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The Calcium Signaling Mechanisms in Arterial Smooth Muscle and Endothelial Cells

Matteo Ottolini, Swapnil K. Sonkusare

10.1002/cphy.c200030

Source: Volume 11, Issue 2, April 2021

Published online: April 2021

Full Article on Wiley Online Library



Abstract

The contractile state of resistance arteries and arterioles is a crucial determinant of blood pressure and blood flow. Physiological regulation of arterial contractility requires constant communication between endothelial and smooth muscle cells. Various Ca2+ signals and Ca2+‐sensitive targets ensure dynamic control of intercellular communications in the vascular wall. The functional effect of a Ca2+ signal on arterial contractility depends on the type of Ca2+‐sensitive target engaged by that signal. Recent studies using advanced imaging methods have identified the spatiotemporal signatures of individual Ca2+ signals that control arterial and arteriolar contractility. Broadly speaking, intracellular Ca2+ is increased by ion channels and transporters on the plasma membrane and endoplasmic reticular membrane. Physiological roles for many vascular Ca2+ signals have already been confirmed, while further investigation is needed for other Ca2+ signals. This article focuses on endothelial and smooth muscle Ca2+ signaling mechanisms in resistance arteries and arterioles. We discuss the Ca2+ entry pathways at the plasma membrane, Ca2+ release signals from the intracellular stores, the functional and physiological relevance of Ca2+ signals, and their regulatory mechanisms. Finally, we describe the contribution of abnormal endothelial and smooth muscle Ca2+ signals to the pathogenesis of vascular disorders. © 2021 American Physiological Society. Compr Physiol 11:1831‐1869, 2021.

Figure 1. Figure 1. The contrasting effects of smooth muscle cell (SMC) and endothelial cell (EC) Ca2+ on vascular contractility. Mechanical and neurohumoral stimuli can increase intracellular Ca2+ in SMCs and ECs. Intracellular Ca2+ in SMCs and ECs, in general, has opposite effects on vascular resistance. Increase in SMC Ca2+ activates the contractile machinery in SMCs (myosin light chain kinase or MLCK/Actin‐Myosin). In contrast, an increase in EC Ca2+ inhibits SMC contractile mechanisms. The dotted red line indicates inhibition of SMC contractility.
Figure 2. Figure 2. Regulation of vascular smooth muscle cell (SMC) contractility by voltage‐gated Ca2+ channels. Ca2+ entry through CaV1.2 and CaV3.1 channels promotes SMC contraction. Ca2+ influx through CaV3.2 channels activates ryanodine receptors (RyRs), triggering Ca2+ release from the sarcoplasmic reticulum (SR) in the vicinity of large conductance, Ca2+‐activated K+ (BK) channels. BK channel activation results in SMC hyperpolarization and vasodilation. The dotted line indicates the deactivation of CaV1.2 and CaV3.1 channels.
Figure 3. Figure 3. Regulation of vascular smooth muscle cell (SMC) contractility by non‐voltage‐gated Ca2+ entry mechanisms. (A) Activation of purinergic P2X receptor, TRPV4, TRPV1, TRPP1, TRPC3, and TRPC6 channels, and NCX in reverse mode increases SMC intracellular Ca2+, leading to vasoconstriction. (B) Ca2+ release from endo‐lysosome via TRPML1 channel, or Ca2+ entry through TRPV4 channel at the plasma membrane activates ryanodine receptors (RyRs), triggering Ca2+ release signals (Ca2+ sparks) from the sarcoplasmic reticulum (SR). Ca2+ sparks activate large‐conductance Ca2+‐activated potassium (BK) channels. BK channels hyperpolarize the SMC membrane and cause vasodilation. Ca2+ release through IP3R induces SMC contraction. Sarco‐endoplasmic reticulum Ca2+‐ATPase (SERCA), by sequestering cytoplasmic Ca2+ back into the SR, maintains low cytosolic Ca2+ concentration. TRPV, TRPP, TRPC, TRPML, members of transient receptor potential channel family; NCX, Na+/Ca2+ exchanger.
Figure 4. Figure 4. Sarco‐endoplasmic reticulum Ca2+‐ATPase (SERCA) transporting cycle. E1 indicates SERCA conformation characterized by a high affinity for Ca2+. E1‐E2 represents a transient high energy state. E2 represents SERCA conformation characterized by a low affinity for Ca2+. Two cytosolic Ca2+ ions bind to SERCA in E1 conformation. ATP tethers to the nucleotide (N) domain and phosphorylates the (P) domain. The phosphorylated (P) domain interacts with the (A) domain resulting in two sequential conformational changes (E1‐E2, and E2). SERCA in E2 conformation releases Ca2+ into the SR lumen. Pi, inorganic phosphate; ADP, adenosine diphosphate; H+, proton.
Figure 5. Figure 5. Ca2+ signaling networks at myoendothelial projections (MEPs). Ca2+ influx via TRPV4/TRPV3/TRPA1/TRPC3 channels or Ca2+ release from the ER via IP3Rs at MEPs activates nearby small (SK) and intermediate (IK) conductance Ca2+‐activated K+ channels. IK/SK channel activation hyperpolarizes endothelial cells (EC) membrane and results in vasodilation. TRPV/TRPA/TRPC, members of transient receptor potential channel family.
Figure 6. Figure 6. Signaling mechanisms at myoendothelial projections (MEPs) that control the communication between endothelial cells (ECs) and smooth muscle cells (SMCs) and SMC contractility. Stimulation of Gq‐protein coupled receptors (GqPCRs) on SMC membrane leads to the formation of inositol triphosphate (IP3) and diacylglycerol (DAG). DAG activates protein kinase C (PKC), which phosphorylates voltage‐gated Ca2+ (CaV1.2) channel, leading to an increase in SMC Ca2+ and vasoconstriction. IP3 and Ca2+ can diffuse to ECs through myoendothelial gap junctions (MEGJ). Elevation of IP3 and Ca2+ at MEPs limits vasoconstriction by activating TRPV4‐IK/SK channel and IP3R‐IK/SK channel signaling. TRPV4, transient receptor potential vanilloid channel 4 (TRPV4); SK and IK, small (SK) and intermediate (IK) conductance Ca2+‐activated K+ channels.
Figure 7. Figure 7. The molecular mechanism underlying selective activation of IK/SK channels in mesenteric arteries versus eNOS in pulmonary arteries. In mesenteric arteries, Ca2+ entry through the TRPV4 channel at the myoendothelial projections (MEPs) determines vasodilation via activation of nearby small (SK) and intermediate (IK) conductance Ca2+‐activated K+ channels. Co‐localization of endothelial nitric oxide synthase (eNOS) with hemoglobin alpha (Hbα), a nitric oxide (NO) scavenging protein, prevents TRPV4‐eNOS signaling. On the contrary, in pulmonary arteries, IK/SK channels and Hbα do not localize at MEPs. Therefore, Ca2+ influx via TRPV4 channel activates eNOS causing NO‐dependent vasodilation. EC, endothelial cell.
Figure 8. Figure 8. The contribution of endothelial P2X purinergic receptor, PIEZO1, TRPP1, and TRPV4 channels to flow‐induced vasodilation. Sheer stress‐dependent activation of P2X, PIEZO1, TRPP1, and TRPV4 channels increases endothelial Ca2+. Shear stress‐induced increase in endothelial Ca2+ can cause vasodilation via one of the two pathways (i) activation of endothelial nitric oxide synthase (eNOS) and nitric oxide (NO)‐mediated vasodilation; and (ii) activation of IK/SK channels, leading to endothelium‐dependent hyperpolarization and vasodilation. TRPP1, transient receptor potential polycystic 1 channel; TRPV4, transient receptor potential vanilloid 4 channel.


Figure 1. The contrasting effects of smooth muscle cell (SMC) and endothelial cell (EC) Ca2+ on vascular contractility. Mechanical and neurohumoral stimuli can increase intracellular Ca2+ in SMCs and ECs. Intracellular Ca2+ in SMCs and ECs, in general, has opposite effects on vascular resistance. Increase in SMC Ca2+ activates the contractile machinery in SMCs (myosin light chain kinase or MLCK/Actin‐Myosin). In contrast, an increase in EC Ca2+ inhibits SMC contractile mechanisms. The dotted red line indicates inhibition of SMC contractility.


Figure 2. Regulation of vascular smooth muscle cell (SMC) contractility by voltage‐gated Ca2+ channels. Ca2+ entry through CaV1.2 and CaV3.1 channels promotes SMC contraction. Ca2+ influx through CaV3.2 channels activates ryanodine receptors (RyRs), triggering Ca2+ release from the sarcoplasmic reticulum (SR) in the vicinity of large conductance, Ca2+‐activated K+ (BK) channels. BK channel activation results in SMC hyperpolarization and vasodilation. The dotted line indicates the deactivation of CaV1.2 and CaV3.1 channels.


Figure 3. Regulation of vascular smooth muscle cell (SMC) contractility by non‐voltage‐gated Ca2+ entry mechanisms. (A) Activation of purinergic P2X receptor, TRPV4, TRPV1, TRPP1, TRPC3, and TRPC6 channels, and NCX in reverse mode increases SMC intracellular Ca2+, leading to vasoconstriction. (B) Ca2+ release from endo‐lysosome via TRPML1 channel, or Ca2+ entry through TRPV4 channel at the plasma membrane activates ryanodine receptors (RyRs), triggering Ca2+ release signals (Ca2+ sparks) from the sarcoplasmic reticulum (SR). Ca2+ sparks activate large‐conductance Ca2+‐activated potassium (BK) channels. BK channels hyperpolarize the SMC membrane and cause vasodilation. Ca2+ release through IP3R induces SMC contraction. Sarco‐endoplasmic reticulum Ca2+‐ATPase (SERCA), by sequestering cytoplasmic Ca2+ back into the SR, maintains low cytosolic Ca2+ concentration. TRPV, TRPP, TRPC, TRPML, members of transient receptor potential channel family; NCX, Na+/Ca2+ exchanger.


Figure 4. Sarco‐endoplasmic reticulum Ca2+‐ATPase (SERCA) transporting cycle. E1 indicates SERCA conformation characterized by a high affinity for Ca2+. E1‐E2 represents a transient high energy state. E2 represents SERCA conformation characterized by a low affinity for Ca2+. Two cytosolic Ca2+ ions bind to SERCA in E1 conformation. ATP tethers to the nucleotide (N) domain and phosphorylates the (P) domain. The phosphorylated (P) domain interacts with the (A) domain resulting in two sequential conformational changes (E1‐E2, and E2). SERCA in E2 conformation releases Ca2+ into the SR lumen. Pi, inorganic phosphate; ADP, adenosine diphosphate; H+, proton.


Figure 5. Ca2+ signaling networks at myoendothelial projections (MEPs). Ca2+ influx via TRPV4/TRPV3/TRPA1/TRPC3 channels or Ca2+ release from the ER via IP3Rs at MEPs activates nearby small (SK) and intermediate (IK) conductance Ca2+‐activated K+ channels. IK/SK channel activation hyperpolarizes endothelial cells (EC) membrane and results in vasodilation. TRPV/TRPA/TRPC, members of transient receptor potential channel family.


Figure 6. Signaling mechanisms at myoendothelial projections (MEPs) that control the communication between endothelial cells (ECs) and smooth muscle cells (SMCs) and SMC contractility. Stimulation of Gq‐protein coupled receptors (GqPCRs) on SMC membrane leads to the formation of inositol triphosphate (IP3) and diacylglycerol (DAG). DAG activates protein kinase C (PKC), which phosphorylates voltage‐gated Ca2+ (CaV1.2) channel, leading to an increase in SMC Ca2+ and vasoconstriction. IP3 and Ca2+ can diffuse to ECs through myoendothelial gap junctions (MEGJ). Elevation of IP3 and Ca2+ at MEPs limits vasoconstriction by activating TRPV4‐IK/SK channel and IP3R‐IK/SK channel signaling. TRPV4, transient receptor potential vanilloid channel 4 (TRPV4); SK and IK, small (SK) and intermediate (IK) conductance Ca2+‐activated K+ channels.


Figure 7. The molecular mechanism underlying selective activation of IK/SK channels in mesenteric arteries versus eNOS in pulmonary arteries. In mesenteric arteries, Ca2+ entry through the TRPV4 channel at the myoendothelial projections (MEPs) determines vasodilation via activation of nearby small (SK) and intermediate (IK) conductance Ca2+‐activated K+ channels. Co‐localization of endothelial nitric oxide synthase (eNOS) with hemoglobin alpha (Hbα), a nitric oxide (NO) scavenging protein, prevents TRPV4‐eNOS signaling. On the contrary, in pulmonary arteries, IK/SK channels and Hbα do not localize at MEPs. Therefore, Ca2+ influx via TRPV4 channel activates eNOS causing NO‐dependent vasodilation. EC, endothelial cell.


Figure 8. The contribution of endothelial P2X purinergic receptor, PIEZO1, TRPP1, and TRPV4 channels to flow‐induced vasodilation. Sheer stress‐dependent activation of P2X, PIEZO1, TRPP1, and TRPV4 channels increases endothelial Ca2+. Shear stress‐induced increase in endothelial Ca2+ can cause vasodilation via one of the two pathways (i) activation of endothelial nitric oxide synthase (eNOS) and nitric oxide (NO)‐mediated vasodilation; and (ii) activation of IK/SK channels, leading to endothelium‐dependent hyperpolarization and vasodilation. TRPP1, transient receptor potential polycystic 1 channel; TRPV4, transient receptor potential vanilloid 4 channel.
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Article Title: The Calcium Signaling Mechanisms in Arterial Smooth Muscle and Endothelial Cells
 

How to Cite

Matteo Ottolini, Swapnil K. Sonkusare. The Calcium Signaling Mechanisms in Arterial Smooth Muscle and Endothelial Cells. Compr Physiol 2021, 11: 1831-1869. doi: 10.1002/cphy.c200030