Cystine-knot peptides: emerging tools for cancer imaging and therapy

References

• Kolmar H. Natural and engineered cystine knot miniproteins for diagnostic and therapeutic applications. Curr Pharm Des 2011;17(38):4329-36
   PubMed Web of Science ®Google Scholar
• Moore SJ, Leung CL, Cochran JR. Knottins: disulfide-bonded therapeutic and diagnostic peptides. Drug Discov Today Technol 2012;9(1):e3-11
   Google Scholar
• Daly NL, Craik DJ. Bioactive cystine knot proteins. Curr Opin Chem Biol 2011;15(3):362-8
   PubMed Web of Science ®Google Scholar
• Le Nguyen D, Heitz A, Chiche L, et al. Molecular recognition between serine proteases and new bioactive microproteins with a knotted structure. Biochimie 1990;72(6-7):431-5
   PubMedGoogle Scholar
• Colgrave ML, Craik DJ. Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: the importance of the cyclic cystine knot. Biochemistry 2004;43(20):5965-75
   PubMed Web of Science ®Google Scholar
• Werle M, Schmitz T, Huang HL, et al. The potential of cystine-knot microproteins as novel pharmacophoric scaffolds in oral peptide drug delivery. J Drug Target 2006;14(3):137-46
   PubMed Web of Science ®Google Scholar
• Gracy J, Le-Nguyen D, Gelly JC, et al. KNOTTIN: the knottin or inhibitor cystine knot scaffold in 2007. Nucleic Acids Res 2008;36(Database issue):D314-19
   Google Scholar
• The KNOTTIN database. Knottins are intriguing miniproteins with strong potential in drug design. Available from: http://knottin.cbs.cnrs.fr
   Google Scholar
• Zhu S, Darbon H, Dyason K, et al. Evolutionary origin of inhibitor cystine knot peptides. FASEB J 2003;17(12):1765-7
   PubMed Web of Science ®Google Scholar
• Pallaghy PK, Nielsen KJ, Craik DJ, Norton RS. A common structural motif incorporating a cystine knot and a triple-stranded beta-sheet in toxic and inhibitory polypeptides. Protein Sci 1994;3(10):1833-9
   PubMed Web of Science ®Google Scholar
• Craik DJ, Daly NL, Bond T, Waine C. Plant cyclotides: a unique family of cyclic and knotted proteins that defines the cyclic cystine knot structural motif. J Mol Biol 1999;294(5):1327-36
   PubMed Web of Science ®Google Scholar
• Wang CK, Kaas Q, Chiche L, Craik DJ. CyBase: a database of cyclic protein sequences and structures, with applications in protein discovery and engineering. Nucleic Acids Res 2008;36(Database issue):D206-10
   Google Scholar
• The database of cyclic proteins. Available from: http://cybase.org.au
   Google Scholar
• Kolmar H. Engineered cystine-knot miniproteins for diagnostic applications. Expert Rev Mol Diagn 2010;10(3):361-8
   PubMed Web of Science ®Google Scholar
• Gould A, Ji Y, Aboye TL, Camarero JA. Cyclotides, a novel ultrastable polypeptide scaffold for drug discovery. Curr Pharm Des 2011;17(38):4294-307
   PubMed Web of Science ®Google Scholar
• Maillere B, Mourier G, Herve M, et al. Immunogenicity of a disulphide-containing neurotoxin: presentation to T-cells requires a reduction step. Toxicon 1995;33(4):475-82
   Google Scholar
• Jiang L, Miao Z, Kimura RH, et al. 111In-labeled cystine-knot peptides based on the Agouti-related protein for targeting tumor angiogenesis. J Biomed Biotechnol 2012;2012:368075
   Google Scholar
• Clark RJ, Craik DJ. Engineering cyclic peptide toxins. Methods Enzymol 2012;503:57-74
   Google Scholar
• Klint JK, Senff S, Saez NJ, et al. Production of recombinant disulfide-rich venom peptides for structural and functional analysis via expression in the periplasm of E. coli. PLoS One 2013;8(5):e63865
   PubMed Web of Science ®Google Scholar
• Moore SJ, Cochran JR. Engineering knottins as novel binding agents. Methods Enzymol 2012;503:223-51
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144(5):646-74
   PubMed Web of Science ®Google Scholar
• Hoelder S, Clarke PA, Workman P. Discovery of small molecule cancer drugs: successes, challenges and opportunities. Mol Oncol 2012;6(2):155-76
   PubMed Web of Science ®Google Scholar
• Goldman JM, Melo JV. Chronic myeloid leukemia – advances in biology and new approaches to treatment. N Engl J Med 2003;349(15):1451-64
   PubMed Web of Science ®Google Scholar
• Castaigne S, Chomienne C, Daniel MT, et al. All-trans retinoic acid as a differentiation therapy for acute promyelocytic leukemia. I. Clinical results. Blood 1990;76(9):1704-9
   PubMed Web of Science ®Google Scholar
• Lerner LJ, Jordan VC. Development of antiestrogens and their use in breast cancer: eighth Cain memorial award lecture. Cancer Res 1990;50(14):4177-89
   PubMed Web of Science ®Google Scholar
• Stegmeier F, Warmuth M, Sellers WR, Dorsch M. Targeted cancer therapies in the twenty-first century: lessons from imatinib. Clin Pharmacol Ther 2010;87(5):543-52
   PubMed Web of Science ®Google Scholar
• Nelson AL, Dhimolea E, Reichert JM. Development trends for human monoclonal antibody therapeutics. Nat Rev Drug Discov 2010;9(10):767-74
   PubMed Web of Science ®Google Scholar
• Lobo ED, Hansen RJ, Balthasar JP. Antibody pharmacokinetics and pharmacodynamics. J Pharm Sci 2004;93(11):2645-68
   PubMed Web of Science ®Google Scholar
• Scott AM, Wolchok JD, Old LJ. Antibody therapy of cancer. Nat Rev Cancer 2012;12(4):278-87
   PubMed Web of Science ®Google Scholar
• Hoogenboom HR. Selecting and screening recombinant antibody libraries. Nat Biotechnol 2005;23(9):1105-16
   PubMed Web of Science ®Google Scholar
• Dennis MS, Jin H, Dugger D, et al. Imaging tumors with an albumin-binding Fab, a novel tumor-targeting agent. Cancer Res 2007;67(1):254-61
   PubMed Web of Science ®Google Scholar
• Verdine GL, Walensky LD. The challenge of drugging undruggable targets in cancer: lessons learned from targeting BCL-2 family members. Clin Cancer Res 2007;13(24):7264-70
   PubMed Web of Science ®Google Scholar
• Condeelis J, Weissleder R. In vivo imaging in cancer. Cold Spring Harb Perspect Biol 2010;2(12):a003848
   PubMed Web of Science ®Google Scholar
• Frangioni JV. New technologies for human cancer imaging. J Clin Oncol 2008;26(24):4012-21
   PubMed Web of Science ®Google Scholar
• Fass L. Imaging and cancer: a review. Mol Oncol 2008;2(2):115-52
   PubMed Web of Science ®Google Scholar
• James ML, Gambhir SS. A molecular imaging primer: modalities, imaging agents, and applications. Physiol Rev 2012;92(2):897-965
   PubMed Web of Science ®Google Scholar
• Friedman M, Stahl S. Engineered affinity proteins for tumour-targeting applications. Biotechnol Appl Biochem 2009;53(Pt 1):1-29
   PubMedGoogle Scholar
• Stern LA, Case BA, Hackel BJ. Alternative non-antibody protein scaffolds for molecular imaging of cancer. Curr Opin Chem Eng 2013;2(4):425-32
   Google Scholar
• Chen K, Chen X. Design and development of molecular imaging probes. Curr Top Med Chem 2010;10(12):1227-36
   PubMed Web of Science ®Google Scholar
• Reynolds F, Kelly KA. Techniques for molecular imaging probe design. Mol Imaging 2011;10(6):407-19
   Google Scholar
• Bouvet M, Hoffman RM. Glowing tumors make for better detection and resection. Sci Transl Med 2011;3(110):110fs110
   Web of Science ®Google Scholar
• Craik DJ, Cemazar M, Wang CK, Daly NL. The cyclotide family of circular miniproteins: nature’s combinatorial peptide template. Biopolymers 2006;84(3):250-66
   Google Scholar
• Sollod BL, Wilson D, Zhaxybayeva O, et al. Were arachnids the first to use combinatorial peptide libraries? Peptides 2005;26(1):131-9
   PubMed Web of Science ®Google Scholar
• Miljanich GP. Ziconotide: neuronal calcium channel blocker for treating severe chronic pain. Curr Med Chem 2004;11(23):3029-40
   PubMed Web of Science ®Google Scholar
• Christmann A, Walter K, Wentzel A, et al. The cystine knot of a squash-type protease inhibitor as a structural scaffold for Escherichia coli cell surface display of conformationally constrained peptides. Protein Eng 1999;12(9):797-806
   Google Scholar
• Getz JA, Cheneval O, Craik DJ, Daugherty PS. Design of a cyclotide antagonist of neuropilin-1 and -2 that potently inhibits endothelial cell migration. ACS Chem Biol 2013;8(6):1147-54
   PubMed Web of Science ®Google Scholar
• Silverman AP, Levin AM, Lahti JL, Cochran JR. Engineered cystine-knot peptides that bind alphav beta3 integrin with antibody-like affinities. J Mol Biol 2009;385(4):1064-75
   PubMed Web of Science ®Google Scholar
• Heitz A, Avrutina O, Le-Nguyen D, et al. Knottin cyclization: impact on structure and dynamics. BMC Struct Biol 2008;8:54
   PubMedGoogle Scholar
• Heitz A, Hernandez JF, Gagnon J, et al. Solution structure of the squash trypsin inhibitor MCoTI-II. A new family for cyclic knottins. Biochemistry 2001;40(27):7973-83
   PubMed Web of Science ®Google Scholar
• Eliasen R, Daly NL, Wulff BS, et al. Design, synthesis, structural and functional characterization of novel melanocortin agonists based on the cyclotide kalata B1. J Biol Chem 2012;287(48):40493-501
   PubMed Web of Science ®Google Scholar
• Jackson PJ, McNulty JC, Yang YK, et al. Design, pharmacology, and NMR structure of a minimized cystine knot with agouti-related protein activity. Biochemistry 2002;41(24):7565-72
   PubMed Web of Science ®Google Scholar
• Jiang L, Kimura RH, Miao Z, et al. Evaluation of a 64Cu-labeled cystine-knot peptide based on agouti-related protein for PET of tumors expressing alphavbeta3 integrin. J Nucl Med 2010;51(2):251-8
   Google Scholar
• Miao Z, Ren G, Liu H, et al. An engineered knottin peptide labeled with 18F for PET imaging of integrin expression. Bioconjug Chem 2009;20(12):2342-7
   Google Scholar
• Soroceanu L, Gillespie Y, Khazaeli MB, Sontheimer H. Use of chlorotoxin for targeting of primary brain tumors. Cancer Res 1998;58(21):4871-9
   PubMed Web of Science ®Google Scholar
• Lippens G, Najib J, Wodak SJ, Tartar A. NMR sequential assignments and solution structure of chlorotoxin, a small scorpion toxin that blocks chloride channels. Biochemistry 1995;34(1):13-21
   PubMed Web of Science ®Google Scholar
• Veiseh M, Gabikian P, Bahrami SB, et al. Tumor paint: a chlorotoxin:cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res 2007;67(14):6882-8
   PubMed Web of Science ®Google Scholar
• Kesavan K, Ratliff J, Johnson EW, et al. Annexin A2 is a molecular target for TM601, a peptide with tumor-targeting and anti-angiogenic effects. J Biol Chem 2010;285(7):4366-74
   PubMed Web of Science ®Google Scholar
• Akcan M, Stroud MR, Hansen SJ, et al. Chemical re-engineering of chlorotoxin improves bioconjugation properties for tumor imaging and targeted therapy. J Med Chem 2011;54(3):782-7
   PubMed Web of Science ®Google Scholar
• Butte PV, Mamelak A, Parrish-Novak J, et al. Near-infrared imaging of brain tumors using the Tumor Paint BLZ-100 to achieve near-complete resection of brain tumors. Neurosurg Focus 2014;36(2):E1
   Google Scholar
• Mamelak AN, Jacoby DB. Targeted delivery of antitumoral therapy to glioma and other malignancies with synthetic chlorotoxin (TM-601). Expert Opin Drug Deliv 2007;4(2):175-86
   PubMed Web of Science ®Google Scholar
• Stroud MR, Hansen SJ, Olson JM. In vivo bio-imaging using chlorotoxin-based conjugates. Curr Pharm Des 2011;17(38):4362-71
   PubMed Web of Science ®Google Scholar
• Mamelak AN, Rosenfeld S, Bucholz R, et al. Phase I single-dose study of intracavitary-administered iodine-131-TM-601 in adults with recurrent high-grade glioma. J Clin Oncol 2006;24(22):3644-50
   PubMed Web of Science ®Google Scholar
• Moore SJ, Leung CL, Norton HK, Cochran JR. Engineering agatoxin, a cystine-knot peptide from spider venom, as a molecular probe for in vivo tumor imaging. PLoS ONE 2013;8(4):e60498
   PubMed Web of Science ®Google Scholar
• Kimura RH, Levin AM, Cochran FV, Cochran JR. Engineered cystine knot peptides that bind alphavbeta3, alphavbeta5, and alpha5beta1 integrins with low-nanomolar affinity. Proteins 2009;77(2):359-69
   PubMed Web of Science ®Google Scholar
• Kimura RH, Cheng Z, Gambhir SS, Cochran JR. Engineered knottin peptides: a new class of agents for imaging integrin expression in living subjects. Cancer Res 2009;69(6):2435-42
   PubMed Web of Science ®Google Scholar
• Nielsen CH, Kimura RH, Withofs N, et al. PET imaging of tumor neovascularization in a transgenic mouse model with a novel 64Cu-DOTA-knottin peptide. Cancer Res 2010;70(22):9022-30
   Google Scholar
• Jiang L, Miao Z, Kimura RH, et al. Preliminary evaluation of 177Lu-labeled knottin peptides for integrin receptor-targeted radionuclide therapy. Eur J Nucl Med Mol Imaging 2010;38(4):613-22
   Google Scholar
• Moore SJ, Hayden Gephart MG, Bergen JM, et al. Engineered knottin peptide enables noninvasive optical imaging of intracranial medulloblastoma. Proc Natl Acad Sci USA 2013;110(36):14598-603
   Google Scholar
• Silverman AP, Kariolis MS, Cochran JR. Cystine-knot peptides engineered with specificities for alpha(IIb)beta(3) or alpha(IIb)beta(3) and alpha(v)beta(3) integrins are potent inhibitors of platelet aggregation. J Mol Recognit 2011;24(1):127-35
   Google Scholar
• Kimura RH, Teed R, Hackel BJ, et al. Pharmacokinetically stabilized cystine knot peptides that bind alpha-v-beta-6 integrin with single-digit nanomolar affinities for detection of pancreatic cancer. Clin Cancer Res 2012;18(3):839-49
   PubMed Web of Science ®Google Scholar
• Hackel BJ, Kimura RH, Miao Z, et al. 18F-fluorobenzoate-labeled cystine knot peptides for PET imaging of integrin alphavbeta6. J Nucl Med 2013;54(7):1101-5
   Google Scholar
• Zhu X, Li J, Hong Y, et al. 99mTc-labeled cystine knot peptide targeting integrin alphavbeta6 for tumor SPECT imaging. Mol Pharm 2014;11(4):1208-17
   Google Scholar
• Gunasekera S, Foley FM, Clark RJ, et al. Engineering stabilized vascular endothelial growth factor-A antagonists: synthesis, structural characterization, and bioactivity of grafted analogues of cyclotides. J Med Chem 2008;51(24):7697-704
   Google Scholar
• Thongyoo P, Bonomelli C, Leatherbarrow RJ, Tate EW. Potent inhibitors of beta-tryptase and human leukocyte elastase based on the MCoTI-II scaffold. J Med Chem 2009;52(20):6197-200
   PubMed Web of Science ®Google Scholar
• Glotzbach B, Reinwarth M, Weber N, et al. Combinatorial optimization of cystine-knot peptides towards high-affinity inhibitors of human matriptase-1. PLoS ONE 2013;8(10):e76956
   Google Scholar
• Greenwood KP, Daly NL, Brown DL, et al. The cyclic cystine knot miniprotein MCoTI-II is internalized into cells by macropinocytosis. Int J Biochem Cell Biol 2007;39(12):2252-64
   Google Scholar
• Ji Y, Majumder S, Millard M, et al. In vivo activation of the p53 tumor suppressor pathway by an engineered cyclotide. J Am Chem Soc 2013;135(31):11623-33
   PubMed Web of Science ®Google Scholar
• Aboye TL, Ha H, Majumder S, et al. Design of a novel cyclotide-based CXCR4 antagonist with anti-human immunodeficiency virus (HIV)-1 activity. J Med Chem 2012;55(23):10729-34
   PubMed Web of Science ®Google Scholar
• DeMarco SJ, Henze H, Lederer A, et al. Discovery of novel, highly potent and selective beta-hairpin mimetic CXCR4 inhibitors with excellent anti-HIV activity and pharmacokinetic profiles. Bioorg Med Chem 2006;14(24):8396-404
   Google Scholar
• Popp MW, Dougan SK, Chuang TY, et al. Sortase-catalyzed transformations that improve the properties of cytokines. Proc Natl Acad Sci USA 2011;108(8):3169-74
   Google Scholar
• Getz JA, Rice JJ, Daugherty PS. Protease-resistant peptide ligands from a knottin scaffold library. ACS Chem Biol 2011;6(8):837-44
   Google Scholar
• Wong CT, Rowlands DK, Wong CH, et al. Orally active peptidic bradykinin B1 receptor antagonists engineered from a cyclotide scaffold for inflammatory pain treatment. Angew Chem Int Ed Engl 2012;51(23):5620-4
   PubMed Web of Science ®Google Scholar
• Clark RJ, Jensen J, Nevin ST, et al. The engineering of an orally active conotoxin for the treatment of neuropathic pain. Angew Chem Int Ed Engl 2010;49(37):6545-8
   PubMed Web of Science ®Google Scholar
• Layer P, Stanghellini V. Review article: linaclotide for the management of irritable bowel syndrome with constipation. Aliment Pharmacol Ther 2014;39(4):371-84
   PubMed Web of Science ®Google Scholar
• Lembo AJ, Schneier HA, Shiff SJ, et al. Two randomized trials of linaclotide for chronic constipation. N Engl J Med 2011;365(6):527-36
   PubMed Web of Science ®Google Scholar
• Gebauer M, Skerra A. Engineered protein scaffolds as next-generation antibody therapeutics. Curr Opin Chem Biol 2009;13(3):245-55
   PubMed Web of Science ®Google Scholar
• Banta S, Dooley K, Shur O. Replacing antibodies: engineering new binding proteins. Annu Rev Biomed Eng 2013;15:93-113
   Web of Science ®Google Scholar
• Lee CH, Park KJ, Sung ES, et al. Engineering of a human kringle domain into agonistic and antagonistic binding proteins functioning in vitro and in vivo. Proc Natl Acad Sci USA 2010;107(21):9567-71
   Google Scholar
• Swedberg JE, de Veer SJ, Harris JM. Natural and engineered kallikrein inhibitors: an emerging pharmacopoeia. Biol Chem 2010;391(4):357-74
   PubMed Web of Science ®Google Scholar
• Silverman J, Liu Q, Bakker A, et al. Multivalent avimer proteins evolved by exon shuffling of a family of human receptor domains. Nat Biotechnol 2005;23(12):1556-61
   PubMed Web of Science ®Google Scholar
• Weidle UH, Auer J, Brinkmann U, et al. The emerging role of new protein scaffold-based agents for treatment of cancer. Cancer Genomics Proteomics 2013;10(4):155-68
   PubMed Web of Science ®Google Scholar
• Orlova A, Magnusson M, Eriksson TL, et al. Tumor imaging using a picomolar affinity HER2 binding affibody molecule. Cancer Res 2006;66(8):4339-48
   PubMed Web of Science ®Google Scholar
• Schmidt MM, Wittrup KD. A modeling analysis of the effects of molecular size and binding affinity on tumor targeting. Mol Cancer Ther 2009;8(10):2861-71
   PubMed Web of Science ®Google Scholar
• Zahnd C, Kawe M, Stumpp MT, et al. Efficient tumor targeting with high-affinity designed ankyrin repeat proteins: effects of affinity and molecular size. Cancer Res 2010;70(4):1595-605
   PubMed Web of Science ®Google Scholar
• Wittrup KD, Thurber GM, Schmidt MM, Rhoden JJ. Practical theoretic guidance for the design of tumor-targeting agents. Methods Enzymol 2012;503:255-68
   Google Scholar
• Krause S, Schmoldt HU, Wentzel A, et al. Grafting of thrombopoietin-mimetic peptides into cystine knot miniproteins yields high-affinity thrombopoietin antagonists and agonists. FEBS J 2007;274(1):86-95
   Google Scholar
• Kontermann RE. Strategies for extended serum half-life of protein therapeutics. Curr Opin Biotechnol 2011;22(6):868-76
   PubMed Web of Science ®Google Scholar
• Willmann JK, Kimura RH, Deshpande N, et al. Targeted contrast-enhanced ultrasound imaging of tumor angiogenesis with contrast microbubbles conjugated to integrin-binding knottin peptides. J Nucl Med 2010;51(3):433-40
   Google Scholar
• Hoffman RM. The multiple uses of fluorescent proteins to visualize cancer in vivo. Nat Rev Cancer 2005;5(10):796-806
   Google Scholar
• Flygare JA, Pillow TH, Aristoff P. Antibody-drug conjugates for the treatment of cancer. Chem Biol Drug Des 2013;81(1):113-21
   PubMed Web of Science ®Google Scholar
• Verma S, Miles D, Gianni L, et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 2012;367(19):1783-91
   PubMed Web of Science ®Google Scholar
• Younes A, Bartlett NL, Leonard JP, et al. Brentuximab vedotin (SGN-35) for relapsed CD30-positive lymphomas. N Engl J Med 2010;363(19):1812-21
   PubMed Web of Science ®Google Scholar
• Gorovits B, Krinos-Fiorotti C. Proposed mechanism of off-target toxicity for antibody-drug conjugates driven by mannose receptor uptake. Cancer Immunol Immunother 2013;62(2):217-23
   PubMed Web of Science ®Google Scholar
• Kryshtafovych A, Moult J, Bales P, et al. Challenging the state of the art in protein structure prediction: highlights of experimental target structures for the 10th Critical Assessment of Techniques for Protein Structure Prediction Experiment CASP10. Proteins 2014;82(Suppl 2):26-42
   Google Scholar