Proteomics for exploiting diversity of lupin seed storage proteins and their use as nutraceuticals for health and welfare

Journal of Proteomics

Volumn 143, Issue , 2016, Pages 57-68

  Cabello Hurtado, Francisco ^a   Keller, Jean ^a   Ley, José ^a   Sanchez Lucas, Rosa ^b   Jorrín Novo, Jesús V ^b   Aïnouche, Abdelkader ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

Conglutins; Lupin proteome; Lupinus germplasm; Nutraceuticals; Seed proteome

Indexed keywords

NUTRACEUTICAL; SEED STORAGE PROTEIN;

ANTIDIABETIC ACTIVITY; ARTICLE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CONTROLLED CLINICAL TRIAL (TOPIC); DIABETES MELLITUS; DOMESTICATED PLANT; GENETIC VARIABILITY; HUMAN; HYPERGLYCEMIA; LUPIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; RANDOMIZED CONTROLLED TRIAL (TOPIC); SPECIES DIVERSITY; CHEMISTRY; DIETARY SUPPLEMENT; GENETIC VARIATION; PROCEDURES;

DIETARY SUPPLEMENTS; GENETIC VARIATION; HUMANS; LUPINUS; PROTEOMICS; SEED STORAGE PROTEINS;

EID: 84961878113     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2016.03.026     Document Type: Article

References (125)

1. [1] Cronk, Q., Ojeda, I., Pennington, R.T., Legume comparative genomics: progress in phylogenetics and phylogenomics. Curr. Opin. Plant Biol. 9 (2006), 99–103.
2. [2] Erbas, M., Certel, M., Uslu, M.K., Some chemical properties of white lupin seeds (Lupinus albus L.). Food Chem. 89 (2005), 341–345.
3. [3] Mikić, A., Ćupina, B., Mihailović, V., Krstić, D., Antanasović, S., Zorić, L., Srebrić, M., Intercropping white (Lupinus albus) and Andean (Lupinus mutabilis) lupins with other annual cool season legumes for forage production. S. Afr. J. Bot. 89 (2013), 296–300.
4. [4] Pastor-Cavada, E., Juan, R., Pastor, J.E., Alaiz, M., Vioque, J., Analytical nutritional characteristics of seed proteins in six wild lupinus species from Southern Spain. Food Chem. 117 (2009), 466–469.
5. [5] Linnemann, A.R., Dijkstra, D.S., Toward sustainable production of protein-rich foods: appraisal of eight crops for Western Europe. part I. analysis of the primary links of the production chain. crit. rev. Food Sci. 42 (2002), 377–401.
6. [6] Cowling, W.A., Bevan, J.B., Tapia, M.E., Lupin: Lupinus L., Promoting the Conservation and Use of Underutilized and Neglected Crops. 1998, International Plant Genetic Resources Institute, Rome, Italy.
7. [7] Dunn, D.B., Cytotaxonomy and distribution of the New World lupin species. Proceedings of the Third International Lupin Conference, La Rochelle, France, 1984, 67–85.
8. [8] Gladstones, J.S., Lupins of the Mediterranean region and Africa. West. Aust. Dep. Agric. Tech. Bull. 26 (1974), 1–48.
9. [9] FAOSTAT (Food and Agriculture Organization of the United Nations, Statistics Division) Database, http://faostat3.fao.org/.
10. [10] Sujak, A., Kotlarz, A., Strobel, W., Compositional and nutritional evaluation of several lupin seeds. Food Chem. 98 (2006), 711–719.
11. [11] Duranti, M., Consonni, A., Magni, C., Sessa, F., Scarafoni, A., The major proteins of lupin seed: characterisation and molecular properties for use as functional and nutraceutical ingredients. Trends Food Sci. Technol. 19 (2008), 624–633.
12. [12] Khan, M.K., Karnpanit, W., Nasar-Abbas, S.M., Huma, Z., Jayasena, V., Phytochemical composition and bioactivities of lupin: a review. Int. J. Food Sci. Technol. 50 (2015), 2004–2012.
13. [13] Danse, B., Roberfroid, M., Breslin, L., Contor, L., Scientific concepts of functional foods in Europe: consensus document. Br. J. Nutr. 81 (1999), S1–S27.
14. [14] Duranti M, Morazzoni P. Nutraceutical properties of lupin seed proteins: a great potential still waiting for full exploitation. Agro Food Ind. Hi Tech. 2011; 22: 20–23.
15. [15] Wang, W., Mejia, D., Gonzalez, E., A new frontier in soy bioactive peptides that may prevent age-related chronic diseases. Compr. Rev. Food Sci. Food 4 (2005), 63–78.
16. [16] Carbonaro, M., Maselli, P., Nucara, A., Structural aspects of legume proteins and nutraceutical properties. Food Res. Int. 76 (2015), 19–30.
17. [17] Dijkstra, D.S., Linnemann, A.R., van Boekel, T.A., Towards sustainable production of protein-rich foods: appraisal of eight crops for Western Europe. PART II: analysis of the technological aspects of the production chain. Crit. Rev. Food 43 (2003), 481–506.
18. [18] Osborne, T.B., The Vegetable Proteins. 1924, Longmans, Green and Co., London, UK.
19. [19] Esnault, M.A., Pichereau, V., Klingler, J., Variability of the low molecular weight globulin, conglutin δ, within lupin species. Bot. Acta 110 (1997), 164–171.
20. [20] Salmanowicz, B.P., Przybylska, J., Electrophoretic patterns of seed albumins in the old-world Lupinus species (Fabaceae): variation in the 2S albumin class. Plant Syst. Evol. 192 (1994), 67–78.
21. [21] Duranti, M., Restani, P., Poniatowska, M., Cerletti, P., The seed globulins of Lupinus albus. Phytochemistry 20 (1981), 2071–2075.
22. [22] Lilley, G.G., Inglis, A.S., Amino acid sequence of conglutin delta, a sulfur-rich seed protein of Lupinus angustifolius l. sequence homology with the C-III alpha-amylase inhibitor from wheat. FEBS Lett. 195 (1986), 235–241.
23. [23] Salmanowich, B.P., Weder, J.K.P., Primary structure of 2S albumin from seeds of Lupinus albus. Z. Lebensm. Unters. Forsch. 204 (1997), 129–135.
24. [24] Gayler, K.R., Kolivas, S., Macfarlane, A.J., Lilley, G.G., Baldi, M., Blagrove, R.J., Johnson, E.D., Biosynthesis, cDNA and amino acid sequences of a precursor of conglutin delta, a sulphur-rich protein from Lupinus angustifolius. Plant Mol. Biol. 15 (1990), 879–893.
25. [25] Blagrove, R.J., Gillespie, J.M., Isolation, purification and characterization of the seed globulins of Lupinus albus. Aust. J. Plant Physiol. 2 (1975), 13–27.
26. [26] Cerletti, P., Fumagalli, A., Venturin, D., Protein composition of seeds of Lupinus albus. J. Food Sci. 43 (1978), 1409–1414.
27. [27] Restani, P., Duranti, M., Cerletti, P., Simonetti, P., Subunit composition of the seed globulins of Lupinus albus. Phytochemistry 20 (1981), 2077–2083.
28. [28] Casero, M., Duranti, M., Cerletti, P., Heterogeneity of subunit composition in lupin globulins. J. Sci. Food Agric. 34 (1983), 1113–1116.
29. [29] Duranti, M., Cerletti, P., Subunit composition of proteins from seeds of Lupinus albus. Plant Foods Hum. Nutr. 33 (1983), 135–138.
30. [30] Melo, T.S., Ferreira, R.M., Teixeira, A.R.N., The seed storage proteins from Lupinus albus seeds. Phytochemistry 37 (1994), 641–648.
31. [31] Gayler, K.R., Wachsmann, F., Kolivas, S., Johnson, E.D., Isolation and characterization of protein bodies in Lupinus angustifolius. Plant Physiol. 91 (1989), 1425–1431.
32. [32] Esnault, M.A., Merceur, A., Citharel, J., Biosynthèse des protéines de réserve et formation Des Corps protéiques dans la graine de lupin jaune (Lupinus luteus l., Légumineuses). Agronomie 13 (1993), 307–316.
33. [33] Duranti, M., Guerrieri, N., Cerletti, P., Vecchio, G., The legumin precursor from white lupin seed. Eur. J. Biochem. 206 (1992), 941–947.
34. [34] Duranti, M., Horstmann, C., Gilroy, J., Croy, R.R.D., The molecular basis for N-glycosylation in the 11S globulin (legumin) of lupin see. J. Protein Chem. 14 (1995), 107–110.
35. [35] Duranti, M., Lovati, M.R., Dani, V., Barbiroli, A., Scarafoni, A., Castiglioni, S., Ponzone, C., Morazzoni, P., The α'subunit from soybean 7S globulin lowers plasma lipids and upregulates liver β-VLDL receptors in rats fed a hypercholesterolemic diet. J. Nutr. 134 (2004), 1334–1339.
36. [36] Duranti, M., Sessa, F., Carpen, A., Identification, purification and properties of the precursor of conglutin β, the 7S storage globulin of Lupinus albus l. seeds. J. Exp. Bot. 43 (1992), 1373–1378.
37. [37] Duranti, M., Gorinstein, S., Cerletti, P., Rapid separation and detection of concanavalin a reacting glycoproteins: application to storage proteins of a legume seed. J. Food Biochem. 14 (1990), 327–330.
38. [38] Duranti, M., Sessa, F., Scarafoni, A., Bellini, T., Dallocchio, F., Thermal stabilities of lupin seed conglutin γ protomers and tetramers. J. Agric. Food Chem. 48 (2000), 1118–1123.
39. [39] Ilgoutz, S.C., Knittel, N., Lin, J.M., Sterle, S., Gayler, K.R., Transcription of genes for conglutin gamma and a leginsulin-like protein in narrow-leafed lupin. Plant Mol. Biol. 34 (1997), 613–627.
40. [40] Eaton-Mordas, C.A., Moore, K.A., Seed glycoproteins of Lupinus angustifolius. Phytochemistry 17 (1978), 619–621.
41. [41] Scarafoni, A., Magni, C., Duranti, M., Molecular nutraceutics as a mean to investigate the positive effects of legume seed proteins on human health. Trends Food Sci. Technol. 18 (2007), 454–463.
42. [42] Komatsu, S., Hirano, H., Plant basic 7 S globulin-like proteins have insulin and insulin-like growth factor binding activity. FEBS Lett. 294 (1991), 210–212.
43. [43] Magni, C., Sessa, F., Accardo, E., Vanoni, M., Morazzoni, P., Scarafoni, A., Duranti, M., Conglutin γ, a lupin seed protein, binds insulin in vitro and reduces plasma glucose levels of hyperglycemic rats. J. Nutr. Biochem. 15 (2004), 646–650.
44. [44] Czubinski, J., Barciszewski, J., Gilski, M., Szpotkowski, K., Debski, J., Lampart-Szczapa, E., Jaskolski, M., Structure of gamma-conglutin: insight into the quaternary structure of 7S basic globulins from legumes. Acta Crystallogr. D Biol. Crystallogr. 71 (2015), 224–238.
45. [45] Sironi, E., Sessa, F., Duranti, M., A simple procedure of lupin seed protein fractionation for selective food applications. Eur. Food Res. Technol. 221 (2005), 145–150.
46. [46] Duranti, M., Scarafoni, A., Di Cataldo, A., Sessa, F., Interaction of metal ions with lupin seed conglutin γ. Phytochemistry 56 (2001), 529–533.
47. [47] Wäsche, A., Müller, K., Knauf, U., New processing of lupin protein isolates and functional properties. Nahrung 45 (2001), 393–395.
48. [48] Heron, M.P., Hoyert, D.L., Murphy, S.L., Xu, J.Q., Kochanek, K.D., Tejada-Vera, B., Deaths: final data for 2006. Natl. Vital Stat. Rep. 57 (2009), 1–134.
49. [49] Lopez, A.D., Mathers, C.D., Ezzati, M., Jamison, D.T., Murray, C.J., Global and regional burden of disease and risk factors 2001: systematic analysis of population health data. Lancet 367 (2006), 1747–1757.
50. [50] Cam, A., González de Mejía E. role of dietary proteins and peptides in cardiovascular disease. Mol. Nutr. Food Res. 56 (2012), 53–66.
51. [51] FDA, U.S.A., Food labeling, health claims, soy protein and coronary heart disease. Fed. Regist. 57 (1999), 699–733.
52. [52] Sirtori, C.R., Lovati, M.R., Manzoni, C., Castiglioni, S., Duranti, M., Magni, C., Morandi, S., D'Agostina, A., Arnoldi, A., Proteins of white lupin seed, a natural isoflavone-poor legume, reduce cholesterolemia in rats and increase LDL receptor activity in HepG2 cells. J. Nutr. 134 (2004), 18–23.
53. [53] Marchesi, M., Parolini, C., Diani, E., Rigamonti, E., Cornelli, L., Arnoldi, A., Sirtori, C.R., Chiesa, G., Hypolipidaemic and anti-atherosclerotic effects of lupin proteins in a rabbit model. Brit. J. Nut. 100 (2008), 707–710.
54. [54] Bettzieche, A., Brandsch, C., Schmidt, M., Weibe, K., Eder, K., Stangl, I.G., Differing effect of protein isolates from different cultivars of blue lupin on plasma lipoproteins of hypercholesterolemic rats. Biosci. Biotechnol. Biochem. 72 (2008), 3114–3121.
55. [55] Bettzieche, A., Brandsch, C., Eder, K., Stangl, G.I., Lupin protein acts hypocholesterolemic and increases milk fat content in lactating rats by influencing the expression of genes involved in cholesterol homeostasis and triglyceride synthesis. Mol. Nutr. Food Res. 53 (2009), 1134–1142.
56. [56] Parolini, C., Rigamonti, E., Marchesi, M., Busnelli, M., Cinquanta, P., Manzini, S., Chiesa, G., Cholesterol-lowering effect of dietary Lupinus angustifolius proteins in adult rats through regulation of genes involved in cholesterol homeostasis. Food Chem. 132 (2012), 1475–1479.
57. [57] Fontanari, G.G., Batistuti, J.P., Cruz, R.J.D., Saldiva, P.H.N., Arêas, J.A.G., Cholesterol-lowering effect of whole lupin (Lupinus albus) seed and its protein isolate. Food Chem. 132 (2012), 1521–1526.
58. [58] Kapravelou, G., Martínez, R., Andrade, A.M., Sánchez, C., Chaves, C.L., López-Jurado, M., Porres, J.M., Health promoting effects of lupin (Lupinus albus var. multolupa) protein hydrolyzate and insoluble fiber in a diet-induced animal experimental model of hypercholesterolemia. Food Res. Int. 54 (2013), 1471–1481.
59. [59] Radtke, J., Schutkowski, A., Brandsch, C., Hirche, F., Hasenkopf, K., Stangl, G.I., Isolated conglutin γ from lupin, but not phytate, lowers serum cholesterol without influencing vascular lesion development in the apoE-deficient mouse model. Plant Foods Hum. Nutr. 70 (2015), 113–118.
60. [60] Radtke, J., Geissler, S., Schutkowski, A., Brandsch, C., Kluge, H., Duranti, M.M., Stangl, G.I., Lupin protein isolate versus casein modifies cholesterol excretion and mRNA expression of intestinal sterol transporters in a pig model. Nutr. Metab., 11, 2014, 9.
61. [61] Weiße, K., Brandsch, C., Zernsdorf, B., Nembongwe, G.S.N., Hofmann, K., Eder, K., Stangl, G.I., Lupin protein compared to casein lowers the LDL cholesterol: HDL cholesterol-ratio of hypercholesterolemic adults. Eur. J. Nutr. 49 (2010), 65–71.
62. [62] Bähr, M., Fechner, A., Krämer, J., Kiehntopf, M., Jahreis, G., Lupin protein positively affects plasma LDL cholesterol and LDL: HDL cholesterol ratio in hypercholesterolemic adults after four weeks of supplementation: a randomized, controlled crossover study. Nutr. J., 12, 2013, 107.
63. [63] Lammi, C., Zanoni, C., Scigliuolo, G.M., D'Amato, A., Arnoldi, A., Lupin peptides lower low-density lipoprotein (LDL) cholesterol through an Up-regulation of the LDL Receptor/sterol regulatory element binding protein 2 (SREBP2) pathway at HepG2 cell line. J. Agric. Food Chem. 62 (2014), 7151–7159.
64. [64] Boschin, G., Scigliuolo, G.M., Resta, D., Arnoldi, A., ACE-inhibitory activity of enzymatic protein hydrolysates from lupin and other legumes. Food Chem. 145 (2014), 34–40.
65. [65] Boschin, G., Scigliuolo, G.M., Resta, D., Arnoldi, A., Optimization of the enzymatic hydrolysis of lupin (Lupinus) proteins for producing ACE-inhibitory peptides. J. Agric. Food Chem. 62 (2014), 1846–1851.
66. [66] Halban, P.A., Ferrannini, E., Nerup, J., Diabetes research investment in the European Union. Nat. Med. 12 (2006), 70–72.
67. [67] Guariguata, L., Tracking the global epidemic—new estimates from the IDF diabetes atlas update for 2012. Diabet. Voice 57 (2012), 12–15.
68. [68] Yach, D., Stuckler, D., Brownell, K.D., Epidemiologic and economic consequences of the global epidemics of obesity and diabetes. Nat. Med. 12 (2006), 62–66.
69. [69] Bi, Y., Wang, T., Xu, M., Advanced research on risk factors of type 2 diabetes. Diabetes Metab. Res. Rev. 28 (2012), 32–39.
70. [70] Gętek, M., Czech, N., Muc-Wierzgoń, M., Grochowska-Niedworok, E., Kokot, T., Nowakowska-Zajdel, E., The active role of Leguminous Plant components in type 2 diabetes. Evid. Based Complement. Alternat., 2014, 2014, 293961.
71. [71] Vargas-Guerrero, B., García-López, P.M., Martínez-Ayala, A.L., Domínguez-Rosales, J.A., Gurrola-Díaz, C.M., Administration of Lupinus albus gamma conglutin (Cγ) to n5 STZ rats augmented Ins-1 gene expression and pancreatic insulin content. Plant Food Hum. Nutr. 69 (2014), 241–247.
72. [72] Bertoglio, J.C., Calvo, M.A., Hancke, J.L., Burgos, R.A., Riva, A., Morazzoni, P., Duranti, M., Hypoglycemic effect of lupin seed γ-conglutin in experimental animals and healthy human subjects. Fitoterapia 82 (2011), 933–938.
73. [73] Terruzzi, I., Senesi, P., Magni, C., Montesano, A., Scarafoni, A., Luzi, L., Duranti, M., Insulin-mimetic action of conglutin-γ, a lupin seed protein, in mouse myoblasts. Nutr. Metab. Cardiovasc. Dis. 21 (2011), 197–205.
74. [74] Capraro, J., Clemente, A., Rubio, L.A., Magni, C., Scarafoni, A., Duranti, M., Assessment of the lupin seed glucose-lowering protein intestinal absorption by using in vitro and ex vivo models. Food Chem. 125 (2011), 1279–1283.
75. [75] Capraro, J., Magni, C., Faoro, F., Maffi, D., Scarafoni, A., Tedeschi, G., Duranti, M., Internalisation and multiple phosphorylation of γ-conglutin, the lupin seed glycaemia-lowering protein, in HepG2 cells. Biochem. Biophys. Res. Commun. 437 (2013), 648–652.
76. [76] Capraro, J., Magni, C., Scarafoni, A., Caramanico, R., Rossi, F., Morlacchini, M., Duranti, M., Pasta supplemented with isolated lupin protein fractions reduces body weight gain and food intake of rats and decreases plasma glucose concentration upon glucose overload trial. Food Funct. 5 (2014), 375–380.
77. [77] Clemente, A., Arques, M.C., Bowman–Birk inhibitors from legumes as colorectal chemopreventive agents. World J. Gastroenterol. 20 (2014), 10305–10315.
78. [78] Clemente, A., Arques, M.C., Dalmais, M., Le Signor, C., Chinoy, C., Olias, R., Rayner, T., Isaac, P.G., Lawson, D.M., Bendahmane, A., Domoney, C., Eliminating anti-nutritional plant food proteins: the case of seed protease inhibitors in pea. PLoS One, 10, 2015, e0134634.
79. [79] Guillamon, E., Rodriguez, J., Burbano, C., Muzquiz, M., Pedrosa, M.M., Cabanillas, B., Crespo, J.F., Sancho, A.I., Mills, E.N.C., Cuadrado, C., Characterization of lupin major allergens (Lupinus albus l.). mol. nutr. Food Res. 54 (2010), 1668–1676.
80. [80] Jappe, U., Vieths, S., Lupine, a source of new as well as hidden food allergens. Mol. Nutr. Food Res. 54 (2010), 113–126.
81. [81] EU (European Union), Commission directive 2007/68/EC, of 27 November 2007, amending annex IIIa to directive 2000/13/EC of the European Parliament and of the council as regards certain food ingredients. Off. J. Eur. Union 310 (2007), 11–14.
82. [82] FDA USA, Food and Drug Administration Consumer Health Information. Allergies to a Legume Called Lupin: What you Need to Know, 2014.
83. [83] Smith, W.B., Gillis, D., Kette, F.E., Lupin: a new hidden food allergen. Med. J. Aust. 181 (2004), 219–220.
84. [84] FSANZ (Food Standard Australian New Zealand). Lupin as an Allergen. Administrative Assessment Report 2013; Proposal P1026.
85. [85] Aïnouche, A., Bayer, R.J., Phylogenetic relationships in lupinus (fabaceae: papilionoideae) based on internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA. Am. J. Bot. 86 (1999), 590–607.
86. [86] Plitmann, U., Evolutionary history of the old world lupines. Taxon 30 (1981), 430–437.
87. [87] Drummond, C.S., Eastwood, R.J., Miotto, S.T.S., Hughes, C.E., Multiple continental radiations and correlates of diversification in Lupinus (leguminosae): testing for key innovation with incomplete taxon sampling. Syst. Biol. 61 (2012), 443–460.
88. [88] Mahé, F., Markova, D., Pasquet, R., Misset, M.T., Aïnouche, A., Isolation, phylogeny and evolution of the SymRK gene in the legume genus Lupinus l. Mol. Phylogenet. Evol. 60 (2011), 49–61.
89. [89] Kamphuis, L.G., Hane, J.K., Nelson, M.N., Gao, L., Atkins, C.A., Singh, K.B., Transcriptome sequencing of different narrow-leafed lupin tissue types provides a comprehensive uni-gene assembly and extensive gene-based molecular markers. Plant Biotechnol. J. 13 (2015), 14–25.
90. [90] Parra-González, L.B., Aravena-Abarzúa, G.A., Navarro-Navarro, C.S., Udall, J., Maughan, J., Peterson, L.M., Salvo-Garrido, H.E., Maureira-Butler, I.J., Yellow lupin (Lupinus luteus l.) transcriptome sequencing: molecular marker development and comparative studies. BMC Genomics, 13, 2012, 425.
91. [91] Yang, H., Tao, Y., Zheng, Z., Zhang, Q., Zhou, G., Sweetingham, M.W., Howieson, J.G., Li, C., Draft genome sequence, and a sequence-defined genetic linkage map of the legume crop species Lupinus angustifolius l. PLoS One, 8, 2013, e64799.
92. [92] Foley, R.C., Gao, L.L., Spriggs, A., Soo, L.Y., Goggin, D.E., Smith, P.M., Atkins, C.A., Singh, K.B., Identification and characterisation of seed storage protein transcripts from Lupinus angustifolius. BMC Plant Biol., 11, 2011, 59.
93. [93] Foley, R.C., Jimenez-Lopez, J.C., Kamphuis, L.G., Hane, J.K., Melser, S., Singh, K.B., Analysis of conglutin seed storage proteins across lupin species using transcriptomic, protein and comparative genomic approaches. BMC Plant Biol., 15, 2015, 106.
94. [94] Frazee, A.C., Sabunciyan, S., Hansen, K.D., Irizarry, R.A., Leek, J.T., Differential expression analysis of RNA-seq data at single-base resolution. Biostatistics 15 (2014), 413–426.
95. [95] Goggin, D.E., Mir, G., Smith, W.B., Stuckey, M., Smith, P.M.C., Proteomic analysis of lupin seed proteins to identify conglutin beta as an allergen, lup an 1. J. Agric. Food Chem. 56 (2008), 6370–6377.
96. [96] Wait, R., Gianazza, E., Brambilla, D., Eberini, I., Morandi, S., Arnoldi, A., Sirtori, C.R., Analysis of Lupinus albus storage proteins by two-dimensional electrophoresis and mass spectrometry. J. Agric. Food Chem. 53 (2005), 4599–4606.
97. [97] Miernyk, J.A., Seed Proteomics. Jorrin-Novo, J.V., Komatsu, S., Weckwerth, W., Wienkoop, S., (eds.) Methods in Molecular Biology Plant Proteomics: Methods and Protocols, vol. 1072, 2013, Springer, Alemania, 361–377.
98. [98] Champagne A, Boutry M. Proteomics of nonmodel plant species. Proteomics 201; 313: 663–673.
99. [99] Magni, C., Scarafoni, A., Herndl, A., Sessa, F., Prinsi, B., Espen, L., Duranti, M., Combined 2D electrophoretic approaches for the study of white lupin mature seed storage proteome. Phytochemistry 68 (2007), 997–1007.
100. [100] Lei, Z., Dai, X., Watson, B.S., Zhao, P.X., Sumner, L.W., A legume specific protein database (LegProt) improves the number of identified peptides, confidence scores and overall protein identification success rates for legume proteomics. Phytochemistry 72 (2011), 1020–1027.
101. [101] Schiarea, S., Arnoldi, L., Fanelli, R., De Combarieu, E., Chiabrando, C., In-depth glycoproteomic characterization of γ-conglutin by high-resolution accurate mass spectrometry. PLoS One, 8, 2013, e73906.
102. [102] Locati, D., Morandi, S., Zanotti, M., Arnoldi, A., Preliminary approaches for the development of a high performance liquid chromatography/electrospray ionization tandem mass spectrometry method for the detection and label/free semiquantitation of the main storage proteins of Lupinus albus in foods. Rapid Commun. Mass Spectrom. 20 (2006), 1305–1316.
103. [103] Brambilla, F., Resta, D., Isak, I., Zanotti, M., Arnoldi, A., A label-free internal standard method for the differential analysis of bioactive lupin proteins using nano HPLC-chip coupled with ion Trap mass spectrometry. Proteomics 9 (2009), 272–286.
104. [104] Sirtori, C.R., Resta, D., Brambilla, F., Zacherl, C., Arnoldi, A., The effects of various processing conditions on a protein isolate from Lupinus angustifolius. Food Chem. 120 (2010), 496–504.
105. [105] Ogura, T., Ogihara, J., Sunairi, M., Takeishi, H., Aizawa, T., Olivos-Trujillo, M.R., Maureira-Butler, I.J., Salvo-Garrido, H.E., Proteomic characterization of seeds from yellow lupin (Lupinus luteus l.). Proteomics 14 (2014), 1543–1546.
106. [106] Mitra, N., Sinha, S., Ramya, T.N., Surolia, A., N-linked oligosaccharides as outfitters for glycoprotein folding, form and function. Trends Biochem. Sci. 31 (2006), 156–163.
107. [107] Gomord, V., Fitchette, A.C., Menu-Bouaouiche, L., Saint-Jore-Dupas, C., Plasson, C., Michaud, D., Faye, L., Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol. J. 8 (2010), 564–587.
108. [108] Deléage, G., Combet, C., Blanchet, C., Geourjon, C., ANTHEPROT: an integrated protein sequence analysis software with client/server capabilities. Comput. Biol. Med. 31 (2001), 259–267.
109. [109] Altmann, F., The role of protein glycosylation in allergy. Int. Arch. Allergy Immunol. 142 (2007), 99–115.
110. [110] Scarafoni, A., Di Cataldo, A., Vassilevskaia, T.D., Bekman, E.P., Rodrigues-Pousada, C., Ceciliani, F., Duranti, M., Cloning, sequencing and expression in the seeds and radicles of two Lupinus albus conglutin γ genes. Biochim. Biophys. Acta 1519 (2001), 147–151.
111. [111] Duranti, M., Gius, C., Sessa, F., Vecchio, G., The saccharide chain of lupin seed conglutin gamma is not responsible for the protection of the native protein from degradation by trypsin, but facilitates the refolding of the acid-treated protein to the resistant conformation. Eur. J. Biochem. 230 (1995), 886–891.
112. [112] Islam, S., Ma, W., Ma, J., Buirchell, B.J., Appels, R., Yan, G., Diversity of seed protein among the Australian narrow-leafed lupin (Lupinus angustifolius l.) cultivars. Crop. Pasture. Sci. 62 (2011), 765–775.
113. [113] Islam, S., Yan, G., Appels, R., Ma, W., Comparative proteome analysis of seed storage and allergenic proteins among four narrow-leafed lupin cultivars. Food Chem. 135 (2012), 1230–1238.
114. [114] Islam, S., Ma, W., Ma, J., Buirchell, B.J., Appels, R., Yan, G., Genetic and environment interactions of seed storage proteins in narrow-leafed lupine (Lupinus angustifolius). Crop. Pasture. Sci. 63 (2012), 1066–1074.
115. [115] Salekdeh, G.H., Komatsu, S., Crop proteomics: aim at sustainable agriculture of tomorrow. Proteomics 7 (2007), 2976–2996.
116. [116] Eldakak, M., Milad, S.I.M., Nawar, A.I., Rohila, J.S., Proteomics: a biotechnology tool for crop improvement. Front. Plant Sci., 4, 2013, 35.
117. [117] Natarajan, S., Xu, C., Bae, H., Bailey, B.A., Proteomic and genomic characterization of kunitz trypsin inhibitors in wild and cultivated soybean genotypes. J. Plant Physiol. 164 (2007), 756–763.
118. [118] Natarajan, S., Xu, C., Bae, H., Bailey, B.A., Cregana, P., Capernad, T.J., Garrette, W.M., Luthriaf, D., Proteomic and genetic analysis of glycinin subunits of sixteen soybean genotypes. Plant Physiol. Biochem. 45 (2007), 436–444.
119. [119] Aïnouche, A., Guerrieri, N., Misset, M.T., Huon, A., Cerletti, P., Diversity of Seed Storage Proteins in Wild Lupin Populations from Algeria (North Africa). Proceedings of the International Conference on Plant Proteins from European Crops, INRA Editions, 1998, 45–49.
120. [120] Aïnouche, A., Diversité et évolution Du Genre Lupinus L. Fabaceae, 1998, Dissertation Université de Rennes1, France.
121. [121] Przybylska, J., Zimniak-Przybylska, Z., Electrophoretic patterns of seed globulins in the old-world Lupinus species. Genet. Resour. Crop. Evol. 42 (1995), 69–75.
122. [122] Zimniak-Przybylska, Z., Przybylska, J., Electrophoretic seed globulin patterns in some new world Lupinus species. Genet. Resour. Crop. Evol. 44 (1997), 57–62.
123. [123] Islam, S., Ma, W., Ma, J., Appels, R., Yan, G., Mass spectrometric fingerprints of seed protein for defining Lupinus spp. relationships. Genet. Resour. Crop. Evol. 60 (2013), 939–952.
124. [124] Boschin, G., Bermudez, T.K., Sirtori, E., Arnoldi, A., Wild Mexican lupins: proteomic analysis of the seeds of four species. Scarafoni, A., (eds.) Developing lupin crop into a major and sustainable food and feed source Proceeding of the 14th International Lupin Conference, 2015, DISTAM, Milan, 113 ISBN 8890598948, 9788890598944.
125. [125] Aiello, G., Boschin, G., Arnoldi, A., Extensive characterization of L. mutabilis using a combined approach based on 2D-electrophoresis and mass spectrometry. Scarafoni, A., (eds.) Developing lupin crop into a major and sustainable food and feed source Proceeding of the 14th International Lupin Conference, 2015, DISTAM, Milan, 116 ISBN 8890598948, 9788890598944.