Minocycline upregulates pro-survival genes and downregulates pro-apoptotic genes in experimental glaucoma

Graefe's Archive for Clinical and Experimental Ophthalmology

Volumn 252, Issue 5, 2014, Pages 761-772

  Levkovitch Verbin, Hani ^a   Waserzoog, Yael ^a   Vander, Shelly ^a   Makarovsky, Daria ^a   Piven, Ilia ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Glaucoma; Minocycline; Neuroprotection; Optic nerve; Retinal ganglion cells

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR 1; CASPASE 4; CD68 ANTIGEN; FAS LIGAND; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; INDUCIBLE NITRIC OXIDE SYNTHASE; INHIBITOR OF APOPTOSIS PROTEIN 1; INTERLEUKIN 18; INTERLEUKIN 1BETA CONVERTING ENZYME; MINOCYCLINE; OSTEOPROTEGERIN; PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; DRUG MECHANISM; EXPERIMENTAL GLAUCOMA; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTRAOCULAR PRESSURE; LASER COAGULATION; MACROPHAGE ACTIVATION; MICROGLIA; MOUSE; MOUSE MODEL; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALS; ANTI-BACTERIAL AGENTS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; BCL-ASSOCIATED DEATH PROTEIN; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GLAUCOMA; INJECTIONS, INTRAPERITONEAL; INTERLEUKIN-18; MICROGLIA; MINOCYCLINE; OPTIC NERVE DISEASES; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; RETINAL GANGLION CELLS; UP-REGULATION;

EID: 84902291651     PISSN: 0721832X     EISSN: 1435702X     Source Type: Journal    
DOI: 10.1007/s00417-014-2588-4     Document Type: Article

References (49)

1. Aronson AL (1980) Pharmacotherapeutics of the newer tetracyclines. J Am Vet Med Assoc 176:1061-1068
2. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci U SA 95:15769-15774 (Pubitemid 29018775)
3. Zhang Y, Metz LM, Yong VW, Bell RB, Yeung M, Patry DG, Mitchell JR (2008) Pilot study of minocycline in relapsing-remitting multiple sclerosis. Can J Neurol Sci 35:185-191 (Pubitemid 351831055)
4. Pattison LR, Kotter MR, Fraga D, Bonelli RM (2006) Apoptotic cascades as possible targets for inhibiting cell death in Huntington's disease. J Neurol 253:1137-1142 (Pubitemid 44511468)
5. Kriz J, Nguyen MD, Julien JP (2002) Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 10:268-278 (Pubitemid 35217580)
6. Kim HS, Suh YH (2009) Minocycline and neurodegenerative diseases. Behav Brain Res 196:168-179
7. Levkovitz Y, Mendlovich S, Riwkes S, Braw Y, Levkovitch-Verbin H, Gal G, Fennig S, Treves I, Kron S (2009) A double-blind, randomized study of minocycline for the treatment of negative and cognitive symptoms in early-phase schizophrenia. J Clin Psychiatry 71(2):138-149
8. Lampl Y, Boaz M, Gilad R, Lorberboym M, Dabby R, Rapoport A, Anca-Hershkowitz M, Sadeh M (2007) Minocycline treatment in acute stroke: an open-label, evaluator-blinded study. Neurology 69:1404-1410 (Pubitemid 47511461)
9. Levkovitch-Verbin H, Kalev-Landoy M, Habot-Wilner Z, Melamed S (2006) Minocycline delays death of retinal ganglion cells in experimental glaucoma and after optic nerve transection. Arch Ophthalmol 124:520-526
10. Levkovitch-Verbin H, Spierer O, Vander S, Dardik R (2011) Similarities and differences between primary and secondary degeneration of the optic nerve and the effect ofminocycline. Graefes Arch Clin Exp Ophthalmol 249(6):849-857. doi:10.1007/s00417-010-1608-2
11. Baptiste DC, Hartwick AT, Jollimore CA, Baldridge WH, Seigel GM, Kelly ME (2004) An investigation of the neuroprotective effects of tetracycline derivatives in experimental models of retinal cell death. Mol Pharmacol 66(5):1113-1122 (Pubitemid 39411052)
12. 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 (Pubitemid 38510345)
13. 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 (Pubitemid 38998874)
14. Teng YD, Choi H, Onario RC, Zhu S, Desilets FC, Lan S, Woodard EJ, Snyder EY, Eichler ME, Friedlander RM (2004) Minocycline inhibits contusion-triggered mitochondrial cytochrome c release and mitigates functional deficits after spinal cord injury. Proc Natl Acad Sci U S A 101:3071-3076 (Pubitemid 38327736)
15. Yang LP, Zhu XA, Tso MO (2007) Minocycline and sulforaphane inhibited lipopolysaccharide-mediated retinal microglial activation. Mol Vis 13:1083-1093
16. Baptiste DC, Powell KJ, Jollimore CA, Hamilton C, LeVatte TL, Archibald ML, Chauhan BC, Robertson GS, Kelly ME (2005) Effects of minocycline and tetracycline on retinal ganglion cell survival after axotomy. Neuroscience 134:575-582 (Pubitemid 41111785)
17. Yuan L, Neufeld AH (2001) Activated microglia in the human glaucomatous optic nerve head. J Neurosci Res 64:523-532 (Pubitemid 32521772)
18. Naskar R, Wissing M, Thanos S (2002) Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest Ophthalmol Vis Sci 43:2962-2968 (Pubitemid 34977046)
19. Chauhan BC, LeVatte TL, Jollimore CA, Yu PK, Reitsamer HA, Kelly ME, Yu DY, Tremblay F, Archibald ML (2004) Model of endothelin-1-induced chronic optic neuropathy in rat. Invest Ophthalmol Vis Sci 45:144-152 (Pubitemid 38055680)
20. 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/2 J mouse model of glaucoma. Invest Ophthalmol Vis Sci 49:1437-1446
21. Du Y, Ma Z, Lin S, Dodel RC, Gao F, Bales KR, Triarhou LC, Chernet E, Perry KW, Nelson DL, Luecke S, Phebus LA, Bymaster FP, Paul SM (2001) Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc Natl Acad Sci U S A 98:14669-14674 (Pubitemid 33121449)
22. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu du C, 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 (Pubitemid 34498818)
23. 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 Med 6:797-801 (Pubitemid 30469429)
24. Sanchez Mejia RO, Ona VO, Li M, Friedlander RM (2001) Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery 48:1393-1399, discussion 1399-1401
25. Wang J, Wei Q, Wang CY, Hill WD, Hess DC, Dong Z (2004) Minocycline up-regulates Bcl-2 and protects against cell death in mitochondria. J Biol Chem 279:19948-19954 (Pubitemid 38623437)
26. Wang X, Zhu S, Drozda M, Zhang W, Stavrovskaya IG, Cattaneo E, Ferrante RJ, Kristal BS, Friedlander RM(2003) Minocycline inhibits caspase-independent and -dependent mitochondrial cell death pathways in models of Huntington's disease. Proc Natl Acad Sci U S A 100:10483-10487 (Pubitemid 37071904)
27. Levkovitch-Verbin H, Dardik R, Vander S, Melamed S (2009) Mechanism of retinal ganglion cells death in secondary degeneration of the optic nerve. Exp Eye Res 2:127-134
28. Kozlowski C, Weimer RM (2012) An automated method to quantify microglia morphology and application to monitor activation state longitudinally in vivo. PLoS One 7(2):e31814
29. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S (1998) Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57(1):1-9 (Pubitemid 28279554)
30. Graeber MB, López-Redondo F, Ikoma E, Ishikawa M, Imai Y, Nakajima K, Kreutzberg GW, Kohsaka S (1998) The microglia/macrophage response in the neonatal rat facial nucleus following axotomy. Brain Res 813(2):241-253 (Pubitemid 29009640)
31. Tikka TM, Koistinaho JE (2001) Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J Immunol 166:7527-7533 (Pubitemid 32525632)
32. Suzuki H, Sugimura Y, Iwama S, Nobuaki O, Nagasaki H, Arima H, Sawada M, Oiso Y (2010) Minocycline prevents osmotic demyelination syndrome by inhibiting the activation of microglia. J Am Soc Nephrol 21: 2090-2098
33. Cho KO, La HO, Cho YJ, Sung KW, Kim SY (2006) Minocycline attenuates white matter damage in a rat model of chronic cerebral hypoperfusion. J Neurosci Res 83:285-291 (Pubitemid 43184392)
34. Wang AL, Yu AC, Lau LT, Lee C, le Wu M, Zhu X, Tso MO (2005) Minocycline inhibits LPS-induced retinal microglia activation. Neurochem Int 47:152-158
35. Antonsson B, Martinou JC (2000) The Bcl-2 protein family. Exp Cell Res 256:50-57 (Pubitemid 30211166)
36. Maier K, Merkler D, Gerber J, Taheri N, Kuhnert AV, Williams SK, Neusch C, Bahr M, Diem R (2007) Multiple neuroprotective mechanisms ofminocycline in autoimmune CNS inflammation. Neurobiol Dis 25:514-525
37. Nickells RW (1999) Apoptosis of retinal ganglion cells in glaucoma: an update of the molecular pathways involved in cell death. Surv Ophthalmol 43(Suppl 1):S151-S161
38. Levkovitch-Verbin H, Dardik R, Vander S, Nisgav Y, Kalev-Landoy M, Melamed S (2006) Experimental glaucoma and optic nerve transection induce simultaneous upregulation of proapoptotic and prosurvival genes. Invest Ophthalmol Vis Sci 47:2491-2497 (Pubitemid 351639832)
39. Fan BJ, Liu K, Wang DY, Tham CC, Tam PO, Lam DS, Pang CP (2010) Association of polymorphisms of tumor necrosis factor and tumor protein p53 with primary open-angle glaucoma. Invest Ophthalmol Vis Sci 51: 4110-4116
40. Baptiste DC, Hartwick AT, Jollimore CA, Baldridge WH, Seigel GM, Kelly ME (2004) An investigation of the neuroprotective effects of tetracycline derivatives in experimental models of retinal cell death. Mol Pharmacol 66:1113-1122 (Pubitemid 39411052)
41. 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
42. Hughes E, Schlichtebrede F, Murphy C, Ali R, Dick A (2003) Minocycline suppresses photoreceptor apoptosis in the rds mouse through a mechanism unrelated to microglial inhibition. ARVO abstract #2843
43. Zhou X, Li F, Kong L, Chodosh J, Cao W (2009) Anti-inflammatory effect of pigment epithelium-derived factor in DBA/2 J mice. Mol Vis 15:438-450
44. Fox C, Dingman A, Derugin N, Wendland MF, Manabat C, Ji S, Ferriero DM, Vexler ZS (2005) Minocycline confers early but transient protection in the immature brain following focal cerebral ischemia-reperfusion. J Cereb Blood Flow Metab 25:1138-1149 (Pubitemid 41710740)
45. Chu YX, Zhang YQ, Zhao ZQ (2012) Involvement of microglia and interleukin-18 in the induction of long-term potentiation of spinal nociceptive responses induced by tetanic sciatic stimulation. Neurosci Bull 28: 49-60
46. Tezel G, Li LY, Patil RV, Wax MB (2001) TNF-alpha and TNF-alpha receptor-1 in the retina of normal and glaucomatous eyes. Invest Ophthalmol Vis Sci 42:1787-1794 (Pubitemid 32652354)
47. Gregory MS, Hackett CG, Abernathy EF, Lee KS, Saff RR, Hohlbaum AM, Moody KS, Hobson MW, Jones A, Kolovou P, Karray S, Giani A, John SW, Chen DF, Marshak-Rothstein A, Ksander BR (2011)Opposing roles for membrane bound and soluble Fas ligand in glaucoma-associated retinal ganglion cell death. PLoS One 6:e17659
48. Blaise S, Kneib M, Rousseau A, Gambino F, Chenard MP, Messadeq N, Muckenstrum M, Alpy F, Tomasetto C, Humeau Y, Rio MC (2012) In vivo evidence that TRAF4 is required for central nervous system myelin homeostasis. PLoS One 7:e30917
49. Armitage RJ, Maliszewski CR, Alderson MR, Grabstein KH, Spriggs MK, Fanslow WC (1993) CD40L: a multi-functional ligand. Semin Immunol 5:401-412