Skip to main content

Hypoxia and Mechanical Factors Drive Coronary Vascular Development

  • Chapter
  • First Online:
Cardiac Adaptations

Part of the book series: Advances in Biochemistry in Health and Disease ((ABHD,volume 4))

  • 1830 Accesses

Abstract

Coronary vascular development requires a variety of signaling molecules expressed spatially and temporally, which are activated by metabolic and mechanical factors. Hypoxia plays the earliest role in this activation via its stimulation of hypoxia inducible factor (HIF–1), and the subsequent activation of VEGF and other growth factors. The early growth of the coronary vasculature consists of a tubular network formed prior to myocardial perfusion. A part of this vascular plexus penetrates the aorta, largely in response to VEGF, to form the coronary ostia, which provides the anatomical substrate for coronary flow. Shear stress then becomes a key regulator of the formation of the coronary hierarchy along with the key growth factors that facilitate the formation of the tunica media of the arterial tree, i.e., FGF, PDGF, and TGF-β. Hypoxia plays a dual role by its activation of HIF-1 and by affecting increases in blood flow and shear stress. Growth of the myocardium involves stretch of both cardiomyocytes and blood vessels, which activates stretch signals in both cell types and causes growth factor paracrine and autocrine signaling and consequently, angiogenesis. Shear stress and stretch are the major mechanical influences that drive coronary vascularization. These mechanical effects are determinants of vessel diameters and composition of their walls. Arterial and venous specification is also affected by blood flow as indicated by endothelial phenotype changes that can occur in response to altered perfusion.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Hanze J, Weissmann N, Grimminger F, Seeger W, Rose F (2007) Cellular and molecular mechanisms of hypoxia-inducible factor driven vascular remodeling. Thromb Haemost 97:774–787

    PubMed  Google Scholar 

  2. Rey S, Semenza GL (2010) Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res 86:236–242

    Article  PubMed  CAS  Google Scholar 

  3. Semenza GL (2010) Vascular responses to hypoxia and ischemia. Arterioscler Thromb Vasc Biol 30:648–652

    Article  PubMed  CAS  Google Scholar 

  4. Iyer NV, Kotch LE, Agani F et al (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Gene Dev 12:149–162

    Article  PubMed  CAS  Google Scholar 

  5. Pugh CW, Ratcliffe PJ (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9:677–684

    Article  PubMed  CAS  Google Scholar 

  6. Manalo DJ, Rowan A, Lavoie T et al (2005) Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105:659–669

    Article  PubMed  CAS  Google Scholar 

  7. Kelly BD, Hackett SF, Hirota K et al (2003) Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ Res 93:1074–1081

    Article  PubMed  CAS  Google Scholar 

  8. Bosch-Marce M, Okuyama H, Wesley JB et al (2007) Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circ Res 101:1310–1318

    Article  PubMed  CAS  Google Scholar 

  9. Nomura M, Yamagishi S, Harada S et al (1995) Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J Biol Chem 270:28316–28324

    Article  PubMed  CAS  Google Scholar 

  10. Yamagishi S, Yonekura H, Yamamoto Y, Fujimori H, Sakurai S, Tanaka N et al (1999) Vascular endothelial growth factor acts as a pericyte mitogen under hypoxic conditions. Lab Invest 79:501–509

    PubMed  CAS  Google Scholar 

  11. Duan LJ, Zhang-Benoit Y, Fong GH (2005) Endothelium-intrinsic requirement for Hif-2alpha during vascular development. Circulation 111:2227–2232

    Article  PubMed  CAS  Google Scholar 

  12. Gruber M, Hu CJ, Johnson RS, Brown EJ, Keith B, Simon MC (2007) Acute postnatal ablation of HIF-2alpha results in anemia. Proc Natl Acad Sci U S A 104:2301–2306

    Article  PubMed  CAS  Google Scholar 

  13. Gerber HP, Condorelli F, Park J, Ferrara N (1997) Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J Biol Chem 272:23659–23667

    Article  PubMed  CAS  Google Scholar 

  14. Marti HH, Risau W (1998) Systemic hypoxia changes the organ-specific distribution of vascular endothelial growth factor and its receptors. Proc Natl Acad Sci U S A 95:15809–15814

    Article  PubMed  CAS  Google Scholar 

  15. Li B, Sharpe EE, Maupin AB et al (2006) VEGF and PlGF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at the site of tumor neovascularization. FASEB J 20:1495–1497

    Article  PubMed  CAS  Google Scholar 

  16. Torry RJ, Tomanek RJ, Zheng W et al (2009) Hypoxia increases placenta growth factor expression in human myocardium and cultured neonatal rat cardiomyocytes. J Heart Lung Transplant 28:183–190

    Article  PubMed  Google Scholar 

  17. Gerhardt H, Golding M, Fruttiger M et al (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161:1163–1177

    Article  PubMed  CAS  Google Scholar 

  18. Tang N, Wang L, Esko J et al (2004) Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell 6:485–495

    Article  PubMed  CAS  Google Scholar 

  19. Skuli N, Liu L, Runge A, Wang T, Yuan L, Patel S et al (2009) Endothelial deletion of hypoxia-inducible factor-2alpha (HIF-2alpha) alters vascular function and tumor angiogenesis. Blood 114:469–477

    Article  PubMed  CAS  Google Scholar 

  20. Van den Eijnde SM, Wenink AC, Vermeij-Keers C (1992) Origin of subepicardial cells in rat embryos. Anat Rec 242:96–102

    Article  Google Scholar 

  21. Manasek FJ (1968) Embryonic development of the heart I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol 125:329–365

    Article  PubMed  CAS  Google Scholar 

  22. Viragh S, Gittenberger-de Groot AC, Poelmann RE, Kalman F (1993) Early development of quail heart epicardium and associated vascular and glandular structures. Anat Embryol (Berl) 188:381–393

    Article  CAS  Google Scholar 

  23. Nahirney PC, Mikawa T, Fischman DA (2003) Evidence for an extracellular matrix bridge guiding proepicardial cell migration to the myocardium of chick embryos. Dev Dyn 27:511–523

    Article  Google Scholar 

  24. Mikawa T, Fischman DA (1992) Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc Natl Acad Sci U S A 89:9504–9508

    Article  PubMed  CAS  Google Scholar 

  25. Red-Horse K, Ueno H, Weissman IL, Krasnow MA (2010) Coronary arteries form by developmental reprogramming of venous cells. Nature 464:549–553

    Article  PubMed  CAS  Google Scholar 

  26. Morabito CJ, Dettman RW, Kattan J, Collier JM, Bristow J (2001) Positive and negative regulation of epicardial-mesenchymal transformation during avian heart development. Dev Biol 234:204–215

    Article  PubMed  CAS  Google Scholar 

  27. Yang K, Doughman YQ, Karunamuni G et al (2009) Expression of active notch1 in avian coronary development. Dev Dyn 238:162–170

    Article  PubMed  CAS  Google Scholar 

  28. Tomanek RJ, Ratajska A, Kitten GT, Yue X, Sandra A (1999) Vascular endothelial growth factor expression coincides with coronary vasculogenesis and angiogenesis. Dev Dyn 215:54–61

    Article  PubMed  CAS  Google Scholar 

  29. Druyan S, Cahaner A, Ashwell CM (2007) The expression patterns of hypoxia-inducing factor subunit alpha-1, heme oxygenase, hypoxia upregulated protein 1, and cardiac troponin T during development of the chicken heart. Poul Sci 86:2384–2389

    Article  CAS  Google Scholar 

  30. Lee YM, Jeong CH, Koo SY et al (2001) Determination of hypoxic region by hypoxia marker in developing mouse embryos in vivo: a possible signal for vessel development. Dev Dyn 220:175–186

    Article  PubMed  CAS  Google Scholar 

  31. Nanka O, Valasek P, Dvorakova M, Grim M (2006) Experimental hypoxia and embryonic angiogenesis. Dev Dyn 235:723–733

    Article  PubMed  CAS  Google Scholar 

  32. Nanka O, Krizova P, Fikrle M et al (2008) Abnormal myocardial and coronary vasculature development in experimental hypoxia. Anat Rec (Hoboken) 291:1187–1199

    Article  Google Scholar 

  33. Wikenheiser J, Wolfram JA, Gargesha M, Yang K, Karunamuni G, Wilson DL et al (2009) Altered hypoxia-inducible factor-1 alpha expression levels correlate with coronary vessel anomalies. Dev Dyn 238:2688–2700

    Article  PubMed  CAS  Google Scholar 

  34. Yue X, Tomanek RJ (1999) Stimulation of coronary vasculogenesis/angiogenesis by hypoxia in cultured embryonic hearts. Dev Dyn 216:28–36

    Article  PubMed  CAS  Google Scholar 

  35. Yue X, Tomanek RJ (2001) Effects of VEGF(165) and VEGF(121) on vasculogenesis and angiogenesis in cultured embryonic quail hearts. Am J Physiol Heart Circ Physiol 280:H2240–H2247

    PubMed  CAS  Google Scholar 

  36. Tomanek RJ, Holifield JS, Reiter RS, Sandra A, Lin JJ (2002) Role of VEGF family members and receptors in coronary vessel formation. Dev Dyn 225:233–240

    Article  PubMed  CAS  Google Scholar 

  37. Enholm B, Paavonen K, Ristimaki A et al (1997) Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene 14:2475–2483

    Article  PubMed  CAS  Google Scholar 

  38. Ramirez-Bergeron DL, Runge A et al (2004) Hypoxia affects mesoderm and enhances hemangioblast specification during early development. Development 131:4623–4634

    Article  PubMed  CAS  Google Scholar 

  39. Han Y, Kuang SZ, Gomer A, Ramirez-Bergeron DL (2010) Hypoxia influences the vascular expansion and differentiation of embryonic stem cell cultures through the temporal expression of vascular endothelial growth factor receptors in an ARNT-dependent manner. Stem Cells 28:799–809

    Article  PubMed  CAS  Google Scholar 

  40. Shalaby F, Rossant J, Yamaguchi TP et al (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62–66

    Article  PubMed  CAS  Google Scholar 

  41. Fong GH, Rossant J, Gertsenstein M, Breitman ML (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66–70

    Article  PubMed  CAS  Google Scholar 

  42. Mascio CE, Olison AK, Ralphe JC et al (2005) Myocardial vascular and metabolic adaptations in chronically anemic fetal sheep. Am J Physiol Regul Integr Comp Physiol 289:R1736–R1745

    Article  PubMed  CAS  Google Scholar 

  43. Davis LE, Hohimer AR (1991) Hemodynamics and organ blood flow in fetal sheep subjected to chronic anemia. Am J Physiol 261:R1542–R1548

    PubMed  CAS  Google Scholar 

  44. Davis LE, Hohimer AR, Morton MJ (1999) Myocardial blood flow and coronary reserve in chronically anemic fetal lambs. Am J Physiol 1999(277):R306–R313

    Google Scholar 

  45. Martin C, Yu AY, Jiang BH et al (1998) Cardiac hypertrophy in chronically anemic fetal sheep: Increased vascularization is associated with increased myocardial expression of vascular endothelial growth factor and hypoxia-inducible factor 1. Am J Obstet Gynecol 178:527–534

    Article  PubMed  CAS  Google Scholar 

  46. Reller MD, Morton MJ, Giraud GD, Wu DE, Thornburg KL (1992) Maximal myocardial blood flow is enhanced by chronic hypoxemia in late gestation fetal sheep. Am J Physiol 263(4pt 2):H1327–H1329

    PubMed  CAS  Google Scholar 

  47. Wothe D, Hohimer A, Morton M et al (2002) Increased coronary blood flow signals growth of coronary resistance vessels in near-term ovine fetuses. Am J Physiol Regul Integr Comp Physiol 282:R295–R302

    PubMed  CAS  Google Scholar 

  48. Torry RJ, O’Brien DM, Connell PM, Tomanek RJ (1992) Dipyridamole-induced capillary growth in normal and hypertrophic hearts. Am J Physiol 262:H980–H986

    PubMed  CAS  Google Scholar 

  49. Pohl U (1990) Endothelial cells as part of a vascular oxygen-sensing system: hypoxia-induced release of autacoids. Experientia 46:1175–1179

    Article  PubMed  CAS  Google Scholar 

  50. Kourembanas S, Morita T, Liu Y, Christou H (1997) Mechanisms by which oxygen regulates gene expression and cell-cell interaction in the vasculature. Kidney Int 51:438–443

    Article  PubMed  CAS  Google Scholar 

  51. Reller MD, Burson MA, Lohr JL, Morton MJ, Thornburg KL (1995) Nitric oxide is an important determinant of coronary flow at rest and during hypoxemic stress in fetal lambs. Am J Physiol 269:H2074–H2081

    PubMed  CAS  Google Scholar 

  52. Xue C, Rengasamy A, Le Cras TD et al (1994) Distribution of NOS in normoxic vs. hypoxic rat lung: upregulation of NOS by chronic hypoxia. Am J Physiol 267:L667–L678

    PubMed  CAS  Google Scholar 

  53. Dong Y, Thompson LP (2006) Differential expression of endothelial nitric oxide synthase in coronary and cardiac tissue in hypoxic fetal guinea pig hearts. J Soc Gynecol Invest 13:483–490

    CAS  Google Scholar 

  54. Thompson LP, Aguan K, Pinkas G, Weiner CP (2000) Chronic hypoxia increases the NO contribution of acetylcholine vasodilation of the fetal guinea pig heart. Am J Physiol Regul Integr Comp Physiol 279:R1813–R1820

    PubMed  CAS  Google Scholar 

  55. Thornburg KL, Reller MD (1999) Coronary flow regulation in the fetal sheep. Am J Physiol 277:R1249–R1260

    PubMed  CAS  Google Scholar 

  56. Ando K, Nakajima Y, Yamagishi T, Yamamoto S, Nakamura H (2004) Development of proximal coronary arteries in quail embryonic heart: multiple capillaries penetrating the aortic sinus fuse to form main coronary trunk. Circ Res 94:346–352

    Article  PubMed  CAS  Google Scholar 

  57. Velkey JM, Bernanke DH (2001) Apoptosis during coronary artery orifice development in the chick embryo. Anat Rec 262:310–317

    Article  PubMed  CAS  Google Scholar 

  58. Bogers AJ, Gittenberger-de Groot AC, Poelmann RE, Peault BM, Huysmans HA (1989) Development of the origin of the coronary arteries, a matter of ingrowth or outgrowth? Anat Embryol (Berl) 180:437–441

    Article  CAS  Google Scholar 

  59. Poelmann RE, Gittenberger-de Groot AC, Mentink MM, Bokenkamp R, Hogers B (1993) Development of the cardiac coronary vascular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras. Circ Res 73:559–568

    Article  PubMed  CAS  Google Scholar 

  60. Waldo KL, Kumiski DH, Kirby ML (1994) Association of the cardiac neural crest with development of the coronary arteries in the chick embryo. Anat Rec 239:315–331

    Article  PubMed  CAS  Google Scholar 

  61. Tomanek RJ, Haung L, Suvarna PR, O’Brien LC, Ratajska A, Sandra A (1996) Coronary vascularization during development in the rat and its relationship to basic fibroblast growth factor. Cardiovasc Res 31:E116–E126

    PubMed  CAS  Google Scholar 

  62. Tomanek RJ, Ishii Y, Holifield JS et al (2006) VEGF family members regulate myocardial tubulogenesis and coronary artery formation in the embryo. Circ Res 98:947–953

    Article  PubMed  CAS  Google Scholar 

  63. Hood LC, Rosenquist TH (1992) Coronary artery development in the chick: origin and deployment of smooth muscle cells, and the effects of neural crest ablation. Anat Rec 234:291–300

    Article  PubMed  CAS  Google Scholar 

  64. Mikawa T, Gourdie RG (1996) Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol 174:221–232

    Article  PubMed  CAS  Google Scholar 

  65. Dettman RW, Denetclaw W Jr, Ordahl CP, Bristow J (1998) Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev Biol 193:169–181

    Article  PubMed  CAS  Google Scholar 

  66. Gittenberger-de Groot A, Vrancken Peeters MP, Mentink M, Gourdie R, Poelmann R (1998) Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 82:1043–1052

    Article  PubMed  CAS  Google Scholar 

  67. Perez-Pomares JM, Carmona R, Gonzalez-Iriarte M et al (2002) Origin of coronary endothelial cells from epicardial mesothelium in avian embryos. Int J Dev Biol 46:1005–1013

    PubMed  CAS  Google Scholar 

  68. Jiang X, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cardiac neural crest. Development 127:1607–1616

    PubMed  CAS  Google Scholar 

  69. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C (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 126:3047–3055

    PubMed  CAS  Google Scholar 

  70. Sridurongrit S, Larsson J, Schwartz R, Ruiz-Lozano P, Kaartinen V (2008) Signaling via the Tgf-beta type I receptor Alk5 in heart development. Dev Biol 322:208–218

    Article  PubMed  CAS  Google Scholar 

  71. Tomanek RJ, Hansen HK, Christensen LP (2008) Temporally expressed PDGF and FGF-2 regulate embryonic coronary artery formation and growth. Arterioscler Thromb Vasc Biol 28:1237–1243

    Article  PubMed  CAS  Google Scholar 

  72. Azambuja AP, Portillo-Sanchez V, Rodrigues MV et al (2010) Retinoic acid and VEGF delay smooth muscle relative to endothelial differentiation to coordinate inner and outer coronary vessel wall morphogenesis. Cir Res 107:204–216

    Article  CAS  Google Scholar 

  73. Pistea A, Bakker EN, Spaan JA, VanBavel E (2005) Flow inhibits inward remodeling in cannulated porcine small coronary arteries. Am J Physiol Heart Circ Physiol 289:H2632–H2640

    Article  PubMed  CAS  Google Scholar 

  74. Tornling G (1982) Capillary neoformation in the heart of dipyridamole-treated rats. Acta Pathol Microbiol Immunol Scand A 90:269–271

    PubMed  CAS  Google Scholar 

  75. Mall G, Schikora I, Mattfeldt T, Bodle R (1987) Dipyridamole-induced neoformation of capillaries in the rat heart. Quantitative stereological study on papillary muscles. Lab Invest 57:86–93

    PubMed  CAS  Google Scholar 

  76. Chien S, Li S, Shyy YJ (1998) Effects of mechanical forces on signal transduction and gene expression in endothelial cells. Hypertension 31:162–169

    Article  PubMed  CAS  Google Scholar 

  77. Li YS, Haga JH, Chien S (2005) Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 38:1949–1971

    Article  PubMed  Google Scholar 

  78. Yamamoto K, Ando J (2011) New molecular mechanisms for cardiovascular disease: blood flow sensing mechanism in vascular endothelial cells. J Pharmacol Sci 116:323–331

    Article  PubMed  CAS  Google Scholar 

  79. Bao X, Lu C, Frangos JA (2001) Mechanism of temporal gradients in shear-induced ERK1/2 activation and proliferation in endothelial cells. Am J Physiol Heart Circ Physiol 281:H22–H29

    PubMed  CAS  Google Scholar 

  80. Chiu JJ, Wung BS, Shyy JY, Hsieh HJ, Wang DL (1997) Reactive oxygen species are involved in shear stress-induced intercellular adhesion molecule-1 expression in endothelial cells. Arterioscler Thromb Vasc Biol 17:3570–3577

    Article  PubMed  CAS  Google Scholar 

  81. Wang DZ, Li S, Hockemeyer D et al (2002) Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci U S A. 99:14855–14860

    Article  PubMed  CAS  Google Scholar 

  82. Chiquet M (1999) Regulation of extracellular matrix gene expression by mechanical stress. Matrix Biol 18:417–426

    Article  PubMed  CAS  Google Scholar 

  83. Fan J, Walsh KB (1999) Mechanical stimulation regulates voltage-gated potassium currents in cardiac microvascular endothelial cells. Circ Res 84:451–457

    Article  PubMed  CAS  Google Scholar 

  84. Fisslthaler B, Popp R, Michaelis UR et al (2001) Cyclic stretch enhances the expression and activity of coronary endothelium-derived hyperpolarizing factor synthase. Hypertension 38:1427–1432

    Article  PubMed  CAS  Google Scholar 

  85. Sokabe M, Naruse K, Sai S, Yamada T, Kawakami K, Inoue M et al (1999) Mechanotransduction and intracellular signaling mechanisms of stretch-induced remodeling in endothelial cells. Heart Vessels Suppl 12:191–193

    Google Scholar 

  86. Zheng W, Seftor EA, Meininger CJ, Hendrix MJ, Tomanek RJ (2001) Mechanisms of coronary angiogenesis in response to stretch: role of VEGF and TGF-beta. Am J Physiol Heart Circ Physiol 280:H909–H917

    PubMed  CAS  Google Scholar 

  87. Zheng W, Christensen LP, Tomanek RJ (2004) Stretch induces upregulation of key tyrosine kinase receptors in microvascular endothelial cells. Am J Physiol Heart Circ Physiol. 2004(287):H2739–H2745

    Article  CAS  Google Scholar 

  88. Chang H, Wang BW, Kuan P, Shyu KG (2003) Cyclical mechanical stretch enhances angiopoietin-2 and Tie2 receptor expression in cultured human umbilical vein endothelial cells. Clin Sci (Lond) 104:421–428

    Article  CAS  Google Scholar 

  89. Li J, Hampton T, Morgan JP, Simons M (1997) Stretch-induced VEGF expression in the heart. J Clin Invest 100:18–24

    Article  PubMed  CAS  Google Scholar 

  90. Batra S, Rakusan K (1992) Capillary network geometry during postnatal growth in rat hearts. Am J Physiol 262:H635–H640

    PubMed  CAS  Google Scholar 

  91. Tomanek RJ, Doty MK, Sandra A (1998) Early coronary angiogenesis in response to thyroxine: growth characteristics and upregulation of basic fibroblast growth factor. Circ Res 82:587–593

    Article  PubMed  CAS  Google Scholar 

  92. Dbaly J (1773) Postnatal development of coronary arteries in the rat. J Anat Entwickl-Gesch 141:89–101

    Google Scholar 

  93. Ito T, Harada K, Tamura M, Takada G (1998) In situ morphometric analysis of the coronary arterial growth in perinatal rats. Early Hum Dev 52:21–26

    Article  PubMed  CAS  Google Scholar 

  94. Yasuoka K, Harada K, Tamura M, Takada G (2002) Left anterior descending coronary artery flow and its relation to age in children. J Am Soc Echocardiogr 15:69–75

    Article  PubMed  Google Scholar 

  95. Kurosawa S, Kurosawa H, Becker AE (1986) The coronary arterioles in newborns, infants and children. A morphometric study of normal hearts and hearts with aortic atresia and complete transposition. Int J Cardiol 10:43–56

    Article  PubMed  CAS  Google Scholar 

  96. Wiest G, Gharehbaghi H, Amann K et al (1992) Physiological growth of arteries in the rat heart parallels the growth of capillaries, but not of myocytes. J Mol Cell Cardiol 24:1423–1431

    Article  PubMed  CAS  Google Scholar 

  97. Ohuchi H, Beighley PE, Dong Y, Zamir M, Ritman EL (2007) Microvascular development in porcine right and left ventricular walls. Pediatr Res 61:676–680

    Article  PubMed  Google Scholar 

  98. Zamir M (2005) The physics of coronary blood flow. Springer, New York

    Google Scholar 

  99. Fisher DJ, Heymann MA, Rudolph AM (1982) Regional myocardial blood flow and oxygen delivery in fetal, newborn, and adult sheep. Am J Physiol 243:H729–H731

    PubMed  CAS  Google Scholar 

  100. dela Paz NG, D’Amore PA (2009) Arterial versus venous endothelial cells. Cell Tissue Res 335:5–16

    Article  PubMed  Google Scholar 

  101. Eichmann A, Yuan L, Moyon D et al (2005) Vascular development: from precursor cells to branched arterial and venous networks. Int J Dev Biol 49:259–267

    Article  PubMed  CAS  Google Scholar 

  102. le Noble F, Moyon D, Pardanaud L et al (2004) Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 131:361–375

    Article  PubMed  CAS  Google Scholar 

  103. Jones EA, le Noble F, Eichmann A (2006) What determines blood vessel structure? Genetic prespecification vs. hemodynamics. Physiology (Bethesda) 21:388–395

    Google Scholar 

  104. Moyon D, Pardanaud L, Yuan L, Breant C, Eichmann A (2001) Plasticity of endothelial cells during arterial-venous differentiation in the avian embryo. Development 128:3359–3370

    PubMed  CAS  Google Scholar 

  105. Haga JH, Li YS, Chien S (2007) Molecular basis of the effects of mechanical stretch on vascular smooth muscle cells. J Biomech 40:947–960

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by funds from the National Institutes of Health grant 5 R01 075446.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert J. Tomanek .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Tomanek, R.J. (2013). Hypoxia and Mechanical Factors Drive Coronary Vascular Development . In: Ostadal, B., Dhalla, N. (eds) Cardiac Adaptations. Advances in Biochemistry in Health and Disease, vol 4. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5203-4_4

Download citation

Publish with us

Policies and ethics