NFAT2 regulates COX-2 expression and modulates the integrin repertoire in endothelial cells at the crossroads of angiogenesis and inflammation

Experimental Cell Research

Volumn 324, Issue 2, 2014, Pages 124-136

  Mena, Mari Pau ^a   Papiewska Pajak, Izabela ^a,b   Przygodzka, Patrycja ^a   Kozaczuk, Anna ^a   Boncela, Joanna ^a   Cierniewski, Czeslaw S ^a,b  

^a INSTITUTE OF MEDICAL BIOLOGY   (Poland)

^b MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

Angiogenesis; COX 2; Inflammation; Integrins; NFAT; TNF ; VEGF A

Indexed keywords

CALCINEURIN; CYCLOOXYGENASE 2; CYCLOSPORIN A; INTEGRIN; MESSENGER RNA; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFAT2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANGIOGENESIS; ARTICLE; CELL ADHESION; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; ENDOTHELIUM CELL; GENE EXPRESSION; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; INFLAMMATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

ANGIOGENESIS; COX-2; INFLAMMATION; INTEGRINS; NFAT; TNF-Α; VEGF-A;

CELLS, CULTURED; CYCLOOXYGENASE 2; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; INTEGRINS; NEOVASCULARIZATION, PHYSIOLOGIC; NFATC TRANSCRIPTION FACTORS; TRANSCRIPTOME; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84901191671     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.03.008     Document Type: Article

References (55)

1. Dinarello C.A. Proinflammatory cytokines. Chest 2000, 118:503-508.
2. Hack C.E., Zeerleder S. The endothelium in sepsis: source of and a target for inflammation. Crit. Care Med 2001, 29:21-27.
3. Denk A., Goebeler M., Schmid S., et al. Activation of NF-kappa B via the Ikappa B kinase complex is both essential and sufficient for proinflammatory gene expression in primary endothelial cells. J. Biol. Chem 2001, 276:28451-28458.
4. Winsauer G., de Martin R. Resolution of inflammation: intracellular feedback loops in the endothelium. Thromb. Haemost 2007, 97:364-369.
5. Sica A., Dorman L., Viggiano V., et al. Interaction of NF-κB and NFAT with the interferon-gamma promoter. J. Biol. Chem. 1997, 272:30412-30420.
6. Graef I.A., Chen F., Crabtree G.R. NFAT signaling in vertebrate development. Curr. Opin. Genet. Dev 2001, 11:505-512.
7. de la Pompa J.L., Timmerman L.A., Takimoto H. Role of the NF-Atc transcription factor in morphogenesis of cardiac valves and septum. Nature 1998, 392:182-186.
8. Mercurio A.M., Rabinovitz I. Towards a mechanistic understanding of tumor invasion-lessons from the α6β4 integrin. Semin. Cancer Biol 2001, 11:129-141.
9. Plyte S., Boncristiano M., Fattori E., et al. Identification and characterization of a novel nuclear factor of activated T-cells-1 isoform expressed in mouse brain. J. Biol. Chem 2001, 276:14350-14358.
10. Rinne A., Banach K., Blatter L.A. Regulation of nuclear factor of activated T cells (NFAT) in vascular endothelial cells. J. Mol. Cell Cardiol 2009, 47:400-410.
11. Nilsson L.M., Nilsson-Ohman J., Zetterqvist A.V., et al. Nuclear factor of activated T-cells transcription factors in the vasculature: the good guys or the bad guys?. Curr. Opin. Lipidol 2008, 19:483-490.
12. Jauliac S., López-Rodriguez C., Shaw L.M., et al. The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nat. Cell Biol 2002, 4:540-544.
13. P.G. Hogan, L. Chen, J. Nardone, et al. (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17, 2205-2232.
14. Macian F., Lopez-Rodriguez C., Rao A. Partners in transcription: NFAT and AP-1. Oncogene 2001, 20:2476-2489.
15. Horsley V., Pavlath G.K. NFAT: ubiquitous regulator of cell differentiation and adaptation. J. Cell Biol. 2002, 156:771-774.
16. Vyas D.R., Spangenburg E.E., Braha T.W. GSK-3beta negatively regulates skeletal myotube hypertrophy. Am. J. Physiol. Cell 2002, 283:C545-C551.
17. Zhu J., Shibasaki F., Price R., et al. Intramolecular masking of nuclear import signal on NF-AT4 by casein kinase I and MEKK1. Cell 1998, 93:851-861.
18. Okamura H., Garcia-Rodriguez C., Martinson H., et al. Conserved docking motif for CK1 binding controls the nuclear localization of NFAT1. Mol. Cell Biol 2004, 24:4184-4195.
19. Hernández G.L., Volpert O.V., Iñiguez M.A., et al. Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin A: roles of the nuclear factor of activated T cells and cyclooxygenase 2. J. Exp. Med 2001, 193:607-620.
20. Armesilla A.L., Lorenzo E., Gómez del Arco P., et al. Vascular endothelial growth factor activates nuclear factor of activated T cells in human endothelial cells: a role for tissue factor gene expression. Mol. Cell Biol 1999, 9:2032-2043.
21. Jones M.K., Wang H., Peskar B.M., et al. Inhibition of angiogenesis by nonsteroidal anti-inflammatory drugs: insight into mechanisms and implications for cancer growth and ulcer healing. Nat. Med 1999, 5:1418-1423.
22. Dormond O., Bezzi M., Mariotti A., et al. Prostaglandin E2 promotes integrin αVβ3-dependent endothelial cell adhesion, rac-activation, and spreading through cAMP/PKA-dependent signaling. J. Biol. Chem 2002, 277:45838-45846.
23. Ruegg C., Dormond O., Mariotti A. Endothelial cell integrins and COX- 2: mediators and therapeutic targets of tumor angiogenesis. Biochim. Biophys. Acta 2004, 1654:51-67.
24. Suehiro J., Hamakubo T., Kodama T., et al. Vascular endothelial growth factor activation of endothelial cells is mediated by early growth response-3. Blood 2010, 115:2520-2532.
25. 2+/NFAT. Blood 2002, 99:199-206.
26. boss V., wang X., koppelman L.F., et al. Histamine induces nuclear factor of activated T cell-mediated transcription and Cyclosporin A-Sensitive Interleukin-8 mRNA Expression in Human Umbilical Vein Endothelial Cells. Mol. Pharmacol. 1998, 54:264-272.
27. Nacev B.A., Low W., Huang Z., et al. A calcineurin-independent mechanism of angiogenesis inhibition by a nonimmunosuppressive cyclosporin A analog. J. Pharmacol. Exp. Ther. 2011, 338:466-475.
28. Urso K., Alfranca A., Martínez-Martínez S., et al. NFATc3 regulates the transcription of genes involved in T-cell activation and angiogenesis. Blood 2011, 118:795-803.
29. Crotti T.N., Flannery M., Walsh N.C., et al. NFATc1 regulation of the human β3 integrin promoter in osteoclast differenciation. Gene 2006, 372:92-102.
30. Carman C.V., Springer T.A. Integrin avidity regulation: are changes in affinity and conformation underemphasized?. Curr. Opin. Cell Biol 2003, 15:547-556.
31. Caswell P.T., Vadrevu S., Norman J.C. Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 2009, 10:843-853.
32. Jović M., Naslavsky N., Rapaport D., et al. EHD1 regulates β1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J. Cell Sci. 2007, 120:802-814.
33. Salicioni A.M., Gaultier A., Brownlee C. Low density lipoprotein receptor-related protein-1 promotes beta1 integrin maturation and transport to the cell surface. J. Biol. Chem 2004, 279:10005-10012.
34. De filippi P., Truffa G., Stefanuto G. Tumor necrosis factor α and interferon γ modulate the expression of the vitronectin receptor (integrin β3) in human endothelial cells. J. Biol. Chem 1991, 266:7638-7645.
35. Kim L.T., Yamada K.M. The regulation of expression of integrin receptors. Proc. Soc. Exp. Biol. Med. 1997, 214:123-131.
36. Medhora M.M., Teitelbaum S., Chappel J., et al. 1,25-Dihydroxyvitamin D3 upregulates expression of the osteoclast integrin αVβ3. J. Biol. Chem. 1993, 268:1456-1461.
37. Eligini S., Barbieri S.S., Cavalca V., et al. Diversity and similarity in signaling events leading to rapid Cox-2 induction by tumor necrosis factor-a and phorbol ester in human endothelial cells. Cardiovasc. Res. 2005, 65:683-693.
38. Zaichuk T.A., Shroff E.H., Emmanuel R., et al. Nuclear factor of activated T cells balances angiogenesis activation and inhibition. J. Exp. Med. 2004, 199:1513-1522.
39. Schweighofer B., Testori J., Sturtzel C. The VEGF-induced transcriptional response comprises gene clusters at the crossroad of angiogenesis and inflammation. Thromb. Haemost 2009, 102:544-554.
40. Plow E.F., Haas T.A., Zhang L., et al. Ligand Binding to Integrins. J. Biol. Chem 2000, 275:21785-21788.
41. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat. Med 2003, 9:669-676.
42. Schabbauer G., Schweighofer B., Mechtcheriakova D., et al. Nuclear factor of activated T cells and early growth response-1 cooperate to mediate tissue factor gene induction by vascular endothelial growth factor in endothelial cells. Thromb. Haemost 2007, 97:988-997.
43. Cao Y., Zhang J., Meng X., et al. TNF induces early growth response gene-1 expression via ERK1/2 activation in endothelial cells. Acta Diabetol 2013, 50:27-31.
44. Zeini M., Hang C.T., Lehrer-Graiwer J., et al. Spatial and temporal regulation of coronary vessel formation by calcineurin-NFAT signaling. Development 2009, 136:3335-3345.
45. Friedlander M., Brooks P.C., Shaffer R.W., et al. Definition of two angiogenic pathways by distinct αV integrins. Science 1995, 270:1500-1502.
46. Yiu G.K., Toker A. NFAT induces breast cancer cell invasion by promoting the induction of cyclooxygenase-2. J. Biol. Chem 2006, 281:12210-12217.
47. Menter D.G., Dubois R.N. Prostaglandins in cancer cell adhesion, migration, and invasion. Int. J. Cell Biol. Article ID 2012, 723419:21.
48. Gao B., Saba T.M., Tsan M. Role of αvβ3-integrin in TNF-α-induced endothelial cell Migration. Am. J. Physiol. Cell Physiol. 2002, 283:C1196-C1205.
49. Ruegg C., Dormond O., Mariotti A. Endothelial cell integrins and COX-2: mediators and therapeutic targets of tumor angiogenesis. Biochim. Biophys. Acta 2004, 1654:51-67.
50. Byzova T.V., Goldman C.K., Pampori N., et al. A mechanism for modulation of cellular responses to VEGF. Activation Integrins Mol. Cell 2000, 6:851-860.
51. Bretscher S., Aguado-Velasco C. Membrane traffic during cell locomotion. Curr. Opin. Cell Biol. 1998, 10:537-541.
52. Alfranca A., Lopez-Oliva J.M., Genis L., et al. PGE2 induces angiogenesis via the MT1-MMP-mediated activation of theTGF β/Alk5 signalling pathway. Blood 2008, 112:1120-1128.
53. Evellin S., Galvagni F., Zippo A., et al. FOSL1 controls the assembly of endothelial cells into capillary tubes by direct repression of αv and β3 integrin transcription. Mol. Cell. Biol 2013, 33:1198-1209.
54. Mechtcheriakova D., Schabbauer G., Lucerna M., et al. Specificity, diversity, and convergence in VEGF and TNF-α signaling events leading to Tissue Factor upregulation via EGR-1 in endothelial cells. FASEB J 2001, 15:230-242.
55. Ranger A.M., Oukka M., Rengarajan J., et al. Inhibitory function of two NFAT family members in lymphoid homeo-stasis and Th2 development. Immunity 1998, 9:627-635.