Strenuous physical exercise adversely affects monocyte chemotaxis

Frauke S. Czepluch; Romain Barrès; Kenneth Caidahl; Servé Olieslagers; Anna Krook; Anette Rickenlund; Anette Rickenlund; Juleen R. Zierath; Johannes Waltenberger

doi:10.1160/TH10-06-0363

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2011; 105(01): 122-130
DOI: 10.1160/TH10-06-0363

Platelets and Blood Cells

Schattauer GmbH

Strenuous physical exercise adversely affects monocyte chemotaxis

Frauke S. Czepluch^*

¹Department of Cardiology, Cardiovascular Research Institute Maastricht, Maastricht University Medical Center, Maastricht, the Netherlands

,

Romain Barrès^**

²Department Molecular Medicine and Surgery, Section of Integrative Physiology, Karolinska Institutet, Stockholm, Sweden

,

Kenneth Caidahl

³Department Molecular Medicine and Surgery, Karolinska Institutet, and Department of Clinical Physiology, Karolinska University Hospital, Stockholm, Sweden

,

Servé Olieslagers

¹Department of Cardiology, Cardiovascular Research Institute Maastricht, Maastricht University Medical Center, Maastricht, the Netherlands

,

Anna Krook

⁴Department Physiology and Pharmacology, Section of Integrative Physiology, Karolinska Institutet, Stockholm, Sweden

,

Anette Rickenlund

³Department Molecular Medicine and Surgery, Karolinska Institutet, and Department of Clinical Physiology, Karolinska University Hospital, Stockholm, Sweden

,

Anette Rickenlund

³Department Molecular Medicine and Surgery, Karolinska Institutet, and Department of Clinical Physiology, Karolinska University Hospital, Stockholm, Sweden

,

Juleen R. Zierath

²Department Molecular Medicine and Surgery, Section of Integrative Physiology, Karolinska Institutet, Stockholm, Sweden

⁴Department Physiology and Pharmacology, Section of Integrative Physiology, Karolinska Institutet, Stockholm, Sweden

,

Johannes Waltenberger^***

¹Department of Cardiology, Cardiovascular Research Institute Maastricht, Maastricht University Medical Center, Maastricht, the Netherlands

› Author Affiliations

Abstract

Summary

Physical exercise is important for proper cardiovascular function and disease prevention, but it may influence the immune system. We evaluated the effect of strenuous exercise on monocyte chemotaxis. Monocytes were isolated from blood of 13 young, healthy, sedentary individuals participating in a three-week training program which consisted of repeated exercise bouts. Monocyte chemotaxis and serological biomarkers were investigated at baseline, after three weeks training and after four weeks recovery. Chemotaxis towards vascular endothelial growth factor-A (VEGF-A) and transforming growth factor-β1 (TGF-β1) was completely inhibited immediately after training (p<0.01), and remained so after four weeks recovery. Likewise, monocyte chemoattractant protein-1 (MCP-1)-induced migration declined after training (p<0.01) and improved only partially during the recovery period. MCP-1 serum levels were significantly reduced after four weeks recovery compared to baseline (p<0.01). Total blood antioxidant capacity was enhanced at this time point (p<0.01). Monocyte chemokinesis, TGF-β1 and nitric oxide serum levels remained unchanged during the study. Strenuous three-week training consisting of repeated exercise bouts in healthy, sedentary individuals reduces monocyte chemotaxis. It remains to be established, whether this is a sound adaptation to increased stimuli or an untoward reaction to overtraining. Nevertheless, the effect remains for several weeks with no exercise.

Keywords

Exercise - monocytes - chemotaxis - VEGF-A - TGF-β1

Full Text

References

References
1 Mora S, Cook N, Buring JE. et al. Physical activity and reduced risk of cardiovascular events: potential mediating mechanisms. Circulation 2007; 116: 2110-2118.
2 Hakim AA, Petrovitch H, Burchfiel CM. et al. Effects of walking on mortality among nonsmoking retired men. N Engl J Med 1998; 338: 94-99.
3 Hedback B, Perk J, Hornblad M. et al. Cardiac rehabilitation after coronary artery bypass surgery: 10-year results on mortality, morbidity and readmissions to hospital. J Cardiovasc Risk 2001; 08: 153-158.
4 Foster C, Porcari JP, Battista RA. et al. The Risk in Exercise Training. American Journal of Lifestyle Medicine 2008; 02: 279-284.
5 Gleeson M. Immune function in sport and exercise. J Appl Physiol 2007; 103: 693-699.
6 Arras M, Ito WD, Scholz D. et al. Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest 1998; 101: 40-50.
7 Czepluch FS, Bergler A, Waltenberger J. Hypercholesterolaemia impairs monocyte function in CAD patients. J Intern Med 2007; 261: 201-204.
8 Stadler N, Eggermann J, Voo S. et al. Smoking-induced monocyte dysfunction is reversed by vitamin C supplementation in vivo. Arterioscler Thromb Vasc Biol 2007; 27: 120-126.
9 Waltenberger J, Lange J, Kranz A. Vascular endothelial growth factor-A-induced chemotaxis of monocytes is attenuated in patients with diabetes mellitus: A potential predictor for the individual capacity to develop collaterals. Circulation 2000; 102: 185-190.
10 Tirziu D, Moodie KL, Zhuang ZW. et al. Delayed arteriogenesis in hypercholesterolemic mice. Circulation 2005; 112: 2501-2509.
11 Achten J, Jeukendrup AE. Heart rate monitoring: applications and limitations. Sports Med 2003; 33: 517-538.
12 Czepluch FS, Waltenberger J. Monocyte responsiveness towards different arteriogenic stimuli: A functional comparison of various chemoattractants and their combinations. Thromb Haemost 2006; 96: 857-858.
13 Halson SL, Jeukendrup AE. Does overtraining exist? An analysis of overreaching and overtraining research. Sports Med 2004; 34: 967-981.
14 Nielsen HG, Hagberg IA, Lyberg T. Marathon running leads to partial exhaustion of ROS-generating capacity in leukocytes. Med Sci Sports Exerc 2004; 36: 68-73.
15 Wolach B, Falk B, Gavrieli R. et al. Neutrophil function response to aerobic and anaerobic exercise in female judoka and untrained subjects. Br J Sports Med 2000; 34: 23-28.
16 Wolach B, Gavrieli R, Ben-Dror SG. et al. Transient decrease of neutrophil chemo-taxis following aerobic exercise. Med Sci Sports Exerc 2005; 37: 949-954.
17 Gavrieli R, Ashlagi-Amiri T, Eliakim A. et al. The effect of aerobic exercise on neutrophil functions. Med Sci Sports Exerc 2008; 40: 1623-1628.
18 Imhof BA, Aurrand-Lions M. Adhesion mechanisms regulating the migration of monocytes. Nat Rev Immunol 2004; 04: 432-444.
19 Connolly PH, Caiozzo VJ, Zaldivar F. et al. Effects of exercise on gene expression in human peripheral blood mononuclear cells. J Appl Physiol 2004; 97: 1461-1469.
20 Whitelaw DM. Observations on human monocyte kinetics after pulse labeling. Cell Tissue Kinet 1972; 05: 311-317.
21 Wong LM, Myers SJ, Tsou CL. et al. Organization and differential expression of the human monocyte chemoattractant protein 1 receptor gene. Evidence for the role of the carboxyl-terminal tail in receptor trafficking. J Biol Chem 1997; 272: 1038-1045.
22 Waltenberger J, Claesson-Welsh L, Siegbahn A. et al. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem 1994; 269: 26988-26995.
23 Wrana JL, Attisano L, Carcamo J. et al. TGF beta signals through a heteromeric protein kinase receptor complex. Cell 1992; 71: 1003-1014.
24 Thompson PD. Exercise prescription and proscription for patients with coronary artery disease. Circulation 2005; 112: 2354-2363.
25 Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352: 1685-1695.
26 Rosa JS, Oliver SR, Flores RL. et al. Kinetic profiles of 18 systemic pro- and anti-inflammatory mediators during and following exercise in children. J Pediatr Endocrinol Metab 2007; 20: 1293-1305.
27 Banerjee AK, Mandal A, Chanda D. et al. Oxidant, antioxidant and physical exercise. Mol Cell Biochem 2003; 253: 307-312.
28 Ji LL. Antioxidants and oxidative stress in exercise. Proc Soc Exp Biol Med 1999; 222: 283-292.
29 Gomez-Cabrera MC, Domenech E, Vina J. Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med 2008; 44: 126-131.
30 Linke A, Erbs S, Hambrecht R. Exercise and the coronary circulation-alterations and adaptations in coronary artery disease. Prog Cardiovasc Dis 2006; 48: 270-284.
31 Jungersten L, Ambring A, Wall B. et al. Both physical fitness and acute exercise regulate nitric oxide formation in healthy humans. J Appl Physiol 1997; 82: 760-764.
32 Van Craenenbroeck EM, Vrints CJ, Haine SE. et al. A maximal exercise bout increases the number of circulating CD34+/KDR+ endothelial progenitor cells in healthy subjects. Relation with lipid profile. J Appl Physiol 2008; 104: 1006-1013.
33 Waltenberger J. Stress testing at the cellular and molecular level to unravel cellular dysfunction and growth factor signal transduction defects: what Molecular Cell Biology can learn from Cardiology. Thromb Haemost 2007; 98: 975-979.
34 Woods J, Lu Q, Ceddia MA. et al. Special feature for the Olympics: effects of exercise on the immune system: exercise-induced modulation of macrophage function. Immunol Cell Biol 2000; 78: 545-553.