Low levels of mutant ubiquitin are degraded by the proteasome in vivo

Journal of Neuroscience Research

Volumn 88, Issue 11, 2010, Pages 2325-2337

  Van Tijn, Paula ^a   Verhage, Marian C ^a   Hobo, Barbara ^a   Van Leeuwen, Fred W ^a,b   Fischer, David F ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Mutant ubiquitin; Neurodegenerative disease; Proteasome inhibitor; Transgenic mouse model; Ubiquitin proteasome system

Indexed keywords

LACTACYSTIN; MG262; POLYGLUTAMINE; PROTEASOME; PROTEASOME INHIBITOR; UBIQUITIN; UNCLASSIFIED DRUG; ACETYLCYSTEINE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; MESSENGER RNA; SERINE PROTEINASE INHIBITOR; UBB PROTEIN, MOUSE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME INHIBITION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN METABOLISM; TRANSGENIC MOUSE; AGING; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; CELL LINE; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; RADIOIMMUNOASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ACETYLCYSTEINE; AGING; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; CELL LINE; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; PROTEASOME ENDOPEPTIDASE COMPLEX; RADIOIMMUNOASSAY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE PROTEINASE INHIBITORS; UBIQUITIN;

EID: 77955353515     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22396     Document Type: Article

References (53)

1. Adams J. 2004. The development of proteasome inhibitors as anticancer drugs. Cancer Cell 5:417-421. (Pubitemid 38610244)
2. Adams J, Behnke M, Chen S, Cruickshank AA, Dick LR, Grenier L, Klunder JM, Ma YT, Plamondon L, Stein RL. 1998. Potent and selective inhibitors of the proteasome: dipeptidyl boronic acids. Bioorg Med Chem Lett 8:333-338.
3. Brown IR, Rush S, Ivy GO. 1989. Induction of a heat shock gene at the site of tissue injury in the rat brain. Neuron 2:1559-1564.
4. Carrard G, Bulteau AL, Petropoulos I, Friguet B. 2002. Impairment of proteasome structure and function in aging. Int J Biochem Cell Biol 34:1461-1474. (Pubitemid 35245402)
5. Chen M, Clark RS, Kochanek PM, Chen J, Schiding JK, Stetler RA, Simon RP, Graham SH. 1998. 72-kDa heat shock protein and mRNA expression after controlled cortical impact injury with hypoxemia in rats. J Neurotrauma 15:171-181.
6. Choi T, Huang M, Gorman C, Jaenisch R. 1991. A generic intron increases gene expression in transgenic mice. Mol Cell Biol 11:3070-3074. (Pubitemid 21895693)
7. Ciechanover A, Brundin P. 2003. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40:427-446. (Pubitemid 37244106)
8. Cook C, Gass J, Dunmore J, Tong J, Taylor J, Eriksen J, McGowan E, Lewis J, Johnston J, Petrucelli L. 2009. Aging is not associated with proteasome impairment in UPS reporter mice. PLoS One 4:e5888.
9. De Pril R, Fischer DF, Maat-Schieman ML, Hobo B, De Vos RA, Brunt ER, Hol EM, Roos RA, Van Leeuwen FW. 2004. Accumulation of aberrant ubiquitin induces aggregate formation and cell death in polyglutamine diseases. Hum Mol Genet 13:1803-1813.
10. De Vrij FM, Sluijs JA, Gregori L, Fischer DF, Hermens WT, Goldgaber D, Verhaagen J, Van Leeuwen FW, Hol EM. 2001. Mutant ubiquitin expressed in Alzheimer's disease causes neuronal death. FASEB J 15:2680-2688.
11. Dick LR, Cruikshank AA, Grenier L, Melandri FD, Nunes SL, Stein RL. 1996. Mechanistic studies on the inactivation of the proteasome by lactacystin: a central role for clasto-lactacystin beta-lactone. J Biol Chem 271:7273-7276. (Pubitemid 26111059)
12. Fenteany G, Standaert RF, Lane WS, Choi S, Corey EJ, Schreiber SL. 1995. Inhibition of proteasome activities and subunit-specific aminoterminal threonine modification by lactacystin. Science 268:726-731.
13. Finley D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78:477-513.
14. Fischer DF, De Vos RA, Van Dijk R, De Vrij FM, Proper EA, Sonnemans MA, Verhage MC, Sluijs JA, Hobo B, Zouambia M, Steur EN, Kamphorst W, Hol EM, Van Leeuwen FW. 2003. Disease-specific accumulation of mutant ubiquitin as a marker for proteasomal dysfunction in the brain. FASEB J 17:2014-2024.
15. Fischer DF, van Dijk R, van Tijn P, Hobo B, Verhage MC, van der Schors RC, Li KW, van Minnen J, Hol EM, van Leeuwen FW. 2009. Long-term proteasome dysfunction in the mouse brain by expression of aberrant ubiquitin. Neurobiol Aging 30:847-863.
16. Fornai F, Lenzi P, Gesi M, Ferrucci M, Lazzeri G, Busceti CL, Ruffoli R, Soldani P, Ruggieri S, Alessandri MG, Paparelli A. 2003. Fine structure and biochemical mechanisms underlying nigrostriatal inclusions and cell death after proteasome inhibition. J Neurosci 23:8955-8966.
17. Fratta P, Engel WK, Van Leeuwen FW, Hol EM, Vattemi G, Askanas V. 2004. Mutant ubiquitin UBB11 is accumulated in sporadic inclusion-body myositis muscle fibers. Neurology 63:1114-1117.
18. Glickman MH, Ciechanover A. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82:373-428. (Pubitemid 34654457)
19. Groll M, Huber R. 2004. Inhibitors of the eukaryotic 20S proteasome core particle: a structural approach. Biochim Biophys Acta 1695:33-44.
20. Hayter JR, Doherty MK, Whitehead C, McCormack H, Gaskell SJ, Beynon RJ. 2005. The subunit structure and dynamics of the 20S proteasome in chicken skeletal muscle. Mol Cell Proteomics 4:1370-1381.
21. +1) is a secretory protein, and the level of APP11 in cerebrospinal fluid is linked to Alzheimer pathology. J Biol Chem 278:39637-39643.
22. Hol EM, van Leeuwen FW, Fischer DF. 2005. The proteasome in Alzheimer's disease and Parkinson's disease: lessons from ubiquitin B11. Trends Mol Med 11:488-495.
23. Hope AD, de Silva R, Fischer DF, Hol EM, van Leeuwen FW, Lees AJ. 2003. Alzheimer's associated variant ubiquitin causes inhibition of the 26S proteasome and chaperone expression. J Neurochem 86:394-404.
24. Iwatsubo T, Yamaguchi H, Fujimuro M, Yokosawa H, Ihara Y, Trojanowski JQ, Lee VM. 1996. Purification and characterization of Lewy bodies from the brains of patients with diffuse Lewy body disease. Am J Pathol 148:1517-1529.
25. Jablonska B, Gierdalski M, Kublik A, Skangiel-Kramska J, Kossut M. 1993. Effects of implantation of Alzet 1007D osmotic minipumps upon 2-deoxyglucose uptake in the cerebral cortex of mice. Acta Neurobiol Exp 53:577-580. (Pubitemid 24062154)
26. Keller JN, Huang FF, Markesbery WR. 2000. Decreased levels of proteasome activity and proteasome expression in aging spinal cord. Neuroscience 98:149-156.
27. Keller JN, Gee J, Ding Q. 2002. The proteasome in brain aging. Ageing Res Rev 1:279-293.
28. Kisselev AF, Goldberg AL. 2001. Proteasome inhibitors: from research tools to drug candidates. Chem Biol 8:739-758.
29. Korolchuk VI, Menzies FM, Rubinsztein DC. 2009. Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett (in press).
30. Lam YA, Pickart CM, Alban A, Landon M, Jamieson C, Ramage R, Mayer RJ, Layfield R. 2000. Inhibition of the ubiquitin-proteasome system in Alzheimer's disease. Proc Natl Acad Sci U S A 97:9902-9906.
31. Lee PD, Sladek R, Greenwood CM, Hudson TJ. 2002. Control genes and variability: absence of ubiquitous reference transcripts in diverse mammalian expression studies. Genome Res 12:292-297.
32. Lindsten K, de Vrij FM, Verhoef LG, Fischer DF, van Leeuwen FW, Hol EM, Masucci MG, Dantuma NP. 2002. Mutant ubiquitin found in neurodegenerative disorders is a ubiquitin fusion degradation substrate that blocks proteasomal degradation. J Cell Biol 157:417-427.
33. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER. 1996. Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683. (Pubitemid 26414891)
34. McNaught KS, Mytilineou C, Jnobaptiste R, Yabut J, Shashidharan P, Jennert P, Olanow CW. 2002. Impairment of the ubiquitin-proteasome system causes dopaminergic cell death and inclusion body formation in ventral mesencephalic cultures. J Neurochem 81:301-306.
35. McPhaul LW, Wang J, Hol EM, Sonnemans MA, Riley N, Nguyen V, Yuan QX, Lue YH, Van Leeuwen FW, French SW. 2002. Molecular misreading of the ubiquitin B gene and hepatic mallory body formation. Gastroenterology 122:1878-1885.
36. Mukhopadhyay D, Riezman H. 2007. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315:201-205. (Pubitemid 46166358)
37. Nicklas W, Baneux P, Boot R, Decelle T, Deeny AA, Fumanelli M, Illgen-Wilcke B. 2002. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab Anim 36:20-42.
38. Pasquini LA, Besio Moreno M, Adamo AM, Pasquini JM, Soto EF. 2000. Lactacystin, a specific inhibitor of the proteasome, induces apoptosis and activates caspase-3 in cultured cerebellar granule cells. J Neurosci Res 59:601-611.
39. Paxinos G, Franklin KBJ. 2001. The mouse brain in stereotaxic coordinates. San Diego, CA: Academic Press.
40. Pickart CM. 2004. Back to the future with ubiquitin. Cell 116:181-190.
41. Qian SB, McDonough H, Boellmann F, Cyr DM, Patterson C. 2006. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440:551-555.
42. Qiu JH, Asai A, Chi S, Saito N, Hamada H, Kirino T. 2000. Proteasome inhibitors induce cytochrome c-caspase-3-like protease-mediated apoptosis in cultured cortical neurons. J Neurosci 20:259-265.
43. Sternberger LA, Hardy PH Jr, Cuculis JJ, Meyer HG. 1970. The unlabeled antibody enzyme method of immunohistochemistry: preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem 18:315-333.
44. Tan Z, Sun X, Hou FS, Oh HW, Hilgenberg LG, Hol EM, van Leeuwen FW, Smith MA, O'Dowd DK, Schreiber SS. 2007. Mutant ubiquitin found in Alzheimer's disease causes neuritic beading of mitochondria in association with neuronal degeneration. Cell Death Differ 14:1721-1732.
45. van Leeuwen FW, de Kleijn DP, van den Hurk HH, Neubauer A, Sonnemans MA, Sluijs JA, Koycu S, Ramdjielal RD, Salehi A, Martens GJ, Grosveld FG, Peter J, Burbach H, Hol EM. 1998. Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients. Science 279:242-247.
46. van Leeuwen FW, van Tijn P, Sonnemans MA, Hobo B, Mann DM, Van Broeckhoven C, Kumar-Singh S, Cras P, Leuba G, Savioz A, Maat-Schieman ML, Yamaguchi H, Kros JM, Kamphorst W, Hol EM, de Vos RA, Fischer DF. 2006. Frameshift proteins in autosomal dominant forms of Alzheimer disease and other tauopathies. Neurology 66:S86-S92.
47. van Tijn P, de Vrij FM, Schuurman KG, Dantuma NP, Fischer DF, van Leeuwen FW, Hol EM. 2007. Dose-dependent inhibition of proteasome activity by a mutant ubiquitin associated with neurodegenerative disease. J Cell Sci 120:1615-1623. (Pubitemid 46831791)
48. van Tijn P, Hol EM, van Leeuwen FW, Fischer DF. 2008. The neuronal ubiquitin-proteasome system: murine models and their neurological phenotype. Prog Neurobiol 85:176-193.
49. Warrington JA, Nair A, Mahadevappa M, Tsyganskaya M. 2000. Comparison of human adult and fetal expression and identification of 535 housekeeping/ maintenance genes. Physiol Genomics 2:143-147.
50. Welchman RL, Gordon C, Mayer RJ. 2005. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat Rev Mol Cell Biol 6:599-609.
51. Yew EH, Cheung NS, Choy MS, Qi RZ, Lee AY, Peng ZF, Melendez AJ, Manikandan J, Koay ES, Chiu LL, Ng WL, Whiteman M, Kandiah J, Halliwell B. 2005. Proteasome inhibition by lactacystin in primary neuronal cells induces both potentially neuroprotective and pro-apoptotic transcriptional responses: a microarray analysis. J Neurochem 94:943-956.
52. Zavrski I, Naujokat C, Niemoller K, Jakob C, Heider U, Langelotz C, Fleissner C, Eucker J, Possinger K, Sezer O. 2003. Proteasome inhibitors induce growth inhibition and apoptosis in myeloma cell lines and in human bone marrow myeloma cells irrespective of chromosome 13 deletion. J Cancer Res Clin Oncol 129:383-391.
53. Zeng BY, Medhurst AD, Jackson M, Rose S, Jenner P. 2005. Proteasomal activity in brain differs between species and brain regions and changes with age. Mech Ageing Dev 126:760-766. (Pubitemid 40693300)