Evaluation of the hypoglycemic potential of a black bean hydrolyzed protein isolate and its pure peptides using in silico, in vitro and in vivo approaches

Journal of Functional Foods

Volumn 31, Issue , 2017, Pages 274-286

  Mojica, Luis ^a,b   Gonzalez de Mejia, Elvira ^a   Granados Silvestre, María Ángeles ^c   Menjivar, Marta ^c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b CENTRO DE INVESTIGACIÓN Y ASISTENCIA EN TECNOLOGÍA Y DISEÑO DEL ESTADO DE JALISCO   (Mexico)

^c Universidad Nacional Autonoma de Mexico Facultad de Quimica   (Mexico)

Author keywords

Black bean; Diabetes; Glucose absorption; Glucose transporters; Hydrolyzed protein isolate; Hyperglycemic rats

Indexed keywords

EID: 85012098056     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2017.02.006     Document Type: Article

References (70)

1. Alzaid, F., Cheung, H.M., Preedy, V.R., Sharp, P.A., Regulation of glucose transporter expression in human intestinal Caco-2 cells following exposure to an anthocyanin-rich berry extract. Plos One 8 (2013), 1–6.
2. Babu, P.V.A., Liu, D., Gilbert, E.R., Recent advances in understanding the anti-diabetic actions of dietary flavonoids. Journal of Nutritional Biochemistry 24:11 (2013), 1777–1789.
3. Banerjee, S.K., Wang, D.W., Alzamora, R., Huang, X.N., Pastor-Soler, N.M., Hallows, K.R., Ahmad, F., SGLT1, a novel cardiac glucose transporter, mediates increased glucose uptake in PRKAG2 cardiomyopathy. Journal of Molecular and Cellular Cardiology 49 (2010), 683–692.
4. Bansal, P., Paul, P., Mudgal, J., Nayaka, P.G., Pannakal, S.T., Priyadarsini, K.I., Unnikrishnana, M.K., Antidiabetic, antihyperlipidemic and antioxidant effects of the flavonoid rich fraction of Pilea microphylla (L.) in high fat diet/streptozotocin-induced diabetes in mice. Experimental and Toxicologic Pathology 64 (2012), 651–658.
5. Bhatt, M.P., Lim, Y.C., Hwang, J.Y., Na, S., Kim, Y.M., Ha, K.S., C-peptide prevents hyperglycemia-induced endothelial apoptosis through inhibition of reactive oxygen species–mediated transglutaminase 2 activation. Diabetes 62 (2013), 243–253.
6. Bikadi, Z., Hazai, E., Application of the PM6 semi-empirical method to modeling proteins enhances docking accuracy of AutoDock. Journal of Cheminformatics 1 (2009), 1–15.
7. Cam, A., Sivaguru, M., de Mejia, E.G., Endocytic mechanism of internalization of dietary peptide lunasin into macrophages in inflammatory condition associated with cardiovascular disease. PLoS One, 8(9), 2013, e72115.
8. Chandramohan, R., Pari, L., Rathinam, A., Sheikh, B.A., Tyrosol, a phenolic compound, ameliorates hyperglycemia by regulating key enzymes of carbohydrate metabolism in streptozotocin induced diabetic rats. Chemico-Biological Interactions 229 (2015), 44–54.
9. Chen, J., Chen, Y., Xia, W., Xiong, Y.L., Ye, R., Wang, H., Grass carp peptides hydrolysed by the combination of Alcalase and Neutrase: Angiotensin-I converting enzyme (ACE) inhibitory activity, antioxidant activities and physicochemical profiles. International Journal of Food Science and Technology 51 (2016), 499–508.
10. Chen, L., Tuo, B., Dong, H., Regulation of intestinal glucose absorption by ion channels and transporters. Nutrients, 8, 2016, 43, 10.3390/nu8010043.
11. D'Cruz, S.C., Jubendradass, R., Jayakanthan, M., Rani, S.J.A., Mathur, P.P., Bisphenol A impairs insulin signaling and glucose homeostasis and decreases steroidogenesis in rat testis: An in vivo and in silico study. Food Chemestry and Toxicology 50 (2012), 1124–1133.
12. de Souza, R.T., Real-Hernández, L.M., Mojica, L., Johnson, M.H., Chang, Y.K., de Mejía, E.G., Effects of germination and alcalase hydrolysis of Phaseolus vulgaris seed proteins to produce bioactive peptides capable of improving markers related to type-2 diabetes. Food Research International 76 (2015), 150–159.
13. Debnam, E.S., Smith, M.W., Sharp, P.A., Srai, S.K., Turvey, A., Keable, S.J., The effects of streptozotocin diabetes on sodium-glucose transporter (SGLT1) expression and function in rat jejunal and ileal villus-attached enterocytes. Pflugers Archiv European Journal of Physiology 430:2 (1995), 151–159.
14. Dong, K., Ni, H., Wu, M., Tang, Z., Halim, M., Shi, D., ROS-mediated glucose metabolic reprogram induces insulin resistance in type 2 diabetes. Biochemical and Biophysical Research Communications 476 (2016), 204–211.
15. Duddela, S., Sekhar, P.N., Padmavati, G.V., Banerjee, A.K., Murty, U.S.N., Probing the structure of human glucose transporter 2 and analysis of protein ligand interactions. Medicinal Chemistry Research 19 (2010), 836–853.
16. Farrell, T.L., Ellam, S.L., Forrelli, T., Williamson, G., Attenuation of glucose transport across Caco-2 cell monolayers by a polyphenol-rich herbal extract: Interactions with SGLT1 and GLUT2 transporters. International Union of Biochemistry and Molecular Biology 39:4 (2013), 448–456.
17. Ferreira, L.G., dos Santos, R.N., Oliva, G., Andricopulo, A.D., Molecular docking and structure-based drug design strategies. Molecules 20 (2015), 13384–13421.
18. Food Chemicals Codex (2015). The United States pharmacopeial convention. The United States pharmacopeial convention (9th Edition). Copyright Date 2014, 978-1, ISBN 978-1-936424-26-9, Electronic Isbn-68015-293-7, Knovel Release date, 2015-01-12.
19. Gao, J., Han, Y.L., Jin, Z.Y., Xu, X.M., Zha, X.Q., Chen, H.Q., Yin, Y.Y., Protective effect of polysaccharides from Opuntia dillenii Haw. fruits on streptozotocin-induced diabetic rats. Carbohydrate Polymers 124 (2015), 25–34.
20. Garcia-Mora, P., Peñas, E., Frias, J., Zieliński, H., Wiczkowski, W., Zielińska, D., Martínez-Villaluenga, C., High-pressure-assisted enzymatic release of peptides and phenolics increases angiotensin converting enzyme inhibitory and antioxidant activities of pinto bean hydrolysates. Journal of Agricultural and Food Chemistry 64:8 (2016), 1730–1740.
21. Goyal, S.N., Reddy, N.M., Patil, K.R., Nakhate, K.T., Ojha, S., Patil, C.R., Agrawal, Y.O., Challenges and issues with streptozotocin-induced diabetes clinically relevant animal model to understand the diabetes pathogenesis and evaluate therapeutics. Chemico-Biological Interactions 244 (2016), 49–63.
22. Halgren, T.A., Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. Journal of Computational Chemistry 17:5–6 (1998), 490–519.
23. Hernandez-Saavedra, D., Mendoza-Sanchez, M., Hernandez-Montiel, H., Reynoso-Camacho, R., Cooked common beans (Phaseolus vulgaris) protect against β-cell damage in streptopzotocin-induced diabetic rats. Plant Foods for Human Nutrition 68:2 (2013), 207–212.
24. Hirano, T., Ito, Y., Saegusa, H., Yoshino, G., A novel and simple method for quantification of small, dense LDL. Journal of Lipid Research 44:11 (2003), 2193–2201.
25. ADA, American Diabetes Association (2016). < http://www.diabetes.org/>. Accessed, 9 March 2016.
26. Jang, S.M., Yee, S.T., Choi, J., Choi, M.S., Ursolic acid enhances the cellular immune system and pancreatic β-cell function in streptozotocin-induced diabetic mice fed a high-fat diet. International Immunopharmacology 9 (2009), 113–119.
27. Jiménez, S., Gascón, S., Luquin, A., Laguna, M., Ancin-Azpilicueta, C., Rodríguez-Yoldi, M.J., Rosa canina extracts have antiproliferative and antioxidant effects on caco-2 human colon cancer. PLoS ONE, 11(7), 2016, e0159136, 10.1371/ journal.pone. 0159136.
28. Johnson, M.H., Wallig, M., Luna-Vital, D.A., de Mejia, E.G., Alcohol-free fermented blueberry–blackberry beverage phenolic extract attenuates diet-induced obesity and blood glucose in C57BL/6J mice. Journal of Nutritional Biochemistry 31 (2016), 45–59.
29. Johnston, K., Sharp, P., Clifford, M., Morgan, L., Dietary polyphenols decrease glucose uptake by human intestinal Caco-2 cells. FEBS Letters 579 (2005), 653–1657.
30. Katsila, T., Spyroulias, G.A., Patrinos, G.P., Matsoukas, M.T., Computational approaches in target identification and drug discovery. Computational and Structural Biotechnology Journal 14 (2016), 177–184.
31. Koepsell, H., The Na+-D-glucose cotransporters SGLT1 and SGLT2 are targets for the treatment of diabetes and cancer. Pharmacology & Therapeutics, 2016, 10.1016/j.pharmthera.2016.10.017.
32. Kumar, S., Verma, A.K., Das, M., Jain, S.K., Dwivedi, P.D., Clinical complications of kidney bean (Phaseolus vulgaris L.) consumption. Nutrition 29 (2013), 821–827.
33. Kumar, S., Verma, A.K., Misra, A., Prasad, R., Jain, S.K., Das, M., Dwivedi, P.D., Allergenic responses of red kidney bean (Phaseolus vulgaris cv chitra) polypeptides in BALB/c mice recognized by bronchial asthma and allergic rhinitis patients. Food Research International 44 (2011), 2868–2879.
34. Kwon, O., Eck, P., Chen, S., Corpe, C.P., Inhibition of the intestinal glucose transporter GLUT2 by flavonoids. FASEB Journal 21 (2007), 366–377.
35. Kyznetsova, M.Y., Lavrovska, D.O., Zhyvolozhnyi, A.Y., Dovgusha, O.V., Halenova, T.I., Savchuk, O.M., Ostapchenko, L.I., Effect of aqueous extract from Phaseolus vulgaris pods on cytokine profile of streptozotocin-induced diabetic rats. RJPBCS 6:1 (2015), 1511–1520.
36. Lacroix, I., Li-Chan, E., Overview of food products and dietary constituents with antidiabetic properties and their natural putative mechanisms of action: A natural approach to complement pharmacotherapy in the management of diabetes. Molecular Nutrition and Food Research 58 (2014), 61–78.
37. Lamers, M.L., Almeida, M.E.S., Vicente-Manzanares, M., Horwitz, A.F., Santos, M.F., High glucose-mediated oxidative stress impairs cell migration. PLoS ONE, 6(8), 2011, e22865, 10.1371/journal.pone.0022865.
38. Li, Z., Geng, Y.-N., Jiang, J.-D., Kong, W.-J., Antioxidant and anti-inflammatory activities of berberine in the treatment of diabetes mellitus. Evidence-Based Complementary and Alternative Medicine, 2014, 289264.
39. Li, Y.W., Li, B., Characterization of structure–antioxidant activity relationship of peptides in free radical systems using QSAR models: Key sequence positions and their amino acid properties. Journal of Theoretical Biology 318 (2013), 29–43.
40. Luna-Vital, D.A., de Mejía, E.G., Mendoza, S., Loarca-Piña, G., Peptides present in the non-digestible fraction of common beans (Phaseolus vulgaris L.) inhibit the angiotensin-I converting enzyme by interacting with its catalytic cavity independent of their antioxidant capacity. Food & Function, 6, 2015, 1470.
41. Luna-Vital, D.A., Mojica, L., de Mejia, E.G., Mendoza, S., Loarca-Pina, G., Biological potential of protein hydrolysates and peptides from common bean (Phaseolus vulgaris L.): A review. Food Research International 76 (2015), 39–50.
42. Mojica, L., Chen, K., de Mejia, E.G., Impact of commercial precooking of common bean (Phaseolus vulgaris) on the generation of peptides, after pepsin–pancreatin hydrolysis, capable to inhibit dipeptidyl peptidase-IV. Journal of Food Science 80:1 (2015), H188–H198.
43. Mojica, L., de Mejía, E.G., Characterization and comparison of protein and peptide profiles and their biological activities of improved common bean cultivars (Phaseolus vulgaris L.) from Mexico and Brazil. Plant Foods for Human Nutrition 70:2 (2015), 105–112.
44. Mojica, L., de Mejía, E.G., Optimization of enzymatic production of anti-diabetic peptides from black bean (Phaseolus vulgaris L.) proteins and their characterization and biological potential. Food & Function 7 (2016), 713–727.
45. Morris, G.M., Goodsell, D.S., Halliday, R.S., Huey, R., Hart, W.E., Belew, R.K., Olson, A.J., Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. Journal of Computational Chemistry 19:14 (1998), 1639–1662.
46. Nath, S., Ghosh, S.K., Choudhury, Y., A murine model of type 2 diabetes mellitus developed using a combination of high fat diet and multiple low doses of streptozotocin treatment mimics the metabolic characteristics of type 2 diabetes mellitus in humans. Journal of Pharmacological and Toxicological Methods 84 (2017), 20–30.
47. Ngoh, Y.-Y., Gan, C.-Y., Enzyme assisted extraction and identification of antioxidative and α-amylase inhibitory peptides from Pinto beans. Food Chemestry 190 (2016), 331–337.
48. Oseguera Toledo, M.E., Gonzalez de Mejia, E., Sivaguru, M., Amaya-Llano, S.L., Common bean (Phaseolus vulgaris L.) protein-derived peptides increased insulin secretion, inhibited lipid accumulation, increased glucose uptake and reduced the phosphatase and tensin homologue activation in vitro. Journal of Functional Foods 27 (2016), 160–177, 10.1016/j.jff.2016.09.001.
49. Oseguera-Toledo, M.E., de Mejia, E.G., Amaya-Llano, S.L., Hard-to-cook bean (Phaseolus vulgaris L.) proteins hydrolyzed by alcalase and bromelain produced bioactive peptide fractions that inhibit targets of type-2 diabetes and oxidative stress. Food Research International 76 (2015), 839–851.
50. Oseguera-Toledo, M.E., de Mejia, E.G., Reynoso-Camacho, R., Cardador-Martinez, A., Amaya-Llano, S.L., Proteins and bioactive peptides: Mechanism of action in diabetes management. Nutrafoods 13 (2014), 147–157.
51. Patil, P., Mandal, S., Tomar, S., Food protein-derived bioactive peptides in management of type 2 diabetes. European Journal of Nutrition 54 (2015), 863–880.
52. Peng, C., Ma, J., Gao, X., Tian, P., Li, W., High glucose induced oxidative stress and apoptosis in cardiac microvascular endothelial cells are regulated by FoxO3a. PLoS ONE, 8(11), 2013, e79739, 10.1371/journal.pone.0079739.
53. Rahimi, R., Nikfar, S., Larijani, B., Abdollahi, M., A review on the role of antioxidants in the management of diabetes and its complications. Biomedicine & Pharmacotherapy 59 (2005), 365–373.
54. Ramachandran, G.N., Ramakrishnan, C., Sasisekharan, V., Stereochemistry of polypeptide chain configurations. Journal of Molecular Biology 7 (1963), 95–99.
55. Reagan-Shaw, S., Nihal, M., Ahmad, N., Dose translation from animal to human studies. The FASEB Journal 22 (2007), 659–661.
56. Roder, P.V., Geillinger, K.E., Zietek, T.S., Thorens, B., Koepsell, H., The role of SGLT1 and GLUT2 in intestinal glucose transport and sensing. PLoS ONE, 9(2), 2014, e89977.
57. Roy, A., Kucukural, A., Zhang, Y., I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols 5 (2010), 725–738.
58. Schmitt, A., Bigl, K., Meiners, I., Schmitt, J., Induction of reactive oxygen species and cell survival in the presence of advanced glycation end products and similar structures. Biochimica et Biophysica Acta 1763 (2006), 927–936.
59. Scow, J.S., Tavakkolizadeh, A., Zheng, Y., Sarr, M.G., Acute “adaptation” by the small intestinal enterocyte: A posttranscriptional mechanism involving apical translocation of nutrient transporters. Surgery 149 (2011), 601–605.
60. Sharma, B.R., Rhy, D.Y., Lespedeza davurica (Lax.) Schindl extract protects against cytokine-induced β-cell damage and streptozotocin-induced diabetes. BioMed Research International 2105 (2015), 1–8.
61. Szablewski, L., Glucose transporters in healthy heart and in cardiac disease. International Journal of Cardiology, 2016, 10.1016/j.ijcard.2016.12.083.
62. Torres-Fuentes, C., Contreras, M.D.M., Recio, I., Alaiz, M., Vioque, J., Identification and characterization of antioxidant peptides from chickpea protein hydrolysates. Food Chemistry 180 (2015), 194–202.
63. USDBC United States Dry Bean Council (2016). < http://www.usdrybeans.com/nutrition/nutrition-facts/> Accessed, 13 August 2016.
64. Vaishnav, S., Kulkarni, G.K., Perumal, P., In silico molecular modelling and docking of quercetin-γ-cyclodextrin inclusion complex on SGLT of Vibrio parahaemolyticus. International Journal of Pharmaceutical Sciences Review and Research 2:3 (2012), 167–175.
65. +-D-glucose cotransporter SGLT1 with high affinity. The Journal of Biological Chemistry 282:39 (2007), 28501–28513.
66. Wang, S., Mateos, R., Goya, L., Amigo-Benavent, M., Sarri, B., Bravo, L., A phenolic extract from grape by-products and its main hydroxybenzoic acids protect Caco-2 cells against pro-oxidant induced toxicity. Food and Chemical Toxicology 88 (2016), 65–74.
67. Whiteside, C.I., Cellular mechanisms and treatment of diabetes vascular complications converge on reactive oxygen species. Current Hypertension Reports 7 (2005), 148–154.
68. Wilson, S., Blaschek, K., de Mejia, E.G., Allergenic proteins in soybean: Processing and reduction of P34 allergenicity. Nutrition Reviews 63:2 (2005), 47–58.
69. Xu, W., Zhou, Q., Yin, J., Yao, Y., Zhang, J., Anti-diabetic effects of polysaccharides from Talinum triangulare in streptozotocin (STZ)-induced type 2 diabetic male mice. International Journal of Biological Macromolecules 72 (2015), 575–579.
70. You, Y., Ren, T., Zhang, S., Shirima, G.G., Hypoglycemic effects of Zanthoxylum alkylamides by enhancing glucose metabolism and ameliorating pancreatic dysfuction in streptozotocin-induced diabetic rats. The Royal Society of Chemistry 6:9 (2015), 3144–3154.