Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair

Journal of Cell Biology

Volumn 189, Issue 6, 2010, Pages 1027-1038

  Tam, Christina ^a,b   Idone, Vincent ^a   Devlin, Cecilia ^c   Fernandes, Maria Cecilia ^b   Flannery, Andrew ^b   He, Xingxuan ^d   Schuchman, Edward ^d   Tabas, Ira ^e,f   Andrews, Norma W ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Bldg 142   (United States)

^c INDIANA UNIVERSITY   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e Och Spine at New York Presbyterian Hospitals   (United States)

^f NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; DESIPRAMINE; SPHINGOMYELIN PHOSPHODIESTERASE;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; EXOCYTOSIS; HUMAN; HUMAN CELL; NIEMANN PICK DISEASE; PRIORITY JOURNAL;

ANIMALS; CELL LINE; CELL MEMBRANE; CERAMIDES; DESIPRAMINE; ENDOCYTOSIS; ENDOSOMES; ENZYME INHIBITORS; EXOCYTOSIS; GENE SILENCING; HUMANS; LYSOSOMES; NIEMANN-PICK DISEASES; RATS; RECOMBINANT PROTEINS; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELINS;

EID: 77953576191     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201003053     Document Type: Article

References (47)

1. Baron, R., L. Neff, D. Louvard, and P.J. Courtoy. 1985. Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. J. Cell Biol. 101:2210-2222. doi:10.1083/jcb.101.6. 2210
2. Bi, G.Q., J.M. Alderton, and R.A. Steinhardt. 1995. Calcium-regulated exocytosis is required for cell membrane resealing. J. Cell Biol. 131:1747-1758. doi:10.1083/jcb.131.6.1747
3. Chakrabarti, S., K.S. Kobayashi, R.A. Flavell, C.B. Marks, K. Miyake, D.R. Liston, K.T. Fowler, F.S. Gorelick, and N.W. Andrews. 2003. Impaired membrane resealing and autoimmune myositis in synaptotagmin VII- deficient mice. J. Cell Biol. 162:543-549. doi:10.1083/jcb.200305131
4. Chambers, R., and E.L. Chambers. 1961. Explorations into the Nature of the Living Cell. Harvard University Press, Cambridge, MA. 352 pp.
5. Egberts, F., M. Heinrich, J.M. Jensen, S. Winoto-Morbach, S. Pfeiffer, M. Wickel, M. Schunck, J. Steude, P. Saftig, E. Proksch, and S. Schütze. 2004. Cathepsin D is involved in the regulation of transglutaminase 1 and epidermal differentiation. J. Cell Sci. 117:2295-2307. doi:10.1242/jcs.01075
6. Fensome-Green, A., N. Stannard, M. Li, S. Bolsover, and S. Cockcroft. 2007. Bromoenol lactone, an inhibitor of Group V1A calcium-independent phospholipase A2 inhibits antigen-stimulated mast cell exocytosis without blocking Ca2+ influx. Cell Calcium. 41:145-153. doi:10.1016/j.ceca.2006.06.002
7. Godell, C.M., M.E. Smyers, C.S. Eddleman, M.L. Ballinger, H.M. Fishman, and G.D. Bittner. 1997. Calpain activity promotes the sealing of severed giant axons. Proc. Natl. Acad. Sci. USA. 94:4751-4756. doi:10.1073/pnas.94.9.4751
8. Grassmé, H., V. Jendrossek, A. Riehle, G. von Kürthy, J. Berger, H. Schwarz, M. Weller, R. Kolesnick, and E. Gulbins. 2003. Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med. 9:322-330. doi:10.1038/nm823
9. Grassmé, H., J. Riethmüller, and E. Gulbins. 2007. Biological aspects of ceramide-enriched membrane domains. Prog. Lipid Res. 46:161-170. doi:10.1016/j.plipres.2007.03.002
10. Gulbins, E. 2003. Regulation of death receptor signaling and apoptosis by ceramide. Pharmacol. Res. 47:393-399. doi:10.1016/S1043-6618(03)00052-5
11. Gulbins, E., and R. Kolesnick. 2003. Raft ceramide in molecular medicine. Oncogene. 22:7070-7077. doi:10.1038/sj.onc.1207146
12. He, X., S.R. Miranda, X. Xiong, A. Dagan, S. Gatt, and E.H. Schuchman. 1999. Characterization of human acid sphingomyelinase purified from the media of overexpressing Chinese hamster ovary cells. Biochim. Biophys. Acta. 1432:251-264.
13. Heilbrunn, L.V. 1956. The Dynamics of Living Protoplasm. Academic Press, New York. 327 pp.
14. Holopainen, J.M., M.I. Angelova, and P.K. Kinnunen. 2000. Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys. J. 78:830-838. doi:10.1016/S0006-3495(00)76640-9
15. Horinouchi, K., S. Erlich, D.P. Perl, K. Ferlinz, C.L. Bisgaier, K. Sandhoff, R.J. Desnick, C.L. Stewart, and E.H. Schuchman. 1995. Acid sphingomyelinase deficient mice: a model of types A and B Niemann-Pick disease. Nat. Genet. 10:288-293. doi:10.1038/ng0795-288
16. Idone, V., C. Tam, and N.W. Andrews. 2008a. Two-way traffic on the road to plasma membrane repair. Trends Cell Biol. 18:552-559. doi:10.1016/j.tcb.2008. 09.001
17. 2+-dependent endocytosis. J. Cell Biol. 180:905-914. doi:10.1083/jcb.200708010
18. Inada, R., M. Matsuki, K. Yamada, Y. Morishima, S.C. Shen, N. Kuramoto, H. Yasuno, K. Takahashi, Y. Miyachi, and K. Yamanishi. 2000. Facilitated wound healing by activation of the Transglutaminase 1 gene. Am. J. Pathol. 157:1875-1882.
19. Jaiswal, J.K., N.W. Andrews, and S.M. Simon. 2002. Membrane proximal lysosomes are the major vesicles responsible for calcium-dependent exocytosis in nonsecretory cells. J. Cell Biol. 159:625-635. doi:10.1083/jcb.200208154
20. Jensen, J.M., R. Fölster-Holst, A. Baranowsky, M. Schunck, S. Winoto-Morbach, C. Neumann, S. Schütze, and E. Proksch. 2004. Impaired sphingomyelinase activity and epidermal differentiation in atopic dermatitis. J. Invest. Dermatol. 122:1423-1431. doi:10.1111/j.0022-202X.2004.22621.x
21. Kölzer, M., N. Werth, and K. Sandhoff. 2004. Interactions of acid sphingomyelinase and lipid bilayers in the presence of the tricyclic antidepressant desipramine. FEBS Lett. 559:96-98. doi:10.1016/S0014-5793(04) 00033-X
22. Linke, T., G. Wilkening, S. Lansmann, H. Moczall, O. Bartelsen, J. Weisgerber, and K. Sandhoff. 2001. Stimulation of acid sphingomyelinase activity by lysosomal lipids and sphingolipid activator proteins. Biol. Chem. 382:283-290. doi:10.1515/BC.2001.035
23. Loike, J.D., and S.C. Silverstein. 1983. A fluorescence quenching technique using trypan blue to differentiate between attached and ingested glutaraldehyde- fixed red blood cells in phagocytosing murine macrophages. J. Immunol. Methods. 57:373-379. doi:10.1016/0022-1759(83)90097-2
24. McNeil, P.L., and R.A. Steinhardt. 2003. Plasma membrane disruption: repair, prevention, adaptation. Annu. Rev. Cell Dev. Biol. 19:697-731. doi:10.1146/annurev.cellbio.19.111301.140101
25. McNeil, P.L., S.S. Vogel, K. Miyake, and M. Terasaki. 2000. Patching plasma membrane disruptions with cytoplasmic membrane. J. Cell Sci. 113: 1891-1902.
26. McNeil, P.L., K. Miyake, and S.S. Vogel. 2003. The endomembrane requirement for cell surface repair. Proc. Natl. Acad. Sci. USA. 100:4592-4597. doi:10.1073/pnas.0736739100
27. Mellgren, R.L., W. Zhang, K. Miyake, and P.L. McNeil. 2007. Calpain is required for the rapid, calcium-dependent repair of wounded plasma membrane. J. Biol. Chem. 282:2567-2575. doi:10.1074/jbc.M604560200
28. Miyake, K., and P.L. McNeil. 1995. Vesicle accumulation and exocytosis at sites of plasma membrane disruption. J. Cell Biol. 131:1737-1745. doi:10.1083/jcb.131.6.1737
29. Pearson, A.M., K. Baksa, M. Rämet, M. Protas, M. McKee, D. Brown, and R.A. Ezekowitz. 2003. Identification of cytoskeletal regulatory proteins required for efficient phagocytosis in Drosophila. Microbes Infect. 5:815-824. doi:10.1016/S1286-4579(03)00157-6
30. Rao, S.K., C. Huynh, V. Proux-Gillardeaux, T. Galli, and N.W. Andrews. 2004. Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. J. Biol. Chem. 279:20471-20479. doi:10.1074/jbc .M400798200
31. Reddy, A., E.V. Caler, and N.W. Andrews. 2001. Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell. 106:157-169. doi:10.1016/S0092-8674(01)00421-4
32. 2+-regulated exocytic vesicles in fibroblasts and epithelial cells. J. Cell Biol. 137:93-104. doi:10.1083/jcb.137.1.93
33. Santana, P., L.A. Peña, A. Haimovitz-Friedman, S. Martin, D. Green, M. McLoughlin, C. Cordon-Cardo, E.H. Schuchman, Z. Fuks, and R. Kolesnick. 1996. Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell. 86:189-199. doi:10.1016/S0092-8674(00) 80091-4
34. Schissel, S.L., X. Jiang, J. Tweedie-Hardman, T. Jeong, E.H. Camejo, J. Najib, J.H. Rapp, K.J. Williams, and I. Tabas. 1998. Secretory sphingomyelinase, a product of the acid sphingomyelinase gene, can hydrolyze atherogenic lipoproteins at neutral pH. Implications for atherosclerotic lesion development. J. Biol. Chem. 273:2738-2746. doi:10.1074/jbc.273.5.2738
35. Schmuth, M., M.Q. Man, F. Weber, W. Gao, K.R. Feingold, P. Fritsch, P.M. Elias, and W.M. Holleran. 2000. Permeability barrier disorder in Niemann-Pick disease: sphingomyelin-ceramide processing required for normal barrier homeostasis. J. Invest. Dermatol. 115:459-466. doi:10.1046/j.1523-1747.2000. 00081.x
36. Schuchman, E.H. 2007. The pathogenesis and treatment of acid sphingomyelinase-deficient Niemann-Pick disease. J. Inherit. Metab. Dis. 30:654-663. doi:10 .1007/s10545-007-0632-9
37. Schuchman, E.H. 2010. Acid sphingomyelinase, cell membranes and human disease: lessons from Niemann-Pick disease. FEBS Lett. 584:1895-1900. doi:10.1016/j.febslet.2009.11.083
38. Schuchman, E.H., M. Suchi, T. Takahashi, K. Sandhoff, and R.J. Desnick. 1991. Human acid sphingomyelinase. Isolation, nucleotide sequence and expression of the full-length and alternatively spliced cDNAs. J. Biol. Chem. 266:8531-8539.
39. Slot, J.W., and H.J. Geuze. 1985. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur. J. Cell Biol. 38:87-93.
40. Steinhardt, R.A., G. Bi, and J.M. Alderton. 1994. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science. 263:390-393. doi:10.1126/science.7904084
41. Togo, T., J.M. Alderton, G.Q. Bi, and R.A. Steinhardt. 1999. The mechanism of facilitated cell membrane resealing. J. Cell Sci. 112:719-731.
42. Trajkovic, K., C. Hsu, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, P. Schwille, B. Brügger, and M. Simons. 2008. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 319:1244-1247. doi:10.1126/science.1153124
43. van Blitterswijk, W.J., A.H. van der Luit, R.J. Veldman, M. Verheij, and J. Borst. 2003. Ceramide: second messenger or modulator of membrane structure and dynamics? Biochem. J. 369:199-211. doi:10.1042/BJ20021528
44. Walev, I., S.C. Bhakdi, F. Hofmann, N. Djonder, A. Valeva, K. Aktories, and S. Bhakdi. 2001. Delivery of proteins into living cells by reversible membrane permeabilization with streptolysin-O. Proc. Natl. Acad. Sci. USA. 98:3185-3190. doi:10.1073/pnas.051429498
45. Weisleder, N., H. Takeshima, and J. Ma. 2009. Mitsugumin 53 (MG53) facilitates vesicle trafficking in striated muscle to contribute to cell membrane repair. Commun. Integr. Biol. 2:225-226.
46. Zeidan, Y.H., and Y.A. Hannun. 2007. Activation of acid sphingomyelinase by protein kinase Cdelta-mediated phosphorylation. J. Biol. Chem. 282:11549-11561. doi:10.1074/jbc.M609424200
47. Zha, X., L.M. Pierini, P.L. Leopold, P.J. Skiba, I. Tabas, and F.R. Maxfield. 1998. Sphingomyelinase treatment induces ATP-independent endocytosis. J. Cell Biol. 140:39-47. doi:10.1083/jcb.140.1.39