A single viral protein HCMV US2 affects antigen presentation and intracellular iron homeostasis by degradation of classical HLA class I and HFE molecules

Blood

Volumn 101, Issue 7, 2003, Pages 2858-2864

  Vahdati Ben Arieh, Sayeh ^b   Laham, Nihay ^b   Schechter, Chana ^b   Yewdell, Jon W ^b   Coligan, John E ^b   Ehrlich, Rachel ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

FERRITIN; HFE PROTEIN; HLA ANTIGEN CLASS 1; IRON; PROTEIN US2; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; HFE PROTEIN, HUMAN; HLA ANTIGEN; MEMBRANE PROTEIN; US2 PROTEIN, VARICELLOVIRUS; VIRUS ENVELOPE PROTEIN;

ANTIGEN PRESENTATION; ARTICLE; CELL METABOLISM; CELL SURFACE; CONTROLLED STUDY; CYTOMEGALOVIRUS; EMBRYO; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC TRANSFECTION; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IRON METABOLISM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN TARGETING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; STATISTICAL SIGNIFICANCE; SYNTHESIS; WESTERN BLOTTING; CELL LINE; CHEMISTRY; DOWN REGULATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ANTIGEN PRESENTATION; CELL LINE; CYTOMEGALOVIRUS; DOWN-REGULATION; FERRITINS; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HOMEOSTASIS; HUMANS; IRON; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; RECEPTORS, TRANSFERRIN; TRANSFECTION; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS;

EID: 0038701031     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2002-07-2158     Document Type: Article

References (52)

1. del Val M, Hengel H, Hacker H, et al. Cytomega-lovirus prevents antigen presentation by blocking the transport of peptide-loaded major histocompatibility complex class I molecules into the medial-Golgi compartment. J Exp Med. 1992;176:729-738.
2. Beersma MF, Bijlmakers MJ, Ploegh HL. Human cytomegalovirus down-regulates HLA class I expression by reducing the stability of class I H chains. J Immunol. 1993;151:4455-4464.
3. Yamashita Y, Shimokata K, Mizuno S, Yamaguchi H, Nishiyama Y. Down-regulation of the surface expression of class I MHC antigens by human cytomegarovirus. Virology. 1993;193:727-736.
4. Jones TR, Hanson LK, Sun L, Slater JS, Stenberg RM, Campbell AE. Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains. J Virol. 1995;69:4830-4841.
5. Jones TR, Wiertz EJ, Sun L, Fish KN, Nelson JA, Ploegh HL. Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc Natl Acad Sci U S A. 1996;93:11327-11333.
6. Wiertz EJ, Jones TR, Sun L, Bogyo M, Geuze HJ, Ploegh HL. The human cytomegarovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell. 1996;84:769-779.
7. Wiertz EJ, Tortorella D, Bogyo M, et al. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature. 1996;384:432-438.
8. Ahn K, Angulo A, Ghazal P, Peterson PA, Yang Y, Fruh K. Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc Natl Acad Sci U S A. 1996;93:10990-10995
9. Hengel H, Flohr T, Hammerling GJ, Koszinowski UH, Momburg F. Human cytomegalovirus inhibits peptide translocation into the endoplasmic reticulum for MHC class I assembly. J Gen Virol. 1996;77:2287-2296.
10. Hengel H, Koopmann JO, Flohr T, et al. Aviral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity. 1997;6:623-632.
11. Lehner PJ, Karttunen JT, Wilkinson GW, Cresswell P. The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc Natl Acad Sci U S A. 1997;94:6904-6909.
12. Machold RP, Wiertz EJ, Jones TR, Ploegh HL. The HCMV gene products US11 and US2 differ in their ability to attack allelic forms of murine major histocompatibility complex (MHC) class I heavy chains. J Exp Med. 1997;185:363-366.
13. Schust DJ, Tortorella D, Seebach J, Phan C, Ploegh HL. Trophoblast class I major histocompatibility complex (MHC) products are resistant to rapid degradation imposed by the human cytomegalovirus (HCMV) gene products US2 and US11. J Exp Med. 1998;188:497-503.
14. Schust DJ, Tortorella D, Ploegh HL. HLA-G and HLA-C at the feto-maternal interface: lessons learned from pathogenic viruses. Semin Cancer Biol. 1999;9:37-46.
15. Gewurz BE, Gaudet R, Tortorella D, Wang EW, Ploegh HL. Virus subversion of immunity: a structural perspective. Curr Opin Immunol. 2001;13:442-450.
16. Tomazin R, Boname J, Hegde NR, et al. Cytomegalovirus US2 destroys two components of the MHC class II pathway, preventing recognition by CD4+ T cells. Nat Med. 1999;5:1039-1043.
17. Chevalier MS, Daniels GM, Johnson DC. Binding of human cytomegalovirus US2 to major histocompatibility complex class I and II proteins is not sufficient for their degradation. J Virol. 2002;76:8265-8275.
18. Rehm A, Engelsberg A, Tortorella D, et al. Human cytomegalovirus gene products US2 and US11 differ in their ability to attack major histocompatibility class I heavy chains in dendritic cells. J Virol. 2002;76:5043-5050.
19. Ben-Arieh SV, Zimerman B, Smorodinsky NI, et al. Human cytomegalovirus protein US2 interferes with the expression of human HFE, a nonclassical class I major histocompatibility complex molecule that regulates iron homeostasis. J Virol. 2001;75:10557-10562.
20. Lebron JA, Bjorkman PJ. The transferrin receptor binding site on HFE, the class I MHC-related protein mutated in hereditary hemochromatosis. J Mol Biol. 1999;289:1109-1118.
21. Lebron JA, West AP Jr, Bjorkman PJ. The hemochromatosis protein HFE competes with transferrin for binding to the transferrin receptor. J Mol Biol. 1999;294;239-245.
22. Roy CN, Penny DM, Feder JN, Enns CA. The hereditary hemochromatosis protein, HFE, specifically regulates transferrin-mediated iron uptake in HeLa cells. J Biol Chem. 1999;274:9022-9028.
23. Salter-Cid L, Brunmark A, Li Y, et al. Transferrin receptor is negatively modulated by the hemochromatosis protein HFE: implications for cellular iron homeostasis. Proc Natl Acad Sci U S A. 1999;96:5434-5439.
24. Feder JN, Tsuchihashi Z, Irrinki A, et al. The hemochromatosis founder mutation in HLA-H disrupts beta2-microglobulin interaction and cell surface expression. J Biol Chem. 1997;272:14025-14028.
25. Feder JN, Gnirke A, Thomas W, et al. A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat Genet. 1996;13:399-408.
26. Rothenberg BE, Voland JR. beta2 knockout mice develop parenchymal iron overload: a putative role for class I genes of the major histocompatibillty complex in iron metabolism. Proc Natl Acad Sci U S A. 1996;93:1529-1534.
27. Santos M, Schilham MW, Rademakers LH, Marx JJ, de Sousa M, Clevers H. Defective iron homeostasis in beta 2-microglobulin knockout mice recapitulates hereditary hemochromatosis in man. J Exp Med. 1996;184:1975-1985.
28. Zhou XY, Tomatsu S, Fleming RE, et al. HFE gene knockout produces mouse model of hereditary hemochromatosis. Proc Natl Acad Sci U S A. 1998;95:2492-2497.
29. Fromm SV, Mey-Tal SW, Coligan JE, Schechter C, Ehrlich R. MHC class I heavy chain mRNA must exceed a threshold level for the reconstitution of cell surface expression of class I MHC complexes in cells transformed by the highly oncogenic adenovirus 12. J Biol Chem. 1998;273:15209-15216.
30. Parham P, Barnstable CJ, Bodmer WF. Use of a monoclonal antibody (W6/32) in structural studies of HLA-A, B, C antigens. J Immunol. 1979;123:342-349.
31. Riedel HD, Muckenthaler MU, Gehrke SG, et al. HFE downregulates iron uptake from transferrin and induces iron-regulatory protein activity in stably transfected cells. Blood. 1999;94:3915-3921.
32. Corsi B, Levi S, Cozzi A, et al. Overexpression of the hereditary hemochromatosis protein, HFE, in HeLa cells induces and iron-deficient phenotype. FEBS Lett. 1999;460:149-152.
33. Roy CN, Blemings KP, Deck KM, et al. Increased IRP1 and IRP2 RNA binding activity accompanies a reduction of the labile iron pool in HFE-expressing cells. J Cell Physiol. 2002;190:218-226.
34. Waheed A, Grubb JH, Zhou XY, et al. Regulation of transferrin-mediated iron uptake by HFE, the protein defective in hereditary hemochromatosis. Proc Natl Acad Sci U S A. 2002;99:3117-3122.
35. Tortorella D, Gewurz BE, Furman MH, Schust DJ, Ploegh HL. Viral subversion of the immune system. Annu Rev Immunol. 2000;18:861-926.
36. Sinzger C, Bissinger AL, Viebahn R, et al. Hepatocytes are permissive for human cytomegalovirus infection in human liver cell culture and in vivo. J Infect Dis. 1999;180:976-986.
37. Sinzger C, Grefte A, Plachter B, Gouw AS, The TH, Jahn G. Fibroblasts, epithelial cells, endothelial cells and smooth muscle cells are major targets of human cytomegalovirus infection in lung and gastrointestinal tissues. J Gen Virol. 1995;76:741-750.
38. Snover DC, Horwitz CA. Liver disease in cytomegalovirus mononucleosis: a light microscopical and immunoperoxidase study of six cases. Hepatology. 1984;4:408-412.
39. Ten Napel HH, Houthoff HJ, The TH. Cytomegalovirus hepatitis in normal and immune compromised hosts. Liver. 1984;4:184-194.
40. Loenen WA, Bruggeman CA, Wiertz EJ. Immune evasion by human cytomegalovirus: lessons in immunology and cell biology. Semin Immunol. 2001;13:41-49.
41. Cotte L, Drouet E, Bissuel F, Denoyel GA, Trepo C. Diagnostic value of amplification of human cytomegalovirus DNA from gastrointestinal biopsies from human immunodeficiency virus-infected patients. J Clin Microbiol. 1993;31:2066-2069.
42. Fiebiger E, Story C, Ploegh HL, Tortorella D. Visualization of the ER-to-cytosol dislocation reaction of a type I membrane protein. EMBO J. 2002;21:1041-1053.
43. Gewurz BE, Gaudet R, Tortorella D, Wang EW, Ploegh HL, Wiley DC. Antigen presentation subverted: structure of the human cytomegalovirus protein US2 bound to the class I molecule HLAA2. Proc Natl Acad Sci U S A. 2001;98:6794-6799.
44. Pazmany L, Mandelboim O, Vales-Gomez M, Davis DM, Reyburn HT, Strominger JL. Protection from natural killer cell-mediated lysis by HLA-G expression on target cells. Science. 1996;274:792-795.
45. Zemmour J, Parham P. Distinctive polymorphism at the HLA-C locus: implications for the expression of HLA-C. J Exp Med. 1992;176:937-950.
46. Di Bisceglie AM, Bonkovsky HL, Chopra S, et al. Iron reduction as an adjuvant to interferon therapy in patients with chronic hepatitis C who have previously not responded to interferon: a multicenter, prospective, randomized, controlled trial. Hepatology. 2000;32:135-138.
47. Cagnoni C, Corsini F, Pancotti D, Carrara G. Effect of iron depletion on long-term response to interferon in patients with chronic hepatitis C with increased plasma iron without accumulation of liver iron]. Ann Ital Med Int. 2000;15:132-138.
48. Kakizaki S, Takagi H, Horiguchi N, et al. Iron enhances hepatitis C virus replication in cultured human hepatocytes. Liver. 2000;20:125-128.
49. Georgiou NA, van der Bruggen T, Oudshoorn M, Nottet HS, Marx JJ, van Asbeck BS. Inhibition of human immunodeficiency virus type 1 replication in human mononuclear blood cells by the iron chelators deferoxamine, deferiprone, and bleomycin. J Infect Dis. 2000;181:484-490.
50. Savarino A, Pescarmona GP, Boelaert JR. Iron metabolism and HIV infection: reciprocal interactions with potentially harmful consequences? Cell Biochem Funct. 1999;17:279-287.
51. Martelius T, Scholz M, Krogerus L, et al. Antiviral and immunomodulatory effects of desferrioxamine in cytomegalovirus-infected rat liver allografts with rejection. Transplantation. 1999;68:1753-1761.
52. Zoll J, Melchers WJ, Galama JM, van Kuppeveld FJ. The mengovirus leader protein suppresses alpha/beta interferon production by inhibition of the iron/ferritin-mediated activation of NF-kappa B. J Virol. 2002;76:9664-9672.