The Journal of Nutritional Biochemistry
Volume 21, Issue 11 , Pages 1127-1133 , November 2010

Feeding conditions control the expression of genes involved in sterol metabolism in peripheral blood mononuclear cells of normoweight and diet-induced (cafeteria) obese rats

  • Antoni Caimari

      Affiliations

    • Laboratory of Molecular Biology, Nutrition and Biotechnology, Universitat de les Illes Balears and CIBER de Fisiopatología de la Obesidad y Nutrición (CIBEROBN), E-07122, Palma de Mallorca, Spain
    • ,
  • Paula Oliver

      Affiliations

    • Laboratory of Molecular Biology, Nutrition and Biotechnology, Universitat de les Illes Balears and CIBER de Fisiopatología de la Obesidad y Nutrición (CIBEROBN), E-07122, Palma de Mallorca, Spain
    • ,
  • Wendy Rodenburg

      Affiliations

    • Human and Animal Physiology, Wageningen University, 6708 PG, Wageningen, The Netherlands
    • Food Bioactives Group, RIKILT – Institute of Food Safety, 6708 PD, Wageningen, The Netherlands
    • ,
  • Jaap Keijer

      Affiliations

    • Human and Animal Physiology, Wageningen University, 6708 PG, Wageningen, The Netherlands
    • ,
  • Andreu Palou

      Affiliations

    • Laboratory of Molecular Biology, Nutrition and Biotechnology, Universitat de les Illes Balears and CIBER de Fisiopatología de la Obesidad y Nutrición (CIBEROBN), E-07122, Palma de Mallorca, Spain
    • Corresponding Author InformationCorresponding author. Lab. Molecular Biology, Nutrition and Biotechnology, Universitat de les Illes Balears, Cra. Valldemossa km 7.5. E-07122-Palma de Mallorca, Spain. Tel.: +34 971173170; fax: +34 971173426.

Received 24 June 2009 ,Revised 24 September 2009 ,Accepted 1 October 2009.

References 

  1. Espenshade PJ, Hughes AL. Regulation of sterol synthesis in eukaryotes. Annu Rev Genet. 2007;41:401–427
  2. Robichon C, Dugail I. De novo cholesterol synthesis at the crossroads of adaptive response to extracellular stress through SREBP. Biochimie. 2007;89:260–264
  3. Horton JD. Sterol regulatory element-binding proteins: transcriptional activators of lipid synthesis. Biochem Soc Trans. 2002;30:1091–1095
  4. Bengoechea-Alonso MT, Ericsson J. SREBP in signal transduction: cholesterol metabolism and beyond. Curr Opin Cell Biol. 2007;19:215–222
  5. McPherson R, Gauthier A. Molecular regulation of SREBP function: the Insig-SCAP connection and isoform-specific modulation of lipid synthesis. Biochem Cell Biol. 2004;82:201–211
  6. Dietschy JM, Turley SD, Spady DK. Role of liver in the maintenance of cholesterol and low density lipoprotein homeostasis in different animal species, including humans. J Lipid Res. 1993;34:1637–1659
  7. Osono Y, Woollett LA, Herz J, et al. Role of the low density lipoprotein receptor in the flux of cholesterol through the plasma and across the tissues of the mouse. J Clin Invest. 1995;95:1124–1132
  8. Spady DK, Dietschy JM. Sterol synthesis in vivo in 18 tissues of the squirrel monkey, guinea pig, rabbit, hamster, and rat. J Lipid Res. 1983;24:303–315
  9. Takeuchi Y, Yahagi N, Nakagawa Y, et al. In vivo promoter analysis on refeeding response of hepatic sterol regulatory element-binding protein-1c expression. Biochem Biophys Res Commun. 2007;363:329–335
  10. Horton JD, Shimomura I, Brown MS, et al. Activation of cholesterol synthesis in preference to fatty acid synthesis in liver and adipose tissue of transgenic mice overproducing sterol regulatory element-binding protein-2. J Clin Invest. 1998;101:2331–2339
  11. Bennett MK, Seo YK, Datta S, et al. Selective binding of sterol regulatory element-binding protein isoforms and co-regulatory proteins to promoters for lipid metabolic genes in liver. J Biol Chem. 2008;283:15628–15637
  12. Turley SD, Spady DK, Dietschy JM. Role of liver in the synthesis of cholesterol and the clearance of low density lipoproteins in the cynomolgus monkey. J Lipid Res. 1995;36:67–79
  13. Spady DK, Huettinger M, Bilheimer DW, et al. Role of receptor-independent low density lipoprotein transport in the maintenance of tissue cholesterol balance in the normal and WHHL rabbit. J Lipid Res. 1987;28:32–41
  14. Sanghvi A, Wight C, Warty V. On the differential suppression of cholesterol synthesis by low density lipoprotein in B and T lymphocytes. Biochim Biophys Acta. 1981;665:48–52
  15. Sutherland WH, Nye ER. Plasma lipoprotein levels and in vitro cholesterol synthesis by cells in human blood. Biochem Med. 1985;34:17–21
  16. McNamara DJ, Bloch CA, Botha A, et al. Sterol synthesis in vitro in freshly isolated blood mononuclear leukocytes from familial hypercholesterolemic patients treated with probucol. Biochim Biophys Acta. 1985;833:412–416
  17. Batetta B, Bonatesta RR, Sanna F, et al. Cell growth and cholesterol metabolism in human glucose-6-phosphate dehydrogenase deficient lymphomononuclear cells. Cell Prolif. 2002;35:143–154
  18. Cuthbert JA, Lipsky PE. Mitogenic stimulation alters the regulation of LDL receptor gene expression in human lymphocytes. J Lipid Res. 1990;31:2067–2078
  19. Fogelman AM, Seager J, Edwards PA, et al. Mechanism of induction of 3-hydroxy-3-methylglutaryl coenzyme A reductase in human leukocytes. J Biol Chem. 1977;252:644–651
  20. Fogelman AM, Seager J, Hokom M, et al. Separation of and cholesterol synthesis by human lymphocytes and monocytes. J Lipid Res. 1979;20:379–388
  21. McNamara DJ, Davidson NO, Fernandez S. In vitro cholesterol synthesis in freshly isolated mononuclear cells of human blood: effect of in vivo administration of clofibrate and/or cholestyramine. J Lipid Res. 1980;21:65–71
  22. Bouwens M, Afman LA, Muller M. Fasting induces changes in peripheral blood mononuclear cell gene expression profiles related to increases in fatty acid beta-oxidation: functional role of peroxisome proliferator activated receptor alpha in human peripheral blood mononuclear cells. Am J Clin Nutr. 2007;86:1515–1523
  23. Bouwens M, Afman LA, Muller M. Activation of peroxisome proliferator-activated receptor alpha in human peripheral blood mononuclear cells reveals an individual gene expression profile response. BMC Genomics. 2008;9:262
  24. Maas K, Chan S, Parker J, et al. Cutting edge: molecular portrait of human autoimmune disease. J Immunol. 2002;169:5–9
  25. Burczynski ME, Dorner AJ. Transcriptional profiling of peripheral blood cells in clinical pharmacogenomic studies. Pharmacogenomics. 2006;7:187–202
  26. Ghanim H, Aljada A, Hofmeyer D, et al. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation. 2004;110:1564–1571
  27. O'Rourke RW, Kay T, Lyle EA, et al. Alterations in peripheral blood lymphocyte cytokine expression in obesity. Clin Exp Immunol. 2006;146:39–46
  28. de Mello VD, Kolehmainen M, Schwab U, et al. Effect of weight loss on cytokine messenger RNA expression in peripheral blood mononuclear cells of obese subjects with the metabolic syndrome. Metabolism. 2008;57:192–199
  29. Napoleone E, DIS A, Amore C, et al. Leptin induces tissue factor expression in human peripheral blood mononuclear cells: a possible link between obesity and cardiovascular risk?. J Thromb Haemost. 2007;5:1462–1468
  30. Bokarewa M, Nagaev I, Dahlberg L, et al. Resistin, an adipokine with potent proinflammatory properties. J Immunol. 2005;174:5789–5795
  31. Tsiotra PC, Tsigos C, Yfanti E, et al. Visfatin, TNF-alpha and IL-6 mRNA expression is increased in mononuclear cells from type 2 diabetic women. Horm Metab Res. 2007;39:758–763
  32. Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–419
  33. Allison DB, Cui X, Page GP, et al. Microarray data analysis: from disarray to consolidation and consensus. Nat Rev Genet. 2006;7:55–65
  34. Pellis L, Franssen-van Hal NL, Burema J, et al. The intraclass correlation coefficient applied for evaluation of data correction, labeling methods, and rectal biopsy sampling in DNA microarray experiments. Physiol Genomics. 2003;16:99–106
  35. Lee HK, Braynen W, Keshav K, et al. ErmineJ: tool for functional analysis of gene expression data sets. BMC Bioinformatics. 2005;6:269
  36. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402–408
  37. Caimari A, Oliver P, Keijer J, Palou A. Peripheral blood mononuclear cells as a model to study the response of energy homeostasis-related genes to acute changes in feeding conditions. OMICS, in press.
  38. Pico C, Sanchez J, Oliver P, et al. Leptin production by the stomach is up-regulated in obese (fa/fa) Zucker rats. Obes Res. 2002;10:932–938
  39. Caimari A, Oliver P, Palou A. Regulation of adiponutrin expression by feeding conditions in rats is altered in the obese state. Obesity (Silver Spring). 2007;15:591–599
  40. Caimari A, Oliver P, Palou A. Impairment of nutritional regulation of adipose triglyceride lipase expression with age. Int J Obes (Lond). 2008;32:1193–1200
  41. Powers AC, Solomon SS, Duckworth WC. Insulin degradation by mononuclear cells. Diabetes. 1980;29:27–32
  42. Bloch K. The biological synthesis of cholesterol. Science. 1965;150:19–28
  43. Ott DB, Lachance PA. Biochemical controls of liver cholesterol biosynthesis. Am J Clin Nutr. 1981;34:2295–2306
  44. Vance DE, Van den Bosch H. Cholesterol in the year 2000. Biochim Biophys Acta. 2000;1529:1–8
  45. Bucher NL, Overath P, Lynen F. beta-Hydroxy-beta-methyl-glutaryl coenzyme A reductase, cleavage and condensing enzymes in relation to cholesterol formation in rat liver. Biochim Biophys Acta. 1960;40:491–501
  46. Slakey LL, Craig MC, Beytia E, et al. The effects of fasting, refeeding, and time of day on the levels of enzymes effecting the conversion of -hydroxy- -methylglutaryl-coenzyme A to squalene. J Biol Chem. 1972;247:3014–3022
  47. Johnson RC, Shah SN. Hepatic cholesterol synthesis from mevalonate and squalene in rats: effect of feeding cholesterol supplemented diet during weaning and following starvation. Lipids. 1974;9:962–970
  48. Wiss O. Influence of fasting and cholesterol feeding on the cholesterol synthesis in rats in vivo. Biochem Biophys Res Commun. 1976;68:353–357
  49. Cases S, Novak S, Zheng YW, et al. ACAT-2, a second mammalian acyl-CoA:cholesterol acyltransferase. Its cloning, expression, and characterization. J Biol Chem. 1998;273:26755–26764
  50. Anderson RA, Joyce C, Davis M, et al. Identification of a form of acyl-CoA:cholesterol acyltransferase specific to liver and intestine in nonhuman primates. J Biol Chem. 1998;273:26747–26754
  51. Chang CC, Sakashita N, Ornvold K, et al. Immunological quantitation and localization of ACAT-1 and ACAT-2 in human liver and small intestine. J Biol Chem. 2000;275:28083–28092
  52. Katsuren K, Tamura T, Arashiro R, et al. Structure of the human acyl-CoA:cholesterol acyltransferase-2 (ACAT-2) gene and its relation to dyslipidemia. Biochim Biophys Acta. 2001;1531:230–240
  53. Klucken J, Buchler C, Orso E, et al. ABCG1 (ABC8), the human homolog of the Drosophila white gene, is a regulator of macrophage cholesterol and phospholipid transport. Proc Natl Acad Sci U S A. 2000;97:817–822
  54. Schmitz G, Langmann T, Heimerl S. Role of ABCG1 and other ABCG family members in lipid metabolism. J Lipid Res. 2001;42:1513–1520
  55. Pollack SE, Furth EE, Kallen CB, et al. Localization of the steroidogenic acute regulatory protein in human tissues. J Clin Endocrinol Metab. 1997;82:4243–4251
  56. Arakane F, King SR, Du Y, et al. Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. J Biol Chem. 1997;272:32656–32662
  57. Stocco DM. Intramitochondrial cholesterol transfer. Biochim Biophys Acta. 2000;1486:184–197
  58. Miller WL. Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter. Biochim Biophys Acta. 2007;1771:663–676
  59. Brown MS, Goldstein JL. Receptor-mediated endocytosis: insights from the lipoprotein receptor system. Proc Natl Acad Sci U S A. 1979;76:3330–3337
  60. Fogelman AM, Van Lenten BJ, Warden C, et al. Macrophage lipoprotein receptors. J Cell Sci Suppl. 1988;9:135–149
  61. May P, Bock HH, Herz J. Integration of endocytosis and signal transduction by lipoprotein receptors. Sci STKE. 2003;2003:PE12
  62. Kraemer FB, Laane C, Park B, et al. Low-density lipoprotein receptors in rat adipocytes: regulation with fasting. Am J Physiol. 1994;266:E26–E32
  63. Costet P, Cariou B, Lambert G, et al. Hepatic PCSK9 expression is regulated by nutritional status via insulin and sterol regulatory element-binding protein 1c. J Biol Chem. 2006;281:6211–6218
  64. Streicher R, Kotzka J, Muller-Wieland D, et al. SREBP-1 mediates activation of the low density lipoprotein receptor promoter by insulin and insulin-like growth factor-I. J Biol Chem. 1996;271:7128–7133
  65. Wang X, Sato R, Brown MS, et al. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell. 1994;77:53–62
  66. Weatherbee SD, Anderson KV, Niswander LA. LDL-receptor-related protein 4 is crucial for formation of the neuromuscular junction. Development. 2006;133:4993–5000
  67. Lu Y, Tian QB, Endo S, et al. A role for LRP4 in neuronal cell viability is related to apoE-binding. Brain Res. 2007;1177:19–28
  68. Battle MA, Maher VM, McCormick JJ. ST7 is a novel low-density lipoprotein receptor-related protein (LRP) with a cytoplasmic tail that interacts with proteins related to signal transduction pathways. Biochemistry. 2003;42:7270–7282
  69. Langmann T, Porsch-Ozcurumez M, Unkelbach U, et al. Genomic organization and characterization of the promoter of the human ATP-binding cassette transporter-G1 (ABCG1) gene. Biochim Biophys Acta. 2000;1494:175–180
  70. Nackley AC, Shea-Eaton W, Lopez D, et al. Repression of the steroidogenic acute regulatory gene by the multifunctional transcription factor Yin Yang 1. Endocrinology. 2002;143:1085–1096

☆ CIBER de Fisiopatología de la Obesidad y Nutrición is an initiative of the ISCIII. This work was supported by the Spanish Government (Ministerio de Educación y Ciencia, AGL2006-04887/ALI and AGL2009-11277/ALI). Our laboratory is a member of the European Research Network of Excellence NuGO (The European Nutrigenomics Organization, EU Contract: FOOD-CT-2004-506360 NUGO). Antoni Caimari is a recipient of a fellowship from the Government of the Balearic Islands.

PII: S0955-2863(09)00213-7

doi: 10.1016/j.jnutbio.2009.10.001

The Journal of Nutritional Biochemistry
Volume 21, Issue 11 , Pages 1127-1133 , November 2010

Article Tools