Human immunodeficiency virus type 1 induces lytic cycle replication of kaposi's-sarcoma-associated herpesvirus: Role of Ras/c-Raf/MEK1/2, PI3K/AKT, and NF-κB signaling pathways

Journal of Molecular Biology

Volumn 410, Issue 5, 2011, Pages 1035-1051

  Zhu, Xiaolei ^a,b   Zhou, Feng ^a   Qin, Di ^a   Zeng, Yi ^a,c   Lv, Zhigang ^a,d   Yao, Shuihong ^a,e   Lu, Chun ^a,b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b Key Laboratory for Laboratory Medicine of Jiangsu Province   (China)

^c YOUJIANG MEDICAL COLLEGE FOR NATIONALITIES   (China)

^d Jiangsu Province Official Hospital   (China)

^e QUZHOU UNIVERSITY   (China)

Author keywords

HIV 1; KSHV; replication; signaling pathway

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; RAS PROTEIN;

ANIMAL CELL; ARTICLE; CELL STRAIN 3T3; CELL STRAIN HEK293; GENE EXPRESSION; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIMARY EFFUSION LYMPHOMA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRION; VIRUS REACTIVATION; VIRUS REPLICATION;

HERPESVIRIDAE; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79960364077     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.03.055     Document Type: Article

References (49)

1. Chang Y.; Cesarman E.; Pessin M.S.; Lee F.; Culpepper J.; Knowles D.M.; and Moore P.S. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma Science 266 1994 1865 1869
2. Deng H.; Liang Y.; and Sun R. Regulation of KSHV lytic gene expression Curr. Top. Microbiol. Immunol. 312 2007 157 183 (Pubitemid 47400347)
3. Verma S.C.; Lan K.; and Robertson E. Structure and function of latency-associated nuclear antigen Curr. Top. Microbiol. Immunol. 312 2007 101 136 (Pubitemid 47400345)
4. Liu J.; Martin H.J.; Liao G.; and Hayward S.D. The Kaposi's sarcoma-associated herpesvirus LANA protein stabilizes and activates c-Myc J. Virol. 81 2007 10451 10459 (Pubitemid 47463318)
5. Kelley-Clarke B.; De Leon-Vazquez E.; Slain K.; Barbera A.J.; and Kaye K.M. Role of Kaposi's sarcoma-associated herpesvirus C-terminal LANA chromosome binding in episome persistence J. Virol. 83 2009 4326 4337
6. Qin D.; Zeng Y.; Qian C.; Huang Z.; Lv Z.; and Cheng L. Induction of lytic cycle replication of Kaposi's sarcoma-associated herpesvirus by herpes simplex virus type 1: involvement of IL-10 and IL-4 Cell. Microbiol. 10 2008 713 728 (Pubitemid 351194097)
7. Varthakavi V.; Browning P.J.; and Spearman P. Human immunodeficiency virus replication in a primary effusion lymphoma cell line stimulates lytic-phase replication of Kaposi's sarcoma-associated herpesvirus J. Virol. 73 1999 10329 10338
8. Merat R.; Amara A.; Lebbe C.; de The H.; Morel P.; and Saib A. HIV-1 infection of primary effusion lymphoma cell line triggers Kaposi's sarcoma-associated herpesvirus (KSHV) reactivation Int. J. Cancer 97 2002 791 795 (Pubitemid 34106334)
9. Vieira J.; O'Hearn P.; Kimball L.; Chandran B.; and Corey L. Activation of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) lytic replication by human cytomegalovirus J. Virol. 75 2001 1378 1386 (Pubitemid 32094696)
10. Morris T.L.; Arnold R.R.; and Webster-Cyriaque J. Signaling cascades triggered by bacterial metabolic end products during reactivation of Kaposi's sarcoma-associated herpesvirus J. Virol. 81 2007 6032 6042 (Pubitemid 46847039)
11. Lu C.; Zeng Y.; Huang Z.; Huang L.; Qian C.; Tang G.; and Qin D. Human herpesvirus 6 activates lytic cycle replication of Kaposi's sarcoma-associated herpesvirus Am. J. Pathol. 166 2005 173 183 (Pubitemid 40051670)
12. Zeng Y.; Zhang X.; Huang Z.; Cheng L.; Yao S.; and Qin D. Intracellular Tat of human immunodeficiency virus type 1 activates lytic cycle replication of Kaposi's sarcoma-associated herpesvirus: role of JAK/STAT signaling J. Virol. 81 2007 2401 2417
13. Chen X.; Cheng L.; Jia X.; Zeng Y.; Yao S.; and Lv Z. Human immunodeficiency virus type 1 Tat accelerates Kaposi sarcoma-associated herpesvirus Kaposin A-mediated tumorigenesis of transformed fibroblasts in vitro as well as in nude and immunocompetent mice Neoplasia 11 2009 1272 1284
14. Varthakavi V.; Smith R.M.; Deng H.; Sun R.; and Spearman P. Human immunodeficiency virus type-1 activates lytic cycle replication of Kaposi's sarcoma-associated herpesvirus through induction of KSHV Rta Virology 297 2002 270 280 (Pubitemid 34734899)
15. Deutsch E.; Cohen A.; Kazimirsky G.; Dovrat S.; Rubinfeld H.; Brodie C.; and Sarid R. Role of protein kinase C delta in reactivation of Kaposi's sarcoma-associated herpesvirus J. Virol. 78 2004 10187 10192 (Pubitemid 39187136)
16. Zoeteweij J.P.; Moses A.V.; Rinderknecht A.S.; Davis D.A.; Overwijk W.W.; and Yarchoan R. Targeted inhibition of calcineurin signaling blocks calcium-dependent reactivation of Kaposi sarcoma-associated herpesvirus Blood 97 2001 2374 2380 (Pubitemid 32291484)
17. Peng L.; Wu T.T.; Tchieu J.H.; Feng J.; Brown H.J.; and Li X. Inhibition of the phosphatidylinositol 3-kinase-Akt pathway enhances gamma-2 herpesvirus lytic replication and facilitates reactivation from latency J. Gen. Virol. 91 2010 463 469
18. He J.; Choe S.; Walker R.; Di Marzio P.; Morgan D.O.; and Landau N.R. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity J. Virol. 69 1995 6705 6711
19. Connor R.I.; Chen B.K.; Choe S.; and Landau N.R. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes Virology 206 1995 935 944
20. Blasig C.; Zietz C.; Haar B.; Neipel F.; Esser S.; and Brockmeyer N.H. Monocytes in Kaposi's sarcoma lesions are productively infected by human herpesvirus 8 J. Virol. 71 1997 7963 7968 (Pubitemid 27391749)
21. Monini P.; Colombini S.; Sturzl M.; Goletti D.; Cafaro A.; and Sgadari C. Reactivation and persistence of human herpesvirus-8 infection in B cells and monocytes by Th-1 cytokines increased in Kaposi's sarcoma Blood 93 1999 4044 4058 (Pubitemid 29279246)
22. Moir S.; Lapointe R.; Malaspina A.; Ostrowski M.; Cole C.E.; and Chun T.W. CD40-mediated induction of CD4 and CXCR4 on B lymphocytes correlates with restricted susceptibility to human immunodeficiency virus type 1 infection: potential role of B lymphocytes as a viral reservoir J. Virol. 73 1999 7972 7980 (Pubitemid 29441655)
23. Lu C.; Gordon G.M.; Chandran B.; Nickoloff B.J.; and Foreman K.E. Human herpesvirus 8 reactivation and human immunodeficiency virus type 1 gp120 Arch. Pathol. Lab. Med. 126 2002 941 946
24. Belec L.; Tevi-Benissan C.; Mohamed A.S.; Carbonel N.; Matta M.; and Gresenguet G. Enhanced detection of human herpesvirus-8 and cytomegalovirus in semen of HIV-seropositive asymptomatic heterosexual men living in Central Africa AIDS 12 1998 674 676 (Pubitemid 28162110)
25. Howard M.R.; Whitby D.; Bahadur G.; Suggett F.; Boshoff C.; and Tenant-Flowers M. Detection of human herpesvirus 8 DNA in semen from HIV-infected individuals but not healthy semen donors AIDS 11 1997 F15 F19
26. Melbye M.; Cook P.M.; Hjalgrim H.; Begtrup K.; Simpson G.R.; and Biggar R.J. Risk factors for Kaposi's-sarcoma-associated herpesvirus (KSHV/HHV-8) seropositivity in a cohort of homosexual men, 1981-1996 Int. J. Cancer 77 1998 543 548 (Pubitemid 28340901)
27. Lempiainen H.; and Halazonetis T.D. Emerging common themes in regulation of PIKKs and PI3Ks EMBO J. 28 2009 3067 3073
28. Engelman J.A. Targeting PI3K signalling in cancer: opportunities, challenges and limitations Nat. Rev.; Cancer 9 2009 550 562
29. Montaner S. Akt/TSC/mTOR activation by the KSHV G protein-coupled receptor: emerging insights into the molecular oncogenesis and treatment of Kaposi's sarcoma Cell Cycle 6 2007 438 443 (Pubitemid 46393447)
30. Morris V.A.; Punjabi A.S.; and Lagunoff M. Activation of Akt through gp130 receptor signaling is required for Kaposi's sarcoma-associated herpesvirus-induced lymphatic reprogramming of endothelial cells J. Virol. 82 2008 8771 8779
31. Cohen A.; Brodie C.; and Sarid R. An essential role of ERK signalling in TPA-induced reactivation of Kaposi's sarcoma-associated herpesvirus J. Gen. Virol. 87 2006 795 802
32. Ford P.W.; Bryan B.A.; Dyson O.F.; Weidner D.A.; Chintalgattu V.; and Akula S.M. Raf/MEK/ERK signalling triggers reactivation of Kaposi's sarcoma-associated herpesvirus latency J. Gen. Virol. 87 2006 1139 1144
33. Sharma-Walia N.; Krishnan H.H.; Naranatt P.P.; Zeng L.; Smith M.S.; and Chandran B. ERK1/2 and MEK1/2 induced by Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) early during infection of target cells are essential for expression of viral genes and for establishment of infection J. Virol. 79 2005 10308 10329 (Pubitemid 41098572)
34. Yu F.; Harada J.N.; Brown H.J.; Deng H.; Song M.J.; and Wu T.T. Systematic identification of cellular signals reactivating Kaposi sarcoma-associated herpesvirus PLoS. Pathog. 3 2007 e44
35. Xie J.; Ajibade A.O.; Ye F.; Kuhne K.; and Gao S.J. Reactivation of Kaposi's sarcoma-associated herpesvirus from latency requires MEK/ERK, JNK and p38 multiple mitogen-activated protein kinase pathways Virology 371 2008 139 154
36. Izumiya Y.; Izumiya C.; Hsia D.; Ellison T.J.; Luciw P.A.; and Kung H.J. NF-kappaB serves as a cellular sensor of Kaposi's sarcoma-associated herpesvirus latency and negatively regulates K-Rta by antagonizing the RBP-Jkappa coactivator J. Virol. 83 2009 4435 4446
37. Schwarz M.; and Murphy P.M. Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor constitutively activates NF-kappa B and induces proinflammatory cytokine and chemokine production via a C-terminal signaling determinant J. Immunol. 167 2001 505 513 (Pubitemid 32567818)
38. Sgarbanti M.; Arguello M.; tenOever B.R.; Battistini A.; Lin R.; and Hiscott J. A requirement for NF-kappaB induction in the production of replication-competent HHV-8 virions Oncogene 23 2004 5770 5780 (Pubitemid 39093022)
39. Konrad A.; Wies E.; Thurau M.; Marquardt G.; Naschberger E.; and Hentschel S. A systems biology approach to identify the combination effects of human herpesvirus 8 genes on NF-kappaB activation J. Virol. 83 2009 2563 2574
40. Brown H.J.; Song M.J.; Deng H.; Wu T.T.; Cheng G.; and Sun R. NF-kappaB inhibits gammaherpesvirus lytic replication J. Virol. 77 2003 8532 8540 (Pubitemid 36871481)
41. Grossmann C.; and Ganem D. Effects of NFkappaB activation on KSHV latency and lytic reactivation are complex and context-dependent Virology 375 2008 94 102
42. Lei X.; Bai Z.; Ye F.; Xie J.; Kim C.G.; Huang Y.; and Gao S.J. Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA Nat. Cell Biol. 12 2010 193 199
43. Li X.; Feng J.; and Sun R. Oxidative stress induces reactivation of Kaposi's sarcoma-associated herpesvirus and death of primary effusion lymphoma cells J. Virol. 85 2011 715 724
44. Ye F.C.; Zhou F.C.; Xie J.P.; Kang T.; Greene W.; and Kuhne K. Kaposi's sarcoma-associated herpesvirus latent gene vFLIP inhibits viral lytic replication through NF-kappaB-mediated suppression of the AP-1 pathway: a novel mechanism of virus control of latency J. Virol. 82 2008 4235 4249 (Pubitemid 351563661)
45. Martin D.; Galisteo R.; Ji Y.; Montaner S.; and Gutkind J.S. An NF-kappaB gene expression signature contributes to Kaposi's sarcoma virus vGPCR-induced direct and paracrine neoplasia Oncogene 27 2008 1844 1852 (Pubitemid 351430813)
46. L.M. Huang, M.F. Chao, M.Y. Chen, H. Shih, Y.P. Chiang, and C.Y. Chuang Reciprocal regulatory interaction between human herpesvirus 8 and human immunodeficiency virus type 1 J. Biol. Chem. 276 2001 13427 13432
47. S. Lefort, and L. Flamand Kaposi's sarcoma-associated herpesvirus K-bZIP protein is necessary for lytic viral gene expression, DNA replication, and virion production in primary effusion lymphoma cell lines J. Virol. 83 2009 5869 5880
48. Krishnan H.H.; Naranatt P.P.; Smith M.S.; Zeng L.; Bloomer C.; and Chandran B. 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 2004 3601 3620 (Pubitemid 38568301)
49. Kim S.; Domon-Dell C.; Kang J.; Chung D.H.; Freund J.N.; and Evers B.M. Down-regulation of the tumor suppressor PTEN by the tumor necrosis factor-alpha/nuclear factor-kappaB (NF-kappaB)-inducing kinase/NF-kappaB pathway is linked to a default IkappaB-alpha autoregulatory loop J. Biol. Chem. 279 2004 4285 4291 (Pubitemid 38199016)