretzschmar H, Herms J (2010) Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat Neurosci 13:411-413. CrossRef Medline
12. García-Bueno B, Serrats J, Sawchenko PE (2009) Cerebrovascular cyclooxygenase-1 expression, regulation, and role in hypothalamicpituitary-adrenal axis activation by inflammatory stimuli. J Neurosci 29: 12970-12981. CrossRef Medline
13. Gargini C, Terzibasi E, Mazzoni F, Strettoi E (2007) Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study. J Comp Neurol 500:222-238. CrossRef Medline
14. Gehrig A, Langmann T, Horling F, Janssen A, Bonin M, Walter M, Poths S, Weber BH (2007) Genome-wide expression profiling of the retinoschisindeficient retina in early postnatal mouse development. Invest Ophthalmol Vis Sci 48:891-900. CrossRef Medline
15. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH (2010) Mechanisms underlying inflammation in neurodegeneration. Cell 140:918-934. CrossRef Medline
16. Griffin ÉW, Skelly DT, Murray CL, Cunningham C (2013) Cyclooxygenase-1-dependent prostaglandins mediate susceptibility to systemic inflammationinduced acute cognitive dysfunction. J Neurosci 33:15248-15258. CrossRef Medline
17. Gupta N, Brown KE, Milam AH (2003) Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp Eye Res 76:463-471. CrossRef Medline
18. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394. CrossRef Medline
19. Harrison JK, Jiang Y, Chen S, Xia Y, Maciejewski D, McNamara RK, Streit WJ, Salafranca MN, Adhikari S, Thompson DA, Botti P, Bacon KB, Feng L (1998) Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci U S A 95:10896-10901. CrossRef Medline
20. Hartong DT, Berson EL, Dryja TP (2006) Retinitis pigmentosa. Lancet 368: 1795-1809. CrossRef Medline
21. Haverkamp S, Wässle H, Duebel J, Kuner T, Augustine GJ, Feng G, Euler T (2005) The primordial, blue-cone color system of the mouse retina. J Neurosci 25:5438-5445. CrossRef Medline
22. Hughes EH, Schlichtenbrede FC, Murphy CC, Broderick C, van Rooijen N, Ali RR, Dick AD (2004) Minocycline delays photoreceptor death in the rds mouse through a microglia-independent mechanism. Exp Eye Res 78:1077-1084. CrossRef Medline
23. Iwakabe H, Katsuura G, Ishibashi C, Nakanishi S (1997) Impairment of pupillary responses and optokinetic nystagmus in the m Glu R6-deficient mouse. Neuropharmacology 36:135-143. CrossRef Medline
24. Jiang J, Quan Y, Ganesh T, Pouliot WA, Dudek FE, Dingledine R (2013) Inhibition of the prostaglandin receptor EP2 following status epilepticus reduces delayed mortality and brain inflammation. Proc Natl Acad Sci U S A 110:3591-3596. CrossRef Medline
25. Kohno H, Chen Y, Kevany BM, Pearlman E, Miyagi M, Maeda T, Palczewski K, Maeda A (2013) Photoreceptor proteins initiate microglial activation via Toll-like receptor 4 in retinal degeneration mediated by all-transretinal. J Biol Chem 288:15326-15341. CrossRef Medline
26. Langmann T (2007) Microglia activation in retinal degeneration. J Leukoc Biol 81:1345-1351. CrossRef Medline
27. Lazarini F, Gabellec MM, Torquet N, Lledo PM (2012) Early activation of microglia triggers long-lasting impairment of adult neurogenesis in the olfactory bulb. J Neurosci 32:3652-3664. CrossRef Medline
28. Liang KJ, Lee JE, Wang YD, Ma W, Fontainhas AM, Fariss RN, Wong WT (2009) Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest Ophthalmol Vis Sci 50:4444-4451. CrossRef Medline
29. Lin B, Masland RH, Strettoi E (2009) Remodeling of cone photoreceptor cells after rod degeneration in rd mice. Exp Eye Res 88:589-599. CrossRef Medline
30. Lucin KM, Wyss-Coray T (2009) Immune activation in brain aging and neurodegeneration: too much or too little? Neuron 64:110-122. CrossRef Medline
31. Meucci O, Fatatis A, Simen AA, Miller RJ (2000) Expression of CX3CR1 chemokine receptors on neurons and their role in neuronal survival. Proc Natl Acad Sci U S A 97:8075-8080. CrossRef Medline
32. Prusky GT, Alam NM, Beekman S, Douglas RM (2004) Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45:4611-4616. CrossRef Medline
33. Roque RS, Imperial CJ, Caldwell RB (1996) Microglial cells invade the outer retina as photoreceptors degenerate in Royal College of Surgeons rats. Invest Ophthalmol Vis Sci 37:196-203. Medline
34. Saijo K, Glass CK (2011) Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol 11:775-787. CrossRef Medline
35. Sasahara M, Otani A, Oishi A, Kojima H, Yodoi Y, Kameda T, Nakamura H, Yoshimura N (2008) Activation of bone marrow-derived microglia promotes photoreceptor survival in inherited retinal degeneration. Am J Pathol 172:1693-1703. CrossRef Medline
36. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complementdependent manner. Neuron 74:691-705. CrossRef Medline
37. Sharma AK, Rohrer B (2007) Sustained elevation of intracellular c GMP causes oxidative stress triggering calpain-mediated apoptosis in photoreceptor degeneration. Curr Eye Res 32:259-269. CrossRef Medline
38. Sheets KG, Jun B, Zhou Y, Zhu M, Petasis NA, Gordon WC, Bazan NG (2013) Microglial ramification and redistribution concomitant with the attenuation of choroidal neovascularization by neuroprotectin D1. Mol Vis 19:1747-1759. Medline
39. Shen D, Cao X, Zhao L, Tuo J, Wong WT, Chan CC (2011) Naloxone ameliorates retinal lesions in Ccl2/Cx3cr1 double-deficient mice via modulation of microglia. Invest Ophthalmol Vis Sci 52:2897-2904. CrossRef Medline
40. Teismann P, Tieu K, Choi DK, Wu DC, Naini A, Hunot S, Vila M, Jackson-Lewis V, Przedborski S (2003a) Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc Natl Acad Sci U S A 100: 5473-5478. CrossRef Medline
41. Teismann P, Vila M, Choi DK, Tieu K, Wu DC, Jackson-Lewis V, Przedborski S (2003b) COX-2 and neurodegeneration in Parkinson's disease. Ann N Y Acad Sci 991:272-277. Medline
42. Umino Y, Solessio E, Barlow RB (2008) Speed, spatial, and temporal tuning of rod and cone vision in mouse. J Neurosci 28:189-198. CrossRef Medline
43. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, Choi DK, Ischiropoulos H, Przedborski S (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 22:1763-1771. Medline
44. Xiao J, Ching YP, Liong EC, Nanji AA, Fung ML, Tipoe GL (2013) Garlicderived S-allylmercaptocysteine is a hepato-protective agent in nonalcoholic fatty liver disease in vivo animal model. Eur J Nutr 52:179-191. CrossRef Medline
45. Yang LP, Li Y, Zhu XA, Tso MO (2007) Minocycline delayed photoreceptor death in rds mice through i NOS-dependent mechanism. Mol Vis 13: 1073-1082. Medline
46. Yong VW, Wells J, Giuliani F, Casha S, Power C, Metz LM (2004) The promise of minocycline in neurology. Lancet Neurol 3:744-751. CrossRef Medline
47. Yoshida N, Ikeda Y, Notomi S, Ishikawa K, Murakami Y, Hisatomi T, Enaida H, Ishibashi T (2013a) Clinical evidence of sustained chronic inflammatory reaction in retinitis pigmentosa. Ophthalmology 120:100-105. CrossRef Medline
48. Yoshida N, Ikeda Y, Notomi S, Ishikawa K, Murakami Y, Hisatomi T, Enaida H, Ishibashi T (2013b) Laboratory evidence of sustained chronic inflammatory reaction in retinitis pigmentosa. Ophthalmology 120:e5-e12. CrossRef Medline
49. Yoshizawa K, Kiuchi K, Nambu H, Yang J, Senzaki H, Kiyozuka Y, Shikata N, Tsubura A (2002) Caspase-3 inhibitor transiently delays inherited retinal degeneration in C3H mice carrying the rd gene. Graefes Arch Clin Exp Ophthalmol 240:214-219. CrossRef Medline
50. Yrjänheikki J, Keinänen R, Pellikka M, Hökfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci U S A 95:15769-15774. CrossRef Medline
51. Yrjänheikki J, Tikka T, Keinänen R, Goldsteins G, Chan PH, Koistinaho J (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci U S A 96:13496-13500. CrossRef Medline
52. Zeiss CJ, Johnson EA (2004) Proliferation of microglia, but not photoreceptors, in the outer nuclear layer of the rd-1 mouse. Invest Ophthalmol Vis Sci 45:971-976. CrossRef Medline
53. Zeiss CJ, Neal J, Johnson EA (2004) Caspase-3 in postnatal retinal development and degeneration. Invest Ophthalmol Vis Sci 45:964-970. CrossRef Medline
54. Zeng HY, Zhu XA, Zhang C, Yang LP, Wu LM, Tso MO (2005) Identification of sequential events and factors associated with microglial activation, migration, and cytotoxicity in retinal degeneration in rd mice. Invest Ophthalmol Vis Sci 46:2992-2999. CrossRef Medline
55. Zhang C, Lei B, Lam TT, Yang F, Sinha D, Tso MO (2004) Neuroprotection of photoreceptors by minocycline in light-induced retinal degeneration. Invest Ophthalmol Vis Sci 45:2753-2759. CrossRef Medline
56. Zhao L, Ma W, Fariss RN, Wong WT (2011) Minocycline attenuates photoreceptor degeneration in a mouse model of subretinal hemorrhage microglial: inhibition as a potential therapeutic strategy. Am J Pathol 179: 1265-1277. CrossRef Medline
57. Zhou Y, Sheets KG, Knott EJ, Regan CE Jr, Tuo J, Chan CC, Gordon WC, Bazan NG (2011) Cellular and 3D optical coherence tomography assessment during the initiation and progression of retinal degeneration in the Ccl2/Cx3cr1-deficient mouse. Exp Eye Res 93:636-648. CrossRef Medline
58. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu DC, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM (2002) Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417: 74-78. CrossRef Medline