Latency-associated nuclear antigen of kaposi sarcoma-associated herpesvirus promotes angiogenesis through targeting notch signaling effector hey

Cancer Research

Volumn 74, Issue 7, 2014, Pages 2026-2037

  Wang, Xing ^a,b   He, Zhiheng ^a   Xia, Tian ^a   Li, Xiaofan ^a   Liang, Deguang ^a   Lin, Xianzhi ^a   Wen, Hao ^b   Lan, Ke ^a  

^a INSTITUTE PASTEUR OF SHANGHAI   (China)

^b XINJIANG MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA SECRETASE INHIBITOR; LATENCY ASSOCIATED NUCLEAR ANTIGEN; MATRIGEL; NOTCH RECEPTOR; PROTEIN DLL4; PROTEIN HEY1; PROTEIN HEYL; TRANSCRIPTOME; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INHIBITION KINETICS; KAPOSI SARCOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; TUMOR VASCULARIZATION; UPREGULATION;

ANIMALS; ANTIGENS, VIRAL; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; FEMALE; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; NUCLEAR PROTEINS; RECEPTORS, NOTCH; REPRESSOR PROTEINS; SARCOMA, KAPOSI; SIGNAL TRANSDUCTION;

EID: 84897389369     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-1467     Document Type: Article

References (50)

1. Klagsbrun M, Moses MA. Molecular angiogenesis. Chem Biol 1999;6: R217-24.
2. Saha A, Kaul R, Murakami M, Robertson ES. Tumor viruses and cancer biology: modulating signaling pathways for therapeutic intervention. Cancer Biol Ther 2010;10:961-78.
3. Mesri EA, Cesarman E, Boshoff C. Kaposi's sarcoma and its associated herpesvirus. Nat Rev Cancer 2010;10:707-19.
4. Dimaio TA, Lagunoff M. KSHV induction of angiogenic and lymphangiogenic phenotypes. Front Microbiol 2012;3:102.
5. Carroll PA, Kenerson HL, Yeung RS, Lagunoff M. Latent Kaposi's sarcoma-Associated herpesvirus infection of endothelial cells activates hypoxia-induced factors. J Virol 2006;80:10802-12.
6. Jham BC, Ma T, Hu J, Chaisuparat R, Friedman ER, Pandolfi PP, et al. Amplification of the angiogenic signal through the activation of the TSC/mTOR/HIF axis by the KSHV vGPCR in Kaposi's sarcoma. PloS ONE 2011;6:e19103.
7. Wang L, Wakisaka N, Tomlinson CC, DeWire SM, Krall S, Pagano JS, et al. The Kaposi's sarcoma-Associated herpesvirus (KSHV/HHV-8) K1 protein induces expression of angiogenic and invasion factors. Cancer Res 2004;64:2774-81.
8. Mesri EA, Cesarman E. Kaposi's sarcoma herpesvirus oncogenesis is a notch better in 3D. Cell Host Microbe 2011;10:529-31.
9. Bridge G, Monteiro R, Henderson S, Emuss V, Lagos D, Georgopoulou D, et al. The microRNA-30 family targets DLL4 to modulate endothelial cell behavior during angiogenesis. Blood 2012;120:5063-72.
10. DiMaio TA, Gutierrez KD, Lagunoff M. Latent KSHV infection of endothelial cells induces integrin beta3 to activate angiogenic phenotypes. PLoS Pathog 2011;7:e1002424.
11. Guilluy C, Zhang Z, Bhende PM, Sharek L, Wang L, Burridge K, et al. Latent KSHV infection increases the vascular permeability of human endothelial cells. Blood 2011;118:5344-54.
12. He M, Zhang W, Bakken T, Schutten M, Toth Z, Jung JU, et al. Cancer angiogenesis induced by Kaposi sarcoma-Associated herpesvirus is mediated by EZH2. Cancer Res 2012;72:3582-92.
13. Phng LK, Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev Cell 2009;16:196-208.
14. Roca C, Adams RH. Regulation of vascular morphogenesis by Notch signaling. Genes Dev 2007;21:2511-24.
15. Curry CL, Reed LL, Golde TE, Miele L, Nickoloff BJ, Foreman KE. Gamma secretase inhibitor blocks Notch activation and induces apoptosis in Kaposi's sarcoma tumor cells. Oncogene 2005;24: 6333-44.
16. Emuss V, Lagos D, Pizzey A, Gratrix F, Henderson SR, Boshoff C. KSHV manipulates Notch signaling by DLL4 and JAG1 to alter cell cycle genes in lymphatic endothelia. PLoS Pathog 2009;5:e1000616.
17. Liu R, Li X, Tulpule A, Zhou Y, Scehnet JS, Zhang S, et al. KSHVinduced notch components render endothelial and mural cell characteristics and cell survival. Blood 2010;115:887-95.
18. Cheng F, Pekkonen P, Laurinavicius S, Sugiyama N, Henderson S, Gunther T, et al. KSHV-initiated notch activation leads to membranetype-1 matrix metalloproteinase-dependent lymphatic endothelial-Tomesenchymal transition. Cell Host Microbe 2011;10:577-90.
19. Li JL, Sainson RC, Oon CE, Turley H, Leek R, Sheldon H, et al. DLL4-Notch signaling mediates tumor resistance to anti-VEGF therapy in vivo. Cancer Res 2011;71:6073-83.
20. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, et al. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 2006;444:1032-7.
21. Benedito R, Rocha SF, Woeste M, Zamykal M, Radtke F, Casanovas O, et al. Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling. Nature 2012;484:110-4.
22. Zeng Q, Li S, Chepeha DB, Giordano TJ, Li J, Zhang H, et al. Crosstalk between tumor and endothelial cells promotes tumor angiogenesis by MAPK activation of Notch signaling. Cancer Cell 2005;8:13-23.
23. Funahashi Y, Hernandez SL, Das I, Ahn A, Huang J, Vorontchikhina M, et al. A notch1 ectodomain construct inhibits endothelial notch signaling, tumor growth, and angiogenesis. Cancer Res 2008;68: 4727-35.
24. Chin MT, Maemura K, Fukumoto S, Jain MK, Layne MD, Watanabe M, et al. Cardiovascular basic helix loop helix factor 1, a novel transcriptional repressor expressed preferentially in the developing and adult cardiovascular system. J Biol Chem 2000;275:6381-7.
25. Fischer A, Schumacher N, Maier M, Sendtner M, Gessler M. The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev 2004;18:901-11.
26. Fischer A, Steidl C, Wagner TU, Lang E, Jakob PM, Friedl P, et al. Combined loss of Hey1 and HeyL causes congenital heart defects because of impaired epithelial to mesenchymal transition. Circ Res 2007;100:856-63.
27. Sharff KA, Song WX, Luo X, Tang N, Luo J, Chen J, et al. Hey1 basic helix-loop-helix protein plays an important role in mediating BMP9-induced osteogenic differentiation of mesenchymal progenitor cells. J Biol Chem 2009;284:649-59.
28. Lin GL, Hankenson KD. Integration of BMP, Wnt, and notch signaling pathways in osteoblast differentiation. J Cell Biochem 2011;112: 3491-501.
29. Heisig J, Weber D, Englberger E, Winkler A, Kneitz S, Sung WK, et al. Target gene analysis by microarrays and chromatin immunoprecipitation identifies HEY proteins as highly redundant bHLH repressors. PLoS Genet 2012;8:e1002728.
30. Lan K, Verma SC, Murakami M, Bajaj B, Kaul R, Robertson ES. Kaposi's sarcoma herpesvirus-encoded latency-Associated nuclear antigen stabilizes intracellular activated Notch by targeting the Sel10 protein. Proc Natl Acad Sci U S A 2007;104:16287-92.
31. Li X, Liang D, Lin X, Robertson ES, Lan K. Kaposi's sarcoma-Associated herpesvirus-encoded latency-Associated nuclear antigen reduces interleukin-8 expression in endothelial cells and impairs neutrophil chemotaxis by degrading nuclear p65. J Virol 2011;85:8606-15.
32. Zhao Q. Vascular endothelial growth factor is necessary in the development of arteriosclerosis by recruiting/activating monocytes in a rat model of long-Term inhibition of nitric oxide synthesis. Circulation 2002;105:1110-5.
33. Anand S, Majeti BK, Acevedo LM, Murphy EA, Mukthavaram R, Scheppke L, et al. MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat Med 2010;16:909-14.
34. Volpert OV, Pili R, Sikder HA, Nelius T, Zaichuk T, Morris C, et al. Id1 regulates angiogenesis through transcriptional repression of thrombospondin-1. Cancer Cell 2002;2:473-83.
35. Toung JM, Morley M, Li M, Cheung VG. RNA-sequence analysis of human B-cells. Genome Res 2011;21:991-8.
36. Henderson AM, Wang SJ, Taylor AC, Aitkenhead M, Hughes CC. The basic helix-loop-helix transcription factor HESR1 regulates endothelial cell tube formation. J Biol Chem 2001;276:6169-76.
37. Taylor KL, Henderson AM, Hughes CC. Notch activation during endothelial cell network formation in vitro targets the basic HLH transcription factor HESR-1 and downregulates VEGFR-2/KDR expression. Microvasc Res 2002;64:372-83.
38. Ma T, Jham BC, Hu J, Friedman ER, Basile JR, Molinolo A, et al. Viral G protein-coupled receptor up-regulates Angiopoietin-like 4 promoting angiogenesis and vascular permeability in Kaposi's sarcoma. Proc Natl Acad Sci U S A 2010;107:14363-8.
39. Ballon G, Chen K, Perez R, Tam W, Cesarman E. Kaposi sarcoma herpesvirus (KSHV) vFLIP oncoprotein induces B cell transdifferentiation and tumorigenesis in mice. J Clin Invest 2011;121:1141-53.
40. Guasparri I, Keller SA, Cesarman E. KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med 2004;199:993-1003.
41. Herbert SP, Stainier DY. Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat Rev Mol Cell Biol 2011; 12:551-64.
42. Wang L, Damania B. Kaposi's sarcoma-Associated herpesvirus confers a survival advantage to endothelial cells. Cancer Res 2008;68: 4640-8.
43. Duarte A, Hirashima M, Benedito R, Trindade A, Diniz P, Bekman E, et al. Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev 2004;18:2474-8.
44. Krop I, Demuth T, Guthrie T, Wen PY, Mason WP, Chinnaiyan P, et al. Phase I pharmacologic and pharmacodynamic study of the gamma secretase (Notch) inhibitor MK-0752 in adult patients with advanced solid tumors. J Clin Oncol 2012;30:2307-13.
45. Trindade A, Kumar SR, Scehnet JS, Lopes-da-Costa L, Becker J, Jiang W, et al. Overexpression of delta-like 4 induces arterialization and attenuates vessel formation in developing mouse embryos. Blood 2008;112:1720-9.
46. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, et al. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 2006;444:1083-7.
47. Gould F, Harrison SM, Hewitt EW, Whitehouse A. Kaposi's sarcomaassociated herpesvirusRTApromotes degradation of the Hey1 repressor protein through the ubiquitin proteasome pathway. J Virol 2009;83:6727-38.
48. Yada K, Do E, Sakakibara S, Ohsaki E, Ito E, Watanabe S, et al. KSHV RTA induces a transcriptional repressor, HEY1 that represses rta promoter. Biochem Biophys Res Commun 2006;345:410-8.
49. Belandia B, Powell SM, Garcia-Pedrero JM, Walker MM, Bevan CL, Parker MG. Hey1, a mediator of notch signaling, is an androgen receptor corepressor. Mol Cell Biol 2005;25:1425-36.
50. Belyea BC, Naini S, Bentley RC, Linardic CM. Inhibition of the Notch-Hey1 axis blocks embryonal rhabdomyosarcoma tumorigenesis. Clin Cancer Res 2011;17:7324-36.