Cigarette smoke inhibits efferocytosis via deregulation of sphingosine kinase signaling: Reversal with exogenous S1P and the S1P analogue FTY720

Journal of Leukocyte Biology

Volumn 100, Issue 1, 2016, Pages 195-202

  Tran, Hai B ^a   Barnawi, Jameel ^a,b,c   Ween, Miranda ^a   Hamon, Rhys ^a   Roscioli, Eugene ^a   Hodge, Greg ^a,b   Reynolds, Paul N ^a,b   Pitson, Stuart M ^b,d   Davies, Lorena T ^d   Haberberger, Rainer ^e   Hodge, Sandra ^a,b  

^a ROYAL ADELAIDE HOSPITAL   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF TABUK   (Saudi Arabia)

^d UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^e FLINDERS UNIVERSITY   (Australia)

Author keywords

COPD; Macrophage; Phagocytosis; SPHK subcellular localization

Indexed keywords

3 (4 CHLOROPHENYL) N (4 PYRIDINYLMETHYL)ADAMANTANE 1 CARBOXAMIDE; CIGARETTE SMOKE; FINGOLIMOD; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2; IMMUNOSUPPRESSIVE AGENT; LYSOPHOSPHOLIPID; PHOSPHOTRANSFERASE; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

ARTICLE; CELL MEMBRANE; CELL SURFACE; CYTOPLASM; DRUG MECHANISM; EFFEROCYTOSIS; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME REGULATION; GOLGI COMPLEX; MACROPHAGE; MEMBRANE BIOLOGY; PRIORITY JOURNAL; ADVERSE EFFECTS; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BRONCHUS; CELL CULTURE; DRUG EFFECTS; ENZYMOLOGY; EPITHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN; LUNG ALVEOLUS MACROPHAGE; PATHOLOGY; PHAGOCYTOSIS; PHOSPHORYLATION; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SIGNAL TRANSDUCTION; SMOKING;

BRONCHI; CELLS, CULTURED; EPITHELIAL CELLS; FINGOLIMOD HYDROCHLORIDE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; IMMUNOSUPPRESSIVE AGENTS; LYSOPHOSPHOLIPIDS; MACROPHAGES, ALVEOLAR; PHAGOCYTOSIS; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SIGNAL TRANSDUCTION; SMOKING; SPHINGOSINE;

EID: 84976601968     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A1015-471R     Document Type: Article

References (39)

1. Hodge, S., Hodge, G., Holmes, M., Reynolds, P. N. (2005) Increased airway epithelial and T-cell apoptosis in COPD remains despite smoking cessation. Eur. Respir. J. 25, 447–454.
2. Respiratory Failure Research Group in Japan. (2004) Increased levels of cell death and proliferation in alveolar wall cells in patients with pulmonary emphysema. Chest 125, 626–632.
3. Hart, S. P., Haslett, C., Dransfield, I. (1996) Recognition of apoptotic cells by phagocytes. Experientia 52, 950–956.
4. Hodge, S., Hodge, G., Scicchitano, R., Reynolds, P. N., Holmes, M. (2003) Alveolar macrophages from subjects with chronic obstructive pulmonary disease are deficient in their ability to phagocytose apoptotic airway epithelial cells. Immunol. Cell Biol. 81, 289–296.
5. Hodge, S., Hodge, G., Ahern, J., Jersmann, H., Holmes, M., Reynolds, P. N. (2007) Smoking alters alveolar macrophage recognition and phagocytic ability: implications in chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol. 37, 748–755.
6. Hodge, S., Hodge, G., Jersmann, H., Matthews, G., Ahern, J., Holmes, M., Reynolds, P. N. (2008) Azithromycin improves macrophage phagocytic function and expression of mannose receptor in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 178, 139–148.
7. Hodge, S., Reynolds, P. N. (2012) Low-dose azithromycin improves phagocytosis of bacteria by both alveolar and monocyte-derived macrophages in chronic obstructive pulmonary disease subjects. Respirology 17, 802–807.
8. Van Brocklyn, J. R., Williams, J. B. (2012) The control of the balance between ceramide and sphingosine-1-phosphate by sphingosine kinase: oxidative stress and the seesaw of cell survival and death. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 163, 26–36.
9. Petrusca, D. N., Gu, Y., Adamowicz, J. J., Rush, N. I., Hubbard, W. C., Smith, P. A., Berdyshev, E. V., Birukov, K. G., Lee, C. H., Tuder, R. M., Twigg H. L., Vandivier, R. W., Petrache, I. (2010) Sphingolipidmediated inhibition of apoptotic cell clearance by alveolar macrophages. J. Biol. Chem. 285, 40322–40332.
10. McQuiston, T., Luberto, C., Del Poeta, M. (2011) Role of sphingosine- 1-phosphate (S1P) and S1P receptor 2 in the phagocytosis of Cryptococcus neoformans by alveolar macrophages. Microbiology 157, 1416–1427.
11. Kusner, D. J., Thompson, C. R., Melrose, N. A., Pitson, S. M., Obeid, L. M., Iyer, S. S. (2007) The localization and activity of sphingosine kinase 1 are coordinately regulated with actin cytoskeletal dynamics in macrophages. J. Biol. Chem. 282, 23147–23162.
12. Kuehnel, M. P., Reiss, M., Anand, P. K., Treede, I., Holzer, D., Hoffmann, E., Klapperstueck, M., Steinberg, T. H., Markwardt, F., Griffiths, G. (2009) Sphingosine-1-phosphate receptors stimulate macrophage plasma-membrane actin assembly via ADP release, ATP synthesis and P2X7R activation. J. Cell Sci. 122, 505–512.
13. Cordts, F., Pitson, S., Tabeling, C., Gibbins, I., Moffat, D. F., Jersmann, H., Hodge, S., Haberberger, R. V. (2011) Expression profile of the sphingosine kinase signalling system in the lung of patients with chronic obstructive pulmonary disease. Life Sci. 89, 806–811.
14. Barnawi, J., Tran, H., Jersmann, H., Pitson, S., Roscioli, E., Hodge, G., Meech, R., Haberberger, R., Hodge, S. (2015) Potential link between the sphingosine-1-phosphate (S1P) system and defective alveolar macrophage phagocytic function in chronic obstructive pulmonary disease/emphysema (COPD). PLoS One 10, e0122771.
15. Gonzalez-Cabrera, P. J., Brown, S., Studer, S. M., Rosen, H. (2014) S1P signaling: new therapies and opportunities. F1000Prime Rep. 6, 109.
16. Berdyshev, E.V., Gorshkova, I., Skobeleva, A., Bittman, R., Lu, X., Dudek, S.M., Mirzapoiazova, T., Garcia, J.G., Natarajan, V. (2009) FTY720 inhibits ceramide synthases and up-regulates dihydrosphingosine 1- phosphate formation in human lung endothelial cells. J. Biol. Chem. 284, 5467–5477.
17. Willis, M. A., Cohen, J. A. (2013) Fingolimod therapy for multiple sclerosis. Semin. Neurol. 33, 37–44.
18. Dehle, F., Mukaro, V., Jurisevic, C., Moffat, D., Meredith, D., Holmes, M., Hodge, G., Jersmann, H., Reynolds, P. N., Hodge, S. (2013) Defective lung macrophage function in lung cancer 6 chronic obstructive pulmonary disease (COPD/emphysema)-mediated by cancer cell production of PGE2? PLoS One 8, e61573.
19. Mukaro, V. R., Bylund, J., Hodge, G., Holmes, M., Jersmann, H., Reynolds, P. N., Hodge, S. (2013) Lectins offer new perspectives in the development of macrophage-targeted therapies for COPD/emphysema. PLoS One 8, e56147.
20. Tran, H. B., Ahern, J., Hodge, G., Holt, P., Dean, M. M., Reynolds, P. N., Hodge, S. (2014) Oxidative stress decreases functional airway mannose binding lectin in COPD. PLoS One 9, e98571.
21. Pitman, M. R., Pham, D. H., Pitson, S. M. (2012) Isoform-selective assays for sphingosine kinase activity. Methods Mol. Biol. 874, 21–31.
22. Maceyka, M., Sankala, H., Hait, N. C., Le Stunff, H., Liu, H., Toman, R., Collier, C., Zhang, M., Satin, L. S., Merrill, Jr., A. H., Milstien, S., Spiegel, S. (2005) SphK1 and SphK2, sphingosine kinase isoenzymes with opposing functions in sphingolipid metabolism. J. Biol. Chem. 280, 37118–37129.
23. Pitson, S. M., Moretti, P. A. B., Zebol, J. R., Lynn, H. E., Xia, P., Vadas, M. A., Wattenberg, B. W. (2003) Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J. 22, 5491–5500.
24. Pitson, S. M., Xia, P., Leclercq, T. M., Moretti, P. A. B., Zebol, J. R., Lynn, H. E., Wattenberg, B. W., Vadas, M. A. (2005) Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J. Exp. Med. 201, 49–54.
25. Johnson, K. R., Becker, K. P., Facchinetti, M. M., Hannun, Y. A., Obeid, L. M. (2002) PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane. Extracellular release of sphingosine-1-phosphate induced by phorbol 12-myristate 13-acetate (PMA). J. Biol. Chem. 277, 35257–35262.
26. Siow, D. L., Anderson, C. D., Berdyshev, E. V., Skobeleva, A., Pitson, S. M., Wattenberg, B. W. (2010) Intracellular localization of sphingosine kinase 1 alters access to substrate pools but does not affect the degradative fate of sphingosine-1-phosphate. J. Lipid Res. 51, 2546–2559.
27. Shen, H., Giordano, F., Wu, Y., Chan, J., Zhu, C., Milosevic, I., Wu, X., Yao, K., Chen, B., Baumgart, T., Sieburth, D., De Camilli, P. (2014) Coupling between endocytosis and sphingosine kinase 1 recruitment. Nat. Cell Biol. 16, 652–662.
28. Takabe, K., Paugh, S. W., Milstien, S., Spiegel, S. (2008) “Inside-out” signaling of sphingosine-1-phosphate: therapeutic targets. Pharmacol. Rev. 60, 181–195.
29. Kim, R. H., Takabe, K., Milstien, S., Spiegel, S. (2009) Export and functions of sphingosine-1-phosphate. Biochim. Biophys. Acta 1791, 692–696.
30. Strub, G. M., Paillard, M., Liang, J., Gomez, L., Allegood, J. C., Hait, N. C., Maceyka, M., Price, M. M., Chen, Q., Simpson, D. C., Kordula, T., Milstien, S., Lesnefsky, E. J., Spiegel, S. (2011) Sphingosine-1-phosphate produced by sphingosine kinase 2 in mitochondria interacts with prohibitin 2 to regulate complex IV assembly and respiration. FASEB J. 25, 600–612.
31. Hait, N. C., Allegood, J., Maceyka, M., Strub, G. M., Harikumar, K. B., Singh, S. K., Luo, C., Marmorstein, R., Kordula, T., Milstien, S., Spiegel, S. (2009) Regulation of histone acetylation in the nucleus by sphingosine-1- phosphate. Science 325, 1254–1257.
32. Ding, G., Sonoda, H., Yu, H., Kajimoto, T., Goparaju, S. K., Jahangeer, S., Okada, T., Nakamura, S. (2007) Protein kinase D-mediated phosphorylation and nuclear export of sphingosine kinase 2. J. Biol. Chem. 282, 27493–27502.
33. Noda, N., Matsumoto, K., Fukuyama, S., Asai, Y., Kitajima, H., Seki, N., Matsunaga, Y., Moriwaki, A., Morimoto, K., Inoue, H., Nakanishi, Y. (2013) Cigarette smoke impairs phagocytosis of apoptotic neutrophils by alveolar macrophages via inhibition of the histone deacetylase/Rac/CD9 pathways. Int. Immunol. 25, 643–650.
34. Uesugi, A., Kataoka, A., Tozaki-Saitoh, H., Koga, Y., Tsuda, M., Robaye, B., Boeynaems, J. M., Inoue, K. (2012) Involvement of protein kinase D in uridine diphosphate-induced microglial macropinocytosis and phagocytosis. Glia 60, 1094–1105.
35. Natarajan, V., Dudek, S. M., Jacobson, J. R., Moreno-Vinasco, L., Huang, L. S., Abassi, T., Mathew, B., Zhao, Y., Wang, L., Bittman, R., Weichselbaum, R., Berdyshev, E., Garcia, J. G. N. (2013) Sphingosine-1-phosphate, FTY720, and sphingosine-1-phosphate receptors in the pathobiology of acute lung injury. Am. J. Respir. Cell Mol. Biol. 49, 6–17.
36. Konishi, K., Inobe, M., Yamada, A., Murakami, M., Todo, S., Uede, T. (2002) Combination treatment with FTY720 and CTLA4IgG preserves the respiratory epithelium and prevents obliterative disease in a murine airway model. J. Heart Lung Transplant. 21, 692–700.
37. Huwiler, A., Pfeilschifter, J. (2008) New players on the center stage: sphingosine 1-phosphate and its receptors as drug targets. Biochem. Pharmacol. 75, 1893–1900.
38. Tonelli, F., Lim, K. G., Loveridge, C., Long, J., Pitson, S. M., Tigyi, G., Bittman, R., Pyne, S., Pyne, N. J. (2010) FTY720 and (S)-FTY720 vinylphosphonate inhibit sphingosine kinase 1 and promote its proteasomal degradation in human pulmonary artery smooth muscle, breast cancer and androgen-independent prostate cancer cells. Cell. Signal. 22, 1536–1542.
39. Vessey, D. A., Kelley, M., Zhang, J., Li, L., Tao, R., Karliner, J. S. (2007) Dimethylsphingosine and FTY720 inhibit the SK1 form but activate the SK2 form of sphingosine kinase from rat heart. J. Biochem. Mol. Toxicol. 21, 273–279.