Angiotensin I Converting Enzyme Inhibitory Peptides Derived from Phycobiliproteins of Dulse Palmaria Palmata

Overview

Journal Mar Drugs

Publisher MDPI

Specialties Biology
Pharmacology

Date 2016 Feb 11

PMID 26861357

Citations 28

Authors

Tomoe Furuta

Yoshikatsu Miyabe

Hajime Yasui

Yasunori Kinoshita

Hideki Kishimura

Affiliations

Soon will be listed here.

Abstract

We examined the inhibitory activity of angiotensin I converting enzyme (ACE) in protein hydrolysates from dulse, Palmaria palmata. The proteins extracted from dulse were mainly composed of phycoerythrin (PE) followed by phycocyanin (PC) and allophycocyanin (APC). The dulse proteins showed slight ACE inhibitory activity, whereas the inhibitory activity was extremely enhanced by thermolysin hydrolysis. The ACE inhibitory activity of hydrolysates was hardly affected by additional pepsin, trypsin and chymotrypsin treatments. Nine ACE inhibitory peptides (YRD, AGGEY, VYRT, VDHY, IKGHY, LKNPG, LDY, LRY, FEQDWAS) were isolated from the hydrolysates by reversed-phase high-performance liquid chromatography (HPLC), and it was demonstrated that the synthetic peptide LRY (IC50: 0.044 μmol) has remarkably high ACE inhibitory activity. Then, we investigated the structural properties of dulse phycobiliproteins to discuss the origin of dulse ACE inhibitory peptides. Each dulse phycobiliprotein possesses α-subunit (Mw: 17,477-17,638) and β-subunit (Mw: 17,455-18,407). The sequences of YRD, AGGEY, VYRT, VDHY, LKNPG and LDY were detected in the primary structure of PE α-subunit, and the LDY also exists in the APC α- and β-subunits. In addition, the LRY sequence was found in the β-subunits of PE, PC and APC. From these results, it was suggested that the dulse ACE inhibitory peptides were derived from phycobiliproteins, especially PE. To make sure the deduction, we carried out additional experiment by using recombinant PE. We expressed the recombinant α- and β-subunits of PE (rPEα and rPEβ, respectively), and then prepared their peptides by thermolysin hydrolysis. As a result, these peptides showed high ACE inhibitory activities (rPEα: 94.4%; rPEβ: 87.0%). Therefore, we concluded that the original proteins of dulse ACE inhibitory peptides were phycobiliproteins.

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References

Fitzgerald C, Mora-Soler L, Gallagher E, OConnor P, Prieto J, Soler-Vila A . Isolation and characterization of bioactive pro-peptides with in vitro renin inhibitory activities from the macroalga Palmaria palmata. J Agric Food Chem. 2012; 60(30):7421-7. DOI: 10.1021/jf301361c. View

Kishimura H, Ojima T, Hayashi K, Nishita K . Bacterial expression and characterization of starfish phospholipase A(2). Comp Biochem Physiol B Biochem Mol Biol. 2001; 128(3):565-73. DOI: 10.1016/s1096-4959(00)00349-3. View

Suetsuna K, Maekawa K, Chen J . Antihypertensive effects of Undaria pinnatifida (wakame) peptide on blood pressure in spontaneously hypertensive rats. J Nutr Biochem. 2004; 15(5):267-72. DOI: 10.1016/j.jnutbio.2003.11.004. View

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

Cheung H, Cushman D . Inhibition of homogeneous angiotensin-converting enzyme of rabbit lung by synthetic venom peptides of Bothrops jararaca. Biochim Biophys Acta. 1973; 293(2):451-63. DOI: 10.1016/0005-2744(73)90352-5. View

Cheung H, Wang F, ONDETTI M, SABO E, Cushman D . Binding of peptide substrates and inhibitors of angiotensin-converting enzyme. Importance of the COOH-terminal dipeptide sequence. J Biol Chem. 1980; 255(2):401-7. View

Apt K, Collier J, Grossman A . Evolution of the phycobiliproteins. J Mol Biol. 1995; 248(1):79-96. DOI: 10.1006/jmbi.1995.0203. View

Nakano D, Ogura K, Miyakoshi M, Ishii F, Kawanishi H, Kurumazuka D . Antihypertensive effect of angiotensin I-converting enzyme inhibitory peptides from a sesame protein hydrolysate in spontaneously hypertensive rats. Biosci Biotechnol Biochem. 2006; 70(5):1118-26. DOI: 10.1271/bbb.70.1118. View

He H, Chen X, Wu H, Sun C, Zhang Y, Zhou B . High throughput and rapid screening of marine protein hydrolysates enriched in peptides with angiotensin-I-converting enzyme inhibitory activity by capillary electrophoresis. Bioresour Technol. 2007; 98(18):3499-505. DOI: 10.1016/j.biortech.2006.11.036. View

10.

Saiga A, Iwai K, Hayakawa T, Takahata Y, Kitamura S, Nishimura T . Angiotensin I-converting enzyme-inhibitory peptides obtained from chicken collagen hydrolysate. J Agric Food Chem. 2008; 56(20):9586-91. DOI: 10.1021/jf072669w. View

11.

Sun L, Wang S, Gong X, Zhao M, Fu X, Wang L . Isolation, purification and characteristics of R-phycoerythrin from a marine macroalga Heterosiphonia japonica. Protein Expr Purif. 2008; 64(2):146-54. DOI: 10.1016/j.pep.2008.09.013. View

12.

Amado I, Vazquez J, Gonzalez P, Esteban-Fernandez D, Carrera M, Pineiro C . Identification of the major ACE-inhibitory peptides produced by enzymatic hydrolysis of a protein concentrate from cuttlefish wastewater. Mar Drugs. 2014; 12(3):1390-405. PMC: 3967217. DOI: 10.3390/md12031390. View

13.

Balti R, Bougatef A, Sila A, Guillochon D, Dhulster P, Nedjar-Arroume N . Nine novel angiotensin I-converting enzyme (ACE) inhibitory peptides from cuttlefish (Sepia officinalis) muscle protein hydrolysates and antihypertensive effect of the potent active peptide in spontaneously hypertensive rats. Food Chem. 2014; 170:519-25. DOI: 10.1016/j.foodchem.2013.03.091. View

14.

Harnedy P, OKeeffe M, FitzGerald R . Purification and identification of dipeptidyl peptidase (DPP) IV inhibitory peptides from the macroalga Palmaria palmata. Food Chem. 2014; 172:400-6. DOI: 10.1016/j.foodchem.2014.09.083. View

15.

Sato M, Hosokawa T, Yamaguchi T, Nakano T, Muramoto K, Kahara T . Angiotensin I-converting enzyme inhibitory peptides derived from wakame (Undaria pinnatifida) and their antihypertensive effect in spontaneously hypertensive rats. J Agric Food Chem. 2002; 50(21):6245-52. DOI: 10.1021/jf020482t. View