Crystal structure of human insulin-regulated aminopeptidase with specificity for cyclic peptides

Protein Science

Volumn 24, Issue 2, 2015, Pages 190-199

  Hermans, Stefan J ^a   Ascher, David B ^a,d   Hancock, Nancy C ^a   Holien, Jessica K ^a   Michell, Belinda J ^a   Chai, Siew Yeen ^b   Morton, Craig J ^a   Parker, Michael W ^a,c  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Alzheimer's disease; aminopeptidase; catalysis; computational modeling; crystallography; cyclic peptide; insulin signaling; memory enhancers

Indexed keywords

CYCLOPEPTIDE; CYSTYL AMINOPEPTIDASE; EXOPEPTIDASE; GLUCOSE; INSULIN REGULATED AMINOPEPTIDASE; OXYTOCIN; UNCLASSIFIED DRUG; VASOPRESSIN; INSULIN; LEUCYL-CYSTINYL AMINOPEPTIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; DRUG CONFORMATION; DRUG SPECIFICITY; ENHANCER REGION; ENZYME SPECIFICITY; EXPERIMENTAL AMNESIA; GLYCOSYLATION; HUMAN; HYDROGEN BOND; MOLECULAR DOCKING; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOPHILICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT; RAT MODEL; STRUCTURE ACTIVITY RELATION; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; METABOLISM; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYSTINYL AMINOPEPTIDASE; HUMANS; INSULIN; MODELS, MOLECULAR; PEPTIDES, CYCLIC; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

EID: 84922810288     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2604     Document Type: Article

References (51)

1. Keller SR, Scott HM, Mastick CC, Aebersold R, Lienhard GE, (1995) Cloning and characterization of a novel insulin-regulated membrane aminopeptidase from Glut4 vesicles. J Biol Chem 270: 23612-23618.
2. Rogi T, Tsujimoto M, Nakazato H, Mizutani S, Tomoda Y, (1996) Human placental leucine aminopeptidase/oxytocinase. A new member of type II membrane-spanning zinc metallopeptidase family. J Biol Chem 271: 56-61.
3. Keller SR, (2004) Role of the insulin-regulated aminopeptidase IRAP in insulin action and diabetes. Biol Pharm Bull 27: 761-764.
4. Braszko JJ, Kupryszewski G, Witczuk B, Wisniewski K, (1988) Angiotensin II-(3-8)-hexapeptide affects motor activity, performance of passive avoidance and a conditioned avoidance response in rats. Neuroscience 27: 777-783.
5. Wright JW, Miller-Wing AV, Shaffer MJ, Higginson C, Wright DE, Hanesworth JM, Harding JW, (1993) Angiotensin II(3-8) (ANG IV) hippocampal binding: potential role in the facilitation of memory. Brain Res Bull 32: 497-502.
6. Pederson ES, Harding JW, Wright JW, (1998) Attenuation of scopolamine-induced spatial learning impairments by an angiotensin IV analog. Regul Pept 74: 97-103.
7. Wright JW, Stubley L, Pederson ES, Kramár EA, Hanesworth JM, Harding JW, (1999) Contributions of the brain angiotensin IV-AT4 receptor subtype system to spatial learning. J Neurosci 19: 3952-3961.
8. Pederson ES, Krishnan R, Harding JW, Wright JW, (2001) A role for the angiotensin AT4 receptor subtype in overcoming scopolamine-induced spatial memory deficits. Regul Pep 102: 147-156.
9. Albiston AL, Pederson ES, Burns P, Purcell B, Wright JW, Harding JW, Mendelsohn FA, Weisinger RS, Chai SY, (2004) Attentuation of scopolamine-induced learning deficits by LVV-hemorphin-7 in rats in the passive avoidance and Morris water maze paradigms. Behav Brain Res 154: 239-243.
10. Lee J, Albiston AL, Allen AM, Mendelsohn FA, Ping SE, Barrett GL, Murphy M, Morris MJ, McDowall SG, Chai SY, (2004) Effect of intracerebroventricular injection of AT4 receptor ligands, Nle1-angiotensin IV and LVV-hemorphin 7, on spatial learning in rats. Neuroscience 124: 341-349.
11. Albiston AL, McDowall SG, Matsacos D, Sim P, Clune E, Mustafa T, Lee J, Mendelsohn FA, Simpson RJ, Connolly LM, Chai SY, (2001) Evidence that the angiotensin IV (AT4) receptor is the enzyme insulin regulated aminopeptidase. J Biol Chem 276: 48263-48266.
12. Lee J, Mustafa T, McDowall SG, Mendelsohn FA, Brennan M, LL, Chai SY, (2003) Structure-activity study of LVV-hemorphin-7: angiotensin AT4 receptor ligand and inhibitor of insulin-regulated aminopeptidase. J Pharmacol Exper Ther 305: 205-211.
13. Lew RA, Mustafa T, Ye S, McDowall SG, Chai SY, Albiston AL, (2003) Angiotensin AT4 ligands are potent, competitive inhibitors of insulin regulated aminopeptidase (IRAP). J Neurochem 86: 344-350.
14. Fernando RN, Albiston AL, Chai SY, (2008) The insulin-regulated aminopeptidase IRAP is colocalised with GLUT4 in the mouse hippocampus-potential role in modulation of glucose uptake in neurons? Eur J Neurosci 28: 588-598.
15. Ragozzino ME, Unick KE, Gold PE, (1996) Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. Proc Natl Acad Sci USA 93: 4693-4698.
16. Thunnissen MM, Nordlund P, Haeggstrom JZ, (2001) Crystal structure of human leukotriene A(4) hydrolase, a bifuntional enzyme in inflammation. Nat Struct Biol 8: 131-135.
17. Albiston AL, Morton CJ, Ng HL, Pham V, Yeatman HR, Ye S, Fernando RN, De Bundel D, Ascher DB, Mendelsohn FA, Parker MW, Chai SY, (2008) Identification and characterization of a new cognitive enhancer based on inhibition of insulin-regulated aminopeptidase. FASEB J 22: 4209-4217.
18. Mountford S, Albiston AL, Charman WN, Ng HL, Holien JK, Parker MW, Nicolazzo JA, Thompson PE, Chai SY, (2014) Synthesis, structure-activity relationships and brain uptake of a novel series of benzopyran inhibitors of insulin-regulated aminopeptidase. J Med Chem 57: 1368-1377.
19. Albiston AL, Diwakarla S, Fernando RN, Mountford SJ, Yeatman HR, Morgan B, Pham V, Holien JK, Parker MW, Thompson PE, Chai SY, (2011) Identification and development of specific inhibitors for insulin-regulated aminopeptidase as a new class of cognitive enhancers. Br J Pharmacol 164: 37-47.
20. Holm L, Sander C, (1993) Protein structure comparison by alignment of distance matrices. J Mol Biol 233: 123-138.
21. Kochan G, Krojer T, Harvey D, Fischer R, Chen L, Vollmar M, von Delft F, Kavanagh KL, Brown MA, Bowness P, Wordsworth P, Kessler BM, Oppermann U, (2011) Crystal structures of the endoplasmic reticulum aminopeptidase-1 (ERAP1) reveal the molecular basis for N-terminal peptide trimming. Proc Natl Acad Sci USA 108: 7745-7750.
22. Nguyen TT, Chang SC, Evnouchidou I, York IA, Rock KL, Goldberg AL, Stratikos E, Stern LJ, (2011) Structural basis for antigenic peptide precursor processing by the endoplasmic reticulum aminopeptidase ERAP1. Nat Struct Mol Biol 18: 604-613.
23. Birtley JR, Saridakis E, Stratikos E, Mavridis IM, (2012) The crystal structure of human endoplasmic reticulum aminopeptidase 2 reveals the atomic basis for distinct roles in antigen processing. Biochemistry 51: 286-295.
24. Wong AHM, Zhou D, Rini JM, (2012) The X-ray crystal structure of human aminopeptidase N reveals a novel dimer and the basis for peptide processing. J Biol Chem 287: 36804-36814.
25. Wang Y, Liu C, Lin YL, Li F, (2013) Structural insights into central hypertension regulation by human aminopeptidase A. J Biol Chem 288: 25638-25645.
26. Ascher DB, Cromer BA, Morton CJ, Volitakis I, Cherny RA, Albiston AL, Chai SY, Parker MW, (2011) Regulation of insulin-regulated membrane aminopeptidase activity by its C-terminal domain. Biochemistry 50: 2611-2622.
27. Sardinia MF, Hanesworth JM, Krebs LT, Harding JW, (1993) AT4 receptor binding characteristics: D-amino acid- and glycine-substituted peptides. Peptides 14: 949-954.
28. Matsumoto H, Rogi T, Yamashiro K, Kodama S, Tsuruoka N, Hattori A, Takio K, Mizutani S, 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.
29. Sardinia MF, Hanesworth JM, Krishnan F, Harding JW, (1994) AT4 receptor structure-binding relationship: N-terminal-modified angiotensin IV analogues. Peptides 15: 1399-1406.
30. Krishnan R, Hanesworth JM, Wright JW, Harding JW, (1999) Structure-binding studies of the adrenal AT4 receptor: analysis of position two- and three-modified angiotensin IV analogs. Peptides 20: 915-920.
31. Laustsen PG, Vang S, Kristensen T, (2001) Mutational analysis of the active site of human insulin-regulated aminopeptidase. Eur J Biochem 268: 98-104.
32. Zervoudi E, Papakyriakou A, Georgiadou D, Evnouchidou I, Gajda A, Poreba M, Salvesen GS, Drag M, Hattori A, Swevers L, Vourloumis D, Stratikos E, (2011). Probing the S1 specificity pocket of the aminopeptidases that generate antigenic peptides. Biochem J 435: 411-420.
33. Ye S, Chai SY, Lew RA, Ascher DB, Morton CJ, Parker MW, Albiston AL, (2008) Identification of modulating residues defining the catalytic cleft of insulin-regulated aminopeptidase. Biochem. Cell Biol 86: 251-261.
34. Crowley PB, Golovin A, (2005) Cation-π interactions in protein-protein interfaces. Proteins 59: 231-239.
35. Herbst JJ, Ross SA, Scott HM, Bobin SA, Morris NJ, Lienhard GE, Keller SR, (1997) Insulin stimulates cell surface aminopeptidase activity toward vasopressin in adipocytes. Am J Physiol 272: E600-606.
36. Matsumoto H, Hattori A, Mizutani S, Tsujimoto M, Cleavage of peptide hormones by placental leucine aminopeptidase/oxytocinase. In:, Mizutani S, Turner AJ, Nomura S, Ino K, Eds. (2001) Cell-surface aminopeptidases: basic and clinical aspects. Amsterdam: Elsevier Science BV, pp 295-299.
37. Matsumoto H, Nagasaka T, Hattori A, Rogi T, Tsuruoka N, Mizutani S, Tsujimoto M, (2001) Expression of placental leucine aminopeptidase/oxytocinase in neuronal cells and its action on neuronal peptides. Eur J Biochem 268: 3259-3266.
38. Albiston AL, Pham V, Ye S, Ng HL, Lew RA, Thompson PE, Holien JK, Morton CJ, Parker MW, Chai SY, (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.
39. Wallis MG, Lankford MF, Keller SR, (2007) Vasopressin is a physiological substrate for the insulin-regulated aminopeptidase IRAP. Am J Physiol Endocrinol Metab 293: E1092-E1102.
40. Albiston AL, Fernando RN, Yeatman HR, Burns P, Ng HL, Daswani D, Diwakarla S, Pham V, Chai SY, (2010) Gene knockout of insulin-regulated aminopeptidase: loss of the specific binding site for angiotensin IV and age-related deficit in spatial memory. Neurobiol Learn Mem 93: 19-30.
41. Engelmann M, Wotjak CT, Neumann I, Ludwig M, Landgraf R, (1996) Behavioral consequences of intracerebral vasopressin and oxytocin: focus on learning and memory. Neurosci Biobehav Rev 20: 341-358.
42. Andersson H, Hallberg M, (2012) Discovery of inhibitors of insulin-regulated aminopeptidase as cognitive enhancers. Int J Hypertens 2012: 789671.
43. McPhillips TM, McPhillips SE, Chiu HJ, Cohen AE, Deacon AM, Ellis PJ, Garman E, Gonzalez A, Sauter NK, Phizackerley RP, Soltis SM, Kuhn P, (2002) Blu-Ice and the distributed control system: software for data acquisition and instrument control at macromolecular crystallography beamlines. J Synchrotron Radiat 9: 401-406.
44. Kabsch W, (2010) XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132.
45. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS, (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242.
46. Matthews BW, (1968) Solvent content of protein crystals. J Mol Biol 33: 491-497.
47. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ, (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
48. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
49. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
50. Bricogne G, Blanc E, Brandl M, Flensburg C, Keller P, Paciorek W, Roversi P, Sharff A, Smart O, Vonrhein C, Womack T, (2011) BUSTER, Version 1.10.0. Cambridge, United Kingdom: Global Phasing, Ltd.
51. DeLano WL, (2002) The PYMOL user's manual. San Carlos, CA: Delano Scientific.