Disulfide-rich peptides in drug development

Yıl 2020, Cilt: 48 Sayı: 3, 219 - 229, 15.06.2020

Şeyda Kara , Muharrem Akcan

https://doi.org/10.15671/hjbc.658764

Öz

Peptides are important biomolecules in drug development with their high specificities to their targets. Many peptide-based drug candidates have been increasingly involved in clinical and preclinical studies. Unfortunately, peptides have some disadvantages such as poor metabolic stability, poor oral bioavailability and high production costs. These problems can be overcome by modifications that have been inspired from highly stable disulfide-rich peptides already found in nature. This review describes the structure and bioactivity of disulfide-rich peptides and their development with various modifications to become candidate molecules in drug design and development studies.

Anahtar Kelimeler

Therapeutic peptides, drug development, cyclotides, peptide stability

Kaynakça

• 1. P. Chames, M. Van Regenmortel, E. Weiss, D. Baty, Therapeutic antibodies: successes, limitations and hopes for the future, Br J Pharmacol, 157 (2009) 220-233.
• 2. N. Munoz-Durango, M. S. Pizarro-Ortega, E. Rey-Jurado, F. E. Diaz, S. M. Bueno, A. M. Kalergis, Patterns of antibody response during natural hRSV infection: insights for the development of new antibody-based therapies. Expert Opin Investig Drugs, 27 (2018) 721-731.
• 3. T. M. Pierpont, C. B. Limper, K. L. Richards, Past, Present, and Future of Rituximab-The World's First Oncology Monoclonal Antibody Therapy. Front Oncol, 8 (2018) 163.
• 4. J. L. Lau, M. K. Dunn, Therapeutic peptides: Historical perspectives, current development trends, and future directions. Bioorg Med Chem, (2017) 2700-2707.
• 5. R. Koradi, M. Billeter, K. Wuthrich, MOLMOL: A program for display and analysis of macromolecular structures. Journal of Molecular Graphics, 14(1996) 51-55.
• 6. L. Thorstholm, D. J. Craik, Discovery and applications of naturally occurring cyclic peptides. Drug Discov Today Technol, 9 (2012) e1-e70.
• 7. J. Koehbach, D. J. Craik, The Vast Structural Diversity of Antimicrobial Peptides, Trends in Pharmacological Sciences, 40 (2019) 517-528.
• 8. J. F. Borel, C. Feurer, H. U. Gubler, H. Stahelin, Biological effects of cyclosporin A: a new antilymphocytic agent. Agents Actions, 6 (1976) 468-475.
• 9. C. Spitzfaden, H. P. Weber, W. Braun, J. Kallen, G. Wider, H. Widmer, M. D. Walkinshaw, K. Wuthrich, Cyclosporin A-cyclophilin complex formation. A model based on X-ray and NMR data. FEBS Lett, 300 (1992) 291-300.
• 10. X. Yang, P. Feng, Y. Yin, K. Bushley, J W. Spatafora, C. Wang, Cyclosporine Biosynthesis in Tolypocladium inflatum Benefits Fungal Adaptation to the Environment. mBio, 9 (2018) e01211-01218.
• 11. J. Klages, C. Neubauer, M. Coles, H. Kessler, B. Luy, Structure refinement of cyclosporin a in chloroform by using RDCs measured in a stretched PDMS-gel. Chembiochem, 6 (2005) 1672-1678.
• 12. J. C. O'Shea, J. E. Tcheng, Eptifibatide: a potent inhibitor of the platelet receptor integrin glycoprotein IIb/IIIa. Expert Opin Pharmacother, 3 (2002) 1199-1210.
• 13. D. W. Cushman, M. A. Ondetti, History of the design of captopril and related inhibitors of angiotensin converting enzyme. Hypertension 17(1991) 589-592.
• 14. A. Lodha, M. Kamaluddeen, A. Akierman, H. Amin, Role of hemocoagulase in pulmonary hemorrhage in preterm infants: a systematic review. Indian J. Pediatrics, 78 (2011) 838-844.
• 15. S. J. Ho, T. A. Brighton, Ximelagatran: Direct thrombin inhibitor. Vasc. Health Risk Manag, 2 (2006) 49-58.
• 16. T. T. Vu, A. R. Stafford, B. A. Leslie, P. Y. Kim, J. C. Fredenburgh, J. I. Weitz, Batroxobin binds fibrin with higher affinity and promotes clot expansion to a greater extent than thrombin. J. Biol. Chem. 288 (2013) 16862-16871.
• 17. T. M. A. El-Aziz, A. G. Soares, J. D. Stockand, Snake Venoms in Drug Discovery: Valuable Therapeutic Tools for Life Saving, Toxins, 11 (2019) E564.
• 18. A. Barnett, Exenatide. Expert Opin Pharmacother, 8, (2007) 2593-2608.
• 19. W. R. Gray, A. Luque, B. M. Olivera, J. Barrett, L. J. Cruz, Peptide toxins from Conus geographus venom. Journal of Biological Chemistry, 256 (1981) 4734-4740.
• 20. H. Terlau, B. M. Olivera, Conus venoms: a rich source of novel ion channel-targeted peptides. Physiological Reviews, 84 (2004) 41-68.
• 21. B. Gao, C. Peng, J. Yang, Y. Yi, J. Zhang, Q. Shi, Cone Snails: A Big Store of Conotoxins for Novel Drug Discovery, Toxins, 9 (2017) E397.
• 22. H. M. Duque, S. C. Dias, O. L. Franco, Structural and Functional Analyses of Cone Snail Toxins, Mar. Drugs, 17 (2019) E370.
• 23. K. K. Jain, An evaluation of intrathecal ziconotide for the treatment of chronic pain. Expert Opin Investig Drugs, 9 (2000) 2403-2410.
• 24. G. P. Miljanich, Ziconotide: Neuronal calcium channel blocker for treating severe chronic pain. Curr Med Chem, 11 (2004) 3029-3040.
• 25. R. J. Clark, H. Fischer, S. T. Nevin, D. J. Adams, D. J. Craik, The synthesis, structural characterization, and receptor specificity of the alpha-conotoxin Vc1.1. J. Biol. Chem. 281 (2006) 23254-23263.
• 26. J. A. DeBin, J. E. Maggio, G. R. Strichartz, Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. American Journal of Physiology Cell Physiology, 264 (1993), C361-369.
• 27. A. N. Mamelak, S. Rosenfeld, R. Bucholz, A. Raubitschek, L. B. Nabors, J. B. Fiveash, S. Shen, M. B. Khazaeli, D. Colcher, A. Liu, M. Osman, B. Guthrie, S. Schade-Bijur, D. M. Hablitz, V. L. Alvarez, M. A. Gonda, Phase I single-dose study of intracavitary-administered iodine-131-TM-601 in adults with recurrent high-grade glioma. J. Clin. Oncol., 24, (2006) 3644-3650.
• 28. M. Veiseh, P. Gabikian, S. B. Bahrami, O. Veiseh, M. Zhang, R. C. Hackman, A. C. Ravanpay, M. R. Stroud, Y. Kusuma, S. J. Hansen, D. Kwok, N. M. Munoz, R. W. Sze, W. M. Grady, N. M. Greenberg, R. G. Ellenbogen, J. M. Olson, Tumor paint: A Chlorotoxin : Cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res, 67 (2007) 6882-6888.
• 29. M. Akcan, M. R. Stroud, S. J. Hansen, R. J. Clark, N. L. Daly, D. J. Craik, J. M. Olson, Chemical Re-engineering of Chlorotoxin Improves Bioconjugation Properties for Tumor Imaging and Targeted Therapy. J Med Chem, 54 (2011) 782-787.
• 30. C. G. Patil, D. G. Walker, D. M. Miller, P. Butte, B. Morrison, D. S. Kittle, S. J. Hansen, K. L. Nufer, K. A. Bymes-Blake, M. Yamada, L. L. Lin, K. Pham, J. Perry, J. Parrish-Novak, L. Ishak, T. Prow, K. Black, A. N. Mamelak, Phase 1 Safety, Pharmacokinetics, and Fluorescence Imaging Study of Tozuleristide (BLZ-100) in Adults With Newly Diagnosed or Recurrent Gliomas. Neurosurgery (2019) E641-E649.
• 31. A. C. Conibear, K. J. Rosengren, P. J. Harvey, D. J. Craik, Structural Characterization of the Cyclic Cystine Ladder Motif of theta-Defensins. Biochemistry, 51 (2012) 9718-9726.
• 32. I. Demori, Z. E. Rashed, V. Corradino, A. Catalano, L. Rovegno, L. Queirolo, S. Salvidio, E. Biggi, M. Zanotti-Russo, L. Canesi, A. Catenazzi, E. Grasselli, Peptides for Skin Protection and Healing in Amphibians. Molecules 347 (2019) E347.
• 33. P. Escoubas, F. Bosmans, Spider peptide toxins as leads for drug development. Expert Opinion on Drug Discovery, 2 (2007) 823-835.
• 34. R. Wehbe, J. Frangieh, M. Rima, D. E. Obeid, J. M. Sabatier, Z. Fajloun, Bee Venom: Overview of Main Compounds and Bioactivities for Therapeutic Interests, Molecules, 24 (2019) E2997.
• 35. S. T. Henriques, D. J. Craik, Cyclotides as templates in drug design. Drug Discovery Today, 15 (2010) 57-64.
• 36. B. Franke, J. S. Mylne, K. L. Rosengren, Buried treasure: biosynthesis, structures and applications of cyclic peptides hidden in seed storage albumins. Nat Prod Rep, 35 (2018) 137-146.
• 37. Y. Q. Long, S. L. Lee, C.Y. Lin, I. J. Enyedy, S. Wang, P. Li, R. B. Dickson, P. P. Roller, Synthesis and evaluation of the sunflower derived trypsin inhibitor as a potent inhibitor of the type II transmembrane serine protease, matriptase. Bioorg Med Chem Lett, 11 (2001) 2515-2519.
• 38. M. L. Colgrave, M. J. Korsinczky, R. J. Clark, F. Foley, D. J. Craik, Sunflower trypsin inhibitor-1, proteolytic studies on a trypsin inhibitor peptide and its analogs. Biopolymers, 94 (2010) 665-672.
• 39. L. Gran, On the effect of a polypeptide isolated from "Kalata-Kalata" (Oldenlandia affinis DC) on the oestrogen dominated uterus. Acta Pharmacol. Toxicol., 33 (1973) 400-408.
• 40. P. K. Pallaghy, K. J. Nielsen, D. J. Craik, R. S. Norton, A common structural motif incorporating a cystine knot and a triple stranded beta sheet in toxic and inhibitory polypeptides. Protein Science, 3 (1994) 1833-1839.
• 41. O. Saether, D. J. Craik, I. D. Campbell, K. Sletten, J. Juul, D. G. Norman, Elucidation of the primary and three-dimensional structure of the uterotonic polypeptide kalata B1. Biochemistry, 34 (1995) 4147-4158.
• 42. J. Weidmann, D. J. Craik, Discovery, structure, function, and applications of cyclotides: circular proteins from plants. J Exp Bot, 67 (2016) 4801-4812.
• 43. K. T. N. Giang, Y. L. Lian, E. W. H. Pang, Q. T. N. Phuong, T. D. Tran, J. P. Tam, Discovery of Linear Cyclotides in Monocot Plant Panicum laxum of Poaceae Family Provides New Insights into Evolution and Distribution of Cyclotides in Plants. Journal of Biological Chemistry, 288 (2013) 3370-3380.
• 44. S. Park, K. O. Yoo, T. Marcussen, A. Backlund, E. Jacobsson, K. J. Rosengren, I. Doo, U. Goransson, Cyclotide Evolution: Insights from the Analyses of Their Precursor Sequences, Structures and Distribution in Violets (Viola). Front Plant Sci, 8 (2017) 2058.
• 45. D. J. Craik, N. L. Daly, T. Bond, C. Waine, Plant Cyclotides: A Unique Family of Cyclic and Knotted Proteins that Defines the Cyclic Cystine Knot Structural Motif, J. Mol. Biol. 294 (1999) 1327-1336.
• 46. D. J. Craik, Joseph Rudinger memorial lecture: Discovery and applications of cyclotides (2013).
• 47. Y. H. Huang, Q. Du, D. J. Craik, Cyclotides: disulfide-rich peptide toxins in plants. Toxicon. 25 (2019) 33-44.
• 48. C. K. Wang, Q. Kaas, L. Chiche, D. J. Craik, CyBase: A database of cyclic protein sequences and structures, with applications in protein discovery and engineering. Nucleic Acids Res., 36 (2008) D206-210.
• 49. M. L. Colgrave, D. J. Craik, Thermal, chemical, and enzymatic stability of the cyclotide kalata B1: The importance of the cyclic cystine knot. Biochemistry, 43 (2004) 5965-5975.
• 50. S. Gunasekera, N. L. Daly, R. J. Clark, D. J. Craik, Dissecting the Oxidative Folding of Circular Cystine Knot Miniproteins. Antioxidants & Redox Signaling, 11 (2009) 971-980.
• 51. T. L. Aboye, R. J. Clark, R. Burman, M. B. Roig, D. J. Craik, U. Goransson, Interlocking Disulfides in Circular Proteins: Toward Efficient Oxidative Folding of Cyclotides. Antioxidants & Redox Signaling, 14 (2011) 77-86.
• 52. C. V. Jennings, K. J. Rosengren, N. L. Daly, M. Plan, J. Stevens, M. J. Scanlon, C. Waine, D. G. Norman, M. A. Anderson, M. A. D. J. Craik, Isolation, solution structure, and insecticidal activity of kalata B2, a circular protein with a twist: do Mobius strips exist in nature? Biochemistry, 44 (2005) 851-860.
• 53. C. Jennings, J. West, C. Waine, D. Craik, M. Anderson, Biosynthesis and insecticidal properties of plant cyclotides: the cyclic knotted proteins from Oldenlandia affinis. Proceedings of the National Academy of Sciences of the United States of America, 98 (2001) 10614-10619.
• 54. M. R. Plan, I. Saska, A. G. Cagauan, D. J. Craik, Backbone Cyclised Peptides from Plants Show Molluscicidal Activity against the Rice Pest Pomacea canaliculata (Golden Apple Snail) (2008) 5237-5241.
• 55. N. L. Daly, K. J. Rosengren, D. J. Craik, Discovery, structure and biological activities of cyclotides. Advanced Drug Delivery Reviews, 61 (2009) 918–930.
• 56. Craik, D. J. Host-defense activities of cyclotides. Toxins (Basel), 4 (2012) 139-156.
• 57. S. T. Henriques, Y. H. Huang, M. Castanho, L. A. Bagatolli, S. Sonza, G. Tachedjian, N. L. Daly, D. J. Craik, Phosphatidylethanolamine Binding Is a Conserved Feature of Cyclotide-Membrane Interactions. Journal of Biological Chemistry, 287 (2012) 33629-33643.
• 58. S. T. Henriques, Y. H. Huang, S. Chaousis, M. A. Sani, A. G. Poth, F. Separovic, D. J. Craik, The Prototypic Cyclotide Kalata B1 Has a Unique Mechanism of Entering Cells. Chem Biol, 22 (2015) 1087-1097.
• 59. L. Cascales, S. T. Henriques, M. C. Kerr, Y. H. Huang, M. J. Sweet, N. L. Daly, D. J. Craik, Identification and characterization of a new family of cell-penetrating peptides: cyclic cell-penetrating peptides. J Biol Chem, 286 (2011) 36932-36943.
• 60. S. J. De Veer, J. Weidmann, D. J. Craik, D. J. Cyclotides as Tools in Chemical Biology. Acc Chem Res, 50 (2017) 1557-1565.
• 61. A. Hermann, E. Syangard, P. Claeson, J. Gullbo, L. Bohlin, U. Göransson, Key role of glutamic acid for the cytotoxic activity of the cyclotide cycloviolacin O2. Cell. Mol. Life Sci. 63 (2006), 235-245.
• 62. P. Lindholm, U. Göransson, S. Johans, P. Claeson, J. Gullbo, R. Larsson, L. Bohlin, A. Backlund, Cyclotides: A Novel Type of Cytotoxic Agents. Molecular Cancer Therapeutics, 1 (2002) 365-369.
• 63. R. Burman, G. S. Stromstedt, M. Malmsten, U. Göransson, Cyclotide–membrane interactions: Defining factors of membrane binding, depletion and disruption, Biochimica et Biophysica Acta 1808 (2011) 2665-2673.
• 64. R. Burman, S. Gunasekera, A. A. Stromstedt, U. Goransson, Chemistry and biology of cyclotides: circular plant peptides outside the box. J Nat Prod, 77 (2014) 724-736.
• 65. R. J. Clark, M. Akcan, Q. Kaas, N. L. Daly, D. J. Craik, Cyclization of conotoxins to improve their biopharmaceutical properties. Toxicon, 59 (2012) 446-455.
• 66. D. J. Craik, J. Du, Cyclotides as drug design scaffolds. Curr Opin Chem Biol, 38 (2017) 8-16.
• 67. C. K. Wang, D. J. Craik. Designing macrocyclic disulfide-rich peptides for biotechnological applications. Nat Chem Biol, 14 (2018) 417-427.
• 68. J. A. Camerero, M. J. Campbell, The Potential of the Cyclotide Scaffold for Drug Development, Biomedicines, 7 (2019) E31.
• 69. P. G. Ojeda, M. H. Cardoso, O. H. Franco, Pharmaceutical applications of cyclotides. Drug Discovery Today, 24 (2019) 2152-2161.
• 70. R. J. Clark, J. Jensen, S. T. Nevin, B. P. Callaghan, D. J. Adams, D. J. Craik, The engineering of an orally active conotoxin for the treatment of neuropathic pain. Angewandte Chemie International Edition, 49 (2010) 6545-6548.
• 71. L. Y. Chan, V. M. Zhang, Y. H. Huang, N. C. Waters, P. S. Bansal, D. J. Craik, N. L. Daly, Cyclization of the antimicrobial peptide gomesin with native chemical ligation: influences on stability and bioactivity. Chembiochem, 14 (2013) 617-624.
• 72. M. Akcan, R. J. Clark, N. L. Daly, A. C. Conibear, A. de Faoite, M. D. Heghinian, T. Sahil, D. J. Adams, F. Mari, D. J. Craik, Transforming conotoxins into cyclotides: Backbone cyclization of P-superfamily conotoxins. Biopolymers, 104 (2015) 682-692.
• 73. R. J. Clark, H. Fischer, L. Dempster, N. L. Daly, K. J. Rosengren, S. T. Nevin, F. A. Meunier, D. J. Adams, D. J. Craik, Engineering stable peptide toxins by means of backbone cyclization: stabilization of the alpha-conotoxin MII. Proceedings of the National Academy of Sciences, 102 (2005) 13767-13772.
• 74. X. Chen, L. Zhang, Y. Wu, L. Wang, C. Ma, X. Xi, O.R. P. Bininda-Emonds, C. Shaw, T. Chen, M Zhou, Evaluation of the bioactivity of a mastoparan peptide from wasp venom and of its analogues designed through targeted engineering. Int J Biol Sci, 14 (2018) 599-607.
• 75. N. Lawrence, A. S. M. Dennis, A. M. Lehane, A. Ehmann, P. J. Harvey, A. H. Benfield, O. Cheneval, S. T. Henriques, D. J. Craik, B. J. McMorran, Defense Peptides Engineered from Human Platelet Factor 4 Kill Plasmodium by Selective Membrane Disruption. Cell Chem Biol, 25 (2018) 1140-1150.
• 76. P. Quimbar, U. Malik, C. P. Sommerhoff, Q. Kaas, L. Y. Chan, Y. H. Huang, M. Grundhuber, K. Dunse, D. J. Craik, M. A. Anderson, N. L. Daly, High-affinity cyclic peptide matriptase inhibitors. J Biol Chem, 288 (2013) 13885-13896.
• 77. C. K. Wang, C. W. Gruber, M. Cemazar, C. Siatskas, P. Tagore, N. Payne, G. Sun, S. Wang, C. C. Bernard, D. J. Craik, Molecular grafting onto a stable framework yields novel cyclic peptides for the treatment of multiple sclerosis. ACS Chem Biol, 9 (2014) 156-163.
• 78. C. D'Souza, S. T. Henriques, C. K. Wang, O. Cheneval, L. Y. Chan, N. J. Bokil, M. J. Sweet, D. J. Craik, Using the MCoTI-II Cyclotide Scaffold To Design a Stable Cyclic Peptide Antagonist of SET, a Protein Overexpressed in Human Cancer. Biochemistry, 55 (2016) 396-405.
• 79. C. Cobos Caceres, P. S. Bansal, S. Navarro, D. Wilson, L. Don, P. Giacomin, A. Loukas, N. L. Daly,. An engineered cyclic peptide alleviates symptoms of inflammation in a murine model of inflammatory bowel disease. J Biol Chem, 292 (2017) 10288-10294.
• 80. L. Y. Chan, D. J. Craik, N. L. Daly, Cyclic thrombospondin-1 mimetics: grafting of a thrombospondin sequence into circular disulfide-rich frameworks to inhibit endothelial cell migration. Biosci Rep, 35 (2015) e00270.
• 81. C. T. T. Wong, D. K. Rowlands, C. H. Wong, T. W. C. Lo, G. K. T. Nguyen, H. Y. Li, J. P. Tam, Orally Active Peptidic Bradykinin B1 Receptor Antagonists Engineered from a Cyclotide Scaffold for Inflammatory Pain Treatment, Angew. Chem. Int. Ed., 51 (2012) 5620-5624.
• 82. Y. Qiu, M. Taichi, N. Wei, H. Yang, K. Q. Luo, J. P. Tam, An Orally Active Bradykinin B1 Receptor Antagonist Engineered as a Bifunctional Chimera of Sunflower Trypsin Inhibitor. J Med Chem, 60 (2017) 504-510.
• 83. F. Jia, J. Wang, J. Peng, P. Zhao, Z. Kong, K. Wang, W. Yan, R. Wang, D-amino acid substitution enhances the stability of antimicrobial peptide polybia-CP. Acta Biochim Biophys Sin (Shanghai), 49 (2017) 916-925.
• 84. L. Sando, S. T. Henriques, F. Foley, S. M. Simonsen, N. L. Daly, K. N. Hall, K. R. Gustafson, M. I. Aguilar, D. J. Craik, A Synthetic mirror image of kalata B1 reveals that cyclotide activity is independent of a protein receptor. Chembiochem, 12 (2011) 2456-2462.
• 85. C. J. Armishaw, N. L. Daly, S. T. Nevin, D. J. Adams, D. J., Craik, P. F. Alewood, alpha-selenoconotoxins, a new class of potent alpha(7) neuronal nicotinic receptor antagonists. Journal of Biological Chemistry, 281 (2006) 14136-14143.
• 86. J. Kindrachuk, E. Scruten, S. Attah-Poku, K. Bell, A. Potter, L. A. Babiuk, P. J. Griebel, S. Napper,. Stability, Toxicity, and Biological Activity of Host Defense Peptide BMAP28 and Its Inversed and Retro-Inversed Isomers, PeptideScience, 96 (2010) 14-24.
• 87. D. J. Craik, D. J. Adams, Chemical modification of conotoxins to improve stability and activity. Acs Chemical Biology, 2 (2007) 457-468.
• 88. N. Yin, Enhancing the Oral Bioavailability of Peptide Drugs by using Chemical Modification and Other Approaches. Medicinal Chemistry, 4 (2014) 763-769.