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European Journal of Nutrition

, Volume 56, Issue 3, pp 1003–1016 | Cite as

Effect of a trans fatty acid-enriched diet on biochemical and inflammatory parameters in Wistar rats

  • Rafael LonghiEmail author
  • Roberto Farina Almeida
  • Letiane Machado
  • Maria Marta Medeiros Frescura Duarte
  • Débora Guerini Souza
  • Priscila Machado
  • Adriano Martimbianco de Assis
  • André Quincozes-Santos
  • Diogo Onofre Souza
Original Contribution

Abstract

Purpose

Recent data regarding trans fatty acids (TFAs) have implicated these lipids as particularly deleterious to human health, causing systemic inflammation, endothelial dysfunction and possibly inflammation in the central nervous system (CNS). We aimed to clarify the impact of partially hydrogenated soybean oil (PHSO) with different TFA concentrations on cerebrospinal fluid (CSF), serum and hepatic parameters in adult Wistar rats.

Methods

Wistar rats (n = 15/group) were fed either a normolipidic diet or a hyperlipidic diet for 90 days. The normolipidic and hyperlipidic diets had the same ingredients except for fat compositions, concentrations and calories. We used lard in the cis fatty acid group and PHSO in the trans fatty acid group. The intervention groups were as follows: (1) low lard (LL), (2) high lard (HL), (3) low partially hydrogenated soybean oil (LPHSO) and (4) high partially hydrogenated soybean oil (HPHSO). Body weight, lipid profiles and the inflammatory responses in the CSF, serum and liver tissue were analyzed.

Results

Surprisingly, with the PHSO diet we observed a worse metabolic response that was associated with oxidative stress in hepatic tissue as well as impaired serum and CSF fluid parameters at both PHSO concentrations. In many analyses, there were no significant differences between the LPHSO and HPHSO diets.

Conclusions

Dietary supplementation with PHSO impaired inflammatory parameters in CSF and blood, induced insulin resistance, altered lipid profiles and caused hepatic damage. Overall, these findings suggest that fat composition is more important than the quantity of fat consumed in terms of cis and trans fatty acid diets.

Keywords

Obesity Hydrogenated vegetable oils Proinflammatory Brain function 

Abbreviations

AD

Alzheimer’s disease

ALT

Alanine aminotransferase

AST

Aspartate aminotransferase

BMI

Body mass index

CVD

Cardiovascular disease

CAT

Catalase

CNS

Central nervous system

CSF

Cerebrospinal fluid

DIO

Diet-induced obesity

GPx

Glutathione peroxidase

HDL

High-density lipoprotein cholesterol

HFD

High-fat diet

HL

High lard

HPHSO

High partially hydrogenated soybean oil

IL1

Interleukin 1

IL6

Interleukin 6

IL10

Interleukin 10

LDL

Low-density lipoprotein cholesterol

LL

Low lard

LPHSO

Low partially hydrogenated soybean oil

NAFLD

Nonalcoholic fatty liver disease

NASH

Nonalcoholic steatohepatitis

OxLDL

Oxidized low-density lipoprotein

PHSO

Partially hydrogenated soybean oil

SOD

Superoxide dismutase

TFA

Trans fatty acid

TNF-α

Tumor necrosis factor alpha

Notes

Acknowledgments

This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS), Instituto Nacional de Ciência e Tecnologia para Excitoxicidade e Neuroproteção (INCTEN) and Universidade Federal do Rio Grande do Sul (UFRGS).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. 1.
    Kris-Etherton PM, Lefevre M, Mensink RP, Petersen B, Fleming J, Flickinger BD (2012) Trans fatty acid intakes and food sources in the U.S. population: NHANES 1999–2002. Lipids 47(10):931–940. doi: 10.1007/s11745-012-3704-z CrossRefGoogle Scholar
  2. 2.
    Brouwer IA, Wanders AJ, Katan MB (2010) Effect of animal and industrial trans fatty acids on HDL and LDL cholesterol levels in humans–a quantitative review. PLoS One 5(3):e9434. doi: 10.1371/journal.pone.0009434 CrossRefGoogle Scholar
  3. 3.
    Chardigny JM, Destaillats F, Malpuech-Brugere C, Moulin J, Bauman DE, Lock AL, Barbano DM, Mensink RP, Bezelgues JB, Chaumont P, Combe N, Cristiani I, Joffre F, German JB, Dionisi F, Boirie Y, Sebedio JL (2008) Do trans fatty acids from industrially produced sources and from natural sources have the same effect on cardiovascular disease risk factors in healthy subjects? Results of the trans fatty acids collaboration (TRANSFACT) study. Am J Clin Nutr 87(3):558–566Google Scholar
  4. 4.
    Tzeng YZ, Hu CH (2014) Radical-induced Cis-Trans isomerization of fatty acids: a theoretical study. J Phys Chem A 118(25):4554–4564. doi: 10.1021/jp502434t CrossRefGoogle Scholar
  5. 5.
    Wang Y, Proctor SD (2013) Current issues surrounding the definition of trans-fatty acids: implications for health, industry and food labels. Br J Nutr 110(8):1369–1383. doi: 10.1017/S0007114513001086 CrossRefGoogle Scholar
  6. 6.
    Tokede OA, Petrone AB, Hanson NQ, Tsai MY, Weir NA, Glynn RJ, Gaziano JM, Djousse L (2013) Plasma phospholipid trans fatty acids and risk of heart failure. Am J Clin Nutr 97(4):698–705. doi: 10.3945/ajcn.112.050120 CrossRefGoogle Scholar
  7. 7.
    Nestel P (2014) Trans fatty acids: Are its cardiovascular risks fully appreciated? Clin Ther 36(3):315–321. doi: 10.1016/j.clinthera.2014.01.020 CrossRefGoogle Scholar
  8. 8.
    Mozaffarian D, Abdollahi M, Campos H, Houshiarrad A, Willett WC (2007) Consumption of trans fats and estimated effects on coronary heart disease in Iran. Eur J Clin Nutr 61(8):1004–1010. doi: 10.1038/sj.ejcn.1602608 CrossRefGoogle Scholar
  9. 9.
    Brunzell JD, Davidson M, Furberg CD, Goldberg RB, Howard BV, Stein JH, Witztum JL (2008) Lipoprotein management in patients with cardiometabolic risk: consensus conference report from the American diabetes association and the American college of cardiology foundation. J Am Coll Cardiol 51(15):1512–1524. doi: 10.1016/j.jacc.2008.02.034 CrossRefGoogle Scholar
  10. 10.
    Okada Y, Tsuzuki Y, Ueda T, Hozumi H, Sato S, Hokari R, Kurihara C, Watanabe C, Tomita K, Komoto S, Kawaguchi A, Nagao S, Miura S (2013) Trans fatty acids in diets act as a precipitating factor for gut inflammation? J Gastroenterol Hepatol 28(Suppl 4):29–32. doi: 10.1111/jgh.12270 CrossRefGoogle Scholar
  11. 11.
    Lichtenstein AH (2014) Dietary trans fatty acids and cardiovascular disease risk: past and present. Curr Atheroscler Rep 16(8):433. doi: 10.1007/s11883-014-0433-1 CrossRefGoogle Scholar
  12. 12.
    Han SN, Leka LS, Lichtenstein AH, Ausman LM, Schaefer EJ, Meydani SN (2002) Effect of hydrogenated and saturated, relative to polyunsaturated, fat on immune and inflammatory responses of adults with moderate hypercholesterolemia. J Lipid Res 43(3):445–452Google Scholar
  13. 13.
    Smit LA, Katan MB, Wanders AJ, Basu S, Brouwer IA (2011) A high intake of trans fatty acids has little effect on markers of inflammation and oxidative stress in humans. J Nutr 141(9):1673–1678. doi: 10.3945/jn.110.134668 CrossRefGoogle Scholar
  14. 14.
    Aronis KN, Khan SM, Mantzoros CS (2012) Effects of trans fatty acids on glucose homeostasis: a meta-analysis of randomized, placebo-controlled clinical trials. Am J Clin Nutr 96(5):1093–1099. doi: 10.3945/ajcn.112.040576 CrossRefGoogle Scholar
  15. 15.
    Yuan X, Desiderio DM (2005) Proteomics analysis of human cerebrospinal fluid. J Chromatogr B 815(1–2):179–189. doi: 10.1016/j.jchromb.2004.06.044 CrossRefGoogle Scholar
  16. 16.
    Arnoldussen IA, Kiliaan AJ, Gustafson DR (2014) Obesity and dementia: adipokines interact with the brain. Eur Neuropsychopharmacol 24(12):1982–1999. doi: 10.1016/j.euroneuro.2014.03.002 CrossRefGoogle Scholar
  17. 17.
    Lampa J, Westman M, Kadetoff D, Agreus AN, Le Maitre E, Gillis-Haegerstrand C, Andersson M, Khademi M, Corr M, Christianson CA, Delaney A, Yaksh TL, Kosek E, Svensson CI (2012) Peripheral inflammatory disease associated with centrally activated IL-1 system in humans and mice. Proc Natl Acad Sci USA 109(31):12728–12733. doi: 10.1073/pnas.1118748109 CrossRefGoogle Scholar
  18. 18.
    Morris MC, Evans DA, Tangney CC, Bienias JL, Schneider JA, Wilson RS, Scherr PA (2006) Dietary copper and high saturated and trans fat intakes associated with cognitive decline. Arch Neurol 63(8):1085–1088. doi: 10.1001/archneur.63.8.1085 CrossRefGoogle Scholar
  19. 19.
    Dorfman SE, Laurent D, Gounarides JS, Li X, Mullarkey TL, Rocheford EC, Sari-Sarraf F, Hirsch EA, Hughes TE, Commerford SR (2009) Metabolic implications of dietary trans-fatty acids. Obesity (Silver Spring) 17(6):1200–1207. doi: 10.1038/oby.2008.662 Google Scholar
  20. 20.
    Andersson A, Nalsen C, Tengblad S, Vessby B (2002) Fatty acid composition of skeletal muscle reflects dietary fat composition in humans. Am J Clin Nutr 76(6):1222–1229Google Scholar
  21. 21.
    Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112(12):1796–1808. doi: 10.1172/JCI19246112/12/1796 CrossRefGoogle Scholar
  22. 22.
    Martin CA, Visentainer JV, Oliveira ANd, Oliveira CCd, Matsushita M, Souza NEd (2008) Fatty acid contents of Brazilian soybean oils with emphasis on trans fatty acids. J Braz Chem Soc 19:117–122CrossRefGoogle Scholar
  23. 23.
    dos Santos B, Estadella D, Hachul AC, Okuda MH, Moreno MF, Oyama LM, Ribeiro EB, Oller do Nascimento CM (2013) Effects of a diet enriched with polyunsaturated, saturated, or trans fatty acids on cytokine content in the liver, white adipose tissue, and skeletal muscle of adult mice. Mediators Inflamm 2013:594958. doi: 10.1155/2013/594958 Google Scholar
  24. 24.
    Almeida RF, Cereser VH Jr, Faraco RB, Bohmer AE, Souza DO, Ganzella M (2010) Systemic administration of GMP induces anxiolytic-like behavior in rats. Pharmacol Biochem Behav 96(3):306–311. doi: 10.1016/j.pbb.2010.05.022 CrossRefGoogle Scholar
  25. 25.
    Holvoet P, Stassen JM, Van Cleemput J, Collen D, Vanhaecke J (1998) Oxidized low density lipoproteins in patients with transplant-associated coronary artery disease. Arterioscler Thromb Vasc Biol 18(1):100–107CrossRefGoogle Scholar
  26. 26.
    Wu R, Lefvert AK (1995) Autoantibodies against oxidized low density lipoproteins (OxLDL): characterization of antibody isotype, subclass, affinity and effect on the macrophage uptake of OxLDL. Clin Exp Immunol 102(1):174–180CrossRefGoogle Scholar
  27. 27.
    Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18(6):499–502Google Scholar
  28. 28.
    Hansel G, Tonon AC, Guella FL, Pettenuzzo LF, Duarte T, Duarte MM, Oses JP, Achaval M, Souza DO (2014) Guanosine protects against cortical focal ischemia involvement of inflammatory response. Mol Neurobiol 52(3):1791–1803. doi: 10.1007/s12035-014-8978-0 CrossRefGoogle Scholar
  29. 29.
    de Assis AM, Rech A, Longoni A, da Silva Morrone M, de Bittencourt Pasquali MA, Perry MLS, Souza DO, Moreira JCF (2015) Dietary n-3 polyunsaturated fatty acids revert renal responses induced by a combination of 2 protocols that increase the amounts of advanced glycation end product in rats. Nutr Res 35(6):512–522. doi: 10.1016/j.nutres.2015.04.013 CrossRefGoogle Scholar
  30. 30.
    de Souza CG, Sattler JA, de Assis AM, Rech A, Perry ML, Souza DO (2012) Metabolic effects of sulforaphane oral treatment in streptozotocin-diabetic rats. J Med Food 15(9):795–801. doi: 10.1089/jmf.2012.0016 CrossRefGoogle Scholar
  31. 31.
    Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509Google Scholar
  32. 32.
    de Assis AM, Rech A, Longoni A, Rotta LN, Denardin CC, Pasquali MA, Souza DO, Perry ML, Moreira JC (2012) Ω3-Polyunsaturated fatty acids prevent lipoperoxidation, modulate antioxidant enzymes, and reduce lipid content but do not alter glycogen metabolism in the livers of diabetic rats fed on a high fat thermolyzed diet. Mol Cell Biochem 361(1–2):151–160. doi: 10.1007/s11010-011-1099-4 CrossRefGoogle Scholar
  33. 33.
    Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefGoogle Scholar
  34. 34.
    Boveris A (1984) Determination of the production of superoxide radicals and hydrogen peroxide in mitochondria. Methods Enzymol 105:429–435CrossRefGoogle Scholar
  35. 35.
    Wendel A (1981) Glutathione peroxidase. Methods Enzymol 77:325–333CrossRefGoogle Scholar
  36. 36.
    de Bittencourt Pasquali MA, Roberto de Oliveira M, De Bastiani MA, da Rocha RF, Schnorr CE, Gasparotto J, Gelain DP, Moreira JC (2012) L-NAME co-treatment prevent oxidative damage in the lung of adult Wistar rats treated with vitamin A supplementation. Cell Biochem Funct 30(3):256–263CrossRefGoogle Scholar
  37. 37.
    Bachorik PS, Albers JJ (1986) Precipitation methods for quantification of lipoproteins. Methods Enzymol 129:78–100CrossRefGoogle Scholar
  38. 38.
    Baierle M, Nascimento SN, Moro AM, Brucker N, Freitas F, Gauer B, Durgante J, Bordignon S, Zibetti M, Trentini CM, Duarte MM, Grune T, Breusing N, Garcia SC (2015) Relationship between inflammation and oxidative stress and cognitive decline in the institutionalized elderly. Oxid Med Cell Longev 2015:804198. doi: 10.1155/2015/804198 CrossRefGoogle Scholar
  39. 39.
    Sain J, Gonzalez MA, Lasa A, Scalerandi MV, Bernal CA, Portillo MP (2013) Effects of trans-fatty acids on liver lipid metabolism in mice fed on diets showing different fatty acid composition. Ann Nutr Metab 62(3):242–249. doi: 10.1159/000339453 CrossRefGoogle Scholar
  40. 40.
    Field CJ, Blewett HH, Proctor S, Vine D (2009) Human health benefits of vaccenic acid. Appl Physiol Nutr Metab 34(5):979–991. doi: 10.1139/H09-079 CrossRefGoogle Scholar
  41. 41.
    Tarkowski E, Andreasen N, Tarkowski A, Blennow K (2003) Intrathecal inflammation precedes development of Alzheimer’s disease. J Neurol Neurosurg Psychiatry 74(9):1200–1205CrossRefGoogle Scholar
  42. 42.
    Kankaanpaa J, Turunen SP, Moilanen V, Horkko S, Remes AM (2009) Cerebrospinal fluid antibodies to oxidized LDL are increased in Alzheimer’s disease. Neurobiol Dis 33(3):467–472. doi: 10.1016/j.nbd.2008.12.001 CrossRefGoogle Scholar
  43. 43.
    Hu N, Yu JT, Tan L, Wang YL, Sun L, Tan L (2013) Nutrition and the risk of Alzheimer’s disease. Biomed Res Int 2013:524820. doi: 10.1155/2013/524820 Google Scholar
  44. 44.
    Morris MC, Evans DA, Bienias JL, Tangney CC, Bennett DA, Aggarwal N, Schneider J, Wilson RS (2003) Dietary fats and the risk of incident Alzheimer disease. Arch Neurol 60(2):194–200CrossRefGoogle Scholar
  45. 45.
    Grimm MO, Rothhaar TL, Grosgen S, Burg VK, Hundsdorfer B, Haupenthal VJ, Friess P, Kins S, Grimm HS, Hartmann T (2012) Trans fatty acids enhance amyloidogenic processing of the Alzheimer amyloid precursor protein (APP). J Nutr Biochem 23(10):1214–1223. doi: 10.1016/j.jnutbio.2011.06.015 CrossRefGoogle Scholar
  46. 46.
    Klementiev B, Li S, Korshunova I, Dmytriyeva O, Pankratova S, Walmod PS, Kjaer LK, Dahllof MS, Lundh M, Christensen DP, Mandrup-Poulsen T, Bock E, Berezin V (2014) Anti-inflammatory properties of a novel peptide interleukin 1 receptor antagonist. J Neuroinflammation 11:27. doi: 10.1186/1742-2094-11-27 CrossRefGoogle Scholar
  47. 47.
    Wullschleger A, Kapina V, Molnarfi N, Courvoisier DS, Seebach JD, Santiago-Raber ML, Hochstrasser DF, Lalive PH (2013) Cerebrospinal fluid interleukin-6 in central nervous system inflammatory diseases. PLoS One 8(8):e72399. doi: 10.1371/journal.pone.0072399PONE-D-13-14313 CrossRefGoogle Scholar
  48. 48.
    He Z, Guo Q, Xiao M, He C, Zou W (2013) Intrathecal lentivirus-mediated transfer of interleukin-10 attenuates chronic constriction injury-induced neuropathic pain through modulation of spinal high-mobility group box 1 in rats. Pain Physician 16(5):E615–E625Google Scholar
  49. 49.
    Woodcock T, Morganti-Kossmann MC (2013) The role of markers of inflammation in traumatic brain injury. Front Neurol 4:18. doi: 10.3389/fneur.2013.00018 CrossRefGoogle Scholar
  50. 50.
    Yan EB, Hellewell SC, Bellander BM, Agyapomaa DA, Morganti-Kossmann MC (2011) Post-traumatic hypoxia exacerbates neurological deficit, neuroinflammation and cerebral metabolism in rats with diffuse traumatic brain injury. J Neuroinflammation 8:147. doi: 10.1186/1742-2094-8-147 CrossRefGoogle Scholar
  51. 51.
    Lessa NM, Nakajima VM, Matta SL, Peluzio MC, Sabarense CM, Costa NM (2010) Deposition of trans fatty acid from industrial sources and its effect on different growth phases in rats. Ann Nutr Metab 57(1):23–34. doi: 10.1159/000314080 CrossRefGoogle Scholar
  52. 52.
    Duque-Guimaraes DE, de Castro J, Martinez-Botas J, Sardinha FL, Ramos MP, Herrera E, do Carmo M (2009) Early and prolonged intake of partially hydrogenated fat alters the expression of genes in rat adipose tissue. Nutrition 25(7–8):782–789. doi: 10.1016/j.nut.2008.12.004 CrossRefGoogle Scholar
  53. 53.
    Estadella D, da Penha Oller do Nascimento CM, Oyama LM, Ribeiro EB, Damaso AR, de Piano A (2013) Lipotoxicity: effects of dietary saturated and transfatty acids. Mediators Inflamm 2013:137579. doi: 10.1155/2013/137579 CrossRefGoogle Scholar
  54. 54.
    Tardy AL, Lambert-Porcheron S, Malpuech-Brugere C, Giraudet C, Rigaudiere JP, Laillet B, Leruyet P, Peyraud JL, Boirie Y, Laville M, Michalski MC, Chardigny JM, Morio B (2009) Dairy and industrial sources of trans fat do not impair peripheral insulin sensitivity in overweight women. Am J Clin Nutr 90(1):88–94. doi: 10.3945/ajcn.2009.27515 CrossRefGoogle Scholar
  55. 55.
    Zhang W, Wang LW, Wang LK, Li X, Zhang H, Luo LP, Song JC, Gong ZJ (2013) Betaine protects against high-fat-diet-induced liver injury by inhibition of high-mobility group box 1 and Toll-like receptor 4 expression in rats. Dig Dis Sci 58(11):3198–3206. doi: 10.1007/s10620-013-2775-x CrossRefGoogle Scholar
  56. 56.
    Kawano Y, Cohen DE (2013) Mechanisms of hepatic triglyceride accumulation in non-alcoholic fatty liver disease. J Gastroenterol 48(4):434–441. doi: 10.1007/s00535-013-0758-5 CrossRefGoogle Scholar
  57. 57.
    Cho YY, Kwon EY, Kim HJ, Jeon SM, Lee KT, Choi MS (2011) Differential effect of corn oil-based low trans structured fat on the plasma and hepatic lipid profile in an atherogenic mouse model: comparison to hydrogenated trans fat. Lipids Health Dis 10:15. doi: 10.1186/1476-511X-10-15 CrossRefGoogle Scholar
  58. 58.
    Koppe SW, Elias M, Moseley RH, Green RM (2009) Trans fat feeding results in higher serum alanine aminotransferase and increased insulin resistance compared with a standard murine high-fat diet. Am J Physiol Gastrointest Liver Physiol 297(2):G378–G384. doi: 10.1152/ajpgi.90543.2008 CrossRefGoogle Scholar
  59. 59.
    Park EM, Ramnath N, Yang GY, Ahn JY, Park Y, Lee TY, Shin HS, Yu J, Ip C, Park YM (2007) High superoxide dismutase and low glutathione peroxidase activities in red blood cells predict susceptibility of lung cancer patients to radiation pneumonitis. Free Radic Biol Med 42(2):280–287. doi: 10.1016/j.freeradbiomed.2006.10.044 CrossRefGoogle Scholar
  60. 60.
    Shah SS, Shah GB, Singh SD, Gohil PV, Chauhan K, Shah KA, Chorawala M (2011) Effect of piperine in the regulation of obesity-induced dyslipidemia in high-fat diet rats. Indian J Pharmacol 43(3):296–299. doi: 10.4103/0253-7613.81516IJPharm-43-296 CrossRefGoogle Scholar
  61. 61.
    Jia YJ, Liu J, Guo YL, Xu RX, Sun J, Li JJ (2013) Dyslipidemia in rat fed with high-fat diet is not associated with PCSK9-LDL-receptor pathway but ageing. J Geriatr Cardiol 10(4):361–368. doi: 10.3969/j.issn.1671-5411.2013.04.007jgc-10-04-361 Google Scholar
  62. 62.
    Maric T, Woodside B, Luheshi GN (2014) The effects of dietary saturated fat on basal hypothalamic neuroinflammation in rats. Brain Behav Immun 36:35–45. doi: 10.1016/j.bbi.2013.09.011 CrossRefGoogle Scholar
  63. 63.
    Sarvas JL, Niccoli S, Walser E, Khaper N, Lees SJ (2014) Interleukin-6 deficiency causes tissue-specific changes in signaling pathways in response to high-fat diet and physical activity. Physiol Rep 2(7):e12064. doi: 10.14814/phy2.12064 CrossRefGoogle Scholar
  64. 64.
    Matthews VB, Allen TL, Risis S, Chan MH, Henstridge DC, Watson N, Zaffino LA, Babb JR, Boon J, Meikle PJ, Jowett JB, Watt MJ, Jansson JO, Bruce CR, Febbraio MA (2006) Interleukin-6-deficient mice develop hepatic inflammation and systemic insulin resistance. Diabetologia 53(11):2431–2441. doi: 10.1007/s00125-010-1865-y CrossRefGoogle Scholar
  65. 65.
    Pedersen BK, Febbraio MA (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88(4):1379–1406. doi: 10.1152/physrev.90100.2007 CrossRefGoogle Scholar
  66. 66.
    Cho HK, Kim SY, Yoo SK, Choi YH, Cheong J (2014) Fatty acids increase hepatitis B virus X protein stabilization and HBx-induced inflammatory gene expression. FEBS J 281(9):2228–2239. doi: 10.1111/febs.12776 CrossRefGoogle Scholar
  67. 67.
    Hong EG, Ko HJ, Cho YR, Kim HJ, Ma Z, Yu TY, Friedline RH, Kurt-Jones E, Finberg R, Fischer MA, Granger EL, Norbury CC, Hauschka SD, Philbrick WM, Lee CG, Elias JA, Kim JK (2009) Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes 58(11):2525–2535. doi: 10.2337/db08-1261 CrossRefGoogle Scholar
  68. 68.
    Charles BA, Doumatey A, Huang H, Zhou J, Chen G, Shriner D, Adeyemo A, Rotimi CN (2011) The roles of IL-6, IL-10, and IL-1RA in obesity and insulin resistance in African–Americans. J Clin Endocrinol Metab 96(12):E2018–E2022. doi: 10.1210/jc.2011-1497 CrossRefGoogle Scholar
  69. 69.
    Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444(7121):860–867. doi: 10.1038/nature05485 CrossRefGoogle Scholar
  70. 70.
    Ding S, Chi MM, Scull BP, Rigby R, Schwerbrock NM, Magness S, Jobin C, Lund PK (2010) High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PLoS One 5(8):e12191. doi: 10.1371/journal.pone.0012191 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Rafael Longhi
    • 1
    Email author
  • Roberto Farina Almeida
    • 1
  • Letiane Machado
    • 1
  • Maria Marta Medeiros Frescura Duarte
    • 2
  • Débora Guerini Souza
    • 1
  • Priscila Machado
    • 1
  • Adriano Martimbianco de Assis
    • 1
  • André Quincozes-Santos
    • 1
  • Diogo Onofre Souza
    • 1
  1. 1.Department of Biochemistry, Postgraduate Program in Biochemistry, Institute of Basic Health SciencesFederal University of Rio Grande do Sul (UFRGS)Porto AlegreBrazil
  2. 2.Health Sciences CenterLutheran University of Brazil (ULBRA)Santa MariaBrazil

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