Reviews |
From the Max-Planck-Institute for Physiological and Clinical Research, Bad Nauheim, Germany.
Correspondence to Wolfgang Schaper, MD, PhD, Dsci, Max-Planck-Institute for Physiological and Clinical Research, Dept. of Experimental Cardiology, Benekestrasse 2, 61231 Bad Nauheim, Germany. E-mail w.schaper{at}kerckhoff.mpg.de
This Review is part of a thematic series on Angiogenesis, which includes the following articles:
Endothelial Progenitor Cells: Characterization and Role in Vascular Biology
Bone MarrowDerived Cells for Enhancing Collateral Development: Mechanisms, Animal Data, and Initial Clinical Experiences
Influence of Mechanical, Cellular, and Molecular Factors on Collateral Artery Growth (Arteriogenesis)
Innate Immunity and Angiogenesis
Syndecans
Growth Factors and Blood Vessels: Differentiation and Maturation
Ralph Kelly Guest Editor
| Abstract |
|---|
|
|
|---|
Key Words: arteriogenesis shear stress monocytes vascular remodeling leukocytes
| Introduction |
|---|
|
|
|---|
It has become common knowledge for many years that blood vessels regress when not constantly perfused, that they enlarge when chronically exposed to high flows, and that their walls become thicker with high pressures. This gives a hint that different physical forces lead to a different outcome. However, the exact cellular and molecular mechanisms responsible for the remodeling of the vascular system are still not completely unraveled. Mature collateral vessels differ only in minor histological aspects from normal arteries of the conductance type: they are muscular and contain more collagen and exhibited transiently during the growth process a significant intima consisting of smooth muscle cells in the synthetic and proliferative phenotype. However, they differ markedly in their anatomical appearance: they are sometimes excessively tortuous.1 In the reentry region, they join up with the distal part of the occluded artery at nonphysiological angles, which adds to the resistance toward flow. Collateral arteries can develop relatively quickly provided a preexistent network of arterioles had existed before occlusion of the artery but they can also quickly regress when the occluded artery is opened up again.2 This may also be the case when the subtended tissue had atrophied or is not used to full potential like in the peripheral circulation supplying the muscles of the leg. Most often, an occluded artery is not replaced by one single large collateral vessel but rather by several smaller ones. But this arrangement is inefficient because according to the Poiseuilles Law the energy losses created by the resistance of the contributing vessels are additive. During the course of collateral artery development many of the smaller contributing vessels regress, whereas the larger ones increase in diameter and make the system more efficient. However, no ideal adaptation is reached. At optimal conditions (no tissue loss after arterial occlusion), collateral vessels recover only approximately 40% of the maximal conductance (flow at a given blood pressure at maximal vasodilatation). This was shown for the canine heart and for the peripheral circulation in pigs, rabbits, and mice.35 Many efforts were made to improve this rather limited recovery by the application of growth factors or their genes. However, improvement by only a few percentage points and only during a narrow window of time after arterial occlusion was achieved. As early as one week after occlusion the system becomes unresponsive to exogenous growth factors because the growth factor receptors had been downregulated.6 Normal arteries are, of course, totally immune against exogenous growth factors. With these restrictions and imperfections of the collateral circulation in mind one has to ask the question whether interventions to stimulate arteriogenesis have a chance of success. If the degree of adaptation by collateral vessels was already imperfect in young animals, what would the chance of success be in elderly human patients experiencing atherosclerosis and/or diabetes mellitus?
One of the most impressive observations of growing collateral arteries is their typical corkscrew-like pattern, which is a consequence of growth in length between two fixed points. Assuming that a combination of growth factors and genetically altered stem cells would indeed restart the growth cycle, would that further increase collateral tortuosity and length? If so, the system may be self-inhibiting because both would increase resistance, thus negatively influencing blood flow conductance.7 The effect of tortuosity on resistance can be expressed by the Dean number (De), which was developed from the Reynolds number (the Reynolds number describes at which point laminar flow turns into turbulent flow) as a correction for curvature flows:
|
|
where D indicates diameter; V, velocity;
, density; L, length; µ, viscosity; and R, radius of curvature. Turbulent flow is not present in small animals because blood flow velocities are too low and the Reynolds number does not achieve a critical value. However, the Dean number nevertheless can be used to estimate the influence of length (L) and tortuosity (radius of curvature, R) on collateral blood flow.
| Physical Forces |
|---|
|
|
|---|
|
|
|
The equation that already includes blood viscosity (
) and the internal radius of a vessel (R), demonstrates that increased blood flow (Q) will directly result in increased FSS (
).8
Furthermore, the wall of the collateral arteriole is influenced by pressure-related forces like longitudinal-, circumferential-, and radial wall stresses. The distention of the vessel wall, structurally weakened by matrix digestion, by the intravascular pressure, increases the circumferential wall stress, a known activator of smooth muscle cells (SMCs) proliferation.9
In contrast, FSS is a relatively weak force, more than two orders of magnitude lower than the pressure-derived forces acting on the arterial wall. The difference is so impressive that other authors questioned the morphogenic force of FSS or posed the hypothesis that FSS can act only in concert with the pressure-dependent forces.9
So far the influence of FSS on arteriogenesis, although highly suggestive, had remained conjectural and the evidence correlative, especially because FSS is almost impossible to measure in small collaterals. Our group recently proposed a decisive experiment where FSS was suddenly increased some time after femoral artery occlusion without changes in the other forces. The experiment consisted of the drainage of most of the collateral blood flow into the venous system by creating an arteriovenous anastomosis between the distal stump of the occluded femoral artery and the accompanying vein.10 Thereby, the reentrant pressure was "clamped" near venous levels and early pressure rises were prevented during the course of collateral artery enlargement. The chronically increased FSS in this experimental setting led to a strongly amplified recapitulation of the endothelial activation as the primary physiological response to FSS and subsequently to monocyte invasion. Finally, collateral artery growth was markedly improved. Normal maximal conductance was indeed reached, thereby answering one of the above hypotheses in the affirmative: yes, it is possible to functionally replace an occluded artery completely by collaterals.
The question how the endothelial cell senses FSS and transforms the signal into a change in gene expression is also not yet completely decided. Ingbers "tensegrity" model suggests an elegant explanation.1113 The tight coupling of the cell membrane with the cytoskeleton forms a tensegrity architecture so that the entire cell, when deformed by FSS, acts as a sensor. In addition, the model includes a hypothesis that the cytoskeleton orients much of the cells metabolic and signal transduction machinery like induction of gene expression and cell differentiation.
However, before the tensegrity structure is deformed, the FFS has to be detected by sensitive structures like integrins, tyrosine kinase receptors, caveolae, and several ion channels within the endothelial cell membrane.1416 An intermediary function is suggested for the actin filaments of the cytoskeleton. It was shown that the endothelial cytoskeleton is at least indirectly (eg, via a signaling cascade including G-proteins and MAPKinases) connected to all shear stress receptors,17,18 which were shown to signal to several endothelial compartments including the nucleus.19,20 More than 40 genes have been reported to contain shear stress responsive elements (SSRE) within their promoter. The biomechanical stimulus finally leads to marked alterations in the expression of numerous genes.2124 Reproducing these in vitro finding in suitable animal models is lagging behind.
Several questions need to be addressed at this point: the cytoskeletal and contractile apparatus of both endothelial and SMCs are rapidly downregulated (resulting in a complete phenotype change) and would not be able to sense FSS after a few days. Another problem is that the collateral endothelium is deformed by FSS, but because of the weakness of this force, it cannot mechanically transmit the disturbance to the underlying layer of smooth muscle from which it is shielded by the extracellular matrix and the internal elastic lamina. A transmission of paracrine signals via junctions between the endothelium and smooth muscle can also be excluded because of the lack of such structures. Of course, diffusional signal transmission is possible and well known for vasoactive agents like sympathomimetics or vasodilators. But growth factors, cytokines, and proteases, necessary for collateral growth, have initially only limited access to SMCs, which is the cell population that expands most in arteriogenesis. Therefore, the development of collateral arteries requires the tear-down of the barriers to signal transmission.
| FSS Activates Endothelium: Prerequisite for Cell-to-Cell Interactions at the Collateral Vessel Wall |
|---|
|
|
|---|
Although the physiological meaning of the endothelial swelling for the arteriogenic process is not completely elucidated, it has become evident that the induction of expression of multiple genes mainly initiates a machinery to trigger attraction and adhesion of circulating blood cells. Mostly genes are upregulated that code for chemoattractant or activating cytokines including growth factors or for adhesion molecules.7,2835 Thus, the collateral endothelium converts from a quiescent vessel layer with very low adhesion tendency into a highly activated one, which is now supporting attraction, activation, and adhesion of leukocytes (of which monocytes and lymphocytes are examined best). Furthermore, surface expression of adhesion molecules like selectins, intercellular adhesion molecules (ICAM-1 and ICAM-2), and vascular cell adhesion molecules (VCAM-1) on endothelial cells is not only increased but they are also clustered in focal adhesion complexes. In previous studies, it was demonstrated that factors like VEGF and MCP-1, released by endothelial cells, have the ability to stimulate integrin expression on monocytes and increase cell adhesion.3638 In addition, a rapid conformation change converts the integrins into an active state.
Mainly two integrins are responsible for the interaction of monocytes with endothelial cells: the heterodimeric proteins Mac-1 and LFA-1, which belong to the group of ß2-integrins. Both molecules have the ß2-subunit in common. The second subunit of Mac-1 is the
M-integrin and of LFA-1 is the
L-integrin. The monocyte interaction with the collateral endothelium is a complex multistep process (Figure 2). After the initial monocyte interaction with the vascular endothelium, which is called "rolling" and is mediated by several selectins, the tight monocyte adhesion to the collateral endothelium is triggered by Mac-1 and LFA-1. These integrins interact with their corresponding adhesion molecules on the endothelial cell surface, preferably ICAM-1, ICAM-2, and VCAM-1, now preferably clustered in focal adhesion complexes.39 In immunohistological studies, we could show that expression of ICAM-1 was markedly increased on endothelial cells of activated collateral arterioles.7,40
|
|
| Monocytes Invade the Collateral Vessel Wall |
|---|
|
|
|---|
4/ß1-integrin).42 However, in our in vitro experiments, both interaction steps were completely inhibited by blocking the ß2-ICAM-1 pathway. Thus, the role of VLA-4 and VCAM-1 for monocyte adhesion to the collateral endothelium and their subsequent transmigration remains open and needs to be further investigated. On the other hand, VCAM-1 was found to be overexpressed in all layers of the collateral vessel wall under conditions of markedly elevated and chronically acting FSS (Figure 3).42a
Monocytes/macrophages adhere first to the endothelium but are later recruited from venules and accumulate in the perivascular space of growing collateral vessels. This starts at
12 hours after occlusion and peaks between one and three days.43 On their migration from the intraluminal side of the collateral arteriole toward deeper vessel wall regions, monocytes have to overcome barriers, ie, the internal elastic lamina and the extracellular matrix. Monocytes are potent producers of proteases like matrix-metalloproteinases and u-PA.4446 Their proteolytic activity could open these barriers and create the gaps by which monocytes could invade the vascular wall. This results in the required tear-down of the barriers to signal transmission and may establish the possibility for paracrine signaling between the endothelium and the smooth muscle cells. In parallel with that, SMCs develop an intercellular signaling system de novo: connexin37, which is a highly specific marker for developing collateral vessels.
| Circulating Blood Monocytes Are Critical Mediators of Arteriogenesis |
|---|
|
|
|---|
We were also interested in the pathway involved in monocyte attraction. What do mediators signal to the monocytes to travel to the collateral vessel wall and to where do they have to migrate? An approach to this question was provided by observations obtained in the rabbit hind limb model by using osmotic minipumps to locally deliver test substances into the collateral system. In these experiments, the most distinct enhancement of arteriogenesis was achieved with pumps either containing a chemotactic agent for monocytes or increasing their activation. The most potent substance that we found to stimulate collateral vessel growth was the monocyte chemoattractant protein-1 (MCP-1). When MCP-1 was locally infused into the collateral network after occlusion of the femoral artery in the rabbit hind limb, a dramatic improvement of the growth process was detected seven days after occlusion,50 which was confirmed later.6 In contrast, in MCP-1 genedeficient mice, recovery of blood flow in the hind limb was reduced, which could be rescued by local delivery of MCP-1.52 Furthermore, the inhibition of arteriogenesis in these mice correlated with reduced monocytes accumulation around the growing collateral vessels, although still a significant number of macrophages were present. To achieve further insights into the pathway of monocyte attraction and invasion, we investigated collateral artery development in mice that were gene-deficient for the chemokine receptor-2 (CCR-2).53 This receptor is known as the major functional receptor for MCP-1, although most likely not the only one of biological relevance.54,55 Using these mice on both the BALB/c and the C57BL/6 background, the importance of the MCP-1CCR2 pathway in arteriogenesis was impressively demonstrated, and it was shown that this pathway is responsible for the recruitment of monocytes during early phases of arteriogenesis56: the data displayed a dramatically reduced recovery of pedal blood flow after femoral artery ligation. This not only correlated with other physiological parameters like the reduction in hemoglobin oxygen saturation in the foot but was also reflected by functional parameters: Because of the reduced blood supply to the distal regions of the leg, the active movement of the limb, assessed in a score, was significantly impaired. Furthermore, histological morphometry of the collateral vessel size confirmed the physiological data by showing decreased collateral vessel diameters in the CCR2 genedeficient mice compared with controls. Finally, using well-established monoclonal antibodies against monocytes/macrophages, it was shown that accumulation of those cells in the perivascular space around collateral arteries was lacking in the CCR2 knockout group.
| Cell Proliferation and Remodeling Are Major Parts of Arteriogenesis |
|---|
|
|
|---|
|
Proliferation of vascular cells is initiated as early as 24 hours after experimental occlusion of the femoral artery in the rabbit model and peaks at days 3 to 7. Weak but markedly above normal mitotic activity is still observed at 3 weeks.40 The signaling cascade uses the mitogen activated protein kinases with activation of the RAS-ERK- and the Rho pathways. Studies with rabbit SMCs in culture make the involvement of the FGF family of growth factors highly likely. No evidence was found so far for the involvement of the PDGF family of growth factors.
Proliferation activity follows the invasion of monocytes with a lag time of about one day. EC mitosis precedes that of SMCs by a few hours and growth factors are released from the matrix and from monocytes during that time.57 In addition to their direct mitogenic activity, these growth factors also influence the transcription of secondary growth factors like FGF-7, inactivation of the MMP inhibitor TIMP, and downregulation of the extracellular matrix component elastin. The increase in cell mitosis also coincides with a morphological change in smooth muscle cells: the appearance of a prominent rough endoplasmic reticulum and many free ribosomes indicates that smooth muscle cells are transformed from the contractile into the proliferative/synthetic phenotype.40 During this phase, a neointima forms composed of smooth muscle cells in which, like in the earlier degradation of the internal elastic lamina, matrix-metalloproteinases (MMPs) are involved.40,58 Several MMPs are known to be expressed by monocytes/macrophages, and we could demonstrate that stimulation of arteriogenesis with MCP-1 locally augments MMP-1, MMP-2, MMP-3, and MMP-9 expression and activity.59 Furthermore, increases in the expression of MMPs, probably produced by macrophages, were also observed in the perivascular space of growing collaterals. This indicates that MMPs participate in the digestion of the extracellular matrix and even of skeletal muscle cells (by T-lymphocytes) to create additional space for the growing collateral vessel.
The increase of collateral vessel diameter reduces FSS, which is inversely related to the cube of the vascular radius. The normalization of FSS is the signal for maturation. The initial thinning of the tension-bearing vessel wall had increased the circumferential wall stress for the smooth muscle cells, a proliferative stimulus. This leads to increased wall thickness by SMC proliferation, which acts via negative feedback to normalization of circumferential wall stress and terminates the remodeling phase. The transformation of a small microvascular resistance vessel into a large conductance artery is now completed.
| Role of Other Nonvascular Cells in Arteriogenesis |
|---|
|
|
|---|
.6266 By the release of GM-CSF, they may in addition prolong monocyte survival of macrophages.66,67 Mast cells can stimulate monocytes/ macrophages to release interleukins, particularly IL-1, which can stimulate production of MMPs in a variety of cells, or they may directly release MMPs or serine protease capable of degrading ECM-components.66 However, to what extent mast cells support arteriogenesis is unknown. Lymphocytes were frequently observed in the wall of growing collateral vessels. So far, only one report by the Epstein group had focused on their possible role for arteriogenesis.68 Using mice with targeted disruption of the gene for the T-cell antigen CD4, they showed a reduction of blood flow recovery in the mouse hind limb after femoral occlusion. When the deficiency of CD4-positive cells was rescued by the injection of isolated T-cells, blood flow recovery was increased, which coincided with an increased macrophage accumulation. Hence, the authors suggest that lymphocytes may support arteriogenesis by participating in monocyte recruitment to the collateral vessel wall.
| Bone MarrowDerived Cells |
|---|
|
|
|---|
|
| Will There Be a Cure? |
|---|
|
|
|---|
24 hours after onset of stimulation to proceed with the cell cycle. If treatment starts later than a week after occlusion in the rabbit, no additional effect over spontaneous growth is achieved.6 Furthermore, the right form of application has yet to be found. A one-shot approach (ie, VEGF protein injected into the coronary artery) may not provide the necessary contact time and nonimmunogenic, safe, and efficient gene transfer methods have not yet been developed. Second, the majority of experiments have been performed with young healthy animals but target groups for arteriogenic therapy are elderly patients experiencing cardiovascular diseases, ie, atherosclerosis. On the other hand, even young animals replace only 40% of their maximal conductance by collateral vessels. Any treatment in animals by drugs, growth factors, combination of factors, or other intervention to increase conductance to 100% in animals would constitute a reasonable basis for therapeutic trials in patients.
The effects of age on arteriogenesis are not conclusively known. Our own earlier studies with old male beagle dogs showed no difference in the ability to develop a coronary collateral circulation after progressive coronary artery occlusion.
One promising therapeutical approach seems to emerge from a recently published clinical study where improvement of coronary collateral flow was observed in patients scheduled for angioplasty but instead received GM-CSF treatment.86 GM-CSF is known to decrease macrophage apoptosis, thus prolonging their lifespan.67 Furthermore, it supports mobilization of mononuclear cells from the bone marrow. Hence, the observed effects of GM-CSF may be secondary to an increased monocyte recruitment and macrophage presence in the growing collateral vasculature.
| Conclusions |
|---|
|
|
|---|
| Acknowledgments |
|---|
| Footnotes |
|---|
| References |
|---|
|
|
|---|
2. Fulton WFM. The time factor in the enlargement of anastomoses in coronary artery disease. Scot Med J. 1964; 9: 1823.[Medline] [Order article via Infotrieve]
3. Kumada T, Gallagher KP, Battler A, White F, Kemper WS, Ross Jr J. Comparison of postpacing and exercise-induced myocardial dysfunction during collateral development in conscious dogs. Circulation. 1982; 65: 11781185.
4. Ito WD, Arras M, Scholz D, Winkler B, Htun P, Schaper W. Angiogenesis but not collateral growth is associated with ischemia after femoral artery occlusion. Am J Physiol. 1997; 273: H1255H1265.[Medline] [Order article via Infotrieve]
5. Elsaesser H, Sauer A, Friedrich C, Helisch A, Luttun A, Carmeliet P, Scholz D, Schaper W. Bone marrow transplants abolish inhibition of arteriogenesis in placenta growth factor k.o. mice. J Mol Cell Cardiol. 2000; 32: A29. Abstract.
6. Hoefer IE, van Royen N, Buschmann IR, Piek JJ, Schaper W. Time course of arteriogenesis following femoral artery occlusion in the rabbit. Cardiovasc Res. 2001; 49: 609617.
7. Scholz D, Ziegelhoeffer T, Helisch A, Wagner S, Friedrich C, Podzuweit T, Schaper W. Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice. J Mol Cell Cardiol. 2002; 34: 775787.[CrossRef][Medline] [Order article via Infotrieve]
8. Cox R. Physiology and hemodynamics of the macrocirculation. In: Stehbens W, eds. Hemodynamics and the Blood Vessel Wall. Springfield, Ill: Charles C. Thomas; 1979: 75156.
9. Scheel KW, Fitzgerald EM, Martin RO, Larsen RA. The possible role of mechanical stresses on coronary collateral development during gradual coronary occlusion. In: Schaper W, eds. The Pathophysiology of Myocardial Perfusion. Amsterdam: Elsevier/North-Holland; 1979: 489518.
10. Pipp F, Cai WJ, Boehm S, Karanovic G, Ziegler B, Ritter R, Farzin A, Schmitz-Rixen T, Schaper W. Chronically increased fluid shear stress following arteriovenous-fistula enhances collateral artery growth in a chronic pig hind limb model. FASEB J. 2003; 17: 338.7.
11. Ingber DE. Tensegrity II. How structural networks influence cellular information processing networks. J Cell Sci. 2003; 116: 13971408.
12. Ingber DE. Tensegrity I. Cell structure and hierarchical systems biology. J Cell Sci. 2003; 116: 11571173.
13. Ingber DE. Mechanical signaling and the cellular response to extracellular matrix in angiogenesis and cardiovascular physiology. Circ Res. 2002; 91: 877887.
14. Resnick N, Yahav H, Shay-Salit A, Shushy M, Schubert S, Zilberman LC, Wofovitz E. Fluid shear stress and the vascular endothelium: for better and for worse. Prog Biophys Mol Biol. 2003; 81: 177199.[CrossRef][Medline] [Order article via Infotrieve]
15. Topper JN, Gimbrone MA, Jr. Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype. Mol Med Today. 1999; 5: 4046.[CrossRef][Medline] [Order article via Infotrieve]
16. Davies PF, Barbee KA, Volin MV, Robotewskyj A, Chen J, Joseph L, Griem ML, Wernick MN, Jacobs E, Polacek DC, dePaola N, Barakat AI. Spatial relationships in early signaling events of flow-mediated endothelial mechanotransduction. Annu Rev Physiol. 1997; 59: 527549.[CrossRef][Medline] [Order article via Infotrieve]
17. Barbee KA. Changes in surface topography in endothelial monolayers with time at confluence: influence on subcellular shear stress distribution due to flow. Biochem Cell Biol. 1995; 73: 501505.[Medline] [Order article via Infotrieve]
18. Helmke BP, Davies PF. The cytoskeleton under external fluid mechanical forces: hemodynamic forces acting on the endothelium. Ann Biomed Eng. 2002; 30: 284296.[CrossRef][Medline] [Order article via Infotrieve]
19. Bojanowski K, Maniotis AJ, Plisov S, Larsen AK, Ingber DE. DNA topoisomerase II can drive changes in higher order chromosome architecture without enzymatically modifying DNA. J Cell Biochem. 1998; 69: 127142.[CrossRef][Medline] [Order article via Infotrieve]
20. Ingber D. In search of cellular control: signal transduction in context. J Cell Biochem Suppl. 1998; 3031: 232237.
21. Gimbrone MA, Jr., Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann N|Y Acad Sci. 2000; 902: 230239; discussion 239240.[Medline] [Order article via Infotrieve]
22. Shyy JY, Li YS, Lin MC, Chen W, Yuan S, Usami S, Chien S. Multiple cis-elements mediate shear stress-induced gene expression. J Biomech. 1995; 28: 14511457.[CrossRef][Medline] [Order article via Infotrieve]
23. Shyy JY, Lin MC, Han J, Lu Y, Petrime M, Chien S. The cis-acting phorbol ester "12-O-tetradecanoylphorbol 13-acetate"-responsive element is involved in shear stress-induced monocyte chemotactic protein 1 gene expression. Proc Natl Acad Sci U S A. 1995; 92: 80698073.
24. Resnick N, Collins T, Atkinson W, Bonthron DT, Dewey CF, Jr., Gimbrone MA, Jr. Platelet-derived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element. Proc Natl Acad Sci U S A. 1993; 90: 45914595.
25. Ziegelhoeffer T, Scholz D, Friedrich C, Helisch A, Wagner S, Fernandez B, Schaper W. Inhibition of collateral artery growth by mibefradil: Possible role of volume-regulated chloride channels. Endothelium. 2003; 10: 237246.[Medline] [Order article via Infotrieve]
26. Manolopoulos VG, Liekens S, Koolwijk P, Voets T, Peters E, Droogmans G, Lelkes PI, De Clercq E, Nilius B. Inhibition of angiogenesis by blockers of volume-regulated anion channels. Gen Pharmacol. 2000; 34: 107116.[CrossRef][Medline] [Order article via Infotrieve]
27. Nilius B, Eggermont J, Voets T, Droogmans G. Volume-activated Cl- channels. Gen Pharmacol. 1996; 27: 11311140.[Medline] [Order article via Infotrieve]
28. Hoefer IE, van Royen N, Rectenwald JE, Bray EJ, Abouhamze Z, Moldawer LL, Voskuil M, Piek JJ, Buschmann IR, Ozaki CK. Direct evidence for tumor necrosis factor-
signaling in arteriogenesis. Circulation. 2002; 105: 16391641.
29. Unger EF, Banai S, Shou M, Lazarous DF, Jaklitsch MT, Sheinowitz M, Correa R, Klingbeil C, Epstein SE. Basic fibroblast growth factor enhances myocardial collateral flow in a canine model. Am J Physiol. 1994; 266: H1588H1595.[Medline] [Order article via Infotrieve]
30. Fernandez B, Buehler A, Wolfram S, Kostin S, Espanion G, Franz WM, Niemann H, Doevendans PA, Schaper W, Zimmermann R. Transgenic myocardial overexpression of fibroblast growth factor-1 increases coronary artery density and branching. Circ Res. 2000; 87: 207213.
31. Deindl E, Hoefer IE, Fernandez B, Barancik M, Heil M, Strniskova M, Schaper W. Involvement of the fibroblast growth factor system in adaptive and chemokine-induced arteriogenesis. Circ Res. 2003; 92: 561568.
32. Rissanen TT, Markkanen JE, Arve K, Rutanen J, Kettunen MI, Vajanto I, Jauhiainen S, Cashion L, Gruchala M, Narvanen O, Taipale P, Kauppinen RA, Rubanyi GM, Yla-Herttuala S. Fibroblast growth factor 4 induces vascular permeability, angiogenesis and arteriogenesis in a rabbit hindlimb ischemia model. Faseb J. 2003; 17: 100102.
33. Emanueli C, Salis MB, Pinna A, Graiani G, Manni L, Madeddu P. Nerve growth factor promotes angiogenesis and arteriogenesis in ischemic hindlimbs. Circulation. 2002; 106: 22572262.
34. Liu ZJ, Shirakawa T, Li Y, Soma A, Oka M, Dotto GP, Fairman RM, Velazquez OC, Herlyn M. Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Mol Cell Biol. 2003; 23: 1425.
35. Lee CW, Stabile E, Kinnaird T, Shou M, Devaney JM, Epstein SE, Burnett MS. Temporal patterns of gene expression after acute hindlimb ischemia in mice: insights into the genomic program for collateral vessel development. J Am Coll Cardiol. 2004; 43: 474482.
36. Heil M, Clauss M, Suzuki K, Buschmann IR, Willuweit A, Fischer S, Schaper W. Vascular endothelial growth factor (VEGF) stimulates monocyte migration through endothelial monolayers via increased integrin expression. Eur J Cell Biol. 2000; 79: 850857.[CrossRef][Medline] [Order article via Infotrieve]
37. Takagi J, Springer TA. Integrin activation and structural rearrangement. Immunol Rev. 2002; 186: 141163.[CrossRef][Medline] [Order article via Infotrieve]
38. Hogg N, Henderson R, Leitinger B, McDowall A, Porter J, Stanley P. Mechanisms contributing to the activity of integrins on leukocytes. Immunol Rev. 2002; 186: 164171.[CrossRef][Medline] [Order article via Infotrieve]
39. Huo Y, Ley K. Adhesion molecules and atherogenesis. Acta Physiol Scand. 2001; 173: 3543.[CrossRef][Medline] [Order article via Infotrieve]
40. Scholz D, Ito W, Fleming I, Deindl E, Sauer A, Wiesnet M, Busse R, Schaper J, Schaper W. Ultrastructure and molecular histology of rabbit hind-limb collateral artery growth (arteriogenesis). Virchows Arch. 2000; 436: 257270.[CrossRef][Medline] [Order article via Infotrieve]
41. Hoefer IE, Van Royen N, Rectenwald JE, Deindl E, Hua J, Jost M, Grundmann S, Voskuil M, Ozaki CK, Piek JJ, Buschmann IR. Arteriogenesis proceeds via ICAM-1/Mac-1-mediated mechanisms. Circ Res. 2004; 94: 11791185.
42. Carlos TM, Harlan JM. Leukocyte-endothelial adhesion molecules. Blood. 1994; 84: 20682101.
42. Pipp F, Boehm S, Cai WJ, Adili F, Ziegler B, Karanovic G, Ritter R, Balzer J, Scheler C, Schaper W, Schmitz-Rixen T. Elevated fluid shear stress enhances postocclusive collateral artery growth and gene expression in the pig hind limb. Arterioscler Thromb Vasc Biol. 2004; 24: 16641668.
43. Heil M, Ziegelhoeffer T, Pipp F, Kostin S, Martin S, Clauss M, Schaper W. Blood monocyte concentration is critical for enhancement of collateral artery growth. Am J Physiol Heart Circ Physiol. 2002; 283: H2411H2419.
44. Kusch A, Tkachuk S, Lutter S, Haller H, Dietz R, Lipp M, Dumler I. Monocyte-expressed urokinase regulates human vascular smooth muscle cell migration in a coculture model. Biol Chem. 2002; 383: 217221.[CrossRef][Medline] [Order article via Infotrieve]
45. Menshikov M, Elizarova E, Plakida K, Timofeeva A, Khaspekov G, Beabealashvilli R, Bobik A, Tkachuk V. Urokinase upregulates matrix metalloproteinase-9 expression in THP-1 monocytes via gene transcription and protein synthesis. Biochem J. 2002; 367: 833839.[CrossRef][Medline] [Order article via Infotrieve]
46. Khan KM, Falcone DJ. Role of laminin in matrix induction of macrophage urokinase-type plasminogen activator and 92-kDa metalloproteinase expression. J Biol Chem. 1997; 272: 82708275.
47. Schaper J, Konig R, Franz D, Schaper W. The endothelial surface of growing coronary collateral arteries. Intimal margination and diapedesis of monocytes. A combined SEM and TEM study. Virchows Arch A Pathol Anat Histol. 1976; 370: 193205.[CrossRef][Medline] [Order article via Infotrieve]
48. Ito WD, Khmelevski E. Tissue macrophages: "Satellite Cells" for growing collateral vessels? A hypothesis. Endothelium. 2003; 10: 233235.[Medline] [Order article via Infotrieve]
49. Pipp F, Heil M, Issbrucker K, Ziegelhoeffer T, Martin S, van den Heuvel J, Weich H, Fernandez B, Golomb G, Carmeliet P, Schaper W, Clauss M. VEGFR-1-selective VEGF homologue PlGF is arteriogenic: evidence for a monocyte-mediated mechanism. Circ Res. 2003; 92: 378385.
50. Ito WD, Arras M, Winkler B, Scholz D, Schaper J, Schaper W. Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ Res. 1997; 80: 829837.
52. Voskuil M. Abnormal monocyte recruitment and collateral artery formation in monocyte chemoattractant protein-1 deficient mice. Universiteit van Amsterdam; 2003: 2535.
53. Kuziel WA, Morgan SJ, Dawson TC, Griffin S, Smithies O, Ley K, Maeda N. Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc Natl Acad Sci U S A. 1997; 94: 1205312058.
54. Garcia-Zepeda EA, Combadiere C, Rothenberg ME, Sarafi MN, Lavigne F, Hamid Q, Murphy PM, Luster AD. Human monocyte chemoattractant protein (MCP)-4 is a novel CC chemokine with activities on monocytes, eosinophils, and basophils induced in allergic and nonallergic inflammation that signals through the CC chemokine receptors (CCR)-2 and -3. J Immunol. 1996; 157: 56135626.[Abstract]
55. Yamagami S, Tanaka H, Endo N. Monocyte chemoattractant protein-2 can exert its effects through the MCP-1 receptor (CC CKR2B). FEBS Lett. 1997; 400: 329332.[CrossRef][Medline] [Order article via Infotrieve]
56. Heil M, Ziegelhoeffer T, Wagner S, Fernandez B, Helisch A, Martin S, Tribulova S, Kuziel WA, Bachmann G, Schaper W. Collateral artery growth (arteriogenesis) after experimental arterial occlusion is impaired in mice lacking CC-chemokine receptor-2. Circ Res. 2004; 94: 671677.
57. Arras M, Ito WD, Scholz D, Winkler B, Schaper J, Schaper W. Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest. 1998; 101: 4050.[Medline] [Order article via Infotrieve]
58. Scholz D, Cai WJ, Schaper W. Arteriogenesis, a new concept of vascular adaptation in occlusive disease. Angiogenesis. 2001; 4: 247257.[CrossRef][Medline] [Order article via Infotrieve]
59. Ziegelhoeffer T, Hoefer I, van Royen N, Buschmann I. Effective reduction in collateral artery formation through matrix metalloproteinase inhibitors. Circulation. 1999; 100: I-705.
60. Tanaka A, Arai K, Kitamura Y, Matsuda H. Matrix metalloproteinase-9 production, a newly identified function of mast cell progenitors, is downregulated by c-kit receptor activation. Blood. 1999; 94: 23902395.
61. Kanbe N, Tanaka A, Kanbe M, Itakura A, Kurosawa M, Matsuda H. Human mast cells produce matrix metalloproteinase 9. Eur J Immunol. 1999; 29: 26452649.[CrossRef][Medline] [Order article via Infotrieve]
62. Pennington DW, Lopez AR, Thomas PS, Peck C, Gold WM. Dog mastocytoma cells produce transforming growth factor ß 1. J Clin Invest. 1992; 90: 3541.[Medline] [Order article via Infotrieve]
63. Qu Z, Liebler JM, Powers MR, Galey T, Ahmadi P, Huang XN, Ansel JC, Butterfield JH, Planck SR, Rosenbaum JT. Mast cells are a major source of basic fibroblast growth factor in chronic inflammation and cutaneous hemangioma. Am J Pathol. 1995; 147: 564573.[Abstract]
64. Reed JA, Albino AP, McNutt NS. Human cutaneous mast cells express basic fibroblast growth factor. Lab Invest. 1995; 72: 215222.[Medline] [Order article via Infotrieve]
65. Grutzkau A, Kruger-Krasagakes S, Baumeister H, Schwarz C, Kogel H, Welker P, Lippert U, Henz BM, Moller A. Synthesis, storage, and release of vascular endothelial growth factor/vascular permeability factor (VEGF/VPF) by human mast cells: implications for the biological significance of VEGF206. Mol Biol Cell. 1998; 9: 875884.
66. Norrby K. Mast cells and angiogenesis. Apmis. 2002; 110: 355371.[CrossRef][Medline] [Order article via Infotrieve]
67. Buschmann IR, Hoefer IE, van Royen N, Katzer E, Braun-Dulleaus R, Heil M, Kostin S, Bode C, Schaper W. GM-CSF: a strong arteriogenic factor acting by amplification of monocyte function. Atherosclerosis. 2001; 159: 343356.[CrossRef][Medline] [Order article via Infotrieve]
68. Stabile E, Burnett MS, Watkins C, Kinnaird T, Bachis A, la Sala A, Miller JM, Shou M, Epstein SE, Fuchs S. Impaired arteriogenic response to acute hindlimb ischemia in CD4-knockout mice. Circulation. 2003; 108: 205210.
69. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999; 85: 221228.
70. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997; 275: 964967.
71. Shi Q, Rafii S, Wu MH, Wijelath ES, Yu C, Ishida A, Fujita Y, Kothari S, Mohle R, Sauvage LR, Moore MA, Storb RF, Hammond WP. Evidence for circulating bone marrow-derived endothelial cells. Blood. 1998; 92: 362367.
72. Orlic D, Kajstura J, Chimenti S, Bodine DM, Leri A, Anversa P. Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann N Y Acad Sci. 2001; 938: 221229;discussion 22930.
73. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med. 2001; 7: 430436.[CrossRef][Medline] [Order article via Infotrieve]
74. Fuchs S, Baffour R, Zhou Y, Shou M, Pierre A, Tio F, Weissman N, Leon M, Epstein S, Kornowski R. Transendocardial delivery of autologous bone marrow enhances collateral perfusion and regional function in pigs with chronic experimental myocardial ischemia. J Am Coll Cardiol. 2001; 37: 17261732.
75. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci U S A. 2000; 97: 34223427.
76. Beck H, Voswinckel R, Wagner S, Ziegelhoeffer T, Heil M, Helisch A, Schaper W, Acker T, Hatzopoulos AK, Plate KH. Participation of bone marrow-derived cells in long-term repair processes after experimental stroke. J Cereb Blood Flow Metab. 2003; 23: 709717.[Medline] [Order article via Infotrieve]
77. Castro RF, Jackson KA, Goodell MA, Robertson CS, Liu H, Shine HD. Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science. 2002; 297: 1299.
78. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science. 2002; 297: 22562259.
79. Rehman J, Li J, Orschell CM, March KL. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation. 2003; 107: 11641169.
80. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res. 2004; 94: 678685.
81. Epstein SE, Fuchs S, Zhou YF, Baffour R, Kornowski R. Therapeutic interventions for enhancing collateral development by administration of growth factors: basic principles, early results and potential hazards. Cardiovasc Res. 2001; 49: 532542.
82. Helisch A, Schaper W. Angiogenesis and arteriogenesisnot yet for prescription. Z Kardiol. 2000; 89: 239244.[CrossRef][Medline] [Order article via Infotrieve]
83. Simons M, Ware JA. Therapeutic angiogenesis in cardiovascular disease. Nat Rev Drug Discov. 2003; 2: 863871.[CrossRef][Medline] [Order article via Infotrieve]
84. Henry TD, Annex BH, McKendall GR, Azrin MA, Lopez JJ, Giordano FJ, Shah PK, Willerson JT, Benza RL, Berman DS, Gibson CM, Bajamonde A, Rundle AC, Fine J, McCluskey ER. The VIVA trial: Vascular endothelial growth factor in Ischemia for Vascular Angiogenesis. Circulation. 2003; 107: 13591365.
85. Simons M. Therapeutic coronary angiogenesis: a fronte praecipitium a tergo lupi? Am J Physiol Heart Circ Physiol. 2001; 280: H1923H1927.
86. Seiler C, Pohl T, Wustmann K, Hutter D, Nicolet PA, Windecker S, Eberli FR, Meier B. Promotion of collateral growth by granulocyte-macrophage colony- stimulating factor in patients with coronary artery disease: a randomized, double-blind, placebo-controlled study. Circulation. 2001; 104: 20122017.
87. Ziegelhoeffer T, Fernandez B, Kostin S, Heil M, Voswinckel R, Helisch A, Schaper W. Bone marrow-derived cells do not incorporate into adult growing vasculature. Circ Res. 2004; 94: 230238.
This article has been cited by other articles:
![]() |
C. Nesselmann, W. Li, N. Ma, and G. Steinhoff Stem cell-mediated neovascularization in heart repair Therapeutic Advances in Cardiovascular Disease, February 1, 2010; 4(1): 27 - 42. [Abstract] [PDF] |
||||
![]() |
L. Vincent, L. Feasson, S. Oyono-Enguelle, V. Banimbek, C. Denis, C. Guarneri, E. Aufradet, G. Monchanin, C. Martin, D. Gozal, et al. Remodeling of skeletal muscle microvasculature in sickle cell trait and {alpha}-thalassemia Am J Physiol Heart Circ Physiol, February 1, 2010; 298(2): H375 - H384. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Zouggari, H. Ait-Oufella, L. Waeckel, J. Vilar, C. Loinard, C. Cochain, A. Recalde, M. Duriez, B. I. Levy, E. Lutgens, et al. Regulatory T Cells Modulate Postischemic Neovascularization Circulation, October 6, 2009; 120(14): 1415 - 1425. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Loinard, A. Ginouves, J. Vilar, C. Cochain, Y. Zouggari, A. Recalde, M. Duriez, B. I. Levy, J. Pouyssegur, E. Berra, et al. Inhibition of Prolyl Hydroxylase Domain Proteins Promotes Therapeutic Revascularization Circulation, July 7, 2009; 120(1): 50 - 59. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Kubo, K. Egashira, T. Inoue, J.-i. Koga, S. Oda, L. Chen, K. Nakano, T. Matoba, Y. Kawashima, K. Hara, et al. Therapeutic Neovascularization by Nanotechnology-Mediated Cell-Selective Delivery of Pitavastatin Into the Vascular Endothelium Arterioscler Thromb Vasc Biol, June 1, 2009; 29(6): 796 - 801. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Oostendorp, M. J. Post, and W. H. Backes Vessel Growth and Function: Depiction with Contrast-enhanced MR Imaging Radiology, May 1, 2009; 251(2): 317 - 335. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. J. Belin de Chantemele, E. Vessieres, A.-L. Guihot, B. Toutain, M. Maquignau, L. Loufrani, and D. Henrion Type 2 diabetes severely impairs structural and functional adaptation of rat resistance arteries to chronic changes in blood flow Cardiovasc Res, March 1, 2009; 81(4): 788 - 796. [Abstract] [Full Text] [PDF] |
||||
![]() |
S H Schirmer, F C van Nooijen, J J Piek, and N van Royen Stimulation of collateral artery growth: travelling further down the road to clinical application Heart, February 1, 2009; 95(3): 191 - 197. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Werner and G. Nickenig Sex Hormones Save Our Skin: The Vascular Networking of Estrogen Circ. Res., January 30, 2009; 104(2): 135 - 137. [Full Text] [PDF] |
||||
![]() |
M. C. van Oostrom, O. van Oostrom, P. H. A. Quax, M. C. Verhaar, and I. E. Hoefer Insights into mechanisms behind arteriogenesis: what does the future hold? J. Leukoc. Biol., December 1, 2008; 84(6): 1379 - 1391. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. M. Krady, J. Zeng, J. Yu, S. MacLauchlan, E. A. Skokos, W. Tian, P. Bornstein, W. C. Sessa, and T. R. Kyriakides Thrombospondin-2 Modulates Extracellular Matrix Remodeling during Physiological Angiogenesis Am. J. Pathol., September 1, 2008; 173(3): 879 - 891. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Demicheva, M. Hecker, and T. Korff Stretch-Induced Activation of the Transcription Factor Activator Protein-1 Controls Monocyte Chemoattractant Protein-1 Expression During Arteriogenesis Circ. Res., August 29, 2008; 103(5): 477 - 484. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Korff, J. Braun, D. Pfaff, H. G. Augustin, and M. Hecker Role of ephrinB2 expression in endothelial cells during arteriogenesis: impact on smooth muscle cell migration and monocyte recruitment Blood, July 1, 2008; 112(1): 73 - 81. [Abstract] [Full Text] [PDF] |
||||
![]() |
D Versteeg, I E Hoefer, A H Schoneveld, D P V de Kleijn, E Busser, C Strijder, M Emons, P R Stella, P A Doevendans, and G Pasterkamp Monocyte toll-like receptor 2 and 4 responses and expression following percutaneous coronary intervention: association with lesion stenosis and fractional flow reserve Heart, June 1, 2008; 94(6): 770 - 776. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Todo, K. Kitagawa, T. Sasaki, E. Omura-Matsuoka, Y. Terasaki, N. Oyama, Y. Yagita, and M. Hori Granulocyte-Macrophage Colony-Stimulating Factor Enhances Leptomeningeal Collateral Growth Induced by Common Carotid Artery Occlusion Stroke, June 1, 2008; 39(6): 1875 - 1882. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Kumar, B. G. Branch, C. B. Pattillo, J. Hood, S. Thoma, S. Simpson, S. Illum, N. Arora, J. H. Chidlow Jr., W. Langston, et al. Chronic sodium nitrite therapy augments ischemia-induced angiogenesis and arteriogenesis PNAS, May 27, 2008; 105(21): 7540 - 7545. [Abstract] [Full Text] [PDF] |
||||
![]() |
C Kalka and I. Baumgartner Gene and stem cell therapy in peripheral arterial occlusive disease Vascular Medicine, May 1, 2008; 13(2): 157 - 172. [Abstract] [PDF] |
||||
![]() |
J.-S. Silvestre, Z. Mallat, A. Tedgui, and B. I. Levy Post-ischaemic neovascularization and inflammation Cardiovasc Res, May 1, 2008; 78(2): 242 - 249. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. N.T.P. Bakker, H. L. Matlung, P. Bonta, C. J. de Vries, N. van Rooijen, and E. VanBavel Blood flow-dependent arterial remodelling is facilitated by inflammation but directed by vascular tone Cardiovasc Res, May 1, 2008; 78(2): 341 - 348. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Lu, W. Jiang, J.-H. Yang, P.-Y. Chang, J. P. Walterscheid, H.-H. Chen, M. Marcelli, D. Tang, Y.-T. Lee, W. S.L. Liao, et al. Electronegative LDL Impairs Vascular Endothelial Cell Integrity in Diabetes by Disrupting Fibroblast Growth Factor 2 (FGF2) Autoregulation Diabetes, January 1, 2008; 57(1): 158 - 166. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. van Weel, R.E.M. Toes, L. Seghers, M.M.L. Deckers, M.R. de Vries, P.H. Eilers, J. Sipkens, A. Schepers, D. Eefting, V.W.M. van Hinsbergh, et al. Natural Killer Cells and CD4+ T-Cells Modulate Collateral Artery Development Arterioscler Thromb Vasc Biol, November 1, 2007; 27(11): 2310 - 2318. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. L. Tressel, R.-P. Huang, N. Tomsen, and H. Jo Laminar Shear Inhibits Tubule Formation and Migration of Endothelial Cells by an Angiopoietin-2-Dependent Mechanism Arterioscler Thromb Vasc Biol, October 1, 2007; 27(10): 2150 - 2156. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. L. Haas, J. L. Doyle, M. R. Distasi, L. E. Norton, K. M. Sheridan, and J. L. Unthank Involvement of MMPs in the outward remodeling of collateral mesenteric arteries Am J Physiol Heart Circ Physiol, October 1, 2007; 293(4): H2429 - H2437. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Mees, S. Wagner, E. Ninci, S. Tribulova, S. Martin, R. van Haperen, S. Kostin, M. Heil, R. de Crom, and W. Schaper Endothelial Nitric Oxide Synthase Activity Is Essential for Vasodilation During Blood Flow Recovery but not for Arteriogenesis Arterioscler Thromb Vasc Biol, September 1, 2007; 27(9): 1926 - 1933. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. W. Kim, A. Lin, R. E. Guldberg, M. Ushio-Fukai, and T. Fukai Essential Role of Extracellular SOD in Reparative Neovascularization Induced by Hindlimb Ischemia Circ. Res., August 17, 2007; 101(4): 409 - 419. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Reiss, J. Droste, M. Heil, S. Tribulova, M. H.H. Schmidt, W. Schaper, D. J. Dumont, and K. H. Plate Angiopoietin-2 Impairs Revascularization After Limb Ischemia Circ. Res., July 6, 2007; 101(1): 88 - 96. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Penuelas, X. L. Aranguren, G. Abizanda, J. M. Marti-Climent, M. Uriz, M. Ecay, M. Collantes, G. Quincoces, J. A. Richter, and F. Prosper 13N-Ammonia PET as a Measurement of Hindlimb Perfusion in a Mouse Model of Peripheral Artery Occlusive Disease J. Nucl. Med., July 1, 2007; 48(7): 1216 - 1223. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Weigel, I. Kajgana, H. Bergmeister, G. Riedl, H.-D. Glogar, M. Gyongyosi, S. Blasnig, G. Heinze, and W. Mohl Beck and back: A paradigm change in coronary sinus interventions--pulsatile stretch on intact coronary venous endothelium J. Thorac. Cardiovasc. Surg., June 1, 2007; 133(6): 1581 - 1587. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Luo, Y. Luo, Y. He, H. Zhang, R. Zhang, X. Li, W. L. Dobrucki, A. J. Sinusas, W. C. Sessa, and W. Min Differential Functions of Tumor Necrosis Factor Receptor 1 and 2 Signaling in Ischemia-Mediated Arteriogenesis and Angiogenesis Am. J. Pathol., November 1, 2006; 169(5): 1886 - 1898. [Abstract] [Full Text] [PDF] |
||||
![]() |
C.-H. Chen and J. P. Walterscheid Plaque Angiogenesis Versus Compensatory Arteriogenesis in Atherosclerosis Circ. Res., October 13, 2006; 99(8): 787 - 789. [Full Text] [PDF] |
||||
![]() |
K. Takaba, C. Jiang, S. Nemoto, Y. Saji, T. Ikeda, S. Urayama, T. Azuma, A. Hokugo, S. Tsutsumi, Y. Tabata, et al. A combination of omental flap and growth factor therapy induces arteriogenesis and increases myocardial perfusion in chronic myocardial ischemia: Evolving concept of biologic coronary artery bypass grafting J. Thorac. Cardiovasc. Surg., October 1, 2006; 132(4): 891 - 899. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. L. Lucitti, R. Visconti, J. Novak, and B. B. Keller Increased arterial load alters aortic structural and functional properties during embryogenesis Am J Physiol Heart Circ Physiol, October 1, 2006; 291(4): H1919 - H1926. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. M. Greve, A. S. Les, B. T. Tang, M. T. Draney Blomme, N. M. Wilson, R. L. Dalman, N. J. Pelc, and C. A. Taylor Allometric scaling of wall shear stress from mice to humans: quantification using cine phase-contrast MRI and computational fluid dynamics Am J Physiol Heart Circ Physiol, October 1, 2006; 291(4): H1700 - H1708. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Lehoux and B. I. Levy Collateral Artery Growth: Making the Most of What You Have Circ. Res., September 15, 2006; 99(6): 567 - 569. [Full Text] [PDF] |
||||
![]() |
F. M. Kouri and O. Eickelberg Transforming Growth Factor-{alpha}, a Novel Mediator of Strain-Induced Vascular Remodeling Circ. Res., August 18, 2006; 99(4): 348 - 350. [Full Text] [PDF] |
||||
![]() |
F. Bussolino Small Molecule Approaches for Promoting Ischemic Tissue Vascularization Circ. Res., August 4, 2006; 99(3): 231 - 233. [Full Text] [PDF] |
||||
![]() |
S. Murphy, B. Larrivee, I. Pollet, K. S. Craig, D. E. Williams, X.-H. Huang, M. Abbott, F. Wong, C. Curtis, T. P. Conrads, et al. Identification of Sokotrasterol Sulfate As a Novel Proangiogenic Steroid Circ. Res., August 4, 2006; 99(3): 257 - 265. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. N.T.P. Bakker, A. Pistea, J. A.E. Spaan, T. Rolf, C. J. de Vries, N. van Rooijen, E. Candi, and E. VanBavel Flow-Dependent Remodeling of Small Arteries in Mice Deficient for Tissue-Type Transglutaminase: Possible Compensation by Macrophage-Derived Factor XIII Circ. Res., July 7, 2006; 99(1): 86 - 92. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. E. Silver and J. A. Vita Shear Stress-Mediated Arterial Remodeling in Atherosclerosis: Too Much of a Good Thing? Circulation, June 20, 2006; 113(24): 2787 - 2789. [Full Text] [PDF] |
||||
![]() |
M. Schmelter, B. Ateghang, S. Helmig, M. Wartenberg, and H. Sauer Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation FASEB J, June 1, 2006; 20(8): 1182 - 1184. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Herve, E. Fadel, P. Herve, and E. Fadel Systemic neovascularization of the lung after pulmonary artery occlusion: "decoding the Da Vinci code" J Appl Physiol, April 1, 2006; 100(4): 1101 - 1102. [Full Text] [PDF] |
||||
![]() |
F. Michel, J.-S. Silvestre, L. Waeckel, S. Corda, T. Verbeuren, J. P. Vilaine, M. Clergue, M. Duriez, and B. I. Levy Thromboxane A2/Prostaglandin H2 Receptor Activation Mediates Angiotensin II-Induced Postischemic Neovascularization Arterioscler Thromb Vasc Biol, March 1, 2006; 26(3): 488 - 493. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Stabile, T. Kinnaird, A. la Sala, S. K. Hanson, C. Watkins, U. Campia, M. Shou, S. Zbinden, S. Fuchs, H. Kornfeld, et al. CD8+ T Lymphocytes Regulate the Arteriogenic Response to Ischemia by Infiltrating the Site of Collateral Vessel Development and Recruiting CD4+ Mononuclear Cells Through the Expression of Interleukin-16 Circulation, January 3, 2006; 113(1): 118 - 124. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Toyota, D. C. Warltier, T. Brock, E. Ritman, C. Kolz, P. O'Malley, P. Rocic, M. Focardi, and W. M. Chilian Vascular Endothelial Growth Factor Is Required for Coronary Collateral Growth in the Rat Circulation, October 4, 2005; 112(14): 2108 - 2113. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Imada, T. Tatsumi, Y. Mori, T. Nishiue, M. Yoshida, H. Masaki, M. Okigaki, H. Kojima, Y. Nozawa, Y. Nishiwaki, et al. Targeted Delivery of Bone Marrow Mononuclear Cells by Ultrasound Destruction of Microbubbles Induces Both Angiogenesis and Arteriogenesis Response Arterioscler Thromb Vasc Biol, October 1, 2005; 25(10): 2128 - 2134. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Kitagawa, Y. Yagita, T. Sasaki, S. Sugiura, E. Omura-Matsuoka, T. Mabuchi, K. Matsushita, and M. Hori Chronic Mild Reduction of Cerebral Perfusion Pressure Induces Ischemic Tolerance in Focal Cerebral Ischemia Stroke, October 1, 2005; 36(10): 2270 - 2274. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Heissig, S. Rafii, H. Akiyama, Y. Ohki, Y. Sato, T. Rafael, Z. Zhu, D. J. Hicklin, K. Okumura, H. Ogawa, et al. Low-dose irradiation promotes tissue revascularization through VEGF release from mast cells and MMP-9-mediated progenitor cell mobilization J. Exp. Med., September 19, 2005; 202(6): 739 - 750. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Chalothorn, S. M. Moore, H. Zhang, S. W. Sunnarborg, D. C. Lee, and J. E. Faber Heparin-Binding Epidermal Growth Factor-Like Growth Factor, Collateral Vessel Development, and Angiogenesis in Skeletal Muscle Ischemia Arterioscler Thromb Vasc Biol, September 1, 2005; 25(9): 1884 - 1890. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Yu, E. D. deMuinck, Z. Zhuang, M. Drinane, K. Kauser, G. M. Rubanyi, H. S. Qian, T. Murata, B. Escalante, and W. C. Sessa Endothelial nitric oxide synthase is critical for ischemic remodeling, mural cell recruitment, and blood flow reserve PNAS, August 2, 2005; 102(31): 10999 - 11004. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Kojda and R. Hambrecht Molecular mechanisms of vascular adaptations to exercise. Physical activity as an effective antioxidant therapy? Cardiovasc Res, August 1, 2005; 67(2): 187 - 197. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Madeddu Therapeutic angiogenesis and vasculogenesis for tissue regeneration Exp Physiol, May 1, 2005; 90(3): 315 - 326. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Puglia Jr, D. S. Liebeskind, and L. H. Sansing Willisian collateralization Neurology, February 22, 2005; 64(4): 767 - 767. [Full Text] [PDF] |
||||
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
|
Circulation Research Home | Subscriptions | Archives | Feedback | Authors | Help | AHA Journals Home | Search Copyright © 2004 American Heart Association, Inc. All rights reserved. Unauthorized use prohibited. |