Measurement of apolipoprotein e and amyloid β clearance rates in the mouse brain using bolus stable isotope labeling

Molecular Neurodegeneration

Volumn 7, Issue 1, 2012, Pages

  Basak, Jacob M ^a,b   Kim, Jungsu ^a,b   Pyatkivskyy, Yuriy ^a,b   Wildsmith, Kristin R ^a,b   Jiang, Hong ^a,b   Parsadanian, Maia ^a,b   Patterson, Bruce W ^a   Bateman, Randall J ^a,b   Holtzman, David M ^a,b  

^a Department of Neurology ^*  (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ABCA1; Amyloid beta; Apolipoprotein E; Kinetics; LDLR; Multiple reaction monitoring mass spectrometry; Protein turnover; Stable isotope

Indexed keywords

ABC TRANSPORTER A1; AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; LEUCINE; LOW DENSITY LIPOPROTEIN RECEPTOR; CARBON; TRACER;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ARTICLE; BRAIN; BRAIN METABOLISM; CHEMICAL REACTION; CLEARANCE; CONTROLLED STUDY; DEGENERATIVE DISEASE; ISOTOPE LABELING; MASS SPECTROMETRY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN METABOLISM; REGULATORY MECHANISM; VALIDATION PROCESS; WILD TYPE; ANIMAL; C57BL MOUSE; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; METABOLISM; METHODOLOGY; TRANSGENIC MOUSE;

MUS;

AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEINS E; BRAIN; CARBON ISOTOPES; CHROMATOGRAPHY, LIQUID; IMMUNOPRECIPITATION; ISOTOPE LABELING; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RADIOACTIVE TRACERS;

EID: 84862225603     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-7-14     Document Type: Article

References (53)

1. Mass spectrometry-based proteomics turns quantitative. Ong SE, Mann M, Nat Chem Biol 2005 1 252 262 10.1038/nchembio736 16408053
2. Protein turnover on the scale of the proteome. Doherty MK, Beynon RJ, Expert Rev Proteomics 2006 3 97 110 10.1586/14789450.3.1.97 16445354 (Pubitemid 43979395)
3. Alzheimers disease: the challenge of the second century. Holtzman DM, Morris JC, Goate AM, Sci Transl Med 2011 3 77sr71
4. Alpha-synuclein and neurodegenerative diseases. Goedert M, Nat Rev Neurosci 2001 2 492 501 10.1038/35081564 11433374 (Pubitemid 33676584)
5. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N, Science 1997 277 1990 1993 10.1126/science.277.5334. 1990 9302293 (Pubitemid 27449140)
6. Update on the neuropathological diagnosis of frontotemporal dementias. Trojanowski JQ, Dickson D, J Neuropathol Exp Neurol 2001 60 1123 1126 11764085 (Pubitemid 33117093)
7. Adapting proteostasis for disease intervention. Balch WE, Morimoto RI, Dillin A, Kelly JW, Science 2008 319 916 919 10.1126/science.1141448 18276881 (Pubitemid 351263754)
8. Decreased clearance of CNS beta-amyloid in Alzheimers disease. Mawuenyega KG, Sigurdson W, Ovod V, Munsell L, Kasten T, Morris JC, Yarasheski KE, Bateman RJ, Science 2010 330 1774 10.1126/science.1197623 21148344
9. Wolfe RR, Chinkes DL, Isotope tracers in metabolic research: principles and practice of kinetic analysis Wiley-Liss, Hoboken 2 2005
10. Mass spectrometry-based proteomics. Aebersold R, Mann M, Nature 2003 422 198 207 10.1038/nature01511 12634793 (Pubitemid 36362757)
11. Dynamics of protein turnover, a missing dimension in proteomics. Pratt JM, Petty J, Riba-Garcia I, Robertson DH, Gaskell SJ, Oliver SG, Beynon RJ, Mol Cell Proteomics 2002 1 579 591 10.1074/mcp.M200046-MCP200 12376573
12. Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. Doherty MK, Hammond DE, Clague MJ, Gaskell SJ, Beynon RJ, J Proteome Res 2009 8 104 112 10.1021/pr800641v 18954100
13. Global analysis of cellular protein translation by pulsed SILAC. Schwanhausser B, Gossen M, Dittmar G, Selbach M, Proteomics 2009 9 205 209 10.1002/pmic.200800275 19053139
14. Proteome dynamics in complex organisms: using stable isotopes to monitor individual protein turnover rates. Doherty MK, Whitehead C, McCormack H, Gaskell SJ, Beynon RJ, Proteomics 2005 5 522 533 10.1002/pmic.200400959 15627957 (Pubitemid 40262069)
15. Analysis of proteome dynamics in the mouse brain. Price JC, Guan S, Burlingame A, Prusiner SB, Ghaemmaghami S, Proc Natl Acad Sci U S A 2010 107 14508 14513 10.1073/pnas.1006551107 20699386
16. Human amyloid-beta synthesis and clearance rates as measured in cerebrospinal fluid in vivo. Bateman RJ, Munsell LY, Morris JC, Swarm R, Yarasheski KE, Holtzman DM, Nat Med 2006 12 856 861 10.1038/nm1438 16799555 (Pubitemid 44050079)
17. Stable isotope labeling tandem mass spectrometry (SILT) to quantify protein production and clearance rates. Bateman RJ, Munsell LY, Chen X, Holtzman DM, Yarasheski KE, J Am Soc Mass Spectrom 2007 18 997 1006 10.1016/j.jasms. 2007.02.009 17383190 (Pubitemid 46755574)
18. A gamma-secretase inhibitor decreases amyloid-beta production in the central nervous system. Bateman RJ, Siemers ER, Mawuenyega KG, Wen G, Browning KR, Sigurdson WC, Yarasheski KE, Friedrich SW, Demattos RB, May PC, et al. Ann Neurol 2009 66 48 54 10.1002/ana.21623 19360898
19. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Mahley RW, Science 1988 240 622 630 10.1126/science.3283935 3283935
20. The role of apolipoprotein E in Alzheimers disease. Kim J, Basak JM, Holtzman DM, Neuron 2009 63 287 303 10.1016/j.neuron.2009.06.026 19679070
21. ApoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. Deane R, Sagare A, Hamm K, Parisi M, Lane S, Finn MB, Holtzman DM, Zlokovic BV, J Clin Invest 2008 118 4002 4013 10.1172/JCI36663 19033669
22. Human apoE Isoforms Differentially Regulate Brain Amyloid-{beta} Peptide Clearance. Castellano JM, Kim J, Stewart FR, Jiang H, Demattos RB, Patterson BW, Fagan AM, Morris JC, Mawuenyega KG, Cruchaga C, et al. Sci Transl Med 2011 3 89ra57 10.1126/scitranslmed.3002156 21715678
23. Das S, Potter H: Amyloid-associated proteins alpha 1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer beta-protein into filaments. Ma J, Yee A, Brewer HB, Nature 1994 372 92 94 10.1038/372092a0 7969426
24. Apolipoprotein E is a kinetic but not a thermodynamic inhibitor of amyloid formation: implications for the pathogenesis and treatment of Alzheimer disease. Evans KC, Berger EP, Cho CG, Weisgraber KH, Lansbury PT, Proc Natl Acad Sci U S A 1995 92 763 767 10.1073/pnas.92.3.763 7846048
25. Lack of apolipoprotein E dramatically reduces amyloid beta-peptide deposition. Bales KR, Verina T, Dodel RC, Du Y, Altstiel L, Bender M, Hyslop P, Johnstone EM, Little SP, Cummins DJ, et al. Nat Genet 1997 17 263 264 10.1038/ng1197-263 9354781
26. Haploinsufficiency of human APOE reduces amyloid deposition in a mouse model of amyloid-beta amyloidosis. Kim J, Jiang H, Park S, Eltorai AE, Stewart FR, Yoon H, Basak JM, Finn MB, Holtzman DM, J Neurosci 2011 31 18007 18012 10.1523/JNEUROSCI.3773-11.2011 22159114
27. Overexpression of low-density lipoprotein receptor in the brain markedly inhibits amyloid deposition and increases extracellular A beta clearance. Kim J, Castellano JM, Jiang H, Basak JM, Parsadanian M, Pham V, Mason SM, Paul SM, Holtzman DM, Neuron 2009 64 632 644 10.1016/j.neuron.2009.11.013 20005821
28. ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocyte-secreted apoE. Wahrle SE, Jiang H, Parsadanian M, Legleiter J, Han X, Fryer JD, Kowalewski T, Holtzman DM, J Biol Chem 2004 279 40987 40993 10.1074/jbc.M407963200 15269217 (Pubitemid 39287699)
29. Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. Hirsch-Reinshagen V, Zhou S, Burgess BL, Bernier L, McIsaac SA, Chan JY, Tansley GH, Cohn JS, Hayden MR, Wellington CL, J Biol Chem 2004 279 41197 41207 10.1074/jbc.M407962200 15269218 (Pubitemid 39287722)
30. Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease. Wahrle SE, Jiang H, Parsadanian M, Kim J, Li A, Knoten A, Jain S, Hirsch-Reinshagen V, Wellington CL, Bales KR, et al. J Clin Invest 2008 118 671 682 18202749 (Pubitemid 351206556)
31. Measurement of tissue protein synthesis rates in vivo: a critical analysis of contrasting methods. Garlick PJ, McNurlan MA, Essen P, Wernerman J, Am J Physiol 1994 266 287 E297 8166249
32. Enhanced synthesis of albumin and fibrinogen at high altitude. Imoberdorf R, Garlick PJ, McNurlan MA, Casella GA, Peheim E, Turgay M, Bartsch P, Ballmer PE, J Appl Physiol 2001 90 528 537 11160051 (Pubitemid 32118912)
33. Measurement of muscle protein fractional synthesis and breakdown rates from a pulse tracer injection. Zhang XJ, Chinkes DL, Wolfe RR, Am J Physiol Endocrinol Metab 2002 283 753 E764 12217893
34. Kinetics of neutral amino acid transport across the blood-brain barrier. Smith QR, Momma S, Aoyagi M, Rapoport SI, J Neurochem 1987 49 1651 1658 10.1111/j.1471-4159.1987.tb01039.x 3668544 (Pubitemid 17161391)
35. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M, Mol Cell Proteomics 2002 1 376 386 10.1074/mcp.M200025-MCP200 12118079
36. Genetic factors controlling structure and expression of apolipoproteins B and E in mice. Lusis AJ, Taylor BA, Quon D, Zollman S, LeBoeuf RC, J Biol Chem 1987 262 7594 7604 3034900
37. Regulation of lipoprotein metabolism by estrogen in inbred strains of mice occurs primarily by posttranscriptional mechanisms. Srivastava RA, Krul ES, Lin RC, Schonfeld G, Mol Cell Biochem 1997 173 161 168 10.1023/A:1006896131186 9278267 (Pubitemid 27389091)
38. A receptor-mediated pathway for cholesterol homeostasis. Brown MS, Goldstein JL, Science 1986 232 34 47 10.1126/science.3513311 3513311 (Pubitemid 16037973)
39. The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. Lawn RM, Wade DP, Garvin MR, Wang X, Schwartz K, Porter JG, Seilhamer JJ, Vaughan AM, Oram JF, J Clin Invest 1999 104 25 R31 10.1172/JCI8119 10525055
40. The absence of ABCA1 decreases soluble ApoE levels but does not diminish amyloid deposition in two murine models of Alzheimer disease. Hirsch-Reinshagen V, Maia LF, Burgess BL, Blain JF, Naus KE, McIsaac SA, Parkinson PF, Chan JY, Tansley GH, Hayden MR, et al. J Biol Chem 2005 280 43243 43256 10.1074/jbc.M508781200 16207707 (Pubitemid 43049291)
41. Lack of ABCA1 considerably decreases brain ApoE level and increases amyloid deposition in APP23 mice. Koldamova R, Staufenbiel M, Lefterov I, J Biol Chem 2005 280 43224 43235 10.1074/jbc.M504513200 16207713 (Pubitemid 43049289)
42. Deletion of Abca1 increases Abeta deposition in the PDAPP transgenic mouse model of Alzheimer disease. Wahrle SE, Jiang H, Parsadanian M, Hartman RE, Bales KR, Paul SM, Holtzman DM, J Biol Chem 2005 280 43236 43242 10.1074/jbc.M508780200 16207708 (Pubitemid 43049290)
43. Cholesterol metabolism, apolipoprotein E, adenosine triphosphate-binding cassette transporters, and Alzheimers disease. Hirsch-Reinshagen V, Wellington CL, Curr Opin Lipidol 2007 18 325 332 10.1097/MOL.0b013e32813aeabf 17495608 (Pubitemid 46743058)
44. Metabolism of high density lipoprotein subfractions and constituents in Tangier disease following the infusion of high density lipoproteins. Schaefer EJ, Anderson DW, Zech LA, Lindgren FT, Bronzert TB, Rubalcaba EA, Brewer HB, J Lipid Res 1981 22 217 228 6787156 (Pubitemid 11125126)
45. Dolnikowski GG, Wang J, Hegele RA, Jones PJ: Cholesterol and apolipoprotein B metabolism in Tangier disease. Schaefer EJ, Brousseau ME, Diffenderfer MR, Cohn JS, Welty FK, OConnor J, Atherosclerosis 2001 159 231 236 10.1016/S0021-9150(01)00688-8 11689226 (Pubitemid 33016640)
46. Enhanced binding by cultured human fibroblasts of apo-E-containing lipoproteins as compared with low density lipoproteins. Innerarity TL, Mahley RW, Biochemistry 1978 17 1440 1447 10.1021/bi00601a013 206278 (Pubitemid 8330378)
47. ATP-binding cassette transporter A1 (ABCA1) deficiency does not attenuate the brain-to-blood efflux transport of human amyloid-beta peptide (1-40) at the blood-brain barrier. Akanuma S, Ohtsuki S, Doi Y, Tachikawa M, Ito S, Hori S, Asashima T, Hashimoto T, Yamada K, Ueda K, et al. Neurochem Int 2008 52 956 961 10.1016/j.neuint.2007.12.002 18201804
48. Turnover of amyloid beta-protein in mouse brain and acute reduction of its level by phorbol ester. Savage MJ, Trusko SP, Howland DS, Pinsker LR, Mistretta S, Reaume AG, Greenberg BD, Siman R, Scott RW, J Neurosci 1998 18 1743 1752 9464999 (Pubitemid 28103082)
49. In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-beta metabolism and half-life. Cirrito JR, May PC, ODell MA, Taylor JW, Parsadanian M, Cramer JW, Audia JE, Nissen JS, Bales KR, Paul SM, et al. J Neurosci 2003 23 8844 8853 14523085 (Pubitemid 37210896)
50. Dynamics of {beta}-amyloid reductions in brain, cerebrospinal fluid, and plasma of {beta}-amyloid precursor protein transgenic mice treated with a {gamma}-secretase inhibitor. Barten DM, Guss VL, Corsa JA, Loo A, Hansel SB, Zheng M, Munoz B, Srinivasan K, Wang B, Robertson BJ, et al. J Pharmacol Exp Ther 2005 312 635 643 15452193 (Pubitemid 40189561)
51. Dynamics of Abeta turnover and deposition in different beta-amyloid precursor protein transgenic mouse models following gamma-secretase inhibition. Abramowski D, Wiederhold KH, Furrer U, Jaton AL, Neuenschwander A, Runser MJ, Danner S, Reichwald J, Ammaturo D, Staab D, et al. J Pharmacol Exp Ther 2008 327 411 424 10.1124/jpet.108.140327 18687920
52. Measurement of 15 N enrichment in multiple amino acids and urea in a single analysis by gas chromatography/mass spectrometry. Patterson BW, Carraro F, Wolfe RR, Biol Mass Spectrom 1993 22 518 523 10.1002/bms.1200220905 8399400
53. Use of stable isotopically labeled tracers to measure very low density lipoprotein-triglyceride turnover. Patterson BW, Mittendorfer B, Elias N, Satyanarayana R, Klein S, J Lipid Res 2002 43 223 233 11861664 (Pubitemid 34184009)