Effect of cyclic AMP on barrier function of human lymphatic microvascular tubes
Open accessAbstract
This work examines the effect of cyclic AMP (cAMP) on the in vitro barrier function of tubes of human dermal lymphatic microvascular endothelial cells (LECs). Under baseline conditions, the barrier function of LEC tubes was weak, with diffusional permeability coefficients to bovine serum albumin and 10 kDa dextran of 1.4(-0.6)(+0.9)x10(-6) cm/s and 1.7(-0.5)(+0.8)x10(-6) cm/s (geometric mean+/-95% CI), respectively, and 1.2+/-0.5 (mean+/-95% CI) focal leaks per mm. Exposure to low concentrations (3 microM) of a cell-permeant analog of cAMP did not alter the barrier function. Exposure to higher concentrations (80 and 400 microM) and/or the phosphodiesterase inhibitor Ro-20-1724 (20 microM) lowered permeabilities and the number of focal leaks, and increased the selectivity of the barrier. Decreased permeabilities were accompanied by an increase in continuous VE-cadherin staining at cell-cell borders. Exposure to 1 mM 2',5'-dideoxyadenosine, an inhibitor of adenylate cyclase, did not increase permeabilities. LECs expressed the lymphatic-specific master transcription factor Prox-1, regardless of whether barrier function was weak or strong. Our results indicate that the permeability of LEC tubes in vitro responds to cAMP in a manner similar to that well-described for the permeability of blood microvessels.
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The permeability of initial lymphatics has not been systematically measured but is estimated to be three- to tenfold higher than that of collecting LVs.
“The permeability of initial lymphatics has not been systematically measured but is estimated to be three- to tenfold higher than that of collecting LVs (31, 35), reflecting the functional differences between button and zipper junctions.”
From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [35]
The Introduction says quantitative permeability of lymphatic microvessels is poorly known because initial lymphatic capillaries are difficult to cannulate. It does not give a three- to tenfold estimate or compare initial with collecting lymphatic vessels; the Results instead measure cultured LEC tubes. (LLM, conf=0.84)
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Cites
Multifunctional strands in tight junctions
Tsukita, S., Furuse, M., & Itoh, M. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35067088 · Cited by 2,514 · see citing works
The endothelial glycocalyx: composition, functions, and visualization
Reitsma, S., Slaaf, D. W., Vink, H., van Zandvoort, M. A. M. J., & Egbrink, M. G. A. O. (2007) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-007-0212-8 · Cited by 1,987 · see citing works
Stevenson, B. R., Siliciano, J. D., Mooseker, M. S., & Goodenough, D. A. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.103.3.755 · Cited by 1,640 · see citing works
Leakage-Resistant Blood Vessels in Mice Transgenically Overexpressing Angiopoietin-1
Thurston, G., Suri, C., Smith, K., McClain, J., Sato, T. T., Yancopoulos, G. D., & McDonald, D. M. (1999) · Science · doi:10.1126/science.286.5449.2511 · Cited by 1,350 · see citing works
Functionally specialized junctions between endothelial cells of lymphatic vessels
Baluk, P., Fuxe, J., Hashizume, H., Romano, T., Lashnits, E., Butz, S., Vestweber, D., Corada, M., Molendini, C., Dejana, E., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20062596 · Cited by 1,006 · see citing works
Cytoskeletal regulation of pulmonary vascular permeability
Dudek, S. M., & Garcia, J. G. N. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.4.1487 · Cited by 985 · see citing works
An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype
Wigle, J. T., Harvey, N., Detmar, M., Lagutina, I., Grosveld, G., Gunn, M. D., Jackson, D. G., & Oliver, G. (2002) · The EMBO Journal · doi:10.1093/emboj/21.7.1505 · Cited by 943 · see citing works
Garcia, J. G. N., Liu, F., Verin, A. D., Birukova, A. A., Dechert, M. A., Gerthoffer, W. T., Bamberg, J. R., & English, D. K. (2001) · Journal of Clinical Investigation · doi:10.1172/jci12450 · Cited by 886 · see citing works
Michel, C. C., & CURRY, F. E. (1999) · Physiological Reviews · doi:10.1152/physrev.1999.79.3.703 · Cited by 813 · see citing works
A cell culture model of the blood-brain barrier.
Rubin, L. L., Hall, D. E., Porter, S., Barbu, K., Cannon, C., Horner, H. C., Janatpour, M. J., Liaw, C. W., Manning, K., & Morales, J. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.115.6.1725 · Cited by 765 · see citing works
Petrova, T. V., Mäkinen, T., Mäkelä, T. P., Saarela, J., Virtanen, I., Ferrell, R. E., Finegold, D. N., Kerjaschki, D., Ylä‐Herttuala, S., & Alitalo, K. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf470 · Cited by 632 · see citing works
Microvascular permeability of normal and neoplastic tissues
Gerlowski, L. E., & Jain, R. K. (1986) · Microvascular Research · doi:10.1016/0026-2862(86)90018-x · Cited by 623 · see citing works
Microlymphatics and lymph flow
Schmid‐Schönbein, G. W. (1990) · Physiological Reviews · doi:10.1152/physrev.1990.70.4.987 · Cited by 615 · see citing works
Lampugnani, M. G., Corada, M., Caveda, L., Breviario, F., Ayalon, O., Geiger, B., & Dejana, E. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.129.1.203 · Cited by 598 · see citing works
Schacht, V., Dadras, S. S., Johnson, L. A., Jackson, D. G., Hong, Y., & Detmar, M. J. (2005) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)62311-5 · Cited by 596 · see citing works
Formation of perfused, functional microvascular tubes in vitro
Chrobak, K. M., Potter, D. R., & Tien, J. (2006) · Microvascular Research · doi:10.1016/j.mvr.2006.02.005 · Cited by 555 · see citing works
Self-citationKriehuber, E., Breiteneder-Geleff, S., Gröger, M., Soleiman, A., SCHOPPMANN, S. F., Stingl, G., Kerjaschki, D., & Maurer, D. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.194.6.797 · Cited by 526 · see citing works
Molecular characterization of lymphatic endothelial cells
Podgrabinska, S., Falter‐Braun, P., Velasco, P., Kloos, B., Pepper, M. S., Jackson, D. G., & Skobe, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242401399 · Cited by 486 · see citing works
Hirakawa, S., Hong, Y., Harvey, N. L., Schacht, V., Matsuda, K. M., Libermann, T. A., & Detmar, M. J. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63851-5 · Cited by 439 · see citing works
Wolburg, H., Neuhaus, J., Kniesel, U., Krauß, B., Schmid, E.-M., Öcalan, M., Farrell, C., & Risau, W. (1994) · Journal of Cell Science · doi:10.1242/jcs.107.5.1347 · Cited by 366 · see citing works
THE PERMEABILITY OF GLOMERULAR CAPILLARIES TO GRADED DEXTRANS
CAULFIELD, J. P., & Farquhar, M. G. (1974) · The Journal of Cell Biology · doi:10.1083/jcb.63.3.883 · Cited by 280 · see citing works
Transcytosis of albumin in capillary endothelium.
Milici, A. J., Watrous, N. E., Stukenbrok, H., & Palade, G. E. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.6.2603 · Cited by 269 · see citing works
Fine structure of the lymphatic capillary and the adjoining connective tissue area
Leak, L. V., & Burke, J. F. (1966) · American Journal of Anatomy · doi:10.1002/aja.1001180308 · Cited by 265 · see citing works
Transport of large molecules from plasma to interstitial fluid and lymph in dogs
Garlick, D., & Renkin, E. M. (1970) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1970.219.6.1595 · Cited by 260 · see citing works
Interendothelial junctions: structure, signalling and functional roles
Lampugnani, M. G., & Dejana, E. (1997) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(97)80121-4 · Cited by 231 · see citing works
Kohn, S., Nagy, J. A., Dvorak, H. F., & Dvořàk, A. M. (1992) · PubMed · Cited by 190 · see citing works
Permeability characteristics of cultured endothelial cell monolayers
Albelda, S. Μ., Sampson, P. M., Haselton, F. R., McNiff, J. M., Mueller, S. N., Williams, S. K., Fishman, A. P., & Levine, E. M. (1988) · Journal of Applied Physiology · doi:10.1152/jappl.1988.64.1.308 · Cited by 182 · see citing works
Quantitative fluorescence microscopy on single capillaries: alpha-lactalbumin transport
Huxley, V. H., CURRY, F. E., & Adamson, R. H. (1987) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1987.252.1.h188 · Cited by 161 · see citing works
STUDIES ON THE PERMEABILITY OF LYMPHATIC CAPILLARIES
Leak, L. V. (1971) · The Journal of Cell Biology · doi:10.1083/jcb.50.2.300 · Cited by 148 · see citing works
Micromanipulation of pressure in terminal lymphatics in the mesentery
Zweifach, B., & Prather, J. (1975) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1975.228.5.1326 · Cited by 148 · see citing works
Microvascular permeability and number of tight junctions are modulated by cAMP
Adamson, R. H., Liu, B., Fry, G. N., Rubin, L. L., & CURRY, F. E. (1998) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1998.274.6.h1885 · Cited by 145 · see citing works
Holgate, S. T., Lewis, R. A., & Austen, K. F. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.11.6800 · Cited by 143 · see citing works
Amatschek, S., Kriehuber, E., Bauer, W. M., Reininger, B., Meraner, P., Wolpl, A., Schweifer, N., Haslinger, C., Stingl, G., & Maurer, D. (2007) · Blood · doi:10.1182/blood-2006-10-053280 · Cited by 136 · see citing works
Permeability of human endothelial monolayers: effect of vasoactive agonists and cAMP
Casnocha, S. A., Eskin, S. G., Hall, E. R., & McIntire, L. V. (1989) · Journal of Applied Physiology · doi:10.1152/jappl.1989.67.5.1997 · Cited by 129 · see citing works
Measurement of albumin permeability across endothelial monolayers in vitro
Cooper, J. A., Vecchio, P. J. D., Minnear, F. L., Burhop, K. E., Selig, W. M., Garcia, J. G. N., & Malik, A. B. (1987) · Journal of Applied Physiology · doi:10.1152/jappl.1987.62.3.1076 · Cited by 114 · see citing works
Compounds that increase cAMP prevent ischemia-reperfusion pulmonary capillary injury
Adkins, W. K., Barnard, J. W., May, S., Seibert, A. F., Haynes, J., & Taylor, A. E. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.72.2.492 · Cited by 93 · see citing works
Dominant role of cAMP in regulation of microvessel permeability
He, P., Zeng, M., & CURRY, F. E. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.278.4.h1124 · Cited by 92 · see citing works
cAMP protects endothelial barrier functions by preventing Rac-1 inhibition
Waschke, J., Drenckhahn, D., Adamson, R. H., Barth, H., & CURRY, F. E. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00556.2004 · Cited by 89 · see citing works
Reversal of increased microvascular permeability associated with ischemia-reperfusion: role of cAMP
Seibert, A. F., Thompson, W. J., Taylor, A. E., Wilborn, W. H., Barnard, J. W., & Haynes, J. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.72.1.389 · Cited by 88 · see citing works
Patterson, C. E., Davis, H. W., Schaphorst, K. L., & Garcia, J. G. N. (1994) · Microvascular Research · doi:10.1006/mvre.1994.1050 · Cited by 78 · see citing works
Malik, A. B., Lynch, J. J., & Cooper, J. A. (1989) · Journal of Investigative Dermatology · doi:10.1038/jid.1989.11 · Cited by 73 · see citing works
Barnard, J. W., Seibert, A. F., Prasad, V. R., Smart, D., Strada, S. J., Taylor, A. E., & Thompson, W. J. (1994) · Journal of Applied Physiology · doi:10.1152/jappl.1994.77.2.774 · Cited by 70 · see citing works
Dye, J. F., Leach, L., Clark, P., & Firth, J. A. (2001) · Microvascular Research · doi:10.1006/mvre.2001.2333 · Cited by 49 · see citing works
Ono, N., Mizuno, R., & Ohhashi, T. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01084.2004 · Cited by 42 · see citing works
Malik, A. B., Lynch, J. J., & Cooper, J. A. (1989) · Journal of Investigative Dermatology · doi:10.1111/1523-1747.ep12581072 · Cited by 34 · see citing works
Adamson, S. L., Liu, B., Fry, G. N., Rubin, L. L., & CURRY, F. E. (1998) · Cited by 31 · see citing works
Method for Determination of Cyclic AMP in Plasma
Rabinowitz, B., & Katz, J. J. (1973) · Clinical Chemistry · doi:10.1093/clinchem/19.3.312 · Cited by 28 · see citing works
Schaeffer, R. C., & Bitrick, M. S. (1995) · Microvascular Research · doi:10.1006/mvre.1995.1031 · Cited by 11 · see citing works
Huber, M., Uk, F., & Bollinger, A. (1984) · PubMed · Cited by 10 · see citing works
An ultrastructural study of transport pathways across rat hepatic lymph vessels.
Niiro, G. K., & O’Morchoe, C. C. C. (1985) · PubMed · Cited by 10 · see citing works
Induction of Endothelial Barrier Function in Vitro
Koch, G., Prätzel, S., Rode, M., & Kräling, B. M. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb05234.x · Cited by 4 · see citing works
Weber, E., Sacchi, G., & Comparini, L. (1991) · Angiology · doi:10.1177/000331979104201109 · Cited by 3 · see citing works
Flagged first, then by citations
1 of the 53 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Taylor AE, Granger DN. Exchange of macromolecules across the microcirculation. In: Renkin EM, Michel CC, editors. Handbook of Physiology; Section 2: The Cardiovascular System. American Physiological Society; Bethesda, MD: 1984. pp. 467–520. [Google Scholar]
Cited by
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Zhang, B., Korolj, A., Lai, B. F. L., & Radisic, M. (2018) · Nature Reviews Materials · doi:10.1038/s41578-018-0034-7 · Cited by 1,017 · see citing works
Lymphatic Vessel Network Structure and Physiology
Breslin, J. W., Yang, Y., Scallan, J. P., Sweat, R. S., Adderley, S., & Murfee, W. L. (2018) · Comprehensive physiology · doi:10.1002/cphy.c180015 · Cited by 402 · see citing works
Hydrogels for Engineering of Perfusable Vascular Networks
Liu, J., Zheng, H., Poh, P. S. P., Machens, H., & Schilling, A. F. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160715997 · Cited by 308 · see citing works
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Hasan, A., Paul, A., Vrana, N. E., Zhao, X., Memic, A., Hwang, Y.-S., Dokmeci, M. R., & Khademhosseini, A. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.04.091 · Cited by 282 · see citing works
Capillary Fluid Exchange: Regulation, Functions, and Pathology
Scallan, J. P., Huxley, V. H., & Korthuis, R. J. (2010) · Colloquium Series on Integrated Systems Physiology From Molecule to Function · doi:10.4199/c00006ed1v01y201002isp003 · Cited by 262 · see citing works
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Microfluidic hydrogels for tissue engineering
Huang, G., Zhou, L. H., Zhang, Q. C., Chen, Y. M., Sun, W., Xu, F., & Lu, T. J. (2011) · Biofabrication · doi:10.1088/1758-5082/3/1/012001 · Cited by 200 · see citing works
Price, G. M., Wong, K. H. K., Truslow, J. G., Leung, A. D., Acharya, C., & Tien, J. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.04.041 · Cited by 184 · see citing works
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Takei, T., Sakai, S., & Yoshida, M. (2016) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2016.03.023 · Cited by 23 · see citing works
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Bittner, K. R., Jiménez, J. M., & Peyton, S. R. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.201901459 · Cited by 23 · see citing works
Martier, A. T., Chen, Z., Schaps, H., Mondrinos, M. J., & Fang, J. (2024) · Frontiers in Physiology · doi:10.3389/fphys.2024.1425618 · Cited by 22 · see citing works
In Vitro Models of Blood and Lymphatic Vessels—Connecting Tissues and Immunity
Bogseth, A., Ramirez, A., Vaughan, E., & Maisel, K. (2022) · Advanced Biology · doi:10.1002/adbi.202200041 · Cited by 18 · see citing works
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Chang, C.-S., Seibel, A. J., & Song, J. W. (2019) · Microcirculation · doi:10.1111/micc.12547 · Cited by 17 · see citing works
Kraus, S., & Lee, E. (2023) · Lab on a Chip · doi:10.1039/d3lc00486d · Cited by 17 · see citing works
Kempe, S., Fois, G., Brunner, C., Hoffmann, T. K., Hahn, J., & Greve, J. (2019) · Microcirculation · doi:10.1111/micc.12592 · Cited by 16 · see citing works
Subtractive Methods for Forming Microfluidic Gels of Extracellular Matrix Proteins
Price, G. M., & Tien, J. (2009) · Cited by 15 · see citing works
Self-citationHarnessing cAMP signaling in musculoskeletal regenerative engineering
Ifegwu, O. C., Awale, G. M., Rajpura, K., Lo, K. W. ‐., & Laurencin, C. T. (2017) · Drug Discovery Today · doi:10.1016/j.drudis.2017.03.008 · Cited by 14 · see citing works
Engineered models of the lymphatic vascular system: Past, present, and future
Selahi, A., & Jain, A. (2022) · Microcirculation · doi:10.1111/micc.12793 · Cited by 10 · see citing works
Lymphatic vessels and the renin-angiotensin-system
Bertoldi, G., Caputo, I., Calò, L. A., & Rossitto, G. (2023) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00023.2023 · Cited by 8 · see citing works
The phosphodiesterase 2A controls lymphatic junctional maturation via cGMP-dependent notch signaling
Carlantoni, C., Liekfeld, L. M. H., Hemkemeyer, S. A., Schreier, D., Saygı, C., Kurelić, R., Cardarelli, S., Kalucka, J. M., Schulte, C., Beerens, M., et al. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.12.002 · Cited by 8 · see citing works
Hong, H., Eom, S., Lee, S. J., Youn, J., Kim, D., Chong, H. B., & Kim, D. S. (2022) · International Journal of Precision Engineering and Manufacturing · doi:10.1007/s12541-021-00615-w · Cited by 7 · see citing works
Role of Lymphatic Endothelium in Vascular Escape of Engineered Human Breast Microtumors
Seibel, A. J., Kelly, O. M., Dance, Y. W., Nelson, C. M., & Tien, J. (2022) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-022-00745-9 · Cited by 7 · see citing works
Self-citationRomanova, L. G., Hansen, E. A., & Lam, C. H. (2014) · Microcirculation · doi:10.1111/micc.12134 · Cited by 7 · see citing works
Tissue Engineering of the Microvasculature
Tien, J. (2019) · Comprehensive physiology · doi:10.1002/j.2040-4603.2019.tb00088.x · Cited by 5 · see citing works
Self-citationInvestigation of nanoparticle extravasation pathways in tumor vessel-on-a-chip devices
Dávila, S., Martín–Asensio, A., Diego, E. S., Hernández, J. J., & Rodríguez, I. (2025) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2025.102863 · Cited by 3 · see citing works
Generation of complex neuronal behaviour in a mammalian nervous system
Bayguinov, P. O., Hennig, G. W., & Smith, T. K. (2010) · Physiology News · doi:10.36866/pn.80.29 · Cited by 3 · see citing works
Collecting lymphatic vessel permeability to albumin and its modification by natriuretic peptides
Scallan, J. P. (2010) · doi:10.32469/10355/8305 · Cited by 2 · see citing works
Hemadyne: accordion-inspired perfusion for microphysiological systems
Kumar, A., Pattanshetti, S., Patel, R. D., Pandey, R., Mahalingam, E., Rahbar, E., & Jain, A. (2026) · Nature Communications · doi:10.1038/s41467-026-73722-9 · Cited by 1 · see citing works
Nan, Y., Li, S.-Y., Ji-long, K., Suzuki, S., Ema, Y., & Nishiwaki, K. (2012) · African Journal of Microbiology Research · doi:10.5897/ajmr11.387 · Cited by 1 · see citing works
Lymphatic vessels – absorptive sumps or leaky pumps?
Scallan, J. P., & Huxley, V. H. (2010) · Physiology News · doi:10.36866/pn.80.16 · Cited by 1 · see citing works
Vascularization of capillary-scale channels in type I collagen gels
Boland, N. F., Linville, R. M., Covarrubias, G., & Tien, J. (2015) · Annual Northeast Biomedical Engineering Conference · doi:10.1109/nebec.2015.7117067
Self-citationThe Lymphatic Vasculature as a Participant in Microvascular Exchange
Scallan, J. P., & Huxley, V. H. (2011) · Annual update in intensive care and emergency medicine · doi:10.1007/978-3-642-18081-1_25
Analytical Applications of Microfluidic Vascular Models
SASAKI, N., & Sato, K. (2016) · BUNSEKI KAGAKU · doi:10.2116/bunsekikagaku.65.241
Kunder, C. A. (2009) · DukeSpace (Duke University)
‘Sensible to feeling as to sight’ Some recent progress on mechanosensory transduction in mammals
Bewick, G. S., & Banks, B. (2010) · Physiology News · doi:10.36866/pn.80.33
(2008) · Lymphatic Research and Biology · doi:10.1089/lrb.2008.63411
Electrical synapses synchronize motor output for tadpole swimming
Zhang, H.-Y., Li, W., Heitler, W. J., & Sillar, K. T. (2010) · Physiology News · doi:10.36866/pn.80.19
Can growth hormone strengthen the connective tissue of muscle and tendon?
Doessing, S., & Kjær, M. (2010) · Physiology News · doi:10.36866/pn.80.25
HIT to get fit: metabolic adaptations to low-volume high-intensity interval training
Little, J. P., & Gibala, M. J. (2010) · Physiology News · doi:10.36866/pn.80.22
Carlantoni, C., Liekfeld, L. M. H., Hemkemeyer, S. A., Schreier, D., Saygı, C., Kurelić, R., Cardarelli, S., Kalucka, J. M., Schulte, C., Beerens, M., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.18.524585
TruD technology for the study of epi- and endothelial tubes in vitro
Hansen, S. H. (2024) · PLoS ONE · doi:10.1371/journal.pone.0301099
Baranowska, P., Flont, M., Żuchowska, A., Brzózka, Z., & Jastrzębska, E. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15978-7.00048-5
VEGF-A/C co-stimulation, without shear stress, triggers the polarization of lymphatic microvesselsPreprint
Edwards, J., Morfoisse, F., Alric, B., Garmy-Susini, B. H., Matsunaga, Y. T., & Bancaud, A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.13.670220
- Authors
- Price, G. M., Chrobak, K. M., & Tien, J.
- Affiliations
- Boston University (US)
- Corresponding author
- Tien, Joe
- ORCID
- Tien, Joe
- Venue
- Microvascular Research
- Publisher
- Elsevier BV
- Published
- 2008-05
- Volume
- 76
- Issue
- 1
- Pages
- 46-51
- ISSN
- 0026-2862 (ISSN-L)
- PMC
- PMC2574545
- OpenAlex
- W2135431568
- Cited by
- 80
- References
- 53
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 5 · 2023: 7 · 2022: 4 · 2021: 2 · 2020: 6 · 2019: 6 · 2018: 2 · 2017: 5 · 2016: 4 · 2015: 5 · 2014: 4 · 2013: 2 · 2012: 3
- FWCI
- 3.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Microvascular Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Biomedical Imaging and Bioengineering (EB002228, EB005792, R21EB002228, R01EB005792)
- Topics
- Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Surgery › Lymphatic Disorders and Treatments
- Keywords
- cyclic AMP, lymphatic endothelial cells, endothelial permeability, phosphodiesterase inhibition, Ro 20-1724, VE-cadherin, Prox1, adenylate cyclase inhibition, dextran permeability
- MeSH terms
- Adenylyl Cyclase Inhibitors, Prospero-Related Homeobox 1 Protein, Podoplanin, Cadherin 5, Cyclic AMP, Capillary Permeability, Cell Nucleus, Cells, Cultured, Dextrans, Bucladesine, Endothelium, Lymphatic, Enzyme Inhibitors, Humans, Membrane Glycoproteins, Membrane Proteins, Phosphoproteins, 4-(3-Butoxy-4-methoxybenzyl)-2-imidazolidinone, Serum Albumin, Bovine, Antigens, CD, Cadherins, Dideoxyadenosine, Homeodomain Proteins, Tight Junctions, Platelet Endothelial Cell Adhesion Molecule-1, Adherens Junctions, Tissue Engineering, Tumor Suppressor Proteins, Endothelial Cells, Zonula Occludens-1 Protein
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