ALG-2-interacting Tubby-like protein superfamily member PLSCR3 is secreted by an exosomal pathway and taken up by recipient cultured cells

Bioscience Reports

Volumn 33, Issue 2, 2013, Pages 281-293

  Inuzuka, Tatsutoshi ^a   Inokawa, Akira ^a   Chen, Cen ^a   Kizu, Kumiko ^b   Narita, Hiroshi ^b   Shibata, Hideki ^a   Maki, Masatoshi ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b KYOTO WOMEN'S UNIVERSITY   (Japan)

Author keywords

Apoptosis linked gene 2 (ALG 2); Endosome; Exosome; Palmitoylation; Unconventional secretion; Vesicle

Indexed keywords

ADENOSINE TRIPHOSPHATASE; APOPTOSIS LINKED GENE 2 PROTEIN; CALCIUM ION; ESCRT PROTEIN; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE PROTEIN; PROTEIN VPS4B; RAB5A PROTEIN; SCRAMBLASE; SCRAMBLASE 3; UNCLASSIFIED DRUG; 2 BROMOPALMITIC ACID; 2-BROMOPALMITATE; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; PALMITIC ACID DERIVATIVE; PDCD6 PROTEIN, HUMAN; PHOSPHOLIPID TRANSFER PROTEIN; PLSCR3 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CELL CULTURE; CONTROLLED STUDY; EMBRYO; ENDOSOME; ENZYME RELEASE; EXOSOME; HUMAN; HUMAN CELL; PALMITOYLATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; LIPOYLATION; METABOLISM; PROTEIN BINDING; SECRETION (PROCESS); SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

APOPTOSIS REGULATORY PROTEINS; BINDING SITES; BIOLOGICAL TRANSPORT; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; EXOSOMES; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; LIPOYLATION; PALMITATES; PHOSPHOLIPID TRANSFER PROTEINS; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 84877763993     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20120123     Document Type: Article

References (51)

1. 2+-dependent transbilayer movement of phospholipid. J. Biol. Chem. 271, 17205-17210
2. Zhou, Q., Zhao, J., Stout, J. G., Luhm, R. A., Wiedmer, T. and Sims, P. J. (1997) Molecular cloning of human plasma membrane phospholipid scramblase. A protein mediating transbilayer movement of plasma membrane phospholipids. J. Biol. Chem. 272, 18240-18244
3. Wiedmer, T., Zhao, J., Nanjundan, M. and Sims, P. J. (2003) Palmitoylation of phospholipid scramblase 1 controls its distribution between nucleus and plasma membrane. Biochemistry 42, 1227-1233 (Pubitemid 36184063)
4. Zhou, Q., Ben-Efraim, I., Bigcas, J. L., Junqueira, D., Wiedmer, T. and Sims, P. J. (2005) Phospholipid scramblase 1 binds to the promoter region of the inositol 1,4,5-triphosphate receptor type 1 gene to enhance its expression. J. Biol. Chem. 280, 35062-35068 (Pubitemid 41504641)
5. Chen, C. W., Sowden, M., Zhao, Q., Wiedmer, T. and Sims, P. J. (2011) Nuclear phospholipid scramblase 1 prolongs the mitotic expansion of granulocyte precursors during G-CSF-induced granulopoiesis. J. Leukoc. Biol. 90, 221-233
6. Kusano, S. and Eizuru, Y. (2012) Human phospholipid scramblase 1 interacts with and regulates transactivation of HTLV-1 Tax. Virology 432, 343-352
7. Zhou, Q., Zhao, J., Wiedmer, T. and Sims, P. J. (2002) Normal hemostasis but defective hematopoietic response to growth factors in mice deficient in phospholipid scramblase 1. Blood 99, 4030-4038 (Pubitemid 35332044)
8. Sun, J., Nanjundan, M., Pike, L. J., Wiedmer, T. and Sims, P. J. (2002) Plasma membrane phospholipid scramblase 1 is enriched in lipid rafts and interacts with the epidermal growth factor receptor. Biochemistry 41, 6338-6345 (Pubitemid 34525998)
9. Py, B., Basmaciogullari, S., Bouchet, J., Zarka, M., Moura, I. C., Benhamou, M., Monteiro, R. C., Hocini, H., Madrid, R. and Benichou, S. (2009) The phospholipid scramblases 1 and 4 are cellular receptors for the secretory leukocyte protease inhibitor and interact with CD4 at the plasma membrane. PLoS ONE 4, e5006
10. Cusick, J. K., Mustian, A., Jacobs, A. T. and Reyland, M. E. (2012) Identification of PLSCR1 as a protein that interacts with RELT family members. Mol. Cell. Biochem. 362, 55-63
11. Talukder, A. H., Bao, M., Kim, T. W., Facchinetti, V., Hanabuchi, S., Bover, L., Zal, T. and Liu, Y. J. (2012) Phospholipid Scramblase 1 regulates Toll-like receptor 9-mediated type I interferon production in plasmacytoid dendritic cells. Cell Res. 22, 1129-1139
12. Amir-Moazami, O., Alexia, C., Charles, N., Launay, P., Monteiro, R. C. and Benhamou, M. (2008) Phospholipid scramblase 1 modulates a selected set of IgE receptor-mediated mast cell responses through LAT-dependent pathway. J. Biol. Chem. 283, 25514-25523
13. Suzuki, J., Umeda, M., Sims, P. J. and Nagata, S. (2010) Calcium-dependent phospholipid scrambling by TMEM16F. Nature 468, 834-838
14. Castoldi, E., Collins, P. W., Williamson, P. L. and Bevers, E. M. (2011) Compound heterozygosity for 2 novel TMEM16F mutations in a patient with Scott syndrome. Blood 117, 4399-4400
15. Bevers, E. M. and Williamson, P. L. (2010) Phospholipid scramblase: an update. FEBS Lett. 584, 2724-2730
16. Lhermusier, T., Chap, H. and Payrastre, B. (2011) Platelet membrane phospholipid asymmetry: from the characterization of a scramblase activity to the identification of an essential protein mutated in Scott syndrome. J Thromb. Haemost. 9, 1883-1891
17. Wiedmer, T., Zhou, Q., Kwoh, D. Y. and Sims, P. J. (2000) Identification of three new members of the phospholipid scramblase gene family. Biochim. Biophys. Acta 1467, 244-253 (Pubitemid 30621602)
18. Liu, J., Dai, Q., Chen, J., Durrant, D., Freeman, A., Liu, T., Grossman, D. and Lee, R. M. (2003) Phospholipid scramblase 3 controls mitochondrial structure, function, and apoptotic response. Mol. Cancer Res. 1, 892-902 (Pubitemid 37303889)
19. Van, Q., Liu, J., Lu, B., Feingold, K. R., Shi, Y., Lee, R. M. and Hatch, G. M. (2007) Phospholipid scramblase-3 regulates cardiolipin de novo biosynthesis and its resynthesis in growing HeLa cells. Biochem. J. 401, 103-109 (Pubitemid 46114604)
20. Liu, J., Epand, R. F., Durrant, D., Grossman, D., Chi, N. W., Epand, R. M. and Lee, R. M. (2008) Role of phospholipid scramblase 3 in the regulation of tumor necrosis factor-α-induced apoptosis. Biochemistry 47, 4518-4529 (Pubitemid 351522102)
21. Ndebele, K., Gona, P., Jin, T. G., Benhaga, N., Chalah, A., Degli-Esposti, M. and Khosravi-Far, R. (2008) Tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL) induced mitochondrial pathway to apoptosis and caspase activation is potentiated by phospholipid scramblase-3. Apoptosis 13, 845-856
22. Wiedmer, T., Zhao, J., Li, L., Zhou, Q., Hevener, A., Olefsky, J. M., Curtiss, L. K. and Sims, P. J. (2004) Adiposity, dyslipidemia, and insulin resistance in mice with targeted deletion of phospholipid scramblase 3 (PLSCR3). Proc. Natl. Acad. Sci. U.S.A. 101, 13296-13301 (Pubitemid 39209659)
23. Maki, M., Kitaura, Y., Satoh, H., Ohkouchi, S. and Shibata, H. (2002) Structures, functions and molecular evolution of the penta-EF-hand Ca2+-binding proteins. Biochim. Biophys. Acta 1600, 51-60 (Pubitemid 38224398)
24. Shibata, H., Suzuki, H., Kakiuchi, T., Inuzuka, T., Yoshida, H., Mizuno, T. and Maki, M. (2008) Identification of Alix-type and Non-Alix-type ALG-2-binding sites in human phospholipid scramblase 3: differential binding to an alternatively spliced isoform and amino acid-substituted mutants. J. Biol. Chem. 283, 9623-9632
25. Bateman, A., Finn, R. D., Sims, P. J., Wiedmer, T., Biegert, A. and Soding, J. (2009) Phospholipid scramblases and Tubby-like proteins belong to a new superfamily of membrane tethered transcription factors. Bioinformatics 25, 159-162
26. Santagata, S., Boggon, T. J., Baird, C. L., Gomez, C. A., Zhao, J., Shan, W. S., Myszka, D. G. and Shapiro, L. (2001) G-protein signaling through tubby proteins. Science 292, 2041-2050 (Pubitemid 32691568)
27. Mukhopadhyay, S. and Jackson, P. K. (2011) The tubby family proteins. Genome Biol. 12, 225
28. Caberoy, N. B. and Li, W. (2009) Unconventional secretion of tubby and tubby-like protein 1. FEBS Lett. 583, 3057-3062
29. Caberoy, N. B., Zhou, Y. and Li, W. (2010) Tubby and tubby-like protein 1 are new MerTK ligands for phagocytosis. EMBO J. 29, 3898-3910
30. Merregaert, J., Van Langen, J., Hansen, U., Ponsaerts, P., El Ghalbzouri, A., Steenackers, E., Van Ostade, X. and Sercu, S. (2010) Phospholipid scramblase 1 is secreted by a lipid raft-dependent pathway and interacts with the extracellular matrix protein 1 in the dermal epidermal junction zone of human skin. J. Biol. Chem. 285, 37823-37837
31. Simons, M. and Raposo, G. (2009) Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581
32. Mathivanan, S., Ji, H. and Simpson, R. J. (2010) Exosomes: extracellular organelles important in intercellular communication. J. Proteomics 73, 1907-1920
33. Cocucci, E., Racchetti, G. and Meldolesi, J. (2009) Shedding microvesicles: artefacts no more. Trends Cell Biol. 19, 43-51
34. Shibata, H., Suzuki, H., Yoshida, H. and Maki, M. (2007) ALG-2 directly binds Sec31A and localizes at endoplasmic reticulum exit sites in a Ca2+-dependent manner. Biochem. Biophys. Res. Commun. 353, 756-763 (Pubitemid 46048735)
35. Hirose, J., Kitabatake, N., Kimura, A. and Narita, H. (2004) Recognition of native and/or thermally induced denatured forms of the major food allergen, ovomucoid, by human IgE and mouse monoclonal IgG antibodies. Biosci. Biotechnol. Biochem. 68, 2490-2497 (Pubitemid 40218178)
36. Horii, M., Shibata, H., Kobayashi, R., Katoh, K., Yorikawa, C., Yasuda, J. and Maki, M. (2006) CHMP7, a novel ESCRT-III-related protein, associates with CHMP4b and functions in the endosomal sorting pathway. Biochem. J. 400, 23-32 (Pubitemid 44763816)
37. Havrylov, S., Ichioka, F., Powell, K., Borthwick, E. B., Baranska, J., Maki, M. and Buchman, V. L. (2008) Adaptor protein Ruk/CIN85 is associated with a subset of COPI-coated membranes of the Golgi complex. Traffic 9, 798-812 (Pubitemid 351494308)
38. 2+-dependent adaptor that bridges Alix and TSG101. Biochem. Biophys. Res. Commun. 386, 237-241
39. Katoh, K., Shibata, H., Suzuki, H., Nara, A., Ishidoh, K., Kominami, E., Yoshimori, T. and Maki, M. (2003) The ALG-2-interacting protein Alix associates with CHMP4b, a human homologue of yeast Snf7 that is involved in multivesicular body sorting. J. Biol. Chem. 278, 39104-39113 (Pubitemid 37221814)
40. Nickel, W. and Rabouille, C. (2009) Mechanisms of regulated unconventional protein secretion. Nat. Rev. Mol. Cell Biol. 10, 148-155
41. Merrick, B. A., Dhungana, S., Williams, J. G., Aloor, J. J., Peddada, S., Tomer, K. B. and Fessler, M. B. (2011) Proteomic profiling of S-acylated macrophage proteins identifies a role for palmitoylation in mitochondrial targeting of phospholipid scramblase 3. Mol. Cell Proteomics 10, M110 006007
42. Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brugger, B. and Simons, M. (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244-1247 (Pubitemid 351323020)
43. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J. and Lotvall, J. O. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659 (Pubitemid 47214727)
44. Pisitkun, T., Shen, R. F. and Knepper, M. A. (2004) Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. U.S.A. 101, 13368-13373 (Pubitemid 39209672)
45. Mathivanan, S., Fahner, C. J., Reid, G. E. and Simpson, R. J. (2012) ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res. 40, D1241-1244
46. Subra, C., Grand, D., Laulagnier, K., Stella, A., Lambeau, G., Paillasse, M., De Medina, P., Monsarrat, B., Perret, B., Silvente-Poirot, S. et al. (2010) Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J. Lipid Res. 51, 2105-2120
47. Mathivanan, S., Lim, J. W., Tauro, B. J., Ji, H., Moritz, R. L. and Simpson, R. J. (2010) Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol. Cell Proteomics 9, 197-208
48. Baietti, M. F., Zhang, Z., Mortier, E., Melchior, A., Degeest, G., Geeraerts, A., Ivarsson, Y., Depoortere, F., Coomans, C., Vermeiren, E. et al. (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell Biol. 14, 677-685
49. Matsuo, H., Chevallier, J., Mayran, N., Le Blanc, I., Ferguson, C., Fauré, J., Blanc, N. S., Matile, S., Dubochet, J., Sadoul, R. et al. (2004) Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303, 531-534 (Pubitemid 38120852)
50. Nabhan, J. F., Hu, R., Oh, R. S., Cohen, S. N. and Lu, Q. (2012) Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc. Natl. Acad. Sci. U.S.A. 109, 4146-4151
51. Kowalczyk, J. E., Beresewicz, M., Gajkowska, B. and Zablocka, B. (2009) Association of protein kinase C delta and phospholipid scramblase 3 in hippocampal mitochondria correlates with neuronal vulnerability to brain ischemia. Neurochem. Int. 55, 157-163