Differential effects of high-fish oil and high-lard diets on cells and cytokines involved in the inflammatory process in rat insulin-sensitive tissues

International Journal of Molecular Sciences

Volumn 15, Issue 2, 2014, Pages 3040-3063

  Lionetti, Lillà ^a   Mollica, Maria Pina ^a   Sica, Raffaella ^a   Donizzetti, Immacolata ^a   Gifuni, Giorgio ^a   Pignalosa, Angelica ^a   Cavaliere, Gina ^a   Putti, Rosalba ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Adipokines; Dietary fat source; MCP1; TGF 1; SMA

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; CYTOKINE; FISH OIL; GLUCOSE; LARD; LEPTIN; LIPID; TUMOR NECROSIS FACTOR ALPHA; ACTIN; EDIBLE OIL; GLUCOSE BLOOD LEVEL; INSULIN; MONOCYTE CHEMOTACTIC PROTEIN 1; SMOOTH MUSCLE ACTIN, RAT;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIET; ELECTROPHORESIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FATTY LIVER; FIBROGENESIS; FOOD INTAKE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INSULIN RESISTANCE; NONHUMAN; RAT; SERUM; SKELETAL MUSCLE; STELLATE CELL; WESTERN BLOTTING; ANALYSIS; ANIMAL; BLOOD; CYTOLOGY; GLUCOSE BLOOD LEVEL; LIPID DIET; LIVER; MALE; METABOLISM; PATHOLOGY; WHITE ADIPOSE TISSUE; WISTAR RAT;

ACTINS; ADIPOKINES; ADIPONECTIN; ADIPOSE TISSUE, WHITE; ANIMALS; BLOOD GLUCOSE; CHEMOKINE CCL2; DIET, HIGH-FAT; DIETARY FATS, UNSATURATED; HEPATIC STELLATE CELLS; IMMUNOHISTOCHEMISTRY; INSULIN; LEPTIN; LIVER; MALE; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; RATS; RATS, WISTAR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84894269846     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15023040     Document Type: Article

References (55)

1. Wellen, K.E.; Hotamisligil, G.S. Obesity-induced inflammatory changes in adipose tissue. J. Clin. Invest. 2003, 112, 1785-1788.
2. Lionetti, L.; Mollica, M.P.; Lombardi, A.; Cavaliere, G.; Gifuni, G.; Barletta, A. From chronic overnutrition to insulin resistance: The role of fat-storing capacity and inflammation. Nutr. Metab. Cardiovasc. Dis. 2009, 19, 146-152.
3. Mollica, M.P.; Lionetti, L.; Putti, R.; Cavaliere, G.; Gaita, M.; Barletta, A. From chronic overfeeding to hepatic injury: Role of endoplasmic reticulum stress and inflammation. Nutr. Metab. Cardiovasc. Dis. 2011, 21, 222-230.
4. Sethi, J.K.; Vidal-Puig, A.J. Adipose tissue function and plasticity orchestrate nutritional adaptation. J. Lip. Res. 2007, 48, 1253-1262.
5. Abete, I.; Goyenechea, E.; Zulet, M.A.; Martínez, J.A. Obesity and metabolic syndrome: Potential benefit from specific nutritional components. Nutr. Metab. Cardiovasc. Dis. 2011, 21, B1-B15.
6. Gonzalez-Periz, A.; Horrillo, R.; Ferre, N.; Gronert, K.; Dong, B.; Morán-Salvador, E.; Titos, E.; Martínez-Clemente, M.; López-Parra, M.; Arroyo, V.; et al. Obesity-induced insulin resistance and hepatic steatosis are alleviated by omega-3 fatty acids: A role for resolvins and protectins. FASEB J. 2009, 23, 1946-1957.
7. Nakatani, T.; Kim, H.J.; Kaburagi, Y.; Yasuda, K.; Ezaki, O. A low fish oil inhibits SREBP-1 proteolytic cascade, while a high-fish-oil feeding decreases SREBP-1 mRNA in mice liver: Relationship to anti-obesity. J. Lip. Res. 2003, 44, 369-379.
8. Xin, Y.N.; Xuan, S.Y.; Zhang, J.H.; Zheng, M.H.; Guan, H.S. Omega-3 polyunsaturated fatty acids: A specific liver drug for non-alcoholic fatty liver disease (NAFLD). Med. Hypotheses. 2008, 71, 820-821.
9. Calder, P.C. Long-chain fatty acids and inflammation. Proc. Natl. Acad. Sci. 2012, 71, 284-289.
10. Kalupahana, N.S.; Claycombe, K.J.; Moustaid-Moussa, N. (n-3) Fatty acids alleviate adipose tissue inflammation and insulin resistance: mechanistic insights. Adv. Nutr. 2011, 2, 304-316.
11. Saidpour, A.; Zahediasl, S.; Kimiagar, M.; Vafa, M.; Ghasemi, A.; Abadi, A.; Daneshpour, M.S.; Zarkesh, M. Fish oil and olive oil can modify insulin resistance and plasma desacyl-ghrelin in rats. J. Res. Med. Sci. 2011, 16, 862-871.
12. Storlien, L.H.; Kraegen, E.W.; Chisholm, D.J.; Ford, G.L.; Bruce, D.G.; Pascoe, W.S. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science 1987, 237, 885-888.
13. Ghafoorunissa, I.A.; Rajkumar, L.; Acharya, V. Dietary (n-3) long chain polyunsaturated fatty acids prevent sucrose-induced insulin resistance in rats. J. Nutr. 2005, 135, 2634-2638.
14. Flachs, P.; Mohamed-Ali, V.; Horakova, O.; Rossmeisl, M.; Hosseinzadeh-Attar, M.J.; Hensler, M.; Ruzickova, J.; Kopecky, J. Polyunsaturated fatty acids of marine origin induce adiponectin in mice fed a high-fat diet. Diabetologia 2006, 49, 394-397.
15. Saraswathi, V.; Morrow, J.D.; Hasty, A.H. Dietary fish oil exerts hypolipidemic effects in lean and insulin sensitizing effects in obese LDLR-/-mice. J. Nutr. 2009, 139, 2380-2386.
16. Kalupahana, N.S.; Claycombe, K.; Newman, S.; Stewart, T.; Siriwardhana, N.; Matthan, N.; Lichtenstein, A.H.; Moustaid-Moussa, N. Eicosapentaenoic acid prevents and reverses insulin resistance in high-fat diet-induced obese mice via modulation of adipose tissue inflammation. J. Nutr. 2010, 140, 1915-1922.
17. Lionetti, L.; Cavaliere, G.; Trinchese, G.; De Filippo, C.; Gifuni, G.; Gaita, M.; Pignalosa, A.; Donizzetti, I.; Putti, R.; Barletta, A. Effects of endoplasmic reticulum (ER) stress on insulin action and mitochondrial energy efficiency in skeletal muscle of rats fed with lard or fish oil. Obesity Facts 2012, 5, S1, 133.
18. Lionetti, L.; Mollica, M.P.; Sica, R.; Donizzetti, I.; Gifuni, G.; Pignalosa, A.; Cavaliere, G.; Putti, R. Hepatic mitochondrial bioenergetic and dynamic behaviour adaptations in response to high-fat feeding. BBA Bioenergetics 2012, 1817, S73.
19. Murata, M.; Kaji, H.; Takahashi, Y.; Iida, K.; Mizuno, I.; Okimura, Y.; Abe, H.; Chihara, K. Stimulation by eicosapentaenoic acids of leptin mRNA expression and its secretion in mouse 3T3-L1 adipocytes in vitro. Biochem. Biophys. Res. Commun. 2000, 270, 343-348.
20. Pérez-Matute, P.; Marti, A.; Martínez, J.A.; Fernández-Otero, M.P.; Stanhope, K.L.; Havel, P.J.; Moreno-Aliaga, M.J. Eicosapentaenoic fatty acid increases leptin secretion from primary cultured rat adipocytes: Role of glucose metabolism. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288, R1682-R1688.
21. Reseland, J.E.; Haugen, F.; Hollung, K.; Solvoll, K.; Halvorsen, B.; Brude, I.R.; Nenseter, M.S.; Christiansen, E.N.; Drevon, C.A. Reduction of leptin gene expression by dietary polyunsaturated fatty acids. J. Lip. Res. 2001, 42, 743-750.
22. Tishinsky, J.M.; Ma, D.W.; Robinson, L.E. Eicosapentaenoic acid and rosiglitazone increase adiponectin in an additive and PPARγ-dependent manner in human adipocytes. Obesity 2011, 19, 262-268.
23. Luo, J.; Rizkalla, S.W.; Boillot, J.; Alamowitch, C.; Chaib, H.;, Bruzzo, F.; Desplanque, N.; Dalix, A.M.; Durand, G.; Slama, G. Dietary (n-3) polyunsaturated fatty acids improve adipocyte insulin action and glucose metabolism in insulin-resistant rats: relation to membrane fatty acids. J. Nutr. 1996, 126, 1951-1958.
24. Cinti, S.; Mitchell, G.; Barbatelli, G.; Murano, I.; Ceresi, E.; Faloia, E.; Wang, S.; Fortier, M.; Greenberg, A.S.; Obin, M.S. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lip. Res. 2005, 46, 2347-2355.
25. Weisberg, S.P.; McCann, D.; Desai, M.; Rosenbaum, M.; Leibel, R.L.; Ferrante, A.W., Jr. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112, 1796-1808.
26. Sartipy, P.; Loskutoff, D.J. Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proc. Natl. Acad. Sci. 2003, 100, 7265-7270.
27. Kanda, H.; Tateya, S.; Tamori, Y.; Kotani, K.; Hiasa, K.; Kitazawa, R.; Kitazawa, S.; Miyachi, H.; Maeda, S.; Egashira, K.; et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J. Clin. Invest. 2006, 116, 1494-1505.
28. Matsushima, K.; Larsen, C.G.; DuBois, G.C.; Oppenheim, J.J. Purification and characterization of a novel monocyte chemotactic and activating factor produced by a human myelomonocytic cell line. J. Exp. Med. 1989, 169, 1485-1490.
29. Xu, H.; Barnes, G.T.; Yang, Q.; Tan, G.; Yang, D.; Chou, C.J.; Sole, J.; Nichols, A.; Ross, J.S.; Tartaglia, L.A.; et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 2003, 112, 1821-1830.
30. Samad, F.; Yamamoto, K.; Pandey, M.; Loskutoff, D.J. Elevated expression of transforming growth factor-β in adipose tissue from obese mice. Mol. Med. 1997, 3, 37-48.
31. Sciarretta, S.; Ferrucci, A.; Ciavarella, G.M.; De Paolis, P.; Venturelli, V.; Tocci, G.; De Biase, L.; Rubattu, S.; Volpe, M. Markers of inflammation and fibrosis are related to cardiovascular damage in hypertensive patients with metabolic syndrome. Am. J. Hypert. 2007, 20, 784-791.
32. Tan, C.K.; Chong, H.C.; Tan, E.H.; Tan, N.S. Getting "Smad" about obesity and diabetes. Nutr. Diabetes 2012, 2, e29-e35.
33. Lumeng, C.N.; Bodzin, J.L.; Saltiel, A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 2007, 117, 175-184.
34. Fujisaka, S.; Usui, I.; Bukhari, A.; Ikutani, M.; Oya, T.; Kanatani, Y.; Tsuneyama, K.; Nagai, Y.; Takatsu, K.; Urakaze, M.; et al. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 2009, 58, 2574-2582.
35. Figueras, M.; Olivan, M.; Busquets, S.; López-Soriano, F.J.; Argilés, J.M. Effects of eicosapentaenoic acid (EPA) treatment on insulin sensitivity in an animal model of diabetes: improvement of the inflammatory status. Obesity 2011, 19, 362-369.
36. Hendrich, S. (n-3) Fatty acids: Clinical trials in people with type 2 diabetes. Adv. Nutr. 2010, 1, 3-7.
37. Puglisi, M.J.; Hasty A.H. Saraswathi V. The role of adipose tissue in mediating the beneficial effects of dietary fish oil. J. Nutr. Biochem. 2011, 22, 101-108.
38. Auwerx J. PPARgamma, the ultimate thrifty gene. Diabetologia 1999, 42, 1033-1049.
39. Banga, A.; Unal, R.; Tripathi, P.; Pokrovskaya, I.; Owens, R.J.; Kern, P.A.; Ranganathan, G. Adiponectin translation is increased by the PPARgamma agonists pioglitazone and omega-3 fatty acids. Am. J. Physiol. Endocrinol. MeTable 2009, 296, E480-E489.
40. Folch, J.; Lees, M.; Stanley, G.H.S. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957, 226, 497-510.
41. Sato, S.; Hughes, C. Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. J. Biol. Chem. 1994, 269, 4424-4430.
42. Li, P.; Lu, M.; Nguyen, M.T., Bae, E.J.; Chapman, J.; Feng, D.; Hawkins, M.; Pessin, J.E.; Sears, D.D.; Nguyen, A.K.; et al. Functional heterogeneity of CD11c-positive adipose tissue macrophages in diet-induced obese mice. J. Biol. Chem. 2010, 285, 15333-15345.
43. Spencer, M.; Yao-Borengasser, A.; Unal, R.; Rasouli, N.; Gurley, C.M.; Zhu, B.; Peterson, C.A.; Kern, P.A. Adipose tissue macrophages in insulin-resistant subjects are associated with collagen IV and fibrosis and demonstrate alternative activation. Am. J. Physiol. 2010, 299, E1016-E1027.
44. Sun, K.; Kusminski, C.M.; Scherer, P.E. Adipose tissue remodeling and obesity. J. Clin. Invest. 2011, 121, 2094-2101.
45. Lionetti, L.; Sica, R.; Mollica, M.P.; Putti, R. High-lard and high-fish oil diets differ in their effects on insulin resistance development, mitochondrial morphology and dynamic behaviour in rat skeletal muscle. Food Nutr. Sci. 2013, 4, 105-112.
46. Yamauchi, T.; Kamon, J.; Minokoshi, Y.; Ito, Y.; Waki, H.; Uchida, S. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 2002, 8, 1288-1295.
47. Henderson, N.C.; Mackinnon, A.C.; Farnworth, S.L.; Poirier, F.; Russo, F.P.; Iredale, J.P.; Haslett, C.; Simpson, K.J.; Sethi, T. Galectin-3 regulates myofibroblast activation and hepatic fibrosis. Proc. Natl. Acad. Sci. 2006, 103, 5060-5065.
48. Gaca, M.D. Regulation of hepatic stellate cell proliferation and collagen synthesis by proteinase-activated. J. Hepat. 2002, 36, 362-369.
49. Sarem, M.; Znaidak, R.; Macías, M.; Rey, R. Hepatic stellate cell: It is role in normal and pathological conditions. Gastroenter. Hepat. 2006, 29, 93-101.
50. Hotamisligil, G.S. Inflammation and metabolic disorders. Nature 2006, 444, 860-867.
51. Long, Y.C.; Zierath, J.R. AMP-activated protein kinase signaling in metabolic regulation. J. Clin. Invest. 2006, 116, 1776-1783.
52. Iossa, S.; Lionetti, L.; Mollica, M.P.; Crescenzo, R.; Botta, M.; Barletta, A.; Liverini, G. Effect of high-fat feeding on metabolic efficiency and mitochondrial oxidative capacity in adult rats. Br. J. Nutr. 2003, 90, 953-960.
53. De Lange, P.; Cioffi, F.; Senese, R.; Moreno, M.; Lombardi, A.; Silvestri, E.; De Matteis, R.; Lionetti, L.; Mollica, M.P.; Goglia, F.; et al. Nonthyrotoxic prevention of diet-induced insulin resistance by 3,5-diiodo-L-thyronine in rats. Diabetes 2011, 60, 2730-2739.
54. Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680-685.
55. Towbin, H.; Staehelintl, T.; Gordon, J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. 1979, 76, 4350-4354.