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Sports Medicine

, Volume 48, Issue 9, pp 2025–2039 | Cite as

Exercise-Derived Microvesicles: A Review of the Literature

  • Eurico N. Wilhelm
  • Laurent Mourot
  • Mark Rakobowchuk
Review Article

Abstract

Initially suggested as simple cell debris, cell-derived microvesicles (MVs) have now gained acceptance as recognized players in cellular communication and physiology. Shed by most, and perhaps all, human cells, these tiny lipid-membrane vesicles carry bioactive agents, such as proteins, lipids and microRNA from their cell source, and are produced under orchestrated events in response to a myriad of stimuli. Physical exercise introduces systemic physiological challenges capable of acutely disrupting cell homeostasis and stimulating the release of MVs into the circulation. The novel and promising field of exercise-derived MVs is expanding quickly, and the following work provides a review of the influence of exercise on circulating MVs, considering both acute and chronic aspects of exercise and training. Potential effects of the MV response to exercise are highlighted and future directions suggested as exercise and sports sciences extend the realm of extracellular vesicles.

Notes

Compliance with Ethical Standards

Conflict of interest

Eurico N. Wilhelm, Laurent Mourot and Mark Rakobowchuk declare that they have no conflicts of interest.

Funding

This research was funded by grants from the French Ministry of National Education, Research and Technology (EA3920), from Tomsk Polytechnic University Competitiveness Enhancement Program grant, Project № BИУ-ИCГT-108/2017—TPU CEP-HSTI-108/2017 and a Natural Science and Engineering Research Council of Canada Discovery Grant to M. R. E. N. W. is supported by the Brazilian Education Ministry Foundation CAPES (Postdoctoral Fellowship).

References

  1. 1.
    Garraud O, Cognasse F. Are platelets cells? and if yes, are they immune cells? Front Immunol. 2015;6:1–8.Google Scholar
  2. 2.
    Berckmans RJ, Nieuwland R, Böing AN, Romijn FP, Hack CE, Sturk A. Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost. 2001;85:639–46.CrossRefPubMedGoogle Scholar
  3. 3.
    Berckmans RJ, Nieuwland R, Tak PP, Böing AN, Romijn FPHTM, Kraan MC, et al. Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII-dependent mechanism. Arthritis Rheum. 2002;46:2857–66.CrossRefPubMedGoogle Scholar
  4. 4.
    Sossdorf M, Otto GP, Claus RA, Gabriel HHW, Lösche W. Cell-derived microparticles promote coagulation after moderate exercise. Med. Sci. Sport. Exerc. 2011;43:1169–76.CrossRefGoogle Scholar
  5. 5.
    Curtis AM, Wilkinson PF, Gui M, Gales TL, Hu E, Edelberg JM. p38 mitogen-activated protein kinase targets the production of proinflammatory endothelial microparticles. J Thromb Haemost. 2009;7:701–9.CrossRefPubMedGoogle Scholar
  6. 6.
    Mause SF, Ritzel E, Liehn EA, Hristov M, Bidzhekov K, Muller-Newen G, et al. Platelet microparticles enhance the vasoregenerative potential of angiogenic early outgrowth cells after vascular injury. Circulation. 2010;122:495–506.CrossRefPubMedGoogle Scholar
  7. 7.
    Kim HK, Song KS, Chung J, Lee KR, Lee S. Platelet microparticles induce angiogenesis in vitro. Br J Haematol. 2004;124:376–84.CrossRefPubMedGoogle Scholar
  8. 8.
    Bernal-Mizrachi L, Jy W, Jimenez JJ, Pastor J, Mauro LM, Horstman LL, et al. High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am Heart J. 2003;145:962–70.CrossRefPubMedGoogle Scholar
  9. 9.
    Dimassi S, Chahed K, Boumiza S, Canault M, Tabka Z, Laurant P, et al. Role of eNOS- and NOX-containing microparticles in endothelial dysfunction in patients with obesity. Obesity. 2016;24:1305–12.CrossRefPubMedGoogle Scholar
  10. 10.
    Feng B, Chen Y, Luo Y, Chen M, Li X, Ni Y. Circulating level of microparticles and their correlation with arterial elasticity and endothelium-dependent dilation in patients with type 2 diabetes mellitus. Atherosclerosis. 2010;208:264–9.CrossRefPubMedGoogle Scholar
  11. 11.
    Horn P, Cortese-krott MM, Amabile N, Hundsöfer C, Kröncke K-D, Kelm M, et al. Circulating microparticles carry a functional endothelial nitric oxide that is decreased in patients with endothelial dysfunction. J Am Heart Assoc. 2012;2:1–12.CrossRefGoogle Scholar
  12. 12.
    Esposito K, Ciotola M, Schisano B, Gualdiero R, Sardelli L, Misso L, et al. Endothelial microparticles correlate with endothelial dysfunction in obese women. J Clin Endocrinol Metab. 2006;91:3676–9.CrossRefPubMedGoogle Scholar
  13. 13.
    Sossdorf M, Otto GP, Claus R a, Gabriel HH, Lösche W. Release of pro-coagulant microparticles after moderate endurance exercise. Platelets. 2010;21:389–91.Google Scholar
  14. 14.
    Rakobowchuk M, Ritter O, Wilhelm EN, Isacco L, Bouhaddi M, Degano B, et al. Divergent endothelial function but similar platelet microvesicle responses following eccentric and concentric cycling at a similar aerobic power output. J Appl Physiol. 2017;122:1031–9.CrossRefPubMedGoogle Scholar
  15. 15.
    Wilhelm EN, González-Alonso J, Parris C, Rakobowchuk M. Exercise intensity modulates the appearance of circulating microvesicles with proangiogenic potential upon endothelial cells. Am J Physiol Heart Circ Physiol. 2016;311:H1297–310.Google Scholar
  16. 16.
    Lansford KA, Shill DD, Dicks AB, Marshburn MP, Southern WM, Jenkins NT. Effect of acute exercise on circulating angiogenic cell and microparticle populations. Exp Physiol. 2016;101:155–67.CrossRefPubMedGoogle Scholar
  17. 17.
    Wilhelm EN, González-Alonso J, Chiesa ST, Trangmar SJ, Kalsi KK, Rakobowchuk M. Whole-body heat stress and exercise stimulate the appearance of platelet microvesicles in plasma with limited influence of vascular shear stress. Physiol Rep. 2017;5:e13496.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Birk GK, Dawson EA, Atkinson C, Haynes A, Cable NT, Thijssen DHJ, et al. Brachial artery adaptation to lower limb exercise training: role of shear stress. J Appl Physiol. 2012;112:1653–8.CrossRefPubMedGoogle Scholar
  19. 19.
    Tinken TM, Thijssen DHJ, Hopkins N, Dawson EA, Cable NT, Green DJ. Shear stress mediates endothelial adaptations to exercise training in humans. Hypertension. 2010;55:312–8.CrossRefPubMedGoogle Scholar
  20. 20.
    Credeur DP, Hollis BC, Welsch MA. Effects of handgrip training with venous restriction on brachial artery vasodilation. Med Sci Sports Exerc. 2010;42:1296–302.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Padilla J, Simmons GH, Bender SB, Arce-Esquivel AA, Whyte JJ, Laughlin MH. Vascular effects of exercise: endothelial adaptations beyond active muscle beds. Physiology. 2011;26:132–45.CrossRefPubMedGoogle Scholar
  22. 22.
    Hargett LA, Bauer NN. On the origin of microparticles: from “platelet dust” to mediators of intercellular communication. Pulm Circ. 2013;3:329–40.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Shantsila E, Kamphuisen PW, Lip GYH. Circulating microparticles in cardiovascular disease: implications for atherogenesis and atherothrombosis. J Thromb Haemost. 2010;8:2358–68.CrossRefPubMedGoogle Scholar
  24. 24.
    Safdar A, Saleem A, Tarnopolsky MA. The potential of endurance exercise-derived exosomes to treat metabolic diseases. Nat Rev Endocrinol. 2016;12:504–17.CrossRefPubMedGoogle Scholar
  25. 25.
    Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569–79.CrossRefPubMedGoogle Scholar
  26. 26.
    Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol. 1967;13:269–88.CrossRefPubMedGoogle Scholar
  27. 27.
    Webber AJ, Johnson SA. Platelet participation in blood coagulation aspects of hemostasis. Am J Pathol. 1970;60:19–42.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Berckmans RJ, Sturk A, van Tienen LM, Schaap MCL, Nieuwland R. Cell-derived vesicles exposing coagulant tissue factor in saliva. Blood. 2011;117:3172–80.CrossRefPubMedGoogle Scholar
  29. 29.
    van der Pol E, van Gemert MJC, Sturk A, Nieuwland R, van Leeuwen TG. Single vs. swarm detection of microparticles and exosomes by flow cytometry. J Thromb Haemost. 2012;10:919–30.Google Scholar
  30. 30.
    Amabile N, Cheng S, Renard JM, Larson MG, Ghorbani A, McCabe E, et al. Association of circulating endothelial microparticles with cardiometabolic risk factors in the Framingham Heart Study. Eur Heart J. 2014;35:2972–9.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Amabile N, Guerin AP, Tedgui A, Boulanger CM, London GM. Predictive value of circulating endothelial microparticles for cardiovascular mortality in end-stage renal failure: a pilot study. Nephrol Dial Transpl. 2012;27:1873–80.CrossRefGoogle Scholar
  32. 32.
    Simak J, Gelderman MP, Yu H, Wright V, Baird AE. Circulating endothelial microparticles in acute ischemic stroke: a link to severity, lesion volume and outcome. J Thromb Haemost. 2006;4:1296–302.CrossRefPubMedGoogle Scholar
  33. 33.
    Jimenez JJ, Jy W, Mauro LM, Soderland C, Horstman LL, Ahn YS. Endothelial cells release phenotypically and quantitatively distinct microparticles in activation and apoptosis. Thromb Res. 2003;109:175–80.CrossRefPubMedGoogle Scholar
  34. 34.
    Jenkins NT, Padilla J, Boyle LJ, Credeur DP, Laughlin MH, Fadel PJ. Disturbed blood flow acutely induces activation and apoptosis of the human vascular endothelium. Hypertension. 2013;61:615–21.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Navasiolava NM, Dignat-George F, Sabatier F, Larina IM, Demiot C, Fortrat J-O, et al. Enforced physical inactivity increases endothelial microparticle levels in healthy volunteers. Am J Physiol Heart Circ Physiol. 2010;299:H248–56.CrossRefPubMedGoogle Scholar
  36. 36.
    Boyle LJ, Credeur DP, Jenkins NT, Padilla J, Leidy HJ, Thyfault JP, et al. Impact of reduced daily physical activity on conduit artery flow-mediated dilation and circulating endothelial microparticles. J Appl Physiol. 2013;115:1519–25.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Chang CP, Zhao J, Wiedmer T, Sims PJ. Contribution of platelet microparticle formation and granule secretion to the transmembrane migration of phosphatidylserine. J Biol Chem. 1993;268:7171–8.PubMedGoogle Scholar
  38. 38.
    Morel O, Jesel L, Freyssinet JM, Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol. 2011;31:15–26.CrossRefPubMedGoogle Scholar
  39. 39.
    Dachary-Prigent J, Pasquet JM, Freyssinet JM, Nurden AT. Calcium involvement in aminophospholipid exposure and microparticle formation during platelet activation: a study using Ca2+ -ATPase inhibitors. Biochemistry. 1995;34:11625–34.CrossRefPubMedGoogle Scholar
  40. 40.
    Fox JE, Austin CD, Reynolds CC, Steffen PK. Evidence that agonist-induced activation of calpain causes the shedding of procoagulant-containing microvesicles from the membrane of aggregating platelets. J Biol Chem. 1991;266:13289–95.PubMedGoogle Scholar
  41. 41.
    Cauwenberghs S, Feijge MAH, Harper AGS, Sage SO, Curvers J, Heemskerk JWM. Shedding of procoagulant microparticles from unstimulated platelets by integrin-mediated destabilization of actin cytoskeleton. FEBS Lett. 2006;580:5313–20.CrossRefPubMedGoogle Scholar
  42. 42.
    Miyazaki Y, Nomura S, Miyake T, Kagawa H, Kitada C, Taniguchi H, et al. High shear stress can initiate both platelet aggregation and shedding of procoagulant containing microparticles. Blood. 1996;88:3456–64.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Tschuor C, Asmis LM, Lenzlinger PM, Tanner M, Härter L, Keel M, et al. In vitro norepinephrine significantly activates isolated platelets from healthy volunteers and critically ill patients following severe traumatic brain injury. Crit Care. 2008;12:R80.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Horstman LL, Ahn YS. Platelet microparticles: a wide-angle perspective. Crit Rev Oncol Hematol. 1999;30:111–42.CrossRefPubMedGoogle Scholar
  45. 45.
    Vion A-C, Ramkhelawon B, Loyer X, Chironi G, Devue C, Loirand G, et al. Shear stress regulates endothelial microparticle release. Circ Res. 2013;112:1323–33.CrossRefPubMedGoogle Scholar
  46. 46.
    Harrison P, Gardiner C. Invisible vesicles swarm within the iceberg. J Thromb Haemost. 2012;10:916–8.CrossRefPubMedGoogle Scholar
  47. 47.
    Headland SE, Jones HR, D’Sa ASV, Perretti M, Norling LV. Cutting-edge analysis of extracellular microparticles using ImageStream(X) imaging flow cytometry. Sci. Rep. 2014;4:5237.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Connor DE, Exner T, Ma DDF, Joseph JE. The majority of circulating platelet-derived microparticles fail to bind annexin V, lack phospholipid-dependent procoagulant activity and demonstrate greater expression of glycoprotein Ib. Thromb Haemost. 2010;103:1044–52.CrossRefPubMedGoogle Scholar
  49. 49.
    Yuana Y, Bertina R, Osanto S. Pre-analytical and analytical issues in the analysis of blood microparticles. Thromb Haemost. 2011;105:396–408.CrossRefPubMedGoogle Scholar
  50. 50.
    Chaar V, Romana M, Tripette J, Broquere C, Huisse MG, Hue O, et al. Effect of strenuous physical exercise on circulating cell-derived microparticles. Clin Hemorheol Microcirc. 2011;47:15–25.PubMedGoogle Scholar
  51. 51.
    Kirk RJ, Peart DJ, Madden LA, Vince RV. Repeated supra-maximal sprint cycling with and without sodium bicarbonate supplementation induces endothelial microparticle release. Eur J Sport Sci. 2014;14:345–52.CrossRefPubMedGoogle Scholar
  52. 52.
    Terrisse AD, Puech N, Allart S, Gourdy P, Xuereb JM, Payrastre B, et al. Internalization of microparticles by endothelial cells promotes platelet/endothelial cell interaction under flow. J Thromb Haemost. 2010;8:2810–9.CrossRefPubMedGoogle Scholar
  53. 53.
    Dasgupta SK, Le A, Chavakis T, Rumbaut RE, Thiagarajan P. Developmental endothelial locus-1 (Del-1) mediates clearance of Platelet microparticles by the endothelium. Circulation. 2012;125:1664–72.CrossRefPubMedGoogle Scholar
  54. 54.
    Abid Hussein MN, Böing AN, Biró É, Hoek FJ, Vogel GMT, Meuleman DG, et al. Phospholipid composition of in vitro endothelial microparticles and their in vivo thrombogenic properties. Thromb Res. 2008;121:865–71.CrossRefPubMedGoogle Scholar
  55. 55.
    Brodsky S V, Zhang F, Nasjletti A, Goligorsky MS. Endothelium-derived microparticles impair endothelial function in vitro. Am J Physiol Heart Circ Physiol. 2004;286:H1910-5.Google Scholar
  56. 56.
    Yang C, Mwaikambo BR, Zhu T, Gagnon C, Lafleur J, Seshadri S, et al. Lymphocytic microparticles inhibit angiogenesis by stimulating oxidative stress and negatively regulating VEGF-induced pathways. Am J Physiol Regul Integr Comp Physiol. 2008;5:467–76.Google Scholar
  57. 57.
    Boulanger CM, Scoazec A, Ebrahimian T, Henry P, Mathieu E, Tedgui A, et al. Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation. 2001;104:2649–52.CrossRefPubMedGoogle Scholar
  58. 58.
    VanWijk MJ, Svedas E, Boer K, Nieuwland R, VanBavel E, Kublickiene KR. Isolated microparticles, but not whole plasma, from women with preeclampsia impair endothelium-dependent relaxation in isolated myometrial arteries from healthy pregnant women. Am J Obstet Gynecol. 2002;187:1686–93.CrossRefPubMedGoogle Scholar
  59. 59.
    Gasser O, Schifferli JA. Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood. 2004;104:2543–8.CrossRefPubMedGoogle Scholar
  60. 60.
    Leroyer AS, Ebrahimian TG, Cochain C, Récalde A, Blanc-Brude O, Mees B, et al. Microparticles from ischemic muscle promotes postnatal vasculogenesis. Circulation. 2009;119:2808–17.CrossRefPubMedGoogle Scholar
  61. 61.
    Arderiu G, Peña E, Badimon L. Angiogenic microvascular endothelial cells release microparticles rich in tissue factor that promotes postischemic collateral vessel formation. Arterioscler Thromb Vasc Biol. 2015;35:348–57.CrossRefPubMedGoogle Scholar
  62. 62.
    Brill A, Dashevsky O, Rivo J, Gozal Y, Varon D. Platelet-derived microparticles induce angiogenesis and stimulate post-ischemic revascularization. Cardiovasc Res. 2005;67:30–8.CrossRefPubMedGoogle Scholar
  63. 63.
    Durrer C, Robinson E, Wan Z, Martinez N, Hummel ML, Jenkins NT, et al. Differential impact of acute high-intensity exercise on circulating endothelial microparticles and insulin resistance between overweight/obese males and females. PLoS One. 2015;10:e0115860.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Schwarz V, Düsing P, Liman T, Werner C, Herm J, Bachelier K, et al. Marathon running increases circulating endothelial- and thrombocyte-derived microparticles. Eur J Prev Cardiol. 2018;25:317–24.CrossRefPubMedGoogle Scholar
  65. 65.
    Mobius-Winkler S, Hilberg T, Menzel K, Golla E, Burman A, Schuler G, et al. Time-dependent mobilization of circulating progenitor cells during strenuous exercise in healthy individuals. J Appl Physiol. 2009;107:1943–50.CrossRefPubMedGoogle Scholar
  66. 66.
    Guiraud T, Gayda M, Juneau M, Bosquet L, Meyer P, Théberge-Julien G, et al. A single bout of high-intensity interval exercise does not increase endothelial or platelet microparticles in stable, physically fit men with coronary heart disease. Can J Cardiol. 2013;29:1285–91.CrossRefPubMedGoogle Scholar
  67. 67.
    Ross MD, Wekesa AL, Phelan JP, Harrison M. Resistance exercise increases endothelial progenitor cells and angiogenic factors. Med Sci Sport Exerc. 2014;46:16–23.CrossRefGoogle Scholar
  68. 68.
    Wahl P, Jansen F, Achtzehn S, Schmitz T, Bloch W, Mester J, et al. Effects of high intensity training and high volume training on endothelial microparticles and angiogenic growth factors. PLoS One. 2014;9:e96024.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Vion AC, Birukova A a, Boulanger CM, Birukov KG. Mechanical forces stimulate endothelial microparticle generation via caspase-dependent apoptosis-independent mechanism. Pulm Circ. 2013;3:95–9.Google Scholar
  70. 70.
    Maruyama K, Kadono T, Morishita E. Plasma levels of platelet-derived microparticles are increased after anaerobic exercise in healthy subjects. J Atheroscler Thromb. 2012;19:585–7.CrossRefPubMedGoogle Scholar
  71. 71.
    Gonzalez-Alonso J, Olsen DB, Saltin B. Erythrocyte and the regulation of human skeletal muscle blood flow and oxygen delivery: role of circulating ATP. Circ Res. 2002;91:1046–55.CrossRefPubMedGoogle Scholar
  72. 72.
    Yegutkin GG, Samburski SS, Mortensen SP, Jalkanen S, González-Alonso J. Intravascular ADP and soluble nucleotidases contribute to acute prothrombotic state during vigorous exercise in humans. J Physiol. 2007;2:553–64.CrossRefGoogle Scholar
  73. 73.
    Padilla J, Simmons GH, Vianna LC, Davis MJ, Laughlin MH, Fadel PJ. Brachial artery vasodilatation during prolonged lower limb exercise: role of shear rate. Exp Physiol. 2011;96:1019–27.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Lacroix R, Judicone C, Mooberry M, Boucekine M, Dignat-George F. Standardization of pre-analytical variables in plasma microparticle determination: results of the International Society on Thrombosis and Haemostasis SSC Collaborative workshop. J Thromb Haemost. 2013;11:1190–3.CrossRefGoogle Scholar
  75. 75.
    Cointe S, Judicone C, Robert S, Mooberry MJ, Poncelet P, Wauben M, et al. Standardization of microparticle enumeration across different flow cytometry platforms: results of a multicenter collaborative workshop. J Thromb Haemost. 2017;15:187–93.CrossRefPubMedGoogle Scholar
  76. 76.
    Cantaluppi V, Gatti S, Medica D, Figliolini F, Bruno S, Deregibus MC, et al. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia—reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 2012;82:412–27.CrossRefPubMedGoogle Scholar
  77. 77.
    Faille D, El-assaad F, Mitchell AJ, Alessi M, Chimini G, Fusai T, et al. Endocytosis and intracellular processing of platelet microparticles by brain endothelial cells. J Cell Mol Med. 2012;16:1731–8.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Ayers L, Nieuwland R, Kohler M, Kraenkel N, Ferry B, Leeson P. Dynamic microvesicle release and clearance within the cardiovascular system: triggers and mechanisms. Clin Sci. 2015;129:915–31.CrossRefPubMedGoogle Scholar
  79. 79.
    Flaumenhaft R. Formation and fate of platelet microparticles. Blood Cells Mol Dis. 2006;36:182–7.Google Scholar
  80. 80.
    Augustine D, Ayers LV, Lima E, Newton L, Lewandowski AJ, Davis EF, et al. Dynamic release and clearance of circulating microparticles during cardiac stress. Circ Res. 2014;114:109–13.CrossRefPubMedGoogle Scholar
  81. 81.
    Miller BJ, Pate RR, Burgess W. Foot impact force and intravascular hemolysis during distance running. Int J Sports Med. 1988;9:56–60.CrossRefPubMedGoogle Scholar
  82. 82.
    Telford RD, Sly GJ, Hahn AG, Cunningham RB, Bryant C, Smith JA. Footstrike is the major cause of hemolysis during running. J Appl Physiol. 2003;94:38–42.CrossRefPubMedGoogle Scholar
  83. 83.
    Ahmadizad S, El-sayed MS, MacLaren DP. Effects of time of day and acute resistance exercise on platelet activation and function. Clin Hemorheol Microcirc. 2010;45:391–9.PubMedGoogle Scholar
  84. 84.
    Ahmadizad S, El-sayed MS. The Effects of graded resistance exercise on platelet aggregation and activation. Med Sci Sport Exerc. 2003;35:1026–32.CrossRefGoogle Scholar
  85. 85.
    Kim HK, Song KS, Lee ES, Lee YJ, Park YS, Lee KR, et al. Optimized flow cytometric assay for the measurement of platelet microparticles in plasma: pre-analytic and analytic considerations. Blood Coagul Fibrinolysis. 2002;13:393–7.CrossRefPubMedGoogle Scholar
  86. 86.
    Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee I-M, et al. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc. 2011;43:1334–59.CrossRefPubMedGoogle Scholar
  87. 87.
    El-Sayed MS, Sale C, Jones PG, Chester M. Blood hemostasis in exercise and training. Med Sci Sports Exerc. 2000;32:918–25.CrossRefPubMedGoogle Scholar
  88. 88.
    Ziche M, Morbidelli L, Choudhuri R, Zhang HT, Donnini S, Granger HJ, et al. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest. 1997;99:2625–34.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Fukumura D, Gohongi T, Kadambi A, Izumi Y, Ang J, Yun C-O, et al. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci. 2001;98:2604–9.CrossRefPubMedGoogle Scholar
  90. 90.
    Whitham M, Parker BL, Friedrichsen M, Hingst JR, Hjorth M, Hughes WE, et al. Extracellular vesicles provide a means for tissue crosstalk during exercise. Cell Metab. Elsevier; 2018;27:237–251.e4.Google Scholar
  91. 91.
    Babbitt DM, Diaz KM, Feairheller DL, Sturgeon KM, Perkins AM, Veerabhadrappa P, et al. Endothelial activation microparticles and inflammation status improve with exercise training in african Americans. Int J Hypertens. 2013;2013:1–8.CrossRefGoogle Scholar
  92. 92.
    Feairheller DL, Diaz KM, Kashem MA, Thakkar SR, Veerabhadrappa P, Sturgeon KM, et al. Effects of moderate aerobic exercise training on vascular health and blood pressure in African Americans. J Clin Hypertens. 2014;16:504–10.Google Scholar
  93. 93.
    Duck MM, Hoffman RP. Impaired endothelial function in healthy African-American adolescents compared with Caucasians. J Pediatr. 2007;150:400–6.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, et al. Heart disease and stroke statistics—2016 update. Circulation. 2016;133:e38–360.CrossRefPubMedGoogle Scholar
  95. 95.
    Heffernan KS, Jae SY, Wilund KR, Woods JA, Fernhall B. Racial differences in central blood pressure and vascular function in young men. Am J Physiol Heart Circ Physiol. 2008;61820:2380–7.Google Scholar
  96. 96.
    Puurunen MK, Hwang S, Larson MG, Vasan RS, O’Donnell CJ, Tofler G, et al. ADP platelet hyperreactivity predicts cardiovascular disease in the FHS (Framingham Heart Study). J Am Heart Assoc. 2018;7:e008522.CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Thaulow E, Erikssen J, Sandvik L, Stormorken H, Cohn PF. Blood platelet count and function are related to total and cardiovascular death in apparently healthy men. Circulation. 1991;84:613–7.CrossRefPubMedGoogle Scholar
  98. 98.
    Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, Biancone L, et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood. 2007;110:2440–8.CrossRefPubMedGoogle Scholar
  99. 99.
    Diehl P, Fricke A, Sander L, Stamm J, Bassler N, Htun N, et al. Microparticles: major transport vehicles for distinct microRNAs in circulation. Cardiovasc Res. 2012;93:633–44.CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Baggish AL, Hale A, Weiner RB, Lewis GD, Systrom D, Wang F, et al. Dynamic regulation of circulating microRNA during acute exhaustive exercise and sustained aerobic exercise training. J Physiol. 2011;589:3983–94.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    De Pauw K, Roelands B, Cheung SS, de Geus B, Rietjens G, Meeusen R. Guidelines to classify subject groups in sport-science research. Int J Sports Physiol Perform. 2013;8:111–22.CrossRefGoogle Scholar
  102. 102.
    Decroix L, De Pauw K, Foster C, Meeusen R. Guidelines to classify female subject groups in sport-science research. Int J Sports Physiol Perform. 2016;11:204–13.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Physical EducationUFPelPelotasBrazil
  2. 2.EA3920 Prognostic Factors and Regulatory Factors of Cardiac and Vascular Pathologies, (Exercise Performance Health Innovation-EPHI)University of Bourgogne Franche-ComtéBesançonFrance
  3. 3.Tomsk Polytechnic UniversityTomskRussia
  4. 4.Department of Biological Sciences, Faculty of ScienceThompson Rivers UniversityKamloopsCanada

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