Human herpesvirus 8 viral interleukin-6 signaling through gp130 promotes virus replication in primary effusion lymphoma and endothelial cells

Journal of Virology

Volumn 88, Issue 20, 2014, Pages 12167-12172

  Cousins, Emily ^a   Gao, Yang ^a   Sandford, Gordon ^a   Nicholas, John ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 130; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; STAT PROTEIN; STAT1 PROTEIN; STAT3 PROTEIN; PRIMER DNA;

APOPTOSIS; ARTICLE; CELL COUNT; CELL CULTURE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; NONHUMAN; PRIMARY EFFUSION LYMPHOMA; PROTEIN DEPLETION; SEQUENCE HOMOLOGY; VIRUS REPLICATION; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIROLOGY;

BASE SEQUENCE; CYTOKINE RECEPTOR GP130; DNA PRIMERS; ENDOTHELIAL CELLS; HERPESVIRUS 8, HUMAN; HUMANS; INTERLEUKIN-6; LYMPHOMA, PRIMARY EFFUSION; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

EID: 84907426932     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01751-14     Document Type: Article

References (38)

1. 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. http://dx.doi.org/10.1016/S1359-6101(97)00037-3.
2. Schulz TF. 2006. The pleiotropic effects of Kaposi's sarcoma herpesvirus. J. Pathol. 208:187-198. http://dx.doi.org/10.1002/path.1904.
3. Uldrick TS, Polizzotto MN, Yarchoan R. 2012. Recent advances in Kaposi sarcoma herpesvirus-associated multicentric Castleman disease. Curr. Opin. Oncol. 24:495-505. http://dx.doi.org/10.1097/CCO.0b013e328355e0f3.
4. Nicholas J. 2007. Human herpesvirus 8-encoded proteins with potential roles in virus-associated neoplasia. Front. Biosci. 12:265-281. http://dx.doi.org/10.2741/2063.
5. Sakakibara S, Tosato G. 2011. Viral interleukin-6: role in Kaposi's sarcoma-associated herpesvirus: associated malignancies. J. Interferon Cytokine Res. 31:791-801. http://dx.doi.org/10.1089/jir.2011.0043.
6. 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.
7. Cousins E, Nicholas J. 2013. Role of human herpesvirus 8 interleukin-6-activated gp130 signal transducer in primary effusion lymphoma cell growth and viability. J. Virol. 87:10816-10827. http://dx.doi.org/10.1128 /JVI.02047-13.
8. Chen D, Sandford G, Nicholas J. 2009. Intracellular signaling mechanisms and activities of human herpesvirus 8 interleukin-6. J. Virol. 83: 722-733. http://dx.doi.org/10.1128/JVI.01517-08.
9. Aoki Y, Jaffe ES, Chang Y, Jones K, Teruya-Feldstein J, Moore PS, Tosato G. 1999. Angiogenesis and hematopoiesis induced by Kaposi's sarcoma-associated herpesvirus-encoded interleukin-6. Blood 93:4034-4043.
10. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. 2003. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 374:1-20. http://dx.doi.org /10.1042/BJ20030407.
11. Molden J, Chang Y, You Y, Moore PS, Goldsmith MA. 1997. A Kaposi's sarcoma-associated herpesvirus-encoded cytokine homolog (vIL-6) activates signaling through the shared gp130 receptor subunit. J. Biol. Chem. 272:19625-19631. http://dx.doi.org/10.1074/jbc.272.31.19625.
12. Chen D, Nicholas J. 2006. Structural requirements for gp80 independence of human herpesvirus 8 interleukin-6 (vIL-6) and evidence for gp80 stabilization of gp130 signaling complexes induced by vIL-6. J. Virol. 80: 9811-9821. http://dx.doi.org/10.1128/JVI.00872-06.
13. Adam N, Rabe B, Suthaus J, Grotzinger J, Rose-John S, Scheller J. 2009. Unraveling viral interleukin-6 binding to gp130 and activation of STATsignaling pathways independently of the interleukin-6 receptor. J. Virol. 83:5117-5126. http://dx.doi.org/10.1128/JVI.01601-08.
14. Chow D, He X, Snow AL, Rose-John S, Garcia KC. 2001. Structure of an extracellular gp130 cytokine receptor signaling complex. Science 291: 2150-2155. http://dx.doi.org/10.1126/science.1058308.
15. Boulanger MJ, Chow DC, Brevnova E, Martick M, Sandford G, Nicholas J, Garcia KC. 2004. Molecular mechanisms for viral mimicry of a human cytokine: activation of gp130 by HHV-8 interleukin-6. J. Mol. Biol. 335:641-654. http://dx.doi.org/10.1016/j.jmb.2003.10.070.
16. Meads MB, Medveczky PG. 2004. Kaposi's sarcoma-associated herpesvirus-encoded viral interleukin-6 is secreted and modified differently than human interleukin-6: evidence for a unique autocrine signaling mechanism. J. Biol. Chem. 279:51793-51803. http://dx.doi.org/10.1074/jbc.M407382200.
17. Chandriani S, Ganem D. 2010. Array-based transcript profiling and limiting-dilution reverse transcription-PCR analysis identify additional latent genes in Kaposi's sarcoma-associated herpesvirus. J. Virol. 84:5565-5573. http://dx.doi.org/10.1128/JVI.02723-09.
18. Chen D, Cousins E, Sandford G, Nicholas J. 2012. Human herpesvirus 8 viral interleukin-6 interacts with splice variant 2 of vitamin K epoxide reductase complex subunit 1. J. Virol. 86:1577-1588. http://dx.doi.org/10.1128/JVI.05782-11.
19. Chen D, Gao Y, Nicholas J. 2014. Human herpesvirus 8 interleukin-6 contributes to primary effusion lymphoma cell viability via suppression of proapoptotic cathepsin D, a cointeraction partner of vitamin K epoxide reductase complex subunit 1 variant 2. J. Virol. 88:1025-1038. http://dx.doi.org/10.1128/JVI.02830-13.
20. Yamanaka Y, Nakajima K, Fukada T, Hibi M, Hirano T. 1996. Differentiation and growth arrest signals are generated through the cytoplasmic region of gp130 that is essential for Stat3 activation. EMBO J. 15:1557-1565.
21. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F, Graeve L. 1998. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 334:297-314.
22. Schiemann WP, Bartoe JL, Nathanson NM. 1997. Box 3-independent signaling mechanisms are involved in leukemia inhibitory factor receptor alpha-and gp130-mediated stimulation of mitogen-activated protein kinase. Evidence for participation of multiple signaling pathways which converge at Ras. J. Biol. Chem. 272:16631-16636.
23. Schaper F, Gendo C, Eck M, Schmitz J, Grimm C, Anhuf D, Kerr IM, Heinrich PC. 1998. Activation of the protein tyrosine phosphatase SHP2 via the interleukin-6 signal transducing receptor protein gp130 requires tyrosine kinase Jak1 and limits acute-phase protein expression. Biochem. J. 335:557-565.
24. Aoki Y, Feldman GM, Tosato G. 2003. Inhibition of STAT3 signaling induces apoptosis and decreases survivin expression in primary effusion lymphoma. Blood 101:1535-1542. http://dx.doi.org/10.1182/blood-2002-07-2130.
25. Nakamura H, Lu M, Gwack Y, Souvlis J, Zeichner SL, Jung JU. 2003. Global changes in Kaposi's sarcoma-associated virus gene expression patterns following expression of a tetracycline-inducible Rta transactivator. J. Virol. 77:4205-4220. http://dx.doi.org/10.1128/JVI.77.7.4205-4220.2003.
26. Cannon JS, Ciufo D, Hawkins AL, Griffin CA, Borowitz MJ, Hayward GS, Ambinder RF. 2000. A new primary effusion lymphoma-derived cell line yields a highly infectious Kaposi's sarcoma herpesvirus-containing supernatant. J. Virol. 74:10187-10193. http://dx.doi.org/10.1128/JVI.74.21.10187-10193.2000.
27. Choi YB, Sandford G, Nicholas J. 2012. Human herpesvirus 8 interferon regulatory factor-mediated BH3-only protein inhibition via Bid BH3-B mimicry. PLoS Pathog. 8:e1002748. http://dx.doi.org/10.1371/journal.ppat.1002748.
28. 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.
29. 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 sarcomaassociated herpesvirus early during infection of primary endothelial and fibroblast cells and subsequent decline of lytic gene expression. J. Virol. 78: 3601-3620. http://dx.doi.org/10.1128/JVI.78.7.3601-3620.2004.
30. Toth Z, Brulois K, Lee HR, Izumiya Y, Tepper C, Kung HJ, Jung JU. 2013. Biphasic euchromatin-to-heterochromatin transition on the KSHV genome following de novo infection. PLoS Pathog. 9:e1003813. http://dx.doi.org/10.1371/journal.ppat.1003813.
31. Wan X, Wang H, Nicholas J. 1999. Human herpesvirus 8 interleukin-6 (vIL-6) signals through gp130 but has structural and receptor-binding properties distinct from those of human IL-6. J. Virol. 73:8268-8278.
32. Chen L, Lagunoff M. 2007. The KSHV viral interleukin-6 is not essential for latency or lytic replication in BJAB cells. Virology 359:425-435. http: //dx.doi.org/10.1016/j.virol.2006.09.044.
33. Najjar I, Fagard R. 2010. STAT1 and pathogens, not a friendly relationship. Biochimie 92:425-444. http://dx.doi.org/10.1016/j.biochi.2010.02.009.
34. Sen N, Che X, Rajamani J, Zerboni L, Sung P, Ptacek J, Arvin AM. 2012. Signal transducer and activator of transcription 3 (STAT3) and survivin induction by varicella-zoster virus promote replication and skin pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 109:600-605. http://dx.doi.org/10.1073/pnas.1114232109.
35. McCartney EM, Helbig KJ, Narayana SK, Eyre NS, Aloia AL, Beard MR. 2013. Signal transducer and activator of transcription 3 is a proviral host factor for hepatitis C virus. Hepatology 58:1558-1568. http://dx.doi.org /10.1002/hep.26496.
36. Reitsma JM, Sato H, Nevels M, Terhune SS, Paulus C. 2013. Human cytomegalovirus IE1 protein disrupts interleukin-6 signaling by sequestering STAT3 in the nucleus. J. Virol. 87:10763-10776. http://dx.doi.org /10.1128/JVI.01197-13.
37. Trilling M, Le VT, Rashidi-Alavijeh J, Katschinski B, Scheller J, Rose-John S, Androsiac GE, Jonjic S, Poli V, Pfeffer K, Hengel H. 2014. “Activated“ STAT proteins: a paradoxical consequence of inhibited JAKSTAT signaling in cytomegalovirus-infected cells. J. Immunol. 192:447-458. http://dx.doi.org/10.4049/jimmunol.1203516.
38. Zhou BY, Ye Z, Chen G, Gao ZP, Zhang YA, Cheng L. 2007. Inducible and reversible transgene expression in human stem cells after efficient and stable gene transfer. Stem Cells 25:779-789.