Skip to main content Accessibility help
×
Home
Hostname: page-component-59b7f5684b-vh8gq Total loading time: 0.391 Render date: 2022-09-27T22:06:09.679Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "displayNetworkTab": true, "displayNetworkMapGraph": false, "useSa": true } hasContentIssue true

Dynamics of Calcium Signal and Leukotriene C4 Release in Mast Cells Network Induced by Mechanical Stimuli and Modulated by Interstitial Fluid Flow

Published online by Cambridge University Press:  21 December 2015

Wei Yao
Affiliation:
Shanghai Key Laboratory of Acupuncture Mechanism and Acupoint Function, Department of Mechanics and Engineering Science, Fudan University, 220 Handan Road, Shanghai 200433, China
Hongwei Yang
Affiliation:
Shanghai Key Laboratory of Acupuncture Mechanism and Acupoint Function, Department of Mechanics and Engineering Science, Fudan University, 220 Handan Road, Shanghai 200433, China
Yabei Li
Affiliation:
Shanghai Key Laboratory of Acupuncture Mechanism and Acupoint Function, Department of Mechanics and Engineering Science, Fudan University, 220 Handan Road, Shanghai 200433, China
Guanghong Ding*
Affiliation:
Shanghai Key Laboratory of Acupuncture Mechanism and Acupoint Function, Department of Mechanics and Engineering Science, Fudan University, 220 Handan Road, Shanghai 200433, China
*
*Corresponding author. Email:weiyao@fudan.edu.cn (W. Yao), 14110290011@fudan.edu.cn (H. W. Yang), 11210290026@fudan.edu.cn (Y. B. Li), m13564899598@163.com (G. H. Ding)
Get access

Abstract

Mast cells (MCs) play an important role in the immune system. Through connective tissues, mechanical stimuli activate intracellular calcium signaling pathways, induce a variety of mediators including leukotriene C4 (LTC4) release, and affect MCs’ microenvironment. This paper focuses on MCs’ intracellular calcium dynamics and LTC4 release responding to mechanical stimuli, explores signaling pathways in MCs and the effect of interstitial fluid flow on the transport of biological messengers and feedback in the MCs network. We use a mathematical model to show that (i) mechanical stimuli including shear stress induced by interstitial fluid flow can activate mechano-sensitive (MS) ion channels on MCs’ membrane and allow Ca2+ entry, which increases intracellular Ca2+ concentration and leads to LTC4 release; (ii) LTC4 in the extracellular space (ECS) acts on surface cysteinyl leukotriene receptors (LTC4R) on adjacent cells, leading to Ca2+ influx through Ca2+ release-activated Ca2+ (CRAC) channels. An elevated intracellular Ca2+ concentration further stimulates LTC4 release and creates a positive feedback in the MCs network. The findings of this study may facilitate our understanding of the mechanotransduction process in MCs induced by mechanical stimuli, contribute to understanding of interstitial flow-related mechanobiology in MCs network, and provide a methodology for quantitatively analyzing physical treatment methods including acupuncture and massage in traditional Chinese medicine (TCM).

Type
Research Article
Copyright
Copyright © Global-Science Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

[1]Capite, J. D. and Parekh, A. B., CRAC channels and Ca2+ signaling in mast cells, Immunolog. Rev., 231 (2009), pp. 4558.CrossRefGoogle ScholarPubMed
[2]Weber, A., Knop, J. and Maurer, M., Pattern analysis of human cutaneous mast cell populations by total body surface mapping, British J. Dermatology, 148 (2003), pp. 224228.CrossRefGoogle ScholarPubMed
[3]Yao, W. and Ding, G. H., Interstitial fluid flow: simulation of mechanical environment of cells in the interosseous membrane, Acta Mech. Sinica, 27 (2011), pp. 602610.CrossRefGoogle Scholar
[4]Zhang, D., Ding, G. H., Shen, X. Y., Yao, W., Zhang, Z. Y., Zhang, Y. Q., Lin, J. and Gu, Q. B., Role of mast cells in acupuncture effect: a pilot study, Explore J. Sci. Heal., 4 (2008), pp. 170177.Google ScholarPubMed
[5]Wang, L. N., Ding, G. H., Gu, Q. B. and Schwarz, W., Single-channel properties of a stretch-sensitive chloride channel in the human mast cell line HMC-1, Euro. Biophys. J., 39 (2010), pp. 757767.CrossRefGoogle ScholarPubMed
[6]Yang, W. Z., Chen, J. Y. and Zhou, L. W., Effects of shear stress on intracellular calcium change and histamine release in rat basophilic leukemia (RBL-2H3) cells, J. Environmental Pathology Oncology, 28 (2009), pp. 223230.CrossRefGoogle ScholarPubMed
[7]Zhang, D., Spielmann, A., Ding, G. H. and Schwarz, W., Activation of mast-cell degranulation by different physical stimuli involves activation of the transient-receptor-potential channel TRPV2, Physiolog. Res., 61 (2012), pp. 113124.Google ScholarPubMed
[8]Turner, H., Del Carmen, K. A. and Stokes, A., Link between TRPV channels and mast cell function, Handb Exp. Pharmacol., 179 (2007), pp. 457471.CrossRefGoogle Scholar
[9]Kuehn, H. S. and Gilfillan, A. M., G protein-coupled receptors and the modification of FcRI-mediated mast cell activation, Immunology Lett., 113 (2007), pp. 5969.CrossRefGoogle Scholar
[10]Dicapite, J. L., Shirley, A., Nelson, C., Bates, G. and Parekh, A. B., Intercellular calcium wave propagation involving positive feedback between CRAC channels and cysteinyl leukotrienes, FASEB J., 23 (2009), pp. 894905.CrossRefGoogle Scholar
[11]Yao, W., Huang, H. and Miura, R. M., A continuum neuronal model for the instigation and propagation of cortical spreading depression, Bull. Math. Biol., 73 (2011), pp. 27732790.CrossRefGoogle ScholarPubMed
[12]Bennett, M. R., Farnell, L. and Gibson, W. G., A quantitative model of purinergicjunctional transmission of calcium waves in astrocyte networks, Biophys. J., 89 (2005), pp. 22352250.CrossRefGoogle ScholarPubMed
[13]Huang, H., Miura, R. M. and Yao, W., A simplified neuronal model for the instigation and propagation of cortical spreading depression, Adv. Appl. Math. Mech., 3 (2011), pp. 759773.CrossRefGoogle Scholar
[14]Li, H. Y., Chen, M. and Yang, J. F., Fluid flow along venous adventitia in rabbits: is it a potential drainage system complementary to vascular circulations?, Plos. One, 7 (2012), e41395. doi: 10.1371 /journal.pone.0041395.Google ScholarPubMed
[15]Yao, W., Li, Y. B. and Ding, G. H., Interstitial fluid flow: the mechanical environment of cells and foundation of meridians, Evidence-Based Complementary and Alternative Medicine, (2012), Article ID 853516, 9 pages doi:10.1155/2012/853516.CrossRefGoogle Scholar
[16]Boyce, J. A., Mast cells and eicosanoid mediators:a system of reciprocal paracrine and autocrine regulation, Immunol Rev., 217 (2007), pp. 168185.CrossRefGoogle ScholarPubMed
[17]Yao, W., Huang, H. X. and Ding, G. H., A dynamic model of calcium signaling in mast cells and LTC4 release induced by mechanical stimuli, China Sci. Bull., 59 (2013), pp. 956963.CrossRefGoogle Scholar
[18]Koch, C. and Segev, I., Methods in Neuronal Modeling: From Ions to Networks, Cambridge: MIT Press, 1998.Google Scholar
[19]Su, J. H., Xu, F., Lu, X. L. and Lu, T. J., Fluid flow induced calcium response in osteoblasts: mathematical modeling, J. Biomech., 44 (2011), pp. 20402046.CrossRefGoogle ScholarPubMed
[20]Youma, Y. B., Hana, J., KIMA, N., Zhang, Y. H., Kim, E., Joo, H., Leem, H. C. H., Kim, S. J., Cha, K. A. and Earm, Y. E., Role of stretch-activated channels on the stretch-induced changes of rat atrial myocytes, Prog. Biophys. Molecular Biology, 90 (2006), pp. 186206.CrossRefGoogle Scholar
[21]Silva, H. S., Kapela, A. and Tsoukias, N. M., A mathematical model of plasma membrane electro physiology and calcium dynamics in vascularendothelial cells, Am. J. PhysiologyCell Physiology, 293 (2007), pp. 277293.CrossRefGoogle Scholar
[22]Fink, C. F., Slepchenko, B. and Loew, L. M., Determination of time-dependent inositol-1,4,5-trisphosphate concentrations during calcium release in a smooth muscle cell, Biophys. J., 77 (1999), pp. 617628.CrossRefGoogle ScholarPubMed
[23]Bennett, M. R., Farnell, L. and Gibson, W. G., A quantitative model of cortical spreading depression due to purinergic and gap-junction transmission in astrocyte networks, Biophys. J., 95 (2008), pp. 56485660.CrossRefGoogle ScholarPubMed
[24]Lemon, G., Gibson, W. G. and Bennett, M. R., Metabotropic receptor activation, desensitization and sequestration-I: modelling calcium and inositol 1,4,5-trisphosphate dynamics following receptor activation, J. Theor. Biol., 223 (2003), pp. 93111.CrossRefGoogle ScholarPubMed
[25]Shi, X. M., Zheng, Y. F. and Liu, Z. R., A model of calcium signaling and degranulation dynamics induced by laser irradiation in mast cells, China Sci. Bull., 53 (2008), pp. 23152325.Google Scholar
[26]Chang, W. C., Nelson, C. and Parekh, A. B., Ca2+ influx through CRAC channels activates cytosolic phospholipase A2, leukotriene C4 secretion and expression of c-fos through ERK-dependent and independent pathways in mast cells, FASEB J., 20 (2006), pp. 23812383.CrossRefGoogle ScholarPubMed
[27]Chang, W. C. and Parekh, A. B., Close functional coupling between Ca2+ release-activated Ca2+ channels, arachidonic acid release, and leukotriene C4 secretion, J. Biol. Chem., 279 (2004), pp. 2999429999.CrossRefGoogle ScholarPubMed
[28]Mazel, T., Raymond, R., Raymond-Stintz, M., Jett, S., Wilson, B. S. and Bridget, B., Stochastic modeling of calcium in 3D geometry, Biophys. J., 96 (2009), pp. 16911706.CrossRefGoogle ScholarPubMed
[29]Chang, W. C., Capite, J. D., Nelson, C. and and Parekh, A. B., All-or-none activation of CRAC channels by agonist elicits graded responses in populations of mast cells, J. Immunol., 179 (2007), pp. 52555263.CrossRefGoogle ScholarPubMed
[30]Stokes, A. J., Shimoda, L. M., Koblan-Huberson, M., Adra, C. N. and Turner, H., A TRPV2-PKA signaling module for transduction of physical stimuli in mast cells, J. Exp. Med., 200 (2004), pp. 137147.CrossRefGoogle ScholarPubMed
[31]Langevin, H. M., Churchill, D. L., Fox, J. R., Badger, G. J., Garra, B. S. and Krag, M. H., Biomechanical response to acupuncture needling in humans, J. Appl. Physiol., 91 (2001), pp. 24712478.CrossRefGoogle ScholarPubMed
[32]Yu, X. J., Ding, G. H., Huang, H., Lin, J., Yao, W. and Zhan, R., Role of collagen fibers in acupuncture analgesia therapy on rats, Connective Tissue Research, 50 (2009), pp. 110120.CrossRefGoogle ScholarPubMed
5
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Dynamics of Calcium Signal and Leukotriene C4 Release in Mast Cells Network Induced by Mechanical Stimuli and Modulated by Interstitial Fluid Flow
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Dynamics of Calcium Signal and Leukotriene C4 Release in Mast Cells Network Induced by Mechanical Stimuli and Modulated by Interstitial Fluid Flow
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Dynamics of Calcium Signal and Leukotriene C4 Release in Mast Cells Network Induced by Mechanical Stimuli and Modulated by Interstitial Fluid Flow
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *