Transcellular Pathways in Lymphatic Endothelial Cells Regulate Changes in Solute Transport by Fluid Stress

Circulation Research

Volumn 120, Issue 9, 2017, Pages 1440-1452

  Triacca, Valentina ^a   Güç, Esra ^a   Kilarski, Witold W ^a,b   Pisano, Marco ^a   Swartz, Melody A ^a,b  

^a EPFL   (Switzerland)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Caveolin 1; Clathrin; Dextran; Endothelial cell; Lymphatic vessel

Indexed keywords

ALBUMIN; ALB PROTEIN, HUMAN; BOVINE SERUM ALBUMIN; SERUM ALBUMIN;

ANIMAL CELL; ARTICLE; CAVEOLA; CLATHRIN-COATED VESICLE; CONTROLLED STUDY; DENDRITIC CELL; ENDOTHELIUM CELL; FLUID FLOW; FLUID STRESS; IN VITRO STUDY; IN VIVO STUDY; INTERSTITIAL FLUID; LYMPH VESSEL ENDOTHELIUM; MECHANICAL STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SOLUTE; TRANSCYTOSIS; ANIMAL; BAGG ALBINO MOUSE; EXTRACELLULAR FLUID; FEMALE; FLUID SHIFT; HUMAN; INTRADERMAL DRUG ADMINISTRATION; MALE; METABOLISM; PERMEABILITY; SKIN; TIME FACTOR; ULTRASTRUCTURE;

ANIMALS; CAVEOLAE; CLATHRIN-COATED VESICLES; ENDOTHELIAL CELLS; ENDOTHELIUM, LYMPHATIC; EXTRACELLULAR FLUID; FEMALE; FLUID SHIFTS; HUMANS; INJECTIONS, INTRADERMAL; MALE; MICE, INBRED BALB C; PERMEABILITY; SERUM ALBUMIN; SERUM ALBUMIN, BOVINE; SKIN; STRESS, MECHANICAL; TIME FACTORS; TRANSCYTOSIS;

EID: 85019627827     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.309828     Document Type: Article

References (76)

1. Wiig H, Swartz MA. Interstitial fluid and lymph formation and transport: Physiological regulation and roles in inflammation and cancer. Physiol Rev. 2012;92:1005-1060. doi: 10.1152/physrev.00037.2011.
2. Huxley VH, Scallan J. Lymphatic fluid: Exchange mechanisms and regulation. J Physiol. 2011;589:2935-2943. doi: 10.1113/jphysiol.2011.208298.
3. Levick JR, Michel CC. Microvascular fluid exchange and the revised Starling principle. Cardiovasc Res. 2010;87:198-210. doi: 10.1093/cvr/cvq062.
4. Feng D, Nagy JA, Dvorak HF, Dvorak AM. Ultrastructural studies define soluble macromolecular, particulate, cellular transendothelial cell pathways in venules, lymphatic vessels, tumor-associated microvessels in man and animals. Microsc Res Tech. 2002;57:289-326. doi: 10.1002/jemt.10087.
5. Breslin JW. Mechanical forces and lymphatic transport. Microvasc Res. 2014;96:46-54. doi: 10.1016/j.mvr.2014.07.013.
6. Negrini D, Moriondo A. Lymphatic anatomy and biomechanics. J Physiol. 2011;589:2927-2934. doi: 10.1113/jphysiol.2011.206672.
7. Trzewik J, Mallipattu SK, Artmann GM, Delano FA, Schmid-Schönbein GW. Evidence for a second valve system in lymphatics: Endothelial microvalves. FASEB J. 2001;15:1711-1717.
8. Schmid-Schönbein GW. The second valve system in lymphatics. Lymphat Res Biol. 2003;1:25-29; discussion 29. doi: 10.1089/15396850360495664.
9. Patterson RM, Ballard CL, Wasserman K, Mayerson HS. Lymphatic permeability to albumin. Am J Physiol. 1958;194:120-124.
10. Reed RK, Rubin K. Transcapillary exchange: Role and importance of the interstitial fluid pressure and the extracellular matrix. Cardiovasc Res. 2010;87:211-217. doi: 10.1093/cvr/cvq143.
11. Renkin EM, Wiig H. Limits to steady-state lymph flow rates derived from plasma-to-tissue uptake measurements. Microvasc Res. 1994;47:318-328. doi: 10.1006/mvre.1994.1025.
12. Reed RK, Ishibashi M, Townsley MI, Parker JC, Taylor AE. Blood-totissue clearance vs. lymph analysis in determining capillary transport characteristics for albumin in skin. Am J Physiol. 1993;264:H1394-H1401.
13. Xie SL, Reed RK, Bowen BD, Bert JL. A model of human microvascular exchange. Microvasc Res. 1995;49:141-162. doi: 10.1006/mvre.1995.1012.
14. Dobbins WO 3rd, Rollins EL. Intestinal mucosal lymphatic permeability: An electron microscopic study of endothelial vesicles and cell junctions. J Ultrastruct Res. 1970;33:29-59.
15. Predescu D, Vogel SM, Malik AB. Functional and morphological studies of protein transcytosis in continuous endothelia. Am J Physiol Lung Cell Mol Physiol. 2004;287:L895-L901. doi: 10.1152/ajplung.00075.2004.
16. Michel CC, Curry FE. Microvascular permeability. Physiol Rev. 1999;79:703-761.
17. Samuel SP, Jain N, O'Dowd F, Paul T, Kashanin D, Gerard VA, Gun'ko YK, Prina-Mello A, Volkov Y. Multifactorial determinants that govern nanoparticle uptake by human endothelial cells under flow. Int J Nanomedicine. 2012;7:2943-2956. doi: 10.2147/IJN.S30624.
18. Rizzo V, Morton C, DePaola N, Schnitzer JE, Davies PF. Recruitment of endothelial caveolae into mechanotransduction pathways by flow conditioning in vitro. Am J Physiol Heart Circ Physiol. 2003;285:H1720-H1729. doi: 10.1152/ajpheart.00344.2002.
19. Hu G, Minshall RD. Regulation of transendothelial permeability by Src kinase. Microvasc Res. 2009;77:21-25. doi: 10.1016/j.mvr.2008.10.002.
20. Vestweber D, Wessel F, Nottebaum AF. Similarities and differences in the regulation of leukocyte extravasation and vascular permeability. Semin Immunopathol. 2014;36:177-192. doi: 10.1007/s00281-014-0419-7.
21. Schulte D, Küppers V, Dartsch N, Broermann A, Li H, Zarbock A, Kamenyeva O, Kiefer F, Khandoga A, Massberg S, Vestweber D. Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO J. 2011;30:4157-4170. doi: 10.1038/emboj.2011.304.
22. Childs EW, Udobi KF, Hunter FA, Dhevan V. Evidence of transcellular albumin transport after hemorrhagic shock. Shock. 2005;23:565-570.
23. Chen J, Braet F, Brodsky S, Weinstein T, Romanov V, Noiri E, Goligorsky MS. VEGF-induced mobilization of caveolae and increase in permeability of endothelial cells. Am J Physiol Cell Physiol. 2002;282:C1053-C1063. doi: 10.1152/ajpcell.00292.2001.
24. Zgraggen S, Ochsenbein AM, Detmar M. An important role of blood and lymphatic vessels in inflammation and allergy. J Allergy (Cairo). 2013;2013:672381. doi: 10.1155/2013/672381.
25. Miteva DO, Rutkowski JM, Dixon JB, Kilarski W, Shields JD, Swartz MA. Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ Res. 2010;106:920-931. doi: 10.1161/CIRCRESAHA.109.207274.
26. Bates DO, Hillman NJ, Williams B, Neal CR, Pocock TM. Regulation of microvascular permeability by vascular endothelial growth factors. J Anat. 2002;200:581-597.
27. Brand CU, Hunziker T, Braathen LR. Isolation of human skin-derived lymph: Flow and output of cells following sodium lauryl sulphate-induced contact dermatitis. Arch Dermatol Res. 1992;284:123-126.
28. He C, Young AJ, West CA, Su M, Konerding MA, Mentzer SJ. Stimulation of regional lymphatic and blood flow by epicutaneous oxazolone. J Appl Physiol (1985). 2002;93:966-973. doi: 10.1152/japplphysiol.00212.2002.
29. Mullins RJ, Hudgens RW. Increased skin lymph protein clearance after a 6-h arterial bradykinin infusion. Am J Physiol. 1987;253:H1462-H1469.
30. Cromer WE, Zawieja SD, Tharakan B, Childs EW, Newell MK, Zawieja DC. The effects of inflammatory cytokines on lymphatic endothelial barrier function. Angiogenesis. 2014;17:395-406. doi: 10.1007/s10456-013-9393-2.
31. Kawai Y, Kaidoh M, Yokoyama Y, Ohhashi T. Pivotal roles of lymphatic endothelial cell layers in the permeability to hydrophilic substances through collecting lymph vessel walls: Effects of inflammatory cytokines. Lymphat Res Biol. 2014;12:124-135. doi: 10.1089/lrb.2014.0002.
32. Schnitzer JE, Oh P, Pinney E, Allard J. Filipin-sensitive caveolae-mediated transport in endothelium: Reduced transcytosis, scavenger endocytosis, capillary permeability of select macromolecules. J Cell Biol. 1994;127:1217-1232.
33. Wagner RC, Chen SC. Transcapillary transport of solute by the endothelial vesicular system: Evidence from thin serial section analysis. Microvasc Res. 1991;42:139-150.
34. Lim HY, Thiam CH, Yeo KP, Bisoendial R, Hii CS, McGrath KC, Tan KW, Heather A, Alexander JS, Angeli V. Lymphatic vessels are essential for the removal of cholesterol from peripheral tissues by SR-BImediated transport of HDL. Cell Metab. 2013;17:671-684. doi: 10.1016/j. cmet.2013.04.002.
35. Reed AL, Rowson SA, Dixon JB. Demonstration of ATP-dependent, transcellular transport of lipid across the lymphatic endothelium using an in vitro model of the lacteal. Pharm Res. 2013;30:3271-3280. doi: 10.1007/s11095-013-1218-x.
36. Dixon JB, Raghunathan S, Swartz MA. A tissue-engineered model of the intestinal lacteal for evaluating lipid transport by lymphatics. Biotechnol Bioeng. 2009;103:1224-1235. doi: 10.1002/bit.22337.
37. Dunworth WP, Fritz-Six KL, Caron KM. Adrenomedullin stabilizes the lymphatic endothelial barrier in vitro and in vivo. Peptides. 2008;29:2243-2249. doi: 10.1016/j.peptides.2008.09.009.
38. Lund AW, Duraes FV, Hirosue S, Raghavan VR, Nembrini C, Thomas SN, Issa A, Hugues S, Swartz MA. VEGF-C promotes immune tolerance in B16 melanomas and cross-presentation of tumor antigen by lymph node lymphatics. Cell Rep. 2012;1:191-199. doi: 10.1016/j.celrep.2012.01.005.
39. Hirosue S, Vokali E, Raghavan VR, Rincon-Restrepo M, Lund AW, Corthésy-Henrioud P, Capotosti F, Halin Winter C, Hugues S, Swartz MA. Steady-state antigen scavenging, cross-presentation, CD8+ T cell priming: A new role for lymphatic endothelial cells. J Immunol. 2014;192:5002-5011. doi: 10.4049/jimmunol.1302492.
40. Dubrot J, Duraes FV, Potin L, Capotosti F, Brighouse D, Suter T, LeibundGut-Landmann S, Garbi N, Reith W, Swartz MA, Hugues S. Lymph node stromal cells acquire peptide-MHCII complexes from dendritic cells and induce antigen-specific CD4? T cell tolerance. J Exp Med. 2014;211:1153-1166. doi: 10.1084/jem.20132000.
41. Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles. 2014;3. doi: 10.3402/jev.v3.24641.
42. Simionescu M, Popov D, Sima A. Endothelial transcytosis in health and disease. Cell Tissue Res. 2009;335:27-40. doi: 10.1007/s00441-008-0688-3.
43. Li HH, Li J, Wasserloos KJ, Wallace C, Sullivan MG, Bauer PM, Stolz DB, Lee JS, Watkins SC, St Croix CM, Pitt BR, Zhang LM. Caveolaedependent and-independent uptake of albumin in cultured rodent pulmonary endothelial cells. PLoS One. 2013;8:e81903. doi: 10.1371/journal. pone.0081903.
44. Azizi PM, Zyla RE, Guan S, Wang C, Liu J, Bolz SS, Heit B, Klip A, Lee WL. Clathrin-dependent entry and vesicle-mediated exocytosis define insulin transcytosis across microvascular endothelial cells. Mol Biol Cell. 2015;26:740-750. doi: 10.1091/mbc.E14-08-1307.
45. Bright NA, Gratian MJ, Luzio JP. Endocytic delivery to lysosomes mediated by concurrent fusion and kissing events in living cells. Curr Biol. 2005;15:360-365. doi: 10.1016/j.cub.2005.01.049.
46. Pryor PR, Mullock BM, Bright NA, Lindsay MR, Gray SR, Richardson SC, Stewart A, James DE, Piper RC, Luzio JP. Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events. EMBO Rep. 2004;5:590-595. doi: 10.1038/sj.embor.7400150.
47. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem. 2001;70:535-602. doi: 10.1146/annurev.biochem.70.1.535.
48. Derby MC, Gleeson PA. New insights into membrane trafficking and protein sorting. Int Rev Cytol. 2007;261:47-116. doi: 10.1016/S0074-7696(07)61002-X.
49. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell. 2006;10:839-850. doi: 10.1016/j.devcel.2006.04.002.
50. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol. 2007;8:603-612. doi: 10.1038/nrm2216.
51. Gharbi SI, Zvelebil MJ, Shuttleworth SJ, Hancox T, Saghir N, Timms JF, Waterfield MD. Exploring the specificity of the PI3K family inhibitor LY294002. Biochem J. 2007;404:15-21. doi: 10.1042/BJ20061489.
52. Araki N, Johnson MT, Swanson JA. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol. 1996;135:1249-1260.
53. Breitfeld PP, McKinnon WC, Mostov KE. Effect of nocodazole on vesicular traffic to the apical and basolateral surfaces of polarized MDCK cells. J Cell Biol. 1990;111:2365-2373.
54. Schmid-Schönbein GW. Microlymphatics and lymph flow. Physiol Rev. 1990;70:987-1028.
55. Ikomi F, Hanna GK, Schmid-Schönbein GW. Mechanism of colloidal particle uptake into the lymphatic system: Basic study with percutaneous lymphography. Radiology. 1995;196:107-113. doi: 10.1148/radiology.196.1.7784553.
56. Ikomi F, Schmid-Schönbein GW. Lymph transport in the skin. Clin Dermatol. 1995;13:419-427.
57. Bazigou E, Wilson JT, Moore JE Jr. Primary and secondary lymphatic valve development: Molecular, functional and mechanical insights. Microvasc Res. 2014;96:38-45. doi: 10.1016/j.mvr.2014.07.008.
58. Murfee WL, Rappleye JW, Ceballos M, Schmid-Schönbein GW. Discontinuous expression of endothelial cell adhesion molecules along initial lymphatic vessels in mesentery: The primary valve structure. Lymphat Res Biol. 2007;5:81-89. doi: 10.1089/lrb.2007.1005.
59. Baluk P, Fuxe J, Hashizume H, Romano T, Lashnits E, Butz S, Vestweber D, Corada M, Molendini C, Dejana E, McDonald DM. Functionally specialized junctions between endothelial cells of lymphatic vessels. J Exp Med. 2007;204:2349-2362. doi: 10.1084/jem.20062596.
60. Dejana E, Orsenigo F, Molendini C, Baluk P, McDonald DM. Organization and signaling of endothelial cell-to-cell junctions in various regions of the blood and lymphatic vascular trees. Cell Tissue Res. 2009;335:17-25. doi: 10.1007/s00441-008-0694-5.
61. Hu G, Place AT, Minshall RD. Regulation of endothelial permeability by Src kinase signaling: Vascular leakage versus transcellular transport of drugs and macromolecules. Chem Biol Interact. 2008;171:177-189. doi: 10.1016/j.cbi.2007.08.006.
62. Yang VV, O'Morchoe PJ, O'Morchoe CC. Transport of protein across lymphatic endothelium in the rat kidney. Microvasc Res. 1981;21:75-91.
63. Albertine KH, O'Morchoe CC. Renal lymphatic ultrastructure and translymphatic transport. Microvasc Res. 1980;19:338-351.
64. Smith KR, Borchardt RT. Permeability and mechanism of albumin, cationized albumin, glycosylated albumin transcellular transport across monolayers of cultured bovine brain capillary endothelial cells. Pharm Res. 1989;6:466-473.
65. Davis MJ, Hill MA, Kuo L. Local regulation of microvascular perfusion. In: Tuma RF, Duran WN, Ley K, eds. Handbook of Physiology. Amsterdam: Elsevier; 2008:161-284.
66. Moriondo A, Mukenge S, Negrini D. Transmural pressure in rat initial subpleural lymphatics during spontaneous or mechanical ventilation. Am J Physiol Heart Circ Physiol. 2005;289:H263-H269. doi: 10.1152/ajpheart.00060.2005.
67. Negrini D, Moriondo A, Mukenge S. Transmural pressure during cardiogenic oscillations in rodent diaphragmatic lymphatic vessels. Lymphat Res Biol. 2004;2:69-81. doi: 10.1089/lrb.2004.2.69.
68. Adamson RH, Lenz JF, Zhang X, Adamson GN, Weinbaum S, Curry FE. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J Physiol. 2004;557:889-907. doi: 10.1113/jphysiol.2003.058255.
69. St Amant EV, Tauseef M, Vogel SM, Gao XP, Mehta D, Komarova YA, Malik AB. Pkc alpha activation of p120-catenin serine 879 phospho-switch disassembles VE-cadherin junctions and disrupts vascular integrity. Circ Res. 2012;111:739-749. doi: 10.1161/CIRCRESAHA.112.269654.
70. Armstrong SM, Khajoee V, Wang C, Wang T, Tigdi J, Yin J, Kuebler WM, Gillrie M, Davis SP, Ho M, Lee WL. Co-regulation of transcellular and paracellular leak across microvascular endothelium by dynamin and Rac. Am J Pathol. 2012;180:1308-1323. doi: 10.1016/j.ajpath.2011.12.002.
71. Xiao K, Garner J, Buckley KM, Vincent PA, Chiasson CM, Dejana E, Faundez V, Kowalczyk AP. p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin. Mol Biol Cell. 2005;16:5141-5151. doi: 10.1091/mbc.E05-05-0440.
72. Orsenigo F, Giampietro C, Ferrari A, et al. Phosphorylation of VEcadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat Commun. 2012;3:1208. doi: 10.1038/ncomms2199.
73. Breslin JW, Kurtz KM. Lymphatic endothelial cells adapt their barrier function in response to changes in shear stress. Lymphat Res Biol. 2009;7:229-237. doi: 10.1089/lrb.2009.0015.
74. Lynch PM, Delano FA, Schmid-Schönbein GW. The primary valves in the initial lymphatics during inflammation. Lymphat Res Biol. 2007;5:3-10. doi: 10.1089/lrb.2007.5102.
75. Chaitanya GV, Franks SE, Cromer W, Wells SR, Bienkowska M, Jennings MH, Ruddell A, Ando T, Wang Y, Gu Y, Sapp M, Mathis JM, Jordan PA, Minagar A, Alexander JS. Differential cytokine responses in human and mouse lymphatic endothelial cells to cytokines in vitro. Lymphat Res Biol. 2010;8:155-164. doi: 10.1089/lrb.2010.0004.
76. Kakei Y, Akashi M, Shigeta T, Hasegawa T, Komori T. Alteration of cellcell junctions in cultured human lymphatic endothelial cells with inflammatory cytokine stimulation. Lymphat Res Biol. 2014;12:136-143. doi: 10.1089/lrb.2013.0035.