European Journal of Nutrition

, Volume 52, Issue 3, pp 1181–1189 | Cite as

Differential effects of high-fat-diet rich in lard oil or soybean oil on osteopontin expression and inflammation of adipose tissue in diet-induced obese rats

  • Xiaoke Wang
  • Mengjie Cheng
  • Min Zhao
  • Aiguo Ge
  • Fangfang Guo
  • Min Zhang
  • Yanhong Yang
  • Liegang Liu
  • Nianhong Yang
Original Contribution

Abstract

Purpose

To examine the effect of different dietary fat types on osteopontin (OPN) expressions and inflammation of adipose tissues in diet-induced obese rats.

Methods

Male Sprague–Dawley rats were randomly assigned to one control group fed standard diet (LF, n = 10) and two high-fat diet groups fed isoenergy diet rich in lard or soybean oil (HL or HS, n = 45 each). Diet-induced obese rats in HL and HS group were then subdivided into two groups either continuously fed high-fat diet or switched to low-fat diet for 8 more weeks. Fasting serum glucose, insulin, and OPN concentrations were assayed and QUICKI was calculated; the expression of OPN, IL-6, IL-10, TNF-α, NF-κB, and F4/80 in adipose tissue was determined.

Results

Both high-fat diets lead to comparable development of obesity characterized by insulin resistance and adipose tissue inflammation. Obese rats continuously fed high-fat diet rich in lard oil exhibited the highest fasting serum insulin level and adipose tissue OPN, F4/80, TNF-α, and NF-κB expression level. In both high-fat diet groups, switching to low-fat diet resulted in less intra-abdominal fat mass, decreased expression of F4/80, TNF-α, and NF-κB, while decreased OPN expression was only observed in lard oil fed rats after switching to low-fat diet.

Conclusions

Reducing diet fat or replacing lard oil with soybean oil in high-fat diet alleviates obesity-related inflammation and insulin resistance by attenuating the upregulation of OPN and macrophage infiltration into adipose tissue induced by high-fat diet.

Keywords

Diet-induced obese Inflammation Insulin resistance Osteopontin High-fat diet Soybean oil Lard oil 

Abbreviations

GAPDH

Glyceraldehyde 3-phosphate dehydrogenase

HL

High-fat diet rich in lard

HS

High-fat diet rich in soybean oil

LF

Low-fat standard chow

MUFA

Monounsaturated fatty acid

NF-κB

Nuclear factor kappa B

OPN

Osteopontin

PPARγ

Peroxisome proliferator-activated receptor gamma

PUFA

Polyunsaturated fatty acids

QUICKI

Quantitative insulin sensitivity check index

TNF-α

Tumor necrosis factor-α

IL-6

Interleukin-6

IL-10

Interleukin-10

References

  1. 1.
    Dandona P, Aljada A, Bandyopadhyay A (2004) Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 25:4–7CrossRefGoogle Scholar
  2. 2.
    Wellen KE, Hotamisligil GS (2003) Obesity-induced inflammatory changes in adipose tissue. J Clin Invest 112:1785–1788Google Scholar
  3. 3.
    Shoelson SE, Herrero L, Naaz A (2007) Obesity, inflammation, and insulin resistance. Gastroenterology 132:2169–2180CrossRefGoogle Scholar
  4. 4.
    Scatena M, Almeida M, Chaisson ML, Fausto N, Nicosia RF, Giachelli CM (1998) NF-kappaB mediates alphavbeta3 integrin-induced endothelial cell survival. J Cell Biol 141:1083–1093CrossRefGoogle Scholar
  5. 5.
    Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117:175–184CrossRefGoogle Scholar
  6. 6.
    Bassaganya-Riera J, Misyak S, Guri AJ, Hontecillas R (2009) PPAR gamma is highly expressed in F4/80(hi) adipose tissue macrophages and dampens adipose-tissue inflammation. Cell Immunol 258:138–146CrossRefGoogle Scholar
  7. 7.
    Standal T, Borset M, Sundan A (2004) Role of osteopontin in adhesion, migration, cell survival and bone remodeling. Exp Oncol 26:179–184Google Scholar
  8. 8.
    Young MF, Kerr JM, Termine JD, Wewer UM, Wang MG, McBride OW, Fisher LW (1990) cDNA cloning, mRNA distribution and heterogeneity, chromosomal location, and RFLP analysis of human osteopontin (OPN). Genomics 7:491–502CrossRefGoogle Scholar
  9. 9.
    Saitoh Y, Kuratsu J, Takeshima H, Yamamoto S, Ushio Y (1995) Expression of osteopontin in human glioma. Its correlation with the malignancy. Lab Invest 72:55–63Google Scholar
  10. 10.
    Weber GF, Cantor H (1996) The immunology of Eta-1/osteopontin. Cytokine Growth Factor Rev 7:241–248CrossRefGoogle Scholar
  11. 11.
    Mazzali M, Kipari T, Ophascharoensuk V, Wesson JA, Johnson R, Hughes J (2002) Osteopontin—a molecule for all seasons. QJM 95:3–13CrossRefGoogle Scholar
  12. 12.
    Xu G, Sun W, He D, Wang L, Zheng W, Nie H, Ni L, Zhang D, Li N, Zhang J (2005) Overexpression of osteopontin in rheumatoid synovial mononuclear cells is associated with joint inflammation, not with genetic polymorphism. J Rheumatol 32:410–416Google Scholar
  13. 13.
    Isoda K, Kamezawa Y, Ayaori M, Kusuhara M, Tada N, Ohsuzu F (2003) Osteopontin transgenic mice fed a high-cholesterol diet develop early fatty-streak lesions. Circulation 107:679–681CrossRefGoogle Scholar
  14. 14.
    Ramaiah SK, Rittling S (2008) Pathophysiological role of osteopontin in hepatic inflammation, toxicity, and cancer. Toxicol Sci 103:4–13CrossRefGoogle Scholar
  15. 15.
    Kiefer FW, Zeyda M, Todoric J, Huber J, Geyeregger R, Weichhart T, Aszmann O, Ludvik B, Silberhumer GR, Prager G, Stulnig TM (2008) Osteopontin expression in human and murine obesity: extensive local up-regulation in adipose tissue but minimal systemic alterations. Endocrinology 149:1350–1357CrossRefGoogle Scholar
  16. 16.
    Gomez-Ambrosi J, Catalan V, Ramirez B, Rodriguez A, Colina I, Silva C, Rotellar F, Mugueta C, Gil MJ, Cienfuegos JA, Salvador J, Fruhbeck G (2007) Plasma osteopontin levels and expression in adipose tissue are increased in obesity. J Clin Endocrinol Metab 92:3719–3727CrossRefGoogle Scholar
  17. 17.
    Chapman J, Miles PD, Ofrecio JM, Neels JG, Yu JG, Resnik JL, Wilkes J, Talukdar S, Thapar D, Johnson K, Sears DD (2010) Osteopontin is required for the early onset of high fat diet-induced insulin resistance in mice. PLoS One 5:e13959CrossRefGoogle Scholar
  18. 18.
    Nomiyama T, Perez-Tilve D, Ogawa D, Gizard F, Zhao Y, Heywood EB, Jones KL, Kawamori R, Cassis LA, Tschop MH, Bruemmer D (2007) Osteopontin mediates obesity-induced adipose tissue macrophage infiltration and insulin resistance in mice. J Clin Invest 117:2877–2888CrossRefGoogle Scholar
  19. 19.
    Kiefer FW, Zeyda M, Gollinger K, Pfau B, Neuhofer A, Weichhart T, Saemann MD, Geyeregger R, Schlederer M, Kenner L, Stulnig TM (2010) Neutralization of osteopontin inhibits obesity-induced inflammation and insulin resistance. Diabetes 59:935–946CrossRefGoogle Scholar
  20. 20.
    Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, Quon MJ (2000) Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 85:2402–2410CrossRefGoogle Scholar
  21. 21.
    Mather K (2009) Surrogate measures of insulin resistance: of rats, mice, and men. Am J Physiol Endocrinol Metab 296:E398–E399CrossRefGoogle Scholar
  22. 22.
    Li S, Zhang HY, Hu CC, Lawrence F, Gallagher KE, Surapaneni A, Estrem ST, Calley JN, Varga G, Dow ER, Chen Y (2008) Assessment of diet-induced obese rats as an obesity model by comparative functional genomics. Obesity (Silver Spring) 16:811–818CrossRefGoogle Scholar
  23. 23.
    Tschop M, Heiman ML (2001) Rodent obesity models: an overview. Exp Clin Endocrinol Diabetes 109:307–319CrossRefGoogle Scholar
  24. 24.
    Van Heek M, Compton DS, France CF, Tedesco RP, Fawzi AB, Graziano MP, Sybertz EJ, Strader CD, Davis HR Jr (1997) Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J Clin Invest 99:385–390CrossRefGoogle Scholar
  25. 25.
    Buettner R, Scholmerich J, Bollheimer LC (2007) High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 15:798–808CrossRefGoogle Scholar
  26. 26.
    Levin BE, Dunn-Meynell AA, Balkan B, Keesey RE (1997) Selective breeding for diet-induced obesity and resistance in Sprague-Dawley rats. Am J Physiol 273:R725–R730Google Scholar
  27. 27.
    Paulino G, Barbier de la Serre C, Knotts TA, Oort PJ, Newman JW, Adams SH, Raybould HE (2009) Increased expression of receptors for orexigenic factors in nodose ganglion of diet-induced obese rats. Am J Physiol Endocrinol Metab 296:E898–E903CrossRefGoogle Scholar
  28. 28.
    Wang C, Yang N, Wu S, Liu L, Sun X, Nie S (2007) Difference of NPY and its receptor gene expressions between obesity and obesity-resistant rats in response to high-fat diet. Horm Metab Res 39:262–267CrossRefGoogle Scholar
  29. 29.
    Ruzickova J, Rossmeisl M, Prazak T, Flachs P, Sponarova J, Veck M, Tvrzicka E, Bryhn M, Kopecky J (2004) Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids 39:1177–1185CrossRefGoogle Scholar
  30. 30.
    Belzung F, Raclot T, Groscolas R (1993) Fish oil n-3 fatty acids selectively limit the hypertrophy of abdominal fat depots in growing rats fed high-fat diets. Am J Physiol 264:R1111–R1118Google Scholar
  31. 31.
    Buettner R, Parhofer KG, Woenckhaus M, Wrede CE, Kunz-Schughart LA, Scholmerich J, Bollheimer LC (2006) Defining high-fat-diet rat models: metabolic and molecular effects of different fat types. J Mol Endocrinol 36:485–501CrossRefGoogle Scholar
  32. 32.
    Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112:1821–1830Google Scholar
  33. 33.
    Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444:860–867CrossRefGoogle Scholar
  34. 34.
    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 112:1796–1808Google Scholar
  35. 35.
    Fain JN (2006) Release of interleukins and other inflammatory cytokines by human adipose tissue is enhanced in obesity and primarily due to the nonfat cells. Vitam Horm 74:443–477CrossRefGoogle Scholar
  36. 36.
    Bertola A, Deveaux V, Bonnafous S, Rousseau D, Anty R, Wakkach A, Dahman M, Tordjman J, Clement K, McQuaid SE, Frayn KN, Huet PM, Gugenheim J, Lotersztajn S, Le Marchand-Brustel Y, Tran A, Gual P (2009) Elevated expression of osteopontin may be related to adipose tissue macrophage accumulation and liver steatosis in morbid obesity. Diabetes 58:125–133CrossRefGoogle Scholar
  37. 37.
    Weber GF, Zawaideh S, Hikita S, Kumar VA, Cantor H, Ashkar S (2002) Phosphorylation-dependent interaction of osteopontin with its receptors regulates macrophage migration and activation. J Leukoc Biol 72:752–761Google Scholar
  38. 38.
    Zeyda M, Gollinger K, Todoric J, Kiefer FW, Keck M, Aszmann O, Prager G, Zlabinger GJ, Petzelbauer P, Stulnig TM (2011) Osteopontin is an activator of human adipose tissue macrophages and directly affects adipocyte function. Endocrinology 152:2219–2227CrossRefGoogle Scholar
  39. 39.
    Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, Red Eagle A, Vats D, Brombacher F, Ferrante AW, Chawla A (2007) Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447:1116–1120CrossRefGoogle Scholar
  40. 40.
    Stienstra R, Duval C, Keshtkar S, van der Laak J, Kersten S, Muller M (2008) Peroxisome proliferator-activated receptor gamma activation promotes infiltration of alternatively activated macrophages into adipose tissue. J Biol Chem 283:22620–22627CrossRefGoogle Scholar
  41. 41.
    Flachs P, Horakova O, Brauner P, Rossmeisl M, Pecina P, Franssen-van Hal N, Ruzickova J, Sponarova J, Drahota Z, Vlcek C, Keijer J, Houstek J, Kopecky J (2005) Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat. Diabetologia 48:2365–2375CrossRefGoogle Scholar
  42. 42.
    Arai T, Kim HJ, Chiba H, Matsumoto A (2009) Anti-obesity effect of fish oil and fish oil-fenofibrate combination in female KK mice. J Atheroscler Thromb 16:674–683CrossRefGoogle Scholar
  43. 43.
    Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH, Hotamisligil GS (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457–461CrossRefGoogle Scholar
  44. 44.
    Cullinan SB, Diehl JA (2006) Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell B 38:317–332CrossRefGoogle Scholar
  45. 45.
    Maziere C, Gomila C, Maziere JC (2010) Oxidized low-density lipoprotein increases osteopontin expression by generation of oxidative stress. Free Radical Bio Med 48:1382–1387CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Xiaoke Wang
    • 1
  • Mengjie Cheng
    • 1
  • Min Zhao
    • 1
  • Aiguo Ge
    • 1
  • Fangfang Guo
    • 1
  • Min Zhang
    • 1
  • Yanhong Yang
    • 1
  • Liegang Liu
    • 1
  • Nianhong Yang
    • 1
  1. 1.Department of Nutrition and Food Hygiene, MOE Key Lab of Environment and Health, School of Public Health, Tongji Medical CollegeHuazhong University of Science and TechnologyWuhanPeople’s Republic of China

Personalised recommendations