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Possible Role of Triacylglycerol-Rich Lipoproteins in the Down-Regulation of Adipose Obese mRNA Expression in Rats Re-Fed a High-Fat Diet

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Journal of Biomedical Science

Summary

The large amount of absorbed dietary lipid after feeding a high-fat diet is mainly transported as triacylglycerol (TG)-rich lipoproteins (TRL) in the post-prandial blood and is subsequently distributed to peripheral tissues including adipose and muscle tissues. An in vivo and an in vitro study were conducted to investigate the possible role of post-prandial TRL after high fat feeding in the regulation of obese (ob) gene expression. Adult male Wistar rats were fasted for 48 h and re-fed either a fat-free/high-carbohydrate diet or a high-fat diet for 2, 4, or 8 h and plasma glucose, insulin, TG, and leptin as well as ob mRNA expression in epididymal fat pads were examined. Rats re-fed the high-fat diet had significantly higher plasma TG (p<0.05) and lower plasma leptin and adipose ob mRNA (p<0.05) than those fed the fat-free/high-carbohydrate diet; however, plasma glucose and insulin concentrations were not significantly different between the two groups. Plasma lipid analysis found large amount of TRL in rats fed with high-fat diet; however, only very small amount of the TRL was found in rats fed with fat-free/high-carbohydrate diet. We speculated that TRL might involve in regulation of ob gene expression. To further examine the regulation of TRL on ob mRNA expression, differentiated 3T3-L1 adipocytes were treated with TRL collected from rats fed 5 ml soybean oil by gastric intubations. TRL down-regulated ob mRNA not only in a dose and time dependent manner but also in the presence of insulin in 3T3-L1 adipocytes. These results suggest a possible role of TRL in the down-regulation of adipose ob mRNA expression and may account, at least in part, for the previous observations that short-term high fat feeding resulted in lower plasma leptin.

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References

  1. Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., Friedman, J.M. (1994) "Positional cloning of the mouse ob gene and its human homologue" Nature 372: 425-432

    Article  PubMed  CAS  Google Scholar 

  2. Campfield, L.A., Smith, F.J., Guisez, Y., Devos, R., Burn, P. (1995) "Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks" Science 269: 546-549

    Article  PubMed  CAS  Google Scholar 

  3. Pelleymounter, M.A., Cullen, M.J., Baker, M.B., Hecht, R., Winters, D., Boone, T., Collins, F. (1995) "Effects of the obese gene product on body weight regulation in ob/ob mice" Science 269: 540-543

    Article  PubMed  CAS  Google Scholar 

  4. Friedman, J.M., Halaas, J.L. (1998) "Leptin and the regulation of body weight in mammals" Nature 395: 763-770

    Article  PubMed  CAS  Google Scholar 

  5. Halaas, J.L., Gajiwala, K.S., Maffei, M., Cohen, S.L., Chait, B.T., Rabinowitz, D., Lallone, R.L., Burley, S.K., Friedman, J.M. (1995) "Weight-reducing effects of the plasma protein encoded by the obese gene" Science 269: 543-546

    Article  PubMed  CAS  Google Scholar 

  6. Saladin, R., De Vos, P., Guerre-Millo, M., Leturque, A., Girard, J., Staels, B., Auwerx, J. (1995) "Transient increase in obese gene expression after food intake or insulin administration" Nature 377: 527-529

    Article  PubMed  CAS  Google Scholar 

  7. Rentsch, J., Chiesi, M. (1996) "Regulation of ob gene mRNA levels in cultured adipocytes" FEBS Lett. 379: 55-59

    Article  PubMed  CAS  Google Scholar 

  8. Leroy, P., Dessolin, S., Villageois, P., Moon, B.C., Friedman, J.M., Ailhaud, G., Dani, C. (1996) "Expression of ob gene in adipose cells. Regulation by insulin" J Biol. Chem. 271: 2365-2368

    Article  PubMed  CAS  Google Scholar 

  9. Slieker, L.J., Sloop, K.W., Surface, P.L., Kriauciunas, A., LaQuier, F., Manetta, J., Bue-Valleskey, J., Stephens, T.W. (1996) "Regulation of expression of ob mRNA and protein by glucocorticoids and cAMP" J. Biol. Chem. 271: 5301-5304

    Article  PubMed  CAS  Google Scholar 

  10. Frederich, R.C., Hamann, A., Anderson, S., Lollmann, B., Lowell, B.B., Flier, J.S. (1995) "Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action" Nat. Med. 1: 1311-1314

    Article  PubMed  CAS  Google Scholar 

  11. Van Heek, M., Compton, D.S., France, C.F., Tedesco, R.P., Fawzi, A.B., Graziano, M.P., Sybertz, E.J., Strader, C.D., Davis, H.R., Jr. (1997) "Diet-induced obese mice develop peripheral, but not central, resistance to leptin" J. Clin. Invest. 99: 385-390

    PubMed  CAS  Google Scholar 

  12. Masuzaki, H., Ogawa, Y., Hosoda, K., Kawada, T., Fushiki, T., Nakao, K. (1995) "Augmented expression of the obese gene in the adipose tissue from rats fed high-fat diet" Biochem. Biophys. Res. Commun. 216: 355-358

    Article  PubMed  CAS  Google Scholar 

  13. Havel, P.J., Townsend, R., Chaump, L., Teff, K. (1999) "High-fat meals reduce 24-h circulating leptin concentrations in women" Diabetes 48: 334-341

    Article  PubMed  CAS  Google Scholar 

  14. Ainslie, D.A., Proietto, J., Fam, B.C., Thorburn, A.W. (2000) "Short-term, high-fat diets lower circulating leptin concentrations in rats" Am. J. Clin. Nutr. 71: 438-442

    PubMed  CAS  Google Scholar 

  15. Lu, S.C., Lin, M.H., Huang, P.C. (1996) "A high cholesterol/ (n-3) polyunsaturated fatty acid diet induces hypercholesterolemia more significantly than a high cholesterol/(n-6) polyunsaturated fatty acid diet in hamsters" J. Nutr. 126: 1759-1765

    PubMed  CAS  Google Scholar 

  16. Bradford, M.M. (1976) "A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding" Anal. Biochem. 72: 248-254

    Article  PubMed  CAS  Google Scholar 

  17. Havel, R., Eder, H., Bragdon, J. (1995) "The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum" J. Clin. Invest. 34: 1345-1353

    Article  Google Scholar 

  18. Lu, S.C., Shieh, W.Y., Chen, C.Y., Hsu, S.C., Chen, H.L. (2002) "Lipopolysaccharide increases resistin gene expression in vivo and in vitro " FEBS Lett. 530: 158-162

    Article  PubMed  CAS  Google Scholar 

  19. Chomczynski, P., Sacchi, N. (1987) "Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction" Anal. Biochem. 162: 156-159

    Article  PubMed  CAS  Google Scholar 

  20. Sniderman, A.D., Cianflone, K., Summers, L., Fielding, B., Frayn, K. (1997) "The acylation-stimulating protein pathway and regulation of postprandial metabolism" Proc. Nutr. Soc. 56: 703-712

    Article  PubMed  CAS  Google Scholar 

  21. Scantlebury, T., Maslowska, M., Cianflone, K. (1998) "Chylomicron-specific enhancement of acylation stimulating protein and precursor protein C3 production in differentiated human adipocytes" J. Biol. Chem. 273: 20903-20909

    Article  PubMed  CAS  Google Scholar 

  22. Arai, T., Kawakami, Y., Matsushima, T., Okuda, Y., Yamashita, K. (2002) "Intracellular fatty acid downregulates ob gene expression in 3T3-L1 adipocytes" Biochem. Biophys. Res. Commun. 297: 1291-1296

    Article  PubMed  CAS  Google Scholar 

  23. Reseland, J.E., Haugen, F., Hollung, K., Solvoll, K., Halvorsen, B., Brude, I.R., Nenseter, M.S., Christiansen, E.N., Drevon, C.A. (2001) "Reduction of leptin gene expression by dietary polyunsaturated fatty acids" J. Lipid Res. 42: 743-750

    PubMed  CAS  Google Scholar 

  24. Ukropec, J., Reseland, J.E., Gasperikova, D., Demcakova, E., Madsen, L., Berge, R.K., Rustan, A.C., Klimes, I., Drevon, C.A., Sebokova, E. (2003) "The hypotriglyceridemic effect of dietary n-3 FA is associated with increased beta-oxidation and reduced leptin expression" Lipids 38: 1023-1029

    PubMed  CAS  Google Scholar 

  25. Takahashi, Y., Ide, T. (2000) "Dietary n-3 fatty acids affect mRNA level of brown adipose tissue uncoupling protein 1, and white adipose tissue leptin and glucose transporter 4 in the rat" Br. J. Nutr. 84: 175-184

    PubMed  CAS  Google Scholar 

  26. Lonnqvist, F., Arner, P., Nordfors, L., Schalling, M. (1995) "Overexpression of the obese (ob) gene in adipose tissue of human obese subjects" Nat. Med. 1: 950-953

    Article  PubMed  CAS  Google Scholar 

  27. Considine, R.V., Sinha, M.K., Heiman, M.L., Kriauciunas, A., Stephens, T.W., Nyce, M.R., Ohannesian, J.P., Marco, C.C., McKee, L.J., Bauer, T.L., Caro, J.F. (1996) "Serum immunoreactive-leptin concentrations in normal-weight and obese humans" N. Engl. J. Med. 334: 292-295

    Article  PubMed  CAS  Google Scholar 

  28. Mizuno, T.M., Bergen, H., Funabashi, T., Kleopoulos, S.P., Zhong, Y.G., Bauman, W.A., Mobbs, C.V. (1996) "Obese gene expression: reduction by fasting and stimulation by insulin and glucose in lean mice, and persistent elevation in acquired (diet-induced) and genetic (yellow agouti) obesity" Proc. Natl. Acad. Sci. USA 93: 3434-3438

    Article  PubMed  CAS  Google Scholar 

  29. Keim, N.L., Stern, J.S., Havel, P.J. (1998) "Relation between circulating leptin concentrations and appetite during a prolonged, moderate energy deficit in women" Am. J. Clin. Nutr. 68: 794-801

    PubMed  CAS  Google Scholar 

  30. Blundell, J.E., Burley, V.J., Cotton, J.R., Lawton, C.L. (1993) "Dietary fat and the control of energy intake: evaluating the effects of fat on meal size and postmeal satiety" Am. J. Clin. Nutr. 57: 772S-777S

    PubMed  CAS  Google Scholar 

  31. Asakuma, S., Hiraku, O., Kurose, Y., Kobayashi, S., Terashima, Y. (2004) "Diurnal rhythm of cerebrospinal fluid and plasma leptin levels related to feeding in non-lactating and lactating rats" J. Endocrinol. 180: 283-286

    Article  PubMed  CAS  Google Scholar 

  32. MacDougald, O.A., Hwang, C.S., Fan, H., Lane, M.D. (1995) "Regulated expression of the obese gene product (leptin) in white adipose tissue and 3T3-L1 adipocytes" Proc. Natl. Acad. Sci. USA 92: 9034-9037

    Article  PubMed  CAS  Google Scholar 

  33. Rentsch, J., Chiesi, M. (1996) "Regulation of ob gene mRNA levels in cultured adipocytes" FEBS Lett. 379: 55-59

    Article  PubMed  CAS  Google Scholar 

  34. Slieker, L.J., Sloop, K.W., Surface, P.L. (1998) "Differentiation method-dependent expression of leptin in adipocyte cell lines" Biochem. Biophys. Res. Commun. 251: 225-229

    Article  PubMed  CAS  Google Scholar 

  35. Leroy, P., Dessolin, S., Villageois, P., Moon, B.C., Friedman, J.M., Ailhaud, G., Dani, C. (1996) "Expression of ob gene in adipose cells. Regulation by insulin" J. Biol. Chem. 271: 2365-2368

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Mei-Ling Chang.

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Chang, ML., Chen, HL. & Lu, SC. Possible Role of Triacylglycerol-Rich Lipoproteins in the Down-Regulation of Adipose Obese mRNA Expression in Rats Re-Fed a High-Fat Diet. J Biomed Sci 12, 621–628 (2005). https://doi.org/10.1007/s11373-005-7456-0

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  • DOI: https://doi.org/10.1007/s11373-005-7456-0

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