CoChat
Sign Up
Cited by 22Lymphatic System and DiseasesIon channel regulation and functionCalcium signaling and nucleotide metabolism

The DOI matches its Crossref record.

IP3R1 underlies diastolic ANO1 activation and pressure-dependent chronotropy in lymphatic collecting vessels

Open access
Zawieja, Scott D., Pea, Grace A., Broyhill, Sarah E., Patro, Advaya, Bromert, Karen H., Li, Min, Norton, Charles E., Castorena-Gonzalez, Jorge A., Hancock, Edward J., Bertram, Christopher D., Davis, Michael J.·2023·Journal of General Physiology
DOI 10.1085/jgp.202313358PMC PMC10585095
Open this paper in CoChat — free accountOpen PDF

Abstract

Pressure-dependent chronotropy of murine lymphatic collecting vessels relies on the activation of the Ca2+-activated chloride channel encoded by Anoctamin 1 (Ano1) in lymphatic muscle cells. Genetic ablation or pharmacological inhibition of ANO1 results in a significant reduction in basal contraction frequency and essentially complete loss of pressure-dependent frequency modulation by decreasing the rate of the diastolic depolarization phase of the ionic pacemaker in lymphatic muscle cells (LMCs). Oscillating Ca2+ release from sarcoendoplasmic reticulum Ca2+ channels has been hypothesized to drive ANO1 activity during diastole, but the source of Ca2+ for ANO1 activation in smooth muscle remains unclear. Here, we investigated the role of the inositol triphosphate receptor 1 (Itpr1; Ip3r1) in this process using pressure myography, Ca2+ imaging, and membrane potential recordings in LMCs of ex vivo pressurized inguinal-axillary lymphatic vessels from control or Myh11CreERT2;Ip3r1fl/fl (Ip3r1ismKO) mice. Ip3r1ismKO vessels had significant reductions in contraction frequency and tone but an increased contraction amplitude. Membrane potential recordings from LMCs of Ip3r1ismKO vessels revealed a depressed diastolic depolarization rate and an elongation of the plateau phase of the action potential (AP). Ca2+ imaging of LMCs using the genetically encoded Ca2+ sensor GCaMP6f demonstrated an elongation of the Ca2+ flash associated with an AP-driven contraction. Critically, diastolic subcellular Ca2+ transients were absent in LMCs of Ip3r1ismKO mice, demonstrating the necessity of IP3R1 activity in controlling ANO1-mediated diastolic depolarization. These findings indicate a critical role for IP3R1 in lymphatic vessel pressure-dependent chronotropy and contractile regulation.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1085/jgp.202313358

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The slope of diastolic depolarization is highly dependent on the activity of ANO1 channels that are regulated by Ca2+ release from IP3R1-dependent stores.

    “The slope of diastolic depolarization is highly dependent on the activity of ANO1 channels (55) that are regulated by Ca2+ release from inositol trisphosphate receptor 1 (IP3R1)-dependent stores (80).”

    From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [80]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 120

  1. Akin, 2023, ANO1, CaV1.2, and IP3R form a localized unit of EC-coupling in mouse pulmonary arterial smooth muscle, J. Gen. Physiol., 155, 10.1085/jgp.202213217 · DOI
  2. Ali, 2021, Nitric oxide signals through IRAG to inhibit TRPM4 channels and dilate cerebral arteries, Function, 2, zqab051, 10.1093/function/zqab051 · DOI
  3. Atchison, 1997, Role of extra- and intracellular Ca2+ in the lymphatic myogenic response, Am. J. Physiol., 272, R326, 10.1152/ajpregu.1997.272.1.R326 · DOI
  4. Atchison, 1998, Intracellular calcium stores modulation in lymph vessels depends on wall stretch, Can. J. Physiol. Pharmacol., 76, 367, 10.1139/y98-037 · DOI
  5. Bachmann, 2019, A distinct role of the autonomic nervous system in modulating the function of lymphatic vessels under physiological and tumor-draining conditions, Cell Rep., 27, 3305, 10.1016/j.celrep.2019.05.050 · DOI
  6. Baker, 2021, Ca2+ transients in ICC-MY define the basis for the dominance of the corpus in gastric pacemaking, Cell Calcium, 99, 102472, 10.1016/j.ceca.2021.102472 · DOI
  7. Baker, 2021, Ca2+ signaling driving pacemaker activity in submucosal interstitial cells of Cajal in the murine colon, eLife, 10, 10.7554/eLife.64099 · DOI
  8. Balla, 1998, Phosphatidylinositol 4-kinases, Biochim. Biophys. Acta, 1436, 69, 10.1016/S0005-2760(98)00134-9 · DOI
  9. Bao, 2008, A close association of RyRs with highly dense clusters of Ca2+-activated Cl− channels underlies the activation of STICs by Ca2+ sparks in mouse airway smooth muscle, J. Gen. Physiol., 132, 145, 10.1085/jgp.200709933 · DOI
  10. Bayguinov, 2011, Movement based artifacts may contaminate extracellular electrical recordings from GI muscles, Neurogastroenterol. Motil., 23, 1029, 10.1111/j.1365-2982.2011.01784.x · DOI
  11. Beckett, 2007, Spontaneous electrical activity in sheep mesenteric lymphatics, Lymphat. Res. Biol., 5, 29, 10.1089/lrb.2007.5104 · DOI
  12. Behringer, 2017, Calcium and electrical dynamics in lymphatic endothelium, J. Physiol., 595, 7347, 10.1113/JP274842 · DOI
  13. Benoit, 1997, Effects of alpha-adrenergic stimuli on mesenteric collecting lymphatics in the rat, Am. J. Physiol., 273, R331, 10.1152/ajpregu.1997.273.1.R331 · DOI
  14. Benoit, 1989, Characterization of intact mesenteric lymphatic pump and its responsiveness to acute edemagenic stress, Am. J. Physiol., 257, H2059, 10.1152/ajpheart.1989.257.6.H2059 · DOI
  15. Boedtkjer, 2015, New selective inhibitors of calcium-activated chloride channels – T16Ainh-A01, CaCCinh-A01 and MONNA – what do they inhibit?, Br. J. Pharmacol, 172, 4158, 10.1111/bph.13201 · DOI
  16. Briggs Boedtkjer, 2013, Identification of interstitial Cajal-like cells in the human thoracic duct, Cells Tissues Organs, 197, 145, 10.1159/000342437 · DOI
  17. Bulley, 2012, TMEM16A/ANO1 channels contribute to the myogenic response in cerebral arteries, Circ. Res., 111, 1027, 10.1161/CIRCRESAHA.112.277145 · DOI
  18. Burke, 1996, Wortmannin inhibits contraction without altering electrical activity in canine gastric smooth muscle, Am. J. Physiol., 270, C1405, 10.1152/ajpcell.1996.270.5.C1405 · DOI
  19. Caputo, 2008, TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity, Science, 322, 590, 10.1126/science.1163518 · DOI
  20. Castorena-Gonzalez, 2018, Mechanisms of connexin-related lymphedema, Circ. Res., 123, 964, 10.1161/CIRCRESAHA.117.312576 · DOI
  21. Chen, 2013, Ultrasensitive fluorescent proteins for imaging neuronal activity, Nature, 499, 295, 10.1038/nature12354 · DOI · Paper page
  22. Cobine, 2017, ANO1 in intramuscular interstitial cells of Cajal plays a key role in the generation of slow waves and tone in the internal anal sphincter, J. Physiol., 595, 2021, 10.1113/JP273618 · DOI
  23. Davis, 2005, An improved, computer-based method to automatically track internal and external diameter of isolated microvessels, Microcirculation, 12, 361, 10.1080/10739680590934772 · DOI
  24. Davis, 2023, A vascular smooth muscle-specific integrin-α8 Cre mouse for lymphatic contraction studies that allows male-female comparisons and avoids visceral myopathy, Front. Physiol., 13, 1060146, 10.3389/fphys.2022.1060146 · DOI
  25. Davis, 2020, Kir6.1-dependent KATP channels in lymphatic smooth muscle and vessel dysfunction in mice with Kir6.1 gain-of-function, J. Physiol., 598, 3107, 10.1113/JP279612 · DOI
  26. Davis, 2012, Intrinsic increase in lymphangion muscle contractility in response to elevated afterload, Am. J. Physiol. Heart Circ. Physiol., 303, H795, 10.1152/ajpheart.01097.2011 · DOI · Paper page
  27. Deaton, 2023, A new autosomal Myh11-CreERT2 smooth muscle cell lineage tracing and gene knockout mouse model-brief report, Arterioscler. Thromb. Vasc. Biol., 43, 203, 10.1161/ATVBAHA.122.318160 · DOI
  28. Drumm, 2022, Ca2+ signalling in interstitial cells of Cajal contributes to generation and maintenance of tone in mouse and monkey lower oesophageal sphincters, J. Physiol., 600, 2613, 10.1113/JP282570 · DOI
  29. Ferrusi, 2004, Cyclopiazonic acid decreases spontaneous transient depolarizations in Guinea pig mesenteric lymphatic vessels in endothelium-dependent and -independent manners, Am. J. Physiol. Heart Circ. Physiol., 286, H2287, 10.1152/ajpheart.00739.2003 · DOI
  30. Gasheva, 2013, Cyclic guanosine monophosphate and the dependent protein kinase regulate lymphatic contractility in rat thoracic duct, J. Physiol., 591, 4549, 10.1113/jphysiol.2013.258681 · DOI
  31. Georgeon-Chartier, 2013, Effect of aging on calcium signaling in C57Bl6J mouse cerebral arteries, Pflugers Arch., 465, 829, 10.1007/s00424-012-1195-7 · DOI
  32. Gonzales, 2010, Ca2+ release from the sarcoplasmic reticulum is required for sustained TRPM4 activity in cerebral artery smooth muscle cells, Am. J. Physiol. Cell Physiol., 299, C279, 10.1152/ajpcell.00550.2009 · DOI
  33. Guo, 2003, Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles, Proc. Natl. Acad. Sci. USA, 100, 3995, 10.1073/pnas.0230488100 · DOI
  34. Hald, 2018, Electrical communication in lymphangions, Biophys. J., 115, 936, 10.1016/j.bpj.2018.07.033 · DOI
  35. Hancock, 2023, A dual-clock-driven model of lymphatic muscle cell pace-making to emulate knock-out of Ano1 or IP3R, J. Gen. Physiol, 155, e202313355, 10.1085/jgp.202313355 · DOI
  36. Hancock, 2022, Modelling the coupling of the M-clock and C-clock in lymphatic muscle cells, Comput. Biol. Med., 142, 105189, 10.1016/j.compbiomed.2021.105189 · DOI
  37. Harraz, 2018, PIP2 depletion promotes TRPV4 channel activity in mouse brain capillary endothelial cells, Elife, 7, 10.7554/eLife.38689 · DOI · Paper page
  38. Hashimoto, 1994, Effects of vasoactive substances on the pig isolated hepatic lymph vessels, J. Pharmacol. Exp. Ther., 269, 482
  39. Hauser, 2022, Common coupling map advances GPCR-G protein selectivity, Elife, 11, 10.7554/eLife.74107 · DOI
  40. Hawn, 2021, Molecular mechanisms of activation and regulation of ANO1-Encoded Ca2+-Activated Cl− channels, Channels, 15, 569, 10.1080/19336950.2021.1975411 · DOI
  41. Igarashi, 1998, Electrical stimulation-induced alpha1- and alpha2-adrenoceptors-mediated contraction in isolated dog thoracic ducts, J. Auton. Nerv. Syst., 71, 18, 10.1016/S0165-1838(98)00057-5 · DOI
  42. Imtiaz, 2007, Pacemaking through Ca2+ stores interacting as coupled oscillators via membrane depolarization, Biophys. J., 92, 3843, 10.1529/biophysj.106.095687 · DOI
  43. Jia, 2021, Specific PIP2 binding promotes calcium activation of TMEM16A chloride channels, Commun. Biol., 4, 259, 10.1038/s42003-021-01782-2 · DOI
  44. Jin, 2013, Activation of the Cl− channel ANO1 by localized calcium signals in nociceptive sensory neurons requires coupling with the IP3 receptor, Sci. Signal., 6, ra73, 10.1126/scisignal.2004184 · DOI
  45. Jo, 2019, Evidence of functional ryanodine receptors in rat mesenteric collecting lymphatic vessels, Am. J. Physiol. Heart Circ. Physiol., 317, H561, 10.1152/ajpheart.00564.2018 · DOI
  46. Krishnan, 2022, STIM1-dependent peripheral coupling governs the contractility of vascular smooth muscle cells, Elife, 11, 10.7554/eLife.70278 · DOI
  47. Lee, 2014, Distinct roles of L- and T-type voltage-dependent Ca2+ channels in regulation of lymphatic vessel contractile activity, J. Physiol., 592, 5409, 10.1113/jphysiol.2014.280347 · DOI
  48. Lee, 2020, Roles of sarcoplasmic reticulum Ca2+ ATPase pump in the impairments of lymphatic contractile activity in a metabolic syndrome rat model, Sci. Rep., 10, 12320, 10.1038/s41598-020-69196-4 · DOI
  49. Lee, 2022, Lymphatic collecting vessel: New perspectives on mechanisms of contractile regulation and potential lymphatic contractile pathways to target in obesity and metabolic diseases, Front. Pharmacol., 13, 848088, 10.3389/fphar.2022.848088 · DOI
  50. Leo, 2021, TMEM16A channel upregulation in arterial smooth muscle cells produces vasoconstriction during diabetes, Am. J. Physiol. Heart Circ. Physiol., 320, H1089, 10.1152/ajpheart.00690.2020 · DOI
  51. Liao, 2011, Impaired lymphatic contraction associated with immunosuppression, Proc. Natl. Acad. Sci. USA, 108, 18784, 10.1073/pnas.1116152108 · DOI · Paper page
  52. Lin, 2016, IP3 receptors regulate vascular smooth muscle contractility and hypertension, JCI Insight, 1, 10.1172/jci.insight.89402 · DOI
  53. Lipskaia, 2014, Expression of sarco (endo) plasmic reticulum calcium ATPase (SERCA) system in normal mouse cardiovascular tissues, heart failure and atherosclerosis, Biochim. Biophys. Acta, 1843, 2705, 10.1016/j.bbamcr.2014.08.002 · DOI
  54. Liu, 2005, Involvement of ryanodine receptors in pacemaker Ca2+ oscillation in murine gastric ICC, Biochem. Biophys. Res. Commun., 328, 640, 10.1016/j.bbrc.2005.01.029 · DOI
  55. Lowie, 2011, On the origin of rhythmic calcium transients in the ICC-MP of the mouse small intestine, Am. J. Physiol. Gastrointest. Liver Physiol., 301, G835, 10.1152/ajpgi.00077.2011 · DOI
  56. Lyashkov, 2018, Positive feedback mechanisms among local Ca releases, NCX, and ICaL ignite pacemaker action potentials, Biophys. J., 114, 2024, 10.1016/j.bpj.2018.03.024 · DOI
  57. Maejima, 2011, Platelet-derived growth factor (PDGF)-BB produces NO-mediated relaxation and PDGF receptor β-dependent tonic contraction in murine iliac lymph vessels, Microcirculation, 18, 474, 10.1111/j.1549-8719.2011.00108.x · DOI
  58. Majgaard, 2022, Positive chronotropic action of HCN channel antagonism in human collecting lymphatic vessels, Physiol. Rep., 10, 10.14814/phy2.15401 · DOI
  59. Maltsev, 2013, Numerical models based on a minimal set of sarcolemmal electrogenic proteins and an intracellular Ca(2+) clock generate robust, flexible, and energy-efficient cardiac pacemaking, J. Mol. Cell. Cardiol., 59, 181, 10.1016/j.yjmcc.2013.03.004 · DOI
  60. Mangoni, 2008, Genesis and regulation of the heart automaticity, Physiol. Rev., 88, 919, 10.1152/physrev.00018.2007 · DOI
  61. Mathias, 2013, Involvement of the NO-cGMP-K(ATP) channel pathway in the mesenteric lymphatic pump dysfunction observed in the Guinea pig model of TNBS-induced ileitis, Am. J. Physiol. Gastrointest. Liver Physiol., 304, G623, 10.1152/ajpgi.00392.2012 · DOI
  62. McCloskey, 2002, Kit-like immunopositive cells in sheep mesenteric lymphatic vessels, Cell Tissue Res., 310, 77, 10.1007/s00441-002-0623-y · DOI
  63. McHale, 1976, The effect of transmural pressure on pumping activity in isolated bovine lymphatic vessels, J. Physiol., 261, 255, 10.1113/jphysiol.1976.sp011557 · DOI
  64. Missiaen, 1991, Spontaneous calcium release from inositol trisphosphate-sensitive calcium stores, Nature, 352, 241, 10.1038/352241a0 · DOI
  65. Mohanakumar, 2018, Spontaneous and α-adrenoceptor-induced contractility in human collecting lymphatic vessels require chloride, Am. J. Physiol. Heart Circ. Physiol., 315, H389, 10.1152/ajpheart.00551.2017 · DOI
  66. Morfoisse, 2021, Sex hormones in lymphedema, Cancers, 13, 530, 10.3390/cancers13030530 · DOI
  67. Nakanishi, 1995, A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositolphospholipids, Proc. Natl. Acad. Sci. USA, 92, 5317, 10.1073/pnas.92.12.5317 · DOI
  68. Ningoo, 2021, PIP2 regulation of TRPC5 channel activation and desensitization, J. Biol. Chem., 296, 100726, 10.1016/j.jbc.2021.100726 · DOI
  69. Olszewski, 2002, Contractility patterns of normal and pathologically changed human lymphatics, Ann. N. Y. Acad. Sci., 979, 52, 10.1111/j.1749-6632.2002.tb04867.x · DOI
  70. Olszewski, 2008, Contractility patterns of human leg lymphatics in various stages of obstructive lymphedema, Ann. N. Y. Acad. Sci., 1131, 110, 10.1196/annals.1413.010 · DOI · Paper page
  71. Ouyang, 2014, Loss of IP3R-dependent Ca2+ signalling in thymocytes leads to aberrant development and acute lymphoblastic leukemia, Nat. Commun., 5, 4814, 10.1038/ncomms5814 · DOI
  72. Pal, 2022, Drug-related lymphedema: Mysteries, mechanisms, and potential therapies, Front. Pharmacol., 13, 850586, 10.3389/fphar.2022.850586 · DOI
  73. Peinelt, 2006, Amplification of CRAC current by STIM1 and CRACM1 (Orai1), Nat. Cell Biol., 8, 771, 10.1038/ncb1435 · DOI
  74. Peppiatt, 2003, 2-Aminoethoxydiphenyl borate (2-APB) antagonises inositol 1,4,5-trisphosphate-induced calcium release, inhibits calcium pumps and has a use-dependent and slowly reversible action on store-operated calcium entry channels, Cell Calcium, 34, 97, 10.1016/S0143-4160(03)00026-5 · DOI
  75. Pritchard, 2014, Inhibitory role of phosphatidylinositol 4,5-bisphosphate on TMEM16A-encoded calcium-activated chloride channels in rat pulmonary artery, Br. J. Pharmacol., 171, 4311, 10.1111/bph.12778 · DOI
  76. Russell, 2022, Lymphatic contractile function: A comprehensive review of drug effects and potential clinical application, Cardiovasc. Res., 118, 2437, 10.1093/cvr/cvab279 · DOI
  77. Saleem, 2014, Interactions of antagonists with subtypes of inositol 1,4,5-trisphosphate (IP3) receptor, Br. J. Pharmacol., 171, 3298, 10.1111/bph.12685 · DOI
  78. Sanders, 2023, Ca(2+) dynamics in interstitial cells: foundational mechanisms for the motor patterns in the gastrointestinal tract, Physiol Rev., 10, 10.1152/physrev.00036.2022 · DOI
  79. Sanders, 2014, Interstitial cells: Regulators of smooth muscle function, Physiol. Rev., 94, 859, 10.1152/physrev.00037.2013 · DOI
  80. Scallan, 2013, Constriction of isolated collecting lymphatic vessels in response to acute increases in downstream pressure, J. Physiol., 591, 443, 10.1113/jphysiol.2012.237909 · DOI · Paper page
  81. Scallan, 2012, Independent and interactive effects of preload and afterload on the lymphatic pump, Am. J. Physiol. Heart Circ. Physiol., 303, H809, 10.1152/ajpheart.01098.2011 · DOI · Paper page
  82. Schroeder, 2008, Expression cloning of TMEM16A as a calcium-activated chloride channel subunit, Cell, 134, 1019, 10.1016/j.cell.2008.09.003 · DOI
  83. Sculptoreanu, 1993, Voltage-dependent potentiation of L-type Ca2+ channels due to phosphorylation by cAMP-dependent protein kinase, Nature, 364, 240, 10.1038/364240a0 · DOI
  84. Seo, 2016, Ani9, A novel potent small-molecule ANO1 inhibitor with negligible effect on ANO2, PLoS One, 11, 10.1371/journal.pone.0155771 · DOI
  85. Sirenko, 2016, Electrochemical Na+ and Ca2+ gradients drive coupled-clock regulation of automaticity of isolated rabbit sinoatrial nodal pacemaker cells, Am. J. Physiol. Heart Circ. Physiol., 311, H251, 10.1152/ajpheart.00667.2015 · DOI
  86. Souza-Smith, 2015, Mechanisms of acute alcohol intoxication-induced modulation of cyclic mobilization of [Ca²⁺] in rat mesenteric lymphatic vessels, Lymphat. Res. Biol., 13, 93, 10.1089/lrb.2014.0048 · DOI
  87. Souza-Smith, 2011, Measurement of cytosolic Ca2+ in isolated contractile lymphatics, J. Vis. Exp, 8, 3438, 10.3791/3438 · DOI
  88. Stolarz, 2019, Doxorubicin activates ryanodine receptors in rat lymphatic muscle cells to attenuate rhythmic contractions and lymph flow, J. Pharmacol. Exp. Ther., 371, 278, 10.1124/jpet.119.257592 · DOI
  89. Sun, 2022, A gain-of-function mutation in the ITPR1 gating domain causes male infertility in mice, J. Cell. Physiol., 237, 3305, 10.1002/jcp.30783 · DOI
  90. Telinius, 2014, The human thoracic duct is functionally innervated by adrenergic nerves, Am. J. Physiol. Heart Circ. Physiol., 306, H206, 10.1152/ajpheart.00517.2013 · DOI
  91. Tembo, 2019, Phosphatidylinositol 4,5-bisphosphate (PIP2) and Ca2+ are both required to open the Cl− channel TMEM16A, J. Biol. Chem., 294, 12556, 10.1074/jbc.RA118.007128 · DOI
  92. Tian, 2011, Calmodulin-dependent activation of the epithelial calcium-dependent chloride channel TMEM16A, FASEB J., 25, 1058, 10.1096/fj.10-166884 · DOI
  93. To, 2020, T-type, but not L-type, voltage-gated calcium channels are dispensable for lymphatic pacemaking and spontaneous contractions, Sci. Rep., 10, 70, 10.1038/s41598-019-56953-3 · DOI
  94. Toland, 2000, Ca(2+)-activated Cl(-) current in sheep lymphatic smooth muscle, Am. J. Physiol. Cell Physiol., 279, C1327, 10.1152/ajpcell.2000.279.5.C1327 · DOI
  95. Trebak, 2009, Complex functions of phosphatidylinositol 4,5-bisphosphate in regulation of TRPC5 cation channels, Pflugers Arch., 457, 757, 10.1007/s00424-008-0550-1 · DOI
  96. Truett, 2000, Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT), Biotechniques, 29, 52, 10.2144/00291bm09 · DOI
  97. Tsutsui, 2018, A coupled-clock system drives the automaticity of human sinoatrial nodal pacemaker cells, Sci. Signal., 11, 10.1126/scisignal.aap7608 · DOI
  98. Van Helden, 1996, Intracellular Ca release: A basis for electrical pacemaking in lymphatic smooth muscle, 355
  99. Van Helden, 1993, Pacemaker potentials in lymphatic smooth muscle of the Guinea-pig mesentery, J. Physiol., 471, 465, 10.1113/jphysiol.1993.sp019910 · DOI
  100. Van, 2021, Dantrolene prevents the lymphostasis caused by doxorubicin in the rat mesenteric circulation, Front. Pharmacol., 12, 727526, 10.3389/fphar.2021.727526 · DOI
  101. von der Weid, 2001, Review article: Lymphatic vessel pumping and inflammation--the role of spontaneous constrictions and underlying electrical pacemaker potentials, Aliment. Pharmacol. Ther., 15, 1115, 10.1046/j.1365-2036.2001.01037.x · DOI
  102. von der Weid, 2008, Spontaneous transient depolarizations in lymphatic vessels of the Guinea pig mesentery: Pharmacology and implication for spontaneous contractility, Am. J. Physiol. Heart Circ. Physiol., 295, H1989, 10.1152/ajpheart.00007.2008 · DOI
  103. Wang, 2016, Local coupling of TRPC6 to ANO1/TMEM16A channels in smooth muscle cells amplifies vasoconstriction in cerebral arteries, Am. J. Physiol. Cell Physiol., 310, C1001, 10.1152/ajpcell.00092.2016 · DOI
  104. Warthi, 2022, Generation and comparative analysis of an Itga8-CreER (T2) mouse with preferential activity in vascular smooth muscle cells, Nat. Cardiovasc. Res., 1, 1084, 10.1038/s44161-022-00162-1 · DOI
  105. Wirth, 2008, G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension, Nat. Med., 14, 64, 10.1038/nm1666 · DOI
  106. Wu, 2006, Contractile activity of lymphatic vessels is altered in the TNBS model of Guinea pig ileitis, Am. J. Physiol. Gastrointest. Liver Physiol., 291, G566, 10.1152/ajpgi.00058.2006 · DOI
  107. Xin, 2002, Smooth muscle expression of Cre recombinase and eGFP in transgenic mice, Physiol Genomics, 3, 211, 10.1152/physiolgenomics.00054.2002 · DOI
  108. Yang, 2008, TMEM16A confers receptor-activated calcium-dependent chloride conductance, Nature, 455, 1210, 10.1038/nature07313 · DOI
  109. Yaniv, 2015, From two competing oscillators to one coupled-clock pacemaker cell system, Front. Physiol., 6, 28, 10.3389/fphys.2015.00028 · DOI
  110. Yu, 2019, A network of phosphatidylinositol 4,5-bisphosphate binding sites regulates gating of the Ca2+-activated Cl− channel ANO1 (TMEM16A), Proc. Natl. Acad. Sci. USA, 116, 19952, 10.1073/pnas.1904012116 · DOI
  111. Zawieja, 2009, Contractile physiology of lymphatics, Lymphat. Res. Biol., 7, 87, 10.1089/lrb.2009.0007 · DOI
  112. Zawieja, 1993, Distribution, propagation, and coordination of contractile activity in lymphatics, Am. J. Physiol., 264, H1283, 10.1152/ajpheart.1993.264.4.H1283 · DOI
  113. Zawieja, 2019, Ano1 mediates pressure-sensitive contraction frequency changes in mouse lymphatic collecting vessels, J. Gen. Physiol., 151, 532, 10.1085/jgp.201812294 · DOI · Paper page
  114. Zawieja, 2018, 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., 314, H991, 10.1152/ajpheart.00499.2017 · DOI · Paper page
  115. Zawieja, 2012, Impairments in the intrinsic contractility of mesenteric collecting lymphatics in a rat model of metabolic syndrome, Am. J. Physiol. Heart Circ. Physiol., 302, H643, 10.1152/ajpheart.00606.2011 · DOI
  116. Zhang, 2020, Distinct pharmacological profiles of ORAI1, ORAI2, and ORAI3 channels, Cell Calcium, 91, 102281, 10.1016/j.ceca.2020.102281 · DOI
  117. Zhao, 2003, ET-1-associated vasomotion and vasospasm in lymphatic vessels of the Guinea-pig mesentery, Br. J. Pharmacol., 140, 1399, 10.1038/sj.bjp.0705573 · DOI
  118. Zheng, 2014, Expression and function of a T-type Ca2+ conductance in interstitial cells of Cajal of the murine small intestine, Am. J. Physiol. Cell Physiol., 306, C705, 10.1152/ajpcell.00390.2013 · DOI
  119. Zhu, 2016, Na+-K+-Cl− cotransporter (NKCC) maintains the chloride gradient to sustain pacemaker activity in interstitial cells of Cajal, Am. J. Physiol. Gastrointest. Liver Physiol., 311, G1037, 10.1152/ajpgi.00277.2016 · DOI
  120. Zhu, 2015, Intracellular Ca(2+) release from endoplasmic reticulum regulates slow wave currents and pacemaker activity of interstitial cells of Cajal, Am. J. Physiol. Cell Physiol., 308, C608, 10.1152/ajpcell.00360.2014 · DOI

Cited by

Sorted by citations

Metadata

Authors
Zawieja, S. D., Pea, G. A., Broyhill, S. E., Patro, A., Bromert, K. H., Li, M., Norton, C. E., Castorena-Gonzalez, J. A., Hancock, E. J., Bertram, C. D., & Davis, M. J.
Affiliations
  • University of Missouri (US)
  • Tulane University 2 Department of Pharmacology, , New Orleans, LA, USA
  • The University of Sydney (AU)
Corresponding author
  • Zawieja, Scott D.
  • Davis, Michael J.
ORCID
Venue
Journal of General Physiology
Publisher
Rockefeller University Press
Published
2023-10-18
Volume
155
Issue
12
ISSN
  • 0022-1295 (ISSN-L)
  • 1540-7748
DOI
10.1085/jgp.202313358
PMC
PMC10585095
OpenAlex
W4387728349
Cited by
22
References
0
Citations by year
2026: 3 · 2025: 9 · 2024: 7 · 2023: 3
FWCI
2.68
Type
journal article
Language
en
Open access
Licence
Locations
  • The Journal of General Physiology (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
National Institutes of Health (HL-125608, HL-122578, HL-143198, HL-141143, HL-168568, CDA-931652)
Topics
  • Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Keywords
IP3R1, TMEM16A, collecting lymphatic vessels, diastolic depolarization, calcium transients, contractile regulation, lymphatic vessel contraction
MeSH terms
Anoctamin-1, Animals, Calcium, Diastole, Lymphatic Vessels, Mice, Inositol 1,4,5-Trisphosphate Receptors

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review