Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014, Article ID 627150, 13 pages
http://dx.doi.org/10.1155/2014/627150
Research Article

Physical Exercise Reduces the Expression of RANTES and Its CCR5 Receptor in the Adipose Tissue of Obese Humans

1Department of Biomedical Research, Dasman Diabetes Institute, 1180 Dasman, Kuwait
2Queensland Children's Medical Research Institute, University of Queensland, Brisbane, QLD 4029, Australia
3Fitness and Rehabilitation Centre, Dasman Diabetes Institute, 1180 Dasman, Kuwait
4Department of Biostatistics and Epidemiology, Dasman Diabetes Institute, 1180 Dasman, Kuwait
5King Fahad Specialist Hospital, Dammam 15215, Saudi Arabia
6Diabetes Research Center, Qatar Biomedical Research Institute, Education City, P.O. Box 5825, Doha, Qatar

Received 19 December 2013; Accepted 30 March 2014; Published 17 April 2014

Academic Editor: Chiara De Luca

Copyright © 2014 Engin Baturcam 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. H. Xu, G. T. Barnes, Q. Yang et al., “Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance,” Journal of Clinical Investigation, vol. 112, no. 12, pp. 1821–1830, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante Jr., “Obesity is associated with macrophage accumulation in adipose tissue,” Journal of Clinical Investigation, vol. 112, no. 12, pp. 1796–1808, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. I. Harman-Boehm, M. Blüher, H. Redel et al., “Macrophage infiltration into omental versus subcutaneous fat across different populations: effect of regional adiposity and the comorbidities of obesity,” Journal of Clinical Endocrinology and Metabolism, vol. 92, no. 6, pp. 2240–2247, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. J. M. Olefsky and C. K. Glass, “Macrophages, inflammation, and insulin resistance,” Annual Review of Physiology, vol. 72, pp. 219–246, 2010. View at Publisher · View at Google Scholar
  5. C. N. Lumeng, J. L. Bodzin, and A. R. Saltiel, “Obesity induces a phenotypic switch in adipose tissue macrophage polarization,” Journal of Clinical Investigation, vol. 117, no. 1, pp. 175–184, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. S. E. Shoelson, J. Lee, and A. B. Goldfine, “Inflammation and insulin resistance,” Journal of Clinical Investigation, vol. 116, no. 7, pp. 1793–1801, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Fujisaka, I. Usui, A. Bukhari et al., “Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice,” Diabetes, vol. 58, no. 11, pp. 2574–2582, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. V. Appay and S. L. Rowland-Jones, “RANTES: a versatile and controversial chemokine,” Trends in Immunology, vol. 22, no. 2, pp. 83–87, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Keophiphath, C. Rouault, A. Divoux, K. Clément, and D. Lacasa, “CCL5 promotes macrophage recruitment and survival in human adipose tissue,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 1, pp. 39–45, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Ross, “Atherosclerosis—an inflammatory disease,” The New England Journal of Medicine, vol. 340, no. 2, pp. 115–126, 1999. View at Publisher · View at Google Scholar
  11. I. Lemieux, A. Pascot, D. Prud'homme et al., “Elevated C-reactive protein: another component of the atherothrombotic profile of abdominal obesity,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 21, no. 6, pp. 961–967, 2001. View at Google Scholar · View at Scopus
  12. C.-H. Tang, C.-J. Hsu, and Y.-C. Fong, “The CCL5/CCR5 axis promotes interleukin-6 production in human synovial fibroblasts,” Arthritis & Rheumatism, vol. 62, no. 12, pp. 3615–3624, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. R. F. Schwabe, R. Bataller, and D. A. Brenner, “Human hepatic stellate cells express CCR5 and RANTES to induce proliferation and migration,” American Journal of Physiology: Gastrointestinal and Liver Physiology, vol. 285, no. 5, pp. G949–G958, 2003. View at Google Scholar · View at Scopus
  14. E. Seki, S. de Minicis, G.-Y. Gwak et al., “CCR1 and CCR5 promote hepatic fibrosis in mice,” Journal of Clinical Investigation, vol. 119, no. 7, pp. 1858–1870, 2009. View at Google Scholar · View at Scopus
  15. J. Melchjorsen and S. R. Paludan, “Induction of RANTES/CCL5 by herpes simplex virus is regulated by nuclear factor κB and interferon regulatory factor 3,” Journal of General Virology, vol. 84, no. 9, pp. 2491–2495, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Shahrara, A. E. I. Proudfoot, J. M. Woods et al., “Amelioration of rat adjuvant-induced arthritis by Met-RANTES,” Arthritis & Rheumatism, vol. 52, no. 6, pp. 1907–1919, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Wu, S. Ghosh, X. D. Perrard et al., “T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity,” Circulation, vol. 115, no. 8, pp. 1029–1038, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Lusso, L. Vangelista, R. Cimbro et al., “Molecular engineering of RANTES peptide mimetics with potent anti-HIV-1 activity,” FASEB Journal, vol. 25, no. 4, pp. 1230–1243, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. E. S. Raborn, F. Marciano-Cabral, N. E. Buckley, B. R. Martin, and G. A. Cabral, “The cannabinoid delta-9-tetrahydrocannabinol mediates inhibition of macrophage chemotaxis to RANTES/CCL5: linkage to the CB2 receptor,” Journal of NeuroImmune Pharmacology, vol. 3, no. 2, pp. 117–129, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M.-L. Berres, R. R. Koenen, A. Rueland et al., “Antagonism of the chemokine Ccl5 ameliorates experimental liver fibrosis in mice,” Journal of Clinical Investigation, vol. 120, no. 11, pp. 4129–4140, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. V. Braunersreuther, C. Pellieux, G. Pelli et al., “Chemokine CCL5/RANTES inhibition reduces myocardial reperfusion injury in atherosclerotic mice,” Journal of Molecular and Cellular Cardiology, vol. 48, no. 4, pp. 789–798, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Duma, D. Häussinger, M. Rogowski, P. Lusso, and S. Grzesiek, “Recognition of RANTES by extracellular parts of the CCR5 receptor,” Journal of Molecular Biology, vol. 365, no. 4, pp. 1063–1075, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Juremalm, N. Olsson, and G. Nilsson, “Selective CCL5/RANTES-induced mast cell migration through interactions with chemokine receptors CCR1 and CCR4,” Biochemical and Biophysical Research Communications, vol. 297, no. 3, pp. 480–485, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Kitade, K. Sawamoto, M. Nagashimada et al., “CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status,” Diabetes, vol. 61, no. 7, pp. 1680–1690, 2012. View at Publisher · View at Google Scholar
  25. S. N. Blair, H. W. Kohl III, R. S. Paffenbarger Jr., D. G. Clark, K. H. Cooper, and L. W. Gibbons, “Physical fitness and all-cause mortality: a prospective study of healthy men and women,” Journal of the American Medical Association, vol. 262, no. 17, pp. 2395–2401, 1989. View at Google Scholar · View at Scopus
  26. V. B. O'Leary, C. M. Marchetti, R. K. Krishnan, B. P. Stetzer, F. Gonzalez, and J. P. Kirwan, “Exercise-induced reversal of insulin resistance in obese elderly is associated with reduced visceral fat,” Journal of Applied Physiology, vol. 100, no. 5, pp. 1584–1589, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Shern-Brewer, N. Santanam, C. Wetzstein, J. White-Welkley, and S. Parthasarathy, “Exercise and cardiovascular disease: a new perspective,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 18, no. 7, pp. 1181–1187, 1998. View at Google Scholar · View at Scopus
  28. M. Gleeson, N. C. Bishop, D. J. Stensel, M. R. Lindley, S. S. Mastana, and M. A. Nimmo, “The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease,” Nature Reviews Immunology, vol. 11, no. 9, pp. 607–615, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. N. Mathur and B. K. Pedersen, “Exercise as a mean to control low-grade systemic inflammation,” Mediators of Inflammation, vol. 2008, Article ID 109502, 6 pages, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. A. M. W. Petersen and B. K. Pedersen, “The anti-inflammatory effect of exercise,” Journal of Applied Physiology, vol. 98, no. 4, pp. 1154–1162, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. K. L. Timmerman, M. G. Flynn, P. M. Coen, M. M. Markofski, and B. D. Pence, “Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise?” Journal of Leukocyte Biology, vol. 84, no. 5, pp. 1271–1278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Vissers, W. Hens, J. Taeymans, J. P. Baeyens, J. Poortmans, and L. van Gaal, “The effect of exercise on visceral adipose tissue in overweight adults: a systematic review and meta-analysis,” PLoS ONE, vol. 8, no. 2, Article ID e56415, 2013. View at Google Scholar
  33. N. Kawanishi, H. Yano, Y. Yokogawa, and K. Suzuki, “Exercise training inhibits inflammation in adipose tissue via both suppression of macrophage infiltration and acceleration of phenotypic switching from M1 to M2 macrophages in high-fat-diet-induced obese mice,” Exercise Immunology Review, vol. 16, pp. 105–118, 2010. View at Google Scholar · View at Scopus
  34. M. A. Király, J. Campbell, E. Park et al., “Exercise maintains euglycemia in association with decreased activation of c-Jun NH2-terminal kinase and serine phosphorylation of IRS-1 in the liver of ZDF rats,” American Journal of Physiology: Endocrinology and Metabolism, vol. 298, no. 3, pp. E671–E682, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Caimi, B. Canino, G. Amodeo, M. Montana, and R. L. Presti, “Lipid peroxidation and total antioxidant status in unprofessional athletes before and after a cardiopulmonary test,” Clinical Hemorheology and Microcirculation, vol. 43, no. 3, pp. 235–241, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. N. P. E. Kadoglou, F. Iliadis, N. Angelopoulou et al., “The anti-inflammatory effects of exercise training in patients with type 2 diabetes mellitus,” European Journal of Cardiovascular Prevention and Rehabilitation, vol. 14, no. 6, pp. 837–843, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. Z. Radák, M. Sasvári, C. Nyakas et al., “Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle,” Archives of Biochemistry and Biophysics, vol. 383, no. 1, pp. 114–118, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Abubaker, A. Tiss, M. Abu-Farha et al., “DNAJB3/HSP-40 cochaperone is downregulated in obese humans and is restored by physical exercise,” PLoS ONE, vol. 8, no. 7, Article ID e69217, 2013. View at Google Scholar
  39. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Huber, F. W. Kiefer, M. Zeyda et al., “CC chemokine and CC chemokine receptor profiles in visceral and subcutaneous adipose tissue are altered in human obesity,” Journal of Clinical Endocrinology and Metabolism, vol. 93, no. 8, pp. 3215–3221, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Gordon, “Alternative activation of macrophages,” Nature Reviews Immunology, vol. 3, no. 1, pp. 23–35, 2003. View at Publisher · View at Google Scholar
  42. H. Kanda, S. Tateya, Y. Tamori et al., “MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity,” Journal of Clinical Investigation, vol. 116, no. 6, pp. 1494–1505, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. A. C. Konner and J. C. Bruning, “Toll-like receptors: linking inflammation to metabolism,” Trends in Endocrinology & Metabolism, vol. 22, no. 1, pp. 16–23, 2011. View at Publisher · View at Google Scholar
  44. R. Madani, K. Karastergiou, N. C. Ogston et al., “RANTES release by human adipose tissue in vivo and evidence for depot-specific differences,” American Journal of Physiology: Endocrinology and Metabolism, vol. 296, no. 6, pp. E1262–E1268, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Gordon and P. R. Taylor, “Monocyte and macrophage heterogeneity,” Nature Reviews Immunology, vol. 5, no. 12, pp. 953–964, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati, “The chemokine system in diverse forms of macrophage activation and polarization,” Trends in Immunology, vol. 25, no. 12, pp. 677–686, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. J. I. Odegaard, R. R. Ricardo-Gonzalez, A. Red Eagle et al., “Alternative M2 activation of kupffer cells by PPARδ ameliorates obesity-induced insulin resistance,” Cell Metabolism, vol. 7, no. 6, pp. 496–507, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. K. J. Katschke Jr., J. B. Rottman, J. H. Ruth et al., “Differential expression of chemokine receptors on peripheral blood, synovial fluid, and synovial tissue monocytes/macrophages in rheumatoid arthritis,” Arthritis & Rheumatology, vol. 44, no. 5, pp. 1022–1032, 2001. View at Publisher · View at Google Scholar
  49. S. Bjorkander, G. Heidari-Hamedani, K. Bremme, I. Gunnarsson, and U. Holmlund, “Peripheral monocyte expression of the chemokine receptors CCR2, CCR5 and CXCR3 is altered at parturition in healthy women and in women with systemic lupus erythematosus,” Scandinavian Journal of Immunology, vol. 77, no. 3, pp. 200–212, 2013. View at Publisher · View at Google Scholar
  50. L. Ziegler-Heitbrock, “The CD14+ CD16+ blood monocytes: their role in infection and inflammation,” Journal of Leukocyte Biology, vol. 81, no. 3, pp. 584–592, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Takahashi, M. Miyashita, N. Kawanishi et al., “Low-volume exercise training attenuates oxidative stress and neutrophils activation in older adults,” European Journal of Applied Physiology, vol. 113, no. 5, pp. 1117–1126, 2013. View at Publisher · View at Google Scholar
  52. N. Kawanishi, H. Yano, T. Mizokami, M. Takahashi, E. Oyanagi, and K. Suzuki, “Exercise training attenuates hepatic inflammation, fibrosis and macrophage infiltration during diet induced-obesity in mice,” Brain, Behavior, and Immunity, vol. 26, no. 6, pp. 931–941, 2012. View at Publisher · View at Google Scholar
  53. G. da Luz, M. J. S. Frederico, S. da Silva et al., “Endurance exercise training ameliorates insulin resistance and reticulum stress in adipose and hepatic tissue in obese rats,” European Journal of Applied Physiology, vol. 111, no. 9, pp. 2015–2023, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. A. G. Oliveira, B. M. Carvalho, N. Tobar et al., “Physical exercise reduces circulating lipopolysaccharide and TLR4 activation and improves insulin signaling in tissues of DIO rats,” Diabetes, vol. 60, no. 3, pp. 784–796, 2011. View at Publisher · View at Google Scholar · View at Scopus