Lysosome fusion to the cell membrane is mediated by the dysferlin C2A domain in coronary arterial endothelial cells

Journal of Cell Science

Volumn 125, Issue 5, 2012, Pages 1225-1234

  Han, Wei Qing ^a   Xia, Min ^a   Xu, Ming ^a   Boini, Krishna M ^a   Ritter, Joseph K ^a   Li, Ning Jun ^a   Li, Pin Lan ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Arterial endothelium; Ferlin; Molecular trafficking; Vesicle fusion

Indexed keywords

CERAMIDE; DYSFERLIN; FAS LIGAND; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORONARY ARTERY; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY ENDOTHELIUM CELL; ENDOTHELIUM CELL; GENE SILENCING; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; VASODILATATION;

ANIMALS; CATTLE; CELL MEMBRANE; CERAMIDES; CORONARY VESSELS; ENDOTHELIAL CELLS; FAS LIGAND PROTEIN; LYSOSOMES; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MUSCLE PROTEINS; NADPH OXIDASE; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN TRANSPORT; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

BOVINAE;

EID: 84861364532     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.094565     Document Type: Article

References (46)

1. Azakir, B. A., Di Fulvio, S., Therrien, C. and Sinnreich, M. (2010). Dysferlin interacts with tubulin and microtubules in mouse skeletal muscle. PLoS ONE 5, e10122.
2. Bao, J. X., Jin, S., Zhang, F., Wang, Z. C., Li, N. and Li, P. L. (2010). Activation of membrane NADPH oxidase associated with lysosome-targeted acid sphingomyelinase in coronary endothelial cells. Antioxid. Redox. Signal. 12, 703-712.
3. Bommert, K., Charlton, M. P., DeBello, W. M., Chin, G. J., Betz, H. and Augustine, G. J. (1993). Inhibition of neurotransmitter release by C2-domain peptides implicates synaptotagmin in exocytosis. Nature 363, 163-165.
4. Brandin, L., Bergstrom, G., Manhem, K. and Gustafsson, H. (2003). Oestrogen modulates vascular adrenergic reactivity of the spontaneously hypertensive rat. J. Hypertens. 21, 1695-1702.
5. Bund, S. J. and Lee, R. M. (2003). Arterial structural changes in hypertension: a consideration of methodology, terminology and functional consequence. J. Vasc. Res. 40, 547-557.
6. Cenacchi, G., Fanin, M., De Giorgi, L. B. and Angelini, C. (2005). Ultrastructural changes in dysferlinopathy support defective membrane repair mechanism. J. Clin. Pathol. 58, 190-195.
7. Chai, Y., Huang, X., Cong, B., Liu, S., Chen, K., Li, G. and Gaisano, H. Y. (2006). Involvement of VAMP-2 in exocytosis of IL-1 beta in turbot (Scophthalmus maximus) leukocytes after Vibrio anguillarum infection. Biochem. Biophys. Res. Commun. 342, 509-513.
8. Davis, D. B., Doherty, K. R., Delmonte, A. J. and McNally, E. M. (2002). Calciumsensitive phospholipid binding properties of normal and mutant ferlin C2 domains. J. Biol. Chem. 277, 22883-22888.
9. Demonbreun, A. R., Fahrenbach, J. P., Deveaux, K., Earley, J. U., Pytel, P. and McNally, E. M. (2011). Impaired muscle growth and response to insulin-like growth factor 1 in dysferlin-mediated muscular dystrophy. Hum. Mol. Genet. 20, 779-789.
10. Doherty, K. R. and McNally, E. M. (2003). Repairing the tears: dysferlin in muscle membrane repair. Trends Mol. Med. 9, 327-330.
11. Eum, S. Y., Andras, I., Hennig, B. and Toborek, M. (2009). NADPH oxidase and lipid raft-associated redox signaling are required for PCB153-induced upregulation of cell adhesion molecules in human brain endothelial cells. Toxicol. Appl. Pharmacol. 240, 299-305.
12. Evesson, F. J., Peat, R. A., Lek, A., Brilot, F., Lo, H. P., Dale, R. C., Parton, R. G., North, K. N. and Cooper, S. T. (2010). Reduced plasma membrane expression of dysferlin mutants is attributed to accelerated endocytosis via a syntaxin-4-associated pathway. J. Biol. Chem. 285, 28529-28539.
13. Gulbins, E. and Li, P. L. (2006). Physiological and pathophysiological aspects of ceramide. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R11-R26.
14. Han, R., Bansal, D., Miyake, K., Muniz, V. P., Weiss, R. M., McNeil, P. L. and Campbell, K. P. (2007). Dysferlin-mediated membrane repair protects the heart from stress-induced left ventricular injury. J. Clin. Invest. 117, 1805-1813.
15. Harata, N. C., Choi, S., Pyle, J. L., Aravanis, A. M. and Tsien, R. W. (2006). Frequency-dependent kinetics and prevalence of kiss-and-run and reuse at hippocampal synapses studied with novel quenching methods. Neuron 49, 243-256.
16. Hochmeister, S., Grundtner, R., Bauer, J., Engelhardt, B., Lyck, R., Gordon, G., Korosec, T., Kutzelnigg, A., Berger, J. J., Bradl, M. et al. (2006). Dysferlin is a new marker for leaky brain blood vessels in multiple sclerosis. J. Neuropathol. Exp. Neurol. 65, 855-865.
17. Illarioshkin, S. N., Ivanova-Smolenskaya, I. A., Greenberg, C. R., Nylen, E., Sukhorukov, V. S., Poleshchuk, V. V., Markova, E. D. and Wrogemann, K. (2000). Identical dysferlin mutation in limb-girdle muscular dystrophy type 2B and distal myopathy. Neurology 55, 1931-1933.
18. Jia, S. J., Jin, S., Zhang, F., Yi, F., Dewey, W. L. and Li, P. L. (2008). Formation and function of ceramide-enriched membrane platforms with CD38 during M1-receptor stimulation in bovine coronary arterial myocytes. Am. J. Physiol. Heart Circ. Physiol. 295, H1743-H1752.
19. Jin, S., Yi, F. and Li, P. L. (2007). Contribution of lysosomal vesicles to the formation of lipid raft redox signaling platforms in endothelial cells. Antioxid. Redox Signal. 9, 1417-1426.
20. Jin, S., Zhang, Y., Yi, F. and Li, P. L. (2008a). Critical role of lipid raft redox signaling platforms in endostatin-induced coronary endothelial dysfunction. Arterioscler. Thromb. Vasc. Biol. 28, 485-490.
21. Jin, S., Yi, F., Zhang, F., Poklis, J. L. and Li, P. L. (2008b). Lysosomal targeting and trafficking of acid sphingomyelinase to lipid raft platforms in coronary endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28, 2056-2062.
22. Johnson, J. E., Rao, N. M., Hui, S. W. and Cornell, R. B. (1998). Conformation and lipid binding properties of four peptides derived from the membrane-binding domain of CTP:phosphocholine cytidylyltransferase. Biochemistry 37, 9509-9519.
23. Karsan, A., Blonder, J., Law, J., Yaquian, E., Lucas, D. A., Conrads, T. P. and Veenstra, T. (2005). Proteomic analysis of lipid microdomains from lipopolysaccharide-activated human endothelial cells. J. Proteome Res. 4, 349-357.
24. Kobayashi, T. and Arakawa, Y. (1991). Transport of exogenous fluorescent phosphatidylserine analogue to the Golgi apparatus in cultured fibroblasts. J. Cell Biol. 113, 235-244.
25. Lek, A., Evesson, F. J., Sutton, R. B., North, K. N. and Cooper, S. T. (2011). Ferlins: regulators of vesicle fusion for auditory neurotransmission, receptor trafficking and membrane repair. Traffic 13, 185-194.
26. Lennon, N. J., Kho, A., Bacskai, B. J., Perlmutter, S. L., Hyman, B. T. and Brown, R. H., Jr (2003). Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing. J. Biol. Chem. 278, 50466-50473.
27. Li, N., Yi, F., Sundy, C. M., Chen, L., Hilliker, M. L., Donley, D. K., Muldoon, D. B. and Li, P. L. (2007). Expression and actions of HIF prolyl-4-hydroxylase in the rat kidneys. Am. J. Physiol. Renal Physiol. 292, F207-F216.
28. Li, N., Chen, L., Yi, F., Xia, M. and Li, P. L. (2008). Salt-sensitive hypertension induced by decoy of transcription factor hypoxia-inducible factor-1alpha in the renal medulla. Circ. Res. 102, 1101-1108.
29. Li, P. L., Zhang, Y. and Yi, F. (2007). Lipid raft redox signaling platforms in endothelial dysfunction. Antioxid. Redox Signal. 9, 1457-1470.
30. Matsuda, C., Aoki, M., Hayashi, Y. K., Ho, M. F., Arahata, K. and Brown, R. H., Jr (1999). Dysferlin is a surface membrane-associated protein that is absent in Miyoshi myopathy. Neurology 53, 1119-1122.
31. McNeil, A. K., Rescher, U., Gerke, V. and McNeil, P. L. (2006). Requirement for annexin A1 in plasma membrane repair. J. Biol. Chem. 281, 35202-35207.
32. Pang, H., Le, P. U. and Nabi, I. R. (2004). Ganglioside GM1 levels are a determinant of the extent of caveolae/raft-dependent endocytosis of cholera toxin to the Golgi apparatus. J. Cell Sci. 117, 1421-1430.
33. Reddy, A., Caler, E. V. and Andrews, N. W. (2001). Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell 106, 157-169.
34. Shao, D., Segal, A. W. and Dekker, L. V. (2003). Lipid rafts determine efficiency of NADPH oxidase activation in neutrophils. FEBS Lett. 550, 101-106.
35. Therrien, C., Di Fulvio, S., Pickles, S. and Sinnreich, M. (2009). Characterization of lipid binding specificities of dysferlin C2 domains reveals novel interactions with phosphoinositides. Biochemistry 48, 2377-2384.
36. Touyz, R. M. (2006). Lipid rafts take center stage in endothelial cell redox signaling by death receptors. Hypertension 47, 16-18.
37. Uchida, K., Emoto, K., Daleke, D. L., Inoue, K. and Umeda, M. (1998). Induction of apoptosis by phosphatidylserine. J. Biochem. 123, 1073-1078.
38. Varsano, S., Rashkovsky, L., Shapiro, H. and Radnay, J. (1998). Cytokines modulate expression of cell-membrane complement inhibitory proteins in human lung cancer cell lines. Am. J. Respir. Cell. Mol. Biol. 19, 522-529.
39. Yi, F., Zhang, A. Y., Janscha, J. L., Li, P. L. and Zou, A. P. (2004). Homocysteine activates NADH/NADPH oxidase through ceramide-stimulated Rac GTPase activity in rat mesangial cells. Kidney Int. 66, 1977-1987.
40. Yi, F., Jin, S., Zhang, F., Xia, M., Bao, J. X., Hu, J., Poklis, J. L. and Li, P. L. (2009). Formation of lipid raft redox signalling platforms in glomerular endothelial cells: an early event of homocysteine-induced glomerular injury. J. Cell Mol. Med. 13, 3303-3314.
41. Zhang, A. Y., Yi, F., Zhang, G., Gulbins, E. and Li, P. L. (2006). Lipid raft clustering and redox signaling platform formation in coronary arterial endothelial cells. Hypertension 47, 74-80.
42. Zhang, A. Y., Yi, F., Jin, S., Xia, M., Chen, Q. Z., Gulbins, E. and Li, P. L. (2007). Acid sphingomyelinase and its redox amplification in formation of lipid raft redox signaling platforms in endothelial cells. Antioxid. Redox Signal. 9, 817-828.
43. Zhang, D. X., Fryer, R. M., Hsu, A. K., Zou, A. P., Gross, G. J., Campbell, W. B. and Li, P. L. (2001). Production and metabolism of ceramide in normal and ischemic-reperfused myocardium of rats. Basic Res. Cardiol. 96, 267-274.
44. Zhang, F., Zhang, G., Zhang, A. Y., Koeberl, M. J., Wallander, E. and Li, P. L. (2006). Production of NAADP and its role in Ca2+ mobilization associated with lysosomes in coronary arterial myocytes. Am. J. Physiol. Heart Circ. Physiol. 291, H274-H282.
45. Zhang, Z., Chen, G., Zhou, W., Song, A., Xu, T., Luo, Q., Wang, W., Gu, X. S. and Duan, S. (2007). Regulated ATP release from astrocytes through lysosome exocytosis. Nat. Cell Biol. 9, 945-953.
46. Zinchuk, V., Zinchuk, O. and Okada, T. (2007). Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem. Cytochem. 40, 101-111.