The two-step biosynthesis of cyclic peptides from linear precursors in a member of the plant family caryophyllaceae involves cyclization by a serine protease-like enzyme

Journal of Biological Chemistry

Volumn 288, Issue 18, 2013, Pages 12500-12510

  Barber, Carla J S ^a   Pujara, Pareshkumar T ^a   Reed, Darwin W ^a   Chiwocha, Shiela ^a   Zhang, Haixia ^a   Covello, Patrick S ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ASSAY; FLANKING SEQUENCE; LINEAR PRECURSORS; PROTEINOGENIC AMINO ACIDS; RIBOSOMAL TRANSLATION; SAPONARIA VACCARIA; SUBSTRATE SPECIFICITY; SYNTHETIC PEPTIDE;

AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; CLONING; CYCLIZATION; ENZYMES; MOLECULAR BIOLOGY; PURIFICATION;

PEPTIDES;

COMPLEMENTARY DNA; CYCLOPEPTIDE; OLIGOPEPTIDASE 1; PEPTIDE CYCLASE 1; PROTEIN PRECURSOR; RECOMBINANT ENZYME; RECOMBINANT PEPTIDE CYCLASE 1; SERINE PROTEINASE; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CARYOPHYLLACEAE; CATALYSIS; CHROMATOGRAPHY; CONTROLLED STUDY; CYCLIZATION; DNA FLANKING REGION; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME SPECIFICITY; MOLECULAR CLONING; NONHUMAN; PLANT SEED; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN SYNTHESIS; PROTEOMICS; SAPONARIA; SAPONARIA VACCARIA;

CARYOPHYLLACEAE; CYCLIC PEPTIDE; PEPTIDASES; PEPTIDE BIOSYNTHESIS; PEPTIDE CYCLASE; PLANT BIOCHEMISTRY; PLANT MOLECULAR BIOLOGY; PROTEASE; SAPONARIA VACCARIA;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; DNA, COMPLEMENTARY; MOLECULAR SEQUENCE DATA; PEPTIDE BIOSYNTHESIS, NUCLEIC ACID-INDEPENDENT; PEPTIDES, CYCLIC; PLANT PROTEINS; SAPONARIA; SEEDS; SERINE PROTEASES;

CARYOPHYLLACEAE; LINACEAE; RUTACEAE; VACCARIA; VACCARIA HISPANICA;

EID: 84877149384     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.437947     Document Type: Article

References (56)

1. Kaufmann, H. P., and Tobschirbel, A. (1959) An oligopeptide from flax-seed. Chem. Ber. 92, 2805-2809
2. Cascales, L., and Craik, D. J. (2010) Naturally occurring circular proteins. Distribution, biosynthesis and evolution. Org. Biomol. Chem. 8, 5035-5047
3. Conlan, B. F., Gillon, A. D., Craik, D. J., and Anderson, M. A. (2010) Circular proteins and mechanisms of cyclization. Biopolymers 94, 573-583
4. Craik, D. J., Daly, N. L., Mulvenna, J., Plan, M. R., and Trabi, M. (2004) Discovery, structure and biological activities of the cyclotides. Curr. Protein Pept. Sci. 5, 297-315 (Pubitemid 39200161)
5. Jones, A. C., Gu, L., Sorrels, C. M., Sherman, D. H., and Gerwick, W. H. (2009) New tricks from ancient algae. Natural products biosynthesis in marine cyanobacteria. Curr. Opin. Chem. Biol. 13, 216-223
6. Picur, B., Cebrat, M., Zabrocki, J., and Siemion, I. Z. (2006) Cyclopeptides of Linum usitatissimum. J. Pept. Sci. 12, 569-574 (Pubitemid 44400224)
7. Pomilio, A. B., Battista, M. E., and Vitale, A. A. (2006) Naturally-occurring cyclopeptides. Structures and bioactivity. Curr. Org. Chem. 10, 2075-2121
8. Selsted, M. E. (2004) θ-Defensins. Cyclic antimicrobial peptides produced by binary ligation of truncated α-defensins. Curr. Protein Pept. Sci. 5, 365-371
9. Arnison, P. G., Bibb, M. J., Bierbaum, G., Bowers, A. A., Bugni, T. S., Bulaj, G., Camarero, J. A., Campopiano, D. J., Challis, G. L., Clardy, J., Cotter, P. D., Craik, D. J., Dawson, M., Dittmann, E., Donadio, S., Dorrestein, P. C., Entian, K. D., Fischbach, M. A., Garavelli, J. S., Göransson, U., Gruber, C. W., Haft, D. H., Hemscheidt, T. K., Hertweck, C., Hill, C., Horswill, A. R., Jaspars, M., Kelly, W. L., Klinman, J. P., Kuipers, O. P., Link, A. J., Liu, W., Marahiel, M. A., Mitchell, D. A., Moll, G. N., Moore, B. S., Müller, R., Nair, S. K., Nes, I. F., Norris, G. E., Olivera, B. M., Onaka, H., Patchett, M. L., Piel, J., Reaney, M. J., Rebuffat, S., Ross, R. P., Sahl, H. G., Schmidt, E. W., Selsted, M. E., Severinov, K., Shen, B., Sivonen, K., Smith, L., Stein, T., Sussmuth, R. D., Tagg, J. R., Tang, G. L., Truman, A. W., Vederas, J. C., Walsh, C. T., Walton, J. D., Wenzel, S. C., Willey, J. M., and van der Donk, W. A. (2013) Ribosomally synthesized and post-translationally modified peptide natural products. Overview and recommendations for a universal nomenclature. Nat. Prod. Rep. 30, 108-160
10. Morita, H., and Takeya, K. (2010) Bioactive cyclic peptides from higher plants. Heterocycles 80, 739-764
11. Morita, H., Eda, M., Iizuka, T., Hirasawa, Y., Sekiguchi, M., Yun, Y. S., Itokawa, H., and Takeya, K. (2006) Structure of a new cyclic nonapeptide, segetalin F, and vasorelaxant activity of segetalins from Vaccaria segetalis. Bioorg. Med. Chem. Lett. 16, 4458-4461 (Pubitemid 44094096)
12. Namjoshi, S., and Benson, H. A. (2010) Cyclic peptides as potential therapeutic agents for skin disorders. Biopolymers 94, 673-680
13. Sancheti, H., and Camarero, J. A. (2009) "Splicing up" drug discovery. Cell-based expression and screening of genetically-encoded libraries of backbone-cyclized polypeptides. Adv. Drug Deliv. Rev. 61, 908-917
14. White, C. J., and Yudin, A. K. (2011) Contemporary strategies for peptide macrocyclization. Nat. Chem. 3, 509-524
15. Meier, J. L., and Burkart, M. D. (2009) The chemical biology of modular biosynthetic enzymes. Chem. Soc Rev. 38, 2012-2045
16. Walsh, C. T., Chen, H., Keating, T. A., Hubbard, B. K., Losey, H. C., Luo, L., Marshall, C. G., Miller, D. A., and Patel, H. M. (2001) Tailoring enzymes that modify nonribosomal peptides during and after chain elongation on NRPS assembly lines. Curr. Opin. Chem. Biol. 5, 525-534 (Pubitemid 32907603)
17. Condie, J. A., Nowak, G., Reed, D. W., Balsevich, J. J., Reaney, M. J., Arnison, P. G., and Covello, P. S. (2011) The biosynthesis of Caryophyllaceaelike cyclic peptides in Saponaria vaccaria L. from DNA-encoded precursors. Plant J. 67, 682-690
18. Poth, A. G., Mylne, J. S., Grassl, J., Lyons, R. E., Millar, A. H., Colgrave, M. L., and Craik, D. J. (2012) Cyclotides associate with leaf vasculature and are the products of a novel precursor in petunia (Solanaceae). J. Biol. Chem. 287, 27033-27046
19. Katoh, T., Goto, Y., Reza, M. S., and Suga, H. (2011) Ribosomal synthesis of backbone macrocyclic peptides. Chem. Commun. (Camb.) 47, 9946-9958
20. Mylne, J. S., Colgrave, M. L., Daly, N. L., Chanson, A. H., Elliott, A. G., McCallum, E. J., Jones, A., and Craik, D. J. (2011) Albumins and their processing machinery are hijacked for cyclic peptides in sunflower. Nat. Chem. Biol. 7, 257-259
21. Poth, A. G., Colgrave, M. L., Lyons, R. E., Daly, N. L., and Craik, D. J. (2011) Discovery of an unusual biosynthetic origin for circular proteins in legumes. Proc. Natl. Acad. Sci. U.S.A. 108, 10127-10132
22. Poth, A. G., Colgrave, M. L., Philip, R., Kerenga, B., Daly, N. L., Anderson, M. A., and Craik, D. J. (2011) Discovery of cyclotides in the fabaceae plant family provides new insights into the cyclization, evolution, and distribution of circular proteins. ACS Chem. Biol. 6, 345-355
23. Saska, I., Gillon, A. D., Hatsugai, N., Dietzgen, R. G., Hara-Nishimura, I., Anderson, M. A., and Craik, D. J. (2007) An asparaginyl endopeptidase mediates in vivo protein backbone cyclization. J. Biol. Chem. 282, 29721-29728 (Pubitemid 350043339)
24. Schmidt, E. W., Nelson, J. T., Rasko, D. A., Sudek, S., Eisen, J. A., Haygood, M. G., and Ravel, J. (2005) Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc. Natl. Acad. Sci. U.S.A. 102, 7315-7320 (Pubitemid 40696376)
25. Jennings, C., West, J., Waine, C., Craik, D., and Anderson, M. (2001) Biosynthesis and insecticidal properties of plant cyclotides. The cyclic knotted proteins from Oldenlandia affinis. Proc. Natl. Acad. Sci. U.S.A. 98, 10614-10619 (Pubitemid 32878669)
26. Walton, J. D., Hallen-Adams, H. E., and Luo, H. (2010) Ribosomal biosynthesis of the cyclic peptide toxins of Amanita mushrooms. Biopolymers 94, 659-664
27. Tan, N. H., and Zhou, J. (2006) Plant cyclopeptides. Chem. Rev. 106, 840-895
28. Morita, H., Yun, Y. S., Takeya, K., and Itokawa, H. (1994) Segetalin A, a new cyclic peptide from Vaccaria segetalis. Tetrahedron Lett. 51, 9593-9596 (Pubitemid 24374297)
29. Gambino, G., Perrone, I., and Gribaudo, I. (2008) A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem. Anal. 19, 520-525
30. Gaasterland, T., and Sensen, C. W. (1996) Fully automated genome analysis that reflects user needs and preferences.Adetailed introduction to the MAGPIE system architecture. Biochimie 78, 302-310 (Pubitemid 26394637)
31. Chevreux, B., Pfisterer, T., Drescher, B., Driesel, A. J., Müller, W. E., Wetter, T., and Suhai, S. (2004) Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 14, 1147-1159 (Pubitemid 38811551)
32. Rappsilber, J., Ishihama, Y., and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670 (Pubitemid 36176744)
33. Meesapyodsuk, D., Balsevich, J., Reed, D. W., and Covello, P. S. (2007) Saponin biosynthesis in Saponaria vaccaria. cDNAs encoding β-amyrin synthase and a triterpene carboxylic acid glucosyltransferase. Plant Physiol. 143, 959-969 (Pubitemid 46940955)
34. Sheoran, I. S., Olson, D. J., Ross, A. R., and Sawhney, V. K. (2005) Proteome analysis of embryo and endosperm from germinating tomato seeds. Proteomics 5, 3752-3764 (Pubitemid 41393306)
35. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207-234
36. Meesapyodsuk, D., Reed, D. W., Covello, P. S., and Qiu, X. (2007) Primary structure, regioselectivity, and evolution of the membrane-bound fatty acid desaturases of Claviceps purpurea. J. Biol. Chem. 282, 20191-20199 (Pubitemid 47100013)
37. Johnston, R. B., Mycek, M. J., and Fruton, J. S. (1950) Catalysis of transpeptidation reactions by chymotrypsin. J. Biol. Chem. 187, 205-211
38. Berkers, C. R., de Jong, A., Ovaa, H., and Rodenko, B. (2009) Transpeptidation and reverse proteolysis and their consequences for immunity. Int. J. Biochem. Cell Biol. 41, 66-71
39. Marx, U. C., Korsinczky, M. L., Schirra, H. J., Jones, A., Condie, B., Otvos, L., Jr., and Craik, D. J. (2003) Enzymatic cyclization of a potent Bowman-Birk protease inhibitor, sunflower trypsin inhibitor-1, and solution structure of an acyclic precursor peptide. J. Biol. Chem. 278, 21782-21789 (Pubitemid 36792582)
40. Akoh, C. C., Lee, G. C., Liaw, Y. C., Huang, T. H., and Shaw, J. F. (2004) GDSL family of serine esterases/lipases. Prog. Lipid Res. 43, 534-552 (Pubitemid 39441345)
41. Fülöp, V., Böcskei, Z., and Polgár, L. (1998) Prolyl oligopeptidase. An unusual β-propeller domain regulates proteolysis. Cell 94, 161-170
42. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (Pubitemid 24007801)
43. Ollis, D. L., Cheah, E., Cygler, M., Dijkstra, B., Frolow, F., Franken, S. M., Harel, M., Remington, S. J., Silman, I., and Schrag, J. (1992) The α/β hydrolase fold. Protein Eng. 5, 197-211
44. Garcia, A. E., and Camarero, J. A. (2010) Biological activities of natural and engineered cyclotides, a novel molecular scaffold for peptide-based therapeutics. Curr. Mol. Pharmacol. 3, 153-163
45. Ghadiri, M. R., Granja, J. R., Milligan, R. A., McRee, D. E., and Khazanovich, N. (1993) Self-assembling organic nanotubes based on a cyclic peptide architecture. Nature 366, 324-327 (Pubitemid 23349358)
46. Hourani, R., Zhang, C., van der Weegen, R., Ruiz, L., Li, C., Keten, S., Helms, B. A., and Xu, T. (2011) Processable cyclic peptide nanotubes with tunable interiors. J. Am. Chem. Soc. 133, 15296-15299
47. Jia, A., Li, X., Tan, N., Liu, X., Shen, Y., and Zhou, J. (2006) Enzymatic cyclization of linear peptide to plant cyclopeptide heterophyllin B. Sci. China Series B Chem. 49, 63-66
48. Mylne, J. S., Chan, L. Y., Chanson, A. H., Daly, N. L., Schaefer, H., Bailey, T. L., Nguyencong, P., Cascales, L., and Craik, D. J. (2012) Cyclic peptides arising by evolutionary parallelism via asparaginyl-endopeptidase- mediated biosynthesis. Plant Cell 24, 2765-2778
49. Gui, B., Shim, Y. Y., Datla, R. S., Covello, P. S., Stone, S. L., and Reaney, M. J. (2012) Identification and quantification of cyclolinopeptides in five flaxseed cultivars. J. Agric. Food Chem. 60, 8571-8579
50. Sivonen, K., Leikoski, N., Fewer, D. P., and Jokela, J. (2010) Cyanobactins-ribosomal cyclic peptides produced by cyanobacteria. Appl. Microbiol. Biotechnol. 86, 1213-1225
51. Lee, J., McIntosh, J., Hathaway, B. J., and Schmidt, E. W. (2009) Using marine natural products to discover a protease that catalyzes peptide macrocyclization of diverse substrates. J. Am. Chem. Soc. 131, 2122-2124
52. Szeltner, Z., Rea, D., Juhász, T., Renner, V., Fülöp, V., and Polgár, L. (2004) Concerted structural changes in the peptidase and the propeller domains of prolyl oligopeptidase are required for substrate binding. J. Mol. Biol. 340, 627-637 (Pubitemid 38798005)
53. Koehnke, J., Bent, A., Houssen, W. E., Zollman, D., Morawitz, F., Shirran, S., Vendome, J., Nneoyiegbe, A. F., Trembleau, L., Botting, C. H., Smith, M. C., Jaspars, M., and Naismith, J. H. (2012) The mechanism of patellamide macrocyclization revealed by the characterization of the PatG macrocyclase domain. Nat. Struct. Mol. Biol. 19, 767-772
54. Agarwal, V., Pierce, E., McIntosh, J., Schmidt, E. W., and Nair, S. K. (2012) Structures of cyanobactin maturation enzymes define a family of transamidating proteases. Chem. Biol. 19, 1411-1422
55. 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 Engl. 51, 5620-5624
56. Hoogerhout, P., Kamphuis, W., Brugghe, H. F., Sluijs, J. A., Timmermans, H. A., Westdijk, J., Zomer, G., Boog, C. J., Hol, E. M., and van den Dobbelsteen, G. P. (2011) A cyclic undecamer peptide mimics a turn in folded Alzheimer amyloid beta and elicits antibodies against oligomeric and fibrillar amyloid and plaques. PLoS One 6, e19110