A unique herpesviral transcriptional program in KSHV-infected lymphatic endothelial cells leads to mTORC1 activation and rapamycin sensitivity

Cell Host and Microbe

Volumn 13, Issue 4, 2013, Pages 429-440

  Chang, Henry H ^a,b   Ganem, Don ^a,b  

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; RAPAMYCIN;

APOPTOSIS; ARTICLE; GENE CONTROL; GENE EXPRESSION; HERPES VIRUS; LYMPH VESSEL ENDOTHELIUM; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; VIRUS LATENCY; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

HUMAN HERPESVIRUS 8;

EID: 84876367196     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.03.009     Document Type: Article

References (57)

1. L. Arvanitakis, E. Geras-Raaka, A. Varma, M.C. Gershengorn, and E. Cesarman Human herpesvirus KSHV encodes a constitutively active G-protein-coupled receptor linked to cell proliferation Nature 385 1997 347 350
2. K. Austgen, S.A. Oakes, and D. Ganem Multiple defects, including premature apoptosis, prevent Kaposi's sarcoma-associated herpesvirus replication in murine cells J. Virol. 86 2012 1877 1882
3. C. Bais, B. Santomasso, O. Coso, L. Arvanitakis, E.G. Raaka, J.S. Gutkind, A.S. Asch, E. Cesarman, M.C. Gershengorn, and E.A. Mesri G-protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator Nature 391 1998 86 89
4. J.T. Bechtel, Y. Liang, J. Hvidding, and D. Ganem Host range of Kaposi's sarcoma-associated herpesvirus in cultured cells J. Virol. 77 2003 6474 6481
5. V. Beral, T.A. Peterman, R.L. Berkelman, and H.W. Jaffe Kaposi's sarcoma among persons with AIDS: a sexually transmitted infection? Lancet 335 1990 123 128
6. C. Boshoff, T.F. Schulz, M.M. Kennedy, A.K. Graham, C. Fisher, A. Thomas, J.O. McGee, R.A. Weiss, and J.J. O'Leary Kaposi's sarcoma-associated herpesvirus infects endothelial and spindle cells Nat. Med. 1 1995 1274 1278
7. J.J. Brooks Kaposi's sarcoma: a reversible hyperplasia Lancet 2 1986 1309 1311
8. K.F. Brulois, H. Chang, A.S. Lee, A. Ensser, L.Y. Wong, Z. Toth, S.H. Lee, H.R. Lee, J. Myoung, and D. Ganem Construction and manipulation of a new Kaposi's sarcoma-associated herpesvirus bacterial artificial chromosome clone J. Virol. 86 2012 9708 9720
9. M. Cannon, N.J. Philpott, and E. Cesarman The Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor has broad signaling effects in primary effusion lymphoma cells J. Virol. 77 2003 57 67
10. A. Carrière, M. Cargnello, L.A. Julien, H. Gao, E. Bonneil, P. Thibault, and P.P. Roux Oncogenic MAPK signaling stimulates mTORC1 activity by promoting RSK-mediated raptor phosphorylation Curr. Biol. 18 2008 1269 1277
11. E. Cesarman, E.A. Mesri, and M.C. Gershengorn Viral G protein-coupled receptor and Kaposi's sarcoma: a model of paracrine neoplasia? J. Exp. Med. 191 2000 417 422
12. S. Chandriani, and D. Ganem Array-based transcript profiling and limiting-dilution reverse transcription-PCR analysis identify additional latent genes in Kaposi's sarcoma-associated herpesvirus J. Virol. 84 2010 5565 5573
13. S. Chandriani, Y. Xu, and D. Ganem The lytic transcriptome of Kaposi's sarcoma-associated herpesvirus reveals extensive transcription of noncoding regions, including regions antisense to important genes J. Virol. 84 2010 7934 7942
14. F. Cheng, P. Pekkonen, S. Laurinavicius, N. Sugiyama, S. Henderson, T. Günther, V. Rantanen, E. Kaivanto, M. Aavikko, and G. Sarek KSHV-initiated notch activation leads to membrane-type-1 matrix metalloproteinase-dependent lymphatic endothelial-to-mesenchymal transition Cell Host Microbe 10 2011 577 590
15. A.Y. Choo, S.O. Yoon, S.G. Kim, P.P. Roux, and J. Blenis Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation Proc. Natl. Acad. Sci. USA 105 2008 17414 17419
16. J. Chung, C.J. Kuo, G.R. Crabtree, and J. Blenis Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kd S6 protein kinases Cell 69 1992 1227 1236
17. B.J. Dezube Clinical presentation and natural history of AIDS - related Kaposi's sarcoma Hematol. Oncol. Clin. North Am. 10 1996 1023 1029
18. D.P. Dittmer Transcription profile of Kaposi's sarcoma-associated herpesvirus in primary Kaposi's sarcoma lesions as determined by real-time PCR arrays Cancer Res. 63 2003 2010 2015
19. D.P. Dittmer Restricted Kaposi's sarcoma (KS) herpesvirus transcription in KS lesions from patients on successful antiretroviral therapy MBio 2 2011 e00138-e11
20. B. Ensoli, C. Sgadari, G. Barillari, M.C. Sirianni, M. Stürzl, and P. Monini Biology of Kaposi's sarcoma Eur. J. Cancer 37 2001 1251 1269
21. D. Ganem KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine J. Clin. Invest. 120 2010 939 949
22. A. Garami, F.J. Zwartkruis, T. Nobukuni, M. Joaquin, M. Roccio, H. Stocker, S.C. Kozma, E. Hafen, J.L. Bos, and G. Thomas Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2 Mol. Cell 11 2003 1457 1466
23. B. Glaunsinger, and D. Ganem Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover Mol. Cell 13 2004 713 723
24. C. Grossmann, S. Podgrabinska, M. Skobe, and D. Ganem 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 2006 7179 7185
25. A. Grundhoff, and D. Ganem Inefficient establishment of KSHV latency suggests an additional role for continued lytic replication in Kaposi sarcoma pathogenesis J. Clin. Invest. 113 2004 124 136
26. C. Guilluy, Z. Zhang, P.M. Bhende, L. Sharek, L. Wang, K. Burridge, and B. Damania Latent KSHV infection increases the vascular permeability of human endothelial cells Blood 118 2011 5344 5354
27. Y.K. Hong, K. Foreman, J.W. Shin, S. Hirakawa, C.L. Curry, D.R. Sage, T. Libermann, B.J. Dezube, J.D. Fingeroth, and M. Detmar Lymphatic reprogramming of blood vascular endothelium by Kaposi sarcoma-associated herpesvirus Nat. Genet. 36 2004 683 685
28. J. Huang, and B.D. Manning A complex interplay between Akt, TSC2 and the two mTOR complexes Biochem. Soc. Trans. 37 2009 217 222
29. K. Inoki, Y. Li, T. Zhu, J. Wu, and K.L. Guan TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling Nat. Cell Biol. 4 2002 648 657
30. E. Kuang, Q. Tang, G.G. Maul, and F. Zhu Activation of p90 ribosomal S6 kinase by ORF45 of Kaposi's sarcoma-associated herpesvirus and its role in viral lytic replication J. Virol. 82 2008 1838 1850
31. E. Kuang, F. Wu, and F. Zhu Mechanism of sustained activation of ribosomal S6 kinase (RSK) and ERK by kaposi sarcoma-associated herpesvirus ORF45: multiprotein complexes retain active phosphorylated ERK AND RSK and protect them from dephosphorylation J. Biol. Chem. 284 2009 13958 13968
32. E. Kuang, B. Fu, Q. Liang, J. Myoung, and F. Zhu Phosphorylation of eukaryotic translation initiation factor 4B (EIF4B) by open reading frame 45/p90 ribosomal S6 kinase (ORF45/RSK) signaling axis facilitates protein translation during Kaposi sarcoma-associated herpesvirus (KSHV) lytic replication J. Biol. Chem. 286 2011 41171 41182
33. L. Ma, Z. Chen, H. Erdjument-Bromage, P. Tempst, and P.P. Pandolfi Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis Cell 121 2005 179 193
34. D.F. Martin, B.D. Kuppermann, R.A. Wolitz, A.G. Palestine, H. Li, C.A. Robinson Roche Ganciclovir Study Group Oral ganciclovir for patients with cytomegalovirus retinitis treated with a ganciclovir implant N. Engl. J. Med. 340 1999 1063 1070
35. E.A. Mesri, E. Cesarman, and C. Boshoff Kaposi's sarcoma and its associated herpesvirus Nat. Rev. Cancer 10 2010 707 719
36. P.S. Moore, and Y. Chang Detection of herpesvirus-like DNA sequences in Kaposi's sarcoma in patients with and without HIV infection N. Engl. J. Med. 332 1995 1181 1185
37. A.D. Mutlu, L.E. Cavallin, L. Vincent, C. Chiozzini, P. Eroles, E.M. Duran, Z. Asgari, A.T. Hooper, K.M. La Perle, and C. Hilsher In vivo-restricted and reversible malignancy induced by human herpesvirus-8 KSHV: a cell and animal model of virally induced Kaposi's sarcoma Cancer Cell 11 2007 245 258
38. J. Myoung, and D. Ganem 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 2011 12 21
39. J. Myoung, and D. Ganem Infection of primary human tonsillar lymphoid cells by KSHV reveals frequent but abortive infection of T cells Virology 413 2011 1 11
40. C.J. Potter, L.G. Pedraza, and T. Xu Akt regulates growth by directly phosphorylating Tsc2 Nat. Cell Biol. 4 2002 658 665
41. P. Pyakurel, F. Pak, A.R. Mwakigonja, E. Kaaya, T. Heiden, and P. Biberfeld Lymphatic and vascular origin of Kaposi's sarcoma spindle cells during tumor development Int. J. Cancer 119 2006 1262 1267
42. R. Renne, W. Zhong, B. Herndier, M. McGrath, N. Abbey, D. Kedes, and D. Ganem Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture Nat. Med. 2 1996 342 346
43. P.P. Roux, B.A. Ballif, R. Anjum, S.P. Gygi, and J. Blenis Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase Proc. Natl. Acad. Sci. USA 101 2004 13489 13494
44. S.H. Sin, D. Roy, L. Wang, M.R. Staudt, F.D. Fakhari, D.D. Patel, D. Henry, W.J. Harrington Jr., B.A. Damania, and D.P. Dittmer Rapamycin is efficacious against primary effusion lymphoma (PEL) cell lines in vivo by inhibiting autocrine signaling Blood 109 2007 2165 2173
45. A. Sodhi, S. Montaner, V. Patel, J.J. Gómez-Román, Y. Li, E.A. Sausville, E.T. Sawai, and J.S. Gutkind Akt plays a central role in sarcomagenesis induced by Kaposi's sarcoma herpesvirus-encoded G protein-coupled receptor Proc. Natl. Acad. Sci. USA 101 2004 4821 4826
46. S.H. Speck, and D. Ganem Viral latency and its regulation: lessons from the gamma-herpesviruses Cell Host Microbe 8 2010 100 115
47. G. Stallone, A. Schena, B. Infante, S. Di Paolo, A. Loverre, G. Maggio, E. Ranieri, L. Gesualdo, F.P. Schena, and G. Grandaliano Sirolimus for Kaposi's sarcoma in renal-transplant recipients N. Engl. J. Med. 352 2005 1317 1323
48. R. Sun, S.F. Lin, L. Gradoville, Y. Yuan, F. Zhu, and G. Miller A viral gene that activates lytic cycle expression of Kaposi's sarcoma-associated herpesvirus Proc. Natl. Acad. Sci. USA 95 1998 10866 10871
49. C.C. Tomlinson, and B. Damania The K1 protein of Kaposi's sarcoma-associated herpesvirus activates the Akt signaling pathway J. Virol. 78 2004 1918 1927
50. J. Vieira, and P.M. O'Hearn Use of the red fluorescent protein as a marker of Kaposi's sarcoma-associated herpesvirus lytic gene expression Virology 325 2004 225 240
51. L. Wang, and B. Damania Kaposi's sarcoma-associated herpesvirus confers a survival advantage to endothelial cells Cancer Res. 68 2008 4640 4648
52. H.W. Wang, M.W. Trotter, D. Lagos, D. Bourboulia, S. Henderson, T. Mäkinen, S. Elliman, A.M. Flanagan, K. Alitalo, and C. Boshoff Kaposi sarcoma herpesvirus-induced cellular reprogramming contributes to the lymphatic endothelial gene expression in Kaposi sarcoma Nat. Genet. 36 2004 687 693
53. J.D. Weber, and D.H. Gutmann Deconvoluting mTOR biology Cell Cycle 11 2012 236 248
54. W. Weninger, T.A. Partanen, S. Breiteneder-Geleff, C. Mayer, H. Kowalski, M. Mildner, J. Pammer, M. Stürzl, D. Kerjaschki, K. Alitalo, and E. Tschachler Expression of vascular endothelial growth factor receptor-3 and podoplanin suggests a lymphatic endothelial cell origin of Kaposi's sarcoma tumor cells Lab. Invest. 79 1999 243 251
55. Y. Yu, J.B. Black, C.S. Goldsmith, P.J. Browning, K. Bhalla, and M.K. Offermann Induction of human herpesvirus-8 DNA replication and transcription by butyrate and TPA in BCBL-1 cells J. Gen. Virol. 80 1999 83 90
56. F.X. Zhu, T. Cusano, and Y. Yuan Identification of the immediate-early transcripts of Kaposi's sarcoma-associated herpesvirus J. Virol. 73 1999 5556 5567
57. F.X. Zhu, S.M. King, E.J. Smith, D.E. Levy, and Y. Yuan A Kaposi's sarcoma-associated herpesviral protein inhibits virus-mediated induction of type I interferon by blocking IRF-7 phosphorylation and nuclear accumulation Proc. Natl. Acad. Sci. USA 99 2002 5573 5578