Endothelial C-Type Natriuretic Peptide Acts on Pericytes to Regulate Microcirculatory Flow and Blood Pressure
Abstract
Background: Peripheral vascular resistance has a major impact on arterial blood pressure levels. Endothelial C-type natriuretic peptide (CNP) participates in the local regulation of vascular tone, but the target cells remain controversial. The cGMP-producing guanylyl cyclase–B (GC-B) receptor for CNP is expressed in vascular smooth muscle cells (SMCs). However, whereas endothelial cell–specific CNP knockout mice are hypertensive, mice with deletion of GC-B in vascular SMCs have unaltered blood pressure. Methods: We analyzed whether the vasodilating response to CNP changes along the vascular tree, ie, whether the GC-B receptor is expressed in microvascular types of cells. Mice with a floxed GC-B ( Npr2 ) gene were interbred with Tie2-Cre or PDGF-Rβ-Cre ERT2 lines to develop mice lacking GC-B in endothelial cells or in precapillary arteriolar SMCs and capillary pericytes. Intravital microscopy, invasive and noninvasive hemodynamics, fluorescence energy transfer studies of pericyte cAMP levels in situ, and renal physiology were combined to dissect whether and how CNP/GC-B/cGMP signaling modulates microcirculatory tone and blood pressure. Results: Intravital microscopy studies revealed that the vasodilatatory effect of CNP increases toward small-diameter arterioles and capillaries. CNP consistently did not prevent endothelin-1–induced acute constrictions of proximal arterioles, but fully reversed endothelin effects in precapillary arterioles and capillaries. Here, the GC-B receptor is expressed both in endothelial and mural cells, ie, in pericytes. It is notable that the vasodilatatory effects of CNP were preserved in mice with endothelial GC-B deletion, but abolished in mice lacking GC-B in microcirculatory SMCs and pericytes. CNP, via GC-B/cGMP signaling, modulates 2 signaling cascades in pericytes: it activates cGMP-dependent protein kinase I to phosphorylate downstream targets such as the cytoskeleton-associated vasodilator-activated phosphoprotein, and it inhibits phosphodiesterase 3A, thereby enhancing pericyte cAMP levels. These pathways ultimately prevent endothelin-induced increases of pericyte calcium levels and pericyte contraction. Mice with deletion of GC-B in microcirculatory SMCs and pericytes have elevated peripheral resistance and chronic arterial hypertension without a change in renal function. Conclusions: Our studies indicate that endothelial CNP regulates distal arteriolar and capillary blood flow. CNP-induced GC-B/cGMP signaling in microvascular SMCs and pericytes is essential for the maintenance of normal microvascular resistance and blood pressure.
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C-type natriuretic peptide can reverse ET-mediated effects by blocking Ca2+ release from internal stores and activating myosin light chain phosphatase.
“C-type natriuretic peptide (CNP), which can reverse ET-mediated effects (36) by blocking Ca2+ release from internal stores and activating myosin light chain phosphatase (Fig. S8).”
From Amyloid β oligomers constrict human capillaries in Alzheimer's disease via signaling to pericytes (2019) · cites this paper as [36]
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- Authors
- Špiranec, K., Chen, W., Werner, F., Nikolaev, V. O., Naruke, T., Koch, F., Werner, A., Eder-Negrin, P., Diéguez-Hurtado, R., Adams, R. H., Baba, H. A., Schmidt, H., Schuh, K., Skryabin, B. V., Movahedi, K., Schweda, F., & Kuhn, M.
- Affiliations
- University of Würzburg (DE)
- University Medical Center Hamburg-Eppendorf (DE)
- University of Regensburg (DE)
- Max-Planck-Institute for Molecular Biomedicine, Department of Tissue Morphogenesis (R.D.-H., R.H.A.)
- Max Planck Institute for Molecular Biomedicine (DE)
- University of Münster (DE)
- University of Tübingen (DE)
- Core Facility Transgenic Animal and genetic engineering Models (B.V.S.)
- Vrije Universiteit Brussel (BE)
- Institute of Physiology, University of Würzburg and Comprehensive Heart Failure Center, University Hospital Würzburg, Germany (K. Špiranec, W.C., S.C., F.W., T.N., F.K., P.E.-N., K. Schuh, M.K.).
- ORCID
- Venue
- Circulation
- Published
- 2018-07-31
- Volume
- 138
- Issue
- 5
- Pages
- 494-508
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- OpenAlex
- W2796415004
- Cited by
- 135
- References
- 53
- Citations by year
- 2026: 12 · 2025: 14 · 2024: 20 · 2023: 10 · 2022: 20 · 2021: 15 · 2020: 21 · 2019: 19 · 2018: 4
- FWCI
- 10.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- Universitätsbibliographie, Universität Duisburg-Essen (submittedVersion)
- University of Regensburg Publication Server (University of Regensburg) (submittedVersion)
- VUBIR (Vrije Universiteit Brussel) (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Health Sciences › Medicine › Surgery › Cardiovascular, Neuropeptides, and Oxidative Stress Research
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Blood Pressure and Hypertension Studies
- Keywords
- guanylyl cyclase B, cGMP signaling, pericytes, microcirculatory resistance, blood pressure regulation, vascular smooth muscle cells, endothelin-1, vasodilation, cGMP-dependent protein kinase I, PDE3A, cyclic AMP, pericyte contraction, systemic vascular resistance, hypertension
- MeSH terms
- Atrial Natriuretic Factor Receptor B, Animals, Cells, Cultured, Cyclic GMP, Hypertension, Mice, Inbred C57BL, Microcirculation, Phenotype, Vasodilation, Vasodilator Agents, Biosensing Techniques, Receptors, Atrial Natriuretic Factor, Mice, Knockout, Paracrine Communication, Calcium Signaling, Genetic Predisposition to Disease, Natriuretic Peptide, C-Type, Pericytes, Receptor, Platelet-Derived Growth Factor beta, Fluorescence Resonance Energy Transfer, Endothelial Cells, Microvessels, Arterial Pressure
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