Reactive glia show increased immunoproteasome activity in Alzheimer's disease

Brain

Volumn 136, Issue 5, 2013, Pages 1415-1431

  Orre, Marie ^a   Kamphuis, Willem ^a   Dooves, Stephanie ^a   Kooijman, Lieneke ^a   Chan, Elena T ^b   Kirk, Christopher J ^b   Dimayuga Smith, Vanessa ^a   Koot, Sanne ^a   Mamber, Carlyn ^a   Jansen, Anne H ^a   Ovaa, Huib ^c   Hol, Elly M ^a,d  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b ONYX PHARMACEUTICALS   (United States)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Alzheimer's disease; astrocytes; immunoproteasome; microglia; neuroinflammation

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; COMPLEMENTARY DNA; IMMUNOPROTEASOME; LIPOPOLYSACCHARIDE; MESSENGER RNA; PROTEASOME; UBIQUITIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOMA; BRAIN HOMOGENATE; CONTROLLED STUDY; ENTORHINAL CORTEX; EX VIVO STUDY; GENE EXPRESSION; GLIA; GLIA CELL; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LASER MICRODISSECTION; MICROGLIA; MOUSE; NERVE CELL CULTURE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

EID: 84877306949     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt083     Document Type: Article

References (66)

1. Almeida CG, Takahashi RH, Gouras GK. Beta-amyloid accumulation impairs multivesicular body sorting by inhibiting the ubiquitin-proteasome system. J Neurosci 2006; 26: 4277-4288.
2. Aso E, Lomoio S, Lopez-Gonzalez I, Joda L, Carmona M, Fernandez-Yague N, et al. Amyloid generation and dysfunctional immunoproteasome activation with disease progression in animal model of familial Alzheimer disease. Brain Pathol 2011; 22: 636-53.
3. Basler M, Dajee M, Moll C, Groettrup M, Kirk CJ. Prevention of experimental colitis by a selective inhibitor of the immunoproteasome. J Immunol 2010; 185: 634-41.
4. Beach TG, Walker R, McGeer EG. Patterns of gliosis in Alzheimer's disease and aging cerebrum. Glia 1989; 2: 420-36.
5. Berkers CR, Van Leeuwen FWB, Groothuis TA, Peperzak V, Van Tilburg EW, Borst J, et al. Profiling proteasome activity in tissue with fluorescent probes. Mol Pharm 2007; 4: 739-48.
6. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991; 82: 239-59.
7. Cameron B, Tse W, Lamb R, Li X, Lamb BT, Landreth GE. Loss of interleukin receptor-associated kinase 4 signaling suppresses amyloid pathology and alters microglial phenotype in a mouse model of Alzheimer's disease. J Neurosci 2012; 32: 15112-23.
8. Chafekar SM, Hoozemans JJ, Zwart R, Baas F, Scheper W. Abeta 1-42 induces mild endoplasmic reticulum stress in an aggregation state-dependent manner. Antioxid Redox Signal 2007; 9: 2245-54.
9. Corona AW, Fenn AM, Godbout JP. Cognitive and behavioral consequences of impaired immunoregulation in aging. J Neuroimmune Pharmacol 2011; 7: 7-23.
10. Delgado M, Varela N, Gonzalez-Rey E. Vasoactive intestinal peptide protects against beta-amyloid-induced neurodegeneration by inhibiting microglia activation at multiple levels. Glia 2008; 56: 1091-103.
11. DiCarlo G, Wilcock D, Henderson D, Gordon M, Morgan D. Intrahippocampal LPS injections reduce Ab load in APP + PS1 transgenic mice. Neurobiol Aging 2001; 22: 1007-012.
12. Durrenberger PF, Fernando FS, Magliozzi R, Kashefi SN, Bonnert TP, Ferrer I, et al. Selection of novel reference genes for use in the human central nervous system: a BrainNet Europe Study. Acta Neuropathol 2012; 124: 893-903.
13. Fergusson J, Landon M, Lowe J, Dawson SP, Layfield R, Hanger DP, et al. Pathological lesions of Alzheimer's disease and dementia with Lewy bodies brains exhibit immunoreactivity to an ATPase that is a regulatory subunit of the 26S proteasome. Neurosci Lett 1996; 219: 167-70.
14. Ferrington DA, Hussong SA, Roehrich H, Kapphahn RJ, Kavanaugh SM, Heuss ND, et al. Immunoproteasome responds to injury in the retina and brain. J Neurochem 2008; 106: 158-69.
15. French BA, Oliva J, Bardag-Gorce F, French SW. The immunoproteasome in steatohepatitis: its role in Mallory-Denk body formation. Exp Mol Pathol 2011; 90: 252-6.
16. Frü h K, Gossen M, Wang K, Bujard H, Peterson PA, Yang Y. Displacement of housekeeping proteasome subunits by MHC-encoded LMPs: a newly discovered mechanism for modulating the multicatalytic proteinase complex. EMBO J 1994; 13: 3236-44.
17. Gaczynska M, Rock KL, Goldberg AL. Gamma-interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. Nature 1993; 365: 264-7.
18. Goldberg AL. Protein degradation and protection against misfolded or damaged proteins. Nature 2003; 426: 895-9.
19. Groettrup M, Kirk CJ, Basler M. Proteasomes in immune cells: more than peptide producers? Nat Rev Immunol 2010; 10: 73-8.
20. Heneka MT, O'Banion MK, Terwel D, Kummer MP. Neuroinflammatory processes in Alzheimer's disease. J Neural Transm 2010; 117: 919-47.
21. Henn A, Kirner S, Leist M. TLR2 Hypersensitivity of astrocytes as functional consequence of previous inflammatory episodes. J Immunol 2011; 186: 3237-47.
22. Hensley K. Neuroinflammation in Alzheimer's disease: mechanisms, pathologic consequences, and potential for therapeutic manipulation. J Alzheimers Dis 2010; 21: 1-14.
23. Hensley SE, Zanker D, Dolan BP, David A, Hickman HD, Embry AC, et al. Unexpected role for the immunoproteasome subunit LMP2 in antiviral humoral and innate immune responses. J Immunol 2010; 184: 4115-22.
24. Hickman SE, Allison EK, El Khoury J. Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci 2008; 28: 8354-60.
25. Janeway CA Jr, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002; 20: 197-216.
26. Jankowsky JL, Slunt HH, Gonzales V, Jenkins NA, Copeland NG, Borchelt DR. APP processing and amyloid deposition in mice haploinsufficient for presenilin 1. Neurobiol Aging 2004; 25: 885-92.
27. Jiang Z, Georgel P, Du X, Shamel L, Sovath S, Mudd S, et al. CD14 is required for MyD88-independent LPS signaling. Nat Immunol 2005; 6: 565-70.
28. Kamphuis W, Orre M, Kooijman L, Dahmen M, Hol EM. Differential cell proliferation in the cortex of the APPswePS1dE9 Alzheimer's disease mouse model. Glia 2012; 60: 615-29.
29. Keck S, Nitsch R, Grune T, Ullrich O. Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J Neurochem 2003; 85: 115-22.
30. Keller JN, Hanni KB, Markesbery WR. Impaired proteasome function in Alzheimer's disease. J Neurochem 2000; 75: 436-9.
31. Kincaid EZ, Che JW, York I, Escobar H, Reyes-Vargas E, Delgado JC, et al. Mice completely lacking immunoproteasomes show major changes in antigen presentation. Nat Immunol 2011; 13: 129-35.
32. Kisselev AF, Goldberg AL. Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol 2005; 398: 364-78.
33. Lindsten K, Menendez-Benito V, Masucci MG, Dantuma NP. A transgenic mouse model of the ubiquitin/proteasome system. Nat Biotechnol 2003; 21: 897-902.
34. Liu S, Liu Yang, Hao W, Wolf L, Kiliaan AJ, Penke B, et al. TLR2 Is a Primary receptor for Alzheimer's amyloid b peptide to trigger neuroin-flammatory activation. J Immunol 2012; 188: 1098-107.
35. Liu Y, Walter S, Stagi M, Cherny D, Letiembre M, Schulz-Schaeffer W, et al. LPS receptor (CD14): a receptor for phagocytosis of Alzheimer's amyloid peptide. Brain 2005; 128: 1778-89.
36. Luo ZF, Qi W, Feng B, Mu J, Zeng W, Guo YH, et al. Prevention of diabetic nephropathy in rats through enhanced renal antioxidative capacity by inhibition of the proteasome. Life Sci 2011; 88: 512-20.
37. Mamber C, Kamphuis W, Haring NL, Peprah N, Middeldorp J, Hol EM. GFAP, Expression in glia of the developmental and adolescent mouse brain. PLoS One 2012; 7: e52659.
38. Middeldorp J, Kamphuis W, Sluijs JA, Achoui D, Leenaars CH, Feenstra MG, et al. Intermediate filament transcription in astrocytes is repressed by proteasome inhibition. FASEB J 2009; 23: 2710-26.
39. Mishto M, Bellavista E, Ligorio C, Textoris-Taube K, Santoro A, Giordano M, et al. 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.
40. Mishto M, Bellavista E, Santoro A, Stolzing A, Ligorio C, Nacmias B, et al. Immunoproteasome and LMP2 polymorphism in aged and Alzheimer's disease brains. Neurobiol Aging 2006; 27: 54-66.
41. Mishto M, Ligorio C, Bellavista E, Martucci M, Santoro A, Giulioni M, et al. Immunoproteasome expression is induced in mesial temporal lobe epilepsy. Biochem Biophys Res Commun 2011; 408: 65-70.
42. Muchamuel T, Basler M, Aujay MA, Suzuki E, Kalim KW, Lauer C, et al. A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nat. Med. 2009; 15: 781-7.
43. Nguyen TP, Soukup VM, Gelman BB. Persistent hijacking of brain proteasomes in HIV-associated dementia. Am J Pathol 2009; 176: 893-902.
44. Nijholt DA, De Graaf TR, Van Haastert ES, Oliveira AO, Berkers CR, Zwart R, et al. Endoplasmic reticulum stress activates autophagy but not the proteasome in neuronal cells: implications for Alzheimer's disease. Cell Death Differ 2011; 18: 1071-81.
45. Oh S, Hong HS, Hwang E, Sim HJ, Lee W, Shin SJ, et al. Amyloid peptide attenuates the proteasome activity in neuronal cells. Mech Ageing Dev 2005; 126: 1292-9.
46. Palombella VJ, Rando OJ, Goldberg AL, Maniatis T. The ubiquitinproteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 1994; 78: 773-85.
47. Parlati F, Lee SJ, Aujay M, Suzuki E, Levitsky K, Lorens JB, et al. Carfilzomib can induce tumor cell death through selective inhibition of the chymotrypsin-like activity of the proteasome. Blood 2009; 114: 3439-47.
48. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol 2010; 6: 193-201.
49. Pickering AM, Koop AL, Teoh CY, Ermak G, Grune T, Davies KJ. The immunoproteasome, the 20S proteasome and the PA28alphabeta proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem J 2010; 432: 585-94.
50. Reed-Geaghan EG, Reed QW, Cramer PE, Landreth GE. Deletion of CD14 attenuates AD pathology by influencing the brain's inflammatory milieu. J Neurosci 2010; 30: 15369-73.
51. Reed-Geaghan EG, Savage JC, Hise AG, Landreth GE. CD14 and toll-like receptors 2 and 4 are required for fibrillar A{beta}-stimulated microglial activation. J Neurosci 2009; 29: 11982-92.
52. Reis J, Hassan F, Guan XQ, Shen J, Monaco JJ, Papasian CJ, et al. The immunoproteasomes regulate LPS-induced TRIF/TRAM signaling pathway in murine macrophages. Cell Biochem Biophys 2011; 60: 119-26.
53. Richard KL, Filali M, Pré fontaine P, Rivest S. Toll-like receptor 2 acts as a natural innate immune receptor to clear Amyloid b1-42 and delay the cognitive decline in a mouse model of Alzheimer's disease. J Neurosci 2008; 28: 5784-93.
54. Rodgers KJ, Dean RT. Assessment of proteasome activity in cell lysates and tissue homogenates using peptide substrates. Int J Biochem Cell Biol 2003; 35: 716-27.
55. Ruan L, Kang Z, Pei G, Le Y. Amyloid deposition and inflammation in Appswe/Ps1de9 mouse model of Alzheimer's disease. Curr Alzheimer Res 2009; 6: 531-40.
56. Schmidt N, Gonzalez E, Visekruna A, Kü hl AA, Loddenkemper C, Mollenkopf H, et al. Targeting the proteasome: partial inhibition of the proteasome by bortezomib or deletion of the immunosubunit LMP7 attenuates experimental colitis. Gut 2010; 59: 896-906.
57. Schubert D, Soucek T, Blouw B. The induction of HIF-1 reduces astrocyte activation by amyloid beta peptide. Eur J Neurosci 2009; 29: 1323-34.
58. Seifert U, Bialy LP, Ebstein F, Bech-Otschir D, Voigt A, Schroter F, et al. Immunoproteasomes preserve protein homeostasis upon interferoninduced oxidative stress. Cell 2010; 142: 613-24.
59. Selkoe DJ. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 2001; 81: 741-66.
60. Thal DR, Rü b U, Schultz C, Sassin I, Ghebremedhin E, Del Tredici K, et al. Sequence of Abeta-protein deposition in the human medial temporal lobe. J Neuropathol Exp Neurol 2000; 59: 733-48.
61. Tseng BP, Green KN, Chan JL, Blurton-Jones M, LaFerla FM. Abeta inhibits the proteasome and enhances amyloid and tau accumulation. Neurobiol Aging 2008; 29: 1607-18.
62. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, DePaepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple interval control genes. Genome Biol 2002; 3: 0034.1-0034.11.
63. Verkhratsky A, Parpura V. Recent advances in (patho)physiology of astroglia. Acta Pharmacol Sin 2010; 31: 1044-54.
64. De Vrij FM, Fischer DF, Van Leeuwen FW, Hol EM. Protein quality control in Alzheimer's disease by the ubiquitin proteasome system. Prog Neurobiol 2004; 74: 249-70.
65. Wang HM, Zhao YX, Zhang S, Liu GD, Kang WY, Tang HD, et al. PPARgamma agonist curcumin reduces the amyloid-beta-stimulated inflammatory responses in primary astrocytes. J Alzheimers Dis 2010; 20: 1189-99.
66. Wang Q, Ishikawa T, Michiue T, Zhu BL, Guan DW, Maeda H. Stability of endogenous reference genes in postmortem human brains for normalization of quantitative real-time PCR data: comprehensive evaluation using geNorm, NormFinder, and BestKeeper. Int J Legal Med 2012; 126: 943-52.