Home LiteratureArticle Details
PMID: 11877468 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Evidence for the importance of angiotensin II type 1 receptor in ischemia-induced angiogenesis.

The Journal of clinical investigation ·Vol. 109 ·No. 5 ·2002-03-00 ·Pages 603-11

Sasaki K, Murohara T, Ikeda H, Sugaya T, Shimada T, Shintani S, Imaizumi T

Abstract

The role of the renin-angiotensin system (RAS) in angiogenesis is little known. Here, we show that the angiotensin II (ATII) type 1 (AT1) receptor plays an important role in ischemia-induced angiogenesis. Well-developed collateral vessels and angiogenesis were observed in wild-type (WT) mice in response to hindlimb ischemia, whereas these responses were reduced in ATII type 1a receptor knockout (AT1a(-/-)) mice. Ischemia-induced angiogenesis was also impaired in WT mice treated with the AT1 receptor blocker TCV-116. These effects were not due to reduced systemic blood pressure (SBP), because hydralazine treatment preserved angiogenesis in WT mice although it reduced SBP to a level similar to that of AT1a(-/-) mice. Infiltration of inflammatory mononuclear cells (MNCs), including macrophages and T lymphocytes, was suppressed in the ischemic tissues of AT1a(-/-) mice compared with WT mice. Double immunofluorescence staining revealed that infiltrated macrophages and T lymphocytes expressed VEGF, and the expression of VEGF and monocyte chemoattractant protein-1 was also decreased in AT1a(-/-). Finally, the impaired angiogenesis in AT1a(-/-) mice was rescued by intramuscular transplantation of MNCs obtained from WT mice, further indicating the importance of MNC infiltration in ischemia-induced angiogenesis. Thus, the ATII--AT1 receptor pathway promotes early angiogenesis by supporting inflammatory cell infiltration and angiogenic cytokine expression.

MeSH Terms
Angiotensin Receptor Antagonists Animals Blood Pressure/drug effects,physiology Capillaries/pathology Chemokine CCL2/physiology Endothelial Growth Factors/physiology Hindlimb/blood supply Hydralazine/pharmacology Imidazoles/pharmacology Inflammation/etiology,pathology Ischemia/complications,physiopathology Leukocytes, Mononuclear/pathology,transplantation Lymphokines/physiology Male Mice Mice, Inbred C57BL Mice, Knockout Neovascularization, Pathologic/etiology,physiopathology Pyridines/pharmacology Receptor, Angiotensin, Type 1 Receptors, Angiotensin/deficiency,genetics,physiology Vascular Endothelial Growth Factor A Vascular Endothelial Growth Factors
Chemicals
Angiotensin Receptor Antagonists Chemokine CCL2 Endothelial Growth Factors Imidazoles Lymphokines Pyridines Receptor, Angiotensin, Type 1 Receptors, Angiotensin Vascular Endothelial Growth Factor A Vascular Endothelial Growth Factors PD 123319 Hydralazine
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Sasaki Ken
The Cardiovascular Research Institute, and Department of Internal Medicine III, Kurume University School of Medicine, Kurume, Japan.
Murohara Toyoaki
Ikeda Hisao
Sugaya Takeshi
Shimada Toshifumi
Shintani Satoshi
Imaizumi Tsutomu
References (50)
50 references, click to expand
  1. Chymase as a proangiogenic factor. A possible involvement of chymase-angiotensin-dependent pathway in the hamster sponge angiogenesis model.
    J Biol Chem. 2000 Feb 25;275(8):5545-52 PMID: 10681534
  2. Age-dependent impairment of angiogenesis.
    Circulation. 1999 Jan 5-12;99(1):111-20 PMID: 9884387
  3. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells.
    J Biol Chem. 2000 Sep 1;275(35):26765-71 PMID: 10837481
  4. Angiotensin II receptor subtypes in the skeletal muscle vasculature of patients with severe congestive heart failure.
    Circulation. 2000 Oct 31;102(18):2210-3 PMID: 11056094
  5. Hypercholesterolemia inhibits angiogenesis in response to hindlimb ischemia: nitric oxide-dependent mechanism.
    Circulation. 2000 Nov 7;102(19 Suppl 3):III370-6 PMID: 11082416
  6. Retinal neovascularization is prevented by blockade of the renin-angiotensin system.
    Hypertension. 2000 Dec;36(6):1099-104 PMID: 11116132
  7. Local delivery of human tissue kallikrein gene accelerates spontaneous angiogenesis in mouse model of hindlimb ischemia.
    Circulation. 2001 Jan 2;103(1):125-32 PMID: 11136697
  8. Time course of arteriogenesis following femoral artery occlusion in the rabbit.
    Cardiovasc Res. 2001 Feb 16;49(3):609-17 PMID: 11166274
  9. Augmentation of postnatal neovascularization with autologous bone marrow transplantation.
    Circulation. 2001 Feb 13;103(6):897-903 PMID: 11171801
  10. Angiotensin II type 1 receptor blockers.
    Circulation. 2001 Feb 13;103(6):904-12 PMID: 11171802
  11. Essential hypertension: renin and aldosterone, heart attack and stroke.
    N Engl J Med. 1972 Mar 2;286(9):441-9 PMID: 4257928
  12. Balloon angioplasty enhances the expression of angiotensin II AT1 receptors in neointima of rat aorta.
    J Clin Invest. 1992 Nov;90(5):1707-12 PMID: 1331171
  13. Angiotensin II receptors and angiotensin II receptor antagonists.
    Pharmacol Rev. 1993 Jun;45(2):205-51 PMID: 8372104
  14. Involvement of platelet-endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo.
    Science. 1993 Dec 3;262(5139):1580-2 PMID: 8248808
  15. Angiotensin II receptor antagonist TCV-116 induces regression of hypertensive left ventricular hypertrophy in vivo and inhibits the intracellular signaling pathway of stretch-mediated cardiomyocyte hypertrophy in vitro.
    Circulation. 1994 May;89(5):2204-11 PMID: 8181146
  16. Cardioprotective effect of the angiotensin II type 1 receptor antagonist TCV-116 on ischemia-reperfusion injury.
    Am Heart J. 1994 Jul;128(1):1-6 PMID: 8017262
  17. Regulation of gene transcription of angiotensin II receptor subtypes in myocardial infarction.
    J Clin Invest. 1995 Jan;95(1):46-54 PMID: 7814645
  18. Characterization of the angiotensin II receptor antagonist TCV-116 in healthy volunteers.
    Hypertension. 1995 Jan;25(1):14-21 PMID: 7843746
  19. Captopril increases skin microvascular blood flow secondary to bradykinin, nitric oxide, and prostaglandins.
    FASEB J. 1995 Mar;9(5):411-8 PMID: 7896012
  20. Regulation of blood pressure by the type 1A angiotensin II receptor gene.
    Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3521-5 PMID: 7724593
  21. Angiotensin II increases vascular permeability factor gene expression by human vascular smooth muscle cells.
    Hypertension. 1995 May;25(5):913-7 PMID: 7737726
  22. Proposed update of angiotensin receptor nomenclature.
    Hypertension. 1995 May;25(5):924-7 PMID: 7737728
  23. Angiotensin II type 1a receptor-deficient mice with hypotension and hyperreninemia.
    J Biol Chem. 1995 Aug 11;270(32):18719-22 PMID: 7642517
  24. Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis.
    Cancer Res. 1995 Sep 15;55(18):4140-5 PMID: 7545086
  25. Angiogenesis in cancer, vascular, rheumatoid and other disease.
    Nat Med. 1995 Jan;1(1):27-31 PMID: 7584949
  26. Monocyte infiltration and adhesion molecules in a rat model of high human renin hypertension.
    Hypertension. 1999 Jan;33(1 Pt 2):389-95 PMID: 9931135
  27. Vascular injury causes neointimal formation in angiotensin II type 1a receptor knockout mice.
    Circ Res. 1999 Feb 5;84(2):179-85 PMID: 9933249
  28. Angiotensin II AT1-receptor blockade inhibits monocyte activation and adherence in transgenic (mRen2)27 rats.
    J Cardiovasc Pharmacol. 1999 Mar;33(3):341-51 PMID: 10069667
  29. Angiotensin II plays a pathogenic role in immune-mediated renal injury in mice.
    J Clin Invest. 1999 Mar;103(5):627-35 PMID: 10074479
  30. Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization.
    J Clin Invest. 1999 May;103(9):1231-6 PMID: 10225965
  31. Tissue inhibition of angiotensin-converting enzyme activity stimulates angiogenesis in vivo.
    Circulation. 1999 Jun 15;99(23):3043-9 PMID: 10368123
  32. Impaired collateral vessel development associated with reduced expression of vascular endothelial growth factor in ApoE-/- mice.
    Circulation. 1999 Jun 22;99(24):3188-98 PMID: 10377084
  33. Upregulation of renin-angiotensin system during differentiation of monocytes to macrophages.
    J Hypertens. 1999 Apr;17(4):537-45 PMID: 10404956
  34. Angiotensin II stimulates intercellular adhesion molecule-1 (ICAM-1) expression by human vascular endothelial cells and increases soluble ICAM-1 release in vivo.
    Circulation. 1999 Oct 12;100(15):1646-52 PMID: 10517737
  35. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization.
    J Clin Invest. 2000 Jun;105(11):1527-36 PMID: 10841511
  36. Blockade of platelet endothelial cell adhesion molecule-1 protects against myocardial ischemia and reperfusion injury in cats.
    J Immunol. 1996 May 1;156(9):3550-7 PMID: 8617985
  37. Captopril inhibits angiogenesis and slows the growth of experimental tumors in rats.
    J Clin Invest. 1996 Aug 1;98(3):671-9 PMID: 8698858
  38. Chronic blockade of AT2-subtype receptors prevents the effect of angiotensin II on the rat vascular structure.
    J Clin Invest. 1996 Jul 15;98(2):418-25 PMID: 8755652
  39. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis.
    Cell. 1996 Aug 9;86(3):353-64 PMID: 8756718
  40. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma.
    Cancer Res. 1996 Oct 15;56(20):4625-9 PMID: 8840975
  41. Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion.
    Circ Res. 1997 Jun;80(6):829-37 PMID: 9168785
  42. Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb.
    J Clin Invest. 1998 Jan 1;101(1):40-50 PMID: 9421464
  43. Effect of lisinopril on progression of retinopathy in normotensive people with type 1 diabetes. The EUCLID Study Group. EURODIAB Controlled Trial of Lisinopril in Insulin-Dependent Diabetes Mellitus.
    Lancet. 1998 Jan 3;351(9095):28-31 PMID: 9433426
  44. Angiotensin II potentiates vascular endothelial growth factor-induced angiogenic activity in retinal microcapillary endothelial cells.
    Circ Res. 1998 Mar 23;82(5):619-28 PMID: 9529167
  45. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia.
    J Clin Invest. 1998 Jun 1;101(11):2567-78 PMID: 9616228
  46. Mouse model of angiogenesis.
    Am J Pathol. 1998 Jun;152(6):1667-79 PMID: 9626071
  47. Angiotensin II regulates cellular immune responses through a calcineurin-dependent pathway.
    J Clin Invest. 1999 Dec;104(12):1693-701 PMID: 10606623
  48. Important role of local angiotensin II activity mediated via type 1 receptor in the pathogenesis of cardiovascular inflammatory changes induced by chronic blockade of nitric oxide synthesis in rats.
    Circulation. 2000 Jan 25;101(3):305-10 PMID: 10645927
  49. Do inhibitors of angiotensin-I-converting enzyme protect against risk of cancer?
    Lancet. 1998 Jul 18;352(9123):179-84 PMID: 9683206
  50. Lack of hypoxic stimulation of VEGF secretion from neutrophils and platelets.
    Am J Physiol Heart Circ Physiol. 2000 Aug;279(2):H817-24 PMID: 10924082
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2002-03-00
Pages
603-11
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC150887
Subset
IM
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: product@genelibs.com