Similar intracellular peptide profile of TAP1/β2 microglobulin double-knockout mice and C57BL/6 wild-type mice as revealed by peptidomic analysis

AAPS Journal

Volumn 12, Issue 4, 2010, Pages 608-616

  Castro, Leandro M ^a,b   Berti, Denise A ^a   Russo, Lilian C ^a   Coelho, Verônica ^a,c   Gozzo, Fábio C ^d   Oliveira, Vitor ^b   Ferro, Emer S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c NATIONAL INSTITUTE OF SCIENCE AND TECHNOLOGY   (Brazil)

^d UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Intracellular peptide; Mass spectrometry; MHC I antigen presentation; Peptidome; Proteasome

Indexed keywords

BETA 2 MICROGLOBULIN; CELL PROTEIN; CHAPERONIN; DIAZEPAM BINDING INHIBITOR; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 1A; HEMOGLOBIN A; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEUROGRANIN; NEUROPEPTIDE; PEPTIDYLPROPYL ISOMERASE A; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN 1; SOMATOSTATIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 91; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DOUBLE KNOCKOUT MOUSE; ISOTOPE LABELING; KNOCKOUT MOUSE; LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; PEPTIDE ANALYSIS; QUANTITATIVE ASSAY; STRAIN DIFFERENCE; TANDEM MASS SPECTROMETRY; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BETA 2-MICROGLOBULIN; CHROMATOGRAPHY, LIQUID; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 78649648123     PISSN: 15507416     EISSN: None     Source Type: Journal    
DOI: 10.1208/s12248-010-9224-y     Document Type: Article

References (58)

1. MH Glickman A Ciechanover 2002 The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction Physiol Rev 82 2 373 428 11917093 1:CAS:528:DC%2BD38XjtFOnsL4%3D
2. A Hershko A Ciechanover A Varshavsky 2000 Basic medical research award. The ubiquitin system Nat Med 6 10 1073 1081 10.1038/80384 11017125 1:CAS:528:DC%2BD3cXntlKns7o%3D
3. BM Kessler R Glas HL Ploegh 2002 MHC class I antigen processing regulated by cytosolic proteolysis-short cuts that alter peptide generation Mol Immunol 39 3-4 171 179 10.1016/S0161-5890(02)00100-1 12200049 1:CAS:528: DC%2BD38XmsVWqtb0%3D (Pubitemid 35013510)
4. BP Dolan L Li K Takeda JR Bennink JW Yewdell 2010 Defective ribosomal products are the major source of antigenic peptides endogenously generated from influenza A virus neuraminidase J Immunol. 184 3 1419 1424 10.4049/jimmunol. 0901907 20038640 1:CAS:528:DC%2BC3cXhtVGitro%3D
5. AL Goldberg 2003 Protein degradation and protection against misfolded or damaged proteins Nature 426 6968 895 899 10.1038/nature02263 14685250 1:CAS:528:DC%2BD3sXpvVGmtbc%3D (Pubitemid 38056882)
6. CM Pickart 2004 Back to the future with ubiquitin Cell 116 2 181 190 10.1016/S0092-8674(03)01074-2 14744430 1:CAS:528:DC%2BD2cXhtValsrg%3D (Pubitemid 38167311)
7. I Dolenc E Seemuller W Baumeister 1998 Decelerated degradation of short peptides by the 20S proteasome FEBS Lett 434 3 357 361 10.1016/S0014-5793(98) 01010-2 9742954 1:CAS:528:DyaK1cXmt1yjur4%3D (Pubitemid 29052256)
8. CJ Aldrich HG Ljunggren L Van Kaer PG Ashton-Rickardt S Tonegawa J Forman 1994 Positive selection of self- and alloreactive CD8+ T cells in Tap-1 mutant mice Proc Natl Acad Sci USA 91 14 6525 6528 10.1073/pnas.91.14.6525 8022816 1:CAS:528:DyaK2cXkvVSqsL4%3D (Pubitemid 24200694)
9. C Herberts E Reits J Neefjes 2003 Proteases, proteases and proteases for presentation Nat Immunol 4 4 306 308 10.1038/ni0403-306 12660727 1:CAS:528:DC%2BD3sXitlyqsrw%3D (Pubitemid 36432309)
10. T Serwold S Gaw N Shastri 2001 ER aminopeptidases generate a unique pool of peptides for MHC class I molecules Nat Immunol 2 7 644 651 10.1038/89800 11429550 1:CAS:528:DC%2BD3MXltFSlu74%3D (Pubitemid 32677633)
11. AL Goldberg P Cascio T Saric KL Rock 2002 The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides Mol Immunol 39 3-4 147 164 10.1016/S0161-5890(02)00098-6 12200047 1:CAS:528:DC%2BD38XmsVWqtLc%3D (Pubitemid 35013508)
12. HL Ploegh 1998 Viral strategies of immune evasion Science 280 5361 248 253 10.1126/science.280.5361.248 9535648 1:CAS:528:DyaK1cXis1SlsLs%3D (Pubitemid 28178062)
13. A Lev MF Princiotta D Zanker K Takeda JS Gibbs C Kumagai, et al. 2010 Compartmentalized MHC class I antigen processing enhances immunosurveillance by circumventing the law of mass action Proc Natl Acad Sci USA 107 15 6964 6969 10.1073/pnas.0910997107 20351281
14. M Wang L Harhaji K Lamberth M Harndahl S Buus NH Heegaard, et al. 2009 Modified human beta 2-microglobulin (desLys(58)) displays decreased affinity for the heavy chain of MHC class I and induces nitric oxide production and apoptosis Scand J Immunol 69 3 203 212 10.1111/j.1365-3083.2008.02213.x 19281532 1:CAS:528:DC%2BD1MXjvFOrtLg%3D
15. L van Kaer PG Ashton-Rickardt HL Ploegh S Tonegawa 1992 TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells Cell 71 7 1205 1214 10.1016/S0092-8674(05)80068-6 1473153 (Pubitemid 23016554)
16. JJ Neefjes F Momburg 1993 Cell biology of antigen presentation Curr Opin Immunol 5 1 27 34 10.1016/0952-7915(93)90077-6 7680870 1:CAS:528: DyaK3sXitFSrsro%3D (Pubitemid 23079444)
17. CA Goddard DA Butts CJ Shatz 2007 Regulation of CNS synapses by neuronal MHC class I Proc Natl Acad Sci USA 104 16 6828 6833 10.1073/pnas.0702023104 17420446 (Pubitemid 47175586)
18. DA Berti C Morano LC Russo LM Castro FM Cunha X Zhang, et al. 2009 Analysis of intracellular substrates and products of thimet oligopeptidase in human embryonic kidney 293 cells J Biol Chem 284 21 14105 14116 10.1074/jbc.M807916200 19282285 1:CAS:528:DC%2BD1MXlvV2jtLc%3D
19. Berezniuk I, Sironi J, Callaway MB, Castro LM, Hirata IY, Ferro ES, et al. CCP1/Nna1 functions in protein turnover in mouse brain: implications for cell death in Purkinje cell degeneration mice. FASEB J. Jan 8 (in press).
20. LD Fricker 2010 Analysis of mouse brain peptides using mass spectrometry-based peptidomics: implications for novel functions ranging from non-classical neuropeptides to microproteins Mol Biosyst 6 8 1355 1365 10.1039/c003317k 20428524 1:CAS:528:DC%2BC3cXos1equrw%3D
21. V Rioli FC Gozzo AS Heimann A Linardi JE Krieger CS Shida, et al. 2003 Novel natural peptide substrates for endopeptidase 24.15, neurolysin, and angiotensin-converting enzyme J Biol Chem 278 10 8547 8555 10.1074/jbc. M212030200 12500972 1:CAS:528:DC%2BD3sXhsF2ht74%3D (Pubitemid 36800608)
22. FM Cunha DA Berti ZS Ferreira CF Klitzke RP Markus ES Ferro 2008 Intracellular peptides as natural regulators of cell signaling J Biol Chem 283 36 24448 24459 10.1074/jbc.M801252200 18617518 1:CAS:528:DC%2BD1cXhtVGktbzJ
23. SI Kim A Pabon TA Swanson MJ Glucksman 2003 Regulation of cell-surface major histocompatibility complex class I expression by the endopeptidase EC3.4.24.15 (thimet oligopeptidase) Biochem J 375 Pt 1 111 120 10.1042/BJ20030490 12877658 1:CAS:528:DC%2BD3sXnsVyju7g%3D (Pubitemid 37255386)
24. CL Silva FC Portaro VL Bonato AC de Camargo ES Ferro 1999 Thimet oligopeptidase (EC 3.4.24.15), a novel protein on the route of MHC class I antigen presentation Biochem Biophys Res Commun 255 3 591 595 10.1006/bbrc.1999.0250 10049755 1:CAS:528:DyaK1MXhtlCiu7k%3D (Pubitemid 29294843)
25. IA York AX Mo K Lemerise W Zeng Y Shen CR Abraham, et al. 2003 The cytosolic endopeptidase, thimet oligopeptidase, destroys antigenic peptides and limits the extent of MHC class I antigen presentation Immunity 18 3 429 440 10.1016/S1074-7613(03)00058-X 12648459 1:CAS:528:DC%2BD3sXisFKgsro%3D (Pubitemid 36351521)
26. JL Harris PB Alper J Li M Rechsteiner BJ Backes 2001 Substrate specificity of the human proteasome Chem Biol 8 12 1131 1141 10.1016/S1074-5521(01)00080-1 11755392 1:CAS:528:DC%2BD38XisFWr (Pubitemid 34029882)
27. AF Kisselev M Garcia-Calvo HS Overkleeft E Peterson MW Pennington HL Ploegh, et al. 2003 The caspase-like sites of proteasomes, their substrate specificity, new inhibitors and substrates, and allosteric interactions with the trypsin-like sites J Biol Chem 278 38 35869 35877 10.1074/jbc.M303725200 12815064 1:CAS:528:DC%2BD3sXnt1aqtL4%3D (Pubitemid 37139904)
28. HG Rammensee 2002 Survival of the fitters Nature 419 6906 443 445 10.1038/419443a 12368840 1:CAS:528:DC%2BD38XnsFaju7o%3D
29. FY Che R Biswas LD Fricker 2005 Relative quantitation of peptides in wild-type and Cpe(fat/fat) mouse pituitary using stable isotopic tags and mass spectrometry J Mass Spectrom 40 2 227 237 10.1002/jms.742 15706630 1:CAS:528:DC%2BD2MXitFyhur0%3D (Pubitemid 40327262)
30. C Morano X Zhang LD Fricker 2008 Multiple isotopic labels for quantitative mass spectrometry Anal Chem 80 23 9298 9309 10.1021/ac801654h 19551992 1:CAS:528:DC%2BD1cXhtlaktb3O
31. R Zhang CS Sioma RA Thompson L Xiong FE Regnier 2002 Controlling deuterium isotope effects in comparative proteomics Anal Chem 74 15 3662 3669 10.1021/ac025614w 12175151 1:CAS:528:DC%2BD38XltV2ms7c%3D (Pubitemid 34855856)
32. BH Koller P Marrack JW Kappler O Smithies 1990 Normal development of mice deficient in beta 2 M, MHC class I proteins, and CD8+ T cells Science 248 4960 1227 1230 10.1126/science.2112266 2112266 1:CAS:528:DC%2BC3cXltVGitbo%3D
33. HG Ljunggren L Van Kaer MS Sabatine H Auchincloss Jr S Tonegawa HL Ploegh 1995 MHC class I expression and CD8+ T cell development in TAP1/beta 2-microglobulin double mutant mice Int Immunol 7 6 975 984 10.1093/intimm/7.6. 975 7577806 1:CAS:528:DyaK2MXmsF2hu7Y%3D
34. S Udenfriend S Stein P Bohlen W Dairman W Leimgruber M Weigele 1972 Fluorescamine: a reagent for assay of amino acids, peptides, proteins, and primary amines in the picomole range Science 178 63 871 872 10.1126/science.178. 4063.871 5085985 1:CAS:528:DyaE3sXis1ShsA%3D%3D
35. FY Che L Yan H Li N Mzhavia LA Devi LD Fricker 2001 Identification of peptides from brain and pituitary of Cpe(fat)/Cpe(fat) mice Proc Natl Acad Sci USA 98 17 9971 9976 10.1073/pnas.161542198 11481435 1:CAS:528: DC%2BD3MXmtlCmtrk%3D (Pubitemid 32769412)
36. JS Gelman J Sironi LM Castro ES Ferro LD Fricker 2010 Hemopressins and other hemoglobin-derived peptides in mouse brain: comparison between brain, blood, and heart peptidome and regulation in Cpefat/fat mice J Neurochem 113 4 871 880 10.1111/j.1471-4159.2010.06653.x 20202081 1:CAS:528:DC%2BC3cXlvFShs7Y%3D
37. SH Lecker AL Goldberg 2002 Slowing muscle atrophy: putting the brakes on protein breakdown J Physiol 545 Pt 3 729 10.1113/jphysiol.2002.030429 12482881 1:CAS:528:DC%2BD3sXpvV2luw%3D%3D (Pubitemid 36024415)
38. M Orlowski 1990 The multicatalytic proteinase complex, a major extralysosomal proteolytic system Biochemistry 29 45 10289 10297 10.1021/bi00497a001 2175651 1:CAS:528:DyaK3cXmtVOisrc%3D
39. G Niedermann E Geier M Lucchiari-Hartz N Hitziger A Ramsperger K Eichmann 1999 The specificity of proteasomes: impact on MHC class I processing and presentation of antigens Immunol Rev 172 29 48 10.1111/j.1600-065X.1999.tb01354. x 10631935 1:CAS:528:DC%2BD3cXkvVajsQ%3D%3D
40. ES Ferro S Hyslop AC Camargo 2004 Intracellullar peptides as putative natural regulators of protein interactions J Neurochem 91 4 769 777 10.1111/j.1471-4159.2004.02757.x 15525330 1:CAS:528:DC%2BD2cXhtVWgsLbF (Pubitemid 39507353)
41. AS Heimann MH Favarato FC Gozzo V Rioli FR Carreno MN Eberlin, et al. 2005 ACE gene titration in mice uncovers a new mechanism for ACE on the control of body weight Physiol Genomics 20 2 173 182 10.1152/physiolgenomics.00145.2004 15522949 1:CAS:528:DC%2BD2MXitVGjtLo%3D (Pubitemid 40388516)
42. HK Lee 2006 Synaptic plasticity and phosphorylation Pharmacol Ther 112 3 810 832 10.1016/j.pharmthera.2006.06.003 16904750 1:CAS:528:DC%2BD28XhtFSksr%2FJ (Pubitemid 44573498)
43. K Broadbelt A Ramprasaud LB Jones 2006 Evidence of altered neurogranin immunoreactivity in areas 9 and 32 of schizophrenic prefrontal cortex Schizophr Res 87 1-3 6 14 10.1016/j.schres.2006.04.028 16797925 (Pubitemid 44428114)
44. D Ruano YS Aulchenko A Macedo MJ Soares J Valente MH Azevedo, et al. 2008 Association of the gene encoding neurogranin with schizophrenia in males J Psychiatr Res 42 2 125 133 10.1016/j.jpsychires.2006.10.008 17140601 (Pubitemid 350081091)
45. H Stefansson RA Ophoff S Steinberg OA Andreassen S Cichon D Rujescu, et al. 2009 Common variants conferring risk of schizophrenia Nature 460 7256 744 747 19571808 1:CAS:528:DC%2BD1MXotVSns74%3D
46. B Castrec S Laurent G Henneke D Flament JP Raffin 2010 The glycine-rich motif of Pyrococcus abyssi DNA polymerase D is critical for protein stability J Mol Biol 396 4 840 848 10.1016/j.jmb.2010.01.006 20070946 1:CAS:528: DC%2BC3cXitValsbg%3D
47. GS Pesiridis VM Lee JQ Trojanowski 2009 Mutations in TDP-43 link glycine-rich domain functions to amyotrophic lateral sclerosis Hum Mol Genet 18 R2 R156 R162 10.1093/hmg/ddp303 19808791 1:CAS:528:DC%2BD1MXhtlCqu7jF
48. R Gong X Peng S Kang H Feng J Huang W Zhang, et al. 2005 Structural characterization of the fusion core in syncytin, envelope protein of human endogenous retrovirus family W Biochem Biophys Res Commun 331 4 1193 1200 10.1016/j.bbrc.2005.04.032 15883002 1:CAS:528:DC%2BD2MXjvFemu70%3D (Pubitemid 40692484)
49. S Jiang Q Zhao AK Debnath 2002 Peptide and non-peptide HIV fusion inhibitors Curr Pharm Des 8 8 563 580 10.2174/1381612024607180 11945159 1:CAS:528:DC%2BD38XivFynt7s%3D
50. DL Gibbons MC Vaney A Roussel A Vigouroux B Reilly J Lepault, et al. 2004 Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus Nature 427 6972 320 325 10.1038/nature02239 14737160 1:CAS:528:DC%2BD2cXltFCgtg%3D%3D (Pubitemid 38133653)
51. FL Huang KP Huang C Boucheron 2007 Long-term enrichment enhances the cognitive behavior of the aging neurogranin null mice without affecting their hippocampal LTP Learn Mem 14 8 512 519 10.1101/lm.636107 17671107 1:CAS:528:DC%2BD1cXmsFCgsrw%3D (Pubitemid 47347430)
52. J Li JH Pak FL Huang KP Huang 1999 N-methyl-d-aspartate induces neurogranin/RC3 oxidation in rat brain slices J Biol Chem 274 3 1294 1300 10.1074/jbc.274.3.1294 9880498 1:CAS:528:DyaK1MXpsFKqsg%3D%3D (Pubitemid 29057942)
53. FR Carreno CN Goni LM Castro ES Ferro 2005 14-3-3 epsilon modulates the stimulated secretion of endopeptidase 24.15 J Neurochem 93 1 10 25 10.1111/j.1471-4159.2004.02967.x 15773901 1:CAS:528:DC%2BD2MXjtFCgtrg%3D (Pubitemid 40463511)
54. W Nickel C Rabouille 2009 Mechanisms of regulated unconventional protein secretion Nat Rev Mol Cell Biol 10 2 148 155 10.1038/nrm2617 19122676 1:CAS:528:DC%2BD1MXhtVyisg%3D%3D
55. LC Russo CN Goni LM Castro AF Asega AC Camargo CA Trujillo, et al. 2009 Interaction with calmodulin is important for the secretion of thimet oligopeptidase following stimulation FEBS J 276 16 4358 4371 10.1111/j.1742-4658.2009.07144.x 19614740 1:CAS:528:DC%2BD1MXhtVSjtbzE
56. P Borst RO Elferink 2002 Mammalian ABC transporters in health and disease Annu Rev Biochem 71 537 592 10.1146/annurev.biochem.71.102301.093055 12045106 1:CAS:528:DC%2BD38Xos1Clt74%3D (Pubitemid 34800230)
57. E Procko R Gaudet 2009 Antigen processing and presentation: TAPping into ABC transporters Curr Opin Immunol 21 1 84 91 10.1016/j.coi.2009.02.003 19261456 1:CAS:528:DC%2BD1MXksVCnt70%3D
58. E Procko ML O'Mara WF Bennett DP Tieleman R Gaudet 2009 The mechanism of ABC transporters: general lessons from structural and functional studies of an antigenic peptide transporter FASEB J 23 5 1287 1302 10.1096/fj.08-121855 19174475 1:CAS:528:DC%2BD1MXlsFSnu7s%3D