Minocycline counter-regulates pro-inflammatory microglia responses in the retina and protects from degeneration

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Scholz, Rebecca ^a   Sobotka, Markus ^a   Caramoy, Albert ^a   Stempfl, Thomas ^b   Moehle, Christoph ^b   Langmann, Thomas ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Age related macular degeneration; Light damage; Microglia; Minocycline; Photoreceptors; Retinal degeneration

Indexed keywords

ACTIVATED MICROGLIA MACROPHAGE WHEY ACIDIC PROTEIN; CASPASE 3; CASPASE 7; CD68 ANTIGEN; CELL MARKER; CELL PROTEIN; GRIESS REAGENT; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MESSENGER RNA; MINOCYCLINE; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; REAGENT; TRANSLOCATOR PROTEIN; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; AUTACOID; CASPASE; LIPOPOLYSACCHARIDE; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BV 2 CELL LINE; CELL STIMULATION; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; FEMALE; GENE EXPRESSION REGULATION; GLIOSIS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; LIGHT EXPOSURE; MALE; MICROGLIA; MICROGLIAL CELL CULTURE; MOUSE; NEURITIS; NEUROTOXICITY; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; PHOTORECEPTOR; PROTECTION; REAL TIME POLYMERASE CHAIN REACTION; RETINA DEGENERATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TRANSCRIPTION TERMINATION; TUNEL ASSAY; WHITE LIGHT; ADVERSE EFFECTS; ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECTS; LIGHT; METABOLISM; NERVE DEGENERATION; PATHOLOGY; RETINA; RETINAL DEGENERATION; RETINAL DISEASES;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CASPASES; INFLAMMATION MEDIATORS; LIGHT; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; MICROGLIA; MINOCYCLINE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; RETINA; RETINAL DEGENERATION; RETINAL DISEASES;

EID: 84946904610     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0431-4     Document Type: Article

References (63)

1. Wong WL, Su X, Li X, Cheung CM, Klein R, Cheng CY, et al. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis. Lancet Glob Health. 2014;2:e106-116.
2. Jager RD, Mieler WF, Miller JW. Age-related macular degeneration. N Engl J Med. 2008;358:2606-17.
3. Xu H, Chen M, Forrester JV. Para-inflammation in the aging retina. Prog Retin Eye Res. 2009;28:348-68.
4. Gupta N, Brown KE, Milam AH. Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration. Exp Eye Res. 2003;76:463-71.
5. Karlstetter M, Scholz R, Rutar M, Wong WT, Provis JM, Langmann T. Retinal microglia: just bystander or target for therapy? Prog Retin Eye Res. 2015;45:30-57.
6. Hume DA, Perry VH, Gordon S. Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J Cell Biol. 1983;97:253-7.
7. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev. 2011;91:461-553.
8. Damani MR, Zhao L, Fontainhas AM, Amaral J, Fariss RN, Wong WT. Age-related alterations in the dynamic behavior of microglia. Aging Cell. 2011;10:263-76.
9. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 2005;308:1314-8.
10. Aloisi F. Immune function of microglia. Glia. 2001;36:165-79.
11. Langmann T. Microglia activation in retinal degeneration. J Leukoc Biol. 2007;81:1345-51.
12. Karlstetter M, Langmann T. Microglia in the aging retina. Adv Exp Med Biol. 2014;801:207-12.
13. Zhao L, Zabel MK, Wang X, Ma W, Shah P, Fariss RN, et al. Microglial phagocytosis of living photoreceptors contributes to inherited retinal degeneration. EMBO Mol Med. 2015;7(9):1179-97.
14. Sierra A, Gottfried-Blackmore AC, McEwen BS, Bulloch K. Microglia derived from aging mice exhibit an altered inflammatory profile. Glia. 2007;55:412-24.
15. Roque RS, Rosales AA, Jingjing L, Agarwal N, Al-Ubaidi MR. Retina-derived microglial cells induce photoreceptor cell death in vitro. Brain Res. 1999;836:110-9.
16. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, et al. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci. 2002;22:1763-71.
17. Amor S, Puentes F, Baker D, van der Valk P. Inflammation in neurodegenerative diseases. Immunology. 2010;129:154-69.
18. Biscaro B, Lindvall O, Tesco G, Ekdahl CT, Nitsch RM. Inhibition of microglial activation protects hippocampal neurogenesis and improves cognitive deficits in a transgenic mouse model for Alzheimer's disease. Neurodegener Dis. 2012;9:187-98.
19. Du Y, Ma Z, Lin S, Dodel RC, Gao F, Bales KR, et al. Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc Natl Acad Sci U S A. 2001;98:14669-74.
20. Popovic N, Schubart A, Goetz BD, Zhang SC, Linington C, Duncan ID. Inhibition of autoimmune encephalomyelitis by a tetracycline. Ann Neurol. 2002;51:215-23.
21. Owolabi SA, Saab CY. Fractalkine and minocycline alter neuronal activity in the spinal cord dorsal horn. FEBS Lett. 2006;580:4306-10.
22. Mika J, Osikowicz M, Makuch W, Przewlocka B. Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain. Eur J Pharmacol. 2007;560:142-9.
23. Garrido-Mesa N, Zarzuelo A, Galvez J. Minocycline: far beyond an antibiotic. Br J Pharmacol. 2013;169:337-52.
24. Niimi N, Kohyama K, Matsumoto Y. Minocycline suppresses experimental autoimmune encephalomyelitis by increasing tissue inhibitors of metalloproteinases. Neuropathology. 2013;33:612-20.
25. Peng B, Xiao J, Wang K, So KF, Tipoe GL, Lin B. Suppression of microglial activation is neuroprotective in a mouse model of human retinitis pigmentosa. J Neurosci. 2014;34:8139-50.
26. Cruickshanks KJ, Klein R, Klein BE. Sunlight and age-related macular degeneration: the beaver dam eye study. Arch Ophthalmol. 1993;111:514-8.
27. Swaroop A, Chew EY, Rickman CB, Abecasis GR. Unraveling a multifactorial late-onset disease: from genetic susceptibility to disease mechanisms for age-related macular degeneration. Annu Rev Genomics Hum Genet. 2009;10:19-43.
28. Grimm C, Reme CE. Light damage as a model of retinal degeneration. Methods Mol Biol. 2013;935:87-97.
29. Marc RE, Jones BW, Watt CB, Vazquez-Chona F, Vaughan DK, Organisciak DT. Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol Vis. 2008;14:782-806.
30. Narimatsu T, Ozawa Y, Miyake S, Kubota S, Hirasawa M, Nagai N, et al. Disruption of cell-cell junctions and induction of pathological cytokines in the retinal pigment epithelium of light-exposed mice. Invest Ophthalmol Vis Sci. 2013;54:4555-62.
31. Pennesi ME, Neuringer M, Courtney RJ. Animal models of age related macular degeneration. Mol Aspects Med. 2012;33:487-509.
32. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol. 1990;27:229-37.
33. Ebert S, Weigelt K, Walczak Y, Drobnik W, Mauerer R, Hume DA, et al. Docosahexaenoic acid attenuates microglial activation and delays early retinal degeneration. J Neurochem. 2009;110:1863-75.
34. Ebert S, Schoeberl T, Walczak Y, Stoecker K, Stempfl T, Moehle C, et al. Chondroitin sulfate disaccharide stimulates microglia to adopt a novel regulatory phenotype. J Leukoc Biol. 2008;84:736-40.
35. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15-21.
36. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106.
37. Eichler GS, Huang S, Ingber DE. Gene expression dynamics inspector (GEDI): for integrative analysis of expression profiles. Bioinformatics. 2003;19:2321-2.
38. Karlstetter M, Walczak Y, Weigelt K, Ebert S, Van den Brulle J, Schwer H, et al. The novel activated microglia/macrophage WAP domain protein, AMWAP, acts as a counter-regulator of proinflammatory response. J Immunol. 2010;185:3379-90.
39. Karlstetter M, Nothdurfter C, Aslanidis A, Moeller K, Horn F, Scholz R, et al. Translocator protein (18 kDa) (TSPO) is expressed in reactive retinal microglia and modulates microglial inflammation and phagocytosis. J Neuroinflammation. 2014;11:3. doi: 10.1186/1742-2094-11-3.
40. Aslanidis A, Karlstetter M, Scholz R, Fauser S, Neumann H, Fried C, et al. Activated microglia/macrophage whey acidic protein (AMWAP) inhibits NFkappaB signaling and induces a neuroprotective phenotype in microglia. J Neuroinflammation. 2015;12:77.
41. Scholz R, Caramoy A, Bhuckory MB, Rashid K, Chen M, Xu H, et al. Targeting translocator protein (18kDa) (TSPO) dampens pro-inflammatory microglia reactivity in the retina and protects from degeneration. J Neuroinflammation. 2015;12:201.
42. Nikodemova M, Watters JJ, Jackson SJ, Yang SK, Duncan ID. Minocycline down-regulates MHC II expression in microglia and macrophages through inhibition of IRF-1 and protein kinase C (PKC)alpha/betaII. J Biol Chem. 2007;282:15208-16.
43. Chen M, Ona VO, Li M, Ferrante RJ, Fink KB, Zhu S, et al. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of huntington disease. Nat Med. 2000;6:797-801.
44. Tikka TM, Vartiainen NE, Goldsteins G, Oja SS, Andersen PM, Marklund SL, et al. Minocycline prevents neurotoxicity induced by cerebrospinal fluid from patients with motor neurone disease. Brain. 2002;125:722-31.
45. Tso MO, Zhu X, Wang AL, Yu AC, Lau LT, Lee C, et al. Minocycline inhibits LPS-induced retinal microglia activation. Neurochem Int. 2005;47:152-8.
46. Henry CJ, Huang Y, Wynne A, Hanke M, Himler J, Bailey MT, et al. Minocycline attenuates lipopolysaccharide (LPS)-induced neuroinflammation, sickness behavior, and anhedonia. J Neuroinflammation. 2008;5:15.
47. Yang L-p, Li Y, Zhu X-a, Tso MOM. Minocycline delayed photoreceptor death in the rds mice through iNOS-dependent mechanism. Mol Vis. 2007;13:1073-82.
48. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci U S A. 1999;96:13496-500.
49. Hoey S, Grabowski PS, Ralston SH, Forrester JV, Liversidge J. Nitric oxide accelerates the onset and increases the severity of experimental autoimmune uveoretinitis through an IFN-gamma-dependent mechanism. J Immunol. 1997;159:5132-42.
50. Amin AR, Patel RN, Thakker GD, Lowenstein CJ, Attur MG, Abramson SB. Post-transcriptional regulation of inducible nitric oxide synthase mRNA in murine macrophages by doxycycline and chemically modified tetracyclines. FEBS Lett. 1997;410:259-64.
51. Matsui T, Svensson CI, Hirata Y, Mizobata K, Hua XY, Yaksh TL. Release of prostaglandin E(2) and nitric oxide from spinal microglia is dependent on activation of p38 mitogen-activated protein kinase. Anesth Analg. 2010;111:554-60.
52. Beattie MS. Inflammation and apoptosis: linked therapeutic targets in spinal cord injury. Trends Mol Med. 2004;10:580-3.
53. Wang X, Zhu S, Drozda M, Zhang W, Stavrovskaya IG, Cattaneo E, et al. Minocycline inhibits caspase-independent and -dependent mitochondrial cell death pathways in models of huntington's disease. Proc Natl Acad Sci U S A. 2003;100:10483-7.
54. Cheng S, Hou J, Zhang C, Xu C, Wang L, Zou X, et al. Minocycline reduces neuroinflammation but does not ameliorate neuron loss in a mouse model of neurodegeneration. Sci Rep. 2015;5:10535.
55. Park CH, Shin TK, Lee HY, Kim SJ, Lee WS. Matrix metalloproteinase inhibitors attenuate neuroinflammation following focal cerebral ischemia in mice. Korean J Physiol Pharmacol. 2011;15:115-22.
56. Koistinaho M, Malm TM, Kettunen MI, Goldsteins G, Starckx S, Kauppinen RA, et al. Minocycline protects against permanent cerebral ischemia in wild type but not in matrix metalloprotease-9-deficient mice. J Cereb Blood Flow Metab. 2005;25:460-7.
57. Bosco A, Inman DM, Steele MR, Wu G, Soto I, Marsh-Armstrong N, et al. Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci. 2008;49:1437-46.
58. Zhang C, Lei B, Lam TT, Yang F, Sinha D, Tso MO. Neuroprotection of photoreceptors by minocycline in light-induced retinal degeneration. Invest Ophthalmol Vis Sci. 2004;45:2753-9.
59. Wenzel A, Grimm C, Samardzija M, Reme CE. Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res. 2005;24:275-306.
60. Youssef PN, Sheibani N, Albert DM. Retinal light toxicity. Eye (Lond). 2011;25:1-14.
61. Grimm C, Wenzel A, Williams T, Rol P, Hafezi F, Reme C. Rhodopsin-mediated blue-light damage to the rat retina: effect of photoreversal of bleaching. Invest Ophthalmol Vis Sci. 2001;42:497-505.
62. Grimm C, Reme CE, Rol PO, Williams TP. Blue light's effects on rhodopsin: photoreversal of bleaching in living rat eyes. Invest Ophthalmol Vis Sci. 2000;41:3984-90.
63. Hughes EH, Schlichtenbrede FC, Murphy CC, Broderick C, van Rooijen N, Ali RR, et al. Minocycline delays photoreceptor death in the rds mouse through a microglia-independent mechanism. Exp Eye Res. 2004;78:1077-84.