Modification of the amaranth 11S globulin storage protein to produce an inhibitory peptide of the angiotensin I converting enzyme, and its expression in Escherichia coli

Journal of Biotechnology

Volumn 148, Issue 4, 2010, Pages 240-247

  Luna Suárez, Silvia ^a   Medina Godoy, Sergio ^a   Cruz Hernández, Andrés ^b   Paredes López, Octavio ^b  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

Author keywords

11S acidic subunit; Amaranth globulin; Angiotensin converting enzyme inhibitor; Biopeptides; Seed storage protein

Indexed keywords

11S GLOBULIN; ANGIOTENSIN CONVERTING ENZYME INHIBITORS; ANGIOTENSIN I-CONVERTING ENZYME; ANGIOTENSIN-CONVERTING ENZYME; BIOPEPTIDES; ESSENTIAL AMINO ACIDS; EXPRESSION IN ESCHERICHIA COLI; HIGH-CONTENT; INHIBITORY ACTIVITY; INHIBITORY PEPTIDES; MASS SPECTROMETRY ANALYSIS; NUTRACEUTICALS; PEPTIDE MASS FINGERPRINTING; PRIMARY STRUCTURES; SEED STORAGE PROTEINS; STORAGE PROTEINS;

AMINO ACIDS; ESCHERICHIA COLI; HYDROLYSIS; MASS SPECTROMETRY; ORGANIC ACIDS; PEPTIDES; PURIFICATION; SEED;

ENZYMES;

AMARANTH; DIPEPTIDYL CARBOXYPEPTIDASE; GLOBULIN;

AMINO ACID SEQUENCE; ARTICLE; BIOENGINEERING; CONTROLLED STUDY; DNA FINGERPRINTING; ENZYME ACTIVITY; ESCHERICHIA COLI; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANTIGENS, PLANT; ESCHERICHIA COLI; PEPTIDES; PEPTIDYL-DIPEPTIDASE A; PROTEIN ENGINEERING; RECOMBINANT PROTEINS; SEED STORAGE PROTEINS;

AMARANTHUS CAUDATUS; ESCHERICHIA COLI;

EID: 77955049376     PISSN: 01681656     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2010.06.009     Document Type: Article

References (54)

1. Adachi M., Kanamori J., Masuda T., Yagasaki K., Nikamura K., Mikami B., Utsumi S. Crystal structure of soybean 11S globulin: glycinin A3B4 homohexamer. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:7395-7400.
2. Adachi M., Takenaka Y., Gidamis A.B., Mikami B., Utsumi S. Crystal structure of soybean proglycinin A1aB1b homotrimer. J. Mol. Biol. 2001, 12:291-305.
3. Baneyx F., Mujacic M. Recombinant protein folding and misfolding in Escherichia coli. Nat. Biotechnol. 2004, 22:1399-1408.
4. Barba de la Rosa A.P., Herrera A., Utsumi S., Paredes-López O. Molecular characterization, cloning and structural analysis of a cDNA encoding an amaranth globulin. J. Plant Physiol. 1996, 149:527-532.
5. Chen S., Paredes-López O. Isolation and characterization of the 11S globulin from amaranth seeds. J. Food Biochem. 1997, 21:53-65.
6. Chobanian A.V., Haudenschild C.C., Nickerson C., Drago R. Antiatherogenic effect of captopril in the Watanabe heritable hyperlipidemic rabbit. Hypertension 1990, 15:327-331.
7. Cinq-Mars C.D., Li-Chan E.C.Y. Optimizing angiotensin I-converting enzyme inhibitory activity of pacific hake (Merluccius productus) fillet hydrolysate using response surface methodology and ultrafiltration. J. Agric. Food Chem. 2007, 55:9380-9388.
8. Curciarello R., Lareu J.F., Fossati C.A., Docena G.H., Petruccelli S. Immunochemical characterization of Glycine max L. Merr. var Raiden, as a possible hypoallergenic substitute for cow's milk-allergic patients. Clin. Exp. Allergy 2008, 38:1559-1565.
9. Dickinson C.D., Scott M.P., Hussein E.H., Argos P., Nielsen N.C. Effect of structural modifications on the assembly of a glycinin subunit. Plant Cell 1990, 2:403-413.
10. Fahnert B., Lile H., Neubauer P.B. Inclusion bodies: formation and utilization. Adv. Biochem. Eng./Biotechnol. 2004, 89:93-142.
11. Hamme V., Sannier F., Piot J.M., Didelot S., Bordenave-Juchereau S. Crude goat whey fermentation by Kluyveromyces marxianus and Lactobacillus rhamnosus: contribution to proteolysis and ACE inhibitory activity. J. Dairy Res. 2009, 76:152-157.
12. Hayes M., Stanton C., Slattery H., O'Sullivan O., Hill C., Fitzgerald G.F., Ross R.P. Casein fermentate of Lactobacillus animalis DPC6134 contains a range of novel propeptide angiotensin-converting enzyme inhibitors. Appl. Environ. Microbiol. 2007, 73:4658-4667.
13. Hernández-Ledesma B., Amigo L., Recio I., Bartolomé B. ACE-inhibitory and radical-scavenging activity of peptides derived from β-lactoglobulin f(19-25). Interactions with ascorbic acid. J. Agric. Food Chem. 2007, 55:3392-3397.
14. Holzhauser T., Wackermann O., Ballmer-Weber B.K., Bindslev-Jensen C., Scibilia J., Perono-Garoffo L., Utsumi S., Poulsen L.K., Vieths S. Soybean (Glycine max) allergy in Europe: Gly m 5 (beta-conglycinin) and Gly m 6 (glycinin) are potential diagnostic markers for severe allergic reactions to soy. J Allergy Clin. Immunol. 2009, 123:452-458.
15. Hong F., Ming L., Yi S., Zhanxia L., Yongquan W., Chi L. The antihypertensive effect of peptides: a novel alternative to drugs?. Peptides 2008, 29:1062-1071.
16. Jauhiainen T., Colline M., Narva M., Cheng Z.J., Poussa T., Vapaatalo H., Korpela R. Effect of long-term intake of milk peptides and minerals on blood pressure and arterial function in spontaneously hypertensive rats. Milchwissenschaft 2005, 60:358-363.
17. Jeong D.W., Shin D.S., Ahn C.W., Song I.S., Lee H.J. Expression of antihypertensive peptide, His-His-Leu, as tandem repeats in Escherichia coli. J. Microbiol. Biotechnol. 2007, 17:952-959.
18. Kawasaki T., Seki E., Osajima K., Yoshida M., Asada K., Matsui T., Osajima Y. Antihypertensive effect of valyl-tyrosine, a short chain peptide derived from sardine muscle hydrolyzate, on mild hypertensive subjects. J. Hum. Hypertens. 2000, 14:519-523.
19. Keil B. Specificity of Proteolysis 1992, Springer Verlag, Berlin/Heidelberg/New York, p. 335.
20. Krishnan H.B., Kim W.S., Jang S., Kerley M.S. All three subunits of soybean beta-conglycinin are potential food allergens. J. Agric. Food Chem. 2009, 57:938-943.
21. Lee J.H., Minn I., Park C.B., Kim S.C. Acidic peptide mediated expression of the antimicrobial peptide buforin II as tandem repeats in Escherichia coli. Protein Expr. Purif. 1998, 12:53-60.
22. Li G.H., Qu M.R., Wan J.Z., You J.M. Antihypertensive effect of rice protein hydrolysate with in vitro angiotensin I-converting enzyme inhibitory activity in spontaneously hypertensive rats. Asia Pac. J. Clin. Nutr. 2007, 16:275-280.
23. Lopez-Fandino R., Otte J., Van-Camp J. Physiological, chemical and technological aspects of milk-protein-derived peptides with antihypertensive and ACE-inhibitory activity. Int. Dairy J. 2006, 16:1277-1293.
24. Luna-Suárez S., Medina-Godoy S., Cruz-Hernández A., Paredes-López O. Expression and characterization of the acidic subunit from 11S amaranth seed protein. Biotechnol. J. 2008, 3:209-219.
25. Mallikarjun G.K.G., Gowda L.R., Rao A., Prakash V. Angiotensin I-converting enzyme inhibitory peptide derived from glycinin, the 11S globulin of soybean (Glycine max). J. Agric. Food Chem. 2006, 54:4568-4573.
26. Masuda O., Nakamura Y., Takano T. Antihypertensive peptides are present in aorta after oral administration of sour milk containing these peptides to spontaneously hypertensive rats. J. Nutr. 1996, 126:3063-3068.
27. Masurekar P.S. Nutritional and engineering aspects of microbial process development. Prog. Drug Res. 2008, 65:293-328.
28. Matoba N., Doyama N., Yamada Y., Maruyama N., Utsumi S., Yoshikawa M. Design and production of genetically modified soybean protein with anti-hypertensive activity by incorporating potent analogue of ovokinin(2-7). FEBS Lett. 2001, 497:50-54.
29. Matsui T., Tamaya K., Sekji E., Osajima K., Matsumoto K., Kawasaki T. Val-Tyr as a natural antihypertensive dipeptide can be absorbed into the human circulatory blood system. Clin. Exp. Pharmacol. Physiol. 2002, 29:204-208.
30. 2+ channel inhibition in cultured vascular smooth muscle cells. Hypertens. Res. 2005, 28:545-552.
31. Matsui T., Zhu X.L., Watanabe K., Tanaka K., Kusano Y., Matsumoto K. Combined administration of captopril with an antihypertensive Val-Tyr di-peptide to spontaneously hypertensive rats attenuates the blood pressure lowering effect. Life Sci. 2006, 79:2492-2498.
32. Medina-Godoy S., Nielsen N.C., Paredes-López O. Expression and characterization of a His-tagged 11S seed globulin from Amaranthus hypochondriacus in Escherichia coli. Biotechnol. Prog. 2004, 20:1749-1756.
33. Medina-Godoy S., Valdez-Ortiz A., Valverde M.A., Paredes-López O. Endoplasmic reticulum-retention C-terminal sequence enhances production of an 11S seed globulin from Amaranthus hypochondriacus in Pichia pastoris. Biotechnol. J. 2006, 1:1085-1092.
34. Nilsson B., Anderson S. Proper and improper folding of proteins in the cellular environment. Annu. Rev. Microbiol. 1991, 45:607-635.
35. Nishizawa K., Kita A., Doi C., Yamada Y., Ohinata K., Yoshikawa M., Ishimoto M. Accumulation of the bioactive peptides, novokinin, LPYPR and rubiscolin, in seeds of genetically modified soybean. Biosci. Biotechnol. Biochem. 2008, 72:3301-33105.
36. Onishi K., Matoba N., Yamada Y., Doyama N., Maruyama N., Utsumi S., Yoshikawa M. Optimal designing of beta-conglycinin to genetically incorporate RPLKPW, a potent anti-hypertensive peptide. Peptides 2004, 25:37-43.
37. Osuna-Castro J.A., Rascón-Cruz Q., Napier J., Fido R.J., Shewry P.R., Paredes-López O. Overexpression, purification, and in vitro refolding of the 11S globulin from amaranth seed in Escherichia coli. J. Agric. Food Chem. 2000, 48:5249-5255.
38. Prak K., Maruyama Y., Maruyama N., Utsumi S. Design of genetically modified soybean proglycinin A1aB1b with multiple copies of bioactive peptide sequences. Peptides 2006, 27:1179-1186.
39. Prak K., Utsumi S. Production of a bioactive peptide (IIAEK) in Escherichia coli using soybean proglycinin A1ab1b as a carrier. J. Agric. Food Chem. 2009, 57:3792-3799.
40. Rao X., Hu J., Li S., Jin X., Zhang C., Cong Y., Hu X., Tan Y., Huang J., Chen Z., Zhu J., Hu F. Design and expression of peptide antibiotic hPAB-β as tandem multimers in Escherichia coli. Peptides 2005, 26:721-729.
41. Rascón-Cruz Q., Sinagawa-García S., Osuna-Castro J.A., Bohorova N., Paredes-López O. Accumulation, assembly, and digestibility of amarantin expressed in transgenic tropical maize. Theor. Appl. Genet. 2004, 108:335-342.
42. Romero-Zepeda H., Paredes-López O. Isolation and characterization of amarantin, the 11S amaranth seed globulin. J. Food Biochem. 1996, 19:329-339.
43. Saiga A., Iwai K., Hayakawa T., Takahata Y., Kitamura S., Nishimura T., Morimatsu F. Angiotensin I-converting enzyme-inhibitory peptides obtained from chicken collagen hydrolysate. J. Agric. Food Chem. 2008, 56:9586-9591.
44. Sambrook J.E., Fritsch E.T., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
45. Seppo L., Jauhiainen T., Poussa T., Korpela R. A fermented milk high in bioactive peptides has a blood pressure lowering effect in hypertensive subjects. Am. J. Clin. Nutr. 2003, 77:326-330.
46. Shewry P.R. Manipulation of seed storage proteins. Transgenic Plant Research 1998, 135-149. Harwood Academic Publishers, Reading. K. Lindsey (Ed.).
47. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68:850-858.
48. Silva-Sánchez C., Barba de la Rosa A.P., León-Galván M.F., De Lumen B.O., León-Rodríguez A., González de Mejía E. Bioactive peptides in amaranth (Amaranthus hypochondriacus) seed. J. Agric. Food Chem. 2008, 56:1233-1240.
49. Sinagawa-García S.R., Rascón-Cruz Q., Valdez-Ortiz A., Medina-Godoy S., Escobar-Gutiérrez A., Paredes-López O. Safety assessment by in vitro digestibility and allergenicity of genetically modified maize with an amaranth 11S globulin. J. Agric. Food Chem. 2004, 52:2709-2714.
50. Tai S.S., Wu L.S., Chen E.C., Tzen J.T. Molecular cloning of 11S globulin and 2S albumin, the two major seed storage proteins in sesame. J. Agric. Food Chem. 1999, 47:4932-4938.
51. Tuomilehto J., Lindstrom J., Hyrynen J., Korpela R., Karhunen M.L., Mikola L., Jauhiainen T., Seppo L., Nissinen A. Effect of ingesting sour milk fermented using Lactobacillus helveticus bacteria producing tripeptides on blood pressure in subjects with mild hypertension. J. Hum. Hypertens. 2004, 18:795-802.
52. Valdez-Ortiz A., Rascón-Cruz Q., Medina-Godoy S., Sinagawa-García S.R., Valverde-González M.E., Paredes-López O. One-step purification and structural characterization of a recombinant His-tag 11S globulin expressed in transgenic tobacco. J. Biotechnol. 2005, 115:413-423.
53. Wright D.J. The seed globulins-part II. Developments in Food Proteins 1988, 119-177. Elsevier Applied Science, London. B.J.F. Hudson (Ed.).
54. Yokoyama S. Protein expression systems for structural genomics and proteomics. Curr. Opin. Chem. Biol. 2003, 7:39-43.