Advertisement

Bioengineering human vascular networks: trends and directions in endothelial and perivascular cell sources

  • Kai Wang
  • Ruei-Zeng Lin
  • Juan M. Melero-Martin
Review

Abstract

Tissue engineering holds great promise in regenerative medicine. However, the field of tissue engineering faces a myriad of difficulties. A major challenge is the necessity to integrate vascular networks into bioengineered constructs to enable physiological functions including adequate oxygenation, nutrient delivery, and removal of waste products. The last two decades have seen remarkable progress in our collective effort to bioengineer human-specific vascular networks. Studies have included both in vitro and in vivo investigations, and multiple methodologies have found varying degrees of success. What most approaches to bioengineer human vascular networks have in common, however, is the synergistic use of both (1) endothelial cells (ECs)—the cells used to line the lumen of the vascular structures and (2) perivascular cells—usually used to support EC function and provide perivascular stability to the networks. Here, we have highlighted trends in the use of various cellular sources over the last two decades of vascular network bioengineering research. To this end, we comprehensively reviewed all life science and biomedical publications available at the MEDLINE database up to 2018. Emphasis was put on selective studies that definitively used human ECs and were specifically related to bioengineering vascular networks. To facilitate this analysis, all papers were stratified by publication year and then analyzed according to their use of EC and perivascular cell types. This study provides an illustrating discussion on how each alternative source of cells has come to be used in the field. Our intention was to reveal trends and to provide new insights into the trajectory of vascular network bioengineering with regard to cellular sources.

Keywords

Vascularization Endothelial progenitor cells iPS cells Stem cells Mesenchymal cells Hydrogel Angiogenesis Vasculogenesis 

Notes

Acknowledgements

This work was supported by National Institutes of Health Grants R01AR069038, R01HL128452, and R21AI123883 to J. M.-M.

Author contributions

KW, R-ZL, and JMM-M conceived and designed the project, analyzed the data, discussed and edited the results and wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.

References

  1. 1.
    Atala A, Kasper FK, Mikos AG (2012) Engineering complex tissues. Sci Transl Med 4:160rv12.  https://doi.org/10.1126/scitranslmed.3004890 CrossRefPubMedGoogle Scholar
  2. 2.
    Takeshita S, Zheng LP, Brogi E et al (1994) Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Investig 93:662–670.  https://doi.org/10.1172/JCI117018 CrossRefPubMedGoogle Scholar
  3. 3.
    Simons M, Ware JA (2003) Therapeutic angiogenesis in cardiovascular disease. Nat Rev Drug Discov 2:863–871.  https://doi.org/10.1038/nrd1226 CrossRefPubMedGoogle Scholar
  4. 4.
    Phelps EA, García AJ (2009) Update on therapeutic vascularization strategies. Regen Med 4:65–80.  https://doi.org/10.2217/17460751.4.1.65 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Said SS, Pickering JG, Mequanint K (2013) Advances in growth factor delivery for therapeutic angiogenesis. J Vasc Res 50:35–51.  https://doi.org/10.1159/000345108 CrossRefPubMedGoogle Scholar
  6. 6.
    Marino D, Luginbühl J, Scola S et al (2014) Bioengineering dermo-epidermal skin grafts with blood and lymphatic capillaries. Sci Transl Med 6:221ra14.  https://doi.org/10.1126/scitranslmed.3006894 CrossRefPubMedGoogle Scholar
  7. 7.
    Maisel K, Sasso MS, Potin L, Swartz MA (2017) Exploiting lymphatic vessels for immunomodulation: rationale, opportunities, and challenges. Adv Drug Deliv Rev 114:43–59.  https://doi.org/10.1016/j.addr.2017.07.005 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Allen P, Melero Martin J, Bischoff J (2011) Type I collagen, fibrin and PuraMatrix matrices provide permissive environments for human endothelial and mesenchymal progenitor cells to form neovascular networks. J Tissue Eng Regen Med 5:e74–e86.  https://doi.org/10.1002/term.389 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Bae H, Puranik AS, Gauvin R et al (2012) Building vascular networks. Sci Transl Med 4:160ps23.  https://doi.org/10.1126/scitranslmed.3003688 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Chen Y-C, Chen Y-C, Lin R-Z et al (2012) Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels. Adv Funct Mater 22:2027–2039.  https://doi.org/10.1002/adfm.201101662 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Serbo JV, Gerecht S (2013) Vascular tissue engineering: biodegradable scaffold platforms to promote angiogenesis. Stem Cell Res Ther 4:8.  https://doi.org/10.1186/scrt156 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Chang WG, Niklason LE (2017) A short discourse on vascular tissue engineering. NPJ Regen Med.  https://doi.org/10.1038/s41536-017-0011-6 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Song H-HG, Rumma RT, Ozaki CK et al (2018) Vascular tissue engineering: progress, challenges, and clinical promise. Cell Stem Cell 22:340–354.  https://doi.org/10.1016/j.stem.2018.02.009 CrossRefPubMedGoogle Scholar
  14. 14.
    Gimbrone MA, Cotran RS, Folkman MJ (1974) Human vascular endothelial cells in culture. Growth and DNA synthesis. J Cell Biol 60:673–684CrossRefGoogle Scholar
  15. 15.
    Black AF, Berthod F, L’heureux N et al (1998) In vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. FASEB J 12:1331–1340CrossRefGoogle Scholar
  16. 16.
    Schechner JS, Nath AK, Zheng L et al (2000) In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci USA 97:9191–9196.  https://doi.org/10.1073/pnas.150242297 CrossRefPubMedGoogle Scholar
  17. 17.
    Koike N, Fukumura D, Gralla O et al (2004) Tissue engineering: creation of long-lasting blood vessels. Nature 428:138–139.  https://doi.org/10.1038/428138a CrossRefPubMedGoogle Scholar
  18. 18.
    Levenberg S, Rouwkema J, Macdonald M et al (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23:879–884.  https://doi.org/10.1038/nbt1109 CrossRefPubMedGoogle Scholar
  19. 19.
    Tsigkou O, Pomerantseva I, Spencer JA et al (2010) Engineered vascularized bone grafts. Proc Natl Acad Sci USA 107:3311–3316.  https://doi.org/10.1073/pnas.0905445107 CrossRefPubMedGoogle Scholar
  20. 20.
    Caspi O, Lesman A, Basevitch Y et al (2007) Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ Res 100:263–272.  https://doi.org/10.1161/01.RES.0000257776.05673.ff CrossRefPubMedGoogle Scholar
  21. 21.
    Davison PM, Bensch K, Karasek MA (1980) Isolation and growth of endothelial cells from the microvessels of the newborn human foreskin in cell culture. J Investig Dermatol 75:316–321CrossRefGoogle Scholar
  22. 22.
    Kern PA, Knedler A, Eckel RH (1983) Isolation and culture of microvascular endothelium from human adipose tissue. J Clin Investig 71:1822–1829CrossRefGoogle Scholar
  23. 23.
    Nör JE, Peters MC, Christensen JB et al (2001) Engineering and characterization of functional human microvessels in immunodeficient mice. Lab Investig 81:453–463CrossRefGoogle Scholar
  24. 24.
    Peters MC, Polverini PJ, Mooney DJ (2002) Engineering vascular networks in porous polymer matrices. J Biomed Mater Res 60:668–678CrossRefGoogle Scholar
  25. 25.
    Szöke K, Beckstrøm KJ, Brinchmann JE (2012) Human adipose tissue as a source of cells with angiogenic potential. Cell Transplant 21:235–250.  https://doi.org/10.3727/096368911X580518 CrossRefPubMedGoogle Scholar
  26. 26.
    Lin R-Z, Moreno-Luna R, Moreno-Luna R et al (2013) Human white adipose tissue vasculature contains endothelial colony-forming cells with robust in vivo vasculogenic potential. Angiogenesis 16:735–744.  https://doi.org/10.1007/s10456-013-9350-0 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Cerqueira MT, Pirraco RP, Martins AR et al (2014) Cell sheet technology-driven re-epithelialization and neovascularization of skin wounds. Acta Biomater 10:3145–3155.  https://doi.org/10.1016/j.actbio.2014.03.006 CrossRefPubMedGoogle Scholar
  28. 28.
    Klar AS, Guven S, Zimoch J et al (2016) Characterization of vasculogenic potential of human adipose-derived endothelial cells in a three-dimensional vascularized skin substitute. Pediatr Surg Int 32:17–27.  https://doi.org/10.1007/s00383-015-3808-7 CrossRefPubMedGoogle Scholar
  29. 29.
    Freiman A, Shandalov Y, Rozenfeld D et al (2016) Adipose-derived endothelial and mesenchymal stem cells enhance vascular network formation on three-dimensional constructs in vitro. Stem Cell Res Ther 7:5.  https://doi.org/10.1186/s13287-015-0251-6 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Yoshida T, Komaki M, Hattori H et al (2010) Therapeutic angiogenesis by implantation of a capillary structure constituted of human adipose tissue microvascular endothelial cells. Arterioscler Thromb Vasc Biol 30:1300–1306.  https://doi.org/10.1161/atvbaha.109.198994 CrossRefPubMedGoogle Scholar
  31. 31.
    Sasagawa T, Shimizu T, Yamato M, Okano T (2014) Expression profiles of angiogenesis-related proteins in prevascular three-dimensional tissues using cell-sheet engineering. Biomaterials 35:206–213.  https://doi.org/10.1016/j.biomaterials.2013.09.104 CrossRefPubMedGoogle Scholar
  32. 32.
    Bhattacharyya A, Lin S, Sandig M, Mequanint K (2014) Regulation of vascular smooth muscle cell phenotype in three-dimensional coculture system by Jagged1-selective Notch3 signaling. Tissue Eng Part A 20:1175–1187.  https://doi.org/10.1089/ten.TEA.2013.0268 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Herland A, van der Meer AD, FitzGerald EA et al (2016) Distinct contributions of astrocytes and pericytes to neuroinflammation identified in a 3D human blood–brain barrier on a chip. PLoS One 11:e0150360.  https://doi.org/10.1371/journal.pone.0150360 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Valarmathi MT, Fuseler JW, Davis JM, Price RL (2017) A novel human tissue-engineered 3-D functional vascularized cardiac muscle construct. Front Cell Dev Biol 5:2.  https://doi.org/10.3389/fcell.2017.00002 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Amano Y, Nishiguchi A, Matsusaki M et al (2016) Development of vascularized iPSC derived 3D-cardiomyocyte tissues by filtration layer-by-layer technique and their application for pharmaceutical assays. Acta Biomater 33:110–121.  https://doi.org/10.1016/j.actbio.2016.01.033 CrossRefPubMedGoogle Scholar
  36. 36.
    Tan Q, Choi KM, Sicard D, Tschumperlin DJ (2017) Human airway organoid engineering as a step toward lung regeneration and disease modeling. Biomaterials 113:118–132.  https://doi.org/10.1016/j.biomaterials.2016.10.046 CrossRefPubMedGoogle Scholar
  37. 37.
    Rafii S, Lyden D (2003) Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9:702–712.  https://doi.org/10.1038/nm0603-702 CrossRefPubMedGoogle Scholar
  38. 38.
    Lin Y, Weisdorf DJ, Solovey A, Hebbel RP (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Investig 105:71–77.  https://doi.org/10.1172/JCI8071 CrossRefPubMedGoogle Scholar
  39. 39.
    Medina RJ, Barber CL, Sabatier F et al (2017) Endothelial progenitors: a consensus statement on nomenclature. Stem Cells Transl Med 229:10–1320.  https://doi.org/10.1002/sctm.16-0360 CrossRefGoogle Scholar
  40. 40.
    Melero-Martin JM, Melero-Martin JM, Khan ZA et al (2007) In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood 109:4761–4768.  https://doi.org/10.1182/blood-2006-12-062471 CrossRefPubMedGoogle Scholar
  41. 41.
    Yoder MC, Mead LE, Prater D et al (2007) Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109:1801–1809.  https://doi.org/10.1182/blood-2006-08-043471 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Sieminski AL, Hebbel RP, Gooch KJ (2005) Improved microvascular network in vitro by human blood outgrowth endothelial cells relative to vessel-derived endothelial cells. Tissue Eng 11:1332–1345.  https://doi.org/10.1089/ten.2005.11.1332 CrossRefPubMedGoogle Scholar
  43. 43.
    Au P, Daheron LM, Duda DG et al (2008) Differential in vivo potential of endothelial progenitor cells from human umbilical cord blood and adult peripheral blood to form functional long-lasting vessels. Blood 111:1302–1305.  https://doi.org/10.1182/blood-2007-06-094318 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Wu X, Rabkin-Aikawa E, Guleserian KJ et al (2004) Tissue-engineered microvessels on three-dimensional biodegradable scaffolds using human endothelial progenitor cells. Am J Physiol Heart Circ Physiol 287:H480–H487.  https://doi.org/10.1152/ajpheart.01232.2003 CrossRefPubMedGoogle Scholar
  45. 45.
    Fuchs S, Hofmann A, Kirkpatrick CJ (2007) Microvessel-like structures from outgrowth endothelial cells from human peripheral blood in 2-dimensional and 3-dimensional co-cultures with osteoblastic lineage cells. Tissue Eng 13:2577–2588.  https://doi.org/10.1089/ten.2007.0022 CrossRefPubMedGoogle Scholar
  46. 46.
    Shepherd BR, Enis DR, Wang F et al (2006) Vascularization and engraftment of a human skin substitute using circulating progenitor cell-derived endothelial cells. FASEB J 20:1739–1741.  https://doi.org/10.1096/fj.05-5682fje CrossRefPubMedGoogle Scholar
  47. 47.
    Chen X, Aledia AS, Popson SA et al (2010) Rapid anastomosis of endothelial progenitor cell-derived vessels with host vasculature is promoted by a high density of cotransplanted fibroblasts. Tissue Eng Part A 16:585–594.  https://doi.org/10.1089/ten.TEA.2009.0491 CrossRefPubMedGoogle Scholar
  48. 48.
    Melero-Martin JM, De Obaldia ME, Kang SY et al (2008) Engineering robust and functional vascular networks in vivo with human adult and cord blood-derived progenitor cells. Circ Res 103:194–202.  https://doi.org/10.1161/CIRCRESAHA.108.178590 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Traktuev DO, Prater DN, Merfeld-Clauss S et al (2009) Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ Res 104:1410–1420.  https://doi.org/10.1161/CIRCRESAHA.108.190926 CrossRefPubMedGoogle Scholar
  50. 50.
    Fuchs S, Ghanaati S, Orth C et al (2009) Contribution of outgrowth endothelial cells from human peripheral blood on in vivo vascularization of bone tissue engineered constructs based on starch polycaprolactone scaffolds. Biomaterials 30:526–534.  https://doi.org/10.1016/j.biomaterials.2008.09.058 CrossRefPubMedGoogle Scholar
  51. 51.
    Kang K-T, Allen P, Bischoff J (2011) Bioengineered human vascular networks transplanted into secondary mice reconnect with the host vasculature and re-establish perfusion. Blood 118:6718–6721.  https://doi.org/10.1182/blood-2011-08-375188 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Tasev D, Koolwijk P, Van Hinsbergh VWM (2016) Therapeutic potential of human-derived endothelial colony-forming cells in animal models. Tissue Eng Part B Rev 22:371–382.  https://doi.org/10.1089/ten.TEB.2016.0050 CrossRefPubMedGoogle Scholar
  53. 53.
    Ingram DA, Mead LE, Tanaka H et al (2004) Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104:2752–2760.  https://doi.org/10.1182/blood-2004-04-1396 CrossRefPubMedGoogle Scholar
  54. 54.
    Mund JA, Estes ML, Yoder MC et al (2012) Flow cytometric identification and functional characterization of immature and mature circulating endothelial cells. Arterioscler Thromb Vasc Biol 32:1045–1053.  https://doi.org/10.1161/ATVBAHA.111.244210 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Rignault-Clerc S, Bielmann C, Delodder F et al (2013) Functional late outgrowth endothelial progenitors isolated from peripheral blood of burned patients. Burns 39:694–704.  https://doi.org/10.1016/j.burns.2012.09.027 CrossRefPubMedGoogle Scholar
  56. 56.
    Stroncek JD, Grant BS, Brown MA et al (2009) Comparison of endothelial cell phenotypic markers of late-outgrowth endothelial progenitor cells isolated from patients with coronary artery disease and healthy volunteers. Tissue Eng Part A 15:3473–3486.  https://doi.org/10.1089/ten.TEA.2008.0673 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Thill M, Strunnikova NV, Berna MJ et al (2008) Late outgrowth endothelial progenitor cells in patients with age-related macular degeneration. Investig Ophthalmol Vis Sci 49:2696–2708.  https://doi.org/10.1167/iovs.07-0955 CrossRefGoogle Scholar
  58. 58.
    Thomson JA, Itskovitz-Eldor J, Shapiro SS et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147CrossRefGoogle Scholar
  59. 59.
    Wilmut I, Beaujean N, de Sousa PA et al (2002) Somatic cell nuclear transfer: PubMed—NCBI. Nature 419:583–587CrossRefGoogle Scholar
  60. 60.
    Levenberg S, Golub JS, Amit M et al (2002) Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 99:4391–4396.  https://doi.org/10.1073/pnas.032074999 CrossRefPubMedGoogle Scholar
  61. 61.
    Wang ZZ, Au P, Chen T et al (2007) Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat Biotechnol 25:317–318.  https://doi.org/10.1038/nbt1287 CrossRefPubMedGoogle Scholar
  62. 62.
    Nourse MB, Halpin DE, Scatena M et al (2010) VEGF induces differentiation of functional endothelium from human embryonic stem cells: implications for tissue engineering. Arterioscler Thromb Vasc Biol 30:80–89.  https://doi.org/10.1161/ATVBAHA.109.194233 CrossRefPubMedGoogle Scholar
  63. 63.
    Kraehenbuehl TP, Ferreira LS, Hayward AM et al (2011) Human embryonic stem cell-derived microvascular grafts for cardiac tissue preservation after myocardial infarction. Biomaterials 32:1102–1109.  https://doi.org/10.1016/j.biomaterials.2010.10.005 CrossRefPubMedGoogle Scholar
  64. 64.
    Takahashi K, Tanabe K, Ohnuki M et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872.  https://doi.org/10.1016/j.cell.2007.11.019 CrossRefPubMedGoogle Scholar
  65. 65.
    Yu J, Vodyanik MA, Smuga-Otto K et al (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920.  https://doi.org/10.1126/science.1151526 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Park I-H, Zhao R, West JA et al (2008) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451:141–146.  https://doi.org/10.1038/nature06534 CrossRefPubMedGoogle Scholar
  67. 67.
    Wu SM, Hochedlinger K (2011) Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nat Cell Biol 13:497–505.  https://doi.org/10.1038/ncb0511-497 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Taura D, Sone M, Homma K et al (2009) Induction and isolation of vascular cells from human induced pluripotent stem cells—brief report. Arterioscler Thromb Vasc Biol 29:1100–1103.  https://doi.org/10.1161/ATVBAHA.108.182162 CrossRefPubMedGoogle Scholar
  69. 69.
    Rufaihah AJ, Huang NF, Jamé S et al (2011) Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in a mouse model of peripheral arterial disease. Arterioscler Thromb Vasc Biol 31:e72–e79.  https://doi.org/10.1161/ATVBAHA.111.230938 CrossRefPubMedGoogle Scholar
  70. 70.
    Barrilleaux B, Knoepfler PS (2011) Inducing iPSCs to escape the dish. Cell Stem Cell 9:103–111.  https://doi.org/10.1016/j.stem.2011.07.006 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Samuel R, Daheron L, Liao S et al (2013) Generation of functionally competent and durable engineered blood vessels from human induced pluripotent stem cells. Proc Natl Acad Sci USA 110:12774–12779.  https://doi.org/10.1073/pnas.1310675110 CrossRefPubMedGoogle Scholar
  72. 72.
    Kusuma S, Gerecht S (2016) Derivation of endothelial cells and pericytes from human pluripotent stem cells. Methods Mol Biol 1307:213–222.  https://doi.org/10.1007/7651_2014_149 CrossRefPubMedGoogle Scholar
  73. 73.
    Cleaver O, Melton DA (2003) Endothelial signaling during development. Nat Med 9:661–668.  https://doi.org/10.1038/nm0603-661 CrossRefPubMedGoogle Scholar
  74. 74.
    Cool J, DeFalco TJ, Capel B (2011) Vascular-mesenchymal cross-talk through Vegf and Pdgf drives organ patterning. Proc Natl Acad Sci USA 108:167–172.  https://doi.org/10.1073/pnas.1010299108 CrossRefPubMedGoogle Scholar
  75. 75.
    Lammert E, Cleaver O, Melton D (2001) Induction of pancreatic differentiation by signals from blood vessels. Science 294:564–567.  https://doi.org/10.1126/science.1064344 CrossRefPubMedGoogle Scholar
  76. 76.
    Matsumoto K, Yoshitomi H, Rossant J, Zaret KS (2001) Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294:559–563.  https://doi.org/10.1126/science.1063889 CrossRefPubMedGoogle Scholar
  77. 77.
    Nolan DJ, Ginsberg M, Israely E et al (2013) Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell 26:204–219.  https://doi.org/10.1016/j.devcel.2013.06.017 CrossRefPubMedGoogle Scholar
  78. 78.
    White MP, Rufaihah AJ, Liu L et al (2013) Limited gene expression variation in human embryonic stem cell and induced pluripotent stem cell-derived endothelial cells. Stem Cells 31:92–103.  https://doi.org/10.1002/stem.1267 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Reed DM, Foldes G, Kirkby NS et al (2014) Morphology and vasoactive hormone profiles from endothelial cells derived from stem cells of different sources. Biochem Biophys Res Commun 455:172–177.  https://doi.org/10.1016/j.bbrc.2014.10.140 CrossRefPubMedGoogle Scholar
  80. 80.
    Yoder M (2015) Differentiation of pluripotent stem cells into endothelial cells. Curr Opin Hematol 22:252–257.  https://doi.org/10.1097/MOH.0000000000000140 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Lippmann ES, Azarin SM, Kay JE et al (2012) Derivation of blood–brain barrier endothelial cells from human pluripotent stem cells. Nat Biotechnol 30:783–791.  https://doi.org/10.1038/nbt.2247 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Stevens KR, Murry CE (2018) Human pluripotent stem cell-derived engineered tissues: clinical considerations. Cell Stem Cell 22:294–297.  https://doi.org/10.1016/j.stem.2018.01.015 CrossRefPubMedGoogle Scholar
  83. 83.
    Jain RK (2003) Molecular regulation of vessel maturation. Nat Med 9:685–693.  https://doi.org/10.1038/nm0603-685 CrossRefPubMedGoogle Scholar
  84. 84.
    Darland DC, D’Amore P (1999) Blood vessel maturation: vascular development comes of age. J Clin Investig 103:157–158.  https://doi.org/10.1172/JCI6127 CrossRefPubMedGoogle Scholar
  85. 85.
    Folkman MJ, D’Amore P (1996) Blood vessel formation: what is its molecular basis? Cell 87:1153–1155CrossRefGoogle Scholar
  86. 86.
    Hellström M, Kalén M, Lindahl P et al (1999) Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126:3047–3055PubMedGoogle Scholar
  87. 87.
    Armulik A, Abramsson A, Betsholtz C (2005) Endothelial/pericyte interactions. Circ Res 97:512–523.  https://doi.org/10.1161/01.RES.0000182903.16652.d7 CrossRefPubMedGoogle Scholar
  88. 88.
    Shepherd BR, Jay SM, Saltzman WM et al (2009) Human aortic smooth muscle cells promote arteriole formation by coengrafted endothelial cells. Tissue Eng Part A 15:165–173.  https://doi.org/10.1089/ten.tea.2008.0010 CrossRefPubMedGoogle Scholar
  89. 89.
    Maier CL, Shepherd BR, Yi T, Pober JS (2010) Explant outgrowth, propagation and characterization of human pericytes. Microcirculation 17:367–380.  https://doi.org/10.1111/j.1549-8719.2010.00038.x CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Lynch MD, Watt FM (2018) Fibroblast heterogeneity: implications for human disease. J Clin Investig 128:26–35.  https://doi.org/10.1172/JCI93555 CrossRefPubMedGoogle Scholar
  91. 91.
    Sato G (2008) Tissue culture: the unrealized potential. Cytotechnology 57:111–114.  https://doi.org/10.1007/s10616-007-9109-9 CrossRefPubMedGoogle Scholar
  92. 92.
    Wilmut I (2007) The first direct reprogramming of adult human fibroblasts. Cell Stem Cell 1:593–594.  https://doi.org/10.1016/j.stem.2007.11.013 CrossRefPubMedGoogle Scholar
  93. 93.
    Shandalov Y, Egozi D, Koffler J et al (2014) An engineered muscle flap for reconstruction of large soft tissue defects. Proc Natl Acad Sci USA 111:6010–6015.  https://doi.org/10.1073/pnas.1402679111 CrossRefPubMedGoogle Scholar
  94. 94.
    Tonello C, Vindigni V, Zavan B et al (2005) In vitro reconstruction of an endothelialized skin substitute provided with a microcapillary network using biopolymer scaffolds. FASEB J 19:1546–1548.  https://doi.org/10.1096/fj.05-3804fje CrossRefPubMedGoogle Scholar
  95. 95.
    Hendrickx B, Verdonck K, Van den Berge S et al (2010) Integration of blood outgrowth endothelial cells in dermal fibroblast sheets promotes full thickness wound healing. Stem Cells 28:1165–1177.  https://doi.org/10.1002/stem.445 CrossRefPubMedGoogle Scholar
  96. 96.
    Sorrell JM, Caplan AI (2004) Fibroblast heterogeneity: more than skin deep. J Cell Sci 117:667–675.  https://doi.org/10.1242/jcs.01005 CrossRefPubMedGoogle Scholar
  97. 97.
    Driskell RR, Watt FM (2015) Understanding fibroblast heterogeneity in the skin. Trends Cell Biol 25:92–99.  https://doi.org/10.1016/j.tcb.2014.10.001 CrossRefPubMedGoogle Scholar
  98. 98.
    Driskell RR, Lichtenberger BM, Hoste E et al (2013) Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature 504:277–281.  https://doi.org/10.1038/nature12783 CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Alt E, Yan Y, Gehmert S et al (2011) Fibroblasts share mesenchymal phenotypes with stem cells, but lack their differentiation and colony-forming potential. Biol Cell 103:197–208.  https://doi.org/10.1042/BC20100117 CrossRefPubMedGoogle Scholar
  100. 100.
    Denu RA, Nemcek S, Bloom DD et al (2016) Fibroblasts and mesenchymal stromal/stem cells are phenotypically indistinguishable. Acta Haematol 136:85–97.  https://doi.org/10.1159/000445096 CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Ankrum JA, Ong JF, Karp JM (2014) Mesenchymal stem cells: immune evasive, not immune privileged: PubMed—NCBI. Nat Biotechnol 32:252–260.  https://doi.org/10.1038/nbt.2816 CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147CrossRefGoogle Scholar
  103. 103.
    Ankrum J, Karp JM (2010) Mesenchymal stem cell therapy: two steps forward, one step back. Trends Mol Med 16:203–209.  https://doi.org/10.1016/j.molmed.2010.02.005 CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Dominici M, Le Blanc K, Mueller I et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8:315–317.  https://doi.org/10.1080/14653240600855905 CrossRefGoogle Scholar
  105. 105.
    Karp JM, Leng Teo GS (2009) Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4:206–216.  https://doi.org/10.1016/j.stem.2009.02.001 CrossRefPubMedGoogle Scholar
  106. 106.
    Bianco P, Robey PG, Simmons PJ (2008) Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2:313–319.  https://doi.org/10.1016/j.stem.2008.03.002 CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Crisan M, Yap S, Casteilla L et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313.  https://doi.org/10.1016/j.stem.2008.07.003 CrossRefPubMedGoogle Scholar
  108. 108.
    Prockop DJ (2009) Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther 17:939–946.  https://doi.org/10.1038/mt.2009.62 CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Pill K, Hofmann S, Redl H, Holnthoner W (2015) Vascularization mediated by mesenchymal stem cells from bone marrow and adipose tissue: a comparison. Cell Regen (Lond) 4:8.  https://doi.org/10.1186/s13619-015-0025-8 CrossRefGoogle Scholar
  110. 110.
    Liang X, Ding Y, Zhang Y et al (2014) Paracrine mechanisms of mesenchymal stem cell-based therapy: current status and perspectives. Cell Transplant 23:1045–1059.  https://doi.org/10.3727/096368913X667709 CrossRefPubMedGoogle Scholar
  111. 111.
    Ranganath SH, Levy O, Inamdar MS, Karp JM (2012) Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 10:244–258.  https://doi.org/10.1016/j.stem.2012.02.005 CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Borges J, Mueller MC, Padron NT et al (2003) Engineered adipose tissue supplied by functional microvessels. Tissue Eng 9:1263–1270.  https://doi.org/10.1089/10763270360728170 CrossRefPubMedGoogle Scholar
  113. 113.
    Wenger A, Stahl A, Weber H et al (2004) Modulation of in vitro angiogenesis in a three-dimensional spheroidal coculture model for bone tissue engineering. Tissue Eng 10:1536–1547.  https://doi.org/10.1089/ten.2004.10.1536 CrossRefPubMedGoogle Scholar
  114. 114.
    Ghajar CM, Blevins KS, Hughes CCW et al (2006) Mesenchymal stem cells enhance angiogenesis in mechanically viable prevascularized tissues via early matrix metalloproteinase upregulation. Tissue Eng 12:2875–2888.  https://doi.org/10.1089/ten.2006.12.2875 CrossRefPubMedGoogle Scholar
  115. 115.
    Rohringer S, Hofbauer P, Schneider KH et al (2014) Mechanisms of vasculogenesis in 3D fibrin matrices mediated by the interaction of adipose-derived stem cells and endothelial cells. Angiogenesis 17:921–933.  https://doi.org/10.1007/s10456-014-9439-0 CrossRefPubMedGoogle Scholar
  116. 116.
    Ghanaati S, Fuchs S, Webber MJ et al (2011) Rapid vascularization of starch-poly(caprolactone) in vivo by outgrowth endothelial cells in co-culture with primary osteoblasts. J Tissue Eng Regen Med 5:e136–e143.  https://doi.org/10.1002/term.373 CrossRefPubMedGoogle Scholar
  117. 117.
    Holnthoner W, Hohenegger K, Husa A-M et al (2015) Adipose-derived stem cells induce vascular tube formation of outgrowth endothelial cells in a fibrin matrix. J Tissue Eng Regen Med 9:127–136.  https://doi.org/10.1002/term.1620 CrossRefPubMedGoogle Scholar
  118. 118.
    Crisan M, Corselli M, Chen WCW, Péault B (2012) Perivascular cells for regenerative medicine. J Cell Mol Med 16:2851–2860.  https://doi.org/10.1111/j.1582-4934.2012.01617.x CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Au P, Tam J, Fukumura D, Jain RK (2008) Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 111:4551–4558.  https://doi.org/10.1182/blood-2007-10-118273 CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Lin R-Z, Moreno-Luna R, Moreno-Luna R et al (2012) Equal modulation of endothelial cell function by four distinct tissue-specific mesenchymal stem cells. Angiogenesis 15:443–455.  https://doi.org/10.1007/s10456-012-9272-2 CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Lin R-Z, Moreno-Luna R, Li D et al (2014) Human endothelial colony-forming cells serve as trophic mediators for mesenchymal stem cell engraftment via paracrine signaling. Proc Natl Acad Sci USA 111:10137–10142.  https://doi.org/10.1073/pnas.1405388111 CrossRefPubMedGoogle Scholar
  122. 122.
    Xie C, Ritchie RP, Huang H et al (2011) Smooth muscle cell differentiation in vitro: models and underlying molecular mechanisms. Arterioscler Thromb Vasc Biol 31:1485–1494.  https://doi.org/10.1161/ATVBAHA.110.221101 CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    Kattman SJ, Huber TL, Keller GM (2006) Multipotent flk-1 + cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev Cell 11:723–732.  https://doi.org/10.1016/j.devcel.2006.10.002 CrossRefPubMedGoogle Scholar
  124. 124.
    Bajpai VK, Mistriotis P, Loh Y-H et al (2012) Functional vascular smooth muscle cells derived from human induced pluripotent stem cells via mesenchymal stem cell intermediates. Cardiovasc Res 96:391–400.  https://doi.org/10.1093/cvr/cvs253 CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Ferreira LS, Gerecht S, Shieh HF et al (2007) Vascular progenitor cells isolated from human embryonic stem cells give rise to endothelial and smooth muscle like cells and form vascular networks in vivo. Circ Res 101:286–294.  https://doi.org/10.1161/CIRCRESAHA.107.150201 CrossRefPubMedGoogle Scholar
  126. 126.
    Reznikoff CA, Bertram JS, Brankow DW, Heidelberger C (1973) Quantitative and qualitative studies of chemical transformation of cloned C3H mouse embryo cells sensitive to postconfluence inhibition of cell division. Can Res 33:3239–3249Google Scholar
  127. 127.
    Hirschi KK, Rohovsky SA, D’Amore P (1998) PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 141:805–814CrossRefGoogle Scholar
  128. 128.
    Hirschi KK, Rohovsky SA, Beck LH et al (1999) Endothelial cells modulate the proliferation of mural cell precursors via platelet-derived growth factor-BB and heterotypic cell contact. Circ Res 84:298–305CrossRefGoogle Scholar
  129. 129.
    Cheng G, Liao S, Wong HK et al (2011) Engineered blood vessel networks connect to host vasculature via wrapping-and-tapping anastomosis. Blood.  https://doi.org/10.1182/blood-2011-02-338426 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Cardiac SurgeryBoston Children’s HospitalBostonUSA
  2. 2.Department of SurgeryHarvard Medical SchoolBostonUSA
  3. 3.Harvard Stem Cell InstituteCambridgeUSA

Personalised recommendations