Discovery and characterization of pseudocyclic cystine-knot α-amylase inhibitors with high resistance to heat and proteolytic degradation

FEBS Journal

Volumn 281, Issue 19, 2014, Pages 4351-4366

  Nguyen, Phuong Q T ^a   Wang, Shujing ^a   Kumar, Akshita ^a   Yap, Li J ^a   Luu, Thuy T ^a   Lescar, Julien ^a   Tam, James P ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

cis proline; Cystine knot; Pseudocyclics; Wrightide; amylase inhibitors

Indexed keywords

AMYLASE INHIBITOR; ANTIINFECTIVE AGENT; D4R PEPTIDE; UNCLASSIFIED DRUG; WR AI1 PEPTIDE; WR AI3 PEPTIDE; AMYLASE; ENZYME INHIBITOR; INSECT PROTEIN; PROTEIN BINDING; SOLUTION AND SOLUBILITY; VEGETABLE PROTEIN;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DRUG BINDING SITE; DRUG ISOLATION; DRUG PROTEIN BINDING; DRUG STABILITY; DRUG STRUCTURE; DRUG SYNTHESIS; HEAT TOLERANCE; HUMAN; MOLECULAR CLONING; MOLECULAR DYNAMICS; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTON NUCLEAR MAGNETIC RESONANCE; THERMOSTABILITY; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; APOCYNACEAE; CHEMISTRY; DRUG DEVELOPMENT; ENZYMOLOGY; HEAT; HYDROGEN BOND; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR DOCKING; MOLECULAR GENETICS; PLANT LEAF; PROTEIN ENGINEERING; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SOLUTION AND SOLUBILITY; TENEBRIO;

ALPHA-AMYLASES; AMINO ACID SEQUENCE; ANIMALS; APOCYNACEAE; CRYSTALLOGRAPHY, X-RAY; DRUG DISCOVERY; ENZYME INHIBITORS; HOT TEMPERATURE; HUMANS; HYDROGEN BONDING; INSECT PROTEINS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANT PROTEINS; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; SOLUTIONS; TENEBRIO;

EID: 84912006717     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12939     Document Type: Article

References (57)

1. Cheek S, Krishna SS & Grishin NV (2006) Structural classification of small, disulfide-rich protein domains. J Mol Biol 359, 215-237.
2. Pallaghy PK, Nielsen KJ, Craik DJ & Norton RS (1994) A common structural motif incorporating a cystine knot and a triple-stranded beta-sheet in toxic and inhibitory polypeptides. Protein Sci 3, 1833-1839.
3. Le Nguyen D, Heitz A, Chiche L, Castro B, Boigegrain RA, Favel A & Coletti-Previero MA (1990) Molecular recognition between serine proteases and new bioactive microproteins with a knotted structure. Biochimie 72, 431-435.
4. Craik DJ, Daly NL, Bond T & Waine C (1999) Plant cyclotides: a unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J Mol Biol 294, 1327-1336.
5. Chagolla-Lopez A, Blanco-Labran A & Patthy A (1994) A novel a-amylase inhibitor from amaranth (Amaranthus hypocondriacus) seeds. J Biol Chem 269, 23675-23680.
6. Le Berre-Anton V, Bompard-Gilles C, Payan F & Rouge P (1997) Characterization and functional properties of the alpha-amylase inhibitor (alpha-AI) from kidney bean (Phaseolus vulgaris) seeds. Biochim Biophys Acta 14, 31-40.
7. Svensson B, Fukuda K, Nielsen PK & Bønsager BC (2004) Proteinaceous alpha-amylase inhibitors. Biochim Biophys Acta 1696, 145-156.
8. Plan MR, Rosengren KJ, Sando L, Daly NL & Craik DJ (2010) Structural and biochemical characteristics of the cyclotide kalata B5 from Oldenlandia affinis. Pept Sci 94, 647-658.
9. Janssen BJC, Schirra HJ, Lay FT, Anderson MA & Craik DJ (2003) Structure of Petunia hybrida defensin 1, a novel plant defensin with five disulfide bonds. Biochemistry 42, 8214-8222.
10. Li D, Xiao Y, Xu X, Xiong X, Lu S, Liu Z, Zhu Q, Wang M, Gu X & Liang S (2004) Structure-activity relationships of hainantoxin-iv and structure determination of active and inactive sodium channel blockers. J Biol Chem 279, 37734-37740.
11. Lee S, Milescu M, Jung HH, Lee JY, Bae CH, Lee CW, Kim HH, Swartz KJ & Kim JI (2010) Solution structure of GxTX-1E, a high-affinity tarantula toxin interacting with voltage sensors in Kv2.1 potassium channels. Biochemistry 49, 5134-5142.
12. Wu WJ & Raleigh DP (1998) Local control of peptide conformation: stabilization of cis proline peptide bonds by aromatic proline interactions. Biopolymers 45, 381-394.
13. Pereira PJ, Lozanov V, Patthy A, Huber R, Bode W, Pongor S & Strobl S (1999) Specific inhibition of insect alpha-amylases: yellow meal worm alpha-amylase in complex with the amaranth alpha-amylase inhibitor at 2.0 A resolution. Structure 7, 1079-1088.
14. Bernfeld P (1955) Amylases a and b. Methods Enzymol 1, 149-158.
15. Milner-White EJ, Bell LH & Maccallum PH (1992) Pyrrolidine ring puckering in cis and trans-proline residues in proteins and polypeptides. Different puckers are favoured in certain situations. J Mol Biol 228, 725-734.
16. Mergaert P, Nikovics K, Kelemen Z, Maunoury N, Vaubert D, Kondorosi A & Kondorosi E (2003) A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 132, 161-173.
17. Jennings C, West JL, Waine C, Craik DJ & Anderson MZ (2001) Biosynthesis and insecticidal properties of plant cyclotides: the cyclic knotted proteins from Oldenlandia affinis. Proc Natl Acad Sci USA 98, 10614-10619.
18. Marahiel MA (2009) Working outside the protein-synthesis rules: insights into non-ribosomal peptide synthesis. J Pept Sci 15, 799-807.
19. Dutton JL, Renda RF, Waine C, Clark RJ, Daly NL, Jennings CV, Anderson MA & Craik DJ (2004) Conserved structural and sequence elements implicated in the processing of gene-encoded circular proteins. J Biol Chem 279, 46858-46867.
20. Mylne JS, Chan LY, Chanson AH, Daly NL, Schaefer H, Bailey TL, Nguyencong P, Cascales L & Craik DJ (2012) Cyclic peptides arising by evolutionary parallelism via asparaginyl-endopeptidase-mediated biosynthesis. Plant Cell 24, 2765-2778.
21. Nguyen GK, Zhang S, Wang W, Wong CT, Nguyen NT & Tam JP (2011) Discovery of a linear cyclotide from the bracelet subfamily and its disulfide mapping by top-down mass spectrometry. J Biol Chem 286, 44833-44844.
22. Ireland DC, Colgrave ML & Craik DJ (2006) A novel suite of cyclotides from Viola odorata: sequence variation and the implications for structure, function and stability. Biochem J 400, 1-12.
23. Nguyen GK, Lian Y, Pang EW, Nguyen PQ, Tran TD & Tam JP (2013) Discovery of linear cyclotides in monocot plant Panicum laxum of Poaceae family provides new insights into evolution and distribution of cyclotides in plants. J Biol Chem 288, 3370-3380.
24. Ling MH, Qi HY & Chi CW (1993) Protein, cDNA, and genomic DNA sequences of the towel gourd trypsin inhibitor. A squash family inhibitor. J Biol Chem 268, 810-814.
25. Colledge CJ, Hunsperger JP, Imperial JS & Hillyard DR (1992) Precursor structure of omega-conotoxin GVIA determined from a cDNA clone. Toxicon 30, 1111-1116.
26. Woodward SR, Cruz LJ, Olivera BM & Hillyard DR (1990) Constant and hypervariable regions in conotoxin propeptides. EMBO J 9, 1015-1020.
27. Nguyen GKT, Zhang S, Nguyen NTK, Nguyen PQT, Chiu MS, Hardjojo A & Tam JP (2011) Discovery and characterization of novel cyclotides originated from chimeric precursors consisting of albumin-1 chain a and cyclotide domains in the Fabaceae family. J Biol Chem 286, 24275-24287.
28. Poth AG, Colgrave ML, Lyons RE, Daly NL & Craik DJ (2011) Discovery of an unusual biosynthetic origin for circular proteins in legumes. Proc Natl Acad Sci USA 108, 10127-10132.
29. Norton RS & Pallaghy PK (1998) The cystine knot structure of ion channel toxins and related polypeptides. Toxicon 36, 1573-1583.
30. Tam JP & Lu Y-A (1997) Synthesis of large cyclic cystine-knot peptide by orthogonal coupling strategy using unprotected peptide precursor. Tetrahedron Lett 38, 5599-5602.
31. Taichi M, Hemu X, Qiu Y & Tam JP (2013) A thioethylalkylamido (TEA) thioester surrogate in the synthesis of a cyclic peptide via a tandem acyl shift. Org Lett 15, 2620-2623.
32. Wong CTT, Taichi M, Nishio H, Nishiuchi Y & Tam JP (2011) Optimal oxidative folding of the novel antimicrobial cyclotide from Hedyotis biflora requires high alcohol concentrations. Biochemitry 50, 7275-7283.
33. Tam JP, Lu Y-A & Yu Q (1999) Thia zip reaction for synthesis of large cyclic peptides: mechanisms and applications. J Am Chem Soc 121, 4316-4324.
34. Wong CTT, Rowlands DK, Wong C-H, Lo TWC, Nguyen GKT, Li H-Y & Tam JP (2012) Orally active peptidic bradykinin b1 receptor antagonists engineered from a cyclotide scaffold for inflammatory pain treatment. Angew Chem Int Ed 51, 5620-5624.
35. Kumar A, Ernst RR & Wuthrich K (1980) A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem Biophys Res Commun 95, 1-6.
36. Piotto M, Saudek V & Sklenar V (1992) Gradienttailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR 2, 661-665.
37. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J & Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6, 277-293.
38. Saether O, Craik DJ, Campbell ID, Sletten K, Juul J & Norman DG (1995) Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1. Biochemistry 34, 4147-4158.
39. Guntert P, Mumenthaler C & Wuthrich K (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 273, 283-298.
40. 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.
41. Kabsch W (2001) Integration, scaling, space-group assignment and post refinement. In International Tables for Crystallography, Volume F: Crystallography of Biological Macromolecules (Rossmann MG & Arnold E, eds), pp. 218-225. Springer, Dordrecht, Netherlands.
42. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr D 62, 72-82.
43. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D 67, 235-242.
44. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC & Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40, 658-674.
45. Langer G, Cohen SX, Lamzin VS & Perrakis A (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 3, 1171-1179.
46. Laskowski RA, MacArthur MW, Moss DS & Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26, 283-291.
47. Harvey MJ, Giupponi G & De Fabritiis G (2009) ACEMD: accelerating biomolecular dynamics in the microsecond time scale. J Chem Theory Comput 5, 1632-1639.
48. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW & Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79, 926-935.
49. Darden T, York D & Pedersen L (1993) Particle mesh Ewald - an N.Log(N) method for Ewald sums in large systems. J Chem Phys 98, 10089-10092.
50. Krautler V, Van Gunsteren WF & Hunenberger PH (2001) A fast SHAKE: algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. J Comput Chem 22, 501-508.
51. Bashford D & Case DA (2000) Generalized Born models of macromolecular solvation effects. Annu Rev Phys Chem 51, 129-152.
52. Onufriev A, Bashford D & Case DA (2000) Modification of the generalized Born model suitable for macromolecules. J Phys Chem B 104, 3712-3720.
53. Hubbard SJ & Thornton JM (1993) NACCESS. Department of Biochemistry and Molecular Biology, University College, London.
54. Humphrey W, Dalke A & Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph Model 14, 33-38.
55. Strobl S, Gomis-Rüth F-X, Maskos K, Frank G, Huber R & Glockshuber R (1997) The α-amylase from the yellow meal worm: complete primary structure, crystallization and preliminary X-ray analysis. FEBS Lett 409, 109-114.
56. Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31, 426-429.
57. Lehrer RI, Rosenman M, Harwig SSSL, Jackson R & Eisenhauer P (1991) Ultrasensitive assays for endogenous antimicrobial polypeptides. J Immunol Methods 137, 167-173.