Probing the S1 specificity pocket of the aminopeptidases that generate antigenic peptides

Biochemical Journal

Volumn 435, Issue 2, 2011, Pages 411-420

  Zervoudi, Efthalia ^a   Papakyriakou, Athanasios ^a   Georgiadou, Dimitra ^a   Evnouchidou, Irini ^a   Gajda, Anna ^b   Poreba, Marcin ^b   Salvesen, Guy S ^c   Drag, Marcin ^b,c   Hattori, Akira ^d   Swevers, Luc ^a   Vourloumis, Dionisios ^a   Stratikos, Efstratios ^a  

^a INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

^b WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

^c BURNHAM INSTITUTE   (United States)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

Aminopeptidase; Antigen; Kinetics; Peptide specificity; Site directed mutagenesis; Substrate library

Indexed keywords

AMINOPEPTIDASE; ANTIGEN; ENDOPLASMIC RETICULUM AMINOPEPTIDASE 1; ENDOPLASMIC RETICULUM AMINOPEPTIDASE 2; INSULIN REGULATED AMINOPEPTIDASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; AMINOPEPTIDASES; BINDING SITES; EPITOPES; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; MODELS, MOLECULAR; MOLECULAR PROBE TECHNIQUES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; PROTEIN BINDING; SUBSTRATE SPECIFICITY;

EID: 79953203538     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20102049     Document Type: Article

References (42)

1. Rock, K. L. and Goldberg, A. L. (1999) Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 17, 739-779
2. Lauvau, G., Kakimi, K., Niedermann, G., Ostankovitch, M., Yotnda, P., Firat, H., Chisari, F. V. and van Endert, P. M. (1999) Human transporters associated with antigen processing (TAPs) select epitope precursor peptides for processing in the endoplasmic reticulum and presentation to T cells. J. Exp. Med. 190, 1227-1240
3. Rock, K. L. and Shen, L. (2005) Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol. Rev. 207, 166-183
4. Cascio, P., Hilton, C., Kisselev, A. F., Rock, K. L. and Goldberg, A. L. (2001) 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. EMBO J. 20, 2357-2366
5. Roelse, J., Gromme, M., Momburg, F., Hammerling, G. and Neefjes, J. (1994) Trimming of TAP-translocated peptides in the endoplasmic reticulum and in the cytosol during recycling. J. Exp. Med. 180, 1591-1597
6. Serwold, T., Gaw, S. and Shastri, N. (2001) ER aminopeptidases generate a unique pool of peptides for MHC class I molecules. Nat. Immunol. 2, 644-651
7. Serwold, T., Gonzalez, F., Kim, J., Jacob, R. and Shastri, N. (2002) ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419, 480-483
8. Saric, T., Chang, S. C., Hattori, A., York, I. A., Markant, S., Rock, K. L., Tsujimoto, M. and Goldberg, A. L. (2002) An IFN-gamma-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat. Immunol. 3, 1169-1176
9. York, I. A., Chang, S. C., Saric, T., Keys, J. A., Favreau, J. M., Goldberg, A. L. and Rock, K. L. (2002) The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat. Immunol. 3, 1177-1184
10. Saveanu, L., Carroll, O., Lindo, V., Del Val, M., Lopez, D., Lepelletier, Y., Greer, F., Schomburg, L., Fruci, D., Niedermann, G. and van Endert, P. M. (2005) Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat. Immunol. 6, 689-697
11. Saveanu, L., Carroll, O., Weimershaus, M., Guermonprez, P., Firat, E., Lindo, V., Greer, F., Davoust, J., Kratzer, R., Keller, S. R. et al. (2009) IRAP identifies an endosomal compartment required for MHC class I cross-presentation. Science 325, 213-217
12. Tsujimoto, M. and Hattori, A. (2005) The oxytocinase subfamily of M1 aminopeptidases. Biochim. Biophys. Acta 1751, 9-18
13. York, I. A., Brehm, M. A., Zendzian, S., Towne, C. F. and Rock, K. L. (2006) Endoplasmic reticulum aminopeptidase 1 (ERAP1) trims MHC class I-presented peptides in vivoand plays an important role in immunodominance. Proc. Natl. Acad. Sci. U.S.A. 103, 9202-9207
14. Hammer, G. E., Gonzalez, F., Champsaur, M., Cado, D. and Shastri, N. (2006) The aminopeptidase ERAAP shapes the peptide repertoire displayed by major histocompatibility complex class I molecules. Nat. Immunol. 7, 103-112
15. Yan, J., Parekh, V. V., Mendez-Fernandez, Y., Olivares-Villagomez, D., Dragovic, S., Hill, T., Roopenian, D. C., Joyce, S. and Van Kaer, L. (2006) In vivo role of ER-associated peptidase activity in tailoring peptides for presentation by MHC class Ia and class Ib molecules. J. Exp. Med. 203, 647-659
16. Firat, E., Saveanu, L., Aichele, P., Staeheli, P., Huai, J., Gaedicke, S., Nil, A., Besin, G., Kanzler, B., van Endert, P. and Niedermann, G. (2007) The role of endoplasmic reticulum-associated aminopeptidase 1 in immunity to infection and in crosspresentation. J. Immunol. 178, 2241-2248 (Pubitemid 46233422)
17. Hammer, G. E., Gonzalez, F., James, E., Nolla, H. and Shastri, N. (2007) In the absence of aminopeptidase ERAAP, MHC class I molecules present many unstable and highly immunogenic peptides. Nat. Immunol. 8, 101-108
18. Chang, S. C., Momburg, F., Bhutani, N. and Goldberg, A. L. (2005) The ER aminopeptidase, ERAP1, trims precursors to lengths of MHC class I peptides by a "molecular ruler" mechanism. Proc. Natl. Acad. Sci. U.S.A. 102, 17107-17112
19. Evnouchidou, I., Momburg, F., Papakyriakou, A., Chroni, A., Leondiadis, L., Chang, S. C., Goldberg, A. L. and Stratikos, E. (2008) The internal sequence of the peptide-substrate determines its N-terminus trimming by ERAP1. PLoS ONE 3, e3658
20. Georgiadou, D., Hearn, A., Evnouchidou, I., Chroni, A., Leondiadis, L., York, I. A., Rock, K. L. and Stratikos, E. (2010) Placental leucine aminopeptidase efficiently generates mature antigenic peptides in vitro but in patterns distinct from endoplasmic reticulum aminopeptidase 1. J. Immunol. 185, 1584-1592
21. Hearn, A., York, I. A. and Rock, K. L. (2009) The specificity of trimming of MHC class I-presented peptides in the endoplasmic reticulum. J. Immunol. 183, 5526-5536
22. Hattori, A., Kitatani, K., Matsumoto, H., Miyazawa, S., Rogi, T., Tsuruoka, N., Mizutani, S., Natori, Y. and Tsujimoto, M. (2000) Characterization of recombinant human adipocyte-derived leucine aminopeptidase expressed in Chinese hamster ovary cells. J. Biochem. 128, 755-762
23. Tanioka, T., Hattori, A., Masuda, S., Nomura, Y., Nakayama, H., Mizutani, S. and Tsujimoto, M. (2003) Human leukocyte-derived arginine aminopeptidase. The third member of the oxytocinase subfamily of aminopeptidases. J. Biol. Chem. 278, 32275-32283
24. Matsumoto, H., Rogi, T., Yamashiro, K., Kodama, S., Tsuruoka, N., Hattori, A., Takio, K., Mizutani, S. and Tsujimoto, M. (2000) Characterization of a recombinant soluble form of human placental leucine aminopeptidase/ oxytocinase expressed in Chinese hamster ovary cells. Eur. J. Biochem. 267, 46-52
25. Drag, M., Bogyo, M., Ellman, J. A. and Salvesen, G.S. (2010) Aminopeptidase fingerprints, an integrated approach for identification of good substrates and optimal inhibitors. J. Biol. Chem. 285, 3310-3318
26. Sali, A. and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815
27. Case, D. A., Cheatham, 3rd, T. E., Darden, T., Gohlke, H., Luo, R., Merz, Jr, K. M., Onufriev, A., Simmerling, C., Wang, B. and Woods, R. J. (2005) The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688
28. Papakyriakou, A., Spyroulias, G. A., Sturrock, E. D., Manessi-Zoupa, E. and Cordopatis, P. (2007) Simulated interactions between angiotensin-converting enzyme and substrate gonadotropin-releasing hormone: novel insights into domain selectivity. Biochemistry 46, 8753-8765 (Pubitemid 47204441)
29. Hawkins, P. C., Skillman, A. G., Warren, G. L., Ellingson, B. A. and Stahl, M. T. (2010) Conformer generation with OMEGA: algorithm and validation using high quality structures from the Protein Databank and Cambridge Structural Database. J. Chem. Inf. Model. 50, 572-584
30. Jakalian, A., Jack, D. B. and Bayly, C. I. (2002) Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and validation. J. Comput. Chem. 23, 1623-1641
31. Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S. and Olson, A. J. (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791
32. Baker, N. A., Sept, D., Joseph, S., Holst, M. J. and McCammon, J. A. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
33. Reference deleted
34. Humphrey, W., Dalke, A. and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38
35. Tsujimoto, M., Goto, Y., Maruyama, M. and Hattori, A. (2008) Biochemical and enzymatic properties of the M1 family of aminopeptidases involved in the regulation of blood pressure. Heart Fail. Rev. 13, 285-291
36. Goto, Y., Tanji, H., Hattori, A. and Tsujimoto, M. (2008) Glutamine-181 is crucial in the enzymatic activity and substrate specificity of human endoplasmic-reticulum aminopeptidase-1. Biochem. J. 416, 109-116
37. Georgiadou, D. and Stratikos, E. (2009) Cellular mechanisms that edit the immunopeptidome. Curr. Proteomics 6, 13-24
38. Hung, S. H. and Hedstrom, L. (1998) Converting trypsin to elastase: substitution of the S1 site and adjacent loops reconstitutes esterase specificity but not amidase activity. Protein Eng. 11, 669-673
39. Caputo, A., James, M. N., Powers, J. C., Hudig, D. and Bleackley, R. C. (1994) Conversion of the substrate specificity of mouse proteinase granzyme B. Nat. Struct. Biol. 1, 364-367
40. Albiston, A. L., Pham, V., Ye, S., Ng, L., Lew, R. A., Thompson, P. E., Holien, J. K., Morton, C. J., Parker, M. W. and Chai, S. Y. (2010) Phenylalanine-544 plays a key role in substrate and inhibitor binding by providing a hydrophobic packing point at the active site of insulin-regulated aminopeptidase. Mol. Pharmacol. 78, 600-607
41. Haroon, N. and Inman, R. D. (2010) Endoplasmic reticulum aminopeptidases: biology and pathogenic potential. Nat. Rev. Rheumatol. 6, 461-467
42. Evnouchidou, I., Kamal, R. P., Seregin, S. S., Goto, Y., Tsujimoto, M., Hattori, A., Voulgari, P. V., Drosos, A. A., Amalfitano, A., York, I. A. and Stratikos, E. (2011) Cutting edge: coding single nucleotide polymorphisms of endoplasmic reticulum aminopeptidase 1 can affect antigenic peptide generation in vitro by influencing basic enzymatic properties of the enzyme. J. Immunol. 186, 1909-1913