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Increase in Hypotonic Stress-Induced Endocytic Activity in Macrophages via ClC-3

  • Yan, Yutao (Department of Immunology, Tongji Medical College) ;
  • Ding, Yu (Department of Immunology, Tongji Medical College) ;
  • Ming, Bingxia (Department of Immunology, Tongji Medical College) ;
  • Du, Wenjiao (Department of Immunology, Tongji Medical College) ;
  • Kong, Xiaoling (Department of Immunology, Tongji Medical College) ;
  • Tian, Li (Department of Immunology, Tongji Medical College) ;
  • Zheng, Fang (Department of Immunology, Tongji Medical College) ;
  • Fang, Min (Department of Immunology, Tongji Medical College) ;
  • Tan, Zheng (Department of Immunology, Tongji Medical College) ;
  • Gong, Feili (Department of Immunology, Tongji Medical College)
  • Received : 2014.02.13
  • Accepted : 2014.04.01
  • Published : 2014.05.31

Abstract

Extracellular hypotonic stress can affect cellular function. Whether and how hypotonicity affects immune cell function remains to be elucidated. Macrophages are immune cells that play key roles in adaptive and innate in immune reactions. The purpose of this study was to investigate the role and underlying mechanism of hypotonic stress in the function of bone marrow-derived macrophages (BMDMs). Hypotonic stress increased endocytic activity in BMDMs, but there was no significant change in the expression of CD80, CD86, and MHC class II molecules, nor in the secretion of TNF-${\alpha}$ or IL-10 by BMDMs. Furthermore, the enhanced endocytic activity of BMDMs triggered by hypotonic stress was significantly inhibited by chloride channel-3 (ClC-3) siRNA. Our findings suggest that hypotonic stress can induce endocytosis in BMDMs and that ClC-3 plays a central role in the endocytic process.

Keywords

References

  1. Abdullaev, I.F., Sabirov, R.Z., and Okada, Y. (2003). Upregulation of swelling-activated $Cl^{-}$ channel sensitivity to cell volume by activation of EGF receptors in murine mammary cells. J. Physiol. 549, 749-758. https://doi.org/10.1113/jphysiol.2003.039784
  2. Bozza, M.T., Martins, Y.C., Carneiro, L.A., and Paiva, C.N. (2012). Macrophage migration inhibitory factor in protozoan infections. J. Parasitol. Res. 2012, 413052.
  3. Cassetta, L., Cassol, E., and Poli, G. (2011). Macrophage polarization in health and disease. ScientificWorldJournal 11, 2391-2402. https://doi.org/10.1100/2011/213962
  4. Chu, X., Filali, M., Stanic, B., Takapoo, M., Sheehan, A., Bhalla, R., Lamb, F.S., and Miller, F.J., Jr. (2011). A critical role for chloride channel-3 (CIC-3) in smooth muscle cell activation and neointima formation. Arterioscler. Thromb. Vasc. Biol. 31, 345-351. https://doi.org/10.1161/ATVBAHA.110.217604
  5. Comes, N., Gasull, X., Gual, A., and Borras, T. (2005). Differential expression of the human chloride channel genes in the trabecular meshwork under stress conditions. Exp. Eye Res. 80, 801-813. https://doi.org/10.1016/j.exer.2004.12.009
  6. Dick, G.M., Kong, I.D., and Sanders, K.M. (1999). Effects of anion channel antagonists in canine colonic myocytes: comparative pharmacology of $Cl^{-}$, $Ca^{2+}$ and $K^+$ currents. Br. J. Pharmacol. 127, 1819-1831. https://doi.org/10.1038/sj.bjp.0702730
  7. Dickerson, R.N., Maish, G.O., 3rd, Weinberg, J.A., Croce, M.A., Minard, G., and Brown, R.O. (2013). Safety and efficacy of intravenous hypotonic 0.225% sodium chloride infusion for the treatment of hypernatremia in critically Ill patients. Nutr. Clin. Pract. 28, 400-408. https://doi.org/10.1177/0884533613483840
  8. Duan, D.D. (2011). The ClC-3 chloride channels in cardiovascular disease. Acta Pharmacol. Sin. 32, 675-684. https://doi.org/10.1038/aps.2011.30
  9. Enz, R., Ross, B.J., and Cutting, G.R. (1999). Expression of the voltage-gated chloride channel ClC-2 in rod bipolar cells of the rat retina. J. Neurosci. 19, 9841-9847.
  10. Gaglio, P., Marfo, K., and Chiodo, J., 3rd (2012). Hyponatremia in cirrhosis and end-stage liver disease: treatment with the vasopressin V(2)-receptor antagonist tolvaptan. Dig. Dis. Sci. 57, 2774-2785. https://doi.org/10.1007/s10620-012-2276-3
  11. Gong, D., Shi, W., Yi, S.J., Chen, H., Groffen, J., and Heisterkamp, N. (2012). TGFbeta signaling plays a critical role in promoting alternative macrophage activation. BMC Immunol. 13, 31. https://doi.org/10.1186/1471-2172-13-31
  12. Hermoso, M., Satterwhite, C.M., Andrade, Y.N., Hidalgo, J., Wilson, S.M., Horowitz, B., and Hume, J.R. (2002). ClC-3 is a fundamental molecular component of volume-sensitive outwardly rectifying Cl- channels and volume regulation in HeLa cells and Xenopus laevis oocytes. J. Biol. Chem. 277, 40066-40074. https://doi.org/10.1074/jbc.M205132200
  13. Inoue, H., Takahashi, N., Okada, Y., and Konishi, M. (2010). Volume-sensitive outwardly rectifying chloride channel in white adipocytes from normal and diabetic mice. Am. J. Physiol. Cell Physiol. 298, C900-909. https://doi.org/10.1152/ajpcell.00450.2009
  14. Kajimoto, K., Shao, D., Takagi, H., Maceri, G., Zablocki, D., Mukai, H., Ono, Y., and Sadoshima, J. (2011). Hypotonic swellinginduced activation of PKN1 mediates cell survival in cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 300, H191-200. https://doi.org/10.1152/ajpheart.00232.2010
  15. Kondo, A., Maeta, M., Oka, A., Tsujitani, S., Ikeguchi, M., and Kaibara, N. (1996). Hypotonic intraperitoneal cisplatin chemotherapy for peritoneal carcinomatosis in mice. Br. J. Cancer 73, 1166-1170. https://doi.org/10.1038/bjc.1996.225
  16. Kong, X., Tang, X., Du, W., Tong, J., Yan, Y., Zheng, F., Fang, M., Gong, F., and Tan, Z. (2013). Extracellular acidosis modulates the endocytosis and maturation of macrophages. Cell. Immunol. 281, 44-50. https://doi.org/10.1016/j.cellimm.2012.12.009
  17. Li, X., and Liu, X. (2005). Effect of curcumin on immune function of mice. J. Huazhong Univ. Sci. Technol. Med. Sci. 25, 137-140. https://doi.org/10.1007/BF02873559
  18. Link, T.M., Park, U., Vonakis, B.M., Raben, D.M., Soloski, M.J., and Caterina, M.J. (2010). TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat. Immunol. 11, 232-239.
  19. Liu, X., Silverstein, P.S., Singh, V., Shah, A., Qureshi, N., and Kumar, A. (2012). Methamphetamine increases LPS-mediated expression of IL-8, TNF-$\alpha$ and IL-$\1beta$ in human macrophages through common signaling pathways. PLoS One 7, e33822. https://doi.org/10.1371/journal.pone.0033822
  20. Medina-Contreras, O., Geem, D., Laur, O., Williams, I.R., Lira, S.A., Nusrat, A., Parkos, C.A., and Denning, T.L. (2011). CX3CR1 regulates intestinal macrophage homeostasis, bacterial translocation, and colitogenic Th17 responses in mice. J. Clin. Invest. 121, 4787-4795. https://doi.org/10.1172/JCI59150
  21. Min, X.J., Li, H., Hou, S.C., He, W., Liu, J., Hu, B., and Wang, J. (2011). Dysfunction of volume-sensitive chloride channels contributes to cisplatin resistance in human lung adenocarcinoma cells. Exp. Biol. Med. 236, 483-491. https://doi.org/10.1258/ebm.2011.010297
  22. Mohammad-Panah, R., Harrison, R., Dhani, S., Ackerley, C., Huan, L.J., Wang, Y., and Bear, C.E. (2003). The chloride channel ClC-4 contributes to endosomal acidification and trafficking. J. Biol. Chem. 278, 29267-29277. https://doi.org/10.1074/jbc.M304357200
  23. Okada, Y., Maeno, E., Shimizu, T., Manabe, K., Mori, S., and Nabekura, T. (2004). Dual roles of plasmalemmal chloride channels in induction of cell death. Pflugers Arch. 448, 287-295. https://doi.org/10.1007/s00424-004-1276-3
  24. Okada, Y., Sato, K., and Numata, T. (2009). Pathophysiology and puzzles of the volume-sensitive outwardly rectifying anion channel. J. Physiol. 587, 2141-2149.
  25. Okamoto, F., Kajiya, H., Toh, K., Uchida, S., Yoshikawa, M., Sasaki, S., Kido, M.A., Tanaka, T., and Okabe, K. (2008). Intracellular ClC-3 chloride channels promote bone resorption in vitro through organelle acidification in mouse osteoclasts. Am. J. Physiol. Cell Physiol. 294, C693-701. https://doi.org/10.1152/ajpcell.00251.2007
  26. Park, K.R., and Bryers, J.D. (2012). Effect of macrophage classical (M1) activation on implant-adherent macrophage interactions with Staphylococcus epidermidis: a murine in vitro model system. J. Biomed. Mater. Res. A 100, 2045-2053.
  27. Parveen, N., Varman, R., Nair, S., Das, G., Ghosh, S., and Mukhopadhyay, S. (2013). Endocytosis of Mycobacterium tuberculosis heat shock protein 60 is required to induce production in macrophages. J. Biol. Chem. 288, 24956-24971. https://doi.org/10.1074/jbc.M113.461004
  28. Roberts, B.N., and Christini, D.J. (2011). NHE inhibition does not improve Na(+) or Ca(2+) overload during reperfusion: using modeling to illuminate the mechanisms underlying a therapeutic failure. PLoS Comput. Biol. 7, e1002241. https://doi.org/10.1371/journal.pcbi.1002241
  29. Roger, T., Delaloye, J., Chanson, A.L., Giddey, M., Le Roy, D., and Calandra, T. (2013). Macrophage migration inhibitory factor deficiency is associated with impaired killing of gram-negative bacteria by macrophages and increased susceptibility to Klebsiella pneumoniae sepsis. J. Infect. Dis. 207, 331-339. https://doi.org/10.1093/infdis/jis673
  30. Schliess, F., Foster, N., Gorg, B., Reinehr, R., and Haussinger, D. (2004). Hypoosmotic swelling increases protein tyrosine nitration in cultured rat astrocytes. Glia 47, 21-29. https://doi.org/10.1002/glia.20019
  31. Shapiro, H., Lutaty, A., and Ariel, A. (2011). Macrophages, metainflammation, and immuno-metabolism. ScientificWorldJournal 11, 2509-2529. https://doi.org/10.1100/2011/397971
  32. Siegel, A.J. (2007). Hypertonic (3%) sodium chloride for emergent treatment of exercise-associated hypotonic encephalopathy. Sports Med. 37, 459-462. https://doi.org/10.2165/00007256-200737040-00049
  33. Stobrawa, S.M., Breiderhoff, T., Takamori, S., Engel, D., Schweizer, M., Zdebik, A.A., Bosl, M.R., Ruether, K., Jahn, H., Draguhn, A., et al. (2001). Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29, 185-196. https://doi.org/10.1016/S0896-6273(01)00189-1
  34. Tamura, N., Hazeki, K., Okazaki, N., Kametani, Y., Murakami, H., Takaba, Y., Ishikawa, Y., Nigorikawa, K., and Hazeki, O. (2009). Specific role of phosphoinositide 3-kinase p110alpha in the regulation of phagocytosis and pinocytosis in macrophages. Biochem J. 423, 99-108. https://doi.org/10.1042/BJ20090687
  35. Tang, C.Y., and Chen, T.Y. (2011). Physiology and pathophysiology of ClC-1: mechanisms of a chloride channel disease, myotonia. J. Biomed. Biotechnol. 2011, 685328.
  36. Thorp, E.B. (2012). Contrasting inflammation resolution during atherosclerosis and post myocardial infarction at the level of monocyte/macrophage phagocytic clearance. Front. Immunol. 3, 39.
  37. Tong, J., Wu, W.N., Kong, X., Wu, P.F., Tian, L., Du, W., Fang, M., Zheng, F., Chen, J.G., Tan, Z., et al. (2011). Acid-sensing ion channels contribute to the effect of acidosis on the function of dendritic cells. J. Immunol. 186, 3686-3692. https://doi.org/10.4049/jimmunol.1001346
  38. Torr, E.E., Gardner, D.H., Thomas, L., Goodall, D.M., Bielemeier, A., Willetts, R., Griffiths, H.R., Marshall, L.J., and Devitt, A. (2012). Apoptotic cell-derived ICAM-3 promotes both macrophage chemoattraction to and tethering of apoptotic cells. Cell Death Differ. 19, 671-679. https://doi.org/10.1038/cdd.2011.167
  39. Tunkel, A.R., and Scheld, W.M. (1993). Pathogenesis and pathophysiology of bacterial meningitis. Ann. Rev. Med. 44, 103-120. https://doi.org/10.1146/annurev.me.44.020193.000535
  40. Wheeler, T.M., Lueck, J.D., Swanson, M.S., Dirksen, R.T., and Thornton, C.A. (2007). Correction of ClC-1 splicing eliminates chloride channelopathy and myotonia in mouse models of myotonic dystrophy. J. Clin. Invest. 117, 3952-3957.
  41. Xiong, D., Heyman, N.S., Airey, J., Zhang, M., Singer, C.A., Rawat, S., Ye, L., Evans, R., Burkin, D.J., Tian, H., et al. (2010). Cardiac-specific, inducible ClC-3 gene deletion eliminates native volume-sensitive chloride channels and produces myocardial hypertrophy in adult mice. J. Mol. Cell. Cardiol. 48, 211-219. https://doi.org/10.1016/j.yjmcc.2009.07.003
  42. Zhang, Y.X., Zhang, J.R., and Wang, Z.G. (2013). Mycophenolate mofetil affects monocyte Toll-like receptor 4 signaling during mouse renal ischemia/reperfusion injury. Chin. Med. J. 126, 1224-1229.

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