Cardiovascular Toxicology

, Volume 19, Issue 3, pp 198–209 | Cite as

Combustion Particle-Induced Changes in Calcium Homeostasis: A Contributing Factor to Vascular Disease?

  • Jørn A. HolmeEmail author
  • Bendik C. Brinchmann
  • Eric Le Ferrec
  • Dominique Lagadic-Gossmann
  • Johan ØvrevikEmail author


Air pollution is the leading environmental risk factor for disease and premature death in the world. This is mainly due to exposure to urban air particle matter (PM), in particular, fine and ultrafine combustion-derived particles (CDP) from traffic-related air pollution. PM and CDP, including particles from diesel exhaust (DEP), and cigarette smoke have been linked to various cardiovascular diseases (CVDs) including atherosclerosis, but the underlying cellular mechanisms remain unclear. Moreover, CDP typically consist of carbon cores with a complex mixture of organic chemicals such as polycyclic aromatic hydrocarbons (PAHs) adhered. The relative contribution of the carbon core and adhered soluble components to cardiovascular effects of CDP is still a matter of discussion. In the present review, we summarize evidence showing that CDP affects intracellular calcium regulation, and argue that CDP-induced impairment of normal calcium control may be a critical cellular event through which CDP exposure contributes to development or exacerbation of cardiovascular disease. Furthermore, we highlight in vitro research suggesting that adhered organic chemicals such as PAHs may be key drivers of these responses. CDP, extractable organic material from CDP (CDP-EOM), and PAHs may increase intracellular calcium levels by interacting with calcium channels like transient receptor potential (TRP) channels, and receptors such as G protein-coupled receptors (GPCR; e.g., beta-adrenergic receptors [βAR] and protease-activated receptor 2 [PAR-2]) and the aryl hydrocarbon receptor (AhR). Clarifying a possible role of calcium signaling and mechanisms involved may increase our understanding of how air pollution contributes to CVD.


Diesel exhaust particles Polycyclic aromatic hydrocarbons Endothelial dysfunction Aryl hydrocarbon receptor Calcium signaling 



Adrenergic receptors


Aryl hydrocarbon receptor


AhR nuclear translocator




Cardiovascular diseases


Combustion-derived particles


Cytochrome P450


Cytosolic concentration of calcium


Diesel exhaust particles


Extractable organic material of DEP


G protein-coupled receptors


Matrix metalloproteinases


Nuclear factor-κB




Organic chemicals


Oxidized low-density lipoproteins


Particular matter


Polycyclic aromatic hydrocarbons


Protease-activated receptor 2


Reactive oxygen species


Receptor-operated calcium entry


Receptor tyrosine kinases


Transient receptor potential


Store-operated calcium entry


Xenobiotic response elements


Author Contributions

JAH and BCB drafted the first version of the manuscript and wrote the final version in collaboration with ELF, DLG, and JØ. All authors read, commented, and approved the final manuscript.


The work was supported by the Research Council of Norway, through the Environmental Exposures and Health Outcomes- and Better Health programs (Grants No. 228143 and 260381).

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interests.


  1. 1.
    WHO. (2016). Ambient air pollution: A global assesment of exposure and burden of disease. Geneva: World Health Organization.Google Scholar
  2. 2.
    Siponen, T., Yli-Tuomi, T., Aurela, M., Dufva, H., Hillamo, R., Hirvonen, M. R., et al. (2015). Source-specific fine particulate air pollution and systemic inflammation in ischaemic heart disease patients. Occupational and Environmental Medicine, 72(4), 277–283.CrossRefPubMedGoogle Scholar
  3. 3.
    Schneider, A., Neas, L. M., Graff, D. W., Herbst, M. C., Cascio, W. E., Schmitt, M. T., et al. (2010). Association of cardiac and vascular changes with ambient PM2.5 in diabetic individuals. Particle and Fibre Toxicology, 7, 14.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Pope, C. A., Bhatnagar, A., McCracken, J. P., Abplanalp, W., Conklin, D. J., & O’Toole, T. (2016). Exposure to fine particulate air pollution is associated with endothelial injury and systemic inflammation. Circulation Research, 119(11), 1204–1214.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Fariss, M. W., Gilmour, M. I., Reilly, C. A., Liedtke, W., & Ghio, A. J. (2013). Emerging mechanistic targets in lung injury induced by combustion-generated particles. Toxicological Science, 132(2), 253–267.CrossRefGoogle Scholar
  6. 6.
    Cassee, F. R., Heroux, M. E., Gerlofs-Nijland, M. E., & Kelly, F. J. (2013). Particulate matter beyond mass: Recent health evidence on the role of fractions, chemical constituents and sources of emission. Inhalation Toxicology, 25(14), 802–812.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Lewtas, J. (2007). Air pollution combustion emissions: Characterization of causative agents and mechanisms associated with cancer, reproductive, and cardiovascular effects. Mutation Research, 636(1–3), 95–133.CrossRefPubMedGoogle Scholar
  8. 8.
    Kawasaki, S., Takizawa, H., Takami, K., Desaki, M., Okazaki, H., Kasama, T., et al. (2001). Benzene-extracted components are important for the major activity of diesel exhaust particles. American Journal of Respiratory Cell and Molecular Biology, 24, 419–426.CrossRefPubMedGoogle Scholar
  9. 9.
    Bonvallot, V., Baeza-Squiban, A., Baulig, A., Brulant, S., Boland, S., Muzeau, F., et al. (2001). Organic compounds from diesel exhaust particles elicit a proinflammatory response in human airway epithelial cells and induce cytochrome p450 1A1 expression. American Journal of Respiratory Cell and Molecular Biology, 25, 515–521.CrossRefPubMedGoogle Scholar
  10. 10.
    Totlandsdal, A. I., Herseth, J. I., Bolling, A. K., Kubatova, A., Braun, A., Cochran, R. E., et al. (2012). Differential effects of the particle core and organic extract of diesel exhaust particles. Toxicology Letters, 208(3), 262–268.CrossRefPubMedGoogle Scholar
  11. 11.
    Ma, J. Y., & Ma, J. K. (2002). The dual effect of the particulate and organic components of diesel exhaust particles on the alteration of pulmonary immune/inflammatory responses and metabolic enzymes. Journal of Environmental Science Health Part C, 20(2), 117–147.CrossRefGoogle Scholar
  12. 12.
    Keebaugh, A. J., Sioutas, C., Pakbin, P., Schauer, J. J., Mendez, L. B., & Kleinman, M. T. (2015). Is atherosclerotic disease associated with organic components of ambient fine particles? Science Total Environment, 533, 69–75.CrossRefGoogle Scholar
  13. 13.
    Brinchmann, B. C., Le Ferrec, E., Podechard, N., Lagadic-Gossmann, D., Shoji, K. F., Penna, A., et al. (2018). Lipophilic chemicals from diesel exhaust particles trigger calcium response in human endothelial cells via aryl hydrocarbon receptor non-genomic signalling. International Journal of Molecular Science, 19(5), 1429.CrossRefGoogle Scholar
  14. 14.
    Shapiro, D., Deering-Rice, C. E., Romero, E. G., Hughen, R. W., Light, A. R., Veranth, J. M., et al. (2013). Activation of transient receptor potential ankyrin-1 (TRPA1) in lung cells by wood smoke particulate material. Chemical Research in Toxicology, 26(5), 750–758.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Mayati, A., Le Ferrec, E., Lagadic-Gossmann, D., & Fardel, O. (2012). Aryl hydrocarbon receptor-independent up-regulation of intracellular calcium concentration by environmental polycyclic aromatic hydrocarbons in human endothelial HMEC-1 cells. Environmental Toxicology, 27(9), 556–562.CrossRefPubMedGoogle Scholar
  16. 16.
    McLaren, J. E., Michael, D. R., Ashlin, T. G., & Ramji, D. P. (2011). Cytokines, macrophage lipid metabolism and foam cells: Implications for cardiovascular disease therapy. Progress in Lipid Research, 50(4), 331–347.CrossRefPubMedGoogle Scholar
  17. 17.
    Ramji, D. P., & Davies, T. S. (2015). Cytokines in atherosclerosis: Key players in all stages of disease and promising therapeutic targets. Cytokine & Growth Factor Reviews, 26(6), 673–685.CrossRefGoogle Scholar
  18. 18.
    Donaldson, K., Stone, V., Borm, P. J. A., Jimenez, L. A., Gilmour, P. S., Schins, R. P. F., et al. (2003). Oxidative stress and calcium signaling in the adverse effects of environmental particles (PM10). Free Radical Biology & Medicine, 34(11), 1369–1382.CrossRefGoogle Scholar
  19. 19.
    Donaldson, K., Stone, V., Seaton, A., & MacNee, W. (2001). Ambient particle inhalation and the cardiovascular system: Potential mechanisms. Environmental Health Perspectives, 109, 523–527.PubMedPubMedCentralGoogle Scholar
  20. 20.
    de Kok, T. M., Driece, H. A., Hogervorst, J. G., & Briede, J. J. (2006). Toxicological assessment of ambient and traffic-related particulate matter: A review of recent studies. Mutation Research, 613(2–3), 103–122.CrossRefPubMedGoogle Scholar
  21. 21.
    Maier, K. L., Alessandrini, F., Beck-Speier, I., Hofer, T. P., Diabate, S., Bitterle, E., et al. (2008). Health effects of ambient particulate matter–biological mechanisms and inflammatory responses to in vitro and in vivo particle exposures. Inhalation Toxicology, 20(3), 319–337.CrossRefPubMedGoogle Scholar
  22. 22.
    Li, N., Hao, M., Phalen, R. F., Hinds, W. C., & Nel, A. E. (2003). Particulate air pollutants and asthma A paradigm for the role of oxidative stress in PM-induced adverse health effects. Clinical Immunology, 109, 250–265.CrossRefPubMedGoogle Scholar
  23. 23.
    Sauer, H., Wartenberg, M., & Hescheler, J. (2001). Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cellular Physiology and Biochemistry, 11, 173–186.CrossRefPubMedGoogle Scholar
  24. 24.
    Ovrevik, J., Refsnes, M., Lag, M., Holme, J. A., & Schwarze, P. E. (2015). Activation of proinflammatory responses in cells of the airway mucosa by particulate matter: Oxidant- and non-oxidant-mediated triggering mechanisms. Biomolecules, 5(3), 1399–1440.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Vogel, C. F. A., Sciullo, E., Wong, P., Kuzmicky, P., Kado, N., & Matsumura, F. (2005). Induction of proinflammatory cytokines and C-Reactive protein in human macrophage cell line U937 exposed to air pollution particulates. Environmental Health Perspectives, 113(11), 1536–1541.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Mills, N. L., Tornqvist, H., Gonzalez, M. C., Vink, E., Robinson, S. D., Soderberg, S., et al. (2007). Ischemic and thrombotic effects of dilute diesel-exhaust inhalation in men with coronary heart disease. The New England journal of medicine, 357(11), 1075–1082.CrossRefPubMedGoogle Scholar
  27. 27.
    Mills, N. L., Tornqvist, H., Robinson, S. D., Gonzalez, M., Darnley, K., MacNee, W., et al. (2005). Diesel exhaust inhalation causes vascular dysfunction and impaired endogenous fibrinolysis. Circulation, 112(25), 3930–3936.CrossRefPubMedGoogle Scholar
  28. 28.
    Lucking, A. J., Lundback, M., Mills, N. L., Faratian, D., Barath, S. L., Pourazar, J., et al. (2008). Diesel exhaust inhalation increases thrombus formation in man. European Heart Journal, 29(24), 3043–3051.CrossRefPubMedGoogle Scholar
  29. 29.
    Araujo, J. A., & Nel, A. E. (2009). Particulate matter and atherosclerosis: Role of particle size, composition and oxidative stress. Particle and Fibre Toxicology, 6, 24.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Cohen, A. J., Brauer, M., Burnett, R., Anderson, H. R., Frostad, J., Estep, K., et al. (2017). Estimates and 25-year trends of the global burden of disease attributable to ambient air pollution: An analysis of data from the Global Burden of Diseases Study 2015. The Lancet, 389(10082), 1907–1918.CrossRefGoogle Scholar
  31. 31.
    Brook, R. D., Rajagopalan, S., Pope, C. A., 3rd, Brook, J. R., Bhatnagar, A., Diez-Roux, A. V., et al. (2010). Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation, 121(21), 2331–2378.CrossRefPubMedGoogle Scholar
  32. 32.
    Perez, C. M., Hazari, M. S., & Farraj, A. K. (2015). Role of autonomic reflex arcs in cardiovascular responses to air pollution exposure. Cardiovascular Toxicology, 15(1), 69–78.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Carll, A. P., Hazari, M. S., Perez, C. M., Krantz, Q. T., King, C. J., Winsett, D. W., et al. (2012). Whole and particle-free diesel exhausts differentially affect cardiac electrophysiology, blood pressure, and autonomic balance in heart failure-prone rats. Toxicological Sciences, 128(2), 490–499.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Kodavanti, U. P. (2016). Stretching the stress boundary: Linking air pollution health effects to a neurohormonal stress response. Biochimica et Biophysica Acta, 1860(12), 2880–2890.CrossRefPubMedGoogle Scholar
  35. 35.
    Hazari, M. S., Haykal-Coates, N., Winsett, D. W., Krantz, Q. T., King, C., Costa, D. L., et al. (2011). TRPA1 and sympathetic activation contribute to increased risk of triggered cardiac arrhythmias in hypertensive rats exposed to diesel exhaust. Environmental Health Perspectives, 119(7), 951–957.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Araujo, J. A., Barajas, B., Kleinman, M., Wang, X., Bennett, B. J., Gong, K. W., et al. (2008). Ambient particulate pollutants in the ultrafine range promote early atherosclerosis and systemic oxidative stress. Circulation Research, 102(5), 589–596.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Borm, P. J., Robbins, D., Haubold, S., Kuhlbusch, T., Fissan, H., Donaldson, K., et al. (2006). The potential risks of nanomaterials: A review carried out for ECETOC. Particle and Fibre Toxicology, 3, 11.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Miller, M. R., Raftis, J. B., Langrish, J. P., McLean, S. G., Samutrtai, P., Connell, S. P., et al. (2017). Inhaled Nanoparticles accumulate at sites of vascular disease. ACS Nano, 11(5), 4542–4552.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Miller, M. R., Raftis, J. B., Langrish, J. P., McLean, S. G., Samutrtai, P., Connell, S. P., et al. (2017). Correction to”Inhaled nanoparticles accumulate at sites of vascular disease”. ACS Nano, 11(10), 10623–10624.CrossRefPubMedGoogle Scholar
  40. 40.
    Penn, A., Murphy, G., Barker, S., Henk, W., & Penn, L. (2005). Combustion-derived ultrafine particles transport organic toxicants to target respiratory cells. Environmental Health Perspectives, 113(8), 956–963.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Gerde, P., Muggenburg, B. A., Lundborg, M., & Dahl, A. R. (2001). The rapid alveolar absorption of diesel soot-adsorbed benzo[a]pyrene: Bioavailability, metabolism and dosimetry of an inhaled particle-borne carcinogen. Carcinogenesis, 22(5), 741–749.CrossRefPubMedGoogle Scholar
  42. 42.
    Bostrom, C. E., Gerde, P., Hanberg, A., Jernstrom, B., Johansson, C., Kyrklund, T., et al. (2002). Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environmental Health Perspectives, 110(Suppl 3), 451–488.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Zhang, Y. J., Weksler, B. B., Wang, L., Schwartz, J., & Santella, R. M. (1998). Immunohistochemical detection of polycyclic aromatic hydrocarbon-DNA damage in human blood vessels of smokers and non-smokers. Atherosclerosis, 140(2), 325–331.CrossRefPubMedGoogle Scholar
  44. 44.
    Korashy, H. M., & El-Kadi, A. O. S. (2008). The role of aryl hydrocarbon receptor in the pathogenesis of cardiovascular diseases. Drug Metabolism Reviews, 38(3), 411–450.CrossRefGoogle Scholar
  45. 45.
    Brinchmann, B. C., Skuland, T., Rambol, M. H., Szoke, K., Brinchmann, J. E., Gutleb, A. C., et al. (2018). Lipophilic components of diesel exhaust particles induce pro-inflammatory responses in human endothelial cells through AhR dependent pathway(s). Particle and Fibre Toxicology, 15(1), 21.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Klein, S. G., Cambier, S., Hennen, J., Legay, S., Serchi, T., Nelissen, I., et al. (2017). Endothelial responses of the alveolar barrier in vitro in a dose-controlled exposure to diesel exhaust particulate matter. Particle and Fibre Toxicology, 14(1), 7.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Forchhammer, L., Loft, S., Roursgaard, M., Cao, Y., Riddervold, I. S., Sigsgaard, T., et al. (2012). Expression of adhesion molecules, monocyte interactions and oxidative stress in human endothelial cells exposed to wood smoke and diesel exhaust particulate matter. Toxicology Letters, 209(2), 121–128.CrossRefPubMedGoogle Scholar
  48. 48.
    Lawal, A. O., Zhang, M., Dittmar, M., Lulla, A., & Araujo, J. A. (2015). Heme oxygenase-1 protects endothelial cells from the toxicity of air pollutant chemicals. Toxicology and Applied Pharmacology, 284(3), 281–291.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Cao, Y., Long, J., Ji, Y., Chen, G., Shen, Y., Gong, Y., et al. (2016). Foam cell formation by particulate matter (PM) exposure: A review. Inhalation Toxicology, 28(13), 583–590.CrossRefPubMedGoogle Scholar
  50. 50.
    Krishnan, R. M., Adar, S. D., Szpiro, A. A., Jorgensen, N. W., Van Hee, V. C., Barr, R. G., et al. (2012). Vascular responses to long- and short-term exposure to fine particulate matter: MESA Air (Multi-Ethnic Study of Atherosclerosis and Air Pollution). Journal of the American College of Cardiology, 60(21), 2158–2166.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Van Eeden, S., Leipsic, J., Paul Man, S. F., & Sin, D. D. (2012). The relationship between lung inflammation and cardiovascular disease. American Journal of Respiratory and Critical Care Medicine, 186(1), 11–16.CrossRefPubMedGoogle Scholar
  52. 52.
    Brauner, E. V., Forchhammer, L., Moller, P., Simonsen, J., Glasius, M., Wahlin, P., et al. (2007). Exposure to ultrafine particles from ambient air and oxidative stress-induced DNA damage. Environmental Health Perspectives, 115(8), 1177–1182.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Sorensen, M., Daneshvar, B., Hansen, M., Dragsted, L. O., Hertel, O., Knudsen, L., et al. (2003). Personal PM2.5 exposure and markers of oxidative stress in blood. Environmental Health Perspectives, 111(2), 161–166.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Moller, P., Christophersen, D. V., Jacobsen, N. R., Skovmand, A., Gouveia, A. C., Andersen, M. H., et al. (2016). Atherosclerosis and vasomotor dysfunction in arteries of animals after exposure to combustion-derived particulate matter or nanomaterials. Critical Reviews in Toxicology, 46(5), 437–476.CrossRefPubMedGoogle Scholar
  55. 55.
    Clapham, D. E. (2007). Calcium signaling. Cell, 131(6), 1047–1058.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Conway, J. D., Bartolotta, T., Abdullah, L. H., & Davis, C. W. (2003). Regulation of mucin secretion from human bronchial epithelial cells grown in murine hosted xenografts. American Journal of Physiology. Lung Cellular and Molecular Physiology, 284(6), L945–954.CrossRefPubMedGoogle Scholar
  57. 57.
    Haller, T., Ortmayr, J., Friedrich, F., Volkl, H., & Dietl, P. (1998). Dynamics of surfactant release in alveolar type II cells. Proceedings of the National academy of Sciences of the United States of America, 95(4), 1579–1584.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Lansley, A. B., & Sanderson, M. J. (1999). Regulation of airway ciliary activity by Ca2+ : Simultaneous measurement of beat frequency and intracellular Ca2+. Biophysical Journal, 77(1), 629–638.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Racioppi, L., & Means, A. R. (2012). Calcium/calmodulin-dependent protein kinase kinase 2: Roles in signaling and pathophysiology. Journal of Biological Chemistry, 287(38), 31658–31665.CrossRefPubMedGoogle Scholar
  60. 60.
    Gorlach, A., Bertram, K., Hudecova, S., & Krizanova, O. (2015). Calcium and ROS: A mutual interplay. Redox Biology, 6, 260–271.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Yao, X., & Garland, C. J. (2005). Recent developments in vascular endothelial cell transient receptor potential channels. Circulation Research, 97(9), 853–863.CrossRefPubMedGoogle Scholar
  62. 62.
    Sandow, S. L., Senadheera, S., Grayson, T. H., Welsh, D. G., & Murphy, T. V. (2012). Calcium and endothelium-mediated vasodilator signaling. Advances in Experimental Medicine and Biology, 740, 811–831.CrossRefPubMedGoogle Scholar
  63. 63.
    Sandow, S. L., Haddock, R. E., Hill, C. E., Chadha, P. S., Kerr, P. M., Welsh, D. G., et al. (2009). What’s where and why at a vascular myoendothelial microdomain signalling complex. Clinical and Experimental Pharmacology and Physiology, 36(1), 67–76.CrossRefPubMedGoogle Scholar
  64. 64.
    Bagher, P., & Segal, S. S. (2011). Regulation of blood flow in the microcirculation: Role of conducted vasodilation. Acta physiologica (Oxford, England), 202(3), 271–284.CrossRefPubMedCentralGoogle Scholar
  65. 65.
    Straub, A. C., Zeigler, A. C., & Isakson, B. E. (2014). The myoendothelial junction: connections that deliver the message. Physiology (Bethesda), 29(4), 242–249.Google Scholar
  66. 66.
    Tiruppathi, C., Minshall, R. D., Paria, B. C., Vogel, S. M., & Malik, A. B. (2002). Role of Ca2 + signaling in the regulation of endothelial permeability. Vascular Pharmacology, 39(4–5), 173–185.CrossRefPubMedGoogle Scholar
  67. 67.
    Tiruppathi, C., Ahmmed, G. U., Vogel, S. M., & Malik, A. B. (2006). Ca2 + signaling, TRP channels, and endothelial permeability. Microcirculation, 13(8), 693–708.CrossRefPubMedGoogle Scholar
  68. 68.
    Barbado, M., Fablet, K., Ronjat, M., & De Waard, M. (2009). Gene regulation by voltage-dependent calcium channels. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1793(6), 1096–1104.CrossRefGoogle Scholar
  69. 69.
    Goswami, R., Merth, M., Sharma, S., Alharbi, M. O., Aranda-Espinoza, H., Zhu, X., et al. (2017). TRPV4 calcium-permeable channel is a novel regulator of oxidized LDL-induced macrophage foam cell formation. Free Radical Biology and Medicine, 110, 142–150.CrossRefPubMedGoogle Scholar
  70. 70.
    Mendes-Silverio, C. B., Alexandre, E. M., Lescano, C. H., Antunes, E., & Monica, F. Z. (2018). Mirabegron, a beta3-adrenoceptor agonist reduced platelet aggregation through cyclic adenosine monophosphate accumulation. European Journal of Pharmacology, 829, 79–84.CrossRefPubMedGoogle Scholar
  71. 71.
    Neri, T., Pergoli, L., Petrini, S., Gravendonk, L., Balia, C., Scalise, V., et al. (2016). Particulate matter induces prothrombotic microparticle shedding by human mononuclear and endothelial cells. Toxicology in Vitro, 32, 333–338.CrossRefPubMedGoogle Scholar
  72. 72.
    Ramsey, I. S., Delling, M., & Clapham, D. E. (2006). An introduction to TRP channels. Annual Review of Physiology, 68, 619–647.CrossRefPubMedGoogle Scholar
  73. 73.
    Caterina, M. J., & Julius, D. (2001). The vanilloid receptor: a molecular gateway to the pain pathway. Annual Review of Neuroscience, 24, 487–517.CrossRefPubMedGoogle Scholar
  74. 74.
    Chakraborty, S., & Hasan, G. (2012). IP3R, store-operated Ca2+ entry and neuronal Ca2+ homoeostasis in Drosophila. Biochemical Society Transactions, 40(1), 279–281.CrossRefPubMedGoogle Scholar
  75. 75.
    Liao, Y., Erxleben, C., Abramowitz, J., Flockerzi, V., Zhu, M. X., Armstrong, D. L., et al. (2008). Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels. Proceedings of the National academy of Sciences of the United States of America, 105(8), 2895–2900.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Ong, H. L., & Ambudkar, I. S. (2017). STIM-TRP Pathways and Microdomain Organization: Contribution of TRPC1 in Store-Operated Ca(2 +) Entry: Impact on Ca(2 +) Signaling and Cell Function. Advances in Experimental Medicine and Biology, 993, 159–188.CrossRefPubMedGoogle Scholar
  77. 77.
    Altier, C. (2012). GPCR and voltage-gated calcium channels (VGCC) signaling complexes. Sub-cellular Biochemistry, 63, 241–262.CrossRefPubMedGoogle Scholar
  78. 78.
    Zamponi, G. W. (2015). Calcium channel signaling complexes with receptors and channels. Current Molecular Pharmacology, 8(1), 8–11.CrossRefPubMedGoogle Scholar
  79. 79.
    Bylund, D. B., Eikenberg, D. C., Hieble, J. P., Langer, S. Z., Lefkowitz, R. J., Minneman, K. P., et al. (1994). International Union of Pharmacology nomenclature of adrenoceptors. Pharmacological Reviews, 46(2), 121–136.PubMedGoogle Scholar
  80. 80.
    Lowell, B. B., & Flier, J. S. (1997). Brown adipose tissue, beta 3-adrenergic receptors, and obesity. Annual Review of Medicine, 48, 307–316.CrossRefPubMedGoogle Scholar
  81. 81.
    Hirano, K. (2007). The roles of proteinase-activated receptors in the vascular physiology and pathophysiology. Arteriosclerosis, Thrombosis, and Vascular Biology, 27(1), 27–36.CrossRefPubMedGoogle Scholar
  82. 82.
    Alberelli, M. A., & De Candia, E. (2014). Functional role of protease activated receptors in vascular biology. Vascular Pharmacology, 62(2), 72–81.CrossRefPubMedGoogle Scholar
  83. 83.
    Esser, C., & Rannug, A. (2015). The aryl hydrocarbon receptor in barrier organ physiology, immunology, and toxicology. Pharmacological Reviews, 67(2), 259–279.CrossRefPubMedGoogle Scholar
  84. 84.
    Barouki, R., Aggerbeck, M., Aggerbeck, L., & Coumoul, X. (2012). The aryl hydrocarbon receptor system. Drug Metabolism and Drug Interactions, 27(1), 3–8.CrossRefPubMedGoogle Scholar
  85. 85.
    Tian, Y., Rabson, A. B., & Gallo, M. A. (2002). Ah receptor and NF-kappaB interactions: Mechanisms and physiological implications. Chemico-Biological Interactions, 141(1–2), 97–115.CrossRefPubMedGoogle Scholar
  86. 86.
    Vogel, C. F., & Matsumura, F. (2009). A new cross-talk between the aryl hydrocarbon receptor and RelB, a member of the NF-kappaB family. Biochemical Pharmacology, 77(4), 734–745.CrossRefPubMedGoogle Scholar
  87. 87.
    Denison, M. S., Soshilov, A. A., He, G., DeGroot, D. E., & Zhao, B. (2011). Exactly the same but different: Promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicological Sciences, 124(1), 1–22.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Guyot, E., Chevallier, A., Barouki, R., & Coumoul, X. (2013). The AhR twist: Ligand-dependent AhR signaling and pharmaco-toxicological implications. Drug Discovery Today, 18(9–10), 479–486.CrossRefPubMedGoogle Scholar
  89. 89.
    Matsumura, F. (2009). The significance of the nongenomic pathway in mediating inflammatory signaling of the dioxin-activated Ah receptor to cause toxic effects. Biochemical Pharmacology, 77(4), 608–626.CrossRefPubMedGoogle Scholar
  90. 90.
    Tomkiewicz, C., Herry, L., Bui, L. C., Metayer, C., Bourdeloux, M., Barouki, R., et al. (2013). The aryl hydrocarbon receptor regulates focal adhesion sites through a non-genomic FAK/Src pathway. Oncogene, 32(14), 1811–1820.CrossRefPubMedGoogle Scholar
  91. 91.
    N’Diaye, M., Le Ferrec, E., Lagadic-Gossmann, D., Corre, S., Gilot, D., Lecureur, V., et al. (2006). Aryl hydrocarbon receptor- and calcium-dependent induction of the chemokine CCL1 by the environmental contaminant benzo[a]pyrene. Journal of Biological Chemistry, 281(29), 19906–19915.CrossRefPubMedGoogle Scholar
  92. 92.
    Monteiro, P., Gilot, D., Le Ferrec, E., Rauch, C., Lagadic-Gossmann, D., & Fardel, O. (2008). Dioxin-mediated up-regulation of aryl hydrocarbon receptor target genes is dependent on the calcium/calmodulin/CaMKIalpha pathway. Molecular Pharmacology, 73(3), 769–777.CrossRefPubMedGoogle Scholar
  93. 93.
    Nicolson, G. L. (2014). The Fluid-Mosaic Model of Membrane Structure: Still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochimica et Biophysica Acta, 1838(6), 1451–1466.CrossRefPubMedGoogle Scholar
  94. 94.
    Bastiani, M., & Parton, R. G. (2010). Caveolae at a glance. Journal of Cell Science, 123(Pt 22), 3831–3836.CrossRefPubMedGoogle Scholar
  95. 95.
    van Deurs, B., Roepstorff, K., Hommelgaard, A. M., & Sandvig, K. (2003). Caveolae: Anchored, multifunctional platforms in the lipid ocean. Trends in Cell Biology, 13(2), 92–100.CrossRefPubMedGoogle Scholar
  96. 96.
    Santos, A. L., & Preta, G. (2018). Lipids in the cell: Organisation regulates function. Cellular and Molecular Life Sciences, 75, 1909–1927.CrossRefPubMedGoogle Scholar
  97. 97.
    Patel, H. H., Murray, F., & Insel, P. A. (2008). Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annual Review of Pharmacology and Toxicology, 48, 359–391.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Isshiki, M., & Anderson, R. G. (1999). Calcium signal transduction from caveolae. Cell Calcium, 26(5), 201–208.CrossRefPubMedGoogle Scholar
  99. 99.
    Pani, B., & Singh, B. B. (2009). Lipid rafts/caveolae as microdomains of calcium signaling. Cell Calcium, 45(6), 625–633.CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Majkova, Z., Toborek, M., & Hennig, B. (2010). The role of caveolae in endothelial cell dysfunction with a focus on nutrition and environmental toxicants. Journal of Cellular and Molecular Medicine, 14(10), 2359–2370.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Saini, H. K., Arneja, A. S., & Dhalla, N. S. (2004). Role of cholesterol in cardiovascular dysfunction. Canadian Journal of Cardiology, 20(3), 333–346.PubMedGoogle Scholar
  102. 102.
    Podechard, N., Chevanne, M., Fernier, M., Tete, A., Collin, A., Cassio, D., et al. (2016). Zebrafish larva as a reliable model for in vivo assessment of membrane remodeling involvement in the hepatotoxicity of chemical agents. Journal of Applied Toxicology, 37, 732–746.CrossRefPubMedGoogle Scholar
  103. 103.
    Tekpli, X., Holme, J. A., Sergent, O., & Lagadic-Gossmann, D. (2011). Importance of plasma membrane dynamics in chemical-induced carcinogenesis. Recent Patents on Anti-Cancer Drug Discovery, 6(3), 347–353.CrossRefPubMedGoogle Scholar
  104. 104.
    Brinchmann, B. C., Ferrec, E. L., Bisson, W. H., Podechard, N., Huitfeldt, H. S., Gallais, I., et al. (2018). Evidence of selective activation of aryl hydrocarbon receptor nongenomic calcium signaling by pyrene. Biochemical Pharmacology, 158, 1–12.CrossRefPubMedGoogle Scholar
  105. 105.
    Li, J., Kanju, P., Patterson, M., Chew, W. L., Cho, S. H., Gilmour, I., et al. (2011). TRPV4-mediated calcium influx into human bronchial epithelia upon exposure to diesel exhaust particles. Environmental Health Perspectives, 119(6), 784–793.CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Mayati, A., Levoin, N., Paris, H., N’Diaye, M., Courtois, A., Uriac, P., et al. (2012). Induction of intracellular calcium concentration by environmental benzo(a)pyrene involves a beta2-adrenergic receptor/adenylyl cyclase/Epac-1/inositol 1,4,5-trisphosphate pathway in endothelial cells. Journal of Biological Chemistry, 287(6), 4041–4052.CrossRefPubMedGoogle Scholar
  107. 107.
    Mayati, A., Le Ferrec, E., Holme, J. A., Fardel, O., Lagadic-Gossmann, D., & Ovrevik, J. (2014). Calcium signaling and beta2-adrenergic receptors regulate 1-nitropyrene induced CXCL8 responses in BEAS-2B cells. Toxicology in Vitro, 28(6), 1153–1157.CrossRefPubMedGoogle Scholar
  108. 108.
    Deering-Rice, C. E., Romero, E. G., Shapiro, D., Hughen, R. W., Light, A. R., Yost, G. S., et al. (2011). Electrophilic components of diesel exhaust particles (DEP) activate transient receptor potential ankyrin-1 (TRPA1): A probable mechanism of acute pulmonary toxicity for DEP. Chemical Research in Toxicology, 24(6), 950–959.CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Roveri, A., Coassin, M., Maiorino, M., Zamburlini, A., van Amsterdam, F. T., Ratti, E., et al. (1992). Effect of hydrogen peroxide on calcium homeostasis in smooth muscle cells. Archives of Biochemistry and Biophysics, 297(2), 265–270.CrossRefPubMedGoogle Scholar
  110. 110.
    Robison, T. W., Zhou, H., & Forman, H. J. (1995). Modulation of ADP-stimulated inositol phosphate metabolism in rat alveolar macrophages by oxidative stress. Archives of Biochemistry and Biophysics, 318(1), 215–220.CrossRefPubMedGoogle Scholar
  111. 111.
    Fusi, F., Saponara, S., Gagov, H., & Sgaragli, G. (2001). 2,5-Di-t-butyl-1,4-benzohydroquinone (BHQ) inhibits vascular L-type Ca(2 +) channel via superoxide anion generation. British Journal of Pharmacology, 133(7), 988–996.CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Deering-Rice, C. E., Johansen, M. E., Roberts, J. K., Thomas, K. C., Romero, E. G., Lee, J., et al. (2012). Transient receptor potential vanilloid-1 (TRPV1) is a mediator of lung toxicity for coal fly ash particulate material. Molecular Pharmacology, 81(3), 411–419.CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Li, Jinju, Kanju, Patrick, Patterson, Michael, Chew, Wei-Leong, Cho, Seung-Hyun, Gilmour, Ian, et al. (2011). TRPV4-mediated calcium influx into human bronchial epithelia upon exposure to diesel exhaust particles. Environmental Health Perspectives, 119, 784–793.CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Barath, S., Mills, N. L., Lundback, M., Tornqvist, H., Lucking, A. J., Langrish, J. P., et al. (2010). Impaired vascular function after exposure to diesel exhaust generated at urban transient running conditions. Particle and Fibre Toxicology, 7, 19.CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Chen, Q., Guo, F., Liu, S., Xiao, J., Wang, C., Snowise, S., et al. (2012). Calcium channel blockers prevent endothelial cell activation in response to necrotic trophoblast debris: Possible relevance to pre-eclampsia. Cardiovascular Research, 96(3), 484–493.CrossRefPubMedGoogle Scholar
  116. 116.
    Smedlund, K., Bah, M., & Vazquez, G. (2012). On the role of endothelial TRPC3 channels in endothelial dysfunction and cardiovascular disease. Cardiovascular & Hematological Agents in Medicinal Chemistry, 10(3), 265–274.CrossRefGoogle Scholar
  117. 117.
    Abramowitz, J., & Birnbaumer, L. (2009). Physiology and pathophysiology of canonical transient receptor potential channels. The Faseb Journal, 23(2), 297–328.CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Dietrich, A., Kalwa, H., Fuchs, B., Grimminger, F., Weissmann, N., & Gudermann, T. (2007). In vivo TRPC functions in the cardiopulmonary vasculature. Cell Calcium, 42(2), 233–244.CrossRefPubMedGoogle Scholar
  119. 119.
    Earley, S. (2012). TRPA1 channels in the vasculature. British Journal of Pharmacology, 167(1), 13–22.CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Sullivan, M. N., & Earley, S. (2013). TRP channel Ca(2 +) sparklets: Fundamental signals underlying endothelium-dependent hyperpolarization. American Journal of Physiology. Cell Physiology, 305(10), C999–c1008.CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Earley, S., & Brayden, J. E. (2015). Transient receptor potential channels in the vasculature. Physiological Reviews, 95(2), 645–690.CrossRefPubMedPubMedCentralGoogle Scholar
  122. 122.
    Liu, D. Y., Thilo, F., Scholze, A., Wittstock, A., Zhao, Z. G., Harteneck, C., et al. (2007). Increased store-operated and 1-oleoyl-2-acetyl-sn-glycerol-induced calcium influx in monocytes is mediated by transient receptor potential canonical channels in human essential hypertension. Journal of Hypertension, 25(4), 799–808.CrossRefPubMedGoogle Scholar
  123. 123.
    Liu, D. Y., Scholze, A., Kreutz, R., Wehland-von-Trebra, M., Zidek, W., Zhu, Z. M., et al. (2007). Monocytes from spontaneously hypertensive rats show increased store-operated and second messenger-operated calcium influx mediated by transient receptor potential canonical Type 3 channels. American Journal of Hypertension, 20(10), 1111–1118.CrossRefPubMedGoogle Scholar
  124. 124.
    De Backer, G. (2003). European guidelines on cardiovascular disease prevention in clinical practice Third Joint Task Force of European and other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of eight societies and by invited experts). European Heart Journal, 24(17), 1601–1610.CrossRefPubMedGoogle Scholar
  125. 125.
    Kolmus, K., Tavernier, J., & Gerlo, S. (2015). beta2-Adrenergic receptors in immunity and inflammation: Stressing NF-kappaB. Brain, Behavior, and Immunity, 45, 297–310.CrossRefPubMedGoogle Scholar
  126. 126.
    Wachter, S. B., & Gilbert, E. M. (2012). Beta-adrenergic receptors, from their discovery and characterization through their manipulation to beneficial clinical application. Cardiology, 122(2), 104–112.CrossRefPubMedGoogle Scholar
  127. 127.
    Mayati, A., Podechard, N., Rineau, M., Sparfel, L., Lagadic-Gossmann, D., Fardel, O., et al. (2017). Benzo(a)pyrene triggers desensitization of beta2-adrenergic pathway. Scientific Reports, 7(1), 3262.CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Ovrevik, J., Refsnes, M., Totlandsdal, A. I., Holme, J. A., Schwarze, P. E., & Lag, M. (2011). TACE/TGF-alpha/EGFR regulates CXCL8 in bronchial epithelial cells exposed to particulate matter components. European Respiratory Journal, 38(5), 1189–1199.CrossRefPubMedGoogle Scholar
  129. 129.
    Li, J., Ghio, A. J., Cho, S.-H., Brinckerhoff, C. E., Simon, S. A., & Liedtke, W. (2009). Diesel exhaust particles activate the matrix-metalloproteinase-1 gene in human bronchial epithelia in a β-arrestin–dependent manner via activation of RAS. Environmental Health Perspectives, 117(3), 400–409.CrossRefPubMedGoogle Scholar
  130. 130.
    Bach, N., Bolling, A. K., Brinchmann, B. C., Totlandsdal, A. I., Skuland, T., Holme, J. A., et al. (2015). Cytokine responses induced by diesel exhaust particles are suppressed by PAR-2 silencing and antioxidant treatment, and driven by polar and non-polar soluble constituents. Toxicology Letters, 238(2), 72–82.CrossRefPubMedGoogle Scholar
  131. 131.
    Brinchmann, B. C., Le Ferrec, E., Podechard, N., Lagadic-Gossmann, D., Holme, J. A., & Ovrevik, J. (2018). Organic chemicals from diesel exhaust particles affects intracellular calcium, inflammation and beta-adrenoceptors in endothelial cells. Toxicology Letters, 302, 18–27.CrossRefPubMedGoogle Scholar
  132. 132.
    Puga, A. (1997). Sustained increase in intracellular free calcium and activation of cyclooxygenase-2 expression in mouse hepatoma cells treated with Dioxin. Biochemical Pharmacology, 54, 1287–1296.CrossRefPubMedGoogle Scholar
  133. 133.
    Karras, J. G., Morris, D. L., Matulka, R. A., Kramer, C. M., & Holsapple, M. P. (1996). 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) elevates basal B-cell intracellular calcium concentration and suppresses surface Ig- but not CD40-induced antibody secretion. Toxicology and Applied Pharmacology, 137(2), 275–284.CrossRefPubMedGoogle Scholar
  134. 134.
    Morales-Hernandez, A., Sanchez-Martin, F. J., Hortigon-Vinagre, M. P., Henao, F., & Merino, J. M. (2012). 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces apoptosis by disruption of intracellular calcium homeostasis in human neuronal cell line SHSY5Y. Apoptosis: An International Journal on Programmed Cell Death, 17(11), 1170–1181.CrossRefGoogle Scholar
  135. 135.
    Nguyen, L. P., & Bradfield, C. A. (2008). The search for endogenous activators of the aryl hydrocarbon receptor. Chemical Research in Toxicology, 21(1), 102–116.CrossRefPubMedGoogle Scholar
  136. 136.
    Savouret, J. F., Berdeaux, A., & Casper, R. F. (2003). The aryl hydrocarbon receptor and its xenobiotic ligands: A fundamental trigger for cardiovascular diseases. Nutrition, Metabolism, and Cardiovascular Diseases: NMCD, 13(2), 104–113.CrossRefPubMedGoogle Scholar
  137. 137.
    Vogel, C. F., Sciullo, E., & Matsumura, F. (2004). Activation of inflammatory mediators and potential role of ah-receptor ligands in foam cell formation. Cardiovascular Toxicology, 4(4), 363–373.CrossRefPubMedGoogle Scholar
  138. 138.
    Wu, D., Nishimura, N., Kuo, V., Fiehn, O., Shahbaz, S., Van Winkle, L., et al. (2011). Activation of aryl hydrocarbon receptor induces vascular inflammation and promotes atherosclerosis in apolipoprotein E-/- mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 31(6), 1260–1267.CrossRefPubMedPubMedCentralGoogle Scholar
  139. 139.
    Sciullo, E. M., Vogel, C. F., Li, W., & Matsumura, F. (2008). Initial and extended inflammatory messages of the nongenomic signaling pathway of the TCDD-activated Ah receptor in U937 macrophages. Archives of Biochemistry and Biophysics, 480(2), 143–155.CrossRefPubMedGoogle Scholar
  140. 140.
    Hanneman, W. H., Legare, M., Barhoumi, R., Burghardt, R., Safe, S., & Tiffany-Castiglioni, E. (1996). Stimulation of calcium uptake in cultured rat hippocampal neurons by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicology, 112(1), 19–28.CrossRefPubMedGoogle Scholar
  141. 141.
    Su, H. H., Lin, H. T., Suen, J. L., Sheu, C. C., Yokoyama, K. K., Huang, S. K., et al. (2016). Aryl hydrocarbon receptor-ligand axis mediates pulmonary fibroblast migration and differentiation through increased arachidonic acid metabolism. Toxicology, 370, 116–126.CrossRefPubMedGoogle Scholar
  142. 142.
    Maaetoft-Udsen, K., Shimoda, L. M., Frokiaer, H., & Turner, H. (2012). Aryl hydrocarbon receptor ligand effects in RBL2H3 cells. Journal of Immunotoxicology, 9(3), 327–337.CrossRefPubMedPubMedCentralGoogle Scholar
  143. 143.
    Rainville, J., Pollard, K., & Vasudevan, N. (2015). Membrane-initiated non-genomic signaling by estrogens in the hypothalamus: Cross-talk with glucocorticoids with implications for behavior. Frontiers in Endocrinology, 6, 18.CrossRefPubMedPubMedCentralGoogle Scholar
  144. 144.
    Foradori, C. D., Weiser, M. J., & Handa, R. J. (2008). Non-genomic actions of androgens. Frontiers in Neuroendocrinology, 29(2), 169–181.CrossRefPubMedGoogle Scholar
  145. 145.
    Ropero, A. B., Juan-Pico, P., Rafacho, A., Fuentes, E., Bermudez-Silva, F. J., Roche, E., et al. (2009). Rapid non-genomic regulation of Ca2+ signals and insulin secretion by PPAR alpha ligands in mouse pancreatic islets of Langerhans. Journal of Endocrinology, 200(2), 127–138.CrossRefPubMedGoogle Scholar
  146. 146.
    Meyer, M. R., Haas, E., Prossnitz, E. R., & Barton, M. (2009). Non-genomic regulation of vascular cell function and growth by estrogen. Molecular and Cellular Endocrinology, 308(1–2), 9–16.CrossRefPubMedPubMedCentralGoogle Scholar
  147. 147.
    Kim, K. H., & Bender, J. R. (2009). Membrane-initiated actions of estrogen on the endothelium. Molecular and Cellular Endocrinology, 308(1–2), 3–8.CrossRefPubMedPubMedCentralGoogle Scholar
  148. 148.
    Moriarty, K., Kim, K. H., & Bender, J. R. (2006). Minireview: Estrogen receptor-mediated rapid signaling. Endocrinology, 147(12), 5557–5563.CrossRefPubMedGoogle Scholar
  149. 149.
    Chambliss, K. L., Yuhanna, I. S., Anderson, R. G., Mendelsohn, M. E., & Shaul, P. W. (2002). ERbeta has nongenomic action in caveolae. Molecular Endocrinology (Baltimore, Md), 16(5), 938–946.Google Scholar
  150. 150.
    Rey-Barroso, J. (2014). The Dioxin receptor modulates Caveolin-1 mobilization during directional migration: Role of cholesterol. Cell Communication and Signaling, 12, 57.CrossRefPubMedGoogle Scholar
  151. 151.
    Dong, B., & Matsumura, F. (2008). Roles of cytosolic phospholipase A2 and Src kinase in the early action of 2,3,7,8-tetrachlorodibenzo-p-dioxin through a nongenomic pathway in MCF10A cells. Molecular Pharmacology, 74(1), 255–263.CrossRefPubMedGoogle Scholar
  152. 152.
    Graziani, A., Bricko, V., Carmignani, M., Graier, W. F., & Groschner, K. (2004). Cholesterol- and caveolin-rich membrane domains are essential for phospholipase A2-dependent EDHF formation. Cardiovascular Research, 64(2), 234–242.CrossRefPubMedGoogle Scholar
  153. 153.
    Murata, M., Peranen, J., Schreiner, R., Wieland, F., Kurzchalia, T. V., & Simons, K. (1995). VIP21/caveolin is a cholesterol-binding protein. Proceedings of the National academy of Sciences of the United States of America, 92(22), 10339–10343.CrossRefPubMedPubMedCentralGoogle Scholar
  154. 154.
    Murata, T., Lin, M. I., Stan, R. V., Bauer, P. M., Yu, J., & Sessa, W. C. (2007). Genetic evidence supporting caveolae microdomain regulation of calcium entry in endothelial cells. Journal of Biological Chemistry, 282(22), 16631–16643.CrossRefPubMedGoogle Scholar
  155. 155.
    Liao, Y., Plummer, N. W., George, M. D., Abramowitz, J., Zhu, M. X., & Birnbaumer, L. (2009). A role for Orai in TRPC-mediated Ca2 + entry suggests that a TRPC: Orai complex may mediate store and receptor operated Ca2+ entry. Proceedings of the National academy of Sciences of the United States of America, 106(9), 3202–3206.CrossRefPubMedPubMedCentralGoogle Scholar
  156. 156.
    Lim, E. J., Majkova, Z., Xu, S., Bachas, L., Arzuaga, X., Smart, E., et al. (2008). Coplanar polychlorinated biphenyl-induced CYP1A1 is regulated through caveolae signaling in vascular endothelial cells. Chemico Biological Interactions, 176(2–3), 71–78.CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Air Pollution and Noise, Division of Infection Control, Environment and HealthNorwegian Institute of Public HealthOsloNorway
  2. 2.Univ Rennes, Inserm, EHESP, Irset (Institut de recherche en santé environnement et travail) - UMR_S 1085RennesFrance
  3. 3.Department of Biosciences, Faculty of Mathematics and Natural SciencesUniversity of OsloOsloNorway

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