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Article ; Online: Dichotomous effects of in vivo and in vitro ionizing radiation exposure on lymphatic function.

Singh, Reetu / Heaps, Cristine L / Muthuchamy, Mariappan / Deveau, Michael A / Stewart, Randolph H / Laine, Glen A / Dongaonkar, Ranjeet M

American journal of physiology. Heart and circulatory physiology

2022 Volume 324, Issue 1, Page(s) H155–H171

Abstract: On the one hand, lymphatic dysfunction induces interstitial edema and inflammation. On the other hand, the formation of edema and inflammation induce lymphatic dysfunction. However, informed by the earlier reports of undetected apoptosis of irradiated ... ...

Abstract	On the one hand, lymphatic dysfunction induces interstitial edema and inflammation. On the other hand, the formation of edema and inflammation induce lymphatic dysfunction. However, informed by the earlier reports of undetected apoptosis of irradiated lymphatic endothelial cells (LECs) in vivo, lymphatic vessels are commonly considered inconsequential to ionizing radiation (IR)-induced inflammatory injury to normal tissues. Primarily because of the lack of understanding of the acute effects of IR exposure on lymphatic function, acute edema and inflammation, common sequelae of IR exposure, have been ascribed solely to blood vessel damage. Therefore, in the present study, the lymphatic acute responses to IR exposure were quantified to evaluate the hypothesis that IR exposure impairs lymphatic pumping. Rat mesenteric lymphatic vessels were irradiated in vivo or in vitro, and changes in pumping were quantified in isolated vessels in vitro. Compared with sham-treated vessels, pumping was lowered in lymphatic vessels irradiated in vivo but increased in vessels irradiated in vitro. Furthermore, unlike in blood vessels, the acute effects of IR exposure in lymphatic vessels were not mediated by nitric oxide-dependent pathways in either in vivo or in vitro irradiated vessels. After cyclooxygenase blockade, pumping was partially restored in lymphatic vessels irradiated in vitro but not in vessels irradiated in vivo. Taken together, these findings demonstrated that lymphatic vessels are radiosensitive and LEC apoptosis alone may not account for all the effects of IR exposure on the lymphatic system.
MeSH term(s)	Rats ; Animals ; Endothelial Cells/metabolism ; Lymphatic Vessels/metabolism ; Inflammation/metabolism ; Radiation, Ionizing ; Edema/metabolism
Language	English
Publishing date	2022-12-02
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	603838-4
ISSN	1522-1539 ; 0363-6135
ISSN (online)	1522-1539
ISSN	0363-6135
DOI	10.1152/ajpheart.00387.2022
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Article ; Online: Adaptation of the hepatic transudation barrier to sinusoidal hypertension.

Dongaonkar, Ranjeet M / Quick, Christopher M / Laine, Glen A / Uray, Karen / Cox, Charles S / Stewart, Randolph H

American journal of physiology. Regulatory, integrative and comparative physiology

2020 Volume 318, Issue 4, Page(s) R722–R729

Abstract: The role of the hepatic transudation barrier in determining ascites volume and protein content in chronic liver disease is poorly understood. Therefore, the purpose of the present study was to characterize how chronic sinusoidal hypertension impacts ... ...

Abstract	The role of the hepatic transudation barrier in determining ascites volume and protein content in chronic liver disease is poorly understood. Therefore, the purpose of the present study was to characterize how chronic sinusoidal hypertension impacts hepatic transudation barrier properties and the transudation rate. The suprahepatic inferior vena cava was surgically constricted, and animals were exposed to either short-term (SVH; 2-3 wk) or long-term venous hypertension (LVH; 5-6 wk). Compared with SVH, LVH resulted in lower peritoneal fluid pressure, ascites volume, and ascites protein concentration. The transudation barrier protein reflection coefficient was significantly higher, and the transudation barrier hydraulic conductivity, transudation rate, and transudate-to-lymph protein concentration ratio were significantly lower in LVH animals compared with SVH animals. The sensitivity of transudation rates to acute changes in interstitial fluid pressures was also significantly lower in LVH animals compared with SVH animals. In contrast, there was no detectable difference in hepatic lymph flow rate or sensitivity of lymph flow to acute changes in interstitial fluid pressures between SVH and LVH animals. Taken together, these data suggest that decreased hepatic transudation barrier permeability to fluid and protein and increased reflection coefficient led to a decrease in the hepatic contribution to ascites volume. The present work, to the best of our knowledge, is the first to quantify an anti-ascites adaptation of the hepatic transudation barrier in response to chronic hepatic sinusoidal hypertension.
MeSH term(s)	Adaptation, Physiological ; Animals ; Ascites/physiopathology ; Constriction, Pathologic/surgery ; Dogs ; Exudates and Transudates ; Hypertension/etiology ; Liver/physiopathology ; Male
Language	English
Publishing date	2020-02-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	603839-6
ISSN	1522-1490 ; 0363-6119
ISSN (online)	1522-1490
ISSN	0363-6119
DOI	10.1152/ajpregu.00178.2019
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Article ; Online: Direct Interstitial Decongestion in an Animal Model of Acute-on-Chronic Ischemic Heart Failure.

Abraham, William T / Jonas, Michael / Dongaonkar, Ranjeet M / Geist, Beth / Ueyama, Yukie / Render, Kevin / Youngblood, Brad / Muir, William / Hamlin, Robert / Del Rio, Carlos L

JACC. Basic to translational science

2021 Volume 6, Issue 11, Page(s) 872–881

Abstract: Removal of excess fluid in acute decompensated heart failure (ADHF) targets the intravascular space, whereas most fluid resides in the interstitial space. The authors evaluated an approach to interstitial decongestion using a device to enhance lymph flow. ...

Abstract	Removal of excess fluid in acute decompensated heart failure (ADHF) targets the intravascular space, whereas most fluid resides in the interstitial space. The authors evaluated an approach to interstitial decongestion using a device to enhance lymph flow. The device was deployed in sheep with induced heart failure (HF) and acute volume overload to create a low-pressure zone at the thoracic duct outlet. Treatment decreased extravascular lung water (EVLW) volume (mL/kg) (-32% ± 9%,
Language	English
Publishing date	2021-11-22
Publishing country	United States
Document type	Journal Article
ISSN	2452-302X
ISSN (online)	2452-302X
DOI	10.1016/j.jacbts.2021.09.008
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Article ; Online: Dichotomous effects on lymphatic transport with loss of caveolae in mice.

Baranwal, Gaurav / Creed, Heidi A / Cromer, Walter E / Wang, Wei / Upchurch, Bradley D / Smithhart, Matt C / Vadlamani, Suman S / Clark, Mary-Catherine C / Busbuso, Napoleon C / Blais, Stephanie N / Reyna, Andrea J / Dongaonkar, Ranjeet M / Zawieja, David C / Rutkowski, Joseph M

Acta physiologica (Oxford, England)

2021 Volume 232, Issue 4, Page(s) e13656

Abstract: Aim: Fluid and macromolecule transport from the interstitium into and through lymphatic vessels is necessary for tissue homeostasis. While lymphatic capillary structure suggests that passive, paracellular transport would be the predominant route of ... ...

Abstract	Aim: Fluid and macromolecule transport from the interstitium into and through lymphatic vessels is necessary for tissue homeostasis. While lymphatic capillary structure suggests that passive, paracellular transport would be the predominant route of macromolecule entry, active caveolae-mediated transcellular transport has been identified in lymphatic endothelial cells (LECs) in vitro. Caveolae also mediate a wide array of endothelial cell processes, including nitric oxide regulation. Thus, how does the lack of caveolae impact "lymphatic function"? Methods: Various aspects of lymphatic transport were measured in mice constitutively lacking caveolin-1 ("CavKO"), the protein required for caveolae formation in endothelial cells, and in mice with a LEC-specific Cav1 gene deletion (Lyve1-Cre x Cav1 Results: In each model, lymphatic architecture was largely unchanged. The lymphatic conductance, or initial tissue uptake, was significantly higher in both CavKO mice and LyCav mice by quantitative microlymphangiography and the permeability to 70 kDa dextran was significantly increased in monolayers of LECs isolated from CavKO mice. Conversely, transport within the lymphatic system to the sentinel node was significantly reduced in anaesthetized CavKO and LyCav mice. Isolated, cannulated collecting vessel studies identified significantly reduced phasic contractility when lymphatic endothelium lacks caveolae. Inhibition of nitric oxide synthase was able to partially restore ex vivo vessel contractility. Conclusion: Macromolecule transport across lymphatics is increased with loss of caveolae, yet phasic contractility reduced, resulting in reduced overall lymphatic transport function. These studies identify lymphatic caveolar biology as a key regulator of active lymphatic transport functions.
MeSH term(s)	Animals ; Caveolae/metabolism ; Caveolin 1 ; Endothelial Cells/metabolism ; Endothelium, Vascular/metabolism ; Lymphatic Vessels ; Mice ; Nitric Oxide Synthase/metabolism
Chemical Substances	Caveolin 1 ; Nitric Oxide Synthase (EC 1.14.13.39)
Language	English
Publishing date	2021-04-09
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2218636-0
ISSN	1748-1716 ; 1748-1708
ISSN (online)	1748-1716
ISSN	1748-1708
DOI	10.1111/apha.13656
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Article ; Online: Hepatic transudation barrier properties.

Dongaonkar, Ranjeet M / Stewart, Randolph H / Quick, Christopher M / Uray, Karen L / Cox, Charles S / Laine, Glen A

Microcirculation (New York, N.Y. : 1994)

2017 Volume 25, Issue 2

Abstract: Objective: Fluid and protein continuously transude from the surface of the liver. Despite a common understanding that transudation plays a critical role in hepatic interstitial and peritoneal fluid balance, transudation from the entire liver has not ... ...

Abstract	Objective: Fluid and protein continuously transude from the surface of the liver. Despite a common understanding that transudation plays a critical role in hepatic interstitial and peritoneal fluid balance, transudation from the entire liver has not been studied. Therefore, the goal of the present work was to provide the first direct measurement of the hepatic transudation rate and transudation barrier properties. Methods: Transudation rates were determined by collecting transudate from the entire liver. Hydraulic conductivity, and fluid transudation and protein reflection coefficients of the transudation barrier (formed by the subscapular interstitial matrix, capsule, and peritoneum) were determined from changes in fluid and protein transudation rates in response to hepatic venous pressure elevation. Results: Following hepatic venous pressure elevation from 6.1 ± 0.9 to 11.1 ± 0.6 mm Hg, transudation rate increased from 0.13 ± 0.03 to 0.37 ± 0.03 mL/min·100 g. Transudation barrier hydraulic conductivity, fluid transudation and protein reflection coefficients (3.9 × 10 Conclusions: Taken together, these findings suggest that the hepatic transudation barrier is highly permeable at elevated sinusoidal pressures. These fundamental studies provide a better understanding of the hepatic transudation barrier properties and transudation under conditions that are physiologically and clinically relevant to ascites formation.
MeSH term(s)	Animals ; Ascites ; Capillary Permeability/physiology ; Exudates and Transudates/metabolism ; Humans ; Kinetics ; Liver/metabolism ; Venous Pressure/physiology
Language	English
Publishing date	2017-10-16
Publishing country	United States
Document type	Journal Article
ZDB-ID	1217758-1
ISSN	1549-8719 ; 1073-9688
ISSN (online)	1549-8719
ISSN	1073-9688
DOI	10.1111/micc.12424
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Article ; Online: Myocardial microvascular permeability, interstitial oedema, and compromised cardiac function.

Dongaonkar, Ranjeet M / Stewart, Randolph H / Geissler, Hans J / Laine, Glen A

Cardiovascular research

2010 Volume 87, Issue 2, Page(s) 331–339

Abstract: The heart, perhaps more than any other organ, is exquisitely sensitive to increases in microvascular permeability and the accumulation of myocardial interstitial oedema fluid. Whereas some organs can cope with profound increases in the interstitial fluid ...

Abstract	The heart, perhaps more than any other organ, is exquisitely sensitive to increases in microvascular permeability and the accumulation of myocardial interstitial oedema fluid. Whereas some organs can cope with profound increases in the interstitial fluid volume or oedema formation without a compromise in function, heart function is significantly compromised with only a few percent increase in the interstitial fluid volume. This would be of little consequence if myocardial oedema were an uncommon pathology. On the contrary, myocardial oedema forms in response to many disease states as well as clinical interventions such as cardiopulmonary bypass and cardioplegic arrest common to many cardiothoracic surgical procedures. The heart's inability to function effectively in the presence of myocardial oedema is further confounded by the perplexing fact that the resolution of myocardial oedema does not restore normal cardiac function. We will attempt to provide some insight as to how microvascular permeability and myocardial oedema formation compromise cardiac function and discuss the acute changes that might take place in the myocardium to perpetuate compromised cardiac function following oedema resolution. We will also discuss compensatory changes in the interstitial matrix of the heart in response to chronic myocardial oedema and the role they play to optimize myocardial function during chronic oedemagenic disease.
MeSH term(s)	Animals ; Body Fluids/metabolism ; Capillary Permeability ; Coronary Vessels/metabolism ; Coronary Vessels/physiopathology ; Diagnostic Imaging/methods ; Edema, Cardiac/diagnosis ; Edema, Cardiac/metabolism ; Edema, Cardiac/physiopathology ; Hemodynamics ; Humans ; Microvessels/metabolism ; Microvessels/physiopathology ; Models, Cardiovascular ; Myocardial Contraction ; Myocardium/metabolism ; Predictive Value of Tests ; Signal Transduction ; Ventricular Function
Language	English
Publishing date	2010-05-13
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	80340-6
ISSN	1755-3245 ; 0008-6363
ISSN (online)	1755-3245
ISSN	0008-6363
DOI	10.1093/cvr/cvq145
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Article ; Online: Blood flow augmentation by intrinsic venular contraction in vivo.

Dongaonkar, Ranjeet M / Quick, Christopher M / Vo, Jonathan C / Meisner, Joshua K / Laine, Glen A / Davis, Michael J / Stewart, Randolph H

American journal of physiology. Regulatory, integrative and comparative physiology

2012 Volume 302, Issue 12, Page(s) R1436–42

Abstract: Venomotion, spontaneous cyclic contractions of venules, was first observed in the bat wing 160 years ago. Of all the functional roles proposed since then, propulsion of blood by venomotion remains the most controversial. Common animal models that require ...

Abstract	Venomotion, spontaneous cyclic contractions of venules, was first observed in the bat wing 160 years ago. Of all the functional roles proposed since then, propulsion of blood by venomotion remains the most controversial. Common animal models that require anesthesia and surgery have failed to provide evidence for venular pumping of blood. To determine whether venomotion actively pumps blood in a minimally invasive, unanesthetized animal model, we reintroduced the batwing model. We evaluated the temporal and functional relationship between the venous contraction cycle and blood flow and luminal pressure. Furthermore, we determined the effect of inhibiting venomotion on blood flow. We found that the active venous contractions produced an increase in the blood flow and exhibited temporal vessel diameter-blood velocity and pressure relationships characteristic of a peristaltic pump. The presence of valves, a characteristic of reciprocating pumps, enhances the efficiency of the venular peristaltic pump by preventing retrograde flow. Instead of increasing blood flow by decreasing passive resistance, venular dilation with locally applied sodium nitroprusside decreased blood flow. Taken together, these observations provide evidence for active venular pumping of blood. Although strong venomotion may be unique to bats, venomotion has also been inferred from venous pressure oscillations in other animal models. The conventional paradigm of microvascular pressure and flow regulation assumes venules only act as passive resistors, a proposition that must be reevaluated in the presence of significant venomotion.
MeSH term(s)	Animals ; Blood Flow Velocity/drug effects ; Blood Flow Velocity/physiology ; Blood Pressure/drug effects ; Blood Pressure/physiology ; Chiroptera ; Nitroprusside/pharmacology ; Regional Blood Flow/drug effects ; Regional Blood Flow/physiology ; Vasodilator Agents/pharmacology ; Venules/drug effects ; Venules/physiology ; Wings, Animal/blood supply
Chemical Substances	Vasodilator Agents ; Nitroprusside (169D1260KM)
Language	English
Publishing date	2012-04-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	603839-6
ISSN	1522-1490 ; 0363-6119
ISSN (online)	1522-1490
ISSN	0363-6119
DOI	10.1152/ajpregu.00635.2011
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Article ; Online: Award article: Microcirculatory Society Award for Excellence in Lymphatic Research: time course of myocardial interstitial edema resolution and associated left ventricular dysfunction.

Dongaonkar, Ranjeet M / Stewart, Randolph H / Quick, Christopher M / Uray, Karen L / Cox, Charles S / Laine, Glen A

Microcirculation (New York, N.Y. : 1994)

2012 Volume 19, Issue 8, Page(s) 714–722

Abstract: Objective: Although the causal relationship between acute myocardial edema and cardiac dysfunction has been established, resolution of myocardial edema and subsequent recovery of cardiac function have not been established. The time to resolve myocardial ...

Abstract	Objective: Although the causal relationship between acute myocardial edema and cardiac dysfunction has been established, resolution of myocardial edema and subsequent recovery of cardiac function have not been established. The time to resolve myocardial edema and the degree that cardiac function is depressed after edema resolves are not known. We therefore characterized temporal changes in cardiac function as acute myocardial edema formed and resolved. Methods: Acute myocardial edema was induced in the canine model by elevating coronary sinus pressure for three hours. Myocardial water content and cardiac function were determined before and during coronary sinus pressure elevation, and after coronary sinus pressure restoration. Results: Although no change in systolic properties was detected, accumulation of water in myocardial interstitium was associated with increased diastolic stiffness. When coronary sinus pressure was relieved, myocardial edema resolved within 180 minutes. Diastolic stiffness, however, remained significantly elevated compared with baseline values, and cardiac function remained compromised. Conclusions: The present work suggests that the cardiac dysfunction caused by the formation of myocardial edema may persist after myocardial edema resolves. With the advent of new imaging techniques to quantify myocardial edema, this insight provides a new avenue for research to detect and treat a significant cause of cardiac dysfunction.
MeSH term(s)	Animals ; Awards and Prizes ; Blood Pressure ; Coronary Sinus/metabolism ; Coronary Sinus/pathology ; Dogs ; Edema ; Myocardium/metabolism ; Myocardium/pathology ; Time Factors ; Ventricular Dysfunction, Left/metabolism ; Ventricular Dysfunction, Left/pathology ; Ventricular Dysfunction, Left/physiopathology ; Water/metabolism
Chemical Substances	Water (059QF0KO0R)
Language	English
Publishing date	2012-06-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1217758-1
ISSN	1549-8719 ; 1073-9688
ISSN (online)	1549-8719
ISSN	1073-9688
DOI	10.1111/j.1549-8719.2012.00204.x
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Article: First-order approximation for the pressure-flow relationship of spontaneously contracting lymphangions.

Quick, Christopher M / Venugopal, Arun M / Dongaonkar, Ranjeet M / Laine, Glen A / Stewart, Randolph H

American journal of physiology. Heart and circulatory physiology

2008 Volume 294, Issue 5, Page(s) H2144–9

Abstract: To return lymph to the great veins of the neck, it must be actively pumped against a pressure gradient. Mean lymph flow in a portion of a lymphatic network has been characterized by an empirical relationship (P(in) - P(out) = -P(p) + R(L)Q(L)), where P( ... ...

Abstract	To return lymph to the great veins of the neck, it must be actively pumped against a pressure gradient. Mean lymph flow in a portion of a lymphatic network has been characterized by an empirical relationship (P(in) - P(out) = -P(p) + R(L)Q(L)), where P(in) - P(out) is the axial pressure gradient and Q(L) is mean lymph flow. R(L) and P(p) are empirical parameters characterizing the effective lymphatic resistance and pump pressure, respectively. The relation of these global empirical parameters to the properties of lymphangions, the segments of a lymphatic vessel bounded by valves, has been problematic. Lymphangions have a structure like blood vessels but cyclically contract like cardiac ventricles; they are characterized by a contraction frequency (f) and the slopes of the end-diastolic pressure-volume relationship [minimum value of resulting elastance (E(min))] and end-systolic pressure-volume relationship [maximum value of resulting elastance (E(max))]. Poiseuille's law provides a first-order approximation relating the pressure-flow relationship to the fundamental properties of a blood vessel. No analogous formula exists for a pumping lymphangion. We therefore derived an algebraic formula predicting lymphangion flow from fundamental physical principles and known lymphangion properties. Quantitative analysis revealed that lymph inertia and resistance to lymph flow are negligible and that lymphangions act like a series of interconnected ventricles. For a single lymphangion, P(p) = P(in) (E(max) - E(min))/E(min) and R(L) = E(max)/f. The formula was tested against a validated, realistic mathematical model of a lymphangion and found to be accurate. Predicted flows were within the range of flows measured in vitro. The present work therefore provides a general solution that makes it possible to relate fundamental lymphangion properties to lymphatic system function.
MeSH term(s)	Animals ; Cattle ; Elasticity ; Lymph/physiology ; Lymphatic Vessels/anatomy & histology ; Lymphatic Vessels/physiology ; Models, Biological ; Muscle Contraction ; Muscle, Smooth/physiology ; Perfusion ; Pressure ; Reproducibility of Results ; Rheology ; Viscosity
Language	English
Publishing date	2008-03-07
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, P.H.S.
ZDB-ID	603838-4
ISSN	1522-1539 ; 0363-6135
ISSN (online)	1522-1539
ISSN	0363-6135
DOI	10.1152/ajpheart.00781.2007
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Article ; Online: Functional adaptation of bovine mesenteric lymphatic vessels to mesenteric venous hypertension.

Quick, Christopher M / Criscione, John C / Kotiya, Akhilesh / Dongaonkar, Ranjeet M / Hardy, Joanne / Wilson, Emily / Gashev, Anatoliy A / Laine, Glen A / Stewart, Randolph H

American journal of physiology. Regulatory, integrative and comparative physiology

2014 Volume 306, Issue 12, Page(s) R901–7

Abstract: Lymph flow is the primary mechanism for returning interstitial fluid to the blood circulation. Currently, the adaptive response of lymphatic vessels to mesenteric venous hypertension is not known. This study sought to determine the functional responses ... ...

Abstract	Lymph flow is the primary mechanism for returning interstitial fluid to the blood circulation. Currently, the adaptive response of lymphatic vessels to mesenteric venous hypertension is not known. This study sought to determine the functional responses of postnodal mesenteric lymphatic vessels. We surgically occluded bovine mesenteric veins to create mesenteric venous hypertension to elevate mesenteric lymph flow. Three days after surgery, postnodal mesenteric lymphatic vessels from mesenteric venous hypertension (MVH; n = 7) and sham surgery (Sham; n = 6) group animals were evaluated and compared. Contraction frequency (MVH: 2.98 ± 0.75 min(-1); Sham: 5.42 ± 0.81 min(-1)) and fractional pump flow (MVH: 1.14 ± 0.30 min(-1); Sham: 2.39 ± 0.32 min(-1)) were significantly lower in the venous occlusion group. These results indicate that postnodal mesenteric lymphatic vessels adapt to mesenteric venous hypertension by reducing intrinsic contractile activity.
MeSH term(s)	Adaptation, Physiological/physiology ; Animals ; Cattle/physiology ; Disease Models, Animal ; Female ; Hypertension/physiopathology ; Lymph/physiology ; Lymphatic System/physiology ; Lymphatic Vessels/physiology ; Mesenteric Veins/physiopathology ; Mesentery/physiology ; Microcirculation/physiology ; Time Factors ; Water-Electrolyte Balance/physiology
Language	English
Publishing date	2014-03-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	603839-6
ISSN	1522-1490 ; 0363-6119
ISSN (online)	1522-1490
ISSN	0363-6119
DOI	10.1152/ajpregu.00185.2013
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