Lipopolysaccharide-induced neuroinflammation leads to the accumulation of ubiquitinated proteins and increases susceptibility to neurodegeneration induced by proteasome inhibition in rat hippocampus

Journal of Neuroinflammation

Diego Ruano⁵  Rosa M Ríos²  Angélica Castaño⁵  Javier Vitorica⁵  Antonia Gutiérrez¹  Luisa García-Cuervo⁴  Elena Gavilán⁴  María P Gavilán²  Cristina Pintado³ 

[1] Departamento de Biología Celular, Genética y Fisiología, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain;Centro Andaluz de Biología y Medicina Regenerativa (CABIMER), 41092, Sevilla, Spain;Departamento de Bioquímica y Biología Molecular, Facultad de Farmacia, Universidad de Sevilla, 41012, Sevilla, Spain;Instituto de Biomedicina de Sevilla (IBIS)-Hospital, Universitario Virgen del Rocío/Consejo Superior de Investigaciones Científicas/Universidad de Sevilla, 41013, Sevilla, Spain;Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), 41013, Sevilla, Spain

关键词: Protein accumulation;    Neuroinflammation;    Neurodegenerative diseases;    Neurodegeneration;    Immunoproteasome;   

Others  :  1212630
DOI  :  10.1186/1742-2094-9-87

 received in 2012-01-10, accepted in 2012-03-12,  发布年份 2012

【 授权许可】

   
2012 Pintado et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Ruano D, Revilla E, Gavilán MP, Vizuete ML, Pintado C, Vitorica J, Castaño A: Role of p38 and inducible nitric oxide synthase in the in vivo dopaminergic cells’ degeneration induced by inflammatory processes after lipopolysaccharide injection. Neuroscience 2006, 140:1157-1168.
• [2]Gavilán MP, Revilla E, Pintado C, Castaño A, Vizuete ML, Moreno-González I, Baglietto-Vargas D, Sánchez-Varo R, Vitorica J, Gutiérrez A, Ruano D: Molecular and cellular characterization of the age-related neuroinflammatory processes occurring in normal rat hippocampus: potential relation with the loss of somatostatin GABAergic neurons. J Neurochem 2007, 103:984-996.
• [3]Jiménez S, Baglietto-Vargas D, Caballero C, Moreno-González I, Torres M, Sanchez-Varo R, Ruano D, Vizuete M, Gutierrez A, Vitorica J: Inflammatory response in the hippocampus of PS1M146L/APP751sl mouse model of Alzheimer’s disease: age-dependent switch in the microglial phenotype from alternative to classic. J Neurosci 2008, 28:11650-11661.
• [4]Lynch MA: Age-related neuroinflammatory changes negatively impact on neuronal function. Front Aging Neurosci 2010, 1:6.
• [5]Pintado C, Revilla E, Vizuete ML, Jiménez S, García-Cuervo L, Vitorica J, Ruano D, Castaño A: Regional difference in inflammatory response to LPS-injection in the brain: role of microglia cell density. J Neuroimmunol 2011, 238:44-51.
• [6]Kiefer R, Streit WJ, Toyka KV, Kreutzberg GW, Hartung HP: Transforming growth factor-beta 1: a lesion-associated cytokine of the nervous system. Int J Dev Neurosci 1995, 13:331-339.
• [7]Imai F, Suzuki H, Oda J, Ninomiya T, Ono K, Sano H, Sawada M: Neuroprotective effect of exogenous microglia in global brain ischemia. J Cereb Blood Flow Metab 2007, 27:488-500.
• [8]Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, Bluethmann H, Faergeman NJ, Meldgaard M, Deierborg T, Finsen B: Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 2009, 29:1319-1330.
• [9]Kraft AD, Harry GJ: Features of microglia and neuroinflammation relevant to environmental exposure and neurotoxicity. Int J Environ Res Public Health 2011, 8:2980-3018.
• [10]Harry GJ, Kraft AD: Neuroinflammation and microglia: considerations and approaches for neurotoxicity assessment. Expert Opin Drug Metab Toxicol 2008, 4:1265-1277.
• [11]Bose S, Brooks P, Mason GG, Rivett AJ: gamma-Interferon decreases the level of 26 S proteasomes and changes the pattern of phosphorylation. Biochem J 2001, 15:291-297.
• [12]Rivett AJ, Bose S, Brooks P, Broadfoot KI: Regulation of proteasome complexes by gamma-interferon and phosphorylation. Biochimie 2001, 83:363-366.
• [13]Jung T, Catalgol B, Grune T: The proteasomal system. Mol Aspects Med 2009, 30:191-296.
• [14]Hochstrasser M: Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr Opin Cell Biol 1995, 7:215-223.
• [15]Rechsteiner M, Hill CP: Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell Biol 2005, 15:27-33.
• [16]Gaczynska M, Rock KL, Goldberg AL: Gamma-interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. Nature 1993, 365:264-267.
• [17]Preckel T, Fung-Leung WP, Cai Z, Vitiello A, Salter-Cid L, Winqvist O, Wolfe TG, von Herrath M, Angulo A, Ghazal P, Lee JD, Fourie AM, Wu Y, Pang J, Ngo K, Peterson PA, Früh K, Yang Y: Impaired immunoproteasome assembly and immune responses in PA28−/− mice. Science 1999, 286:2162-2165.
• [18]Kloetzel PM: Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2001, 2:179-187.
• [19]Goldberg AL: Protein degradation and protection against misfolded or damaged proteins. Nature 2003, 426:895-899.
• [20]Paz Gavilán M, Vela J, Castaño A, Ramos B, del Río JC, Vitorica J, Ruano D: Cellular environment facilitates protein accumulation in aged rat hippocampus. Neurobiol Aging 2006, 27:973-982.
• [21]Gavilán MP, Castaño A, Torres M, Portavella M, Caballero C, Jiménez S, García-Martínez A, Parrado J, Vitorica J, Ruano D: Age-related increase in the immunoproteasome content in rat hippocampus: molecular and functional aspects. J Neurochem 2009, 108:260-270.
• [22]Gavilán MP, Pintado C, Gavilán E, Jiménez S, Ríos RM, Vitorica J, Castaño A, Ruano D: Dysfunction of the unfolded protein response increases neurodegeneration in aged rat hippocampus following proteasome inhibition. Aging Cell 2009, 8:654-665.
• [23]Seifert U, Bialy LP, Ebstein F, Bech-Otschir D, Voigt A, Schröter F, Prozorovski T, Lange N, Steffen J, Rieger M, Kuckelkorn U, Aktas O, Kloetzel PM, Krüger E: Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 2010, 142:613-624.
• [24]Witt E, Zantopf D, Schmidt M, Kraft R, Kloetzel PM, Kruger E: Characterisation of the newly identified human Ump1 homologue POMP and analysis of LMP7(β5i) incorporation into 20 S proteasomes. J Mol Biol 2000, 301:1-9.
• [25]Fricke B, Heink S, Steffen J, Kloetzel PM, Krüger E: The proteasome maturation protein POMP facilitates major steps of 20 S proteasome formation at the endoplasmic reticulum. EMBO reports 2007, 8:1170-1175.
• [26]Heink S, Ludwig D, Kloetzel PM, Kruger E: IFN-gamma induced immune adaptation of the proteasome system is an accelerated and transient response. Proc Natl Acad Sci USA 2005, 102:9241-9246.
• [27]Deol P, Zaiss DMW, Monaco JJ, Sijts AJAM: Rates of processing determine the immunogenicity of immunoproteasome-generated epitopes. J Immunol 2007, 178:7557-7562.
• [28]Ebstein F, Lange N, Urban S, Seifert U, Kruger E, Kloetzel PM: Maturation of human dendritic cells is accompanied by functional remodelling of the ubiquitin-proteasome system. Int J Biochem Cell Biol 2009, 41:1205-1215.
• [29]de Graaf N, van Helden MJG, Textoris-Taube K, Chiba T, Topham DJ, Kloetzel PM, Zaiss DMW, Sijts AJAM: PA28 and the proteasome immunosubunits play a central and independent role in the production of MHC class I-binding peptides in vivo. Eur J Immunol 2011, 41:926-935.
• [30]Strehl B, Seifert U, Krüger E, Heink S, Kuckelkorn U, Kloetzel PM: Interferon-γ, the functional plasticity of the ubiquitin-proteasome system, and MHC class I antigen processing. Immunol Rev 2005, 207:19-30.
• [31]Griffin R, Nally R, Nolan Y, McCartney Y, Linden J, Lynch MA: The age-related attenuation in long-term potentiation is associated with microglial activation. J Neurochem 2006, 99:1263-1272.
• [32]Keller JN, Hanni KB, Markesbery WR: Possible involvement of proteasome inhibition in aging: implications for oxidative stress. Mech Ageing Dev 2000, 113:61-70.
• [33]Ding Q, Keller JN: Proteasomes and proteasome inhibition in the central nervous system. Free Radic Biol Med 2001, 31:574-584.
• [34]Perry VH: Contribution of systemic inflammation to chronic neurodegeneration. Acta Neuropathol 2010, 120:277-286.
• [35]Mishto M, Bellavista E, Santero A, Stolzing A, Liborio C, Nacmias B, Spazzafumo L, Chiappelli M, Licastro F, Sorbi S, Pession A, Ohm T, Grune T, Franceschi C: Immunoproteasome and LMP2 polymorphism in aged and Alzheimer’s disease brains. Neurobiol Aging 2006, 27:54-66.
• [36]Díaz-Hernández M, Hernández F, Martín-Aparicio E, Gómez-Ramos P, Morán MA, Castaño JG, Ferrer I, Avila J, Lucas JJ: Neuronal induction of the immunoproteasome in Huntington’s disease. J Neurosci 2003, 23:11653-11661.
• [37]Mishto M, Bellavista E, Liborio C, Textoris-Taube K, Santero A, Giordano M, D’Alfonso S, Listi F, Nacmias B, Cellini E, Leone M, Grimaldi LM, Fenoglio C, Esposito F, Martinelli-Boneschi F, Galimberti D, Scarpini E, Seifert U, Amato MP, Caruso C, Foschini MP, Kloetzel MP, Franceschi C: Immunoproteasome LMP2 60HH variant alters MBP epitope generation and reduces the risk to develop multiple sclerosis in Italian female population. PLoS One 2010, 5:e9287.
• [38]Mishto M, Liborio C, Bellavista E, Martucci M, Santero A, Giulioni M, Marucci G, Franceschi C: Immunoproteasome expression is induced in mesial temporal lobe epilepsy. Biochem Biophys Res Com 2011, 408:65-70.