Engineering Agatoxin, a Cystine-Knot Peptide from Spider Venom, as a Molecular Probe for In Vivo Tumor Imaging

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Moore, Sarah J ^a   Leung, Cheuk Lun ^a   Norton, Heidi K ^a   Cochran, Jennifer R ^a,b  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AF 680; AGATOXIN; CONTRAST MEDIUM; FLUORESCENT DYE; KNOTTIN; KNOTTIN DERIVATIVE; SCAFFOLD PROTEIN; SPIDER VENOM; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONCENTRATION (PARAMETERS); CONJUGATION; CONTROLLED STUDY; DIAGNOSTIC IMAGING EQUIPMENT; DRUG TARGETING; FEMALE; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; IMAGING SOFTWARE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR IMAGING; MOLECULAR PROBE; MOUSE; NONHUMAN; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RECEPTOR BINDING; RENOGRAPHY; TISSUE DISTRIBUTION;

AGATOXINS; AMINO ACID SUBSTITUTION; ANIMALS; CARBOCYANINES; CYSTEINE; CYSTINE KNOT MOTIFS; FEMALE; FLUORESCENT DYES; HUMANS; INTEGRIN ALPHAVBETA3; K562 CELLS; MICE; MICE, NUDE; MUTAGENESIS, SITE-DIRECTED; NEOPLASM TRANSPLANTATION; NEOPLASMS; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN FOLDING;

AGOUTI; ARANEAE; ECBALLIUM ELATERIUM; MAMMALIA;

EID: 84875701679     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060498     Document Type: Article

References (70)

1. Reynolds F, Kelly KA, (2011) Techniques for molecular imaging probe design. Mol Imaging 10: 407-419.
2. Chen K, Chen X, (2010) Design and development of molecular imaging probes. Curr Top Med Chem 10: 1227-1236.
3. Friedman M, Stahl S, (2009) Engineered affinity proteins for tumour-targeting applications. Biotechnol Appl Biochem 53: 1-29.
4. Batra SK, Jain M, Wittel UA, Chauhan SC, Colcher D, (2002) Pharmacokinetics and biodistribution of genetically engineered antibodies. Curr Opin Biotechnol 13: 603-608.
5. Daly NL, Craik DJ, (2011) Bioactive cystine knot proteins. Curr Opin Chem Biol 15: 362-368.
6. Kolmar H, (2011) Natural and engineered cystine knot miniproteins for diagnostic and therapeutic applications. Curr Pharm Des 17: 4329-4336.
7. Moore SJ, Leung CL, Cochran JR, (2011) Knottins: Disulfide-bonded therapeutic and diagnostic peptides. Drug Discovery Today: Technologies 9: e3-e11.
8. 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.
9. Colgrave ML, Craik DJ, (2004) Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: the importance of the cyclic cystine knot. Biochemistry 43: 5965-5975.
10. Werle M, Schmitz T, Huang HL, Wentzel A, Kolmar H, et al. (2006) The potential of cystine-knot microproteins as novel pharmacophoric scaffolds in oral peptide drug delivery. J Drug Target 14: 137-146.
11. Miao Z, Levi J, Cheng Z, (2010) Protein scaffold-based molecular probes for cancer molecular imaging. Amino Acids epub Feb 12.
12. Reinwarth M, Nasu D, Kolmar H, Avrutina O, (2012) Chemical Synthesis, Backbone Cyclization and Oxidative Folding of Cystine-knot Peptides; Promising Scaffolds for Applications in Drug Design. Molecules 17: 12533-12552.
13. Zhu S, Darbon H, Dyason K, Verdonck F, Tytgat J, (2003) Evolutionary origin of inhibitor cystine knot peptides. FASEB J 17: 1765-1767.
14. Gracy J, Le-Nguyen D, Gelly JC, Kaas Q, Heitz A, et al. (2008) KNOTTIN: the knottin or inhibitor cystine knot scaffold in 2007. Nucleic Acids Res 36: D314-319.
15. Williams JA, Day M, Heavner JE, (2008) Ziconotide: an update and review. Expert Opin Pharmacother 9: 1575-1583.
16. Veiseh M, Gabikian P, Bahrami SB, Veiseh O, Zhang M, et al. (2007) Tumor paint: a chlorotoxin:Cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res 67: 6882-6888.
17. Craik DJ, Swedberg JE, Mylne JS, Cemazar M, (2012) Cyclotides as a basis for drug design. Expert Opin Drug Discov 7: 179-194.
18. Kolmar H, (2010) Engineered cystine-knot miniproteins for diagnostic applications. Expert Rev Mol Diagn 10: 361-368.
19. Moore SJ, Cochran JR, (2012) Engineering knottins as novel binding agents. Methods in Enzymology 503: 223-251.
20. Getz JA, Rice JJ, Daugherty PS, (2011) Protease-resistant peptide ligands from a knottin scaffold library. ACS Chem Biol 6: 837-844.
21. Favel A, Mattras H, Coletti-Previero MA, Zwilling R, Robinson EA, et al. (1989) Protease inhibitors from Ecballium elaterium seeds. Int J Pept Protein Res 33: 202-208.
22. Le Nguyen D, Heitz A, Chiche L, Castro B, Boigegrain RA, et al. (1990) Molecular recognition between serine proteases and new bioactive microproteins with a knotted structure. Biochimie 72: 431-435.
23. Ollmann MM, Wilson BD, Yang YK, Kerns JA, Chen Y, et al. (1997) Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 278: 135-138.
24. Jackson PJ, McNulty JC, Yang YK, Thompson DA, Chai B, et al. (2002) Design, pharmacology, and NMR structure of a minimized cystine knot with agouti-related protein activity. Biochemistry 41: 7565-7572.
25. 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.
26. Kimura RH, Levin AM, Cochran FV, Cochran JR, (2009) Engineered cystine knot peptides that bind alphav beta3, alphav beta5, and alpha5 beta1 integrins with low-nanomolar affinity. Proteins 77: 359-369.
27. Silverman AP, Levin AM, Lahti JL, Cochran JR, (2009) Engineered cystine-knot peptides that bind alphav beta3 integrin with antibody-like affinities. J Mol Biol 385: 1064-1075.
28. Jiang H, Moore SJ, Liu S, Liu H, Miao Z, et al. (2012) A novel radiofluorinated agouti-related protein for tumor angiogenesis imaging. Amino Acids doi:10.1007/s00726-00012-01391-y.
29. Jiang L, Kimura RH, Miao Z, Silverman AP, Ren G, et al. (2010) Evaluation of a 64Cu-labeled cystine-knot peptide based on agouti-related protein for PET of tumors expressing alphav beta3 integrin. J Nucl Med 51: 251-258.
30. Kimura RH, Cheng Z, Gambhir SS, Cochran JR, (2009) Engineered knottin peptides: a new class of agents for imaging integrin expression in living subjects. Cancer Res 69: 2435-2442.
31. Kimura RH, Miao Z, Cheng Z, Gambhir SS, Cochran JR, (2010) A dual-labeled knottin peptide for PET and near-infrared fluorescence imaging of integrin expression in living subjects. Bioconjug Chem 21: 436-444.
32. Liu S, Liu H, Ren G, Kimura RH, Cochran JR, et al. (2012) PET imaging of integrin positive tumors using 18F-labeled knottin peptides. Theranostics 1: 403-412.
33. Miao Z, Ren G, Liu H, Kimura RH, Jiang L, et al. (2009) An engineered knottin peptide labeled with 18F for PET imaging of integrin expression. Bioconjug Chem 20: 2342-2347.
34. Nielsen CH, Kimura RH, Withofs N, Tran PT, Miao Z, et al. (2010) PET imaging of tumor neovascularization in a transgenic mouse model with a novel 64Cu-DOTA-knottin peptide. Cancer Res 70: 9022-9030.
35. Jiang L, Miao Z, Kimura RH, Silverman AP, Ren G, et al. (2012) 111In-labeled cystine-knot peptides based on the Agouti-related protein for targeting tumor angiogenesis. J Biomed Biotechnol 2012 Article ID 368075.
36. Willmann JK, Kimura RH, Deshpande N, Lutz AM, Cochran JR, et al. (2010) Targeted contrast-enhanced ultrasound imaging of tumor angiogenesis with contrast microbubbles conjugated to integrin-binding knottin peptides. J Nucl Med 51: 433-440.
37. Brooks PC, Clark RA, Cheresh DA, (1994) Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264: 569-571.
38. Kim S, Bell K, Mousa SA, Varner JA, (2000) Regulation of angiogenesis in vivo by ligation of integrin alpha5beta1 with the central cell-binding domain of fibronectin. Am J Pathol 156: 1345-1362.
39. Brooks PC, Montgomery AM, Rosenfeld M, Reisfeld RA, Hu T, et al. (1994) Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 79: 1157-1164.
40. Friedlander M, Brooks PC, Shaffer RW, Kincaid CM, Varner JA, et al. (1995) Definition of two angiogenic pathways by distinct alpha v integrins. Science 270: 1500-1502.
41. Gaertner FC, Schwaiger M, Beer AJ, (2010) Molecular imaging of avb3 expression in cancer patients. Q J Nucl Med Mol Imaging.
42. Cai W, Rao J, Gambhir SS, Chen X, (2006) How molecular imaging is speeding up antiangiogenic drug development. Mol Cancer Ther 5: 2624-2633.
43. Escoubas P, Rash L, (2004) Tarantulas: eight-legged pharmacists and combinatorial chemists. Toxicon 43: 555-574.
44. Wood DL, Miljenovic T, Cai S, Raven RJ, Kaas Q, et al. (2009) ArachnoServer: a database of protein toxins from spiders. BMC Genomics 10: 375.
45. Adams ME, Mintz IM, Reily MD, Thanabal V, Bean BP, (1993) Structure and properties of omega-agatoxin IVB, a new antagonist of P-type calcium channels. Mol Pharmacol 44: 681-688.
46. Kim JI, Konishi S, Iwai H, Kohno T, Gouda H, et al. (1995) Three-dimensional solution structure of the calcium channel antagonist omega-agatoxin IVA: consensus molecular folding of calcium channel blockers. J Mol Biol 250: 659-671.
47. Rink H, Sieber P, Raschdorf F, (1984) Coversion of NG-urethane protected arginine to ornithine in peptide solid phase synthesis. Tetrahedron Letters 25: 621-624.
48. Rubina A, Bespalova Zh D, Bushuev VN, (2000) The solid-phase synthesis of peptides containing an arginine residue with an unprotected guanidine group. Russian Journal of Bioorganic Chemistry 26: 235-244.
49. Zhang Y, Skolnick J, (2005) TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res 33: 2302-2309.
50. Blystone SD, Graham IL, Lindberg FP, Brown EJ, (1994) Integrin alphav beta3 differentially regulates adhesive and phagocytic functions of the fibronectin receptor alpha5 beta1. J Cell Biol 127: 1129-1137.
51. Xiong JP, Stehle T, Goodman SL, Arnaout MA, (2003) Integrins, cations and ligands: making the connection. J Thromb Haemost 1: 1642-1654.
52. Haubner R, Finsinger D, Kessler H, (1997) Stereoisomeric peptide libaries and peptidomimetics for designing selective inhibitors of the avb3 integrin for a new cancer therapy. Angew Chem Int Ed 36: 1374-1389.
53. Cochran FV, Cochran JR, (2010) Phage display and molecular imaging: expanding fields of vision in living subjects. Biotechnology and Genetic Engineering Reviews 27: 57-94.
54. McNulty JC, Jackson PJ, Thompson DA, Chai B, Gantz I, et al. (2005) Structures of the agouti signaling protein. J Mol Biol 346: 1059-1070.
55. Haubner R, (2006) Alphavbeta3-integrin imaging: a new approach to characterise angiogenesis? Eur J Nucl Med Mol Imaging 33 (Suppl 1): 54-63.
56. Beer AJ, Schwaiger M, (2008) Imaging of integrin alphavbeta3 expression. Cancer Metastasis Rev 27: 631-644.
57. Zahnd C, Kawe M, Stumpp MT, de Pasquale C, Tamaskovic R, et al. (2010) Efficient tumor targeting with high-affinity designed ankyrin repeat proteins: effects of affinity and molecular size. Cancer Res 70: 1595-1605.
58. Orlova A, Magnusson M, Eriksson TL, Nilsson M, Larsson B, et al. (2006) Tumor imaging using a picomolar affinity HER2 binding affibody molecule. Cancer Res 66: 4339-4348.
59. Schmidt MM, Wittrup KD, (2009) A modeling analysis of the effects of molecular size and binding affinity on tumor targeting. Mol Cancer Ther 8: 2861-2871.
60. Wittrup KD, Thurber GM, Schmidt MM, Rhoden JJ, (2012) Practical theoretic guidance for the design of tumor-targeting agents. Methods Enzymol 503: 255-268.
61. Hackel BJ, Kimura RH, Gambhir SS, (2012) Use of 64Cu-labeled fibronectin domain with EGFR-overexpressing tumor xenograft: molecular imaging. Radiology 263: 179-188.
62. Kaur S, Venktaraman G, Jain M, Senapati S, Garg PK, et al. (2012) Recent trends in antibody-based oncologic imaging. Cancer Lett 315: 97-111.
63. Lofblom J, Feldwisch J, Tolmachev V, Carlsson J, Stahl S, et al. (2010) Affibody molecules: engineered proteins for therapeutic, diagnostic and biotechnological applications. FEBS Lett 584: 2670-2680.
64. Wu AM, Olafsen T, (2008) Antibodies for molecular imaging of cancer. Cancer J 14: 191-197.
65. Akizawa H, Uehara T, Arano Y, (2008) Renal uptake and metabolism of radiopharmaceuticals derived from peptides and proteins. Adv Drug Deliv Rev 60: 1319-1328.
66. Vegt E, de Jong M, Wetzels JF, Masereeuw R, Melis M, et al. (2010) Renal toxicity of radiolabeled peptides and antibody fragments: mechanisms, impact on radionuclide therapy, and strategies for prevention. J Nucl Med 51: 1049-1058.
67. Kimura RH, Teed R, Hackel BJ, Pysz MA, Chuang CZ, et al. (2012) Pharmacokinetically stabilized cystine knot peptides that bind alphav beta6 integrin with single-digit nanomolar affinities for detection of pancreatic cancer. Clin Cancer Res 18: 839-849.
68. Hackel BJ, Sathirachinda A, Gambhir SS, (2012) Designed hydrophilic and charge mutations of the fibronectin domain: towards tailored protein biodistribution. Protein Eng Des Sel 25: 639-648.
69. Maillere B, Mourier G, Herve M, Cotton J, Leroy S, et al. (1995) Immunogenicity of a disulphide-containing neurotoxin: presentation to T-cells requires a reduction step. Toxicon 33: 475-482.
70. Zhang X, Xiong Z, Wu Y, Cai W, Tseng JR, et al. (2006) Quantitative PET imaging of tumor integrin alphav beta3 expression with 18F-FRGD2. J Nucl Med 47: 113-121.