Abstract
Purpose
Obesity is an inflammatory-related disease, which recruits immune system cells triggering to imbalanced production of cytokines. Obesity management and treatment using foods bioactive compounds have gained clinical and scientific relevance. Juçara (Euterpe edulis Mart.) fruit is rich in fibers, unsaturated lipids and, anthocyanins showing potential health benefits. Thus, we investigated the effect of juçara pulp intake on inflammatory status of monocytes from obese individuals.
Methods
It is a placebo-controlled, randomized double-blind trial. Twenty-seven obese participants (BMI between 30.0 and 39.9 kg/m2) of both genders from 31 to 59-year-old, divided into two groups: 5 g juçara freeze-dried pulp or 5 g of placebo for 6 weeks. Before and after supplementation, blood samples were collected and monocytes obtained and stimulated with lipopolysaccharides. After 24 h of incubation, the cells and supernatants were analyzed.
Results
Post-treatment, juçara reduced TLR4, and IL-6 mRNA compared to placebo. Juçara also increased IL-10 mRNA in post-treatment. The protein expression of TLR4 pathway post-treatment, MYD88 expression reduced in juçara group compared to placebo. The juçara post-treatment reduced pIKKα/β compared to the placebo. Ob-R protein levels were higher in the juçara group post-treatment compared to pre-treatment. IL-6, TNF-α, and MCP-1 production by monocytes were reduced by juçara in post-treatment compared to pre-treatment levels. The supplementation increased IL-10 in juçara group with LPS compared to pre-treatment and versus juçara group without LPS.
Conclusion
These results demonstrated a proinflammatory state at the beginning, which was improved by juçara pulp consumption. Our results suggest juçara pulp as a potential tool against the proinflammatory status of obesity.
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References
Engin AB (2017) Adipocyte-macrophage cross-talk in obesity. In: Engin AB, Engin A (eds) Obesity and lipotoxicity. Springer International Publishing, Cham, pp 327–343
Dey A, Allen J, Hankey-Giblin PA (2015) Ontogeny and polarization of macrophages in inflammation: blood monocytes versus tissue macrophages. Front Immunol 6:1–15. https://doi.org/10.3389/fimmu.2014.00683
Kraakman MJ, Murphy AJ, Jandeleit-Dahm K, Kammoun HL (2014) Macrophage polarization in obesity and type 2 diabetes: weighing down our understanding of macrophage function? Front Immunol 5:1–6. https://doi.org/10.3389/fimmu.2014.00470
Lovren F, Pan Y, Quan A et al (2010) Adiponectin primes human monocytes into alternative anti-inflammatory M2 macrophages. AJP Heart Circ Physiol 299:H656–H663. https://doi.org/10.1152/ajpheart.00115.2010
Brikos C, O’Neill LAJ (2008) Signalling of toll-like receptors. Handb Exp Pharmacol 183:21–50. https://doi.org/10.1007/978-3-540-72167-3-2
O’Neill LAJ (2008) The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol Rev 226:10–18. https://doi.org/10.1111/j.1600-065X.2008.00701.x
Gribar SC, Anand RJ, Sodhi CP, Hackam DJ (2008) The role of epithelial Toll-like receptor signaling in the pathogenesis of intestinal inflammation. J Leukoc Biol 83:493–498. https://doi.org/10.1189/jlb.0607358
Jialal I, Kaur H, Devaraj S (2014) Toll-like receptor status in obesity and metabolic syndrome: a translational perspective. J Clin Endocrinol Metab 99:39–48. https://doi.org/10.1210/jc.2013-3092
Kim K-A, Gu W, Lee I-A et al (2012) High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One 7:e47713. https://doi.org/10.1371/journal.pone.0047713
Da Silva NA, Rodrigues E, Mercadante AZ, De Rosso VV (2014) Phenolic compounds and carotenoids from four fruits native from the Brazilian Atlantic forest. J Agric Food Chem 62:5072–5084. https://doi.org/10.1021/jf501211p
Silva P, Carmo L, Silva G et al (2013) Physical, chemical, and lipid composition of juçara (Euterpe edulis Mart.) Pulp. Braz J Food Nutr 24:7–13
Sousa De Brito E, De Araújo MCP, Alves RE et al (2007) Anthocyanins present in selected tropical fruits: acerola, jambolão, jussara, and guajiru. J Agric Food Chem 55:9389–9394. https://doi.org/10.1021/jf0715020
Menaa F (2015) The berry fruit açai (Euterpe oleracea Mart): bringing Health benefits and exotism to the modern table. Adv Food Technol Nutr Sci Open J 1:1–4. https://doi.org/10.17140/AFTNSOJ-1-101
Santamarina AB, Jamar G, Mennitti LV et al (2018) The use of juçara (Euterpe edulis Mart.) supplementation for suppression of NF-κB pathway in the hypothalamus after high-fat diet in Wistar rats. Molecules (Basel, Switzerland) 23:1–13. https://doi.org/10.3390/molecules23071814
Argentato PP, Morais CA, Santamarina AB et al (2017) Jussara (Euterpe edulis Mart.) supplementation during pregnancy and lactation modulates UCP-1 and inflammation biomarkers induced by trans-fatty acids in the brown adipose tissue of offspring. Clin Nutr Exp 12:50–65. https://doi.org/10.1016/j.yclnex.2016.12.002
Almeida Morais C, Oyama LM, De Oliveira JL et al (2014) Jussara (Euterpe edulis Mart.) supplementation during pregnancy and lactation modulates the gene and protein expression of inflammation biomarkers induced by trans-fatty acids in the colon of offspring. Mediat Inflamm 2014:1–11. https://doi.org/10.1155/2014/987927
Oyama LM, Silva FP, Carnier J et al (2016) Jucąra pulp supplementation improves glucose tolerance in mice. Diabetol Metab Syndr 8:1–8. https://doi.org/10.1186/s13098-015-0122-4
Morais CA, Oyama LM, de Moura Conrado R et al (2015) Polyphenols-rich fruit in maternal diet modulates inflammatory markers and the gut microbiota and improves colonic expression of ZO-1 in offspring. Food Res Int 77:186–193. https://doi.org/10.1016/j.foodres.2015.06.043
Jamar G, Santamarina AB, Mennitti LV et al (2018) Bifidobacterium spp. reshaping in the gut microbiota by low dose of juçara supplementation and hypothalamic insulin resistance in Wistar rats. J Funct Foods 46:212–219. https://doi.org/10.1016/j.jff.2018.05.002
WHO (2000) Obesity: preventing and managing the global epidemic. Report of a WHO consultation
Haun R, José Gondim Pitanga F, Lessa I (2009) Razão Cintura/estatura Comparado a outros indicadores antropométricos de obesidade como preditor de risco coronário elevado. Artigo Original Rev Assoc Med Bras 55:705–711. https://doi.org/10.1590/S0104-42302009000600015
Santamarina AB, Jamar G, Mennitti LV et al (2018) Supplementation of juçara berry (Euterpe edulis Mart.). Modulates epigenetic markers in monocytes from obese adults: a double-blind randomized trial. Nutrients 10:1899. https://doi.org/10.3390/nu10121899
Inada KOP, Oliveira AA, Revorêdo TB et al (2015) Screening of the chemical composition and occurring antioxidants in jabuticaba (Myrciaria jaboticaba) and jussara (Euterpe edulis) fruits and their fractions. J Funct Foods 17:422–433. https://doi.org/10.1016/j.jff.2015.06.002
Felzenszwalb I, da Costa Marques MR, Mazzei JL, Aiub CAF (2013) Toxicological evaluation of Euterpe edulis: a potential superfruit to be considered. Food Chem Toxicol 58:536–544. https://doi.org/10.1016/j.fct.2013.05.029
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Faul F, Erdfelder E, Lang A-G, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39, pp. 175–191. https://doi.org/10.3758/BF03193146
Lancaster GI, Langley KG, Berglund NA et al (2018) Evidence that TLR4 is not a receptor for saturated fatty acids but mediates lipid-induced inflammation by reprogramming macrophage metabolism. Cell Metab 27:1096–1110.e5. https://doi.org/10.1016/j.cmet.2018.03.014
Arner P, Kulyté A (2015) MicroRNA regulatory networks in human adipose tissue and obesity. Nat Rev Endocrinol 11:276–288. https://doi.org/10.1038/nrendo.2015.25
Nunez Lopez YO, Garufi G, Seyhan AA (2017) Altered levels of circulating cytokines and microRNAs in lean and obese individuals with prediabetes and type 2 diabetes. Mol Biosyst 13:106–121. https://doi.org/10.1039/C6MB00596A
Marques-Rocha JL, Samblas M, Milagro FI et al (2015) Noncoding RNAs, cytokines, and inflammation-related diseases. FASEB J 29:3595–3611. https://doi.org/10.1096/fj.14-260323
Pisani LP, Estadella D, Ribeiro DA (2017) The role of toll like receptors (TLRs) in oral carcinogenesis. Anticancer Res 37:5389–5394. https://doi.org/10.21873/anticanres.11965
Estadella D, da Penha Oller do Nascimento CM, Oyama LM et al (2013) Lipotoxicity: effects of dietary saturated and transfatty acids. Mediat Inflamm 2013:1–13. https://doi.org/10.1155/2013/137579
Kang L, Heng W, Yuan A et al (2010) Resveratrol modulates adipokine expression and improves insulin sensitivity in adipocytes: relative to inhibition of inflammatory responses. Biochimie 92:789–796. https://doi.org/10.1016/j.biochi.2010.02.024
Kang NE, Ha AW, Kim JY, Kim WK (2012) Resveratrol inhibits the protein expression of transcription factors related adipocyte differentiation and the activity of matrix metalloproteinase in mouse fibroblast 3T3–L1 preadipocytes. Nutr Res Pract 6:499–504. https://doi.org/10.4162/nrp.2012.6.6.499
Valenti L, Riso P, Mazzocchi A et al (2013) Dietary anthocyanins as nutritional therapy for nonalcoholic fatty liver disease. Oxid Med Cell Longev. https://doi.org/10.1155/2013/145421
Hassellund SS, Flaa A, Kjeldsen SE et al (2013) Effects of anthocyanins on cardiovascular risk factors and inflammation in pre-hypertensive men: a double-blind randomized placebo-controlled crossover study. J Hum Hypertens 27:100–106. https://doi.org/10.1038/jhh.2012.4
Azzini E, Giacometti J, Russo GL (2017) Antiobesity effects of anthocyanins in preclinical and clinical studies. Oxid Med Cell Longev 1:1. https://doi.org/10.1155/2017/2740364
Campión J, Milagro FI, Goyenechea E, Martínez JA (2009) TNF-α promoter methylation as a predictive biomarker for weight-loss response. Obesity 17:1293–1297. https://doi.org/10.1038/oby.2008.679
Naranjo MC, Bermudez B, Garcia I et al (2017) Dietary fatty acids on aortic root calcification in mice with metabolic syndrome. Food Funct 8:1468–1474. https://doi.org/10.1039/c7fo00143f
Neele AE, Van Den Bossche J, Hoeksema MA, De Winther MPJ (2015) Epigenetic pathways in macrophages emerge as novel targets in atherosclerosis. Eur J Pharmacol 763:79–89. https://doi.org/10.1016/j.ejphar.2015.03.101
Boden G (2011) NIH Public Access. Curr Opin Endocrinol Diabetes Obes 18:139–143. https://doi.org/10.1097/MED.0b013e3283444b09.45Obesity
Woo HM, Kang JH, Kawada T et al (2007) Active spice-derived components can inhibit inflammatory responses of adipose tissue in obesity by suppressing inflammatory actions of macrophages and release of monocyte chemoattractant protein-1 from adipocytes. Life Sci 80:926–931. https://doi.org/10.1016/j.lfs.2006.11.030
Lira FS, Rosa JC, Dos Santos RV et al (2011) Visceral fat decreased by long-term interdisciplinary lifestyle therapy correlated positively with interleukin-6 and tumor necrosis factor-α and negatively with adiponectin levels in obese adolescents. Metab Clin Exp 60:359–365. https://doi.org/10.1016/j.metabol.2010.02.017
Palacz-Wrobel M, Borkowska P, Paul-Samojedny M et al (2017) Effect of apigenin, kaempferol and resveratrol on the gene expression and protein secretion of tumor necrosis factor alpha (TNF-α) and interleukin-10 (IL-10) in RAW-264.7 macrophages. Biomed Pharmacother 93:1205–1212. https://doi.org/10.1016/j.biopha.2017.07.054
Lovren F, Pan Y, Quan A et al (2010) Adiponectin primes human monocytes into alternative anti-inflammatory M2 macrophages. AJP Heart Circ Physiol 299:H656–H663. https://doi.org/10.1152/ajpheart.00115.2010
Klok MD, Jakobsdottir S, Drent ML (2007) The role of leptin and ghrelin in the regulation of food intake and body weight in humans: a review. Obes Rev 8:21–34. https://doi.org/10.1111/j.1467-789X.2006.00270.x
Matarese G, Moschos S, Mantzoros CS (2005) Leptin in immunology. J Immunol 174:3137–3142. https://doi.org/10.4049/jimmunol.174.6.3137
Otero M, Lago R, Gomez R et al (2006) Towards a pro-inflammatory and immunomodulatory emerging role of leptin. Rheumatology 45:944–950. https://doi.org/10.1093/rheumatology/kel157
Różańska D, Regulska-Ilow B (2018) The significance of anthocyanins in the prevention and treatment of type 2 diabetes. Adv Clin Exp Med 27:135–142. https://doi.org/10.17219/acem/64983
da Costa GF, Santos IB, de Bem GF et al (2017) The beneficial effect of anthocyanidin-rich Vitis vinifera L. grape skin extract on metabolic changes induced by high-fat diet in mice involves antiinflammatory and antioxidant actions. Phytother Res 31:1621–1632. https://doi.org/10.1002/ptr.5898
de Bem GF, Costa CA, Santos IB et al (2018) Antidiabetic effect of Euterpe oleracea Mart. (acai) extract and exercise training on high-fat diet and streptozotocin-induced diabetic rats: a positive interaction. PLoS One 13:e0199207. https://doi.org/10.1371/journal.pone.0199207
Crujeiras AB, Carreira MC, Cabia B et al (2015) Leptin resistance in obesity: an epigenetic landscape. Life Sci 140:57–63. https://doi.org/10.1016/j.lfs.2015.05.003
Acknowledgements
The authors acknowledge to Dylbert Fragoso Silvestre for technical assistance on the English language. Part of these results was previously presented as a conference abstract, in the 25th European Congress on Obesity by the authors.
Funding
Supported by Fundação de Amparo à Pesquisa do Estado de São Paulo, (2016/14133-0; 2015/13875-0). LPP, LMO, VVR and JRV are recipients of CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) fellowship.
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LPP, LMO and VVR designed the study protocol; ABS, LVM, HCC, and GJ conducted experiments and analyzed data. LPP and ABS critically revised the article for important intellectual content; LPP and ABS contributed to writing the manuscript.
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The study procedures were in accordance with the guidelines set in the International Declaration of Helsinki and approved by the Ethics Committee of the Universidade Federal de São Paulo (CEP-UNIFESP No. 0319/2017) and registered in Plataforma Brasil database. The written informed consent was obtained from all volunteers.
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Santamarina, A.B., Jamar, G., Mennitti, L.V. et al. Obesity-related inflammatory modulation by juçara berry (Euterpe edulis Mart.) supplementation in Brazilian adults: a double-blind randomized controlled trial. Eur J Nutr 59, 1693–1705 (2020). https://doi.org/10.1007/s00394-019-02024-2
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DOI: https://doi.org/10.1007/s00394-019-02024-2