Skip to main content

Advertisement

SpringerLink
Log in

Endothelial progenitor cells as the target for cardiovascular disease prediction, personalized prevention, and treatments: progressing beyond the state-of-the-art

  • Minireview
  • Published:
EPMA Journal Aims and scope Submit manuscript

Abstract

Stimulated by the leading mortalities of cardiovascular diseases (CVDs), various types of cardiovascular biomaterials have been widely investigated in the past few decades. Although great therapeutic effects can be achieved by bare metal stents (BMS) and drug-eluting stents (DES) within months or years, the long-term complications such as late thrombosis and restenosis have limited their further applications. It is well accepted that rapid endothelialization is a promising approach to eliminate these complications. Convincing evidence has shown that endothelial progenitor cells (EPCs) could be mobilized into the damaged vascular sites systemically and achieve endothelial repair in situ, which significantly contributes to the re-endothelialization process. Therefore, how to effectively capture EPCs via specific molecules immobilized on biomaterials is an important point to achieve rapid endothelialization. Further, in the context of predictive, preventive, personalized medicine (PPPM), the abnormal number alteration of EPCs in circulating blood and certain inflammation responses can also serve as important indicators for predicting and preventing early cardiovascular disease. In this contribution, we mainly focused on the following sections: the definition and classification of EPCs, the mechanisms of EPCs in treating CVDs, the potential diagnostic role of EPCs in predicting CVDs, as well as the main strategies for cardiovascular biomaterials to capture EPCs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

CVDs:

Cardiovascular diseases

BMS:

Bare metal stents

DES:

drug-eluting stents

EPCs:

Endothelial progenitor cells

PPPM:

Predictive, preventive and personalized medicine

SMCs:

Smooth muscle cells

ISR:

In-stent restenosis

ECS:

Endothelial progenitor cell capturing stent

ECs:

Endothelial cells

CEPCs:

Circulating endothelial progenitor cells

NO:

Nitric oxide

eEPCs:

Early endothelial progenitor cells

lEPCs:

Late endothelial progenitor cells

OECs:

Outgrowth endothelial cells

KDR:

Kinase insert domain receptor

CXCR-1:

Chemokine receptor 1

MMPs:

Matrix metalloproteinase

VEGF:

Vascular endothelial growth factor

cGMP:

Cyclic guanylate monophosphate

Dopa:

Dopamine

SeCA:

Selenocystamine

ECM:

Extracellular matrix

VEGF-R2:

Vascular endothelial growth factor receptor 2

PGI2 :

Prostaglandin I2

PAD:

Peripheral arterial disease

CAD:

Coronary artery disease

GM-CSF:

Granulocyte-macrophage colony-stimulating factor

VE-cadherin+ :

Vascular endothelial-cadherin+

CFU-ECs:

Endothelial cell colony-forming units

CECs:

Circulating endothelial cells

lECs:

Inflammatory endothelial cells

REDV:

Arg-Glu-Asp-Val

PEG:

Polyethylene glycol

vWF:

Von Willebrand factor

SELEX:

Systematic evolution of ligands by exponential enrichment

PPAam:

Plasma polymerized allylamine

RGD:

Arg-Gly-Asp

cRGD:

Cyclic Arg-Gly-Asp

PCL:

Polycaprolactone

PLLA:

Poly (L-lactic acid)

ECFCs:

Endothelial colony forming cells

TPS:

TPSLEQRTVYAK

HCP-1:

Hemocompatible peptide-1

EMF:

External magnetic field

SPION:

Superparamagnetic iron oxide nanoparticles

CA:

Citric acid

References

  1. Piepoli MF, Hoes AW, Agewall S, Albus C, Brotons C, Catapano AL, et al. 2016 European guidelines on cardiovascular disease prevention in clinical practice: The sixth joint task force of the european society of cardiology and other societies on cardiovascular disease prevention in clinical practice (constituted by representatives of 10 societies and by invited experts) developed with the special contribution of the European Association for Cardiovascular Prevention & Rehabilitation (EACPR). Atherosclerosis. 2016;252:207–74. https://doi.org/10.1016/j.atherosclerosis.2016.05.037.

    Article  CAS  PubMed  Google Scholar 

  2. Liu J, Zheng B, Wang P, Wang X, Zhang B, Shi Q, et al. Enhanced in vitro and in vivo performance of Mg-Zn-Y-Nd alloy achieved with APTES pretreatment for drug-eluting vascular stent application. ACS Appl Mater Interfaces. 2016;8(28):17842–58. https://doi.org/10.1021/acsami.6b05038.

    Article  CAS  PubMed  Google Scholar 

  3. Borhani S, Hassanajili S, Ahmadi Tafti SH, Rabbani S. Cardiovascular stents: overview, evolution, and next generation. Prog Biomater. 2018;7(3):175–205. https://doi.org/10.1007/s40204-018-0097-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Fuster V. Top 10 cardiovascular therapies and interventions for the next decade. Nat Rev Cardiol. 2014;11(11):671–83. https://doi.org/10.1038/nrcardio.2014.137.

    Article  PubMed  Google Scholar 

  5. Cyrus T, Wickline SA, Lanza GM. Nanotechnology in interventional cardiology. Wiley Interdiscip Rev-Nanomed Nanobiotechnol. 2012;4(1):82–95. https://doi.org/10.1002/wnan.154.

    Article  CAS  PubMed  Google Scholar 

  6. Fischell TA. Editorial: the “JET” technique for provisional side-branch stenting back to the future, and in the right direction. J Interv Cardiol. 2017;30(6):535–6. https://doi.org/10.1111/joic.12453.

    Article  PubMed  Google Scholar 

  7. Wawrzynska M, Duda M, Wysokinska E, Strzadala L, Bialy D, Ulatowska-Jarza A, et al. Functionalized CD133 antibody coated stent surface simultaneously promotes EPCs adhesion and inhibits smooth muscle cell proliferation-a novel approach to prevent in-stent restenosis. Colloids Surf, B. 2019;174:587–97. https://doi.org/10.1016/j.colsurfb.2018.11.061.

    Article  CAS  Google Scholar 

  8. Daemen J, Wenaweser P, Tsuchida K, Abrecht L, Sophia V, Morger C, et al. Early and late coronary stent thrombosis of sirolimus-eluting and paclitaxel-eluting stents in routine clinical practice: data from a large two-institutional cohort study. Lancet. 2007;369(9562):667–78. https://doi.org/10.1016/s0140-6736(07)60314-6.

    Article  CAS  PubMed  Google Scholar 

  9. Finn AV, Joner M, Nakazawa G, Kolodgie F, Newell J, John MC, et al. Pathological correlates of late drug-eluting stent thrombosis - strut coverage as a marker of endothelialization. Circulation. 2007;115(18):2435–41. https://doi.org/10.1161/circulationaha.107.693739.

    Article  PubMed  Google Scholar 

  10. Luscher TF, Steffel J, Eberli FR, Joner M, Nakazawa G, Tanner FC, et al. Drug-eluting stent and coronary thrombosis - biological mechanisms and clinical implications. Circulation. 2007;115(8):1051–8. https://doi.org/10.1161/Circulationaha.106.675934.

    Article  PubMed  Google Scholar 

  11. Veleva AN, Cooper SL, Patterson C. Selection and initial characterization of novel peptide ligands that bind specifically to human blood outgrowth endothelial cells. Biotechnol Bioeng. 2007;98(1):306–12. https://doi.org/10.1002/bit.21420.

    Article  CAS  PubMed  Google Scholar 

  12. Wang J, Chen Y, Liu T, Wang X, Liu Y, Wang Y, et al. Covalent co-immobilization of heparin/laminin complex that with different concentration ratio on titanium surface for selectively direction of platelets and vascular cells behavior. Appl Surf Sci. 2014;317:776–86. https://doi.org/10.1016/j.apsusc.2014.07.129.

    Article  CAS  Google Scholar 

  13. Woudstra P, De Winter RJ, Beijk MA. Next-generation DES: the COMBO dual therapy stent with genous endothelial progenitor capturing technology and an abluminal sirolimus matrix. Expert Rev Med Devices. 2014;11(2):121–35. https://doi.org/10.1586/17434440.2014.882046.

    Article  CAS  PubMed  Google Scholar 

  14. Golubnitschaja O, Baban B, Boniolo G, Wang W, Bubnov R, Kapalla M, et al. Medicine in the early twenty-first century: paradigm and anticipation - EPMA position paper 2016. EPMA J. 2016;7:23. https://doi.org/10.1186/s13167-016-0072-4.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Berger JS, Haskell L, Ting W, Lurie F, Chang S-C, Mueller LA, et al. Evaluation of machine learning methodology for the prediction of healthcare resource utilization and healthcare costs in patients with critical limb ischemia-is preventive and personalized approach on the horizon? EPMA J. 2020;11(1):53–64. https://doi.org/10.1007/s13167-019-00196-9.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Ferda J, Baxa J, Ferdova E, Kucera R, Topolcan O, Molacek J. Abdominal aortic aneurysm in prostate cancer patients: the “road map” from incidental detection to advanced predictive, preventive, and personalized approach utilizing common follow-up for both pathologies. EPMA J. 2019;10(4):415–23. https://doi.org/10.1007/s13167-019-00193-y.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Golubnitschaja O, Costigliola V, EPMA. General report & recommendations in predictive, preventive and personalised medicine 2012: white paper of the European Association for Predictive, Preventive and Personalised Medicine. EPMA J. 2012;3(1):14. https://doi.org/10.1186/1878-5085-3-14.

  18. Asahara T, Kawamoto A, Masuda H. Concise review: circulating endothelial progenitor cells for vascular medicine. Stem Cells. 2011;29(11):1650–5. https://doi.org/10.1002/stem.745.

    Article  CAS  PubMed  Google Scholar 

  19. Asahara T, Murohara T, Sullivan A, Silver M, Vanderzee R, Li T, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275(5302):964–7. https://doi.org/10.1126/science.275.5302.964.

    Article  CAS  PubMed  Google Scholar 

  20. Chong MSK, Ng WK, Chan JKY. Concise review: endothelial progenitor cells in regenerative medicine: applications and challenges. Stem Cells Transl Med. 2016;5(4):530–8. https://doi.org/10.5966/sctm.2015-0227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Patel J, Seppanen EJ, Rodero MP, Wong HY, Donovan P, Neufeld Z, et al. Functional definition of progenitors versus mature endothelial cells reveals key SoxF-dependent differentiation process. Circulation. 2017;135(8):786–805. https://doi.org/10.1161/circulationaha.116.024754.

    Article  CAS  PubMed  Google Scholar 

  22. Urbich C, Dimmeler S. Endothelial progenitor cells - characterization and role in vascular biology. Circ Res. 2004;95(4):343–53. https://doi.org/10.1161/01.Res.0000137877.89448.78.

    Article  CAS  PubMed  Google Scholar 

  23. Ravindranath RR, Romaschin A, Thompson M. In vitro and in vivo cell-capture strategies using cardiac stent technology - a review. Clin Biochem. 2016;49(1–2):186–91. https://doi.org/10.1016/j.clinbiochem.2015.09.012.

    Article  CAS  PubMed  Google Scholar 

  24. Doyle B, Caplice N. A new source of endothelial progenitor cells - vascular biology redefined? Trends Biotechnol. 2005;23(9):444–6. https://doi.org/10.1016/j.tibtech.2005.05.013.

    Article  CAS  PubMed  Google Scholar 

  25. Finney MR, Greco NJ, Haynesworth SE, Martin JM, Hedrick DP, Swan JZ, et al. Direct comparison of umbilical cord blood versus bone marrow-derived endothelial precursor cells in mediating neovascularization in response to vascular ischemia. Biol Blood Marrow Transplant. 2006;12(5):585–93. https://doi.org/10.1016/j.bbmt.2005.12.037.

    Article  PubMed  Google Scholar 

  26. Pacilli A, Pasquinelli G. Vascular wall resident progenitor cells a review. Exp Cell Res. 2009;315(6):901–14. https://doi.org/10.1016/j.yexcr.2008.12.018.

    Article  CAS  PubMed  Google Scholar 

  27. Wu H, Riha GM, Yang H, Li M, Yao Q, Chen C. Differentiation and proliferation of endothelial progenitor cells from canine peripheral blood mononuclear cells. J Surg Res. 2005;126(2):193–8. https://doi.org/10.1016/j.jss.2005.01.016.

    Article  CAS  PubMed  Google Scholar 

  28. Zammaretti P, Zisch AH. Adult ‘endothelial progenitor cells’ - renewing vasculature. Int J Biochem Cell Biol. 2005;37(3):493–503. https://doi.org/10.1016/j.biocel.2004.06.018.

    Article  CAS  PubMed  Google Scholar 

  29. Fu G, Yu Z, Chen Y, Chen Y, Tian F, Yang X. Direct adsorption of anti-CD34 antibodies on the nano-porous stent surface to enhance endothelialization. Acta Cardiol Sin. 2016;32(3):273–80. https://doi.org/10.6515/acs20150813a.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Hu Y, Davison F, Zhang Z, Xu Q. Endothelial replacement and angiogenesis in arteriosclerotic lesions of allografts are contributed by circulating progenitor cells. Circulation. 2003;108(25):3122–7. https://doi.org/10.1161/01.Cir.0000105722.96112.67.

    Article  PubMed  Google Scholar 

  31. Ingram DA, Mead LE, Moore DB, Woodard W, Fenoglio A, Yoder MC. Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood. 2005;105(7):2783–6. https://doi.org/10.1182/blood-2004-08-3057.

    Article  CAS  PubMed  Google Scholar 

  32. Medina RJ, Barber CL, Sabatier F, Dignat George F, Melero Martin JM, Khosrotehrani K, et al. Endothelial progenitors: a consensus statement on nomenclature. Stem Cells Transl Med. 2017;6(5):1316–20. https://doi.org/10.1002/sctm.16-0360.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Butruk-Raszeja BA, Dresler MS, Kuzminska A, Ciach T. Endothelialization of polyurethanes: surface silanization and immobilization of REDV peptide. Colloids Surf, B. 2016;144:335–43. https://doi.org/10.1016/j.colsurfb.2016.04.017.

    Article  CAS  Google Scholar 

  34. Chen H, Zhao Y, Xiong K, Li J, Chen J, Yang P, et al. Multifunctional coating based on EPC-specific peptide and phospholipid polymers for potential applications in cardiovascular implants fate. J Mater Chem. 2016;4(48):7870–81. https://doi.org/10.1039/c6tb01811d.

    Article  CAS  Google Scholar 

  35. Otsuka F, Finn AV, Yazdani SK, Nakano M, Kolodgie FD, Virmani R. The importance of the endothelium in atherothrombosis and coronary stenting. Nat Rev Cardiol. 2012;9(8):439–53. https://doi.org/10.1038/nrcardio.2012.64.

    Article  CAS  PubMed  Google Scholar 

  36. Zhang K, Liu T, Li J, Chen J, Wang J, Huang N. Surface modification of implanted cardiovascular metal stents: from antithrombosis and antirestenosis to endothelialization. J Biomed Mater Res A. 2014;102(2):588–609. https://doi.org/10.1002/jbm.a.34714.

    Article  CAS  PubMed  Google Scholar 

  37. Abebe W, Mozaffari M. Endothelial dysfunction in diabetes: potential application of circulating markers as advanced diagnostic and prognostic tools. EPMA J. 2010;1(1):32–45. https://doi.org/10.1007/s13167-010-0012-7.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med. 2005;353(10):999–1007. https://doi.org/10.1056/NEJMoa043814.

    Article  CAS  PubMed  Google Scholar 

  39. Poole-Warren LA, Schindhelm K, Graham AR, Slowiaczek PR, Noble KR. Performance of small diameter synthetic vascular prostheses with confluent autologous endothelial cell linings. J Biomed Mater Res. 1996;30(2):221–9. https://doi.org/10.1002/(sici)1097-4636(199602)30:2<221::Aid-jbm12>3.0.Co;2-p.

    Article  CAS  PubMed  Google Scholar 

  40. Liu Y, Munisso MC, Mahara A, Kambe Y, Yamaoka T. Anti-platelet adhesion and in situ capture of circulating endothelial progenitor cells on ePTFE surface modified with poly(2-methacryloyloxyethyl phosphorylcholine) (PMPC) and hemocompatible peptide 1 (HCP-1). Colloids Surf, B. 2020;193:111113. https://doi.org/10.1016/j.colsurfb.2020.111113.

    Article  CAS  Google Scholar 

  41. Li Q, Wang Z, Zhang S, Zheng W, Zhao Q, Zhang J, et al. Functionalization of the surface of electrospun poly (epsilon-caprolactone) mats using zwitterionic poly (carboxybetaine methacrylate) and cell-specific peptide for endothelial progenitor cells capture. Mater Sci Eng C-Mater Biol Appl. 2013;33(3):1646–53. https://doi.org/10.1016/j.msec.2012.12.074.

    Article  CAS  PubMed  Google Scholar 

  42. Patel J, Donovan P, Khosrotehrani K. Concise review: functional definition of endothelial progenitor cells: a molecular perspective. Stem Cells Transl Med. 2016;5(10):1302–6. https://doi.org/10.5966/sctm.2016-0066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Yang H-M, Hur J, Yoon C-H, Park K-W, Lee C-S, Kim J-Y, et al. A novel subset of T cells (angiogenic T cells) facilitates EPC differentiation and has clinical relevance. Am J Cardiol. 2007;100(8A):80L-L.

    Google Scholar 

  44. Rehman J, Li JL, Orschell CM, March KL. Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation. 2003;107(8):1164–9. https://doi.org/10.1161/01.Cir.0000058702.69484.A0.

    Article  PubMed  Google Scholar 

  45. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104(9):2752–60. https://doi.org/10.1182/blood-2004-04-1396.

    Article  CAS  PubMed  Google Scholar 

  46. Madonna R, De Caterina R. Circulating endothelial progenitor cells: Do they live up to their name? Vasc Pharmacol. 2015;67–69:2–5. https://doi.org/10.1016/j.vph.2015.02.018.

    Article  CAS  Google Scholar 

  47. Peichev M, Naiyer AJ, Pereira D, Zhu ZP, Lane WJ, Williams M, et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood. 2000;95(3):952–8. https://doi.org/10.1182/blood.V95.3.952.003k27_952_958.

    Article  CAS  PubMed  Google Scholar 

  48. Agudo J, Ruzo A, Tung N, Salmon H, Leboeuf M, Hashimoto D, et al. The miR-126-VEGFR2 axis controls the innate response to pathogen-associated nucleic acids. Nat Immunol. 2014;15(1):54–62. https://doi.org/10.1038/ni.2767.

    Article  CAS  PubMed  Google Scholar 

  49. Elias I, Franckhauser S, Ferre T, Vila L, Tafuro S, Munoz S, et al. Adipose tissue overexpression of vascular endothelial growth factor protects against diet-induced obesity and insulin resistance. Diabetes. 2012;61(7):1801–13. https://doi.org/10.2337/db11-0832.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Yoon CH, Hur J, Park KW, Kim JH, Lee CS, Oh IY, et al. Synergistic neovascularization by mixed transplantation of early endothelial progenitor cells and late outgrowth endothelial cells: the role of angiogenic cytokines and matrix metalloproteinases. Circulation. 2005;112(11):1618–27. https://doi.org/10.1161/CIRCULATIONAHA.104.503433.

    Article  PubMed  Google Scholar 

  51. Hur J, Yoon CH, Kim HS, Choi JH, Kang HJ, Hwang KK, et al. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler Thromb Vasc Biol. 2004;24(2):288–93. https://doi.org/10.1161/01.Atv.0000114236.77009.06.

    Article  CAS  PubMed  Google Scholar 

  52. Kaushik K, Das A. Endothelial progenitor cell therapy for chronic wound tissue regeneration. Cytotherapy. 2019;21(11):1137–50. https://doi.org/10.1016/j.jcyt.2019.09.002.

    Article  CAS  PubMed  Google Scholar 

  53. Ravishankar P, Zeballos MA, Balachandran K. Isolation of endothelial progenitor cells from human umbilical cord blood. J Vis Exp. 2017;127:e56021. https://doi.org/10.3791/56021.

    Article  CAS  Google Scholar 

  54. Wils J, Favre J, Bellien J. Modulating putative endothelial progenitor cells for the treatment of endothelial dysfunction and cardiovascular complications in diabetes. Pharmacol Ther. 2017;170:98–115. https://doi.org/10.1016/j.pharmthera.2016.10.014.

    Article  CAS  PubMed  Google Scholar 

  55. Zampetaki A, Kirton JP, Xu Q. Vascular repair by endothelial progenitor cells. Cardiovasc Res. 2008;78(3):413–21. https://doi.org/10.1093/cvr/cvn081.

    Article  CAS  PubMed  Google Scholar 

  56. Shantsila E, Watson T, Lip GY. Endothelial progenitor cells in cardiovascular disorders. J Am Coll Cardiol. 2007;49(7):741–52. https://doi.org/10.1016/j.jacc.2006.09.050.

    Article  CAS  PubMed  Google Scholar 

  57. Asahara T, Takahashi T, Masuda H, Kalka C, Chen DH, Iwaguro H, et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 1999;18(14):3964–72. https://doi.org/10.1093/emboj/18.14.3964.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Cai X, Chen Z, Pan X, Xia L, Chen P, Yang Y, et al. Inhibition of angiogenesis, fibrosis and thrombosis by tetramethylpyrazine: mechanisms contributing to the SDF-1/CXCR4 axis. PLoS One. 2014;9(2):e88176. https://doi.org/10.1371/journal.pone.0088176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Meng Q, Wang W, Yu X, Li W, Kong L, Qian A, et al. Upregulation of microRNA-126 contributes to endothelial progenitor cell function in deep vein thrombosis via its target PIK3R2. J Cell Biochem. 2015;116(8):1613–23. https://doi.org/10.1002/jcb.25115.

    Article  CAS  PubMed  Google Scholar 

  60. Li P, Luo Z, Li X, Wang R, Chen H, Zhao Y, et al. Preparation, evaluation and functionalization of biomimetic block copolymer coatings for potential applications in cardiovascular implants. Appl Surf Sci. 2020;502(1):144085–96. https://doi.org/10.1016/j.apsusc.2019.144085.

    Article  CAS  Google Scholar 

  61. Wang S, Zhu S, Zhang X, Li J, Guan S. Effects of degradation products of biomedical magnesium alloys on nitric oxide release from vascular endothelial cells. Med Gas Res. 2019;9(3):153–9. https://doi.org/10.4103/2045-9912.266991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Yang Z, Yang Y, Zhang L, Xiong K, Li X, Zhang F, et al. Mussel-inspired catalytic selenocystamine-dopamine coatings for long-term generation of therapeutic gas on cardiovascular stents. Biomaterials. 2018;178:1–10. https://doi.org/10.1016/j.biomaterials.2018.06.008.

    Article  CAS  PubMed  Google Scholar 

  63. Deatrick KB, Eliason JL, Lynch EM, Moore AJ, Dewyer NA, Varma MR, et al. Vein wall remodeling after deep vein thrombosis involves matrix metalloproteinases and late fibrosis in a mouse model. J Vasc Surg. 2005;42(1):140–8. https://doi.org/10.1016/j.jvs.2005.04.014.

    Article  PubMed  Google Scholar 

  64. Kanayasu-Toyoda T, Tanaka T, Ishii-Watabe A, Kitagawa H, Matsuyama A, Uchida E, et al. Angiogenic role of MMP-2/9 expressed on the cell surface of early endothelial progenitor cells/myeloid angiogenic cells. J Cell Physiol. 2015;230(11):2763–75. https://doi.org/10.1002/jcp.25002.

    Article  CAS  PubMed  Google Scholar 

  65. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85(3):221–8. https://doi.org/10.1161/01.Res.85.3.221.

    Article  CAS  PubMed  Google Scholar 

  66. Kalka C, Tehrani H, Laudenberg B, Vale PR, Isner JM, Asahara T, et al. VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease. Ann Thorac Surg. 2000;70(3):829–34. https://doi.org/10.1016/s0003-4975(00)01633-7.

    Article  CAS  PubMed  Google Scholar 

  67. Kebir A, Harhouri K, Guillet B, Liu JW, Foucault-Bertaud A, Lamy E, et al. CD146 short isoform increases the proangiogenic potential of endothelial progenitor cells in vitro and in vivo. Circ Res. 2010;107(1):66–75. https://doi.org/10.1161/circresaha.109.213827.

    Article  CAS  PubMed  Google Scholar 

  68. Dimmeler S, Zeiher AM. Vascular repair by circulating endothelial progenitor cells: the missing link in atherosclerosis? J Mol Med. 2004;82(10):671–7. https://doi.org/10.1007/s00109-004-0580-x.

    Article  PubMed  Google Scholar 

  69. Kong DL, Melo LG, Gnecchi M, Zhang LN, Mostoslavsky G, Liew CC, et al. Cytokine-induced mobilization of circulating endothelial progenitor cells enhances repair of injured arteries. Circulation. 2004;110(14):2039–46. https://doi.org/10.1161/01.Cir.0000143161.01901.Bd.

    Article  CAS  PubMed  Google Scholar 

  70. Miglionico M, Patti G, D'ambrosio A, Di Sciascio G. Percutaneous coronary intervention utilizing a new endothelial progenitor cells antibody-coated stent: a prospective single-center registry in high-risk patients. Catheter Cardiovasc Interv. 2008;71(5):600–4. https://doi.org/10.1002/ccd.21437.

    Article  PubMed  Google Scholar 

  71. Li W, Li X. Endothelial progenitor cells accelerate the resolution of deep vein thrombosis. Vasc Pharmacol. 2016;83:10–6. https://doi.org/10.1016/j.vph.2015.07.007.

    Article  CAS  Google Scholar 

  72. Yu Y, Ricciotti E, Scalia R, Tang SY, Grant G, Yu Z, et al. Vascular COX-2 modulates blood pressure and thrombosis in mice. Sci Transl Med. 2012;4(132):132ra54. https://doi.org/10.1126/scitranslmed.3003787.

    Article  PubMed  Google Scholar 

  73. Polivka J Jr, Polivka J, Pesta M, Rohan V, Celedova L, Mahajani S, et al. Risks associated with the stroke predisposition at young age: facts and hypotheses in light of individualized predictive and preventive approach. EPMA J. 2019;10(1):81–99. https://doi.org/10.1007/s13167-019-00162-5.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Imanishi T, Kobayashi K, Hano T, Nishio I. Effect of estrogen on differentiation and senescence in endothelial progenitor cells derived from bone marrow in spontaneously hypertensive rats. Hypertens Res. 2005;28(9):763–72. https://doi.org/10.1291/hypres.28.763.

    Article  CAS  PubMed  Google Scholar 

  75. Lee PSS, Poh KK. Endothelial progenitor cells in cardiovascular diseases. World J Stem Cells. 2014;6(3):355–66. https://doi.org/10.4252/wjsc.v6.i3.355.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Fadini GP, Miorin M, Facco M, Bonamico S, Baesso I, Grego F, et al. Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus. J Am Coll Cardiol. 2005;45(9):1449–57. https://doi.org/10.1016/j.jacc.2004.11.067.

    Article  CAS  PubMed  Google Scholar 

  77. Fadini GP, Sartore S, Albiero M, Baesso I, Murphy E, Menegolo M, et al. Number and function of endothelial progenitor cells as a marker of severity for diabetic vasculopathy. Arterioscler Thromb Vasc Biol. 2006;26(9):2140–6. https://doi.org/10.1161/01.Atv.0000237750.44469.88.

    Article  CAS  PubMed  Google Scholar 

  78. Hayek SS, Macnamara J, Tahhan AS, Awad M, Yadalam A, Ko Y-A, et al. Circulating progenitor cells identify peripheral arterial disease in patients with coronary artery disease. Circ Res. 2016;119(4):564–71. https://doi.org/10.1161/circresaha.116.308802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Bitterli L, Afan S, Buehler S, Disanto S, Zwahlen M, Schmidlin K, et al. Endothelial progenitor cells as a biological marker of peripheral artery disease. Vasc Med. 2016;21(1):3–11. https://doi.org/10.1177/1358863x15611225.

    Article  CAS  PubMed  Google Scholar 

  80. Morishita T, Uzui H, Nakano A, Mitsuke Y, Geshi T, Ueda T, et al. Number of endothelial progenitor cells in peripheral artery disease as a marker of severity and association with pentraxin-3, malondialdehyde-modified low-density lipoprotein and membrane type-1 matrix metalloproteinase. J Atheroscler Thromb. 2012;19(2):149–58. https://doi.org/10.5551/jat.10074.

    Article  CAS  PubMed  Google Scholar 

  81. Delva P, De Marchi S, Prior M, Degan M, Lechi A, Trettene M, et al. Endothelial progenitor cells in patients with severe peripheral arterial disease. Endothelium. 2008;15(5–6):246–53. https://doi.org/10.1080/10623320802487718.

  82. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 2001;89(1):E1–7. https://doi.org/10.1161/hh1301.093953.

    Article  CAS  PubMed  Google Scholar 

  83. Briguori C, Testa U, Riccioni R, Colombo A, Petrucci E, Condorelli G, et al. Correlations between progression of coronary artery disease and circulating endothelial progenitor cells. FASEB J. 2010;24(6):1981–8. https://doi.org/10.1096/fj.09-138198.

    Article  CAS  PubMed  Google Scholar 

  84. Eizawa T, Ikeda U, Murakami Y, Matsui K, Yoshioka T, Takahashi M, et al. Decrease in circulating endothelial progenitor cells in patients with stable coronary artery disease. Heart. 2004;90(6):685–6. https://doi.org/10.1136/hrt.2002.008144.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Pirro M, Schillaci G, Menecali C, Bagaglia F, Paltriccia R, Vaudo G, et al. Reduced number of circulating endothelial progenitors and HOXA9 expression in CD34+cells of hypertensive patients. J Hypertens. 2007;25(10):2093–9. https://doi.org/10.1097/HJH.0b013e32828e506d.

    Article  CAS  PubMed  Google Scholar 

  86. Oliveras A, Soler MJ, Martinez-Estrada OM, Vazquez S, Marco-Feliu D, Vila JS, et al. Endothelial progenitor cells are reduced in refractory hypertension. J Hum Hypertens. 2008;22(3):183–90. https://doi.org/10.1038/sj.jhh.1002304.

    Article  CAS  PubMed  Google Scholar 

  87. Budzyn M, Gryszczynka B, Boruczkowski M, Kaczmarek M, Begier-Krasinska B, Osinska A, et al. The potential role of circulating endothelial cells and endothelial progenitor cells in the prediction of left ventricular hypertrophy in hypertensive patients. Front Physiol. 2019;10. https://doi.org/10.3389/fphys.2019.01005.

  88. Szpera-Gozdziewicz A, Majcherek M, Boruczkowski M, Gozdziewicz T, Dworacki G, Wicherek L, et al. Circulating endothelial cells, circulating endothelial progenitor cells, and von Willebrand factor in pregnancies complicated by hypertensive disorders. Am J Reprod Immunol. 2017;77(3):e12625. https://doi.org/10.1111/aji.12625.

    Article  CAS  Google Scholar 

  89. Miyaki A, Maeda S, Yoshizawa M, Misono M, Sasai H, Shimojo N, et al. Is pentraxin 3 involved in obesity-induced decrease in arterial distensibility. J Atheroscler Thromb. 2010;17(3):278–84. https://doi.org/10.5551/jat.2741.

    Article  CAS  PubMed  Google Scholar 

  90. Rajavashisth TB, Xu XP, Jovinge S, Meisel S, Xu XO, Chai NN, et al. Membrane type 1 matrix metalloproteinase expression in human atherosclerotic plaques: evidence for activation by proinflammatory mediators. Circulation. 1999;99(24):3103–9. https://doi.org/10.1161/01.Cir.99.24.3103.

    Article  CAS  PubMed  Google Scholar 

  91. Balistreri CR, Buffa S, Pisano C, Lio D, Ruvolo G, Mazzesi G. Are endothelial progenitor cells the real solution for cardiovascular diseases? Focus on controversies and perspectives. Biomed Res Int. 2015;835934:1–17. https://doi.org/10.1155/2015/835934.

    Article  CAS  Google Scholar 

  92. Kaihan AB, Hishida M, Imaizumi T, Okazaki M, Kaihan AN, Katsuno T, et al. Circulating levels of CD34(+) cells predict longterm cardiovascular outcomes in patients on maintenance hemodialysis. PLoS One. 2019;14(10):e0223390. https://doi.org/10.1371/journal.pone.0223390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Golubnitschaja O, Flammer J. Individualised patient profile: clinical utility of Flammer syndrome phenotype and general lessons for predictive, preventive and personalised medicine. EPMA J. 2018;9(1):15–20. https://doi.org/10.1007/s13167-018-0127-9.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Sabatier F, Camoin-Jau L, Anfosso F, Sampol J, Dignat-George F. Circulating endothelial cells, microparticles and progenitors: key players towards the definition of vascular competence. J Cell Mol Med. 2009;13(3):454–71. https://doi.org/10.1111/j.1582-4934.2008.00639.x.

    Article  CAS  PubMed  Google Scholar 

  95. Budzyn M, Gryszczynka B, Boruczkowski M, Kaczmarek M, Begier-Krasinska B, Osinska A, et al. The endothelial status reflected by circulating endothelial cells, circulating endothelial progenitor cells and soluble thrombomodulin in patients with mild and resistant hypertension. Vasc Pharmacol. 2019;113:77–85. https://doi.org/10.1016/j.vph.2018.12.005.

    Article  CAS  Google Scholar 

  96. Luo S, Xia W, Chen C, Robinson EA, Tao J. Endothelial progenitor cells and hypertension: current concepts and future implications. Clin Sci. 2016;130(22):2029–42. https://doi.org/10.1042/cs20160587.

    Article  CAS  Google Scholar 

  97. Eirin A, Zhu X-Y, Woollard JR, Herrmann SM, Gloviczki ML, Saad A, et al. Increased circulating inflammatory endothelial cells in blacks with essential hypertension. Hypertension. 2013;62(3):585–91. https://doi.org/10.1161/hypertensionaha.113.01621.

    Article  CAS  PubMed  Google Scholar 

  98. Holmen C, Elsheikh E, Stenvinkel P, Qureshi AR, Pettersson E, Jalkanen S, et al. Circulating inflammatory endothelial cells contribute to endothelial progenitor cell dysfunction in patients with vasculitis and kidney involvement. J Am Soc Nephrol. 2005;16(10):3110–20. https://doi.org/10.1681/asn.2005040347.

    Article  PubMed  Google Scholar 

  99. Eirin A, Zhu X-Y, Li Z, Ebrahimi B, Zhang X, Tang H, et al. Endothelial outgrowth cells shift macrophage phenotype and improve kidney viability in swine renal artery stenosis. Arterioscler Thromb Vasc Biol. 2013;33(5):1006–13. https://doi.org/10.1161/atvbaha.113.301164.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Rotmans JI, Verhagen HJM, Velema E, De Kleijn DPV, Van Den Heuvel M, Kastelein JJP, et al. Local overexpression of C-type natriuretic peptide ameliorates vascular adaptation of porcine hemodialysis grafts. Kidney Int. 2004;65(5):1897–905. https://doi.org/10.1111/j.1523-1755.2004.00598.x.

    Article  CAS  PubMed  Google Scholar 

  101. Wu Y, Chang L, Li J, Wang L, Guan S. Conjugating heparin, Arg-Glu-Asp-Val peptide, and anti-CD34 to the silanic Mg-Zn-Y-Nd alloy for better endothelialization. J Biomater Appl. 2020;35(2):158–68. https://doi.org/10.1177/0885328220926655.

    Article  CAS  PubMed  Google Scholar 

  102. Chen J, Li Q, Xu J, Zhang L, Maitz MF, Li J. Thromboresistant and rapid-endothelialization effects of dopamine and staphylococcal protein A mediated anti-CD34 coating on 316L stainless steel for cardiovascular devices. J Mater Chem. 2015;3(13):2615–23. https://doi.org/10.1039/c4tb01825g.

    Article  CAS  Google Scholar 

  103. Chen J, Cao J, Wang J, Maitz MF, Guo L, Zhao Y, et al. Biofunctionalization of titanium with PEG and anti-CD34 for hemocompatibility and stimulated endothelialization. J Colloid Interface Sci. 2012;368:636–47. https://doi.org/10.1016/j.jcis.2011.11.039.

    Article  CAS  PubMed  Google Scholar 

  104. Chen J, Li Q, Li J, Maitz MF. The effect of anti-CD34 antibody orientation control on endothelial progenitor cell capturing cardiovascular devices. J Bioact Compat Polym. 2016;31(6):583–99. https://doi.org/10.1177/0883911516637376.

    Article  CAS  Google Scholar 

  105. Hoyt J, Lerman A, Lennon RJ, Rihal CS, Prasad A. Left anterior descending artery length and coronary atherosclerosis in apical ballooning syndrome (Takotsubo/stress induced cardiomyopathy). Int J Cardiol. 2010;145(1):112–5. https://doi.org/10.1016/j.ijcard.2009.06.018.

    Article  PubMed  Google Scholar 

  106. Takahashi M, Matsuoka Y, Sumide K, Nakatsuka R, Fujioka T, Kohno H, et al. CD133 is a positive marker for a distinct class of primitive human cord blood-derived CD34-negative hematopoietic stem cells. Leukemia. 2014;28(6):1308–15. https://doi.org/10.1038/leu.2013.326.

    Article  CAS  PubMed  Google Scholar 

  107. Park K-S, Kang SN, Kim DH, Kim H-B, Im KS, Park W, et al. Late endothelial progenitor cell-capture stents with CD146 antibody and nanostructure reduce in-stent restenosis and thrombosis. Acta Biomater. 2020;111:91–101. https://doi.org/10.1016/j.actbio.2020.05.011.

    Article  CAS  PubMed  Google Scholar 

  108. Kang CK, Lim WH, Kyeong S, Choe WS, Kim HS, Jun BH, et al. Fabrication of biofunctional stents with endothelial progenitor cell specificity for vascular re-endothelialization. Colloids Surf, B. 2013;102:744–51. https://doi.org/10.1016/j.colsurfb.2012.09.008.

    Article  CAS  Google Scholar 

  109. Tan KX, Danquah MK, Sidhu A, Yon LS, Ongkudon CM. Aptamer-mediated polymeric vehicles for enhanced cell-targeted drug delivery. Curr Drug Targets. 2018;19(3):248–58. https://doi.org/10.2174/1389450117666160617120926.

    Article  CAS  PubMed  Google Scholar 

  110. Tan KX, Pan S, Jeevanandam J, Danquah MK. Cardiovascular therapies utilizing targeted delivery of nanomedicines and aptamers. Int J Pharm. 2019;558:413–25. https://doi.org/10.1016/j.ijpharm.2019.01.023.

    Article  CAS  PubMed  Google Scholar 

  111. Hoffmann J, Paul A, Harwardt M, Groll J, Reeswinkel T, Klee D, et al. Immobilized DNA aptamers used as potent attractors for porcine endothelial precursor cells. J Biomed Mater Res A. 2008;84A(3):614–21. https://doi.org/10.1002/jbm.a.31309.

    Article  CAS  Google Scholar 

  112. Chen L, Li JA, Chang J, Jin S, Wu D, Yan H, et al. Mg-Zn-Y-Nd coated with citric acid and dopamine by layer-by-layer self-assembly to improve surface biocompatibility. Sci China Technol Sci. 2018;61(8):1228–37. https://doi.org/10.1007/s11431-017-9190-2.

    Article  CAS  Google Scholar 

  113. Qi P, Yan W, Yang Y, Li Y, Fan Y, Chen J, et al. Immobilization of DNA aptamers via plasma polymerized allylamine film to construct an endothelial progenitor cell-capture surface. Colloids Surf, B. 2015;126:70–9. https://doi.org/10.1016/j.colsurfb.2014.12.001.

    Article  CAS  Google Scholar 

  114. Deng J, Yuan S, Li X, Wang K, Xie L, Li N, et al. Heparin/DNA aptamer co-assembled multifunctional catecholamine coating for EPC capture and improved hemocompatibility of vascular devices. Mater Sci Eng C-Mater Biol Appl. 2017;79:305–14. https://doi.org/10.1016/j.msec.2017.05.057.

    Article  CAS  PubMed  Google Scholar 

  115. Deng J, Yuan S, Wang J, Luo R, Chen S, Wang J, et al. Fabrication of endothelial progenitor cell capture surface via DNA aptamer modifying dopamine/polyethyleneimine copolymer film. Appl Surf Sci. 2016;386:138–50. https://doi.org/10.1016/j.apsusc.2016.06.015.

    Article  CAS  Google Scholar 

  116. Tan A, Goh D, Farhatnia Y, Natasha G, Lim J, Teoh SH, et al. An anti-CD34 antibody-functionalized clinical-grade POSS-PCU nanocomposite polymer for cardiovascular stent coating applications: a preliminary assessment of endothelial progenitor cell capture and hemocompatibility. PLoS One. 2013;8(10):e77112. https://doi.org/10.1371/journal.pone.0077112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Qi P, Maitz MF, Huang N. Surface modification of cardiovascular materials and implants. Surf Coat Technol. 2013;233:80–90. https://doi.org/10.1016/j.surfcoat.2013.02.008.

    Article  CAS  Google Scholar 

  118. Ventura RD, Padalhin AR, Park CM, Lee BT. Enhanced decellularization technique of porcine dermal ECM for tissue engineering applications. Mater Sci Eng C-Mater Biol Appl. 2019;104:109841. https://doi.org/10.1016/j.msec.2019.109841.

    Article  CAS  PubMed  Google Scholar 

  119. Colin T, Durrieu M-C, Joie J, Lei Y, Mammeri Y, Poignard C, et al. Modeling of the migration of endothelial cells on bioactive micropatterned polymers. Math Biosci Eng. 2013;10(4):997–1015. https://doi.org/10.3934/mbe.2013.10.997.

    Article  PubMed  Google Scholar 

  120. Royer C, Guay-Begin A-A, Chanseau C, Chevallier P, Bordenave L, Laroche G, et al. Bioactive micropatterning of biomaterials for induction of endothelial progenitor cell differentiation: acceleration of in situ endothelialization. J Biomed Mater Res A. 2020;108(7):1479–92. https://doi.org/10.1002/jbm.a.36918.

    Article  CAS  PubMed  Google Scholar 

  121. Blindt R, Vogt F, Astafieva I, Fach C, Hristov M, Krott N, et al. A novel drug-eluting stent coated with an integrin-binding cyclic Arg-Gly-Asp peptide inhibits neointimal hyperplasia by recruiting endothelial progenitor cells. J Am Coll Cardiol. 2006;47(9):1786–95. https://doi.org/10.1016/j.jacc.2005.11.081.

    Article  CAS  PubMed  Google Scholar 

  122. Chollet C, Chanseau C, Remy M, Guignandon A, Bareille R, Labrugere C, et al. The effect of RGD density on osteoblast and endothelial cell behavior on RGD-grafted polyethylene terephthalate surfaces. Biomaterials. 2009;30(5):711–20. https://doi.org/10.1016/j.biomaterials.2008.10.033.

    Article  CAS  PubMed  Google Scholar 

  123. Ji Y, Wei Y, Liu X, Wang J, Ren K, Ji J. Zwitterionic polycarboxybetaine coating functionalized with REDV peptide to improve selectivity for endothelial cells. J Biomed Mater Res A. 2012;100A(6):1387–97. https://doi.org/10.1002/jbm.a.34077.

    Article  CAS  Google Scholar 

  124. Qin Z. The use of THP-1 cells as a model for mimicking the function and regulation of monocytes and macrophages in the vasculature. Atherosclerosis. 2012;221(1):2–11. https://doi.org/10.1016/j.atherosclerosis.2011.09.003.

    Article  CAS  PubMed  Google Scholar 

  125. Hao D, Xiao W, Liu R, Kumar P, Li Y, Zhou P, et al. Discovery and characterization of a potent and specific peptide ligand targeting endothelial progenitor cells and endothelial cells for tissue regeneration. ACS Chem Biol. 2017;12(4):1075–86. https://doi.org/10.1021/acschembio.7b00118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Hao D, Fan Y, Xiao W, Liu R, Pivetti C, Walimbe T, et al. Rapid endothelialization of small diameter vascular grafts by a bioactive integrin-binding ligand specifically targeting endothelial progenitor cells and endothelial cells. Acta Biomater. 2020;108:178–93. https://doi.org/10.1016/j.actbio.2020.03.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Chen H, Li X, Zhao Y, Li J, Chen J, Yang P, et al. Construction of a multifunctional coating consisting of phospholipids and endothelial progenitor cell-specific peptides on titanium substrates. Appl Surf Sci. 2015;347:169–77. https://doi.org/10.1016/j.apsusc.2015.02.032.

    Article  CAS  Google Scholar 

  128. Chen Z, Li Q, Chen J, Luo R, Maitz MF, Huang N. Immobilization of serum albumin and peptide aptamer for EPC on polydopamine coated titanium surface for enhanced in-situ self-endothelialization. Mater Sci Eng C-Mater Biol Appl. 2016;60:219–29. https://doi.org/10.1016/j.msec.2015.11.044.

    Article  CAS  PubMed  Google Scholar 

  129. Jun HW, West JL. Modification of polyurethaneurea with PEG and YIGSR peptide to enhance endothelialization without platelet adhesion. J Biomed Mater Res Part B. 2005;72B(1):131–9. https://doi.org/10.1002/jbm.b.30135.

    Article  CAS  Google Scholar 

  130. Avci-Adali M, Ziemer G, Wendel HP. Induction of EPC homing on biofunctionalized vascular grafts for rapid in vivo self-endothelialization - a review of current strategies. Biotechnol Adv. 2010;28(1):119–29. https://doi.org/10.1016/j.biotechadv.2009.10.005.

    Article  CAS  PubMed  Google Scholar 

  131. Wilhelm C, Gazeau F. Universal cell labelling with anionic magnetic nanoparticles. Biomaterials. 2008;29(22):3161–74. https://doi.org/10.1016/j.biomaterials.2008.04.016.

    Article  CAS  PubMed  Google Scholar 

  132. Carenza E, Barcelo V, Morancho A, Montaner J, Rosell A, Roig A. Rapid synthesis of water-dispersible superparamagnetic iron oxide nanoparticles by a microwave-assisted route for safe labeling of endothelial progenitor cells. Acta Biomater. 2014;10(8):3775–85. https://doi.org/10.1016/j.actbio.2014.04.010.

    Article  CAS  PubMed  Google Scholar 

  133. Arbab AS, Bashaw LA, Miller BR, Jordan EK, Bulte JWM, Frank JA. Intracytoplasmic tagging of cells with ferumoxides and transfection agent for cellular magnetic resonance imaging after cell transplantation: methods and techniques. Transplantation. 2003;76(7):1123–30. https://doi.org/10.1097/01.Tp.0000089237.39220.83.

    Article  CAS  PubMed  Google Scholar 

  134. Himes N, Min JY, Lee R, Brown C, Shea J, Huang XL, et al. In vivo MRI of embryonic stem cells in a mouse model of myocardial infarction. Magn Reson Med. 2004;52(5):1214–9. https://doi.org/10.1002/mrm.20220.

    Article  PubMed  Google Scholar 

  135. Wei M, Wen D, Wang X, Huan Y, Yang Y, Xu J, et al. Experimental study of endothelial progenitor cells labeled with superparamagnetic iron oxide in vitro. Mol Med Rep. 2015;11(5):3814–9. https://doi.org/10.3892/mmr.2014.3122.

    Article  CAS  PubMed  Google Scholar 

  136. Zhang B, Jiang H, Chen J, Hu Q, Yang S, Liu X. Silica-coated magnetic nanoparticles labeled endothelial progenitor cells alleviate ischemic myocardial injury and improve long-term cardiac function with magnetic field guidance in rats with myocardial infarction. J Cell Physiol. 2019;234(10):18544–59. https://doi.org/10.1002/jcp.28492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Chen J, Wang S, Wu Z, Wei Z, Zhang W, Li W. Anti-CD34-grafted magnetic nanoparticles promote endothelial progenitor cell adhesion on an iron stent for rapid endothelialization. ACS Omega. 2019;4(21):19469–77. https://doi.org/10.1021/acsomega.9b03016.

Download references

Funding

This research was funded by National Key Research and Development Program of China (2017YFB0702500, 2018YFC1106703 and 2016YFC1102403), and Top Doctor Program of Zhengzhou University (grant number 32210475).

Author information

Authors and Affiliations

  1. School of Materials Science and Engineering & Henan Key Laboratory of Advanced Magnesium Alloy & Key Laboratory of Materials Processing and Mold Technology (Ministry of Education), Zhengzhou University, Zhengzhou, 450001, China

    Fang Kou, Chao Zhu, Hongjiang Wan, Fulong Xue, Jianfeng Wang & Jingan Li

  2. CAM-SU Genomic Resource Center, Soochow University, Suzhou, 215123, China

    Lijie Xiang

Authors
  1. Fang Kou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chao Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hongjiang Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fulong Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jianfeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lijie Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jingan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lijie Xiang or Jingan Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kou, F., Zhu, C., Wan, H. et al. Endothelial progenitor cells as the target for cardiovascular disease prediction, personalized prevention, and treatments: progressing beyond the state-of-the-art. EPMA Journal 11, 629–643 (2020). https://doi.org/10.1007/s13167-020-00223-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13167-020-00223-0

Keywords

Search

Navigation