1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biomedical Engineering
  4. Volume 20, 2018
  5. Article

Annual Review of Biomedical Engineering

Volume 20, 2018

Arterial Venous Differentiation for Vascular Bioengineering

Abstract

The development processes of arteries and veins are fundamentally different, leading to distinct differences in anatomy, structure, and function as well as molecular profiles. Understanding the complex interaction between genetic and epigenetic pathways, as well as extracellular and biomechanical signals that orchestrate arterial venous differentiation, is not only critical for the understanding of vascular diseases of arteries and veins but also valuable for vascular tissue engineering strategies. Recent research has suggested that certain transcriptional factors not only control arterial venous differentiation during development but also play a critical role in adult vessel function and disease processes. This review summarizes the signaling pathways and critical transcription factors that are important for arterial versus venous specification. We focus on those signals that have a direct relation to the structure and function of arteries and veins, and have implications for vascular disease processes and tissue engineering applications.

Keyword(s): arterial venous endothelial cells, stem cell differentiation, vascular bioengineering, vascular development
Loading

Article metrics loading...

/content/journals/10.1146/annurev-bioeng-062117-121231
2018-06-04
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/20/1/annurev-bioeng-062117-121231.html?itemId=/content/journals/10.1146/annurev-bioeng-062117-121231&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Wang HU, Chen ZF, Anderson DJ 1998. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93:741–53
     [Google Scholar]
  2. 2.  Jones EA 2011. The initiation of blood flow and flow induced events in early vascular development. Semin. Cell Dev. Biol. 22:1028–35
     [Google Scholar]
  3. 3.  Shin D, Garcia-Cardena G, Hayashi S, Gerety S, Asahara T et al. 2001. Expression of ephrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev. Biol. 230:139–50
     [Google Scholar]
  4. 4.  Herzog Y, Guttmann-Raviv N, Neufeld G 2005. Segregation of arterial and venous markers in subpopulations of blood islands before vessel formation. Dev. Dyn. 232:1047–55
     [Google Scholar]
  5. 5.  Zhong TP, Childs S, Leu JP, Fishman MC 2001. Gridlock signalling pathway fashions the first embryonic artery. Nature 414:216–20
     [Google Scholar]
  6. 6.  Lindskog H, Kim YH, Jelin EB, Kong Y, Guevara-Gallardo S et al. 2014. Molecular identification of venous progenitors in the dorsal aorta reveals an aortic origin for the cardinal vein in mammals. Development 141:1120–28
     [Google Scholar]
  7. 7.  Herbert SP, Huisken J, Kim TN, Feldman ME, Houseman BT et al. 2009. Arterial-venous segregation by selective cell sprouting: an alternative mode of blood vessel formation. Science 326:294–98
     [Google Scholar]
  8. 8.  Red-Horse K, Ueno H, Weissman IL, Krasnow MA 2010. Coronary arteries form by developmental reprogramming of venous cells. Nature 464:549–53
     [Google Scholar]
  9. 9.  Kohli V, Schumacher JA, Desai SP, Rehn K, Sumanas S 2013. Arterial and venous progenitors of the major axial vessels originate at distinct locations. Dev. Cell 25:196–206
     [Google Scholar]
  10. 10.  Xu C, Hasan SS, Schmidt I, Rocha SF, Pitulescu ME et al. 2014. Arteries are formed by vein-derived endothelial tip cells. Nat. Commun. 5:5758
     [Google Scholar]
  11. 11.  De Val S, Black BL 2009. Transcriptional control of endothelial cell development. Dev. Cell 16:180–95
     [Google Scholar]
  12. 12.  De Val S 2011. Key transcriptional regulators of early vascular development. Arterioscler. Thromb. Vasc. Biol. 31:1469–75
     [Google Scholar]
  13. 13.  De Val S, Chi NC, Meadows SM, Minovitsky S, Anderson JP et al. 2008. Combinatorial regulation of endothelial gene expression by Ets and Forkhead transcription factors. Cell 135:1053–64
     [Google Scholar]
  14. 14.  Dejana E, Taddei A, Randi AM 2007. Foxs and Ets in the transcriptional regulation of endothelial cell differentiation and angiogenesis. Biochim. Biophys. Acta 1775:298–312
     [Google Scholar]
  15. 15.  Shutter JR, Scully S, Fan W, Richards WG, Kitajewski J et al. 2000. Dll4, a novel Notch ligand expressed in arterial endothelium. Genes Dev 14:1313–18
     [Google Scholar]
  16. 16.  Krebs LT, Xue Y, Norton CR, Shutter JR, Maguire M et al. 2000. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 14:1343–52
     [Google Scholar]
  17. 17.  Lawson ND, Scheer N, Pham VN, Kim CH, Chitnis AB et al. 2001. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128:3675–83
     [Google Scholar]
  18. 18.  Fischer A, Schumacher N, Maier M, Sendtner M, Gessler M 2004. The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev 18:901–11
     [Google Scholar]
  19. 19.  Domenga V, Fardoux P, Lacombe P, Monet M, Maciazek J et al. 2004. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev 18:2730–35
     [Google Scholar]
  20. 20.  Duarte A, Hirashima M, Benedito R, Trindade A, Diniz P et al. 2004. Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev 18:2474–78
     [Google Scholar]
  21. 21.  Quillien A, Moore JC, Shin M, Siekmann AF, Smith T et al. 2014. Distinct Notch signaling outputs pattern the developing arterial system. Development 141:1544–52
     [Google Scholar]
  22. 22.  Kokubo H, Miyagawa-Tomita S, Nakazawa M, Saga Y, Johnson RL 2005. Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Dev. Biol. 278:301–9
     [Google Scholar]
  23. 23.  Villa N, Walker L, Lindsell CE, Gasson J, Iruela-Arispe ML, Weinmaster G 2001. Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech. Dev. 108:161–64
     [Google Scholar]
  24. 24.  Lawson ND, Vogel AM, Weinstein BM 2002. sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell 3:127–36
     [Google Scholar]
  25. 25.  Kume T 2010. Specification of arterial, venous, and lymphatic endothelial cells during embryonic development. Histol. Histopathol. 25:637–46
     [Google Scholar]
  26. 26.  Lawson ND, Weinstein BM 2002. Arteries and veins: making a difference with zebrafish. Nat. Rev. Genet. 3:674–82
     [Google Scholar]
  27. 27.  Weinstein BM, Lawson ND 2002. Arteries, veins, Notch, and VEGF. Cold Spring Harb. Symp. Quant. Biol. 67:155–62
     [Google Scholar]
  28. 28.  van Tuyl M, Groenman F, Wang J, Kuliszewski M, Liu J et al. 2007. Angiogenic factors stimulate tubular branching morphogenesis of sonic hedgehog–deficient lungs. Dev. Biol. 303:514–26
     [Google Scholar]
  29. 29.  Visconti RP, Richardson CD, Sato TN 2002. Orchestration of angiogenesis and arteriovenous contribution by angiopoietins and vascular endothelial growth factor (VEGF). PNAS 99:8219–24
     [Google Scholar]
  30. 30.  Lanner F, Sohl M, Farnebo F 2007. Functional arterial and venous fate is determined by graded VEGF signaling and Notch status during embryonic stem cell differentiation. Arterioscler. Thromb. Vasc. Biol. 27:487–93
     [Google Scholar]
  31. 31.  Deng Y, Larrivee B, Zhuang ZW, Atri D, Moraes F et al. 2013. Endothelial RAF1/ERK activation regulates arterial morphogenesis. Blood 121:3988–96
     [Google Scholar]
  32. 32.  Hong CC, Peterson QP, Hong J-Y, Peterson RT 2006. Artery/vein specification is governed by opposing phosphatidylinositol-3 kinase and MAP kinase/ERK signaling. Curr. Biol. 16:1366–72
     [Google Scholar]
  33. 33.  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. 103:573–79
     [Google Scholar]
  34. 34.  Ren B, Deng Y, Mukhopadhyay A, Lanahan AA, Zhuang ZW et al. 2010. ERK1/2-Akt1 crosstalk regulates arteriogenesis in mice and zebrafish. J. Clin. Investig. 120:1217–28
     [Google Scholar]
  35. 35.  Wythe JD, Dang LTH, Devine WP, Boudreau E, Artap ST et al. 2013. ETS factors regulate Vegf-dependent arterial specification. Dev. Cell 26:45–58
     [Google Scholar]
  36. 36.  Mukouyama YS, Shin D, Britsch S, Taniguchi M, Anderson DJ 2002. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109:693–705
     [Google Scholar]
  37. 37.  Mukouyama YS, Gerber HP, Ferrara N, Gu C, Anderson DJ 2005. Peripheral nerve–derived VEGF promotes arterial differentiation via neuropilin 1–mediated positive feedback. Development 132:941–52
     [Google Scholar]
  38. 38.  Lanahan A, Zhang X, Fantin A, Zhuang Z, Rivera-Molina F et al. 2013. The neuropilin 1 cytoplasmic domain is required for VEGF-A-dependent arteriogenesis. Dev. Cell 25:156–68
     [Google Scholar]
  39. 39.  Herzog Y, Kalcheim C, Kahane N, Reshef R, Neufeld G 2001. Differential expression of neuropilin-1 and neuropilin-2 in arteries and veins. Mech. Dev. 109:115–19
     [Google Scholar]
  40. 40.  Moyon D, Pardanaud L, Yuan L, Bréant C, Eichmann A 2001. Plasticity of endothelial cells during arterial-venous differentiation in the avian embryo. Development 128:3359–70
     [Google Scholar]
  41. 41.  Jones EAV, Yuan L, Breant C, Watts RJ, Eichmann A 2008. Separating genetic and hemodynamic defects in neuropilin 1 knockout embryos. Development 135:2479–88
     [Google Scholar]
  42. 42.  Herpers R, van de Kamp E, Duckers HJ, Schulte-Merker S 2008. Redundant roles for Sox7 and Sox18 in arteriovenous specification in zebrafish. Circ. Res. 102:12–15
     [Google Scholar]
  43. 43.  Cermenati S, Moleri S, Cimbro S, Corti P, Del Giacco L et al. 2008. Sox18 and Sox7 play redundant roles in vascular development. Blood 111:2657–66
     [Google Scholar]
  44. 44.  Pendeville H, Winandy M, Manfroid I, Nivelles O, Motte P et al. 2008. Zebrafish Sox7 and Sox18 function together to control arterial-venous identity. Dev. Biol. 317:405–16
     [Google Scholar]
  45. 45.  Sacilotto N, Monteiro R, Fritzsche M, Becker PW, Sanchez-Del-Campo L et al. 2013. Analysis of Dll4 regulation reveals a combinatorial role for Sox and Notch in arterial development. PNAS 110:11893–98
     [Google Scholar]
  46. 46.  Chiang IK, Fritzsche M, Pichol-Thievend C, Neal A, Holmes K et al. 2017. SoxF factors induce Notch1 expression via direct transcriptional regulation during early arterial development. Development 144:2629–39
     [Google Scholar]
  47. 47.  Corada M, Orsenigo F, Morini MF, Pitulescu ME, Bhat G et al. 2013. Sox17 is indispensable for acquisition and maintenance of arterial identity. Nat. Commun. 4:2609
     [Google Scholar]
  48. 48.  Foroud T, Koller DL, Lai D, Sauerbeck L, Anderson C et al. 2012. Genome-wide association study of intracranial aneurysms confirms role of Anril and SOX17 in disease risk. Stroke 43:2846–52
     [Google Scholar]
  49. 49.  Bilguvar K, Yasuno K, Niemela M, Ruigrok YM, von und zu Fraunberg M et al. 2008. Susceptibility loci for intracranial aneurysm in European and Japanese populations. Nat. Genet. 40:1472–77
     [Google Scholar]
  50. 50.  Yasuno K, Bilguvar K, Bijlenga P, Low SK, Krischek B et al. 2010. Genome-wide association study of intracranial aneurysm identifies three new risk loci. Nat. Genet. 42:420–25
     [Google Scholar]
  51. 51.  Chen X, Qin J, Cheng C-M, Tsai M-J, Tsai SY 2012. COUP-TFII is a major regulator of cell cycle and Notch signaling pathways. Mol. Endocrinol. 26:1268–77
     [Google Scholar]
  52. 52.  Chu M, Li T, Shen B, Cao X, Zhong H et al. 2016. Angiopoietin receptor Tie2 is required for vein specification and maintenance via regulating COUP-TFII. eLife 5:e21032
     [Google Scholar]
  53. 53.  Arita Y, Nakaoka Y, Matsunaga T, Kidoya H, Yamamizu K et al. 2014. Myocardium-derived angiopoietin-1 is essential for coronary vein formation in the developing heart. Nat. Commun. 5:4552
     [Google Scholar]
  54. 54.  Davis RB, Curtis CD, Griffin CT 2013. BRG1 promotes COUP-TFII expression and venous specification during embryonic vascular development. Development 140:1272–81
     [Google Scholar]
  55. 55.  Carmeliet P, Tessier-Lavigne M 2005. Common mechanisms of nerve and blood vessel wiring. Nature 436:193–200
     [Google Scholar]
  56. 56.  Carmeliet P 2003. Blood vessels and nerves: common signals, pathways and diseases. Nat. Rev. Genet. 4:710–20
     [Google Scholar]
  57. 57.  Li W, Kohara H, Uchida Y, James JM, Soneji K et al. 2013. Peripheral nerve–derived CXCL12 and VEGF-A regulate the patterning of arterial vessel branching in developing limb skin. Dev. Cell 24:359–71
     [Google Scholar]
  58. 58.  Pardanaud L, Pibouin-Fragner L, Dubrac A, Mathivet T, English I et al. 2016. Sympathetic innervation promotes arterial fate by enhancing endothelial ERK activity. Circ. Res. 119:607–20
     [Google Scholar]
  59. 59.  Buschmann I, Pries A, Styp-Rekowska B, Hillmeister P, Loufrani L et al. 2010. Pulsatile shear and Gja5 modulate arterial identity and remodeling events during flow-driven arteriogenesis. Development 137:2187–96
     [Google Scholar]
  60. 60.  Le Noble F, Moyon D, Pardanaud L, Yuan L, Djonov V et al. 2004. Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 131:361–75
     [Google Scholar]
  61. 61.  Chong DC, Koo Y, Xu K, Fu S, Cleaver O 2011. Stepwise arteriovenous fate acquisition during mammalian vasculogenesis. Dev. Dyn. 240:2153–65
     [Google Scholar]
  62. 62.  Udan RS, Vadakkan TJ, Dickinson ME 2013. Dynamic responses of endothelial cells to changes in blood flow during vascular remodeling of the mouse yolk sac. Development 140:4041–50
     [Google Scholar]
  63. 63.  Kudo FA, Muto A, Maloney SP, Pimiento JM, Bergaya S et al. 2007. Venous identity is lost but arterial identity is not gained during vein graft adaptation. Arterioscler. Thromb. Vasc. Biol. 27:1562–71
     [Google Scholar]
  64. 64.  Wang M, Collins MJ, Foster TR, Bai H, Hashimoto T et al. 2017. Eph-B4 mediates vein graft adaptation by regulation of endothelial nitric oxide synthase. J. Vasc. Surg. 65:179–89
     [Google Scholar]
  65. 65.  Muto A, Yi T, Harrison KD, Dávalos A, Fancher TT et al. 2011. Eph-B4 prevents venous adaptive remodeling in the adult arterial environment. J. Exp. Med. 208:561–75
     [Google Scholar]
  66. 66.  Cui X, Lu YW, Lee V, Kim D, Dorsey T et al. 2015. Venous endothelial marker COUP-TFII regulates the distinct pathologic potentials of adult arteries and veins. Sci. Rep. 5:16193
     [Google Scholar]
  67. 67.  Lin Y, Jiang W, Ng J, Jina A, Wang RA 2014. Endothelial ephrin-B2 is essential for arterial vasodilation in mice. Microcirculation 21:578–86
     [Google Scholar]
  68. 68.  Braun J, Hoffmann SC, Feldner A, Ludwig T, Henning R et al. 2011. Endothelial cell ephrinB2-dependent activation of monocytes in arteriosclerosis. Arterioscler. Thromb. Vasc. Biol. 31:297–305
     [Google Scholar]
  69. 69.  Castillo-Díaz SA, Garay-Sevilla ME, Hernández-González MA, Solís-Martínez MO, Zaina S 2010. Extensive demethylation of normally hypermethylated CpG islands occurs in human atherosclerotic arteries. Int. J. Mol. Med. 26:691–700
     [Google Scholar]
  70. 70.  Zhou X, Xiao Y, Mao Z, Huang J, Geng Q et al. 2015. Soluble Jagged-1 inhibits restenosis of vein graft by attenuating Notch signaling. Microvasc. Res. 100:9–16
     [Google Scholar]
  71. 71.  Xiao YG, Wang W, Gong D, Mao ZF 2014. γ-Secretase inhibitor DAPT attenuates intimal hyperplasia of vein grafts by inhibition of Notch1 signaling. Lab. Investig. 94:654–62
     [Google Scholar]
  72. 72.  Fukuda D, Aikawa E, Swirski FK, Novobrantseva TI, Kotelianski V et al. 2012. Notch ligand δ–like 4 blockade attenuates atherosclerosis and metabolic disorders. PNAS 109:E1868–77
     [Google Scholar]
  73. 73.  Nakano T, Fukuda D, Koga J, Aikawa M 2016. Delta-like ligand 4–Notch signaling in macrophage activation. Arterioscler. Thromb. Vasc. Biol. 36:2038–47
     [Google Scholar]
  74. 74.  Crist AM, Young C, Meadows SM 2017. Characterization of arteriovenous identity in the developing neonate mouse retina. Gene. Expr. Patterns 23/24:22–31
     [Google Scholar]
  75. 75.  Dancu MB, Tarbell JM 2007. Coronary endothelium expresses a pathologic gene pattern compared to aortic endothelium: correlation of asynchronous hemodynamics and pathology in vivo. Atherosclerosis 192:9–14
     [Google Scholar]
  76. 76.  Aranguren XL, Agirre X, Beerens M, Coppiello G, Uriz M et al. 2013. Unraveling a novel transcription factor code determining the human arterial-specific endothelial cell signature. Blood 122:3982–92
     [Google Scholar]
  77. 77.  Geenen IL, Molin DG, van den Akker NM, Jeukens F, Spronk HM et al. 2015. Endothelial cells (ECs) for vascular tissue engineering: Venous ECs are less thrombogenic than arterial ECs. J. Tissue Eng. Regen. Med. 9:564–76
     [Google Scholar]
  78. 78.  Zahr A, Alcaide P, Yang J, Jones A, Gregory M et al. 2016. Endomucin prevents leukocyte–endothelial cell adhesion and has a critical role under resting and inflammatory conditions. Nat. Commun. 7:10363
     [Google Scholar]
  79. 79.  Palpant NJ, Pabon L, Friedman CE, Roberts M, Hadland B et al. 2017. Generating high-purity cardiac and endothelial derivatives from patterned mesoderm using human pluripotent stem cells. Nat. Protoc. 12:15–31
     [Google Scholar]
  80. 80.  Lian X, Bao X, Al-Ahmad A, Liu J, Wu Y et al. 2014. Efficient differentiation of human pluripotent stem cells to endothelial progenitors via small-molecule activation of WNT signaling. Stem Cell Rep 3:804–16
     [Google Scholar]
  81. 81.  Obi S, Yamamoto K, Shimizu N, Kumagaya S, Masumura T et al. 2009. Fluid shear stress induces arterial differentiation of endothelial progenitor cells. J. Appl. Physiol. 106:203–11
     [Google Scholar]
  82. 82.  Masumura T, Yamamoto K, Shimizu N, Obi S, Ando J 2009. Shear stress increases expression of the arterial endothelial marker ephrinB2 in murine ES cells via the VEGF–Notch signaling pathways. Arterioscler. Thromb. Vasc. Biol. 29:2125–31
     [Google Scholar]
  83. 83.  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 53:621–33
     [Google Scholar]
  84. 84.  Yurugi-Kobayashi T, Itoh H, Schroeder T, Nakano A, Narazaki G et al. 2006. Adrenomedullin/cyclic AMP pathway induces Notch activation and differentiation of arterial endothelial cells from vascular progenitors. Arterioscler. Thromb. Vasc. Biol. 26:1977–84
     [Google Scholar]
  85. 85.  Yamamizu K, Matsunaga T, Uosaki H, Fukushima H, Katayama S et al. 2010. Convergence of Notch and β-catenin signaling induces arterial fate in vascular progenitors. J. Cell Biol. 189:325–38
     [Google Scholar]
  86. 86.  Lanner F, Lee KL, Ortega GC, Sohl M, Li X et al. 2013. Hypoxia-induced arterial differentiation requires adrenomedullin and Notch signaling. Stem Cells Dev 22:1360–69
     [Google Scholar]
  87. 87.  Tsang KM, Hyun JS, Cheng KT, Vargas M, Mehta D et al. 2017. Embryonic stem cell differentiation to functional arterial endothelial cells through sequential activation of ETV2 and NOTCH1 signaling by HIF1α. Stem Cell Rep 9:796–806
     [Google Scholar]
  88. 88.  Zhang J, Chu LF, Hou Z, Schwartz MP, Hacker T et al. 2017. Functional characterization of human pluripotent stem cell–derived arterial endothelial cells. PNAS 114:E6072–78
     [Google Scholar]
/content/journals/10.1146/annurev-bioeng-062117-121231
Loading
Arterial Venous Differentiation for Vascular Bioengineering
Annual Review of Biomedical Engineering 20, 431 (2018); https://doi.org/10.1146/annurev-bioeng-062117-121231
/content/journals/10.1146/annurev-bioeng-062117-121231
/content/journals/10.1146/annurev-bioeng-062117-121231
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error