Kaposi's sarcoma-associated herpesvirus latency in endothelial and B cells activates Gamma interferon-inducible protein 16-Mediated inflammasomes

Journal of Virology

Volumn 87, Issue 8, 2013, Pages 4417-4431

  Singh, Vivek Vikram ^a   Kerur, Nagaraj ^a,b   Bottero, Virginie ^a   Dutta, Sujoy ^a   Chakraborty, Sayan ^a,c   Ansari, Mairaj Ahmed ^a   Paudel, Nitika ^a   Chikoti, Leela ^a   Chandran, Bala ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CRYOPYRIN; GAMMA INTERFERON INDUCIBLE PROTEIN 16; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 8; MESSENGER RNA; PRO INTERLEUKIN 18; PRO INTERLEUKIN 1BETA; PROTEIN AIM2; PROTEIN ASC; UNCLASSIFIED DRUG;

ARTICLE; B CELL LYMPHOMA; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; EXOSOME; FLIP GENE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; HUMAN TISSUE; INNATE IMMUNITY; LYMPHOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TELOMERASE IMMORTALIZED HUMAN UMBILICAL CELL; UMBILICAL VEIN ENDOTHELIAL CELL; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS GENOME; VIRUS LATENCY;

B-LYMPHOCYTES; BLOTTING, WESTERN; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMASOMES; NUCLEAR PROTEINS; PHOSPHOPROTEINS; VIRUS LATENCY;

HUMAN HERPESVIRUS 8;

EID: 84875800370     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03282-12     Document Type: Article

References (47)

1. Ganem D. 2006. KSHV infection and the pathogenesis of Kaposi's sarcoma. Annu. Rev. Pathol. 1:273-296.
2. Ganem D. 2007. Kaposi's sarcoma-associated herpesvirus, p 2847-2888. In KnipeDMet al. (ed), Fields virology, 5th ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
3. Chandran B. 2010. Early events in Kaposi's sarcoma-associated herpesvirus infection of target cells. J. Virol. 84:2188-2199.
4. Ensoli B, Sturzl M. 1998. Kaposi's sarcoma: a result of the interplay among inflammatory cytokines, angiogenic factors and viral agents. Cytokine Growth Factor Rev. 9:63-83.
5. Gasperini P, Sakakibara S, Tosato G. 2008. Contribution of viral and cellular cytokines to Kaposi's sarcoma-associated herpesvirus pathogenesis. J. Leukoc. Biol. 84:994-1000.
6. Sharma-Walia N, Paul AG, Bottero V, Sadagopan S, Veettil MV, Kerur N, Chandran B. 2010. Kaposi's sarcoma associated herpes virus (KSHV) induced COX-2: a key factor in latency, inflammation, angiogenesis, cell survival and invasion. PLoS Pathog. 6:e1000777. doi:10.1371/journal.ppat .1000777.
7. Paludan SR, Bowie AG, Horan KA, Fitzgerald KA. 2011. Recognition of herpesviruses by the innate immune system. Nat. Rev. Immunol. 11:143-154.
8. Gregory SM, West JA, Dillon PJ, Hilscher C, Dittmer DP, Damania B. 2009. Toll-like receptor signaling controls reactivation of KSHV from latency. Proc. Natl. Acad. Sci. U. S. A. 106:11725-11730.
9. Gregory SM, Davis BK, West JA, Taxman DJ, Matsuzawa S, Reed JC, Ting JP, Damania B. 2011. Discovery of a viral NLR homolog that inhibits the inflammasome. Science 331:330-334.
10. Kerur N, Veettil MV, Sharma-Walia N, Bottero V, Sadagopan S, Otageri P, Chandran B. 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.
11. Veeranki S, Choubey D. 2012. Interferon-inducible p200-family protein IFI16, an innate immune sensor for cytosolic and nuclear double-stranded DNA: regulation of subcellular localization. Mol. Immunol. 49:567-571.
12. An FQ, Folarin HM, Compitello N, Roth J, Gerson SL, McCrae KR, Fakhari FD, Dittmer DP, Renne R. 2006. Long-term-infected telomerase- immortalized endothelial cells: a model for Kaposi's sarcomaassociated herpesvirus latency in vitro and in vivo. J. Virol. 80:4833-4846.
13. Nun TK, Kroll DJ, Oberlies NH, Soejarto DD, Case RJ, Piskaut P, Matainaho T, Hilscher C, Wang L, Dittmer DP, Gao SJ, Damania B. 2007. Development of a fluorescence-based assay to screen antiviral drugs against Kaposi's sarcoma associated herpesvirus. Mol. Cancer Ther. 6:2360-2370.
14. Paul AG, Sharma-Walia N, Chandran B. 2011. Targeting KSHV/HHV-8 latency with COX-2 selective inhibitor nimesulide: a potential chemotherapeutic modality for primary effusion lymphoma. PLoS One 6:e24379. doi:10.1371/journal.pone.0024379.
15. Sharma-Walia N, Krishnan HH, Naranatt PP, Zeng L, Smith MS, Chandran B. 2005. ERK1/2 and MEK1/2 induced by Kaposi's sarcomaassociated herpesvirus (human herpesvirus 8) early during infection oftarget cells are essential for expression of viral genes and for establishment of infection. J. Virol. 79:10308-10329.
16. Naranatt PP, Krishnan HH, Svojanovsky SR, Bloomer C, Mathur S, Chandran B. 2004. Host gene induction and transcriptional reprogramming in Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8)- infected endothelial, fibroblast, and B cells: insights into modulation events early during infection. Cancer Res. 64:72-84.
17. Krishnan HH, Naranatt PP, Smith MS, Zeng L, Bloomer C, Chandran B. 2004. Concurrent expression of latent and a limited number of lytic genes with immune modulation and antiapoptotic function by Kaposi's sarcoma-associated herpesvirus early during infection of primary endothelial and fibroblast cells and subsequent decline of lytic gene expression. J. Virol. 78:3601-3620.
18. Sharma-Walia N, Raghu H, Sadagopan S, Sivakumar R, Veettil MV, Naranatt PP, Smith MM, Chandran B. 2006. Cyclooxygenase 2 induced by Kaposi's sarcoma-associated herpesvirus early during in vitro infection of target cells plays a role in the maintenance of latent viral gene expression. J. Virol. 80:6534-6552.
19. Vart RJ, Nikitenko LL, Lagos D, Trotter MW, Cannon M, Bourboulia D, Gratrix F, Takeuchi Y, Boshoff C. 2007. Kaposi's sarcoma-associated herpesvirus-encoded interleukin-6 and G-protein-coupled receptor regulate angiopoietin-2 expression in lymphatic endothelial cells. Cancer Res. 67:4042-4051.
20. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L. 1998. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:8463-8471.
21. Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM. 1998. Development of a self-inactivating lentivirus vector. J. Virol. 72:8150-8157.
22. Sadagopan S, Sharma-Walia N, Veettil MV, Raghu H, Sivakumar R, Bottero V, Chandran B. 2007. Kaposi's sarcoma-associated herpesvirus induces sustained NF-kappaB activation during de novo infection of primary human dermal microvascular endothelial cells that is essential for viral gene expression. J. Virol. 81:3949-3968.
23. Alkharsah KR, Singh VV, Bosco R, Santag S, Grundhoff A, Konrad A, Sturzl M, Wirth D, Dittrich-Breiholz O, Kracht M, Schulz TF. 2011. Deletion of Kaposi's sarcoma-associated herpesvirus FLICE inhibitory protein, vFLIP, from the viral genome compromises the activation of STAT1-responsive cellular genes and spindle cell formation in endothelial cells. J. Virol. 85:10375-10388.
24. Thery C, Amigorena S, Raposo G, Clayton A. 2006. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Chapter 3:Unit 3.22.
25. Stutz A, Golenbock DT, Latz E. 2009. Inflammasomes: too big to miss. J. Clin. Invest. 119:3502-3511.
26. Schroder K, Tschopp J. 2010. The inflammasomes. Cell 140:821-832.
27. Grossmann C, Podgrabinska S, Skobe M, Ganem D. 2006. Activation of NF-kappaB by the latent vFLIP gene of Kaposi's sarcoma-associated herpesvirus is required for the spindle shape of virus-infected endothelial cells and contributes to their proinflammatory phenotype. J. Virol. 80:7179-7185.
28. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, Caffrey DR, Latz E, Fitzgerald KA. 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514-518.
29. Bryan NB, Dorfleutner A, Rojanasakul Y, Stehlik C. 2009. Activation of inflammasomes requires intracellular redistribution of the apoptotic speck-like protein containing a caspase recruitment domain. J. Immunol. 182:3173-3182.
30. Thery C, Ostrowski M, Segura E. 2009. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9:581-593.
31. Zhu M, Li Y, Shi J, Feng W, Nie G, Zhao Y. 2012. Exosomes as extrapulmonary signaling conveyors for nanoparticle-induced systemic immune activation. Small 8:404-412.
32. Simons M, Raposo G. 2009. Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21:575-581.
33. Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10:513-525.
34. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, Seabra MC, Darchen F, Amigorena S, Moita LF, Thery C. 2010. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 12:19-30.
35. Jones KD, Aoki Y, Chang Y, Moore PS, Yarchoan R, Tosato G. 1999. Involvement of interleukin-10 (IL-10) and viral IL-6 in the spontaneous growth of Kaposi's sarcoma herpesvirus-associated infected primary effusion lymphoma cells. Blood 94:2871-2879.
36. Arguello M, Paz S, Hernandez E, Corriveau-Bourque C, Fawaz LM, Hiscott J, Lin R. 2006. Leukotriene A4 hydrolase expression in PEL cells is regulated at the transcriptional level and leads to increased leukotriene B4 production. J. Immunol. 176:7051-7061.
37. van de Berg PJ, Heutinck KM, Raabe R, Minnee RC, Young SL, van Donselaar-van der Pant KA, Bemelman FJ, van Lier RA, ten Berge IJ. 2010. Human cytomegalovirus induces systemic immune activation characterized by a type 1 cytokine signature. J. Infect. Dis. 202:690-699.
38. Theil D, Derfuss T, Paripovic I, Herberger S, Meinl E, Schueler O, Strupp M, Arbusow V, Brandt T. 2003. Latent herpesvirus infection in human trigeminal ganglia causes chronic immune response. Am. J. Pathol. 163:2179-2184.
39. Ensoli B, Nakamura S, Salahuddin SZ, Biberfeld P, Larsson L, Beaver B, Wong-Staal F, Gallo RC. 1989. AIDS-Kaposi's sarcoma-derived cells express cytokines with autocrine and paracrine growth effects. Science 243:223-226.
40. Gariano GR, Dell'Oste V, Bronzini M, Gatti D, Luganini A, De Andrea M, Gribaudo G, Gariglio M, Landolfo S. 2012. The intracellular DNA sensor IFI16 gene acts as restriction factor for human cytomegalovirus replication. PLoS Pathog. 8:e1002498. doi:10.1371/journal.ppat.1002498.
41. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, Sirois CM, Jin T, Latz E, Xiao TS, Fitzgerald KA, Paludan SR, Bowie AG. 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11:997-1004.
42. Li T, Diner BA, Chen J, Cristea IM. 2012. Acetylation modulates cellular distribution and DNA sensing ability of interferon-inducible protein IFI16. Proc. Natl. Acad. Sci. U. S. A. 109:10558-10563.
43. Jin T, Perry A, Jiang J, Smith P, Curry JA, Unterholzner L, Jiang Z, Horvath G, Rathinam VA, Johnstone RW, Hornung V, Latz E, Bowie AG, Fitzgerald KA, Xiao TS. 2012. Structures of the HIN domain:DNA complexes reveal ligand binding and activation mechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 36:561-571.
44. Aglipay JA, Lee SW, Okada S, Fujiuchi N, Ohtsuka T, Kwak JC, Wang Y, Johnstone RW, Deng C, Qin J, Ouchi T. 2003. A member of the Pyrin family, IFI16, is a novel BRCA1-associated protein involved in the p53- mediated apoptosis pathway. Oncogene 22:8931-8938.
45. Robert T, Vanoli F, Chiolo I, Shubassi G, Bernstein KA, Rothstein R, Botrugno OA, Parazzoli D, Oldani A, Minucci S, Foiani M. 2011. HDACs link the DNA damage response, processing of double-strand breaks and autophagy. Nature 471:74-79.
46. Miller KM, Tjeertes JV, Coates J, Legube G, Polo SE, Britton S, Jackson SP. 2010. Human HDAC1 and HDAC2 function in the DNA-damage response to promoteDNAnonhomologous end-joining. Nat. Struct. Mol. Biol. 17:1144-1151.
47. Costa S, Borgogna C, Mondini M, De Andrea M, Meroni PL, Berti E, Gariglio M, Landolfo S. 2011. Redistribution of the nuclear protein IFI16 into the cytoplasm of ultraviolet B-exposed keratinocytes as a mechanism of autoantigen processing. Br. J. Dermatol. 164:282-290.