Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014 (2014), Article ID 413921, 10 pages
http://dx.doi.org/10.1155/2014/413921
Research Article

Association of Immune and Metabolic Receptors C5aR and C5L2 with Adiposity in Women

1Centre de Recherche de l’Institut Universitaire de Cardiologie et de Pneumologie de Québec (CRIUCPQ), Laval University, Y4323, 2725 Chemin Ste-Foy, Québec, QC, Canada G1V 4G5
2Department of Medicine, Laval University, 1050 Avenue de la Médecine, Québec, QC, Canada G1V 0A6

Received 2 October 2013; Revised 7 December 2013; Accepted 11 December 2013; Published 12 January 2014

Academic Editor: Simi Ali

Copyright © 2014 Pegah Poursharifi 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. M. Adamczak and A. Wiecek, “The adipose tissue as an endocrine organ,” Seminars in Nephrology, vol. 33, pp. 2–13, 2013. View at Google Scholar
  2. J.-P. Despres, S. Moorjani, P. J. Lupien, A. Tremblay, A. Nadeau, and C. Bouchard, “Regional distribution of body fat, plasma lipoproteins, and cardiovascular disease,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 10, no. 4, pp. 497–511, 1990. View at Google Scholar · View at Scopus
  3. E. Maury and S. M. Brichard, “Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome,” Molecular and Cellular Endocrinology, vol. 314, no. 1, pp. 1–16, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. B. Nikolajczyk, M. Jagannathan-Bogdan, and G. Denis, “The outliers become a stampede as immunometabolism reaches a tipping point,” Immunological Reviews, vol. 249, pp. 253–275, 2012. View at Google Scholar
  5. A. Schäffler and J. Schölmerich, “Innate immunity and adipose tissue biology,” Trends in Immunology, vol. 31, no. 6, pp. 228–235, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Cianflone, Z. Xia, and L. Y. Chen, “Critical review of acylation-stimulating protein physiology in humans and rodents,” Biochimica et Biophysica Acta, vol. 1609, no. 2, pp. 127–143, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. H. A. Koistinen, H. Vidal, S.-L. Karonen et al., “Plasma acylation stimulating protein concentration and subcutaneous adipose tissue C3 mRNA expression in nondiabetic and type 2 diabetic men,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 21, no. 6, pp. 1034–1039, 2001. View at Google Scholar · View at Scopus
  8. D. Kalant, R. MacLaren, W. Cui et al., “C5L2 is a functional receptor for acylation-stimulating protein,” The Journal of Biological Chemistry, vol. 280, no. 25, pp. 23936–23944, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Gerard and N. P. Gerard, “C5a anaphylatoxin and its seven transmembrane-segment receptor,” Annual Review of Immunology, vol. 12, pp. 775–808, 1994. View at Google Scholar · View at Scopus
  10. S. Okinaga, D. Slattery, A. Humbles et al., “C5L2, a nonsignaling C5A binding protein,” Biochemistry, vol. 42, no. 31, pp. 9406–9415, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Basen-Engquist and M. Chang, “Obesity and cancer risk: recent review and evidence,” Current Oncology Reports, vol. 13, no. 1, pp. 71–76, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. M. I. Fonseca, R. R. Ager, S.-H. Chu et al., “Treatment with a C5aR antagonist decreases pathology and enhances behavioral performance in murine models of Alzheimer's disease,” Journal of Immunology, vol. 183, no. 2, pp. 1375–1383, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Rittirsch, M. A. Flierl, and P. A. Ward, “Harmful molecular mechanisms in sepsis,” Nature Reviews Immunology, vol. 8, no. 10, pp. 776–787, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. Z. Xun, I. Schmudde, Y. Laumonnier et al., “A critical role for C5L2 in the pathogenesis of experimental allergic asthma,” Journal of Immunology, vol. 185, no. 11, pp. 6741–6752, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. Y.-Y. Zheng, X. Xie, Y.-T. Ma et al., “Relationship between a novel polymorphism of the C5L2 gene and coronary artery disease,” PLoS ONE, vol. 6, no. 6, Article ID e20984, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Poursharifi, M. Lapointe, D. Petrin et al., “C5L2 and C5aR interaction in adipocytes and macrophages: insights into adipoimmunology,” Cellular Signalling, vol. 25, pp. 910–918, 2013. View at Google Scholar
  17. M. Bosmann, M. Haggadone, F. Zetoune, J. Sarma, and P. A. Ward, “The interaction between C5a and both C5aR and C5L2 receptors is required for production of G-CSF during acute inflammation,” European Journal of Immunology, vol. 43, pp. 1907–1913, 2013. View at Google Scholar
  18. J. V. Sarma and P. A. Ward, “New developments in C5a receptor signaling,” Cell Health Cytoskelet, vol. 2012, pp. 73–82, 2012. View at Publisher · View at Google Scholar
  19. T. M. Woodruff, K. S. Nandakumar, and F. Tedesco, “Inhibiting the C5-C5a receptor axis,” Molecular Immunology, vol. 48, no. 14, pp. 1631–1642, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Poursharifi, M. Lapointe, A. Fisette et al., “C5aR and C5L2 act in concert to balance immunometabolism in adipose tissue,” Molecular and Cellular Endocrinology, vol. 382, pp. 325–333, 2013. View at Google Scholar
  21. C. E. Bamberg, C. R. Mackay, H. Lee et al., “The C5a receptor (C5aR) C5L2 is a modulator of C5aR-mediated signal transduction,” The Journal of Biological Chemistry, vol. 285, no. 10, pp. 7633–7644, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. J. D. Smith, K. Cianflone, J. Martin, P. Poirier, T. L. Broderick, and M. Noël, “Plasma adipokine and hormone changes in mountaineers on ascent to 5300 meters,” Wilderness and Environmental Medicine, vol. 22, no. 2, pp. 107–114, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. S. A. Bustin, V. Benes, J. A. Garson et al., “The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments,” Clinical Chemistry, vol. 55, no. 4, pp. 611–622, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. R. Sturm, “Increases in morbid obesity in the USA: 2000–2005,” Public Health, vol. 121, no. 7, pp. 492–496, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Nagao, S. Kashine, H. Nishizawa et al., “Vascular complications and changes in body mass index in Japanese type 2 diabetic patients with abdominal obesity,” Cardiovascular Diabetology, vol. 12, no. 1, article 88, 2013. View at Google Scholar
  26. A. Tchernof and J. Despres, “Pathophysiology of human visceral obesity: an update,” Physiological Reviews, vol. 93, pp. 359–404, 2013. View at Google Scholar
  27. Y. Gao, D. Gauvreau, W. Cui, M. Lapointe, S. Paglialunga, and K. Cianflone, “Evaluation of chylomicron effect on ASP production in 3T3-L1 adipocytes,” Acta Biochimica et Biophysica Sinica, vol. 43, no. 2, pp. 154–159, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Wen, H. Wang, R. MacLaren, J. Wu, H. Lu, and K. Cianflone, “Palmitate and oleate induction of acylation stimulating protein resistance in 3T3-L1 adipocytes and preadipocytes,” Journal of Cellular Biochemistry, vol. 104, no. 2, pp. 391–401, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Paglialunga, P. Schrauwen, C. Roy et al., “Reduced adipose tissue triglyceride synthesis and increased muscle fatty acid oxidation in C5L2 knockout mice,” The Journal of Endocrinology, vol. 194, no. 2, pp. 293–304, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Huber-Lang, J. V. Sarma, D. Rittirsch et al., “Changes in the novel orphan, C5a receptor (C5L2), during experimental sepsis and sepsis in humans,” The Journal of Immunology, vol. 174, no. 2, pp. 1104–1110, 2005. View at Google Scholar · View at Scopus
  31. E. Apostolidou, K. Kambas, A. Chrysanthopoulou et al., “Genetic analysis of C5a receptors in neutrophils from patients with familial Mediterranean fever,” Molecular Biology Reports, vol. 39, no. 5, pp. 5503–5510, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. A.-C. Raby, B. Holst, J. Davies et al., “TLR activation enhances C5a-induced pro-inflammatory responses by negatively modulating the second C5a receptor, C5L2,” European Journal of Immunology, vol. 41, no. 9, pp. 2741–2752, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. R. MacLaren, D. Kalant, and K. Cianflone, “The ASP receptor C5L2 is regulated by metabolic hormones associated with insulin resistance,” Biochemistry and Cell Biology, vol. 85, no. 1, pp. 11–21, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Tahiri, F. Karpe, G. D. Tan, and K. Cianflone, “Rosiglitazone decreases postprandial production of acylation stimulating protein in type 2 diabetics,” Nutrition and Metabolism, vol. 4, article 11, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Fisette, M. Munkonda, K. Oikonomopoulou, S. Paglialunga, J. Lambris, and K. Cianflone, “C5L2 receptor disruption enhances the development of diet-induced insulin resistance in mice,” Immunobiology, vol. 218, pp. 127–133, 2013. View at Google Scholar
  36. A. Fisette, M. Lapointe, and K. Cianflone, “Obesity-inducing diet promotes acylation stimulating protein resistance,” Biochemical and Biophysical Research Communications, vol. 437, pp. 403–407, 2013. View at Google Scholar
  37. A. Fisette, P. Poursharifi, K. Oikonomopoulou, M. Munkonda, M. Lapointe, and K. Cianflone, “Paradoxical glucose-sensitizing yet proinflammatory effects of acute ASP administration in mice,” Mediators of Inflammation, vol. 2013, Article ID 713284, 9 pages, 2013. View at Publisher · View at Google Scholar
  38. F. Tom, D. Gauvreau, M. Lapointe et al., “Differential chemoattractant response in adipocytes and macrophages to the action of acylation stimulating protein,” European Journal of Cell Biology, vol. 92, pp. 61–69, 2013. View at Google Scholar
  39. C. Roy, A. Gupta, A. Fisette et al., “C5a receptor deficiency alters energy utilization and fat storage,” PLoS ONE, vol. 8, Article ID e62531, 2013. View at Google Scholar
  40. J. Lim, A. Iyer, J. Suen, R. Reid, L. Brown, and D. Fairlie, “C5aR and C3aR antagonists each inhibit diet-induced obesity, metabolic dysfunction, and adipocyte and macrophage signaling,” FASEB Journal, vol. 27, pp. 822–831, 2013. View at Google Scholar
  41. P. N. Monk, A.-M. Scola, P. Madala, and D. P. Fairlie, “Function, structure and therapeutic potential of complement C5a receptors,” British Journal of Pharmacology, vol. 152, no. 4, pp. 429–448, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. L. M. Proctor, T. V. Arumugam, I. Shiels, R. C. Reid, D. P. Fairlie, and S. M. Taylor, “Comparative anti-inflammatory activities of antagonists to C3a and C5a receptors in a rat model of intestinal ischaemia/reperfusion injury,” British Journal of Pharmacology, vol. 142, no. 4, pp. 756–764, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. W. Blogowski, M. Budkowska, D. Salata et al., “Clinical analysis of selected complement-derived molecules in human adipose tissue,” Journal of Translational Medicine, vol. 11, article 11, 2013. View at Google Scholar
  44. D. E. Croker, R. Halai, D. P. Fairlie, and M. A. Cooper, “C5a, but not C5a-des Arg, induces upregulation of heteromer formation between complement C5a receptors C5aR and C5L2,” Immunology & Cell Biology, vol. 91, pp. 625–633, 2013. View at Google Scholar
  45. D. Rittirsch, M. A. Flierl, B. A. Nadeau et al., “Functional roles for C5a receptors in sepsis,” Nature Medicine, vol. 14, no. 5, pp. 551–557, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Gauvreau, A. Gupta, A. Fisette, F. Tom, and K. Cianflone, “Deficiency of C5L2 increases macrophage infiltration and alters adipose tissue function in mice,” PLoS ONE, vol. 8, Article ID e60795, 2013. View at Google Scholar
  47. J. Yuan, S. J. Gou, J. Huang, J. Hao, M. Chen, and M. H. Zhao, “C5a and its receptors in human Anti-Neutrophil Cytoplasmic Antibody (ANCA)-associated vasculitis,” Arthritis Research & Therapy, vol. 14, no. 3, article R140, 2012. View at Google Scholar
  48. G. Milligan, “A day in the life of a G protein-coupled receptor: the contribution to function of G protein-coupled receptor dimerization,” British Journal of Pharmacology, vol. 153, no. 1, pp. S216–S229, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Bost, M. Aouadi, L. Caron, and B. Binétruy, “The role of MAPKs in adipocyte differentiation and obesity,” Biochimie, vol. 87, no. 1, pp. 51–56, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. C. J. Carlson, S. Koterski, R. J. Sciotti, G. B. Poccard, and C. M. Rondinone, “Enhanced basal activation of mitogen-activated protein kinases in adipocytes from type 2 diabetes: potential role of p38 in the downregulation of GLUT4 expression,” Diabetes, vol. 52, no. 3, pp. 634–641, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Saleh, N. Christou, and K. Cianflone, “Regional specificity of ASP binding in human adipose tissue,” American Journal of Physiology: Endocrinology and Metabolism, vol. 276, no. 5, pp. E815–E821, 1999. View at Google Scholar · View at Scopus