Membrane-associated RING-CH proteins associate with Bap31 and Target CD81 and CD44 to lysosomes

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Bartee, Eric ^b   Eyster, Craig A ^c   Viswanathan, Kasinath ^a   Mansouri, Mandana ^a   Donaldson, Julie G ^c   Früh, Klaus ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; CHAPERONE; HERMES ANTIGEN; MEMBRANE ASSOCIATED RING CH PROTEIN; MEMBRANE ASSOCIATED RING CH PROTEIN IV; MEMBRANE ASSOCIATED RING CH PROTEIN VIII; MEMBRANE PROTEIN; PROTEIN BAP31; TETRASPANIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; BCAP31 PROTEIN, HUMAN; CD9 ANTIGEN; HYALURONIC ACID; LEUKOCYTE ANTIGEN; PROTEOME;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; FIBROBLAST CULTURE; GENE SILENCING; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; LYSOSOME; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEOMICS; UBIQUITINATION; BIOLOGICAL MODEL; CELL MEMBRANE; CHEMISTRY; ENDOSOME; FIBROBLAST; HELA CELL; METABOLISM; METHODOLOGY; TANDEM MASS SPECTROMETRY;

ANTIGENS, CD; ANTIGENS, CD44; CELL MEMBRANE; ENDOSOMES; FIBROBLASTS; HELA CELLS; HUMANS; HYALURONIC ACID; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PROTEOME; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 78649915674     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015132     Document Type: Article

References (58)

1. Jackson S, Xiong Y (2009) CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem Sci 34: 562-570.
2. Nathan JA, Lehner PJ (2009) The trafficking and regulation of membrane receptors by the RING-CH ubiquitin E3 ligases. Exp Cell Res 315: 1593-1600.
3. Coscoy L, Ganem D (2000) Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc Natl Acad Sci U S A 97: 8051-8056.
4. Stevenson PG, Efstathiou S, Doherty PC, Lehner PJ (2000) Inhibition of MHC class I-restricted antigen presentation by gamma 2-herpesviruses. Proc Natl Acad Sci U S A 97: 8455-8460.
5. Ishido S, Wang C, Lee BS, Cohen GB, Jung JU (2000) Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J Virol 74: 5300-5309.
6. Mansouri M, Bartee E, Gouveia K, Hovey Nerenberg BT, Barrett J, et al. (2003) The PHD/LAP-domain protein M153R of myxomavirus is a ubiquitin ligase that induces the rapid internalization and lysosomal destruction of CD4. J Virol 77: 1427-1440.
7. Guerin JL, Gelfi J, Boullier S, Delverdier M, Bellanger FA, et al. (2002) Myxoma virus leukemia-associated protein is responsible for major histocompatibility complex class I and Fas-CD95 down-regulation and defines scrapins, a new group of surface cellular receptor abductor proteins. J Virol 76: 2912-2923.
8. Coscoy L, Sanchez DJ, Ganem D (2001) A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J Cell Biol 155: 1265-1273.
9. Cadwell K, Coscoy L (2005) Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309: 127-130.
10. Wang X, Herr RA, Chua WJ, Lybarger L, Wiertz EJ, et al. (2007) Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J Cell Biol 177: 613-624.
11. Dodd RB, Allen MD, Brown SE, Sanderson CM, Duncan LM, et al. (2004) Solution structure of the Kaposi's sarcoma-associated herpesvirus K3 N-terminal domain reveals a Novel E2-binding C4HC3-type RING domain. J Biol Chem 279: 53840-53847.
12. Mansouri M, Douglas J, Rose PP, Gouveia K, Thomas G, et al. (2006) Kaposi sarcoma herpesvirus K5 removes CD31/PECAM from endothelial cells. Blood 108: 1932-1940.
13. Bartee E, Mansouri M, Hovey Nerenberg BT, Gouveia K, Fruh K (2004) Downregulation of major histocompatibility complex class I by human ubiquitin ligases related to viral immune evasion proteins. J Virol 78: 1109-1120.
14. Bartee E, McCormack A, Fruh K (2006) Quantitative membrane proteomics reveals new cellular targets of viral immune modulators. PLoS Pathog 2: e107.
15. Morokuma Y, Nakamura N, Kato A, Notoya M, Yamamoto Y, et al. (2007) MARCH-XI, a novel transmembrane ubiquitin ligase implicated in ubiquitindependent protein sorting in developing spermatids. J Biol Chem 282: 24806-24815.
16. Goto E, Ishido S, Sato Y, Ohgimoto S, Ohgimoto K, et al. (2003) c-MIR, a human E3 ubiquitin ligase, is a functional homolog of herpesvirus proteins MIR1 and MIR2 and has similar activity. J Biol Chem 278: 14657-14668.
17. Hoer S, Smith L, Lehner PJ (2007) MARCH-IX mediates ubiquitination and downregulation of ICAM-1. FEBS Lett 581: 45-51.
18. Ohmura-Hoshino M, Matsuki Y, Aoki M, Goto E, Mito M, et al. (2006) Inhibition of MHC class II expression and immune responses by c-MIR. J Immunol 177: 341-354.
19. Matsuki Y, Ohmura-Hoshino M, Goto E, Aoki M, Mito-Yoshida M, et al. (2007) Novel regulation of MHC class II function in B cells. EMBO J 26: 846-854.
20. Ohmura-Hoshino M, Matsuki Y, Mito-Yoshida M, Goto E, Aoki-Kawasumi M, et al. (2009) Cutting edge: requirement of MARCH-I-mediated MHC II ubiquitination for the maintenance of conventional dendritic cells. J Immunol 183: 6893-6897.
21. Young LJ, Wilson NS, Schnorrer P, Proietto A, ten Broeke T, et al. (2008) Differential MHC class II synthesis and ubiquitination confers distinct antigenpresenting properties on conventional and plasmacytoid dendritic cells. Nat Immunol 9: 1244-1252.
22. Thibodeau J, Bourgeois-Daigneault MC, Huppe G, Tremblay J, Aumont A, et al. (2008) Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes. Eur J Immunol 38: 1225-1230.
23. De Gassart A, Camosseto V, Thibodeau J, Ceppi M, Catalan N, et al. (2008) MHC class II stabilization at the surface of human dendritic cells is the result of maturation-dependent MARCH I down-regulation. Proc Natl Acad Sci U S A 105: 3491-3496.
24. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, et al. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1: 376-386.
25. Ong SE, Kratchmarova I, Mann M (2003) Properties of 13C-substituted arginine in stable isotope labeling by amino acids in cell culture (SILAC). J Proteome Res 2: 173-181.
26. Gottlinger HG (2008) HIV/AIDS: virus kept on a leash. Nature 451: 406-408.
27. Hor S, Ziv T, Admon A, Lehner PJ (2009) Stable isotope labeling by amino acids in cell culture and differential plasma membrane proteome quantitation identify new substrates for the MARCH9 transmembrane E3 ligase. Mol Cell Proteomics 8: 1959-1971.
28. Douglas JL, Viswanathan K, McCarroll MN, Gustin JK, Fruh K, et al. (2009) Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a {beta}TrCP-dependent mechanism. J Virol 83: 7931-7947.
29. Link AJ, Eng J, Schieltz DM, Carmack E, Mize GJ, et al. (1999) Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol 17: 676-682.
30. Yates JR, 3rd, Eng JK, McCormack AL, Schieltz D (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67: 1426-1436.
31. Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392.
32. Li XJ, Zhang H, Ranish JA, Aebersold R (2003) Automated statistical analysis of protein abundance ratios from data generated by stable-isotope dilution and tandem mass spectrometry. Anal Chem 75: 6648-6657.
33. Isacke CM, Yarwood H (2002) The hyaluronan receptor, CD44. Int J Biochem Cell Biol 34: 718-721.
34. Charrin S, le Naour F, Silvie O, Milhiet PE, Boucheix C, et al. (2009) Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J 420: 133-154.
35. Abache T, Le Naour F, Planchon S, Harper F, Boucheix C, et al. (2007) The transferrin receptor and the tetraspanin web molecules CD9, CD81, and CD9P-1 are differentially sorted into exosomes after TPA treatment of K562 cells. J Cell Biochem 102: 650-664.
36. Stojanovic M, Germain M, Nguyen M, Shore GC (2005) BAP31 and its caspase cleavage product regulate cell surface expression of tetraspanins and integrinmediated cell survival. J Biol Chem 280: 30018-30024.
37. Spiliotis ET, Manley H, Osorio M, Zuniga MC, Edidin M (2000) Selective export of MHC class I molecules from the ER after their dissociation from TAP. Immunity 13: 841-851.
38. Abe F, Van Prooyen N, Ladasky JJ, Edidin M (2009) Interaction of Bap31 and MHC class I molecules and their traffic out of the endoplasmic reticulum. J Immunol 182: 4776-4783.
39. Paquet ME, Cohen-Doyle M, Shore GC, Williams DB (2004) Bap29/31 influences the intracellular traffic of MHC class I molecules. J Immunol 172: 7548-7555.
40. Szczesna-Skorupa E, Kemper B (2006) BAP31 is involved in the retention of cytochrome P450 2C2 in the endoplasmic reticulum. J Biol Chem 281: 4142-4148.
41. Ducret A, Nguyen M, Breckenridge DG, Shore GC (2003) The resident endoplasmic reticulum protein, BAP31, associates with gamma-actin and myosin B heavy chain. Eur J Biochem 270: 342-349.
42. Annaert WG, Becker B, Kistner U, Reth M, Jahn R (1997) Export of cellubrevin from the endoplasmic reticulum is controlled by BAP31. J Cell Biol 139: 1397-1410.
43. Lambert G, Becker B, Schreiber R, Boucherot A, Reth M, et al. (2001) Control of cystic fibrosis transmembrane conductance regulator expression by BAP31. J Biol Chem 276: 20340-20345.
44. Schamel WW, Kuppig S, Becker B, Gimborn K, Hauri HP, et al. (2003) A highmolecular- weight complex of membrane proteins BAP29/BAP31 is involved in the retention of membrane-bound IgD in the endoplasmic reticulum. Proc Natl Acad Sci U S A 100: 9861-9866.
45. Zen K, Utech M, Liu Y, Soto I, Nusrat A, et al. (2004) Association of BAP31 with CD11b/CD18. Potential role in intracellular trafficking of CD11b/CD18 in neutrophils. J Biol Chem 279: 44924-44930.
46. Regan JA, Laimins LA (2008) Bap31 is a novel target of the human papillomavirus E5 protein. J Virol 82: 10042-10051.
47. Wang B, Heath-Engel H, Zhang D, Nguyen N, Thomas DY, et al. (2008) BAP31 interacts with Sec61 translocons and promotes retrotranslocation of CFTRDeltaF508 via the derlin-1 complex. Cell 133: 1080-1092.
48. Bell AW, Ward MA, Blackstock WP, Freeman HN, Choudhary JS, et al. (2001) Proteomics characterization of abundant Golgi membrane proteins. J Biol Chem 276: 5152-5165.
49. Pure E, Cuff CA (2001) A crucial role for CD44 in inflammation. Trends Mol Med 7: 213-221.
50. Marhaba R, Zoller M (2004) CD44 in cancer progression: adhesion, migration and growth regulation. J Mol Histol 35: 211-231.
51. Johnson P, Ruffell B (2009) CD44 and its role in inflammation and inflammatory diseases. Inflamm Allergy Drug Targets 8: 208-220.
52. de la Hera A, Acevedo A, Marston W, Sanchez-Madrid F (1989) Function of CD44(Pgp-1) homing receptor in human T cell precursors. Int Immunol 1: 598-604.
53. Goodison S, Urquidi V, Tarin D (1999) CD44 cell adhesion molecules. Mol Pathol 52: 189-196.
54. Ishido S, Matsuki Y, Goto E, Kajikawa M, Ohmura-Hoshino M. MARCH-I: a new regulator of dendritic cell function. Mol Cells 29: 229-232.
55. Thankamony SP, Knudson W (2006) Acylation of CD44 and its association with lipid rafts are required for receptor and hyaluronan endocytosis. J Biol Chem 281: 34601-34609.
56. Levy S, Shoham T (2005) The tetraspanin web modulates immune-signalling complexes. Nat Rev Immunol 5: 136-148.
57. Fukuda H, Nakamura N, Hirose S (2006) MARCH-III Is a novel component of endosomes with properties similar to those of MARCH-II. J Biochem 139: 137-145.
58. Nakamura N, Fukuda H, Kato A, Hirose S (2005) MARCH-II is a syntaxin-6- binding protein involved in endosomal trafficking. Mol Biol Cell 16: 1696-1710.