Latent KSHV infection of endothelial cells induces integrin beta3 to activate angiogenic phenotypes

PLoS Pathogens

Volumn 7, Issue 12, 2011, Pages

  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

BETA3 INTEGRIN; FOCAL ADHESION KINASE; INTEGRIN; PROTEIN TYROSINE KINASE; VITRONECTIN RECEPTOR; SMALL INTERFERING RNA;

ANGIOGENESIS; ARTICLE; CANCER CELL; CAPILLARY ENDOTHELIUM; CELL ADHESION; CELL CULTURE; CELL MOTILITY; CELL SURFACE; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; KAPOSI SARCOMA; LATENT VIRUS INFECTION; PHENOTYPE; PROTEIN FUNCTION; PROTEIN INDUCTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; VIRUS INFECTIVITY; VIRUS LATENCY; BIOSYNTHESIS; CELL LINE; CELL MOTION; CELL SEPARATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY;

HUMAN HERPESVIRUS 8;

CELL ADHESION; CELL LINE; CELL MOVEMENT; CELL SEPARATION; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HERPESVIRUS 8, HUMAN; HUMANS; INTEGRIN BETA3; NEOVASCULARIZATION, PATHOLOGIC; PHENOTYPE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SARCOMA, KAPOSI; SIGNAL TRANSDUCTION; VIRUS LATENCY;

EID: 84855294124     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002424     Document Type: Article

References (74)

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.
2. Chokunonga E, Levy L, Bassett M, Mauchaza B, Thomas D, et al. (2000) Cancer incidence in the African population of Harare, Zimbabwe: second results from the cancer registry 1993-1995. Int J Cancer 85: 54-59.
3. Staskus K, Zhong W, Gebhard K, Herndier B, Wang H, et al. (1997) Kaposi's sarcoma-associated herpesvirus gene expression in endothelial (spindle) tumor cells. J Virol 71: 715-719.
4. Lagunoff M, Bechtel J, Venetsanakos E, Roy A, Abbey N, et al. (2002) De novo infection and serial transmission of Kaposi's sarcoma-associated herpesvirus in cultured endothelial cells. J Virol 76: 2440-2448.
5. Bechtel JT, Liang Y, Hvidding J, Ganem D, (2003) Host range of Kaposi's sarcoma-associated herpesvirus in cultured cells. J Virol 77: 6474-6481.
6. Lagunoff M, Lukac DM, Ganem D, (2001) Immunoreceptor tyrosine-based activation motif-dependent signaling by Kaposi's sarcoma-associated herpesvirus K1 protein: effects on lytic viral replication. J Virol 75: 5891-5898.
7. Wang L, Damania B, (2008) Kaposi's sarcoma-associated herpesvirus confers a survival advantage to endothelial cells. Cancer Res 68: 4640-4648.
8. 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.
9. 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.
10. Sadagopan S, Sharma-Walia N, Veettil M, Bottero V, Levine R, et al. (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.
11. Sadagopan S, Sharma-Walia N, Veettil M, Raghu H, Sivakumar R, et al. (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.
12. Sivakumar R, Sharma-Walia N, Raghu H, Veettil M, Sadagopan S, et al. (2008) Kaposi's sarcoma-associated herpesvirus induces sustained levels of vascular endothelial growth factors A and C early during in vitro infection of human microvascular dermal endothelial cells: biological implications. J Virol 82: 1759-1776.
13. Masood R, Cesarman E, Smith DL, Gill PS, Flore O, (2002) Human herpesvirus-8-transformed endothelial cells have functionally activated vascular endothelial growth factor/vascular endothelial growth factor receptor. Am J Pathol 160: 23-29.
14. Carroll P, Brazeau E, Lagunoff M, (2004) Kaposi's sarcoma-associated herpesvirus infection of blood endothelial cells induces lymphatic differentiation. Virology 328: 7-18.
15. Carroll P, Kenerson H, Yeung R, Lagunoff M, (2006) Latent Kaposi's sarcoma-associated herpesvirus infection of endothelial cells activates hypoxia-induced factors. J Virol 80: 10802-10812.
16. Wang HW, Trotter MW, Lagos D, Bourboulia D, Henderson S, et al. (2004) Kaposi sarcoma herpesvirus-induced cellular reprogramming contributes to the lymphatic endothelial gene expression in Kaposi sarcoma. Nat Genet 36: 687-693.
17. Hong YK, Foreman K, Shin JW, Hirakawa S, Curry CL, et al. (2004) Lymphatic reprogramming of blood vascular endothelium by Kaposi sarcoma-associated herpesvirus. Nat Genet 36: 683-685.
18. Sharma-Walia N, Paul AG, Bottero V, Sadagopan S, Veettil MV, et al. (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.
19. Vart R, Nikitenko L, Lagos D, Trotter M, Cannon M, et al. (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. Ye F, Blackbourn D, Mengel M, Xie J, Qian L, et al. (2007) Kaposi's sarcoma-associated herpesvirus promotes angiogenesis by inducing angiopoietin-2 expression via AP-1 and Ets1. J Virol 81: 3980-3991.
21. Ma T, Jham BC, Hu J, Friedman ER, Basile JR, et al. (2010) Viral G protein-coupled receptor up-regulates Angiopoietin-like 4 promoting angiogenesis and vascular permeability in Kaposi's sarcoma. Proc Natl Acad Sci USA 107: 14363-14368.
22. Mansouri M, Rose P, Moses A, Früh K, (2008) Remodeling of endothelial adherens junctions by Kaposi's sarcoma-associated herpesvirus. J Virol 82: 9615-9628.
23. Guilluy C, Zhang Z, Bhende PM, Sharek L, Wang L, et al. (2011) Latent KSHV infection increases the vascular permeability of human endothelial cells. Blood 118: 5344-5354.
24. Qian L, Greene W, Ye F, Gao S, (2008) Kaposi's sarcoma-associated herpesvirus disrupts adherens junctions and increases endothelial permeability by inducing degradation of VE-cadherin. J Virol 82: 11902-11912.
25. Dwyer J, Le Guelte A, Galan Moya EM, Sumbal M, Carlotti A, et al. (2011) Remodeling of VE-cadherin junctions by the human herpes virus 8 G-protein coupled receptor. Oncogene 30: 190-200.
26. Qin Z, Dai L, Slomiany MG, Toole BP, Parsons C, (2010) Direct activation of emmprin and associated pathogenesis by an oncogenic herpesvirus. Cancer Res 70: 3884-3889.
27. Dai L, Bratoeva M, Toole BP, Qin Z, Parsons C, (2011) KSHV activation of VEGF secretion and invasion for endothelial cells is mediated through viral upregulation of emmprin-induced signal transduction. Int J Cancer. E-pub ahead of print doi:10.1002/ijc.26428.
28. Aoki Y, Jaffe E, Chang Y, Jones K, Teruya-Feldstein J, et al. (1999) Angiogenesis and hematopoiesis induced by Kaposi's sarcoma-associated herpesvirus-encoded interleukin-6. Blood 93: 4034-4043.
29. Bakken T, He M, Cannon ML, (2010) The phosphatase Shp2 is required for signaling by the Kaposi's sarcoma-associated herpesvirus viral GPCR in primary endothelial cells. Virology 397: 379-388.
30. Masood R, Xia G, Smith DL, Scalia P, Still JG, et al. (2005) Ephrin B2 expression in Kaposi sarcoma is induced by human herpesvirus type 8: phenotype switch from venous to arterial endothelium. Blood 105: 1310-1318.
31. Xie J, Pan H, Yoo S, Gao S, (2005) Kaposi's sarcoma-associated herpesvirus induction of AP-1 and interleukin 6 during primary infection mediated by multiple mitogen-activated protein kinase pathways. J Virol 79: 15027-15037.
32. McAllister SC, Hansen SG, Ruhl RA, Raggo CM, DeFilippis VR, et al. (2004) Kaposi sarcoma-associated herpesvirus (KSHV) induces heme oxygenase-1 expression and activity in KSHV-infected endothelial cells. Blood 103: 3465-3473.
33. Fonsato V, Buttiglieri S, Deregibus MC, Bussolati B, Caselli E, et al. (2008) PAX2 expression by HHV-8-infected endothelial cells induced a proangiogenic and proinvasive phenotype. Blood 111: 2806-2815.
34. Cai Q, Murakami M, Si H, Robertson E, (2007) A potential alpha-helix motif in the amino terminus of LANA encoded by Kaposi's sarcoma-associated herpesvirus is critical for nuclear accumulation of HIF-1alpha in normoxia. J Virol 81: 10413-10423.
35. Shin Y, Joo C, Gack M, Lee H, Jung J, (2008) Kaposi's sarcoma-associated herpesvirus viral IFN regulatory factor 3 stabilizes hypoxia-inducible factor-1 alpha to induce vascular endothelial growth factor expression. Cancer Res 68: 1751-1759.
36. Wang L, Dittmer D, Tomlinson C, Fakhari F, Damania B, (2006) Immortalization of primary endothelial cells by the K1 protein of Kaposi's sarcoma-associated herpesvirus. Cancer Res 66: 3658-3666.
37. Boshoff C, Endo Y, Collins P, Takeuchi Y, Reeves J, et al. (1997) Angiogenic and HIV-inhibitory functions of KSHV-encoded chemokines. Science 278: 290-294.
38. Stine J, Wood C, Hill M, Epp A, Raport C, et al. (2000) KSHV-encoded CC chemokine vMIP-III is a CCR4 agonist, stimulates angiogenesis, and selectively chemoattracts TH2 cells. Blood 95: 1151-1157.
39. Arvanitakis L, Geras-Raaka E, Varma A, Gershengorn M, Cesarman E, (1997) Human herpesvirus KSHV encodes a constitutively active G-protein-coupled receptor linked to cell proliferation. Nature 385: 347-350.
40. Montaner S, Sodhi A, Pece S, Mesri E, Gutkind J, (2001) The Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor promotes endothelial cell survival through the activation of Akt/protein kinase B. Cancer Res 61: 2641-2648.
41. Sodhi A, Montaner S, Patel V, Zohar M, Bais C, et al. (2000) The Kaposi's sarcoma-associated herpes virus G protein-coupled receptor up-regulates vascular endothelial growth factor expression and secretion through mitogen-activated protein kinase and p38 pathways acting on hypoxia-inducible factor 1alpha. Cancer Res 60: 4873-4880.
42. Bais C, Santomasso B, Coso O, Arvanitakis L, Raaka E, et al. (1998) G-protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator. Nature 391: 86-89.
43. Bais C, Van Geelen A, Eroles P, Mutlu A, Chiozzini C, et al. (2003) Kaposi's sarcoma associated herpesvirus G protein-coupled receptor immortalizes human endothelial cells by activation of the VEGF receptor-2/KDR. Cancer Cell 3: 131-143.
44. Shan B, Morris CA, Zhuo Y, Shelby BD, Levy DR, et al. (2007) Activation of proMMP-2 and Src by HHV8 vGPCR in human pulmonary arterial endothelial cells. J Mol Cell Cardiol 42: 517-525.
45. Dourmishev L, Dourmishev A, Palmeri D, Schwartz R, Lukac D, (2003) Molecular genetics of Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8) epidemiology and pathogenesis. Microbiol Mol Biol Rev 67: 175-212 table of contents.
46. Murakami Y, Yamagoe S, Noguchi K, Takebe Y, Takahashi N, et al. (2006) Ets-1-dependent expression of vascular endothelial growth factor receptors is activated by latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus through interaction with Daxx. J Biol Chem 281: 28113-28121.
47. Mitra S, Schlaepfer D, (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18: 516-523.
48. Avraamides CJ, Garmy-Susini B, Varner JA, (2008) Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer 8: 604-617.
49. Hehlgans S, Haase M, Cordes N, (2007) Signalling via integrins: implications for cell survival and anticancer strategies. Biochim Biophys Acta 1775: 163-180.
50. Gasparini G, Brooks PC, Biganzoli E, Vermeulen PB, Bonoldi E, et al. (1998) Vascular integrin alpha(v)beta3: a new prognostic indicator in breast cancer. Clin Cancer Res 4: 2625-2634.
51. Bello L, Zhang J, Nikas DC, Strasser JF, Villani RM, et al. (2000) Alpha(v)beta3 and alpha(v)beta5 integrin expression in meningiomas. Neurosurgery 47: 1185-1195.
52. Brooks PC, Clark RA, Cheresh DA, (1994) Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264: 569-571.
53. Brooks PC, Montgomery AM, Rosenfeld M, Reisfeld RA, Hu T, et al. (1994) Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 79: 1157-1164.
54. Brooks PC, Strömblad S, Klemke R, Visscher D, Sarkar FH, et al. (1995) Antiintegrin alpha v beta 3 blocks human breast cancer growth and angiogenesis in human skin. J Clin Invest 96: 1815-1822.
55. Sheu JR, Yen MH, Kan YC, Hung WC, Chang PT, et al. (1997) Inhibition of angiogenesis in vitro and in vivo: comparison of the relative activities of triflavin, an Arg-Gly-Asp-containing peptide and anti-alpha(v)beta3 integrin monoclonal antibody. Biochim Biophys Acta 1336: 445-454.
56. Garrigues HJ, Rubinchikova YE, Dipersio CM, Rose TM, (2008) Integrin alphaVbeta3 Binds to the RGD motif of glycoprotein B of Kaposi's sarcoma-associated herpesvirus and functions as an RGD-dependent entry receptor. J Virol 82: 1570-1580.
57. Desgrosellier JS, Barnes LA, Shields DJ, Huang M, Lau SK, et al. (2009) An integrin alpha(v)beta(3)-c-Src oncogenic unit promotes anchorage-independence and tumor progression. Nat Med 15: 1163-1169.
58. Dyson OF, Oxendine TL, Hamden KE, Ford PW, Akula SM, (2008) Differential regulation of the attachment of Kaposi's sarcoma-associated herpesvirus (KSHV)-infected human B cells to extracellular matrix by KSHV-encoded gB and cellular alphaV integrins. Cell Microbiol 10: 1546-1558.
59. Dyson O, Bryan B, Lambert P, Ford P, Akula S, (2007) Beta1 integrins mediate tubule formation induced by supernatants derived from KSHV-infected cells. Intervirology 50: 245-253.
60. Desgrosellier JS, Cheresh DA, (2010) Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 10: 9-22.
61. Mahabeleshwar GH, Feng W, Reddy K, Plow EF, Byzova TV, (2007) Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ Res 101: 570-580.
62. Reynolds LE, Wyder L, Lively JC, Taverna D, Robinson SD, et al. (2002) Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat Med 8: 27-34.
63. Reynolds AR, Reynolds LE, Nagel TE, Lively JC, Robinson SD, et al. (2004) Elevated Flk1 (vascular endothelial growth factor receptor 2) signaling mediates enhanced angiogenesis in beta3-integrin-deficient mice. Cancer Res 64: 8643-8650.
64. Mahabeleshwar GH, Feng W, Phillips DR, Byzova TV, (2006) Integrin signaling is critical for pathological angiogenesis. J Exp Med 203: 2495-2507.
65. De S, Razorenova O, McCabe NP, O'Toole T, Qin J, et al. (2005) VEGF-integrin interplay controls tumor growth and vascularization. Proc Natl Acad Sci USA 102: 7589-7594.
66. Nemerow G, Cheresh D, (2002) Herpesvirus hijacks an integrin. Nat Cell Biol 4: E69-71.
67. Veettil M, Sadagopan S, Sharma-Walia N, Wang F, Raghu H, et al. (2008) Kaposi's sarcoma-associated herpesvirus forms a multimolecular complex of integrins (alphaVbeta5, alphaVbeta3, and alpha3beta1) and CD98-xCT during infection of human dermal microvascular endothelial cells, and CD98-xCT is essential for the postentry stage of infection. J Virol 82: 12126-12144.
68. Krishnan H, Sharma-Walia N, Streblow D, Naranatt P, Chandran B, (2006) Focal adhesion kinase is critical for entry of Kaposi's sarcoma-associated herpesvirus into target cells. J Virol 80: 1167-1180.
69. Sharma-Walia N, Naranatt P, Krishnan H, Zeng L, Chandran B, (2004) Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8 envelope glycoprotein gB induces the integrin-dependent focal adhesion kinase-Src-phosphatidylinositol 3-kinase-rho GTPase signal pathways and cytoskeletal rearrangements. J Virol 78: 4207-4223.
70. Wang F, Akula S, Sharma-Walia N, Zeng L, Chandran B, (2003) Human herpesvirus 8 envelope glycoprotein B mediates cell adhesion via its RGD sequence. J Virol 77: 3131-3147.
71. Venetsanakos E, Mirza A, Fanton C, Romanov SR, Tlsty T, et al. (2002) Induction of tubulogenesis in telomerase-immortalized human microvascular endothelial cells by glioblastoma cells. Exp Cell Res 273: 21-33.
72. Renne R, Zhong W, Herndier B, McGrath M, Abbey N, et al. (1996) Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat Med 2: 342-346.
73. Chen L, Lagunoff M, (2005) Establishment and maintenance of Kaposi's sarcoma-associated herpesvirus latency in B cells. J Virol 79: 14383-14391.
74. Rothermel T, Engelhardt B, Sheibani N, (2005) Polyoma virus middle-T-transformed PECAM-1 deficient mouse brain endothelial cells proliferate rapidly in culture and form hemangiomas in mice. J Cell Physiol 202: 230-239.