Identification of the essential role of viral Bcl-2 for Kaposi's sarcoma-associated herpesvirus lytic replication

Journal of Virology

Volumn 89, Issue 10, 2015, Pages 5308-5317

  Liang, Qiming ^a   Chang, Brian ^a   Lee, Patrick ^a   Brulois, Kevin F ^a   Ge, Jianning ^a   Shi, Mude ^a   Rodgers, Mary A ^a,c   Feng, Pinghui ^a   Oh, Byung Ha ^b   Liang, Chengyu ^a   Jung, Jae U ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^c ABBOTT LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; GLUTAMIC ACID; MESSENGER RNA; PROTEIN BCL 2; VIRUS DNA; BCL-2 PROTEIN, HUMAN HERPESVIRUS 8; K7 PROTEIN, HUMAN HERPESVIRUS 8; MITOCHONDRIAL PROTEIN; ONCOPROTEIN; VIRAL FLIP PROTEIN, HUMAN HERPESVIRUS 8; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BCL 2 GENE; CONTROLLED STUDY; DNA REPLICATION; GENE DELETION; GENE DOSAGE; GENE EXPRESSION; HUMAN HERPESVIRUS 8; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; VIRUS GENOME; VIRUS REPLICATION; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; APOPTOSIS; AUTOPHAGY; CELL LINE; GENE INACTIVATION; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS;

HUMAN HERPESVIRUS 8;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; APOPTOSIS; AUTOPHAGY; BASE SEQUENCE; CELL LINE; DNA REPLICATION; DNA, VIRAL; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; GENOME, VIRAL; HEK293 CELLS; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; ONCOGENE PROTEINS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84928555434     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00102-15     Document Type: Article

References (45)

1. Mesri EA, Cesarman E, Boshoff C. 2010. Kaposi's sarcoma and its associated herpesvirus. Nat Rev Cancer 10:707-719. http://dx.doi.org/10.1038/nrc2888.
2. Gross A, McDonnell JM, Korsmeyer SJ. 1999. BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13:1899-1911. http://dx.doi.org/10.1101/gad.13.15.1899.
3. Ye F, Lei X, Gao SJ. 2011. Mechanisms of Kaposi's sarcoma-associated herpesvirus latency and reactivation. Adv Virol 2011:193860. http://dx.doi.org/10.1155/2011/193860.
4. Ganem D. 2010. KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. J Clin Invest 120:939-949. http://dx.doi.org/10.1172/JCI40567.
5. Sun R, Lin SF, Staskus K, Gradoville L, Grogan E, Haase A, Miller G. 1999. Kinetics of Kaposi's sarcoma-associated herpesvirus gene expression. J Virol 73:2232-2242.
6. Klionsky DJ. 2005. The molecular machinery of autophagy: unanswered questions. J Cell Sci 118:7-18. http://dx.doi.org/10.1242/jcs.01620.
7. Rodgers MA, Bowman JW, Liang Q, Jung JU. 2014. Regulation where autophagy intersects the inflammasome. Antioxid Redox Signal 20:495-506. http://dx.doi.org/10.1089/ars.2013.5347.
8. Liang C, Lee JS, Jung JU. 2008. Immune evasion in Kaposi's sarcomaassociated herpes virus associated oncogenesis. Semin Cancer Biol 18: 423-436. http://dx.doi.org/10.1016/j.semcancer.2008.09.003.
9. Liang Q, Chang B, Brulois KF, Castro K, Min CK, Rodgers MA, Shi M, Ge J, Feng P, Oh BH, Jung JU. 2013. Kaposi's sarcoma-associated herpesvirus K7 modulates Rubicon-mediated inhibition of autophagosome maturation. J Virol 87:12499-12503. http://dx.doi.org/10.1128/JVI.01898-13.
10. Liang Q, Fu B, Wu F, Li X, Yuan Y, Zhu F. 2012. ORF45 of Kaposi's sarcoma-associated herpesvirus inhibits phosphorylation of interferon regulatory factor 7 by IKKepsilon and TBK1 as an alternative substrate. J Virol 86:10162-10172. http://dx.doi.org/10.1128/JVI.05224-11.
11. E X, Hwang S, Oh S, Lee JS, Jeong JH, Gwack Y, Kowalik TF, Sun R, Jung JU, Liang C. 2009. Viral Bcl-2-mediated evasion of autophagy aids chronic infection of gammaherpesvirus 68. PLoS Pathog 5:e1000609. http://dx.doi.org/10.1371/journal.ppat.1000609.
12. Lee JS, Li Q, Lee JY, Lee SH, Jeong JH, Lee HR, Chang H, Zhou FC, Gao SJ, Liang C, Jung JU. 2009. FLIP-mediated autophagy regulation in cell death control. Nat Cell Biol 11:1355-1362. http://dx.doi.org/10.1038/ncb1980.
13. Sarid R, Sato T, Bohenzky RA, Russo JJ, Chang Y. 1997. Kaposi's sarcoma-associated herpesvirus encodes a functional bcl-2 homologue. Nat Med 3:293-298. http://dx.doi.org/10.1038/nm0397-293.
14. Skommer J, Wlodkowic D, Deptala A. 2007. Larger than life: mitochondria and the Bcl-2 family. Leuk Res 31:277-286. http://dx.doi.org/10.1016/j.leukres.2006.06.027.
15. Walensky LD. 2006. BCL-2 in the crosshairs: tipping the balance of life and death. Cell Death Differ 13:1339-1350. http://dx.doi.org/10.1038/sj.cdd.4401992.
16. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, Hsieh JJ, Cheng EH. 2006. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 8:1348-1358. http://dx.doi.org/10.1038/ncb1499.
17. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, Czabotar PE, Ierino H, Lee EF, Fairlie WD, Bouillet P, Strasser A, Kluck RM, Adams JM, Huang DC. 2007. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315:856-859. http://dx.doi.org/10.1126/science.1133289.
18. Antignani A, Youle RJ. 2006. How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr Opin Cell Biol 18:685-689. http://dx.doi.org/10.1016/j.ceb.2006.10.004.
19. Green DR, Kroemer G. 2004. The pathophysiology of mitochondrial cell death. Science 305:626-629. http://dx.doi.org/10.1126/science.1099320.
20. Adams JM, Cory S. 2001. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci 26:61-66. http://dx.doi.org/10.1016/S0968-0004(00)01740-0.
21. Opferman JT, Korsmeyer SJ. 2003. Apoptosis in the development and maintenance of the immune system. Nat Immunol 4:410-415. http://dx.doi.org/10.1038/ni0503-410.
22. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, Herman B, Levine B. 1998. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol 72:8586-8596.
23. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927-939. http://dx.doi.org/10.1016/j.cell.2005.07.002.
24. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, Hickman JA, Geneste O, Kroemer G. 2007. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 26:2527-2539. http://dx.doi.org/10.1038/sj.emboj.7601689.
25. de Lima BD, May JS, Marques S, Simas JP, Stevenson PG. 2005. Murine gammaherpesvirus 68 bcl-2 homologue contributes to latency establishment in vivo. J Gen Virol 86:31-40. http://dx.doi.org/10.1099/vir.0.80480-0.
26. Gangappa S, van Dyk LF, Jewett TJ, Speck SH, Virgin HW, IV. 2002. Identification of the in vivo role of a viral bcl-2. J Exp Med 195:931-940. http://dx.doi.org/10.1084/jem.20011825.
27. Herskowitz JH, Jacoby MA, Speck SH. 2005. The murine gammaherpesvirus 68 M2 gene is required for efficient reactivation from latently infected B cells. J Virol 79:2261-2273. http://dx.doi.org/10.1128/JVI.79.4.2261-2273.2005.
28. Loh J, Huang Q, Petros AM, Nettesheim D, van Dyk LF, Labrada L, Speck SH, Levine B, Olejniczak ET, Virgin HW, IV. 2005. A surface groove essential for viral Bcl-2 function during chronic infection in vivo. PLoS Pathog 1:e10. http://dx.doi.org/10.1371/journal.ppat.0010010.
29. Brulois KF, Chang H, Lee AS, Ensser A, Wong LY, Toth Z, Lee SH, Lee HR, Myoung J, Ganem D, Oh TK, Kim JF, Gao SJ, Jung JU. 2012. Construction and manipulation of a new Kaposi's sarcoma-associated herpesvirus bacterial artificial chromosome clone. J Virol 86:9708-9720. http://dx.doi.org/10.1128/JVI.01019-12.
30. Gelgor A, Kalt I, Bergson S, Brulois KF, Jung JU, Sarid R. 2015. Viral Bcl-2 encoded by the Kaposi's sarcoma-associated herpesvirus is vital for virus reactivation. J Virol 89:5298-5307. http://dx.doi.org/10.1128/JVI.00098-15.
31. Ciufo DM, Cannon JS, Poole LJ, Wu FY, Murray P, Ambinder RF, Hayward GS. 2001. Spindle cell conversion by Kaposi's sarcomaassociated herpesvirus: formation of colonies and plaques with mixed lytic and latent gene expression in infected primary dermal microvascular endothelial cell cultures. J Virol 75:5614-5626. http://dx.doi.org/10.1128/JVI.75.12.5614-5626.2001.
32. Li M, MacKey J, Czajak SC, Desrosiers RC, Lackner AA, Jung JU. 1999. Identification and characterization of Kaposi's sarcoma-associated herpesvirus K8.1 virion glycoprotein. J Virol 73:1341-1349.
33. Amini-Bavil-Olyaee S, Choi YJ, Lee JH, Shi M, Huang IC, Farzan M, Jung JU. 2013. The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe 13:452-464. http://dx.doi.org/10.1016/j.chom.2013.03.006.
34. Liang Q, Seo GJ, Choi YJ, Kwak MJ, Ge J, Rodgers MA, Shi M, Leslie BJ, Hopfner KP, Ha T, Oh BH, Jung JU. 2014. Crosstalk between the cGAS DNA sensor and Beclin-1 autophagy protein shapes innate antimicrobial immune responses. Cell Host Microbe 15:228-238. http://dx.doi.org/10.1016/j.chom.2014.01.009.
35. Liang Q, Seo GJ, Choi YJ, Ge J, Rodgers MA, Shi M, Jung JU. 2014. Autophagy side of MB21D1/cGAS DNA sensor. Autophagy 10:1146-1147. http://dx.doi.org/10.4161/auto.28769.
36. Vieira J, O'Hearn PM. 2004. Use of the red fluorescent protein as a marker of Kaposi's sarcoma-associated herpesvirus lytic gene expression. Virology 325:225-240. http://dx.doi.org/10.1016/j.virol.2004.03.049.
37. Tischer BK, Smith GA, Osterrieder N. 2010. En passant mutagenesis: a two step markerless Red recombination system. Methods Mol Biol 634: 421-430. http://dx.doi.org/10.1007/978-1-60761-652-8_30.
38. Tischer BK, von Einem J, Kaufer B, Osterrieder N. 2006. Two-step Red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques 40:191-197. http://dx.doi.org/10.2144/000112096.
39. Myoung J, Ganem D. 2011. Generation of a doxycycline-inducible KSHV producer cell line of endothelial origin: maintenance of tight latency with efficient reactivation upon induction. J Virol Methods 174:12-21. http://dx.doi.org/10.1016/j.jviromet.2011.03.012.
40. Ku B, Woo JS, Liang C, Lee KH, Hong HS, E X, Kim KS, Jung JU, Oh BH. 2008. Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. PLoS Pathog 4:e25. http://dx.doi.org/10.1371/journal.ppat.0040025.
41. Altmann M, Hammerschmidt W. 2005. Epstein-Barr virus provides a new paradigm: a requirement for the immediate inhibition of apoptosis. PLoS Biol 3:e404. http://dx.doi.org/10.1371/journal.pbio.0030404.
42. Wu TT, Liao HI, Tong L, Leang RS, Smith G, Sun R. 2011. Construction and characterization of an infectious murine gammaherpesivrus-68 bacterial artificial chromosome. J Biomed Biotechnol 2011:926258. http://dx.doi.org/10.1155/2011/926258.
43. Marc D. 2014. Influenza virus non-structural protein NS1: interferon antagonism and beyond. J Gen Virol 95:2594-2611. http://dx.doi.org/10.1099/vir.0.069542-0.
44. Audet J, Kobinger GP. 2015. Immune evasion in ebolavirus infections. Viral Immunol 28:10-18. http://dx.doi.org/10.1089/vim.2014.0066.
45. Hagglund R, Roizman B. 2004. Role of ICP0 in the strategy of conquest of the host cell by herpes simplex virus 1. J Virol 78:2169-2178. http://dx.doi.org/10.1128/JVI.78.5.2169-2178.2004.