Skip to main content
Top
Published in: European Journal of Applied Physiology 9/2016

Open Access 01-09-2016 | Original Article

Moderate-intensity exercise alters markers of alternative activation in circulating monocytes in females: a putative role for PPARγ

Authors: J. S. Ruffino, N. A. Davies, K. Morris, M. Ludgate, L. Zhang, R. Webb, A. W. Thomas

Published in: European Journal of Applied Physiology | Issue 9/2016

Login to get access

Abstract

Purpose

Monocytes may be primed towards differentiation into classically activated M1 macrophages or alternatively activated M2 macrophages. M1 macrophages greatly contribute to the inflammation which promotes insulin resistance, whereas M2 macrophages resolve inflammation. We have previously shown that exercise increases M2 marker expression in mixed mononuclear cells, possibly via activation of the nuclear transcription factor PPARγ. However, these effects have not been demonstrated specifically within monocytes. Thus, we aimed to investigate whether moderate-intensity exercise elicited similar effects on monocytic M1/M2 marker expression and PPARγ activity to those reported previously in mononuclear cells, so as to further elucidate the mechanisms by which exercise may alter inflammatory status and, accordingly, prevent insulin resistance.

Methods/results

19 sedentary females completed an 8 week moderate-intensity exercise programme (walking 45 min, thrice weekly). Monocytes were isolated from blood via immunomagnetic separation; monocyte expression of M2 markers (Dectin-1: 2.6 ± 1.9-fold; IL-10: 3.0 ± 2.8-fold) significantly increased, whilst the expression of the M1 marker MCP-1 significantly decreased (0.83 ± 0.2 cf. basal), over the duration of the programme. Serum PPARγ activity levels and PPARγ target-genes (CD36: 1.9 ± 1.5-fold; LXRα: 5.0 ± 4.7-fold) were significantly increased after the 8 week exercise programme. Associated with these effects were significant improvements in systemic insulin sensitivity (McAuley’s ISI: Δ0.98 M/mU/L cf. basal).

Conclusion

Exercise participation suppressed M1 markers and induced M2 markers in monocytes, potentially via PPARγ-triggered signalling, and these effects may contribute (perhaps via priming of monocytes for differentiation into M2 tissue-macrophages) to improved systemic insulin sensitivity in exercising participants. These findings provide an alternative mechanism by which exercise may exert its anti-inflammatory effects in order to prevent insulin resistance and type 2 diabetes.
Appendix
Available only for authorised users
Literature
go back to reference Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, Wynshaw-Boris A, Poli G, Olefsky J, Karin M (2005) IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 11(2):191–198CrossRefPubMed Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, Wynshaw-Boris A, Poli G, Olefsky J, Karin M (2005) IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 11(2):191–198CrossRefPubMed
go back to reference Ascaso JF, Pardo S, Real JT, Lorente RI, Priego A, Carmena R (2003) Diagnosing insulin resistance by simple quantitative methods in subjects with normal glucose metabolism. Diabetes Care 26(12):3320–3325CrossRefPubMed Ascaso JF, Pardo S, Real JT, Lorente RI, Priego A, Carmena R (2003) Diagnosing insulin resistance by simple quantitative methods in subjects with normal glucose metabolism. Diabetes Care 26(12):3320–3325CrossRefPubMed
go back to reference Bagchi D, Preuss HG (2012) Obesity: epidemiology, pathophysiology, and prevention, 2nd edn. CRC Press, LondonCrossRef Bagchi D, Preuss HG (2012) Obesity: epidemiology, pathophysiology, and prevention, 2nd edn. CRC Press, LondonCrossRef
go back to reference Bouhlel MA, Derudas B, Rigamonti E, Dievart R, Brozek J, Haulon S, Zawadzki C, Jude B, Torpier G, Marx N, Staels B, Chinetti-Gbaguidi G (2007) PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab 6(2):137–143CrossRefPubMed Bouhlel MA, Derudas B, Rigamonti E, Dievart R, Brozek J, Haulon S, Zawadzki C, Jude B, Torpier G, Marx N, Staels B, Chinetti-Gbaguidi G (2007) PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab 6(2):137–143CrossRefPubMed
go back to reference Bruun JM, Helge JW, Richelsen B, Stallknecht B (2006) 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(5):E961–E967CrossRefPubMed Bruun JM, Helge JW, Richelsen B, Stallknecht B (2006) 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(5):E961–E967CrossRefPubMed
go back to reference Butcher LR, Thomas A, Backx K, Roberts A, Webb R, Morris K (2008) Low-intensity exercise exerts beneficial effects on plasma lipids via PPARgamma. Med Sci Sports Exerc 40(7):1263–1270CrossRefPubMed Butcher LR, Thomas A, Backx K, Roberts A, Webb R, Morris K (2008) Low-intensity exercise exerts beneficial effects on plasma lipids via PPARgamma. Med Sci Sports Exerc 40(7):1263–1270CrossRefPubMed
go back to reference Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, Chasan-Taber L, Albright AL, Braun B, American College of Sports Medicine, American Diabetes Association (2010) Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement. Diabetes Care 33(12):e147–e167CrossRefPubMedPubMedCentral Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, Chasan-Taber L, Albright AL, Braun B, American College of Sports Medicine, American Diabetes Association (2010) Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement. Diabetes Care 33(12):e147–e167CrossRefPubMedPubMedCentral
go back to reference Collingwood TN, Butler A, Tone Y, Clifton-Bligh RJ, Parker MG, Chatterjee VK (1997) Thyroid hormone-mediated enhancement of heterodimer formation between thyroid hormone receptor beta and retinoid X receptor. J Biol Chem 272(20):13060–13065CrossRefPubMed Collingwood TN, Butler A, Tone Y, Clifton-Bligh RJ, Parker MG, Chatterjee VK (1997) Thyroid hormone-mediated enhancement of heterodimer formation between thyroid hormone receptor beta and retinoid X receptor. J Biol Chem 272(20):13060–13065CrossRefPubMed
go back to reference Dalmas E, Clement K, Guerre-Millo M (2011) Defining macrophage phenotype and function in adipose tissue. Trends Immunol 32(7):307–314CrossRefPubMed Dalmas E, Clement K, Guerre-Millo M (2011) Defining macrophage phenotype and function in adipose tissue. Trends Immunol 32(7):307–314CrossRefPubMed
go back to reference Diabetes Prevention Program Research Group (2002) The Diabetes Prevention Program (DPP): description of lifestyle intervention. Diabetes Care 25(12):2165–2171CrossRef Diabetes Prevention Program Research Group (2002) The Diabetes Prevention Program (DPP): description of lifestyle intervention. Diabetes Care 25(12):2165–2171CrossRef
go back to reference Díaz-Gandarilla JA, Osorio-Trujillo C, Hernandez-Ramirez VI, Talamas-Rohana P (2013) PPAR activation induces M1 macrophage polarization via cPLA(2)-COX-2 inhibition, activating ROS production against Leishmania mexicana. BioMed Res Int 2013:215283CrossRefPubMedPubMedCentral Díaz-Gandarilla JA, Osorio-Trujillo C, Hernandez-Ramirez VI, Talamas-Rohana P (2013) PPAR activation induces M1 macrophage polarization via cPLA(2)-COX-2 inhibition, activating ROS production against Leishmania mexicana. BioMed Res Int 2013:215283CrossRefPubMedPubMedCentral
go back to reference Dishman RK, Heath G, Lee IM (2013) Physical activity epidemiology, 2nd edn. Human Kinetics, Leeds Dishman RK, Heath G, Lee IM (2013) Physical activity epidemiology, 2nd edn. Human Kinetics, Leeds
go back to reference Eriksson J, Lindström J, Valle T, Aunola S, Hämäläinen H, Ilanne-Parikka P, Keinänen-Kiukaanniemi S, Laakso M, Lauhkonen M, Lehto P, Lehtonen A, Louheranta A, Mannelin M, Martikkala V, Rastas M, Sundvall J, Turpeinen A, Viljanen T, Uusitupa M, Tuomilehto J (1999) Prevention of Type II diabetes in subjects with impaired glucose tolerance: the Diabetes Prevention Study (DPS) in Finland. Study design and 1-year interim report on the feasibility of the lifestyle intervention programme. Diabetologia 42(7):793–801CrossRefPubMed Eriksson J, Lindström J, Valle T, Aunola S, Hämäläinen H, Ilanne-Parikka P, Keinänen-Kiukaanniemi S, Laakso M, Lauhkonen M, Lehto P, Lehtonen A, Louheranta A, Mannelin M, Martikkala V, Rastas M, Sundvall J, Turpeinen A, Viljanen T, Uusitupa M, Tuomilehto J (1999) Prevention of Type II diabetes in subjects with impaired glucose tolerance: the Diabetes Prevention Study (DPS) in Finland. Study design and 1-year interim report on the feasibility of the lifestyle intervention programme. Diabetologia 42(7):793–801CrossRefPubMed
go back to reference Febbraio MA, Pedersen BK (2002) Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J 16(11):1335–1347CrossRefPubMed Febbraio MA, Pedersen BK (2002) Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J 16(11):1335–1347CrossRefPubMed
go back to reference Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18(6):499–502PubMed Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18(6):499–502PubMed
go back to reference Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K (2010) Development of monocytes, macrophages, and dendritic cells. Science 327(5966):656–661CrossRefPubMedPubMedCentral Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K (2010) Development of monocytes, macrophages, and dendritic cells. Science 327(5966):656–661CrossRefPubMedPubMedCentral
go back to reference Ginhoux F, Jung S (2014) Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat Rev Immunol 14(6):392–404CrossRefPubMed Ginhoux F, Jung S (2014) Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat Rev Immunol 14(6):392–404CrossRefPubMed
go back to reference Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA (2011) The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol 11(9):607–615CrossRefPubMed Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA (2011) The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol 11(9):607–615CrossRefPubMed
go back to reference Golbidi S, Badran M, Laher I (2012) Antioxidant and anti-inflammatory effects of exercise in diabetic patients. Exp Diabetes Res (Article ID 941868) Golbidi S, Badran M, Laher I (2012) Antioxidant and anti-inflammatory effects of exercise in diabetic patients. Exp Diabetes Res (Article ID 941868)
go back to reference Goldfine AB, Conlin PR, Halperin F, Koska J, Permana P, Schwenke D, Shoelson SE, Reaven PD (2013) A randomised trial of salsalate for insulin resistance and cardiovascular risk factors in persons with abnormal glucose tolerance. Diabetologia 56(4):714–723CrossRefPubMedPubMedCentral Goldfine AB, Conlin PR, Halperin F, Koska J, Permana P, Schwenke D, Shoelson SE, Reaven PD (2013) A randomised trial of salsalate for insulin resistance and cardiovascular risk factors in persons with abnormal glucose tolerance. Diabetologia 56(4):714–723CrossRefPubMedPubMedCentral
go back to reference Han MS, Jung DY, Morel C, Lakhani SA, Kim JK, Flavell RA, Davis RJ (2013) JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation. Science 339(6116):218–222CrossRefPubMed Han MS, Jung DY, Morel C, Lakhani SA, Kim JK, Flavell RA, Davis RJ (2013) JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation. Science 339(6116):218–222CrossRefPubMed
go back to reference Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM (2012) Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012:948098CrossRefPubMedPubMedCentral Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM (2012) Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012:948098CrossRefPubMedPubMedCentral
go back to reference Harford KA, Reynolds CM, McGillicuddy FC, Roche HM (2011) Fats, inflammation and insulin resistance: insights to the role of macrophage and T-cell accumulation in adipose tissue. Proc Nutr Soc 70(4):408–417CrossRefPubMed Harford KA, Reynolds CM, McGillicuddy FC, Roche HM (2011) Fats, inflammation and insulin resistance: insights to the role of macrophage and T-cell accumulation in adipose tissue. Proc Nutr Soc 70(4):408–417CrossRefPubMed
go back to reference Heusinkveld M, de Vos van Steenwijk PJ, Goedemans R, Ramwadhdoebe TH, Gorter A, Welters MJ, van Hall T, van der Burg SH (2011) M2 macrophages induced by prostaglandin E2 and IL-6 from cervical carcinoma are switched to activated M1 macrophages by CD4 + Th1 cells. J Immunol 187(3):1157–1165CrossRefPubMed Heusinkveld M, de Vos van Steenwijk PJ, Goedemans R, Ramwadhdoebe TH, Gorter A, Welters MJ, van Hall T, van der Burg SH (2011) M2 macrophages induced by prostaglandin E2 and IL-6 from cervical carcinoma are switched to activated M1 macrophages by CD4 + Th1 cells. J Immunol 187(3):1157–1165CrossRefPubMed
go back to reference Hevener AL, Olefsky JM, Reichart D, Nguyen MT, Bandyopadyhay G, Leung HY, Watt MJ, Benner C, Febbraio MA, Nguyen AK, Folian B, Subramaniam S, Gonzalez FJ, Glass CK, Ricote M (2007) Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J Clin Invest 117(6):1658–1669CrossRefPubMedPubMedCentral Hevener AL, Olefsky JM, Reichart D, Nguyen MT, Bandyopadyhay G, Leung HY, Watt MJ, Benner C, Febbraio MA, Nguyen AK, Folian B, Subramaniam S, Gonzalez FJ, Glass CK, Ricote M (2007) Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J Clin Invest 117(6):1658–1669CrossRefPubMedPubMedCentral
go back to reference Huang W, Metlakunta A, Dedousis N, Zhang P, Sipula I, Dube JJ, Scott DK, O’Doherty RM (2010) Depletion of liver Kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance. Diabetes 59(2):347–357CrossRefPubMed Huang W, Metlakunta A, Dedousis N, Zhang P, Sipula I, Dube JJ, Scott DK, O’Doherty RM (2010) Depletion of liver Kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance. Diabetes 59(2):347–357CrossRefPubMed
go back to reference Ikeda S, Tamura Y, Kakehi S, Takeno K, Kawaguchi M, Watanabe T, Sato F, Ogihara T, Kanazawa A, Fujitani Y, Kawamori R, Watada H (2013) Exercise-induced enhancement of insulin sensitivity is associated with accumulation of M2-polarized macrophages in mouse skeletal muscle. Biochem Biophys Res Commun 441(1):36–41CrossRefPubMed Ikeda S, Tamura Y, Kakehi S, Takeno K, Kawaguchi M, Watanabe T, Sato F, Ogihara T, Kanazawa A, Fujitani Y, Kawamori R, Watada H (2013) Exercise-induced enhancement of insulin sensitivity is associated with accumulation of M2-polarized macrophages in mouse skeletal muscle. Biochem Biophys Res Commun 441(1):36–41CrossRefPubMed
go back to reference Kawanishi N, Yano H, Yokogawa Y, Suzuki K (2010) 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 16:105–118PubMed Kawanishi N, Yano H, Yokogawa Y, Suzuki K (2010) 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 16:105–118PubMed
go back to reference Kharraz Y, Guerra J, Mann CJ, Serrano AL, Munoz-Canoves P (2013) Macrophage plasticity and the role of inflammation in skeletal muscle repair. Mediat Inflamm (Article ID 491497) Kharraz Y, Guerra J, Mann CJ, Serrano AL, Munoz-Canoves P (2013) Macrophage plasticity and the role of inflammation in skeletal muscle repair. Mediat Inflamm (Article ID 491497)
go back to reference Kline GM, Porcari JP, Hintermeister R, Freedson PS, Ward A, McCarron RF, Ross J, Rippe JM (1987) Estimation of VO2max from a one-mile track walk, gender, age, and body weight. Med Sci Sports Exerc 19(3):253–259CrossRefPubMed Kline GM, Porcari JP, Hintermeister R, Freedson PS, Ward A, McCarron RF, Ross J, Rippe JM (1987) Estimation of VO2max from a one-mile track walk, gender, age, and body weight. Med Sci Sports Exerc 19(3):253–259CrossRefPubMed
go back to reference Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA, Nathan DM, Group DPPR (2002) Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 346(6):393–403CrossRefPubMed Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA, Nathan DM, Group DPPR (2002) Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 346(6):393–403CrossRefPubMed
go back to reference Kraus WE, Slentz CA (2009) Exercise training, lipid regulation, and insulin action: a tangled web of cause and effect. Obesity 17(Suppl 3):S21–S26CrossRefPubMed Kraus WE, Slentz CA (2009) Exercise training, lipid regulation, and insulin action: a tangled web of cause and effect. Obesity 17(Suppl 3):S21–S26CrossRefPubMed
go back to reference Kristiansen OP, Mandrup-Poulsen T (2005) Interleukin-6 and diabetes: the good, the bad, or the indifferent? Diabetes 54(Suppl 2):S114–S124CrossRefPubMed Kristiansen OP, Mandrup-Poulsen T (2005) Interleukin-6 and diabetes: the good, the bad, or the indifferent? Diabetes 54(Suppl 2):S114–S124CrossRefPubMed
go back to reference Lee HW, Choi HJ, Ha SJ, Lee KT, Kwon YG (2013) Recruitment of monocytes/macrophages in different tumor microenvironments. Biochim Biophys Acta 1835(2):170–179PubMed Lee HW, Choi HJ, Ha SJ, Lee KT, Kwon YG (2013) Recruitment of monocytes/macrophages in different tumor microenvironments. Biochim Biophys Acta 1835(2):170–179PubMed
go back to reference Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25(12):677–686CrossRefPubMed Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25(12):677–686CrossRefPubMed
go back to reference Mauer J, Chaurasia B, Goldau J, Vogt MC, Ruud J, Nguyen KD, Theurich S, Hausen AC, Schmitz J, Bronneke HS, Estevez E, Allen TL, Mesaros A, Partridge L, Febbraio MA, Chawla A, Wunderlich FT, Bruning JC (2014) Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesity-associated resistance to insulin. Nat Immunol 15(5):423–430CrossRefPubMedPubMedCentral Mauer J, Chaurasia B, Goldau J, Vogt MC, Ruud J, Nguyen KD, Theurich S, Hausen AC, Schmitz J, Bronneke HS, Estevez E, Allen TL, Mesaros A, Partridge L, Febbraio MA, Chawla A, Wunderlich FT, Bruning JC (2014) Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesity-associated resistance to insulin. Nat Immunol 15(5):423–430CrossRefPubMedPubMedCentral
go back to reference McAuley KA, Williams SM, Mann JI, Walker RJ, Lewis-Barned NJ, Temple LA, Duncan AW (2001) Diagnosing insulin resistance in the general population. Diabetes Care 24(3):460–464CrossRefPubMed McAuley KA, Williams SM, Mann JI, Walker RJ, Lewis-Barned NJ, Temple LA, Duncan AW (2001) Diagnosing insulin resistance in the general population. Diabetes Care 24(3):460–464CrossRefPubMed
go back to reference Moldoveanu AI, Shephard RJ, Shek PN (2000) Exercise elevates plasma levels but not gene expression of IL-1beta, IL-6, and TNF-alpha in blood mononuclear cells. J Appl Physiol 89(4):1499–1504PubMed Moldoveanu AI, Shephard RJ, Shek PN (2000) Exercise elevates plasma levels but not gene expression of IL-1beta, IL-6, and TNF-alpha in blood mononuclear cells. J Appl Physiol 89(4):1499–1504PubMed
go back to reference Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, Red Eagle A, Vats D, Brombacher F, Ferrante AW, Chawla A (2007) Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447(7148):1116–1120CrossRefPubMedPubMedCentral Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, Red Eagle A, Vats D, Brombacher F, Ferrante AW, Chawla A (2007) Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447(7148):1116–1120CrossRefPubMedPubMedCentral
go back to reference Oh J, Riek AE, Weng S, Petty M, Kim D, Colonna M, Cella M, Bernal-Mizrachi C (2012) Endoplasmic reticulum stress controls M2 macrophage differentiation and foam cell formation. J Biol Chem 287(15):11629–11641CrossRefPubMedPubMedCentral Oh J, Riek AE, Weng S, Petty M, Kim D, Colonna M, Cella M, Bernal-Mizrachi C (2012) Endoplasmic reticulum stress controls M2 macrophage differentiation and foam cell formation. J Biol Chem 287(15):11629–11641CrossRefPubMedPubMedCentral
go back to reference Olefsky JM, Glass CK (2010) Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72:219–246CrossRefPubMed Olefsky JM, Glass CK (2010) Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72:219–246CrossRefPubMed
go back to reference Oliveira AG, Araujo TG, Carvalho BM, Guadagnini D, Rocha GZ, Bagarolli RA, Carvalheira JB, Saad MJ (2013) Acute exercise induces a phenotypic switch in adipose tissue macrophage polarization in diet-induced obese rats. Obesity (Silver Spring) 21(12):2545–2556CrossRef Oliveira AG, Araujo TG, Carvalho BM, Guadagnini D, Rocha GZ, Bagarolli RA, Carvalheira JB, Saad MJ (2013) Acute exercise induces a phenotypic switch in adipose tissue macrophage polarization in diet-induced obese rats. Obesity (Silver Spring) 21(12):2545–2556CrossRef
go back to reference Osborn O, Olefsky JM (2012) The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 18(3):363–374CrossRefPubMed Osborn O, Olefsky JM (2012) The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med 18(3):363–374CrossRefPubMed
go back to reference Pan XR, Li GW, Hu YH, Wang JX, Yang WY, An ZX, Hu ZX, Lin J, Xiao JZ, Cao HB, Liu PA, Jiang XG, Jiang YY, Wang JP, Zheng H, Zhang H, Bennett PH, Howard BV (1997) Effects of diet and exercise in preventing NIDDM in people with impaired glucose tolerance: the Da Qing IGT and Diabetes Study. Diabetes Care 20(4):537–544CrossRefPubMed Pan XR, Li GW, Hu YH, Wang JX, Yang WY, An ZX, Hu ZX, Lin J, Xiao JZ, Cao HB, Liu PA, Jiang XG, Jiang YY, Wang JP, Zheng H, Zhang H, Bennett PH, Howard BV (1997) Effects of diet and exercise in preventing NIDDM in people with impaired glucose tolerance: the Da Qing IGT and Diabetes Study. Diabetes Care 20(4):537–544CrossRefPubMed
go back to reference Pan H, Xu X, Hao X, Chen Y (2012) Changes of myogenic reactive oxygen species and interleukin-6 in contracting skeletal muscle cells. Oxid Med Cell Longev 2012:145418CrossRefPubMedPubMedCentral Pan H, Xu X, Hao X, Chen Y (2012) Changes of myogenic reactive oxygen species and interleukin-6 in contracting skeletal muscle cells. Oxid Med Cell Longev 2012:145418CrossRefPubMedPubMedCentral
go back to reference Pedersen BK, Febbraio MA (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88(4):1379–1406CrossRefPubMed Pedersen BK, Febbraio MA (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88(4):1379–1406CrossRefPubMed
go back to reference Petersen AM, Pedersen BK (2005) The anti-inflammatory effect of exercise. J Appl Physiol 98(4):1154–1162CrossRefPubMed Petersen AM, Pedersen BK (2005) The anti-inflammatory effect of exercise. J Appl Physiol 98(4):1154–1162CrossRefPubMed
go back to reference Petersen KF, Dufour S, Savage DB, Bilz S, Solomon G, Yonemitsu S, Cline GW, Befroy D, Zemany L, Kahn BB, Papademetris X, Rothman DL, Shulman GI (2007) The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci USA 104(31):12587–12594CrossRefPubMedPubMedCentral Petersen KF, Dufour S, Savage DB, Bilz S, Solomon G, Yonemitsu S, Cline GW, Befroy D, Zemany L, Kahn BB, Papademetris X, Rothman DL, Shulman GI (2007) The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci USA 104(31):12587–12594CrossRefPubMedPubMedCentral
go back to reference Pradhan Nabzdyk L, Kuchibhotla S, Guthrie P, Chun M, Auster ME, Nabzdyk C, Deso S, Andersen N, Gnardellis C, LoGerfo FW, Veves A (2013) Expression of neuropeptides and cytokines in a rabbit model of diabetic neuroischemic wound healing. J Vasc Surg 58(3):766–775CrossRefPubMed Pradhan Nabzdyk L, Kuchibhotla S, Guthrie P, Chun M, Auster ME, Nabzdyk C, Deso S, Andersen N, Gnardellis C, LoGerfo FW, Veves A (2013) Expression of neuropeptides and cytokines in a rabbit model of diabetic neuroischemic wound healing. J Vasc Surg 58(3):766–775CrossRefPubMed
go back to reference Romeo GR, Lee J, Shoelson SE (2012) Metabolic syndrome, insulin resistance, and roles of inflammation—mechanisms and therapeutic targets. Arterioscler Thromb Vasc Biol 32(8):1771–1776CrossRefPubMedPubMedCentral Romeo GR, Lee J, Shoelson SE (2012) Metabolic syndrome, insulin resistance, and roles of inflammation—mechanisms and therapeutic targets. Arterioscler Thromb Vasc Biol 32(8):1771–1776CrossRefPubMedPubMedCentral
go back to reference Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S (2011) The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta 1813(5):878–888CrossRefPubMed Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S (2011) The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta 1813(5):878–888CrossRefPubMed
go back to reference Szanto A, Balint BL, Nagy ZS, Barta E, Dezso B, Pap A, Szeles L, Poliska S, Oros M, Evans RM, Barak Y, Schwabe J, Nagy L (2010) STAT6 transcription factor is a facilitator of the nuclear receptor PPARgamma-regulated gene expression in macrophages and dendritic cells. Immunity 33(5):699–712CrossRefPubMedPubMedCentral Szanto A, Balint BL, Nagy ZS, Barta E, Dezso B, Pap A, Szeles L, Poliska S, Oros M, Evans RM, Barak Y, Schwabe J, Nagy L (2010) STAT6 transcription factor is a facilitator of the nuclear receptor PPARgamma-regulated gene expression in macrophages and dendritic cells. Immunity 33(5):699–712CrossRefPubMedPubMedCentral
go back to reference Thomas AW, Davies NA, Moir H, Watkeys L, Ruffino JS, Isa SA, Butcher LR, Hughes MG, Morris K, Webb R (2012) Exercise-associated generation of PPARgamma ligands activates PPARgamma signaling events and upregulates genes related to lipid metabolism. J Appl Physiol 112(5):806–815CrossRefPubMed Thomas AW, Davies NA, Moir H, Watkeys L, Ruffino JS, Isa SA, Butcher LR, Hughes MG, Morris K, Webb R (2012) Exercise-associated generation of PPARgamma ligands activates PPARgamma signaling events and upregulates genes related to lipid metabolism. J Appl Physiol 112(5):806–815CrossRefPubMed
go back to reference Tzameli I, Fang H, Ollero M, Shi H, Hamm JK, Kievit P, Hollenberg AN, Flier JS (2004) Regulated production of a peroxisome proliferator-activated receptor-gamma ligand during an early phase of adipocyte differentiation in 3T3-L1 adipocytes. J Biol Chem 279(34):36093–36102CrossRefPubMed Tzameli I, Fang H, Ollero M, Shi H, Hamm JK, Kievit P, Hollenberg AN, Flier JS (2004) Regulated production of a peroxisome proliferator-activated receptor-gamma ligand during an early phase of adipocyte differentiation in 3T3-L1 adipocytes. J Biol Chem 279(34):36093–36102CrossRefPubMed
go back to reference Wahli W, Michalik L (2012) PPARs at the crossroads of lipid signaling and inflammation. Trends Endocrinol Metab 23(7):351–363CrossRefPubMed Wahli W, Michalik L (2012) PPARs at the crossroads of lipid signaling and inflammation. Trends Endocrinol Metab 23(7):351–363CrossRefPubMed
go back to reference Yakeu G, Butcher L, Isa S, Webb R, Roberts AW, Thomas AW, Backx K, James PE, Morris K (2010) Low-intensity exercise enhances expression of markers of alternative activation in circulating leukocytes: roles of PPARgamma and Th2 cytokines. Atherosclerosis 212(2):668–673CrossRefPubMed Yakeu G, Butcher L, Isa S, Webb R, Roberts AW, Thomas AW, Backx K, James PE, Morris K (2010) Low-intensity exercise enhances expression of markers of alternative activation in circulating leukocytes: roles of PPARgamma and Th2 cytokines. Atherosclerosis 212(2):668–673CrossRefPubMed
go back to reference You H, Gao T, Cooper TK, Brian Reeves W, Awad AS (2013) Macrophages directly mediate diabetic renal injury. Am J Physiol Renal Physiol 305(12):1719–1727CrossRef You H, Gao T, Cooper TK, Brian Reeves W, Awad AS (2013) Macrophages directly mediate diabetic renal injury. Am J Physiol Renal Physiol 305(12):1719–1727CrossRef
Metadata
Title
Moderate-intensity exercise alters markers of alternative activation in circulating monocytes in females: a putative role for PPARγ
Authors
J. S. Ruffino
N. A. Davies
K. Morris
M. Ludgate
L. Zhang
R. Webb
A. W. Thomas
Publication date
01-09-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 9/2016
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-016-3414-y

Other articles of this Issue 9/2016

European Journal of Applied Physiology 9/2016 Go to the issue