Current Perspectives on Antihypertensive Probiotics

Probiotics and Antimicrobial Proteins

Volumn 9, Issue 2, 2017, Pages 91-101

  Daliri, Eric Banan Mwine ^a   Lee, Byong H ^a,b   Oh, Deog H ^a  

^a Kangwon National University   (South Korea)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Cholesterol; Hypertension; Inflammation; Microbiota; Renin angiotensin system

Indexed keywords

ANTIHYPERTENSIVE AGENT; CHOLESTEROL; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; NITROGEN OXIDE; PROBIOTIC AGENT; REACTIVE OXYGEN METABOLITE;

AMINO ACID SEQUENCE; BIFIDOBACTERIUM LONGUM SUBSP. INFANTIS; BLOOD LEVEL; BLOOD PRESSURE; CARDIOVASCULAR RISK; CHOLESTEROL SYNTHESIS; CHRONIC INFLAMMATION; DYSBIOSIS; ENDOTHELIAL DYSFUNCTION; FERMENTED PRODUCT; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTENSION; INFLAMMATION; INTESTINE FLORA; LACTIC ACID BACTERIUM; LACTOBACILLUS; META ANALYSIS (TOPIC); MULTICENTER STUDY (TOPIC); NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; ANIMAL; DRUG EFFECTS; METABOLISM; MICROBIOLOGY; PATHOPHYSIOLOGY;

ANIMALS; ANTIHYPERTENSIVE AGENTS; BLOOD PRESSURE; CHOLESTEROL; GASTROINTESTINAL MICROBIOME; HUMANS; HYPERTENSION; PROBIOTICS; RENIN-ANGIOTENSIN SYSTEM;

EID: 85000542463     PISSN: 18671306     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12602-016-9241-y     Document Type: Review

References (121)

1. James P, Oparil S, Carter BL, Cushman WC et al (2014) Evidence-based guideline for the management of high blood pressure in adults: report from the panel members appointed to the Eighth Joint National Committee (JNC 8). JAMA 311(5):507–520
2. Hall JE, do Carmo JM, da Silva AA et al (2015) Obesity-induced hypertension: interaction of neurohumoral and renal mechanisms. Circ Res 116(6):991–1006
3. Stevens VJ, Corrigan SA, Obarzanek E, Bernauer E et al (1993) Weight loss intervention in phase 1 of the Trials of Hypertension Prevention. The TOHP Collaborative Research Group. Arch Intern Med, 1993 153(7):849–858
4. Stevens VJ, Obarzanek E, Cook NR et al (2001) Long-term weight loss and changes in blood pressure: results of the Trials of Hypertension Prevention, phase II. Ann Intern Med 134(1):1–11
5. Turnbull F, Blood Pressure Lowering Treatment Trialists’ Collaboration (2003) Blood pressure lowering treatment trialists, effects of different blood-pressure-lowering regimens on major cardiovascular events: results of prospectively-designed overviews of randomised trials. Lancet 362(9395):1527–1535
6. Gomez-Guzman M, Toral M, Romero M et al (2015) Antihypertensive effects of probiotics Lactobacillus strains in spontaneously hypertensive rats. Mol Nutr Food Res 59(11):2326–2336
7. Aburto NJ, Hanson S, Gutierrez H et al (2013) Effect of increased potassium intake on cardiovascular risk factors and disease: systematic review and meta-analyses. BMJ 346:f1378
8. Lye HS, Kuan CY, Ewe JA et al (2009) The improvement of hypertension by probiotics: effects on cholesterol, diabetes, renin, and phytoestrogens. Int J Mol Sci 10(9):3755–3775
9. Nelson RH (2013) Hyperlipidemia as a risk factor for cardiovascular disease. Prim Care 40(1):195–211
10. Majumder K, Wu J (2015) Molecular targets of antihypertensive peptides: understanding the mechanisms of action based on the pathophysiology of hypertension. Int J Mol Sci 16(1):256–283
11. Guang C, Phillips RD, Jiang B et al (2012) Three key proteases—angiotensin-I-converting enzyme (ACE), ACE2 and renin—within and beyond the renin-angiotensin system. Arch Cardiovasc Dis 105(6–7):373–385
12. Skidgel RA, Stanisavljevic S, Erdos EG (2006) Kinin- and angiotensin-converting enzyme (ACE) inhibitor-mediated nitric oxide production in endothelial cells. Biol Chem 387(2):159–165
13. Kuoppala A, Lindstedt KA, Saarinen J et al (2000) Inactivation of bradykinin by angiotensin-converting enzyme and by carboxypeptidase N in human plasma. Am J Physiol Heart Circ Physiol 278(4):H1069–H1074
14. Yang T, Santisteban MM, Rodriguez V et al (2015) Gut dysbiosis is linked to hypertension. Hypertension 65(6):1331–1340
15. Honour JW (2015) Historical perspective: gut dysbiosis and hypertension. Physiol Genomics 47(10):443–446
16. Yang G, Jiang Y, Yang W et al (2015) Effective treatment of hypertension by recombinant Lactobacillus plantarum expressing angiotensin converting enzyme inhibitory peptide. Microb Cell Factories 14:202
17. Khalesi S, Sun J, Buys N et al (2014) Effect of probiotics on blood pressure: a systematic review and meta-analysis of randomized, controlled trials. Hypertension 64(4):897–903
18. Aluko RE (2015) Antihypertensive peptides from food proteins. Annu Rev Food Sci Technol 6:235–262
19. Korhonen R, Korpela R, Saxelin M et al (2001) Induction of nitric oxide synthesis by probiotic Lactobacillus rhamnosus GG in J774 macrophages and human T84 intestinal epithelial cells. Inflammation 25(4):223–232
20. Tejada-Simon MV, Ustunol Z, Pestka JJ (1999) Ex vivo effects of lactobacilli, streptococci, and bifidobacteria ingestion on cytokine and nitric oxide production in a murine model. J Food Prot 62(2):162–169
21. Linsalata M, Russo F, Berloco P et al. (2005) Effects of probiotic bacteria (VSL#3) on the polyamine biosynthesis and cell proliferation of normal colonic mucosa of rats. In Vivo 19(6): 989–995.
22. Linsalata M, Russo F, Berloco P et al (2004) The influence of Lactobacillus breves on ornithine decarboxylase activity and polyamine profiles in Helicobacter pylori-infected gastric mucosa. Helicobacter 9(2):165–172
23. Kullisaar T, Zilmer M, Mikelsaar M et al (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72(3):215–224
24. Carroll IM, Andrus JM, Bruno-Bárcena JM et al (2007) Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am J Physiol Gastrointest Liver Physiol 293(4):G729–G738
25. Andrus JM, Bowen SW, Klaenhammer TR et al (2003) Molecular characterization and functional analysis of the manganese-containing superoxide dismutase gene (sodA) from Streptococcus thermophilus AO54. Arch Biochem Biophys 420(1):103–113
26. Xing J, Wang G, Zhang Q et al (2015) Determining antioxidant activities of lactobacilli cell-free supernatants by cellular antioxidant assay: a comparison with traditional methods. PLoS One 10(3):e0119058
27. Ahire JJ, Mokashe NU, Patil HJ et al (2013) Antioxidative potential of folate producing probiotic Lactobacillus helveticus CD6. J Food Sci Technol 50(1):26–34
28. Parvaneh K, Jamaluddin R, Karimi G et al (2014) Effect of probiotics supplementation on bone mineral content and bone mass density. ScientificWorldJournal 2014:595962
29. Vinderola G, Matar C, Perdigon G (2007) Milk fermentation products of L. helveticus R389 activate calcineurin as a signal to promote gut mucosal immunity. BMC Immunol 8:19
30. Resnick LM (1999) The role of dietary calcium in hypertension: a hierarchical overview. Am J Hypertens 12(1 Pt 1):99–112
31. Sakurai M, Stamler J, Miura K et al (2011) Relationship of dietary cholesterol to blood pressure: the INTERMAP study. J Hypertens 29(2):222–228
32. Stamler J, Caggiula A, Grandits GA, Kjelsberg M, Cutler JA (1996) Relationship to blood pressure of combinations of dietary macronutrients. Findings of the Multiple Risk Factor Intervention Trial (MRFIT). Circulation 94(10):2417–2423
33. Stamler J, Liu K, Ruth KJ et al (2002) Eight-year blood pressure change in middle-aged men: relationship to multiple nutrients. Hypertension 39(5):1000–1006
34. Hashimoto M, Eto M, Akishita M, Kozaki K, Ako J, Iijima K, Kim S, Toba K, Yoshizumi M, Ouchi Y (1999) Correlation between flow-mediated vasodilatation of the brachial artery and intima-media thickness in the carotid artery in men. Arterioscler Thromb Vasc Biol 19(11):2795–2800
35. Ferrara LA, Guida L, Iannuzzi R et al (2002) Serum cholesterol affects blood pressure regulation. J Hum Hypertens 16(5):337–343
36. Prakash S, Rodes L, Coussa-Charley M et al (2011) Gut microbiota: next frontier in understanding human health and development of biotherapeutics. Biologics 5:71–86
37. Larsen N, Vogensen FK, van den Berg FW et al (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5(2):e9085
38. Ley RE, Bäckhed F, Turnbaugh P et al (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102(31):11070–11075
39. Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A et al (2011) Effect of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium lactis on lipid profile in individuals with type 2 diabetes mellitus. J Dairy Sci 94(7):3288–3294
40. Anderson JW, Gilliland SE (1999) Effect of fermented milk (yogurt) containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. J Am Coll Nutr 18(1):43–50
41. Agerbaek M, Gerdes LU, Richelsen B (1995) Hypocholesterolaemic effect of a new fermented milk product in healthy middle-aged men. Eur J Clin Nutr 49(5):346–352
42. Bertolami MC, Faludi AA, Batlouni M (1999) Evaluation of the effects of a new fermented milk product (Gaio) on primary hypercholesterolemia. Eur J Clin Nutr 53(2):97–101
43. Jones ML, Martoni CJ, Prakash S (2012) Cholesterol lowering and inhibition of sterol absorption by Lactobacillus reuteri NCIMB 30242: a randomized controlled trial. Eur J Clin Nutr 66(11):1234–1241
44. Jones ML, Martoni CJ, Parent M et al (2012) Cholesterol-lowering efficacy of a microencapsulated bile salt hydrolase-active Lactobacillus reuteri NCIMB 30242 yoghurt formulation in hypercholesterolaemic adults. Br J Nutr 107(10):1505–1513
45. Ishimwe N, Daliri EB, Lee BH et al (2015) The perspective on cholesterol-lowering mechanisms of probiotics. Mol Nutr Food Res 59(1):94–105
46. Lye H, Rahmat-Ali G, Liong M (2010) Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. Int Dairy J 20:6
47. Huang Y, Wang X, Wang J, Wu F, Sui Y, Yang L, Wang Z (2013) Lactobacillus plantarum strains as potential probiotic cultures with cholesterol-lowering activity. J Dairy Sci 96(5):2746–2753
48. Chiang JY (2013) Bile acid metabolism and signaling. Compr Physiol 3(3):1191–1212
49. Lye HS, Rusul G, Liong MT (2010) Removal of cholesterol by lactobacilli via incorporation and conversion to coprostanol. J Dairy Sci 93(4):1383–1392
50. Marcil V, Delvin E, Garofalo C, Levy E (2003) Butyrate impairs lipid transport by inhibiting microsomal triglyceride transfer trotein in caco-2 cells. J Nutr 133:4
51. Ooi LG, Ahmad R, Yuen KH et al (2010) Lactobacillus gasseri [corrected] CHO-220 and inulin reduced plasma total cholesterol and low-density lipoprotein cholesterol via alteration of lipid transporters. J Dairy Sci 93(11):5048–5058
52. Remagni MC, Paladino M, Locci F et al (2013) Cholesterol removal capability of lactic acid bacteria and related cell membrane fatty acid modifications. Folia Microbiol (Praha) 58(6):443–449
53. Ferrier KE, Muhlmann MH, Baguet JP et al (2002) Intensive cholesterol reduction lowers blood pressure and large artery stiffness in isolated systolic hypertension. J Am Coll Cardiol 39(6):1020–1025
54. Buchwald H, Boen JR, Williams SE, Nguyen PA, Matts JP (2003) Blood pressure, weight, and cholesterol. J Am Coll Cardiol 41:1
55. Gurantz D, Cowling RT, Varki N, Frikovsky E, Moore CD, Greenberg BH (2005) IL-1β and TNF-α upregulate angiotensin II type 1 (AT 1) receptors on cardiac fibroblasts and are associated with increased AT1 density in the post-MI heart. J Mol Cell Cardiol 38(3):505–515
56. Hoch NE, Guzik TJ, Chen W et al (2009) Regulation of T-cell function by endogenously produced angiotensin II. Am J Physiol Regul Integr Comp Physiol 296(2):R208–R216
57. Marvar PJ, Vinh A, Thabet S et al (2012) T lymphocytes and vascular inflammation contribute to stress-dependent hypertension. Biol Psychiatry 71(9):774–782
58. Bautista LE, Vera LM, Arenas IA, Gamarra G (2005) Independent association between inflammatory markers (C-reactiveprotein, interleukin-6, and TNF-alpha) and essential hypertension. J Hum Hypertens 19(19):5
59. Lakoski SG, Cushman M, Palmas W, Blumenthal R, D’Agostino RB Jr (1869-1874) Herrington DM (2005) the relationship between blood pressure and C-reactive protein in the multi-ethnic study of atherosclerosis (MESA). J Am Coll Cardiol 46:5
60. Sesso HD, Buring JE, Rifai N et al (2003) C-reactive protein and the risk of developing hypertension. JAMA 290(22):2945–2951
61. Niskanen L, Laaksonen D, Nyyssönen K, Punnonen K, Valkonen VP, Fuentes R, Tuomainen TP, Salonen R, Salonen JT (2004) Inflammation, abdominal obesity, and smoking as predictors of hypertension. Hypertension 44(6):6
62. Ghanem FA, Movahed A (2007) Inflammation in high blood pressure: a clinician perspective. J Am Soc Hypertens 1(2):113–119
63. Yu B, Shahid M, Egorina EM, Sovershaev MA et al (2010) Endothelial dysfunction enhances vasoconstriction due to scavenging of nitric oxide by a hemoglobin-based oxygen carrier. Anesthesiology 112(3):586–594
64. Guzik TJ, Hoch NE, Brown KA et al (2007) Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 204(10):2449–2460
65. Jurewicz M, McDermott DH, Sechler JM et al (2007) Human T and natural killer cells possess a functional renin-angiotensin system: further mechanisms of angiotensin II-induced inflammation. J Am Soc Nephrol 18(4):1093–1102
66. Trott DW, Harrison DG (2014) The immune system in hypertension. Adv Physiol Educ 38(1):20–24
67. Jiang W, Wu N, Wang X et al (2015) Dysbiosis gut microbiota associated with inflammation and impaired mucosal immune function in intestine of humans with non-alcoholic fatty liver disease. Sci Rep 5:8096
68. Fallucca F, Porrata C, Fallucca S et al (2014) Influence of diet on gut microbiota, inflammation and type 2 diabetes mellitus. First experience with macrobiotic Ma-Pi 2 diet. Diabetes Metab Res Rev 30(Suppl 1):48–54
69. Shaw KA, Bertha M, Hofmekler T et al (2016) Dysbiosis, inflammation, and response to treatment: a longitudinal study of pediatric subjects with newly diagnosed inflammatory bowel disease. Genome Med 8(1):75
70. Gevers D, Kugathasan S, Denson LA et al (2014) The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe 15(3):382–392
71. Konieczna P, Akdis CA, Quigley EM et al (2012) Portrait of an immunoregulatory Bifidobacterium. Gut Microbes 3(3):261–266
72. Corthay A, Miyara M, Costantino CM (2009) How do regulatory T cells work? Scand J Immunol 70(4):490–500
73. Sakaguchi S, Miyara M, Costantino CM et al (2010) FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 10(7):490–500
74. O'Mahony C, Scully P, O'Mahony D et al (2008) Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog 4(8):e1000112
75. Konieczna P, Groeger D, Ziegler M et al (2012) Bifidobacterium infantis 35624 administration induces Foxp3 T regulatory cells in human peripheral blood: potential role for myeloid and plasmacytoid dendritic cells. Gut 61(3):354–366
76. Sugawara G, Nagino M, Nishio H, Ebata T, Takagi K, Asahara T, Nomoto K, Nimura Y Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg 244:8
77. Furrie E, Macfarlane S, Kennedy A, Cummings JH, Walsh SV, O’neil DA, Macfarlane GT (2005) Synbiotic therapy (Bifidobacterium longum/synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: a randomised controlled pilot trial. Gut 54:8
78. Chen L, Liu W, Li Y et al (2013) Lactobacillus acidophilus ATCC 4356 attenuates the atherosclerotic progression through modulation of oxidative stress and inflammatory process. Int Immunopharmacol 17(1):108–115
79. Rong J, Zheng H, Liu M et al (2015) Probiotic and anti-inflammatory attributes of an isolate Lactobacillus helveticus NS8 from Mongolian fermented koumiss. BMC Microbiol 15:196
80. Mirpuri J, Sotnikov I, Myers L et al (2012) Lactobacillus rhamnosus (LGG) regulates IL-10 signaling in the developing murine colon through upregulation of the IL-10R2 receptor subunit. PLoS One 7(12):e51955
81. Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, Järvenpää S, Kautiainen H, Julkunen I, Vapaatalo H, Korpela R (2008) Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J Gastroenterol 14(13):7
82. Koyama M, Naramoto K, Nakajima T et al (2013) Purification and identification of antihypertensive peptides from fermented buckwheat sprouts. J Agric Food Chem 61(12):3013–3021
83. Ruiz-Gimenez P, Ibáñez A, Salom JB et al (2010) Antihypertensive properties of lactoferricin B-derived peptides. J Agric Food Chem 58(11):6721–6727
84. García-Tejedor A, Sánchez-Rivera L, Castelló-Ruiz M, Recio I, Salom JB, Manzanares P (2014) Novel antihypertensive lactoferrin-derived peptides produced by Kluyveromyces marxianus: gastrointestinal stability profile and in vivo angiotensin I-converting enzyme (ACE) inhibition. J Agric Food Chem 62(7):1609–1616
85. Cook NR, Cohen J, Hebert PR et al (1995) Implications of small reductions in diastolic blood pressure for primary prevention. Arch Intern Med 155(7):701–709
86. Chakrabarti S, Jahandideh F, Wu J (2014) Food-derived bioactive peptides on inflammation and oxidative stress. Biomed Res Int 2014:608979
87. Gannon TH, Eby TL (1990) Angioedema from angiotensin converting enzyme inhibitors: a cause of upper airway obstruction. Laryngoscope 100(11):1156–1160
88. Israili ZH, Hall WD (1992) Cough and angioneurotic edema associated with angiotensin-converting enzyme inhibitor therapy. A review of the literature and pathophysiology. Ann Intern Med 117(3):234–242
89. Liu M, Bayjanov JR, Renckens B et al (2010) The proteolytic system of lactic acid bacteria revisited: a genomic comparison. BMC Genomics 11:36
90. Broadbent JR, Cai H, Larsen RL et al (2011) Genetic diversity in proteolytic enzymes and amino acid metabolism among Lactobacillus helveticus strains. J Dairy Sci 94(9):4313–4328
91. Pastar I, Tonic I, Golic N et al (2003) Identification and genetic characterization of a novel proteinase, PrtR, from the human isolate Lactobacillus rhamnosus BGT10. Appl Environ Microbiol 69(10):5802–5811
92. Fernandez-Espla MD, Rul F (1999) PepS from Streptococcus thermophilus. A new member of the aminopeptidase T family of thermophilic bacteria. Eur J Biochem 263(2):502–510
93. Savijoki K, Ingmer H, Varmanen P (2006) Proteolytic systems of lactic acid bacteria. Appl Microbiol Biotechnol 71(4):394–406
94. Mozzi F, Raya RlR, Vignolo, G.M (2010) Biotechnology of lactic acid bacteria: novel applications., Ames, Iowa: Wiley-Blackwell. xii, 393
95. Wu J, Aluko RE, Nakai S (2006) Structural requirements of angiotensin I-converting enzyme inhibitory peptides: quantitative structure-activity relationship study of di- and tripeptides. J Agric Food Chem 54(3):732–738
96. Vermeulen N, Pavlovic M, Ehrmann MA et al (2005) Functional characterization of the proteolytic system of Lactobacillus sanfranciscensis DSM 20451T during growth in sourdough. Appl Environ Microbiol 71(10):6260–6266
97. Fekete AA, Givens DI, Lovegrove JA (2015) Casein-derived lactotripeptides reduce systolic and diastolic blood pressure in a meta-analysis of randomised clinical trials. Nutrients 7(1):659–681
98. Manzanares P, Salom JB, García-Tejedor A et al (2015) Unraveling the mechanisms of action of lactoferrin-derived antihypertensive peptides: ACE inhibition and beyond. Food Funct 6(8):2440–2452
99. Varmanen P, Rantanen T, Palva A et al (1998) Cloning and characterization of a prolinase gene (pepR) from Lactobacillus rhamnosus. Appl Environ Microbiol 64(5):1831–1836
100. Navidghasemizad S, Takala TM, Alatossava T et al (2013) Proline iminopeptidase PepI overexpressing Lactobacillus casei as an adjunct starter in Edam cheese. Bioengineered 4(6):408–412
101. Sanz Y, Toldra F (2001) Purification and characterization of an X-prolyl-dipeptidyl peptidase from Lactobacillus sakei. Appl Environ Microbiol 67(4):1815–1820
102. Habibi-Najafi MB, Lee BH (1994) Purification and characterization of X-prolyl dipeptidyl peptidase from Lactobacillus casei subsp. casei LLG. Appl Microbiol Biotechnol 42(2–3):280–286
103. Cicero AF, Gerocarni B, Laghi L et al (2011) Blood pressure lowering effect of lactotripeptides assumed as functional foods: a meta-analysis of current available clinical trials. J Hum Hypertens 25(7):425–436
104. Cicero AF, Aubin F, Azais-Braesco V et al (2013) Do the lactotripeptides isoleucine-proline-proline and valine-proline-proline reduce systolic blood pressure in European subjects? A meta-analysis of randomized controlled trials. Am J Hypertens 26(3):442–449
105. Rao S, Su Y, Li J et al (2009) Design and expression of recombinant antihypertensive peptide multimer gene in Escherichia coli BL21. J Microbiol Biotechnol 19(12):1620–1627
106. Rao S, Xu Z, Su Y et al (2011) Cloning, soluble expression, and production of recombinant antihypertensive peptide multimer (AHPM-2) in Escherichia coli for bioactivity identification. Protein Pept Lett 18(7):699–706
107. Huang L, Ma H, Li Y, Li S (2012) Antihypertensive activity of recombinant peptide IYPR expressed in Escherichia coli as inclusion bodies. Protein Expr Purif 83(1):15–20
108. Jung WK, Mendis E, Je JY, Park PJ, Son BW, Kim CK, Choi YK, Kim SK (2006) Angiotensin I-converting enzyme inhibitory peptide from yellowfin sole (Limanda aspera) frame protein and its antihypertensive effect in spontaneously hypertensive rats. Foodchem 94(1):6
109. Seppo L, Jauhianen T, Poussa T, Korpela R (2003) A fermented milk high in bioactive peptides has a blood pressure-lowering effect in hypertensive subjects. Am J Clin Nutr 77:5
110. Chen Y, Liu W, Xue J et al (2014) Angiotensin-converting enzyme inhibitory activity of Lactobacillus helveticus strains from traditional fermented dairy foods and antihypertensive effect of fermented milk of strain H9. J Dairy Sci 97(11):6680–6692
111. Dong JY, Szeto IM, Makinen K et al (2013) Effect of probiotic fermented milk on blood pressure: a meta-analysis of randomised controlled trials. Br J Nutr 110(7):1188–1194
112. Tuomilehto J, Lindström J, Hyyrynen J et al (2004) Effect of ingesting sour milk fermented using Lactobacillus helveticus bacteria producing tripeptides on blood pressure in subjects with mild hypertension. J Hum Hypertens 18(11):795–802
113. Aihara K, Kajimoto O, Hirata H et al (2005) Effect of powdered fermented milk with Lactobacillus helveticus on subjects with high-normal blood pressure or mild hypertension. J Am Coll Nutr 24(4):257–265
114. Mizushima S, Ohshige K, Watanabe J et al (2004) Randomized controlled trial of sour milk on blood pressure in borderline hypertensive men. Am J Hypertens 17(8):701–706
115. Inoue K, Shirai T, Ochiai H, Kasao M, Hayakawa K, Kimura M, Sansawa H (2003) Blood-pressure-lowering effect of a novel fermented milk containing big gamma-aminobutyric acid (GABA) in mild hypertensives. Eur J Clin Nutr 57:490–495
116. Hariri M, Salehi R, Feizi A et al (2015) The effect of probiotic soy milk and soy milk on anthropometric measures and blood pressure in patients with type II diabetes mellitus: a randomized double-blind clinical trial. ARYA Atheroscler 11(Suppl 1):74–80
117. Hata Y, Yamamoto M, Ohni M et al (1996) A placebo-controlled study of the effect of sour milk on blood pressure in hypertensive subjects. Am J Clin Nutr 64(5):767–771
118. Nakamura Y, Yamamoto M, Ohni M et al (1995) Antihypertensive effect of sour milk and peptides isolated from it that are inhibitors to angiotensin I-converting enzyme. J Dairy Sci 78(6):1253–12537
119. Jauhiainen T, Vapaatalo H, Poussa T et al (2005) Lactobacillus helveticus fermented milk lowers blood pressure in hypertensive subjects in 24-h ambulatory blood pressure measurement. Am J Hypertens 18(12 Pt 1):1600–1605
120. Kawase M, Hashimoto H, Hosoda M, Morita H, Hosono A (2000) Effect of administration of fermented milk containing whey protein concentrate to rats and healthy men on serum lipids and blood pressure. J Dairy Sci 83(2):10
121. Sharafedtinov KK, Plotnikova OA, Alexeeva RI et al (2013) Hypocaloric diet supplemented with probiotic cheese improves body mass index and blood pressure indices of obese hypertensive patients--a randomized double-blind placebo-controlled pilot study. Nutr J 12:138