Legume Research

  • Chief EditorJ. S. Sandhu

  • Print ISSN 0250-5371

  • Online ISSN 0976-0571

  • NAAS Rating 6.80

  • SJR 0.391

  • Impact Factor 0.8 (2023)

Frequency :
Monthly (January, February, March, April, May, June, July, August, September, October, November and December)
Indexing Services :
BIOSIS Preview, ISI Citation Index, Biological Abstracts, Elsevier (Scopus and Embase), AGRICOLA, Google Scholar, CrossRef, CAB Abstracting Journals, Chemical Abstracts, Indian Science Abstracts, EBSCO Indexing Services, Index Copernicus
Legume Research, volume 43 issue 3 (june 2020) : 337-344

Inhibitory activity of salivary glycoproteins on phytohemagglutins (PHA): Possible molecules to enhance nutritional quality of red kidney beans

Vishwanath B. Chachadi, Tejashwini R. Nayanegali, Bharamappa G. Pujari, Lakshmi V. Umarji, Vasundhara Budyhalamath, Shashikala R. Inamdar, Pi-Wan Cheng
1Department of Studies in Biochemistry, Karnatak University, Dharwad-580 003, Karnataka, India.
  • Submitted01-05-2018|

  • Accepted20-08-2018|

  • First Online 15-11-2018|

  • doi 10.18805/LR-4034

Cite article:- Chachadi B. Vishwanath, Nayanegali R. Tejashwini, Pujari G. Bharamappa, Umarji V. Lakshmi, Budyhalamath Vasundhara, Inamdar R. Shashikala, Cheng Pi-Wan (2018). Inhibitory activity of salivary glycoproteins on phytohemagglutins (PHA): Possible molecules to enhance nutritional quality of red kidney beans. Legume Research. 43(3): 337-344. doi: 10.18805/LR-4034.
Food allergy caused by red kidney bean (Phaseolus vulgaris L.) is of serious health concern and is mainly due to its phytohemagglutinins (PHA) content. PHA can enter the circulation after oral uptake and cause IgE mediated allergy. However, studies describing enhancement of nutritional quality of red kidney beans by targeting PHA are not reported. This study was carried out to identify, PHA-inhibitory molecules present in saliva secretions. Results describe that PHA can be effectively inhibited by salivary glycoproteins. Fractionation of salivary proteins by ammonium sulphate precipitation revealed that, PHA-inhibitory proteins can be specifically precipitated at 30-60% of ammonium sulphate saturation. Gel filtration chromatography and lectin-blot analysis of 30-60% ammonium sulphate fraction suggest that only high molecular weight glycoproteins can act as potent inhibitors of PHA. In conclusion, human saliva secretions contain inhibitory glycoproteins which can be used to inhibit PHA effectively. If these glycoproteins are purified to homogeneity, can be used as potent food supplements in order to neutralize allergic potential of PHA, thus increasing the nutritional value of red kidney beans.
  1. Beyer, K., Morrow, E., Li, X. M., Bardina, L., Bannon, G. A., Burks, A. W., Sampson, H. A. (2001). Effects of cooking methods on peanut allergenicity. The Journal of Allergy and Clinical Immunology, 107:1077–1081. https://doi.org/10.1067/mai.2001.115480
  2. Bouckaert, J., Li, Z., Xavier, C., Almant, M., Caveliers V, Lahoutte, T., Weeks, S. D., Kovensky, J., Gouin, S. G. (2013). Heptyl alpha-    D-mannosides grafted on a beta-cyclodextrin core to interfere with Escherichia coli adhesion: an in vivo multivalent effect. Chemistry (Weinheim an Der Bergstrasse, Germany), 19:7847–7855. https://doi.org/10.1002/chem.201204015.
  3. Boyce, J. A., Assa’ad, A., Burks, A. W., Jones, S. M., Sampson, H. A., Wood, R. A., Schwaninger, J. M. (2011). Guidelines for the diagnosis and management of food allergy in the United States: summary of the NIAID-sponsored expert panel report. Nutrition Research (New York, N.Y.), 31:61–75. https://doi.org/10.1016/j.nutres.2011.01.001.
  4. Chen, Y., Zhao, Y. H., Kalaslavadi, T. B., Hamati, E., Nehrke, K., Le, A. D., Ann, D. k., Wu, R. (2004). Genome-wide search and identification of a novel gel-forming mucin MUC19/Muc19 in glandular tissues. American Journal of Respiratory Cell and Molecular Biology, 30:155–165. https://doi.org/10.1165/rcmb.2003-0103OC.
  5. Culp, D. J., Robinson, B., Cash, M. N., Bhattacharyya, I., Stewart, C., Cuadra-Saenz, G. (2015). Salivary mucin 19 glycoproteins: innate immune functions in Streptococcus mutans-induced caries in mice and evidence for expression in human saliva. The Journal of Biological Chemistry, 290:2993–3008. https://doi.org/10.1074/jbc.M114.597906.
  6. Duk, M., Lisowska, E., Wu, J. H., Wu, A. M. (1994). The biotin/avidin-mediated microtiter plate lectin assay with the use of chemically modified glycoprotein ligand. Analytical Biochemistry, 221:266–272. https://doi.org/10.1006/abio.1994.1410.
  7. Fitches, E., Ilett, C., Gatehouse, A. M. R., Gatehouse, L. N., Greene, R., Edwards, J. P., Gatehouse, J. A. (2001). The effects of Phaseolus vulgaris erythro- and leucoagglutinating isolectins (PHA-E and PHA-L) delivered via artificial diet and transgenic plants on the growth and development of tomato moth (Lacanobia oleracea) larvae; lectin binding to gut glycoprotein. Journal of Insect Physiology, 47:1389–1398.
  8. Glass, W. F. 2nd, Briggs, R. C., Hnilica, L. S. (1981). Use of lectins for detection of electrophoretically separated glycoproteins transferred onto nitrocellulose sheets. Analytical Biochemistry, 115:219–224.
  9. Guile, G. R., Harvey, D. J., O’Donnell, N., Powell, A. K., Hunter, A. P., Zamze, S., … Wing, D. R. (1998). Identification of highly fucosylated N-linked oligosaccharides from the human parotid gland. European Journal of Biochemistry, 258:623–656.
  10. Hall, S. C., Hassis, M. E., Williams, K. E., Albertolle, M. E., Prakobphol, A., Dykstra, A. B., Laurance, M., Ona, K., Niles, et al. (2017). Alterations in the Salivary Proteome and N-Glycome of Sjogren’s Syndrome Patients. Journal of Proteome Research, 16:1693–1705. https://doi.org/10.1021/acs.jproteome.6b01051.
  11. Hatton, M. N., Loomis, R. E., Levine, M. J., Tabak, L. A. (1985). Masticatory lubrication. The role of carbohydrate in the lubricating property of a salivary glycoprotein-albumin complex. The Biochemical Journal, 230:817–820.
  12. Heine, R. G. (2015). Food intolerance and allergy. World Review of Nutrition and Dietetics, 113:195–202. https://doi.org/10.1159/    000360340.
  13. Helmerhorst, E. J. and Oppenheim, F. G. (2007). Saliva: a dynamic proteome. Journal of Dental Research, 86:680–693. https://    doi.org/10.1177/154405910708600802.
  14. Kamboj, R. and Nanda, V. (2018), Proximate composition, nutritional profile and health benefits of legumes – A review, Legume research-An international Journal 41: 325-332, DOI: 10.18805/LR-3748.
  15. Kumar, D., Kumar, S., Verma, A. K., Sharma, A., Tripathi, A., Chaudhari, B. P., Kant, S., Das, M., Jain, S. K. and Dwivedi, P. D. (2014). Hypersensitivity linked to exposure of broad bean protein(s) in allergic patients and BALB/c mice. Nutrition (Burbank, Los Angeles County, Calif.), 30:903–914. https://doi.org/10.1016/j.nut.2013.11.024.
  16. Kumar, S., Verma, A. K., Sharma, A., Kumar, D., Tripathi, A., Chaudhari, B. P., Das, M., Jain, S. K. and Dwivedi, P. D. (2013). Phytohemagglutinins augment red kidney bean (Phaseolus vulgaris L.) induced allergic manifestations. Journal of Proteomics, 93:50–64. https://doi.org/10.1016/j.jprot.2013.02.003.
  17. Li, Y., St John, M. A. R., Zhou, X., Kim, Y., Sinha, U., Jordan, R. C. K., Eisele, D., et al., (2004). Salivary transcriptome diagnostics for oral cancer detection. Clinical Cancer Research/ : An Official Journal of the American Association for Cancer Research, 10:8442–8450. https://doi.org/10.1158/1078-0432.CCR-04-1167.
  18. Liener, I. E. and Hill, E. G. (1953). The effect of heat treatment on the nutritive value and hemagglutinating activity of soybean oil meal. The Journal of Nutrition, 49:609–620. https://doi.org/10.1093/jn/49.4.609
  19. Linden, S. K., Sutton, P., Karlsson, N. G., Korolik, V., McGuckin, M. A. (2008). Mucins in the mucosal barrier to infection. Mucosal Immunology, 1:183–197. https://doi.org/10.1038/mi.2008.5.
  20. Liu, B., Lague, J. R., Nunes, D. P., Toselli, P., Oppenheim, F. G., Soares, R. V, Troxler, R. F., Offner, G. D. (2002). Expression of membrane-associated mucins MUC1 and MUC4 in major human salivary glands. The Journal of Histochemistry and Cytochemistry/ : Official Journal of the Histochemistry Society, 50:811–820. https://doi.org/10.1177/002215540205000607.
  21. Lonardi, E., Moonens, K., Buts, L., de Boer, A. R., Olsson, J. D. M., Weiss, M. S., et al (2013). Structural sampling of glycan. interaction profiles reveals mucosal receptors for fimbrial adhesins of enterotoxigenic escherichia coli. Biology, 2:894–    917. https://doi.org/10.3390/biology2030894.
  22. Manage, L., Joshi, A., Sohonie, K. (1972). Toxicity to rats and mice of purified phytohaemagglutinins from four Indian legumes. Toxicon/ : Official Journal of the International Society on Toxinology, 10:89–91.
  23. Mankotia, K., Modgil, R., (2004). Nutritional and physico-chemical quality changes in soaked, sprouted and cooked kidney beans (phaseolus vulgaris). Legume Research-An International Journal, 27: ARCC3822.
  24. Martos, G., Lopez-Exposito, I., Bencharitiwong, R., Berin, M. C., Nowak-Wegrzyn, A. (2011). Mechanisms underlying differential food allergy response to heated egg. The Journal of Allergy and Clinical Immunology, 127: 990–992. https://doi.org/10.1016/    j.jaci.2011.01.057.
  25. Misra, A., Prasad, R., Das, M., Dwivedi, P. D. (2009). Probing novel allergenic proteins of commonly consumed legumes. Immunopharmacology and Immunotoxicology, 31:186–194. https://doi.org/10.1080/08923970802578782.
  26. Modgil, R., Mankotia, K., Verma, R., Sandal, A. (2016). Biological protein quality and phytic acid content of domestically processed kidney beans (Phaseolus vulgaris), Legume Research-An international journal, 35:315-318 DOI: 10.18805/ajdfr.v35i4.6631
  27. Nagae, M., Soga, K., Morita-Matsumoto, K., Hanashima, S., Ikeda, A., Yamamoto, K., Yamaguchi, Y. (2014). Phytohemagglutinin from Phaseolus vulgaris (PHA-E) displays a novel glycan recognition mode using a common legume lectin fold. Glycobiology, 24:368–378. https://doi.org/10.1093/glycob/cwu004.
  28. Navazesh, M. (1993). Methods for collecting saliva. Annals of the New York Academy of Sciences, 694:72–77.
  29. Nielsen, P. A., Bennett, E. P., Wandall, H. H., Therkildsen, M. H., Hannibal, J., Clausen, H. (1997). Identification of a major human high molecular weight salivary mucin (MG1) as tracheobronchial mucin MUC5B. Glycobiology, 7:413–419.
  30. Pol, J., Buczkowska-Radlinska, J., Binczak-Kuleta, A., Trusewicz, M. (2007). [Human salivary mucins—their role and meaning]. Annales Academiae Medicae Stetinensis, 53:87–91.
  31. Ramachandran, P., Boontheung, P., Pang, E., Yan, W., Wong, D. T., Loo, J. A. (2008). Comparison of N-linked Glycoproteins in Human Whole Saliva, Parotid, Submandibular, and Sublingual Glandular Secretions Identified using Hydrazide Chemistry and Mass Spectrometry. Clinical Proteomics, 4:80–104. https://doi.org/10.1007/s12014-008-9005-0.
  32. Rouge, P., Culerrier, R., Thibau, F., Didier, A., Barre, A. (2011). A case of severe anaphylaxis to kidney bean: phaseolin (vicilin) and PHA (lectin) identified as putative allergens. Allergy, 66:301–302. https://doi.org/10.1111/j.1398-9995.2010.02466.x.
  33. Rousseau, K., Kirkham, S., Johnson, L., Fitzpatrick, B., Howard, M., Adams, E. J., et al (2008). Proteomic analysis of polymeric salivary mucins: no evidence for MUC19 in human saliva. The Biochemical Journal, 413:545–552. https://doi.org/10.1042/    BJ20080260.
  34. Sampson, H. A. (2004). Update on food allergy. The Journal of Allergy and Clinical Immunology, 113:805–19; quiz 820. https://    doi.org/10.1016/j.jaci.2004.03.014.
  35. Sengupta, A., Valdramidou, D., Huntley, S., Hicks, S. J., Carrington, S. D., Corfield, A. P. (2001). Distribution of MUC1 in the normal human oral cavity is localized to the ducts of minor salivary glands. Archives of Oral Biology, 46:529–538.
  36. Sharon, N. (2007). Lectins: carbohydrate-specific reagents and biological recognition molecules. The Journal of Biological Chemistry, 282:2753–2764. https://doi.org/10.1074/jbc.X600004200.
  37. Sicherer, S. H., Sampson, H. A. (2010). Food allergy. The Journal of Allergy and Clinical Immunology, 125:116-25. https://doi.org/    10.1016/j.jaci.2009.08.028.
  38. Sutton, B. J., Gould, H. J. (1993). The human IgE network. Nature, 366:421–428. https://doi.org/10.1038/366421a0.
  39. Venter, F. S., Thiel, P. G. (1995). Red kidney beans—to eat or not to eat? South African Medical Journal = Suid-Afrikaanse Tydskrif Vir Geneeskunde, 85:250–252.
  40. Verma, A. K., Kumar, S., Das, M., Dwivedi, P. D. (2013). A comprehensive review of legume allergy. Clinical Reviews in Allergy & Immunology, 45:30–46. https://doi.org/10.1007/s12016-012-8310-6.
  41. Wiener, A. S., Moor-Jankowski, J., Gordon, E. B. (1969). The specificity of hemagglutinating bean and seed extracts (lectins). Implications for the nature of A-B-H agglutinins. International Archives of Allergy and Applied Immunology, 36:582–591.
  42. Yamaguchi, H. (1993). Isolation and characterization of the subunits of a heat-labile alpha-amylase inhibitor from Phaseolus vulgaris white kidney bean. Bioscience, Biotechnology, and Biochemistry, 57:297–302.
  43. Yin, S.-W., Tang, C.-H., Wen, Q.-B., Yang, X.-Q. (2011). Conformational and thermal properties of phaseolin, the major storage protein of red kidney bean (Phaseolus vulgaris L.). Journal of the Science of Food and Agriculture, 91:94–99. https://    doi.org/10.1002/jsfa.4155.
  44. Zalewska, A., Zwierz, K., Zolkowski, K., Gindzienski, A. (2000). Structure and biosynthesis of human salivary mucins. Acta Biochimica Polonica, 47:1067–1079.
  45. Zamindar, N., Mosaffa, L., Bashash, M., Amoheidari, M., Golabadi, M. (2016). The effect of diverse treatments on biophysical characteristics of red kidney beans. Legume Research-An International Journal, 39:550-557, DOI: 10.18805/lr.v39i4.11258. 

Editorial Board

View all (0)