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Lymphatic Vessels and Their Surroundings: How Local Physical Factors Affect Lymph Flow

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Lymphatic Vessels and Their Surroundings: How Local Physical Factors Affect Lymph Flow biology Review Lymphatic Vessels and Their Surroundings: How Local Physical Factors Affect Lymph Flow Eleonora Solari y , Cristiana Marcozzi y , Daniela Negrini and Andrea Moriondo * Department of Medicine and Surgery, University of Insubria, I-21100 Varese, Italy; [email protected] (E.S.); [email protected] (C.M.); [email protected] (D.N.) * Correspondence: [email protected] Both authors have equally contributed. y Received: 7 November 2020; Accepted: 9 December 2020; Published: 11 December 2020 Simple Summary: Lymphatic vessels are responsible for the drainage of liquids, solutes, and cells from interstitial spaces and serosal cavities. Their task is fundamental in order to avoid fluid accumulation leading to tissue swelling and edema. The lymphatic system does not possess a central pump, instead lymph is propelled against an overall hydraulic pressure gradient from interstitial spaces to central veins thanks to two pumping mechanisms, which rely on extrinsic forces or the intrinsic rhythmic contractility of lymphatic muscle cells embedded in vessel walls. This latter mechanism can very rapidly adapt to subtle changes in the microenvironment due to hydraulic pressure, lymph flow-induced wall shear stress, liquid osmolarity, and local tissue temperature. Thus, endothelial and lymphatic muscle cells possess mechanosensors that sense these stimuli and promote a change in contraction frequency and amplitude to modulate lymph flow accordingly. In this review, we will focus on the known physical parameters that can modulate lymph flow and on their putative cellular and molecular mechanisms of transduction. Abstract: Lymphatic vessels drain and propel lymph by exploiting external forces that surrounding tissues exert upon vessel walls (extrinsic mechanism) and by using active, rhythmic contractions of lymphatic muscle cells embedded in the vessel wall of collecting lymphatics (intrinsic mechanism). The latter mechanism is the major source of the hydraulic pressure gradient where scant extrinsic forces are generated in the microenvironment surrounding lymphatic vessels. It is mainly involved in generating pressure gradients between the interstitial spaces and the vessel lumen and between adjacent lymphatic vessels segments. Intrinsic pumping can very rapidly adapt to ambient physical stimuli such as hydraulic pressure, lymph flow-derived shear stress, fluid osmolarity, and temperature. This adaptation induces a variable lymph flow, which can precisely follow the local tissue state in terms of fluid and solutes removal. Several cellular systems are known to be sensitive to osmolarity, temperature, stretch, and shear stress, and some of them have been found either in lymphatic endothelial cells or lymphatic muscle. In this review, we will focus on how known physical stimuli affect intrinsic contractility and thus lymph flow and describe the most likely cellular mechanisms that mediate this phenomenon. Keywords: lymphatic vessels; intrinsic contractility; extrinsic mechanism; hydraulic pressure; shear stress; lymph flow; osmolarity; tissue temperature 1. Introduction The lymphatic system drains fluid, macromolecules, and cells from the surrounding interstitium and from serosal cavities, thus contributing to tissue homeostasis and fluid balance [1,2]. Lymph Biology 2020, 9, 463; doi:10.3390/biology9120463 www.mdpi.com/journal/biology Biology 2020, 9, 463 2 of 15 Biology 2020, 9, x FOR PEER REVIEW 2 of 15 entersenters blind-endedblind-ended lymphaticlymphatic capillariescapillaries byby meansmeans ofof overlappingoverlapping endothelialendothelial cellscells formingforming primaryprimary unidirectionalunidirectional valves [3–5] [3–5] and and then then it itis ispropelled propelled afferently afferently through through collecting collecting vessels, vessels, lined lined with withmuscle muscle cells cellsin their in their walls walls and and with with intraluminal intraluminal unidirectional unidirectional valves valves [6] [6] delimitingdelimiting adjacentadjacent lymphangions,lymphangions, thethe lymphaticlymphatic functionalfunctional unitsunits (Figure(Figure1 )[1) 7[7,8].,8]. LymphLymph formationformation andand propulsionpropulsion dependdepend uponupon twotwo didifferentfferent mechanisms,mechanisms, namednamed “intrinsic“intrinsic andand extrinsic.”extrinsic.” TheyThey bothboth aaffectffect locallocal pressurepressure gradientsgradients betweenbetween interstitialinterstitial spacesspaces andand vesselvessel lumenlumen andand between adjacent lymphangions. TheThe intrinsicintrinsic mechanism,mechanism, predominantpredominant inin softsoft tissuestissues suchsuch asas thethe mesentery,mesentery, reliesrelies onon thethe lymphaticlymphatic musclemuscle (LM)(LM) netnet [[9–12]9–12] surroundingsurrounding thethe collectingcollecting vesselvessel wall.wall. Lymphatic musclemuscle cellscells spontaneouslyspontaneously contractcontract byby meansmeans ofof electricalelectrical commandscommands arisingarising inin pacemakerpacemaker cellscells withinwithin thethe lymphaticlymphatic musclemuscle layer,layer, duedue to to spontaneous spontaneous transient transient depolarizations depolarizations (STDs,(STDs, inducedinduced byby calcium-dependentcalcium-dependent chloridechloride currents)currents) oror I f-like-like currents currents mediated mediated by by HCN HCN channels channels such such as asit occurs it occurs in the in theheart heart [13–17]. [13– The17]. Theelectrical electrical signal signal then thenpropagates propagates to adjacent to adjacent LM cells LM cellsalong along the lymphatic the lymphatic network network through through GAP GAPjunctions junctions [18]. [Conversely,18]. Conversely, the extrinsic the extrinsic mechanism mechanism depends depends upon upon mechanical mechanical stresses stresses originating originating in insurrounding surrounding tissues tissues [19] [19 ]and and transmitted transmitted to to the the vessel vessel wall wall through fibrousfibrous extracellularextracellular matrixmatrix componentscomponents [[20–22].20–22]. ThisThis mechanismmechanism isis predominantpredominant inin lymphaticslymphatics locatedlocated inin tissuestissues undergoingundergoing significantsignificant cycliccyclic movements,movements, asas thethe heartheart oror skeletalskeletal muscularmuscular tissuetissue [[21],21], oror isis duedue toto cardiogeniccardiogenic oror respiratory-inducedrespiratory-induced displacementdisplacement [[23,24].23,24]. ArteriolarArteriolar vasomotionvasomotion [[25]25] andand externalexternal compressioncompression [[26]26] alsoalso aaffectffect lymphaticlymphatic function,function, eventuallyeventually inducinginducing rhythmicrhythmic vesselvessel compressioncompression andand expansionexpansion (Figure(Figure1 ).1). Figure 1. Functional scheme of how lymph is drained and propelled. Extrinsic forces and/or Figure 1. Functional scheme of how lymph is drained and propelled. Extrinsic forces and/or intrinsic intrinsic rhythmic contractions generate transmural pressure gradients (DPTM) across the wall of initial rhythmic contractions generate transmural pressure gradients (ΔPTM) across the wall of initial lymphatic capillaries and intraluminal pressure gradients (DPLymph) between adjacent lymphangions. lymphatic capillaries and intraluminal pressure gradients (ΔPLymph) between adjacent lymphangions. Intraluminal valve leaflets are devoid of LM. (Pin) interstitial hydraulic pressure; (PL) intraluminal hydraulicIntraluminal pressure; valve (leafletsEC) lymphatic are devoid endothelial of LM. cells;(Pin) interstitial (LM) lymphatic hydraulic muscle pressure; cells. (PL) intraluminal hydraulic pressure; (EC) lymphatic endothelial cells; (LM) lymphatic muscle cells. Extrinsic and intrinsic mechanisms may coexist in several areas of the body, and their relative importanceExtrinsic is variableand intrinsic since themechanisms sources of may extrinsic coexist pumping in several may areas vary of in the strength body, fromand their blood relative vessel vasomotionimportance causedis variable by thesince pulsatile the sources blood of flow extrinsic to external pumping forces may coming vary in from strength nearby from muscles, bloodwhich vessel contractvasomotion and caused relax, to by relatively the pulsatile small blood contributions flow to ex internal the mesentery. forces coming Thoracic from nearby cavity ismuscles, one region which of thecontract body and where relax, the to continuous relatively rhythmicsmall contributions activity of in the the heart mesentery. and respiration Thoracic gives cavity rise is toone a constantregion of interplaythe body ofwhere the two the lymphatic continuous pumping rhythmic mechanisms. activity of the In the heart rat and diaphragm, respiration both gives extrinsic rise andto a intrinsicconstant mechanismsinterplay of cooperatethe two lymphatic [27], as the extrinsicpumping rhythmic mechanisms. respiratory In the movements rat diaphragm, mainly both sustain extrinsic lymphatic and propulsionintrinsic mechanisms in the central cooperate tendon and[27], in as the the medial extrinsic muscular rhythmic region. respiratory In this movements regard, longitudinal mainly sustain rather thanlymphatic perpendicular propulsion lymphatic in the central orientation tendon [28] and with in respect the medial to muscle muscular fibers arrangementregion. In this results regard, in longitudinal rather than perpendicular lymphatic orientation [28] with respect to muscle fibers arrangement results in functional differences. On the contrary,
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