Response of lymphatic endothelial cells to combined spatial and temporal variations in fluid flow.
Ca2+ dynamics
FOXC2
NFATc1
PROX1
fluid shear stress
lymphatic endothelial cell
lymphatic valve maintenance
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
12 2023
12 2023
Historique:
revised:
02
09
2023
received:
29
08
2019
accepted:
22
09
2023
medline:
31
10
2023
pubmed:
30
10
2023
entrez:
30
10
2023
Statut:
ppublish
Résumé
One-way valves within lymphatic vessels are required for the efficient drainage of lymphatic fluids. Fluid flow is proposed to be a key cue in regulating both the formation and maintenance of lymphatic valves. However, to our knowledge, no previous study has systematically examined the response of LECs to the complex combination of spatially and temporally varying fluid flows that occur at lymphatic valves in vivo. We built an in vitro microfluidic device that reproduces key aspects of the flow environment found at lymphatic valves. Using this device, we found that a combination of spatially and temporally varying wall shear stresses (WSSs) led to upregulated transcription of PROX1 and FOXC2. In addition, we observed that combined spatial and temporal variations in WSS-modulated Ca
Identifiants
pubmed: 37902497
doi: 10.1096/fj.201902205RRRR
doi:
Substances chimiques
Transcription Factors
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23240Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM130332
Pays : United States
Informations de copyright
© 2023 Federation of American Societies for Experimental Biology.
Références
Rockson SG. Lymphedema. Am J Med. 2001;110:288-295.
Rockson SG. Diagnosis and management of lymphatic vascular disease. J Am Coll Cardiol. 2008;52:799-806.
Nakano T, Nakashima Y, Yonemitsu Y, et al. Angiogenesis and lymphangiogenesis and expression of lymphangiogenic factors in the atherosclerotic intima of human coronary arteries. Hum Pathol. 2005;36:330-340.
Alitalo K. The lymphatic vasculature in disease. Nat Med. 2011;17:1371-1380.
Planas-Paz L, Lammert E. Mechanical forces in lymphatic vascular development and disease. Cell Mol Life Sci C. 2013;70:4341-4354.
Bazigou E, Makinen T. Flow control in our vessels: vascular valves make sure there is no way back. Cell Mol Life Sci. 2013;70:1055-1066.
Bazigou E, Xie S, Chen C, et al. Integrin-α9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis. Dev Cell. 2009;17:175-186.
Danussi C, del Bel Belluz L, Pivetta E, et al. EMILIN1/α9β1 integrin interaction is crucial in lymphatic valve formation and maintenance. Mol Cell Biol. 2013;33:4381-4394.
Choi D, Park E, Jung E, et al. Piezo1 incorporates mechanical force signals into the genetic program that governs lymphatic valve development and maintenance. JCI Insight. 2019;4:1-15.
Lapinski PE, Kwon S, Lubeck BA, et al. RASA1 maintains the lymphatic vasculature in a quiescent functional state in mice. J Clin Invest. 2012;122:733-747.
Norrmén C, Ivanov KI, Cheng J, et al. FOXC2 controls formation and maturation of lymphatic collecting vessels through cooperation with NFATc1. J Cell Biol. 2009;185:439-457.
Vittet D. Lymphatic collecting vessel maturation and valve morphogenesis. Microvasc Res. 2014;96:31-37.
Sabine A, Petrova TV. Interplay of mechanotransduction, FOXC2, connexins, and calcineurin signaling in lymphatic valve formation. In: Kiefer F, Schulte-Merker S, eds. Developmental Aspects of the Lymphatic Vascular System. Advances in Anatomy, Embryology and Cell Biology. Springer; 2014:67-80.
Sabine A, Agalarov Y, Maby-el Hajjami H, et al. Mechanotransduction, PROX1, and FOXC2 cooperate to control connexin37 and calcineurin during lymphatic-valve formation. Dev Cell. 2012;22:430-445.
Sweet DT, Jiménez JM, Chang J, et al. Lymph flow regulates collecting lymphatic vessel maturation in vivo. J Clin Invest. 2015;125:2995-3007.
Dixon JB, Greiner ST, Gashev AA, Cote GL, Moore JE Jr, Zawieja DC. Lymph flow, shear stress, and lymphocyte velocity in rat mesenteric prenodal lymphatics. Microcirculation. 2006;13:597-610.
Rahbar E, Akl T, Coté GL, Moore JE Jr, Zawieja DC. Lymph transport in rat mesenteric lymphatics experiencing edemagenic stress. Microcirculation. 2014;21:359-367.
Choi D, Park E, Jung E, et al. Laminar flow downregulates Notch activity to promote lymphatic sprouting. J Clin Invest. 2017;127:1225-1240.
Choi D, Park E, Jung E, et al. ORAI1 activates proliferation of lymphatic endothelial cells in response to laminar flow through Krüppel-like factors 2 and 4. Circ Res. 2017;120:1426-1439.
Clapham DE. Calcium signaling. Cell. 2007;131:1047-1058.
Nonomura K, Lukacs V, Sweet DT, et al. Mechanically activated ion channel PIEZO1 is required for lymphatic valve formation. Proc Natl Acad Sci. 2018;115:12817-12822.
Ranade SS, Qiu Z, Woo SH, et al. Piezo1, a mechanically activated ion channel, is required for vascular development in mice. Proc Natl Acad Sci. 2014;111:10347-10352.
Shin Y, Han S, Jeon JS, et al. Microfluidic assay for simultaneous culture of multiple cell types on surfaces or within hydrogels. Nat Protoc. 2012;7:1247-1259.
Vickerman V, Blundo J, Chung S, Kamm R. Design, fabrication and implementation of a novel multi-parameter control microfluidic platform for three-dimensional cell culture and real-time imaging. Lab Chip. 2008;8:1468-1477.
Sudo R, Chung S, Zervantonakis IK, et al. Transport-mediated angiogenesis in 3D epithelial coculture. FASEB J. 2009;23:2155-2164.
Michalaki E, Surya VN, Fuller GG, Dunn AR. Perpendicular alignment of lymphatic endothelial cells in response to spatial gradients in wall shear stress. Commun Biol. 2020;3:1-9.
Surya VN, Michalaki E, Fuller GG, Dunn AR. Lymphatic endothelial cell calcium pulses are sensitive to spatial gradients in wall shear stress. Mol Biol Cell. 2019;30:923-931.
Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature. 1997;386:855-858.
Smedler E, Uhlén P. Frequency decoding of calcium oscillations. Biochim Biophys Acta. 2014;1840:964-969.
Yissachar N, Sharar Fischler T, Cohen AA, et al. Dynamic response diversity of NFAT isoforms in individual living cells. Mol Cell. 2013;49:322-330.
Zhao M, Joy J, Zhou W, et al. Transcriptional outcomes and kinetic patterning of gene expression in response to NF-κB activation. PLoS Biol. 2018;16:e2006347.
Telinius N, Drewsen N, Pilegaard H, et al. Human thoracic duct in vitro: diameter-tension properties, spontaneous and evoked contractile activity. Am J Physiol Hear Circ Physiol. 2010;299:811-818.
Kornuta JA, Nipper ME, Dixon JB. Low-cost microcontroller platform for studying lymphatic biomechanics in vitro. J Biomech. 2013;46:183-186.
Kornuta JA, Nepiyushchikh Z, Gasheva OY, Mukherjee A, Zawieja DC, Dixon JB. Effects of dynamic shear and transmural pressure on wall shear stress sensitivity in collecting lymphatic vessels. Am J Physiol Regul Integr Comp Physiol. 2015;309:1122-1134.
Bray M-A, Vokes MS, Carpenter AE. Using CellProfiler for automatic identification and measurement of biological objects in images. Curr Protoc Mol Biol. 2015;109:14.17.1-14.17.13.
Khan RA. A note on estimating the mean of a normal distribution with known coefficient of variation. J Am Stat Assoc. 1968;63:1039-1041.
Olsson U. Confidence intervals for the mean of a log-normal distribution. J Stat Educ. 2005;13:1-9.
Zawieja DC. Contractile physiology of lymphatics the lymphatic transport system. Lymphat Res Biol. 2009;7:87-96.
Chiu J-J, Chien S. Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol Rev. 2011;91:327-387.
Cha B, Geng X, Mahamud MR, et al. Mechanotransduction activates canonical Wnt/β-catenin signaling to promote lymphatic vascular patterning and the development of lymphatic and lymphovenous valves. Genes Dev. 2016;30:1454-1469.
Tatin F, Taddei A, Weston A, et al. Planar cell polarity protein Celsr1 regulates endothelial adherens junctions and directed cell rearrangements during valve morphogenesis. Dev Cell. 2013;26:31-44.
Murtomaki A, Uh MK, Kitajewski C, et al. Notch signaling functions in lymphatic valve formation. Development. 2014;141:2446-2451.
Fatima A, Wang Y, Uchida Y, et al. Foxc1 and Foxc2 deletion causes abnormal lymphangiogenesis and correlates with ERK hyperactivation. J Clin Invest. 2016;126:2437-2451.
Sabine A, Bovay E, Demir CS, et al. FOXC2 and fluid shear stress stabilize postnatal lymphatic vasculature. J Clin Invest. 2015;125:3861-3877.
Wigle JT, Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell. 1999;98:769-778.
Srinivasan RS, Oliver G. Prox1 dosage controls the number of lymphatic endothelial cell progenitors and the formation of the lymphovenous valves. Genes Dev. 2011;25:2187-2197.
Kanady JD, Munger SJ, Witte MH, Simon AM. Combining Foxc2 and Connexin37 deletions in mice leads to severe defects in lymphatic vascular growth and remodeling. Dev Biol. 2015;405:33-46.
Kanady JD, Simon AM. Lymphatic communication: connexin junction, what's your function? Lymphology. 2011;44:102.