Lymphatic fluid: exchange mechanisms and regulation

Abstract  Regulation of fluid and material movement between the vascular space of microvessels penetrating functioning organs and the cells therein has been studied extensively. Unanswered questions as to the regulatory mechanisms and routes remain. Significantly less is known about the lymphatic vascular system given the difficulties in seeing, no less isolating, these vessels lying deeper in these same tissues. It has become evident that the exchange microvasculature is not simply a passive biophysical barrier separating the vascular and interstitial compartments but a dynamic, multicellular structure subject to acute regulation and chronic adaptation to stimuli including inflammation, sepsis, diabetes, injury, hypoxia and exercise. Similarly lymphatic vessels range, in their simplest form, from lymphatic endothelium attached to the interstitial matrix, to endothelia and phasic lymphatic smooth muscle that act as Starling resistors. Recent work has demonstrated that among the microvascular lymphatic elements, the collecting lymphatics have barrier properties similar to venules, and thus participate in exchange. As with venules, vasoactive agents can alter both the permeability and contractile properties thereby setting up previously unanticipated gradients in the tissue space and providing potential targets for the pharmacological prevention and/or resolution of oedema.

[1]  R. Sumagin,et al.  Leukocyte-endothelial cell interactions are linked to vascular permeability via ICAM-1-mediated signaling. , 2008, American journal of physiology. Heart and circulatory physiology.

[2]  C. Michel,et al.  Steady‐state fluid filtration at different capillary pressures in perfused frog mesenteric capillaries. , 1987, The Journal of physiology.

[3]  C. K. Drinker The Functional Significance of the Lymphatic System: Harvey Lecture, December 16, 1937. , 1938, Bulletin of the New York Academy of Medicine.

[4]  E. M. Renkin,et al.  Exchange of Substances Through Capillary Walls , 2008 .

[5]  V. Huxley,et al.  Altered basal and adenosine-mediated protein flux from coronary arterioles isolated from exercise-trained pigs. , 1997, Acta physiologica Scandinavica.

[6]  William C. Aird,et al.  Phenotypic Heterogeneity of the Endothelium: I. Structure, Function, and Mechanisms , 2007, Circulation research.

[7]  V. Huxley,et al.  In vivo determination of collecting lymphatic vessel permeability to albumin: a role for lymphatics in exchange , 2010, The Journal of physiology.

[8]  Elisabetta Dejana,et al.  Functionally specialized junctions between endothelial cells of lymphatic vessels , 2007, The Journal of experimental medicine.

[9]  M. J. Davis,et al.  Signaling mechanisms underlying the vascular myogenic response. , 1999, Physiological reviews.

[10]  J. Scallan Collecting lymphatic vessel permeability to albumin and its modification by natriuretic peptides , 2010 .

[11]  V. Huxley,et al.  Increased capillary hydraulic conductivity induced by atrial natriuretic peptide. , 1987, Circulation research.

[12]  V. Huxley,et al.  Macromolecule permeability of in situ and excised rodent skeletal muscle arterioles and venules. , 2006, American journal of physiology. Heart and circulatory physiology.

[13]  A. Malik,et al.  Signaling mechanisms regulating endothelial permeability. , 2006, Physiological reviews.

[14]  J. Burnett,et al.  Natriuretic peptides in the pathophysiology of congestive heart failure , 2000, Current cardiology reports.

[15]  Virginia H Huxley,et al.  Cardiovascular sex differences influencing microvascular exchange. , 2010, Cardiovascular research.

[16]  R. Reed,et al.  Transcapillary exchange: role and importance of the interstitial fluid pressure and the extracellular matrix. , 2010, Cardiovascular research.

[17]  E. Starling On the Absorption of Fluids from the Connective Tissue Spaces , 1896, The Journal of physiology.

[18]  V. Huxley,et al.  Adaptation of coronary microvascular exchange in arterioles and venules to exercise training and a role for sex in determining permeability responses. , 2007, American journal of physiology. Heart and circulatory physiology.

[19]  M. Fabbro,et al.  Subatmospheric pressure in the rabbit pleural lymphatic network , 1999, The Journal of physiology.

[20]  Pingnian He,et al.  Endothelial [Ca2+]i and caveolin-1 antagonistically regulate eNOS activity and microvessel permeability in rat venules. , 2010, Cardiovascular research.

[21]  W. Aird Phenotypic Heterogeneity of the Endothelium: II. Representative Vascular Beds , 2007, Circulation research.

[22]  D. Hocking,et al.  Extracellular Matrix Fibronectin Mechanically Couples Skeletal Muscle Contraction With Local Vasodilation , 2008, Circulation research.

[23]  J. Benoit Effects of alpha-adrenergic stimuli on mesenteric collecting lymphatics in the rat. , 1997, The American journal of physiology.

[24]  V. Huxley,et al.  Vasoactive hormones and autocrine activation of capillary exchange barrier function. , 1993, Blood cells.

[25]  Zhe Sun,et al.  Extracellular matrix-specific focal adhesions in vascular smooth muscle produce mechanically active adhesion sites. , 2008, American journal of physiology. Cell physiology.

[26]  V. Huxley,et al.  Differential actions of albumin and plasma on capillary solute permeability. , 1991, The American journal of physiology.

[27]  F. Curry,et al.  Microvascular permeability. , 1999, Physiological reviews.

[28]  K. Druey,et al.  Narrative Review: The Systemic Capillary Leak Syndrome , 2010, Annals of Internal Medicine.

[29]  D. Zawieja,et al.  Chapter 5 – Microlymphatic Biology , 2008 .

[30]  V. Huxley,et al.  Sexual dimorphism in the permeability response of coronary microvessels to adenosine. , 2005, American journal of physiology. Heart and circulatory physiology.

[31]  Rajiva Gupta,et al.  Idiopathic systemic capillary leak syndrome (SCLS): case report and systematic review of cases reported in the last 16 years. , 2007, Internal medicine.

[32]  Vh Huxley,et al.  The Microvasculature As A Dynamic Regulator Of Volume And Solute Exchange , 2000, Clinical and experimental pharmacology & physiology.

[33]  V. Huxley,et al.  Adenosine A2A receptor modulation of juvenile female rat skeletal muscle microvessel permeability. , 2006, American journal of physiology. Heart and circulatory physiology.

[34]  J. Levick,et al.  Microvascular fluid exchange and the revised Starling principle. , 2010, Cardiovascular research.

[35]  David C Zawieja,et al.  Contractile physiology of lymphatics. , 2009, Lymphatic research and biology.

[36]  V. Huxley,et al.  ANP increases capillary permeability to protein independent of perfusate protein composition. , 1995, The American journal of physiology.

[37]  L. Zimmerli,et al.  Angiogenesis and hypertension: an update , 2009, Journal of Human Hypertension.

[38]  G. Schmid-Schönbein,et al.  Microlymphatics and lymph flow. , 1990, Physiological reviews.

[39]  R. Sarai,et al.  Epac/Rap1 pathway regulates microvascular hyperpermeability induced by PAF in rat mesentery. , 2008, American journal of physiology. Heart and circulatory physiology.

[40]  A. Taylor,et al.  Lymph formation and flow. , 1977, Annual review of physiology.

[41]  G. Clough,et al.  Simultaneous measurement of pressure in the interstitium and the terminal lymphatics of the cat mesentery. , 1978, The Journal of physiology.

[42]  M. Tsai,et al.  Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. , 2007, Genes & development.