Golgi-to-phagosome transport of acid sphingomyelinase and prosaposin is mediated by sortilin

Journal of Cell Science

Volumn 123, Issue 14, 2010, Pages 2502-2511

  Wähe, Anna ^a,h   Kasmapour, Bahram ^a,b   Schmaderer, Christoph ^c,d   Liebl, David ^a,i   Sandhoff, Konrad ^e   Nykjaer, Anders ^f   Griffiths, Gareth ^a,g   Gutierrez, Maximiliano G ^a,b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF BONN   (Germany)

^f AARHUS UNIVERSITY   (Denmark)

^g UNIVERSITY OF OSLO   (Norway)

^h UNIVERSITY OF MUNICH   (Germany)

ⁱ UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Golgi; Phagosome; Sortilin

Indexed keywords

BREFELDIN A; CATHEPSIN D; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; PROSAPOSIN; SORTILIN; SPHINGOMYELIN PHOSPHODIESTERASE; TUBULIN;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; GOLGI COMPLEX; MACROPHAGE; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BREFELDIN A; CELL LINE, TUMOR; FEMALE; GOLGI APPARATUS; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PHAGOCYTOSIS; PHAGOSOMES; PROTEIN TRANSPORT; SAPOSINS; SPHINGOMYELIN PHOSPHODIESTERASE;

MUS;

EID: 77954898687     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.067686     Document Type: Article

References (50)

1. Anes, E., Kuhnel, M. P., Bos, E., Moniz-Pereira, J., Habermann, A. and Griffiths, G. (2003). Selected lipids activate phagosome actin assembly and maturation resulting in killing of pathogenic mycobacteria. Nat. Cell Biol. 5, 793-802. (Pubitemid 37087167)
2. Anes, E., Peyron, P., Staali, L., Jordao, L., Gutierrez, M. G., Kress, H., Hagedorn, M., Maridonneau-Parini, I., Skinner, M. A., Wildeman, A. G. et al. (2006). Dynamic life and death interactions between Mycobacterium smegmatis and J774 macrophages. Cell Microbiol. 8, 939-960.
3. Beron, W., Alvarez-Dominguez, C., Mayorga, L. and Stahl, P. D. (1995). Membrane trafficking along the phagocytic pathway. Trends Cell. Biol. 5, 100-104.
4. Bonifacino, J. S. and Rojas, R. (2006). Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 7, 568-579.
5. Braulke, T. and Bonifacino, J. S. (2009). Sorting of lysosomal proteins. Biochim. Biophys. Acta 1793, 605-614.
6. Bujny, M. V., Ewels, P. A., Humphrey, S., Attar, N., Jepson, M. A. and Cullen, P. J. (2008). Sorting nexin-1 defines an early phase of Salmonella-containing vacuole-remodeling during Salmonella infection. J. Cell Sci. 121, 2027-2036. (Pubitemid 352015200)
7. Canuel, M., Korkidakis, A., Konnyu, K. and Morales, C. R. (2008). Sortilin mediates the lysosomal targeting of cathepsins D and H. Biochem. Biophys. Res. Commun. 373, 292-297.
8. Claus, V., Jahraus, A., Tjelle, T., Berg, T., Kirschke, H., Faulstich, H. and Griffiths, G. (1998). Lysosomal enzyme trafficking between phagosomes, endosomes, and lysosomes in J774 macrophages. Enrichment of cathepsin H in early endosomes. J. Biol. Chem. 273, 9842-9851. (Pubitemid 28183080)
9. De la Fuente, M., Garrido, J. J., Arahuetes, R. M. and Hernanz, A. (1993). Stimulation of phagocytic function in mouse macrophages by neurotensin and neuromedin N. J. Neuroimmunol. 42, 97-104.
10. Desjardins, M. and Griffiths, G. (2003). Phagocytosis: latex leads the way. Curr. Opin. Cell Biol. 15, 498-503.
11. Desjardins, M., Huber, L. A., Parton, R. G. and Griffiths, G. (1994). Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124, 677-688. (Pubitemid 24085778)
12. Fratti, R. A., Chua, J. and Deretic, V. (2002). Cellubrevin alterations and Mycobacterium tuberculosis phagosome maturation arrest. J. Biol. Chem. 277, 17320-17326. (Pubitemid 34967768)
13. Fratti, R. A., Chua, J., Vergne, I. and Deretic, V. (2003). Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl. Acad. Sci. USA 100, 5437-5442. (Pubitemid 36542723)
14. Gerisch, G., Benjak, A., Kohler, J., Weber, I. and Schneider, N. (2004). GFP-golvesin constructs to study Golgi tubulation and post-Golgi vesicle dynamics in phagocytosis. Eur. J. Cell Biol. 83, 297-303. (Pubitemid 39307167)
15. Gutierrez, M. G., Mishra, B. B., Jordao, L., Elliott, E., Anes, E. and Griffiths, G. (2008). NF-kappa B activation controls phagolysosome fusion-mediated killing of mycobacteria by macrophages. J. Immunol. 181, 2651-2663.
16. Haas, A. (2007). The phagosome: compartment with a license to kill. Traffic 8, 311-330.
17. Hackstadt, T., Scidmore, M. A. and Rockey, D. D. (1995). Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc. Natl. Acad. Sci. USA 92, 4877-4881.
18. Hackstadt, T., Rockey, D. D., Heinzen, R. A. and Scidmore, M. A. (1996). Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J. 15, 964-977.
19. Jansen, P., Giehl, K., Nyengaard, J. R., Teng, K., Lioubinski, O., Sjoegaard, S. S., Breiderhoff, T., Gotthardt, M., Lin, F., Eilers, A. et al. (2007). Roles for the proneurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat. Neurosci. 10, 1449-1457.
20. Jutras, I. and Desjardins, M. (2005). Phagocytosis: at the crossroads of innate and adaptive immunity. Annu. Rev. Cell Dev. Biol. 21, 511-527. (Pubitemid 41740644)
21. Kim, H. S., Yumkham, S., Choi, J. H., Lee, S. H., Kim, T. H., Ryu, S. H. and Suh, P. G. (2006). Neurotensin enhances nitric oxide generation via the JAK2-STAT1 pathway in murine macrophage Raw264.7 cells during costimulation with LPS and IFNgamma. Neuropeptides 40, 221-229.
22. Kolter, T., Winau, F., Schaible, U. E., Leippe, M. and Sandhoff, K. (2005). Lipid-binding proteins in membrane digestion, antigen presentation, and antimicrobial defense. J. Biol. Chem. 280, 41125-41128. (Pubitemid 41832164)
23. Lefrancois, S., Zeng, J., Hassan, A. J., Canuel, M. and Morales, C. R. (2003). The lysosomal trafficking of sphingolipid activator proteins (SAPs) is mediated by sortilin. EMBO J. 22, 6430-6437. (Pubitemid 38009591)
24. Leippe, M., Bruhn, H., Hecht, O. and Grotzinger, J. (2005). Ancient weapons: the three-dimensional structure of amoebapore A. Trends Parasitol. 21, 5-7. (Pubitemid 40082091)
25. Lippincott-Schwartz, J., Yuan, L., Tipper, C., Amherdt, M., Orci, L. and Klausner, R. D. (1991). Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67, 601-616. (Pubitemid 121001474)
26. Ludwig, T., Griffiths, G. and Hoflack, B. (1991). Distribution of newly synthesized lysosomal enzymes in the endocytic pathway of normal rat kidney cells. J. Cell Biol. 115, 1561-1572. (Pubitemid 21909996)
27. Marcusson, E. G., Horazdovsky, B. F., Cereghino, J. L., Gharakhanian, E. and Emr, S. D. (1994). The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell 77, 579-586. (Pubitemid 24153997)
28. Mari, M., Bujny, M. V., Zeuschner, D., Geerts, W. J., Griffith, J., Petersen, C. M., Cullen, P. J., Klumperman, J. and Geuze, H. J. (2008). SNX1 defines an early endosomal recycling exit for sortilin and mannose 6-phosphate receptors. Traffic 9, 380-393. (Pubitemid 351188997)
29. Martin, S., Vincent, J. P. and Mazella, J. (2003). Involvement of the neurotensin receptor-3 in the neurotensin-induced migration of human microglia. J. Neurosci. 23, 1198-1205. (Pubitemid 36258899)
30. Martin, S., Dicou, E., Vincent, J. P. and Mazella, J. (2005). Neurotensin and the neurotensin receptor-3 in microglial cells. J. Neurosci. Res. 81, 322-326.
31. Mazella, J. (2001). Sortilin/neurotensin receptor-3: a new tool to investigate neurotensin signaling and cellular trafficking? Cell Signal. 13, 1-6.
32. Mazella, J., Zsurger, N., Navarro, V., Chabry, J., Kaghad, M., Caput, D., Ferrara, P., Vita, N., Gully, D., Maffrand, J. P. et al. (1998). The 100-kDa neurotensin receptor is gp95/sortilin, a non-G-protein-coupled receptor. J. Biol. Chem. 273, 26273-26276.
33. Morinville, A., Martin, S., Lavallee, M., Vincent, J. P., Beaudet, A. and Mazella, J. (2004). Internalization and trafficking of neurotensin via NTS3 receptors in HT29 cells. Int. J. Biochem. Cell Biol. 36, 2153-2168.
34. Ni, X. and Morales, C. R. (2006). The lysosomal trafficking of acid sphingomyelinase is mediated by sortilin and mannose 6-phosphate receptor. Traffic 7, 889-902.
35. Nielsen, M. S., Madsen, P., Christensen, E. I., Nykjaer, A., Gliemann, J., Kasper, D., Pohlmann, R. and Petersen, C. M. (2001). The sortilin cytoplasmic tail conveys Golgi-endosome transport and binds the VHS domain of the GGA2 sorting protein. EMBO J. 20, 2180-2190.
36. Nykjaer, A., Lee, R., Teng, K. K., Jansen, P., Madsen, P., Nielsen, M. S., Jacobsen, C., Kliemannel, M., Schwarz, E., Willnow, T. E. et al. (2004). Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-848.
37. Petersen, C. M., Nielsen, M. S., Nykjaer, A., Jacobsen, L., Tommerup, N., Rasmussen, H. H., Roigaard, H., Gliemann, J., Madsen, P. and Moestrup, S. K. (1997). Molecular identification of a novel candidate sorting receptor purified from human brain by receptor-associated protein affinity chromatography. J. Biol. Chem. 272, 3599-3605.
38. Rogers, L. D. and Foster, L. J. (2007). The dynamic phagosomal proteome and the contribution of the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 104, 18520-18525.
39. Rouille, Y., Rohn, W. and Hoflack, B. (2000). Targeting of lysosomal proteins. Semin. Cell Dev. Biol. 11, 165-171.
40. Salcedo, S. P. and Holden, D. W. (2003). SseG, a virulence protein that targets Salmonella to the Golgi network. EMBO J. 22, 5003-5014.
41. Schramm, M., Herz, J., Haas, A., Kronke, M. and Utermohlen, O. (2008). Acid sphingomyelinase is required for efficient phago-lysosomal fusion. Cell Microbiol. 10, 1839-1853.
42. Ullrich, H. J., Beatty, W. L. and Russell, D. G. (1999). Direct delivery of procathepsin D to phagosomes: implications for phagosome biogenesis and parasitism by Mycobacterium. Eur. J. Cell Biol. 78, 739-748.
43. Utermohlen, O., Herz, J., Schramm, M. and Kronke, M. (2008). Fusogenicity of membranes: the impact of acid sphingomyelinase on innate immune responses. Immunobiology 213, 307-314.
44. Van Rhijn, I., Young, D. C., De Jong, A., Vazquez, J., Cheng, T. Y., Talekar, R., Barral, D. C., Leon, L., Brenner, M. B., Katz, J. T. et al. (2009). CD1c bypasses lysosomes to present a lipopeptide antigen with 12 amino acids. J. Exp. Med. 206, 1409-1422.
45. Vieira, O. V., Botelho, R. J. and Grinstein, S. (2002). Phagosome maturation: aging gracefully. Biochem. J. 366, 689-704.
46. Vielhaber, G., Hurwitz, R. and Sandhoff, K. (1996). Biosynthesis, processing, and targeting of sphingolipid activator protein (SAP)precursor in cultured human fibroblasts. Mannose 6-phosphate receptor-independent endocytosis of SAP precursor. J. Biol. Chem. 271, 32438-3246.
47. Westergaard, U. B., Sorensen, E. S., Hermey, G., Nielsen, M. S., Nykjaer, A., Kirkegaard, K., Jacobsen, C., Gliemann, J., Madsen, P. and Petersen, C. M. (2004). Functional organization of the sortilin Vps10p domain. J. Biol. Chem. 279, 50221-50229.
48. Willnow, T. E., Petersen, C. M. and Nykjaer, A. (2008). VPS10P-domain receptorsregulators of neuronal viability and function. Nat. Rev. Neurosci. 9, 899-909.
49. Winau, F., Schwierzeck, V., Hurwitz, R., Remmel, N., Sieling, P. A., Modlin, R. L., Porcelli, S. A., Brinkmann, V., Sugita, M., Sandhoff, K. et al. (2004). Saposin C is required for lipid presentation by human CD1b. Nat. Immunol. 5, 169-174.
50. Yuan, W., Qi, X., Tsang, P., Kang, S. J., Illarionov, P. A., Besra, G. S., Gumperz, J. and Cresswell, P. (2007). Saposin B is the dominant saposin that facilitates lipid binding to human CD1d molecules. Proc. Natl. Acad. Sci. USA 104, 5551-5556.