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Information Networks in the Arterial Wall

Jean-Louis Bény

J.-L. Bény is Professor in the Department of Zoology and Animal Biology at Geneva University, Sciences III, 30 quai E. Ansermet, 1211 Geneva 4, Switzerland.

	Abstract

 
The main task of the arterial system is to secure an adequate supply of oxygen to organs. This fact implies the integration of multiple signals in the vascular wall. This review deals with the exchange of information between and among smooth muscle and endothelial cells through gap junctions in the vessel walls of arteries and arterioles.

	Introduction

Top Introduction Transmission mode of messages... Homocellular coupling between... Homocellular coupling between... Heterocellular coupling between... Arterioles Arteries Conclusion References

 
The main task of the arterial system is to secure an adequate supply of oxygen to organs for their short- and long-term metabolic demand. Therefore, the diameter of the arteries must be finely adjusted because the blood flow rate is proportional to the fourth power of the vessel radius. The arteries receive information of central origin via the autonomic nerves and the endocrine system. In addition, the blood vessels are under the influence of local metabolic factors such as PO₂, PCO₂, pH, potassium, and autocrine and paracrine factors. Physical forces such as blood pressure, blood flow, and shear stress modulate vascular diameter. The convergence of all these factors implies the integration of multiple signals in the vascular wall. This integration could be realized by the intercellular communication through gap junctions; this is the focus of this review.

	Transmission mode of messages through gap junctions

Top Introduction Transmission mode of messages... Homocellular coupling between... Homocellular coupling between... Heterocellular coupling between... Arterioles Arteries Conclusion References

 
When cells are coupled by gap junctions, four modes of message transmission can be envisaged (Fig. 1).

View larger version (46K): [in this window] [in a new window]   FIGURE 1. The intercellular transfer of information through gap junctions can be accomplished by passive diffusion of an intracellular messenger such as inositol 1,4,5-trisphosphate (A); a regenerative calcium wave in calcium-excitable cells (B); electrotonic conduction of a cell membrane potential change (C); and the regenerative action potential in excitable cells (D). STI, stimulation.

Second, a small local increase in calcium concentration within a cell could induce regenerative calcium release and thus achieve a high concentration, thanks to a calcium-induced calcium release phenomenon. Such a regenerative calcium wave could slowly propagate from cell to cell at a speed close to that of diffusion but, in principle, over an infinite distance.

Third, in a tissue made up of electrically unexcitable cells (i.e., containing no voltage-gated sodium or calcium channels and therefore unable to generate action potentials), a change in the membrane potential could electrotonically propagate intercellularly with an exponential decrease in amplitude over distance. This coupling could extend only a few millimeters but could be very rapid (a few milliseconds).

Fourth, in excitable cells, action potentials could propagate rapidly from cell to cell (many meters per second) and, in principle, over an infinite distance. This occurs with the cardiac heart action potential propagating from cell to cell.

	Homocellular coupling between endothelial cells

Top Introduction Transmission mode of messages... Homocellular coupling between... Homocellular coupling between... Heterocellular coupling between... Arterioles Arteries Conclusion References

 
By means of electron microscopy, endothelium gap junctions are frequently observed between the endothelial cells of small and large arteries. In addition, the molecules that form the gap junction, the connexins, are expressed and detected by immunohistology in the endothelium of all of the arteries. Connexin 40 is the most frequently observed; at times it coexists with connexin 37 or 43 (7). Therefore, morphological and chemical bases exist for cell-to-cell intercellular communication between the endothelial cells. The functionality of these junctions has been demonstrated by the intracellular injection of a tracer such as the fluorescent dye lucifer yellow or propidium iodide. The cell membrane is impermeant to these hydrophilic dyes, but they are small enough (<1,000 Da) to be able to diffuse intracellularly across the gap junctions. All these dyes demonstrate dye coupling between endothelial cells in arteries and arterioles.

When two cells are dye coupled, this implies an electrical coupling that can be demonstrated by intracellular stimulation of one cell via a microelectrode and by recording in a neighboring cell. Such coupling is poor in smooth muscle, but because of the presence of numerous functional gap junctions, the endothelial cells are well suited to propagate messages along the length of the arteries (15).

Does a physiological signal exist that could use the endothelium as a pathway for propagation along the arterial wall? The endothelial cells are not excitable, and thus these cells cannot generate action potentials that would propagate regeneratively along the endothelium over long distances. However, when endothelium-dependent vasodilation is produced by the stimulation of the endothelial cells, there is an associated hyperpolarization. Acetylcholine, substance P, bradykinin, adenosine, and mechanical stimulation hyperpolarize the endothelial cell by 15–20 mV (2). Such signals conduct rapidly and electrotonically over a distance of a few millimeters, with an exponential decay with distance. This appears to be the pattern by which the conducted vasodilation is conveyed in arterioles (15).

The synthesis of nitric oxide by the endothelial cells is linked to an increase in IP₃ that releases an intracellular calcium pool into the cytoplasm. IP₃ diffuses more rapidly than calcium and can thus stimulate neighboring cells by diffusion through gap junctions. This was demonstrated in cultured endothelial cells but has yet to be shown in intact vessels (12).

	Homocellular coupling between smooth muscle cells

Top Introduction Transmission mode of messages... Homocellular coupling between... Homocellular coupling between... Heterocellular coupling between... Arterioles Arteries Conclusion References

 
In the muscular arteries, the smooth muscle cells are also coupled to coordinate the vasoconstrictor and vasodilator signals over several cell layers. However, it is rare to observe gap junctions using electron microscopy in the media of large arteries. Close apposition of two cells is common, however, and it is assumed that the absence of junctional plaques in the presence of cell-to-cell coupling reflects the fact that the gap junctions are isolated rather than being assembled in a cluster. The connexins, predominantly connexin 43, are expressed in this smooth muscle as detected by immunohistology (3, 7), and they are functional as demonstrated by dye coupling. In addition, the space constant of the electrical signal spreading within the media, as measured with a partition chamber, demonstrates that the smooth muscles in the blood vessel wall behave as an electrical syncytium (3, 9).

The vascular smooth muscle cells are more or less excitable, depending on the vessel. In the portal vein, the smooth muscle cells spontaneously generate bursts of action potentials that are responsible for the intense vasomotion that characterizes this particular vein. In pig coronary artery, even electrical stimulation cannot evoke an action potential. However, these cells can fire spontaneously when incubated in the presence of a potassium-channel blocker such as tetrabutylammonium (2).

Therefore, depending on the artery, either action potential propagation or electrotonic conduction through the syncytium of coupled smooth muscles would coordinate the contraction-relaxation within the media of the blood vessel.

Indeed, the link among smooth muscle cell membrane potential, cytosolic free calcium, and force development has been widely discussed (11, 13).

	Heterocellular coupling between endothelial and smooth muscle cells

Top Introduction Transmission mode of messages... Homocellular coupling between... Homocellular coupling between... Heterocellular coupling between... Arterioles Arteries Conclusion References

 
The endothelial and smooth muscle cells are separated by connective tissue, the internal elastic membrane. However, these two cell types establish close contacts, thanks to myoendothelial bridges that cross the internal elastic lamina through fenestration in this membrane (5). The effect of these connections is dependent on the vessel type and especially on the number of layers of smooth muscle.

Two cases should be considered: the arterioles, in which one layer of smooth muscle surrounds the monolayer of endothelial cells, and the large muscular arteries, in which several layers of coupled smooth muscle cells surround the intima.

	Arterioles

Top Introduction Transmission mode of messages... Homocellular coupling between... Homocellular coupling between... Heterocellular coupling between... Arterioles Arteries Conclusion References

 
In these vessels, the microiontophoretic injection of the dye lucifer yellow either in the endothelium or the smooth muscle cells does not show heterocellular dye coupling. However, in this tissue, the absence of dye coupling observed with lucifer yellow as a tracer seems to be an artifact. Injection of ethidium bromide, propidium bromide, or biocytin demonstrates heterocellular dye coupling (8). When two cells are dye coupled, as a consequence, they should be electrically coupled. In addition, the input resistance that illustrates the energy needed to change the membrane potential of a cluster of cells must be of the same order of magnitude in the endothelium and the smooth muscle cell because these two layers have a comparable size in arterioles. Therefore, in principle, a change in the membrane potential of the endothelial cells should be electrotonically transmitted to the smooth muscle cells, and in the reverse direction, the endothelial cell membrane potential should be influenced by that of the smooth muscle cells (Fig. 2). Such a bidirectional electrical communication was demonstrated although the relation of these observations to the in vivo situation is still controversial (14, 15). This reciprocal influence between smooth and endothelial cells also serves to apply to exchanges of cytosolic free calcium. A rise in free calcium in the smooth muscle cell of a cheek pouch arteriole seems to be directly coupled to a calcium increase in the underlying endothelium (6).

View larger version (60K): [in this window] [in a new window]   FIGURE 2. Nonregenerative conduction processes, such as diffusion of molecules or electrotonic spreading, can convey messages symmetrically between the endothelial cells (EC) and the smooth muscle cells (SMC) in arterioles where the input resistance of the endothelial and the smooth muscle layer are similar. In contrast, in muscular arteries, the conduction is efficient from the smooth muscle to the endothelium, but signals passing in the opposite direction are rapidly dissipated in the multiple layers of smooth muscle cell.

View larger version (54K): [in this window] [in a new window]   FIGURE 3. Although the hyperpolarization of endothelial cells caused by bradykinin (BK) and the endothelium-dependent hyperpolarization that simultaneously occurs in smooth muscle cells are superimposable, these two hyperpolarizations are linked to an opposite effect on cytosolic free calcium. In the endothelial cells, calcium is increased and this causes the opening of calcium-dependent potassium channels (KCa++) that leads to the hyperpolarization. In the smooth muscle cells, the hyperpolarization closes voltage-dependent calcium channels (Ca++voc), which lowers the cytosolic calcium concentration that is responsible for the relaxation. IP3, inositol 1,4,5-trisphosphate; Vm, membrane potential; G, G protein.

	Arteries

Top Introduction Transmission mode of messages... Homocellular coupling between... Homocellular coupling between... Heterocellular coupling between... Arterioles Arteries Conclusion References

These observations imply that in an even larger artery, such as the porcine coronary artery, this unidirectional influence of the smooth muscle on the endothelial cells should be even more pronounced because the syncytium of coupled smooth muscle cells of the media is huge. In fact, the strong influence of the smooth muscle cells on the membrane potential of the endothelial cells has been clearly shown in this artery. The catecholaminergic ß-agonist isoproterenol hyperpolarizes and relaxes coronary artery smooth muscle cells independent of an intact endothelium. This agonist also has no effect on the membrane potential of endothelial cells from the same vessel in primary culture. However, the smooth muscle cell hyperpolarization is transmitted to the endothelial cells on a strip of coronary artery in vitro (2), thus causing a smooth muscle-dependent endothelial cell hyperpolarization. Additional evidence showing smooth muscle-endothelial cell coupling is based on the behavior of the vessel segment in which the potassium channels are inhibited by tetrabutylammonium. Under these conditions, these cells generate repetitive spontaneous action potential series and this causes an oscillating vasomotion or a tonic vasoconstriction. These smooth muscle cell action potentials are independent of the presence of an intact endothelium; they are myogenic in origin. Despite the origin in vascular smooth muscle, these action potentials are easily recorded from the endothelial cells of a strip of coronary artery. Furthermore, oscillations of the endothelial cell membrane potential are synchronous with those recorded in the smooth muscle cells. Porcine coronary artery endothelial cells have no voltage-gated sodium or calcium channel and thus cannot generate action potentials. Thus action potentials must be electrotonically transmitted from the smooth muscle to the endothelial cells (2). An exhaustive confirmation of this electrical heterocellular coupling was carried out using a partition chamber similar to that used by Tomita and Abe (see Ref. 1) to demonstrate that the intestinal smooth muscles behave as a syncytium. This device allows the imposition of rectangular hyperpolarization or depolarization across a deendothelialized area of a coronary strip by field stimulation. The resulting membrane potential changes in smooth muscle cells can spread electrotonically through the media of the denuded segment into the smooth muscle cells in an adjacent segment of the vessels in which the endothelium is intact. To determine whether the electrical signals from vascular smooth muscle could spread into the endothelium in the intact portion of the vessel, recordings were made from the endothelium. Hyperpolarizations or depolarizations selectively initiated in smooth muscle cells were recorded consistently in the endothelial cells. This demonstrates a functional electrotonic conduction from the smooth muscle to the endothelial cells (1).

Physiological significance of the coupling of smooth muscle cell membrane potentials on the endothelial cells has yet to be determined but could be a key determinant of function.

A bidirectional communication.
As already mentioned, in a large artery such as the porcine coronary artery, a change in the membrane potential of the endothelial cells should quickly dissipate within the big syncytium of smooth muscle cells that constitutes the media. Curiously, however, the hyperpolarizations induced in the endothelial cells by substance P or bradykinin are simultaneously recorded in the underlining smooth muscle cells in a strip of coronary artery in vitro (2). This observation seems to contradict the above-described biophysical considerations that predict an asymmetry in the input resistance of the endothelial versus the smooth muscle cells in large arteries. It appears, however, that in these circumstances, the transmission of the kinin-induced endothelial cell hyperpolarizations to the smooth muscles is not caused by electrotonic spreading. This is suggested by the fact that molecules known to uncouple cells coupled by gap junction do not block the signals. The endothelium-dependent smooth muscle cell hyperpolarizations caused by the kinins are not inhibited by either halothane or palmitoleic acid (2). As a control, the isoproterenol-caused smooth muscle cell-dependent endothelial cell hyperpolarization could be inhibited by halothane (2). This indicates that a phenomenon other than a passive electrical coupling alone is responsible for the transmission of the endothelial cell hyperpolarization to the neighboring smooth muscle cells in porcine coronary artery. This phenomenon has been attributed to an endothelium-derived hyperpolarizing factor (EDHF). The chemical nature of this important factor is yet undefined (10). Alternatively, EDHF could be explained by a regeneration in the smooth muscle cells of the hyperpolarization transmitted from the endothelium.

It is thus proposed that in porcine coronary artery, as opposed to the ciliary artery, the EDHF, in some way, occults the passive dissipation of a change in membrane potential that is transmitted electrotonically from the endothelial cells to the first layer of smooth muscle cells. The result of this complex cell signaling is that in the ciliary artery, in which the phenomenon of EDHF is absent, inhibitors of nitric oxide synthesis virtually abolish the endothelium-dependent relaxation, whereas in the coronary artery, these inhibitors only slightly diminish this relaxation.

	Conclusion

Top Introduction Transmission mode of messages... Homocellular coupling between... Homocellular coupling between... Heterocellular coupling between... Arterioles Arteries Conclusion References

 
A wall of arteries and arterioles seems to be composed of two parallel networks of electrically coupled cells. The unexcitable endothelial cells make up the intima, and the excitable smooth muscle cells constitute the media. These two networks are heterocellularly coupled, but the interplay of electrical signals between the networks depends on complex biophysical considerations that vary with the size of the vessel. In the arteriole, in which the ratio of smooth muscle to endothelium approaches 1, the influence of the membrane potential of the cells of one network on the other is symmetric. As a consequence, the phenomenon of endothelium-dependent hyperpolarization can be explained entirely by the electrotonic spread of endothelial cell hyperpolarization to the smooth muscle cells. In larger arteries, the coupling is such that the endothelial cell signal is rapidly dissipated within the smooth muscle layer. As a result, EDHF cannot only be explained by conduction propagation of an endothelial cell hyperpolarization to the smooth muscle cells. In contrast, in large arteries the membrane potential of the endothelial cells is strongly influenced by the smooth muscle cells. The physiological consequence of this coupling has yet to be fully explored.

Furthermore, intercellular connections discussed in this review are likely to contribute in complex ways to integrative physiology. The recent availability of transgenic mice with transformed connexin expression may soon facilitate the solution to this question.

	Acknowledgments

 
The authors thank Dr. Brian Duling for his helpful comments on the manuscript. This work was supported by Swiss National Foundation Grant 3100–39124.93/1.

	References

Top Introduction Transmission mode of messages... Homocellular coupling between... Homocellular coupling between... Heterocellular coupling between... Arterioles Arteries Conclusion References

 

1. Bény, J.-L. Electrical coupling between smooth muscle cells and endothelial cells in pig coronary arteries. Pflügers Arch. 433: 364–367, 1997.[Medline]
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