CoChat
Sign Up
Cited by 476Tissue Engineering and Regenerative Medicine3D Printing in Biomedical ResearchElectrospun Nanofibers in Biomedical Applications

Vascular Tissue Engineering: Progress, Challenges, and Clinical Promise

Open access
Song, H.-H. Greco, Rumma, Rowza T., Ozaki, C. Keith, Edelman, Elazer R., Chen, Christopher S.·2018·Cell Stem Cell
DOI 10.1016/j.stem.2018.02.009PMC PMC5849079
Open this paper in CoChat — free accountOpen PDF

Abstract

Although the clinical demand for bioengineered blood vessels continues to rise, current options for vascular conduits remain limited. The synergistic combination of emerging advances in tissue fabrication and stem cell engineering promises new strategies for engineering autologous blood vessels that recapitulate not only the mechanical properties of native vessels but also their biological function. Here we explore recent bioengineering advances in creating functional blood macro and microvessels, particularly featuring stem cells as a seed source. We also highlight progress in integrating engineered vascular tissues with the host after implantation as well as the exciting pre-clinical and clinical applications of this technology.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.stem.2018.02.009

Cites

10 of 10 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • iPSC-ECs have been produced from different cell sources by multiple methods with superior proliferative capacity.

    “iPSC-ECs have been produced from different cell sources by multiple methods with superior proliferative capacity [236].”

    From Liver tissue engineering using decellularized scaffolds: Current progress, challenges, and opportunities (2024) · cites this paper as [236]

    The Stem Cells as Seed Sources section describes iPSC-derived ECs and says that iPSCs have superior proliferative capacity in vitro. The Microvessels sections describe iPSC-ECs from diabetic patients and healthy donors and different approaches to generating them. But the proliferation finding concerns iPSCs, not specifically the differentiated iPSC-ECs named in the claim; no page numbers are available in our copy. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Endothelial cells have limited application due to donor variability, technical challenges of isolation, limited proliferative capacity, senescence, and heterogeneity.

    “However, their application is limited due to the donor variability, technical challenges of isolation, limited proliferative capacity, senescence, and heterogeneity [235,236].”

    From Liver tissue engineering using decellularized scaffolds: Current progress, challenges, and opportunities (2024) · cites this paper as [236]

    In “Stem Cells as Seed Sources” (page unavailable), the paper identifies harvesting challenges and reduced proliferative capacity for primary autologous vascular cells, a category that includes endothelial cells; it also discusses senescence as a possible explanation. “Future Directions” describes endothelial-cell heterogeneity as a challenge for engineering organ-specific cells. The copy does not establish donor variability as a limitation, and not all the listed limitations are stated specifically for endothelial cells. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 165

  1. Abaci HE Guo Z Coffman A Gillette B Lee WH Sia SK Christiano AM 2016 Human Skin Constructs with Spatially Controlled Vasculature Using Primary and iPSC-Derived Endothelial Cells Adv Healthc Mater 5 1800 1807 27333469 PMC5031081
  2. Adams WJ Zhang Y Cloutier J Kuchimanchi P Newton G Sehrawat S Aird WC Mayadas TN Luscinskas FW García-Cardeña G 2013 Functional Vascular Endothelium Derived from Human Induced Pluripotent Stem Cells Stem Cell Reports 1 105 113 24052946 PMC3757754
  3. Akoh JA Patel N 2010 Infection of hemodialysis arteriovenous grafts J Vasc Access 11 155 158 20175060
  4. Alimperti S Mirabella T Bajaj V Polacheck W Pirone DM Duffield J Eyckmans J Assoian RK Chen CS 2017 Three-dimensional biomimetic vascular model reveals a RhoA, Rac1, and N -cadherin balance in mural cell–endothelial cell-regulated barrier function Proc Natl Acad Sci 114 201618333 PMC5565405 28765370
  5. Ayala P Dai E Hawes M Liu L Chaudhuri O Haller CA Mooney DJ Chaikof EL 2017 Evaluation of a bioengineered construct for tissue engineering applications J Biomed Mater Res Part B Appl Biomater 1 10 29130596
  6. Baltzis D Eleftheriadou I Veves A 2014 Pathogenesis and Treatment of Impaired Wound Healing in Diabetes Mellitus: New Insights Adv Ther 31 817 836 25069580
  7. Baranski JD Chaturvedi RR Stevens KR Eyckmans J Carvalho B Solorzano RD Yang MT Miller JS Bhatia SN Chen CS 2013 Geometric control of vascular networks to enhance engineered tissue integration and function Proc Natl Acad Sci U S A 110 7586 7591 23610423 PMC3651499
  8. Bekhite MM Finkensieper A Rebhan J Huse S Schultze-Mosgau S Figulla HR Sauer H Wartenberg M 2014 Hypoxia, Leptin, and Vascular Endothelial Growth Factor Stimulate Vascular Endothelial Cell Differentiation of Human Adipose Tissue-Derived Stem Cells Stem Cells Dev 23 333 351 24134622
  9. Benrashid E MC C Youngwirth LM Kim J Manson RJ Otto JC Lawson JH 2016 Tissue engineered vascular grafts: Origins, development, and current strategies for clinical application Methods 99 13 19 26216054
  10. Bowers SLK Meng CX Davis MT Davis GE 2014 Investigating Human Vascular Tube Morphogenesis and Maturation Using Endothelial Cell-Pericyte Co-cultures and a Doxycycline-Inducible Genetic System in 3D Extracellular Matrices Tissue Morphogenesis New York, NY Springer New York 171 189 25245694
  11. Brem H Tomic-Canic M 2007 Cellular and molecular basis of wound healing in diabetes J Clin Invest 117 1219 1222 17476353 PMC1857239
  12. Brown TE Marozas IA Anseth KS 2017 Amplified Photodegradation of Cell-Laden Hydrogels via an Addition–Fragmentation Chain Transfer Reaction Adv Mater 29 1605001 PMC5489340 28112845
  13. Burdick JA Prestwich GD 2011 Hyaluronic Acid Hydrogels for Biomedical Applications Adv Mater 23 H41 H56 21394792 PMC3730855
  14. Camp JG Sekine K Gerber T Loeffler-Wirth H Binder H Gac M Kanton S Kageyama J Damm G Seehofer D 2017 Multilineage communication regulates human liver bud development from pluripotency Nature 546 533 538 28614297
  15. Canver CC 1995 Conduit options in coronary artery bypass surgery Chest 108 1150 1155 7555129
  16. Ceccarelli J Putnam AJ 2014 Sculpting the blank slate: How fibrin’s support of vascularization can inspire biomaterial design Acta Biomater 10 1515 1523 23933102 PMC3864148
  17. Chan XY Black R Dickerman K Federico J Lévesque M Mumm J Gerecht S 2015 Three-Dimensional Vascular Network Assembly From Diabetic Patient-Derived Induced Pluripotent Stem CellsSignificance Arterioscler Thromb Vasc Biol 35 2677 2685 26449749 PMC4603427
  18. Chan XY Elliott MB Macklin B Gerecht S 2017 Human Pluripotent Stem Cells to Engineer Blood Vessels Advances in Biochemical Engineering/Biotechnology 1 22 29090328
  19. Chang WG Niklason LE 2017 A short discourse on vascular tissue engineering NPJ Regen Med 2 PMC5649630 29057097
  20. Chard RB Johnson DC Nunn GR Cartmill TB 1987 Aorta-coronary bypass grafting with polytetrafluoroethylene conduits. Early and late outcome in eight patients J Thorac Cardiovasc Surg 94 132 134 3496497
  21. Chaturvedi RR Stevens KR Solorzano RD Schwartz RE Eyckmans J Baranski JD Stapleton SC Bhatia SN Chen CS 2015 Patterning Vascular Networks In Vivo for Tissue Engineering Applications Tissue Eng Part C Methods 21 509 517 25390971 PMC4410304
  22. Chen X Aledia AS Ghajar CM Griffith CK Putnam AJ Hughes CCW George SC 2009 Prevascularization of a Fibrin-Based Tissue Construct Accelerates the Formation of Functional Anastomosis with Host Vasculature Tissue Eng Part A 15 1363 1371 18976155 PMC2792096
  23. Chen X Aledia AS Popson SA Him L Hughes CCW George SC 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 19737050 PMC2813071
  24. Cheng G Liao S Wong HK Lacorre DA Di Tomaso E Au P Fukumura D Jain RK Munn LL 2011 Engineered blood vessel networks connect to host vasculature via wrapping-and-tapping anastomosis Blood 118 4740 4749 21835951 PMC3208287
  25. Corovic S Markelc B Dolinar M Cemazar M Jarm T 2015 Modeling of microvascular permeability changes after electroporation PLoS One 10 1 16 PMC4368817 25793292
  26. Cuchiara MP Gould DJ McHale MK Dickinson ME West JL 2012 Integration of Self-Assembled Microvascular Networks with Microfabricated PEG-Based Hydrogels Adv Funct Mater 22 4511 4518 23536744 PMC3607213
  27. Cukierman E Pankov R Stevens DR Yamada KM 2001 Taking Cell-Matrix Adhesions to the Third Dimension Science (80-) 294 1708 1712 11721053
  28. Davis GE Camarillo CW 1996 An alpha 2 beta 1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix Exp Cell Res 224 39 51 8612690
  29. Davis GE Speichinger KR Norden PR Kim DJ Bowers SLK 2015 Endothelial cell polarization during lumen formation, tubulogenesis, and vessel maturation in 3D extracellular matrices Cell Polarity 1: Biological Role and Basic Mechanisms Cham Springer International Publishing 205 220
  30. DeBakey ME Crawford ES Garrett HE Beall AC Jr Howell JF 1965 Surgical considerations in the treatment of aneurysms of the thoraco-abdominal aorta Ann Surg 162 650 662 5833590 PMC1476956
  31. Delgado LM Fuller K Zeugolis DI 2017 Collagen Cross-Linking: Biophysical, Biochemical, and Biological Response Analysis Tissue Eng Part A 23 ten.tea.2016.0415 28071973
  32. Dimitrievska S Niklason LE 2017 Historical Perspective and Future Direction of Blood Vessel Developments Cold Spring Harb Perspect Med a025742 PMC5685928 28348177
  33. Doyle AD Carvajal N Jin A Matsumoto K Yamada KM 2015 Local 3D matrix microenvironment regulates cell migration through spatiotemporal dynamics of contractility-dependent adhesions Nat Commun 6 8720 26548801 PMC4643399
  34. Eoh JH Shen N Burke JA Hinderer S Xia Z Schenke-Layland K Gerecht S 2017 Enhanced elastin synthesis and maturation in human vascular smooth muscle tissue derived from induced-pluripotent stem cells Acta Biomater 52 49 59 28163239
  35. Fantin A Vieira JM Gestri G Denti L Schwarz Q Prykhozhij S Peri F Wilson SW Ruhrberg C 2010 Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction Blood 116 829 840 20404134 PMC2938310
  36. Franco CA Jones ML Bernabeu MO Geudens I Mathivet T Rosa A Lopes FM Lima AP Ragab A Collins RT 2015 Dynamic Endothelial Cell Rearrangements Drive Developmental Vessel Regression PLOS Biol 13 e1002125 25884288 PMC4401640
  37. Galie PA Nguyen DHT Choi CK Cohen DM Janmey PA Chen CS 2014 Fluid shear stress threshold regulates angiogenic sprouting Proc Natl Acad Sci U S A 111 7968 7973 24843171 PMC4050561
  38. Galili U 2005 The alpha-gal epitope and the anti-Gal antibody in xenotransplantation and in cancer immunotherapy Immunol Cell Biol 83 674 686 16266320
  39. GBD 2015 Mortality and Causes of Death Collaborators, G. 2015 M. and C. of D 2016 Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015 Lancet London, England 388 1459 1544 27733281 PMC5388903
  40. Gebala V Collins R Geudens I Phng LK Gerhardt H 2016 Blood flow drives lumen formation by inverse membrane blebbing during angiogenesis in vivo Nat Cell Biol 18 443 450 26928868 PMC6485462
  41. Géraud C Koch PS Zierow J Klapproth K Busch K Olsavszky V Leibing T Demory A Ulbrich F Diett M 2017 GATA4-dependent organ-specific endothelial differentiation controls liver development and embryonic hematopoiesis J Clin Invest 127 1099 1114 28218627 PMC5330741
  42. Gerri C Marín-Juez R Marass M Marks A Maischein HM Stainier DYR 2017 Hif-1α regulates macrophage-endothelial interactions during blood vessel development in zebrafish Nat Commun 8 15492 28524872 PMC5493593
  43. Godbey WT Hindy BSS Sherman ME Atala A 2004 A novel use of centrifugal force for cell seeding into porous scaffolds Biomaterials 25 2799 2805 14962558
  44. Gui L Dash BC Luo J Qin L Zhao L Yamamoto K Hashimoto T Wu H Dardik A Tellides G 2016 Implantable tissue-engineered blood vessels from human induced pluripotent stem cells Biomaterials 102 120 129 27336184 PMC4939127
  45. Hanjaya-Putra D Wong KT Hirotsu K Khetan S Burdick JA Gerecht S 2012 Spatial control of cell-mediated degradation to regulate vasculogenesis and angiogenesis in hyaluronan hydrogels Biomaterials 33 6123 6131 22672833 PMC3481551
  46. Haskal ZJ Trerotola S Dolmatch B Schuman E Altman S Mietling S Berman S McLennan G Trimmer C Ross J 2010 Stent Graft versus Balloon Angioplasty for Failing Dialysis-Access Grafts N Engl J Med 362 494 503 20147715
  47. Heintz KA Bregenzer ME Mantle JL Lee KH West JL Slater JH 2016 Fabrication of 3D Biomimetic Microfluidic Networks in Hydrogels Adv Healthc Mater 5 2153 2160 27239785 PMC5014628
  48. Herbert SP Stainier DYR 2011 Molecular control of endothelial cell behaviour during blood vessel morphogenesis Nat Rev Mol Cell Biol 12 551 564 21860391 PMC3319719
  49. Herring M Gardner A Glover J 1979 Seeding Endothelium Onto Canine Arterial Prostheses: The Effects of Graft Design Arch Surg 114 679 682 156532
  50. Hibino N McGillicuddy E Matsumura G Ichihara Y Naito Y Breuer C Shinoka T 2010 Late-term results of tissue-engineered vascular grafts in humans J Thorac Cardiovasc Surg 139 431 436 436 2 20106404
  51. Hill KL Obrtlikova P Alvarez DF King JA Keirstead SA Allred JR Kaufman DS 2010 Human embryonic stem cell-derived vascular progenitor cells capable of endothelial and smooth muscle cell function Exp Hematol 38 246 257.e1 20067819 PMC2838385
  52. Hong CC Kume T Peterson RT 2008 Role of crosstalk between phosphatidylinositol 3-kinase and extracellular signal-regulated kinase/mitogen-activated protein kinase pathways in artery-vein specification Circ Res 103 573 579 18796644 PMC2768581
  53. Huang AH Niklason LE 2014 Engineering of arteries in vitro Cell Mol Life Sci 71 2103 2118 24399290 PMC4024341
  54. Huber TS Carter JW Carter RL Seeger JM 2003 Patency of autogenous and polytetrafluoroethylene upper extremity arteriovenous hemodialysis accesses: a systematic review J Vasc Surg 38 1005 1011 14603208
  55. Isner JM Asahara T 1999 Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization J Clin Invest 103 1231 1236 10225965 PMC408362
  56. Jeon JS Bersini S Whisler JA Chen MB Dubini G Charest JL Moretti M Kamm RD 2014 Generation of 3D functional microvascular networks with human mesenchymal stem cells in microfluidic systems Integr Biol 6 555 563 PMC4307755 24676392
  57. Johnson DJ Robson P Hew Y Keeley FW 1995 Decreased elastin synthesis in normal development and in long-term aortic organ and cell cultures is related to rapid and selective destabilization of mRNA for elastin Circ Res 77 1107 1113 7586222
  58. Kang H Liu J Sun A Liu X Fan Y Deng X 2017 Vascular smooth muscle cell glycocalyx mediates shear stress-induced contractile responses via a Rho kinase (ROCK)-myosin light chain phosphatase (MLCP) pathway Sci Rep 7 42092 28191820 PMC5304191
  59. Kassab GS 2006 Scaling laws of vascular trees: of form and function Am J Physiol Heart Circ Physiol 290 H894 903 16143652
  60. Klar AS Güven S Biedermann T Luginbühl J Böttcher-Haberzeth S Meuli-Simmen C Meuli M Martin I Scherberich A Reichmann E 2014 Tissue-engineered dermoepidermal skin grafts prevascularized with adipose-derived cells Biomaterials 35 5065 5078 24680190
  61. Klinger RY Blum JL Hearn B Lebow B Niklason LE 2006 Relevance and safety of telomerase for human tissue engineering Proc Natl Acad Sci 103 2500 2505 16477025 PMC1413782
  62. Koike N Fukumura D Gralla O Au P Schechner JS Jain RK 2004 Tissue engineering: Creation of long-lasting blood vessels Nature 428 138 139 15014486
  63. Kolesky DB Truby RL Gladman AS Busbee TA Homan KA Lewis JA 2014 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs Adv Mater 26 3124 3130 24550124
  64. Kolesky DB Homan KA Skylar-Scott MA Lewis JA 2016 Three-dimensional bioprinting of thick vascularized tissues Proc Natl Acad Sci 113 3179 3184 26951646 PMC4812707
  65. Konig G McAllister TN Dusserre N Garrido SA Iyican C Marini A Fiorillo A Avila H Wystrychowski W Zagalski K 2009 Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery Biomaterials 30 1542 1550 19111338 PMC2758094
  66. Krock BL Skuli N Simon MC 2011 Hypoxia-Induced Angiogenesis: Good and Evil Genes Cancer 2 1117 1133 22866203 PMC3411127
  67. Krug A de Rochemont Du Mesnil Korb G 1966 Blood supply of the myocardium after temporary coronary occlusion Circ Res 19 57 62 5912914
  68. Kubota Y Kleinman HK Martin GR Lawley TJ 1988 Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures J Cell Biol 107 1589 1598 3049626 PMC2115245
  69. Kusuma S Shen YI Hanjaya-Putra D Mali P Cheng L Gerecht S 2013 Self-organized vascular networks from human pluripotent stem cells in a synthetic matrix Proc Natl Acad Sci 110 12601 12606 23858432 PMC3732921
  70. Kusuma S Peijnenburg E Patel P Gerecht S 2014 Low oxygen tension enhances endothelial fate of human pluripotent stem cells Arterioscler Thromb Vasc Biol 34 913 920 24526696 PMC3978126
  71. Kutys ML Doyle AD Yamada KM 2013 Regulation of cell adhesion and migration by cell-derived matrices Exp Cell Res 319 2434 2439 23751565 PMC3780580
  72. L’Heureux N Pâquet S Labbé R Germain L Auger FA 1998 A completely biological tissue-engineered human blood vessel FASEB J 12 47 56 9438410
  73. L’Heureux N Dusserre N Konig G Victor B Keire P Wight TN Chronos NAF Kyles AE Gregory CR Hoyt G 2006 Human tissue-engineered blood vessels for adult arterial revascularization Nat Med 12 361 365 16491087 PMC1513140
  74. Lawson JH Glickman MH Ilzecki M Jakimowicz T Jaroszynski A Peden EK Pilgrim AJ Prichard HL Guziewicz M Przywara S 2016 Bioengineered human acellular vessels for dialysis access in patients with end-stage renal disease: two phase 2 single-arm trials Lancet (London, England) 387 2026 2034 PMC4915925 27203778
  75. Lenard A Ellertsdottir E Herwig L Krudewig A Sauteur L Belting HG Affolter M 2013 In vivo analysis reveals a highly stereotypic morphogenetic pathway of vascular anastomosis Dev Cell 25 492 506 23763948
  76. Levenberg S Golub JS Amit M Itskovitz-Eldor J Langer R 2002 Endothelial cells derived from human embryonic stem cells Proc Natl Acad Sci U S A 99 4391 4396 11917100 PMC123658
  77. 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 23 879 884 15965465
  78. Li S Nih LR Bachman H Fei P Li Y Nam E Dimatteo R Carmichael ST Barker TH Segura T 2017 Hydrogels with precisely controlled integrin activation dictate vascular patterning and permeability Nat Mater 16 953 961 28783156 PMC5809173
  79. Lin SL Kisseleva T Brenner DA Duffield JS 2008 Pericytes and Perivascular Fibroblasts Are the Primary Source of Collagen-Producing Cells in Obstructive Fibrosis of the Kidney Am J Pathol 173 1617 1627 19008372 PMC2626374
  80. Lok CE Sontrop JM Tomlinson G Rajan D Cattral M Oreopoulos G Harris J Moist L 2013 Cumulative patency of contemporary fistulas versus grafts (2000–2010) Clin J Am Soc Nephrol 8 810 818 23371955 PMC3641610
  81. Lucitti JL Jones EAV Huang C Chen J Fraser SE Dickinson ME 2007 Vascular remodeling of the mouse yolk sac requires hemodynamic force Development 134 3317 3326 17720695 PMC4260474
  82. Makris EA Responte DJ Paschos NK Hu JC Athanasiou KA 2014 Developing functional musculoskeletal tissues through hypoxia and lysyl oxidase-induced collagen cross-linking Proc Natl Acad Sci 111 E4832 E4841 25349395 PMC4234579
  83. McAllister TN Maruszewski M Garrido SA Wystrychowski W Dusserre N Marini A Zagalski K Fiorillo A Avila H Manglano X 2009 Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: a multicentre cohort study Lancet 373 1440 1446 19394535
  84. McIlhenny S Zhang P Tulenko T Comeau J Fernandez S Policha A Ferroni M Faul E Bagameri G Shapiro I 2015 eNOS transfection of adipose-derived stem cells yields bioactive nitric oxide production and improved results in vascular tissue engineering J Tissue Eng Regen Med 9 1277 1285 23319464 PMC4050122
  85. Miller JS Stevens KR Yang MT Baker BM Nguyen DHT Cohen DM Toro E Chen AA Galie PA Yu X 2012 Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues Nat Mater 11 768 774 22751181 PMC3586565
  86. Mirabella T MacArthur JW Cheng D Ozaki CK Woo YJ Yang MT Chen CS 2017 3D-printed vascular networks direct therapeutic angiogenesis in ischaemia Nat Biomed Eng 1 83 PMC5837070 29515935
  87. Miranda-Nieves D Chaikof EL 2017 Collagen and Elastin Biomaterials for the Fabrication of Engineered Living Tissues ACS Biomater Sci Eng 3 694 711 33440491
  88. Mironov V Visconti RP Kasyanov V Forgacs G Drake CJ Markwald RR 2009 Organ printing: Tissue spheroids as building blocks Biomaterials 30 2164 2174 19176247 PMC3773699
  89. Morgan JP Delnero PF Zheng Y Verbridge SS Chen J Craven M Choi NW Diaz-Santana A Kermani P Hempstead B 2013 Formation of microvascular networks in vitro Nat Protoc 8 1820 1836 23989676
  90. Moya ML Hsu YH Lee AP Hughes CCW George SC 2013 In Vitro Perfused Human Capillary Networks Dx.doi.org PMC3719485 23320912
  91. Mozaffarian D Benjamin EJ Go AS Arnett DK Blaha MJ Cushman M Das SR de Ferranti S Després JP Fullerton HJ 2016 Executive Summary: Heart Disease and Stroke Statistics—2016 Update Circulation 133 447 454 26811276
  92. Murray CD 1926 The Physiological Principle of Minimum Work: I. The Vascular System and the Cost of Blood Volume Proc Natl Acad Sci U S A 12 207 214 16576980 PMC1084489
  93. Nesmith JE Chappell JC Cluceru JG Bautch VL 2017 Blood vessel anastomosis is spatially regulated by Flt1 during angiogenesis Development 144 889 896 28246215 PMC5374355
  94. Nguyen DHT Stapleton SC Yang MT Cha SS Choi CK Galie PA Chen CS 2013 Biomimetic model to reconstitute angiogenic sprouting morphogenesis in vitro Proc Natl Acad Sci U S A 110 6712 6717 23569284 PMC3637738
  95. Nieponice A Soletti L Guan J Deasy BM Huard J Wagner WR Vorp DA 2008 Rotational Vacuum Seeding Technique Glass 29 825 833 PMC2354918 18035412
  96. Niklason LE Gao J Abbott WM Hirschi KK Houser S Marini R Langer R 1999 Functional Arteries Grown in Vitro Science (80-) 284 489 493 10205057
  97. Niu D Wei HJ Lin L George H Wang T Lee IH Zhao HY Wang Y Kan Y Shrock E 2017 Inactivation of porcine endogenous retrovirus in pigs using CRISPR-Cas9 Science (80-) 357 eaan4187 PMC5813284 28798043
  98. Noishiki Y Yamane Y Tomizawa Y Okoshi T Satoh S Wildevuur CR 1990 Endothelialization of vascular prostheses by transplantation of venous tissue fragments ASAIO Trans 36 M346 8 2252695
  99. Norotte C Marga FS Niklason LE Forgacs G 2009 Scaffold-free vascular tissue engineering using bioprinting Biomaterials 30 5910 5917 19664819 PMC2748110
  100. Nugent HM Edelman ER 2003 Tissue engineering therapy for cardiovascular disease Circ Res 92 1068 1078 12775655
  101. Ong L Li W Oldigs JK Kaminski A Gerstmayer B Piechaczek C Wagner W Li R Ma N Steinhoff G 2010 Hypoxic/Normoxic Preconditioning Increases Endothelial Differentiation Potential of Human Bone Marrow CD133+ Cells Tissue Eng Part C Methods 16 1069 1081 20073989
  102. Park KM Gerecht S 2014 Hypoxia-inducible hydrogels Nat Commun 5 PMC4161608 24909742
  103. Patience C Takeuchi Y Weiss RA 1997 Infection of human cells by an endogenous retrovirus of pigs Nat Med 3 282 286 9055854
  104. Pawlowski KJ Rittgers SE Schmidt SP Bowlin GL 2004 Endothelial cell seeding of polymeric vascular grafts Front Biosci 9 1412 1421 14977556
  105. Poh M Boyer M Solan A Dahl SL Pedrotty D Banik SS McKee JA Klinger RY Counter CM Niklason LE 2005 Blood vessels engineered from human cells Lancet 365 2122 2124 15964449
  106. Polacheck WJ Kutys ML Yang J Eyckmans J Wu Y Vasavada H Hirschi KK Chen CS 2017 A non-canonical Notch complex regulates adherens junctions and vascular barrier function Nature 552 258 262 29160307 PMC5730479
  107. Potente M Mäkinen T 2017 Vascular heterogeneity and specialization in development and disease Nat Rev Mol Cell Biol 18 477 494 28537573
  108. Potente M Gerhardt H Carmeliet P 2011 Basic and therapeutic aspects of angiogenesis Cell 146 873 887 21925313
  109. Prado-Lopez S Conesa A Armminan A Marti-nez-Losa M Escobedo-Lucea C Gandia C Tarazona S Melguizo D Blesa D Montaner D 2009 Hypoxia Promotes Efficient Differentiation of Human Embryonic Stem Cells to Functional Endothelium Stem Cells 28 N/A-N/A 20049902
  110. Rabkin E Schoen FJ 2002 Cardiovascular tissue engineering Cardiovasc Pathol 11 305 317 12459430
  111. Randeria PS Seeger MA Wang XQ Wilson H Shipp D Mirkin CA Paller AS 2015 siRNA-based spherical nucleic acids reverse impaired wound healing in diabetic mice by ganglioside GM3 synthase knockdown Proc Natl Acad Sci 112 5573 5578 25902507 PMC4426446
  112. Ratz PH Ratz HP 2015 Mechanics of Vascular Smooth Muscle Comprehensive Physiology Hoboken, NJ, USA John Wiley & Sons, Inc. 111 168 26756629
  113. Ravi S Qu Z Chaikof EL 2009 Polymeric Materials for Tissue Engineering of Arterial Substitutes Vascular 17 S45 S54 19426609 PMC2714487
  114. Roh JD Sawh-Martinez R Brennan MP Jay SM Devine L Rao DA Yi T Mirensky TL Nalbandian A Udelsman B 2010 Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling Proc Natl Acad Sci 107 4669 4674 20207947 PMC2842056
  115. Roosens A Somers P De Somer F Carriel V Van Nooten G Cornelissen R 2016 Impact of Detergent-Based Decellularization Methods on Porcine Tissues for Heart Valve Engineering Ann Biomed Eng 44 2827 2839 26842626
  116. Sagnella S Anderson E Sanabria N Marchant RE Kottke-Marchant K 2005 Human endothelial cell interaction with biomimetic surfactant polymers containing Peptide ligands from the heparin binding domain of fibronectin Tissue Eng 11 226 236 15738677 PMC1236992
  117. Sakaguchi K Shimizu T Horaguchi S Sekine H Yamato M Umezu M Okano T 2013 In Vitro Engineering of Vascularized Tissue Surrogates Sci Rep 3 1316 23419835 PMC3575583
  118. Salacinski HJ Tiwari A Hamilton G Seifalian AM 2001 Cellular engineering of vascular bypass grafts: role of chemical coatings for enhancing endothelial cell attachment Med Biol Eng Comput 39 609 618 11804165
  119. Samuel R Daheron L Liao S Vardam T Kamoun WS Batista A Buecker C Schäfer R Han X Au P 2013 Generation of functionally competent and durable engineered blood vessels from human induced pluripotent stem cells Proc Natl Acad Sci U S A 110 12774 12779 23861493 PMC3732948
  120. Samuel R Duda DG Fukumura D Jain RK 2015 Vascular diseases await translation of blood vessels engineered from stem cells Sci Transl Med 7 309rv6 PMC4799660 26468328
  121. Sapoznik E Niu G Nomi M Wang Z Soker S 2015 Regeneration of the Vascular System In Translational Regenerative Medicine Elsevier 357 373
  122. Saunders WB Bohnsack BL Faske JB Anthis NJ Bayless KJ Hirschi KK Davis GE 2006 Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3 J Cell Biol 175 179 191 17030988 PMC2064509
  123. Sauteur L Krudewig A Herwig L Ehrenfeuchter N Lenard A Affolter M Belting HG 2014 Cdh5/VE-cadherin Promotes Endothelial Cell Interface Elongation via Cortical Actin Polymerization during Angiogenic Sprouting Cell Rep 9 504 513 25373898
  124. Seifu DG Purnama A Mequanint K Mantovani D 2013 Small-diameter vascular tissue engineering Nat Rev Cardiol 10 410 421 23689702
  125. Sekine H Shimizu T Sakaguchi K Dobashi I Wada M Yamato M Kobayashi E Umezu M Okano T 2013 In vitro fabrication of functional three-dimensional tissues with perfusable blood vessels Nat Commun 4 1399 23360990 PMC3660653
  126. Semenza GL 2012 Hypoxia-Inducible Factors in Physiology and Medicine Cell 148 399 408 22304911 PMC3437543
  127. Shandalov Y Egozi D Koffler J Dado-Rosenfeld D Ben-Shimol D Freiman A Shor E Kabala A Levenberg S 2014 An engineered muscle flap for reconstruction of large soft tissue defects Proc Natl Acad Sci 111 6010 6015 24711414 PMC4000846
  128. Shen YI Cho H Papa AE Burke JA Chan XY Duh EJ Gerecht S 2016 Engineered human vascularized constructs accelerate diabetic wound healing Biomaterials 102 107 119 27328431
  129. Shin’oka T Imai Y Ikada Y 2001 Transplantation of a Tissue-Engineered Pulmonary Artery N Engl J Med 344 532 533 11221621
  130. Shirakigawa N Ijima H 2017 Decellularized tissue engineering Advanced Structured Materials Springer Singapore 185 226
  131. Simionescu A Schulte JB Fercana G Simionescu DT 2011 Inflammation in cardiovascular tissue engineering: the challenge to a promise: a minireview Int J Inflam 2011 958247 21755031 PMC3132660
  132. Sivarapatna A Ghaedi M Le AV Mendez JJ Qyang Y Niklason LE 2015 Arterial specification of endothelial cells derived from human induced pluripotent stem cells in a biomimetic flow bioreactor Biomaterials 53 621 633 25890758 PMC4405661
  133. Skardal A Zhang J Prestwich GD 2010 Bioprinting vessel-like constructs using hyaluronan hydrogels crosslinked with tetrahedral polyethylene glycol tetracrylates Biomaterials 31 6173 6181 20546891
  134. Skardal A Mack D Kapetanovic E Atala A Jackson JD Yoo J Soker S 2012 Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds Stem Cells Transl Med 1 792 802 23197691 PMC3659666
  135. Song JW Munn LL 2011 Fluid forces control endothelial sprouting Proc Natl Acad Sci 108 15342 15347 21876168 PMC3174629
  136. Song HHG Park KM Gerecht S 2014 Hydrogels to model 3D in vitro microenvironment of tumor vascularization Adv Drug Deliv Rev 79 80 19 29 PMC4258430 24969477
  137. Stenzel KH Miyata T Rubin AL 1974 Collagen as a Biomaterial Annu Rev Biophys Bioeng 3 231 253 4607533
  138. Stevens KR Scull MA Ramanan V Fortin CL Chaturvedi RR Knouse KA Xiao JW Fung C Mirabella T Chen AX 2017 In situ expansion of engineered human liver tissue in a mouse model of chronic liver disease Sci Transl Med 9 eaah5505 28724577 PMC5896001
  139. Stratman AN Davis GE 2012 Endothelial Cell-Pericyte Interactions Stimulate Basement Membrane Matrix Assembly: Influence on Vascular Tube Remodeling, Maturation, and Stabilization Microsc Microanal 18 68 80 22166617 PMC3919655
  140. Sugden WW Meissner R Aegerter-Wilmsen T Tsaryk R Leonard EV Bussmann J Hamm MJ Herzog W Jin Y Jakobsson L 2017 Endoglin controls blood vessel diameter through endothelial cell shape changes in response to haemodynamic cues Nat Cell Biol 19 653 665 28530658 PMC5455977
  141. Sundaram S Niklason LE 2012 Smooth muscle and other cell sources for human blood vessel engineering Cells Tissues Organs 195 15 25 22041291 PMC3257813
  142. Swift MR Weinstein BM 2009 Arterial-Venous Specification During Development Circ Res 104 576 588 19286613
  143. Syedain Z Reimer J Lahti M Berry J Johnson S Tranquillo RT Tranquillo RT 2016 Tissue engineering of acellular vascular grafts capable of somatic growth in young lambs Nat Commun 7 12951 27676438 PMC5052664
  144. Szymborska A Gerhardt H 2017 Hold Me, but Not Too Tight—Endothelial Cell–Cell Junctions in Angiogenesis Cold Spring Harb Perspect Biol a029223 28851748 PMC6071488
  145. Takebe T Zhang RR Koike H Kimura M Yoshizawa E Enomura M Koike N Sekine K Taniguchi H 2014 Generation of a vascularized and functional human liver from an iPSC-derived organ bud transplant Nat Protoc 9 396 409 24457331
  146. Trappmann B Baker BM Polacheck WJ Choi CK Burdick JA Chen CS 2017 Matrix degradability controls multicellularity of 3D cell migration Nat Commun 8 371 28851858 PMC5575316
  147. Ueba H Kawakami M Yaginuma T 1997 Shear stress as an inhibitor of vascular smooth muscle cell proliferation. Role of transforming growth factor-beta 1 and tissue-type plasminogen activator Arterioscler Thromb Vasc Biol 17 1512 1516 9301628
  148. Valarmathi MT Fuseler JW Potts JD Davis JM Price RL 2017 Functional Tissue Engineering: A Prevascularized Cardiac Muscle Construct for Validating Human Mesenchymal Stem Cells Engraftment Potential In Vitro Tissue Eng Part A 0 ten.tea.2016.0539 PMC5770135 28457188
  149. Wang C Baker BM Chen CS Schwartz MA 2013 Endothelial cell sensing of flow direction Arterioscler Thromb Vasc Biol 33 2130 2136 23814115 PMC3812824
  150. Wang KC Yeh YT Nguyen P Limqueco E Lopez J Thorossian S Guan KL Li YSJ Chien S 2016 Flow-dependent YAP/TAZ activities regulate endothelial phenotypes and atherosclerosis Proc Natl Acad Sci U S A 113 11525 11530 27671657 PMC5068257
  151. Wang Y Yin P Bian GL Huang HY Shen H Yang JJ Yang ZY Shen ZY 2017 The combination of stem cells and tissue engineering: an advanced strategy for blood vessels regeneration and vascular disease treatment Stem Cell Res Ther 8 194 28915929 PMC5603030
  152. Weinberg C Bell E 1986 A Blood Vessel Model Constructed from Collagen and Cultured Vascular Cells Science (80-) 231 397 400 2934816
  153. Whisler JA Chen MB Kamm RD 2014 Control of Perfusable Microvascular Network Morphology Using a Multiculture Microfluidic System Tissue Eng Part C Methods 20 543 552 24151838 PMC4074745
  154. White SL Hirth R Mahíllo B Domínguez-Gil B Delmonico FL Noel L Chapman J Matesanz R Carmona M Alvarez M 2014 The global diffusion of organ transplantation: trends, drivers and policy implications Bull World Health Organ 92 826 835 25378744 PMC4221768
  155. Wiles K Fishman JM De Coppi P Birchall MA 2016 The Host Immune Response to Tissue-Engineered Organs: Current Problems and Future Directions Tissue Eng Part B Rev 22 208 219 26701069
  156. Williams C Wick TM 2004 Tissue-Engineered Arteries 10 930 941 15265311
  157. Wolf K te Lindert M Krause M Alexander S te Riet J Willis AL Hoffman RM Figdor CG Weiss SJ Friedl P 2013 Physical limits of cell migration: Control by ECM space and nuclear deformation and tuning by proteolysis and traction force J Cell Biol 201 1069 1084 23798731 PMC3691458
  158. Xie CQ Zhang J Villacorta L Cui T Huang H Chen YE 2007 A Highly Efficient Method to Differentiate Smooth Muscle Cells From Human Embryonic Stem Cells Arterioscler Thromb Vasc Biol 27 e311 e312 18029907
  159. Yang L Guell M Niu D George H Lesha E Grishin D Aach J Shrock E Xu W Poci J 2015 Genome-wide inactivation of porcine endogenous retroviruses (PERVs) Science (80-) 350 1101 1104 26456528
  160. Yoshida T Owens GK 2005 Molecular determinants of vascular smooth muscle cell diversity Circ Res 96 280 291 15718508
  161. You LR Lin FJ Lee CT DeMayo FJ Tsai MJ Tsai SY 2005 Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity Nature 435 98 104 15875024
  162. Yow KH Ingram J Korossis SA Ingham E Homer-Vanniasinkam S 2006 Tissue engineering of vascular conduits Br J Surg 93 652 661 16703652
  163. Zhang B Montgomery M Chamberlain MD Ogawa S Korolj A Pahnke A Wells LA Massé S Kim J Reis L 2016 Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis Nat Mater 15 669 678 26950595 PMC4879054
  164. Zheng Y Chen J Craven M Choi NW Totorica S Diaz-Santana A Kermani P Hempstead B Fischbach-Teschl C Lopez JA 2012 In vitro microvessels for the study of angiogenesis and thrombosis Proc Natl Acad Sci 109 9342 9347 22645376 PMC3386137
  165. Zhou J Li YS Chien S 2014 Shear stress-initiated signaling and its regulation of endothelial function Arterioscler Thromb Vasc Biol 34 2191 2198 24876354 PMC4169328

Cited by

Sorted by citations

Authors
Song, H.-H. G., Rumma, R. T., Ozaki, C. K., Edelman, E. R., & Chen, C. S.
Affiliations
  • Boston University (US)
  • Brigham and Women's Hospital (US)
Corresponding author
Chen, Christopher S.
ORCID
Venue
Cell Stem Cell
Publisher
Elsevier BV
Published
2018-03
Volume
22
Issue
3
Pages
340-354
ISSN
  • 1875-9777 (ISSN-L)
  • 1934-5909
DOI
10.1016/j.stem.2018.02.009
PMC
PMC5849079
OpenAlex
W2791878273
Cited by
476
References
10
Citations by year
2026: 32 · 2025: 56 · 2024: 61 · 2023: 65 · 2022: 71 · 2021: 78 · 2020: 63 · 2019: 36 · 2018: 13
FWCI
10.57
Type
journal article
Language
en
Update notices
erratum (2018-04-05)
Open access
Licence
Locations
  • Cell stem cell (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
Funders
National Institute of Biomedical Imaging and Bioengineering (R01EB008396, R01EB000262)
Topics
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
  • Physical Sciences › Materials Science › Biomaterials › Electrospun Nanofibers in Biomedical Applications
Keywords
vascular tissue engineering, vascular conduits, stem cell engineering, microvessels, clinical translation
MeSH terms
Biocompatible Materials, Blood Vessels, Humans, Stem Cells, Prostheses and Implants, Tissue Engineering, Printing, Three-Dimensional

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review