Chronic administration of the probiotic kefir improves the endothelial function in spontaneously hypertensive rats

Journal of Translational Medicine

Volumn 13, Issue 1, 2015, Pages

  Friques, Andreia G F ^a   Arpini, Clarisse M ^a   Kalil, Ieda C ^a   Gava, Agata L ^b   Leal, Marcos A ^c   Porto, Marcella L ^c,d   Nogueira, Breno V ^c   Dias, Ananda T ^c   Andrade, Tadeu U ^a   Pereira, Thiago Melo C ^a,d   Meyrelles, Silvana S ^c   Campagnaro, Bianca P ^a   Vasquez, Elisardo C ^a,c  

^a UNIVERSIDADE VILA VELHA   (Brazil)

^b MCMASTER UNIVERSITY   (Canada)

^c FEDERAL UNIVERSITY OF ESPÍRITO SANTO   (Brazil)

^d Institute of Education   (Brazil)

Author keywords

Endothelial dysfunction; Kefir; Oxidative stress; Probiotics; Spontaneously hypertensive rat

Indexed keywords

ACETYLCHOLINE; KEFIR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; PROBIOTIC AGENT;

ACETOBACTER; ACETOBACTER ACETI; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIHYPERTENSIVE ACTIVITY; AREA UNDER THE CURVE; ARTICLE; BLOOD VESSEL REACTIVITY; CANDIDA FAMATA; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL PROGENITOR CELL; ENTEROCOCCUS FAECIUM; ENZYME INHIBITION; ESSENTIAL HYPERTENSION; FLOW CYTOMETRY; LACTOBACILLUS; LACTOBACILLUS DELBRUECKII DELBRUECKII; LACTOBACILLUS FERMENTUM; LACTOBACILLUS FRUCTIVORANS; LACTOBACILLUS KEFIRANOFACIENS; LEUCONOSTOC; LONG TERM CARE; MALE; NONHUMAN; PICHIA KUDRIAVZEVII; RAT; SCANNING ELECTRON MICROSCOPY; SPONTANEOUSLY HYPERTENSIVE RAT; TACHYCARDIA; VASCULAR ENDOTHELIUM; VASCULAR RING; VASODILATATION; ANIMAL; FERMENTED MILK PRODUCT; HYPERTENSION; PATHOPHYSIOLOGY;

ANIMALS; CULTURED MILK PRODUCTS; ENDOTHELIUM, VASCULAR; FLOW CYTOMETRY; HYPERTENSION; MICROSCOPY, ELECTRON, SCANNING; PROBIOTICS; RATS; RATS, INBRED SHR;

EID: 84951971583     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-015-0759-7     Document Type: Article

References (47)

1. Fraga-Silva RA, Costa-Fraga FP, Murça TM, Moraes PL, Martins Lima A, Lautner RQ, Castro CH, Soares CM, Borges CL, Nadu AP, Oliveira ML, Shenoy V, Katovich MJ, Santos RA, Raizada MK, Ferreira AJ. Angiotensin-converting enzyme 2 activation improves endothelial function. Hypertension. 2013;61(6):1233-8. doi: 10.1161/HYPERTENSIONAHA.111.00627.
2. Balarini CM, Leal MA, Gomes IB, Pereira TMC, Gava AL, Meyrelles SS, Vasquez EC. Sildenafil restores endothelial function in the apolipoprotein E knockout mouse. J Transl Med. 2013;11:3. doi: 10.1186/1479-5876-11-3.
3. Dias AT, Cintra AS, Frossard JC, Palomino Z, Casarini DE, Gomes I, Balarini CM, Gava AL, Campagnaro BP, Pereira TMC, Meyrelles SS, Vasquez EC. Inhibition of phosphodiesterase 5 restores endothelial function in renovascular hypertension. J Transl Med. 2014;12:35. doi: 10.1186/s12967-014-0250-x.
4. Meyrelles SS, Peotta VA, Pereira TMC, Vasquez EC. Endothelial dysfunction in the apolipoprotein E-deficient mouse: insights into the influence of diet, gender and aging. Lipids Health Dis. 2011;10:211. doi: 10.1186/1476-511X-10-211.
5. Félétou M, Vanhoutte PM. Endothelial dysfunction: a multifaceted disorder (The Wiggers Award Lecture). Am J Physiol Heart Circ Physiol. 2006;291:H985-1002.
6. Touyz RM, Schiffrin EL. Reactive oxygen species in vascular biology: implications in hypertension. Histochem Cell Biol. 2004;122:339-52. doi: 10.1007/s00418-004-0696-7.
7. Astrup A. Yogurt and dairy product consumption to prevent cardiometabolic diseases: epidemiologic and experimental studies. Am J Clin Nutr. 2014;99(5 Suppl):1235S-42S. doi: 10.3945/ajcn.113.073015.
8. Turpeinen AM, Ehlers PI, Kivimäki AS, Järvenpää S, Filler I, Wiegert E, Jähnchen E, Vapaatalo H, Korpela R, Wagner F. Ile-Pro-Pro and Val-Pro-Pro tripeptide-containing milk product has acute blood pressure lowering effects in mildly hypertensive subjects. Clin Exp Hypertens. 2011;33(6):388-96. doi: 10.3109/10641963.2010.549267.
9. Jakala P, Pere E, Lehtinen R, Turpeinen A, Korpela R, Vapaatalo H. Cardiovascular activity of milk casein-derived tripeptides and plant sterols in spontaneously hypertensive rats. J Physiol Pharmacol. 2009;60(4):11-20.
10. Lopitz-Otsoa F, Rementeria A, Elguezabal N, Garaizar J. Kefir: a symbiotic yeasts-bacteria community with alleged healthy capabilities. Rev Iberoam Micol. 2006;23(2):67-74.
11. Yener AU, Sehitoglu MH, Ozkan MT, Bekler A, Ekin A, Cokkalender O, Deniz M, Sacar M, Karaca T, Ozcan S, Kurt T. Effects of kefir on ischemia-reperfusion injury. Eur Rev Med Pharmacol Sci. 2015;19(5):887-96.
12. Magalhães KT, de Melo Pereira GV, Campos CR, Dragone G, Schwan RF. Brazilian kefir: structure, microbial communities and chemical composition. Braz J Microbiol. 2011;42(2):693-702. doi: 10.1590/S1517-838220110002000034.
13. Lu M, Wang X, Sun G, Qin B, Xiao J, Yan S, Pan Y, Wang Y. Fine structure of Tibetan kefir grains and their yeast distribution, diversity, and shift. PLoS One. 2014;9(6):e101387. doi: 10.1371/journal.pone.0101387.
14. Jauhiainen T, Vapaatalo H, Poussa T, Kyronpalo S, Rasmussen M, Korpela R. Lactobacillus helveticus fermented milk lowers blood pressure in hypertensive subjects in 24-h ambulatory blood pressure measurement. Am J Hypertens. 2005;18:1600-5. doi: 10.1016/j.amjhyper.2005.06.006.
15. Kanbak G, Uzuner K, Kuşat Ol K, Oğlakçi A, Kartkaya K, Şentürk H. Effect of kefir and low-dose aspirin on arterial blood pressure measurements and renal apoptosis in unhypertensive rats with 4 weeks salt diet. Clin Exp Hypertens. 2014;36(1):1-8. doi: 10.3109/10641963.2013.783046
16. Gómez-Guzmán M, Toral M, Romero M, Jiménez R, Galindo P, Sánchez M, Zarzuelo MJ, Olivares M, Gálvez J, Duarte J. Antihypertensive effects of probiotics Lactobacillus strains in spontaneously hypertensive rats. Mol Nutr Food Res. 2015. doi: 10.1002/mnfr.201500290(Epub ahead of print).
17. De Oliveira Leite AM, Miguel MA, Peixoto RS, Rosado AS, Silva JT, Paschoalin VM. Microbiological, technological and therapeutic properties of kefir: a natural probiotic beverage. Braz J Microbiol. 2013;44(2):341-9. doi: 10.1590/S1517-83822013000200001.
18. Fahning BM, Dias AT, Oliveira JP, Gava AL, Porto ML, Gomes IB, Nogueira BV, Campagnaro BP, Pereira TM, Vasquez EC, Balarini CM, Meyrelles SS. Sildenafil improves vascular endothelial structure and function in renovascular hypertension. Curr Pharm Biotechnol. 2015;16(9):823-31. doi: 10.2174/1389201016666150610161330.
19. Hamet MF, Londero A, Medrano M, Vercammen E, Van Hoorde K, Garrote GL, Huys G, Vandamme P, Abraham AG. Application of culture-dependent and culture-independent methods for the identification of Lactobacillus kefiranofaciens in microbial consortia present in kefir grains. Food Microbiol. 2013;36(2):327-34. doi: 10.1016/j.fm.2013.06.022.
20. Leite AM, Mayo B, Rachid CT, Peixoto RS, Silva JT, Paschoalin VM, Delgado S. Assessment of the microbial diversity of Brazilian kefir grains by PCR-DGGE and pyrosequencing analysis. Food Microbiol. 2012;31(2):215-21. doi: 10.1016/j.fm.2012.03.011.
21. Ostadrahimi A, Taghizadeh A, Mobasseri M, Farrin N, Payahoo L, Beyramalipoor Gheshlaghi Z, Vahedjabbari M. Effect of probiotic fermented milk (kefir) on glycemic control and lipid profile in type 2 diabetic patients: a randomized double-blind placebo-controlled clinical trial. Iran J Public Health 2015;44(2):228-37 (PubMed PMID: 25905057).
22. Hayakawa H, Hirata Y, Suzuki E, Sugimoto T, Matsuoka H, Kikuchi K, Nagano T, Hirobe M, Sugimoto T. Mechanisms for altered endothelium-dependent vasorelaxation in isolated kidneys from experimental hypertensive rats. Am J Physiol. 1993;264(5 Pt 2):H1535-41.
23. Kauser K, Rubanyi GM. Gender difference in endothelial dysfunction in the aorta of spontaneously hypertensive rats. Hypertension. 1995;25(4 Pt 1):517-23. doi: 10.1161/01.HYP.25.4.517.
24. Honda H, Unemoto T, Kogo H. Different mechanisms for testosterone-induced relaxation of aorta between normotensive and spontaneously hypertensive rats. Hypertension. 1999;34(6):1232-6. doi: 10.1161/01.HYP.34.6.1232.
25. Virdis A, Colucci R, Versari D, Ghisu N, Fornai M, Antonioli L, Duranti E, Daghini E, Giannarelli C, Blandizzi C, Taddei S, Del Tacca M. Atorvastatin prevents endothelial dysfunction in mesenteric arteries from spontaneously hypertensive rats: role of cyclooxygenase 2-derived contracting prostanoids. Hypertension. 2009;53(6):1008-16. doi: 10.1161/HYPERTENSIONAHA.109.132258.
26. Zhang JX, Yang JR, Chen GX, Tang LJ, Li WX, Yang H, Kong X. Sesamin ameliorates arterial dysfunction in spontaneously hypertensive rats via downregulation of NADPH oxidase subunits and upregulation of eNOS expression. Acta Pharmacol Sin. 2013;34(7):912-20. doi: 10.1038/aps.2013.1.
27. Zalba G, Beaumont FJ, San José G, Fortuño A, Fortuño MA, Etayo JC, Díez J. Vascular NADH/NADPH oxidase is involved in enhanced superoxide production in spontaneously hypertensive rats. Hypertension. 2000;35(5):1055-61. doi: 10.1161/01.HYP.35.5.1055.
28. Yang D, Félétou M, Boulanger CM, Wu HF, Levens N, Zhang JN, Vanhoutte PM. Oxygen-derived free radicals mediate endothelium-dependent contractions to acetylcholine in aortas from spontaneously hypertensive rats. Br J Pharmacol. 2002;136:104-10. doi: 10.1038/sj.bjp.0704669.
29. Tang EH, Vanhoutte PM. Prostanoids and reactive oxygen species: team players in endothelium-dependent contractions. Pharmacol Ther. 2009;122:140-9. doi: 10.1016/j.pharmthera.2009.02.006.
30. Leal MA, Balarini CM, Dias AT, Porto ML, Gava AL, Pereira TMC, Meyrelles SS, Vasquez EV. Mechanisms of enhanced vasoconstriction in the mouse model of atherosclerosis: the beneficial effects of sildenafil. Curr Pharmac Biotech. 2015;16(6):517-30. doi: 10.2174/138920101606150407113458.
31. Domínguez González KN, Cruz Guerrero AE, Márquez HG, Gómez Ruiz LC, García-Garibay M, Rodríguez Serrano GM. The antihypertensive effect of fermented milks. Rev Argent Microbiol. 2014; 46(1):58-65.
32. Toral M, Gómez-Guzmán M, Jiménez R, Romero M, Sánchez M, Utrilla MP, Garrido-Mesa N, Rodríguez-Cabezas ME, Olivares M, Gálvez J, Duarte J. The probiotic Lactobacillus coryniformis CECT5711 reduces the vascular pro-oxidant and pro-inflammatory status in obese mice. Clin Sci (Lond). 2014;127(1):33-45. doi: 10.1042/CS20130339.
33. Campagnaro BP, Tonini CL, Doche LM, Nogueira BV, Vasquez EC, Meyrelles SS. Renovascular hypertension leads to DNA damage and apoptosis in bone marrow cells. DNA Cell Biol. 2013;32(8):458-66. doi: 10.1089/dna.2013.2065.
34. Guven M, Akman T, Yener AU, Sehitoglu MH, Yuksel Y, Cosar M. The neuroprotective effect of kefir on spinal cord ischemia/reperfusion injury in rats. J Korean Neurosurg Soc. 2015;57(5):335-41. doi: 10.3340/jkns.2015.57.5.335.
35. Tilling L, Chowienczyk P, Clapp B. Progenitors in motion: mechanisms of mobilization of endothelial progenitor cells. Br J Clin Pharmacol. 2009;68(4):484-92. doi: 10.1111/j.1365-2125.2009.03486.x.
36. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, Dimmeler S. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med. 2003;9(11):1370-6 (Erratum in: Nat Med. 2004;10(9):999).
37. Saad MI, Abdelkhalek TM, Saleh MM, Kamel MA, Youssef M, Tawfik SH, Dominguez H. Insights into the molecular mechanisms of diabetes-induced endothelial dysfunction: focus on oxidative stress and endothelial progenitor cells. Endocrine. 2015;50(3):537-67. doi: 10.1007/s12020-015-0709-4.
38. Veresh Z, Racz A, Lotz G, Koller A. ADMA impairs nitric oxide-mediated arteriolar function due to increased superoxide production by angiotensin II-NAD(P)H oxidase pathway. Hypertension. 2008;52(5):960-6. doi: 10.1161/HYPERTENSIONAHA.108.116731.
39. McMaster WG, Kirabo A, Madhur MS, Harrison DG. Inflammation, immunity, and hypertensive end-organ damage. Circ Res. 2015;116(6):1022-33. doi: 10.1161/CIRCRESAHA.116.303697.
40. Desouza CV. Does drug therapy reverse endothelial progenitor cell dysfunction in diabetes? J Diabetes Complications. 2013;27(5):519-25. doi: 10.1016/j.jdiacomp.2013.04.007.
41. Peng J, Liu B, Ma QL, Luo XJ. Dysfunctional endothelial progenitor cells in cardiovascular diseases: role of NADPH oxidase. J Cardiovasc Pharmacol. 2015;65(1):80-7. doi: 10.1097/FJC.0000000000000166.
42. Porto ML, Lima LC, Pereira TM, Nogueira BV, Tonini CL, Campagnaro BP, Meyrelles SS, Vasquez EC. Mononuclear cell therapy attenuates atherosclerosis in apoE KO mice. Lipids Health Dis. 2011;10:155. doi: 10.1186/1476-511X-10-155.
43. Lima LC, Porto ML, Campagnaro BP, Tonini CL, Nogueira BV, Pereira TM, Vasquez EC, Meyrelles SS. Mononuclear cell therapy reverts cuff-induced thrombosis in apolipoprotein E-deficient mice. Lipids Health Dis. 2012;11:96. doi: 10.1186/1476-511X-11-96.
44. Lin PP, Hsieh YM, Kuo WW, Lin YM, Yeh YL, Lin CC, Tsai FJ, Tsai CH, Tsai CC, Huang CY. Suppression of TLR-4-related inflammatory pathway and anti-fibrosis effects of probiotic-fermented purple sweet potato yogurt in hearts of spontaneously hypertensive rats. Chin J Physiol. 2013;56(3):174-83. doi: 10.1155/2013/845037.
45. Bauersachs J, Bouloumié A, Mülsch A, Wiemer G, Fleming I, Busse R. Vasodilator dysfunction in aged spontaneously hypertensive rats: changes in NO synthase III and soluble guanylyl cyclase expression, and in superoxide anion production. Cardiovasc Res. 1998;37(3):772-9. doi: 10.1016/S0008-6363(97)00250-2.
46. Yang D, Félétou M, Boulanger CM, Wu HF, Levens N, Zhang JN, Vanhoutte PM. Oxygen-derived free radicals mediate endothelium-dependent contractions to acetylcholine in aortas from spontaneously hypertensive rats. Br J Pharmacol. 2002;136:104-10. doi: 10.1038/sj.bjp.0704669.
47. Beaulieu J, Millette E, Trottier E, Précourt LP, Dupont C, Lemieux P. Regulatory function of a malleable protein matrix as a novel fermented whey product on features defining the metabolic syndrome. J Med Food. 2010;13(3):509-19. doi: 10.1089/jmf.2009.0083.