Identification of Caspase Cleavage Sites in KSHV Latency-Associated Nuclear Antigen and Their Effects on Caspase-Related Host Defense Responses

PLoS Pathogens

Volumn 11, Issue 7, 2015, Pages

  Davis, David A ^a   Naiman, Nicole E ^a   Wang, Victoria ^a   Shrestha, Prabha ^a   Haque, Muzammel ^a   Hu, Duosha ^a   Anagho, Holda A ^a   Carey, Robert F ^a   Davidoff, Katharine S ^a   Yarchoan, Robert ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 3; HYDROGEN PEROXIDE; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LATENCY ASSOCIATED NUCLEAR ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; VIRUS DNA; CASP3 PROTEIN, HUMAN; LATENCY-ASSOCIATED NUCLEAR ANTIGEN; NUCLEAR PROTEIN; VIRUS ANTIGEN;

ANGIOFOLLICULAR LYMPH NODE HYPERPLASIA; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; KAPOSI SARCOMA; MUTATION; OXIDATIVE STRESS; PRIMARY EFFUSION LYMPHOMA; PROTEIN CLEAVAGE; SEQUENCE ANALYSIS; VIRUS GENE; VIRUS LATENCY; GENETICS; HOST PARASITE INTERACTION; METABOLISM; PHYSIOLOGY; VIROLOGY;

HERPESVIRIDAE; HUMAN HERPESVIRUS 8;

ANTIGENS, VIRAL; APOPTOSIS; CASPASE 1; CASPASE 3; HERPESVIRUS 8, HUMAN; HOST-PARASITE INTERACTIONS; HUMANS; LYMPHOMA, PRIMARY EFFUSION; NUCLEAR PROTEINS; SARCOMA, KAPOSI; VIRUS LATENCY;

EID: 84938791570     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005064     Document Type: Article

References (52)

1. Benedict CA, Norris PS, Ware CF, (2002) To kill or be killed: viral evasion of apoptosis. Nat Immunol 3: 1013–1018. 12407409
2. Clem RJ, (2001) Baculoviruses and apoptosis: the good, the bad, and the ugly. Cell Death Differ 8: 137–143. 11313715
3. Means RE, Choi JK, Nakamura H, Chung YH, Ishido S, et al. (2002) Immune evasion strategies of Kaposi's sarcoma-associated herpesvirus. Curr Top Microbiol Immunol 269: 187–201. 12224509
4. Moore PS, (2007) KSHV manipulation of the cell cycle and apoptosis.
5. Richard A, Tulasne D, (2012) Caspase cleavage of viral proteins, another way for viruses to make the best of apoptosis. Cell Death Dis 3: e277. doi: 10.1038/cddis.2012.18 22402601
6. Singh VV, Kerur N, Bottero V, Dutta S, Chakraborty S, et al. (2013) Kaposi's sarcoma-associated herpesvirus latency in endothelial and B cells activates gamma interferon-inducible protein 16-mediated inflammasomes. J Virol 87: 4417–4431. doi: 10.1128/JVI.03282-12 23388709
7. Gantt S, Casper C, (2011) Human herpesvirus 8-associated neoplasms: the roles of viral replication and antiviral treatment. Curr Opin Infect Dis 24: 295–301. doi: 10.1097/QCO.0b013e3283486d04 21666458
8. Polizzotto MN, Uldrick TS, Hu D, Yarchoan R, (2012) Clinical Manifestations of Kaposi Sarcoma Herpesvirus Lytic Activation: Multicentric Castleman Disease (KSHV-MCD) and the KSHV Inflammatory Cytokine Syndrome. Front Microbiol 3: 73. doi: 10.3389/fmicb.2012.00073 22403576
9. Belanger C, Gravel A, Tomoiu A, Janelle ME, Gosselin J, et al. (2001) Human herpesvirus 8 viral FLICE-inhibitory protein inhibits Fas-mediated apoptosis through binding and prevention of procaspase-8 maturation. J Hum Virol 4: 62–73. 11437316
10. Guasparri I, Keller SA, Cesarman E, (2004) KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med 199: 993–1003. 15067035
11. Sun Q, Matta H, Chaudhary PM, (2003) The human herpes virus 8-encoded viral FLICE inhibitory protein protects against growth factor withdrawal-induced apoptosis via NF-kappa B activation. Blood 101: 1956–1961. 12406869
12. Thurau M, Marquardt G, Gonin-Laurent N, Weinlander K, Naschberger E, et al. (2009) Viral inhibitor of apoptosis vFLIP/K13 protects endothelial cells against superoxide-induced cell death. J Virol 83: 598–611. doi: 10.1128/JVI.00629-08 18987137
13. Friborg J, Jr.Kong W, Hottiger MO, Nabel GJ, (1999) p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 402: 889–894. 10622254
14. Suffert G, Malterer G, Hausser J, Viiliainen J, Fender A, et al. (2011) Kaposi's sarcoma herpesvirus microRNAs target caspase 3 and regulate apoptosis. PLoS Pathog 7: e1002405. doi: 10.1371/journal.ppat.1002405 22174674
15. Lagos D, Trotter MW, Vart RJ, Wang HW, Matthews NC, et al. (2007) Kaposi sarcoma herpesvirus-encoded vFLIP and vIRF1 regulate antigen presentation in lymphatic endothelial cells. Blood 109: 1550–1558. 17047149
16. Kwun HJ, da Silva SR, Qin H, Ferris RL, Tan R, et al. (2011) The central repeat domain 1 of Kaposi's sarcoma-associated herpesvirus (KSHV) latency associated-nuclear antigen 1 (LANA1) prevents cis MHC class I peptide presentation. Virology 412: 357–365. doi: 10.1016/j.virol.2011.01.026 21324504
17. Gregory SM, Davis BK, West JA, Taxman DJ, Matsuzawa S, et al. (2011) Discovery of a viral NLR homolog that inhibits the inflammasome. Science 331: 330–334. doi: 10.1126/science.1199478 21252346
18. Mathew SS, Bryant PW, Burch AD, (2010) Accumulation of oxidized proteins in Herpesvirus infected cells. Free Radic Biol Med 49: 383–391. doi: 10.1016/j.freeradbiomed.2010.04.026 20441790
19. Kamranvar SA, Masucci MG, The Epstein-Barr virus nuclear antigen-1 promotes telomere dysfunction via induction of oxidative stress. Leukemia 25: 1017–1025. doi: 10.1038/leu.2011.35 21394098
20. Kim JC, Choi SH, Kim JK, Kim Y, Kim HJ, et al. (2008) [Herpes simplex virus type 1 ICP27 induces apoptotic cell death by increasing intracellular reactive oxygen species]. Mol Biol (Mosk) 42: 470–477.
21. Lassoued S, Ben Ameur R, Ayadi W, Gargouri B, Ben Mansour R, et al. (2008) Epstein-Barr virus induces an oxidative stress during the early stages of infection in B lymphocytes, epithelial, and lymphoblastoid cell lines. Mol Cell Biochem 313: 179–186. doi: 10.1007/s11010-008-9755-z 18414998
22. Ma Q, Cavallin LE, Leung HJ, Chiozzini C, Goldschmidt-Clermont PJ, et al. (2012) A role for virally induced reactive oxygen species in Kaposi's sarcoma herpesvirus tumorigenesis. Antioxid Redox Signal 18: 80–90. doi: 10.1089/ars.2012.4584 22746102
23. Qin Z, Freitas E, Sullivan R, Mohan S, Bacelieri R, et al. Upregulation of xCT by KSHV-encoded microRNAs facilitates KSHV dissemination and persistence in an environment of oxidative stress. PLoS Pathog 6: e1000742. doi: 10.1371/journal.ppat.1000742 20126446
24. Li X, Feng J, Sun R, (2010) Oxidative stress induces reactivation of Kaposi's sarcoma-associated herpesvirus and death of primary effusion lymphoma cells. J Virol 85: 715–724. doi: 10.1128/JVI.01742-10 21068240
25. Ye F, Zhou F, Bedolla RG, Jones T, Lei X, et al. (2011) Reactive oxygen species hydrogen peroxide mediates Kaposi's sarcoma-associated herpesvirus reactivation from latency. PLoS Pathog 7: e1002054. doi: 10.1371/journal.ppat.1002054 21625536
26. Ahn BY, Moss B, (1992) Glutaredoxin homolog encoded by vaccinia virus is a virion-associated enzyme with thioltransferase and dehydroascorbate reductase activities. Proc Natl Acad Sci U S A 89: 7060–7064. 1496000
27. Toptan T, Fonseca L, Kwun HJ, Chang Y, Moore PS, (2013) Complex alternative cytoplasmic protein isoforms of the Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 generated through noncanonical translation initiation. J Virol 87: 2744–2755. doi: 10.1128/JVI.03061-12 23255808
28. Song J, Tan H, Shen H, Mahmood K, Boyd SE, et al. Cascleave: towards more accurate prediction of caspase substrate cleavage sites. Bioinformatics 26: 752–760. doi: 10.1093/bioinformatics/btq043 20130033
29. Brooks H, Lebleu B, Vives E, (2005) Tat peptide-mediated cellular delivery: back to basics. Adv Drug Deliv Rev 57: 559–577. 15722164
30. Garnier P, Ying W, Swanson RA, (2003) Ischemic preconditioning by caspase cleavage of poly(ADP-ribose) polymerase-1. J Neurosci 23: 7967–7973. 12954857
31. Benedettini E, Sholl LM, Peyton M, Reilly J, Ware C, et al. Met activation in non-small cell lung cancer is associated with de novo resistance to EGFR inhibitors and the development of brain metastasis. Am J Pathol 177: 415–423. doi: 10.2353/ajpath.2010.090863 20489150
32. Muruve DA, Petrilli V, Zaiss AK, White LR, Clark SA, et al. (2008) The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 452: 103–107. doi: 10.1038/nature06664 18288107
33. Jacobs SR, Damania B, (2012) NLRs, inflammasomes, and viral infection. J Leukoc Biol 92: 469–477. doi: 10.1189/jlb.0312132 22581934
34. McAuley JL, Tate MD, MacKenzie-Kludas CJ, Pinar A, Zeng W, et al. (2013) Activation of the NLRP3 inflammasome by IAV virulence protein PB1-F2 contributes to severe pathophysiology and disease. PLoS Pathog 9: e1003392. doi: 10.1371/journal.ppat.1003392 23737748
35. Earnshaw WC, Martins LM, Kaufmann SH, (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68: 383–424. 10872455
36. Cherezova L, Burnside KL, Rose TM, (2011) Consrvation of Complex Nuclear Localization Signals Utilizing Classical and Non-classical Nuclear Import Pathways in LANA Homologs of KSHV and RFHV. PLoS One 6: e18920. doi: 10.1371/journal.pone.0018920 21559489
37. Schwam DR, Luciano RL, Mahajan SS, Wong L, Wilson AC, (2000) Carboxy terminus of human herpesvirus 8 latency-associated nuclear antigen mediates dimerization, transcriptional repression, and targeting to nuclear bodies. J Virol 74: 8532–8540. 10954554
38. Campbell M, Chang PC, Huerta S, Izumiya C, Davis R, et al. (2012) Protein arginine methyltransferase 1-directed methylation of Kaposi sarcoma-associated herpesvirus latency-associated nuclear antigen. J Biol Chem 287: 5806–5818. doi: 10.1074/jbc.M111.289496 22179613
39. Woodard C, Shamay M, Liao G, Zhu J, Ng AN, et al. (2012) Phosphorylation of the chromatin binding domain of KSHV LANA. PLoS Pathog 8: e1002972. doi: 10.1371/journal.ppat.1002972 23093938
40. Bajaj BG, Verma SC, Lan K, Cotter MA, Woodman ZL, et al. (2006) KSHV encoded LANA upregulates Pim-1 and is a substrate for its kinase activity. Virology 351: 18–28. 16647097
41. Moore PS, Chang Y, (2001) Molecular virology of Kaposi's sarcoma-associated herpesvirus. Philos Trans R Soc Lond B Biol Sci 356: 499–516. 11313008
42. 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. 9055856
43. Zoeteweij JP, Rinderknecht AS, Davis DA, Yarchoan R, Blauvelt A, (2002) Minimal reactivation of Kaposi's sarcoma-associated herpesvirus by corticosteroids in latently infected B cell lines. J Med Virol 66: 378–383. 11793390
44. Wang L, Damania B, (2008) Kaposi's sarcoma-associated herpesvirus confers a survival advantage to endothelial cells. Cancer Res 68: 4640–4648. doi: 10.1158/0008-5472.CAN-07-5988 18559509
45. Kanneganti TD, (2010) Central roles of NLRs and inflammasomes in viral infection. Nat Rev Immunol 10: 688–698. doi: 10.1038/nri2851 20847744
46. Gram AM, Frenkel J, Ressing ME, (2012) Inflammasomes and viruses: cellular defence versus viral offence. J Gen Virol 93: 2063–2075. doi: 10.1099/vir.0.042978-0 22739062
47. Kerur N, Veettil MV, Sharma-Walia N, Bottero V, Sadagopan S, et al. (2011) IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe 9: 363–375. doi: 10.1016/j.chom.2011.04.008 21575908
48. Gregory SM, Damania B, (2011) Inhibition of the inflammasome response by a viral protein that interacts with NLRs. Commun Integr Biol 4: 416–418. doi: 10.4161/cib.4.4.15252 21966559
49. Ballestas ME, Kaye KM, (2011) The latency-associated nuclear antigen, a multifunctional protein central to Kaposi's sarcoma-associated herpesvirus latency. Future Microbiol 6: 1399–1413. doi: 10.2217/fmb.11.137 22122438
50. Cai Q, Lan K, Verma SC, Si H, Lin D, et al. (2006) Kaposi's sarcoma-associated herpesvirus latent protein LANA interacts with HIF-1 alpha to upregulate RTA expression during hypoxia: Latency control under low oxygen conditions. J Virol 80: 7965–7975. 16873253
51. Prasad A, Lu M, Lukac DM, Zeichner SL, (2012) An alternative Kaposi's sarcoma-associated herpesvirus replication program triggered by host cell apoptosis. J Virol 86: 4404–4419. doi: 10.1128/JVI.06617-11 22345480
52. Arvanitakis L, Mesri EA, Nador RG, Said JW, Asch AS, et al. (1996) Establishment and characterization of a primary effusion (body cavity- based) lymphoma cell line (BC-3) harboring kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) in the absence of Epstein-Barr virus. Blood 88: 2648–2654. 8839859