Kaposi's sarcoma-associated herpesvirus downregulates transforming growth factor β2 to promote enhanced stability of capillary-like tube formation

Journal of Virology

Volumn 88, Issue 24, 2014, Pages 14301-14309

  DiMaio, Terri A ^a   Gutierrez, Kimberley D ^a   Lagunoff, Michael ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 130; INTERLEUKIN 6; MATRIGEL; MICRORNA; MICRORNA K3; MICRORNA K8; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG; IL6ST PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ANGIOGENESIS; APOPTOSIS; ARTICLE; CAPILLARY BASEMENT MEMBRANE; CAPILLARY LIKE TUBE FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; HERPES VIRUS INFECTION; HUMAN HERPESVIRUS 8; MEMBRANE STABILIZATION; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; TUMOR CELL; TUMOR PROMOTION; TUMOR VASCULARIZATION; VIRUS INFECTIVITY; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; NEOVASCULARIZATION (PATHOLOGY); PHYSIOLOGY; VIROLOGY;

HUMAN HERPESVIRUS 8;

CELL LINE; CYTOKINE RECEPTOR GP130; ENDOTHELIAL CELLS; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; TRANSFORMING GROWTH FACTOR BETA2;

EID: 84911465399     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01696-14     Document Type: Article

References (35)

1. Wabinga H, Parkin D, Wabwire-Mangen F, Mugerwa J. 1993. Cancer in Kampala, Uganda, in 1989-91: changes in incidence in the era of AIDS. Int. J. Cancer 54:26-36. http://dx.doi.org/10.1002/ijc.2910540106.
2. Chokunonga E, Levy LM, Bassett MT, Mauchaza BG, Thomas DB, Parkin DM. 2000. Cancer incidence in the African population of Harare, Zimbabwe: second results from the cancer registry 1993-1995. Int. J. Cancer 85:54-59. http://dx.doi.org/10.1002/(SICI)1097-0215(20000101)85:1<54::AID-IJC10>3.0.CO;2-D.
3. Dimmeler S, Zeiher AM. 2000. Endothelial cell apoptosis in angiogenesis and vessel regression. Circ. Res. 87:434-439. http://dx.doi.org/10.1161/01.RES.87.6.434.
4. Govinden R, Bhoola KD. 2003. Genealogy, expression, and cellular function of transforming growth factor-beta. Pharmacol. Ther. 98:257-265. http://dx.doi.org/10.1016/S0163-7258(03)00035-4.
5. Lebrin F, Deckers M, Bertolino P, Ten Dijke P. 2005. TGF-beta receptor function in the endothelium. Cardiovasc. Res. 65:599-608. http://dx.doi.org/10.1016/j.cardiores.2004.10.036.
6. Zhu HJ, Burgess AW. 2001. Regulation of transforming growth factorbeta signaling. Mol. Cell Biol. Res. Commun. 4:321-330. http://dx.doi.org/10.1006/mcbr.2001.0301.
7. Wordinger RJ, Sharma T, Clark AF. 2014. The role of TGF-β2 and bone morphogenetic proteins in the trabecular meshwork and glaucoma. J. Ocul. Pharmacol. Ther. 30:154-162. http://dx.doi.org/10.1089/jop.2013.0220.
8. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T. 1997. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124:2659-2670.
9. Mercado-Pimentel ME, Runyan RB. 2007. Multiple transforming growth factor-beta isoforms and receptors function during epithelialmesenchymal cell transformation in the embryonic heart. Cells Tissues Organs 185:146-156. http://dx.doi.org/10.1159/000101315.
10. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR. 2010. Conversion of vascular endothelial cells into multipotent stem-like cells. Nat. Med. 16:1400-1406. http://dx.doi.org/10.1038/nm.2252.
11. Di Bernardini E, Campagnolo P, Margariti A, Zampetaki A, Karamariti E, Hu Y, Xu Q. 2014. Endothelial lineage differentiation from induced pluripotent stem cells is regulated by microRNA-21 and transforming growth factor β2 (TGF-β2) pathways. J. Biol. Chem. 289:3383-3393. http://dx.doi.org/10.1074/jbc.M113.495531.
12. Wang L, Damania B. 2008. Kaposi's sarcoma-associated herpesvirus confers a survival advantage to endothelial cells. Cancer Res. 68:4640-4648. http://dx.doi.org/10.1158/0008-5472.CAN-07-5988.
13. Couty J, Lupu-Meiri M, Oron Y, Gershengorn M. 2009. Kaposi's sarcoma-associated herpesvirus-G protein-coupled receptor-expressing endothelial cells exhibit reduced migration and stimulated chemotaxis by chemokine inverse agonists. J. Pharmacol. Exp. Ther. 329:1142-1147. http://dx.doi.org/10.1124/jpet.108.147686.
14. Qian L, Xie J, Ye F, Gao S. 2007. Kaposi's sarcoma-associated herpesvirus infection promotes invasion of primary human umbilical vein endothelial cells by inducing matrix metalloproteinases. J. Virol. 81:7001-7010. http://dx.doi.org/10.1128/JVI.00016-07.
15. Sadagopan S, Sharma-Walia N, Veettil M, Bottero V, Levine R, Vart RJ, Chandran B. 2009. Kaposi's sarcoma-associated herpesvirus upregulates angiogenin during infection of human dermal microvascular endothelial cells, which induces 45S rRNA synthesis, antiapoptosis, cell proliferation, migration, and angiogenesis. J. Virol. 83:3342-3364. http://dx.doi.org/10.1128/JVI.02052-08.
16. Sadagopan S, Sharma-Walia N, Veettil M, 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. http://dx.doi.org/10.1128/JVI.02333-06.
17. DiMaio TA, Gutierrez KD, Lagunoff M. 2011. Latent KSHV infection of endothelial cells induces integrin beta3 to activate angiogenic phenotypes. PLoS Pathog. 7:e1002424. http://dx.doi.org/10.1371/journal.ppat.1002424.
18. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, Grässer FA, van Dyk LF, Ho CK, Shuman S, Chien M, Russo JJ, Ju J, Randall G, Lindenbach BD, Rice CM, Simon V, Ho DD, Zavolan M, Tuschl T. 2005. Identification of microRNAs of the herpesvirus family. Nat. Methods 2:269-276. http://dx.doi.org/10.1038/nmeth746.
19. Cai X, Lu S, Zhang Z, Gonzalez CM, Damania B, Cullen BR. 2005. Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc. Natl. Acad. Sci. U. S. A. 102: 5570-5575. http://dx.doi.org/10.1073/pnas.0408192102.
20. Samols MA, Hu J, Skalsky RL, Renne R. 2005. Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi's sarcoma-associated herpesvirus. J. Virol. 79:9301-9305. http://dx.doi.org/10.1128/JVI.79.14.9301-9305.2005.
21. Samols MA, Skalsky RL, Maldonado AM, Riva A, Lopez MC, Baker HV, Renne R. 2007. Identification of cellular genes targeted by KSHV-encoded microRNAs. PLoS Pathog. 3:e65. http://dx.doi.org/10.1371/journal.ppat.0030065.
22. Liu Y, Sun R, Lin X, Liang D, Deng Q, Lan K. 2012. Kaposi's sarcomaassociated herpesvirus-encoded microRNA miR-K12-11 attenuates transforming growth factor beta signaling through suppression of SMAD5. J. Virol. 86:1372-1381. http://dx.doi.org/10.1128/JVI.06245-11.
23. Lei X, Zhu Y, Jones T, Bai Z, Huang Y, Gao SJ. 2012. A Kaposi's sarcoma-associated herpesvirus microRNA and its variants target the transforming growth factor β pathway to promote cell survival. J. Virol. 86:11698-11711. http://dx.doi.org/10.1128/JVI.06855-11.
24. Lagunoff M, Bechtel J, Venetsanakos E, Roy AM, Abbey N, Herndier B, McMahon M, Ganem D. 2002. De novo infection and serial transmission of Kaposi's sarcoma-associated herpesvirus in cultured endothelial cells. J. Virol. 76:2440-2448. http://dx.doi.org/10.1128/jvi.76.5.2440-2448.2002.
25. Renne R, Zhong W, Herndier B, McGrath M, Abbey N, Kedes D, Ganem D. 1996. Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat. Med. 2:342-346. http://dx.doi.org/10.1038/nm0396-342.
26. Brulois KF, Chang H, Lee AS, Ensser A, Wong LY, Toth Z, Lee SH, Lee HR, Myoung J, Ganem D, Oh TK, Kim JF, Gao SJ, Jung JU. 2012. Construction and manipulation of a new Kaposi's sarcoma-associated herpesvirus bacterial artificial chromosome clone. J. Virol. 86:9708-9720. http://dx.doi.org/10.1128/JVI.01019-12.
27. Krueger B, Plaisance K, Sangani R, Lanier C, Jain V, Hu J, Renne R. 2012. A core laboratory for the generation of quality controlled γ-herpesvirus bacmids: generation of KSHV microRNA mutants. Infect. Agents Cancer 7(Suppl 1):P27. http://dx.doi.org/10.1186/1750-9378-7-S1-P27.
28. Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O. 2009. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 5:376-385. http://dx.doi.org/10.1016/j.chom.2009.03.003.
29. Cullen BR. 2004. Derivation and function of small interfering RNAs and microRNAs. Virus Res. 102:3-9. http://dx.doi.org/10.1016/j.virusres.2004.01.009.
30. Ziegelbauer JM. 2011. Functions of Kaposi's sarcoma-associated herpesvirus microRNAs. Biochim. Biophys. Acta 1809:623-630. http://dx.doi.org/10.1016/j.bbagrm.2011.05.003.
31. Morris VA, Punjabi AS, Lagunoff M. 2008. Activation of Akt through gp130 receptor signaling is required for Kaposi's sarcoma-associated herpesvirus-induced lymphatic reprogramming of endothelial cells. J. Virol. 82:8771-8779. http://dx.doi.org/10.1128/JVI.00766-08.
32. Morris VA, Punjabi AS, Wells RC, Wittkopp CJ, Vart R, Lagunoff M. 2012. The KSHV viral IL-6 homolog is sufficient to induce blood to lymphatic endothelial cell differentiation. Virology 428:112-120. http://dx.doi.org/10.1016/j.virol.2012.03.013.
33. Shi Y, Massagué J. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700. http://dx.doi.org/10.1016/S0092-8674(03)00432-X.
34. Zhu Y, Haecker I, Yang Y, Gao SJ, Renne R. 2013. γ-Herpesvirusencoded miRNAs and their roles in viral biology and pathogenesis. Curr. Opin. Virol. 3:266-275. http://dx.doi.org/10.1016/j.coviro.2013.05.013.
35. Di Bartolo DL, Cannon M, Liu YF, Renne R, Chadburn A, Boshoff C, Cesarman E. 2008. KSHV LANA inhibits TGF-beta signaling through epigenetic silencing of the TGF-beta type II receptor. Blood 111:4731-4740. http://dx.doi.org/10.1182/blood-2007-09-110544.