Abnormal immune responses in fa/fa Zucker rats and effects of feeding conjugated linoleic acid

Obesity

Volumn 16, Issue 8, 2008, Pages 1770-1779

  Ruth, Megan R ^a   Taylor, Carla G ^b   Zahradka, Peter ^b   Field, Catherine J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CONJUGATED LINOLEIC ACID; CYTOKINE; IMMUNOGLOBULIN; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; NITRIC OXIDE; UNSATURATED FATTY ACID;

ANIMAL; ARTICLE; BODY WEIGHT; CELL CULTURE; CYTOLOGY; DIET; DISEASE MODEL; DRUG EFFECT; EATING; IMMUNE SYSTEM; IMMUNOLOGY; MALE; METABOLISM; OBESITY; PATHOPHYSIOLOGY; RAT; SPLEEN; ZUCKER RAT;

ANIMALS; BODY WEIGHT; CELLS, CULTURED; CYTOKINES; DIET; DISEASE MODELS, ANIMAL; EATING; FATTY ACIDS, UNSATURATED; IMMUNE SYSTEM; IMMUNOGLOBULINS; INTERLEUKIN-10; INTERLEUKIN-2; INTERLEUKIN-4; LINOLEIC ACIDS, CONJUGATED; MALE; NITRIC OXIDE; OBESITY; RATS; RATS, ZUCKER; SPLEEN;

RATTUS;

EID: 48749109525     PISSN: 19307381     EISSN: 1930739X     Source Type: Journal    
DOI: 10.1038/oby.2008.266     Document Type: Article

References (73)

1. Falagas ME, Kompoti M. Obesity and infection. Lancet Infect Dis 2006;6:438-446.
2. Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 2004;4:579-591.
3. Pan SY, Johnson KC, Ugnat AM, Wen SW, Mao Y. Association of obesity and cancer risk in Canada. Am J Epidemiol 2004;159:259-268.
4. Weber DJ, Rutala WA, Samsa GP, Santimaw JE, Lemon SM. Obesity as a predictor of poor antibody response to hepatitis B plasma vaccine. JAMA 1985;254:3187-3189.
5. Eliakim A, Schwindt C, Zaldivar F, Casali P, Cooper DM. Reduced tetanus antibody titers in overweight children. Autoimmunity 2006;39:137-141.
6. Ghanim H, Aljada A, Hofmeyer D et al. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation 2004;110:1564-1571.
7. Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 2005;115:911-919.
8. Skapenko A, Leipe J, Lipsky PE, Schulze-Koops H. The role of the T cell in autoimmune inflammation. Arthritis Res Ther 2005;7(Suppl 2):S4-S14.
9. Ahima RS, Osei SY. Leptin signaling. Physiol Behav 2004;81:223-241.
10. Clement K, Vaisse C, Lahlou N et al. A mutation in the human leptin receptor gene causes obesity and pituitary dysfunction. Nature 1998;392:398-401.
11. Shimizu H, Oh-I S, Okada S, Mori M. Leptin resistance and obesity. Endocr J 2007;54:17-26.
12. Kasiske BL, O'Donnell MP, Keane WF. The Zucker rat model of obesity, insulin resistance, hyperlipidemia, and renal injury. Hypertension 1992;19(1 Suppl):I110-I115.
13. Kurtz TW, Morris RC, Pershadsingh HA. The Zucker fatty rat as a genetic model of obesity and hypertension. Hypertension 1989;13:896-901.
14. Plotkin BJ, Paulson D. Zucker rat (fa/fa), a model for the study of immune function in type-II diabetes mellitus: effect of exercise and caloric restriction on the phagocytic activity of macrophages. Lab Anim Sci 1996;46:682-684.
15. Plotkin BJ, Paulson D, Chelich A et al. Immune responsiveness in a rat model for type II diabetes (Zucker rat, fa/fa): susceptibility to Candida albicans infection and leucocyte function. J Med Microbiol 1996;44:277-283.
16. Tanaka S, Isoda F, Yamakawa T, Ishihara M, Sekihara H. T lymphopenia in genetically obese rats. Clin Immunol Immunopathol 1998;86:219-225.
17. Moriguchi S, Kato M, Sakai K, Yamamoto S, Shimizu E. Decreased mitogen response of splenic lymphocytes in obese Zucker rats is associated with the decreased expression of glucose transporter 1 (GLUT-1). Am J Clin Nutr 1998;67:1124-1129.
18. Moriguchi S, Kato M, Sakai K, Yamamoto S, Shimizu E. Exercise training restores decreased cellular immune functions in obese Zucker rats. J Appl Physiol 1998;84:311-317.
19. Calder PC, Grimble RF. Polyunsaturated fatty acids, inflammation and immunity. Eur J Clin Nutr 2002;56(Suppl 3):S14-S19.
20. O'Shea M, Bassaganya-Riera J, Mohede IC. Immunomodulatory properties of conjugated linoleic acid. Am J Clin Nutr 2004;79(6 Suppl):1199S-1206S.
21. Kelley DS, Taylor PC, Rudolph IL et al. Dietary conjugated linoleic acid did not alter immune status in young healthy women. Lipids 2000;35:1065-1071.
22. Kelley DS, Simon VA, Taylor PC et al. Dietary supplementation with conjugated linoleic acid increased its concentration in human peripheral blood mononuclear cells, but did not alter their function. Lipids 2001;36:669-674.
23. Kreider RB, Ferreira MP, Greenwood M, Wilson M, Almada AL. Effects of conjugated linoleic acid supplementation during resistance training on body composition, bone density, strength, and selected hematological markers. J Strength Cond Res 2002;16:325-334.
24. Albers R, van der Wielen RP, Brink EJ et al. Effects of cis-9, trans-11 and trans-10, cis-12 conjugated linoleic acid (CLA) isomers on immune function in healthy men. Eur J Clin Nutr 2003;57:595-603.
25. Ritzenthaler KL, McGuire MK, McGuire MA et al. Consumption of conjugated linoleic acid (CLA) from CLA-enriched cheese does not alter milk fat or immunity in lactating women. J Nutr 2005;135:422-430.
26. Nugent AP, Roche HM, Noone EJ et al. The effects of conjugated linoleic acid supplementation on immune function in healthy volunteers. Eur J Clin Nutr 2005;59:742-750.
27. Tricon S, Burdge GC, Jones EL et al. Effects of dairy products naturally enriched with cis-9,trans-11 conjugated linoleic acid on the blood lipid profile in healthy middle-aged men. Am J Clin Nutr 2006;83:744-753.
28. Smedman A, Basu S, Jovinge S, Fredrikson GN, Vessby B. Conjugated linoleic acid increased C-reactive protein in human subjects. Br J Nutr 2005;94:791-795.
29. Hontecillas R, Wannemeulher MJ, Zimmerman DR et al. Nutritional regulation of porcine bacterial-induced colitis by conjugated linoleic acid. J Nutr 2002;132:2019-2027.
30. Changhua L, Jindong Y, Defa L et al. Conjugated linoleic acid attenuates the production and gene expression of proinflammatory cytokines in weaned pigs challenged with lipopolysaccharide. J Nutr 2005;135:239-244.
31. Yang M, Cook ME. Dietary conjugated linoleic acid decreased cachexia, macrophage tumor necrosis factor-alpha production, and modifies splenocyte cytokines production. Exp Biol Med (Maywood) 2003;228:51-58.
32. Riserus U, Basu S, Jovinge S et al. Supplementation with conjugated linoleic acid causes isomer-dependent oxidative stress and elevated C-reactive protein: a potential link to fatty acid-induced insulin resistance. Circulation 2002;106:1925-1929.
33. Riserus U, Vessby B, Arnlov J, Basu S. Effects of cis-9,trans-11 conjugated linoleic acid supplementation on insulin sensitivity, lipid peroxidation, and proinflammatory markers in obese men. Am J Clin Nutr 2004;80:279-283.
34. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 1993;123:1939-1951.
35. Field CJ, Ryan EA, Thomson AB, Clandinin MT. Diet fat composition alters membrane phospholipid composition, insulin binding, and glucose metabolism in adipocytes from control and diabetic animals. J Biol Chem 1990;265:11143-11150.
36. Lamas O, Martinez JA, Marti A. T-helper lymphopenia and decreased mitogenic response in cafeteria diet-induced obese rats. Nutr Res 2002;22:497-506.
37. Stillie R, Bell RC, Field CJ. Diabetes-prone BioBreeding rats do not have a normal immune response when weaned to a diet containing fermentable fibre. Br J Nutr 2005;93:645-653.
38. Field CJ, Thomson CA, Van Aerde JE et al. Lower proportion of CD45R0+ cells and deficient interleukin-10 production by formula-fed infants, compared with human-fed, is corrected with supplementation of long-chain polyunsaturated fatty acids. J Pediatr Gastroenterol Nutr 2000;31:291-299.
39. Green LC, Wagner DA, Glogowski J et al. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 1982;126:131-138.
40. Field CJ, Ryan EA, Thomson AB, Clandinin MT. Dietary fat and the diabetic state alter insulin binding and the fatty acyl composition of the adipocyte plasma membrane. Biochem J 1988;253:417-424.
41. Layne KS, Goh YK, Jumpsen JA et al. Normal subjects consuming physiological levels of 18:3(n-3) and 20:5(n-3) from flaxseed or fish oils have characteristic differences in plasma lipid and lipoprotein fatty acid levels. J Nutr 1996;126:2130-2140.
42. Cruz-Hernandez C, Deng Z, Zhou J et al. Methods for analysis of conjugated linoleic acids and trans-18:1 isomers in dairy fats by using a combination of gas chromatography, silver-ion thin-layer chromatography/gas chromatography, and silver-ion liquid chromatography. J AOAC Int 2004;87:545-562.
43. Mito N, Hosoda T, Kato C, Sato K. Change of cytokine balance in diet-induced obese mice. Metabolism 2000;49:1295-1300.
44. Lamas O, Martínez JA, Marti A. Effects of a beta3-adrenergic agonist on the immune response in diet-induced (cafeteria) obese animals. J Physiol Biochem 2003;59:183-191.
45. Fan J, Bass HZ, Fahey JL. Elevated IFN-gamma and decreased IL-2 gene expression are associated with HIV infection. J Immunol 1993;151:5031-5040.
46. Bal AM, Lakhashe SK, Thakar MR, Tripathy SP, Paranjape RS. Dysregulation of proinflammatory and regulatory cytokines in HIV infected persons with active tuberculosis. Cytokine 2005;30:275-281.
47. Lamas O, Martinez JA, Marti A. Decreased splenic mRNA expression levels of TNF-alpha and IL-6 in diet-induced obese animals. J Physiol Biochem 2004;60:279-283.
48. Morrow WJ, Ohashi Y, Hall J et al. Dietary fat and immune function. I. Antibody responses, lymphocyte and accessory cell function in (NZB x NZW)F1 mice. J Immunol 1985;135:3857-3863.
49. Wallace FA, Miles EA, Evans C et al. Dietary fatty acids influence the production of Th1- but not Th2-type cytokines. J Leukoc Biol 2001;69:449-457.
50. Lord GM, Matarese G, Howard JK et al. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 1998;394:897-901.
51. Duncan BB, Schmidt MI, Pankow JS et al. Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 2003;52:1799-1805.
52. Ridker PM, Rifai N, Pfeffer M et al. Elevation of tumor necrosis factor-alpha and increased risk of recurrent coronary events after myocardial infarction. Circulation 2000;101:2149-2153.
53. Ridker PM, Hennekens CH, Buring JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med 2000;342:836-843.
54. Hang L, Theofilopoulos AN, Dixon FJ. A spontaneous rheumatoid arthritis-like disease in MRL/l mice. J Exp Med 1982;155:1690-1701.
55. Wernhoff P, Olofsson P, Holmdahl R. The genetic control of rheumatoid factor production in a rat model of rheumatoid arthritis. Arthritis Rheum 2003;48:3584-3596.
56. Hwang D. Fatty acids and immune responses - a new perspective in searching for clues to mechanism. Annu Rev Nutr 2000;20:431-456.
57. Field CJ, Schley PD. Evidence for potential mechanisms for the effect of conjugated linoleic acid on tumor metabolism and immune function: lessons from n-3 fatty acids. Am J Clin Nutr 2004;79(6 Suppl):1190S-1198S.
58. Phinney SD, Tang AB, Thurmond DC, Nakamura MT, Stern JS. Abnormal polyunsaturated lipid metabolism in the obese Zucker rat, with partial metabolic correction by gamma-linolenic acid administration. Metabolism 1993;42:1127-1140.
59. Guesnet P, Bourre JM, Guerre-Millo M, Pascal G, Durand G. Tissue phospholipid fatty acid composition in genetically lean (Fa/-) or obese (fa/fa) Zucker female rats on the same diet. Lipids 1990;25:517-522.
60. Wahle KW, Milne L, McIntosh G. Regulation of polyunsaturated fatty acid metabolism in tissue phospholipids of obese (fa/fa) and lean (Fa/-) Zucker rats. 1. Effect of dietary lipids on cardiac tissue. Lipids 1991;26:16-22.
61. Blond JP, Henchiri C, Bezard J. Delta 6 and delta 5 desaturase activities in liver from obese Zucker rats at different ages. Lipids 1989;24:389-395.
62. Jolly CA, Jiang YH, Chapkin RS, McMurray DN. Dietary (n-3) polyunsaturated fatty acids suppress murine lymphoproliferation, interleukin-2 secretion, and the formation of diacylglycerol and ceramide. J Nutr 1997;127:37-43.
63. Calder PC. Polyunsaturated fatty acids, inflammation, and immunity. Lipids 2001;36:1007-1024.
64. Papathanassoglou E, El-Haschimi K, Li XC et al. Leptin receptor expression and signaling in lymphocytes: kinetics during lymphocyte activation, role in lymphocyte survival, and response to high fat diet in mice. J Immunol 2006;176:7745-7752.
65. Palacios R. Concanavalin A triggers T lymphocytes by directly interacting with their receptors for activation. J Immunol 1982;128:337-342.
66. Chatila T, Silverman L, Miller R, Geha R. Mechanisms of T cell activation by the calcium ionophore ionomycin. J Immunol 1989;143:1283-1289.
67. Dixit VD, Mielenz M, Taub DD, Parvizi N. Leptin induces growth hormone secretion from peripheral blood mononuclear cells via a protein kinase C- and nitric oxide-dependent mechanism. Endocrinology 2003;144:5595-5603.
68. Garcia-Sainz JA, cantara-Hernandez R, Robles-Flores M et al. Modulation by protein kinase C of the hormonal responsiveness of hepatocytes from lean (Fa/fa?) and obese (fa/fa) Zucker rats. Biochim Biophys Acta 1992;1135:221-225.
69. Loffreda S, Yang SQ, Lin HZ et al. Leptin regulates proinflammatory immune responses. FASEB J 1998;12:57-65.
70. Busso N, So A, Chobaz-Peclat V et al. Leptin signaling deficiency impairs humoral and cellular immune responses and attenuates experimental arthritis. J Immunol 2002;168:875-882.
71. Ramakers JD, Plat J, Sébédio JL, Mensink RP. Effects of the individual isomers cis-9,trans-11 vs. trans-10,cis-12 of conjugated linoleic acid (CLA) on inflammation parameters in moderately overweight subjects with LDL-phenotype B. Lipids 2005;40:909-918.
72. Burdge GC, Lupoli B, Russell JJ et al. Incorporation of cis-9,trans-11 or trans-10,cis-12 conjugated linoleic acid into plasma and cellular lipids in healthy men. J Lipid Res 2004;45:736-741.
73. Noto A, Zahradka P, Yurkova N et al. Conjugated linoleic acid reduces hepatic steatosis, improves liver function, and favorably modifies lipid metabolism in obese insulin-resistant rats. Lipids 2006;41:179-188.