Skip to main content
Log in

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

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

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.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

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. Dandona P, Aljada A, Bandyopadhyay A (2004) Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 25:4–7

    Article  CAS  Google Scholar 

  2. Wellen KE, Hotamisligil GS (2003) Obesity-induced inflammatory changes in adipose tissue. J Clin Invest 112:1785–1788

    CAS  Google Scholar 

  3. Shoelson SE, Herrero L, Naaz A (2007) Obesity, inflammation, and insulin resistance. Gastroenterology 132:2169–2180

    Article  CAS  Google Scholar 

  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 141:1083–1093

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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 258:138–146

    Article  CAS  Google Scholar 

  7. Standal T, Borset M, Sundan A (2004) Role of osteopontin in adhesion, migration, cell survival and bone remodeling. Exp Oncol 26:179–184

    CAS  Google Scholar 

  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 7:491–502

    Article  CAS  Google Scholar 

  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 72:55–63

    CAS  Google Scholar 

  10. Weber GF, Cantor H (1996) The immunology of Eta-1/osteopontin. Cytokine Growth Factor Rev 7:241–248

    Article  CAS  Google Scholar 

  11. Mazzali M, Kipari T, Ophascharoensuk V, Wesson JA, Johnson R, Hughes J (2002) Osteopontin—a molecule for all seasons. QJM 95:3–13

    Article  CAS  Google Scholar 

  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 32:410–416

    CAS  Google Scholar 

  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 107:679–681

    Article  CAS  Google Scholar 

  14. Ramaiah SK, Rittling S (2008) Pathophysiological role of osteopontin in hepatic inflammation, toxicity, and cancer. Toxicol Sci 103:4–13

    Article  CAS  Google Scholar 

  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 149:1350–1357

    Article  CAS  Google Scholar 

  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 92:3719–3727

    Article  CAS  Google Scholar 

  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:e13959

    Article  Google Scholar 

  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 117:2877–2888

    Article  CAS  Google Scholar 

  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 59:935–946

    Article  CAS  Google Scholar 

  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 85:2402–2410

    Article  CAS  Google Scholar 

  21. Mather K (2009) Surrogate measures of insulin resistance: of rats, mice, and men. Am J Physiol Endocrinol Metab 296:E398–E399

    Article  CAS  Google Scholar 

  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) 16:811–818

    Article  CAS  Google Scholar 

  23. Tschop M, Heiman ML (2001) Rodent obesity models: an overview. Exp Clin Endocrinol Diabetes 109:307–319

    Article  CAS  Google Scholar 

  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 99:385–390

    Article  Google Scholar 

  25. Buettner R, Scholmerich J, Bollheimer LC (2007) High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 15:798–808

    Article  CAS  Google Scholar 

  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–R730

    CAS  Google Scholar 

  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–E903

    Article  CAS  Google Scholar 

  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 39:262–267

    Article  CAS  Google Scholar 

  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 39:1177–1185

    Article  CAS  Google Scholar 

  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–R1118

    CAS  Google Scholar 

  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 36:485–501

    Article  CAS  Google Scholar 

  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 112:1821–1830

    CAS  Google Scholar 

  33. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444:860–867

    Article  CAS  Google Scholar 

  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 112:1796–1808

    CAS  Google Scholar 

  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 74:443–477

    Article  CAS  Google Scholar 

  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 58:125–133

    Article  CAS  Google Scholar 

  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 72:752–761

    CAS  Google Scholar 

  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 152:2219–2227

    Article  CAS  Google Scholar 

  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 447:1116–1120

    Article  CAS  Google Scholar 

  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 283:22620–22627

    Article  CAS  Google Scholar 

  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 48:2365–2375

    Article  CAS  Google Scholar 

  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 16:674–683

    Article  CAS  Google Scholar 

  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 306:457–461

    Article  Google Scholar 

  44. Cullinan SB, Diehl JA (2006) Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell B 38:317–332

    Article  CAS  Google Scholar 

  45. Maziere C, Gomila C, Maziere JC (2010) Oxidized low-density lipoprotein increases osteopontin expression by generation of oxidative stress. Free Radical Bio Med 48:1382–1387

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by National Natural Science Foundation of China (No. 30671765) and Scientific Research Foundation for Returned overseas Chinese Scholars, Ministry of Education of China (No. 20101561).

Conflict of interest

The authors have declared no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nianhong Yang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, X., Cheng, M., Zhao, M. et al. 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. Eur J Nutr 52, 1181–1189 (2013). https://doi.org/10.1007/s00394-012-0428-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-012-0428-z

Keywords

Navigation