Abstract
Background: Diabetes and hypertension are the major health concern and alleged to be of epidemic proportions. This has made it a numero uno subject at various levels of investigation. Glucosidase inhibitor provides the reasonable option in treatment of Diabetes Mellitus (DM) as it specifically targets post prandial hyperglycemia. The Angiotensin Converting Enzyme (ACE) plays an important role in hypertension. Therefore, inhibition of ACE in treatment of elevated blood pressure attracts special interest of the scientific community. Chickpea is a food legume and seeds contain carbohydrate binding protein- a lectin. Some of the biological properties of this lectin hitherto been elucidated.
Methods: Purified by ion exchange chromatography, chickpea lectin was tested for its in vitro antioxidant, ACE-I inhibitory and anti-diabetic characteristic.
Results: Lectin shows a characteristic improvement over the synthetic drugs like acarbose (oral anti-diabetic drug) and captopril (standard antihypertensive drug) when, their IC50 values are compared. Lectin significantly inhibited α-glucosidase and α-amylase in a concentration dependent manner with IC50 values of 85.41 ± 1.21 µg/ml and 65.05 ± 1.2 µg/ml compared to acarbose having IC50 70.20 ± 0.47 value of µg/ml and 50.52 ± 1.01 µg/ml respectively. β-Carotene bleaching assay showed antioxidant activity of lectin (72.3%) to be as active as Butylated Hydroxylanisole (BHA). In addition, lectin demonstrated inhibition against ACE-I with IC50 value of 57.43 ± 1.20 µg/ml compared to captopril.
Conclusion: Lectin demonstrated its antioxidant character, ACE-I inhibition and significantly inhibitory for α-glucosidase and α-amylase seems to qualify as an anti-hyperglycemic therapeutic molecule. The biological effects of chickpea lectin display potential for reducing the parameters of medically debilitating conditions. These characteristics however needs to be established under in vivo systems too viz. animals through to humans.
Keywords: Chickpea, Angiotensin Converting Enzyme-I (ACE-I), α-glucosidase, α-amylase, lectin, diabetes mellitus, antioxidant.
Graphical Abstract
[1]
Kumar, A.; Rana, D. Is there a role for Sodium orthovanadate in the treatment of diabetes? Curr. Diabetes Rev., 2019, 15(4), 284-287. [http://dx.doi.org/10.2174/1573399814666180903162556]. [PMID: 30179137].
[2]
Chaudhury, A.; Duvoor, C.; Reddy Dendi, V.S.; Kraleti, S.; Chada, A.; Ravilla, R.; Marco, A.; Shekhawat, N.S.; Montales, M.T.; Kuriakose, K.; Sasapu, A.; Beebe, A.; Patil, N.; Musham, C.K.; Lohani, G.P.; Mirza, W. Clinical review of antidiabetic drugs: Implications for type 2 diabetes mellitus management. Front. Endocrinol. (Lausanne), 2017, 8, 6. [http://dx.doi.org/10.3389/fendo.2017.00006]. [PMID: 28167928].
[3]
Kumar, A.; Goel, M.K.; Jain, R.B.; Khanna, P.; Chaudhary, V. India towards diabetes control: Key issues. Australas. Med. J., 2013, 6(10), 524-531. [http://dx.doi.org/10.4066/AMJ.2013.1791]. [PMID: 24223071].
[4]
Puri, P.; Singh, S.K.; Srivastava, S. Reporting heterogeneity in the measurement of hypertension and diabetes in India. J. Public Health; Berl, 2019, pp. 1-8. [https://doi.org/10.1007/s10389-019-01017-z]
[5]
Diagnosis and classification of diabetes mellitus. Diabetes Care, 2009, 32(Suppl. 1), S62-S67. [http://dx.doi.org/10.2337/dc09-S062]. [PMID: 19118289].
[6]
Misra, A.; Khurana, L. Obesity and the metabolic syndrome in developing countries. J. Clin. Endocrinol. Metab., 2008, 93(11)(Suppl. 1), S9-S30. [http://dx.doi.org/10.1210/jc.2008-1595]. [PMID: 18987276].
[7]
Deepthi, B.; Sowjanya, K.; Lidiya, B.; Bhargavi, R.S.; Babu, P.S. A modern review of diabetes mellitus: An annihilatory metabolic
disorder. J. In silico In vitro Pharmacol., 2017, 3, 1.
[8]
Kaul, K.; Tarr, J.M.; Ahmad, S.I.; Kohner, E.M.; Chibber, R. Diabetes: An old disease, a new insight; Springer-Verlag: New York, 2013.
[9]
Kalita, D.; Holm, D.G.; LaBarbera, D.V.; Petrash, J.M.; Jayanty, S.S. Inhibition of α-glucosidase, α-amylase, and aldose reductase by potato polyphenolic compounds. PLoS One, 2018, 13(1)e0191025 [http://dx.doi.org/10.1371/journal.pone.0191025]. [PMID: 29370193].
[10]
A.N.Hossain, M.S.; Naim, H.B.; Kumar, D.M.; Sapon, A.; Sen, M.K. A review on medicinal plants with antidiabetic activity. J. Pharmacog. Phytochem., 2014, 3, 149-159.
[11]
Williamson, J.R.; Kilo, C.; Tilton, R.G. Hyperglycemia, diabetes and vascular disease; Oxford University Press: New York, 1992, pp. 691-714.
[12]
Yao, Y.; Sang, W.; Zhou, M.; Ren, G. Antioxidant and α-glucosidase inhibitory activity of colored grains in China. J. Agric. Food Chem., 2010, 58(2), 770-774. [http://dx.doi.org/10.1021/jf903234c]. [PMID: 19904935].
[13]
Wang, H.; Du, Y.D.; Song, H. α-Glucosidase and α-amylase inhibitory activities of guava leaves. Food Chem., 2010, 123, 6-13. [http://dx.doi.org/10.1016/j.foodchem.2010.03.088].
[14]
Park, H.J.; Lee, M.K.; Park, Y.B.; Shin, Y.C.; Choi, M.S. Beneficial effects of Undaria pinnatifida ethanol extract on diet-induced-insulin resistance in C57BL/6J mice. Food Chem. Toxicol., 2011, 49(4), 727-733. [http://dx.doi.org/10.1016/j.fct.2010.11.032]. [PMID: 21146577].
[15]
Shai, J.L.; Magano, R.S.; Lebelo, S.L.; Mogale, A.M. Inhibitory effects of five medicinal plants on rat alpha-glucosidase: Comparison with their effects on yeast alpha-glucosidase. J. Med. Plants Res., 2011, 5, 2863-2867.
[16]
Rafe, M.R. A review of five traditionally used anti-diabetic plants of Bangladesh and their pharmacological activities. Asian Pac. J. Trop. Med., 2017, 10(10), 933-939. [http://dx.doi.org/10.1016/j.apjtm.2017.09.002]. [PMID: 29111187].
[17]
Hua, Z.Y.; Jun, G.J.; Hua, L.Z.; Jing, T. Research progress of ACE inhibitory peptide. Cereals Oil, 2011, 25, 44-46.
[18]
Wu, W.L.; Wu, G.J.; Liang, D.S.; Yang, F. The physiological function and research progress of angiotensin-I-converting enzyme inhibitory peptides. Modern Food Sci. Tech., 2006, 22, 251-254.
[19]
Wang, F.J.; Yin, X.Y.; Regenstein, J.M.; Wang, J.Z. Separation and purification of Angiotensin-I-Converting Enzyme (ACE) inhibitory peptides from walnuts (Juglans regia L.) meal. Eur. Food Res. Technol., 2016, 242, 911-918. [http://dx.doi.org/10.1007/s00217-015-2597-5].
[20]
McCarty, M.F. ACE inhibition may decrease diabetes risk by boosting the impact of bradykinin on adipocytes. Med. Hypotheses, 2003, 60(6), 779-783. [http://dx.doi.org/10.1016/S0306-9877(02)00234-7]. [PMID: 12699703].
[21]
International Year of Pulses Food and Agriculture Organization of the United Nations: Rome, Italy, 2016.
[22]
Roy, F.; Boye, J.I.; Simpson, B.K. Bioactive proteins and peptides in pulse crops: Pea, chickpea and lentil. Food Res. Int., 2010, 43, 432-442. [http://dx.doi.org/10.1016/j.foodres.2009.09.002].
[23]
Naeem, A.; Haque, S.; Khan, R.H. Purification and characterization of a novel β-D-galactosides-specific lectin from Clitoria ternatea. Protein J., 2007, 26(6), 403-413. [http://dx.doi.org/10.1007/s10930-007-9080-5]. [PMID: 17514413].
[24]
Gautam, A.K.; Gupta, N.; Narvekar, D.T.; Bhadkariya, R.; Bhagyawant, S.S. Characterization of chickpea (Cicer arietinum L.) lectin for biological activity. Physiol. Mol. Biol. Plants, 2018, 24(3), 389-397. [http://dx.doi.org/10.1007/s12298-018-0508-5]. [PMID: 29692547].
[25]
Gautam, A.K.; Srivastava, N.; Nagar, D.P.; Bhagyawant, S.S. Biochemical
and functional properties of a lectin purified from the
seeds of Cicer arietinum L. 3 Biotech., 8, 272. 2018.
[26]
Koleva, I.I.; van Beek, T.A.; Linssen, J.P.; de Groot, A.; Evstatieva, L.N. Screening of plant extracts for antioxidant activity: A comparative study on three testing methods. Phytochem. Anal., 2002, 13(1), 8-17. [http://dx.doi.org/10.1002/pca.611]. [PMID: 11899609].
[27]
Ueno, H.; Yamakura, S.; Arastoo, R.S.; Oshima, T.; Kokubo, K. Systematic evaluation and mechanistic investigation of antioxidant activity of fullerenols using carotene bleaching assay. J. Nanomater., 2014, 2014802596 [http://dx.doi.org/10.1155/2014/802596].
[28]
Cushman, D.W.; Cheung, H.S. Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem. Pharmacol., 1971, 20(7), 1637-1648. [http://dx.doi.org/10.1016/0006-2952(71)90292-9]. [PMID: 4355305].
[29]
Gupta, N.; Srivastava, N.; Bhagyawant, S.S. Vicilin-A major storage protein of mungbean exhibits antioxidative potential, antiproliferative effects and ACE inhibitory activity. PLoS One, 2018, 13(2)e0191265 [http://dx.doi.org/10.1371/journal.pone.0191265]. [PMID: 29408872].
[30]
Yu, Z.; Yin, Y.; Zhao, W.; Liu, J.; Chen, F. Anti-diabetic activity peptides from albumin against α-glucosidase and α-amylase. Food Chem., 2012, 135(3), 2078-2085. [http://dx.doi.org/10.1016/j.foodchem.2012.06.088]. [PMID: 22953959].
[31]
Kızıl, K.; Kızıl, M.; Çeken, B.; Yavuz, M.; Demir, H. Protective ability of ethanol extracts of Hypericum scabrum L. and Hypericum retusum Aucher against the protein oxidation and DNA damage. Int. J. Food Prop., 2011, 14, 926-940. [http://dx.doi.org/10.1080/10942910903491181].
[32]
Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 1970, 227(5259), 680-685. [http://dx.doi.org/10.1038/227680a0]. [PMID: 5432063].
[33]
Siddiqi, M.K.; Alam, P.; Iqbal, T.; Majid, N.; Malik, S.; Nusrat, S.; Alam, A.; Ajmal, M.R.; Uversky, V.N.; Khan, R.H. Elucidating the inhibitory potential of designed peptides against amyloid fibrillation and amyloid associated cytotoxicity. Front Chem., 2018, 6, 311. [http://dx.doi.org/10.3389/fchem.2018.00311]. [PMID: 30123793].
[34]
Siddiqi, M.K.; Alam, P.; Malik, S.; Majid, N.; Chaturvedi, S.K.; Rajan, S.; Ajmal, M.R.; Khan, M.V.; Uversky, V.N.; Khan, R.H. Stabilizing proteins to prevent conformational changes required for amyloid fibril formation. J. Cell. Biochem., 2018, 1-15. [https://doi.org/10.1002/jcb.27576]. [PMID: 30242891].
[35]
Kao, Y.H.; Chang, H.H.; Lee, M.J.; Chen, C.L. Tea, obesity, and diabetes. Mol. Nutr. Food Res., 2006, 50(2), 188-210. [http://dx.doi.org/10.1002/mnfr.200500109]. [PMID: 16416476].
[36]
Regan, T.J.; Lyons, M.M.; Ahmed, S.S.; Levinson, G.E.; Oldewurtel, H.A.; Ahmad, M.R.; Haider, B. Evidence for cardiomyopathy in familial diabetes mellitus. J. Clin. Invest., 1977, 60(4), 884-899. [http://dx.doi.org/10.1172/JCI108843]. [PMID: 893679].
[37]
Mizushige, K.; Yao, L.; Noma, T.; Kiyomoto, H.; Yu, Y.; Hosomi, N.; Ohmori, K.; Matsuo, H. Alteration in left ventricular diastolic filling and accumulation of myocardial collagen at insulin-resistant prediabetic stage of a type II diabetic rat model. Circulation, 2000, 101(8), 899-907. [http://dx.doi.org/10.1161/01.CIR.101.8.899]. [PMID: 10694530].
[38]
Nguyen, A.D.; Nguyen, Q.V.; Wang, S.L. Porcine pancreatic α-amylase inhibitors from Euonymus laxiflorus Champ. Res. Chem. Intermed., 2017, 43(1), 259-269. [http://dx.doi.org/10.1007/s11164-016-2619-3].
[39]
Messina, M.J. Legumes and soybeans: Overview of their nutritional profiles and health effects. Am. J. Clin. Nutr., 1999, 70(3)(Suppl.), 439S-450S. [http://dx.doi.org/10.1093/ajcn/70.3.439s]. [PMID: 10479216].
[40]
Katre, U.V.; Gaikwad, S.M.; Bhagyawant, S.S.; Deshpande, U.D.; Khan, M.I.; Suresh, C.G. Crystallization and preliminary X-ray characterization of a lectin from Cicer arietinum (chickpea). Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 2005, 61(Pt 1), 141-143. [http://dx.doi.org/10.1107/S1744309104032166]. [PMID: 16508116].
[41]
Aisa, H.A.; Yanhua, G.; Abulimiti, Y.; Qingling, M.; Zhen, C. Beneficial role of chickpea (Cicer arietinum L.) functional factors
in the intervention of metabolic syndrome and diabetes mellitus In: Bioactive Food as dietary interventions for diabetes; B.V; Preedy,
V.R., Ed.; Elsevier Science: Amsterdam. , 2019; pp. 615-627.
[42]
Zhuang, H.; Tang, N.; Yuan, Y. Purification and identification of antioxidant peptides from corn gluten meal. J. Funct. Foods, 2013, 5, 1810-1821. [http://dx.doi.org/10.1016/j.jff.2013.08.013].
[43]
Vioque, J. Production of ace inhibitory peptides by digestion of chickpea legumin with alcalase. Food Chem., 2003, 81(3), 363-369. [http://dx.doi.org/10.1016/S0308-8146(02)00431-4].
[44]
Yili, A.; Ma, Q.L.; Lv, Q.Y.; Gao, Y.H.; Zhao, B.; Veshkurova, O.N.; Salikhov, S.I.; Aisa, H.A. Antioxidant peptides from Cicer arietinum of Xinjiang, China. Chem. Nat. Compd., 2012, 48(4), 643-645. [http://dx.doi.org/10.1007/s10600-012-0332-z].
[45]
Ghassem, M.; Arihara, K.; Babji, A.S.; Said, M.; Ibrahim, S. Purification and identification of ACE inhibitory peptides from Haruan (Channa striatus) myofibrillar protein hydrolysate using HPLCESI-TOF MS/ MS. Food Chem., 2011, 129, 1770-1777. [http://dx.doi.org/10.1016/j.foodchem.2011.06.051].
[46]
Flather, M.D.; Yusuf, S.; Køber, L.; Pfeffer, M.; Hall, A.; Murray, G.; Torp-Pedersen, C.; Ball, S.; Pogue, J.; Moyé, L.; Braunwald, E. Long-term ACE-inhibitor therapy in patients with heart failure or left-ventricular dysfunction: A systematic overview of data from individual patients. Lancet, 2000, 355(9215), 1575-1581. [http://dx.doi.org/10.1016/S0140-6736(00)02212-1]. [PMID: 10821360].
[47]
Pahor, M.; Psaty, B.M.; Alderman, M.H.; Applegate, W.B.; Williamson, J.D.; Furberg, C.D. Therapeutic benefits of ACE inhibitors and other antihypertensive drugs in patients with type 2 diabetes. Diabetes Care, 2000, 23(7), 888-892. [http://dx.doi.org/10.2337/diacare.23.7.888]. [PMID: 10895836].
[48]
Intarasirisawat, R.; Benjakul, S.; Wu, J.; Visessanguan, W. Isolation of antioxidative and ACE inhibitory peptides from protein hydrolysate of skipjack (Katsuwana pelamis) roe. J. Funct. Foods, 2013, 5, 1854-1862. [http://dx.doi.org/10.1016/j.jff.2013.09.006].
[49]
Khan, M.Y.; Kumar, V. Mechanism & inhibition kinetics of bioassay-guided fractions of Indian medicinal plants and foods as ACE inhibitors. J. Tradit. Complement. Med., 2018, 9(1), 73-84. [http://dx.doi.org/10.1016/j.jtcme.2018.02.001]. [PMID: 30671369].
[50]
Gropper, S.S.; Smith, J.L. Advanced nutrition and human metabolism; Yalanda Cossio Inc: Belmont, 2013.
[51]
Wilson, A.L.; Mehra, I.V. Managing the patient with type II diabetes; Aspen Publishers: Gaithersburg, 1997.
[52]
Wang, Z.; Chen, M.; Zhu, Y.; Qian, P.; Zhou, Y.; Wei, J.; Shen, Y.; Mijiti, A.; Gu, A.; Wang, Z.; Zhang, H.; Ma, H. Yali, Zhou.; Wei, J.; Shen, Y.; Mijiti, A.; Gu, A.; Wang, Z.; Zhang, H.; Ma, H. Isolation, identification and characterization of a new type of lectin with α-amylase inhibitory activity in chickpea (Cicer arietinum L.). Protein Pept. Lett., 2017, 24(11), 1008-1020. [https://doi.org/10.2174/0929866524666170711120501]. [PMID: 29081299].
[53]
Lin, H.; Li, L.; Tian, Y.; Zhang, X.; Li, B. Protein hydrolysate from brewer’s spent grain and its inhibitory ability of α-glucosidase. Adv. Mat. Res., 2012, 581, 138-141. [http://dx.doi.org/10.4028/www.scientific.net/AMR.581-582.138].
[54]
Bhat, M.; Zinjarde, S.S.; Bhargava, S.Y.; Kumar, A.R.; Joshi, B.N. Antidiabetic Indian plants: A good source of potent amylase inhibitors. Evid. Based Complement. Alternat. Med., 2011, 2011810207 [http://dx.doi.org/10.1093/ecam/nen040]. [PMID: 18955350].
[55]
Alarcon-Aguilara, F.J.; Roman-Ramos, R.; Perez-Gutierrez, S.; Aguilar-Contreras, A.; Contreras-Weber, C.C.; Flores-Saenz, J.L. Study of the anti-hyperglycemic effect of plants used as antidiabetics. J. Ethnopharmacol., 1998, 61(2), 101-110. [http://dx.doi.org/10.1016/S0378-8741(98)00020-8]. [PMID: 9683340].
[56]
Chhetri, D.R.; Parajuli, P.; Subba, G.C. Antidiabetic plants used by Sikkim and Darjeeling Himalayan tribes, India. J. Ethnopharmacol., 2005, 99(2), 199-202. [http://dx.doi.org/10.1016/j.jep.2005.01.058]. [PMID: 15894127].
[57]
Sarikurkcu, C.; Eskici, M.; Karanfil, A.; Tepe, B. Phenolic profile, enzyme inhibitory and antioxidant activities of two endemic Nepeta species: Nepeta nuda subsp. glandulifera and N. cadmea. S. Afr. J. Bot., 2018, 120, 298-301. [http://dx.doi.org/10.1016/j.sajb.2018.09.008].
[58]
Pomin, V.H. Seaweed: Ecology, nutrient composition and medicinal uses; Nova Science Publishers Inc: New York, 2012.
[59]
Zaharudin, N.; Staerk, D.; Dragsted, L.O. Inhibition of α-glucosidase activity by selected edible seaweeds and fucoxanthin. Food Chem., 2019, 270, 481-486. [http://dx.doi.org/10.1016/j.foodchem.2018.07.142]. [PMID: 30174076].
[60]
Maeda, H. Anti-obesity and anti-diabetic activities of algae.Domínguez, H., Ed.; Woodhead Publishing Series in Food Science;
Technology and Nutrition , 2013; pp. 453-472. [http://dx.doi.org/10.1533/9780857098689.2.453]
[61]
Herrera, T.; Navarro Del Hierro, J.; Fornari, T.; Reglero, G.; Martin, D. Inhibitory effect of quinoa and fenugreek extracts on pancreatic lipase and α-amylase under in vitro traditional conditions or intestinal simulated conditions. Food Chem., 2019, 270, 509-517. [http://dx.doi.org/10.1016/j.foodchem.2018.07.145]. [PMID: 30174080].
[62]
Taha, M.; Shah, S.A.A.; Afifi, M.; Imran, S.; Sultan, S.; Rahim, F.; Khan, K.M. Synthesis, α-glucosidase inhibition and molecular docking study of coumarin based derivatives. Bioorg. Chem., 2018, 77, 586-592. [http://dx.doi.org/10.1016/j.bioorg.2018.01.033]. [PMID: 29477126].
[63]
Khan, J.M.; Qadeer, A.; Ahmad, E.; Ashraf, R.; Bhushan, B.; Chaturvedi, S.K.; Rabbani, G.; Khan, R.H. Monomeric banana lectin at acidic pH overrules conformational stability of its native dimeric form. PLoS One, 2013, 8(4)e62428 [http://dx.doi.org/10.1371/journal.pone.0062428]. [PMID: 23638080].
[64]
Bertoft, E.; Andtfolk, C.; Kulp, S.E. Effect of pH, temperature, and calcium ions on barley malt α‐amylase isoenzymes. J. Inst. Brew., 1984, 90, 298-302. [https://doi.org/10.1002/j.2050-0416.1984.tb04278.x].
[65]
Naseem, F.; Khan, R.H. Characterization of a common intermediate of pea lectin in the folding pathway induced by TFE and HFIP. Biochim. Biophys. Acta, 2005, 1723(1-3), 192-200. [http://dx.doi.org/10.1016/j.bbagen.2005.02.009]. [PMID: 15840464].
[66]
Oliveira, J.T.A.; Vasconcelos, I.M.; Gondim, M.J.L.; Cavada, B.S.; Moreira, R.A.; Santos, C.F.; Moreira, L.I.M. Canavalia brasiliensis seeds protein quality and nutritional implications of dietary lectin. J. Sci. Food Agric., 1994, 64, 417-424. [https://doi.org/10.1002/jsfa.2740640405].
[67]
E, Lacerda. R.R.; do Nascimento, E.S.; de Lacerda, J.T.; Pinto, L.D.; Rizzi, C.; Bezerra, M.M.; Pinto, I.R.; Filho, S.M.; Pinto, V.P.; Filho, G.C.; Gadelha, C.A.; Gadelha, T.S. Lectin from seeds of a Brazilian lima bean variety (Phaseolus lunatus L. var. cascavel) presents antioxidant, antitumour and gastroprotective activities. Int. J. Biol. Macromol., 2017, 95, 1072-1081. [http://dx.doi.org/10.1016/j.ijbiomac.2016.10.097]. [PMID: 27984144].
Related Journals
Current Protein & Peptide Science
Related Books
Frontiers in Protein and Peptide Sciences
Article Metrics
36
7
2
2