The internal sequence of the peptide-substrate determines its N-Terminus trimming by ERAP1

PLoS ONE

Volumn 3, Issue 11, 2008, Pages

  Evnouchidou, Irini ^a   Momburg, Frank ^b   Papakyriakou, Athanasios ^a   Chroni, Angeliki ^a   Leondiadis, Leondios ^a   Chang, Shih Chung ^c   Goldberg, Alfred L ^d   Stratikos, Efstratios ^a  

^a INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPEPTIDASE I; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; AMINO ACID; AMINOPEPTIDASE; ARTS 1 PROTEIN, HUMAN; ARTS-1 PROTEIN, HUMAN; EPITOPE; HYBRID PROTEIN; OLIGOPEPTIDE; PEPTIDE LIBRARY; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ELECTRIC POTENTIAL; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; GENE SEQUENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HYDROPHOBICITY; IN VITRO STUDY; MOLECULAR MECHANICS; MOLECULAR MODEL; MOLECULAR RECOGNITION; NONHUMAN; SEQUENCE ALIGNMENT; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; MOLECULAR GENETICS; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN PROCESSING;

AMINO ACID SEQUENCE; AMINO ACIDS; AMINOPEPTIDASES; ANTIGEN PRESENTATION; EPITOPES; HUMANS; HYDROPHOBICITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OLIGOPEPTIDES; PEPTIDE LIBRARY; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

EID: 56349128364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003658     Document Type: Article

References (41)

1. Rock KL, Goldberg AL (1999) Degradation of cell proteins and the generation of MHC classI-presented peptides. Annu Rev Immunol 17: 739-779.
2. Shastri N, Schwab S, Serwold T (2002) Producing nature's gene-chips: the generation of peptides for display by MHC class I molecules. Annu Rev Immunol 20: 463-493.
3. Yewdell JW, Bennink JR (2001) Cut and trim: generating MHC class I peptide ligands. Curr Opin Immunol 13: 13-18.
4. Rock KL, York IA, Saric T, Goldberg AL (2002) Protein degradation and the generation of MHC class I-presented peptides. Adv Immunol 80: 1-70.
5. Zwickl P, Voges D, Baumeister W (1999) The proteasome: a macromolecular assembly designed for controlled proteolysis. Philos Trans R Soc Lond B Biol Sci 354: 1501-1511.
6. Kloetzel PM (2001) Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2: 179-187.
7. Goldberg AL, Cascio P, Saric T, Rock KL (2002) The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides. Mol Immunol 39: 147-164.
8. Roelse J, Gromme M, Momburg F, Hammerling G, Neefjes J (1994) Trimming of TAP-translocated peptides in the endoplasmic reticulum and in the cytosol during recycling. J Exp Med 180: 1591-1597.
9. York IA, Mo AX, Lemerise K, Zeng W, Shen Y, et al. (2003) The cytosolic endopeptidase, thimet oligopeptidase, destroys antigenic peptides and limits the extent of MHC class I antigen presentation. Immunity 18: 429-440.
10. Saric T, Beninga J, Graef CI, Akopian TN, Rock KL, et al. (2001) Major histocompatibility complex class I-presented antigenic peptides are degraded in cytosolic extracts primarily by thimet oligopeptidase. J Biol Chem 276: 36474-36481.
11. Neefjes J, Gottfried E, Roelse J, Gromme M, Obst R, et al. (1995) Analysis of the fine specificity of rat, mouse and human TAP peptide transporters. Eur J Immunol 25: 1133-1136.
12. Lauvau G, Kakimi K, Niedermann G, Ostankovitch M, Yotnda P, et al. (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.
13. Abele R, Tampe R (2006) Modulation of the antigen transport machinery TAP by friends and enemies. FEBS Lett 580: 1156-1163.
14. Serwold T, Gonzalez F, Kim J, Jacob R, Shastri N (2002) ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419: 480-483.
15. Saric T, Chang SC, Hattori A, York IA, Markant S, et al. (2002) An IFN-gamma-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat Immunol 3: 1169-1176.
16. Chang SC, Momburg F, Bhutani N, Goldberg AL (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.
17. Saveanu L, Carroll O, Lindo V, Del Val M, Lopez D, et al. (2005) Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat Immunol 6: 689-697.
18. Falk K, Rotzschke O (2002) The final cut: how ERAP1 trims MHC ligands to size. Nat Immunol 3: 1121-1122.
19. York IA, Chang SC, Saric T, Keys JA, Favreau JM, et al. (2002) The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat Immunol 3: 1177-1184.
20. Cascio P, Hilton C, Kisselev AF, Rock KL, Goldberg AL (2001) 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. Embo J 20: 2357-2366.
21. Matsumoto H, Rogi T, Yamashiro K, Kodama S, Tsuruoka N, et al. (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.
22. Schomburg L, Kollmus H, Friedrichsen S, Bauer K (2000) Molecular characterization of a puromycin-insensitive leucyl-specific aminopeptidase, PILS-AP. Eur J Biochem 267: 3198-3207.
23. Hattori A, Matsumoto H, Mizutani S, Tsujimoto M (1999) Molecular cloning of adipocyte-derived leucine aminopeptidase highly related to placental leucine aminopeptidase/oxytocinase. J Biochem (Tokyo) 125: 931-938.
24. Firat E, Saveanu L, Aichele P, Staeheli P, Huai J, et al. (2007) The role of endoplasmic reticulum-associated aminopeptidase 1 in immunity to infection and in cross-presentation. J Immunol 178: 2241-2248.
25. York IA, Brehm MA, Zendzian S, Towne CF, Rock KL (2006) Endoplasmic reticulum aminopeptidase 1 (ERAP1) trims MHC class I-presented peptides in vivo and plays an important role in immunodominance. Proc Natl Acad Sci U S A 103: 9202-9207.
26. Yan J, Parekh VV, Mendez-Fernandez Y, Olivares-Villagomez D, Dragovic S, et al. (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.
27. Hammer GE, Gonzalez F, Champsaur M, Cado D, Shastri N (2006) The aminopeptidase ERAAP shapes the peptide repertoire displayed by major histocompatibility complex class I molecules. Nat Immunol 7: 103-112.
28. Momburg F, Roelse J, Hammerling GJ, Neefjes JJ (1994) Peptide size selection by the major histocompatibility complex-encoded peptide transporter. J Exp Med 179: 1613-1623.
29. Momburg F, Roelse J, Howard JC, Butcher GW, Hammerling GJ, et al. (1994) Selectivity of MHC-encoded peptide transporters from human, mouse and rat. Nature 367: 648-651.
30. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
31. Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
32. Case DA, Cheatham TE 3rd, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688.
33. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486.
34. Papakyriakou A, Spyroulias GA, Sturrock ED, Manessi-Zoupa E, Cordopatis P (2007) Simulated interactions between angiotensin-converting enzyme and substrate gonadotropin-releasing hormone: novel insights into domain selectivity. Biochemistry 46: 8753-8765.
35. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38, 27-38.
36. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041.
37. DeLano WL. The Pymol Molecular Graphics System, DeLano Scientific, San Carlos, CA. http://www.pymol.org.
38. Kyrieleis OJ, Goettig P, Kiefersauer R, Huber R, Brandstetter H (2005) Crystal structures of the tricorn interacting factor F3 from Thermoplasma acidophilum, a zinc aminopeptidase in three different conformations. J Mol Biol 349: 787-800.
39. Kisselev AF, Akopian T, Woo KM, Goldberg AL (1999) The sizes of peptides generated from protein by mammalian 26 and 20S proteasomes. Implications for understanding the degradative mechanism and antigen presentation. J Biol Chem 274: 3363-3371.
40. Kanaseki T, Blanchard N, Hammer GE, Gonzalez F, Shastri N (2006) ERAAP Synergizes with MHC Class I Molecules to Make the Final Cut in the Antigenic Peptide Precursors in the Endoplasmic Reticulum. Immunity 25: 795-806.
41. Hammer GE, Gonzalez F, James E, Nolla H, 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.