1932

Abstract

▪ Abstract 

Communication between endothelial cells and cardiomyocytes regulates not only early cardiac development but also adult cardiomyocyte function, including the contractile state. In the normal mammalian myocardium, each cardiomyocyte is surrounded by an intricate network of capillaries and is next to endothelial cells. Cardiomyocytes depend on endothelial cells not only for oxygenated blood supply but also for local protective signals that promote cardiomyocyte organization and survival. While endothelial cells direct cardiomyocytes, cardiomyocytes reciprocally secrete factors that impact endothelial cell function. Understanding how endothelial cells communicate with cardiomyocytes will be critical for cardiac regeneration, in which the ultimate goal is not simply to improve systolic function transiently but to establish new myocardium that is both structurally and functionally normal in the long term.

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/content/journals/10.1146/annurev.physiol.68.040104.124629
2006-03-17
2024-05-18
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Literature Cited

  1. Cleaver O, Melton DA. 2003. Endothelial signaling during development. Nat. Med. 9:661–68 [Google Scholar]
  2. Brutsaert DL. 2003. Cardiac endothelial-myocardial signaling: its role in cardiac growth, contractile performance, and rhythmicity. Physiol. Rev. 83:59–115 [Google Scholar]
  3. Korecky B, Hai CM, Rakusan K. 1982. Functional capillary density in normal and transplanted rat hearts. Can. J. Physiol. Pharmacol. 60:23–32 [Google Scholar]
  4. Lough J, Sugi Y. 2000. Endoderm and heart development. Dev. Dyn. 217:327–42 [Google Scholar]
  5. Harvey RP. 2002. Patterning the vertebrate heart. Nat. Rev. Genet. 3:544–56 [Google Scholar]
  6. Moorman AF, Christoffels VM. 2003. Cardiac chamber formation: development, genes, and evolution. Physiol. Rev. 83:1223–67 [Google Scholar]
  7. Linask KK, Lash JW. 1993. Early heart development: dynamics of endocardial cell sorting suggests a common origin with cardiomyocytes. Dev. Dyn. 196:62–69 [Google Scholar]
  8. Marchionni MA. 1995. Cell-cell signalling: neu tack on neuregulin. Nature 378:334–35 [Google Scholar]
  9. Meyer D, Birchmeier C. 1995. Multiple essential functions of neuregulin in development. Nature 378:386–90 [Google Scholar]
  10. Gassmann M, Casagranda F, Orioli D, Simon H, Lai C. et al. 1995. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378:390–94 [Google Scholar]
  11. Lee KF, Simon H, Chen H, Bates B, Hung MC. et al. 1995. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378:394–98 [Google Scholar]
  12. Zhao YY, Sawyer DR, Baliga RR, Opel DJ, Han X. et al. 1998. Neuregulins promote survival and growth of cardiac myocytes. Persistence of ErbB2 and ErbB4 expression in neonatal and adult ventricular myocytes. J. Biol. Chem. 273:10261–69 [Google Scholar]
  13. Lin AE, Birch PH, Korf BR, Tenconi R, Niimura M. et al. 2000. Cardiovascular malformations and other cardiovascular abnormalities in neurofibromatosis 1. Am. J. Med. Genet. 95:108–17 [Google Scholar]
  14. Gitler AD, Zhu Y, Ismat FA, Lu MM, Yamauchi Y. et al. 2003. Nf1 has an essential role in endothelial cells. Nat. Genet. 33:75–79 [Google Scholar]
  15. Hoch RV, Soriano P. 2003. Roles of PDGF in animal development. Development 130:4769–84 [Google Scholar]
  16. Bjarnegard M, Enge M, Norlin J, Gustafsdottir S, Fredriksson S. et al. 2004. Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 131:1847–57 [Google Scholar]
  17. Haigh JJ, Gerber HP, Ferrara N, Wagner EF. 2000. Conditional inactivation of VEGF-A in areas of collagen2a1 expression results in embryonic lethality in the heterozygous state. Development 127:1445–53 [Google Scholar]
  18. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF. et al. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62–66 [Google Scholar]
  19. Giordano FJ, Gerber HP, Williams SP, VanBruggen N, Bunting S. et al. 2001. A cardiac myocyte vascular endothelial growth factor paracrine pathway is required to maintain cardiac function. Proc. Natl. Acad. Sci. USA 98:5780–85 [Google Scholar]
  20. Miquerol L, Langille BL, Nagy A. 2000. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 127:3941–46 [Google Scholar]
  21. Dor Y, Camenisch TD, Itin A, Fishman GI, McDonald JA. et al. 2001. A novel role for VEGF in endocardial cushion formation and its potential contribution to congenital heart defects. Development 128:1531–38 [Google Scholar]
  22. Dor Y, Klewer SE, McDonald JA, Keshet E, Camenisch TD. 2003. VEGF modulates early heart valve formation. Anat. Rec. 271:202–8 [Google Scholar]
  23. Lambrechts D, Carmeliet P. 2004. Sculpting heart valves with NFATc and VEGF. Cell 118:532–34 [Google Scholar]
  24. Chang CP, Neilson JR, Bayle JH, Gestwicki JE, Kuo A. et al. 2004. A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis. Cell 118:649–63 [Google Scholar]
  25. Sato TN, Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y. et al. 1995. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376:70–74 [Google Scholar]
  26. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC. et al. 1996. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171–80 [Google Scholar]
  27. Puri MC, Partanen J, Rossant J, Bernstein A. 1999. Interaction of the TEK and TIE receptor tyrosine kinases during cardiovascular development. Development 126:4569–80 [Google Scholar]
  28. Ward NL, Van Slyke P, Sturk C, Cruz M, Dumont DJ. 2004. Angiopoietin 1 expression levels in the myocardium direct coronary vessel development. Dev. Dyn. 229:500–9 [Google Scholar]
  29. Godecke A, Heinicke T, Kamkin A, Kiseleva I, Strasser RH. et al. 2001. Inotropic response to β-adrenergic receptor stimulation and anti-adrenergic effect of ACh in endothelial NO synthase-deficient mouse hearts. J. Physiol. 532:195–204 [Google Scholar]
  30. Champion HC, Georgakopoulos D, Takimoto E, Isoda T, Wang Y. et al. 2004. Modulation of in vivo cardiac function by myocyte-specific nitric oxide synthase-3. Circ. Res. 94:657–63 [Google Scholar]
  31. Barouch LA, Harrison RW, Skaf MW, Rosas GO, Cappola TP. et al. 2002. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature 416:337–39 [Google Scholar]
  32. Ozcelik C, Erdmann B, Pilz B, Wettschureck N, Britsch S. et al. 2002. Conditional mutation of the ErbB2 (HER2) receptor in cardiomyocytes leads to dilated cardiomyopathy. Proc. Natl. Acad. Sci. USA 99:8880–85 [Google Scholar]
  33. Crone SA, Zhao YY, Fan L, Gu Y, Minamisawa S. et al. 2002. ErbB2 is essential in the prevention of dilated cardiomyopathy. Nat. Med. 8:459–65 [Google Scholar]
  34. Lemmens K, Fransen P, Sys SU, Brutsaert DL, DeKeulenaer GW. 2004. Neuregulin-1 induces a negative inotropic effect in cardiac muscle: role of nitric oxide synthase. Circulation 109:324–26 [Google Scholar]
  35. Rich S, McLaughlin VV. 2003. Endothelin receptor blockers in cardiovascular disease. Circulation 108:2184–90 [Google Scholar]
  36. Zolk O, Quattek J, Sitzler G, Schrader T, Nickenig G. et al. 1999. Expression of endothelin-1, endothelin-converting enzyme, and endothelin receptors in chronic heart failure. Circulation 99:2118–23 [Google Scholar]
  37. Luscher TF, Enseleit F, Pacher R, Mitrovic V, Schulze MR. et al. 2002. Hemodynamic and neurohumoral effects of selective endothelin A (ET(A)) receptor blockade in chronic heart failure: the Heart Failure ET(A) Receptor Blockade Trial (HEAT). Circulation 106:2666–72 [Google Scholar]
  38. O'Connor CM, Gattis WA, Adams KF Jr, Hasselblad V, Chandler B. et al. 2003. Tezosentan in patients with acute heart failure and acute coronary syndromes: results of the Randomized Intravenous TeZosentan Study (RITZ-4). J. Am. Coll. Cardiol. 41:1452–55 [Google Scholar]
  39. Packer M, McMurray J, Massie BM, Caspi A, Charlon V. et al. 2005. Clinical effects of endothelin receptor antagonism with bosentan in patients with severe chronic heart failure: results of a pilot study. J. Card. Fail. 11:12–20 [Google Scholar]
  40. Becker RO, Chapin S, Sherry R. 1974. Regeneration of the ventricular myocardium in amphibians. Nature 248:145–47 [Google Scholar]
  41. Poss KD, Wilson LG, Keating MT. 2002. Heart regeneration in zebrafish. Science 298:2188–90 [Google Scholar]
  42. Anversa P. 2000. Myocyte death in the pathological heart. Circ. Res. 86:121–24 [Google Scholar]
  43. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F. et al. 2003. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763–76 [Google Scholar]
  44. Engel FB, Schebesta M, Duong MT, Lu G, Ren SX. et al. 2005. p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev. 19:1175–87 [Google Scholar]
  45. Deb A, Wang S, Skelding KA, Miller D, Simper D. et al. 2003. Bone marrow-derived cardiomyocytes are present in adult human heart: A study of gender-mismatched bone marrow transplantation patients. Circulation 107:1247–49 [Google Scholar]
  46. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V. et al. 2003. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc. Natl. Acad. Sci. USA 100:12313–18 [Google Scholar]
  47. Laugwitz KL, Moretti A, Lam J, Gruber P, Chen YH. et al. 2005. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433:647–53 [Google Scholar]
  48. Rosenblatt-Velin N, Lepore MG, Cartoni C, Beermann F, Pedrazzini T. 2005. FGF-2 controls the differentiation of resident cardiac precursors into functional cardiomyocytes. J. Clin. Invest. 115:1724–33 [Google Scholar]
  49. Reffelmann T, Kloner RA. 2003. Cellular cardiomyoplasty: cardiomyocytes, skeletal myoblasts, or stem cells for regenerating myocardium and treatment of heart failure. Cardiovasc. Res. 58:358–68 [Google Scholar]
  50. Zimmermann WH, Schneiderbanger K, Schubert P, Didie M, Munzel F. et al. 2002. Tissue engineering of a differentiated cardiac muscle construct. Circ. Res. 90:223–30 [Google Scholar]
  51. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D. et al. 2001. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat. Med. 7:430–36 [Google Scholar]
  52. Itescu S, Kocher AA, Schuster MD. 2003. Myocardial neovascularization by adult bone marrow-derived angioblasts: strategies for improvement of cardiomyocyte function. Heart Fail. Rev. 8:253–58 [Google Scholar]
  53. Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO. et al. 2004. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428:664–68 [Google Scholar]
  54. Rehman J, Li JL, Orschell CM, March KL. 2003. Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107:1164–69 [Google Scholar]
  55. Annex BH, Simons M. 2005. Growth factor-induced therapeutic angiogenesis in the heart: protein therapy. Cardiovasc. Res. 65:649–55 [Google Scholar]
  56. Kuramochi Y, Cote GM, Guo X, Lebrasseur NK, Cui L. et al. 2004. Cardiac endothelial cells regulate reactive oxygen species-induced cardiomyocyte apoptosis through neuregulin-1β/erbB4 signaling. J. Biol. Chem. 279:51141–47 [Google Scholar]
  57. Fukazawa R, Miller TA, Kuramochi Y, Frantz S, Kim YD. et al. 2003. Neuregulin-1 protects ventricular myocytes from anthracycline-induced apoptosis via erbB4-dependent activation of PI3-kinase/Akt. J. Mol. Cell. Cardiol. 35:1473–79 [Google Scholar]
  58. Remondino A, Kwon SH, Communal C, Pimentel DR, Sawyer DB. et al. 2003. β-adrenergic receptor–stimulated apoptosis in cardiac myocytes is mediated by reactive oxygen species/c-Jun NH2-terminal kinase–dependent activation of the mitochondrial pathway. Circ. Res. 92:136–38 [Google Scholar]
  59. Narmoneva D, Davis ME, Vukmirovich R, Kamm RD, Lee RT. 2004. Endothelial cells promote cardiac myocyte survival and spatial reorganization: implications for cardiac regeneration. Circulation 110:962–68 [Google Scholar]
  60. Edelberg JM, Aird WC, Wu W, Rayburn H, Mamuya WS. et al. 1998. PDGF mediates cardiac microvascular communication. J. Clin. Invest. 102:837–43 [Google Scholar]
  61. Edelberg JM, Lee SH, Kaur M, Tang L, Feirt NM. et al. 2002. Platelet-derived growth factor-AB limits the extent of myocardial infarction in a rat model: feasibility of restoring impaired angiogenic capacity in the aging heart. Circulation 105:608–13 [Google Scholar]
  62. Xaymardan M, Zheng JG, Duignan I, Chin A, Holm JM. et al. 2004. Senescent impairment in synergistic cytokine pathways that provide rapid cardioprotection in the rat heart. J. Exp. Med. 199:797–804 [Google Scholar]
  63. Dallabrida SM, Ismail N, Oberle JR, Himes BE, Rupnick MA. 2005. Angiopoietin-1 promotes cardiac and skeletal myocyte survival through integrins. Circ. Res. 96:e8–24 [Google Scholar]
  64. Takahashi K, Ito Y, Morikawa M, Kobune M, Huang J. et al. 2003. Adenoviral-delivered angiopoietin-1 reduces the infarction and attenuates the progression of cardiac dysfunction in the rat model of acute myocardial infarction. Mol. Ther. 8:584–92 [Google Scholar]
  65. Condorelli G, Borello U, De Angelis L, Latronico M, Sirabella D. et al. 2001. Cardiomyocytes induce endothelial cells to trans-differentiate into cardiac muscle: implications for myocardium regeneration. Proc. Natl. Acad. Sci. USA 98:10733–38 [Google Scholar]
  66. Badorff C, Brandes RP, Popp R, Rupp S, Urbich C. et al. 2003. Transdifferentiation of blood-derived human adult endothelial progenitor cells into functionally active cardiomyocytes. Circulation 107:1024–32 [Google Scholar]
  67. Yeh ET, Zhang S, Wu HD, Korbling M, Willerson JT. et al. 2003. Transdifferentiation of human peripheral blood CD34+-enriched cell population into cardiomyocytes, endothelial cells, and smooth muscle cells in vivo. Circulation 108:2070–73 [Google Scholar]
  68. Koyanagi M, Brandes RP, Haendeler J, Zeiher AM, Dimmeler S. 2005. Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: a novel mechanism for cell fate changes. Circ. Res. 96:1039–41 [Google Scholar]
  69. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO. et al. 2003. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425:968–73 [Google Scholar]
  70. Matsuura K, Wada H, Nagai T, Iijima Y, Minamino T. et al. 2004. Cardiomyocytes fuse with surrounding noncardiomyocytes and reenter the cell cycle. J. Cell Biol. 167:351–63 [Google Scholar]
  71. Yue X, Tomanek RJ. 1999. Stimulation of coronary vasculogenesis/angiogenesis by hypoxia in cultured embryonic hearts. Dev. Dyn. 216:28–36 [Google Scholar]
  72. Lee KW, Lip GY, Blann AD. 2004. Plasma angiopoietin-1, angiopoietin-2, angiopoietin receptor tie-2, and vascular endothelial growth factor levels in acute coronary syndromes. Circulation 110:2355–60 [Google Scholar]
  73. Lee SH, Wolf PL, Escudero R, Deutsch R, Jamieson SW. et al. 2000. Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N. Engl. J. Med. 342:626–33 [Google Scholar]
  74. Lee RJ, Springer ML, Blanco-Bose WE, Shaw R, Ursell PC. et al. 2000. VEGF gene delivery to myocardium: deleterious effects of unregulated expression. Circulation 102:898–901 [Google Scholar]
  75. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S. et al. 2001. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103:634–37 [Google Scholar]
  76. Kawamoto A, Tkebuchava T, Yamaguchi J, Nishimura H, Yoon YS. et al. 2003. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 107:461–68 [Google Scholar]
  77. Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R. et al. 2002. Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation 106:3009–17 [Google Scholar]
  78. Kang HJ, Kim HS, Zhang SY, Park KW, Cho HJ. et al. 2004. Effects of intracoronary infusion of peripheral blood stem-cells mobilised with granulocyte-colony stimulating factor on left ventricular systolic function and restenosis after coronary stenting in myocardial infarction: the MAGIC cell randomised clinical trial. Lancet 363:751–56 [Google Scholar]
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