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Cited by 49Lymphatic System and DiseasesLymphatic Disorders and TreatmentsIon Transport and Channel Regulation

Permeability and contractile responses of collecting lymphatic vessels elicited by atrial and brain natriuretic peptides

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Scallan, Joshua P., Davis, Michael J., Huxley, Virginia H.·2013·The Journal of Physiology
DOI 10.1113/jphysiol.2013.260042PMC PMC3810810
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Abstract

Key points: Atrial and brain natriuretic peptides (ANP and BNP, respectively) are hormones released into the bloodstream when heart muscle is stretched (e.g. zero‐gravity, hypertension, congestive heart failure) and serve to reduce the blood volume. One way that these peptides relieve blood volume is to increase the permeability of the smallest blood vessels, facilitating fluid and protein distribution into the tissue spaces. Whether these peptides target lymphatic vessel function to participate in fluid distribution is currently unknown. ANP and BNP (100 n m ) both elicited significant increases in lymphatic vessel permeability, but altered contractile function differentially in vivo. A likely consequence is that more fluid leaks from the lymphatics into the tissues, which represents a novel compensation for volume overload. This work demonstrates for the first time that lymphatic vessel permeability can be regulated in vivo . Abstract Atrial and brain natriuretic peptides (ANP and BNP, respectively) are cardiac hormones released into the bloodstream in response to hypervolaemia or fluid shifts to the central circulation. The actions of both peptides include natriuresis and diuresis, a decrease in systemic blood pressure, and inhibition of the renin–angiotensin–aldosterone system. Further, ANP and BNP elicit increases in blood microvessel permeability sufficient to cause protein and fluid extravasation into the interstitium to reduce the vascular volume. Given the importance of the lymphatic vasculature in maintaining fluid balance, we tested the hypothesis that ANP or BNP (100 n m ) would likewise elevate lymphatic permeability ( P s ) to serum albumin. Using a microfluorometric technique adapted to in vivo lymphatic vessels, we determined that rat mesenteric collecting lymphatic P s to rat serum albumin increased by 2.0 ± 0.4‐fold ( P = 0.01, n = 7) and 2.7 ± 0.8‐fold ( P = 0.07, n = 7) with ANP and BNP, respectively. In addition to measuring P s responses, we observed changes in spontaneous contraction amplitude and frequency from the albumin flux tracings in vivo . Notably, ANP abolished spontaneous contraction amplitude ( P = 0.005) and frequency ( P = 0.006), while BNP augmented both parameters by ∼2‐fold ( P < 0.01 each). These effects of ANP and BNP on contractile function were examined further by using an in vitro assay. In aggregate, these data support the theory that an increase in collecting lymphatic permeability opposes the absorptive function of the lymphatic capillaries , and aids in the retention of protein and fluid in the interstitial space to counteract volume expansion.

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  • Collecting vessel permeability to albumin is comparable to that of venules.

    “Collecting vessel permeability to albumin has been measured only in a few studies (31–33) and is comparable to that of venules.”

    From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [32]

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1 of the 40 references couldn’t be matched to a known paper.

Research works printed but not linked: 4

  1. Curry FE. Mechanics and thermodynamics of trancapillary exchange. In: Renkin EM, Michel CC, editors. Handbook of Physiology, section II, The Cardiovascular System, vol. IV, Microcirculation. Bethesda, MD, USA: American Physiological Society; 1984. pp. 309–374. [Google Scholar]
  2. Ji L-P, Huxley VH. Elevation of skeletal muscle arteriole permeability to protein by atrial natriuretic peptide. FASEB J. 2000;14:A25. [Google Scholar]
  3. Landis EM, Pappenheimer JR. Exchange of substances through the capillary walls. In: Hamilton WF, editor. Handbook of Physiology. Washington, DC, USA: American Physiological Society; 1963. pp. 961–1034. [Google Scholar]
  4. McKay MK. Department of Medical Pharmacology and Physiology. Columbia, MO, USA: University of Missouri at Columbia; 1994. Studies on the permeability of the capillary barrier: effects of perfusate proteins and natriuretic factors. [Google Scholar]

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Authors
Scallan, J. P., Davis, M. J., & Huxley, V. H.
Affiliations
  • University of Missouri Health System (US)
  • University of Missouri (US)
ORCID
Venue
The Journal of Physiology
Publisher
Wiley
Published
2013-08-29
Volume
591
Issue
20
Pages
5071-5081
ISSN
  • 0022-3751 (ISSN-L)
  • 1469-7793
DOI
10.1113/jphysiol.2013.260042
PMC
PMC3810810
OpenAlex
W2169165477
Cited by
49
References
40
Citations by year
2026: 2 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 4 · 2021: 5 · 2020: 2 · 2019: 4 · 2018: 7 · 2017: 6 · 2016: 5 · 2015: 3 · 2014: 2 · 2013: 1
FWCI
1.96
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • The Journal of Physiology (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • University of Missouri
  • National Institutes of Health
  • National Heart, Lung, and Blood Institute (HL089784, HL078816, R01HL078816, R01HL089784)
Topics
  • Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
  • Health Sciences › Medicine › Surgery › Lymphatic Disorders and Treatments
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
Keywords
natriuretic peptides, atrial natriuretic peptide, brain natriuretic peptide, lymphatic vessel contractility, serum albumin, mesenteric lymphatics, fluid balance, fluid overload, lymphatic microcirculation, lymphatic endothelium
MeSH terms
Animals, Capillary Permeability, Male, Muscle Contraction, Atrial Natriuretic Factor, Serum Albumin, Rats, Sprague-Dawley, Natriuretic Peptide, Brain, Lymphatic Vessels, Rats

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