TOSO, the Fcμ receptor, is highly expressed on chronic lymphocytic leukemia B cells, internalizes upon IgM binding, shuttles to the lysosome, and is downregulated in response to TLR activation

Journal of Immunology

Volumn 187, Issue 8, 2011, Pages 4040-4050

  Vire, Bérengère ^a   David, Alexandre ^b   Wiestner, Adrian ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; BORTEZOMIB; CHLOROQUINE; CPG OLIGODEOXYNUCLEOTIDE; DACTINOMYCIN; FC MU RECEPTOR; FC RECEPTOR; IMIQUIMOD; IMMUNOGLOBULIN M; MESSENGER RNA; PROLINE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; MEMBRANE PROTEIN; TOSO PROTEIN, HUMAN;

ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; CELL MEMBRANE; CELL SURFACE; CHRONIC LYMPHATIC LEUKEMIA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; DRUG ACTIVITY; ENDOSOME; GENE DELETION; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTERNALIZATION; LYMPHOCYTE ACTIVATION; LYSOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TRANSPORT; TRANS GOLGI NETWORK; TREATMENT RESPONSE; CELL SEPARATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

APOPTOSIS REGULATORY PROTEINS; B-LYMPHOCYTES; BLOTTING, WESTERN; CELL SEPARATION; DOWN-REGULATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOSYLATION; HUMANS; IMMUNOGLOBULIN M; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOCYTE ACTIVATION; LYSOSOMES; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; PROTEIN TRANSPORT; RECEPTORS, FC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTORS;

EID: 80054751083     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100532     Document Type: Article

References (48)

1. Chiorazzi, N., K. R. Rai, and M. Ferrarini. 2005. Chronic lymphocytic leukemia. N. Engl. J. Med. 352: 804-815.
2. Klein, U., Y. Tu, G. A. Stolovitzky, M. Mattioli, G. Cattoretti, H. Husson, A. Freedman, G. Inghirami, L. Cro, L. Baldini, et al. 2001. Gene expression profiling of B cell chronic lymphocytic leukemia reveals a homogeneous phenotype related to memory B cells. J. Exp. Med. 194: 1625-1638. (Pubitemid 33126813)
3. Herishanu, Y., P. Pérez-Galán, D. Liu, A. Biancotto, S. Pittaluga, B. Vire, F. Gibellini, N. Njuguna, E. Lee, L. Stennett, et al. 2011. The lymph node microenvironment promotes B-cell receptor signaling, NF-κB activation, and tumor proliferation in chronic lymphocytic leukemia. Blood 117: 563-574.
4. Nimmerjahn, F., and J. V. Ravetch. 2007. Fc-receptors as regulators of immunity. Adv. Immunol. 96: 179-204. (Pubitemid 350018720)
5. Powell, M. S., and P. M. Hogarth. 2008. Fc receptors. Adv. Exp. Med. Biol. 640: 22-34.
6. Kraft, S., and J. P. Kinet. 2007. New developments in FcεRI regulation, function and inhibition. Nat. Rev. Immunol. 7: 365-378. (Pubitemid 46674486)
7. Nimmerjahn, F., and J. V. Ravetch. 2008. Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 8: 34-47.
8. Hitoshi, Y., J. Lorens, S. I. Kitada, J. Fisher, M. LaBarge, H. Z. Ring, U. Francke, J. C. Reed, S. Kinoshita, and G. P. Nolan. 1998. Toso, a cell surface, specific regulator of Fas-induced apoptosis in T cells. Immunity 8: 461-471. (Pubitemid 28196800)
9. Kubagawa, H., S. Oka, Y. Kubagawa, I. Torii, E. Takayama, D. W. Kang, G. L. Gartland, L. F. Bertoli, H. Mori, H. Takatsu, et al. 2009. Identity of the elusive IgM Fc receptor (FcμR) in humans. J. Exp. Med. 206: 2779-2793.
10. Rosenwald, A., A. A. Alizadeh, G. Widhopf, R. Simon, R. E. Davis, X. Yu, L. Yang, O. K. Pickeral, L. Z. Rassenti, J. Powell, et al. 2001. Relation of gene expression phenotype to immunoglobulin mutation genotype in B cell chronic lymphocytic leukemia. J. Exp. Med. 194: 1639-1647. (Pubitemid 33126814)
11. Pallasch, C. P., A. Schulz, N. Kutsch, J. Schwamb, S. Hagist, H. Kashkar, A. Ultsch, C. Wickenhauser, M. Hallek, and C. M. Wendtner. 2008. Overexpression of TOSO in CLL is triggered by B-cell receptor signaling and associated with progressive disease. Blood 112: 4213-4219.
12. Proto-Siqueira, R., R. A. Panepucci, F. P. Careta, A. Lee, A. Clear, K. Morris, C. Owen, E. G. Rizzatti, W. A. Silva, Jr., R. P. Falcão, et al. 2008. SAGE analysis demonstrates increased expression of TOSO contributing to Fas-mediated resistance in CLL. Blood 112: 394-397.
13. Wiestner, A., A. Rosenwald, T. S. Barry, G. Wright, R. E. Davis, S. E. Henrickson, H. Zhao, R. E. Ibbotson, J. A. Orchard, Z. Davis, et al. 2003. ZAP-70 expression identifies a chronic lymphocytic leukemia subtype with unmutated immunoglobulin genes, inferior clinical outcome, and distinct gene expression profile. Blood 101: 4944-4951. (Pubitemid 36857758)
14. Julenius, K., A. Mølgaard, R. Gupta, and S. Brunak. 2005. Prediction, conservation analysis, and structural characterization of mammalian mucin-type Oglycosylation sites. Glycobiology 15: 153-164. (Pubitemid 40227920)
15. Sigruener, A., C. Buechler, S. M. Bared, M. Grandl, C. Aslanidis, P. Ugocsai, M. Gehrmann, and G. Schmitz. 2007. E-LDL upregulates TOSO expression and enhances the survival of human macrophages. Biochem. Biophys. Res. Commun. 359: 723-728. (Pubitemid 46899011)
16. Hansen, J. E., O. Lund, N. Tolstrup, A. A. Gooley, K. L. Williams, and S. Brunak. 1998. NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconj. J. 15: 115-130. (Pubitemid 28260915)
17. Delannoy, P., I. Kim, N. Emery, C. De Bolos, A. Verbert, P. Degand, and G. Huet. 1996. Benzyl-N-acetyl-α-D-galactosaminide inhibits the sialylation and the secretion of mucins by a mucin secreting HT-29 cell subpopulation. Glycoconj. J. 13: 717-726. (Pubitemid 26354264)
18. Kuan, S. F., J. C. Byrd, C. Basbaum, and Y. S. Kim. 1989. Inhibition of mucin glycosylation by aryl-N-acetyl-α-galactosaminides in human colon cancer cells. J. Biol. Chem. 264: 19271-19277. (Pubitemid 19285840)
19. Klíma, M., J. Zájedová, L. Doubravská, and L. Andera. 2009. Functional analysis of the posttranslational modifications of the death receptor 6. Biochim. Biophys. Acta 1793: 1579-1587.
20. Song, Y., and C. O. Jacob. 2005. The mouse cell surface protein TOSO regulates Fas/Fas ligand-induced apoptosis through its binding to Fas-associated death domain. J. Biol. Chem. 280: 9618-9626. (Pubitemid 40409658)
21. Prescott, A. R., J. M. Lucocq, J. James, J. M. Lister, and S. Ponnambalam. 1997. Distinct compartmentalization of TGN46 and β1,4-galactosyltransferase in HeLa cells. Eur. J. Cell Biol. 72: 238-246. (Pubitemid 27117130)
22. De Matteis, M. A., and A. Luini. 2008. Exiting the Golgi complex. Nat. Rev. Mol. Cell Biol. 9: 273-284. (Pubitemid 351430855)
23. Griffiths, G., and K. Simons. 1986. The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234: 438-443. (Pubitemid 17181425)
24. Bonifacino, J. S., and R. Rojas. 2006. Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 7: 568-579. (Pubitemid 44325348)
25. Faussner, A., S. Schuessler, C. Seidl, and M. Jochum. 2004. Inhibition of sequestration of human B2 bradykinin receptor by phenylarsine oxide or sucrose allows determination of a receptor affinity shift and ligand dissociation in intact cells. Biol. Chem. 385: 835-843. (Pubitemid 39335306)
26. Hertel, C., S. J. Coulter, and J. P. Perkins. 1985. A comparison of catecholamine-induced internalization of beta-adrenergic receptors and receptor-mediated endocytosis of epidermal growth factor in human astrocytoma cells: inhibition by phenylarsine oxide. J. Biol. Chem. 260: 12547-12553. (Pubitemid 16233457)
27. Cravatt, B. F., D. K. Giang, S. P. Mayfield, D. L. Boger, R. A. Lerner, and N. B. Gilula. 1996. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384: 83-87. (Pubitemid 26374593)
28. Sudol, M. 1998. From Src homology domains to other signaling modules: proposal of the 'protein recognition code.' Oncogene 17(11 Reviews): 1469-1474.
29. Blott, E. J., G. Bossi, R. Clark, M. Zvelebil, and G. M. Griffiths. 2001. Fas ligand is targeted to secretory lysosomes via a proline-rich domain in its cytoplasmic tail. J. Cell Sci. 114: 2405-2416. (Pubitemid 32684796)
30. Suzuki-Inoue, K., D. Tulasne, Y. Shen, T. Bori-Sanz, O. Inoue, S. M. Jung, M. Moroi, R. K. Andrews, M. C. Berndt, and S. P. Watson. 2002. Association of Fyn and Lyn with the proline-rich domain of glycoprotein VI regulates intracellular signaling. J. Biol. Chem. 277: 21561-21566. (Pubitemid 34952302)
31. Collawn, J. F., A. Lai, D. Domingo, M. Fitch, S. Hatton, and I. S. Trowbridge. 1993. YTRF is the conserved internalization signal of the transferrin receptor, and a second YTRF signal at position 31-34 enhances endocytosis. J. Biol. Chem. 268: 21686-21692. (Pubitemid 23320664)
32. Collawn, J. F., and Y. Paterson. 1990. Stabilization of helical structure in two 17-residue amphipathic analogues of the C-terminal peptide of cytochrome c. Biopolymers 29: 1289-1296. (Pubitemid 20177498)
33. Boes, M., A. P. Prodeus, T. Schmidt, M. C. Carroll, and J. Chen. 1998. A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J. Exp. Med. 188: 2381-2386. (Pubitemid 29028511)
34. Ehrenstein, M. R., and C. A. Notley. 2010. The importance of natural IgM: scavenger, protector and regulator. Nat. Rev. Immunol. 10: 778-786.
35. Ochsenbein, A. F., T. Fehr, C. Lutz, M. Suter, F. Brombacher, H. Hengartner, and R. M. Zinkernagel. 1999. Control of early viral and bacterial distribution and disease by natural antibodies. Science 286: 2156-2159. (Pubitemid 129516290)
36. Ungar, D. 2009. Golgi linked protein glycosylation and associated diseases. Semin. Cell Dev. Biol. 20: 762-769.
37. Wopereis, S., D. J. Lefeber, E. Morava, and R. A. Wevers. 2006. Mechanisms in protein O-glycan biosynthesis and clinical and molecular aspects of protein O-glycan biosynthesis defects: a review. Clin. Chem. 52: 574-600.
38. Wilson, T. J., S. Gilfillan, and M. Colonna. 2010. Fc receptor-like A associates with intracellular IgG and IgM but is dispensable for antigen-specific immune responses. J. Immunol. 185: 2960-2967.
39. Shima, H., H. Takatsu, S. Fukuda, M. Ohmae, K. Hase, H. Kubagawa, J. Y. Wang, and H. Ohno. 2010. Identification of TOSO/FAIM3 as an Fc receptor for IgM. Int. Immunol. 22: 149-156.
40. Boehm, M., and J. S. Bonifacino. 2001. Adaptins: the final recount. Mol. Biol. Cell 12: 2907-2920. (Pubitemid 33062950)
41. Collawn, J. F., M. Stangel, L. A. Kuhn, V. Esekogwu, S. Q. Jing, I. S. Trowbridge, and J. A. Tainer. 1990. Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis. Cell 63: 1061-1072. (Pubitemid 120034947)
42. Muzio, M., C. Scielzo, M. T. Bertilaccio, M. Frenquelli, P. Ghia, and F. Caligaris-Cappio. 2009. Expression and function of toll like receptors in chronic lymphocytic leukaemia cells. Br. J. Haematol. 144: 507-516.
43. Leadbetter, E. A., I. R. Rifkin, A.M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607. (Pubitemid 34406754)
44. Ngo, V. N., R. M. Young, R. Schmitz, S. Jhavar, W. Xiao, K. H. Lim, H. Kohlhammer, W. Xu, Y. Yang, H. Zhao, et al. 2011. Oncogenically active MYD88 mutations in human lymphoma. Nature 470: 115-119.
45. Alley, S. C., N. M. Okeley, and P. D. Senter. 2010. Antibody-drug conjugates: targeted drug delivery for cancer. Curr. Opin. Chem. Biol. 14: 529-537.
46. Ansell, S. M. 2011. Brentuximab vedotin: delivering an antimitotic drug to activated lymphoma cells. Expert Opin. Investig. Drugs 20: 99-105.
47. Burris, H. A., III, H. S. Rugo, S. J. Vukelja, C. L. Vogel, R. A. Borson, S. Limentani, E. Tan-Chiu, I. E. Krop, R. A. Michaelson, S. Girish, et al. 2011. Phase II study of the antibody drug conjugate trastuzumab-DM1 for the treatment of human epidermal growth factor receptor 2 (HER2)-positive breast cancer after prior HER2-directed therapy. J. Clin. Oncol. 29: 398-405.
48. Okeley, N. M., J. B. Miyamoto, X. Zhang, R. J. Sanderson, D. R. Benjamin, E. L. Sievers, P. D. Senter, and S. C. Alley. 2010. Intracellular activation of SGN-35, a potent anti-CD30 antibody-drug conjugate. Clin. Cancer Res. 16: 888-897.