High-salt diet causes expansion of the lymphatic network and increased lymph flow in skin and muscle of rats

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 38, Issue 9, 2018, Pages 2054-2064

  Karlsen, Tine V ^g   Nikpey, Elham ^a,g   Han, Jianhua ^g   Reikvam, Tore ^g   Rakova, Natalia ^b   Castorena Gonzalez, Jorge A ^c   Davis, Michael J ^c   Titze, Jens M ^d,e,f   Tenstad, Olav ^g   Wiig, Helge ^g  

^a HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c University of Missouri   (United States)

^d UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^e VANDERBILT UNIVERSITY   (United States)

^f DUKE NUS MEDICAL SCHOOL   (Singapore)

^g UNIVERSITY OF BERGEN   (Norway)

Author keywords

Blood pressure; Body water; Extracellular fluid; Extracellular matrix; Hypertension

Indexed keywords

CLODRONIC ACID; SODIUM CHLORIDE; SODIUM ION; VASCULOTROPIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE REGULATION; CAPILLARY; FEMALE; HIGH SALT DIET; HYPERTENSION; LYMPH FLOW; LYMPH VESSEL; LYMPHANGIOGENESIS; MACROPHAGE; MALE; MONOCYTE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY-COMPUTED TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; SKELETAL MUSCLE; TISSUE WATER; WATER RETENTION; ANIMAL; C57BL MOUSE; DIAGNOSTIC IMAGING; DRUG EFFECT; ELECTROLYTE BALANCE; LYMPH; METABOLISM; MONONUCLEAR PHAGOCYTE; SALT INTAKE; SKIN; SPRAGUE DAWLEY RAT;

ANIMALS; CLODRONIC ACID; LYMPH; LYMPHANGIOGENESIS; MALE; MICE, INBRED C57BL; MONONUCLEAR PHAGOCYTE SYSTEM; MUSCLE, SKELETAL; POSITRON EMISSION TOMOGRAPHY COMPUTED TOMOGRAPHY; RATS, SPRAGUE-DAWLEY; SKIN; SODIUM CHLORIDE, DIETARY; VASCULAR ENDOTHELIAL GROWTH FACTOR C; WATER-ELECTROLYTE BALANCE;

EID: 85055597102     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.118.311149     Document Type: Article

References (29)

1. Guyton AC, Coleman TG, Cowley AW, Manning RD, Norman RA, Ferguson JD. A systems analysis approach to understanding long-range arterial blood pressure control and hypertension. Circ Res. 1974;35:159-176.
2. Heer M, Baisch F, Kropp J, Gerzer R, Drummer C. High dietary sodium chloride consumption may not induce body fluid retention in humans. Am J Physiol Renal Physiol. 2000;278:F585-F595. doi: 10.1152/ajprenal.2000.278.4.F585
3. Palacios C, Wigertz K, Martin BR, Jackman L, Pratt JH, Peacock M, McCabe G, Weaver CM. Sodium retention in black and white female adolescents in response to salt intake. J Clin Endocrinol Metab. 2004;89:1858-1863. doi: 10.1210/jc.2003-031446
4. Titze J, Maillet A, Lang R, Gunga HC, Johannes B, Gauquelin-Koch G, Kihm E, Larina I, Gharib C, Kirsch KA. Long-term sodium balance in humans in a terrestrial space station simulation study. Am J Kidney Dis. 2002;40:508-516. doi: 10.1053/ajkd.2002.34908
5. Rakova N, Jüttner K, Dahlmann A, et al. Long-term space flight simulation reveals infradian rhythmicity in human Na(+) balance. Cell Metab. 2013;17:125-131. doi: 10.1016/j.cmet.2012.11.013
6. Titze J, Lang R, Ilies C, Schwind KH, Kirsch KA, Dietsch P, Luft FC, Hilgers KF. Osmotically inactive skin Na+ storage in rats. Am J Physiol Renal Physiol. 2003;285:F1108-F1117. doi: 10.1152/ajprenal.00200.2003
7. Machnik A, Dahlmann A, Kopp C, Goss J, Wagner H, van Rooijen N, Eckardt KU, Müller DN, Park JK, Luft FC, Kerjaschki D, Titze J. Mononuclear phagocyte system depletion blocks interstitial tonicity-responsive enhancer binding protein/vascular endothelial growth factor C expression and induces salt-sensitive hypertension in rats. Hypertension. 2010;55:755-761. doi: 10.1161/HYPERTENSIONAHA.109.143339
8. Schafflhuber M, Volpi N, Dahlmann A, Hilgers KF, Maccari F, Dietsch P, Wagner H, Luft FC, Eckardt KU, Titze J. Mobilization of osmotically inactive Na+ by growth and by dietary salt restriction in rats. Am J Physiol Renal Physiol. 2007;292:F1490-F1500. doi: 10.1152/ajprenal.00300.2006
9. Titze J, Krause H, Hecht H, Dietsch P, Rittweger J, Lang R, Kirsch KA, Hilgers KF. Reduced osmotically inactive Na storage capacity and hypertension in the Dahl model. Am J Physiol Renal Physiol. 2002;283:F134-F141. doi: 10.1152/ajprenal.00323.2001
10. Titze J, Luft FC, Bauer K, Dietsch P, Lang R, Veelken R, Wagner H, Eckardt KU, Hilgers KF. Extrarenal Na+ balance, volume, and blood pressure homeostasis in intact and ovariectomized deoxycorticosterone-acetate salt rats. Hypertension. 2006;47:1101-1107. doi: 10.1161/01.HYP.0000221039.17735.1a
11. Wiig H, Schröder A, Neuhofer W, et al. Immune cells control skin lymphatic electrolyte homeostasis and blood pressure. J Clin Invest. 2013;123:2803-2815. doi: 10.1172/JCI60113
12. Machnik A, Neuhofer W, Jantsch J, et al. Macrophages regulate salt-dependent volume and blood pressure by a vascular endothelial growth factor-C-dependent buffering mechanism. Nat Med. 2009;15:545-552. doi: 10.1038/nm.1960
13. Karlsen TV, McCormack E, Mujic M, Tenstad O, Wiig H. Minimally invasive quantification of lymph flow in mice and rats by imaging depot clearance of near-infrared albumin. Am J Physiol Heart Circ Physiol. 2012;302:H391-H401. doi: 10.1152/ajpheart.00842.2011
14. Kopp C, Linz P, Dahlmann A, Hammon M, Jantsch J, Müller DN, Schmieder RE, Cavallaro A, Eckardt KU, Uder M, Luft FC, Titze J. 23Na magnetic resonance imaging-determined tissue sodium in healthy subjects and hypertensive patients. Hypertension. 2013;61:635-640. doi: 10.1161/HYPERTENSIONAHA.111.00566
15. Wiig H, Tenstad O, Bert JL. Effect of hydration on interstitial distribution of charged albumin in rat dermis in vitro. J Physiol. 2005;569(pt 2):631-641. doi: 10.1113/jphysiol.2005.096792
16. Karlsen TV, Reikvam T, Tofteberg A, Nikpey E, Skogstrand T, Wagner M, Tenstad O, Wiig H. Lymphangiogenesis facilitates initial lymph formation and enhances the dendritic cell mobilizing chemokine CCL21 without affecting migration. Arterioscler Thromb Vasc Biol. 2017;37:2128-2135. doi: 10.1161/ATVBAHA.117.309883
17. Scallan JP, Davis MJ. Genetic removal of basal nitric oxide enhances contractile activity in isolated murine collecting lymphatic vessels. J Physiol. 2013;591:2139-2156. doi: 10.1113/jphysiol.2012.250662
18. Scallan JP, Wolpers JH, Davis MJ. Constriction of isolated collecting lymphatic vessels in response to acute increases in downstream pressure. J Physiol. 2013;591:443-459. doi: 10.1113/jphysiol.2012.237909
19. Gashev AA, Davis MJ, Zawieja DC. Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct. J Physiol. 2002;540(pt 3):1023-1037.
20. Nikpey E, Karlsen TV, Rakova N, Titze JM, Tenstad O, Wiig H. High-salt diet causes osmotic gradients and hyperosmolality in skin without affecting interstitial fluid and lymph. Hypertension. 2017;69:660-668. doi: 10.1161/HYPERTENSIONAHA.116.08539
21. Weissleder R, Pittet MJ. Imaging in the era of molecular oncology. Nature. 2008;452:580-589. doi: 10.1038/nature06917
22. Mumprecht V, Honer M, Vigl B, Proulx ST, Trachsel E, Kaspar M, Banziger-Tobler NE, Schibli R, Neri D, Detmar M. In vivo imaging of inflammation- and tumor-induced lymph node lymphangiogenesis by immuno-positron emission tomography. Cancer Res. 2010;70:8842-8851. doi: 10.1158/0008-5472.CAN-10-0896
23. Kwon S, Agollah GD, Chan W, Sevick-Muraca EM. Altered lymphatic function and architecture in salt-induced hypertension assessed by near-infrared fluorescence imaging. J Biomed Opt. 2012;17:080504-080501. doi: 10.1117/1.JBO.17.8.080504
24. Zawieja SD, Castorena-Gonzalez JA, Scallan JP, Davis MJ. Differences in L-type Ca2+ channel activity partially underlie the regional dichotomy in pumping behavior by murine peripheral and visceral lymphatic vessels. Am J Physiol Heart Circ Physiol. 2018;314:H991-H1010. doi: 10.1152/ajpheart.00499.2017
25. Breslin JW, Gaudreault N, Watson KD, Reynoso R, Yuan SY, Wu MH. Vascular endothelial growth factor-C stimulates the lymphatic pump by a VEGF receptor-3-dependent mechanism. Am J Physiol Heart Circ Physiol. 2007;293:H709-H718. doi: 10.1152/ajpheart.00102.2007
26. Randolph GJ, Ivanov S, Zinselmeyer BH, Scallan JP. The lymphatic system: integral roles in immunity. Annu Rev Immunol. 2017;35:31-52. doi: 10.1146/annurev-immunol-041015-055354
27. Lankhorst S, Severs D, Markó L, Rakova N, Titze J, Müller DN, Danser AH, van den Meiracker AH. Salt sensitivity of angiogenesis inhibition-induced blood pressure rise: role of interstitial sodium accumulation? Hypertension. 2017;69:919-926. doi: 10.1161/HYPERTENSIONAHA.116.08565
28. Dahlmann A, Dörfelt K, Eicher F, et al. Magnetic resonance-determined sodium removal from tissue stores in hemodialysis patients. Kidney Int. 2015;87:434-441. doi: 10.1038/ki.2014.269
29. Kleinewietfeld M, Manzel A, Titze J, Kvakan H, Yosef N, Linker RA, Muller DN, Hafler DA. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature. 2013;496:518-522. doi: 10.1038/nature11868