Differential effects of endurance training and weight loss on plasma adiponectin multimers and adipose tissue macrophages in younger, moderately overweight men

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 5, 2013, Pages

  Auerbach, Pernille ^a   Nordby, Pernille ^a   Bendtsen, Line Q ^a   Mehlsen, Jesper L ^a   Basnet, Smita K ^a   Vestergaard, Henrik ^a   Ploug, Thorkil ^a   Stallknecht, Bente ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Adipokines; Aerobic exercise; Cytokines; Low grade inflammation; Obesity

Indexed keywords

ADIPONECTIN; C REACTIVE PROTEIN; CD68 ANTIGEN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LEPTIN; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ABDOMINAL SUBCUTANEOUS FAT; ADIPOSE TISSUE; ADULT; ARTICLE; ENDURANCE TRAINING; ENERGY EXPENDITURE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MOLECULAR WEIGHT; OBESITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; WEIGHT REDUCTION; WESTERN BLOTTING;

ADIPOKINES; AEROBIC EXERCISE; CYTOKINES; LOW-GRADE INFLAMMATION; OBESITY;

ADIPONECTIN; ADIPOSE TISSUE; ADULT; HUMANS; MACROPHAGES; MALE; OVERWEIGHT; PHYSICAL ENDURANCE; PHYSICAL FITNESS; PROTEIN MULTIMERIZATION; TREATMENT OUTCOME; WEIGHT LOSS;

EID: 84883378533     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00575.2012     Document Type: Article

References (45)

1. Ando D, Hosaka Y, Suzuki K, Yamagata Z. Effects of exercise training on circulating high molecular weight adiponectin and adiponectin oligomer composition: a randomized controlled trial. J Atheroscler Thromb 16: 733-739, 2009.
2. Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 257: 79-83, 1999.
3. Beavers KM, Brinkley TE, Nicklas BJ. Effect of exercise training on chronic inflammation. Clin Chim Acta 411: 785-793, 2010.
4. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35: 609-616, 1975.
5. Bobbert T, Rochlitz H, Wegewitz U, Akpulat S, Mai K, Weickert MO, Mohlig M, Pfeiffer AF, Spranger J. Changes of adiponectin oligomer composition by moderate weight reduction. Diabetes 54: 2712-2719, 2005.
6. Bruun JM, Helge JW, Richelsen B, Stallknecht B. Diet and exercise reduce low-grade inflammation and macrophage infiltration in adipose tissue but not in skeletal muscle in severely obese subjects. Am J Physiol Endocrinol Metab 290: E961-E967, 2006.
7. Bruun JM, Pedersen SB, Kristensen K, Richelsen B. Opposite regulation of interleukin-8 and tumor necrosis factor-alpha by weight loss. Obes Res 10: 499-506, 2002.
8. Buechler C, Ritter M, Orso E, Langmann T, Klucken J, Schmitz G. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro-and antiinflammatory stimuli. J Leukoc Biol 67: 97-103, 2000.
9. Cancello R, Henegar C, Viguerie N, Taleb S, Poitou C, Rouault C, Coupaye M, Pelloux V, Hugol D, Bouillot JL, Bouloumie A, Barbatelli G, Cinti S, Svensson PA, Barsh GS, Zucker JD, Basdevant A, Langin D, Clement K. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 54: 2277-2286, 2005.
10. Cannon CP, Kumar A. Treatment of overweight and obesity: lifestyle, pharmacologic, and surgical options. Clin Cornerstone 9: 55-68, 2009.
11. Christiansen T, Paulsen SK, Bruun JM, Ploug T, Pedersen SB, Richelsen B. Diet-induced weight loss and exercise alone and in combination enhance the expression of adiponectin receptors in adipose tissue and skeletal muscle, but only diet-induced weight loss enhanced circulating adiponectin. J Clin Endocrinol Metab 95: 911-919, 2010.
12. Combs TP, Berg AH, Obici S, Scherer PE, Rossetti L. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J Clin Invest 108: 1875-1881, 2001.
13. Dandona P, Aljada A, Bandyopadhyay A. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 25: 4-7, 2004.
14. Ebinuma H, Miyazaki O, Yago H, Hara K, Yamauchi T, Kadowaki T. A novel ELISA system for selective measurement of human adiponectin multimers by using proteases. Clin Chim Acta 372: 47-53, 2006.
15. Eligini S, Crisci M, Bono E, Songia P, Tremoli E, Colombo GI, Colli S. Human monocyte-derived macrophages spontaneously differentiated in vitro show distinct phenotypes. J Cell Physiol 2012.
16. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 3: 23-35, 2003.
17. Halberg N, Schraw TD, Wang ZV, Kim JY, Yi J, Hamilton MP, Luby-Phelps K, Scherer PE. Systemic fate of the adipocyte-derived factor adiponectin. Diabetes 58: 1961-1970, 2009.
18. Holness CL, Simmons DL. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 81: 1607-1613, 1993.
19. Kawanishi N, Yano H, Yokogawa Y, Suzuki K. 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. Exerc Immunol Rev 16: 105-118, 2010.
20. Klimcakova E, Kovacikova M, Stich V, Langin D. Adipokines and dietary interventions in human obesity. Obes Rev 11: 446-456, 2010.
21. Kong LQ, Zhu XD, Xu HX, Zhang JB, Lu L, Wang WQ, Zhang QB, Wu WZ, Wang L, Fan J, Tang ZY, Sun HC. The clinical significance of the CD163+ and CD68+ macrophages in patients with hepatocellular carcinoma. PLos One 8: e59771, 2013.
22. Kovacikova M, Sengenes C, Kovacova Z, Siklova-Vitkova M, Klimcakova E, Polak J, Rossmeislova L, Bajzova M, Hejnova J, Hnevkovska Z, Bouloumie A, Langin D, Stich V. Dietary intervention-induced weight loss decreases macrophage content in adipose tissue of obese women. Int J Obes (Lond) 35: 91-98, 2011.
23. Kristiansen M, Graversen JH, Jacobsen C, Sonne O, Hoffman HJ, Law SK, Moestrup SK. Identification of the haemoglobin scavenger receptor. Nature 409: 198-201, 2001.
24. Landis RC, Philippidis P, Domin J, Boyle JJ, Haskard DO. Haptoglobin genotype-dependent anti-inflammatory signaling in CD163(+) macrophages. Int J Inflam 2013: 980327, 2013.
25. Lau SK, Chu PG, Weiss LM. CD163: a specific marker of macrophages in paraffin-embedded tissue samples. Am J Clin Pathol 122: 794-801, 2004.
26. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117: 175-184, 2007.
27. Madsen EL, Rissanen A, Bruun JM, Skogstrand K, Tonstad S, Hougaard DM, Richelsen B. Weight loss larger than 10% is needed for general improvement of levels of circulating adiponectin and markers of inflammation in obese subjects: a 3-year weight loss study. Eur J Endocrinol 158: 179-187, 2008.
28. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23: 549-555, 2002.
29. Morris DL, Singer K, Lumeng CN. Adipose tissue macrophages: phenotypic plasticity and diversity in lean and obese states. Curr Opin Clin Nutr Metab Care 14: 341-346, 2011.
30. Nielsen NB, Hojbjerre L, Sonne MP, Alibegovic AC, Vaag A, Dela F, Stallknecht B. Interstitial concentrations of adipokines in subcutaneous abdominal and femoral adipose tissue. Regul Pept 155: 39-45, 2009.
31. Nordby P, Auerbach PL, Rosenkilde M, Kristiansen L, Thomasen JR, Rygaard L, Groth R, Brandt N, Helge JW, Richter EA, Ploug T, Stallknecht B. Endurance training per se increases metabolic health in young, moderately overweight men. Obesity (Silver Spring) 20: 2202-2212, 2012.
32. O'Leary VB, Jorett AE, Marchetti CM, Gonzalez F, Phillips SA, Ciaraldi TP, Kirwan JP. Enhanced adiponectin multimer ratio and skeletal muscle adiponectin receptor expression following exercise training and diet in older insulin-resistant adults. Am J Physiol Endocrinol Metab 293: E421-E427, 2007.
33. Ouchi N, Walsh K. Adiponectin as an anti-inflammatory factor. Clin Chim Acta 380: 24-30, 2007.
34. Pilling D, Fan T, Huang D, Kaul B, Gomer RH. Identification of markers that distinguish monocyte-derived fibrocytes from monocytes, macrophages, and fibroblasts. PLos One 4: e7475, 2009.
35. Polak J, Kovacova Z, Jacek M, Klimcakova E, Kovacikova M, Vitkova M, Kuda O, Sebela M, Samcova E, Stich V. An increase in plasma adiponectin multimeric complexes follows hypocaloric diet-induced weight loss in obese and overweight pre-menopausal women. Clin Sci (Lond) 112: 557-565, 2007.
36. Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF. A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem 270: 26746-26749, 1995.
37. Selvin E, Paynter NP, Erlinger TP. The effect of weight loss on C-reactive protein: a systematic review. Arch Intern Med 167: 31-39, 2007.
38. Simpson KA, Singh MA. Effects of exercise on adiponectin: a systematic review. Obesity (Silver Spring) 16: 241-256, 2008.
39. Waki H, Yamauchi T, Kamon J, Ito Y, Uchida S, Kita S, Hara K, Hada Y, Vasseur F, Froguel P, Kimura S, Nagai R, Kadowaki T. Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J Biol Chem 278: 40352-40363, 2003.
40. Warnberg J, Cunningham K, Romeo J, Marcos A. Physical activity, exercise and low-grade systemic inflammation. Proc Nutr Soc 69: 400-406, 2010.
41. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808, 2003.
42. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 8: 1288-1295, 2002.
43. You T, Berman DM, Ryan AS, Nicklas BJ. Effects of hypocaloric diet and exercise training on inflammation and adipocyte lipolysis in obese postmenopausal women. J Clin Endocrinol Metab 89: 1739-1746, 2004.
44. Zeyda M, Farmer D, Todoric J, Aszmann O, Speiser M, Gyori G, Zlabinger GJ, Stulnig TM. Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production. Int J Obes (Lond) 31: 1420-1428, 2007.
45. Zwadlo G, Voegeli R, Schulze OK, Sorg C. A monoclonal antibody to a novel differentiation antigen on human macrophages associated with the down-regulatory phase of the inflammatory process. Exp Cell Biol 55: 295-304, 1987.