Skip to main content
SpringerLink
Log in

Effects of Preconditioning with Sevoflurane on TNF-α-Induced Permeability and Activation of p38 MAPK in Rat Pulmonary Microvascular Endothelial Cells

  • Original Paper
  • Published:
Cell Biochemistry and Biophysics Aims and scope Submit manuscript

Abstract

Preconditioning with sevoflurane (SPC) diminishes effusion of rat alveolar membrane during inflammation. It is not clear whether this preconditioning directly inhibits permeability of pulmonary microvascular endothelial cell (PMVEC) monolayer. In this article, we evaluated effects of SPC on permeability of PMVEC monolayer and identified signaling pathways involved in these effects. PMVEC monolayer was exposed to different conditions (5-hydroxydecanoate (5-HD), TNF-α, SPC, SPC with subsequent exposure to TNF-α and 5-HD, and SPC with subsequent exposure to TNF-α alone), and the permeability of PMVEC monolayer was assessed using FITC-bovine serum albumin (ELISA). Expression of ICAM-1 (Western blot and RT-PCR) and activation of p38 MAPK (Western blot) were also assessed. Compared to the TNF-α group, permeability of PMVEC monolayer in the SPC + TNF-α group was significantly lower. Activation of p38 MAPK was also diminished in the TNF-α group. Pre-treatment with 5-HD reverted beneficial effects of SPC. Expression of ICAM-1 was not modulated by any of the tested experimental exposures. The results of this study demonstrate that SPC is capable of diminishing the TNF-α-induced increase of permeability of PMVEC monolayer, and that this beneficial effect is partly reversed by 5-HD. Further, SPC suppresses activation of p38 MAPK.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Bibliography

  1. Zimmerman, G. A., Albertine, K. H., Carveth, H. J., Gill, E. A., Grissom, C. K., Hoidal, J. R., et al. (1999). Endothelial activation in ARDS. Chest, 116, 18S–24S.

    Article  PubMed  CAS  Google Scholar 

  2. Asaduzzaman, M., Wang, Y., & Thorlacius, H. (2008). Critical role of p38 mitogen-activated protein kinase signaling in septic lung injury. Critical Care Medicine, 36, 482–488.

    Article  PubMed  CAS  Google Scholar 

  3. Borbiev, T., Birukova, A., Liu, F., Nurmukhambetova, S., Gerthoffer, W. T., Garcia, J. G., et al. (2004). p38 MAP kinase-dependent regulation of endothelial cell permeability. American Journal of Physiology Lung Cellular and Molecular Physiology, 287, L911–L918.

    Article  PubMed  CAS  Google Scholar 

  4. Nwariaku, F. E., Chang, J., Zhu, X., Liu, Z., Duffy, S. L., Halaihel, N. H., et al. (2002). The role of p38 map kinase in tumor necrosis factor-induced redistribution of vascular endothelial cadherin and increased endothelial permeability. Shock, 18, 82–85.

    Article  PubMed  Google Scholar 

  5. Sniecinski, R., & Liu, H. (2004). Reduced efficacy of volatile anesthetic preconditioning with advanced age in isolated rat myocardium. Anesthesiology, 100, 589–597.

    Article  PubMed  CAS  Google Scholar 

  6. Yonemochi, H., Ichinose, M., Anan, F., Taniguti, Y., Shinohara, T., Takahashi, N., et al. (2006). Diazoxide-induced cardioprotection via DeltaPsim loss depending on timing of application. Life Science, 79, 1906–1912.

    Article  CAS  Google Scholar 

  7. Tanaka, K., Ludwig, L. M., Krolikowski, J. G., Alcindor, D., Pratt, P. F., Kersten, J. R., et al. (2004). Isoflurane produces delayed preconditioning against myocardial ischemia and reperfusion injury: Role of cyclooxygenase-2. Anesthesiology, 100, 525–531.

    Article  PubMed  CAS  Google Scholar 

  8. Xiong, L., Zheng, Y., Wu, M., Hou, L., Zhu, Z., Zhang, X., et al. (2003). Preconditioning with isoflurane produces dose-dependent neuroprotection via activation of adenosine triphosphate-regulated potassium channels after focal cerebral ischemia in rats. Anesthesia and Analgesia, 96, 233–237. table.

    PubMed  CAS  Google Scholar 

  9. Plachinta, R. V., Hayes, J. K., Cerilli, L. A., & Rich, G. F. (2003). Isoflurane pretreatment inhibits lipopolysaccharide-induced inflammation in rats. Anesthesiology, 98, 89–95.

    Article  PubMed  CAS  Google Scholar 

  10. Allen, M., Svensson, L., Roach, M., Hambor, J., McNeish, J., & Gabel, C. A. (2000). Deficiency of the stress kinase p38alpha results in embryonic lethality: characterization of the kinase dependence of stress responses of enzyme-deficient embryonic stem cells. Journal of Experimental Medicine, 191, 859–870.

    Article  PubMed  CAS  Google Scholar 

  11. Sun, Y. H., Zhang, Q., Wang, J. K., & Cui, Y. (2004). Effects of sevoflurane on membrane permeability of alveolar capillaries in rats with acute lung injury caused by endotoxin. Zhonghua Wai Ke Za Zhi, 42, 1014–1017.

    PubMed  Google Scholar 

  12. Chen, S. F., Fei, X., & Li, S. H. (1995). A new simple method for isolation of microvascular endothelial cells avoiding both chemical and mechanical injuries. Microvascular Research, 50, 119–128.

    Article  PubMed  Google Scholar 

  13. Nooteboom, A., Hendriks, T., Otteholler, I., & van der Linden, C. J. (2000). Permeability characteristics of human endothelial monolayers seeded on different extracellular matrix proteins. Mediators Inflammation, 9, 235–241.

    Article  CAS  Google Scholar 

  14. Predescu, D., & Palade, G. E. (1993). Plasmalemmal vesicles represent the large pore system of continuous microvascular endothelium. American Journal of Physiology, 265, H725–H733.

    PubMed  CAS  Google Scholar 

  15. Michel, C. C., & Curry, F. E. (1999). Microvascular permeability. Physiological Reviews, 79, 703–761.

    PubMed  CAS  Google Scholar 

  16. Malik, A. B., & Horgan, M. J. (1987). Mechanisms of thrombin-induced lung vascular injury and edema. American Review of Respiratory Disease, 136, 467–470.

    PubMed  CAS  Google Scholar 

  17. Malik, A. B., & Lo, S. K. (1996). Vascular endothelial adhesion molecules and tissue inflammation. Pharmacological Reviews, 48, 213–229.

    PubMed  CAS  Google Scholar 

  18. Bates, D. O., Hillman, N. J., Pocock, T. M., & Neal, C. R. (2002). Regulation of microvascular permeability by vascular endothelial growth factors. Journal of Anatomy, 200, 529–530.

    Article  Google Scholar 

  19. Michel, C. C., & Neal, C. R. (1999). Openings through endothelial cells associated with increased microvascular permeability. Microcirculation, 6, 45–54.

    PubMed  CAS  Google Scholar 

  20. van Hinsbergh, W. M. (1997). Endothelial permeability for macromolecules. Mechanistic aspects of pathophysiological modulation. Arteriosclerosis, Thrombosis, and Vascular Biology, 17, 1018–1023.

    Article  PubMed  Google Scholar 

  21. Garcia, J. G., Davis, H. W., & Patterson, C. E. (1995). Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. Journal of Cellular Physiology, 163, 510–522.

    Article  PubMed  CAS  Google Scholar 

  22. van Nieuw Amerongen, G. P., Draijer, R., Vermeer, M. A., & van Hinsbergh, V. W. (1998). Transient and prolonged increase in endothelial permeability induced by histamine and thrombin: role of protein kinases, calcium, and RhoA. Circulation Research, 83, 1115–1123.

    PubMed  Google Scholar 

  23. Vuong, P. T., Malik, A. B., Nagpala, P. G., & Lum, H. (1998). Protein kinase C beta modulates thrombin-induced Ca2+ signaling and endothelial permeability increase. Journal of Cellular Physiology, 175, 379–387.

    Article  PubMed  CAS  Google Scholar 

  24. Angelini, D. J., Hyun, S. W., Grigoryev, D. N., Garg, P., Gong, P., Singh, I. S., et al. (2006). TNF-alpha increases tyrosine phosphorylation of vascular endothelial cadherin and opens the paracellular pathway through fyn activation in human lung endothelia. American Journal of Physiology Lung Cellular and Molecular Physiology, 291, L1232–L1245.

    Article  PubMed  CAS  Google Scholar 

  25. van Hinsbergh, V. W., & van Nieuw Amerongen, G. P. (2002). Intracellular signalling involved in modulating human endothelial barrier function. Journal of Anatomy, 200, 549–560.

    Article  PubMed  Google Scholar 

  26. Leeper-Woodford, S. K., Carey, P. D., Byrne, K., Jenkins, J. K., Fisher, B. J., Blocher, C., et al. (1991). Tumor necrosis factor. Alpha and beta subtypes appear in circulation during onset of sepsis-induced lung injury. American Review of Respiratory Disease, 143, 1076–1082.

    PubMed  CAS  Google Scholar 

  27. Goldblum, S. E., Ding, X., & Campbell-Washington, J. (1993). TNF-alpha induces endothelial cell F-actin depolymerization, new actin synthesis, and barrier dysfunction. American Journal of Physiology, 264, C894–C905.

    PubMed  CAS  Google Scholar 

  28. Hildt, E., & Oess, S. (1999). Identification of Grb2 as a novel binding partner of tumor necrosis factor (TNF) receptor I. Journal of Experimental Medicine, 189, 1707–1714.

    Article  PubMed  CAS  Google Scholar 

  29. Petrache, I., Verin, A. D., Crow, M. T., Birukova, A., Liu, F., & Garcia, J. G. (2001). Differential effect of MLC kinase in TNF-alpha-induced endothelial cell apoptosis and barrier dysfunction. American Journal of Physiology Lung Cellular and Molecular Physiology, 280, L1168–L1178.

    PubMed  CAS  Google Scholar 

  30. Deyhimy, D. I., Fleming, N. W., Brodkin, I. G., & Liu, H. (2007). Anesthetic preconditioning combined with postconditioning offers no additional benefit over preconditioning or postconditioning alone. Anesthesia and Analgesia, 105, 316–324.

    Article  PubMed  Google Scholar 

  31. Chiari, P. C., Pagel, P. S., Tanaka, K., Krolikowski, J. G., Ludwig, L. M., Trillo, R. A., Jr., et al. (2004). Intravenous emulsified halogenated anesthetics produce acute and delayed preconditioning against myocardial infarction in rabbits. Anesthesiology, 101, 1160–1166.

    Article  PubMed  CAS  Google Scholar 

  32. Zaugg, M., Lucchinetti, E., Spahn, D. R., Pasch, T., & Schaub, M. C. (2002). Volatile anesthetics mimic cardiac preconditioning by priming the activation of mitochondrial K(ATP) channels via multiple signaling pathways. Anesthesiology, 97, 4–14.

    Article  PubMed  CAS  Google Scholar 

  33. Kaneda, K., Miyamae, M., Sugioka, S., Okusa, C., Inamura, Y., Domae, N., et al. (2008). Sevoflurane enhances ethanol-induced cardiac preconditioning through modulation of protein kinase C, mitochondrial KATP channels, and nitric oxide synthase, in guinea pig hearts. Anesthesia and Analgesia, 106, 9–16. table.

    Article  PubMed  CAS  Google Scholar 

  34. Zhou, Z., Connell, M. C., & MacEwan, D. J. (2007). TNFR1-induced NF-kappaB, but not ERK, p38MAPK or JNK activation, mediates TNF-induced ICAM-1 and VCAM-1 expression on endothelial cells. Cellular Signalling, 19, 1238–1248.

    Article  PubMed  CAS  Google Scholar 

  35. Paul, A., Wilson, S., Belham, C. M., Robinson, C. J., Scott, P. H., Gould, G. W., et al. (1997). Stress-activated protein kinases: activation, regulation and function. Cellular Signalling, 9, 403–410.

    Article  PubMed  CAS  Google Scholar 

  36. Hu, J. H., Chen, T., Zhuang, Z. H., Kong, L., Yu, M. C., Liu, Y., et al. (2007). Feedback control of MKP-1 expression by p38. Cellular Signalling, 19, 393–400.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank all the lab members for helpful discussion. This study is supported by the National Natural Science Foundation of China (project 30872430).

Author information

Authors and Affiliations

  1. Department of Anesthesiology, Zhongshan Hospital, Fudan University, 180 Fenglin Road, Shanghai, 200032, China

    Shao-Xiao Sun & Chang-Hong Miao

  2. Joint Immunology Laboratory of Health Science Center and Shanghai Institute of Immunology, Shanghai Jiao-Tong University School of Medicine and Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, 200025, China

    Bao-Xue Ge

Authors
  1. Shao-Xiao Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bao-Xue Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chang-Hong Miao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chang-Hong Miao.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sun, SX., Ge, BX. & Miao, CH. Effects of Preconditioning with Sevoflurane on TNF-α-Induced Permeability and Activation of p38 MAPK in Rat Pulmonary Microvascular Endothelial Cells. Cell Biochem Biophys 61, 123–129 (2011). https://doi.org/10.1007/s12013-011-9168-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12013-011-9168-6

Keywords

Search

Navigation