Wild blueberries (vaccinium myrtillus) alleviate inflammation and hypertension associated with developing obesity in mice fed with a high-fat diet

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Mykkänen, Otto T ^a   Huotari, Anne ^a   Herzig, Karl Heinz ^b   Dunlop, Thomas W ^a   Mykkänen, Hannu ^a   Kirjavainen, Pirkka V ^a,c  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF OULU   (Finland)

^c NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 9; LEPTIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; RESISTIN; TUMOR NECROSIS FACTOR ALPHA; ADIPOCYTOKINE; ANTHOCYANIN; BIOLOGICAL MARKER; CYTOKINE; GLUCOSE; LIPID; VACCINIUM MYRTILLUS EXTRACT;

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY FAT; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; ENERGY METABOLISM; FAT CONTENT; FOOD INTAKE; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HYPERTENSION; IMMUNOMODULATION; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; MOUSE; NONHUMAN; OBESITY; SYSTOLIC BLOOD PRESSURE; TH1 CELL; THERAPY EFFECT; VACCINIUM MYRTILLUS; WEIGHT GAIN; ADIPOSE TISSUE; ADVERSE EFFECTS; ANIMAL; BILBERRY; BLOOD; BLOOD PRESSURE; BODY WEIGHT; C57BL MOUSE; CHEMISTRY; COMPLICATION; DRUG EFFECTS; EATING; IMMUNOLOGY; MALE; METABOLISM;

MUS; VACCINIUM; VACCINIUM MYRTILLUS;

ADIPOKINES; ADIPOSE TISSUE; ANIMALS; ANTHOCYANINS; BIOMARKERS; BLOOD PRESSURE; BODY WEIGHT; CYTOKINES; DIET, HIGH-FAT; EATING; ENERGY METABOLISM; GLUCOSE; HYPERTENSION; IMMUNOMODULATION; INFLAMMATION; INSULIN RESISTANCE; LIPIDS; MALE; MICE; MICE, INBRED C57BL; OBESITY; VACCINIUM MYRTILLUS;

EID: 84918542726     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114790     Document Type: Article

References (82)

1. Ouchi N, Parker JL, Lugus JJ, Walsh K (2011) Adipokines in inflammation and metabolic disease. Nat Rev Immunol 11: 85-97.
2. Colosia AD, Palencia R, Khan S (2013) Prevalence of hypertension and obesity in patients with type 2 diabetes mellitus in observational studies: A systematic literature review. Diabetes Metab Syndr Obes 6: 327-338.
3. Xu H, Barnes GT, Yang Q, Tan G, Yang D, et al. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830.
4. Winer S, Winer DA (2012) The adaptive immune system as a fundamental regulator of adipose tissue inflammation and insulin resistance. Immunol Cell Biol 90: 755-762.
5. Xu H (2013) Obesity and metabolic inflammation. Drug Discov Today Dis Mech 10: 21-25.
6. DeFuria J, Bennett G, Strissel KJ, Perfield JW 2nd, Milbury PE, et al. (2009) Dietary blueberry attenuates whole-body insulin resistance in high fat-fed mice by reducing adipocyte death and its inflammatory sequelae. J Nutr 139: 1510-1516.
7. Karlsen A, Paur I, Bohn SK, Sakhi AK, Borge GI, et al. (2010) Bilberry juice modulates plasma concentration of NF-kappaB related inflammatory markers in subjects at increased risk of CVD. Eur J Nutr 49: 345-355.
8. Kolehmainen M, Mykkanen O, Kirjavainen PV, Leppanen T, Moilanen E, et al. (2012) Bilberries reduce low-grade inflammation in individuals with features of metabolic syndrome. Mol Nutr Food Res 56: 1501-1510.
9. Vendrame S, Daugherty A, Kristo AS, Riso P, Klimis-Zacas D (2013) Wild blueberry (vaccinium angustifolium) consumption improves inflammatory status in the obese zucker rat model of the metabolic syndrome. J Nutr Biochem 24: 1508-1512.
10. Kolb H, Mandrup-Poulsen T (2010) The global diabetes epidemic as a consequence of lifestyleinduced low-grade inflammation. Diabetologia 53: 10-20.
11. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, et al. (2009) CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15: 914-920.
12. Ohmura K, Ishimori N, Ohmura Y, Tokuhara S, Nozawa A, et al. (2010) Natural killer T cells are involved in adipose tissues inflammation and glucose intolerance in diet-induced obese mice. Arterioscler Thromb Vasc Biol 30: 193-199.
13. Strissel KJ, DeFuria J, Shaul ME, Bennett G, Greenberg AS, et al. (2010) T-cell recruitment and Th1 polarization in adipose tissue during diet-induced obesity in C57BL/6 mice. Obesity (Silver Spring) 18: 1918-1925.
14. Mills E, Kuhn CM, Feinglos MN, Surwit R (1993) Hypertension in CB57BL/6J mouse model of non-insulin-dependent diabetes mellitus. Am J Physiol 264: R73-8.
15. Rossmeisl M, Rim JS, Koza RA, Kozak LP (2003) Variation in type 2 diabetes-related traits in mouse strains susceptible to diet-induced obesity. Diabetes 52: 1958-1966.
16. Collins S, Martin TL, Surwit RS, Robidoux J (2004) Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: Physiological and molecular characteristics. Physiol Behav 81: 243-248.
17. Montgomery MK, Hallahan NL, Brown SH, Liu M, Mitchell TW, et al. (2013) Mouse strain-dependent variation in obesity and glucose homeostasis in response to high-fat feeding. Diabetologia 56: 1129-1139.
18. Riihinen K, Jaakola L, Kärenlampi S, Hohtola A (2008) Organ-specific distribution of phenolic compounds in bilberry (vaccinium myrtillus) and 'northblue' blueberry (vaccinium corymbosum x V. angustifolium). Food Chem 110: 156-160.
19. Koponen JM, Happonen AM, Mattila PH, Torronen AR (2007) Contents of anthocyanins and ellagitannins in selected foods consumed in finland. J Agric Food Chem 55: 1612-1619.
20. Ovaskainen ML, Torronen R, Koponen JM, Sinkko H, Hellstrom J, et al. (2008) Dietary intake and major food sources of polyphenols in finnish adults. J Nutr 138: 562-566.
21. He J, Giusti MM (2010) Anthocyanins: Natural colorants with health-promoting properties. Annu Rev Food Sci Technol 1: 163-187.
22. Nile SH, Park SW (2014) Edible berries: Bioactive components and their effect on human health. Nutrition 30: 134-144.
23. Ghosh D, Konishi T (2007) Anthocyanins and anthocyanin-rich extracts: Role in diabetes and eye function. Asia Pac J Clin Nutr 16: 200-208.
24. Helmstadter A, Schuster N (2010) Vaccinium myrtillus as an antidiabetic medicinal plant-research through the ages. Pharmazie 65: 315-321.
25. Jayaprakasam B, Olson LK, Schutzki RE, Tai MH, Nair MG (2006) Amelioration of obesity and glucose intolerance in high-fat-fed C57BL/6 mice by anthocyanins and ursolic acid in cornelian cherry (cornus mas). J Agric Food Chem 54: 243-248.
26. Prior RL, Wilkes SE, Rogers TR, Khanal RC, Wu X, et al. (2010) Purified blueberry anthocyanins and blueberry juice alter development of obesity in mice fed an obesogenic high-fat diet. J Agric Food Chem 58: 3970-3976.
27. Takikawa M, Inoue S, Horio F, Tsuda T (2010) Dietary anthocyanin-rich bilberry extract ameliorates hyperglycemia and insulin sensitivity via activation of AMP-activated protein kinase in diabetic mice. J Nutr 140: 527-533.
28. Prior RL, Wu X, Gu L, Hager TJ, Hager A, et al. (2008) Whole berries versus berry anthocyanins: Interactions with dietary fat levels in the C57BL/6J mouse model of obesity. J Agric Food Chem 56: 647-653.
29. Prior RL, Wu X, Gu L, Hager T, Hager A, et al. (2009) Purified berry anthocyanins but not whole berries normalize lipid parameters in mice fed an obesogenic high fat diet. Mol Nutr Food Res 53: 1406-1418.
30. Shindo M, Kasai T, Abe A, Kondo Y (2007) Effects of dietary administration of plant-derived anthocyanin-rich colors to spontaneously hypertensive rats. J Nutr Sci Vitaminol (Tokyo) 53: 90-93.
31. Elks CM, Reed SD, Mariappan N, Shukitt-Hale B, Joseph JA, et al. (2011) A blueberry-enriched diet attenuates nephropathy in a rat model of hypertension via reduction in oxidative stress. PLoS One 6: e24028.
32. Rodriguez-Mateos A, Ishisaka A, Mawatari K, Vidal-Diez A, Spencer JP, et al. (2013) Blueberry intervention improves vascular reactivity and lowers blood pressure in high-fat-, high-cholesterol-fed rats. Br J Nutr 109: 1746-1754.
33. Mykkanen OT, Kalesnykas G, Adriaens M, Evelo CT, Torronen R, et al. (2012) Bilberries potentially alleviate stress-related retinal gene expression induced by a high-fat diet in mice. Mol Vis 18: 2338-2351.
34. Tauriainen E, Luostarinen M, Martonen E, Finckenberg P, Kovalainen M, et al. (2011) Distinct effects of calorie restriction and resveratrol on diet-induced obesity and fatty liver formation. J Nutr Metab 2011: 525094.
35. Sharma S, Fulton S (2013) Diet-induced obesity promotes depressive-like behaviour that is associated with neural adaptations in brain reward circuitry. Int J Obes (Lond) 37: 382-389.
36. Thomas EL, Saeed N, Hajnal JV, Brynes A, Goldstone AP, et al. (1998) Magnetic resonance imaging of total body fat. J Appl Physiol (1985) 85: 1778-1785.
37. Heikkinen S, Argmann CA, Champy MF, Auwerx J (2007) Evaluation of glucose homeostasis. Curr Protoc Mol Biol Chapter 29: Unit 29B.3.
38. Kleemann R, Zadelaar S, Kooistra T (2008) Cytokines and atherosclerosis: A comprehensive review of studies in mice. Cardiovasc Res 79: 360-376.
39. Akdis M, Burgler S, Crameri R, Eiwegger T, Fujita H, et al. (2011) Interleukins, from 1 to 37, and interferon-gamma: Receptors, functions, and roles in diseases. J Allergy Clin Immunol 127: 701-21.e1-70.
40. Seruga B, Zhang H, Bernstein LJ, Tannock IF (2008) Cytokines and their relationship to the symptoms and outcome of cancer. Nat Rev Cancer 8: 887-899.
41. Kirjavainen PV, ElNezami HS, Salminen SJ, Ahokas JT, Wright PF (1999) Effects of orally administered viable lactobacillus rhamnosus GG and propionibacterium freudenreichii subsp. shermanii JS on mouse lymphocyte proliferation. Clin Diagn Lab Immunol 6: 799-802.
42. Kirjavainen PV, Pautler S, Baroja ML, Anukam K, Crowley K, et al. (2009) Abnormal immunological profile and vaginal microbiota in women prone to urinary tract infections. Clin Vaccine Immunol 16: 29-36.
43. Johns C, Gavras I, Handy DE, Salomao A, Gavras H (1996) Models of experimental hypertension in mice. Hypertension 28: 1064-1069.
44. Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN (1988) Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37: 1163-1167.
45. Tsuda T, Horio F, Uchida K, Aoki H, Osawa T (2003) Dietary cyanidin 3-O-beta-D-glucoside-rich purple corn color prevents obesity and ameliorates hyperglycemia in mice. J Nutr 133: 2125-2130.
46. Heyman L, Axling U, Blanco N, Sterner O, Holm C, et al. (2014) Evaluation of beneficial metabolic effects of berries in high-fat fed C57BL/6J mice. Journal of Nutrition and Metabolism 2014: 12.
47. Yang M, Koo SI, Song WO, Chun OK (2011) Food matrix affecting anthocyanin bioavailability: Review. Curr Med Chem 18: 291-300.
48. Agouni A, Owen C, Czopek A, Mody N, Delibegovic M (2010) In vivo differential effects of fasting, refeeding, insulin and insulin stimulation time course on insulin signaling pathway components in peripheral tissues. Biochem Biophys Res Commun 401: 104-111.
49. Mathieu P, Lemieux I, Despres JP (2010) Obesity, inflammation, and cardiovascular risk. Clin Pharmacol Ther 87: 407-416.
50. De Ciuceis C, Rossini C, La Boria E, Porteri E, Petroboni B, et al. (2014) Immune mechanisms in hypertension. High Blood Press Cardiovasc Prev.
51. Schiffrin EL (2014) Immune mechanisms in hypertension and vascular injury. Clin Sci (Lond) 126: 267-274.
52. Wu Y, Wu T, Wu J, Zhao L, Li Q, et al. (2013) Chronic inflammation exacerbates glucose metabolism disorders in C57BL/6J mice fed with high-fat diet. J Endocrinol 219: 195-204.
53. Rocha VZ, Folco EJ, Sukhova G, Shimizu K, Gotsman I, et al. (2008) Interferon-gamma, a Th1 cytokine, regulates fat inflammation: A role for adaptive immunity in obesity. Circ Res 103: 467-476.
54. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, et al. (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116: 1494-1505.
55. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, et al. (2001) The hormone resistin links obesity to diabetes. Nature 409: 307-312.
56. Graf D, Seifert S, Jaudszus A, Bub A, Watzl B (2013) Anthocyanin-rich juice lowers serum cholesterol, leptin, and resistin and improves plasma fatty acid composition in fischer rats. PLoS One 8: e66690.
57. Pang SS, Le YY (2006) Role of resistin in inflammation and inflammation-related diseases. Cell Mol Immunol 3: 29-34.
58. Park HK, Ahima RS (2013) Resistin in rodents and humans. Diabetes Metab J 37: 404-414.
59. Park HK, Qatanani M, Briggs ER, Ahima RS, Lazar MA (2011) Inflammatory induction of human resistin causes insulin resistance in endotoxemic mice. Diabetes 60: 775-783.
60. Sautebin L, Rossi A, Serraino I, Dugo P, Di Paola R, et al. (2004) Effect of anthocyanins contained in a blackberry extract on the circulatory failure and multiple organ dysfunction caused by endotoxin in the rat. Planta Med 70: 745-752.
61. Takano H, Ueda K, Hasegawa H, Komuro I (2007) G-CSF therapy for acute myocardial infarction. Trends Pharmacol Sci 28: 512-517.
62. Stas SN, El-Atat FA, Sowers JR (2004) Pathogenesis of hypertension in diabetes. Rev Endocr Metab Disord 5: 221-225.
63. Harrison DG, Guzik TJ, Goronzy J, Weyand C (2008) Is hypertension an immunologic disease? Curr Cardiol Rep 10: 464-469.
64. Vlasova M, Purhonen AK, Jarvelin MR, Rodilla E, Pascual J, et al. (2010) Role of adipokines in obesity-associated hypertension. Acta Physiol (Oxf) 200: 107-127.
65. Houston M (2013) Nutrition and nutraceutical supplements for the treatment of hypertension: Part I. J Clin Hypertens (Greenwich) 15: 752-757.
66. Shaughnessy KS, Boswall IA, Scanlan AP, Gottschall-Pass KT, Sweeney MI (2009) Diets containing blueberry extract lower blood pressure in spontaneously hypertensive stroke-prone rats. Nutr Res 29: 130-138.
67. Papadopoulos DP, Makris TK, Krespi PG, Poulakou M, Stavroulakis G, et al. (2005) Adiponectin and resistin plasma levels in healthy individuals with prehypertension. J Clin Hypertens (Greenwich) 7: 729-733.
68. Cheng X, Folco EJ, Shimizu K, Libby P (2012) Adiponectin induces pro-inflammatory programs in human macrophages and CD4+ T cells. J Biol Chem 287: 36896-36904.
69. Aoqui C, Chmielewski S, Scherer E, Eissler R, Sollinger D, et al. (2014) Microvascular dysfunction in the course of metabolic syndrome induced by high-fat diet. Cardiovasc Diabetol 13: 31-2840-13-31.
70. Baumann M, von Eynatten M, Dan L, Richart T, Kouznetsova T, et al. (2009) Altered molecular weight forms of adiponectin in hypertension. J Clin Hypertens (Greenwich) 11: 11-16.
71. Mendes A, Desgranges C, Cheze C, Vercauteren J, Freslon JL (2003) Vasorelaxant effects of grape polyphenols in rat isolated aorta. possible involvement of a purinergic pathway. Fundam Clin Pharmacol 17: 673-681.
72. Bell DR, Gochenaur K (2006) Direct vasoactive and vasoprotective properties of anthocyanin-rich extracts. J Appl Physiol (1985) 100: 1164-1170.
73. Kalea AZ, Clark K, Schuschke DA, Kristo AS, Klimis-Zacas DJ (2010) Dietary enrichment with wild blueberries (vaccinium angustifolium) affects the vascular reactivity in the aorta of young spontaneously hypertensive rats. J Nutr Biochem 21: 14-22.
74. Horrigan LA, Holohan CA, Lawless GA, Murtagh MA, Williams CT, et al. (2013) Blueberry juice causes potent relaxation of rat aortic rings via the activation of potassium channels and the H(2)S pathway. Food Funct 4: 392-400.
75. Jennings A, Welch AA, Fairweather-Tait SJ, Kay C, Minihane AM, et al. (2012) Higher anthocyanin intake is associated with lower arterial stiffness and central blood pressure in women. Am J Clin Nutr 96: 781-788.
76. Cassidy A, O'Reilly EJ, Kay C, Sampson L, Franz M, et al. (2011) Habitual intake of flavonoid subclasses and incident hypertension in adults. Am J Clin Nutr 93: 338-347.
77. Basu A, Du M, Leyva MJ, Sanchez K, Betts NM, et al. (2010) Blueberries decrease cardiovascular risk factors in obese men and women with metabolic syndrome. J Nutr 140: 1582-1587.
78. Riso P, Klimis-Zacas D, Del Bo' C, Martini D, Campolo J, et al. (2013) Effect of a wild blueberry (vaccinium angustifolium) drink intervention on markers of oxidative stress, inflammation and endothelial function in humans with cardiovascular risk factors. Eur J Nutr 52: 949-961.
79. Reaven GM (2011) Relationships among insulin resistance, type 2 diabetes, essential hypertension, and cardiovascular disease: Similarities and differences. J Clin Hypertens (Greenwich) 13: 238-243.
80. Wedick NM, Pan A, Cassidy A, Rimm EB, Sampson L, et al. (2012) Dietary flavonoid intakes and risk of type 2 diabetes in US men and women. Am J Clin Nutr 95: 925-933.
81. Muraki I, Imamura F, Manson JE, Hu FB, Willett WC, et al. (2013) Fruit consumption and risk of type 2 diabetes: Results from three prospective longitudinal cohort studies. BMJ 347: f5001.
82. Joseph SV, Edirisinghe I, Burton-Freeman BM (2014) Berries: Anti-inflammatory effects in humans. J Agric Food Chem.