Abstract
Emerging evidence supports a novel view of hypertension as a disease of inadequate or aberrant responses to angiogenic growth factors (AGF). Patients with hypertension have reduced microvascular density, with some evidence supporting a primary role for rarefaction in causing hypertension. Two clinical models have demonstrated a link between inhibition of AGF activity and hypertension. A major side effect of bevacizumab, a monoclonal antibody to vascular endothelial growth factor (VEGF), is hypertension. Pre-eclampsia is accompanied by high circulating levels of soluble VEGF receptor-1, which forms inactive complexes with VEGF and placental growth factor (PlGF). Paradoxically, early studies have demonstrated high circulating levels of AGF in hypertension. Several mechanisms may account for this finding including increased vascular stretch, tissue ischemia, compensatory responses, decreased clearance or a combination of these mechanisms. High AGF in hypertension could contribute to clinical sequelae such as peripheral and pulmonary edema, microalbuminuria, and progression of atherosclerosis. However, a role for altered angiogenesis in the pathogenesis of hypertension or its sequelae has not been established. Novel studies to understand the roles of AGF in hypertensive patients are warranted.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- EGFR:
-
epidermal growth factor receptor
- ELISA:
-
enzyme linked immunosorbent assay
- eNOS:
-
endothelial type nitric oxide synthase
- EPC:
-
endothelial progenitor cells
- EPO:
-
erythropoietin
- ERK1/2:
-
extracellular signal-related kinase 1/2
- ET-1:
-
endothelin-1
- ACE(−2):
-
angiotensin converting enzyme (−2)
- AGF:
-
angiogenic growth factor(s)
- AKT:
-
protein kinase B
- AM:
-
adrenomedullin
- ASCOT:
-
the Anglo Scandinavian Cardiac Outcomes Trial
- AT:
-
angiotensin II receptor
- BK:
-
bradykinin
- CHF:
-
congestive heart failure
- FGF-1:
-
fibroblast growth factor-1 (acidic FGF)
- GLUT1:
-
glucose transporter 1
- HGF:
-
hepatocyte growth factor
- HIF1α:
-
hypoxia inducible factor-1α
- IC:
-
intracoronary
- IGF-1:
-
insulin-like growth factor-1
- IV:
-
intravenous
- KDR:
-
kinase insert domain-containing receptor
- LVH:
-
left ventricular hypertrophy
- NEPs:
-
neutral endopeptidases
- PDGF-AB:
-
platelet derived growth factor-AB
- PE:
-
prolyl endopeptidases
- PGI2:
-
prostacyclin
- PKB:
-
protein kinase B
- PlGF:
-
placental growth factor
- SC:
-
subcutaneous
- SHR:
-
spontaneously hypertensive rats
- SU1498:
-
4-amino-5-(4-cholorophenyl)-7-(t-butyl)pyrazolo; [3,4-d]pyrimidine
- SVR:
-
systemic vascular resistance
- TGF-β:
-
transforming growth factor-beta
- VEGF:
-
vascular endothelial growth factor
- VEGFR-2:
-
VEGF receptor-2
- VIVA:
-
VEGF in Ischemia for Vascular Angiogenesis (clinical trial)
- VTI 4:
-
[(4′-chloro-2′-fluoro)phenylamino]-6,7-dimethoxyquinazoline
References
FN Kiefer S Neysari R Humar et al. (2003) ArticleTitleHypertension and angiogenesis Curr Pharm Des 9 1733–44
AS Greene (2003) Microvascular regulation and dysregulation JL Izzo HR Black (Eds) Hypertension Primer EditionNumber3 Lippincott Williams & Wilkins Philadelphia 183–5
A Koller (2002) ArticleTitleSignaling pathways of mechanotransduction in arteriolar endothelium and smooth muscle cells in hypertension Microcirculation 9 277–94
PM Hutchins AE Darnell (1974) ArticleTitleObservation of a decreased number of small arterioles in spontaneously hypertensive rats Circ Res 34 I161–5
FM Hansen-Smith LW Morris AS Greene et al. (1996) ArticleTitleRapid microvessel rarefaction with elevated salt intake and reduced renal mass hypertension in rats Circ Res 79 324–30
JP Noon BR Walker DJ Webb et al. (1997) ArticleTitleImpaired microvascular dilatation and capillary rarefaction in young adults with a predisposition to high blood pressure J Clin Invest 99 1873–9
TFT Antonios FM Rattray DRJ Singer et al. (2003) ArticleTitleRarefaction of skin capillaries in normotensive offspring of individuals with essential hypertension Heart 89 175–8
JM Sullivan RL Prewitt JA Josephs (1983) ArticleTitleAttenuation of the microcirculation in young patients with high-output borderline hypertension Hypertension 5 844–51
P Gasser FR Buhler (1992) ArticleTitleNailfold microcirculation in normotensive and essential hypertensive subjects, as assessed by video-microscopy J Hypertens 10 83–6
HA Henrich W Romen W Heimgartner et al. (1998) ArticleTitleCapillary rarefaction characteristic of the skeletal muscle of hypertensive patients Klin Wochenshrift 66 54–60
A Prasad GS Dunnill PS Mortimer et al. (1995) ArticleTitleCapillary rarefaction in the forearm skin in essential hypertension J Hypertension 13 265–8
WE Sonntag CD Lynch PT Cooney et al. (1997) ArticleTitleDecreases in cerebral microvasculature with age are associated with the decline in growth hormone and insulin-like growth factor 1 Endocrinology 138 3515–20
AS Khan CD Lynch DC Sane et al. (2001) ArticleTitleGrowth hormone increases regional coronary blood flow and capillary density in aged rats J Gerontol Ser A, Biol Sci Med Sci 56 B364–71
TM Edelberg MJ Reed (2003) ArticleTitleAging and angiogenesis Front Biosci 8 s1199–209
PM Hutchins CD Lynch PT Cooney et al. (1996) ArticleTitleThe microcirculation in experimental hypertension and aging Cardiovasc Res 32 772–80
RS Vasan A Beiser S Seshadri et al. (2002) ArticleTitleResidual lifetime risk for developing hypertension in middle-aged women and men JAMA 287 1003–10
DD Ku JE Zaleski S Liu TA Brock (1993) ArticleTitleVascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries Am J Physiol 265 H586–92
RJ Laham J Li M Tofukuji et al. (2003) ArticleTitleSpatial heterogeneity in VEGF-induced vasodilation: VEGF dilates microvessels but not epicardial and systemic arteries and veins Ann Vasc Surg 17 245–52
TD Henry BH Annex GR McKendall et al. (2003) ArticleTitleThe VIVA trial: Vascular endothelial growth factor in Ischemia for Vascular Angiogenesis Circulation 107 1359–65
P Cuevas F Carceller S Ortega et al. (1991) ArticleTitleHypotensive activity of fibroblast growth factor Science 254 1208–10
EF Unger L Goncalves SE Epstein et al. (2000) ArticleTitleEffects of a single intracoronary injection of basic fibroblast growth factor in stable angina pectoris Am J Cardiol 85 1414–9
RJ Laham NA Chronos M Pike et al. (2000) ArticleTitleIntracoronary basic fibroblast growth factor (FGF-2) in patients with severe ischemic heart disease: Results of a phase I open-label dose escalation study J Am Coll Cardiol 36 2132–9
M Simons BH Annex RJ Laham et al. (2002) ArticleTitlePharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: Double-blind, randomized, controlled clinical trial Circulation 105 788–93
JA Keiser MJ. Ryan (1996) ArticleTitleHemodynamic effects of epidermal growth factor in conscious rats and monkeys Proc Natl Acad Sci USA 93 4957–61
H Jin R Yang W Li et al. (2003) ArticleTitleEarly treatment with hepatocyte growth factor improves cardiac function in experimental heart failure induced by myocardial infarction J Pharmacol Exp Ther 304 654–60
PR Ebeling JD Jones WM O’Fallon et al. (1993) ArticleTitleShort-term effects of recombinant human insulin-like growth factor I on bone turnover in normal women J Clin Endocrin Metab 77 1384–7
JG Lainchbury RW Troughton LK Lewis et al. (2000) ArticleTitleHemodynamic, hormonal, and renal effects of short-term adrenomedullin infusion in healthy volunteers J Clin Endocrinol Metab 85 1016–20
I Zachary G Gliki (2001) ArticleTitleSignaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family Cardiovas Res 49 568–81
E Chavakis S. Dimmeler (2002) ArticleTitleRegulation of endothelilal cell survival and apoptosis during angiogenesis Arterioscler Thromb Vasc Biol 22 887–93
S Dimmeler B Fisslthaler I Fleming et al. (1999) ArticleTitleActivation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation Nature 399 601–5
JD Hood CJ Meininger M Ziche et al. (1998) ArticleTitleVEGF upregulates ecNOS message, protein, and NO production in human endothelial cells Am J Physiol 274 H1054–8
JP Cooke (2003) ArticleTitleNO and angiogenesis Atherosclerosis Supplements 4 53–60
M Ziche L Morbidelli R Choudhuri et al. (1997) ArticleTitleNitric oxide synthase lies downstream from vascular endothelial growth factor-induced buy not basic fibroblast growth factor-induced angiogenesis J Clin Invest 99 2625–34
T Murohara T Asahara M Silver et al. (1998) ArticleTitleNitric oxide synthase modulates angiogenesis in response to tissue ischemia J Clin Invest 101 2567–78
Y Shizukuda S Tang R Yokota et al. (1999) ArticleTitleVascular endothelial growth factor-induced endothelial cell migration and proliferation depend on a nitric oxide-mediated decrease in protein kinase Cδ activity Circ Res 85 247–56
H He VJ Venema X Gu et al. (1999) ArticleTitleVascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through Flk-1/KDR activation of c-Src J Biol Chem 274 25130–5
Z-G Jin H Ueba T Tanimoto et al. (2003) ArticleTitleLigand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase Circ Res 93 354–63
M Friedlander PC Brooks RW Shaffer et al. (1995) ArticleTitleDefinition of two angiogenic pathways by distinct αv integrins Science 270 1500–10
JE Mogford GE David SH Platts et al. (1996) ArticleTitleVascular smooth muscle αvβ3 integrin mediates arteriolar vasodilation in response to RGD peptides Circ Res 79 821–6
JYJ Shyy S Chien (2002) ArticleTitleRole of integrins in endothelial mechanosensing of shear stress Circ Res 91 769–75
Y Wang H Miao S Li et al. (2002) ArticleTitleInterplay between integrins and FLK-1 in shear stress-induced signaling Am J Physiol Cell Physiol 283 C1540–7
JC Yang L Haworth RM Sherry et al. (2003) ArticleTitleA randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer NEJM 349 427–34
MA Cobleigh VK Langmuir GW Sledge et al. (2003) ArticleTitleA phase I/II dose-escalation trial of bevacizumab in previously treated metastatic breast cancer Seminars in Oncology 30 IssueIDSuppl 16 117–24
CG Willett Y Boucher E Tomaso Particledi et al. (2004) ArticleTitleDirect evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer Nat Med 10 145–7
AL Thomas B Morgan J Drevs et al. (2003) ArticleTitleVascular endothelial growth factor receptor tyrosine kinase inhibitors: PTK787/ZK 222584 Semin Oncol 30 IssueIDsuppl 6 32–8
DC Felmeden CG Spencer FM Belgore et al. (2003) ArticleTitleEndothelial damage and angiogenesis in hypertensive patients: relationship to cardiovascular risk factors and risk factor management Am J Hypertens 16 11–20
S Nakamura A Moriguchi R Morishita et al. (1998) ArticleTitleA novel vascular modulator, hepatocyte growth factor (HGF), as a potential index of the severity of hypertension Biochem Biophys Res Commun 242 238–43
J Nakao-Hayashi H Ito T Kanayasu et al. (1992) ArticleTitleStimulatory effects of insulin and insulin-like growth factor I on migration and tube formation by vascular endothelial cells Atherosclerosis 92 141–9
RF Nicosia SV Nicosia M Smith (1994) ArticleTitleVascular endothelial growth factor, platelet-derived growth factor, and insulin-like growth factor-1 promote rat aortic angiogenesis in vitro Am J Pathol 145 1023–9
P Delafontaine Y-H Song Y Li (2004) ArticleTitleExpression, regulation, and function of IGF-1, IGF-1R, and IGF-1 binding proteins in blood vessels Arterioscler Thromb Vasc Biol 24 1–10
J. Díez (1999) ArticleTitleInsulin-like growth factor I in essential hypertension Kidney Int 55 744–59
S Cottone A Vadalá MT Mangano et al. (2000) ArticleTitleEndothelium-derived factors in microalbuminuric and nonmicroalbuminuric essential hypertensives Am J Hypertens 13 172–6
A Bagnato F Spinella (2003) ArticleTitleEmerging role of endothelin-1 in tumor angiogenesis Trends Endocrinol Metab 14 44–50
M-J Goumans F Lebrin G Valdimarsdotti (2003) ArticleTitleControlling the angiogenic switch. A balance between two distinct TGF-β receptor signaling pathways Trends Cardiovasc Med 13 301–7
U Derhaschnig M Shehata H Herkner et al. (2002) ArticleTitleIncreased levels of transforming growth factor-β<inf>1</inf> in essential hypertension Am J Hypertens 15 207–11
M Suthanthiran B Li JO Song et al. (2000) ArticleTitleTransforming growth factor-β1 hyperexpression in African–American hypertensives: A novel mediator of hypertension and/or target organ damage Proc Natl Acad Sci USA 97 3479–84
E Porreca CD Febbo E Vitacolonna et al. (2002) ArticleTitleTransforming growth factor-β1 levels in hypertensive patients: association with body mass index and leptin Am J Hypertens 15 759–65
PJ Lijnen VV Petrov RH Fagard (2003) ArticleTitleAssociation between transforming growth factor-β and hypertension Am J Hypertens 16 604–11
R De Matteo CN May (2003) ArticleTitleDirect coronary vasodilator action of adrenomedullin is mediated by nitric oxide Br J Pharmacol 140 1414–20
Y Zhao S Hague S Manek et al. (1998) ArticleTitlePCR display identifies tamoxifen induction of the novel angiogenic factor adrenomedullin by a non estrogenic mechanism in the human endometrium Oncogene 16 409–15
J Kato K Kitamura E Matsui et al. (1999) ArticleTitlePlasma adrenomedullin and natriuretic peptides in patients with essential or malignant hypertension Hypertens Res 22 61–5
JM Roberts DW Cooper (2001) ArticleTitlePathogenesis and genetics of pre-eclampsia Lancet 357 53–6
SE Maynard JY Min J Merchan et al. (2003) ArticleTitleExcess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. JCI 111 649–58
V Tsatsaris F Goffin C Munaut et al. (2003) ArticleTitleOverexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: Pathophysiological consequences J Clin Endocrine Metab 88 5555–63
RJ Levine SE Maynard C Qian et al. (2004) ArticleTitleCirculating angiogenic factors and the risk of preeclampsia New Engl J Med 350 672–83
A Luttun P Carmeliet (2003) ArticleTitleSoluble VEGF receptor Flt1: The elusive preeclampsia factor discovered?. JCI 111 600–2
CG Solomon EW Seely (2004) ArticleTitlePreeclampsia – searching for the cause New Engl J Med 350 641–2
MJ Cross J Dixelius T Matsumoto et al. (2003) ArticleTitleVEGF-receptor signal transduction Trends Biochem Sci 28 488–94
TJ Robelink HC Boer Particlede EJP Koning Particlede A-J Zonneveld Particlevan (2004) ArticleTitleEndothelial progenitor cells: More than an inflammatory response? Arterioscler Thromb Vasc Biol 24 834–8
W Zheng EA Sefton CJ Meininger et al. (2001) ArticleTitleMechanisms of coronary angiogenesis in response to stretch: Role of VEGF and TGF-β Am J Physiol 280 H909–17
Y Feng JH Yang H Huang et al. (1999) ArticleTitleTranscriptional profile of mechanically induced genes in human vascular smooth muscle cells Circ Res 85 1118–23
H Chang K-G Shyu B-W Wang et al. (2003) ArticleTitleRegulation of hypoxia-inducible factor-1α by cyclical mechanical stretch in rat vascular smooth muscle cells Clin Sci 105 447–56
F Kuwahara H Kai K Tokuda et al. (2002) ArticleTitleHypoxia-inducible factor-1α/vascular endothelial growth factor pathway for adventitial vasa vasorum formation in hypertensive rat aorta Hypertension 39 46–50
M Safran WG. Kaelin SuffixJr. (2003) ArticleTitleHIF hydroxylation and the mammalian oxygen-sensing pathway J Clin Invest 111 779–83
CC Chua RC Hamdy BH Chua (1998) ArticleTitleUpregulation of vascular endothelial growth factor by anigiotensin II in rat heart endothelial cells Biochim Biophys Acta 1401 187–194
B Williams AQ Baker B Gallacher et al. (1995) ArticleTitleAngiotensin II increases vascular permeability factor gene expression by human vascular smooth muscle cells Hypertension 25 913–7
R Yang AK Ogasawara TF Zioncheck et al. (2002) ArticleTitleExaggerated hypotensive effect of vascular endothelial growth factor in spontaneously hypertensive rats Hypertension 39 815–20
Dr Senger CA Perruzzi J Feder et al. (1986) ArticleTitleA highly conserved vascular permeability factor secreted by a variety of human and rodent tumor cell lines Cancer Res 46 5629–32
C Lenfant EJ Roccella (1999) ArticleTitleA call to action for more aggressive treatment of hypertension J Hypertens 17 IssueIDSuppl 1 S3–7
DD Heistad WJ Lawton WT Talman (2003) Pathogenesis of acute hypertension encephalopathy JL Izzo HR Black (Eds) Hypertension Primer EditionNumber3 Lippincott Williams & Wilkins Philadelphia 201–3
HJ Schoch S Fischer HH Marti (2002) ArticleTitleHypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain Brain 125 2549–57
J Josko K Knefel (2003) ArticleTitleThe role of vascular endothelial growth factor in cerebral oedema formation Folia Neuropathol 41 161–6
JS Jensen K Borch-Johnsen G Jensen et al. (1995) ArticleTitleMicroalbuminuria reflects a generalized transvascular albumin leakiness in clinically healthy subjects Clin Sci (Colch) 88 629–33
F Mor FJ Quintana IR Cohen (2004) ArticleTitleAngiogenesis-inflammation cross-talk: Vascular endothelial growth factor is secreted by activated T cells and induces Th1 polarization J Immunol 172 4618–23
I Kim S-O Moon SH Kim et al. (2001) ArticleTitleVascular endothelial growth factor expression of intercellular adhesion molecule 1 (ICAM-1), vascular cell adhesion molecule 1 (VCAM-1), and E-selectin through nuclear factor-κB activation in endothelial cells J Biol Chem 276 7614–20
T Arisato T Hashiguchi KP Sarker et al. (2003) ArticleTitleHighly accumulated platelet vascular endothelial growth factor in coagulant thrombotic region J Thromb Haemost 1 2589–93
BQ Shen DY Lee KM Cortopassi et al. (2001) ArticleTitleVascular endothelial growth factor KDR receptor signaling potentiates tumor necrosis factor-induced tissue factor expression in endothelial cells J Biol Chem 276 5281–6
V Eremina M Sood J Haigh et al. (2003) ArticleTitleGlomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal disease J Clin Invest 111 707–16
E Bortoloso D Prete M Vestra et al. (2004) ArticleTitleQuantitate and qualitative changes in vascular endothelial growth factor gene expression in glomeruli of patients with type 2 diabetes Eur J Endocrinol 150 799–807
V Eremina M Sood J Haigh et al. (2003) ArticleTitleGlomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal disease J Clin Invest 111 707–16
FW Asselbergs RA deBoer GFH Diercks et al. (2004) ArticleTitleVascular endothelial growth factor: the link between cardiovascular risk factors and microalbuminuria? Int J Cardiol 93 211–5
F Santilli A Spagnoli A Mohn et al. (2001) ArticleTitleIncreased vascular endothelial growth factor serum concentrations may help identify patients with onset of Type I diabetes during childhood at risk for developing persistent microalbuminuria J Clin Endocrinol Metab 86 3871–6
S Cottone A Vadalá MT Mangano et al. (2000) ArticleTitleEndothelium-derived factors in microalbuminuric and nonmicroalbuminuric essential hypertensives Am J Hypertens 13 172–6
LT Cooper WR Hiatt MA Creager et al. (2001) ArticleTitleProteinuria in a placebo-controlled study of basic fibroblast growth factor for intermittent claudication Vasc Med 6 235–9
RS Vasan A Beiser S Seshadri et al. (2002) ArticleTitleResidual lifetime risk for developing hypertension in middle-aged women and men: The Framingham Heart Study JAMA 287 1003–10
RJ Scheubel H Zorn RE Silber et al. (2003) ArticleTitleAge-dependent depression in circulating endothelial progenitor cells in patients undergoing coronary artery bypass grafting J Am Coll Cardiol 42 2073–80
D Goodman-Gruen E Barrett-Connor (1997) ArticleTitleEpidemiology of insulin-like growth factor-I in elderly men and women The Rancho Bernardo Study. Am J Epidemiol 145 970–6
TB Harris D Kiel R Roubenoff et al. (1997) ArticleTitleAssociation of insulin-like growth factor-I with body composition weight history, and past health behaviors in the very old: the Framingham Heart Study J Am Ger Soc 45 133–9
S Dimmeler M Vasa-Nicotera (2003) ArticleTitleAging of progenitor cells: Limitation for regenerative capacity? J Am Coll Cardiol 42 2081–2
C Emanueli MB Salis T Stacca et al. (2002) ArticleTitleAngiotensin AT1 receptor signaling modulates reparative angiogenesis induced by limb ischemia Br J Pharmacol 135 87–92
DH Munzemaier AS Greene (1996) ArticleTitleOpposing actions of antgiotensin II on microvascular growth and arterial blood pressure Hypertension 27 760–5
FA Le Noble NH schreurs HW Straaten Particlevan et al. (1993) ArticleTitleEvidence for a novel angiotensin II receptor involved in angiogenesis in chick embryo chorioallantoic membrane Am J Physiol 264 R460–5
LA Fernandez J Twickler A Mead (1985) ArticleTitleNeovascularization produced by angiotensin II J Lab Invest Clin 105 R141–5
EL Page GA Robitaille J Poussegur et al. (2002) ArticleTitleInduction of hypoxia-inducible factor-1α by transcriptional and translational mechanisms J Biol Chem 277 48403–9
A Otani H Takagi K Suzuma Y Honda (1998) ArticleTitleAngiotensin II potentiates vascular endothelial growth factor-induced angiogenic activity in retinal microcapillary endothelial cells Circ Res 82 619–28
SL Amaral JR Linderman MM Morse et al. (2001) ArticleTitleAngiogenesis induced by electrical stimulation is mediated by angiotensin II and VEGF Microcirculation 8 57–67
M Stoll UM Steckelings M Paul et al. (1995) ArticleTitleThe angiotensin AT2-receptor mediates inhibition of cell proliferation in coronary endothelial cells J Clin Invest 95 651–7
K Sasaki T Murohara H Ikeda et al. (2002) ArticleTitleEvidence for the importance of angiotensin II type 1 receptor in ischemia-induced angiogenesis J Clin Invest 109 603–11
H Toko Y Zou T Minamino et al. (2004) ArticleTitleAngiotensin II type 1a receptor is involved in cell infiltration, cytokine production, and neovascularization in infarcted myocardium Arterioscler Thromb Vasc Biol 24 664–70
OV Volpert WF Ward MW Lingen et al. (1996) ArticleTitleCaptopril inhibits angiogenesis and slows the growth of experimental tumors in rats J Clin Invest 98 671–9
JS Silvestre R Tamarat T Senbonmatsu et al. (2002) ArticleTitleAntiangiogenic effect of angiotensin II type 2 receptor in ischemia-induced angiogenesis in mice hindlimb Circ Res 90 1072–9
R Benndorf RH Böger S Ergün et al. (2003) ArticleTitleAngiotensin II type 2 receptor inhibits vascular endothelial growth factor-induced migration and in vitro tube formation of human endothelial cells Circ Res 93 438–47
BI Levy (2004) ArticleTitleCan angiotensin II type 2 receptors have deleterious effects in cardiovascular disease? Implications for therapeutic blockade of the renin-angiotensin system Circulation 109 8–13
T Walther A Menrad H Orzechowski et al. (2003) ArticleTitleDifferential regulation of in vivo angiogenesis by angiotensin II receptors FASEB J 17 2061–7
M De Gaspara KJ Catt T Inagami et al. (2000) ArticleTitleInternational union of pharmacology. XXXII. The angiotensin II receptors Pharmacol Rev 52 415–72
CM Ferrario KB Brosnihan DI Diz et al. (1991) ArticleTitleAngiotensin-(1-7): A new hormone of the angiotensin system Hypertension 18 IssueIDSuppl 5 126–33
EJ Freeman GM Chisolm CM Ferrario et al. (1996) ArticleTitleAngiotensin-(1-7) inhibits vascular smooth muscle cell growth Hypertension 28 104–8
W Zeng MA Hong L Wang et al. (2001) ArticleTitleThe role of angiontensin-(1-7) in the proliferative response of vascular smooth cells induced by endothelin-1 Chin J Geriatr Cardiovasc Cerebrovasc Dis 3 107–9
WB Strawn CM Ferrario EA Tallant (1999) ArticleTitleAngiotensin-(1-7) reduces smooth muscle growth after vascular injury Hypertension 33 207–11
RD Machado RA Santos SP Andrade (2000) ArticleTitleOpposing actions of angiotensins on angiogenesis Life Sci 66 67–76
RD Machado RA Santos SP Andrade (2001) ArticleTitleMechanisms of angiotensin- (1-7)-induced inhibition of angiogenesis Am J Physiol Regul Integr Comp Physiol 280 R994–1000
NE Cameron MA Cotter S Robertson (1992) ArticleTitleAngiotensin converting enzyme inhibition prevents development of muscle and nerve dysfunction and stimulates angiogenesis in streptozotocin-diabetic rats Diabetologia 35 12–18
P Gohlke I Kuwer A Schnell et al. (1997) ArticleTitleBlockade of bradykinin B2 receptors prevents the increase in capillary density induced by chronic angiotensin-converting enzyme inhibitor treatment in stroke-prone spontaneously hypertensive rats Hypertension. 29 478–82
JE Fabre A Rivard M Magner et al. (1999) ArticleTitleTissue inhibition of angiotensin-converting enzyme activity stimulates angiogenesis in vivo Circulation 99 3043–49
JO Kokkonen KA Lindstedt A Kuoppala et al. (2000) ArticleTitleKinin-degrading pathways in the human heart Trends Cardiovasc Med 10 42–5
JS Silvestre S Bergaya R Tamarat et al. (2001) ArticleTitleProangiogenic effect of angiotensin-converting enzyme inhibition is mediated by the bradykinin B2 receptor pathway Circ Res 89 678–83
J Celerier A Cruz N Lamande et al. (2002) ArticleTitleAngiotensinogen and its cleaved derivatives inhibit angiogenesis Hypertension 39 224–28
D Tewksbury (1990) Angiotensinogen: Biochemistry and molecular biology JH Laragh GM Brenner (Eds) Hypertension. Raven Press New York 1197–216
RW Colman BA Jameson Y Lin et al. (2000) ArticleTitleDomain 5 of high molecular weight kininogen (kinostatin) down-regulates endothelial cell proliferation and migration and inhibits angiogenesis Blood 95 543–50
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sane, D.C., Anton, L. & Brosnihan, K.B. Angiogenic growth factors and hypertension. Angiogenesis 7, 193–201 (2004). https://doi.org/10.1007/s10456-004-2699-3
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10456-004-2699-3