Potent inhibitors of human matriptase-1 based on the scaffold of sunflower trypsin inhibitor

Journal of Peptide Science

Volumn 20, Issue 6, 2014, Pages 415-420

  Fittler, Heiko ^a   Avrutina, Olga ^a   Empting, Martin ^b   Kolmar, Harald ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

Bowman Birk inhibitors; human matriptase 1; rational design; SFTI 1

Indexed keywords

ASPARTIC ACID; GLYCINE; MACROCYCLIC COMPOUND; MATRIPTASE; PLANT EXTRACT; PROLINE; SUNFLOWER TRYPSIN INHIBITOR 1; TRYPSIN INHIBITOR; UNCLASSIFIED DRUG; CYCLOPEPTIDE; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; SFTI-1 PEPTIDE, SUNFLOWER; ST14 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CYCLIZATION; DISULFIDE BOND; DRUG ACTIVITY; DRUG STRUCTURE; HUMAN; NONHUMAN; PRIORITY JOURNAL; SUNFLOWER; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; METABOLISM; STRUCTURE ACTIVITY RELATION;

HELIANTHUS;

DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PEPTIDES, CYCLIC; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84900500098     PISSN: 10752617     EISSN: 10991387     Source Type: Journal    
DOI: 10.1002/psc.2629     Document Type: Article

References (37)

1. Miller GS, List K,. The matriptase-prostasin proteolytic cascade in epithelial development and pathology. Cell Tissue Res. 2013; 351: 245-253.
2. Oberst MD, Chen LY, Kiyomiya K, Williams CA, Lee MS, Johnson MD, Dickson RB, Lin CY,. HAI-1 regulates activation and expression of matriptase, a membrane-bound serine protease. Am. J. Physiol. Cell Physiol. 2005; 289: C462-470.
3. Szabo R, Hobson JP, List K, Molinolo A, Lin CY, Bugge TH,. Potent inhibition and global co-localization implicate the transmembrane Kunitz-type serine protease inhibitor hepatocyte growth factor activator inhibitor-2 in the regulation of epithelial matriptase activity. J. Biol. Chem. 2008; 283: 29495-29504.
4. Oberst MD, Johnson MD, Dickson RB, Lin CY, Singh B, Stewart M, Williams A, al-Nafussi A, Smyth JF, Gabra H, Sellar GC,. Expression of the serine protease matriptase and its inhibitor HAI-1 in epithelial ovarian cancer: correlation with clinical outcome and tumor clinicopathological parameters. Clin. Cancer Res. 2002; 8: 1101-1107.
5. Seitz I, Hess S, Schulz H, Eckl R, Busch G, Montens HP, Brandl R, Seidl S, Schomig A, Ott I,. Membrane-type serine protease-1/matriptase induces interleukin-6 and -8 in endothelial cells by activation of protease-activated receptor-2: potential implications in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2007; 27: 769-775.
6. Milner JM, Patel A, Davidson RK, Swingler TE, Desilets A, Young DA, Kelso EB, Donell ST, Cawston TE, Clark IM, Ferrell WR, Plevin R, Lockhart JC, Leduc R, Rowan AD,. Matriptase is a novel initiator of cartilage matrix degradation in osteoarthritis. Arthritis Rheum. 2010; 62: 1955-1966.
7. Kang JY, Dolled-Filhart M, Ocal IT, Singh B, Lin CY, Dickson RB, Rimm DL, Camp RL,. Tissue microarray analysis of hepatocyte growth factor/Met pathway components reveals a role for Met, matriptase, and hepatocyte growth factor activator inhibitor 1 in the progression of node-negative breast cancer. Cancer Res. 2003; 63: 1101-1105.
8. Saleem M, Adhami VM, Zhong W, Longley BJ, Lin CY, Dickson RB, Reagan-Shaw S, Jarrard DF, Mukhtar H,. A novel biomarker for staging human prostate adenocarcinoma: overexpression of matriptase with concomitant loss of its inhibitor, hepatocyte growth factor activator inhibitor-1. Cancer Epidemiol. Biomarkers Prev. 2006; 15: 217-227.
9. Santin AD, Cane S, Bellone S, Bignotti E, Palmieri M, De Las Casas LE, Anfossi S, Roman JJ, O'Brien T, Pecorelli S,. The novel serine protease tumor-associated differentially expressed gene-15 (matriptase/MT-SP1) is highly overexpressed in cervical carcinoma. Cancer 2003; 98: 1898-1904.
10. Lee JW, Yong Song S, Choi JJ, Lee SJ, Kim BG, Park CS, Lee JH, Lin CY, Dickson RB, Bae DS,. Increased expression of matriptase is associated with histopathologic grades of cervical neoplasia. Hum. Pathol. 2005; 36: 626-633.
11. Gao L, Liu M, Dong N, Jiang Y, Lin CY, Huang M, Wu D, Wu Q,. Matriptase is highly upregulated in chronic lymphocytic leukemia and promotes cancer cell invasion. Leukemia 2013; 27: 1191-1194.
12. Colombo E, Desilets A, Duchene D, Chagnon F, Najmanovich R, Leduc R, Marsault E,. Design and synthesis of potent, selective inhibitors of matriptase. Acs Medicinal Chemistry Letters 2012; 3: 530-534.
13. Uhland K, Siphos B, Arkona C, Schuster M, Petri B, Steinmetzer P, Mueller F, Schweinitz A, Steinmetzer T, Van De Locht A,. Use of IHC and newly designed matriptase inhibitors to elucidate the role of matriptase in pancreatic ductal adenocarcinoma. Int. J. Oncol. 2009; 35: 347-357.
14. Glotzbach B, Reinwarth M, Weber N, Fabritz S, Tomaszowski M, Fittler H, Christmann A, Avrutina O, Kolmar H,. Combinatorial optimization of cystine-knot peptides towards high-affinity inhibitors of human matriptase-1. Plos One 2013; 8: e76956.
15. Laskowski Jr M, Kato I,. Protein inhibitors of proteinases. Annu. Rev. Biochem. 1980; 49: 593-626.
16. Jaulent AM, Brauer AB, Matthews SJ, Leatherbarrow RJ,. Solution structure of a novel C2-symmetrical bifunctional bicyclic inhibitor based on SFTI-1. J. Biomol. NMR 2005; 33: 57-62.
17. Daly NL, Chen YK, Foley FM, Bansal PS, Bharathi R, Clark RJ, Sommerhoff CP, Craik DJ,. The absolute structural requirement for a proline in the P3'-position of Bowman-Birk protease inhibitors is surmounted in the minimized SFTI-1 scaffold. J. Biol. Chem. 2006; 281: 23668-23675.
18. Tischler M, Nasu D, Empting M, Schmelz S, Heinz DW, Rottmann P, Kolmar H, Buntkowsky G, Tietze D, Avrutina O,. Braces for the peptide backbone: insights into structure-activity relationships of protease inhibitor mimics with locked amide conformations. Angew. Chem. Int. Ed. Engl. 2012; 51: 3708-3712.
19. Debowski D, Lukajtis R, Filipowicz M, Strzelecka P, Wysocka M, Legowska A, Lesner A, Rolka K,. Hybrid analogues of SFTI-1 modified in P1 position by beta- and gamma-amino acids and N-substituted beta-alanines. Biopolymers 2013; 100: 154-159.
20. Luckett S, Garcia RS, Barker JJ, Konarev AV, Shewry PR, Clarke AR, Brady RL,. High-resolution structure of a potent, cyclic proteinase inhibitor from sunflower seeds. J. Mol. Biol. 1999; 290: 525-533.
21. Fittler H, Avrutina O, Glotzbach B, Empting M, Kolmar H,. Combinatorial tuning of peptidic drug candidates: high-affinity matriptase inhibitors through incremental structure-guided optimization. Org. Biomol. Chem. 2013; 11: 1848-1857.
22. Quimbar P, Malik U, Sommerhoff CP, Kaas Q, Chan LY, Huang YH, Grundhuber M, Dunse K, Craik DJ, Anderson MA, Daly NL,. High-affinity cyclic peptide matriptase inhibitors. J. Biol. Chem. 2013; 288: 13885-13896.
23. Rafal L, Anna L, Magdalena W, Dawid D, Adam L, Krzysztof R,. Analogues of trypsin inhibitor SFTI-1 modified in the conserved P(1)' position by synthetic or non-proteinogenic amino acids retain their inhibitory activity. J. Pept. Sci. 2011; 17: 281-287.
24. McBride JD, Freeman HN, Leatherbarrow RJ,. Selection of human elastase inhibitors from a conformationally constrained combinatorial peptide library. Eur. J. Biochem. 1999; 266: 403-412.
25. Swedberg JE, de Veer SJ, Sit KC, Reboul CF, Buckle AM, Harris JM,. Mastering the canonical loop of serine protease inhibitors: enhancing potency by optimising the internal hydrogen bond network. Plos One 2011; 6: e19302.
26. Hilpert K, Hansen G, Wessner H, Volkmer-Engert R, Hohne W,. Complete substitutional analysis of a sunflower trypsin inhibitor with different serine proteases. J. Biochem. 2005; 138: 383-390.
27. Legowska A, Debowski D, Lesner A, Wysocka M, Rolka K,. Introduction of non-natural amino acid residues into the substrate-specific P1 position of trypsin inhibitor SFTI-1 yields potent chymotrypsin and cathepsin G inhibitors. Bioorg. Med. Chem. 2009; 17: 3302-3307.
28. Rothemund S, Sonnichsen FD, Polte T,. Therapeutic potential of the peptide leucine arginine as a new nonplant Bowman-Birk-like serine protease inhibitor. J. Med. Chem. 2013; 56: 6732-6744.
29. Fittler H, Avrutina O, Glotzbach B, Empting M, Kolmar H,. Combinatorial tuning of peptidic drug candidates: high-affinity matriptase inhibitors through incremental structure-guided optimization. Organic & biomolecular chemistry 2013; 11: 1848-1857.
30. Avrutina O, Fittler H, Glotzbach B, Kolmar H, Empting M,. Between two worlds: a comparative study on in vitro and in silico inhibition of trypsin and matriptase by redox-stable SFTI-1 variants at near physiological pH. Organic biomolecular chemistry 2012; 10: 7753-7762.
31. Lesner A, Karna N, Psurski M, Legowska A, Wysocka M, Guzow K, Sieradzan A, Sienczyk M, Trzonkowski P, Pikula M, Zielinski M, Kosikowska P, Lukajtis R, Legowska M, Debowski D, Wiczk W, Rolka K,. Fluorescent analogs of trypsin inhibitor SFTI-1 isolated from sunflower seeds-synthesis and applications. Biopolymers 2014; 102: 124-135.
32. Yuan C, Chen L, Meehan EJ, Daly N, Craik DJ, Huang M, Ngo JC,. Structure of catalytic domain of Matriptase in complex with Sunflower trypsin inhibitor-1. Bmc Struct. Biol. 2011; 11: 30.
33. Quimbar P, Malik U, Sommerhoff CP, Kaas Q, Chan LY, Huang Y-H, Grundhuber M, Dunse K, Craik DJ, Anderson Ma, Daly NL,. High-affinity cyclic peptide matriptase inhibitors. The Journal of biological chemistry 2013; 288: 13885-13896.
34. Li P, Jiang S, Lee S-L, Lin CY, Johnson MD, Dickson RB, Michejda CJ, Roller PP,. Design and synthesis of novel and potent inhibitors of the type II transmembrane serine protease, matriptase, based upon the sunflower trypsin inhibitor-1. J. Med. Chem. 2007; 50: 5976-5983.
35. Jullian M, Hernandez A, Maurras A, Puget K, Amblard M, Martinez J, Subra G,. N-terminus FITC labeling of peptides on solid support: the truth behind the spacer. Tetrahedron Lett. 2009; 50: 260-263.
36. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang J, Kollman P,. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 2003; 24: 1999-2012.
37. Krieger E, Joo K, Lee J, Raman S, Thompson J, Tyka M, Baker D, Karplus K,. Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins 2009; 77 (Suppl 9): 114-122.