Skip to main content

Advertisement

SpringerLink
Log in

Rice bran prevents high-fat diet-induced inflammation and macrophage content in adipose tissue

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Background

The inflammatory process associated with obesity mainly arises from white adipose tissue (WAT) alterations. In the last few years, nutritional-based strategies have been positioned as promising alternatives to pharmacological approaches against these pathologies. Our aim was to determine the potential of a rice bran enzymatic extract (RBEE)-supplemented diet in the prevention of metabolic, biochemical and functional adipose tissue and macrophage changes associated with a diet-induced obesity (DIO) in mice.

Methods

C57BL/6J mice were fed high-fat diet (HF), 1 and 5 % RBEE-supplemented high-fat diet (HF1 % and HF5 %, respectively) and standard diet as control. Serum cardiometabolic parameters, adipocytes size and mRNA expression of pro-inflammatory biomarkers and macrophage polarization-related genes from WAT and liver were evaluated.

Results

RBEE administration significantly decreased insulin resistance in obese mice. Serum triglycerides, total cholesterol, glucose, insulin, adiponectin and nitrites from treated mice were partially restored, mainly by 1 % RBEE-enriched diet. The incremented adipocytes size observed in HF group was reduced by RBEE treatment, being 1 % more effective than 5 % RBEE. Pro-inflammatory biomarkers in WAT such as IL-6 and IL-1β were significantly decreased in RBEE-treated mice. Adiponectin, PPARγ, TNF-α, Emr1 or M1/M2 levels were significantly restored in WAT from HF1 % compared to HF mice.

Conclusions

RBEE-supplemented diet attenuated insulin resistance, dyslipidemia and morphological and functional alterations of adipose tissue in DIO mice. These benefits were accompanied by a modulating effect in adipocytes secretion and some biomarkers associated with macrophage polarization. Therefore, RBEE may be considered an alternative nutritional complement over metabolic syndrome and its complications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Hossain P, Kawar B, El Nahas M (2007) Obesity and diabetes in the developing world—a growing challenge. N Engl J Med 356(3):213–215

    Article  CAS  Google Scholar 

  2. Hotamisligil G, Erbay E (2008) Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol 8(12):923–934

    Article  CAS  Google Scholar 

  3. Gregor M, Hotamisligil G (2011) Inflammatory mechanisms in obesity. Annu Rev Immunol 29:415–445

    Article  CAS  Google Scholar 

  4. Makki K, Froguel P, Wolowczuk I (2013) Adipose tissue in obesity-related inflammation and insulin resistance: cells, cytokines, and chemokines. ISRN Inflamm 2013:139239

    Article  Google Scholar 

  5. Bluher M (2009) Adipose tissue dysfunction in obesity. Exp Clin Endocrinol Diabetes 117(06):241–250

    Article  CAS  Google Scholar 

  6. Yang J, Eliasson B, Smith U, Cushman S, Sherman A (2012) The size of large adipose cells is a predictor of insulin resistance in first-degree relatives of type 2 diabetic patients. Obesity 20(5):932–938

    Article  CAS  Google Scholar 

  7. Hotamisligil G, Shargill N, Spiegelman B (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259(5091):87–91

    Article  CAS  Google Scholar 

  8. Ndisang J (2010) Role of heme oxygenase in inflammation, insulin-signalling, diabetes and obesity. Mediat Inflamm 2010:359732

    Article  Google Scholar 

  9. Malagón M, Díaz-Ruiz A, Guzmán-Ruíz R, Jimenez-Gómez Y, Moreno NR, Garcia-Navarro S et al (2013) Adipobiology for novel therapeutic approaches in metabolic syndrome. Curr Vasc Pharmacol 11(6):954–967

    Article  Google Scholar 

  10. Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117(1):175–184

    Article  CAS  Google Scholar 

  11. Odegaard J, Ricardo-Gonzalez R, Goforth M, Morel C, Subramanian V, Mukundan L et al (2007) Macrophage-specific PPARgamma; controls alternative activation and improves insulin resistance. Nature 447(7148):1116–1120

    Article  CAS  Google Scholar 

  12. Tontonoz P, Spiegelman B (2008) Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 77:289–312

    Article  CAS  Google Scholar 

  13. Islam S, Nagasaka R, Ohara K, Hosoya T, Ozaki H, Ushio H et al (2011) Biological abilities of rice bran-derived antioxidant phytochemicals for medical therapy. Curr Top Med Chem 11(14):1847–1853

    Article  CAS  Google Scholar 

  14. Fabian C, Ju Y (2011) A review on rice bran protein: its properties and extraction methods. Crit Rev Food Sci Nutr 51(9):816–827

    Article  CAS  Google Scholar 

  15. Parrado J, Miramontes E, Jover M, Gutierrez J, Collantes de Ter’an L, Bautista J (2006) Preparation of a rice bran enzymatic extract with potential use as functional food. Food Chem 98(4):742–748

    Article  CAS  Google Scholar 

  16. Park N, Rico C, Lee S, Kang M (2012) Comparative effects of doenjang prepared from soybean and brown rice on the body weight and lipid metabolism in high fat-fed mice. J Clin Biochem Nutr 51(3):235

    CAS  Google Scholar 

  17. Dhara R, Dhar P, Ghosh M (2012) Dietary effects of pure and diacylglycerol-rich rice bran oil on growth pattern and lipid profile of rats. J Oleo Sci 61(7):369–375

    Article  CAS  Google Scholar 

  18. Misra A, Singhal N, Khurana L (2010) Obesity, the metabolic syndrome, and type 2 diabetes in developing countries: role of dietary fats and oils. J Am Coll Nutr 29(sup3):289–301

    Article  Google Scholar 

  19. Justo M, Rodriguez-Rodriguez R, Claro C, de Sotomayor M, Parrado J, Herrera M (2013) Water-soluble rice bran enzymatic extract attenuates dyslipidemia, hypertension and insulin resistance in obese Zucker rats. Eur J Nutr 52(2):789–797

    Article  CAS  Google Scholar 

  20. Justo M, Candiracci M, Dantas A, de Sotomayor M, Parrado J, Vila E et al (2013) Rice bran enzymatic extract restores endothelial function and vascular contractility in obese rats by reducing vascular inflammation and oxidative stress. J Nutr Biochem 24(8):1453–1461

    Article  CAS  Google Scholar 

  21. Justo M, Claro C, Vila E, Herrera M, Rodriguez-Rodriguez R (2014) Microvascular disorders in obese Zucker rats are restored by a rice bran diet. Nutr Metab Cardiovasc Dis 24(5):524–531

    Article  CAS  Google Scholar 

  22. Candiracci M, Justo M, Castaño A, Rodriguez-Rodriguez R, Herrera M (2014) Rice bran enzymatic extract-supplemented diets modulate adipose tissue inflammation markers in Zucker rats. Nutrition 30(4):466–472

    Article  CAS  Google Scholar 

  23. Mingorance C, Sotomayor M, Jimenez-Palacios F, Mochón M, Casto C, Marhuenda E et al (2009) Effects of chronic treatment with the CB1 antagonist, rimonabant on the blood pressure, and vascular reactivity of obese Zucker rats. Obesity 17(7):1340–1347

    CAS  Google Scholar 

  24. Rodriguez-Rodriguez R, Herrera M, de Sotomayor M, Ruiz-Gutierrez V (2007) Pomace olive oil improves endothelial function in spontaneously hypertensive rats by increasing endothelial nitric oxide synthase expression. Am J Hypertens 20(7):728–734

    Article  CAS  Google Scholar 

  25. Cicero A, Gaddi A (2001) Rice bran oil and gamma-oryzanol in the treatment of hyperlipoproteinaemias and other conditions. Phytother Res 15(4):277–289

    Article  CAS  Google Scholar 

  26. Wang Y, Jones P, Pischel I, Fairow C (2003) Effects of policosanols and phytosterols on lipid levels and cholesterol biosynthesis in hamsters. Lipids 38(2):165–170

    Article  CAS  Google Scholar 

  27. Wilson T, Nicolosi R, Woolfrey B, Kritchevsky D (2007) Rice bran oil and oryzanol reduce plasma lipid and lipoprotein cholesterol concentrations and aortic cholesterol ester accumulation to a greater extent than ferulic acid in hypercholesterolemic hamsters. J Nutr Biochem 18(2):105–112

    Article  CAS  Google Scholar 

  28. Shirakawa H, Koseki T, Hashizume K, Komai M et al (2007) The Driselase-treated fraction of rice bran is a more effective dietary factor to improve hypertension, glucose and lipid metabolism in stroke-prone spontaneously hypertensive rats compared to ferulic acid. Br J Nutr 97(1):67–76

    Article  Google Scholar 

  29. Islam M, Murata T, Fujisawa M, Nagasaka R, Ushio H, Bari A et al (2008) Anti-inflammatory effects of phytosteryl ferulates in colitis induced by dextran sulphate sodium in mice. Br J Pharmacol 154(4):812–824

    Article  CAS  Google Scholar 

  30. Manosroi A, Chutoprapat R, Abe M, Manosroi W, Manosroi J (2012) Anti-aging efficacy of topical formulations containing niosomes entrapped with rice bran bioactive compounds. Pharm Biol 50(2):208–224

    Article  CAS  Google Scholar 

  31. Kesh S, Sikder K, Manna K, Das D, Khan A, Das N et al (2013) Promising role of ferulic acid, atorvastatin and their combination in ameliorating high fat diet-induced stress in mice. Life Sci 92(17):938–949

    Article  CAS  Google Scholar 

  32. Revilla E, Maria C, Miramontes E, Bautista J, García-Martínez A, Cremades O et al (2009) Nutraceutical composition, antioxidant activity and hypocholesterolemic effect of a water-soluble enzymatic extract from rice bran. Food Res Int 42(3):387–393

    Article  CAS  Google Scholar 

  33. Minhajuddin M, Beg ZH, Iqbal J (2005) Hypolipidemic and antioxidant properties of tocotrienol rich fraction isolated from rice bran oil in experimentally induced hyperlipidemic rats. Food Chem Toxicol 43:747–753

    Article  CAS  Google Scholar 

  34. Qureshi AA, Sami SA, Salser WA, Khan FA (2002) Dose-dependent suppression of serum cholesterol by tocotrienol-rich fraction (TRF25) of rice bran in hypercholesterolemic humans. Atherosclerosis 161:199–207

    Article  CAS  Google Scholar 

  35. Odegaard J, Chawla A (2013) Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis. Science 339(6116):172–177

    Article  CAS  Google Scholar 

  36. Waki H, Tontonoz P (2007) Endocrine functions of adipose tissue. Annu Rev Pathol Mech Dis 2:31–56

    Article  CAS  Google Scholar 

  37. Tilg H, Moschen A (2008) Inflammatory mechanisms in the regulation of insulin resistance. Mol Med 14(3–4):222

    CAS  Google Scholar 

  38. Rotter V, Nagaev I, Smith U (2003) Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. J Biol Chem 278(46):45777–45784

    Article  CAS  Google Scholar 

  39. Olefsky J, Glass C (2010) Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72:219–246

    Article  CAS  Google Scholar 

  40. Nakatsuji H, Kishida K, Sekimoto R, Komura N, Kihara S, Funahashi T et al (2014) Accumulation of adiponectin in inflamed adipose tissues of obese mice. Metabolism 63(4):542–553

    Article  CAS  Google Scholar 

  41. Campbell S, Stone W, Whaley S, Qui M, Krishnan K (2003) Gamma-tocopherol upregulates peroxisome proliferator activated receptor (PPAR)-gamma expression in SW 480 human colon cancer cell lines. BMC Cancer 3(1):25

    Article  Google Scholar 

  42. Ortuño Sahagún D, Márquez-Aguirre A, Quintero-Fabian S, López-Roa R, Rojas-Mayorquín A (2012) Modulation of PPAR-gamma by nutraceutics as complementary treatment for obesity-related disorders and inflammatory diseases. PPAR Res 2012:318613

    Article  Google Scholar 

  43. Westerbacka J, Corner A, Kannisto K, Kolak M, Makkonen J, Korsheninnikova E et al (2006) Acute in vivo effects of insulin on gene expression in adipose tissue in insulin-resistant and insulin-sensitive subjects. Diabetologia 49(1):132–140

    Article  CAS  Google Scholar 

  44. Imam M, Ismail M, Ithnin H, Tubesha Z, Omar A (2013) Effects of germinated brown rice and its bioactive compounds on the expression of the peroxisome proliferator-activated receptor gamma gene. Nutrients 5(2):468–477

    Article  Google Scholar 

  45. Ho J, Son M, Lim W, Lim S, Cho H (2013) Germinated brown rice extract inhibits adipogenesis through the down-regulation of adipogenic genes in 3T3-L1 adipocytes. Plant Foods Hum Nutr 68(3):274–278

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the Spanish Ministry of Science and Innovation (AGL2009-1159). M.L. Justo is a recipient of a FPU Fellowship from the Spanish Government. Part of the experiments showed in this study was made in a short stay supported by the Spanish Government and supervised by the professor Dr. Stulnig and its research group in the Medical University of Vienna (Austria).

Grants, sponsors and funding sources

This research was supported by The Spanish Ministry of Science and Technology (AGL2009-1159). Justo ML has been a recipient of a FPU fellowship from the Spanish Government.

Author information

Author notes

  1. Rosalía Rodríguez-Rodríguez

    Present address: Basic Sciences Department, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya (UiC), Josep Trueta s/n, 08195, Sant Cugat del Vallés, Barcelona, Spain

Authors and Affiliations

  1. Department of Pharmacology, School of Pharmacy, University of Seville, C/Profesor Garcia-Gonzalez 2, 41012, Seville, Spain

    Maria Luisa Justo, Carmen Claro, María Dolores Herrera & Rosalía Rodríguez-Rodríguez

  2. Department of Health Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya (UiC), Sant Cugat del Vallés, Spain

    Rosalía Rodríguez-Rodríguez

  3. Christian Doppler Laboratory for Cardio-Metabolic Immunotherapy and Clinical Division for Endocrinology and Metabolism, Department of Medicine III, Medical University Vienna, 1090, Vienna, Austria

    Maximilian Zeyda & Thomas M. Stulnig

Authors
  1. Maria Luisa Justo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carmen Claro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maximilian Zeyda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas M. Stulnig
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. María Dolores Herrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rosalía Rodríguez-Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosalía Rodríguez-Rodríguez.

Ethics declarations

Conflict of interest

The authors confirm that this article content has no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 126 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Justo, M.L., Claro, C., Zeyda, M. et al. Rice bran prevents high-fat diet-induced inflammation and macrophage content in adipose tissue. Eur J Nutr 55, 2011–2019 (2016). https://doi.org/10.1007/s00394-015-1015-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-015-1015-x

Keywords

Search

Navigation