Cyclotides associate with leaf vasculature and are the products of a novel precursor in Petunia (Solanaceae)

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 27033-27046

  Poth, Aaron G ^a,b   Mylne, Joshua S ^a   Grassl, Julia ^c   Lyons, Russell E ^b   Millar, A Harvey ^c   Colgrave, Michelle L ^b   Craik, David J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b CSIRO   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CONVERGENT EVOLUTION; CUCURBITACEAE; CYCLOPEPTIDES; CYCLOTIDES; DIFFERENT PRECURSORS; DISULFIDE BONDS; LEAF-SECTION; NOVEL PRECURSORS; PLANT FAMILIES; PLANT KINGDOM; PLANT PEPTIDES; RUBIACEAE; SOLANACEAE; VASCULATURE;

COVALENT BONDS; GENE ENCODING; PEPTIDES;

ENCODING (SYMBOLS);

ACYCLOTIDE; CYCLINE; CYCLOTIDE; CYSTINE; PETUNIA EXTRACT; PLANT EXTRACT; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONCENTRATION (PARAMETERS); GENETIC TRANSCRIPTION; LEAF LAMINA; LEAF MORPHOLOGY; LEAF STRUCTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PETUNIA; PHYLOGENY; PLANT GENETICS; PLANT LEAF; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; VASCULARIZATION;

AMINO ACID SEQUENCE; CYCLOTIDES; GENES, PLANT; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANT PROTEINS; PROTEIN PRECURSORS; SEQUENCE HOMOLOGY, AMINO ACID; SOLANACEAE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

CUCURBITACEAE; FABACEAE; PETUNIA; RUBIACEAE; SOLANACEAE; VIOLACEAE;

EID: 84864551708     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.370841     Document Type: Article

References (73)

1. Craik, D. J., Daly, N. L., Bond, T., and 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 (Pubitemid 30008803)
2. 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)
3. Plan, M. R., Saska, I., Cagauan, A. G., and Craik, D. J. (2008) Backbone cyclized peptides from plants show molluscicidal activity against the rice pest Pomacea canaliculata (golden apple snail). J. Agric. Food Chem. 56, 5237-5241 (Pubitemid 352039129)
4. Colgrave, M. L., Kotze, A. C., Huang, Y. H., O'Grady, J., Simonsen, S. M., and Craik, D. J. (2008) Cyclotides. Natural, circular plant peptides that possess significant activity against gastrointestinal nematode parasites of sheep. Biochemistry 47, 5581-5589 (Pubitemid 351705169)
5. Gran, L. (1973) On the effect of a polypeptide isolated from "Kalata-Kalata" (Oldenlandia affinis DC) on the estrogen-dominated uterus. Acta Pharmacol. Toxicol. 33, 400-408
6. Gustafson, K. R., Sowder, R. C., Henderson, L. E., Parsons, I. C., Kashman, Y., Cardellina, J. H., McMahon, J. B., Buckheit, R. W., Pannell, L. K., and Boyd, M. R. (1994) Circulins A and B: novel HIV-inhibitory macrocyclic peptides from the tropical tree Chassalia parvifolia. J. Am. Chem. Soc. 116, 9337-9338
7. Lindholm, P., Göransson, U., Johansson, S., Claeson, P., Gullbo, J., Larsson, R., Bohlin, L., and Backlund, A. (2002) Cyclotides. A novel type of cytotoxic agents. Mol. Cancer Ther. 1, 365-369
8. Witherup, K. M., Bogusky, M. J., Anderson, P. S., Ramjit, H., Ransom, R. W., Wood, T., and Sardana, M. (1994) Cyclopsychotride A, a biologically active, 31-residue cyclic peptide isolated from Psychotria longipes. J. Nat. Prod. 57, 1619-1625
9. 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. 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 (Pubitemid 38669464)
11. Heitz, A., Avrutina, O., Le-Nguyen, D., Diederichsen, U., Hernandez, J. F., Gracy, J., Kolmar, H., and Chiche, L. (2008) Knottin cyclization. Impact on structure and dynamics. BMC Struct. Biol. 8, 54
12. 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 (Pubitemid 30307960)
13. Craik, D. J., Cemazar, M., Wang, C. K., and Daly, N. L. (2006) The cyclotide family of circular miniproteins. Nature's combinatorial peptide template. Biopolymers 84, 250-266
14. Craik, D. J., Cemazar, M., and Daly, N. L. (2006) Curr. Opin. Drug Discov. Dev. 9, 251-260
15. 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
16. 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
17. Sommerhoff, C. P., Avrutina, O., Schmoldt, H. U., Gabrijelcic-Geiger, D., Diederichsen, U., and Kolmar, H. (2010) Engineered cystine knot miniproteins as potent inhibitors of human mast cell tryptase β. J. Mol. Biol. 395, 167-175
18. Dutton, J. L., Renda, R. F., Waine, C., Clark, R. J., Daly, N. L., Jennings, C. V., Anderson, M. A., and Craik, D. J. (2004) Conserved structural and sequence elements implicated in the processing of gene-encoded circular proteins. J. Biol. Chem. 279, 46858-46867 (Pubitemid 39518337)
19. Kaas, Q., and Craik, D. J. (2010) Analysis and classification of circular proteins in CyBase. Biopolymers 94, 584-591
20. 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
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. Nguyen, G. K., Zhang, S., Nguyen, N. T., Nguyen, P. Q., Chiu, M. S., Hardjojo, A., and Tam, J. P. (2011) Discovery and characterization of novel cyclotides originated from chimeric precursors consisting of albumin-1 chain a and cyclotide domains in the Fabaceae family. J. Biol. Chem. 286, 24275-24287
23. Higgins, T. J., Chandler, P. M., Randall, P. J., Spencer, D., Beach, L. R., Blagrove, R. J., Kortt, A. A., and Inglis, A. S. (1986) Gene structure, protein structure, and regulation of the synthesis of a sulfur-rich protein in pea seeds. J. Biol. Chem. 261, 11124-11130 (Pubitemid 17216714)
24. Gerlach, S. L., Burman, R., Bohlin, L., Mondal, D., and Göransson, U. (2010) Isolation, characterization, and bioactivity of cyclotides from the Micronesian plant Psychotria leptothyrsa. J. Nat. Prod. 73, 1207-1213
25. Mylne, J. S., Wang, C. K., van der Weerden, N. L., and Craik, D. J. (2010) Cyclotides are a component of the innate defense of Oldenlandia affinis. Biopolymers 94, 635-646
26. Trabi, M., and Craik, D. J. (2004) Tissue-specific expression of head-to-tail cyclized miniproteins in Violaceae and structure determination of the root cyclotide Viola hederacea root cyclotide1. Plant Cell 16, 2204-2216 (Pubitemid 39059738)
27. Conlan, B. F., Gillon, A. D., Barbeta, B. L., and Anderson, M. A. (2011) Subcellular targeting and biosynthesis of cyclotides in plant cells. Am. J. Bot. 98, 2018-2026
28. Jennings, C. V., Rosengren, K. J., Daly, N. L., Plan, M., Stevens, J., Scanlon, M. J., Waine, C., Norman, D. G., Anderson, M. A., and Craik, D. J. (2005) Isolation, solution structure, and insecticidal activity of kalata B2, a circular protein with a twist. Do Möbius strips exist in nature? Biochemistry 44, 851-860 (Pubitemid 40129645)
29. Simonsen, S. M., Sando, L., Rosengren, K. J., Wang, C. K., Colgrave, M. L., Daly, N. L., and Craik, D. J. (2008) Alanine scanning mutagenesis of the prototypic cyclotide reveals a cluster of residues essential for bioactivity. J. Biol. Chem. 283, 9805-9813
30. Caprioli, R. M., Farmer, T. B., and Gile, J. (1997) Molecular imaging of biological samples. Localization of peptides and proteins using MALDITOF MS. Anal. Chem. 69, 4751-4760
31. Chughtai, K., and Heeren, R. M. (2010) Mass spectrometric imaging for biomedical tissue analysis. Chem. Rev. 110, 3237-3277
32. Menger, R. F., Stutts, W. L., Anbukumar, D. S., Bowden, J. A., Ford, D. A., and Yost, R. A. (2012) MALDI mass spectrometric imaging of cardiac tissue following myocardial infarction in a rat coronary artery ligation model. Anal. Chem. 84, 1117-1125
33. Ljungdahl, A., Hanrieder, J., Fälth, M., Bergquist, J., and Andersson, M. (2011) Imaging mass spectrometry reveals elevated nigral levels of dynorphin neuropeptides in L-DOPA-induced dyskinesia in rat model of Parkinson's disease. PLoS One 6, e25653
34. Gemoll, T., Roblick, U. J., and Habermann, J. K. (2011) MALDI mass spectrometry imaging in oncology. Mol. Med. Rep. 4, 1045-1051
35. Castellino, S., Groseclose, M. R., and Wagner, D. (2011) MALDI imaging mass spectrometry. Bridging biology and chemistry in drug development. Bioanalysis 3, 2427-2441
36. Greer, T., Sturm, R., and Li, L. (2011) Mass spectrometry imaging for drugs and metabolites. J. Proteomics 74, 2617-2631
37. Grassl, J., Taylor, N. L., and Millar, A. H. (2011) Matrix-assisted laser desorption/ionization mass spectrometry imaging and its development for plant protein imaging. Plant Methods 7, 21
38. Kondo, T., Sawa, S., Kinoshita, A., Mizuno, S., Kakimoto, T., Fukuda, H., and Sakagami, Y. (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313, 845-848 (Pubitemid 44223355)
39. Shroff, R., Vergara, F., Muck, A., Svatos, A., and Gershenzon, J. (2008) Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proc. Natl. Acad. Sci. U.S.A. 105, 6196-6201 (Pubitemid 351758422)
40. Becerra, J. X., and Venable, D. L. (1990) Rapid-terpene-bath and "squirt-gun"defense in Bursera schlechtendalii and the counterploy of Chrysomelid beetles. Biotropica 22, 320-323
41. Dannenhoffer, J. M., Suhr, R. C., and Thompson, G. A. (2001) Phloemspecific expression of the pumpkin fruit trypsin inhibitor. Planta 212, 155-162 (Pubitemid 32139871)
42. Lopez, L., Camas, A., Shivaji, R., Ankala, A., Williams, P., and Luthe, D. (2007) Mir1-CP, a novel defense cysteine protease accumulates in maize vascular tissues in response to herbivory. Planta 226, 517-527 (Pubitemid 46889528)
43. Do, H. M., Lee, S. C., Jung, H. W., Sohn, K. H., and Hwang, B. K. (2004) Differential expression and in situ localization of a pepper defensin (CADEF1) gene in response to pathogen infection, abiotic elicitors, and environmental stresses in Capsicum annuum. Plant Sci. 166, 1297-1305 (Pubitemid 38473392)
44. Thurnham, D. I. (1999) Functional foods. Cholesterol-lowering benefits of plant sterols. Br. J. Nutr. 82, 255-256
45. Ntanios, F. (2001) Plant sterol-ester-enriched spreads as an example of a new functional food. Eur. J. Lipid Sci. Technol. 103, 102-106
46. Ahmad, A., Anjum, F. M., Zahoor, T., Nawaz, H., and Dilshad, S. M. (2012) β-Glucan. A valuable functional ingredient in foods. Crit. Rev. Food Sci. Nutr. 52, 201-212
47. 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)
48. Saska, I., Colgrave, M. L., Jones, A., Anderson, M. A., and Craik, D. J. (2008) Quantitative analysis of backbone-cyclised peptides in plants. J. Chromatogr. B 872, 107-114
49. Box, M. S., Coustham, V., Dean, C., and Mylne, J. S. (2011) Protocol. A simple phenol-based method for 96-well extraction of high quality RNA from Arabidopsis. Plant Methods 7, 7
50. Broussalis, A. M., Göransson, U., Coussio, J. D., Ferraro, G., Martino, V., and Claeson, P. (2001) First cyclotide from Hybanthus (Violaceae). Phytochemistry 58, 47-51 (Pubitemid 32750848)
51. Gillon, A. D., Saska, I., Jennings, C. V., Guarino, R. F., Craik, D. J., and Anderson, M. A. (2008) Biosynthesis of circular proteins in plants. Plant J. 53, 505-515 (Pubitemid 351172020)
52. Ovesen, R. G., Göransson, U., Hansen, S. H., Nielsen, J., and Hansen, H. C. B. (2011) J. Chromatogr. 1218, 7964-7970
53. Gran, L. (1970) An oxytocic principle found in Oldenlandia affinis DC. Medd. Norsk Farm. Selskap 32, 173-180
54. Bokesch, H. R., Pannell, L. K., Cochran, P. K., Sowder, R. C., 2nd, McKee, T. C., and Boyd, M. R. (2001) A novel anti-HIV macrocyclic peptide from Palicourea condensata. J. Nat. Prod. 64, 249-250 (Pubitemid 32198360)
55. Nguyen, G. K., Lim, W. H., Nguyen, P. Q., and Tam, J. P. (2012) Novel cyclotides and uncyclotides with highly shortened precursors from Chassalia chartacea and effects of methionine oxidation on bioactivities. J. Biol. Chem. 287, 17598-17607
56. Ireland, D. C., Colgrave, M. L., Nguyencong, P., Daly, N. L., and Craik, D. J. (2006) Discovery and characterization of a linear cyclotide from Viola odorata. Implications for the processing of circular proteins. J. Mol. Biol. 357, 1522-1535
57. Nguyen, G. K., Zhang, S., Wang, W., Wong, C. T., Nguyen, N. T., and Tam, J. P. (2011) Discovery of a linear cyclotide from the bracelet subfamily and its disulfide mapping by top-down mass spectrometry. J. Biol. Chem. 286, 44833-44844
58. IUPAC (1979) Nomenclature of Organic Chemistry, Sections A, B, C, D, E, F, and H, Pergamon Press, Oxford
59. Barry, D. G., Daly, N. L., Clark, R. J., Sando, L., and Craik, D. J. (2003) Linearization of a naturally occurring circular protein maintains structure but eliminates hemolytic activity. Biochemistry 42, 6688-6695 (Pubitemid 36666109)
60. Daly, N. L., Gustafson, K. R., and Craik, D. J. (2004) The role of the cyclic peptide backbone in the anti-HIV activity of the cyclotide kalata B1. FEBS Lett. 574, 69-72 (Pubitemid 39200896)
61. Min, W., and Jones, D. H. (1994) In vitro splicing of concanavalin A is catalyzed by asparaginyl endopeptidase. Nat. Struct. Biol. 1, 502-504
62. Abe, Y., Shirane, K., Yokosawa, H., Matsushita, H., Mitta, M., Kato, I., and Ishii, S. (1993) Asparaginyl endopeptidase of jack bean seeds. Purification, characterization, and high utility in protein sequence analysis. J. Biol. Chem. 268, 3525-3529 (Pubitemid 23070993)
63. Otegui, M. S., Herder, R., Schulze, J., Jung, R., and Staehelin, L. A. (2006) The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies. Plant Cell 18, 2567-2581 (Pubitemid 44749890)
64. Hiraiwa, N., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (1997) An aspartic endopeptidase is involved in the breakdown of propeptides of storage proteins in protein-storage vacuoles of plants. Eur. J. Biochem. 246, 133-141 (Pubitemid 27229679)
65. D'Hondt, K., Bosch, D., Van Damme, J., Goethals, M., Vandekerckhove, J., and Krebbers, E. (1993) An aspartic proteinase present in seeds cleaves Arabidopsis 2 S albumin precursors in vitro. J. Biol. Chem. 268, 20884-20891 (Pubitemid 23292266)
66. Shimada, T., Yamada, K., Kataoka, M., Nakaune, S., Koumoto, Y., Kuroyanagi, M., Tabata, S., Kato, T., Shinozaki, K., Seki, M., Kobayashi, M., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2003) Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J. Biol. Chem. 278, 32292-32299 (Pubitemid 37048423)
67. Gruis, D., Schulze, J., and Jung, R. (2004) Storage protein accumulation in the absence of the vacuolar processing enzyme family of cysteine proteases. Plant Cell 16, 270-290 (Pubitemid 38162368)
68. Hara-Hishimura, I., Takeuchi, Y., Inoue, K., and Nishimura, M. (1993) Vesicle transport and processing of the precursor to 2S albumin in pumpkin. Plant J. 4, 793-800 (Pubitemid 2017537)
69. 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
70. Beck, A., Bussat, M. C., Klinguer-Hamour, C., Goetsch, L., Aubry, J. P., Champion, T., Julien, E., Haeuw, J. F., Bonnefoy, J. Y., and Corvaia, N. (2001) Stability and CTL activity of N-terminal glutamic acid-containing peptides. J. Pept. Res. 57, 528-538 (Pubitemid 32552194)
71. Nilsson, A., Fehniger, T. E., Gustavsson, L., Andersson, M., Kenne, K., Marko-Varga, G., and Andrén, P. E. (2010) Fine mapping the spatial distribution and concentration of unlabeled drugs within tissue micro-compartments using imaging mass spectrometry. PLoS One 5, e11411
72. Murata, N., Kajiura, H., Fujimura, Y., Miyao, M., Murata, T., Watanabe, A., and Shinozaki, K. (1987) Progress in Photosynthesis Research, Martinus Nijhoff, Dordrecht, The Netherlands
73. Pinto, M. F. S., Almeida, R. G., Porto, W. F., Fensterseifer, I. C. M., Lima, L. A., Dias, S. C., and Franco, O. L. (2012) Cyclotides: From gene structure to promiscuous multifunctionality. J. Evid. Based Comp. Alt. Med. 17, 40-53