Adaptation of mesenteric lymphatic vessels to prolonged changes in transmural pressure

Dongaonkar, Ranjeet M.; Nguyen, Tam Luong; Quick, Christopher M.; Hardy, Joanne; Laine, Glen A.; Wilson, Emily; Stewart, Randolph H.

doi:10.1152/ajpheart.00677.2012

Cited by 32 publications

(23 citation statements)

References 44 publications

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“…[115][116][117][118][119][120][121][122] Lymphatic obstruction and impaired contraction may lead to lymphangiogenesis and immunosuppression. [123][124][125] The altered lymphatic features have been recapitulated in experimental colitis, supporting the notion that lymphangitis may be related to the pathogenesis of CD.…”

Section: Lymphaticsmentioning

confidence: 99%

The Role of the Mesentery in Crohnʼs Disease

Zhu

Zuo

et al. 2016

Inflammatory Bowel Diseases

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Crohn's disease (CD) is a complex gastrointestinal disorder involving multiple levels of cross talk between the immunological, neural, vascular, and endocrine systems. The current dominant theory in CD is based on the unidirectional axis of dysbiosis-innate immunity-adaptive immunity-mesentery-body system. Emerging clinical evidence strongly suggests that the axis be bidirectional. The morphologic and/or functional abnormalities in the mesenteric structures likely contribute to the disease progression of CD, to a less extent the disease initiation. In addition to adipocytes, mesentery contains nerves, blood vessels, lymphatics, stromal cells, and fibroblasts. By the secretion of adipokines that have endocrine functions, the mesenteric fat tissue exerts its activity in immunomodulation mainly through response to afferent signals, neuropeptides, and functional cytokines. Mesenteric nerves are involved in the pathogenesis and prognosis of CD mainly through neuropeptides. In addition to angiogenesis observed in CD, lymphatic obstruction, remodeling, and impaired contraction maybe a cause and consequence of CD. Lymphangiogenesis and angiogenesis play a concomitant role in the progress of chronic intestinal inflammation. Finally, the interaction between neuropeptides, adipokines, and vascular and lymphatic endothelia leads to adipose tissue remodeling, which makes the mesentery an active participator, not a bystander, in the disease initiation and precipitation CD. The identification of the role of mesentery, including the structure and function of mesenteric nerves, vessels, lymphatics, and fat, in the intestinal inflammation in CD has important implications in understanding its pathogenesis and clinical management.

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Section: Lymphaticsmentioning

confidence: 99%

The Role of the Mesentery in Crohnʼs Disease

Zhu

Zuo

et al. 2016

Inflammatory Bowel Diseases

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“…Mesenteric venous hypertension and resulting interstitial edema may also result from chronic conditions such as mesenteric venous thrombosis or portal hypertension. However, how lymphangion function is affected by increases in pressure and flow over the course of days has been investigated only recently (11,38). Exposure to sustained increases in transmural pressure resulted in bovine mesenteric lymphangions adapting to become better pumps (11), whereas exposure to sustained mesenteric venous hypertension resulted in them adapting to become less effective pumps (38).…”

Section: Mesenteric Venous Hypertension Alters Lymphatic Transmural Pmentioning

confidence: 99%

“…However, how lymphangion function is affected by increases in pressure and flow over the course of days has been investigated only recently (11,38). Exposure to sustained increases in transmural pressure resulted in bovine mesenteric lymphangions adapting to become better pumps (11), whereas exposure to sustained mesenteric venous hypertension resulted in them adapting to become less effective pumps (38). These two studies characterized adaptation of lymphatic vessels in terms of standard indices of lymphatic function such as ejection fraction and pump index.…”

Section: Mesenteric Venous Hypertension Alters Lymphatic Transmural Pmentioning

confidence: 99%

“…Gashev et al (17) reported that mesenteric lymphatic vessel function adapts when rats were chronically exposed to simulated microgravity. Dongaonkar et al (11) used lymphatic coarctation in vivo to study the effect of a 3-day change in transmural pressure on mesenteric lymphatic vessel function. They found that vessel segments exposed to higher pressures adapted to become stronger pumps.…”

Section: Extending Understanding Of Adaptive Responses Of Lymphatic Vmentioning

confidence: 99%

“…Dongaonkar et al (11) recently reported that lymphatic vessels adapt to changes in transmural pressure within a 3-day period. Blood vessels also have been reported to functionally adapt within 3 days of altered luminal flow (44).…”

Section: Implications To Edema Resolutionmentioning

confidence: 99%

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Mesenteric lymphatic vessels adapt to mesenteric venous hypertension by becoming weaker pumps

Dongaonkar¹,

Nguyen²,

Quick³

et al. 2015

American Journal of Physiology-Regulatory, Integrative and Comp

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Lymphangions, the segments of lymphatic vessels between two adjacent lymphatic valves, actively pump lymph. Acute changes in transmural pressure and lymph flow have profound effects on lymphatic pump function in vitro. Chronic changes in pressure and flow in vivo have also been reported to lead to significant changes in lymphangion function. Because changes in pressure and flow are both cause and effect of adaptive processes, characterizing adaptation requires a more fundamental analysis of lymphatic muscle properties. Therefore, the purpose of the present work was to use an intact lymphangion isovolumetric preparation to evaluate changes in mesenteric lymphatic muscle mechanical properties and the intracellular Ca(2+) in response to sustained mesenteric venous hypertension. Bovine mesenteric veins were surgically occluded to create mesenteric venous hypertension. Postnodal mesenteric lymphatic vessels from mesenteric venous hypertension (MVH; n = 6) and sham surgery (Sham; n = 6) animals were isolated and evaluated 3 days after the surgery. Spontaneously contracting MVH vessels generated end-systolic active tension and end-diastolic active tension lower than the Sham vessels. Furthermore, steady-state active tension and intracellular Ca(2+) concentration levels in response to KCl stimulation were also significantly lower in MVH vessels compared with those of the Sham vessels. There was no significant difference in passive tension in lymphatic vessels from the two groups. Taken together, these results suggest that following 3 days of mesenteric venous hypertension, postnodal mesenteric lymphatic vessels adapt to become weaker pumps with decreased cytosolic Ca(2+) concentration.

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High‐speed microscopy for in vivo monitoring of lymph dynamics

Sarimollaoglu

Stolarz

Nedosekin

et al. 2018

Journal of Biophotonics

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The lymphatic system contributes to body homeostasis by clearing fluid, lipids, plasma proteins and immune cells from the interstitial space. Many studies have been performed to understand lymphatic function under normal conditions and during disease. Nevertheless, a further improvement in quantification of lymphatic behavior is needed. Here, we present advanced bright-field microscopy for in vivo imaging of lymph vessels (LVs) and automated quantification of lymphatic function at a temporal resolution of 2 milliseconds. Full frame videos were compressed and recorded continuously at up to 540 frames per second. A new edge detection algorithm was used to monitor vessel diameter changes across multiple cross sections, while individual cells in the LVs were tracked to estimate flow velocity. The system performance initially was verified in vitro using 6- and 10-μm microspheres as cell phantoms on slides and in 90-μm diameter tubes at flow velocities up to 4 cm/second. Using an in vivo rat model, we explored the mechanisms of lymphedema after surgical lymphadenectomy of the mesentery. The system revealed reductions of mesenteric LV contraction and flow rate. Thus, the described imaging system may be applicable to the study of lymphatic behavior during therapeutic and surgical interventions, and potentially during lymphatic system diseases.

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Adaptation of mesenteric lymphatic vessels to prolonged changes in transmural pressure

Cited by 32 publications

References 44 publications

The Role of the Mesentery in Crohnʼs Disease

The Role of the Mesentery in Crohnʼs Disease

Mesenteric lymphatic vessels adapt to mesenteric venous hypertension by becoming weaker pumps

High‐speed microscopy for in vivo monitoring of lymph dynamics

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