Hydrolyzates from Pyropia columbina seaweed have antiplatelet aggregation, antioxidant and ACE I inhibitory peptides which maintain bioactivity after simulated gastrointestinal digestion

LWT

Volumn 64, Issue 2, 2015, Pages 881-888

  Cian, Raúl E ^a,b   Garzón, Antonela G ^a,b   Ancona, David Betancur ^c   Guerrero, Luis Chel ^c   Drago, Silvina R ^a,b  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

^b Consejo Nacional de Investigaciones Científicas y Técnicas ^*  (Argentina)

^c UNIVERSIDAD AUTÓNOMA DE YUCATÁN   (Mexico)

Author keywords

Accessibility; Bioactive peptides; Gastrointestinal digestion; Red seaweeds

Indexed keywords

ANTIOXIDANTS; DIALYSIS MEMBRANES; ENZYMATIC HYDROLYSIS; ENZYME ACTIVITY; ENZYME INHIBITION; SEAWEED;

ACCESSIBILITY; ANGIOTENSIN-CONVERTING ENZYME; BIOACTIVE PEPTIDES; CHELATING ACTIVITY; GASTROINTESTINAL DIGESTION; INHIBITORY PEPTIDES; RED SEAWEEDS; SIMULATED DIGESTION;

PEPTIDES;

EID: 84944321182     PISSN: 00236438     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.lwt.2015.06.043     Document Type: Article

References (47)

1. A.O.A.C. (1995). Official methods of analysis (16th ed.). Washigton DC, USA: Horowitz.
2. Alaiz, M., Navarro, J., Giron, J., Vioque, E. (1992). Amino acid analysis by highperformanceliquid chromatography after derivatization with diethylethoxymethylenemalonate. Journal of Chromatography A, 591, 181e186.
3. Andronati, S., Karaseva, T., Krysko, A. (2004). Peptidomimetics - antagonists of the fibrinogen receptors: molecular design, structures, properties and therapeutic applications. Current Medicinal Chemistry, 11, 1183e1211.
4. Brand-Williams,W., Cuvelier, M., Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. Lebensmittel-Wissenschaft und Technologie, 28, 25e30.
5. Carrasco-Castilla, J., Hernández-Álvarez, A., Jiménez-Martínez, C., Jacinto- Hernández, C., Alaiz, M., Girón-Calle, J., et al. (2012). Antioxidant and metal chelating activities of peptide fractions from phaseolin and bean protein hydrolysates. Food Chemistry, 135, 1789e1795.
6. Chang, C., Wu, K., Chiang, S. (2007). Antioxidant properties and protein compositions of porcine haemoglobin hydrolysates. Food Chemistry, 100, 1537e1543.
7. Cian, R., Martínez-Augustin, O., Drago, S. (2012). Bioactive properties of peptides obtained by enzymatic hydrolysis from protein by products of Porphyra columbina. Food Research International, 49,364e49,372.
8. Cian, R., Salgado, P., Drago, S., González, R., Mauri, A. (2014). Development of naturally activated edible films with antioxidant properties prepared from red seaweed Porphyra columbina biopolymers. Food Chemistry, 146, 6e14.
9. Dávalos, A., Miguel, M., Bartolomé, B., López-Fadĩno, R. (2004). Antioxidant activity of peptides derived from egg white proteins by enzymatic hydrolysis. Journal of Food Protection, 67, 1939e1944.
10. Denis, C., Massé, A., Fleurence, J., Jaouen, P. (2009). Concentration and prepurification with ultrafiltration of a R-phycoerythrin solution extracted from macro-algae Grateloupia turuturu: process definition and up-scaling. Separation and Purification Technology, 69(15), 37e42.
11. Dubois, M., Gillis, K., Hamilton, J., Rebers, P., Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350e356.
12. Fleurence, J. (1999). Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends in Food Science and Technology, 10, 25e28.
13. Galland-Irmouli, A., Fleurence, J., Lamghari, R., Luçon, M., Rouxel, C., Barbaroux, O., et al. (1999). Nutritional value of proteins from edible seaweed Palmaria palmate (Dulse). The Journal of Nutrition and Biochemistry, 10, 353e359.
14. Harnedy, P., Fitzgerald, R. (2011). Bioactive proteins, peptides and amino acids from macroalgae. Journal of Phycology, 47, 218e232.
15. Hayakari, M., Kondo, Y., Izumi, H. (1978). A rapid and simple spectrophotometric assay of angiotensin-converting enzyme. Analytical Biochemistry, 84, 361e369.
16. Jao, C.-L., Huang, S.-L., Hsu, K.-C. (2012). Angiotensin I-converting enzyme inhibitory peptides: inhibition mode, bioavailability, and antihypertensive effects. BioMedicine, 2, 130e136.
17. Jiménez-Escrig, A., Gómez-Ordónez, E., Rupérez, P. (2012). Brown and red seaweeds as potential sources of antioxidant nutraceuticals. Journal of Applied Phycology, 24, 1123e1132.
18. Kim, S., Wijesekara, I. (2010). Development and biological activities of marinederived bioactive peptides: a review. Journal of Functional Foods, 2, 1e9.
19. Ko, S., Nalae, K., Kim, E., Kang, M., Lee, S., Kang, S. (2012). A novel angiotensin Iconverting enzyme (ACE) inhibitory peptide from a marine Chlorella ellipsoidea and its antihypertensive effect in spontaneously hypertensive rats. Process Biochemistry, 45, 2005e2011.
20. Megías, C., Pedroche, J., Yust, M., Girón-Calle, J., Alaiz, M., Millán, F., et al. (2008). Production of copper-chelating peptides after hydrolysis of sunflower proteins with pepsin and pancreatin. LWT - Food Science and Technology, 41, 1973e1977.
21. Miyashita, M., Akamatsu, M., Ueno, H., Nakagawa, Y., Nishimura, K., Hayashi, Y., et al. (1999). Structure-activity relationships of RGD mimetics as fibrinogen-receptor antagonists. Bioscience Biotechnology and Biochemistry, 63, 1684e1690.
22. Mohamed, S., Hashim, S., Rahman, H. (2012). Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends in Food Science and Technology, 23, 83e96.
23. Morris, H., Carrillo, O., Almarales, A., Bermúdez, R., Lebeque, Y., Fontaine, R. (2007). Immunostimulant activity of an enzymatic protein hydrolysate from green microalga Chlorella vulgaris on undernourished mice. Enzyme Microbiology Technology, 40, 456e460.
24. Nielsen, P., Petersen, D., Dambmann, C. (2001). Improved method for determining food protein degree of hydrolysis. Journal of Food Science, 66, 642e646.
25. Ni, H., Li, L., Liu, G., Hu, S. (2012). Inhibition mechanism and model of an angiotensin I-converting enzyme (ACE)-inhibitory hexapeptide from yeast (Saccharomyces cerevisiae). PLoS One, 7, e37077. http://dx.doi.org/10.1371/ journal.pone.0037077.
26. Norziah, M., Ching, C. (2000). Nutritional composition of edible seaweed Gracilaria changi. Food Chemistry, 68, 69e76.
27. Orsini, M., Tironi, V., Ãnón, M. (2011). Antioxidant activity of amaranth protein or their hydrolysates under simulated gastrointestinal digestion. LWT - Food Science & Technology, 44, 1752e1760.
28. Oyaizu, M. (1986). Studies on product of browning reaction prepared from glucose amine. Japanese Journal of Nutrition, 44, 307e315.
29. Pappenheimer, J., Michel, C. (2013). Role of villus microcirculation in intestinal absorption of glucose: coupling of epithelial with endothelial transport. Journal of Physiology, 553, 561e574.
30. Pedroche, J., Yust, M., Lqari, H., Megias, C., Girón-Calle, J., Alaiz, M., et al. (2007). Obtaining of Brassica carinata protein hydrolysates enriched in bioactive peptides using immobilized digestive proteases. Food Research International, 40, 931e938.
31. Qu, W., Maa, H., Pan, Z., Luo, L., Wanga, Z., He, R. (2010). Preparation and antihypertensive activity of peptides from Porphyra yezoensis. Food Chemistry, 123, 14e20.
32. Sato, M., Hoskawa, T., Yamaguchi, T., Nakano, T., Muramoto, K., Kahara, T. (2002). Angiotensin I-converting enzyme inhibitory peptides derived from wakame (Undaria pinnatifida) and their antihypertensive effect in spontaneously hypertensive rats. Journal of Agricultural and Food Chemistry, 50, 6245e6252.
33. Schanderl, S. (1970). Tannins and related phenolics. In M. A. Joslyn (Ed.), Methods in food: Analysis physical, chemical and instrumental methods of analysis (pp. 701e725). New York: Academic.
34. Segura Campos, M., Peralta González, F., Chel Guerrero, L., Betancur Ancona, D. (2013). Angiotensin i-converting enzyme inhibitory peptides of chia (Salvia hispanica) produced by enzymatic hydrolysis. International Journal of Food Science. http://dx.doi.org/10.1155/2013/15848.
35. Segura-Campos, M., Chel-Guerrero, L., Betancur-Ancona, D. (2010). Angiotensin-I converting enzyme inhibitory and antioxidant activities of peptide fraction extracted by ultrafiltration of cowpea Vigna unguiculata hydrolysates. Journal of the Science of Food and Agriculture, 90, 2512e2518.
36. Segura-Campos, M., Chel-Guerrero, L., Betancur-Ancona, D., Hernández-Escalante, V. (2011). Bioavailability of bioactive peptides. Food Reviews International, 27, 213e226.
37. Sheih, I., Fang, T., Wu, T. (2009). Isolation and characterization of a novel angiotensin I converting enzyme (ACE) inhibitory peptide from the algae protein waste. Food Chemistry, 115, 279e284.
38. Stevenson, B., Keon, B. (1998). The tight junction: morphology to molecules. Annual Review of Cell and Developmental and Biology, 14, 89e109.
39. Suetsuna, K., Maekawa, K., Chen, J. (2004). Antihypertensive effects of Undaria pinnatifida (wakame) peptide on blood pressure in spontaneously hypertensive rats. Journal of Nutrition and Biochemistry, 15, 267e272.
40. Tarola, A., Van de Velde, F., Salvagni, L., Preti, R. (2013). Determination of phenolic compounds in strawberries (Fragaria ananassa Duch) by high performance liquid chromatography with diode array detection. Food Analytical Methods, 6, 227e237.
41. Torres-Fuentes, C., Alaiz, M., Vioque, J. (2011). Affinity purification and characterization of chelating peptides from chickpea protein hydrolysates. Food Chemistry, 129, 485e490.
42. Vermeirssen, V., Van Camp, J., Verstraete,W. (2004). Bioavailability of angiotensin I converting enzyme inhibitory peptides. British Journal of Nutrition, 92, 357e366.
43. Wang, T., Jónsdóttir, R., Ólafsdóttir, G. (2009). Total phenolic compounds, radical scavenging and metal chelation of extracts form Icelandic seaweeds. Food Chemistry, 116, 240e248.
44. Wijesekara, I., Qian, Z., Ryu, B., Ngo, D., Kim, S. (2011). Purification and identification of antihypertensive peptides from seaweeds pipefish (Syngnathus schlegeli) muscle protein hydrolysate. Food Research International, 44, 703e707.
45. Yust, M., Millán-Linares, M., Alcaide-Hidalgo, J., Millán, F., Pedroche, J. (2012). Hypocolestereloaemic and antioxidant activity of chickpea (Cicer arietinum L.) protein hydrolysates. Journal of the Science of Food and Agriculture, 92, 1994e2001.
46. Yust, M., Millán-Linares, M., Alcaide-Hidalgo, J., Millán, F., Pedroche, J. (2013). Hydrolysis of chickpea proteins with Flavourzyme immobilized on glyoxylagarose gels improves functional properties. Food Science and Technology International, 19, 217e223.
47. Yust, M., Pedroche, J., Girón-Calle, J., Vioque, J., Millán, F., Alaiz, M. (2004). Determination of tryptophan by high-performance liquid chromatography of alkaline hydrolyzates with spectrophotometric detection. Food Chemistry, 85, 317e320.