Ephrin-A1 Is Up-Regulated by Hypoxia in Cancer Cells and Promotes Angiogenesis of HUVECs through a Coordinated Cross-Talk with eNOS

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Song, Yong ^a   Zhao, Xiao Ping ^a   Song, Kai ^a   Shang, Zheng Jun ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EPHRIN A1; N(G) NITROARGININE METHYL ESTER; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SERINE DERIVATIVE;

ANGIOGENESIS; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; PROTEIN CROSS LINKING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TUMOR MICROENVIRONMENT; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; WESTERN BLOTTING;

CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMONES; COCULTURE TECHNIQUES; ENZYME INHIBITORS; EPHRIN-A1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MORPHOLINES; NEOVASCULARIZATION, PATHOLOGIC; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84883637332     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074464     Document Type: Article

References (41)

1. Saharinen P, Eklund L, Pulkki K, BonoK P, Alitalo K, (2011) VEGF and angiopoietin signaling in tumor angiogenesis and metastasis. Trends in molecular medicine 17(7): 347-362.
2. Ongusaha PP, Kwak JC, Zwible AJ, Macip S, Higashiyama S, et al. (2004) HB-EGF is a potent inducer of tumor growth and angiogenesis. Cancer research 64(15): 5283-5290.
3. Izumi Y, Xu L, Tomaso ED, Fukumura D, Jain RK, (2002) Tumour biology: herceptin acts as an anti-angiogenic cocktail. Nature 416(6878): 279-280.
4. Beauchamp, Beauchamp, Debinski W, (2011) Ephs and ephrins in cancer: Ephrin-A1 signaling. Seminars in Cell & Developmental Biology 23(2012): 109-115.
5. Brantley-Sieders DM, Fang WB, Hwang Y, Hicks D, Chen J, (2006) Ephrin-A1 facilitates mammary tumor metastasis through an angiogenesis-dependent mechanism mediated by EphA receptor and vascular endothelial growth factor in mice. Cancer research 66(21): 10315-10324.
6. Shao Z, Zhang WF, Chen XM, Shang ZJ, (2008) Expression of EphA2 and VEGF in squamous cell carcinoma of the tongue: correlation with the angiogenesis and clinical outcome. Oral Oncol 44(12): 1110-1117.
7. Brantley DM, Cheng N, Thompson EJ, Lin Q, Brekken RA, et al. (2002) Soluble Eph A receptors inhibit tumor angiogenesis and progression in vivo. Oncogene 21(46): 7011-7026.
8. Cheng N, Brantley DM, Chen J, (2002) The ephrins and Eph receptors in angiogenesis. Cytokine Growth Factor Rev 13(1): 75-85.
9. Acker T, Plate KH, (2003) Role of hypoxia in tumor angiogenesis-molecular and cellular angiogenic crosstalk. Cell and tissue research 314(1): 145-155.
10. Vihanto MM, Plock J, Erni D, Frey BM, Frey FJ, et al. (2005) Hypoxia up-regulates expression of Eph receptors and ephrins in mouse skin. The FASEB journal 19(12): 1689-1691.
11. Le QT, Kong C, Lavori PW, O'Byrne K, Erler JT, et al. (2007) Expression and prognostic significance of a panel of tissue hypoxia markers in head-and-neck squamous cell carcinomas. Int J Radiat Oncol Biol Phys 69(1): 167-175.
12. Pratt RL, Kinch MS, (2002) Activation of the EphA2 tyrosine kinase stimulates the MAP/ERK kinase signaling cascade. Oncogene 21(50): 7690-7699.
13. Brantley-Sieders DM, Caughron J, Hicks D, Pozzi A, Ruiz JC, et al. (2004) EphA2 receptor tyrosine kinase regulates endothelial cell migration and vascular assembly through phosphoinositide 3-kinase-mediated Rac1 GTPase activation. J Cell Sci 117(Pt10): 2037-2049.
14. Fukumura D, Gohongi T, Kadambi A, Izumi Y, Ang J, et al. (2001) Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proceedings of the National Academy of Sciences 98(5): 2604-2609.
15. Gallo O, Fini-Storchi I, Vergari WA, Masini E, Morbidelli L, et al. (1998) Role of nitric oxide in angiogenesis and tumor progression in head and neck cancer. Journal of the National Cancer Institute 90(8): 587-596.
16. Fukumura D, Kashiwagi S, Jain RK, (2006) The role of nitric oxide in tumour progression. Nature Reviews Cancer 6(7): 521-534.
17. Chen G, Zhang W, Li YP, Ren JG, Xu N, et al. (2013) Hypoxia-induced autophagy in endothelial cells: A double-edged sword in the progression of infantile hemangioma? Cardiovascular Research 98 (3): 437-448.
18. Beauchamp A, Lively MO, Mintz A, Gibo D, Wykosky J, et al. (2012) EphrinA1 Is Released in Three Forms from Cancer Cells by Matrix Metalloproteases. Molecular and cellular biology 32(16): 3253-3264.
19. Saik JE, Gould DJ, Keswani AH, Dickinson ME, West JL, (2011) Biomimetic hydrogels with immobilized EphrinA1 for therapeutic angiogenesis. Biomacromolecules 12: 2715-2722.
20. Dudzinski DM, Michel T, (2007) Life history of eNOS: partners and pathways. Cardiovascular Research 75(2): 247-260.
21. Vanhaesebroeck B, Leevers SJ, Panayotou G, Waterfield MD, (1997) Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends in biochemical sciences 22(7): 267-272.
22. Cantley LC, (2002) The phosphoinositide 3-kinase pathway. Science 296(5573): 1655-1657.
23. Zhuang G, Hunter S, Hwang Y, Chen J, (2007) Regulation of EphA2 receptor endocytosis by SHIP2 lipid phosphatase via phosphatidylinositol 3-Kinase-dependent Rac1 activation. J Biol Chem 282(4): 2683-2694.
24. Pasquale EB, (2010) Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat Rev Cancer 10(3): 165-180.
25. Wykosky J, Palma E, Gibo DM, Ringler S, Turner CP, et al. (2008) Soluble monomeric EphrinA1 is released from tumor cells and is a functional ligand for the EphA2 receptor. Oncogene 27(58): 7260-7273.
26. Wykosky J, Gibo DM, Stanton C, Debinski W, (2005) EphA2 as a novel molecular marker and target in glioblastoma multiforme. Mol Cancer Res 3(10): 541-551.
27. Papapetropoulos A, Garcia-Cardena G, Madri JA, Sessa WC, (1997) Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 100(12): 3131-3139.
28. Sbaa E, Frérart F, Feron O, (2005) The double regulation of endothelial nitric oxide synthase by caveolae and caveolin: a paradox solved through the study of angiogenesis. Trends in cardiovascular medicine 15(5): 157-162.
29. Cale JM, Bird IM, (2006) Inhibition of MEK/ERK1/2 signalling alters endothelial nitric oxide synthase activity in an agonist-dependent manner. Biochem J 398(2): 279-288.
30. Mount PF, Kemp BE, Power DA, (2007) Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. Journal of molecular and cellular cardiology 42(2): 271-279.
31. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, et al. (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399(6736): 601-605.
32. Liu W, Ahmad S, Reinmuth N, Shaheen RM, Jung YD, et al. (2000) Endothelial cell survival and apoptosis in the tumor vasculature. Apoptosis 5(4): 323-328.
33. Sessa WC, (2004) eNOS at a glance. Journal of cell science 117(12): 2427-2429.
34. Namkoong S, Kim CK, Cho YL, Kim JH, Lee H, et al. (2009) Forskolin increases angiogenesis through the coordinated cross-talk of PKA-dependent VEGF expression and Epac-mediated PI3K/Akt/eNOS signaling. Cell Signal 21(6): 906-915.
35. Shi F, Wang YC, Zhao TZ, Zhang S, Du TY, et al. (2012) Effects of Simulated Microgravity on Human Umbilical Vein Endothelial Cell Angiogenesis and Role of the PI3K-Akt-eNOS Signal Pathway. PLoS One 7(7): e40365.
36. Harris AL, (2002) Hypoxia-a key regulatory factor in tumour growth. Nature Reviews Cancer 2(1): 38-47.
37. Cheng NL, Chen J, (2001) TNF-alpha induction of endothelial ephrinA1 expression is mediated by a p38MAPK and SAPK/JNK-dependent but NF-kappaB-independent mechanism. Journal of Biological Chemistry 276(17): 13771-13777.
38. Uemura M, Yamamoto H, Takemasa I, Mimori K, Hemmi H, et al. (2010) Jumonji domain containing 1A is a novel prognostic marker for colorectal cancer: in vivo identification from hypoxic tumor cells. Clinical Cancer Research 16(18): 4636-4646.
39. Yamashita T, Ohneda K, Nagano M, Miyoshi C, Kaneko N, et al. (2008) Hypoxia-inducible transcription factor-2α in endothelial cells regulates tumor neovascularization through activation of ephrin A1. Journal of Biological Chemistry 283(27): 18926-18936.
40. Davis S, Gale NW, Aldrich TH, Maisonpierre PC, Lhotak V, et al. (1994) Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266(5186): 816-819.
41. Cui XD, Lee MJ, Yu GR, Kim IH, Yu HC, et al. (2010) EFNA1 ligand and its receptor EphA2: potential biomarkers for hepatocellular carcinoma. Int J Cancer 126(4): 940-949.