Chlorella modulates insulin signaling pathway and prevents high-fat diet-induced insulin resistance in mice

Life Sciences

Volumn 95, Issue 1, 2014, Pages 45-52

  Vecina, Juliana Falcato ^a   Oliveira, Alexandre Gabarra ^a   Araujo, Tiago Gomes ^a   Baggio, Sueli Regina ^b   Torello, Cristiane Okuda ^a   Saad, Mario Jose Abdalla ^a   Queiroz, Mary Luci De Souza ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b INSTITUTO DE TECNOLOGIA DE ALIMENTOS   (Brazil)

Author keywords

Chlorella vulgaris; Insulin resistance; Insulin signaling pathway; Obesity

Indexed keywords

CARBOHYDRATE; CHOLESTEROL; FATTY ACID; GLUCOSE; GUANINE NUCLEOTIDE BINDING PROTEIN; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; IRON; LEPTIN; LIPID; MONOUNSATURATED FATTY ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; POLYUNSATURATED FATTY ACID; PROTEIN KINASE B; SATURATED FATTY ACID; SERINE; TRIACYLGLYCEROL;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASH; BODY WEIGHT; CALORIE; CHLORELLA VULGARIS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DYSLIPIDEMIA; ENZYME LINKED IMMUNOSORBENT ASSAY; FATTY ACID BLOOD LEVEL; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN TOLERANCE TEST; LIPID COMPOSITION; LIPID DIET; LIPID METABOLISM; LIVER; MALE; MOISTURE; MOUSE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TARGET ORGAN; TRANS ISOMER; TRIACYLGLYCEROL BLOOD LEVEL; WESTERN BLOTTING;

CHLORELLA VULGARIS; MUS; RODENTIA;

CHLORELLA VULGARIS; INSULIN RESISTANCE; INSULIN SIGNALING PATHWAY; OBESITY;

ADIPOSE TISSUE; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; CHLORELLA VULGARIS; DIET, HIGH-FAT; DYSLIPIDEMIAS; GLUCOSE TOLERANCE TEST; INSULIN; INSULIN RESISTANCE; LEPTIN; LIPIDS; LIVER; MALE; MICE; MICE, INBRED BALB C; MUSCLE, SKELETAL; OBESITY; PHOSPHORYLATION; PLANT EXTRACTS; SIGNAL TRANSDUCTION;

EID: 84892374361     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2013.11.020     Document Type: Article

References (70)

1. V. Aguirre, E.D. Werner, J. Giraud, Y.H. Lee, S.E. Shoelson, and M.F. White Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action J Biol Chem 277 2002 1531 1537
2. T.G. Araujo, A.G. Oliveira, B.M. Carvalho, D. Guadagnini, A.O. Protzek, and J.B. Carvalheira et al. Hepatocyte growth factor plays a key role in insulin resistance-associated compensatory mechanisms Endocrinology 153 2012 5760 5769
3. S. Boura-Halfon, and Y. Zick Phosphorylation of IRS proteins, insulin action, and insulin resistance Am J Physiol Endocrinol Metab 296 2009 E581 E591
4. A.M. Caricilli, P.K. Picardi, L.L. de Abreu, M. Ueno, P.O. Prada, and E.R. Ropelle et al. Gut microbiota is a key modulator of insulin resistance in TLR 2 knockout mice PLoS Biol 9 2011 e1001212
5. J.F. Caro, J.W. Kolaczynski, M.R. Nyce, J.P. Ohannesian, I. Opentanova, and W.G. Goldman Decreased cerebrospinal-fluid/serum leptin ratio in obesity: a possible mechanism for leptin resistance Lancet 348 1996 159 161
6. C.L. Chang, Y. Lin, A.P. Bartolome, Y.C. Chen, S.C. Chiu, and W.C. Yang Herbal therapies for type 2 diabetes mellitus: chemistry, biology, and potential application of selected plants and compounds Evid Based Complement Alternat Med 2013 2013 378657
7. J.Y. Cherng, and M.F. Shih Improving glycogenesis in streptozocin (STZ) diabetic mice after administration of green algae Chlorella Life Sci 78 2006 1181 1186
8. Y.C. Chou, E. Prakash, C.F. Huang, T.W. Lien, X. Chen, and I.J. Su et al. Bioassay-guided purification and identification of PPARalpha/gamma agonists from Chlorella sorokiniana Phytother Res 22 2008 605 613
9. N.T. Chou, C.F. Cheng, H.C. Wu, C.P. Lai, L.T. Lin, and I.H. Pan et al. Chlorella sorokiniana-induced activation and maturation of human monocyte-derived dendritic cells through NF-kappaB and PI3K/MAPK pathways Evid Based Complement Alternat Med 2012 2012 735396
10. M. Chovanèíková, and V. Simek Effects of high-fat and Chlorella vulgaris feeding on changes in lipid metabolism in mice Biol Bratislava 56 2001 661 666
11. R.V. Considine, M.K. Sinha, M.L. Heiman, A. Aidas Kriauciunas, T.W. Stephens, and M.R. Nyce et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans N Engl J Med 334 1996 292 295
12. D.C.M. Dantas, and M.L.S. Queiroz Effects of Chlorella vulgaris on bone marrow progenitor cells of mice infected with Listeria monocytogenes Int J Immunopharmacol 21 1999 499 508
13. D.C.M. Dantas, R. Kaneno, and M.L.S. Queiroz The effects of Chlorella vulgaris in the protection of mice infected with Listeria monocytogenes. Role of natural killer cells Immunopharmacol Immunotoxicol 21 3 1999 609 619
14. M.Y. Donath, and S.E. Shoelson Type 2 diabetes as an inflammatory disease Nat Rev Immunol 11 2011 98 107
15. A. Gonzalez-Periz, R. Horrillo, N. Ferre, K. Gronert, B. Dong, and E. Moran-Salvador et al. Obesity-induced insulin resistance and hepatic steatosis are alleviated by omega-3 fatty acids: a role for resolvins and protectins FASEB J 23 2009 1946 1957
16. M.F. Gregor, and G.S. Hotamisligil Inflammatory mechanisms in obesity Annu Rev Immunol 29 2011 415 445
17. T. Hasegawa, K. Noda, S. Kumamoto, Y. Ando, A. Yamada, and Y. Yoshikai Chlorella vulgaris culture supernatant (CVS) reduces psychological stress-induced apoptosis in thymocytes of mice Int J Immunopharmacol 22 2000 877 885
18. S. Hidaka, Y. Okamoto, and M. Arita A hot water extract of Chlorella pyrenoidosa reduces body weight and serum lipids in ovariectomized rats Phytother Res 18 2004 164 168
19. J. Hirosumi, G. Tuncman, L. Chang, C.Z. Gorgun, K.T. Uysal, and K. Maeda et al. A central role for JNK in obesity and insulin resistance Nature 420 2002 333 336
20. G.S. Hotamisligil, P. Peraldi, A. Budavari, R. Ellis, M.F. White, and B.M. Spiegelman IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance Science 271 1996 665 668
21. B.V. Howard, G. Ruotolo, and D.C. Robbins Obesity and dyslipidemia Endocrinol Metab Clin N Am 32 2003 855 867
22. H. Jeong, H.J. Kwon, and M.K. Kim Hypoglycemic effect of Chlorella vulgaris intake in type 2 diabetic Goto-Kakizaki and normal Wistar rats Nutr Res Pract 3 2009 23 30
23. C. Jong-Yuh, and S. Mei-Fen Potential hypoglycemic effects of Chlorella in streptozotocin-induced diabetic mice Life Sci 77 2005 980 990
24. G.Z. Justo, M.R. Silva, and M.L.S. Queiroz Effects of the green algae Chlorella vulgaris on the response of the host hematopoietic system to intraperitoneal Ehrlich ascites tumor transplantation in mice Immunopharmacol Immunotoxicol 23 1 2001 119 132
25. R.A. Kay Microalgae as food and supplement Crit Rev Food Sci Nutr 30 1991 555 573
26. F. Konishi, K. Tanaka, K. Himeno, K. Taniguchi, and K. Nomoto Antitumor effect induced by a hot water extract of Chlorella vulgaris (CE): resistance to meth-A tumor growth mediated by CE-induced polymorphonuclear leukocytes Cancer Immunol Immunother CII 19 1985 73 78
27. H.S. Lee, and M.K. Kim Effect of Chlorella vulgaris on glucose metabolism in Wistar rats fed high fat diet J Med Food 12 2009 1029 1037
28. H.S. Lee, H.J. Park, and M.K. Kim Effect of Chlorella vulgaris on lipid metabolism in Wistar rats fed high fat diet Nutr Res Pract 2 2008 204 210
29. S.H. Lee, K.H. Min, J.S. Han, D.H. Lee, D.B. Park, and W.K. Jung et al. Effects of brown alga, Ecklonia cava on glucose and lipid metabolism in C57BL/KsJ-db/db mice, a model of type 2 diabetes mellitus Food Chem Toxicol 50 2012 575 582
30. D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, and R.C. Turner Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man Diabetologia 28 1985 412 419
31. A.E. Mehran, N.M. Templeman, G.S. Brigidi, G.E. Lim, K.Y. Chu, and X. Hu et al. Hyperinsulinemia drives diet-induced obesity independently of brain insulin production Cell Metab 16 2012 723 737
32. T. Mizoguchi, I. Takehara, T. Masuzawa, T. Saito, and Y. Naoki Nutrigenomic studies of effects of Chlorella on subjects with high-risk factors for lifestyle-related disease J Med Food 11 2008 395 404
33. K.M. Narayan, E.W. Gregg, A. Fagot-Campagna, M.M. Engelgau, and F. Vinicor Diabetes - a common, growing, serious, costly, and potentially preventable public health problem Diabetes Res Clin Pract 50 Suppl. 2 2000 S77 S84
34. K. Noda, N. Ohno, K. Tanaka, M. Okuda, T. Yadomae, and K. Nomoto et al. A new type of biological response modifier from Chlorella vulgaris which needs protein moiety to show an antitumour activity Phytother Res 12 1998 309 319
35. N. Noguchi, F. Konishi, S. Kumamoto, I. Maruyama, Y. Ando, and T. Yanagita Beneficial effects of Chlorella on glucose and lipid metabolism in obese rodents on a high-fat diet Obes Res Clin Pract 7 2 2013 95 105
36. M. Okudo, T. Hasegawa, M. Sonoda, T. Okabe, and M. Tanaka The effects of Chlorella on the level of cholesterol in serum and liver Jap J Nutr 33 1975 3 8
37. A.G. Oliveira, B.M. Carvalho, N. Tobar, E.R. Ropelle, J.R. Pauli, and R.A. Bagarolli et al. Physical exercise reduces circulating lipopolysaccharide and TLR4 activation and improves insulin signaling in tissues of DIO rats Diabetes 60 2011 784 796
38. Y. Panahi, S. Tavana, A. Sahebkar, H. Masoudi, and N. Madanchi Impact of adjunctive therapy with Chlorella vulgaris extract on antioxidant status, pulmonary function, and clinical symptoms of patients with obstructive pulmonary diseases Sci Pharm 80 2012 719 730
39. J.E. Pessin, and A.R. Saltiel Signaling pathways in insulin action: molecular targets of insulin resistance J Clin Invest 106 2000 165 169
40. G.G. Piroli, C.A. Grillo, L.R. Reznikov, S. Adams, B.S. McEwen, M.J. Charron, and L.P. Reagan Corticosterone impairs insulin-stimulated translocation of GLUT4 in the rat hippocampus Neuroendocrinology 85 2 2007 71 80
41. M.L.S. Queiroz, C. Bincoletto, M.C. Valadares, D.C.M. Dantas, and L.M.B. Santos Effects of Chlorella vulgaris extract on citocynes production in Listeria monocytogenes infected mice Immunopharmacol Immunotoxicol 24 2002 483 496
42. M.L. Queiroz, A.P. Rodrigues, C. Bincoletto, C.A. Figueiredo, and S. Malacrida Protective effects of Chlorella vulgaris in lead-exposed mice infected with Listeria monocytogenes Int Immunopharmacol 3 2003 889 900
43. M.L.S. Queiroz, C.O. Torello, S.M. Perhs, M.C. Rocha, E.J. Bechara, and M.A. Morgano et al. Chlorella vulgaris up-modulation of myelossupression induced by lead: the role of stromal cells Food Chem Toxicol 46 2008 3147 3154
44. M.L.S. Queiroz, M.C. Rocha, C.O. Torello, J. Souza-Queiroz, C. Bincoletto, and M.A. Morgano et al. Chlorella vulgaris restores bone marrow cellularity and cytokine production in lead-exposed mice Food Chem Toxicol 49 2011 2934 2941
45. A.L. Ramos, C.O. Torello, and M.L. Queiroz Chlorella vulgaris modulates immunomyelopoietic activity and enhances the resistance of tumor-bearing mice Nutr Cancer 62 2010 1170 1180
46. A.L. Ramos, C.O. Torello, M.C. Rocha, S.C. Oliveira, I. Souza, and E. Antunes et al. Chlorella vulgaris modulates macrophages activities in Ehrlich ascites tumor-bearing mice Nutr Cancer. 2013 [submitted for publication]
47. I. Rodriguez-Garcia, and J.L. Guil-Guerrero Evaluation of the antioxidant activity of three microalgal species for use as dietary supplements and in the preservation of foods Food Chem 108 2008 1023 1026
48. M. Rodriguez-Lopez, and C. Lopez-Quijada Plasma-glucose and plasma-insulin in normal and alloxanized rats treated with Chlorella Life Sci Pt 2 Biochem Gen Mol Biol 10 1971 57 60
49. S.M. Saad, Y.A.M. Yusof, and W.Z.W. Ngah Comparison between locally produced Chlorella vulgaris and Chlorella vulgaris from Japan on proliferation and apoptosis of liver cancer cell line, HepG2 Malays J Biochem Mol Biol 13 2006 32 36
50. A.R. Saltiel, and C.R. Kahn Insulin signalling and the regulation of glucose and lipid metabolism Nature 414 2001 799 806
51. A.R. Saltiel, and J.E. Pessin Insulin signaling pathways in time and space Trends Cell Biol 12 2002 65 71
52. T. Sano, Y. Kumamoto, N. Kamiya, M. Okuda, and Y. Tanaka Effect of lipophilic extract of Chlorella vulgaris on alimentary hyperlipidemia in cholesterol-fed rats Artery 15 1988 217 224
53. J.C. Seidell Obesity and weight control: the evidence Proc Nutr Soc 59 2000 419 420
54. T. Senthilkumar, N. Sangeetha, and N. Ashokkumar Antihyperglycemic, antihyperlipidemic, and renoprotective effects of Chlorella pyrenoidosa in diabetic rats exposed to cadmium Toxicol Mech Methods 22 2012 617 624
55. S. Shibata, K. Oda, N. Onodera-Masuoka, S. Matsubara, H. Kikuchi-Hayakawa, and F. Ishikawa et al. Hypocholesterolemic effect of indigestible fraction of Chlorella regularis in cholesterol-fed rats J Nutr Sci Vitaminol (Tokyo) 47 2001 373 377
56. S.E. Shoelson, J. Lee, and A.B. Goldfine Inflammation and insulin resistance J Clin Invest 116 2006 1793 1801
57. A.P. Simopoulos The importance of the ratio of omega-6/omega-3 essential fatty acids Biomedecine Pharmacotherapie 56 2002 365 379
58. A. Singh, L. Sharma, and N. Mallick Antioxidative role of nitric oxide on copper toxicity to a chlorophycean alga, Chlorella Ecotoxicol Environ Saf 59 2004 223 227
59. G. Solinas, and M. Karin JNK1 and IKKbeta: molecular links between obesity and metabolic dysfunction FASEB J 24 2010 2596 2611
60. J. Souza-Queiroz, S.A. Malacrida, G.Z. Justo, and M.L.S. Queiroz Myelopoietic response in mice exposed to acute/cold restraint stress: modulation by Chlorella vulgaris prophylactic treatment Immunopharmacol Immunotoxicol 26 2004 455 467
61. J. Souza-Queiroz, C.O. Torello, J. Palermo-Neto, M.C. Valadares, and M.L. Queiroz Hematopoietic response of rats exposed to the impact of an acute psychophysiological stressor on responsiveness to an in vivo challenge with Listeria monocytogenes: modulation by Chlorella vulgaris prophylactic treatment Brain Behav Immun 22 2008 1056 1065
62. J. Souza-Queiroz, M.C. Rocha, C.M.V. Barbosa, C. Bincoletto, M.L.S. Queiroz, and E.J. Paredes-Gamero et al. Chlorella vulgaris treatment ameliorates the suppressive effects of single and repeated stressors on hematopoiesis Brain Behav Immun 29 2013 39 50
63. J. Souza-Queiroz, I. Marin-Blasco, A. Gómez-Román, X. Belda, M.C. Rocha, and J. Carrasco et al. Chlorella vulgaris reduces the impact of stress on hypothalamic-pituitary-adrenal axis and brain c-fos expression Brain Behav Immun 2013 [Submitted for publication]
64. M. Stumvoll, B.J. Goldstein, and T.W. van Haeften Type 2 diabetes: principles of pathogenesis and therapy Lancet 365 2005 1333 1346
65. K. Tanaka, T. Koga, F. Konishi, M. Nakamura, M. Mitsuyama, and K. Himeno et al. Augmentation of host defense by a unicellular green alga, Chlorella vulgaris, to Escherichia coli infection Infect Immun 53 1986 267 271
66. K. Tanaka, A. Yamada, K. Noda, T. Hasegawa, M. Okuda, and Y. Shoyama et al. A novel glycoprotein obtained from Chlorella vulgaris strain CK22 shows antimetastatic immunopotentiation Cancer Immunol Immunother 45 1998 313 320
67. K. Vijayavel, C. Anbuselvam, and M.P. Balasubramanian Antioxidant effect of the marine algae Chlorella vulgaris against naphthalene-induced oxidative stress in the albino rats Mol Cell Biochem 303 2007 39 44
68. T.L. Visscher, and J.C. Seidell The public health impact of obesity Annu Rev Public Health 22 2001 355 375
69. J. Wang, S. Obici, K. Morgan, N. Barzilai, Z. Feng, and L. Rossetti Overfeeding rapidly induces leptin and insulin resistance Diabetes 50 12 2001 2786 2791
70. WHO Obesity and overweight In Fact Sheet 311 2012