Abstract
Immediate-early genes are those that are rapidly induced in response to a cellular stimulus in the absence of protein synthesis and can influence the biology and pathobiology of the cell. These span transcription factors, cytokines, growth factors, enzymes, secreted factors, cytoskeletal proteins, transporters and anti-apoptotic proteins that are attractive targets for the control of pathologic angiogenesis. This chapter focuses on immediate-early genes and specifically their regulation of processes underpinning angiogenesis.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Sweeney C et al (2001) Growth factor-specific signaling pathway stimulation and gene expression mediated by ErbB receptors. J Biol Chem 276(25):22685–22698
Khachigian LM, Collins T (1997) Inducible expression of Egr-1-dependent genes. A paradigm of transcriptional activation in vascular endothelium. Circ Res 81(4):457–461
Lau LF, Nathans D (1987) Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc. Proc Natl Acad Sci USA 84(5):1182–1186
Healy S, Khan P, Davie JR (2013) Immediate early response genes and cell transformation. Pharmacol Ther 137(1):64–77
Tullai JW et al (2007) Immediate-early and delayed primary response genes are distinct in function and genomic architecture. J Biol Chem 282(33):23981–23995
Herschman HR (1991) Primary response genes induced by growth factors and tumor promoters. Annu Rev Biochem 60:281–319
O’Donnell A, Odrowaz Z, Sharrocks AD (2012) Immediate-early gene activation by the MAPK pathways: what do and don’t we know? Biochem Soc Trans 40(1):58–66
McKay MM, Morrison DK (2007) Integrating signals from RTKs to ERK/MAPK. Oncogene 26(22):3113–3121
Dunn KL et al (2005) The Ras-MAPK signal transduction pathway, cancer and chromatin remodeling. Biochem Cell Biol 83(1):1–14
Yang SH, Sharrocks AD, Whitmarsh AJ (2003) Transcriptional regulation by the MAP kinase signaling cascades. Gene 320:3–21
Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438(7070):932–936
Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407(6801):249–257
Hanahan D, Folkman J (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86(3):353–364
Ferrara N, Kerbel RS (2005) Angiogenesis as a therapeutic target. Nature 438(7070):967–974
O’Donovan KJ et al (1999) The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci 22(4):167–173
Madden SL, Rauscher FJ 3rd (1993) Positive and negative regulation of transcription and cell growth mediated by the EGR family of zinc-finger gene products. Ann N Y Acad Sci 684:75–84
Gashler A, Sukhatme VP (1995) Early growth response protein 1 (Egr-1): prototype of a zinc-finger family of transcription factors. Prog Nucleic Acid Res Mol Biol 50:191–224
Cao XM et al (1990) Identification and characterization of the Egr-1 gene product, a DNA-binding zinc finger protein induced by differentiation and growth signals. Mol Cell Biol 10(5):1931–1939
Khachigian LM et al (1997) Egr-1 is activated in endothelial cells exposed to fluid shear stress and interacts with a novel shear-stress-response element in the PDGF A-chain promoter. Arterioscler Thromb Vasc Biol 17(10):2280–2286
Lee SL et al (1996) Luteinizing hormone deficiency and female infertility in mice lacking the transcription factor NGFI-A (Egr-1). Science 273(5279):1219–1221
Silverman ES, Collins T (1999) Pathways of Egr-1-mediated gene transcription in vascular biology. Am J Pathol 154(3):665–670
Lucerna M et al (2003) NAB2, a corepressor of EGR-1, inhibits vascular endothelial growth factor-mediated gene induction and angiogenic responses of endothelial cells. J Biol Chem 278(13):11433–11440
Kundumani-Sridharan V et al (2010) 15(S)-hydroxyeicosatetraenoic acid-induced angiogenesis requires Src-mediated Egr-1-dependent rapid induction of FGF-2 expression. Blood 115(10):2105–2116
Szabo IL et al (2001) NSAIDs inhibit the activation of egr-1 gene in microvascular endothelial cells. A key to inhibition of angiogenesis? J Physiol Paris 95(1–6):379–383
Worden B et al (2005) Hepatocyte growth factor/scatter factor differentially regulates expression of proangiogenic factors through Egr-1 in head and neck squamous cell carcinoma. Cancer Res 65(16):7071–7080
Abdel-Malak NA et al (2009) Early growth response-1 regulates angiopoietin-1-induced endothelial cell proliferation, migration, and differentiation. Arterioscler Thromb Vasc Biol 29(2):209–216
Fahmy RG et al (2003) Transcription factor Egr-1 supports FGF-dependent angiogenesis during neovascularization and tumor growth. Nat Med 9(8):1026–1032
Abe M, Sato Y (2001) cDNA microarray analysis of the gene expression profile of VEGF-activated human umbilical vein endothelial cells. Angiogenesis 4(4):289–298
Suehiro J et al (2010) Vascular endothelial growth factor activation of endothelial cells is mediated by early growth response-3. Blood 115(12):2520–2532
Patwardhan S et al (1991) EGR3, a novel member of the Egr family of genes encoding immediate-early transcription factors. Oncogene 6(6):917–928
Liu D et al (2008) The zinc-finger transcription factor, early growth response 3, mediates VEGF-induced angiogenesis. Oncogene 27(21):2989–2998
Moll UM, Marchenko N, Zhang XK (2006) p53 and Nur77/TR3 – transcription factors that directly target mitochondria for cell death induction. Oncogene 25(34):4725–4743
Liu D et al (2003) Vascular endothelial growth factor-regulated gene expression in endothelial cells: KDR-mediated induction of Egr3 and the related nuclear receptors Nur77, Nurr1, and Nor1. Arterioscler Thromb Vasc Biol 23(11):2002–2007
Ha CH et al (2008) Protein kinase D-dependent phosphorylation and nuclear export of histone deacetylase 5 mediates vascular endothelial growth factor-induced gene expression and angiogenesis. J Biol Chem 283(21):14590–14599
Zeng H et al (2006) Orphan nuclear receptor TR3/Nur77 regulates VEGF-A-induced angiogenesis through its transcriptional activity. J Exp Med 203(3):719–729
Arkenbout EK et al (2003) TR3 orphan receptor is expressed in vascular endothelial cells and mediates cell cycle arrest. Arterioscler Thromb Vasc Biol 23(9):1535–1540
Qin L et al (2013) The vascular permeabilizing factors histamine and serotonin induce angiogenesis through TR3/Nur77 and subsequently truncate it through thrombospondin-1. Blood 121(11):2154–2164
Zhao D et al (2011) Orphan nuclear transcription factor TR3/Nur77 regulates microvessel permeability by targeting endothelial nitric oxide synthase and destabilizing endothelial junctions. Proc Natl Acad Sci USA 108(29):12066–12071
Eferl R, Wagner EF (2003) AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3(11):859–868
Shaulian E, Karin M (2001) AP-1 in cell proliferation and survival. Oncogene 20(19):2390–2400
Shaulian E, Karin M (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4(5):E131–E136
Angel P, Karin M (1991) The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim Biophys Acta 1072(2–3):129–157
Vleugel MM et al (2006) c-Jun activation is associated with proliferation and angiogenesis in invasive breast cancer. Hum Pathol 37(6):668–674
Kraemer M et al (1999) Rat embryo fibroblasts transformed by c-Jun display highly metastatic and angiogenic activities in vivo and deregulate gene expression of both angiogenic and antiangiogenic factors. Cell Growth Differ 10(3):193–200
Michel JB et al (1994) Biphasic induction of immediate early gene expression accompanies activity-dependent angiogenesis and myofiber remodeling of rabbit skeletal muscle. J Clin Invest 94(1):277–285
Jiao X et al (2008) Disruption of c-Jun reduces cellular migration and invasion through inhibition of c-Src and hyperactivation of ROCK II kinase. Mol Biol Cell 19(4):1378–1390
Katiyar S et al (2007) Somatic excision demonstrates that c-Jun induces cellular migration and invasion through induction of stem cell factor. Mol Cell Biol 27(4):1356–1369
Giles N et al (2008) A peptide inhibitor of c-Jun promotes wound healing in a mouse full-thickness burn model. Wound Repair Regen 16(1):58–64
Zhang G et al (2004) Effect of deoxyribozymes targeting c-Jun on solid tumor growth and angiogenesis in rodents. J Natl Cancer Inst 96(9):683–696
Fahmy RG et al (2006) Suppression of vascular permeability and inflammation by targeting of the transcription factor c-Jun. Nat Biotechnol 24(7):856–863
Cai H et al (2012) DNAzyme targeting c-jun suppresses skin cancer growth. Sci Transl Med 4(139):139ra82
Marconcini L et al (1999) c-Fos-induced growth factor/vascular endothelial growth factor D induces angiogenesis in vivo and in vitro. Proc Natl Acad Sci USA 96(17):9671–9676
Saez E et al (1995) c-Fos is required for malignant progression of skin tumors. Cell 82(5):721–732
Lai HC et al (2004) Effect of EGCG, a major component of green tea, on the expression of Ets-1, c-Fos, and c-Jun during angiogenesis in vitro. Cancer Lett 213(2):181–188
Belguise K et al (2005) FRA-1 expression level regulates proliferation and invasiveness of breast cancer cells. Oncogene 24(8):1434–1444
Kustikova O et al (1998) Fra-1 induces morphological transformation and increases in vitro invasiveness and motility of epithelioid adenocarcinoma cells. Mol Cell Biol 18(12):7095–7105
Hilfiker-Kleiner D et al (2005) Lack of JunD promotes pressure overload-induced apoptosis, hypertrophic growth, and angiogenesis in the heart. Circulation 112(10):1470–1477
Schmidt D et al (2007) Critical role for NF-kappaB-induced JunB in VEGF regulation and tumor angiogenesis. EMBO J 26(3):710–719
Brown PH, Chen TK, Birrer MJ (1994) Mechanism of action of a dominant-negative mutant of c-Jun. Oncogene 9(3):791–799
Kang MI et al (2012) Targeting of noncanonical Wnt5a signaling by AP-1 blocker dominant-negative Jun when it inhibits skin carcinogenesis. Genes Cancer 3(1):37–50
Andersen H et al (2005) Immediate and delayed effects of E-cadherin inhibition on gene regulation and cell motility in human epidermoid carcinoma cells. Mol Cell Biol 25(20):9138–9150
Shiratsuchi T, Ishibashi H, Shirasuna K (2002) Inhibition of epidermal growth factor-induced invasion by dexamethasone and AP-1 decoy in human squamous cell carcinoma cell lines. J Cell Physiol 193(3):340–348
Weber WM et al (2006) TPA-induced up-regulation of activator protein-1 can be inhibited or enhanced by analogs of the natural product curcumin. Biochem Pharmacol 72(8):928–940
Matsuo M et al (2007) Curcumin inhibits the formation of capillary-like tubes by rat lymphatic endothelial cells. Cancer Lett 251(2):288–295
Tsuchida K et al (2004) Design, synthesis, and biological evaluation of new cyclic disulfide decapeptides that inhibit the binding of AP-1 to DNA. J Med Chem 47(17):4239–4246
Tsuchida K et al (2006) Discovery of nonpeptidic small-molecule AP-1 inhibitors: lead hopping based on a three-dimensional pharmacophore model. J Med Chem 49(1):80–91
Ruocco KM et al (2007) A high-throughput cell-based assay to identify specific inhibitors of transcription factor AP-1. J Biomol Screen 12(1):133–139
Aikawa Y et al (2008) Treatment of arthritis with a selective inhibitor of c-Fos/activator protein-1. Nat Biotechnol 26(7):817–823
Hai T et al (1999) ATF3 and stress responses. Gene Expr 7(4–6):321–335
Volpert OV et al (2002) Id1 regulates angiogenesis through transcriptional repression of thrombospondin-1. Cancer Cell 2(6):473–483
Nawa T et al (2002) Expression of transcriptional repressor ATF3/LRF1 in human atherosclerosis: colocalization and possible involvement in cell death of vascular endothelial cells. Atherosclerosis 161(2):281–291
Okamoto A, Iwamoto Y, Maru Y (2006) Oxidative stress-responsive transcription factor ATF3 potentially mediates diabetic angiopathy. Mol Cell Biol 26(3):1087–1097
Nesbit CE, Tersak JM, Prochownik EV (1999) MYC oncogenes and human neoplastic disease. Oncogene 18(19):3004–3016
Shanmugham R et al (2004) Tumour angiogenesis and C-myc expression in breast carcinomas. Indian J Pathol Microbiol 47(3):340–342
Fodinger M et al (2000) Erythropoietin-inducible immediate-early genes in human vascular endothelial cells. J Investig Med 48(2):137–149
Baudino TA et al (2002) c-Myc is essential for vasculogenesis and angiogenesis during development and tumor progression. Genes Dev 16(19):2530–2543
Souders CA et al (2012) c-Myc is required for proper coronary vascular formation via cell- and gene-specific signaling. Arterioscler Thromb Vasc Biol 32(5):1308–1319
Ngo CV et al (2000) An in vivo function for the transforming Myc protein: elicitation of the angiogenic phenotype. Cell Growth Differ 11(4):201–210
Janz A et al (2000) Activation of the myc oncoprotein leads to increased turnover of thrombospondin-1 mRNA. Nucleic Acids Res 28(11):2268–2275
Dews M et al (2006) Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38(9):1060–1065
Lelievre E et al (2001) The Ets family contains transcriptional activators and repressors involved in angiogenesis. Int J Biochem Cell Biol 33(4):391–407
Hashiya N et al (2004) In vivo evidence of angiogenesis induced by transcription factor Ets-1: Ets-1 is located upstream of angiogenesis cascade. Circulation 109(24):3035–3041
Sato Y (1998) Transcription factor ETS-1 as a molecular target for angiogenesis inhibition. Hum Cell 11(4):207–214
Iwasaka C et al (1996) Ets-1 regulates angiogenesis by inducing the expression of urokinase-type plasminogen activator and matrix metalloproteinase-1 and the migration of vascular endothelial cells. J Cell Physiol 169(3):522–531
Oettgen P (2010) The role of ets factors in tumor angiogenesis. J Oncol 2010:767384
Wei G et al (2009) Ets1 and Ets2 are required for endothelial cell survival during embryonic angiogenesis. Blood 114(5):1123–1130
Pesce S, Benezra R (1993) The loop region of the helix-loop-helix protein Id1 is critical for its dominant-negative activity. Mol Cell Biol 13(12):7874–7880
Lyden D et al (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401(6754):670–677
Ling MT et al (2005) Overexpression of Id-1 in prostate cancer cells promotes angiogenesis through the activation of vascular endothelial growth factor (VEGF). Carcinogenesis 26(10):1668–1676
Mellick AS et al (2010) Using the transcription factor inhibitor of DNA binding 1 to selectively target endothelial progenitor cells offers novel strategies to inhibit tumor angiogenesis and growth. Cancer Res 70(18):7273–7282
Nurrish SJ, Treisman R (1995) DNA-binding specificity determinants in mads-box transcription factors. Mol Cell Biol 15(8):4076–4085
Vialou V et al (2012) Serum response factor and camp response element binding protein are both required for cocaine induction of delta FosB. J Neurosci 32(22):7577–7584
Lee SM, Vasishtha M, Prywes R (2010) Activation and repression of cellular immediate early genes by serum response factor cofactors. J Biol Chem 285(29):22036–22049
Chai J, Jones MK, Tarnawski AS (2004) Serum response factor is a critical requirement for VEGF signaling in endothelial cells and VEGF-induced angiogenesis. FASEB J 18(11):1264–1266
Franco CA et al (2008) Serum response factor is required for sprouting angiogenesis and vascular integrity. Dev Cell 15(3):448–461
Schratt G et al (2001) Serum response factor is required for immediate-early gene activation yet is dispensable for proliferation of embryonic stem cells. Mol Cell Biol 21(8):2933–2943
Qiao Y et al (2011) MiR-483-5p controls angiogenesis in vitro and targets serum response factor. FEBS Lett 585(19):3095–3100
Chang LH et al (2012) Role of macrophage CCAAT/enhancer binding protein delta in the pathogenesis of rheumatoid arthritis in collagen-induced arthritic mice. PLoS One 7(9):e45378
Min Y et al (2011) C/EBP-delta regulates VEGF-C autocrine signaling in lymphangiogenesis and metastasis of lung cancer through HIF-1alpha. Oncogene 30(49):4901–4909
Gabay C (2006) Interleukin-6 and chronic inflammation. Arthritis Res Ther 8:S3
Li W et al (2001) Global changes in interleukin-6-dependent gene expression patterns in mouse livers after partial hepatectomy. Hepatology 33(6):1377–1386
Cohen T et al (1996) Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem 271(2):736–741
Huang SP et al (2004) Interleukin-6 increases vascular endothelial growth factor and angiogenesis in gastric carcinoma. J Biomed Sci 11(4):517–527
Koch AE et al (1992) Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 258(5089):1798–1801
Bancroft CC et al (2001) Coexpression of proangiogenic factors IL-8 and VEGF by human head and neck squamous cell carcinoma involves coactivation by MEK-MAPK and IKK-NF-kappaB signal pathways. Clin Cancer Res 7(2):435–442
Huang S et al (2002) Fully humanized neutralizing antibodies to interleukin-8 (ABX-IL8) inhibit angiogenesis, tumor growth, and metastasis of human melanoma. Am J Pathol 161(1):125–134
Florczyk U et al (2011) Opposite effects of HIF-1alpha and HIF-2alpha on the regulation of IL-8 expression in endothelial cells. Free Radic Biol Med 51(10):1882–1892
Nishida T et al (2007) CCN2 (connective tissue growth factor) is essential for extracellular matrix production and integrin signaling in chondrocytes. J Cell Commun Signal 1(1):45–58
Hall-Glenn F et al (2012) CCN2/connective tissue growth factor is essential for pericyte adhesion and endothelial basement membrane formation during angiogenesis. PLoS One 7(2):e30562
Markiewicz M et al (2011) Connective tissue growth factor (CTGF/CCN2) mediates angiogenic effect of S1P in human dermal microvascular endothelial cells. Microcirculation 18(1):1–11
Brigstock DR (2002) Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis 5(3):153–165
Suzuma K et al (2000) Vascular endothelial growth factor induces expression of connective tissue growth factor via KDR, Flt1, and phosphatidylinositol 3-kinase-akt-dependent pathways in retinal vascular cells. J Biol Chem 275(52):40725–40731
Inoki I et al (2002) Connective tissue growth factor binds vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis. FASEB J 16(2):219–221
Hashimoto G et al (2002) Matrix metalloproteinases cleave connective tissue growth factor and reactivate angiogenic activity of vascular endothelial growth factor 165. J Biol Chem 277(39):36288–36295
Kondo S et al (2002) Connective tissue growth factor increased by hypoxia may initiate angiogenesis in collaboration with matrix metalloproteinases. Carcinogenesis 23(5):769–776
Aikawa T et al (2006) Connective tissue growth factor-specific antibody attenuates tumor growth, metastasis, and angiogenesis in an orthotopic mouse model of pancreatic cancer. Mol Cancer Ther 5(5):1108–1116
Nantel F et al (1999) Distribution and regulation of cyclooxygenase-2 in carrageenan-induced inflammation. Br J Pharmacol 128(4):853–859
Tsujii M et al (1998) Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 93(5):705–716
Gately S (2000) The contributions of cyclooxygenase-2 to tumor angiogenesis. Cancer Metastasis Rev 19(1–2):19–27
Iniguez MA et al (2003) Cyclooxygenase-2: a therapeutic target in angiogenesis. Trends Mol Med 9(2):73–78
Taylor DM et al (2013) MAP kinase phosphatase 1 (MKP-1/DUSP1) is neuroprotective in Huntington’s disease via additive effects of JNK and p38 inhibition. J Neurosci 33(6):2313–2325
Denkert C et al (2002) Expression of mitogen-activated protein kinase phosphatase-1 (MKP-1) in primary human ovarian carcinoma. Int J Cancer 102(5):507–513
Kinney CM et al (2008) VEGF and thrombin induce MKP-1 through distinct signaling pathways: role for MKP-1 in endothelial cell migration. Am J Physiol Cell Physiol 294(1):C241–C250
Moncho-Amor V et al (2011) DUSP1/MKP1 promotes angiogenesis, invasion and metastasis in non-small-cell lung cancer. Oncogene 30(6):668–678
Song HY, Rothe M, Goeddel DV (1996) The tumor necrosis factor-inducible zinc finger protein A20 interacts with TRAF1/TRAF2 and inhibits NF-kappaB activation. Proc Natl Acad Sci USA 93(13):6721–6725
Opipari AW, Boguski MS, Dixit VM (1990) The A20 cDNA induced by tumor necrosis factor-alpha encodes a novel type of zinc finger protein. J Biol Chem 265(25):14705–14708
Elsby LM et al (2010) Functional evaluation of TNFAIP3 (A20) in rheumatoid arthritis. Clin Exp Rheumatol 28(5):708–714
Chng HW et al (2006) A new role for the anti-apoptotic gene A20 in angiogenesis. Exp Cell Res 312(15):2897–2907
Daniel S et al (2004) A20 protects endothelial cells from TNF-, Fas-, and NK-mediated cell death by inhibiting caspase 8 activation. Blood 104(8):2376–2384
Balsara RD, Castellino FJ, Ploplis VA (2006) A novel function of plasminogen activator inhibitor-1 in modulation of the AKT pathway in wild-type and plasminogen activator inhibitor-1-deficient endothelial cells. J Biol Chem 281(32):22527–22536
Lakka SS et al (2005) Specific interference of urokinase-type plasminogen activator receptor and matrix metalloproteinase-9 gene expression induced by double-stranded RNA results in decreased invasion, tumor growth, and angiogenesis in gliomas. J Biol Chem 280(23):21882–21892
Soncin F et al (2003) VE-statin, an endothelial repressor of smooth muscle cell migration. EMBO J 22(21):5700–5711
Nichol D et al (2010) Impaired angiogenesis and altered Notch signaling in mice overexpressing endothelial Egfl7. Blood 116(26):6133–6143
Campagnolo L et al (2005) EGFL7 is a chemoattractant for endothelial cells and is up-regulated in angiogenesis and arterial injury. Am J Pathol 167(1):275–284
Parker LH et al (2004) The endothelial-cell-derived secreted factor Egfl7 regulates vascular tube formation. Nature 428(6984):754–758
Babic AM et al (1998) CYR61, a product of a growth factor-inducible immediate early gene, promotes angiogenesis and tumor growth. Proc Natl Acad Sci USA 95(11):6355–6360
Fataccioli V et al (2002) Stimulation of angiogenesis by Cyr61 gene: a new therapeutic candidate. Hum Gene Ther 13(12):1461–1470
Mo FE et al (2002) CYR61 (CCN1) is essential for placental development and vascular integrity. Mol Cell Biol 22(24):8709–8720
Mo FE, Lau LF (2006) The matricellular protein CCN1 is essential for cardiac development. Circ Res 99(9):961–969
Airley RE, Mobasheri A (2007) Hypoxic regulation of glucose transport, anaerobic metabolism and angiogenesis in cancer: novel pathways and targets for anticancer therapeutics. Chemotherapy 53(4):233–256
Tsukioka M et al (2007) Expression of glucose transporters in epithelial ovarian carcinoma: correlation with clinical characteristics and tumor angiogenesis. Oncol Rep 18(2):361–367
Mimura I et al (2012) Dynamic change of chromatin conformation in response to hypoxia enhances the expression of GLUT3 (SLC2A3) by cooperative interaction of hypoxia-inducible factor 1 and KDM3A. Mol Cell Biol 32(15):3018–3032
Regard JB et al (2004) Verge: a novel vascular early response gene. J Neurosci 24(16):4092–4103
Maallem S et al (2008) Gene expression profiling in brain following acute systemic hypertonicity: novel genes possibly involved in osmoadaptation. J Neurochem 105(4):1198–1211
Liu F et al (2012) Loss of vascular early response gene reduces edema formation after experimental stroke. Exp Transl Stroke Med 4(1):12
Sun HL et al (2009) EPOX inhibits angiogenesis by degradation of Mcl-1 through ERK inactivation. Clin Cancer Res 15(15):4904–4914
Abbott A (2002) On the offensive. Nature 416(6880):470–474
Gibbs JB (2000) Mechanism-based target identification and drug discovery in cancer research. Science 287(5460):1969–1973
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Wien
About this chapter
Cite this chapter
Prado-Lourenço, L., Alhendi, A.M.N., Khachigian, L.M. (2013). Insights into Roles of Immediate-Early Genes in Angiogenesis. In: Dulak, J., Józkowicz, A., Łoboda, A. (eds) Angiogenesis and Vascularisation. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1428-5_7
Download citation
DOI: https://doi.org/10.1007/978-3-7091-1428-5_7
Published:
Publisher Name: Springer, Vienna
Print ISBN: 978-3-7091-1427-8
Online ISBN: 978-3-7091-1428-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)