Epigenetic control of hypoxia inducible factor-1α-dependent expression of placental growth factor in hypoxic conditions

Epigenetics

Volumn 9, Issue 4, 2014, Pages 600-610

  Tudisco, Laura ^a   Ragione, Floriana Della ^a,b   Tarallo, Valeria ^a   Apicella, Ivana ^a   D'Esposito, Maurizio ^a,b   Matarazzo, Maria Rosaria ^a,b   De Falco, Sandro ^a  

^a INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^b IRCCS NEUROMED   (Italy)

Author keywords

Angiogenesis; Chromatin; DNA methylation; Histone modification; Hypoxia; Hypoxia inducible factor (HIF); Placental growth factor (PlGF); VEGF family

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; PLACENTAL GROWTH FACTOR; HISTONE; PLACENTA PROTEIN;

ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; GENE SILENCING; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HYPOXIA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ACETYLATION; ANIMAL; CELL CULTURE; CELL HYPOXIA; CPG ISLAND; CYTOLOGY; DNA METHYLATION; ENDOTHELIUM CELL; GENETIC EPIGENESIS; GENETICS; METABOLISM; MICROVASCULATURE; PROMOTER REGION; UMBILICAL VEIN ENDOTHELIAL CELL;

ACETYLATION; ANIMALS; CELL HYPOXIA; CELLS, CULTURED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CPG ISLANDS; DNA METHYLATION; ENDOTHELIAL CELLS; EPIGENESIS, GENETIC; HISTONES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICROVESSELS; PREGNANCY PROTEINS; PROMOTER REGIONS, GENETIC;

EID: 84899136534     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.27835     Document Type: Article

References (60)

1. De Falco S. The discovery of placenta growth factor and its biological activity. Exp Mol Med 2012; 44:1-9; PMID:22228176; http://dx.doi.org/10.3858/ emm.2012.44.1.025
2. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 2001; 7:575-83; PMID:11329059; http://dx.doi.org/10.1038/87904
3. Dewerchin M, Carmeliet P. PlGF: a multitasking cytokine with disease-restricted activity. Cold Spring Harb Perspect Med 2012; 2.
4. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011; 473:298-307; PMID:21593862; http://dx.doi. org/10.1038/nature10144
5. Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011; 146:873-87; PMID:21925313; http://dx.doi. org/10.1016/j.cell.2011.08.039
6. Baeriswyl V, Christofori G. The angiogenic switch in carcinogenesis. Semin Cancer Biol 2009; 19:329-37; PMID:19482086; http://dx.doi.org/10.1016/j. semcancer.2009.05.003
7. Semenza GL. HIF-1, O(2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 2001; 107:1-3; PMID:11595178; http://dx.doi. org/10.1016/S0092-8674(01)00518-9
8. Maxwell PH, Ratcliffe PJ. Oxygen sensors and angiogenesis. Semin Cell Dev Biol 2002; 13:29-37; PMID:11969369; http://dx.doi.org/10.1006/ scdb.2001.0287
9. Simon MP, Tournaire R, Pouyssegur J. The angiopoietin-2 gene of endothelial cells is up-regulated in hypoxia by a HIF binding site located in its first intron and by the central factors GATA-2 and Ets-1. J Cell Physiol 2008; 217:809-18; PMID:18720385; http://dx.doi.org/10.1002/jcp.21558
10. Eyries M, Siegfried G, Ciumas M, Montagne K, Agrapart M, Lebrin F, Soubrier F. Hypoxiainduced apelin expression regulates endothelial cell proliferation and regenerative angiogenesis. Circ Res 2008; 103:432-40; PMID:18617693; http://dx.doi. org/10.1161/CIRCRESAHA.108.179333
11. Michiels C, Arnould T, Remacle J. Endothelial cell responses to hypoxia: initiation of a cascade of cellular interactions. Biochim Biophys Acta 2000; 1497:1-10; PMID:10838154; http://dx.doi.org/10.1016/ S0167-4889(00)00041-0
12. Nomura M, Yamagishi S, Harada S, Hayashi Y, Yamashima T, Yamashita J, Yamamoto H. Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J Biol Chem 1995; 270:28316-24; PMID:7499331; http:// dx.doi.org/10.1074/jbc.270.47.28316
13. Yonekura H, Sakurai S, Liu X, Migita H, Wang H, Yamagishi S, Nomura M, Abedin MJ, Unoki H, Yamamoto Y, et al. Placenta growth factor and vascular endothelial growth factor B and C expression in microvascular endothelial cells and pericytes. Implication in autocrine and paracrine regulation of angiogenesis. J Biol Chem 1999; 274:35172-8; PMID:10575000; http://dx.doi.org/10.1074/ jbc.274.49.35172
14. Adini A, Kornaga T, Firoozbakht F, Benjamin LE. Placental growth factor is a survival factor for tumor endothelial cells and macrophages. Cancer Res 2002; 62:2749-52; PMID:12019148
15. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996; 16:4604-13; PMID:8756616
16. Gerber HP, Condorelli F, Park J, Ferrara N. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J Biol Chem 1997; 272:23659-67; PMID:9295307; http://dx.doi.org/10.1074/jbc.272.38.23659
17. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003; 9:669-76; PMID:12778165; http://dx.doi.org/10.1038/ nm0603-669
18. Tugues S, Koch S, Gualandi L, Li X, Claesson-Welsh L. Vascular endothelial growth factors and receptors: anti-angiogenic therapy in the treatment of cancer. Mol Aspects Med 2011; 32:88-111; PMID:21565214; http://dx.doi.org/10.1016/j.mam.2011.04.004
19. Cao Y. Positive and negative modulation of angiogenesis by VEGFR1 ligands. Sci Signal 2009; 2:re1; PMID:19244214; http://dx.doi.org/10.1126/ scisignal.259re1
20. Tarallo V, Vesci L, Capasso O, Esposito MT, Riccioni T, Pastore L, Orlandi A, Pisano C, De Falco S. A placental growth factor variant unable to recognize vascular endothelial growth factor (VEGF) receptor-1 inhibits VEGF-dependent tumor angiogenesis via heterodimerization. Cancer Res 2010; 70:1804-13; PMID:20145150; http://dx.doi.org/10.1158/0008-5472.CAN-09-2609
21. Green CJ, Lichtlen P, Huynh NT, Yanovsky M, Laderoute KR, Schaffner W, Murphy BJ. Placenta growth factor gene expression is induced by hypoxia in fibroblasts: a central role for metal transcription factor-1. Cancer Res 2001; 61:2696-703; PMID:11289150
22. Oura H, Bertoncini J, Velasco P, Brown LF, Carmeliet P, Detmar M. A critical role of placental growth factor in the induction of inflammation and edema formation. Blood 2003; 101:560-7; PMID:12393422; http://dx.doi.org/10.1182/ blood-2002-05-1516
23. Selvaraj SK, Giri RK, Perelman N, Johnson C, Malik P, Kalra VK. Mechanism of monocyte activation and expression of proinflammatory cytochemokines by placenta growth factor. Blood 2003; 102:1515-24; PMID:12689930; http://dx.doi.org/10.1182/ blood-2002-11-3423
24. Cramer M, Nagy I, Murphy BJ, Gassmann M, Hottiger MO, Georgiev O, Schaffner W. NF-kappaB contributes to transcription of placenta growth factor and interacts with metal responsive transcription factor-1 in hypoxic human cells. Biol Chem 2005; 386:865-72; PMID:16164411; http://dx.doi. org/10.1515/BC.2005.101
25. Yamakawa M, Liu LX, Date T, Belanger AJ, Vincent KA, Akita GY, Kuriyama T, Cheng SH, Gregory RJ, Jiang C. Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors. Circ Res 2003; 93:664-73; PMID:12958144; http://dx.doi. org/10.1161/01.RES.0000093984.48643.D7
26. Kelly BD, Hackett SF, Hirota K, Oshima Y, Cai Z, Berg-Dixon S, Rowan A, Yan Z, Campochiaro PA, Semenza GL. Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxiainducible factor 1. Circ Res 2003; 93:1074-81; PMID:14576200; http://dx.doi.org/10.1161/01. RES.0000102937.50486.1B
27. Torry RJ, Tomanek RJ, Zheng W, Miller SJ, Labarrere CA, Torry DS. Hypoxia increases placenta growth factor expression in human myocardium and cultured neonatal rat cardiomyocytes. J Heart Lung Transplant 2009; 28:183-90; PMID:19201345; http://dx.doi.org/10.1016/j.healun.2008.11.917
28. Sung CY, Son MW, Ahn TS, Jung DJ, Lee MS, Baek MJ. Expression of placenta growth factor in colorectal carcinomas. J Korean Soc Coloproctol 2012; 28:315-20; PMID:23346511; http://dx.doi.org/10.3393/ jksc.2012.28.6.315
29. Snuderl M, Batista A, Kirkpatrick ND, Ruiz de Almodovar C, Riedemann L, Walsh EC, Anolik R, Huang Y, Martin JD, Kamoun W, et al. Targeting placental growth factor/neuropilin 1 pathway inhibits growth and spread of medulloblastoma. Cell 2013; 152:1065-76; PMID:23452854; http://dx.doi. org/10.1016/j.cell.2013.01.036
30. Schödel J, Oikonomopoulos S, Ragoussis J, Pugh CW, Ratcliffe PJ, Mole DR. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood 2011; 117:e207-17; PMID:21447827; http://dx.doi. org/10.1182/blood-2010-10-314427
31. Garlanda C, Parravicini C, Sironi M, De Rossi M, Wainstok de Calmanovici R, Carozzi F, Bussolino F, Colotta F, Mantovani A, Vecchi A. Progressive growth in immunodeficient mice and host cell recruitment by mouse endothelial cells transformed by polyoma middle-sized T antigen: implications for the pathogenesis of opportunistic vascular tumors. Proc Natl Acad Sci U S A 1994; 91:7291-5; PMID:8041783; http://dx.doi.org/10.1073/ pnas.91.15.7291
32. Schultze A, Ben Batalla I, Riethdorf S, Bubenheim M, Yekebas E, Erbersdobler A, Reichelt U, Effenberger KE, Schmidt T, Izbicki JR, et al. VEGFR-1 expression levels predict occurrence of disseminated tumor cells in the bone marrow of patients with esophageal carcinoma. Clin Exp Metastasis 2012; 29:879-87; PMID:22484977; http://dx.doi.org/10.1007/ s10585-012-9477-1
33. Matarazzo MR, De Bonis ML, Gregory RI, Vacca M, Hansen RS, Mercadante G, D'Urso M, Feil R, D'Esposito M. Allelic inactivation of the pseudoautosomal gene SYBL1 is controlled by epigenetic mechanisms common to the X and Y chromosomes. Hum Mol Genet 2002; 11:3191-8; PMID:12444103; http://dx.doi.org/10.1093/ hmg/11.25.3191
34. Gobble RM, Groesch KA, Chang M, Torry RJ, Torry DS. Differential regulation of human PlGF gene expression in trophoblast and nontrophoblast cells by oxygen tension. Placenta 2009; 30:869-75; PMID:19712973; http://dx.doi.org/10.1016/j. placenta.2009.08.003
35. Tazuke SI, Mazure NM, Sugawara J, Carland G, Faessen GH, Suen LF, Irwin JC, Powell DR, Giaccia AJ, Giudice LC. Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. Proc Natl Acad Sci U S A 1998; 95:10188-93; PMID:9707622; http://dx.doi.org/10.1073/pnas.95.17.10188
36. Kang HJ, Kim HJ, Rih JK, Mattson TL, Kim KW, Cho CH, Isaacs JS, Bae I. BRCA1 plays a role in the hypoxic response by regulating HIF-1alpha stability and by modulating vascular endothelial growth factor expression. J Biol Chem 2006; 281:13047-56; PMID:16543242; http://dx.doi.org/10.1074/jbc. M513033200
37. Maemura K, Hsieh CM, Jain MK, Fukumoto S, Layne MD, Liu Y, Kourembanas S, Yet SF, Perrella MA, Lee ME. Generation of a dominant-negative mutant of endothelial PAS domain protein 1 by deletion of a potent C-terminal transactivation domain. J Biol Chem 1999; 274:31565-70; PMID:10531360; http:// dx.doi.org/10.1074/jbc.274.44.31565
38. Chavez JC, Baranova O, Lin J, Pichiule P. The transcriptional activator hypoxia inducible factor 2 (HIF-2/EPAS-1) regulates the oxygen-dependent expression of erythropoietin in cortical astrocytes. J Neurosci 2006; 26:9471-81; PMID:16971531; http:// dx.doi.org/10.1523/JNEUROSCI.2838-06.2006
39. Loges S, Schmidt T, Carmeliet P. "Antimyeloangiogenic" therapy for cancer by inhibiting PlGF. Clin Cancer Res 2009; 15:3648-53; PMID:19470735; http://dx.doi.org/10.1158/1078-0432.CCR-08-2276
40. Yoo SA, Yoon HJ, Kim HS, Chae CB, De Falco S, Cho CS, Kim WU. Role of placenta growth factor and its receptor flt-1 in rheumatoid inflammation: a link between angiogenesis and inflammation. Arthritis Rheum 2009; 60:345-54; PMID:19180491; http://dx.doi.org/10.1002/art.24289
41. Carnevale D, Lembo G. Placental growth factor and cardiac inflammation. Trends Cardiovasc Med 2012; 22:209-12; PMID:22925712; http://dx.doi. org/10.1016/j.tcm.2012.07.022
42. de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 1992; 255:989-91; PMID:1312256; http:// dx.doi.org/10.1126/science.1312256
43. Wenger RH, Kvietikova I, Rolfs A, Camenisch G, Gassmann M. Oxygen-regulated erythropoietin gene expression is dependent on a CpG methylation-free hypoxia-inducible factor-1 DNA-binding site. Eur J Biochem 1998; 253:771-7; PMID:9654078; http:// dx.doi.org/10.1046/j.1432-1327.1998.2530771.x
44. Rössler J, Stolze I, Frede S, Freitag P, Schweigerer L, Havers W, Fandrey J. Hypoxia-induced erythropoietin expression in human neuroblastoma requires a methylation free HIF-1 binding site. J Cell Biochem 2004; 93:153-61; PMID:15352172; http:// dx.doi.org/10.1002/jcb.20133
45. Xu L, Jain RK. Down-regulation of placenta growth factor by promoter hypermethylation in human lung and colon carcinoma. Mol Cancer Res 2007; 5:873-80; PMID:17704140; http://dx.doi. org/10.1158/1541-7786.MCR-06-0141
46. Flamme I, Fröhlich T, von Reutern M, Kappel A, Damert A, Risau W. HRF, a putative basic helixloop-helix-PAS-domain transcription factor is closely related to hypoxia-inducible factor-1 alpha and developmentally expressed in blood vessels. Mech Dev 1997; 63:51-60; PMID:9178256; http://dx.doi. org/10.1016/S0925-4773(97)00674-6
47. Yamashita T, Ohneda K, Nagano M, Miyoshi C, Kaneko N, Miwa Y, Yamamoto M, Ohneda O, Fujii-Kuriyama Y. Hypoxia-inducible transcription factor-2alpha in endothelial cells regulates tumor neovascularization through activation of ephrin A1. J Biol Chem 2008; 283:18926-36; PMID:18434321; http://dx.doi.org/10.1074/jbc.M709133200
48. Chen C, Pore N, Behrooz A, Ismail-Beigi F, Maity A. Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J Biol Chem 2001; 276:9519-25; PMID:11120745; http://dx.doi.org/10.1074/jbc.M010144200
49. Chun SY, Johnson C, Washburn JG, Cruz-Correa MR, Dang DT, Dang LH. Oncogenic KRAS modulates mitochondrial metabolism in human colon cancer cells by inducing HIF-1α and HIF-2α target genes. Mol Cancer 2010; 9:293; PMID:21073737; http://dx.doi.org/10.1186/1476-4598-9-293
50. Rius J, Guma M, Schachtrup C, Akassoglou K, Zinkernagel AS, Nizet V, Johnson RS, Haddad GG, Karin M. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 2008; 453:807-11; PMID:18432192; http://dx.doi.org/10.1038/ nature06905
51. Bocci G, Man S, Green SK, Francia G, Ebos JM, du Manoir JM, Weinerman A, Emmenegger U, Ma L, Thorpe P, et al. Increased plasma vascular endothelial growth factor (VEGF) as a surrogate marker for optimal therapeutic dosing of VEGF receptor-2 monoclonal antibodies. Cancer Res 2004; 64:6616-25; PMID:15374976; http://dx.doi. org/10.1158/0008-5472.CAN-04-0401
52. Bertolini F, Shaked Y, Mancuso P, Kerbel RS. The multifaceted circulating endothelial cell in cancer: towards marker and target identification. Nat Rev Cancer 2006; 6:835-45; PMID:17036040; http:// dx.doi.org/10.1038/nrc1971
53. Rini BI, Michaelson MD, Rosenberg JE, Bukowski RM, Sosman JA, Stadler WM, Hutson TE, Margolin K, Harmon CS, DePrimo SE, et al. Antitumor activity and biomarker analysis of sunitinib in patients with bevacizumab-refractory metastatic renal cell carcinoma. J Clin Oncol 2008; 26:3743-8; PMID:18669461; http://dx.doi.org/10.1200/ JCO.2007.15.5416
54. Bergers G, Hanahan D. Modes of resistance to antiangiogenic therapy. Nat Rev Cancer 2008; 8:592-603; PMID:18650835; http://dx.doi.org/10.1038/ nrc2442
55. Xu HX, Zhu XD, Zhuang PY, Zhang JB, Zhang W, Kong LQ, Wang WQ, Liang Y, Wu WZ, Wang L, et al. Expression and prognostic significance of placental growth factor in hepatocellular carcinoma and peritumoral liver tissue. Int J Cancer 2011; 128:1559-69; PMID:20521248; http://dx.doi. org/10.1002/ijc.25492
56. Patel N, Kalra VK. Placenta growth factorinduced early growth response 1 (Egr-1) regulates hypoxia-inducible factor-1alpha (HIF-1alpha) in endothelial cells. J Biol Chem 2010; 285:20570-9; PMID:20448047; http://dx.doi.org/10.1074/jbc. M110.119495
57. Fraser P. Transcriptional control thrown for a loop. Curr Opin Genet Dev 2006; 16:490-5; PMID:16904310; http://dx.doi.org/10.1016/j. gde.2006.08.002
58. Matarazzo MR, Boyle S, D'Esposito M, Bickmore WA. Chromosome territory reorganization in a human disease with altered DNA methylation. Proc Natl Acad Sci U S A 2007; 104:16546-51; PMID:17923676; http://dx.doi.org/10.1073/ pnas.0702924104
59. Errico M, Riccioni T, Iyer S, Pisano C, Acharya KR, Persico MG, De Falco S. Identification of placenta growth factor determinants for binding and activation of Flt-1 receptor. J Biol Chem 2004; 279:43929-39; PMID:15272021; http://dx.doi.org/10.1074/jbc. M401418200
60. De Bonis ML, Cerase A, Matarazzo MR, Ferraro M, Strazzullo M, Hansen RS, Chiurazzi P, Neri G, D'Esposito M. Maintenance of X-and Y-inactivation of the pseudoautosomal (PAR2) gene SPRY3 is independent from DNA methylation and associated to multiple layers of epigenetic modifications. Hum Mol Genet 2006; 15:1123-32; PMID:16500999; http://dx.doi.org/10.1093/hmg/ddl027