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Planta Med 2015; 81(02): 123-129
DOI: 10.1055/s-0034-1383409
DOI: 10.1055/s-0034-1383409
Biological and Pharmacological Activity
Original Papers
Identification of Angiotensin-Converting Enzyme Inhibitory Proteins from Mycelium of Pleurotus pulmonarius (Oyster Mushroom)
Authors
Further Information
Publication History
received 24 May 2014
revised 09 November 2014
accepted 22 November 2014
Publication Date:
15 January 2015 (online)
Abstract
Pleurotus pulmonarius (grey oyster mushroom) has been acknowledged as a recuperative agent for many diseases in addition to its recognition as a nutritious provision. We performed a study on P. pulmonarius mycelium for an antihypertensive effect via the angiotensin-converting enzyme inhibitory activity. The preliminary assay on the mycelial water extract demonstrated that the angiotensin-converting enzyme inhibitory activity had an IC50 value of 720 µg/mL. Further protein purifications via ammonium sulphate precipitation and RP-HPLC resulted in 60× stronger angiotensin-converting enzyme inhibitory activity than that of the mycelial water extract (IC50 = 12 µg/mL). Protein identification and characterisation by MALDI-TOF/TOF, later corroborated by LC-MS/MS, indicated three proteins that are responsible for the blood pressure lowering effects via different mechanisms: serine proteinase inhibitor-like protein, nitrite reductase-like protein, and DEAD/DEAH box RNA helicase-like protein.
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References
- 1 Hoyert DL, Xu J. Death: preliminary data for 2011. Natl Vital Stat Rep 2012; 61: 1-51
- 2 World Health Organization. Global Status Report on noncommunicable Diseases 2010. Geneva: WHO Press; 2011
- 3 Barbosa-Filho JM, Martins VKM, Rabelo LA, Moura MD, Silva MS, Cunha EVL, Souza MFV, Almeida RM, Medeiros IA. Natural product inhibitors of the angiotensin converting enzyme (ACE). A review between 1980–2000. Rev Bras Farmacogn 2006; 16: 421-446
- 4 Atlas SA. The rennin-angiotensin-aldosteron system: pathophysiological role and pharmacologic inhibition. J Manag Care Pharm 2007; 13 (Suppl.) S9-S20
- 5 Kim JH, Lee DH, Jeong SC, Chung KS, Lee JS. Characterization of antihypertensive angiotensin I-converting enzyme inhibitor from Saccharomyces cerevisiae . J Microbiol Biotechnol 2004; 14: 1318-1323
- 6 Wong J, Patel RA, Kowey PR. The clinical use of angiotensin-converting enzyme inhibitors. Progr Cardiovasc Dis 2004; 47: 116-130
- 7 Reid JL. From kinetics to dynamics: are there differences between ACE inhibitors?. Eur Heart J Suppl 1997; 18: E14-E18
- 8 Lee JE, Bae IY, Lee HG, Yang CB. Tyr-Pro-Lys, an angiotensin I-converting enzyme inhibitory peptide derived from broccoli (Brassica oleracea Italica). Food Chem 2006; 99: 143-148
- 9 Yang Y, Marczak ED, Yokoo M, Usui H, Yoshikawa M. Isolation and antihypertensive effect of angiotensin I-converting enzyme (ACE) inhibitory peptides from spinach Rubisco. J Agr Food Chem 2003; 51: 4897-4902
- 10 Ni H, Li L, Liu G, Hu SQ. Inhibition mechanism and model of angiotensin I-converting enzyme (ACE) inhibitory hexapeptide from yeast (Saccharomyces cerevisiae). PLoS One 2012; 7: e37077
- 11 Ando T, Okada S, Uchida I, Hemmi K, Nishikawa M, Tsurumi Y, Fujie A, Yoshida K, Okuhara M. WF-10129, a novel angiotensin converting enzyme inhibitor produced by a fungus, Doratomyces putredinis . J Antibiot 1987; 40: 468-475
- 12 Prasanna R, Nandhini B, Praveesh BV, Angayarkanni J, Palaniswamy M. Novel angiotensin converting enzyme inhibitor from Aspergillus sp. by solid state fermentation. Int J Pharm Pharm Sci 2012; 4: 371-377
- 13 Lijun W, Saito M, Tatsumi E, Lite L. Antioxidative and angiotensin I-converting enzyme inhibitory activities of sufu (fermented tofu) extracts. JARQ-JPN Agr Res Q 2003; 37: 129-132
- 14 FitzGerald R, Meisel H. Milk protein-derived peptide inhibitors of angiotensin-I-converting enzyme. Br J Nutr 2000; 84 (Suppl.) S33-S37
- 15 Kong WS. Descriptions of commercially important Pleurotus species. In: Oyster mushroom cultivation (Mushroom growersʼ handbook, 1). Part II. Oyster mushrooms. Seoul: Heineart Incorporation; 2004: 67-74
- 16 Shahid MN, Abbasi NA, Saleem N. Effect of different methods of compost preparation and lime concentration on the yield of Pleurotus sajor-caju . Int J Agr Biol 2006; 8: 129-131
- 17 Ng TB. Peptides and proteins from fungi. Peptides 2004; 25: 1055-1073
- 18 Kanagasabapathy G, Malek SNA, Kuppusamy UR, Vikineswary S. Chemical composition and antioxidant properties of extracts of fresh fruiting bodies of Pleurotus sajor-caju (Fr.) Singer. J Agr Food Chem 2011; 59: 2618-2626
- 19 Gregori A, Svagelj M, Pohleven F. Cultivation technique and medicinal properties of Pleurotus sp. Food Technol Biotechnol 2007; 45: 236-247
- 20 Nitha B, Meera CR, Janardhanan KK. Anti-inflammatory and antitumour activities of cultured mycelium of morel mushroom, Morchella esculenta . Curr Sci 2007; 92: 235-239
- 21 Dundar A, Okumus V, Ozdemir S, Yildiz A. Antioxidant properties of cultured mycelia from four Pleurotus species produced in submerged medium. Int J Food Prop 2013; 16: 1105-1116
- 22 Patel PD, Patel NJ, Patel DD, Patel RK. In-vivo evaluation of Pleurotus sajorcaju mycelium extract for anti-inflammatory activity. Pharmacologyonline 2011; 2: 784-789
- 23 Confortin FG, Marchetto R, Bettin F, Camassola M, Salvador M, Dillon AJP. Production of Pleurotus sajor-caju strain PS-2001 biomass in submerged culture. J Ind Microbiol Biotechnol 2008; 35: 1149-1155
- 24 Yan PS, Gao XJ. Inhibitory activity of extracts from mycelia materials of several mushrooms on the angiotensin I-converting enzyme. Adv Mater Res 2013; 610–613: 3541-3544
- 25 Wu J, Aluko RE, Naka S. Structural requirements of Angiotensin I-converting enzyme inhibitory peptides: quantitative structure-activity relationship of study of di- and tripeptides. J Agr Food Chem 2006; 54: 732-738
- 26 Choi HS, Cho HY, Yang HC, Ra KS, Suh HJ. Angiotensin I-converting enzyme inhibitor from Grifola frondosa . Food Res Int 2001; 34: 177-182
- 27 Lee DH, Kim JH, Park JS, Choi YJ, Lee JS. Isolation and characterization of a novel angiotensin I-converting enzyme inhibitory peptide derived from the edible mushroom Tricholoma giganteum . Peptides 2004; 25: 621-627
- 28 Koo KC, Lee DH, Kim JH, Yu HE, Park JS, Lee JS. Production and characterisation of antihypertensive angiotensin I-converting enzyme inhibitor from Pholiota adiposa . J Microbiol Biotechnol 2006; 16: 757-763
- 29 Jang JH, Jeong SC, Kim JH, Lee YH, Ju YC, Lee JS. Characterisation of new antihypertensive angiotensin I-converting enzyme inhibitory peptide from Pleurotus cornucopiae . Food Chem 2011; 127: 412-418
- 30 You LR, Chen CM, Yeh TS, Tsai TY, Mai RT, Lin CH, Lee YHW. Hepatitis C virus core protein interacts with cellular putative RNA helicase. J Virol 1999; 7: 2841-2853
- 31 Petsko GA, Ringe D. From sequence to function: Case study in structural and functional genomics. In: Lawrence E, Robertson M, editors Protein structure and function. London: New Science Press Ltd.; 2004: 130-164
- 32 Sahni A, Wang N, Alexis JD. UAP56 is an important regulator of protein synthesis and growth in cardiomyocytes. Biochem Biophys Res Commun 2010; 393: 106-110
- 33 Liu ZP, Olson EN. Suppression of proliferation and cardiomyocyte hypertrophy by CHAMP, a cardiac-specific RNA helicase. Proc Natl Acad Sci U S A 2002; 99: 2043-2048
- 34 Frey N, Olsen EN. Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol 2003; 65: 45-79
- 35 Mohamad Ansor N, Abdullah N, Aminudin N. Anti-angiotensin converting enzyme (ACE) proteins from mycelia of Ganoderma lucidum (Curtis) P. Karst. BMC Compl Alternative Med 2013; 13: 256-264
- 36 Zhang Y, Palla M, Sun A, Liao JC. Identification of unique interactions between the flexible linker and the RecA-like domains of DEAD-box helicase Mss116. J Phys Condens Matter 2013; 25: 1-8
- 37 Kovacsovics M, Martinon F, Micheau O, Bodmer JL, Hofmann K, Tschopp J. Overexpression of helicard, a CARD-containing helicase cleaved during apoptosis, accelerates DNA degradation. Curr Biol 2002; 12: 838-843
- 38 Paniagua OA, Bryant MB, Panza JO. Role of endothelial nitric oxide in shear stress-induced vasodilation of human microvasculature: diminished activity in hypertensive and hypercholesterolemic patients. Circulation 2001; 103: 1752-1758
- 39 Gladwin MT, Raat NJ, Shiva S, Dezfulian C, Hogg N, Kim-Shapiro DB, Patel RP. Nitrite as a vascular endocrine nitric oxide reservoir that contributes to hypoxic signaling, cytoprotection, and vasodilation. Am J Physiol Heart Circ Physiol 2006; 291: 2026-2035
- 40 Ghosh SM, Kapil V, Fuentes-Calvo I, Bubb KJ, Pearl V, Milsom AB, Khambata R, Maleki-Toyserkani S, Yousuf M, Benjamin N, Webb AJ, Caulfield MJ, Hobbs AJ, Ahluwalia A. Enhanced vasodilator activity of nitrite in hypertension: critical role for erythrocytic xanthine oxidoreductase and translational potential. Hypertension 2013; 61: 1091-1102
- 41 Imanishi T, Goto M, Akasaka T. The rennin-angiotensin-aldosteron system as a therapeutic target for endothelial dysfunction. Vasc Dis Prev 2009; 6: 65-74
- 42 Prodouz KN, Garrett RH. Neurospora crassa NAD(P)H-nitrite reductase. Studies on its composition and structure. J Biol Chem 1981; 28: 9711-9717
- 43 Bowsher CG, Emes MJ, Cammack R, Hucklesby DP. Purification and properties of nitrite reductase from roots of pea (Pisum sativum cv. Meteor). Planta 1988; 75: 334-340
- 44 Hjelmeland LM, Chrambach A. Electrophoresis and electrofocusing in detergent containing media: a discussion of the basic concepts. Electrophoresis 1981; 2: 1-11
- 45 Steensma E, Gordon E, Oster LM, Ferguson SJ, Hajdu J. Heme ligation and conformational plasticity in the isolated c domain of cytochrome cd1 nitrite reductase. J Biol Chem 2001; 276: 5846-5855
- 46 Fear G, Komarnytsky S, Raskin I. Protease inhibitors and their peptidomimetic derivatives as potential drugs. Pharmacol Ther 2007; 113: 354-368
- 47 Richard V, Hurel-Merle S, Scalbert E, Ferry G, Lallemand F, Bessou JP, Thuillez C. Functional evidence for a role of vascular chymase in the production of angiotensin II in isolated human arteries. Circulation 2001; 104: 750-752
- 48 Erjavac J, Kos J, Ravnikar M, Dreo T, Sabotic J. Proteins of higher fungi – from forest to application. Trends Biotechnol 2012; 30: 259-273
- 49 Dohmae N, Takio K, Tsumuraya Y, Hashimoto Y. The complete amino acid sequences of two serine proteinase inhibitors from the fruiting bodies of a basidiomycetes, Pleurotus ostreatus . Arch Biochem Biophys 1995; 316: 498-506
- 50 Odani S, Tomiga K, Kondou S, Hori H, Koide T, Hara S, Isemura M, Tsunasawa S. The inhibitory properties and primary structure of a novel serine proteinase inhibitor from the fruiting body of the basidiomycete, Lentinus edodes . Eur J Biochem 1999; 262: 915-923
- 51 Wolny A, Clozel JP, Rein J, Mory P, Vogt P, Turino M, Kiowski W, Fischli W. Functional and biochemical analysis of angiotensin II-forming pathways in the human heart. Circ Res 1997; 80: 219-227
- 52 Petrov V, Fagard R, Lijnen P. Effect of protease inhibitors on angiotensin converting enzyme activity in human T-lymphocytes. Am J Hypertens 2000; 13: 535-539
- 53 Dojindo Laboratories. ACE Kit – WST (100 tests) technical manual. Available at. http://www.dojindo.eu.com/TechnicalManual/Manual_A502.pdf Accessed August 23, 2013
- 54 Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-685