LST1 promotes the assembly of a molecular machinery responsible for tunneling nanotube formation

Journal of Cell Science

Volumn 126, Issue 3, 2013, Pages 767-777

  Schiller, Christian ^a,b   Diakopoulos, Kalliope N ^a   Rohwedder, Ina ^a   Kremmer, Elisabeth ^b   Toerne, Christine von ^b   Ueffing, Marius ^b   Weidle, Ulrich H ^c   Ohno, Hiroshi ^d   Weiss, Elisabeth H ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c ROCHE DIAGNOSTICS GMBH   (Germany)

^d RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

Cell cell communication; LST1; Membrane nanotubes; RalA; TNT; Tunneling nanotubes

Indexed keywords

ACTIN; CONTRACTILE PROTEIN; EXOCYST; FILAMIN; GUANOSINE TRIPHOSPHATASE; LEUKOCYTE SPECIFIC TRANSCRIPT 1; M SEC PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 3; MYOFERLIN; MYOSIN; NANOTUBE; RALA PROTEIN; TUNNELING NANOTUBE; UNCLASSIFIED DRUG;

ARTICLE; CELL COMMUNICATION; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; HELA CELL; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION;

CALCIUM-BINDING PROTEINS; CELL COMMUNICATION; CELL MEMBRANE; CONTRACTILE PROTEINS; CYTOSKELETON; HEK293 CELLS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; MULTIPROTEIN COMPLEXES; MUSCLE PROTEINS; MYOSINS; NANOTUBES; PROTEIN BINDING; RAL GTP-BINDING PROTEINS; TRANSGENES; U937 CELLS;

EID: 84876322075     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.114033     Document Type: Article

References (46)

1. Abounit, S. and Zurzolo, C. (2012). Wiring through tunneling nanotubes-from electrical signals to organelle transfer. J. Cell Sci. 125, 1089-1098.
2. Almeida, C. G., Yamada, A., Tenza, D., Louvard, D., Raposo, G. and Coudrier, E. (2011). Myosin 1b promotes the formation of post-Golgi carriers by regulating actin assembly and membrane remodelling at the trans-Golgi network. Nat. Cell Biol. 13, 779-789.
3. Bukoreshtliev, N. V., Wang, X., Hodneland, E., Gurke, S., Barroso, J. F. and Gerdes, H. H. (2009). Selective block of tunneling nanotube (TNT) formation inhibits intercellular organelle transfer between PC12 cells. FEBS Lett. 583, 1481- 1488.
4. Chauveau, A., Aucher, A., Eissmann, P., Vivier, E. and Davis, D. M. (2010). Membrane nanotubes facilitate long-distance interactions between natural killer cells and target cells. Proc. Natl. Acad. Sci. USA 107, 5545-5550.
5. Chinnery, H. R., Pearlman, E. and McMenamin, P. G. (2008). Cutting edge: Membrane nanotubes in vivo: a feature of MHC class II+ cells in the mouse cornea. J. Immunol. 180, 5779-5783.
6. Clancy, E. K. and Duncan, R. (2009). Reovirus FAST protein transmembrane domains function in a modular, primary sequence-independent manner to mediate cell-cell membrane fusion. J. Virol. 83, 2941-2950.
7. de Baey, A., Fellerhoff, B., Maier, S., Martinozzi, S., Weidle, U. and Weiss, E. H. (1997). Complex expression pattern of the TNF region gene LST1 through differential regulation, initiation, and alternative splicing. Genomics 45, 591-600.
8. Doherty, K. R., Cave, A., Davis, D. B., Delmonte, A. J., Posey, A., Earley, J. U., Hadhazy, M. and McNally, E. M. (2005). Normal myoblast fusion requires myoferlin. Development 132, 5565-5575.
9. Draber, P., Stepanek, O., Hrdinka, M., Drobek, A., Chmatal, L., Mala, L., Ormsby, T., Angelisova, P., Horejsi, V. and Brdicka, T. (2012). LST1/A is a myeloid leukocyte-specific transmembrane adaptor protein recruiting protein tyrosine phosphatases SHP-1 and SHP-2 to the plasma membrane. J. Biol. Chem. 287, 22812-22821.
10. Dubey, G. P. and Ben-Yehuda, S. (2011). Intercellular nanotubes mediate bacterial communication. Cell 144, 590-600.
11. Eugenin, E. A., Gaskill, P. J. and Berman, J. W. (2009). Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking. Cell. Immunol. 254, 142-148.
12. Fifadara, N. H., Beer, F., Ono, S. and Ono, S. J. (2010). Interaction between activated chemokine receptor 1 and FcepsilonRI at membrane rafts promotes communication and F-actin-rich cytoneme extensions between mast cells. Int. Immunol. 22, 113-128.
13. Gousset, K., Schiff, E., Langevin, C., Marijanovic, Z., Caputo, A., Browman, D. T., Chenouard, N., de Chaumont, F., Martino, A., Enninga, J. et al. (2009). Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 11, 328-336.
14. Gupta, N. and DeFranco, A. L. (2003). Visualizing lipid raft dynamics and early signaling events during antigen receptor-mediated B-lymphocyte activation. Mol. Biol. Cell 14, 432-444.
15. Gurke, S., Barroso, J. F., Hodneland, E., Bukoreshtliev, N. V., Schlicker, O. and Gerdes, H. H. (2008). Tunneling nanotube (TNT)-like structures facilitate a constitutive, actomyosin-dependent exchange of endocytic organelles between normal rat kidney cells. Exp. Cell Res. 314, 3669-3683.
16. Hase, K., Kimura, S., Takatsu, H., Ohmae, M., Kawano, S., Kitamura, H., Ito, M., Watarai, H., Hazelett, C. C., Yeaman, C. et al. (2009). M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat. Cell Biol. 11, 1427-1432.
17. Hauck, S. M., Dietter, J., Kramer, R. L., Hofmaier, F., Zipplies, J. K., Amann, B., Feuchtinger, A., Deeg, C. A. and Ueffing, M. (2010). Deciphering membraneassociated molecular processes in target tissue of autoimmune uveitis by label-free quantitative mass spectrometry. Mol. Cell. Proteomics 9, 2292-2305.
18. Heasman, S. J. and Ridley, A. J. (2008). Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690-701.
19. Holzinger, I., de Baey, A., Messer, G., Kick, G., Zwierzina, H. and Weiss, E. H. (1995). Cloning and genomic characterization of LST1: a new gene in the human TNF region. Immunogenetics 42, 315-322.
20. Ikeda, M., Ishida, O., Hinoi, T., Kishida, S. and Kikuchi, A. (1998). Identification and characterization of a novel protein interacting with Ral-binding protein 1, a putative effector protein of Ral. J. Biol. Chem. 273, 814-821.
21. Jin, R., Junutula, J. R., Matern, H. T., Ervin, K. E., Scheller, R. H. and Brunger, A. T. (2005). Exo84 and Sec5 are competitive regulatory Sec6/8 effectors to the RalA GTPase. EMBO J. 24, 2064-2074.
22. Lim, K. H., Brady, D. C., Kashatus, D. F., Ancrile, B. B., Der, C. J., Cox, A. D. and Counter, C. M. (2010). Aurora-A phosphorylates, activates, and relocalizes the small GTPase RalA. Mol. Cell. Biol. 30, 508-523.
23. Mattila, P. K. and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-454.
24. Miserey-Lenkei, S., Chalancon, G., Bardin, S., Formstecher, E., Goud, B. and Echard, A. (2010). Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat. Cell Biol. 12, 645-654.
25. Moskalenko, S., Henry, D. O., Rosse, C., Mirey, G., Camonis, J. H. and White, M. A. (2002). The exocyst is a Ral effector complex. Nat. Cell Biol. 4, 66-72.
26. Moskalenko, S., Tong, C., Rosse, C., Mirey, G., Formstecher, E., Daviet, L., Camonis, J. and White, M. A. (2003). Ral GTPases regulate exocyst assembly through dual subunit interactions. J. Biol. Chem. 278, 51743-51748.
27. Mukerji, J., Olivieri, K. C., Misra, V., Agopian, K. A. and Gabuzda, D. (2012). Proteomic analysis of HIV-1 Nef cellular binding partners reveals a role for exocyst complex proteins in mediating enhancement of intercellular nanotube formation. Retrovirology 9, 33.
28. Ohta, Y., Suzuki, N., Nakamura, S., Hartwig, J. H. and Stossel, T. P. (1999). The small GTPase RalA targets filamin to induce filopodia. Proc. Natl. Acad. Sci. USA 96, 2122-2128.
29. Onfelt, B., Nedvetzki, S., Yanagi, K. and Davis, D. M. (2004). Cutting edge: Membrane nanotubes connect immune cells. J. Immunol. 173, 1511-1513.
30. Onfelt, B., Nedvetzki, S., Benninger, R. K., Purbhoo, M. A., Sowinski, S., Hume, A. N., Seabra, M. C., Neil, M. A., French, P. M. and Davis, D. M. (2006). Structurally distinct membrane nanotubes between human macrophages support longdistance vesicular traffic or surfing of bacteria. J. Immunol. 177, 8476-8483.
31. Raghunathan, A., Sivakamasundari, R., Wolenski, J., Poddar, R. and Weissman, S. M. (2001). Functional analysis of B144/LST1: a gene in the tumor necrosis factor cluster that induces formation of long filopodia in eukaryotic cells. Exp. Cell Res. 268, 230-244.
32. Ramírez-Weber, F. A. and Kornberg, T. B. (1999). Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97, 599- 607.
33. Rollinger-Holzinger, I., Eibl, B., Pauly, M., Griesser, U., Hentges, F., Auer, B., Pall, G., Schratzberger, P., Niederwieser, D., Weiss, E. H. et al. (2000). LST1: a gene with extensive alternative splicing and immunomodulatory function. J. Immunol. 164, 3169-3176.
34. Rottach, A., Kremmer, E., Nowak, D., Leonhardt, H. and Cardoso, M. C. (2008). Generation and characterization of a rat monoclonal antibody specific for multiple red fluorescent proteins. Hybridoma (Larchmt) 27, 337-343.
35. Rustom, A., Saffrich, R., Markovic, I., Walther, P. and Gerdes, H. H. (2004). Nanotubular highways for intercellular organelle transport. Science 303, 1007-1010.
36. Schiller, C., Nitschké, M. J., Seidl, A., Kremmer, E. and Weiss, E. H. (2009). Rat monoclonal antibodies specific for LST1 proteins. Hybridoma (Larchmt) 28, 281-286.
37. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N., Palmer, A. E. and Tsien, R. Y. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572.
38. Sherer, N. M., Lehmann, M. J., Jimenez-Soto, L. F., Horensavitz, C., Pypaert, M. and Mothes, W. (2007). Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat. Cell Biol. 9, 310-315.
39. Sowinski, S., Jolly, C., Berninghausen, O., Purbhoo, M. A., Chauveau, A., Köhler, K., Oddos, S., Eissmann, P., Brodsky, F. M., Hopkins, C. et al. (2008). Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10, 211-219.
40. Stricker, D. (2008). BrightStat.com: free statistics online. Comput. Methods Programs Biomed. 92, 135-143.
41. Théry, C., Amigorena, S., Raposo, G. and Clayton, A. (2006). Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. 3.22.1-3.22.29.
42. Wang, X., Veruki, M. L., Bukoreshtliev, N. V., Hartveit, E. and Gerdes, H. H. (2010). Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. Proc. Natl. Acad. Sci. USA 107, 17194-17199.
43. Watkins, S. C. and Salter, R. D. (2005). Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 23, 309-318.
44. Wittig, D., Wang, X., Walter, C., Gerdes, H. H., Funk, R. H. and Roehlecke, C. (2012). Multi-level communication of human retinal pigment epithelial cells via tunneling nanotubes. PLoS ONE 7, e33195.
45. Woo, M. S., Ohta, Y., Rabinovitz, I., Stossel, T. P. and Blenis, J. (2004). Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Mol. Cell. Biol. 24, 3025-3035.
46. Zuo, X., Zhang, J., Zhang, Y., Hsu, S. C., Zhou, D. and Guo, W. (2006). Exo70 interacts with the Arp2/3 complex and regulates cell migration. Nat. Cell Biol. 8, 1383-1388.