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Int J Sports Med 2021; 42(12): 1047-1057
DOI: 10.1055/a-1273-8390
Review

Effects of Exercise Training on the Paracrine Function of Circulating Angiogenic Cells

William S. Evans
1   Department of Kinesiology, University of Maryland School of Public Health, College Park
,
Ryan M. Sapp
1   Department of Kinesiology, University of Maryland School of Public Health, College Park
,
Katherine I. Kim
1   Department of Kinesiology, University of Maryland School of Public Health, College Park
,
James M. Heilman
1   Department of Kinesiology, University of Maryland School of Public Health, College Park
,
James Hagberg
1   Department of Kinesiology, University of Maryland School of Public Health, College Park
,
Steven J. Prior
1   Department of Kinesiology, University of Maryland School of Public Health, College Park
2   Baltimore Veterans Affairs Geriatric Research, Education and Clinical Center, Department of Veterans Affairs, Baltimore
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Abstract

Exercise training has various benefits on cardiovascular health, and circulating angiogenic cells have been proposed as executing these changes. Work from the late 1990s supported an important role of these circulating post-natal cells in contributing to the maintenance and repair of the endothelium and vasculature. It was later found that circulating angiogenic cells were a heterogenous population of cells and primarily functioned in a paracrine manner by adhering to damaged endothelium and releasing growth factors. Many studies have discovered novel circulating angiogenic cell secreted proteins, microRNA and extracellular vesicles that mediate their angiogenic potential, and some studies have shown that both acute and chronic aerobic exercise training have distinct benefits. This review highlights work establishing an essential role of secreted factors from circulating angiogenic cells and summarizes studies regarding the effects of exercise training on these factors. Finally, we highlight the various gaps in the literature in hopes of guiding future work.

Key words

microRNA - angiogenesis - extracellular vesicle - cytokine


Publication History

Received: 02 June 2020

Accepted: 15 September 2020

Article published online:
29 October 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

Letter to this article:

Letter to the Editor on: “Effects of Exercise Training on the Paracrine Function of Circulating Angiogenic Cells.”Int J Sports Med 2021; 42(12): 1137-1138
DOI: 10.1055/a-1527-5012

Letter to this article:

Re: Letter to the Editor on: “Effects of Exercise Training on the Paracrine Function of Circulating Angiogenic Cells.”Int J Sports Med 2021; 42(12): 1139-1139
DOI: 10.1055/a-1527-5024

 

  • References

  • 1 Sietsema WK, Kawamoto A, Takagi H. et al. Autologous CD34+ cell therapy for ischemic tissue repair. Circ J 2019; 83: 1422-1430
    CrossrefPubMedGoogle Scholar
  • 2 Kinnaird T, Stabile E, Burnett MS. et al. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 2004; 94: 678-685
    CrossrefPubMedGoogle Scholar
  • 3 Di Santo S, Yang Z, Wyler von Ballmoos M. et al. Novel cell-free strategy for therapeutic angiogenesis: In vitro generated conditioned medium can replace progenitor cell transplantation. PLoS One 2009; 4: e5643
    CrossrefPubMedGoogle Scholar
  • 4 Zafar N, Krishnasamy SS, Shah J. et al. Circulating angiogenic stem cells in type 2 diabetes are associated with glycemic control and endothelial dysfunction. PLoS One 2018; 13: e0205851
    CrossrefPubMedGoogle Scholar
  • 5 Vasa M, Fichtlscherer S, Aicher A. et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 2001; 89: E1-E7
    CrossrefPubMedGoogle Scholar
  • 6 Cavalcante SL, Lopes S, Bohn L. et al. Effects of exercise on endothelial progenitor cells in patients with cardiovascular disease: A systematic review and meta-analysis of randomized controlled trials. Rev Port Cardiol 2019; 38: 817-827
    CrossrefPubMedGoogle Scholar
  • 7 Rehman J, Li J, Orschell CM. et al. Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 2003; 107: 1164-1169
    CrossrefPubMedGoogle Scholar
  • 8 Rohde E, Malischnik C, Thaler D. et al. Blood monocytes mimic endothelial progenitor cells. Stem Cells 2006; 24: 357-367
    CrossrefPubMedGoogle Scholar
  • 9 Hur J, Yang H-M, Yoon C-H. et al. Identification of a novel role of T cells in postnatal vasculogenesis. Circulation 2007; 116: 1671-1682
    CrossrefPubMedGoogle Scholar
  • 10 Iwase T, Nagaya N, Fujii T. et al. Comparison of angiogenic potency between mesenchymal stem cells and mononuclear cells in a rat model of hindlimb ischemia. Cardiovasc Res 2005; 66: 543-551
    CrossrefPubMedGoogle Scholar
  • 11 Fadini GP, Losordo D, Dimmeler S. Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 2012; 110: 624-637
    CrossrefPubMedGoogle Scholar
  • 12 Hill JM, Zalos G, Halcox JP. et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 2003; 348: 593-600
    CrossrefPubMedGoogle Scholar
  • 13 Asahara T, Murohara T, Sullivan A. et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275: 964-967
    CrossrefPubMedGoogle Scholar
  • 14 Bielak LF, Horenstein RB, Ryan KA. et al. Circulating CD34+ cell count is associated with extent of subclinical atherosclerosis in asymptomatic amish men, independent of 10-year framingham risk. Clin Med Cardiol 2009; 3: 53-60
    CrossrefPubMedGoogle Scholar
  • 15 Kim S-W, Kim H, Cho H-J. et al. Human peripheral blood-derived CD31+ cells have robust angiogenic and vasculogenic properties and are effective for treating ischemic vascular disease. J Am Coll Cardiol 2010; 56: 593-607
    CrossrefPubMedGoogle Scholar
  • 16 Kim S-W, Kim H, Yoon Y-s. Advances in bone marrow-derived cell therapy: CD31-expressing cells as next generation cardiovascular cell therapy. Regen Med 2011; 6: 335-349
    CrossrefPubMedGoogle Scholar
  • 17 Erdbruegger U, Dhaygude A, Haubitz M. et al. Circulating endothelial cells: markers and mediators of vascular damage. Curr Stem Cell Res Ther 2010; 5: 294-302
    CrossrefPubMedGoogle Scholar
  • 18 Goon PKY, Boos CJ, Stonelake PS. et al. Detection and quantification of mature circulating endothelial cells using flow cytometry and immunomagnetic beads: A methodological comparison. Thromb Haemost 2006; 96: 45-52
    Article in Thieme ConnectPubMedGoogle Scholar
  • 19 Kushner EJ, MacEneaney OJ, Morgan RG. et al. CD31+ T cells represent a functionally distinct vascular T cell phenotype. Blood Cells Mol Dis 2010; 44: 74-78
    CrossrefPubMedGoogle Scholar
  • 20 Hur J, Yang HM, Yoon CH. et al. Identification of a novel role of T cells in postnatal vasculogenesis: characterization of endothelial progenitor cell colonies. Circulation 2007; 116: 1671-1682
    CrossrefPubMedGoogle Scholar
  • 21 Kim S-J, Kim J-S, Papadopoulos J. et al. Circulating monocytes expressing CD31: Implications for acute and chronic angiogenesis. Am J Pathol 2009; 174: 1972-1980
    CrossrefPubMedGoogle Scholar
  • 22 Waller E, Olweus J, Lund-Johansen F. et al. The “common stem cell” hypothesis reevaluated: human fetal bone marrow contains separate populations of hematopoietic and stromal progenitors. Blood 1995; 85: 2422-2435
    CrossrefPubMedGoogle Scholar
  • 23 Landers-Ramos RQ, Sapp RM, Shill DD. et al. Exercise and cardiovascular progenitor cells. Compr Physiol 2019; 9: 767-797
    CrossrefPubMedGoogle Scholar
  • 24 Khan SS, Solomon MA, McCoy JP. Detection of circulating endothelial cells and endothelial progenitor cells by flow cytometry. Cytometry B Clin Cytom. 2006; 70: 104-105
    PubMedGoogle Scholar
  • 25 Lertkiatmongkol P, Liao D, Mei H. et al. Endothelial functions of platelet/endothelial cell adhesion molecule-1 (CD31). Curr Opin Hematol 2016; 23: 253-259
    CrossrefPubMedGoogle Scholar
  • 26 Ziegelhoeffer T, Fernandez B, Kostin S. et al. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res 2004; 94: 230-238
    CrossrefPubMedGoogle Scholar
  • 27 Gnecchi M, Zhang Z, Ni A. et al. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008; 103: 1204-1219
    CrossrefPubMedGoogle Scholar
  • 28 Yang Z, von Ballmoos MW, Faessler D. et al. Paracrine factors secreted by endothelial progenitor cells prevent oxidative stress-induced apoptosis of mature endothelial cells. Atherosclerosis 2010; 211: 103-109
    CrossrefPubMedGoogle Scholar
  • 29 Xu S, Zhu J, Yu L. et al. Endothelial progenitor cells: Current development of their paracrine factors in cardiovascular therapy. J Cardiovasc Pharmacol 2012; 59: 387-396
    CrossrefPubMedGoogle Scholar
  • 30 Bollini S, Gentili C, Tasso R. et al. The Regenerative role of the fetal and adult stem cell secretome. J Clin Med 2013; 2: 302-327
    CrossrefPubMedGoogle Scholar
  • 31 Kamihata H, Matsubara H, Nishiue T. et al. Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation 2001; 104: 1046-1052
    CrossrefPubMedGoogle Scholar
  • 32 Urbich C, Aicher A, Heeschen C. et al. Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J Mol Cell Cardiol 2005; 39: 733-742
    CrossrefPubMedGoogle Scholar
  • 33 Asahara T, Masuda H, Takahashi T. et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999; 85: 221-228
    CrossrefPubMedGoogle Scholar
  • 34 Akita T, Murohara T, Ikeda H. et al. Hypoxic preconditioning augments efficacy of human endothelial progenitor cells for therapeutic neovascularization. Lab Invest 2003; 83: 65-73
    CrossrefPubMedGoogle Scholar
  • 35 Medina RJ, O’Neill CL, O’Doherty TM. et al. Myeloid angiogenic cells act as alternative M2 macrophages and modulate angiogenesis through interleukin-8. Mol Med 2011; 17: 1045-1055
    CrossrefPubMedGoogle Scholar
  • 36 Medina RJ, O’Neill CL, Sweeney M. et al. Molecular analysis of endothelial progenitor cell (EPC) subtypes reveals two distinct cell populations with different identities. BMC Med Genomics 2010; 3: 18
    CrossrefPubMedGoogle Scholar
  • 37 Zemani F, Silvestre JS, Fauvel-Lafeve F. et al. Ex vivo priming of endothelial progenitor cells with SDF-1 before transplantation could increase their proangiogenic potential. Arterioscler Thromb Vasc Biol 2008; 28: 644-650
    CrossrefPubMedGoogle Scholar
  • 38 Odent Grigorescu G, Rosca AM, Preda MB. et al. Synergic effects of VEGF-A and SDF-1 on the angiogenic properties of endothelial progenitor cells. J Tissue Eng Regen Med 2017; 11: 3241-3252
    CrossrefPubMedGoogle Scholar
  • 39 Yin Y, Huang L, Zhao X. et al. AMD3100 mobilizes endothelial progenitor cells in mice, but inhibits its biological functions by blocking an autocrine/paracrine regulatory loop of stromal cell derived factor-1 in vitro. J Cardiovasc Pharmacol 2007; 50: 61-67
    CrossrefPubMedGoogle Scholar
  • 40 Grunewald M, Avraham I, Dor Y. et al. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 2006; 124: 175-189
    CrossrefPubMedGoogle Scholar
  • 41 Pula G, Mayr U, Evans C. et al. Proteomics identifies thymidine phosphorylase as a key regulator of the angiogenic potential of colony-forming units and endothelial progenitor cell cultures. Circ Res 2009; 104: 32-40
    CrossrefPubMedGoogle Scholar
  • 42 Urbich C, De Souza AI, Rossig L. et al. Proteomic characterization of human early pro-angiogenic cells. J Mol Cell Cardiol 2011; 50: 333-336
    CrossrefPubMedGoogle Scholar
  • 43 Felice F, Piras AM, Rocchiccioli S. et al. Endothelial progenitor cell secretome delivered by novel polymeric nanoparticles in ischemic hindlimb. Int J Pharm 2018; 542: 82-89
    CrossrefPubMedGoogle Scholar
  • 44 Wara AK, Foo S, Croce K. et al. TGF-beta1 signaling and Kruppel-like factor 10 regulate bone marrow-derived proangiogenic cell differentiation, function, and neovascularization. Blood 2011; 118: 6450-6460
    CrossrefPubMedGoogle Scholar
  • 45 Tan Q, Zhang S, Qi X. et al. Permanent atrial fibrillation impairs the function of circulating endothelial progenitor cells. Postgrad Med 2017; 129: 198-204
    CrossrefPubMedGoogle Scholar
  • 46 Teraa M, Sprengers RW, Westerweel PE. et al. Bone marrow alterations and lower endothelial progenitor cell numbers in critical limb ischemia patients. PLoS One 2013; 8: e55592
    CrossrefPubMedGoogle Scholar
  • 47 Heida N-M, Müller J-P, Cheng IF. et al. Effects of obesity and weight loss on the functional properties of early outgrowth endothelial progenitor cells. J Am Coll Cardiol 2010; 55: 357-367
    CrossrefPubMedGoogle Scholar
  • 48 Jarajapu YPR, Hazra S, Segal M. et al. Vasoreparative dysfunction of CD34+ cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms. PLoS One 2014; 9: e93965
    CrossrefPubMedGoogle Scholar
  • 49 Kanzler I, Tuchscheerer N, Steffens G. et al. Differential roles of angiogenic chemokines in endothelial progenitor cell-induced angiogenesis. Basic Res Cardiol 2013; 108: 310
    CrossrefPubMedGoogle Scholar
  • 50 Wu Y, Li L, Chen W. et al. Maintaining Moderate platelet aggregation and improving metabolism of endothelial progenitor cells increase the patency rate of tissue-engineered blood vessels. Tissue Eng Part A 2015; 21: 2001-2012
    CrossrefPubMedGoogle Scholar
  • 51 Han J-K, Kim H-L, Jeon K-H. et al. Peroxisome proliferator-activated receptor-δ activates endothelial progenitor cells to induce angio-myogenesis through matrix metallo-proteinase-9-mediated insulin-like growth factor-1 paracrine networks. Eur Heart J 2011; 34: 1755-1765
    CrossrefPubMedGoogle Scholar
  • 52 Leifheit-Nestler M, Conrad G, Heida NM. et al. Overexpression of integrin beta 5 enhances the paracrine properties of circulating angiogenic cells via Src kinase-mediated activation of STAT3. Arterioscler Thromb Vasc Biol 2010; 30: 1398-1406
    CrossrefPubMedGoogle Scholar
  • 53 Wara AK, Manica A, Marchini JF. et al. Bone marrow-derived Kruppel-like factor 10 controls reendothelialization in response to arterial injury. Arterioscler Thromb Vasc Biol 2013; 33: 1552-1560
    CrossrefPubMedGoogle Scholar
  • 54 Scheubel RJ, Holtz J, Friedrich I. et al. Paracrine effects of CD34 progenitor cells on angiogenic endothelial sprouting. Int J Cardiol 2010; 139: 134-141
    CrossrefPubMedGoogle Scholar
  • 55 Burlacu A, Grigorescu G, Rosca AM. et al. Factors secreted by mesenchymal stem cells and endothelial progenitor cells have complementary effects on angiogenesis in vitro. Stem Cells Dev 2013; 22: 643-653
    CrossrefPubMedGoogle Scholar
  • 56 Krenning G, van der Strate BWA, Schipper M. et al. Combined implantation of CD34+ and CD14+ cells increases neovascularization through amplified paracrine signalling. J Tissue Eng Regen Med 2013; 7: 118-128
    CrossrefPubMedGoogle Scholar
  • 57 Jackson RJ, Standart N how do micrornas regulate gene expression? Sci STKE 2007; 2007: re1
    PubMed
  • 58 Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009; 136: 642-655
    CrossrefPubMedGoogle Scholar
  • 59 Fabian MR, Sonenberg N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 2012; 19: 586-593
    CrossrefPubMedGoogle Scholar
  • 60 Chistiakov DA, Orekhov AN, Bobryshev YV. The role of miR-126 in embryonic angiogenesis, adult vascular homeostasis, and vascular repair and its alterations in atherosclerotic disease. J Mol Cell Cardiol 2016; 97: 47-55
    CrossrefPubMedGoogle Scholar
  • 61 Fish JE, Santoro MM, Morton SU. et al. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 2008; 15: 272-284
    CrossrefPubMedGoogle Scholar
  • 62 Shan C, Ma Y. MicroRNA-126/stromal cell-derived factor 1/C-X-C chemokine receptor type 7 signaling pathway promotes post-stroke angiogenesis of endothelial progenitor cell transplantation. Mol Med Rep 2018; 17: 5300-5305
    PubMedGoogle Scholar
  • 63 Zhang J, Zhang Z, Zhang DY. et al. microRNA 126 inhibits the transition of endothelial progenitor cells to mesenchymal cells via the PIK3R2-PI3K/Akt signalling pathway. PLoS One 2013; 8: e83294
    CrossrefPubMedGoogle Scholar
  • 64 Pan Q, Zheng J, Du D. et al. MicroRNA-126 priming enhances functions of endothelial progenitor cells under physiological and hypoxic conditions and their therapeutic efficacy in cerebral ischemic damage. Stem Cells Int 2018; 2018: 2912347
    PubMedGoogle Scholar
  • 65 Li Y, Zhou Q, Pei C. et al. Hyperglycemia and advanced glycation end products regulate miR-126 expression in endothelial progenitor cells. J Vascular Res 2016; 53: 94-104
    CrossrefPubMedGoogle Scholar
  • 66 Jakob P, Doerries C, Briand S. et al. Loss of AngiomiR-126 and 130a in angiogenic early outgrowth cells from patients with chronic heart failure. Circulation 2012; 126: 2962-2975
    CrossrefPubMedGoogle Scholar
  • 67 Meng S, Cao J, Zhang X. et al. Downregulation of microRNA-130a contributes to endothelial progenitor cell dysfunction in diabetic patients via its target Runx3. PLoS One 2013; 8: e68611
    CrossrefPubMedGoogle Scholar
  • 68 Weber M, Baker MB, Moore JP. et al. MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem Biophys Res Commun 2010; 393: 643-648
    CrossrefPubMedGoogle Scholar
  • 69 Zuo K, Li M, Zhang X. et al. MiR-21 suppresses endothelial progenitor cell proliferation by activating the TGFβ signaling pathway via downregulation of WWP1. Int J Clin Exp Pathol 2015; 8: 414-422
    PubMedGoogle Scholar
  • 70 Fleissner F, Jazbutyte V, Fiedler J. et al. Short communication: asymmetric dimethylarginine impairs angiogenic progenitor cell function in patients with coronary artery disease through a microRNA-21-dependent mechanism. Circ Res 2010; 107: 138-143
    CrossrefPubMedGoogle Scholar
  • 71 Thum T, Tsikas D, Stein S. et al. Suppression of endothelial progenitor cells in human coronary artery disease by the endogenous nitric oxide synthase inhibitor asymmetric dimethylarginine. J Am Coll Cardiol 2005; 46: 1693-1701
    CrossrefPubMedGoogle Scholar
  • 72 Zhang HW, Li H, Yan H. et al. MicroRNA-142 promotes the expression of eNOS in human peripheral blood-derived endothelial progenitor cells in vitro. Eur Rev Med Pharmacol Sci 2016; 20: 4167-4175
    PubMedGoogle Scholar
  • 73 Spinetti G, Fortunato O, Caporali A. et al. MicroRNA-15a and MicroRNA-16 impair human circulating proangiogenic cell functions and are increased in the proangiogenic cells and serum of patients with critical limb ischemia. Circ Res 2013; 112: 335-346
    CrossrefPubMedGoogle Scholar
  • 74 Goretti E, Rolland-Turner M, Leonard F. et al. MicroRNA-16 affects key functions of human endothelial progenitor cells. J Leukoc Biol 2013; 93: 645-655
    CrossrefPubMedGoogle Scholar
  • 75 Wang H-W, Lo H-H, Chiu Y-L. et al. Dysregulated miR-361-5p/VEGF axis in the plasma and endothelial progenitor cells of patients with coronary artery disease. Puc L One 2014; 9: e98070
    PubMedGoogle Scholar
  • 76 Olivieri F, Lazzarini R, Recchioni R. et al. MiR-146a as marker of senescence-associated pro-inflammatory status in cells involved in vascular remodelling. Age (Dordr) 2013; 35: 1157-1172
    CrossrefPubMedGoogle Scholar
  • 77 Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9: 581-593
    CrossrefPubMedGoogle Scholar
  • 78 Gould SJ, Raposo G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. J Extracell Vesicles 2013; 2: 20389
    CrossrefPubMedGoogle Scholar
  • 79 van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 2018; 19: 213-228
    CrossrefPubMedGoogle Scholar
  • 80 Deregibus MC, Cantaluppi V, Calogero R. et al. Endothelial progenitor cell–derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007; 110: 2440-2448
    CrossrefPubMedGoogle Scholar
  • 81 Mathiyalagan P, Liang Y, Kim D. et al. Angiogenic mechanisms of human CD34(+) stem cell exosomes in the repair of ischemic hindlimb. Circ Res 2017; 120: 1466-1476
    CrossrefPubMedGoogle Scholar
  • 82 Sahoo S, Klychko E, Thorne T. et al. Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circ Res 2011; 109: 724-728
    CrossrefPubMedGoogle Scholar
  • 83 Hristov M, Erl W, Linder S. et al. Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood 2004; 104: 2761-2766
    CrossrefPubMedGoogle Scholar
  • 84 Zernecke A, Bidzhekov K, Noels H. et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2009; 2: ra81
    CrossrefPubMedGoogle Scholar
  • 85 Wu K, Yang Y, Zhong Y. et al. The effects of microvesicles on endothelial progenitor cells are compromised in type 2 diabetic patients via downregulation of the miR-126/VEGFR2 pathway. Am J Physiol Endocrinol Metab 2016; 310: E828-E837
    CrossrefPubMedGoogle Scholar
  • 86 Yue Y, Garikipati VNS, Verma SK. et al. Interleukin-10 deficiency impairs reparative properties of bone marrow-derived endothelial progenitor cell exosomes. Tissue Eng Part A 2017; 23: 1241-1250
    CrossrefPubMedGoogle Scholar
  • 87 Landers-Ramos RQ, Sapp RM, VandeWater E. et al. Investigating the extremes of the continuum of paracrine functions in CD34-/CD31+ CACs across diverse populations. Am J Physiol Heart Circ Physiol 2017; 312: H162-H172
    CrossrefPubMedGoogle Scholar
  • 88 Landers-Ramos RQ, Sapp RM, Jenkins NT. et al. Chronic endurance exercise affects paracrine action of CD31+ and CD34+ cells on endothelial tube formation. Am J Physiol Heart Circ Physiol 2015; 309: H407-H420
    CrossrefPubMedGoogle Scholar
  • 89 Landers-Ramos RQ, Corrigan KJ, Guth LM. et al. Short-term exercise training improves flow-mediated dilation and circulating angiogenic cell number in older sedentary adults. Appl Physiol Nutr Metab 2016; 41: 832-841
    CrossrefPubMedGoogle Scholar
  • 90 Wang S, Song R, Wang Z. et al. S100A8/A9 in Inflammation. Front Immunol 2018; 9: 1298
    CrossrefPubMedGoogle Scholar
  • 91 Minami Y, Satoh M, Maesawa C. et al. Effect of atorvastatin on microRNA 221/222 expression in endothelial progenitor cells obtained from patients with coronary artery disease. Eur J Clin Invest 2009; 39: 359-367
    CrossrefPubMedGoogle Scholar
  • 92 Radom-Aizik S, Zaldivar F, Leu SY. et al. Effects of exercise on microRNA expression in young males peripheral blood mononuclear cells. Clin Transl Sci 2012; 5: 32-38
    CrossrefPubMedGoogle Scholar
  • 93 Guo Y, Luo F, Zhang X. et al. TPPU enhanced exercise-induced epoxyeicosatrienoic acid concentrations to exert cardioprotection in mice after myocardial infarction. J Cell Mol Med 2018; 22: 1489-1500
    CrossrefPubMedGoogle Scholar
  • 94 Ma C, Wang J, Liu H. et al. Moderate exercise enhances endothelial progenitor cell exosomes release and function. Med Sci Sports Exerc 2018; 50: 2024-2032
    CrossrefPubMedGoogle Scholar
  • 95 Wang J, Liu H, Chen S. et al. Moderate exercise has beneficial effects on mouse ischemic stroke by enhancing the functions of circulating endothelial progenitor cell-derived exosomes. Exp Neurol 2020; 330: 113325
    CrossrefPubMedGoogle Scholar
  • 96 Cirilli I, Silvestri S, Marcheggiani F. et al. Three Months monitored metabolic fitness modulates cardiovascular risk factors in diabetic patients. Diabetes Metab J 2019; 43: 893-897
    CrossrefPubMedGoogle Scholar
  • 97 Sapp RM, Shill DD, Roth SM. et al. Circulating microRNAs in acute and chronic exercise: more than mere biomarkers. J Appl Physiol (1985) 2016: 702-717
    PubMedGoogle Scholar
  • 98 Lansford KA, Shill DD, Dicks AB. et al. Effect of acute exercise on circulating angiogenic cell and microparticle populations. Exp Physiol 2016; 101: 155-167
    CrossrefPubMedGoogle Scholar
  • 99 Chaar V, Romana M, Tripette J. et al. Effect of strenuous physical exercise on circulating cell-derived microparticles. Clin Hemorheol Microcirc 2011; 47: 15-25
    CrossrefPubMedGoogle Scholar
  • 100 Sossdorf M, Otto GP, Claus RA. et al. Cell-derived microparticles promote coagulation after moderate exercise. Med Sci Sports Exerc 2011; 43: 1169-1176
    CrossrefPubMedGoogle Scholar
  • 101 Harriss DJ, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817
    Article in Thieme ConnectPubMedGoogle Scholar
  • 102 Zhu S, Deng S, Ma Q. et al. MicroRNA-10A* and MicroRNA-21 modulate endothelial progenitor cell senescence via suppressing high-mobility group A2. Circ Res 2013; 112: 152-164
    CrossrefPubMedGoogle Scholar