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MASS SPECTROMETRY

Technological Advancements in Mass Spectrometry and Its Impact on Proteomics

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Pages 1498-1520 | Received 13 Apr 2010, Accepted 08 Jul 2010, Published online: 14 Jun 2011

REFERENCES

  • Bailey , C. M. , S. M. M. Sweet , D. L. Cunningham , M. Zeller , J. K. Heath , and H. J. Cooper . 2009 . SLoMo: Automated site localization of modifications from ETD/ECD mass spectra . J. Proteome. Res. 8 : 1965 – 1971 .
  • Bakhtiar , R. , and Z. Guan . 2006 . Electron capture dissociation mass spectrometry in characterization of peptides and proteins . Biotechnol. Lett. 28 : 1047 – 1059 .
  • Bogdanov , B. , and R. D. Smith . 2005 . Proteomics by FTICR mass spectrometry: Top down and bottom up . Mass Spectrom. Rev. 24 : 168 – 200 .
  • Brock , A. , D. M. Horn , E. C. Peters , C. M. Shaw , C. Ericson , Q. T. Phung , and A. R. Salomon . 2002 . Automated liquid chromatography MALDI-FTICR-MS platform for proteomics. Automated high performance mass spectrometry and data analysis . Am. Pharm. Rev. 5 : 94 – 99 .
  • Brodbelt , J. S. , and J. L. Wilson . 2009 . Infrared multiphoton dissociation in quadrupole ion traps . Mass Spectrom. Rev. 28 : 390 – 424 .
  • Chamot-Rooke , J. , G. van der Rest , A. Dalleu , S. Bay , and J. Lemoine . 2007. The combination of electron capture dissociation and fixed charge derivatization increases sequence coverage for O-glycosylated and O-phosphorylated peptides. J. Am. Soc. Mass Spectrom. 18: 1405–1413.
  • Chapman , K. 2002 . The ProteinChip® biomarker system from Ciphergen Biosystems: A novel proteomics platform for rapid biomarker discovery and validation . Biochem. Soc. Trans. 30 : 82 – 87 .
  • Chen , C. H. 2008 . Review of a current role of mass spectrometry for proteome research . Anal Chim Acta. 624 : 16 – 36 .
  • Cole , R. B. 1997 . Combining liquid chromatography with electrospray mass spectrometry . In Electrospray Ionization Mass Spectrometry: Fundamentals, Instrumentation and Applications, , 1st ed. , 323 – 342 . New York : Wiley .
  • Colinge , J. , A. Masselot , M. Giron , T. Dessingy , and J. Magnin . 2003 . OLAV: Towards high-throughput tandem mass spectrometry data identification . Proteomics. 3 : 1454 – 1463 .
  • Cooper , H. J. , K. Hakansson , and A. G. Marshall . 2005 . The role of electron capture dissociation in biomolecular analysis . Mass Spectrom. Rev. 24 : 201 – 222 .
  • Craig , R. , and R. C. Beavis . 2004 . TANDEM: Matching proteins with tandem mass spectra . Bioinformatics. 20 : 1466 – 1467 .
  • Dodds , E. D. , J. B. German , and C. B. Lebrilla . 2007 . Enabling MALDI-FTICR-MS/MS for high-performance proteomics through combination of infrared and collisional activation . Anal. Chem. 79 : 9547 – 9556 .
  • Drogaris , P. , J. C. Le Blanc , J. E. Fitzgerald , N. F. Lowndes , A. Verreault , and P. Thibault . 2009 . Enhanced protein detection using a trapping mode on a hybrid quadrupole linear ion trap (Q-Trap) . Anal. Chem. 81 : 6300 – 6309 .
  • Eng , J. K. , A. L. McCormack , and J. R. Yates . 1994 . An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database . J. Am. Soc. Mass Spectrom. 5 : 976 – 989 .
  • Gardner , M. W. , S. I. Smith , A. R. Ledvina , J. A. Madsen , J. J. Coon , J. C. Schwartz , G. C. Stafford , and J. S. Brodbelt . 2009 . Infrared multiphoton dissociation of peptide cations in a dual pressure linear ion trap mass spectrometer . Anal. Chem. 81 : 8109 – 8118 .
  • Ge , F. , and Q. Y. He . 2009 . Genomic and proteomic approaches for predicting toxicity and adverse drug reactions . Expert Opin. Drug Metabol. Toxicol. 5 : 29 – 37 .
  • Geer , L. Y. , S. P. Markey , J. A. Kowalak , L. Wagner , M. Xu , D. M. Maynard , X. Yang , W. Shi , and S. H. Bryant . 2004 . Open mass spectrometry search algorithm . J. Proteome Res. 3 : 958 – 964 .
  • Hager , J. W. 2004 . QTRAP™ mass spectrometer technology for proteomics and applications . Drug Discovery Today. 3 : S31 – S36 .
  • Hakansson , K. , M. J. Chalmers , J. P. Quinn , M. A. McFarland , C. L. Hendrickson , and A. G. Marshall . 2003 . Combined electron capture and infrared multiphoton dissociation for multistage MS/MS in a Fourier transform ion cyclotron resonance mass spectrometer . Anal. Chem. 75 : 3256 – 3262 .
  • Han , X. , A. Aslanian , and J. R. Yates . 2008 . Mass spectrometry for proteomics . Curr. Opin. Chem. Biol. 12 : 483 – 490 .
  • Hashimo , Y. , H. Hasegawa , K. Yoshinari , and I. Waki . 2003 . Collision-activated infrared multiphoton dissociation in a quadrupole ion trap mass spectrometer . Anal. Chem. 75 : 420 – 425 .
  • Hillenkamp , F. , and J. Peter-Katalinić . 2007 . MALDI mass spectrometry instrumentation . In MALDI MS: A practical guide to instrumentation, methods and applications . New York : Wiley , 29 – 82 .
  • Hopfgartner , G. , and E. Varesio . 2005 . Application of mass spectrometry for quantitative and qualitative analysis in life sciences . CHIMIA: Int. J. Chem. 59 : 321 – 325 .
  • Hopfgartner , G. , E. Varesio , V. Tschappat , C. Grivet , E. Bourgogne , and L. A. Leuthold . 2004. Triple quadrupole linear ion trap mass spectrometer for the analysis of small molecules and macromolecules. J. Mass Spectrom. 39: 845–855.
  • Hortin , G. L. 2006 . The MALDI-TOF mass spectrometric view of the plasma proteome and peptidome . Clin. Chem. 52 : 1223 – 1237 .
  • Hoteling , A. J. , and K. G. Owens . 2004 . Improved PSD and CID on a MALDI TOFMS . J. Am. Soc. Mass Spectrom. 15 : 523 – 535 .
  • Hu , Q. , R. J. Noll , H. Li , A. Makarov , M. Hardman , and R. G. Cooks . 2005 . The orbitrap: A new mass spectrometer . J. Mass Spectrom. 40 : 430 – 443 .
  • Hu , Y. , S. Zhang , J. Yu , J. Liu , and S. Zheng . 2005 . SELDI-TOF-MS: The proteomics and bioinformatics approaches in the diagnosis of breast cancer . The Breast. 14 : 250 – 255 .
  • Huang , M. Z. , H. J. Hsu , J. Y. Lee , J. Jeng , and J. Shiea . 2006 . Direct protein detection from biological media through electrospray-assisted laser desorption ionization/mass spectrometry . J. Proteome. Res. 5 : 1107 – 1116 .
  • Ifa , D. R. , J. M. Wiseman , Q. Song , and R. G. Cooks . 2007 . Development of capabilities for imaging mass spectrometry under ambient conditions with desorption electrospray ionization (DESI) . Int. J. Mass Spectrom. 259 : 8 – 15 .
  • Jenuwein , T. D. A. 2001 . Translating the Histone code . Science. 293 : 1074 – 1080 .
  • Kelleher , N. L. 2004 . Top-down proteomics . Anal. Chem. 76 : 197A – 203A .
  • Kjeldsen , F. , O. B. Hørning , S. S. Jensen , A. M. B. Giessing , and O. N. Jensen . 2008 . Towards liquid chromatography time-scale peptide sequencing and characterization of post-translational modifications in the negative-ion mode using electron detachment dissociation tandem mass spectrometry . J. Am. Soc. Mass Spectrom. 19 : 1156 – 1162 .
  • Klen , T. G. , C. M. Andreasen , H. R. Kjeldal , L. R. Leonardsen , T. N. Krogh , P. F. Nielsen , M. V. Sorensen , and O. N. Jensen . 2004 . MALDI MS peptide mapping performance by in-gel digestion on a probe with prestructured sample supports . Anal. Chem. 76 : 3576 – 3583 .
  • Laskin , J. , and J. H. Futrell . 2005 . Activation of large ions in FT-ICR mass spectrometry . Mass Spectrom. Rev. 24 : 135 – 167 .
  • Le Blanc , J. C. Y. 2003 . Unique scanning capabilities of a new hybrid linear ion trap mass spectrometer (QTRAP™) used for high sensitivity proteomics applications . Proteomics. 3 : 859 – 869 .
  • Loo , J. A. , C. G. Edmonds , and R. D. Smith . 1990 . Primary sequence information from intact proteins by electrospray ionization tandem mass spectrometry . Science. 248 : 201 – 204 .
  • Macek , B. , L. F. Waanders , J. V. Olsen , and M. Mann . 2006 . Top-down protein sequencing and MS3 on a hybrid linear quadrupole ion trap-orbitrap mass spectrometer . Mol. Cell Proteomics. 5 : 949 – 958 .
  • Mackay , C. L. , B. Ramsahoye , K. Burgess , K. Cook , S. Weidt , J. Creanor , D. Harrison , P. L. Smith , T. Hupp , and L. Hayward . 2008 . Sensitive, specific, and quantitative FTICR mass spectrometry of combinatorial post-translational modifications in intact Histone H4 . Anal. Chem. 80 : 4147 – 4153 .
  • Madsen , J. A. , M. W. Gardner , S. I. Smith , A. R. Ledvina , J. J. Coon , J. C. Schwartz , G. C. Stafford , and J. S. Brodbelt . 2009 . Top-down protein fragmentation by infrared multiphoton dissociation in a dual pressure linear ion trap . Anal. Chem. 81 : 8677 – 8686 .
  • Mathivanan , S. , and A. Pandey . 2008 . Human proteinpedia as a resource for clinical proteomics . Mol. Cell Proteomics. 7 : 2038 – 2047 .
  • McAlister , G. C. , D. Phanstiel , D. M. Good , W. T. Berggren , and J. J. Coon . 2007 . Implementation of electron-transfer dissociation on a hybrid linear ion trap-orbitrap mass spectrometer . Anal. Chem. 79 : 3525 – 3534 .
  • McLafferty , F. W. , K. Breuker , M. Jin , X. Han , G. Infusini , H. Jiang , X. Kong , and T. P. Begley . 2007 . Top-down MS, a powerful complement to the high capabilities of proteolysis proteomics . FEBS J. 274 : 6256 – 6268 .
  • Meltretter , J. , A. Schmidt , A. Humeny , C. M. Becker , and M. Pischetsrieder . 2008. Analysis of the peptide profile of milk and its changes during thermal treatment and storage. J. Agric. Food Chem. 56: 2899–2906.
  • Miao , Z. , and H. Chen . 2009 . Direct analysis of liquid samples by desorption electrospray ionization-mass spectrometry (DESI-MS) . J. Am. Soc. Mass Spectrom. 20 : 10 – 19 .
  • Mihalca , R. , Y. E. M. van der Burgt , L. A. McDonnell , D. Marc , C. Iliya , J. R. H. Albert , and M. A. H. Ron . 2006 . Combined infrared multiphoton dissociation and electron-capture dissociation using co-linear and overlapping beams in Fourier transform ion cyclotron resonance mass spectrometry . Rapid Commun. Mass Spectrom. 20 : 1838 – 1844 .
  • Mikesh , L. M. , B. Ueberheide , A. Chi , J. J. Coon , J. E. Syka , J. Shabanowitz , and D. F. Hunt . 2006 . The utility of ETD mass spectrometry in proteomic analysis . Biochim. Biophys. Acta. 1764 : 1811 – 1822 .
  • M'Komaa , A. E. , D. L. Bluma , J. L. Norrisb , and T. Koyama . 2007 . Detection of pre-neoplastic and neoplastic prostate disease by MADI profiling of urine . Biochem. Biophys. Res. Commun. 353 : 829 – 834 .
  • Molina , H. , D. M. Horn , N. Tang , S. Mathivanan , and A. Pandey . 2007 . Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry . PNAS. 104 : 2199 – 2204 .
  • Motoyama , A. , J. D. Venable , C. I. Ruse , and J. R. Yates . 2006 . Automated ultra-high-pressure multidimensional protein identification technology (UHP-MudPIT) for improved peptide identification of proteomic samples . Anal. Chem. 78 : 5109 – 5118 .
  • Motoyama , A. , and J. R. Yates . 2008 . Multidimensional LC separations in shotgun proteomics . Anal. Chem. 80 : 7187 – 7193 .
  • Nesvizhskii , A. I. , O. Vitek , and R. Aebersold . 2007 . Analysis and validation of proteomic data generated by tandem mass spectrometry . Nat. Methods. 4 : 787 – 797 .
  • O'Malley , R. 2002 . Life's (more than) a BLAST™ . The Biochemist. 21 – 23 .
  • Ouvry-Patat , S. A. , M. P. Torres , C. A. Gelfand , H. H. Quek , M. Easterling , J. P. Speir , and C. H. Borchers . 2009 . Top-down proteomics on a high-field Fourier transform ion cyclotron resonance mass spectrometer . Methods Mol. Biol. 492 : 215 – 231 .
  • Palagi , P. M. , P. Hernandez , D. Walther , and R. D. Appel . 2006 . Proteome informatics I: Bioinformatics tools for processing experimental data . Proteomics. 6 : 5435 – 5444 .
  • Peng , I. X. , J. Shiea , R. R. O. Loo , and J. A. Loo . 2007 . Electrospray-assisted laser desorption/ionization and tandem mass spectrometry of peptides and proteins . Rapid Commun. Mass Spectrom. 21 : 2541 – 2546 .
  • Perkins , D. N. , D. J. C. Pappin , D. M. Creasy , and J. S. Cottrell . 1999 . Probability-based protein identification by searching sequence databases using mass spectrometry data . Electrophoresis. 20 : 3551 – 3567 .
  • Petricoin , E. F. , and L. A. Liotta . 2004 . SELDI-TOF-based serum proteomic pattern diagnostics for early detection of cancer . Curr. Opin. Biotechnol. 15 : 24 – 30 .
  • Pipes , G. D. , P. Campbell , P. V. Bondarenko , B. A. Kerwin , M. J. Treuheit , and H. S. Gadgil . 2010 . Middle-down fragmentation for the identification and quantitation of site-specific methionine oxidation in an IgG1 molecule . J. Pharm. Sci. 99 ( 11 ): 4469 – 4476 .
  • Poon , T. C. W. 2007 . Opportunities and limitations of SELDI-TOF-MS in biomedical research: Practical advices . Expert Rev. Proteomics. 4 : 51 – 65 .
  • Qian , W. J. , D. G. Camp , and R. D. Smith . 2004 . High-throughput proteomics using Fourier transform ion cyclotron resonance mass spectrometry . Expert Rev. Proteomics. 1 : 87 – 95 .
  • Raspopov , S. A. , A. El-Faramawy , B. A. Thomson , and K. W. M. Siu . 2006 . Infrared multiphoton dissociation in quadrupole time-of-flight mass spectrometry: Top-down characterization of proteins . Anal. Chem. 78 : 4572 – 4577 .
  • Renfrow , M. B. , H. J. Cooper , M. Tomana , R. Kulhavy , Y. Hiki , K. Toma , M. R. Emmett , J. Mestecky , A. G. Marshall , and J. Novak . 2005. Determination of aberrant o-glycosylation in the IgA1 hinge region by electron capture dissociation Fourier transform-ion cyclotron resonance mass spectrometry. J. Biol. Chem. 280: 19136–19145.
  • Resing , K. A. , and N. G. Ahn . 2005 . Proteomics strategies for protein identification . FEBS Lett. 579 : 885 – 889 .
  • Reyzer , M. L. , and R. M. Caprioli . 2005 . MALDI mass spectrometry for direct tissue analysis: A new tool for biomarker discovery . J. Proteome. Res. 4 : 1138 – 1142 .
  • Ryu , O. H. , J. C. Atkinson , G. T. Hoehn , G. G. Illei , and T. C. Hart . 2006 . Identification of parotid salivary biomarkers in Sjögren's syndrome by surface-enhanced laser desorption/ionization time-of-flight mass spectrometry and two-dimensional difference gel electrophoresis . Rheumatology. 45 : 1077 – 1086 .
  • Schwartz , J. C. , M. W. Senko , and J. E. P. Syka . 2002 . A two-dimensional quadrupole ion trap mass spectrometer . J. Am. Soc. Mass. Spectrom. 13 : 659 – 669 .
  • Searle , B. C. 2010 . Scaffold: A bioinformatic tool for validating MS/MS-based proteomic studies . Proteomics. 10 : 1265 – 1269 .
  • Shiea , J. , M. Z. Huang , H. J. Hsu , C. Y. Lee , C. H. Yuan , I. Beech , and J. Sunner . 2005 . Electrospray-assisted laser desorption/ionization mass spectrometry for direct ambient analysis of solids . Rapid Commun. Mass Spectrom. 19 : 3701 – 3704 .
  • Sihlbom , C. 2004 . Glycoproteomics of cerebrospinal fluid in neurodegenerative disease . Int. J. Mass Spectrom. 234 : 145 – 152 .
  • Simpkins , F. , J. A. Czechowicz , L. Liotta , and E. C. Kohn . 2005 . SELDI-TOF mass spectrometry for cancer biomarker discovery and serum proteomic diagnostics . Pharmacogenomics. 6 : 647 – 653 .
  • Siuti , N. , and N. L. Kelleher . 2007 . Decoding protein modifications using top-down mass spectrometry . Nat. Methods. 4 : 817 – 821 .
  • Steen , H. , and M. Mann . 2004 . The ABC's (and XYZ's) of peptide sequencing . Nat. Rev. Mol. Cell Biol. 5 : 699 – 711 .
  • Syka , J. E. , J. J. Coon , M. J. Schroeder , J. Shabanowitz , and D. F. Hunt . 2004 . Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry . Proc. Natl. Acad. Sci. 101 : 9528 – 9533 .
  • Tabb , D. L. , C. G. Fernando , and M. C. Chambers . 2007 . MyriMatch: Highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis . J. Proteome Res. 6 : 654 – 661 .
  • Takáts , Z. , J. M. Wiseman , and R. G. Cooks . 2005 . Ambient mass spectrometry using desorption electrospray ionization (DESI): Instrumentation, mechanisms and applications in forensics, chemistry, and biology . J. Mass Spectrom. 40 : 1261 – 1275 .
  • Takáts , Z. , J. M. Wiseman , B. Gologan , and R. G. Cooks . 2004 . Mass spectrometry sampling under ambient conditions with desorption electrospray ionization . Science. 306 : 471 – 473 .
  • Tanaka , K. , H. Waki , Y. Ido , S. Akita , Y. Yoshida , T. Yoshida , and T. Matsuo . 2005 . Protein and polymer analyses up to m/z 100 000 by laser ionization time-of-flight mass spectrometry . Rapid Commun. Mass Spectrom. 2 : 151 – 153 .
  • Tang , N. , P. Tornatore , and S. R. Weinberger . 2004 . Current developments in SELDI affinity technology . Mass Spectrom. Rev. 23 : 34 – 44 .
  • Tanner , S. , H. Shu , A. Frank , L. C. Wang , E. Zandi , M. Mumby , P. A. Pevzner , and V. Bafna . 2005 . InsPecT: Identification of posttranslationally modified peptides from tandem mass spectra . Anal. Chem. 77 : 4626 – 4639 .
  • Thiede , B. , W. Höhenwarter , A. Krah , J. Mattow , M. Schmid , F. Schmidt , and P. R. Jungblut . 2005 . Peptide mass fingerprinting . Methods. 35 : 237 – 247 .
  • Tsai , Y. S. , A. Scherl , J. L. Shaw , C. L. MacKay , S. A. Shaffer , P. R. Langridge-Smith , and D. R. Goodlett . 2009 . Precursor ion independent algorithm for top-down shotgun proteomics . J. Am. Soc. Mass Spectrom. 20 : 2154 – 2166 .
  • Twerenbold , D. , D. Gerber , D. Gritti , Y. Gonin , A. Netuschill , F. Rossel , D. Schenker , and J. L. Vuilleumier . 2001. Single molecule detector for mass spectrometry with mass independent detection efficiency. Proteomics. 1: 66–69.
  • Venter , A. , and R. G. Cooks . 2007 . Desorption electrospray ionization in a small pressure-tight enclosure . Anal. Chem. 79 : 6398 – 6403 .
  • Vestal , M. L. , and J. M. Campbell . 2005 . Tandem time-of-flight mass spectrometry . Methods Enzymol. 402 : 79 – 108 .
  • Voortman , J. , T. V. Pham , J. C. Knol , G. Giaccone , and C. R. Jimenez . 2008 . Time-course MALDI-TOF-MS serum peptide profiling of non-small cell lung cancer patients treated with bortezomib, cisplatin and gemcitabine . J. Clin. Oncol. 26 : 8007 .
  • Watson , J. T. 2007 . “Top Down” Analysis of proteins for the masses . Int. J. Appl. Sci. Eng. 5 : 81 – 95 .
  • Watt , S. J. , M. M. Sheil , J. L. Beck , P. Prosselkov , G. Otting , and N. E. Dixon . 2007 . Effect of protein stabilization on charge state distribution in positive- and negative-ion electrospray ionization mass spectra . J. Am. Soc. Mass Spectrom. 18 : 1605 – 1611 .
  • Wisniewski , J. R. , A. Zougman , S. Krüger , and M. Mann . 2007 . Mass spectrometric mapping of linker histone H1 variants reveals multiple acetylations, methylations, and phosphorylation as well as differences between cell culture and tissue . Mol. Cell Proteomics. 6 : 72 – 87 .
  • Wu , J. , C. S. Hughes , P. Picard , S. Letarte , M. Gaudreult , J. F. Levesque , D. A. Nicoll-Griffith , and K. P. Bateman . 2007 . High-throughput cytochrome P450 inhibition assays using laser diode thermal desorption-atmospheric pressure chemical ionization-tandem mass spectrometry . Anal. Chem. 79 : 4657 – 4665 .
  • Wu , S. , H. Amato , R. Biringer , G. Choudhary , P. Shieh , and W. S. Hancock . 2002 . Targeted proteomics of low-level proteins in human plasma by LC/MSn: Using human growth hormone as a model system . J. Proteome Res. 1 : 459 – 465 .
  • Wuhrer , M. , M. I. Catalina , A. M. Deelder , and C. H. Hokke . 2007 . Glycoproteomics based on tandem mass spectrometry of glycopeptides . J. Chromatogr. B. 849 : 115 – 128 .
  • Xu , P. , and J. Peng . 2008 . Characterization of polyubiquitin chain structure by middle-down mass spectrometry . Anal. Chem. 80 : 3438 – 3444 .
  • Yocum , A. K. , and A. M. Chinnaiyan . 2009 . Current affairs in quantitative targeted proteomics: Multiple reaction monitoring–mass spectrometry . Brief. Functional Genomics Proteomics. 8 : 145 – 157 .
  • Zappacosta , F. , T. S. Collingwood , M. J. Huddleston , and R. S. Annan . 2006 . A quantitative results-driven approach to analyzing multisite protein phosphorylation . Mol. Cell Proteomics. 5 : 2019 – 2030 .
  • Zhang , H. , B. Kong , X. Qu , L. Jia , B. Deng , and Q. Yang . 2006 . Biomarker discovery for ovarian cancer using SELDI-TOF-MS . Gynecol. Oncol. 102 : 61 – 66 .
  • Zhang , Z. 2004 . Prediction of low-energy collision-induced dissociation spectra of peptides . Anal. Chem. 76 : 3908 – 3922 .
  • Zubarev , R. A. 2003 . Reactions of poly peptides with electrons in gas phase . Mass. Spectrom. Rev. 22 : 57 – 77 .
  • Zubarev , R. A. 2009 . Electron capture dissociation LC/MS/MS for bottom-up proteomics . Methods Mol. Biol. 492 : 413 – 416 .

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