Epstein-barr virus independent dysregulation of UBP43 expression alters interferon-stimulated gene expression in Burkitt lymphoma

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  Ruf, Ingrid K ^a   Houmani, Jennifer L ^a,c   Sample, Jeffery T ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c SHRINERS HOSPITAL FOR CHILDREN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; INTERFERON; INTERFERON RECEPTOR; JANUS KINASE 1; PROTEIN ISG15; PROTEIN UBP43; STAT1 PROTEIN; STAT2 PROTEIN; TYROSINE; UBIQUITIN; UNCLASSIFIED DRUG; PROTEINASE; STAT1 PROTEIN, HUMAN; STAT1 PROTEIN, MOUSE; USP18 PROTEIN, HUMAN; USP18 PROTEIN, MOUSE;

ARTICLE; BURKITT LYMPHOMA; CANCER CELL CULTURE; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EPSTEIN BARR VIRUS; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NEGATIVE FEEDBACK; NONHUMAN; SIGNAL TRANSDUCTION; VIRUS LATENCY; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; METABOLISM; MOUSE; PHOSPHORYLATION; TRANSGENIC MOUSE; TUMOR CELL LINE;

HUMAN HERPESVIRUS 4; MURINAE;

ANIMALS; BURKITT LYMPHOMA; CELL LINE, TUMOR; ENDOPEPTIDASES; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE EXPRESSION REGULATION, VIRAL; INTERFERONS; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; PHOSPHORYLATION; STAT1 TRANSCRIPTION FACTOR;

EID: 67650314599     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006023     Document Type: Article

References (41)

1. Boxer LM, Dang CV (2001) Translocations involving c-myc and c-myc function. Oncogene 20: 5595-5610.
2. Cai X, Schafer A, Lu S, Bilello JP, Desrosiers RC, et al. (2006) Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog 2: e23.
3. Kieff ED, Rickinson AB (2007) Epstein-Barr Virus and Its Replication. In: Knipe DM, H PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE, eds. Fields Virology. 5th ed. Philadelphia, PA: Lippincott, Williams & Wilkins. pp 2603-2654.
4. Pfeffer S, Zavolan M, Grasser FA, Chien M, Russo JJ, et al. (2004) Identification of Virus-Encoded MicroRNAs. Science 304: 734-736.
5. Thorley-Lawson DA, Allday MJ (2008) The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat Rev Microbiol 6: 913-924.
6. Hochberg D, Middeldorp JM, Catalina M, Sullivan JL, Luzuriaga K, et al. (2004) Demonstration of the Burkitt's lymphoma Epstein-Barr virus phenotype in dividing latently infected memory cells in vivo. Proc Natl Acad Sci U S A 101: 239-244.
7. Nanbo A, Inoue K, Adachi-Takasawa K, Takada K (2002) Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt's lymphoma. Embo J 21: 954-965.
8. Ruf IK, Lackey KA, Warudkar S, Sample JT (2005) Protection from Interferon-Induced Apoptosis by Epstein-Barr Virus Small RNAs Is Not Mediated by Inhibition of PKR. J Virol 79: 14562-14569.
9. Samanta M, Iwakiri D, Kanda T, Imaizumi T, Takada K (2006) EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. Embo J 25: 4207-4214.
10. Geiger TR, Martin JM (2006) The Epstein-Barr virus-encoded LMP-1 oncoprotein negatively affects Tyk2 phosphorylation and interferon signaling in human B cells. J Virol 80: 11638-11650.
11. Malakhov MP, Malakhova OA, Kim KI, Ritchie KJ, Zhang DE (2002) UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J Biol Chem 277: 9976-9981.
12. Malakhova OA, Yan M, Malakhov MP, Yuan Y, Ritchie KJ, et al. (2003) Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev 17: 455-460.
13. Malakhova OA, Kim KI, Luo JK, Zou W, Kumar KG, et al. (2006) UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. Embo J 25: 2358-2367.
14. Shimizu N, Tanabe-Tochikura A, Kuroiwa Y, Takada K (1994) Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBV-positive Burkitt's lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J Virol 68: 6069-6073.
15. Komano J, Maruo S, Kurozumi K, Oda T, Takada K (1999) Oncogenic role of Epstein-Barr virus-encoded RNAs in Burkitt's lymphoma cell line Akata. J Virol 73: 9827-9831.
16. Komano J, Sugiura M, Takada K (1998) Epstein-Barr virus contributes to the malignant phenotype and to apoptosis resistance in Burkitt's lymphoma cell line Akata. J Virol 72: 9150-9156.
17. Ruf IK, Rhyne PW, Yang C, Cleveland JL, Sample JT (2000) Epstein-Barr virus small RNAs potentiate tumorigenicity of Burkitt lymphoma cells independently of an effect on apoptosis. J Virol 74: 10223-10228.
18. Ruf IK, Rhyne PW, Yang H, Borza CM, Hutt-Fletcher LM, et al. (1999) Epstein-barr virus regulates c-MYC, apoptosis, and tumorigenicity in Burkitt lymphoma. Mol Cell Biol 19: 1651-1660.
19. Kelly G, Bell A, Rickinson A (2002) Epstein-Barr virus-associated Burkitt lymphomagenesis selects for downregulation of the nuclear antigen EBNA2. Nat Med 8: 1098-1104.
20. Yasukawa H, Sasaki A, Yoshimura A (2000) Negative regulation of cytokine signaling pathways. Annu Rev Immunol 18: 143-164.
21. Wen Z, Zhong Z, Darnell JE Jr (1995) Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82: 241-250.
22. Der SD, Zhou A, Williams BR, Silverman RH (1998) Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci U S A 95: 15623-15628.
23. Krebs DL, Hilton DJ (2001) SOCS proteins: negative regulators of cytokine signaling. Stem Cells 19: 378-387.
24. Randall G, Chen L, Panis M, Fischer AK, Lindenbach BD, et al. (2006) Silencing of USP18 potentiates the antiviral activity of interferon against hepatitis C virus infection. Gastroenterology 131: 1584-1591.
25. Loeb KR, Haas AL (1992) The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J Biol Chem 267: 7806-7813.
26. Kim KI, Yan M, Malakhova O, Luo JK, Shen MF, et al. (2006) Ube1L and protein ISGylation are not essential for alpha/beta interferon signaling. Mol Cell Biol 26: 472-479.
27. Knobeloch KP, Utermohlen O, Kisser A, Prinz M, Horak I (2005) Reexamination of the role of ubiquitin-like modifier ISG15 in the phenotype of UBP43-deficient mice. Mol Cell Biol 25: 11030-11034.
28. Osiak A, Utermohlen O, Niendorf S, Horak I, Knobeloch KP (2005) ISG15, an interferon-stimulated ubiquitin-like protein, is not essential for STAT1 signaling and responses against vesicular stomatitis and lymphocytic choriomeningitis virus. Mol Cell Biol 25: 6338-6345.
29. Kang D, Jiang H, Wu Q, Pestka S, Fisher PB (2001) Cloning and characterization of human ubiquitin-processing protease-43 from terminally differentiated human melanoma cells using a rapid subtraction hybridization protocol RaSH. Gene 267: 233-242.
30. Li XL, Hassel BA (2001) Involvement of proteasomes in gene induction by interferon and double-stranded RNA. Cytokine 14: 247-252.
31. Kim KI, Malakhova OA, Hoebe K, Yan M, Beutler B, et al. (2005) Enhanced antibacterial potential in UBP43-deficient mice against Salmonella typhimurium infection by up-regulating type I IFN signaling. J Immunol 175: 847-854.
32. Ritchie KJ, Hahn CS, Kim KI, Yan M, Rosario D, et al. (2004) Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat Med 10: 1374-1378.
33. Liu LQ, Ilaria R Jr, Kingsley PD, Iwama A, van Etten RA, et al. (1999) A novel ubiquitin-specific protease, UBP43, cloned from leukemia fusion protein AML1-ETO-expressing mice, functions in hematopoietic cell differentiation. Mol Cell Biol 19: 3029-3038.
34. Schwer H, Liu LQ, Zhou L, Little MT, Pan Z, et al. (2000) Cloning and characterization of a novel human ubiquitin-specific protease, a homologue of murine UBP43 (Usp18). Genomics 65: 44-52.
35. Rempel LA, Austin KJ, Ritchie KJ, Yan M, Shen M, et al. (2007) Ubp43 gene expression is required for normal Isg15 expression and fetal development. Reprod Biol Endocrinol 5: 13.
36. Ritchie KJ, Malakhov MP, Hetherington CJ, Zhou L, Little MT, et al. (2002) Dysregulation of protein modification by ISG15 results in brain cell injury. Genes Dev 16: 2207-2212.
37. Yan M, Luo JK, Ritchie KJ, Sakai I, Takeuchi K, et al. (2007) Ubp43 regulates BCR-ABL leukemogenesis via the type 1 interferon receptor signaling. Blood 110: 305-312.
38. Fok V, Friend K, Steitz JA (2006) Epstein-Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nucleocytoplasmic shuttling. J Cell Biol 173: 319-325.
39. Sample J, Henson EB, Sample C (1992) The Epstein-Barr virus nuclear protein 1 promoter active in type I latency is autoregulated. J Virol 66: 4654-4661.
40. Scholer HR, Hatzopoulos AK, Balling R, Suzuki N, Gruss P (1989) A family of octamer-specific proteins present during mouse embryogenesis: evidence for germline-specific expression of an Oct factor. Embo J 8: 2543-2550.
41. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.