Minocycline reduces proinflammatory cytokine expression, microglial activation, and caspase-3 activation in a rodent model of diabetic retinopathy

Diabetes

Volumn 54, Issue 5, 2005, Pages 1559-1565

  Krady, J Kyle ^a   Basu, Anirban ^a   Allen, Colleen M ^a   Xu, Yuping ^a   LaNoue, Kathryn F ^a   Gardner, Thomas W ^a   Levison, Steven W ^a,b  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CYTOKINE; CYTOTOXIN; INTERLEUKIN 1BETA; MESSENGER RNA; MINOCYCLINE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOASSAY; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DIABETES MELLITUS; DIABETIC RETINOPATHY; DISEASE COURSE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MEDIATOR RELEASE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA NERVE CELL; VISUAL IMPAIRMENT;

ANIMALS; CASPASE 3; CASPASES; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; DISEASE MODELS, ANIMAL; INFLAMMATION; MICROGLIA; MINOCYCLINE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 17844392902     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.54.5.1559     Document Type: Article

References (45)

1. Miyamoto K, Khosrof S, Bursell SE, Rohan R, Murata T, Clermont AC, Aiello LP, Ogura Y, Adamis AP: Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci U S A 96:10836-10841, 1999
2. Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP: Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol 158:147-152, 2001
3. Funatsu H, Yamashita H, Noma H, Mimura T, Yamashita T, Hori S: Increased levels of vascular endothelial growth factor and interleukin-6 in the aqueous humor of diabetics with macular edema. Am J Ophthalmol 133:70-77, 2002
4. Giulian D, Li J, Bartel S, Broker J, Li X, Kirkpatrick JB: Cell surface morphology identifies microglia as a distinct class of mononuclear phagocyte. J Neurosci 15:7712-7726, 1995
5. Streit WJ, Graeber MB, Kreutzberg GW: Peripheral nerve lesion produces increased levels of major histocompatibility complex antigens in the central nervous system. J Neuroimmunol 21:117-123, 1989
6. Streit WJ, Kreutzberg GW: Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J Comp Neurol 268:248-263, 1988
7. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J: Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580-2588, 2001
8. Levison SW, McCarthy KD: Astroglia in culture. In Culturing Nerve Cells. 1st ed. Banker GA, Goslin K, Eds. Cambridge, MA, MIT Press, 1991, p. 309-336
9. Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45, 2001
10. Romanko MJ, Rothstein RP, Levison SW: Neural stem cells in the subventricular zone are resilient to hypoxia/ischemia whereas progenitors are vulnerable. J Cereb Blood Flow Metab 24:814-825, 2004
11. Rungger-Brandle E, Dosso AA, Leuenberger PM: Glial reactivity, an early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci 41:1971-1980, 2000
12. Zeng XX, Ng YK, Ling EA: Neuronal and microglial response in the retina of streptozotocin-induced diabetic rats. Vis Neurosci 17:463-471, 2000
13. Thornalley PJ: Cell activation by glycated proteins: AGE receptors, receptor recognition factors and functional classification of AGEs. Cell Mol Biol (Noisy-le-grand) 44:1013-1023, 1998
14. Griffin WS, Sheng JG, Royston MC, Gentleman SM, McKenzie JE, Graham DI, Roberts GW, Mrak RE: Glial-neuronal interactions in Alzheimer's disease: the potential role of a "cytokine cycle" in disease progression. Brain Pathol 8:65-72, 1998
15. Gebicke-Haerter PJ, Lieb K, Illes P, Berger M: [Microglia: mechanisms of activation and significance in pathogenesis of neuropsychiatric illnesses]. Nervenarzt 69:752-762, 1998
16. Prineas JW, Kwon EE, Cho ES, Sharer LR: Continual breakdown and regeneration of myelin in progressive multiple sclerosis plaques. Ann N Y Acad Sci 436:11-32, 1984
17. D'Amelio FE, Smith ME, Eng LF: Sequence of tissue responses in the early stages of experimental allergic encephalomyelitis (EAE): immunohistochemical, light microscopic, and ultrastructural observations in the spinal cord. Glia 3:229-240, 1990
18. Kolson DL, Lavi E, Gonzalez-Scarano F: The effects of human immunodeficiency virus in the central nervous system. Adv Virus Res 50:1-47, 1998
19. Funatsu H, Yamashita H, Noma H, Mimura T, Yamashita T, Hori S: Increased levels of vascular endothelial growth factor and interleukin-6 in the aqueous humor of diabetics with macular edema. Am J Ophthalmol 133:70-77, 2002
20. Armstrong D, Augustin AJ, Spengler R, Al-Jada A, Nickola T, Grus F, Koch F: Detection of vascular endothelial growth factor and tumor necrosis factor alpha in epiretinal membranes of proliferative diabetic retinopathy, proliferative vitreoretinopathy and macular pucker. Ophthalmologica 212:410-414, 1998
21. Limb GA, Webster L, Soomro H, Janikoun S, Shilling J: Platelet expression of tumour necrosis factor-alpha (TNF-alpha), TNF- receptors and intercellular adhesion molecule-1 (ICAM-1) in patients with proliferative diabetic retinopathy. Clin Exp Immunol 118:213-218, 1999
22. Barouch FC, Miyamoto K, Allport JR, Fujita K, Bursell SE, Aiello LP, Luscinskas FW, Adamis AP: Integrin-mediated neutrophil adhesion and retinal leukostasis in diabetes. Invest Ophthalmol Vis Sci 41:1153-1158, 2000
23. Carmo A, Cunha-Vaz JG, Carvalho AP, Lopes MC: Effect of cyclosporin-A on the blood-retinal barrier permeability in streptozotocin-induced diabetes. Mediators Inflamm 9:243-248, 2000
24. Joussen AM, Poulaki V, Mitsiades N, Kirchhof B, Koizumi K, Dohmen S, Adamis AP: Nonsteroidal anti-inflammatory drugs prevent early diabetic retinopathy via TNF-alpha suppression. FASEB J 16:438-440, 2002
25. Suzumura A, Sawada M, Yamamoto H, Marunouchi T: Effects of colony stimulating factors on isolated microglia in vitro. J Neuroimmunol 30:111-120, 1990
26. Loughlin AJ, Woodroofe MN, Cuzner ML: Regulation of Fc receptor and major histocompatibility complex antigen expression on isolated rat microglia by tumour necrosis factor, interleukin-1 and lipopolysaccharide: effects on interferon-gamma induced activation. Immunology 75:170-175, 1992
27. Basu A, Krady JK, Enterline JR, Levison SW: Transforming growth factor beta1 prevents IL-1beta-induced microglial activation, whereas TNF-alpha- and IL-6-stimulated activation are not antagonized. Glia 40:109-120, 2002
28. Patrizio M: Tumor necrosis factor reduces cAMP production in rat microglia. Glia 48:241-249, 2004
29. Romeo G, Liu WH, Asnaghi V, Kern TS, Lorenzi M: Activation of nuclear factor-kappaB induced by diabetes and high glucose regulates a proapoptotic program in retinal pericytes. Diabetes 51:2241-2248, 2002
30. Gehrmann J, Matsumoto Y, Kreutzberg GW: Microglia: intrinsic immuneffector cell of the brain. Brain Res Brain Res Rev 20:269-287, 1995
31. Colton CA, Gilbert DL: Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett 223:284-288, 1987
32. Banati RB, Rothe G, Valet G, Kreutzberg GW: Detection of lysosomal cysteine proteinases in microglia: flow cytometric measurement and histochemical localization of cathepsin B and L. Glia 7:183-191, 1993
33. Adamis AP, D'Amato RJ: Shedding light on diabetic retinopathy. Ophthalmology 102:1127-1128, 1995
34. Shen WH, Zhou JH, Broussard SR, Johnson RW, Dantzer R, Kelley KW: Tumor necrosis factor alpha inhibits insulin-like growth factor I-induced hematopoietic cell survival and proliferation. Endocrinology 145:3101-3105, 2004
35. Venters HD, Tang Q, Liu Q, VanHoy RW, Dantzer R, Kelley KW: A new mechanism of neurodegeneration: a proinflammatory cytokine inhibits receptor signaling by a survival peptide. Proc Natl Acad Sci U S A 96:9879-9884, 1999
36. Abu El-Asrar AM, Desmet S, Meersschaert A, Dralands L, Missotten L, Geboes K: Expression of the inducible isoform of nitric oxide synthase in the retinas of human subjects with diabetes mellitus. Am J Ophthalmol 132:551-556, 2001
37. Elner SG, Elner VM, Jaffe GJ, Stuart A, Kunkel SL, Strieter RM: Cytokines in proliferative diabetic retinopathy and proliferative vitreoretinopathy. Curr Eye Res 14:1045-1053, 1995
38. Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, Shah ST, Pasquale LR, Thieme H, Iwamoto MA, Park JE: Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 331:1480-1487, 1994
39. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW: Neural apoptosis in the retina during experimental and human diabetes: early onset and effect of insulin. J Clin Invest 102:783-791, 1998
40. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J: Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci U S A 95:15769-15774, 1998
41. 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 96:13496-13500, 1999
42. 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 45:2753-2759, 2004
43. Friedlander RM: Apoptosis and caspases in neurodegenerative diseases. N Engl J Med 348:1365-1375, 2003
44. 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: Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 6:797-801, 2000
45. Teng YD, Choi H, Onario RC, Zhu S, Desilets FC, Lan S, Woodard EJ, Snyder EY, Eichler ME, Friedlander RM: 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, 2004