Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014, Article ID 451620, 13 pages
http://dx.doi.org/10.1155/2014/451620
Research Article

Expression of Genes Related to Prostaglandin Synthesis or Signaling in Human Subcutaneous and Omental Adipose Tissue: Depot Differences and Modulation by Adipogenesis

1Endocrinology and Nephrology, CHU de Québec, 2705 Laurier Boulevard (R-4779), Québec, QC, Canada G1V 4G2
2Department of Nutrition, Laval University, 2425 Rue de l’Agriculture, Québec, QC, Canada G1V 0A6
3Reproduction and Biology, CHU de Québec, 2705 Laurier Boulevard, Québec, QC, Canada G1V 4G2
4Gynecology Unit, CHU de Québec, 2705 Laurier Boulevard, Québec, QC, Canada G1V 4G2
5Department of Surgery, Institut Universitaire de Cardiologie et de Pneumologie, 2725 Chemin Sainte-Foy, Québec, QC, Canada G1V 4G5

Received 13 June 2014; Revised 29 September 2014; Accepted 30 September 2014; Published 11 November 2014

Academic Editor: Hermann Gram

Copyright © 2014 Andréanne Michaud et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. E. Wellen and G. S. Hotamisligil, “Obesity-induced inflammatory changes in adipose tissue,” The Journal of Clinical Investigation, vol. 112, no. 12, pp. 1785–1788, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. S. K. Fried, D. A. Bunkin, and A. S. Greenberg, “Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid,” The Journal of Clinical Endocrinology and Metabolism, vol. 83, no. 3, pp. 847–850, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. A. H. Berg and P. E. Scherer, “Adipose tissue, inflammation, and cardiovascular disease,” Circulation Research, vol. 96, no. 9, pp. 939–949, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. E. Arner, P. O. Westermark, K. L. Spalding et al., “Adipocyte turnover: relevance to human adipose tissue morphology,” Diabetes, vol. 59, no. 1, pp. 105–109, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Drolet, C. Richard, A. D. Sniderman et al., “Hypertrophy and hyperplasia of abdominal adipose tissues in women,” International Journal of Obesity, vol. 32, no. 2, pp. 283–291, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. E. D. Rosen, C. J. Walkey, P. Puigserver, and B. M. Spiegelman, “Transcriptional regulation of adipogenesis,” Genes and Development, vol. 14, no. 11, pp. 1293–1307, 2000. View at Google Scholar · View at Scopus
  7. F. M. Gregoire, C. M. Smas, and H. S. Sul, “Understanding adipocyte differentiation,” Physiological Reviews, vol. 78, no. 3, pp. 783–809, 1998. View at Google Scholar · View at Scopus
  8. A. Michaud, N. Lacroix-Pépin, M. Pelletier et al., “Prostaglandin (PG) F2 alpha synthesis in human subcutaneous and omental adipose tissue: modulation by inflammatory cytokines and role of the human aldose reductase AKR1B1,” PLoS ONE, vol. 9, no. 3, Article ID e90861, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Trayhurn and I. S. Wood, “Signalling role of adipose tissue: adipokines and inflammation in obesity,” Biochemical Society Transactions, vol. 33, no. 5, pp. 1078–1081, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Fujimori, “Prostaglandins as PPARgamma modulators in adipogenesis,” PPAR Research, vol. 2012, Article ID 527607, 8 pages, 2012. View at Publisher · View at Google Scholar
  11. W. L. Smith, Y. Urade, and P.-J. Jakobsson, “Enzymes of the cyclooxygenase pathways of prostanoid biosynthesis,” Chemical Reviews, vol. 111, no. 10, pp. 5821–5865, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Jaworski, M. Ahmadian, R. E. Duncan et al., “AdPLA ablation increases lipolysis and prevents obesity induced by high-fat feeding or leptin deficiency,” Nature Medicine, vol. 15, no. 2, pp. 159–168, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. W. L. Smith, R. M. Garavito, and D. L. DeWitt, “Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2,” The Journal of Biological Chemistry, vol. 271, no. 52, pp. 33157–33160, 1996. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Tanioka, Y. Nakatani, N. Semmyo, M. Murakami, and I. Kudo, “Molecular identification of cytosolic prostaglandin E2 synthase that is functionally coupled with cyclooxygenase-1 in immediate prostaglandin E2 biosynthesis,” The Journal of Biological Chemistry, vol. 275, no. 42, pp. 32775–32782, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. P.-J. Jakobsson, S. Thorén, R. Morgenstern, and B. Samuelsson, “Identification of human prostaglandin E synthase: a microsomal, glutathione-dependent, inducible enzyme, constituting a potential novel drug target,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 13, pp. 7220–7225, 1999. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Fujimori, M. Yano, and T. Ueno, “Synergistic suppression of early phase of adipogenesis by microsomal PGE synthase-1 (PTGES1)-produced PGE2 and aldo-keto reductase 1B3-produced PGF2alpha,” PLoS ONE, vol. 7, no. 9, Article ID e44698, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Watanabe, “Prostaglandin F synthase,” Prostaglandins and Other Lipid Mediators, vol. 68-69, pp. 401–407, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Watanabe, R. Yoshida, T. Shimizu, and O. Hayaishi, “Enzymatic formation of prostaglandin F(2α) from prostaglandin H2 and D2. Purification and properties of prostaglandin F synthetase from bovine lung,” The Journal of Biological Chemistry, vol. 260, no. 11, pp. 7035–7041, 1985. View at Google Scholar · View at Scopus
  19. O. Hayaishi, K. Watanabe, Y. Fujii et al., “Prostaglandin F synthetase, a dual function enzyme,” Progress in Clinical and Biological Research, vol. 274, pp. 577–587, 1988. View at Google Scholar · View at Scopus
  20. E. Bresson, S. Boucher-Kovalik, P. Chapdelaine et al., “The human aldose reductase AKR1B1 qualifies as the primary prostaglandin F synthase in the endometrium,” The Journal of Clinical Endocrinology and Metabolism, vol. 96, no. 1, pp. 210–219, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Bresson, N. Lacroix-Pépin, S. Boucher-Kovalik, P. Chapdelaine, and M. A. Fortier, “The prostaglandin F synthase activity of the human aldose reductase AKR1B1 brings new lenses to look at pathologic conditions,” Frontiers in Pharmacology, vol. 3, article 98, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Madore, N. Harvey, J. Parent, P. Chapdelaine, J. A. Arosh, and M. A. Fortier, “An aldose reductase with 20α-hydroxysteroid dehydrogenase activity is most likely the enzyme responsible for the production of prostaglandin F2α in the bovine endometrium,” The Journal of Biological Chemistry, vol. 278, no. 13, pp. 11205–11212, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. J.-P. Després and I. Lemieux, “Abdominal obesity and metabolic syndrome,” Nature, vol. 444, no. 7121, pp. 881–887, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Tsuboi, Y. Sugimoto, T. Kainoh, and A. Ichikawa, “Prostanoid EP4 receptor is involved in suppression of 3T3-L1 adipocyte differentiation,” Biochemical and Biophysical Research Communications, vol. 322, no. 3, pp. 1066–1072, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. D. A. Casimir, C. W. Miller, and J. M. Ntambi, “Preadipocyte differentiation blocked by prostaglandin stimulation of prostanoid FP2 receptor in murine 3T3-L1 cells,” Differentiation, vol. 60, no. 4, pp. 203–210, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. L. Liu and N. A. Clipstone, “Prostaglandin F2α inhibits adipocyte differentiation via a Gαq-calcium-calcineurin-dependent signaling pathway,” Journal of Cellular Biochemistry, vol. 100, no. 1, pp. 161–173, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. C. W. Miller, D. A. Casimir, and J. M. Ntambi, “The mechanism of inhibition of 3T3-L1 preadipocyte differentiation by prostaglandin F2α,” Endocrinology, vol. 137, no. 12, pp. 5641–5650, 1996. View at Google Scholar · View at Scopus
  28. G. Serrero and N. M. Lepak, “Prostaglandin F(2α) receptor (FP receptor) agonists are potent adipose differentiation inhibitors for primary culture of adipocyte precursors in defined medium,” Biochemical and Biophysical Research Communications, vol. 233, no. 1, pp. 200–202, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Fujimori, K. Aritake, and Y. Urade, “A novel pathway to enhance adipocyte differentiation of 3T3-L1 cells by up-regulation of lipocalin-type prostaglandin D synthase mediated by liver X receptor-activated sterol regulatory element-binding protein-1c,” Journal of Biological Chemistry, vol. 282, no. 25, pp. 18458–18466, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. B. M. Forman, P. Tontonoz, J. Chen, R. P. Brun, B. M. Spiegelman, and R. M. Evans, “15-deoxy-Δ12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPARγ,” Cell, vol. 83, no. 5, pp. 803–812, 1995. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Quinkler, I. J. Bujalska, J. W. Tomlinson, D. M. Smith, and P. M. Stewart, “Depot-specific prostaglandin synthesis in human adipose tissue: a novel possible mechanism of adipogenesis,” Gene, vol. 380, no. 2, pp. 137–143, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Michaud, R. Drolet, S. Noël, G. Paris, and A. Tchernof, “Visceral fat accumulation is an indicator of adipose tissue macrophage infiltration in women,” Metabolism: Clinical and Experimental, vol. 61, no. 5, pp. 689–698, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Deschênes, P. Couture, P. Dupont, and A. Tchernof, “Subdivision of the subcutaneous adipose tissue compartment and lipid-lipoprotein levels in women,” Obesity Research, vol. 11, no. 3, pp. 469–476, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Rodbell, “Metabolism of isolated fat cells. I. Effects of hormones on glucose metabolism and lipolysis,” The Journal of Biological Chemistry, vol. 239, pp. 375–380, 1964. View at Google Scholar · View at Scopus
  35. V. Van Harmelen, K. Röhrig, and H. Hauner, “Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from the omental and subcutaneous adipose tissue depot of obese subjects,” Metabolism: Clinical and Experimental, vol. 53, no. 5, pp. 632–637, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Asselin, A. K. Goff, H. Bergeron, and M. A. Fortier, “Influence of sex steroids on the production of prostaglandins F2α and E2 and response to oxytocin in cultured epithelial and stromal cells of the bovine endometrium,” Biology of Reproduction, vol. 54, no. 2, pp. 371–379, 1996. View at Publisher · View at Google Scholar · View at Scopus
  37. V. Luu-The, N. Paquet, E. Calvo, and J. Cumps, “Improved real-time RT-PCR method for high-throughput measurements using second derivative calculation and double correction,” BioTechniques, vol. 38, no. 2, pp. 287–293, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. M. G. Farb, S. Tiwari, S. Karki et al., “Cyclooxygenase inhibition improves endothelial vasomotor dysfunction of visceral adipose arterioles in human obesity,” Obesity, vol. 22, no. 2, pp. 349–355, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Tchernof and J.-P. Després, “Pathophysiology of human visceral obesity: an update,” Physiological Reviews, vol. 93, no. 1, pp. 359–404, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. H. T. Park, E. S. Lee, Y.-P. Cheon et al., “The relationship between fat depot-specific preadipocyte differentiation and metabolic syndrome in obese women,” Clinical Endocrinology, vol. 76, no. 1, pp. 59–66, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Tchkonia, N. Giorgadze, T. Pirtskhalava et al., “Fat depot origin affects adipogenesis in primary cultured and cloned human preadipocytes,” American Journal of Physiology: Regulatory Integrative and Comparative Physiology, vol. 282, no. 5, pp. R1286–R1296, 2002. View at Google Scholar · View at Scopus
  42. T. Tchkonia, Y. D. Tchoukalova, N. Giorgadze et al., “Abundance of two human preadipocyte subtypes with distinct capacities for replication, adipogenesis, and apoptosis varies among fat depots,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 288, no. 1, pp. E267–E277, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Lessard and A. Tchernof, “Depot- and obesity-related differences in adipogenesis,” Clinical Lipidology, vol. 7, no. 5, pp. 587–596, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. J. L. Lessard, M. Pelletier, M. Leboeuf, L. Blackburn, and A. Tchernof, “Low abdominal subcutaneous preadipocyte adipogenesis is associated with visceral obesity, visceral adipocyte hypertrophy, and a dysmetabolic state,” Adipocyte, vol. 3, no. 3, pp. 197–205, 2014. View at Publisher · View at Google Scholar
  45. T. Inazumi, N. Shirata, K. Morimoto, H. Takano, E. Segi-Nishida, and Y. Sugimoto, “Prostaglandin E2-EP4 signaling suppresses adipocyte differentiation in mouse embryonic fibroblasts via an autocrine mechanism,” Journal of Lipid Research, vol. 52, no. 8, pp. 1500–1508, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. K. Fujimori, T. Ueno, N. Nagata et al., “Suppression of adipocyte differentiation by aldo-keto reductase 1B3 acting as prostaglandin F2α synthase,” The Journal of Biological Chemistry, vol. 285, no. 12, pp. 8880–8886, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Xie, X. Kang, W. E. Ackerman et al., “Differentiation-dependent regulation of the cyclooxygenase cascade during adipogenesis suggests a complex role for prostaglandins,” Diabetes, Obesity and Metabolism, vol. 8, no. 1, pp. 83–93, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. P.-O. Hétu and D. Riendeau, “Down-regulation of microsomal prostaglandin E2 synthase-1 in adipose tissue by high-fat feeding,” Obesity, vol. 15, no. 1, pp. 60–68, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. J. N. Fain, A. Kanu, S. W. Bahouth, G. S. M. Cowan Jr., M. L. Hiler, and C. W. Leffler, “Comparison of PGE2, prostacyclin and leptin release by human adipocytes versus explants of adipose tissue in primary culture,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 67, no. 6, pp. 467–473, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Chatzipanteli, S. Rudolph, and L. Axelrod, “Coordinate control of lipolysis by prostaglandin E2 and prostacyclin in rat adipose tissue,” Diabetes, vol. 41, no. 8, pp. 927–935, 1992. View at Publisher · View at Google Scholar · View at Scopus
  51. J. D. Børglum, S. B. Pedersen, G. Ailhaud, R. Négrel, and B. Richelsen, “Differential expression of prostaglandin receptor mRNAs during adipose cell differentiation,” Prostaglandins and Other Lipid Mediators, vol. 57, no. 5-6, pp. 305–317, 1999. View at Publisher · View at Google Scholar · View at Scopus
  52. J. N. Fain, B. Buehrer, S. W. Bahouth, D. S. Tichansky, and A. K. Madan, “Comparison of messenger RNA distribution for 60 proteins in fat cells vs the nonfat cells of human omental adipose tissue,” Metabolism, vol. 57, no. 7, pp. 1005–1015, 2008. View at Publisher · View at Google Scholar · View at Scopus