Hyperglycemia and redox status regulate RUNX2 DNA-binding and an angiogenic phenotype in endothelial cells

Microvascular Research - Tập 97 - Trang 55-64 - 2015
Maria T. Mochin1,2,3,4, Karen F. Underwood1,2,3,4, Brandon Cooper1,2,3,4, John C. McLenithan1,2,3,4, Adam D. Pierce1,2,3,4, Cesar Nalvarte1,2,3,4, Jack Arbiser5,6, Anna I. Karlsson5,6, Alexander R. Moise7, Jackob Moskovitz7, Antonino Passaniti1,2,3,4,8
1Department of Pathology, The University of Maryland School of Medicine, Baltimore, MD 21201, USA
2Department of Biochemistry & Molecular Biology, The University of Maryland School of Medicine, Baltimore, MD 21201, USA
3Department of Medicine, The University of Maryland School of Medicine, Baltimore, MD 21201, USA
4Marlene & Stewart Greenebaum Cancer Center, The University of Maryland School of Medicine, Baltimore, MD 21201, USA
5Department of Dermatology, Emory University, Atlanta, GA, USA
6Atlanta Veterans Administration Medical Center, Atlanta, GA, USA
7Department of Pharmacology and Toxicology, University of Kansas, Lawrence, KS 66045, USA
8The Veteran's Health Administration Research & Development Service, Baltimore, MD, USA

Tài liệu tham khảo

Agbas, 2009, The role of methionine oxidation/reduction in the regulation of immune response, Curr. Signal Transduct. Ther., 4, 46, 10.2174/157436209787048748 Akamatsu, 1997, A simple screening for mutant DNA binding proteins: application to murine transcription factor PEBP2alpha subunit, a founding member of the Runt domain protein family, Gene, 185, 111, 10.1016/S0378-1119(96)00644-0 Aronson, 2008, Hyperglycemia and the pathobiology of diabetic complications, Adv. Cardiol., 45, 1, 10.1159/000115118 Blyth, 2005, The RUNX genes: gain or loss of function in cancer, Nat. Rev. Cancer, 5, 376, 10.1038/nrc1607 Brash, 2002, New careers for antioxidants, Proc. Natl. Acad. Sci. U. S. A., 99, 13969, 10.1073/pnas.232574399 Brautigam, 2013, Glutaredoxin regulates vascular development by reversible glutathionylation of sirtuin 1, Proc. Natl. Acad. Sci. U. S. A., 110, 20057, 10.1073/pnas.1313753110 Bronckers, 2005, Expression of Runx2/Cbfa1/Pebp2alphaA during angiogenesis in postnatal rodent and fetal human orofacial tissues, J. Bone Miner. Res., 20, 428, 10.1359/JBMR.041118 Brownlee, 2001, Biochemistry and molecular cell biology of diabetic complications, Nature, 414, 813, 10.1038/414813a Cao, 2013, Angiogenesis and vascular functions in modulation of obesity, adipose metabolism, and insulin sensitivity, Cell Metab., 18, 478, 10.1016/j.cmet.2013.08.008 Cao, 2014, VEGF-targeted cancer therapeutics-paradoxical effects in endocrine organs, Nat. Rev. Endocrinol., 10, 530, 10.1038/nrendo.2014.114 Cao, 2010, Optimizing the delivery of cancer drugs that block angiogenesis, Sci. Transl. Med., 2, 15ps3, 10.1126/scitranslmed.3000399 Cao, 2011, Forty-year journey of angiogenesis translational research, Sci. Transl. Med., 3, 114rv3, 10.1126/scitranslmed.3003149 Counter, 1998, Telomerase activity is restored in human cells by ectopic expression of hTERT (hEST2), the catalytic subunit of telomerase, Oncogene, 16, 1217, 10.1038/sj.onc.1201882 De Luca, 2010, Methionine sulfoxide reductase A down-regulation in human breast cancer cells results in a more aggressive phenotype, Proc. Natl. Acad. Sci. U. S. A., 107, 18628, 10.1073/pnas.1010171107 D'Souza, 2009, Hyperglycemia regulates RUNX2 activation and cellular wound healing through the aldose reductase polyol pathway, J. Biol. Chem., 284, 17947, 10.1074/jbc.M109.002378 Fomenko, 2009, MsrB1 (methionine-R-sulfoxide reductase 1) knock-out mice: roles of MsrB1 in redox regulation and identification of a novel selenoprotein form, J. Biol. Chem., 284, 5986, 10.1074/jbc.M805770200 Fowlkes, 2008, Runt-related transcription factor 2 (RUNX2) and RUNX2-related osteogenic genes are down-regulated throughout osteogenesis in type 1 diabetes mellitus, Endocrinology, 149, 1697, 10.1210/en.2007-1408 Gius, 2004, Redox-sensitive signaling factors and antioxidants: how tumor cells respond to ionizing radiation, J. Nutr., 134, 3213S, 10.1093/jn/134.11.3213S Glotzer, 2008, Impaired skin and hair follicle development in Runx2 deficient mice, Dev. Biol., 315, 459, 10.1016/j.ydbio.2008.01.005 Hamanaka, 2010, Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes, Trends Biochem. Sci., 35, 505, 10.1016/j.tibs.2010.04.002 Hanson, 2005, Redox factor 1 (Ref-1) enhances specific DNA binding of p53 by promoting p53 tetramerization, Oncogene, 24, 1641, 10.1038/sj.onc.1208351 Jones, 2008, Radical-free biology of oxidative stress, Am. J. Physiol. Cell Physiol., 295, C849, 10.1152/ajpcell.00283.2008 Juttner, 2007, High-dose estrogen-induced osteogenesis is decreased in aged RUNX2(+/−) mice, Bone, 41, 25, 10.1016/j.bone.2007.03.012 Kim, 2006, Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms, Circulation, 113, 1888, 10.1161/CIRCULATIONAHA.105.563213 Kohen, 2002, Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification, Toxicol. Pathol., 30, 620, 10.1080/01926230290166724 Komori, 1997, Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts [see comments], Cell, 89, 755, 10.1016/S0092-8674(00)80258-5 Kurokawa, 1996, A conserved cysteine residue in the runt homology domain of AML1 is required for the DNA binding ability and the transforming activity on fibroblasts, J. Biol. Chem., 271, 16870, 10.1074/jbc.271.28.16870 Lass, 1998, Caloric restriction prevents age-associated accrual of oxidative damage to mouse skeletal muscle mitochondria, Free Radic. Biol. Med., 25, 1089, 10.1016/S0891-5849(98)00144-0 Lei, 2007, Identification of MSRA gene on chromosome 8p as a candidate metastasis suppressor for human hepatitis B virus-positive hepatocellular carcinoma, BMC Cancer, 7, 172, 10.1186/1471-2407-7-172 Leto, 2006, Role of Nox family NADPH oxidases in host defense, Antioxid. Redox Signal., 8, 1549, 10.1089/ars.2006.8.1549 Lu, 2003, Diabetes interferes with the bone formation by affecting the expression of transcription factors that regulate osteoblast differentiation, Endocrinology, 144, 346, 10.1210/en.2002-220072 Miki, 2012, Regulation of intracellular signalling through cysteine oxidation by reactive oxygen species, J. Biochem., 151, 255, 10.1093/jb/mvs006 Moskovitz, 2005, Methionine sulfoxide reductases: ubiquitous enzymes involved in antioxidant defense, protein regulation, and prevention of aging-associated diseases, Biochim. Biophys. Acta, 1703, 213, 10.1016/j.bbapap.2004.09.003 Moskovitz, 1995, Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage, J. Bacteriol., 177, 502, 10.1128/jb.177.3.502-507.1995 Moskovitz, 2000, Identification and characterization of a putative active site for peptide methionine sulfoxide reductase (MsrA) and its substrate stereospecificity, J. Biol. Chem., 275, 14167, 10.1074/jbc.275.19.14167 Moskovitz, 2001, Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals, Proc. Natl. Acad. Sci. U. S. A., 98, 12920, 10.1073/pnas.231472998 Moskovitz, 2002, Purification and characterization of methionine sulfoxide reductases from mouse and Staphylococcus aureus and their substrate stereospecificity, Biochem. Biophys. Res. Commun., 290, 62, 10.1006/bbrc.2001.6171 Namba, 2000, Indispensable role of the transcription factor PEBP2/CBF in angiogenic activity of a murine endothelial cell MSS31, Oncogene, 19, 106, 10.1038/sj.onc.1203257 Nomura, 2009, Oxidation of methionine residue at hydrophobic core destabilizes p53 tetrameric structure, Biopolymers, 91, 78, 10.1002/bip.21084 Oien, 2008, Substrates of the methionine sulfoxide reductase system and their physiological relevance, Curr. Top. Dev. Biol., 80, 93, 10.1016/S0070-2153(07)80003-2 Oien, 2008, MsrA knockout mouse exhibits abnormal behavior and brain dopamine levels, Free Radic. Biol. Med., 45, 193, 10.1016/j.freeradbiomed.2008.04.003 Oien, 2009, Detection of oxidized methionine in selected proteins, cellular extracts and blood serums by novel anti-methionine sulfoxide antibodies, Arch. Biochem. Biophys., 485, 35, 10.1016/j.abb.2009.01.020 Oien, 2009, Clearance and phosphorylation of alpha-synuclein are inhibited in methionine sulfoxide reductase a null yeast cells, J. Mol. Neurosci., 39, 323, 10.1007/s12031-009-9274-8 Oien, 2010, Caloric restriction alleviates abnormal locomotor activity and dopamine levels in the brain of the methionine sulfoxide reductase A knockout mouse, Neurosci. Lett., 468, 38, 10.1016/j.neulet.2009.10.058 Ortiz, 2011, Quantification of reserve pool dopamine in methionine sulfoxide reductase A null mice, Neuroscience, 177, 223, 10.1016/j.neuroscience.2011.01.001 Pierce, 2012, Glucose-activated RUNX2 phosphorylation promotes endothelial cell proliferation and an angiogenic phenotype, J. Cell. Biochem., 113, 218, 10.1002/jcb.23354 Pili, 1994, Altered angiogenesis underlying age-dependent changes in tumor growth, J. Natl. Cancer Inst., 86, 1303, 10.1093/jnci/86.17.1303 Potente, 2011, Basic and therapeutic aspects of angiogenesis, Cell, 146, 873, 10.1016/j.cell.2011.08.039 Qiao, 2004, Insulin-like growth factor-1 regulates endogenous RUNX2 activity in endothelial cells through a PI3K/ERK-dependent and Akt-independent signaling pathway, J. Biol. Chem., 279, 42709, 10.1074/jbc.M404480200 Qiao, 2006, Cell cycle-dependent phosphorylation of the RUNX2 transcription factor by cdc2 regulates endothelial cell proliferation, J. Biol. Chem., 281, 7118, 10.1074/jbc.M508162200 Qutub, 2008, Reactive oxygen species regulate hypoxia-inducible factor 1alpha differentially in cancer and ischemia, Mol. Cell. Biol., 28, 5106, 10.1128/MCB.00060-08 Renard, 2001, Development of a sensitive multi-well colorimetric assay for active NFkappaB, Nucleic Acids Res., 29, E21, 10.1093/nar/29.4.e21 Sato, 2003, Molecular diagnosis of tumor angiogenesis and anti-angiogenic cancer therapy, Int. J. Clin. Oncol., 8, 200, 10.1007/s10147-003-0342-8 Sohal, 1998, Role of oxidative stress in senescence, Aging (Milano), 10, 149 Srivastava, 2005, Role of aldose reductase and oxidative damage in diabetes and the consequent potential for therapeutic options, Endocr. Rev., 26, 380, 10.1210/er.2004-0028 Stadtman, 2003, Oxidation of methionine residues of proteins: biological consequences, Antioxid. Redox Signal., 5, 577, 10.1089/152308603770310239 Stadtman, 2005, Methionine oxidation and aging, Biochim. Biophys. Acta, 1703, 135, 10.1016/j.bbapap.2004.08.010 Sun, 2001, Runt-related gene 2 in endothelial cells: inducible expression and specific regulation of cell migration and invasion, Cancer Res., 61, 4994 Sun, 2004, Regulation of TGFß1-mediated growth inhibition and apoptosis by RUNX2 isoforms, Oncogene, 23, 4722, 10.1038/sj.onc.1207589 Sundaresan, 1996, Regulation of reactive-oxygen-species generation in fibroblasts by Rac1, Biochem. J., 318, 379, 10.1042/bj3180379 Tahirov, 2001, Structural analyses of DNA recognition by the AML1/Runx-1 Runt domain and its allosteric control by CBFbeta, Cell, 104, 755, 10.1016/S0092-8674(01)00271-9 Tsuji, 2004, Aged mice require full transcription factor, Runx2/Cbfa1, gene dosage for cancellous bone regeneration after bone marrow ablation, J. Bone Miner. Res., 19, 1481, 10.1359/JBMR.040601 Underwood, 2012, Regulation of RUNX2 transcription factor-DNA interactions and cell proliferation by Vitamin D3 (cholecalciferol) prohormone activity, J. Bone Miner. Res., 27, 913, 10.1002/jbmr.1504 Underwood, 2013, A quantitative assay to study protein:DNA interactions, discover transcriptional regulators of gene expression, and identify novel anti-tumor agents, J. Vis. Exp., 10.3791/50512 Vitolo, 2007, The RUNX2 transcription factor cooperates with the YES-associated protein, YAP65, to promote cell transformation, Cancer Biol. Ther., 6, 856, 10.4161/cbt.6.6.4241 Weissbach, 2005, Methionine sulfoxide reductases: history and cellular role in protecting against oxidative damage, Biochim. Biophys. Acta, 1703, 203, 10.1016/j.bbapap.2004.10.004 Winterbourn, 2008, Thiol chemistry and specificity in redox signaling, Free Radic. Biol. Med., 45, 549, 10.1016/j.freeradbiomed.2008.05.004 Wood, 2003, Biomarkers of lipid peroxidation, airway inflammation and asthma, Eur. Respir. J., 21, 177, 10.1183/09031936.03.00017003a Zelzer, 2001, Tissue specific regulation of VEGF expression during bone development requires Cbfa1/Runx2, Mech. Dev., 106, 97, 10.1016/S0925-4773(01)00428-2