[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Springer Nature Link
Log in

Quantitative Proteomic Analysis of Mitochondria from Primary Neuron Cultures Treated with Amyloid Beta Peptide

  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Increasing evidence supports a role for altered mitochondrial function in the pathogenesis of neuron degeneration in Alzheimer’s disease (AD). Although several studies have examined the effect of amyloid beta peptide (Aß), on activities of individual proteins in primary neuron cultures, there have been no studies of the effects of Aß on the mitochondrial proteome. Here, we quantitatively measured changes in mitochondrial proteins of primary rat cortical neuron cultures exposed to 25 μM Aß25–35 for 16 h using isotope coded affinity tag (ICAT) labeling and 2-dimensional liquid chromatography/tandem mass spectrometry (2D-LC/MS/MS) which allows simultaneous identification and quantification of cysteine-containing proteins. The analysis of enriched mitochondrial fractions identified 10 proteins including sodium/potassium-transporting ATPase, cofilin, dihydropyrimidinase, pyruvate kinase and voltage dependent anion channel 1 that were statistically significantly (P < 0.05) altered in Aß-treated cultures. Elevations of proteins associated with energy production suggest that cells undergoing Aß-mediated apoptosis increase synthesis of proteins essential for ATP production and efflux in an attempt to maintain metabolic function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • D. A. Evans H. H. Funkenstein M. S. Albert P. A. Scherr N. R. Cook M. J. Chown L. E. Hebert C. H. Hennekens J. O. Taylor (1989) ArticleTitlePrevalence of Alzheimer’s disease in a community population of older persons. Higher than previously reported JAMA 262 2551–2556 Occurrence Handle10.1001/jama.262.18.2551

    Article  Google Scholar 

  • P.H. St. George-Hyslop Tanzi R. E. Polinsky R.J. (1987) ArticleTitleThe genetic defect causing familial Alzheimer’s disease maps on chromosome 21 Science 235 885–890

    Google Scholar 

  • P.H. St. George-Hyslop (1994) The molecular genetics of Alzheimer’s disease R. D. Terry R. Katzman L. L. Bick (Eds) Alzheimer’s Disease Raven Press New York 345–352

    Google Scholar 

  • M. F. Beal (1992) ArticleTitleDoes impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann. Neurol. 31 119–130 Occurrence Handle10.1002/ana.410310202

    Article  Google Scholar 

  • D. R. Crapper-MacLachlan (1986) ArticleTitleAluminum and Alzheimer’s disease Neurobiol. Aging. 7 525–532 Occurrence Handle10.1016/0197-4580(86)90102-8

    Article  Google Scholar 

  • W. R. Markesbery W. D. Ehmann (1994) Trace element alterations in Alzheimer’s disease R. D. Terry R. Katzman (Eds) Alzheimer’s Disease Raven Press New York

    Google Scholar 

  • K. M. Regula K. Ens L. A. Kirshenbaum (2003) ArticleTitleMitochondria-assisted cell suicide: a license to kill J. Mol. Cell. Cardiol. 35 559–567 Occurrence Handle10.1016/S0022-2828(03)00118-4

    Article  Google Scholar 

  • M. Pollack Leeuwaenburgh (2001) ArticleTitleApoptosis and aging: role of the mitochondria J. Gerontol. 56A B475–482

    Google Scholar 

  • R. H. Swerdlow S. J. Kish (2002) ArticleTitleMitochondria in Alzheimer’s disease Int. Rev. Neurobiol. 53 341–385

    Google Scholar 

  • D. M. Bowen P. White J. A. Spillane M. J. Goodhardt G. Curzon P. Iwangoff W. Meier-Ruge A. N. Davison (1979) ArticleTitleAccelerated ageing or selective neuronal loss as an important cause of dementia? Lancet 1 11–14

    Google Scholar 

  • S. Minoshima B. Giordani S. Berent K. A. Frey N. L. Foster D. E. Kuhl (1997) ArticleTitleMetabolic reduction in the posterior cingulate cortex in very early Alzheimer’s disease Ann. Neurol. 42 85–94 Occurrence Handle10.1002/ana.410420114

    Article  Google Scholar 

  • S. Hoyer (1993) ArticleTitleIntermediary metabolism disturbance in AD/SDAT and its relation to molecular events Prog. Neuropsychopharmacol. Biol. Psychiatry 17 199–228 Occurrence Handle10.1016/0278-5846(93)90043-R

    Article  Google Scholar 

  • H. Fukuyama M. Ogawa H. Yamauchi S. Yamaguchi J. Kimura Y. Yonekura J. Konishi (1994) ArticleTitleAltered cerebral energy metabolism in Alzheimer’s disease: a PET study J. Nucl. Med. 35 1–6

    Google Scholar 

  • J. P. Blass (2000) ArticleTitleThe mitochondrial spiral an adequate cause of dementia in the Alzheimer’s syndrome Ann. N. Y. Acad. Sci. 924 170–183

    Google Scholar 

  • K. Hirai G. Aliev A. Nunomura H. Fujioka R. L. Russell C. S. Atwood A. B. Johnson Y. Kress H. V. Vinters M. Tabaton S. Shimohama A. D. Cash S. L. Siedlak P. L. Harris P. K. Jones R. B. Petersen G. Perry M. A. Smith (2001) ArticleTitleMitochondrial abnormalities in Alzheimer’s disease J. Neurosci. 21 3017–3023

    Google Scholar 

  • R. J. Mark Z. Pang J. W. Geddes K. Uchida M. P. Mattson (1997) ArticleTitleAmyloid beta-peptide impairs glucose transport in hippocampal and cortical neurons: involvement of membrane lipid peroxidation J. Neurosci. 17 1046–1054

    Google Scholar 

  • R. J. Mark K. Hensley D. A. Butterfield M. P. Mattson (1995) ArticleTitleAmyloid beta-peptide impairs ion-motive ATPase activities: evidence for a role in loss of neuronal Ca2+ homeostasis and cell death J. Neurosci. 15 6239–6249

    Google Scholar 

  • M. B. Smolka H. Zhou S. Purkayastha R. Aebersold (2001) ArticleTitleOptimization of the isotope-coded affinity tag-labeling procedure for quantitative proteome analysis Anal. Biochem. 297 25–31 Occurrence Handle10.1006/abio.2001.5318

    Article  Google Scholar 

  • D. K. Han J. Eng H. Zhou R. Aebersold (2001) ArticleTitleQuantitative profiling of differentiation-induced microsomal proteins using isotope-coded affinity tags and mass spectrometry Nat. Biotechnol. 19 946–951 Occurrence Handle10.1038/nbt1001-946

    Article  Google Scholar 

  • S. P. Gygi B. Rist T. J. Griffin J. Eng R. Aebersold (2002) ArticleTitleProteome analysis of low-abundance proteins using multidimensional chromatography and isotope-coded affinity tags J. Proteome Res. 1 47–54 Occurrence Handle10.1021/pr015509n

    Article  Google Scholar 

  • P. D. Von Haller E. Yi S. Donohoe K. Vaughn A. Keller A. I. Nesvizhskii J. Eng X. J. Li D. R. Goodlett R. Aebersold J. D. Watts (2003) ArticleTitleThe application of new software tools to quantitative protein profiling via Isotope-coded Affinity Tag (ICAT) and tandem mass spectrometry: II. evaluation of tandem mass spectrometry methodologies for large-scale protein analysis, and the application of statistical tools for data analysis and interpretation Mol. Cell. Proteomics 2 428–442

    Google Scholar 

  • Y. Qiu E. A. Sousa R. M. Hewick J. H. Wang (2002) ArticleTitleAcid-labile isotope-coded extractants: a class of reagents for quantitative mass spectrometric analysis of complex protein mixtures Anal. Chem. 74 4969–4979 Occurrence Handle10.1021/ac0256437

    Article  Google Scholar 

  • W. A. Tao R. Aebersold (2003) ArticleTitleAdvances in quantitative proteomics via stable isotope tagging and mass spectrometry Curr. Opin. Biotechnol. 14 110–118 Occurrence Handle10.1016/S0958-1669(02)00018-6

    Article  Google Scholar 

  • K. C. Hansen G. Schmitt-Ulms R. J. Chalkley J. Hirsch M. A. Baldwin A. L. Burlingame (2003) ArticleTitleMass spectrometric analysis of protein mixtures at low levels using cleavable 13C-isotope-coded affinity tag and multidimensional chromatography Mol. Cell. Proteomics 2 299–314

    Google Scholar 

  • S.W. Barger Van Eldik L.J. M.P. Mattson (1995) ArticleTitleS100 beta protects hippocampal neurons from damage induced by glucose deprivation Brain Res. 677 167–170 Occurrence Handle10.1016/0006-8993(95)00160-R

    Article  Google Scholar 

  • C. Xie W. R. Markesbery M. A. Lovell (2000) ArticleTitleSurvival of hippocampal and cortical neurons in a mixture of MEM+ and B27-supplemented neurobasal medium Free Radic. Biol. Med. 28 665–672 Occurrence Handle10.1016/S0891-5849(99)00268-3

    Article  Google Scholar 

  • T. Mossman (1983) ArticleTitleRapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J. Immunol. 65 55–63 Occurrence Handle10.1016/0022-1759(83)90303-4

    Article  Google Scholar 

  • I. Kruman Q. Guo M. P. Mattson (1998) ArticleTitleCalcium and reactive oxygen species mediate staurosporine-induced mitochondrial dysfunction and apoptosis in PC12 cells J. Neurosci. Res. 51 293–308 Occurrence Handle10.1002/(SICI)1097-4547(19980201)51:3<293::AID-JNR3>3.0.CO;2-B

    Article  Google Scholar 

  • J. Peng S. P. Gygi (2001) ArticleTitleProteomics: the move to mixtures J. Mass Spectrom. 36 1083–1091 Occurrence Handle10.1002/jms.229

    Article  Google Scholar 

  • M.P. Washburn D. Wolters J. R. Yates Suffix3rd (2001) ArticleTitleLarge-scale analysis of the yeast proteome by multidimensional protein identification technology Nat. Biotechnol. 19 242–247 Occurrence Handle10.1038/85686

    Article  Google Scholar 

  • S. W. Taylor E. Fahy B. Zhang G. M. Glenn D. E. Warnock S. Wiley A. N. Murphy S. P. Gaucher R. A. Capaldi B. W. Gibson S. S. Ghosh (2003) ArticleTitleCharacterization of the human heart mitochondrial proteome Nat. Biotechnol. 21 281–286 Occurrence Handle10.1038/nbt793

    Article  Google Scholar 

  • Fountoulakis, M., Berndt, P., Langen, H., and Suter, L. 2002. The rat liver mitochondrial proteins. Electrophoresis 23.

  • S. W. Taylor D. E. Warnock G. M. Glenn B. Zhang E. Fahy S. P. Gaucher R. A. Capaldi B. W. Gibson S. S. Ghosh (2002) ArticleTitleAn alternative strategy to determine the mitochondrial proteome using sucrose gradient fractionation and 1D PAGE on highly purified human heart mitochondria J. Proteome Res. 1 451–458 Occurrence Handle10.1021/pr025533g

    Article  Google Scholar 

  • D. Pflieger J.P. Le Caer C. Lemaire B.A. Bernard G. Dujardin J. Rossier (2002) ArticleTitleSystematic identification of mitochondrial proteins by LC-MS/MS Anal. Chem. 74 2400–2406 Occurrence Handle10.1021/ac011295h

    Article  Google Scholar 

  • M. Bigl M. K. Bruckner T. Arendt V. Bigl K. Eschrich (1999) ArticleTitleActivities of key glycolytic enzymes in the brains of patients with Alzheimer’s disease J. Neural Transm. 106 499–511 Occurrence Handle10.1007/s007020050174

    Article  Google Scholar 

  • A. Castegna M. Aksenov M. Aksenova V. Thongboonkerd J. B. Klein W. M. Pierce R. Booze W. R. Markesbery D. A. Butterfield (2002) ArticleTitleProteomic identification of oxidatively modified proteins in Alzheimer’s disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1 Free Radic. Biol. Med. 33 562–571 Occurrence Handle10.1016/S0891-5849(02)00914-0

    Article  Google Scholar 

  • A. Atlante P. Calissano A. Bobba S. Giannattasio E. Marra S. Passarella (2001) ArticleTitleGlutamate neurotoxicity, oxidative stress and mitochondria FEBS Lett. 497 1–5 Occurrence Handle10.1016/S0014-5793(01)02437-1

    Article  Google Scholar 

  • M. D. Johnson L. R. Yu T. P. Conrads Y. Kinoshita T. Uo J. D. Matthews S. W. Lee R. D. Smith T. D. Veenstra R. S. Morrison (2004) ArticleTitleProteome analysis of DNA damage-induced neuronal death using high throughput mass spectrometry J Biol. Chem. 279 26685–26697 Occurrence Handle10.1074/jbc.M401274200

    Article  Google Scholar 

  • U. Soomets R. Mahlapuu R. Tehranian J. Jarvet E. Karelson M. Zilmer K. Iverfeldt M. Zorko A. Graslund U. Langel (1999) ArticleTitleRegulation of GTPase and adenylate cyclase activity by amyloid beta-peptide and its fragments in rat brain tissue Brain Res. 850 179–188 Occurrence Handle10.1016/S0006-8993(99)02142-3

    Article  Google Scholar 

  • D. L. Rymer T. A. Good (2001) ArticleTitleThe role of G protein activation in the toxicity of amyloidogenic Abeta-(1-40), Abeta-(25–35), and bovine calcitonin J. Biol. Chem. 276 2523–2530 Occurrence Handle10.1074/jbc.M005800200

    Article  Google Scholar 

  • B. M. Ross M. McLaughlin M. Roberts G. Milligan J. McCulloch J. T. Knowler (1993) ArticleTitleAlterations in the activity of adenylate cyclase and high affinity GTPase in Alzheimer’s disease Brain Res. 622 35–42 Occurrence Handle10.1016/0006-8993(93)90798-R

    Article  Google Scholar 

  • X. Li A. F. Greenwood R. Powers R. S. Jope (1996) ArticleTitleEffects of postmortem interval, age, and Alzheimer’s disease on G-proteins in human brain Neurobiol. Aging 17 115–122 Occurrence Handle10.1016/0197-4580(95)02023-3

    Article  Google Scholar 

  • A. Garcia-Jimenez R. F. Cowburn T. G. Ohm H. Lasn B. Winblad N. Bogdanovic J. Fastbom (2002) ArticleTitleLoss of stimulatory effect of guanosine triphosphate on [(35)S]GTPgammaS binding correlates with Alzheimer’s disease neurofibrillary pathology in entorhinal cortex and CA1 hippocampal subfield J. Neurosci. Res. 67 388–398 Occurrence Handle10.1002/jnr.10125

    Article  Google Scholar 

  • C. O’Neill B. Wiehager C.J. Fowler R. Ravid B. Winblad R.F. Cowburn (1994) ArticleTitleRegionally selective alterations in G protein subunit levels in the Alzheimer’s disease brain Brain Res. 636 193–201 Occurrence Handle10.1016/0006-8993(94)91017-0

    Article  Google Scholar 

  • H. Y. Wang E. Friedman (1994) ArticleTitleReceptor-mediated activation of G proteins is reduced in postmortem brains from Alzheimer’s disease patients Neurosci. Lett. 173 37–39 Occurrence Handle10.1016/0304-3940(94)90144-9

    Article  Google Scholar 

  • Z. Molnar P. Kovacs I. Laczko K. Soos L. Fulop B. Penke I. Lengyel (2004) ArticleTitleEnhanced G-protein activation by a mixture of Abeta(25–35), Abeta(1–40/42) and zinc J. Neurochem. 89 1215–1223 Occurrence Handle10.1111/j.1471-4159.2004.02427.x

    Article  Google Scholar 

  • B. T. Chua C. Volbracht K. O. Tan R. Li V. C. Yu P. Li (2003) ArticleTitleMitochondrial translocation of cofilin is an early step in apoptosis induction Nat. Cell. Biol. 5 1083–1089 Occurrence Handle10.1038/ncb1070

    Article  Google Scholar 

  • M. Crompton (1999) ArticleTitleThe mitochondrial permeability transition pore and its role in cell death Biochem. J. 341 233–249 Occurrence Handle10.1042/0264-6021:3410233

    Article  Google Scholar 

  • B. C. Yoo M. Fountoulakis N. Cairns G. Lubec (2001) ArticleTitleChanges of voltage-dependent anion-selective channel proteins VDAC1 and VDAC2 brain levels in patients with Alzheimer’s disease and Down syndrome Electrophoresis 22 172–179 Occurrence Handle10.1002/1522-2683(200101)22:1<172::AID-ELPS172>3.0.CO;2-P

    Article  Google Scholar 

  • C. Cande N. Vahsen I. Kouranti E. Schmitt E. Daugas C. Spahr J. Luban R. T. Kroemer F. Giordanetto C. Garrido J. M. Penninger G. Kroemer (2004) ArticleTitleAIF and cyclophilin A cooperate in apoptosis-associated chromatinolysis Oncogene 23 1514–1521 Occurrence Handle10.1038/sj.onc.1207279

    Article  Google Scholar 

  • V. Doyle S. Virji M. Crompton (1999) ArticleTitleEvidence that cyclophilin-A protects cells against oxidative stress Biochem. J. 341 127–132 Occurrence Handle10.1042/0264-6021:3410127

    Article  Google Scholar 

  • H. Ansari G. Greco J. Luban (2002) ArticleTitleCyclophilin A peptidyl-prolyl isomerase activity promotes ZPR1 nuclear export Mol. Cell. Biol. 22 6993–7003 Occurrence Handle10.1128/MCB.22.20.6993-7003.2002

    Article  Google Scholar 

  • C. R. Brown D. Y. Cui G. G. Hung H. L. Chiang (2001) ArticleTitleCyclophilin A mediates Vid22p function in the import of fructose-1,6-bisphosphatase into Vid vesicles J. Biol. Chem. 276 48017–48026

    Google Scholar 

  • T. Huang H. Deng A. W. Wolkoff R. J. Stockert (2002) ArticleTitlePhosphorylation-dependent interaction of the asialoglycoprotein receptor with molecular chaperones J. Biol. Chem. 277 37798–37803 Occurrence Handle10.1074/jbc.M204786200

    Article  Google Scholar 

  • A. Uittenbogaard Y. Ying E. J. Smart (1998) ArticleTitleCharacterization of a cytosolic heat-shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking J. Biol. Chem. 273 6525–6532 Occurrence Handle10.1074/jbc.273.11.6525

    Article  Google Scholar 

  • N. Hamajima K. Matsuda S. Sakata N. Tamaki M. Sasaki M. Nonaka (1996) ArticleTitleA novel gene family defined by human dihydropyrimidinase and three related proteins with differential tissue distribution Gene 180 157–163 Occurrence Handle10.1016/S0378-1119(96)00445-3

    Article  Google Scholar 

  • A. Castegna M. Aksenov V. Thongboonkerd J. B. Klein W. M. Pierce R. Booze W. R. Markesbery D. A. Butterfield (2002) ArticleTitleProteomic identification of oxidatively modified proteins in Alzheimer’s disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71 J. Neurochem. 82 1524–1532 Occurrence Handle10.1046/j.1471-4159.2002.01103.x

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry, University of Kentucky, Lexington, KY, USA, 40536

    Mark A. Lovell & Bert C. Lynn

  2. Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY, USA, 40536

    Mark A. Lovell, Shuling Xiong, William R. Markesbery & Bert C. Lynn

  3. Departments of Neurology and Pathology, University of Kentucky, Lexington, KY, USA, 40536

    William R. Markesbery

  4. University of Kentucky Mass Spectrometry Facility, University of Kentucky, Lexington, KY, USA, 40536

    Bert C. Lynn

  5. Mark A. Lovell, 135 Sanders-Brown Bldg., 800 S. Limestone St., Lexington, KY, USA, 40536

    Mark A. Lovell

Authors
  1. Mark A. Lovell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuling Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William R. Markesbery
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bert C. Lynn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark A. Lovell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lovell, M.A., Xiong, S., Markesbery, W.R. et al. Quantitative Proteomic Analysis of Mitochondria from Primary Neuron Cultures Treated with Amyloid Beta Peptide. Neurochem Res 30, 113–122 (2005). https://doi.org/10.1007/s11064-004-9692-5

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-004-9692-5

Keywords

Search

Navigation