Structure of the Plasmodium falciparum M17 aminopeptidase and significance for the design of drugs targeting the neutral exopeptidases

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 6, 2010, Pages 2449-2454

  McGowan, Sheena ^a   Oellig, Christine A ^a   Birru, Woldeamanuel A ^a   Caradoc Davies, Tom T ^b   Stack, Colin M ^c   Lowther, Jonathan ^d   Skinner Adams, Tina ^e   Mucha, Artur ^f   Kafarski, Pawel ^f   Grembecka, Jolanta ^g   Trenholme, Katharine R ^e   Buckle, Ashley M ^a   Gardiner, Donald L ^e   Dalton, John P ^h,i   Whisstock, James C ^a  

^a MONASH UNIVERSITY   (Australia)

^b AUSTRALIAN SYNCHROTRON   (Australia)

^c UNIVERSITY OF WESTERN SYDNEY   (Australia)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^f WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

^g UNIVERSITY OF VIRGINIA   (United States)

^h UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

ⁱ MCGILL UNIVERSITY   (Canada)

Author keywords

Drug design; Malaria; Neutral aminopeptidases; Protease; Structural biology

Indexed keywords

AMINOPEPTIDASE; AMINOPEPTIDASE M1; AMINOPEPTIDASE M17; BESTATIN; EXOPEPTIDASE; PHOSPHINIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

AMINOPEPTIDASES; ANTIMALARIALS; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; HYDROPHOBICITY; METALS; MODELS, MOLECULAR; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; SUBSTRATE SPECIFICITY;

PLASMODIUM FALCIPARUM;

EID: 77249144842     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0911813107     Document Type: Article

References (38)

1. Enserink M (2008) Malaria. Signs of drug resistance rattle experts, trigger bold plan. Science, 322(5909):1776.
2. D'Alessandro U (2009) Existing antimalarial agents and malaria-treatment strategies. Expert Opin Pharmaco, 10(8):1291-1306.
3. 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(6906):480-483.
4. McGowan S, et al. (2009) Structural basis for the inhibition of the essential Plasmodium falciparum M1 neutral aminopeptidase. Proc Natl Acad Sci USA, 106(8):2537-2542.
5. Skinner-Adams TS, et al. (2007) Identification of phosphinate dipeptide analog inhibitors directed against the Plasmodium falciparum M17 leucine aminopeptidase as lead antimalarial compounds. J Med Chem, 50(24):6024-6031.
6. Skinner-Adams TS, et al. (2009) Plasmodium falciparum neutral aminopeptidases: New targets for anti-malarials. Trends Biochem Sci http://dx.doi.org/10.1016/j.tibs.2009.08.004.
7. Stack CM, et al. Characterization of the Plasmodium falciparum M17 leucyl aminopeptidase A protease involved in amino acid regulation with potential for antimalarial drug development. J Biol Chem, 282(3):2069-2080.
8. Dalal S, Klemba M (2007) Roles for two aminopeptidases in vacuolar hemoglobin catabolism in Plasmodium falciparum. J Biol Chem, 282(49):35978-35987.
9. Liu J, Istvan ES, Gluzman IY, Gross J, Goldberg DE (2006) Plasmodium falciparum ensures its amino acid supply with multiple acquisition pathways and redundant proteolytic enzyme systems. Proc Natl Acad Sci USA, 103(23):8840-8845.
10. Flipo M, et al. (2007) Novel selective inhibitors of the zinc plasmodial aminopeptidase PfA-M1 as potential antimalarial agents. J Med Chem, 50(6):1322-1334.
11. Allary M, Schrevel J, Florent I (2002) Properties, stage-dependent expression and localization of Plasmodium falciparum M1 family zinc-aminopeptidase. Parasitology, 125(Pt 1):1-10.
12. Florent I, et al. (1998) A Plasmodium falciparum aminopeptidase gene belonging to the M1 family of zinc-metallopeptidases is expressed in erythrocytic stages. Mol Biochem Parasitol, 97(1-2):149-160.
13. Maric S, et al. (2009) The M17 leucine aminopeptidase of the malaria parasite Plasmodium falciparum: Importance of active site metal ions in the binding of substrates and inhibitors. Biochemistry, 48(23):5435-5439.
14. Burley SK, David PR, Taylor A, Lipscomb WN (1990) Molecular structure of leucine aminopeptidase at 2.7-A resolution. Proc Natl Acad Sci USA, 87(17):6878-6882.
15. MatsuiM, Fowler JH, Walling LL (2006) Leucine aminopeptidases: Diversity in structure and function. Biol Chem, 387(12):1535-1544.
16. Kim H, Lipscomb WN (1993) X-ray crystallographic determination of the structure of bovine lens leucine aminopeptidase complexed with amastatin: Formulation of a catalytic mechanism featuring a gem-diolate transition state. Biochemistry, 32(33):8465-8478.
17. Konagurthu AS, Whisstock JC, Stuckey PJ, Lesk AM(2006) MUSTANG: A multiple structural alignment algorithm. Proteins, 64(3):559-574.
18. 2+ of the zinc metalloenzyme, amino acid composition, and sulfhydryl content. J Biol Chem, 248(1):294-304.
19. Strater N, Lipscomb WN (1995) Two-metal ion mechanism of bovine lens leucine aminopeptidase: Active site solvent structure and binding mode of L-leucinal, a gem-diolate transition state analogue, by x-ray crystallography. Biochemistry, 34(45):14792-14800.
20. Blackman MJ (2008) Malarial proteases and host cell egress: An 'emerging' cascade. Cell Microbiol, 10(10):1925-1934.
21. Sijwali PS, Rosenthal PJ (2004) Gene disruption confirms a critical role for the cysteine protease falcipain-2 in hemoglobin hydrolysis by Plasmodium falciparum. Proc Natl Acad Sci USA, 101(13):4384-4389.
22. Whisstock JC, McGowan S, Trenholme KR, Gardiner DL, Dalton JP (2009) Reply to Klemba: Intracellular processing of the membrane-bound PfA-M17 neutral aminopeptidase, a target for new antimalarials. Proc Natl Acad Sci USA, 106(22):E56.
23. Klemba M (2009) On the location of the aminopeptidase N homolog PfA-M17 in Plasmodium falciparum. Proc Natl Acad Sci USA, 106(22):E55.
24. Goldberg DE, Slater AF, Cerami A, Henderson GB (1990) Hemoglobin degradation in the malaria parasite Plasmodium falciparum: An ordered process in a unique organelle. Proc Natl Acad Sci USA, 87(8):2931-2935.
25. Martin RE, Kirk K (2007) Transport of the essential nutrient isoleucine in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Blood, 109(5):2217-2224.
26. Leslie AG (2006) The integration of macromolecular diffraction data. Acta Crystallogr D, 62(1):48-57.
27. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr D, 62(Pt 1):72-82.
28. CCP4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr, D50:760-763.
29. Brunger AT (1993) Assessment of phase accuracy by cross validation: The free R value methods and applications. Acta Crystallogr D, 49(Pt 1):24-36.
30. Potterton E, Briggs P, TurkenburgM, Dodson E (2003) A graphical user interface to the CCP4 program suite. Acta Crystallogr D, 59(Pt 7):1131-1137.
31. Vagin A, Teplyakov A (1997) MOLREP: An automated program for molecular replacement. J Appl Crystallogr, 30:1022-1025.
32. Jaroszewski L, Rychlewski L, Li Z, Li W, Godzik A (2005) FFAS03: A server for profile-profile sequence alignments. Nucleic Acids Res, 33:W284-288 (Web Server issue).
33. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallographica, D53:240-255.
34. Brunger AT, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D, 54(Pt 5):905-921.
35. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D, 60((Part 12, number 1)):2126-2132.
36. Cohen SX, et al. (2008) ARP/wARP and molecular replacement: The next generation. Acta Crystallogr D, 64(Pt 1):49-60.
37. Potterton L, et al. (2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr D, 60((Part 12, number 1)):2288-2294.
38. Androulakis S, et al. (2008) Federated repositories of x-ray diffraction images. Acta Crystallogr D, D64(Pt 7):810-814.