Minocycline inhibits the production of the precursor form of nerve growth factor by retinal microglial cells

doi:10.3969/j.issn.1673-5374.2013.04.004

Abstract

Abstract:

A rat model of acute ocular hypertension was established by enhancing the perfusion of balanced salt solution in the anterior chamber of the right eye. Minocycline (90 mg/kg) was administered intraperitoneally into rats immediately after the operation for 3 consecutive days. Immunofluorescence, western blot assay and PCR detection revealed that the expression of the precursor form of nerve growth factor, nerve growth factor and the p75 neurotrophin receptor, and the mRNA expression of nerve growth factor and the p75 neurotrophin receptor, increased after acute ocular hypertension. The number of double-labeled CD11B- and precursor form of nerve growth factor-positive cells, glial fibrillary acidic protein- and p75 neurotrophin receptor-positive cells, glial fibrillary acidic protein- and caspase-3-positive cells in the retina markedly increased after acute ocular hypertension. The above-described expression decreased after minocycline treatment. These results suggested that minocycline inhibited the increased expression of the precursor form of nerve growth factor in microglia, the p75 neurotrophin receptor in astroglia, and protected cells from apoptosis.

Key words: neural regeneration, biological factor, precursor form of nerve growth factor, p75 neurotrophin receptor, minocycline, apoptosis, nerve growth factor, acute ocular hypertension, retina, photographs-containing paper, neuroregeneration

Xiaochun Yang, Xuanchu Duan. Minocycline inhibits the production of the precursor form of nerve growth factor by retinal microglial cells[J]. Neural Regeneration Research, 2013, 8(4): 320-327.

References

[1] Almasieh M, Zhou Y, Kelly ME, et al. Structural and functional neuroprotection in glaucoma: role of galantamine-mediated activation of muscarinic acetylcholine receptors. Cell Death Dis. 2010;1:e27.

[2] Zhang S, Wang H, Lu Q, et al. Detection of early neuron degeneration and accompanying glial responses in the visual pathway in a rat model of acute intraocular hypertension. Brain Res. 2009;1303:131-143.

[3] Lam D, Jim J, To E, et al. Astrocyte and microglial activation in the lateral geniculate nucleus and visual cortex of glaucomatous and optic nerve transected primates. Mol Vis. 2009;15:2217-2229.

[4] Balaratnasingam C, Morgan WH, Bass L, et al. Elevated pressure induced astrocyte damage in the optic nerve. Brain Res. 2008;1244:142-154.

[5] Hernandez MR, Miao H, Lukas T. Astrocytes in glaucomatous optic neuropathy. Prog Brain Res. 2008; 173:353-373.

[6] Wang L, Cioffi GA, Cull G, et al. Immunohistologic evidence for retinal glial cell changes in human glaucoma. Invest Ophthalmol Vis Sci. 2002;43(4):1088-1094.

[7] Naskar R, Wissing M, Thanos S. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest Ophthalmol Vis Sci. 2002;43(9):2962-2968.

[8] Ebneter A, Casson RJ, Wood JP, et al. Microglial activation in the visual pathway in experimental glaucoma: spatiotemporal characterization and correlation with axonal injury. Invest Ophthalmol Vis Sci. 2010;51(12): 6448-6460.

[9] Wirenfeldt M, Babcock AA, Vinters HV. Microglia - insights into immune system structure, function, and reactivity in the central nervous system. Histol Histopathol. 2011; 26(4):519-530.

[10] Iwama S, Sugimura Y, Suzuki H, et al. Time-dependent changes in proinflammatory and neurotrophic responses of microglia and astrocytes in a rat model of osmotic demyelination syndrome. Glia. 2011;59(3):452-462.

[11] Fahnestock M, Michalski B, Xu B, et al. The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol Cell Neurosci. 2001;18(2):210-220.

[12] Davidson NO, Powell LM, Wallis SC, et al. Thyroid hormone modulates the introduction of a stop codon in rat liver apolipoprotein B messenger RNA. J Biol Chem. 1988; 263(27):13482-13485.

[13] Al-Gayyar MM, Matragoon S, Pillai BA, et al. Epicatechin blocks pro-nerve growth factor (proNGF)-mediated retinal neurodegeneration via inhibition of p75 neurotrophin receptor expression in a rat model of diabetes [corrected]. Diabetologia. 2011;54(3):669-680.

[14] Wang T, Liu YY, Wang X, et al. Protective effects of octacosanol on 6-hydroxydopamine-induced Parkinsonism in rats via regulation of ProNGF and NGF signaling. Acta Pharmacol Sin. 2010;31(7):765-774.

[15] Zhang J, Brodie C, Li Y, et al. Bone marrow stromal cell therapy reduces proNGF and p75 expression in mice with experimental autoimmune encephalomyelitis. J Neurol Sci. 2009;279(1-2):30-38.

[16] Rogers ML, Bailey S, Matusica D, et al. ProNGF mediates death of Natural Killer cells through activation of the p75NTR-sortilin complex. J Neuroimmunol. 2010;226(1-2): 93-103.

[17] Song W, Volosin M, Cragnolini AB, et al. ProNGF induces PTEN via p75NTR to suppress Trk-mediated survival signaling in brain neurons. J Neurosci. 2010;30(46): 15608-15615.

[18] Xu F, Wei Y, Lu Q, et al. Immunohistochemical localization of sortilin and p75(NTR) in normal and ischemic rat retina. Neurosci Lett. 2009;454(1):81-85.

[19] Clewes O, Fahey MS, Tyler SJ, et al. Human ProNGF: biological effects and binding profiles at TrkA, P75NTR and sortilin. J Neurochem. 2008;107(4):1124-1135.

[20] Pang Y, Campbell L, Zheng B, et al. Lipopolysaccharide- activated microglia induce death of oligodendrocyte progenitor cells and impede their development. Neuroscience. 2010;166(2):464-475.

[21] Yang L, Kim JH, Kovacs KD, et al. Minocycline inhibition of photoreceptor degeneration. Arch Ophthalmol. 2009; 127(11):1475-1480.

[22] Tang CM, Hwang CS, Chen SD, et al. Neuroprotective mechanisms of minocycline against sphingomyelinase/ ceramide toxicity: Roles of Bcl-2 and thioredoxin. Free Radic Biol Med. 2011;50(6):710-721.

[23] Bosco A, Inman DM, Steele MR, 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(4): 1437-1446.

[24] Yune TY, Lee JY, Jung GY, et al. Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J Neurosci. 2007;27(29):7751-7761.

[25] Balaratnasingam C, Morgan WH, Bass L, et al. Elevated pressure induced astrocyte damage in the optic nerve. Brain Res. 2008;1244:142-154.

[26] Lee R, Kermani P, Teng KK, et al. Regulation of cell survival by secreted proneurotrophins. Science. 2001; 294(5548):1945-1948.

[27] Masoudi R, Ioannou MS, Coughlin MD, et al. Biological activity of nerve growth factor precursor is dependent upon relative levels of its receptors. J Biol Chem. 2009; 284(27):18424-18433.

[28] Al-Shawi R, Hafner A, Olsen J, et al. Neurotoxic and neurotrophic roles of proNGF and the receptor sortilin in the adult and ageing nervous system. Eur J Neurosci. 2008;27(8):2103-2114.

[29] Wei Y, Wang N, Lu Q, et al. Enhanced protein expressions of sortilin and p75NTR in retina of rat following elevated intraocular pressure-induced retinal ischemia. Neurosci Lett. 2007;429(2-3):169-174.

[30] Suter U, Heymach JV Jr, Shooter EM. Two conserved domains in the NGF propeptide are necessary and sufficient for the biosynthesis of correctly processed and biologically active NGF. EMBO J. 1991;10(9):2395-2400.

[31] Bergami M, Santi S, Formaggio E, et al. Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J Cell Biol. 2008;183(2):213-221.

[32] Kernt M, Neubauer AS, Eibl KH, et al. Minocycline is cytoprotective in human trabecular meshwork cells and optic nerve head astrocytes by increasing expression of XIAP, survivin, and Bcl-2. Clin Ophthalmol. 2010;4: 591-604.

[33] Bosco A, Steele MR, Vetter ML. Early microglia activation in a mouse model of chronic glaucoma. J Comp Neurol. 2011;519(4):599-620.

[34] Peng S, Wuu J, Mufson EJ, et al. Increased proNGF levels in subjects with mild cognitive impairment and mild Alzheimer disease. J Neuropathol Exp Neurol. 2004;63(6): 641-649.

[35] Festoff BW, Ameenuddin S, Arnold PM, et al. Minocycline neuroprotects, reduces microgliosis, and inhibits caspase protease expression early after spinal cord injury. J Neurochem. 2006;97(5):1314-1326.

[36] Büchi ER, Suivaizdis I, Fu J. Pressure-induced retinal ischemia in rats: an experimental model for quantitative study. Ophthalmologica. 1991;203(3):138-147.

[37] Kaur S, Mishra MN, Tripathi AK. Regulation of expression and biochemical characterization of a beta-class carbonic anhydrase from the plant growth-promoting rhizobacterium, Azospirillum brasilense Sp7. FEMS Microbiol Lett. 2009;299(2):149-158.

[38] Ale MT, Maruyama H, Tamauchi H, et al. Fucose- containing sulfated polysaccharides from brown seaweeds inhibit proliferation of melanoma cells and induce apoptosis by activation of caspase-3 in vitro. Mar Drugs. 2011;9(12):2605-2621.