Actividad antiinflamatoria y antioxidante in vitro de fracciones de hidrolizado de proteínas de garbanzo (Cicer arietinum L.)


  • Ofelia Gabriela Meza Márquez Instituto Politécnico Nacional. Escuela Nacional de Ciencias Biológicas-Zacatenco. Departamento de Ingeniería Bioquímica.
  • Milagros Faridy Juárez-Chairez
  • Yazmín Karina Márquez-Flores
  • Cristian Jiménez-Martínez
  • Guillermo Osorio-Revilla


Palabras clave:

Actividad antiinflamatoria, actividad antioxidante, hidrolizados de proteínas, macrófagos, Cicer arietinum


El garbanzo es una leguminosa que ha exhibido diversas actividades biológicas. Se evaluaron las actividades antiinflamatorias y antioxidantes de las fracciones de hidrolizado de proteínas de garbanzo. El hidrolizado de proteína extenso (más del 50 %) obtenido por hidrólisis enzimática se fraccionó y se obtuvieron fracciones de 5-10 kDa, 3-5 kDa, 1-3 kDa y ≤1 kDa. La actividad antiinflamatoria se determinó en macrófagos peritoneales murinos estimulados con lipopolisacárido (LPS). Las fracciones de F5-10 kDa, F3-5 kDa, F1-3 kDa presentaron la mayor inhibición de la síntesis de óxido nítrico (76 %), factor de necrosis tumoral-α (93 %) e interleucina-1β (90 %). La actividad antioxidante se evaluó por métodos ABTS, DPPH, poder reductor de Fe3+ y capacidad quelante de Cu2+. La fracción F1-3 kDa mostró mayor inhibición de radicales ABTS (78 %) y DPPH (7.76 %), además mostró la mayor capacidad reductora de Fe3+ (0.508 Abs700nm), para Cu2+ capacidad quelante F≤1 kDa mostró mayor inhibición (52.60 % ). La proteína de garbanzo muestra actividades biológicas como antiinflamatoria y antioxidante, por lo que puede considerarse como una fuente de péptidos bioactivos de bajo peso molecular que pueden utilizarse como terapias alternativas para ciertas enfermedades relacionadas con la inflamación crónica.


Adegbola, P.I., Adetutu, A. and Olaniyi, T.D. 2020. Antioxidant activity of Amaranthus species from the Amaranthaceae family-A review. South African Journal of Botany. 133: 111-117.

Adegbola, P.I., Adetutu, A. and Olaniyi, T.D. 2020. Antioxidant activity of Amaranthus species from the Amaranthaceae family-A review. South African Journal of Botany. 133: 111-117.

Agyei, D., Ongkudon, C.M., Wei, C.Y., Chan, A.S. and Danquah, M.K. 2016. Bioprocess challenges to the isolation and purification of bioactive peptides. Food and Bioproducts Processing. 98: 244-256.

Arcan, I. and Yemenicioglu, A. 2007. Antioxidant activity of protein extracts from heat-treated or thermally processed chickpeas and white beans. Food Chemistry. 103: 301-312.

Arcan, I. and Yemenicioglu, A. 2010. Effects of controlled pepsin hydrolysis on antioxidant potential and fractional changes of chickpea proteins. Food Research International. 43: 140-147.

Avdagić, N., Zaćiragić, A., Babić, N., Hukić, M., Seremet, M., Lepara, O. and Nakaš-Ićindić, E. 2013. Nitric oxide as a potential biomarker in inflammatory bowel disease. Bosnian Journal of Basic Medical Sciences. 13: 5-9.

Brand-Williams, W., Cuvelier, M.E. and Berset, C.M. 1995. Use of a free radical method to evaluate antioxidant activity. Lebensmittel Wissenschaft Und Technologie. 28: 25-30.

Carrasco-Castilla, J., Hernández-Álvarez, A.J., Jiménez-Martínez, C., Jacinto-Hernández, C., Alaíz, M., Jirón-Calle, J., Vioque, J. and Dávila-Ortíz, G. 2012. Antioxidant and metal chelating activities of Phaseolus vulgaris var. Jamapa protein isolates, phaseolin and lectin hydrolysates. Food Chemistry. 131: 1157-1164.

Chen, Z., Li, W., Santhanam, R.K., Wang, C., Gao, X., Chen, Y., Wang, C., Xu, L. and Chen, H. 2018. Bioactive peptide with antioxidant and anticancer activities from black soybean [Glycine max (L.) Merr.] byproduct: Isolation, identification and molecular docking study. European Food Research and Technology. 245: 677-689.

Daliri, E. B. M., Oh, D. H. and Lee, B. H. 2017. Bioactive peptides. Foods. 6: 2–21

Dia, V. P., Wang, W., Oh, V. L., de Lumen, B. O. and González de Mejia, E. 2009. Isolation, purification and characterization of lunasin from defatted soybean flour and in vitro evaluation of its anti-inflammatory activity. Food Chemistry. 114:108–115.

Dinis, T., Madera, V. and Almeida, L. 1994. Action of phenolic derivatives (acetaminophen, salicylate and 5-amino sacylate) as inhibitors of membrane lipid peroxidation, and as peroxil radical scavengers. Archives Biochemistry Biophysis. 315: 161-169.

Elshafei, A. M. 2020. When oxygen can be toxic? A mini review. Journal of Applied Life Sciences International. 23: 1-9.

Ercan, P. and Neheir, S. 2016. Inhibitory effects of chickpea and Tribulus terrestris on lipase, alpha-amylase and alpha-glucosidase. Food Chemistry. 205: 163-169.

García-Lafuente, A., Moro, C., Manchón, N., Gonzalo-Ruiz, A., Villares, A., Guillamón, E., Rostagno, M. and Mateo-Vivaracho, L. 2014. In vitro anti-inflammatory activity of phenolic rich extracts from white and red common beans. Food Chemistry. 161: 216–223.

Ghribi, M.A., Gafsi, M.I., Sila, A., Blecker, C., Danthine, S., Attia, H., Bougatef, A. and Besbes, S. 2015a. Effects of enzymatic hydrolysis on conformational and functional properties of chickpea protein isolate. Food Chemistry. 187: 322-330.

Ghribi, M.A., Sila, A., Przybylski, R., Nedjar-Arroume, N., Makhlouf, I., Blecker, C., Attia, H., Dhulster, P., Bougatef, A. and Besbes, S. 2015b. Purification and identification of novel antioxidant peptides from enzymatic hydrolysate of chickpea (Cicer arietinum L.) protein concentrate. Journal of Functional Foods. 12: 512-525.

González-Montoya, M., Hernández-Ledesma, B., Silván, J. M., Mora-Escobedo, R. and Martínez-Villaluenga, C. 2018. Peptides derived from in vitro gastrointestinal digestion of germinated soybean proteins inhibit human colon cancer cells proliferation and inflammation. Food Chemistry. 242: 75–82.

Guo, Y., Zhang, T., Jiang, B., Miao, M. and Mu, W. 2014. The effects of an antioxidative pentapeptide derived from chickpea protein hydrolysates on oxidative stress in Caco-2 and HT-29 cell lines. Journal of Functional Foods. 7: 719–726.

Hassan-Ahmed, L. E., Dahham, S. S., Fadul, S. M., Umar, M. I., Abdul Majid, S. A., Khaw, K. Y. and Abdul Majid, A. M. S. 2016. Evaluation of in vitro and in vivo anti-inflammatory effects of (-)-pseudosemiglabrin, a major phytoconstituent isolated from Tephrosia apollinea (Delile) DC. Journal of Ethnopharmacology. 193: 312–320.

Huang, M., Lin, J., Lu, K., Xu, H., Geng, Z., Sun, P. and Chen, W. 2016. Anti-inflammatory effects of Cajaninstilbene acid and derivatives. Journal of Agriculture and Food Chemistry. 64: 2893-900.

Layoun, A., Samba, M. and Santos, M.M. 2015. Isolation of murine peritoneal macrophages to carry out gene expression analysis upon toll-like receptors stimulation. Journal of Visualized Experiments. 1: 1-5.

Li, Y., Jiang, B., Zhang, T., Mu, W. and Lui, J. 2008. Antioxidant and free radical-scavenging activities of chickpea protein hydrolysate. Food Chemistry. 106: 444-450.

Li, K.K., Zhou, X., Wong, H.L., Ng, F., Fu, W. M., Leung, P.C. and Ko, C.H. 2016. In vivo and in vitro anti-inflammatory effects of Zao-Jiao-Ci (the spine of Gleditsia sinensis Lam.) aqueous extract and its mechanisms of action. Journal of Ethnopharmacology. 192: 192-200.

López-Barrios, L., Antunes-Ricardo, M. and Gutiérrez-Uribe, J. 2016. Changes in antioxidant an anti-inflammatory activity of black bean (Phaselus vulgaris L.) protein isolates due to germination and enzymatic digestion. Food Chemistry. 1: 417-424.

Megías, C., Pedroche, J., Yust, M., Girón-Calle, J., Alaiz, F., Millan, N. and Vioque, J. 2007. Affinity purification of copper chelating peptides from chickpea protein hydrolysates. Journal Agriculture Food Chemistry. 55: 3949-3954.

Mieszkowska, A. and Marzec, A. 2016. Effect of polydextrose and inulin on texture and consumer preference of short-dough biscuits with chickpea flour. LWT-Food Science and Technology. 73: 60-66.

Milán-Noris, A. K., Gutiérrez-Uribe, J. A., Santacruz, A., Serna-Saldívar, S. O. and Martínez-Villaluenga, C. 2018. Peptides and isoflavones in gastrointestinal digests contribute to the anti-inflammatory potential of cooked or germinated desi and kabuli chickpea (Cicer arietinum L.). Food Chemistry. 268: 66–76.

Millán-Linares, M.C., Millán, F., Pedroche, J. and Yust, M. 2015. GPETAFLR: A new anti-inflammatory peptide from Lupinus angustifolius L. protein hydrolysate. Journal of Functional Foods. 18: 358-367.

Mondor, M., Aksay, S., Drolet, H., Roufik, S., Farnworth, E. and Boye J. 2009. Influence of processing on composition and antinutritional factors of chickpea protein concentrates produced by isoelectric precipitation and ultrafiltration. Innovative Food Science and Emerging Technologies. 10: 342-347.

Montoya-Rodríguez, A., de Mejía, E. G., Dia, V. P., Reyes-Moreno, C. and Milán-Carrillo, J. 2014. Extrusion improved the anti-inflammatory effect of amaranth (Amaranthus hypochondriacus) hydrolysates in LPS-induced human THP-1 macrophage-like and mouse RAW 264.7 macrophages by preventing activation of NF-κB signaling. Molecular Nutrition and Food Research. 58:1028–1041.

Nasri, M. 2016. Protein hydrolysates and biopeptides: Production, biological activities, and applications in foods and health benefits. A review. Advances in Food and Nutrition Research. 81: 109-159.

Ndiaye, F., Vuong, T., Duarte, J., Aluko, R. and Matar, C. 2012. Anti-oxidant, anti-inflammatory and immunomodulating properties of an enzymatic protein hydrolysate from yellow fields peas seeds. European Journal of Nutrition. 51: 29-37.

Ngoh, Y.Y. and Gan, C.Y. 2016. Enzyme-assisted extraction and identification of antioxidative and α-amylase inhibitory peptides from Pinto beans (Phaseolus vulgaris cv. Pinto). Food Chemistry. 190: 331-337.

Nielsen, P., Peterse, D. and Dambmann C. 2001. Improved method for determining food protein degree of hydrolysis. Journal of Food Science. 66: 642-646.

Orellana E.A. and Kasinki A.L. 2016. Sulforhodamine B (SRB) Assay in cell culture to investigate cell proliferation. Bio Protoc. 1: 6.

Oseguera-Toledo, M. E., González De Mejia, E., Dia, V. P. and Amaya-Llano, S. L. 2011. Common bean (Phaseolus vulgaris L.) hydrolysates inhibit inflammation in LPS-induced macrophages through suppression of NF-κB pathways. Food Chemistry. 127: 1175–1185.

Oyaizu, M. 1986. Studies on products of browning reactions: antioxidative activities of products of browning reaction prepare from glucosamine. Japanese Journal of Nutrition. 44: 307-315.

Real-Hernandez, L. M. and Gonzalez de Mejia, E. 2019. Enzymatic production, bioactivity, and bitterness of chickpea (Cicer arietinum) peptides. Comprehensive Reviews in Food Science and Food Safety. 18: 1913–1946.

Rizzello, C., Tagliazucchi, D., Babini, E., Rutella, G., Saa, D. and Gianotti, A. 2016. Bioactive peptides from vegetable food matrices: Research trends and novel biotechnologies for synthesis and recovery. Journal of Functional Foods. 27: 549-569.

Rizzo, G. 2020. The antioxidant role of soy and soy foods in human health. Antioxidants. 9: 635.

Samaei, S. P., Ghorbani, M., Tagliazucchi, D., Martini, S., Gotti, R., Themelis, T. Tesini F., Gianotti, A., Toschi, T.G. and Babini, E. 2020. Functional, nutritional, antioxidant, sensory properties and comparative peptidomic profile of faba bean (Vicia faba, L.) seed protein hydrolysates and fortified apple juice. Food Chemistry. 127120.

Sarmadi, B.H. and Ismail, A. 2010. Antioxidative peptides from food proteins: A review. Peptides. 31: 1949-1956.

Sharma, S., Singh, R. and Rana, S. 2011. Bioactive peptides: A review. International Journal Bioautomation. 15: 223–250.

Shi, W., Hou, T., Guo, D. and He, H. 2019. Evaluation of hypolipidemic peptide (Val-Phe-Val-Arg-Asn) virtual screened from chickpea peptides by pharmacophore model in high-fat diet-induced obese rat. Journal of Functional Foods. 54: 136–145.

Sies, H. and Jones, D. P. 2020. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nature Reviews Molecular Cell Biology. 1: 1-21.

Soudi, S., Zavaran-Hosseini, A., Muhammad-Hassan, Z., Soleimani, M., Jamshidi-Adegani, F. and Mahmoud-Hashemi, S. 2013. Comparative Study of the effect of LPS on the function of BALBc and C57BL/6 peritoneal macrophages. Cell J. 15: 45–54.

Tacias-Pascacio, V. G., Morellon-Sterling, R., Siar, E. H., Tavano, O., Berenguer-Murcia, Á. and Fernandez-Lafuente, R. 2020. Use of Alcalase in the production of bioactive peptides: A review. International Journal of Biological Macromolecules. 165: 2143–2196.

Torres-Fuentes, C., Alaiz, M. and Vioque, J. 2011. Affinity purification and characterization of chelating peptides from chickpea protein hydrolysates. Food Chemistry. 129: 485-490.

Torres-Fuentes, C., Contreras, M. M., Recio, I., Alaiz, M. and Vioque J. 2015. Identification and characterization of antioxidant peptides from chickpea protein hydrolysates. Food Chemistry. 180: 194-202.

Udenigwe, C. C. and Rajendran, S. R. C. K. 2016. Old products, new applications? Considering the multiple bioactivities of plastein in peptide-based functional food design. Current Opinion in Food Science. 8: 8–13.

Vernaza, M.G., Dia, P.V., Gonzalez de Mejia, E. and Chang, K.Y. 2012. Antioxidant and anti-inflammatory properties of germinated and hydrolysed Brazilian soybean flours. Food Chemistry. 134: 2217-2225.

Wali, A., Mijiti, Y., Yanhua, G., Yili, A., Aisa, H. A. and Kawuli, A. 2020. Isolation and identification of a novel antioxidant peptide from chickpea (Cicer arietinum L.) sprout protein hydrolysates. International Journal of Peptide Research and Therapeutics. 27: 219–227.

Wen, C., Zhang, J., Zhang, H., Duan, Y. and Ma, H. 2020. Plant protein-derived antioxidant peptides: Isolation, identification, mechanism of action and application in food systems: A review. Trends in Food Science & Technology. 105: 308-322.

Xie, J., Du, M., Shen, M., Wu, T. and Lin, L. 2019. Physico-chemical properties, antioxidant activities and angiotensin-I converting enzyme inhibitory of protein hydrolysates from mung bean (Vigna radiate). Food Chemistry. 270: 243–250.

Yu, M., He, S., Tang, M., Zhang, Z., Zhu, Y. and Sun, H. 2018. Antioxidant activity and sensory characteristics of Maillard reaction products derived from different peptide fractions of soybean meal hydrolysate. Food Chemistry. 243: 249-257.

Yust, M.M., Millán-Linares, M.C., Alcaide-Hidalgo, J.M., Millán, F. and Pedroche, J. 2012. Hypocholesterolaemic and antioxidant activities of chickpea (Cicer arietinum L.) protein hydrolysates. Journal Agriculture Food Chemistry. 92: 1994-2001.

Zhang, Q., Tong, X., Sui, X., Wang, Z., Qi, B., Li, Y. and Jiang, L. 2018. Antioxidant activity and protective effects of Alcalase-hydrolyzed soybean hydrolysate in human intestinal epithelial Caco-2 cells. Food Research International. 111: 256-264.

Zhang, T., Li, Y. and Miao, J. 2011. Purification and characterisation of a new antioxidant peptide from chickpea (Cicer arietinum L.) protein hydrolysates. Food Chemistry. 128: 28-33.