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Perinatal Tissue-Derived Endothelial Progenitor Cells

  • Abbas Shafiee
  • Kiarash Khosrotehrani
Chapter
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)

Abstract

Endothelial progenitor cells (EPC) have been proposed as a cell population with de novo vessel formation potential for cardiovascular disease treatment, through improving neovascularization in ischemic tissues. Although initially the bone marrow was considered as the main source, EPC have been isolated from other tissues, including perinatal sources: umbilical cord blood and placenta. Perinatal EPC demonstrated similar phenotypic characteristics to other sources; however, they harbor advanced EPC quantity with improved proliferative potential. In vivo experiments also confirmed de novo vessel formation upon perinatal EPC transplantation and enhanced blood perfusion in engraftment areas. Altogether, the fetal EPC have been isolated and characterized from perinatal tissues with improved vascularization potential and at clinically relevant quantities. In this chapter, we will first review vascularization processes in the human placenta and then highlight strategies which have been conducted to harvest EPC from the human term placenta.

Keywords

Endothelial Progenitor Cells EPC Perinatal Placenta Vascularization Stem cell 

Notes

Acknowledgements

This study was supported by the National Health and Medical Research Council (Project Grant 1023368). K.K. was supported by the National Health and Medical Research Council Career Development Fellowship (Grant 1023371).

Conflict of Interest. The authors report no potential conflicts of interest.

References

  1. Abumaree M, Al Jumah M, Kalionis B, Jawdat D, Al Khaldi A, AlTalabani A, Knawy B (2013) Phenotypic and functional characterization of mesenchymal stem cells from chorionic villi of human term placenta. Stem Cell Rev Rep 9(1):16–31CrossRefGoogle Scholar
  2. Aoki J, Serruys PW, van Beusekom H, Ong AT, McFadden EP, Sianos G, van der Giessen WJ, Regar E, de Feyter PJ, Davis HR (2005) Endothelial progenitor cell capture by stents coated with antibody against CD34: the HEALING-FIM (Healthy Endothelial Accelerated Lining Inhibits Neointimal Growth-First In Man) registry. J Am Coll Cardiol 45(10):1574–1579CrossRefPubMedGoogle Scholar
  3. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302):964–966CrossRefPubMedGoogle Scholar
  4. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85(3):221–228CrossRefPubMedGoogle Scholar
  5. Awad O, Dedkov EI, Jiao C, Bloomer S, Tomanek RJ, Schatteman GC (2006) Differential healing activities of CD34+ and CD14+ endothelial cell progenitors. Arterioscler Thromb Vasc Biol 26(4):758–764CrossRefPubMedGoogle Scholar
  6. Bailey AS, Jiang S, Afentoulis M, Baumann CI, Schroeder DA, Olson SB, Wong MH, Fleming WH (2004) Transplanted adult hematopoietic stems cells differentiate into functional endothelial cells. Blood 103(1):13–19CrossRefPubMedGoogle Scholar
  7. Baldwin HS (1996) Early embryonic vascular development. Cardiovasc Res 31Spec No:E34–45Google Scholar
  8. Beck L Jr, D’Amore PA (1997) Vascular development: cellular and molecular regulation. FASEB J 11(5):365–373PubMedGoogle Scholar
  9. Beck F, Erler T, Russell A, James R (1995) Expression of Cdx‐2 in the mouse embryo and placenta: possible role in patterning of the extra‐embryonic membranes. Dev Dyn 204(3):219–227CrossRefPubMedGoogle Scholar
  10. Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438(7070):932–936CrossRefPubMedGoogle Scholar
  11. Case J, Mead LE, Bessler WK, Prater D, White HA, Saadatzadeh MR, Bhavsar JR, Yoder MC, Haneline LS, Ingram DA (2007) Human CD34< sup>+ AC133< sup>+ VEGFR-2< sup>+ cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp Hematol 35(7):1109–1118Google Scholar
  12. Caspi O, Lesman A, Basevitch Y, Gepstein A, Arbel G, Habib IHM, Gepstein L, Levenberg S (2007) Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 100(2):263–272CrossRefPubMedGoogle Scholar
  13. Castrechini N, Murthi P, Gude NM, Erwich JJ, Gronthos S, Zannettino A, Brennecke SP, Kalionis B (2010) Mesenchymal stem cells in human placental chorionic villi reside in a vascular Niche. Placenta 31(3):203–212CrossRefPubMedGoogle Scholar
  14. Charnock-Jones D, Kaufmann P, Mayhew T (2004) Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation. Placenta 25(2):103–113CrossRefPubMedGoogle Scholar
  15. Choong CS, Hutmacher DW, Triffitt JT (2006) Co-culture of bone marrow fibroblasts and endothelial cells on modified polycaprolactone substrates for enhanced potentials in bone tissue engineering. Tissue Eng 12(9):2521–2531CrossRefPubMedGoogle Scholar
  16. Demir R, Seval Y, Huppertz B (2007) Vasculogenesis and angiogenesis in the early human placenta. Acta Histochem 109(4):257–265CrossRefPubMedGoogle Scholar
  17. Dimmeler S, Zeiher AM (2009) Cell therapy of acute myocardial infarction: open questions. Cardiology 113(3):155–160. doi: 10.1159/000187652 CrossRefPubMedGoogle Scholar
  18. Duttenhoefer F, Lara de Freitas R, Meury T, Loibl M, Benneker LM, Richards RG, Alini M, Verrier S (2013) 3D scaffolds co-seeded with human endothelial progenitor and mesenchymal stem cells: evidence of prevascularisation within 7 days. Eur Cells Mater 26:49–65Google Scholar
  19. Eichmann A, Pardanaud L, Yuan L, Moyon D (2002) Vasculogenesis and the search for the hemangioblast. J Hematother Stem Cell Res 11(2):207–214CrossRefPubMedGoogle Scholar
  20. Fadini GP, Losordo D, Dimmeler S (2012) Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 110(4):624–637CrossRefPubMedPubMedCentralGoogle Scholar
  21. Ghabrial AS, Krasnow MA (2006) Social interactions among epithelial cells during tracheal branching morphogenesis. Nature 441(7094):746–749CrossRefPubMedGoogle Scholar
  22. Golos TG (2011) Stem cells from the placenta. In: Kay HH, Michael Nelson D, Wang Y (eds) The placenta: from development to disease, from development to disease. Wiley, New York, pp 327–333CrossRefGoogle Scholar
  23. Grant MB, May WS, Caballero S, Brown GA, Guthrie SM, Mames RN, Byrne BJ, Vaught T, Spoerri PE, Peck AB (2002) Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat Med 8(6):607–612CrossRefPubMedGoogle Scholar
  24. Grellier M, Bordenave L, Amedee J (2009) Cell-to-cell communication between osteogenic and endothelial lineages: implications for tissue engineering. Trends Biotechnol 27(10):562–571CrossRefPubMedGoogle Scholar
  25. He T, Smith LA, Harrington S, Nath KA, Caplice NM, Katusic ZS (2004) Transplantation of circulating endothelial progenitor cells restores endothelial function of denuded rabbit carotid arteries. Stroke 35(10):2378–2384CrossRefPubMedGoogle Scholar
  26. Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA, Finkel T (2003) Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348(7):593–600. doi: 10.1056/NEJMoa022287 CrossRefPubMedGoogle Scholar
  27. Hirata K, Li T-S, Nishida M, Ito H, Matsuzaki M, Kasaoka S, Hamano K (2003) Autologous bone marrow cell implantation as therapeutic angiogenesis for ischemic hindlimb in diabetic rat model. Am J Phys Heart Circ Phys 284(1):H66–H70Google Scholar
  28. Hofmann A, Ritz U, Verrier S, Eglin D, Alini M, Fuchs S, Kirkpatrick CJ, Rommens PM (2008) The effect of human osteoblasts on proliferation and neo-vessel formation of human umbilical vein endothelial cells in a long-term 3D co-culture on polyurethane scaffolds. Biomaterials 29(31):4217–4226. doi: 10.1016/j.biomaterials.2008.07.024 CrossRefPubMedGoogle Scholar
  29. Hofmann NA, Reinisch A, Strunk D (2009) Isolation and large scale expansion of adult human endothelial colony forming progenitor cells. Journal of visualized experiments: JoVE 32:1524Google Scholar
  30. Hristov M, Erl W, Weber PC (2003) Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 23(7):1185–1189. doi: 10.1161/01.ATV.0000073832.49290.B5 CrossRefPubMedGoogle Scholar
  31. Huppertz B, Peeters LL (2005) Vascular biology in implantation and placentation. Angiogenesis 8(2):157–167CrossRefPubMedGoogle Scholar
  32. Hur J, Yoon C-H, Kim H-S, Choi J-H, Kang H-J, Hwang K-K, Oh B-H, Lee M-M, Park Y-B (2004) Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arteriosclerosis, thrombosis, and vascular biology 24 (2):288–293Google Scholar
  33. Igura K, Zhang X, Takahashi K, Mitsuru A, Yamaguchi S, Takahashi T (2004) Isolation and characterization of mesenchymal progenitor cells from chorionic villi of human placenta. Cytotherapy 6(6):543–553CrossRefPubMedGoogle Scholar
  34. Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, Pollok K, Ferkowicz MJ, Gilley D, Yoder MC (2004) Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104(9):2752–2760CrossRefPubMedGoogle Scholar
  35. Iwasaki H, Kawamoto A, Ishikawa M, Oyamada A, Nakamori S, Nishimura H, Sadamoto K, Horii M, Matsumoto T, Murasawa S (2006) Dose-dependent contribution of CD34-positive cell transplantation to concurrent vasculogenesis and cardiomyogenesis for functional regenerative recovery after myocardial infarction. Circulation 113(10):1311–1325CrossRefPubMedGoogle Scholar
  36. Jaffredo T, Gautier R, Eichmann A, Dieterlen-Lievre F (1998) Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 125(22):4575–4583PubMedGoogle Scholar
  37. Joe AW, Yi L, Natarajan A, Le Grand F, So L, Wang J, Rudnicki MA, Rossi FM (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12(2):153–163. doi: 10.1038/ncb2015 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T (2000) Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A 97(7):3422–3427. doi: 10.1073/pnas.070046397 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kara RJ, Bolli P, Karakikes I, Matsunaga I, Tripodi J, Tanweer O, Altman P, Shachter NS, Nakano A, Najfeld V (2012) Fetal cells traffic to injured maternal myocardium and undergo cardiac differentiation. Circ Res 110(1):82–93CrossRefPubMedGoogle Scholar
  40. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM, Asahara T (2001) Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103(5):634–637CrossRefPubMedGoogle Scholar
  41. Kawamoto A, Tkebuchava T, Yamaguchi J, Nishimura H, Yoon YS, Milliken C, Uchida S, Masuo O, Iwaguro H, Ma H, Hanley A, Silver M, Kearney M, Losordo DW, Isner JM, Asahara T (2003) Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 107(3):461–468CrossRefPubMedGoogle Scholar
  42. Kawamoto A, Katayama M, Handa N, Kinoshita M, Takano H, Horii M, Sadamoto K, Yokoyama A, Yamanaka T, Onodera R (2009) Intramuscular transplantation of G‐CSF‐mobilized CD34+ cells in patients with critical limb ischemia: a phase I/IIa, multicenter, single‐blinded, dose‐escalation clinical trial. Stem Cells 27(11):2857–2864CrossRefPubMedGoogle Scholar
  43. Lee JM, Choe W, Kim B-K, Seo W-W, Lim W-H, Kang C-K, Kyeong S, Eom KD, Cho H-J, Kim Y-C (2012) Comparison of endothelialization and neointimal formation with stents coated with antibodies against CD34 and vascular endothelial-cadherin. Biomaterials 33(35):8917–8927CrossRefPubMedGoogle Scholar
  44. Leeper NJ, Hunter AL, Cooke JP (2010) Stem cell therapy for vascular regeneration adult, embryonic, and induced pluripotent stem cells. Circulation 122(5):517–526CrossRefPubMedPubMedCentralGoogle Scholar
  45. Leistner DM, Fischer-Rasokat U, Honold J, Seeger FH, Schächinger V, Lehmann R, Martin H, Burck I, Urbich C, Dimmeler S (2011) Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI): final 5-year results suggest long-term safety and efficacy. Clin Res Cardiol 100(10):925–934CrossRefPubMedGoogle Scholar
  46. Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, Marini R, van Blitterswijk CA, Mulligan RC, D’Amore PA (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23(7):879–884CrossRefPubMedGoogle Scholar
  47. Lim W-H, Seo W-W, Choe W, Kang C-K, Park J, Cho H-J, Kyeong S, Hur J, Yang H-M, Cho H-J (2011) Stent coated with antibody against vascular endothelial-cadherin captures endothelial progenitor cells, accelerates re-endothelialization, and reduces neointimal formation. Arterioscler Thromb Vasc Biol 31(12):2798–2805CrossRefPubMedGoogle Scholar
  48. Liu Y, Teoh SH, Chong MS, Lee ES, Mattar CN, Randhawa NK, Zhang ZY, Medina RJ, Kamm RD, Fisk NM, Choolani M, Chan JK (2012) Vasculogenic and osteogenesis-enhancing potential of human umbilical cord blood endothelial colony-forming cells. Stem Cells 30(9):1911–1924. doi: 10.1002/stem.1164 CrossRefPubMedGoogle Scholar
  49. Lucitti JL, Jones EA, Huang C, Chen J, Fraser SE, Dickinson ME (2007) Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134(18):3317–3326. doi: 10.1242/dev.02883 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Markway BD, McCarty OJ, Marzec UM, Courtman DW, Hanson SR, Hinds MT (2008) Capture of flowing endothelial cells using surface-immobilized anti-kinase insert domain receptor antibody. Tissue Eng Part C Methods 14(2):97–105CrossRefPubMedGoogle Scholar
  51. Masuda H, Alev C, Akimaru H, Ito R, Shizuno T, Kobori M, Horii M, Ishihara T, Isobe K, Isozaki M (2011) Methodological development of a clonogenic assay to determine endothelial progenitor cell potential. Circ Res 109(1):20–37CrossRefPubMedGoogle Scholar
  52. Mathews S, Rao KL, Prasad KS, Kanakavalli M, Reddy AG, Raj TA, Thangaraj K, Pande G (2015) Propagation of pure fetal and maternal mesenchymal stromal cells from terminal chorionic villi of human term placenta. Sci Rep 5Google Scholar
  53. Matoba S, Tatsumi T, Murohara T, Imaizumi T, Katsuda Y, Ito M, Saito Y, Uemura S, Suzuki H, Fukumoto S (2008) Long-term clinical outcome after intramuscular implantation of bone marrow mononuclear cells (Therapeutic Angiogenesis by Cell Transplantation [TACT] trial) in patients with chronic limb ischemia. Am Heart J 156(5):1010–1018CrossRefPubMedGoogle Scholar
  54. Mondrinos MJ, Koutzaki SH, Poblete HM, Crisanti MC, Lelkes PI, Finck CM (2008) In vivo pulmonary tissue engineering: contribution of donor-derived endothelial cells to construct vascularization. Tissue Eng A 14(3):361–368. doi: 10.1089/tea.2007.0041 CrossRefGoogle Scholar
  55. Murohara T, Ikeda H, Duan J, Shintani S, K-i S, Eguchi H, Onitsuka I, Matsui K, Imaizumi T (2000) Transplanted cord blood–derived endothelial precursor cells augment postnatal neovascularization. J Clin Investig 105(11):1527–1536CrossRefPubMedPubMedCentralGoogle Scholar
  56. Nagano M, Yamashita T, Hamada H, Ohneda K, K-i K, Nakagawa T, Shibuya M, Yoshikawa H, Ohneda O (2007) Identification of functional endothelial progenitor cells suitable for the treatment of ischemic tissue using human umbilical cord blood. Blood 110(1):151–160CrossRefPubMedGoogle Scholar
  57. Patel J, Seppanen E, Chong MS, Yeo JS, Teo EY, Chan JK, Fisk NM, Khosrotehrani K (2013) Prospective surface marker-based isolation and expansion of fetal endothelial colony-forming cells from human term placenta. Stem Cells Transl Med 2(11):839–847CrossRefPubMedPubMedCentralGoogle Scholar
  58. Patel J, Shafiee A, Wang W, Fisk N, Khosrotehrani K (2014) Novel isolation strategy to deliver pure fetal-origin and maternal-origin mesenchymal stem cell (MSC) populations from human term placenta. Placenta 35(11):969–971CrossRefPubMedGoogle Scholar
  59. Patel J, Wong HY, Wang W, Alexis J, Shafiee A, Stevenson AJ, Gabrielli B, Fisk NM, Khosrotehrani K (2016) Self‐renewal and high proliferative colony forming capacity of late‐outgrowth endothelial progenitors is regulated by cyclin‐dependent kinase inhibitors driven by notch signaling. Stem Cells 34(4):902–912CrossRefPubMedGoogle Scholar
  60. Pelosi E, Valtieri M, Coppola S, Botta R, Gabbianelli M, Lulli V, Marziali G, Masella B, Müller R, Sgadari C (2002) Identification of the hemangioblast in postnatal life. Blood 100(9):3203–3208CrossRefPubMedGoogle Scholar
  61. Rafii S, Lyden D (2003) Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9(6):702–712. doi: 10.1038/nm0603-702 CrossRefPubMedGoogle Scholar
  62. Rafii S, Butler JM, Ding B-S (2016) Angiocrine functions of organ-specific endothelial cells. Nature 529(7586):316–325CrossRefPubMedPubMedCentralGoogle Scholar
  63. Rapp BM, Saadatzedeh MR, Ofstein RH, Bhavsar JR, Tempel ZS, Moreno O, Morone P, Booth DA, Traktuev DO, Dalsing MC (2012) Resident endothelial progenitor cells from human placenta have greater vasculogenic potential than circulating endothelial progenitor cells from umbilical cord blood. Cell Med 2(3):85–96PubMedGoogle Scholar
  64. Red-Horse K, Crawford Y, Shojaei F, Ferrara N (2007) Endothelium-microenvironment interactions in the developing embryo and in the adult. Dev Cell 12(2):181–194CrossRefPubMedGoogle Scholar
  65. Reinisch A, Hofmann NA, Obenauf AC, Kashofer K, Rohde E, Schallmoser K, Flicker K, Lanzer G, Linkesch W, Speicher MR (2009) Humanized large-scale expanded endothelial colony–forming cells function in vitro and in vivo. Blood 113 (26):6716–6725Google Scholar
  66. Reynolds LP, Redmer DA (2001) Angiogenesis in the placenta. Biol Reprod 64(4):1033–1040CrossRefPubMedGoogle Scholar
  67. Reynolds LP, Grazul‐Bilska AT, Redmer DA (2002) Angiogenesis in the female reproductive organs: pathological implications. Int J Exp Pathol 83(4):151–164CrossRefPubMedPubMedCentralGoogle Scholar
  68. Rhodes KE, Gekas C, Wang Y, Lux CT, Francis CS, Chan DN, Conway S, Orkin SH, Yoder MC, Mikkola HK (2008) The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell 2(3):252–263CrossRefPubMedPubMedCentralGoogle Scholar
  69. Ribatti D, Vacca A, Nico B, Roncali L, Dammacco F (2001) Postnatal vasculogenesis. Mech Dev 100(2):157–163CrossRefPubMedGoogle Scholar
  70. Robin C, Bollerot K, Mendes S, Haak E, Crisan M, Cerisoli F, Lauw I, Kaimakis P, Jorna R, Vermeulen M (2009) Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. Cell Stem Cell 5(4):385–395CrossRefPubMedPubMedCentralGoogle Scholar
  71. Rouwkema J, Rivron NC, van Blitterswijk CA (2008) Vascularization in tissue engineering. Trends Biotechnol 26(8):434–441. doi: 10.1016/j.tibtech.2008.04.009 CrossRefPubMedGoogle Scholar
  72. Santos MI, Unger RE, Sousa RA, Reis RL, Kirkpatrick CJ (2009) Crosstalk between osteoblasts and endothelial cells co-cultured on a polycaprolactone–starch scaffold and the< i> in vitro development of vascularization. Biomaterials 30(26):4407–4415Google Scholar
  73. Schatteman GC, Hanlon HD, Jiao C, Dodds SG, Christy BA (2000) Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest 106(4):571–578. doi: 10.1172/JCI9087 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Scheubel RJ, Zorn H, Silber R-E, Kuss O, Morawietz H, Holtz J, Simm A (2003) Age-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting. J Am Coll Cardiol 42(12):2073–2080CrossRefPubMedGoogle Scholar
  75. Schoenwolf GC (2009) Larsen’s human embryology. Churchill Livingstone, PhiladelphiaGoogle Scholar
  76. Sethi R, LEE CH (2012) Endothelial progenitor cell capture stent: safety and effectiveness. J Interv Cardiol 25(5):493–500CrossRefPubMedGoogle Scholar
  77. Shafiee A, Fisk NM, Hutmacher DW, Khosrotehrani K, Patel J (2015) Fetal endothelial and mesenchymal progenitors from the human term placenta: potency and clinical potential. Stem Cells Transl Med 4(5):419–423CrossRefPubMedPubMedCentralGoogle Scholar
  78. Shepherd BR, Enis DR, Wang F, Suarez Y, Pober JS, Schechner JS (2006) Vascularization and engraftment of a human skin substitute using circulating progenitor cell-derived endothelial cells. FASEB J 20(10):1739–1741CrossRefPubMedGoogle Scholar
  79. Sukmawati D, Tanaka R (2015) Introduction to next generation of endothelial progenitor cell therapy: a promise in vascular medicine. Am J Transl Res 7(3):411–421PubMedPubMedCentralGoogle Scholar
  80. Tanaka R, Wada M, Kwon SM, Masuda H, Carr J, Ito R, Miyasaka M, Warren SM, Asahara T, Tepper OM (2008) The effects of flap ischemia on normal and diabetic progenitor cell function. Plast Reconstr Surg 121(6):1929–1942CrossRefPubMedGoogle Scholar
  81. Tanaka R, Masuda H, Kato S, Imagawa K, Kanabuchi K, Nakashioya C, Yoshiba F, Fukui T, Ito R, Kobori M (2014) Autologous G-CSF-mobilized peripheral blood CD34+ cell therapy for diabetic patients with chronic nonhealing ulcer. Cell Transplant 23(2):167–179CrossRefPubMedGoogle Scholar
  82. Tateishi-Yuyama E, Matsubara H, Murohara T, Ikeda U, Shintani S, Masaki H, Amano K, Kishimoto Y, Yoshimoto K, Akashi H (2002) Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet 360(9331):427–435CrossRefPubMedGoogle Scholar
  83. Tepper OM, Carr J, Allen RJ, Chang CC, Lin CD, Tanaka R, Gupta SM, Levine JP, Saadeh PB, Warren SM (2010) Decreased circulating progenitor cell number and failed mechanisms of stromal cell-derived factor-1α mediated bone marrow mobilization impair diabetic tissue repair. Diabetes 59(8):1974–1983CrossRefPubMedPubMedCentralGoogle Scholar
  84. Timmermans F, Plum J, Yöder MC, Ingram DA, Vandekerckhove B, Case J (2009) Endothelial progenitor cells: identity defined? J Cell Mol Med 13(1):87–102CrossRefPubMedGoogle Scholar
  85. Tremblay PL, Hudon V, Berthod F, Germain L, Auger FA (2005) Inosculation of tissue-engineered capillaries with the host’s vasculature in a reconstructed skin transplanted on mice. Am J Transplant 5(5):1002–1010. doi: 10.1111/j.1600-6143.2005.00790.x CrossRefPubMedGoogle Scholar
  86. Ulrich C, Rolauffs B, Abele H, Bonin M, Nieselt K, Hart ML, Aicher WK (2013) Low osteogenic differentiation potential of placenta-derived mesenchymal stromal cells correlates with low expression of the transcription factors Runx2 and Twist2. Stem Cells Dev 22(21):2859–2872CrossRefPubMedPubMedCentralGoogle Scholar
  87. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S (2001) Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89(1):e1–e7CrossRefPubMedGoogle Scholar
  88. Yang J, Ii M, Kamei N, Alev C, Kwon S-M, Kawamoto A, Akimaru H, Masuda H, Sawa Y, Asahara T (2011) CD34+ cells represent highly functional endothelial progenitor cells in murine bone marrow. PLoS One 6(5):e20219CrossRefPubMedPubMedCentralGoogle Scholar
  89. Yoder MC, Hiatt K, Mukherjee P (1997) In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proc Natl Acad Sci 94(13):6776–6780CrossRefPubMedPubMedCentralGoogle Scholar
  90. Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F, Krasich R, Temm CJ, Prchal JT, Ingram DA (2007) Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109(5):1801–1809CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.UQ Centre for Clinical ResearchThe University of QueenslandBrisbaneAustralia
  2. 2.Institute of Health and Biomedical InnovationQueensland University of TechnologyBrisbaneAustralia
  3. 3.UQ Diamantina Institute, Translational Research InstituteThe University of QueenslandBrisbaneAustralia

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