Potent and specific inhibition of the biological activity of the type-II transmembrane serine protease matriptase by the cyclic microprotein MCoTI-II

Thrombosis and Haemostasis

Volumn 112, Issue 2, 2014, Pages 402-411

  Gray, Kelly ^a   Elghadban, Salma ^a   Thongyoo, Panumart ^b   Owen, Kate A ^a   Szabo, Roman ^c   Bugge, Thomas H ^c   Tate, Edward W ^b   Leatherbarrow, Robin J ^b   Ellis, Vincent ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

Cyclotide; Epithelial cell; Hepatocyte growth factor; Matriptase; Protease inhibitor; Serine protease; Tight junctions

Indexed keywords

MATRIPTASE; SERINE PROTEINASE; CYCLOTIDE; PRO-HEPATOCYTE GROWTH FACTOR; PROSTASIN; PROTEIN PRECURSOR; SCATTER FACTOR; SERINE PROTEINASE INHIBITOR; ST14 PROTEIN, HUMAN; TRYPSIN INHIBITOR MCOTI-II;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTRIC RESISTANCE; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNTHESIS; ANIMAL; CELL MOTION; COMPARATIVE STUDY; DOG; DRUG EFFECTS; ENZYME SPECIFICITY; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; IMPEDANCE; MALE; MDCK CELL LINE; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PROSTATE TUMOR; TIGHT JUNCTION; TIME FACTOR; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CYCLOTIDES; DOGS; ELECTRIC IMPEDANCE; HEK293 CELLS; HEPATOCYTE GROWTH FACTOR; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MALE; MOLECULAR TARGETED THERAPY; NEOPLASM INVASIVENESS; PROSTATIC NEOPLASMS; PROTEIN PRECURSORS; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS; SUBSTRATE SPECIFICITY; TIGHT JUNCTIONS; TIME FACTORS; TRANSFECTION;

EID: 84905191677     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH13-11-0895     Document Type: Article

References (52)

1. Ellis V, Murphy G. Cellular strategies for proteolytic targeting during migration and invasion. FEBS Lett 2001; 506: 1-5.
2. Qiu D, Owen K, Gray K, et al. Roles and regulation of membrane-associated serine proteases. Biochem Soc Trans 2007; 35: 583-587.
3. Szabo R, Wu Q, Dickson RB, et al. Type II transmembrane serine proteases. Thromb Haemost 2003; 90: 185-193.
4. Kang JY, Dolled-Filhart M, Ocal IT, et al. 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.
5. Riddick AC, Shukla CJ, Pennington CJ, et al. Identification of degradome components associated with prostate cancer progression by expression analysis of human prostatic tissues. Br J Cancer 2005; 92: 2171-2180.
6. List K, Szabo R, Molinolo A, et al. Deregulated matriptase causes ras-independent multistage carcinogenesis and promotes ras-mediated malignant transformation. Genes Dev 2005; 19: 1934-1950.
7. Szabo R, Rasmussen AL, Moyer AB, et al. c-Met-induced epithelial carcinogenesis is initiated by the serine protease matriptase. Oncogene 2011; 30: 2003-2016.
8. List K, Haudenschild CC, Szabo R, et al. Matriptase/MT-SP1 is required for postnatal survival, epidermal barrier function, hair follicle development, and thymic homeostasis. Oncogene 2002; 21: 3765-3779.
9. Basel-Vanagaite L, Attia R, Ishida-Yamamoto A, et al. Autosomal recessive ichthyosis with hypotrichosis caused by a mutation in ST14, encoding type II transmembrane serine protease matriptase. Am J Hum Genet 2007; 80: 467-477.
10. List K, Kosa P, Szabo R, et al. Epithelial integrity is maintained by a matriptasedependent proteolytic pathway. Am J Pathol 2009; 175: 1453-1463.
11. Buzza MS, Netzel-Arnett S, Shea-Donohue T, et al. Membrane-anchored serine protease matriptase regulates epithelial barrier formation and permeability in the intestine. Proc Natl Acad Sci USA 2010; 107: 4200-4205.
12. Takeuchi T, Harris JL, Huang W, et al. Cellular localization of membrane-type serine protease 1 and identification of protease-activated receptor-2 and singlechain urokinase-type plasminogen activator as substrates. J Biol Chem 2000; 275: 26333-26342.
13. Owen KA, Qiu D, Alves J, et al. Pericellular activation of hepatocyte growth factor by the transmembrane serine proteases matriptase and hepsin, but not by the membrane-associated protease uPA. Biochem J 2010; 426: 219-228.
14. Lee SL, Dickson RB, Lin CY. Activation of hepatocyte growth factor and Urokinase/Plasminogen activator by matriptase, an epithelial membrane serine protease. J Biol Chem 2000; 275: 36720-36725.
15. Kilpatrick LM, Harris RL, Owen KA, et al. Initiation of plasminogen activation on the surface of monocytes expressing the type II transmembrane serine protease matriptase. Blood 2006; 108: 2616-2623.
16. Netzel-Arnett S, Currie BM, Szabo R, et al. Evidence for a matriptase-prostasin proteolytic cascade regulating terminal epidermal differentiation. J Biol Chem 2006; 281: 32941-32945.
17. Bugge TH, Antalis TM, Wu Q. Type II transmembrane serine proteases. J Biol Chem 2009; 284: 23177-23181.
18. Kirchhofer D, Peek M, Lipari MT, et al. Hepsin activates pro-hepatocyte growth factor and is inhibited by hepatocyte growth factor activator inhibitor-1B (HAI-1B) and HAI-2. FEBS Lett 2005; 579: 1945-1950.
19. Moran P, Li W, Fan B, et al. Pro-urokinase-type plasminogen activator is a substrate for hepsin. J Biol Chem 2006; 281: 30439-30446.
20. Chen MQ, Chen LM, Lin CY, et al. Hepsin activates prostasin and cleaves the extracellular domain of the epidermal growth factor receptor. Mol Cell Biochem 2010; 337: 259-266.
21. Hopkins AL, Groom CR. The druggable genome. Nat Rev Drug Discov 2002; 1: 727-730.
22. Overall CM, Lopez-Otin C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2002; 2: 657-672.
23. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002; 295: 2387-2392.
24. Werle M, Kafedjiiski K, Kolmar H, et al. Evaluation and improvement of the properties of the novel cystine-knot microprotein McoEeTI for oral administration. Intern J Pharmaceut 2007; 332: 72-79.
25. Thongyoo P, Tate EW, Leatherbarrow RJ. Total synthesis of the macrocyclic cysteine knot microprotein MCoTI-II. Chem Commun 2006; 2848-2850.
26. Thongyoo P, Jaulent AM, Tate EW, et al. Immobilized protease-assisted synthesis of engineered cysteine-knot microproteins. Chembiochem 2007; 8: 1107-1109.
27. Thongyoo P, Bonomelli C, Leatherbarrow RJ, et al. Potent inhibitors of betatryptase and human leukocyte elastase based on the MCoTI-II scaffold. J Med Chem 2009; 52: 6197-6200.
28. Dukes JD, Whitley P, Chalmers AD. The MDCK variety pack: choosing the right strain. BMC Cell Biology 2011; 12: 43.
29. Förbs D, Thiel S, Stella MC, et al. In vitro inhibition of matriptase prevents invasive growth of cell lines of prostate and colon carcinoma. Int J Oncol 2005; 27: 1061-1070.
30. Nigam SK, Rodriguez-Boulan E, Silver RB. Changes in intracellular calcium during the development of epithelial polarity and junctions. PNAS 1992; 89: 6162-6166.
31. Deu E, Verdoes M, Bogyo M. New approaches for dissecting protease functions to improve probe development and drug discovery. Nat Struct Mol Biol 2012; 19: 9-16.
32. Bode W, Turk D, Karshikov A. The refined 1. 9-Å X-ray crystal structure of d-Phe-Pro-Arg chloromethylketone-inhibited human α-thrombin: Structure analysis, overall structure, electrostatic properties, detailed active-site geometry, and structure-function relationships. Protein Sci 1992; 1: 426-471.
33. Friedrich R, Fuentes-Prior P, Ong E, et al. Catalytic domain structures of MTSP1/matriptase, a matrix-degrading transmembrane serine proteinase. J Biol Chem 2002; 277: 2160-2168.
34. Quimbar P, Malik U, Sommerhoff CP, et al. High-affinity cyclic peptide matriptase inhibitors. J Biol Chem 2013; 288: 13885-13896.
35. Stoop AA, Craik CS. Engineering of a macromolecular scaffold to develop specific protease inhibitors. Nat Biotechnol 2003; 21: 1063-1068.
36. Desilets A, Longpre JM, Beaulieu ME, et al. Inhibition of human matriptase by eglin c variants. FEBS Lett 2006; 580: 2227-2232.
37. Li P, Jiang S, Lee SL, et al. 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.
38. Fittler H, Avrutina O, Glotzbach B, et al. Combinatorial tuning of peptidic drug candidates: high-affinity matriptase inhibitors through incremental structureguided optimization. Orga Biomol Chem 2013; 11: 1848-1857.
39. Salameh MA, Soares AS, Navaneetham D, et al. Determinants of Affinity and Proteolytic Stability in Interactions of Kunitz Family Protease Inhibitors with Mesotrypsin. J Biol Chem 2010; 285: 36884-36896.
40. Galkin AV, Mullen L, Fox WD, et al. CVS-3983, a selective matriptase inhibitor, suppresses the growth of androgen independent prostate tumor xenografts. Prostate 2004; 61: 228-235.
41. Steinmetzer T, Schweinitz A, Sturzebecher A, et al. Secondary amides of sulfonylated 3-amidinophenylalanine. New potent and selective inhibitors of matriptase. J Med Chem 2006; 49: 4116-4126.
42. Xu ZH, Chen YW, Battu A, et al. Targeting zymogen activation to control the matriptase-prostasin proteolytic cascade. J Med Chem 2011; 54: 7567-7578.
43. Szabo R, Hobson JP, Christoph K, et al. Regulation of cell surface protease matriptase by HAI2 is essential for placental development, neural tube closure and embryonic survival in mice. Development 2009; 136: 2653-2663.
44. Delaria KA, Muller DK, Marlor CW, et al. Characterization of placental bikunin, a novel human serine protease inhibitor. J Biol Chem 1997; 272: 12209-12214.
45. Scudamore CL, Jepson MA, Hirst BH, et al. The rat mucosal mast cell chymase, RMCP-II, alters epithelial cell monolayer permeability in association with altered distribution of the tight junction proteins ZO-1 and occludin. Eur J Cell Biol 1998; 75: 321-330.
46. Willemsen LEM, Hoetjes JP, Van Deventer SJH, et al. Abrogation of IFN-gamma mediated epithelial barrier disruption by serine protease inhibition. Clin Exp Immunol 2005; 142: 275-284.
47. Buzza MS, Martin EW, Driesbaugh KH, et al. Prostasin Is Required for Matriptase Activation in Intestinal Epithelial Cells to Regulate Closure of the Paracellular Pathway. J Biol Chem 2013; 288: 10328-10337.
48. Tripathi M, Potdar AA, Yamashita H, et al. Laminin-332 cleavage by matriptase alters motility parameters of prostate cancer cells. Prostate 2011; 71: 184-196.
49. Chen YW, Wang JK, Chou FP, et al. Regulation of the matriptase-prostasin cell surface proteolytic cascade by hepatocyte growth factor activator inhibitor-1 during epidermal differentiation. J Biol Chem 2010; 285: 31755-31762.
50. Tseng IC, Xu H, Chou FP, et al. Matriptase activation, an early cellular response to acidosis. J Biol Chem 2010; 285: 3261-3270.
51. Friis S, Uzzun Sales K, Godiksen S, et al. A matriptase-prostasin reciprocal zymogen activation complex with unique features: Prostasin as a non-enzymatic co-factor for matriptase activation. J Biol Chem 2013; 288: 19028-19039.
52. Kosa P, Szabo R, Molinolo AA, et al. Suppression of Tumorigenicity-14, encoding matriptase, is a critical suppressor of colitis and colitis-associated colon carcinogenesis. Oncogene 2012; 31: 3679-3695.