Eliminating anti-nutritional plant food proteins: The case of seed protease inhibitors in pea

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Clemente, Alfonso ^a   Arques, Maria C ^a   Dalmais, Marion ^b   Le Signor, Christine ^c   Chinoy, Catherine ^d   Olias, Raquel ^a   Rayner, Tracey ^d   Isaac, Peter G ^e   Lawson, David M ^d   Bendahmane, Abdelhafid ^b   Domoney, Claire ^d  

^a CSIC   (Spain)

^b INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^c UNIV BOURGOGNE FRANCHE COMTÉ   (France)

^d JOHN INNES CENTRE   (United Kingdom)

^e iDNA Genetics Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BOWMAN BIRK INHIBITOR; TI1 PROTEIN; TI2 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; CHYMOTRYPSIN; PLANT PROTEIN; PROTEINASE INHIBITOR; TRYPSIN; TRYPSIN INHIBITOR;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; GERMPLASM; INTROGRESSION; MISSENSE MUTATION; MUTANT; NONHUMAN; NUTRIENT; PEA; PISUM; PISUM ELATIUS; PLANT SEED; SEED QUALITY; STRUCTURE ACTIVITY RELATION; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DIET; GENETICS; HUMAN; METABOLISM; MUTATION;

AMINO ACID SEQUENCE; ANIMALS; CHYMOTRYPSIN; DIET; HUMANS; MUTATION; PEAS; PLANT PROTEINS; PROTEASE INHIBITORS; SEEDS; TRYPSIN; TRYPSIN INHIBITORS;

EID: 84943165688     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0134634     Document Type: Article

References (51)

1. Crévieu I, Carré B, Chagneau AM, Quillien L, Guéguen J, Berot S (1997) Identification of resistant pea (Pisum sativum L.) proteins in the digestive tract of chickens. J Agric Food Chem 45: 1295-1300. doi: 10.1021/jf960806b
2. Salgado P, Freire JPB, Ferreira RB, Teixeira A, Bento O, Abreu MC, et al. (2003) Immunodetection of legume proteins resistant to small intestinal digestion in weaned piglets. J Sci Food Agric 15: 1571-1580. doi: 10.1002/jsfa.1581
3. Rubio LA, Pedrosa MM, Cuadrado C, Gelencser E, Clemente A, Burbano C, et al. (2006) Recovery at the terminal ileum of some legume non-nutritional factors in cannulated pigs. J Sci Food Agric 86: 979-987. doi: 10.1002/jsfa.2446
4. Le Gall M, Quillien L, Sève B, Guéquen J, Lallés JP (2007) Weaned piglets display low gastrointestinal digestion of pea (Pisum sativum L.) lectin and albumin pea albumin 2. J Anim Sci 85: 2972-2981. doi: 10.2527/jas.2006-795 PMID: 17565068
5. Carbonaro M Maselli P, Nucara A (2014) Structural aspects of legume proteins and nutraceutical properties. Food Res Int (in press). doi: 10.1016/j.foodres.2014.11.007
6. Vaz Patto MC, Amarowicz R, Aryee AN, Boye JI, Chung HJ, Martín-Cabrejas MA, et al. (2015) Achievements and challenges in improving the nutritional quality of food legumes. Crit Rev Plant Sci 34: 105-143. doi: 10.1080/07352689.2014.897907
7. Bode W, Huber R (1992) Natural protein proteinase inhibitors and their interaction with proteinases. Eur J Biochem 204: 433-451. doi: 10.1111/j.1432-1033.1992.tb16654.x PMID: 1541261
8. Perona JJ, Craik CS (1995) Structural basis of substrate-specificity in the serine proteases. Protein Sci 4: 337-360. PMID: 7795518
9. Wiseman J, Al-Mazooqi W, Welham T, Domoney C (2003) The apparent ileal digestibility, determined with young broilers, of amino acids in near-isogenic lines of peas (Pisum sativum L.) differing in trypsin inhibitor activity. J Sci Food Agric 83: 644-651. doi: 10.1002/jsfa.1340
10. Domoney C, Welham T (1992) Trypsin inhibitors in Pisum: variation in amount and pattern of accumulation in developing seed. Seed Sci Res 2: 147-154. doi: 10.1017/S0960258500001276
11. Domoney C. Inhibitors of legume seeds. In: Shewry PR, Casey R, editors. Kluwer Academic Publishers. Seed Proteins; 1999. pp. 635-655. doi: 10.1007/978-94-011-4431-5-27
12. Domoney C, Welham T, Ellis N, Mozzanega P, Turner L (2002) Three classes of proteinase inhibitor gene have distinct but overlapping patterns of expression in Pisum sativum plants. Plant Mol Biol 48: 319-329. doi: 10.1023/A:1013379430582 PMID: 11855733
13. Clemente A, Domoney C (2006) Biological significance of polymorphism in legume protease inhibitors from the Bowman-Birk family. Curr Prot Pept Sci 7: 201-216. doi: 10.2174/138920306777452349 PMID: 16787260.
14. Ramasarma PR, Rao AG, Rao DR (1995) Role of disulfide linkages in structure and activity of proteinase inhibitor from horsegram (Dolichos biflorus). Biochim Biophys Acta 1248: 35-42. doi: 10.1016/0167-4838(95)00004-E PMID: 7711055
15. Kumar V, Gowda LR (2013). The contribution of two disulphide bonds in the trypsin binding domain of horsegram (Dolichos biflorus) Bowman-Birk inhibitor to thermal stability and functionality. Arch Biochem Biophys 537: 49-61. doi: 10.1016/j.abb.2013.06.002 PMID: 23791628
16. Jofuku KD, Schipper RD, Goldberg RB (1989) A frameshift mutation prevents Kunitz trypsin-inhibitor messanger-RNA accumulation in soybean embryos. Plant Cell 1: 427-435. doi: 10.1105/tpc.1.4.427 PMID: 2562563
17. Kim DS, Lee KJ, Kim JB, Kim SH, Song JY, Seo YW, et al. (2010) Identification of Kunitz trypsin inhibitor mutations using SNAP markers in soybean mutant lines. Theor Appl Genet 4: 751-760. doi: 10.1007/s00122-010-1346-1 PMID: 20445958
18. Ha BK, Lee KJ, Velusamy V, Kim JB, Kim SH, Ahn JW, et al. (2014) Improvement of soybean through radiation-induced mutation breeding techniques in Korea. Plant Genet Resourc 12: S54-S57. doi: 10.1017/S1479262114000264
19. Wang KJ, Li XH, Takahata Y, Yamashita T (2010) Allelic diversity and geographical pattern at soybean Kunitz trypsin inhibitor single locus in Chinese wild soja (Glycine soja Sieb. & Zucc.). Plant Breeding 129: 264-270. doi: 10.1111/j.1439-0523.2009.01734.x
20. Livingstone D, Beilinson V, Kalyaeva M, Schmidt MA, Herman EM, Nielsen NC (2007) Reduction of protease inhibitor activity by expression of a mutant Bowman-Birk gene in soybean seed. Plant Mol Biol 64: 397-408. doi: 10.1007/s11103-007-9163-x PMID: 17429741
21. Schillinger JA (2012) US patent application US2012/0317675. Ultra-low tripsin inhibitor soybean.
22. Wu K, Horejsi T, Byrum JR, Bringe N, Yang J, Pei D, et al. (2014) US patent application US2014/0259196. Agronomically elite soybeans with beta-conglycinin content.
23. Jing RC, Vershinin A, Grzebyta J, Shaw P, Smykal P, Marshall D, et al. (2010) The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis. BMC Evol Biol 10: 44. doi: 10.1186/1471-2148-10-44 PMID: 20156342
24. Dalmais M, Schmidt J, Le Signor C, Moussy F, Burstin J, Savois V, et al. (2008) UTILLdb, a Pisum sativum in silico forward and reverse genetics tool. Genome Biol 9: R43. doi: 10.1186/gb-2008-9-2-r43 PMID: 18302733
25. Hofer J, Turner L, Moreau C, Ambrose M, Isaac P, Butcher S, et al. (2009) Tendril-less regulates tendril formation in pea leaves. Plant Cell 21: 420-428. doi: 10.1105/tpc.108.064071 PMID: 19208900
26. D'Erfurth I, Le Signor C, Aubert G, Sanchez M, Vernoud V, Darchy B, et al. (2012) A role for an endosperm-localized subtilase in the control of seed size in legumes. New Phytol 196: 738-751. doi: 10.1111/j.1469-8137.2012.04296.x PMID: 22985172
27. Domoney C, Welham T, Sidebottom C, Firmin JL (1995) Multiple isoforms of Pisum trypsin inhibitors result from modification of two primary gene products. FEBS Lett 360: 15-20. doi: 10.1016/0014-5793(95)00070-P PMID: 7875292
28. de la Sierra IL, Quillien L, Flecker P, Gueguen J, Brunie S (1999) Dimeric crystal structure of a Bowman-Birk protease inhibitor from pea seeds. J Mol Biol 285: 1195-1207. doi: 10.1006/jmbi.1998.2351 PMID: 9887273
29. Clemente A, MacKenzie DA, Jeenes DJ, Domoney C (2004) The effect of variation within inhibitory domains on the activity of pea protease inhibitors from the Bowman-Birk class. Prot Express Purific 36: 106-114. doi: 10.1016/j.pep.2004.03.015 PMID: 15177291
30. Rao KN, Suresh CG (2007) Bowman-Birk protease inhibitor from the seeds of Vigna unguiculata forms a highly stable dimeric structure. Biochim Biophys Acta 1774: 1264-1273. doi: 10.1016/j.bbapap.2007.07.009 PMID: 17869196
31. Page D, Aubert G, Duc G, Welham T, Domoney C (2002) Combinatorial variation in coding and promoter sequences of genes at the Tri locus in Pisum sativum accounts for variation in trypsin inhibitor activity in seeds. Mol Gen Genomics 267: 359-369. PMID: 12073038
32. Lu W, Apostol I, Qasim MA, Warne N, Wynn R, Zhang WL, et al. (1997) Binding of amino acid sidechains to S1 cavities of serine proteinases. J Mol Biol 266: 441-461. doi: 10.1006/jmbi.1996.0781 PMID: 9047374
33. Gariani T, McBride JD, Leatherbarrow RJ (1999) The role of the P2′ position of Bowman-Birk proteinase inhibitor in the inhibition of trypsin. Studies on P2′ variation in cyclic peptides encompassing the reactive site loop. Biochim Biophys Acta 1431: 232-237. doi: 10.1016/S0167-4838(99)00035-7 PMID: 10209295
34. Galasso I, Piergiovanni AR, Lioi L, Campion B, Bollini R, Spavoli F (2009) Genomic organization of Bowman-Birk inhibitor in common bean (Phaseolus vulgaris L.). Mol Breeding 23: 617-624.
35. Kumar P, Rao AG, Hariharaputran S, Chandra N, Gowda L (2004) Molecular mechanism of dimerization of Bowman-Birk inhibitors. J Biol Chem 29: 30425-30432. doi: 10.1074/jbc.M402972200 PMID: 15123729
36. Muricken DG, Gowda LR (2010) Functional expression of horsegram (Dolichos biflorus) Bowman-Birk inhibitor and its self-association. Biochim Biophys Acta 1804: 1413-1423. doi: 10.1016/j.bbapap.2010.02.012 PMID: 20227530
37. Li P, Jiang S, Lee SL, Lin CY, Johnson MD, Dickson RB, et al. (2007) Design and synthesis of novel and potent inhibitors of the type II transmembrane serine protease, matriptase, based upon the sunflower trypsin inhibitor-1. J Med Chem 50: 5976-5983. doi: 10.1021/jm0704898 PMID: 17985858
38. Chen YW, Huang SC, Lin-Shiau SY, Lin JK (2005) Bowman-Birk inhibitor abates proteasome function and suppresses the proliferation of MCF7 breast cancer cells through accumulation of MAP kinasephosphatase-1. Carcinogenesis 26: 1296-1305. doi: 10.1093/carcin/bgi062 PMID: 15746161
39. Clemente A, Moreno FJ, Marín-Manzano MC, Jiménez E, Domoney C (2010) The cytotoxic effect of Bowman-Birk isoinhibitors, IBB1 and IBBD2, from soybean on HT29 human colorectal cancer cells is related to their intrinsic ability to inhibit serine proteases. Mol Nutr Food Res 54: 396-405. doi: 10.1002/mnfr.200900122 PMID: 19885848
40. da Costa Souza L, Camargo R, Demasi M, Santana JM, de Sá CM, de Freitas SM (2014). Effects of an anticarcinogenic Bowman-Birk protease inhibitor on purified 20S proteasome and MCF-7 breast cancer cells. PLOS ONE 9, e86600. doi: 10.1371/journal.pone.0086600 PMID: 24475156
41. Vigeolas H, Chinoy C, Zuther E, Blessington B, Geigenberger P, Domoney C (2008) Combined metabolomics and genetic approaches reveal a link between the polyamine pathway and albumin 2 in developing pea seeds. Plant Physiol 146: 74-82. doi: 10.1104/pp.107.111369 PMID: 18024559
42. Forster C, North H, Afzal N, Domoney C, Hornostaj A, Robinson DS, et al. (1999) Molecular analysis of a null mutant for pea (Pisum sativum L.) seed lipoxygenase-2. Plant Mol Biol 39: 1209-1220. doi: 10.1023/A:1006173313548 PMID: 10380807
43. Domoney C, Knox M, Moreau C, Ambrose M, Palmer S, Smith P, et al. (2013) Exploiting a fast neutron mutant genetic resource in Pisum sativum (pea) for functional genomics. Funct Plant Biol 40: 1261-1270. doi: 10.1071/FP13147
44. Hellens RP, Moreau C, Lin-Wang K, Schwinn KE, Thomson SJ, Fiers MW, et al. (2010) Identification of Mendel's white flower character. PLoS ONE 5: e13230. doi: 10.1371/journal.pone.0013230 PMID: 20949001
45. Chinoy C, Welham T, Turner L, Moreau C, Domoney C (2011). The genetic control of seed quality traits: effects of allelic variation at the Tri and Vc-2 genetic loci in Pisum sativum L. Euphytica 180: 107-122. doi: 10.1007/s10681-011-0363-8
46. Arques MC, Marín-Manzano MC, Clarissa-Brito L, Hernandez-Ledesma B, Recio I, Clemente A (2014) Quantitative determination of active Bowman-Birk isoinhibitors, IBB1 and IBBD2, in commercial soymilks. Food Chem 155: 24-30. doi: 10.1016/j.foodchem.2014.01.024 PMID: 24594149
47. Clemente A, Marín-Manzano MC, Jiménez E, Arques MC, Domoney C (2012) The anti-proliferative effect of TI1B, a major Bowman-Birk isoinhibitor from pea (Pisum sativum L.) on HT29 colon cancer cells is mediated through protease inhibition. Br J Nutr 108: 135-144. doi: 10.1017/S000711451200075X PMID: 22916809
48. Clemente A, Gee JM, Johnson IT, Mackenzie DA, Domoney C (2005) Pea (Pisum sativum L.) protease inhibitors from the Bowman-Birk class influence the growth of human colorectal adenocarcinoma HT29 cells in vitro. J Agric Food Chem 53: 8979-8986. doi: 10.1021/jf051528w PMID: 16277391
49. Erlanger BF, Edel F, Cooper AG (1966) The action of chymotrypsin on two new chromogenic substrates. Arch Biochem Biophys 115: 206-210. PMID: 5966518
50. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10: 845-858. doi: 10.1038/nprot.2015.053 PMID: 25950237
51. Capaldi S, Perduca M, Faggion B, Carrizo ME, Tava A, Ragona L, Monaco HL (2007) Crystal structure of the anticarcinogenic Bowman-Birk inhibitor from snail medic (Medicago scutellata) seeds complexed with bovine trypsin. J Struct Biol 158: 71-79. doi: 10.1016/j.jsb.2006.10.017 PMID: 17142058.