Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish

Lasse Dahl Ejby Jensen; Renhai Cao; Eva-Maria Hedlund; Iris Söll; Jon O Lundberg; Giselbert Hauptmann; John Fleng Steffensen; Yihai Cao

doi:10.1073/pnas.0907608106

Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish

Lasse Dahl Ejby Jensen, Renhai Cao, Eva-Maria Hedlund, Iris Söll, Jon O Lundberg, Giselbert Hauptmann, John Fleng Steffensen, Yihai Cao

Marine Biology

40 Citations (Scopus)

Abstract

The blood and lymphatic vasculatures are structurally and functionally coupled in controlling tissue perfusion, extracellular interstitial fluids, and immune surveillance. Little is known, however, about the molecular mechanisms that underlie the regulation of bloodlymphatic vessel connections and lymphatic perfusion. Here we show in the adult zebrafish and glass catfish (Kryptopterus bicirrhis) that blood-lymphatic conduits directly connect arterial vessels to the lymphatic system. Under hypoxic conditions, arterial-lymphatic conduits (ALCs) became highly dilated and linearized by NO-induced vascular relaxation, which led to blood perfusion into the lymphatic system. NO blockage almost completely abrogated hypoxia-induced ALC relaxation and lymphatic perfusion. These findings uncover mechanisms underlying hypoxia-induced oxygen compensation by perfusion of existing lymphatics in fish. Our results might also imply that the hypoxia-induced NO pathway contributes to development of progression of pathologies, including promotion of lymphatic metastasis by modulating arterial-lymphatic conduits, in the mammalian system.

Original language	English
Journal	Proceedings of the National Academy of Science of the United States of America
Volume	106
Issue number	43
Pages (from-to)	18408-13
Number of pages	5
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.0907608106
Publication status	Published - 2009

Access to Document

10.1073/pnas.0907608106

Cite this

Dahl Ejby Jensen, L., Cao, R., Hedlund, E-M., Söll, I., Lundberg, J. O., Hauptmann, G., Steffensen, J. F., & Cao, Y. (2009). Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish. Proceedings of the National Academy of Science of the United States of America, 106(43), 18408-13. https://doi.org/10.1073/pnas.0907608106

Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish. / Dahl Ejby Jensen, Lasse; Cao, Renhai; Hedlund, Eva-Maria et al.

In: Proceedings of the National Academy of Science of the United States of America, Vol. 106, No. 43, 2009, p. 18408-13.

Research output: Contribution to journal › Journal article › Research › peer-review

Dahl Ejby Jensen, L, Cao, R, Hedlund, E-M, Söll, I, Lundberg, JO, Hauptmann, G, Steffensen, JF & Cao, Y 2009, 'Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish', Proceedings of the National Academy of Science of the United States of America, vol. 106, no. 43, pp. 18408-13. https://doi.org/10.1073/pnas.0907608106

@article{00a3bc00e65611deba73000ea68e967b,

title = "Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish",

abstract = "The blood and lymphatic vasculatures are structurally and functionally coupled in controlling tissue perfusion, extracellular interstitial fluids, and immune surveillance. Little is known, however, about the molecular mechanisms that underlie the regulation of bloodlymphatic vessel connections and lymphatic perfusion. Here we show in the adult zebrafish and glass catfish (Kryptopterus bicirrhis) that blood-lymphatic conduits directly connect arterial vessels to the lymphatic system. Under hypoxic conditions, arterial-lymphatic conduits (ALCs) became highly dilated and linearized by NO-induced vascular relaxation, which led to blood perfusion into the lymphatic system. NO blockage almost completely abrogated hypoxia-induced ALC relaxation and lymphatic perfusion. These findings uncover mechanisms underlying hypoxia-induced oxygen compensation by perfusion of existing lymphatics in fish. Our results might also imply that the hypoxia-induced NO pathway contributes to development of progression of pathologies, including promotion of lymphatic metastasis by modulating arterial-lymphatic conduits, in the mammalian system.",

author = "{Dahl Ejby Jensen}, Lasse and Renhai Cao and Eva-Maria Hedlund and Iris S{\"o}ll and Lundberg, {Jon O} and Giselbert Hauptmann and Steffensen, {John Fleng} and Yihai Cao",

year = "2009",

doi = "10.1073/pnas.0907608106",

language = "English",

volume = "106",

pages = "18408--13",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "The National Academy of Sciences of the United States of America",

number = "43",

}

TY - JOUR

T1 - Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish

AU - Dahl Ejby Jensen, Lasse

AU - Cao, Renhai

AU - Hedlund, Eva-Maria

AU - Söll, Iris

AU - Lundberg, Jon O

AU - Hauptmann, Giselbert

AU - Steffensen, John Fleng

AU - Cao, Yihai

PY - 2009

Y1 - 2009

N2 - The blood and lymphatic vasculatures are structurally and functionally coupled in controlling tissue perfusion, extracellular interstitial fluids, and immune surveillance. Little is known, however, about the molecular mechanisms that underlie the regulation of bloodlymphatic vessel connections and lymphatic perfusion. Here we show in the adult zebrafish and glass catfish (Kryptopterus bicirrhis) that blood-lymphatic conduits directly connect arterial vessels to the lymphatic system. Under hypoxic conditions, arterial-lymphatic conduits (ALCs) became highly dilated and linearized by NO-induced vascular relaxation, which led to blood perfusion into the lymphatic system. NO blockage almost completely abrogated hypoxia-induced ALC relaxation and lymphatic perfusion. These findings uncover mechanisms underlying hypoxia-induced oxygen compensation by perfusion of existing lymphatics in fish. Our results might also imply that the hypoxia-induced NO pathway contributes to development of progression of pathologies, including promotion of lymphatic metastasis by modulating arterial-lymphatic conduits, in the mammalian system.

AB - The blood and lymphatic vasculatures are structurally and functionally coupled in controlling tissue perfusion, extracellular interstitial fluids, and immune surveillance. Little is known, however, about the molecular mechanisms that underlie the regulation of bloodlymphatic vessel connections and lymphatic perfusion. Here we show in the adult zebrafish and glass catfish (Kryptopterus bicirrhis) that blood-lymphatic conduits directly connect arterial vessels to the lymphatic system. Under hypoxic conditions, arterial-lymphatic conduits (ALCs) became highly dilated and linearized by NO-induced vascular relaxation, which led to blood perfusion into the lymphatic system. NO blockage almost completely abrogated hypoxia-induced ALC relaxation and lymphatic perfusion. These findings uncover mechanisms underlying hypoxia-induced oxygen compensation by perfusion of existing lymphatics in fish. Our results might also imply that the hypoxia-induced NO pathway contributes to development of progression of pathologies, including promotion of lymphatic metastasis by modulating arterial-lymphatic conduits, in the mammalian system.

U2 - 10.1073/pnas.0907608106

DO - 10.1073/pnas.0907608106

M3 - Journal article

C2 - 19822749

SN - 0027-8424

VL - 106

SP - 18408

EP - 18413

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 43

ER -

Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish

Abstract

Access to Document

Fingerprint

Cite this