Download PDF
Thromb Haemost 2004; 91(03): 587-594
DOI: 10.1160/TH03-10-0644
Wound Healing and Inflammation/Infection
Schattauer GmbH

Moderate-intensity exercise suppresses platelet activation and polymorphonuclear leukocyte interaction with surface-adherent platelets under shear flow in men

Jong-Shyan Wang
1   Graduate Institute of Rehabilitation Science and Center for Gerontological Research, Chang Gung University, Taoyuan, Taiwan
,
Chang-Hui Liao
2   Graduate Institute of Natural Products, Chang Gung University, Taoyuan, Taiwan
› Author AffiliationsFinancial support The study was support under the National Science Council Grant NSC 92-2314-B-182-021.
Further Information

Publication History

Received 23 October 2003

Accepted after revision 04 January 2003

Publication Date:
05 December 2017 (online)

Also available at
    Permissions and Reprints

Summary

The reciprocal modulation of platelet and polymorphonuclear leukocyte (PMN) activities is important in the pathogenesis of thrombosis and inflammation. This study investigated how moderate exercise affects shear-induced platelet activation and subsequent PMNs interaction with platelet-related thrombi under shear flow. Sixteen sedentary healthy men engaged in moderate exercise (about 60% V·O2max) on a bicycle ergometer. Platelet activation, PMNs interaction with surface-adherent platelets, and PMN-dependent inhibition of platelet activation under shear flow were measured both before and immediately after exercise. The results of this study can be summarized as follows: (1) moderate exercise was associated with lower extents of shear-induced platelet adhesion and aggregation, binding of von Willbrand factor (vWF) to platelets, and glycoprotein IIb/IIIa activation and P-selectin expression on platelet than at rest; (2) the velocity and percentage of rolling PMNs increased while the number of PMNs remaining bound to surface-adherent platelets decreased after moderate exercise; (3) although treating the PMNs with oxidized-low density lipoprotein (Ox-LDL) enhanced PMNs interaction with surface-adherent platelets, moderate exercise suppressed the enhancement of platelet-PMN interaction by Ox-LDL; (4) moderate exercise decreased platelet [Ca2+]i elevation induced by ADP and platelet [Ca2+]i levels mediated by PMN and Ox-LDL-treated PMN; and (5) plasma and PMN-derived nitric oxide metabolites and plasma vWF antigen and activity increased after moderate exercise, whereas plasma and platelet-derived soluble P-selectin levels remained unchanged in response to exercise. Therefore, we conclude that moderate-intensity exercise suppresses shear-induced platelet activation and subsequent PMNs adhesion to platelets deposited at sites of vascular injury under flow, thereby reducing the risks of vascular thrombosis and inflammation.

Keywords

Moderate exercise - shear stress - platelet-PMN interaction
 

  • References

  • 1 Wang JS, Jen CJ, Chen HI. Effects of exercise training and deconditioning on platelet function in men. Arterioscler Thromb Vasc Biol 1995; 15: 1668-74.
    CrossrefPubMedGoogle Scholar
  • 2 Wang JS, Jen CJ, Chen HI. Effects of chronic exercise and deconditioning on platelet function in women. J Appl Physiol 1997; 83: 2080-5.
    CrossrefPubMedGoogle Scholar
  • 3 Arraiz GA, Wigle DT, Mao Y. Risk assessment of physical activity and physical fitness in the Canada Health Survey mortality followup study. J Clin Epidemiol 1992; 45: 419-28.
    CrossrefPubMedGoogle Scholar
  • 4 Konstantopoulos K, Grotta JC, Sills C. et al. Shear-induced platelet aggregation in normal subjects and stroke patients. Thromb Haemost 1995; 74: 1329-34.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 5 Neumann F-J, Marx N, Gawaz M. et al. Induction of cytokine expression in leukocytes by binding of thrombin-stimulated platelets. Circulation 1996; 94: 2387-94.
    PubMedGoogle Scholar
  • 6 Bazzoni G, Dejana E, Del Maschio A. Platelet-neutrophil interactions possible relevance in the pathogenesis of thrombosis and inflammation. Haematologica 1991; 76: 491-9.
    PubMedGoogle Scholar
  • 7 Mickelson JK, Lakkis NM. Villarreal-Levy et al. Leukocyte activation with platelet adhesion after coronary angioplasty: a mechanism for recurrent disease?. J Am Coll Cardiol 1996; 28: 345-53.
    CrossrefPubMedGoogle Scholar
  • 8 Hagberg IA, Roald HE, Lyberg T. Adhesion of leukocytes to growing arterial thrombosis. Thromb Haemost 1998; 80: 852-8.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 Zatta A, Prosdocimi M, Bazzoni G. et al. Inhibition of platelet function by polymorphonuclear leukocytes. J Lab Clin Med 1990; 116: 651-60.
    PubMedGoogle Scholar
  • 10 Faint RW, Mackie IJ, Machin SJ. Platelet aggregation is inhibited by a nitric oxide-like factor released from human neutrophils in vitro. Br J Haematol 1991; 71: 539-45.
    PubMedGoogle Scholar
  • 11 Wang JS, Jen CJ, Kung HC. et al. Different effects of strenuous exercise and moderate exercise on platelet function in men. Circulation 1994; 90: 2877-85.
    CrossrefPubMedGoogle Scholar
  • 12 Wang JS, Jen CJ, Lee H. et al. Effects of shortterm exercise on female platelet function during different phases of the menstrual cycle. Arterioscler Thromb Vasc Biol 1997; 17: 1682-6.
    CrossrefPubMedGoogle Scholar
  • 13 Pedersen BK, Nielsen HB. Acute exercise and the immune system. In Pedersen BK. (ed). Exercise Immunology. Austin, Texas: Landes Company; 1997: 5-32.
    Google Scholar
  • 14 Wang JS, Chow SE, Chen JK. Strenuous, acute exercise affects reciprocal modulation of platelet and polymorphonuclear leukocyte activities under shear flow in men. J Thromb Haemost 2003; 01: 2031-7.
    CrossrefPubMedGoogle Scholar
  • 15 Li N, Wallen NH, Hjemdahl P. Evidence for prothrombotic effects of exercise and limited protection by aspirin. Circulation 1999; 100: 1374-9.
    CrossrefPubMedGoogle Scholar
  • 16 Hilberg T, Schmidt V, Glaser D. et al. Platelet activity, sensitivity to agonist, and plateletleukocyte conjugate formation after long-term exercise. Platelets 2002; 13: 273-7.
    CrossrefPubMedGoogle Scholar
  • 17 Hilberg T, Glaser D, Schmidt V. et al. Shortterm exercise and platelet activity, sensitivity to agonist, and platelet-leukocyte conjugate formation. Platelets 2003; 14: 67-74.
    CrossrefPubMedGoogle Scholar
  • 18 Wang JS, Cheng L-J. The effect of strenuous acute exercise on α2-adrenergic agonist-potentiated platelet activation. Arterioscler Thromb Vasc Biol 1999; 19: 1559-65.
    CrossrefPubMedGoogle Scholar
  • 19 Konstantopoulos K, Chow TW, Turner NA. et al. Shear stress-induced binding of von Willebrand factor to platelet. Biorheology 1997; 34: 57-71.
    CrossrefPubMedGoogle Scholar
  • 20 Diacovo TG, Roth SJ, Buccola JM. et al. Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the β2-integrin CD11b/CD18. Blood 1996; 88: 146-57.
    PubMedGoogle Scholar
  • 21 Wang JS, Chow S-E, Chen J-K. et al. Effect of exercise training on oxidized LDL-mediated platelet function in rats. Thromb Haemost 2000; 83: 503-8.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 22 Green Lc, Wagner DA, Glogowski J. et al. Analysis of nitrate, nitrite and [15N]nitrate in biological fluids. Anal Biochem 1982; 126: 131-8.
    CrossrefPubMedGoogle Scholar
  • 23 Lee KW, Lip GY. Effects of lifestyle on hemostasis, fibrinolysis, and platelet reactivity: a systematic review. Arch Inter Med 2003; 163: 2368-92.
    CrossrefPubMedGoogle Scholar
  • 24 Siscovick DS, Weiss NS, Fletcher RH. et al. The incidence of primary cardiac arrest during vigorous exercise. N Engl J Med 1984; 311: 987-7.
    PubMedGoogle Scholar
  • 25 El-Sayed MS, Sale C, Jones PGW. et al. Blood hemostasis in exercise and training. Med Sci Sports Exerc 2000; 32: 918-25.
    PubMedGoogle Scholar
  • 26 Holme PA, Orvim U, Hamers MJ. et al. Shearinduced platelet activation and platelet microparticle formation at blood flow conditions as in arteries with a severe stenosis. Arterioscler Thromb Vasc Biol 1997; 17: 646-53.
    CrossrefPubMedGoogle Scholar
  • 27 Goto S, Salomon DR, Ikeda Y. et al. Characterization of the unique mechanism mediating the shear-dependent binding of soluble von Willebrand factor to platelets. J Biol Chem 1995; 270: 23352-61.
    CrossrefPubMedGoogle Scholar
  • 28 Ikeda Y, Handa M, Kawano K. et al. The role of von Willebrand factor and fibrinogen in platelet aggregation under varying shear stress. J Clin Invest 1991; 87: 1234-40.
    CrossrefPubMedGoogle Scholar
  • 29 Beumer S, Heijnen HFG, Ijsseldijk MJW. et al. Platelet adhesion to fibronectin in flow: The importance of von Willebrand factor and glycoprotein Ib. Blood 1995; 86: 3452-60.
    PubMedGoogle Scholar
  • 30 Beumer S, Heijnen HFG, Ijsseldijk MJW. et al. Platelet adhesion to fibronectin in flow: The importance of von Willebrand factor and glycoprotein Ib. Blood 1995; 86: 3452-60.
    PubMedGoogle Scholar
  • 31 Dong J-F, Bernat MC, Schade A. et al. Ristocetin-dependent, but not botrocetindependent, binding of von Willebrand factor to the platelet glycoprotein Ib-IX-V complex correlates with shear-dependent interactions. Blood 2001; 97: 162-8.
    CrossrefPubMedGoogle Scholar
  • 32 Depraetere H, Ajzenberg N, Girma J-P. et al. Platelet aggregation induced by a monoclonal antibody to A1 Domain of von Willebrand factor. Blood 1998; 91: 3792-9.
    PubMedGoogle Scholar
  • 33 Chow TW, Hellums JD, Moake JL. et al. Shear stress-induced von Willebrand factor binding to platelet glycoprotein Ib initials calcium influx associated with aggregation. Blood 1992; 80: 113-20.
    PubMedGoogle Scholar
  • 34 Stenberg PE, McEver RP, Shuman MA. et al. A platelet alpha-granule membrance protein (GMP 140) is expressed to plasma membrane after activation. J Cell Biol 1985; 101: 880-6.
    CrossrefPubMedGoogle Scholar
  • 35 Spangenberg P, Redlich H, Bergmann I. et al. The platelet glycoprotein IIb/IIIa complex is involved in the adhesion of activation activated platelets to leukocytes. Thromb Haemost 1993; 70: 514-21.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 36 Kaul S, Makkar RR, Nakamura M. et al. Inhibition of acute stent thrombosis under high-shear flow conditions by a nitric oxide donor, DMHD/NO. An ex vivo porcine arteriovenous shunt study. Circulation 1996; 94: 2228-32.
    CrossrefPubMedGoogle Scholar
  • 37 Michelson AD, Benoit SE, Furman MI. et al. Effects of nitric oxide/EDRF on platelet surface glycoproteins. Am J Physiol 1996; 270: H1640-8.
    PubMedGoogle Scholar
  • 38 Jenkins RR. Free radical chemistry. Relationship exercise. Sports Med 1988; 156-70.
    PubMedGoogle Scholar
  • 39 Cooke JP, Tsao PS. Is NO an endogenous antiatherogenic molecule?. Arterioscl Thromb 1994; 14: 653-5.
    CrossrefPubMedGoogle Scholar