Using the MCoTI-II Cyclotide Scaffold to Design a Stable Cyclic Peptide Antagonist of SET, a Protein Overexpressed in Human Cancer

Biochemistry

Volumn 55, Issue 2, 2016, Pages 396-405

  D'Souza, Charlotte ^a   Henriques, Sónia Troeira ^a   Wang, Conan K ^a   Cheneval, Olivier ^a   Chan, Lai Yue ^a   Bokil, Nilesh J ^a   Sweet, Matthew J ^a   Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CELL CULTURE; CELL SIGNALING; CELLS; CYTOTOXICITY; DISEASES; DRUG THERAPY; ENZYME INHIBITION; GENE THERAPY; GRAFTING (CHEMICAL); ONCOLOGY; PROTEINS; SCAFFOLDS (BIOLOGY);

APOLIPOPROTEIN E (APOE); LIPOPOLYSACCHARIDES; NUCLEAR FACTOR KAPPAB; PROTEIN PHOSPHATASE 2A; PROTEOLYTIC STABILITY; SIGNALING PATHWAYS; THERAPEUTIC POTENTIALS; TUMOR SUPPRESSOR GENES;

PEPTIDES;

ANTINEOPLASTIC AGENT; COG 1410; COG PEPTIDE; CYCLOPEPTIDE; CYCLOTIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MOMORDICA COCHINCHINENSIS TRYPSIN INHIBITOR II; NUCLEAR PROTEIN; PEPTIDE ANTAGONIST; PROTEIN INHIBITOR; SET PROTEIN; UNCLASSIFIED DRUG; APOLIPOPROTEIN E; CHAPERONE; PHOSPHOPROTEIN PHOSPHATASE 2; SET PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRYPSIN INHIBITOR MCOTI-II;

ANIMAL CELL; ARTICLE; CANCER CELL; CANCER CELL LINE; CANCER THERAPY; CONTROLLED STUDY; CYTOTOXICITY; DRUG BIOAVAILABILITY; DRUG DESIGN; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SERUM; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PROMOTER REGION; TUMOR CELL LINE;

APOLIPOPROTEINS E; CELL LINE, TUMOR; CELL SURVIVAL; CYCLOTIDES; HISTONE CHAPERONES; HUMANS; MAGNETIC RESONANCE IMAGING; NF-KAPPA B; PEPTIDES, CYCLIC; PROMOTER REGIONS, GENETIC; PROTEIN PHOSPHATASE 2; TRANSCRIPTION FACTORS;

EID: 84955499376     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00529     Document Type: Article

References (62)

1. Cristobal, I., Garcia-Orti, L., Cirauqui, C., Cortes-Lavaud, X., Garcia-Sanchez, M. A., Calasanz, M. J., and Odero, M. D. (2012) Overexpression of SET is a recurrent event associated with poor outcome and contributes to protein phosphatase 2A inhibition in acute myeloid leukemia Haematologica 97, 543-550 10.3324/haematol.2011.050542
2. Cervoni, N., Detich, N., Seo, S. B., Chakravarti, D., and Szyf, M. (2002) The oncoprotein Set/TAF-1beta, an inhibitor of histone acetyltransferase, inhibits active demethylation of DNA, integrating DNA methylation and transcriptional silencing J. Biol. Chem. 277, 25026-25031 10.1074/jbc.M202256200
3. Compagnone, N. A., Zhang, P., Vigne, J. L., and Mellon, S. H. (2000) Novel role for the nuclear phosphoprotein SET in transcriptional activation of P450c17 and initiation of neurosteroidogenesis Mol. Endocrinol. 14, 875-888 10.1210/mend.14.6.0469
4. Christensen, D. J., Chen, Y. W., Oddo, J., Matta, K. M., Neil, J., Davis, E. D., Volkheimer, A. D., Lanasa, M. C., Friedman, D. R., Goodman, B. K., Gockerman, J. P., Diehl, L. F., de Castro, C. M., Moore, J. O., Vitek, M. P., and Weinberg, J. B. (2011) SET oncoprotein overexpression in B-cell chronic lymphocytic leukemia and non-Hodgkin lymphoma: A predictor of aggressive disease and a new treatment target Blood 118, 4150-4158 10.1182/blood-2011-04-351072
5. Saito, S., Miyaji-Yamaguchi, M., Shimoyama, T., and Nagata, K. (1999) Functional domains of template-activating factor-I as a protein phosphatase 2A inhibitor Biochem. Biophys. Res. Commun. 259, 471-475 10.1006/bbrc.1999.0790
6. Janssens, V. and Goris, J. (2001) Protein phosphatase 2A: A highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling Biochem. J. 353, 417-439 10.1042/bj3530417
7. Li, M., Makkinje, A., and Damuni, Z. (1996) The myeloid leukemia-associated protein SET is a potent inhibitor of protein phosphatase 2A J. Biol. Chem. 271, 11059-11062 10.1074/jbc.271.19.11059
8. Liu, H., Gu, Y. X., Yin, J., Zheng, G. P., Wang, C. K., Zhang, Z. J., Deng, M., Liu, J. F., Jia, X. T., and He, Z. M. (2014) SET-mediated NDRG1 inhibition is involved in acquisition of epithelial-to-mesenchymal transition phenotype and cisplatin resistance in human lung cancer cell Cell. Signalling 26, 2710-2720 10.1016/j.cellsig.2014.08.010
9. Rincon, R., Cristobal, I., Zazo, S., Arpi, O., Menendez, S., Manso, R., Lluch, A., Eroles, P., Rovira, A., Albanell, J., Garcia-Foncillas, J., Madoz-Gurpide, J., and Rojo, F. (2015) PP2A inhibition determines poor outcome and doxorubicin resistance in early breast cancer and its activation shows promising therapeutic effects Oncotarget 6, 4299-4314 10.18632/oncotarget.3012
10. Switzer, C. H., Cheng, R. Y., Vitek, T. M., Christensen, D. J., Wink, D. A., and Vitek, M. P. (2011) Targeting SET/I(2)PP2A oncoprotein functions as a multi-pathway strategy for cancer therapy Oncogene 30, 2504-2513 10.1038/onc.2010.622
11. Christensen, D. J., Ohkubo, N., Oddo, J., Van Kanegan, M. J., Neil, J., Li, F., Colton, C. A., and Vitek, M. P. (2011) Apolipoprotein E and peptide mimetics modulate inflammation by binding the SET protein and activating protein phosphatase 2A J. Immunol. 186, 2535-2542 10.4049/jimmunol.1002847
12. Singh, K., Chaturvedi, R., Asim, M., Barry, D. P., Lewis, N. D., Vitek, M. P., and Wilson, K. T. (2008) The apolipoprotein E-mimetic peptide COG112 inhibits the inflammatory response to Citrobacter rodentium in colonic epithelial cells by preventing NF-kappaB activation J. Biol. Chem. 283, 16752-16761 10.1074/jbc.M710530200
13. Singh, K., Chaturvedi, R., Barry, D. P., Coburn, L. A., Asim, M., Lewis, N. D., Piazuelo, M. B., Washington, M. K., Vitek, M. P., and Wilson, K. T. (2011) The apolipoprotein E-mimetic peptide COG112 inhibits NF-kappaB signaling, proinflammatory cytokine expression, and disease activity in murine models of colitis J. Biol. Chem. 286, 3839-3850 10.1074/jbc.M110.176719
14. Li, F. Q., Sempowski, G. D., McKenna, S. E., Laskowitz, D. T., Colton, C. A., and Vitek, M. P. (2006) Apolipoprotein E-derived peptides ameliorate clinical disability and inflammatory infiltrates into the spinal cord in a murine model of multiple sclerosis J. Pharmacol. Exp. Ther. 318, 956-965 10.1124/jpet.106.103671
15. Laskowitz, D. T., Fillit, H., Yeung, N., Toku, K., and Vitek, M. P. (2006) Apolipoprotein E-derived peptides reduce CNS inflammation: Implications for therapy of neurological disease Acta Neurol. Scand. 114, 15-20 10.1111/j.1600-0404.2006.00680.x
16. Laskowitz, D. T., McKenna, S. E., Song, P., Wang, H., Durham, L., Yeung, N., Christensen, D., and Vitek, M. P. (2007) COG1410, a novel apolipoprotein E-based peptide, improves functional recovery in a murine model of traumatic brain injury J. Neurotrauma 24, 1093-1107 10.1089/neu.2006.0192
17. Craik, D. J. (2010) Discovery and applications of the plant cyclotides Toxicon 56, 1092-1102 10.1016/j.toxicon.2010.02.021
18. Colgrave, M. L. and Craik, D. J. (2004) Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: The importance of the cyclic cystine knot Biochemistry 43, 5965-5975 10.1021/bi049711q
19. Poth, A. G., Chan, L. Y., and Craik, D. J. (2013) Cyclotides as grafting frameworks for protein engineering and drug design applications Biopolymers 100, 480-491 10.1002/bip.22284
20. Gunasekera, S., Foley, F. M., Clark, R. J., Sando, L., Fabri, L. J., Craik, D. J., and Daly, N. L. (2008) Engineering Stabilized Vascular Endothelial Growth Factor-A Antagonists: Synthesis, Structural Characterization, and Bioactivity of Grafted Analogues of Cyclotides J. Med. Chem. 51, 7697-7704 10.1021/jm800704e
21. Chan, L. Y., Gunasekera, S., Henriques, S. T., Worth, N. F., Le, S. J., Clark, R. J., Campbell, J. H., Craik, D. J., and Daly, N. L. (2011) Engineering pro-angiogenic peptides using stable, disulfide-rich cyclic scaffolds Blood 118, 6709-6717 10.1182/blood-2011-06-359141
22. Wang, C. K., Gruber, C. W., Cemazar, M., Siatskas, C., Tagore, P., Payne, N., Sun, G. Z., Wang, S. H., Bernard, C. C., and Craik, D. J. (2014) Molecular Grafting onto a Stable Framework Yields Novel Cyclic Peptides for the Treatment of Multiple Sclerosis ACS Chem. Biol. 9, 156-163 10.1021/cb400548s
23. Thongyoo, P., Bonomelli, C., Leatherbarrow, R. J., and Tate, E. W. (2009) Potent Inhibitors of beta-Tryptase and Human Leukocyte Elastase Based on the MCoTI-II Scaffold J. Med. Chem. 52, 6197-6200 10.1021/jm901233u
24. Thongyoo, P., Roque-Rosell, N., Leatherbarrow, R. J., and Tate, E. W. (2008) Chemical and biomimetic total syntheses of natural and engineered MCoTI cyclotides Org. Biomol. Chem. 6, 1462-1470 10.1039/b801667d
25. Aboye, T. L., Ha, H., Majumder, S., Christ, F., Debyser, Z., Shekhtman, A., Neamati, N., and Camarero, J. A. (2012) Design of a novel cyclotide-based CXCR4 antagonist with anti-human immunodeficiency virus (HIV)-1 activity J. Med. Chem. 55, 10729-10734 10.1021/jm301468k
26. Wong, C. T., Rowlands, D. K., Wong, C. H., Lo, T. W., Nguyen, G. K., Li, H. Y., and Tam, J. P. (2012) Orally active peptidic bradykinin B1 receptor antagonists engineered from a cyclotide scaffold for inflammatory pain treatment Angew. Chem., Int. Ed. 51, 5620-5624 10.1002/anie.201200984
27. Saether, O., Craik, D. J., Campbell, I. D., Sletten, K., Juul, J., and Norman, D. G. (1995) Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1 Biochemistry 34, 4147-4158 10.1021/bi00013a002
28. Hernandez, J. F., Gagnon, J., Chiche, L., Nguyen, T. M., Andrieu, J. P., Heitz, A., Trinh Hong, T., Pham, T. T., and Le Nguyen, D. (2000) Squash trypsin inhibitors from Momordica cochinchinensis exhibit an atypical macrocyclic structure Biochemistry 39, 5722-5730 10.1021/bi9929756
29. Felizmenio-Quimio, M. E., Daly, N. L., and Craik, D. J. (2001) Circular proteins in plants-Solution structure of a novel macrocyclic trypsin inhibitor from Momordica cochinchinensis J. Biol. Chem. 276, 22875-22882 10.1074/jbc.M101666200
30. Cascales, L., Henriques, S. T., Kerr, M. C., Huang, Y. H., Sweet, M. J., Daly, N. L., and Craik, D. J. (2011) Identification and characterization of a new family of cell-penetrating peptides: Cyclic cell-penetrating peptides J. Biol. Chem. 286, 36932-36943 10.1074/jbc.M111.264424
31. Greenwood, K. P., Daly, N. L., Brown, D. L., Stow, J. L., and Craik, D. J. (2007) The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis Int. J. Biochem. Cell Biol. 39, 2252-2264 10.1016/j.biocel.2007.06.016
32. Contreras, J., Elnagar, A. Y. O., Hamm-Alvarez, S. F., and Camarero, J. A. (2011) Cellular uptake of cyclotide MCoTI-I follows multiple endocytic pathways J. Controlled Release 155, 134-143 10.1016/j.jconrel.2011.08.030
33. D'Souza, C., Henriques, S. T., Wang, C. K., and Craik, D. J. (2014) Structural parameters modulating the cellular uptake of disulfide-rich cyclic cell-penetrating peptides: MCoTI-II and SFTI-1 Eur. J. Med. Chem. 88, 10-18 10.1016/j.ejmech.2014.06.047
34. Ji, Y., Majumder, S., Millard, M., Borra, R., Bi, T., Elnagar, A. Y., Neamati, N., Shekhtman, A., and Camarero, J. A. (2013) In vivo activation of the p53 tumor suppressor pathway by an engineered cyclotide J. Am. Chem. Soc. 135, 11623-11633 10.1021/ja405108p
35. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline Proteins: Struct., Funct., Genet. 59, 687-696 10.1002/prot.20449
36. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids; Wiley Interscience, New York.
37. de Araujo, A. D., Hoang, H. N., Kok, W. M., Diness, F., Gupta, P., Hill, T. A., Driver, R. W., Price, D. A., Liras, S., and Fairlie, D. P. (2014) Comparative alpha-helicity of cyclic pentapeptides in water Angew. Chem., Int. Ed. 53, 6965-6969 10.1002/anie.201310245
38. Klein, E., Ben-Bassat, H., Neumann, H., Ralph, P., Zeuthen, J., Polliack, A., and Vanky, F. (1976) Properties of the K562 cell line, derived from a patient with chronic myeloid leukemia Int. J. Cancer 18, 421-431 10.1002/ijc.2910180405
39. Stacey, K. J., Young, G. R., Clark, F., Sester, D. P., Roberts, T. L., Naik, S., Sweet, M. J., and Hume, D. A. (2003) The molecular basis for the lack of immunostimulatory activity of vertebrate DNA J. Immunol. 170, 3614-3620 10.4049/jimmunol.170.7.3614
40. O'brien, J., Wilson, I., Orton, T., and Pognan, F. (2000) Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity Eur. J. Biochem. 267, 5421-5426 10.1046/j.1432-1327.2000.01606.x
41. Torcato, I. M., Huang, Y. H., Franquelim, H. G., Gaspar, D. D., Craik, D. J., Castanho, M. A. R. B., and Henriques, S. T. (2013) The antimicrobial activity of Sub3 is dependent on membrane binding and cell-penetrating ability ChemBioChem 14, 2013-2022 10.1002/cbic.201300274
42. Torcato, I. M., Huang, Y. H., Franquelim, H. G., Gaspar, D., Craik, D. J., Castanho, M. A., and Troeira Henriques, S. (2013) Design and characterization of novel antimicrobial peptides, R-BP100 and RW-BP100, with activity against Gram-negative and Gram-positive bacteria Biochim. Biophys. Acta, Biomembr. 1828, 944-955 10.1016/j.bbamem.2012.12.002
43. Laskowitz, D. T., Thekdi, A. D., Thekdi, S. D., Han, S. K., Myers, J. K., Pizzo, S. V., and Bennett, E. R. (2001) Downregulation of microglial activation by apolipoprotein E and apoE-mimetic peptides Exp. Neurol. 167, 74-85 10.1006/exnr.2001.7541
44. Li, C., Pazgier, M., Liu, M., Lu, W. Y., and Lu, W. (2009) Apamin as a template for structure-based rational design of potent peptide activators of p53 Angew. Chem., Int. Ed. 48, 8712-8715 10.1002/anie.200904550
45. Wedemeyer, W. J., Welker, E., and Scheraga, H. A. (2002) Proline cis-trans isomerization and protein folding Biochemistry 41, 14637-14644 10.1021/bi020574b
46. Otting, G., Liepinsh, E., and Wuthrich, K. (1993) Disulfide bond isomerization in BPTI and BPTI(G36S): An NMR study of correlated mobility in proteins Biochemistry 32, 3571-3582 10.1021/bi00065a008
47. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects J. Biomol. NMR 5, 67-81 10.1007/BF00227471
48. Brown, C. J., Dastidar, S. G., Quah, S. T., Lim, A., Chia, B., and Verma, C. S. (2011) C-terminal substitution of MDM2 interacting peptides modulates binding affinity by distinctive mechanisms PLoS One 6, e24122 10.1371/journal.pone.0024122
49. Glotzbach, B., Reinwarth, M., Weber, N., Fabritz, S., Tomaszowski, M., Fittler, H., Christmann, A., Avrutina, O., and Kolmar, H. (2013) Combinatorial optimization of cystine-knot peptides towards high-affinity inhibitors of human matriptase-1 PLoS One 8, e76956 10.1371/journal.pone.0076956
50. Luo, X., Jiang, Q., Song, G., Liu, Y. L., Xu, Z. G., and Guo, Z. Y. (2012) Efficient oxidative folding and site-specific labeling of human hepcidin to study its interaction with receptor ferroportin FEBS J. 279, 3166-3175 10.1111/j.1742-4658.2012.08695.x
51. Hider, R. C., Kupryszewski, G., Rekowski, P., and Lammek, B. (1988) Origin of the positive 225-230 nm circular dichroism band in proteins. Its application to conformational analysis Biophys. Chem. 31, 45-51 10.1016/0301-4622(88)80007-3
52. Sando, L., Troeira Henriques, S., Foley, F., Simonsen, S. M., Daly, N. L., Hall, K. N., Gustafson, K. R., Aguilar, M. I., and Craik, D. J. (2011) A Synthetic mirror image of kalata B1 reveals that cyclotide activity is independent of a protein receptor ChemBioChem 12, 2456-2462 10.1002/cbic.201100450
53. Neviani, P., Santhanam, R., Trotta, R., Notari, M., Blaser, B. W., Liu, S. J., Mao, H., Chang, J. S., Galietta, A., Uttam, A., Roy, D. C., Valtieri, M., Bruner-Klisovic, R., Caligiuri, M. A., Bloomfield, C. D., Marcucci, G., and Perrotti, D. (2005) The tumor suppressor PP2A is functionally inactivated in blast crisis CML through the inhibitory activity of the BCR/ABL-regulated SET protein Cancer Cell 8, 355-368 10.1016/j.ccr.2005.10.015
54. Drin, G., Cottin, S., Blanc, E., Rees, A. R., and Temsamani, J. (2003) Studies on the internalization mechanism of cationic cell-penetrating peptides J. Biol. Chem. 278, 31192-31201 10.1074/jbc.M303938200
55. Bahnsen, J. S., Franzyk, H., Sandberg-Schaal, A., and Nielsen, H. M. (2013) Antimicrobial and cell-penetrating properties of penetratin analogs: effect of sequence and secondary structure Biochim. Biophys. Acta, Biomembr. 1828, 223-232 10.1016/j.bbamem.2012.10.010
56. Kojima, T., Fujimitsu, Y., and Kojima, H. (2005) Anti-tumor activity of an antibiotic peptide derived from apoprotein E In Vivo 19, 261-264
57. Rossol, M., Heine, H., Meusch, U., Quandt, D., Klein, C., Sweet, M. J., and Hauschildt, S. (2011) LPS-induced cytokine production in human monocytes and macrophages Crit. Rev. Immunol. 31, 379-446 10.1615/CritRevImmunol.v31.i5.20
58. Beffert, U., Stolt, P. C., and Herz, J. (2003) Functions of lipoprotein receptors in neurons J. Lipid Res. 45, 403-409 10.1194/jlr.R300017-JLR200
59. Sticht, J., Humbert, M., Findlow, S., Bodem, J., Muller, M., Dietrich, U., Werner, J., and Krausslich, H. G. (2005) A peptide inhibitor of HIV-1 assembly in vitro Nat. Struct. Mol. Biol. 12, 671-677 10.1038/nsmb964
60. Letai, A., Bassik, M. C., Walensky, L. D., Sorcinelli, M. D., Weiler, S., and Korsmeyer, S. J. (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics Cancer Cell 2, 183-192 10.1016/S1535-6108(02)00127-7
61. de la Roche, M., Worm, J., and Bienz, M. (2008) The function of BCL9 in Wnt/beta-catenin signaling and colorectal cancer cells BMC Cancer 8, 199 10.1186/1471-2407-8-199
62. Huang, Y. H., Chaousis, S., Cheneval, O., Craik, D. J., and Henriques, S. T. (2015) Optimization of the cyclotide framework to improve cell penetration properties Front. Pharmacol. 6, 17 10.3389/fphar.2015.00017