Home LiteratureArticle Details
PMID: 12003666 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S. Review

Potentiation of angiogenic response by ischemic and hypoxic preconditioning of the heart.

Journal of cellular and molecular medicine ·Vol. 6 ·No. 1 ·2002-00-00 ·Pages 13-24

Maulik N, Das DK

Abstract

This review is intended to discuss the newly discovered role of preconditioning which should make it an attractive therapeutic stimulus for repairing the injured myocardium. We recently found that apart from rendering the myocardium tolerant to ischemic reperfusion injury, preconditioning also potentiates angiogenesis. Our study demonstrated for the first time that both ischemic and hypoxic preconditioning triggered myocardial angiogenesis at the capillary and arteriolar levels which nicely corroborated with the improved myocardial contractile function. Hypoxic preconditioning resulted in the stimulation of VEGF, the most potent angiogenic factor known to date. In concert, endothelial cell specific tyrosine kinase receptors, Tie 1, Tie 2 and Flt-1 and Flk-1 were also significantly enhanced in the preconditioned myocardium. The redox-regulated transcription factor NF kappa B was found to play an essential role in the preconditioning regulation of angiogenesis.

MeSH Terms
Animals Coronary Vessels/physiology Endothelial Growth Factors/metabolism Humans Hypoxia/physiopathology Intercellular Signaling Peptides and Proteins/metabolism Ischemic Preconditioning, Myocardial Lymphokines/metabolism Mitogen-Activated Protein Kinases/metabolism Muscle, Smooth, Vascular/cytology,metabolism Myocardium/cytology,metabolism Neovascularization, Physiologic Receptor Protein-Tyrosine Kinases/metabolism Receptor, TIE-1 Receptor, TIE-2 Receptors, Cell Surface/metabolism Receptors, TIE Transcription Factors/metabolism Vascular Endothelial Growth Factor A Vascular Endothelial Growth Factors
Chemicals
Endothelial Growth Factors Intercellular Signaling Peptides and Proteins Lymphokines Receptors, Cell Surface Transcription Factors Vascular Endothelial Growth Factor A Vascular Endothelial Growth Factors Receptor Protein-Tyrosine Kinases Receptor, TIE-1 Receptor, TIE-2 Receptors, TIE Mitogen-Activated Protein Kinases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Maulik Nilanjana
Cardiovascular Research Center, University of Connecticut School of Medicine, Farmington, CT 06030-1110, USA. [email protected]
Das D K
References (80)
80 references, click to expand
  1. Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of Bcl-2 expression.
    Am J Pathol. 1999 Feb;154(2):375-84 PMID: 10027396
  2. Interleukin-1 beta upregulates cardiac expression of vascular endothelial growth factor and its receptor KDR/flk-1 via activation of protein tyrosine kinases.
    J Mol Cell Cardiol. 1999 Mar;31(3):607-17 PMID: 10198191
  3. Vascular endothelial growth factor expression coincides with coronary vasculogenesis and angiogenesis.
    Dev Dyn. 1999 May;215(1):54-61 PMID: 10340756
  4. Suppression of retinal neovascularization by the NF-kappaB inhibitor pyrrolidine dithiocarbamate in mice.
    Invest Ophthalmol Vis Sci. 1999 Jun;40(7):1624-9 PMID: 10359349
  5. Reduction of infarct size in the rat heart by LPS preconditioning is associated with expression of angiogenic growth factors and increased capillary density.
    Shock. 1999 Jul;12(1):25-31 PMID: 10468048
  6. Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/survivin pathway.
    J Biol Chem. 2000 Mar 31;275(13):9102-5 PMID: 10734041
  7. Induction of Tie-1 and Tie-2 receptor protein expression after cerebral ischemia-reperfusion.
    J Cereb Blood Flow Metab. 2001 Jun;21(6):690-701 PMID: 11488538
  8. Hypoxic preconditioning triggers myocardial angiogenesis: a novel approach to enhance contractile functional reserve in rat with myocardial infarction.
    J Mol Cell Cardiol. 2002 Mar;34(3):335-48 PMID: 11945025
  9. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis.
    Nature. 1992 Oct 29;359(6398):843-5 PMID: 1279431
  10. Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro.
    Biochem Biophys Res Commun. 1992 Dec 15;189(2):824-31 PMID: 1281999
  11. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor.
    Science. 1992 Feb 21;255(5047):989-91 PMID: 1312256
  12. ras mediates nerve growth factor receptor modulation of three signal-transducing protein kinases: MAP kinase, Raf-1, and RSK.
    Cell. 1992 Mar 20;68(6):1041-50 PMID: 1312393
  13. A novel endothelial cell surface receptor tyrosine kinase with extracellular epidermal growth factor homology domains.
    Mol Cell Biol. 1992 Apr;12(4):1698-707 PMID: 1312667
  14. Angiogenesis in skeletal and cardiac muscle.
    Physiol Rev. 1992 Apr;72(2):369-417 PMID: 1372998
  15. Salvage of infarcted myocardium by angiogenic action of basic fibroblast growth factor.
    Science. 1992 Sep 4;257(5075):1401-3 PMID: 1382313
  16. Proto-oncogene expression in porcine myocardium subjected to ischemia and reperfusion.
    Circ Res. 1992 Dec;71(6):1351-60 PMID: 1385005
  17. Protective effects of adenosine in myocardial ischemia.
    Circulation. 1992 Mar;85(3):893-904 PMID: 1537125
  18. The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing.
    J Biol Chem. 1991 Jun 25;266(18):11947-54 PMID: 1711045
  19. Intravenous pretreatment with A1-selective adenosine analogues protects the heart against infarction.
    Circulation. 1992 Feb;85(2):659-65 PMID: 1735160
  20. Purification and NH2-terminal amino acid sequence of guinea pig tumor-secreted vascular permeability factor.
    Cancer Res. 1990 Mar 15;50(6):1774-8 PMID: 2155059
  21. Tumor necrosis factor type alpha, a potent inhibitor of endothelial cell growth in vitro, is angiogenic in vivo.
    Proc Natl Acad Sci U S A. 1987 Aug;84(15):5277-81 PMID: 2440047
  22. Macrophage-induced angiogenesis is mediated by tumour necrosis factor-alpha.
    Nature. 1987 Oct 15-21;329(6140):630-2 PMID: 2443857
  23. Different requirements for formation of Jun: Jun and Jun: Fos complexes.
    Genes Dev. 1989 Dec;3(12B):2091-100 PMID: 2516828
  24. Role of glycolytic products in damage to ischemic myocardium. Dissociation of adenosine triphosphate levels and recovery of function of reperfused ischemic hearts.
    Circ Res. 1984 Dec;55(6):816-24 PMID: 6499136
  25. Magnetic resonance mapping demonstrates benefits of VEGF-induced myocardial angiogenesis.
    Nat Med. 1995 Oct;1(10):1085-9 PMID: 7489368
  26. Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model.
    J Clin Invest. 1994 Feb;93(2):662-70 PMID: 7509344
  27. Angiogenic-induced enhancement of collateral blood flow to ischemic myocardium by vascular endothelial growth factor in dogs.
    Circulation. 1994 May;89(5):2183-9 PMID: 7514110
  28. Upregulation of vascular endothelial growth factor expression induced by myocardial ischaemia: implications for coronary angiogenesis.
    Cardiovasc Res. 1994 Aug;28(8):1176-9 PMID: 7525061
  29. Endothelial receptor tyrosine kinases involved in angiogenesis.
    J Cell Biol. 1995 May;129(4):895-8 PMID: 7538139
  30. Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells.
    J Biol Chem. 1995 Aug 25;270(34):19761-6 PMID: 7544346
  31. Hypoxia induces AP-1-regulated genes and AP-1 transcription factor binding in human endothelial and other cell types.
    Biochim Biophys Acta. 1995 Oct 17;1264(1):72-8 PMID: 7578260
  32. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium.
    Nature. 1995 Jul 6;376(6535):66-70 PMID: 7596436
  33. Tumor necrosis factor-alpha gene and protein expression in adult feline myocardium after endotoxin administration.
    J Clin Invest. 1995 Aug;96(2):1042-52 PMID: 7635940
  34. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development.
    Dev Dyn. 1995 May;203(1):80-92 PMID: 7647376
  35. Angiogenic role of endogenous basic fibroblast growth factor released by rat aorta after injury.
    Am J Pathol. 1993 Jul;143(1):181-90 PMID: 7686343
  36. Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. Modulation of gene expression by nitric oxide.
    J Clin Invest. 1995 Apr;95(4):1798-807 PMID: 7706486
  37. Gene expression in acute myocardial stress. Induction by hypoxia, ischemia, reperfusion, hyperthermia and oxidative stress.
    J Mol Cell Cardiol. 1995 Jan;27(1):181-93 PMID: 7760341
  38. A unique signal transduction from FLT tyrosine kinase, a receptor for vascular endothelial growth factor VEGF.
    Oncogene. 1995 Jan 5;10(1):135-47 PMID: 7824266
  39. Involvement of NF-kappa B in the induction of NAD(P)H:quinone oxidoreductase (DT-diaphorase) by hypoxia, oltipraz and mitomycin C.
    Biochem Pharmacol. 1995 Jan 31;49(3):275-82 PMID: 7857313
  40. Hypoxic preconditioning preserves antioxidant reserve in the working rat heart.
    Cardiovasc Res. 1995 Jan;29(1):133-40 PMID: 7895231
  41. Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo.
    Lab Invest. 1994 Sep;71(3):374-9 PMID: 7933988
  42. Rapid induction of vascular endothelial growth factor expression by transient ischemia in rat heart.
    Am J Physiol. 1994 Nov;267(5 Pt 2):H1948-54 PMID: 7977826
  43. Enhanced expression of the tie receptor tyrosine kinase mesenger RNA in the vascular endothelium of metastatic melanomas.
    Cancer Res. 1994 Dec 15;54(24):6571-7 PMID: 7987857
  44. Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant.
    Nature. 1994 Feb 10;367(6463):576-9 PMID: 8107827
  45. Expression of tie-2, a member of a novel family of receptor tyrosine kinases, in the endothelial cell lineage.
    Development. 1993 Nov;119(3):957-68 PMID: 8187650
  46. Preconditioning and post-ischaemic contractile dysfunction: the role of impaired oxygen delivery vs extracellular metabolite accumulation.
    J Mol Cell Cardiol. 1993 Jul;25(7):847-57 PMID: 8230245
  47. Ca2+ preconditioning elicits a unique protection against the Ca2+ paradox injury in rat heart. Role of adenosine. Fixed.
    Circ Res. 1994 Feb;74(2):360-7 PMID: 8293574
  48. Stretch preconditions canine myocardium.
    Am J Physiol. 1994 Jan;266(1 Pt 2):H137-46 PMID: 8304494
  49. Hypoxic preconditioning attenuates stunning caused by repeated coronary artery occlusions in dog heart.
    Cardiovasc Res. 1993 Apr;27(4):559-64 PMID: 8324786
  50. Ischaemic and hypoxic preconditioning enhance postischaemic recovery of function in the rat heart.
    Cardiovasc Res. 1993 Apr;27(4):565-70 PMID: 8324787
  51. Hypoxia is a strong inducer of vascular endothelial growth factor mRNA expression in the heart.
    Biochem Biophys Res Commun. 1993 Sep 15;195(2):1005-10 PMID: 8373380
  52. Molecular cloning and characterization of a novel receptor protein tyrosine kinase from human placenta.
    Oncogene. 1993 Mar;8(3):663-70 PMID: 8382358
  53. Preconditioning against myocardial dysfunction after ischemia and reperfusion by an alpha 1-adrenergic mechanism.
    Circ Res. 1993 Oct;73(4):656-70 PMID: 8396503
  54. Mitogen-activated protein kinases p42mapk and p44mapk are required for fibroblast proliferation.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8319-23 PMID: 8397401
  55. Tie-1 and tie-2 define another class of putative receptor tyrosine kinase genes expressed in early embryonic vascular system.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9355-8 PMID: 8415706
  56. Inducible operation of the erythropoietin 3' enhancer in multiple cell lines: evidence for a widespread oxygen-sensing mechanism.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2423-7 PMID: 8460154
  57. Pretreatment with pertussis toxin blocks the protective effects of preconditioning: evidence for a G-protein mechanism.
    J Mol Cell Cardiol. 1993 Mar;25(3):311-20 PMID: 8510172
  58. Hypoxia-induced paracrine regulation of vascular endothelial growth factor receptor expression.
    J Clin Invest. 1996 Jan 15;97(2):469-76 PMID: 8567969
  59. Hypoxia regulates vascular endothelial growth factor receptor KDR/Flk gene expression through adenosine A2 receptors in retinal capillary endothelial cells.
    Invest Ophthalmol Vis Sci. 1996 Jun;37(7):1311-21 PMID: 8641834
  60. Clinical evidence of angiogenesis after arterial gene transfer of phVEGF165 in patient with ischaemic limb.
    Lancet. 1996 Aug 10;348(9024):370-4 PMID: 8709735
  61. Induction of vascular endothelial growth factor by tumor necrosis factor alpha in human glioma cells. Possible roles of SP-1.
    J Biol Chem. 1996 Nov 8;271(45):28220-8 PMID: 8910439
  62. Ischemic preconditioning triggers the activation of MAP kinases and MAPKAP kinase 2 in rat hearts.
    FEBS Lett. 1996 Nov 4;396(2-3):233-7 PMID: 8914993
  63. Vascular endothelial growth factor administration in chronic myocardial ischemia.
    Am J Physiol. 1996 May;270(5 Pt 2):H1791-802 PMID: 8928888
  64. VEGF, flk-1, and flt-1 expression in a rat myocardial infarction model of angiogenesis.
    Am J Physiol. 1996 May;270(5 Pt 2):H1803-11 PMID: 8928889
  65. An improved permeabilization protocol for the introduction of peptides into cardiac myocytes. Application to protein kinase C research.
    Circ Res. 1996 Dec;79(6):1086-99 PMID: 8943947
  66. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning.
    Cell. 1996 Dec 27;87(7):1161-9 PMID: 8980223
  67. Involvement of interleukin-8, vascular endothelial growth factor, and basic fibroblast growth factor in tumor necrosis factor alpha-dependent angiogenesis.
    Mol Cell Biol. 1997 Jul;17(7):4015-23 PMID: 9199336
  68. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis.
    Science. 1997 Jul 4;277(5322):55-60 PMID: 9204896
  69. Tie2 expression and phosphorylation in angiogenic and quiescent adult tissues.
    Circ Res. 1997 Oct;81(4):567-74 PMID: 9314838
  70. Vascular endothelial growth factor attenuates myocardial ischemia-reperfusion injury.
    Ann Thorac Surg. 1997 Oct;64(4):993-8 PMID: 9354516
  71. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells.
    Oncogene. 1997 Oct;15(18):2169-77 PMID: 9393975
  72. Role of NF-kappaB-mediated interleukin-8 expression in intraocular neovascularization.
    Invest Ophthalmol Vis Sci. 1998 Jun;39(7):1097-106 PMID: 9620068
  73. An essential role of NFkappaB in tyrosine kinase signaling of p38 MAP kinase regulation of myocardial adaptation to ischemia.
    FEBS Lett. 1998 Jun 16;429(3):365-9 PMID: 9662450
  74. Tie2 receptor ligands, angiopoietin-1 and angiopoietin-2, modulate VEGF-induced postnatal neovascularization.
    Circ Res. 1998 Aug 10;83(3):233-40 PMID: 9710115
  75. Regulation of angiopoietin-2 mRNA levels in bovine microvascular endothelial cells by cytokines and hypoxia.
    Circ Res. 1998 Oct 19;83(8):852-9 PMID: 9776732
  76. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation.
    J Biol Chem. 1998 Nov 13;273(46):30336-43 PMID: 9804796
  77. Ischemic preconditioning triggers tyrosine kinase signaling: a potential role for MAPKAP kinase 2.
    Am J Physiol. 1998 Nov;275(5):H1857-64 PMID: 9815094
  78. Critical role of the TIE2 endothelial cell receptor in the development of definitive hematopoiesis.
    Immunity. 1998 Nov;9(5):677-86 PMID: 9846489
  79. Prolonged hypoxia increases vascular endothelial growth factor mRNA and protein in adult mouse brain.
    J Appl Physiol (1985). 1999 Jan;86(1):260-4 PMID: 9887138
  80. On the possible role of reactive oxygen species in angiogenesis.
    Adv Exp Med Biol. 1998;454:295-310 PMID: 9889904
Article Info
Journal
Journal of cellular and molecular medicine
Abbr.
J Cell Mol Med
ISSN
1582-1838
DOI
10.1111/j.1582-4934.2002.tb00308.x
Email
[email protected]
Published
2002-00-00
Pages
13-24
Language
English
Region
England
NLM ID
101083777
PMCID
PMC6740104
Subset
IM
Grants
NHLBI NIH HHS · HL 22559 · United States
NHLBI NIH HHS · HL 33889 · United States
NHLBI NIH HHS · HL 56803 · United States
External Links
PubMed source DOI: 10.1111/j.1582-4934.2002.tb00308.x PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2