Characterization of the human Activin-A receptor type II-like kinase 1 (ACVRL1) promoter and its regulation by Sp1

BMC Molecular Biology

Volumn 11, Issue , 2010, Pages

  Garrido Martin, Eva M ^a   Blanco, Francisco J ^a   Fernandez L, Africa ^a,b   Langa, Carmen ^a   Vary, Calvin P ^c   Lee, Ursula E ^d   Friedman, Scott L ^d   Botella, Luisa M ^a   Bernabeu, Carmelo ^a  

^a CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c Maine Medical Center Research Institute   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; COMPLEMENTARY DNA; MESSENGER RNA; TRANSCRIPTION FACTOR SP1; ACTIVIN RECEPTOR 2; ACVRL1 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL STRAIN HEK293; CHROMATIN IMMUNOPRECIPITATION; COMPUTER ANALYSIS; CONCENTRATION RESPONSE; CONSENSUS SEQUENCE; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; ENZYME ACTIVITY; ENZYME REGULATION; EXON; GC RICH SEQUENCE; GEL MOBILITY SHIFT ASSAY; GENE AMPLIFICATION; GENE EXPRESSION; IN VITRO STUDY; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN FUNCTION; SEQUENCE ALIGNMENT; TATA BOX; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; 5' UNTRANSLATED REGION; ANIMAL; CATTLE; DNA METHYLATION; DOG; GENETICS; HORSE; HUMAN; MACACA; METABOLISM; MOLECULAR GENETICS; MOUSE; ORANG UTAN; PROTEIN BINDING; RAT; TRANSCRIPTION INITIATION;

5' UNTRANSLATED REGIONS; ACTIVIN RECEPTORS, TYPE II; ANIMALS; BASE SEQUENCE; BINDING SITES; CATTLE; CHROMATIN IMMUNOPRECIPITATION; CPG ISLANDS; DNA METHYLATION; DOGS; HORSES; HUMANS; MACACA MULATTA; MICE; MOLECULAR SEQUENCE DATA; PONGO; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RATS; SEQUENCE ALIGNMENT; SP1 TRANSCRIPTION FACTOR; TRANSCRIPTION INITIATION SITE; TRANSCRIPTIONAL ACTIVATION;

EID: 77953920377     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-11-51     Document Type: Article

References (53)

1. Johnson DW, Berg JN, Baldwin MA, Gallione CJ, Marondel I, Yoon SJ, Stenzel TT, Speer M, Pericak-Vance MA, Diamond A, et al. Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat Genet 1996, 13:189-195. 10.1038/ng0696-189, 8640225.
2. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 2004, 101:6062-6067. 10.1073/pnas.0400782101, 395923, 15075390.
3. Roelen BA, van Rooijen MA, Mummery CL. Expression of ALK-1, a type 1 serine/threonine kinase receptor, coincides with sites of vasculogenesis and angiogenesis in early mouse development. Dev Dyn 1997, 209:418-430. 10.1002/(SICI)1097-0177(199708)209:4<418::AID-AJA9>3.0.CO;2-L, 9264265.
4. Sanz-Rodriguez F, Fernandez LA, Zarrabeitia R, Perez-Molino A, Ramirez JR, Coto E, Bernabeu C, Botella LM. Mutation analysis in Spanish patients with hereditary hemorrhagic telangiectasia: deficient endoglin up-regulation in activated monocytes. Clin Chem 2004, 50:2003-2011. 10.1373/clinchem.2004.035287, 15375013.
5. Konig HG, Kogel D, Rami A, Prehn JH. TGF-β1 activates two distinct type I receptors in neurons: implications for neuronal NF-κB signaling. J Cell Biol 2005, 168:1077-1086. 10.1083/jcb.200407027, 2171851, 15781474.
6. Beger B, Robertson K, Evans A, Grant A, Berg J. Expression of endoglin and the activin receptor-like kinase 1 in skin suggests a role for these receptors in normal skin function and skin tumorigenesis. Brit J Dermatol 2006, 154:379-382.
7. Li L, Zhao XY, Wang BE. Down-regulation of transforming growth factor beta 1/activin receptor-like kinase 1 pathway gene expression by herbal compound 861 is related to deactivation of LX-2 cells. World J Gastroenterol 2008, 14:2894-2899. 10.3748/wjg.14.2894, 2710734, 18473417.
8. Finnson KW, Parker WL, ten Dijke P, Thorikay M, Philip A. ALK1 opposes ALK5/Smad3 signaling and expression of extracellular matrix components in human chondrocytes. J Bone Miner Res 2008, 23:896-906. 10.1359/jbmr.080209, 18333754.
9. Mancini ML, Verdi JM, Conley BA, Nicola T, Spicer DB, Oxburgh LH, Vary CP. Endoglin is required for myogenic differentiation potential of neural crest stem cells. Dev Biol 2007, 308:520-533. 10.1016/j.ydbio.2007.06.009, 2041841, 17628518.
10. Velasco S, Alvarez-Munoz P, Pericacho M, Dijke PT, Bernabeu C, Lopez-Novoa JM, Rodriguez-Barbero A. L- and S-endoglin differentially modulate TGFbeta1 signaling mediated by ALK1 and ALK5 in L6E9 myoblasts. J Cell Sci 2008, 121:913-919. 10.1242/jcs.023283, 18303046.
11. Oh SP, Seki T, Goss KA, Imamura T, Yi Y, Donahoe PK, Li L, Miyazono K, ten Dijke P, Kim S, et al. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci USA 2000, 97:2626-2631. 10.1073/pnas.97.6.2626, 15979, 10716993.
12. Lux A, Salway F, Dressman HK, Kroner-Lux G, Hafner M, Day PJ, Marchuk DA, Garland J. ALK1 signalling analysis identifies angiogenesis related genes and reveals disparity between TGF-beta and constitutively active receptor induced gene expression. BMC Cardiovasc Disord 2006, 6:13. 10.1186/1471-2261-6-13, 1534055, 16594992.
13. Seki T, Yun J, Oh SP. Arterial endothelium-specific activin receptor-like kinase 1 expression suggests its role in arterialization and vascular remodeling. Circ Res 2003, 93:682-689. 10.1161/01.RES.0000095246.40391.3B, 12970115.
14. Urness LD, Sorensen LK, Li DY. Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat Genet 2000, 26:328-331. 10.1038/81634, 11062473.
15. Lux A, Attisano L, Marchuk DA. Assignment of transforming growth factor beta1 and beta3 and a third new ligand to the type I receptor ALK-1. J Biol Chem 1999, 274:9984-9992. 10.1074/jbc.274.15.9984, 10187774.
16. David L, Mallet C, Mazerbourg S, Feige JJ, Bailly S. Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 2007, 109:1953-1961. 10.1182/blood-2006-07-034124, 17068149.
17. Bernabeu C, Lopez-Novoa JM, Quintanilla M. The emerging role of TGF-beta superfamily coreceptors in cancer. Biochim Biophys Acta 2009, 1792:954-973.
18. Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, Thorikay M, Mummery C, Arthur HM, ten Dijke P. Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J 2004, 23:4018-4028. 10.1038/sj.emboj.7600386, 524335, 15385967.
19. Goumans MJ, Lebrin F, Valdimarsdottir G. Controlling the angiogenic switch: a balance between two distinct TGF-β receptor signaling pathways. Trends Cardiovas Med 2003, 13:301-307.
20. David L, Mallet C, Keramidas M, Lamande N, Gasc JM, Dupuis-Girod S, Plauchu H, Feige JJ, Bailly S. Bone morphogenetic protein-9 is a circulating vascular quiescence factor. Circ Res 2008, 102:914-922. 10.1161/CIRCRESAHA.107.165530, 2561062, 18309101.
21. ten Dijke P, Ichijo H, Franzen P, Schulz P, Saras J, Toyoshima H, Heldin CH, Miyazono K. Activin receptor-like kinases: a novel subclass of cell-surface receptors with predicted serine/threonine kinase activity. Oncogene 1993, 8:2879-2887.
22. Attisano L, Carcamo J, Ventura F, Weis FM, Massague J, Wrana JL. Identification of human activin and TGF beta type I receptors that form heteromeric kinase complexes with type II receptors. Cell 1993, 75:671-680. 10.1016/0092-8674(93)90488-C, 8242742.
23. McAllister KA, Grogg KM, Johnson DW, Gallione CJ, Baldwin MA, Jackson CE, Helmbold EA, Markel DS, McKinnon WC, Murrell J, et al. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet 1994, 8:345-351. 10.1038/ng1294-345, 7894484.
24. Li DY, Sorensen LK, Brooke BS, Urness LD, Davis EC, Taylor DG, Boak BB, Wendel DP. Defective angiogenesis in mice lacking endoglin. Science 1999, 284:1534-1537. 10.1126/science.284.5419.1534, 10348742.
25. Arthur HM, Ure J, Smith AJ, Renforth G, Wilson DI, Torsney E, Charlton R, Parums DV, Jowett T, Marchuk DA, et al. Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol 2000, 217:42-53. 10.1006/dbio.1999.9534, 10625534.
26. Bourdeau A, Dumont DJ, Letarte M. A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest 1999, 104:1343-1351. 10.1172/JCI8088, 409846, 10562296.
27. Govani FS, Shovlin CL. Hereditary haemorrhagic telangiectasia: a clinical and scientific review. Eur J Hum Genet 2009, 17:860-871. 10.1038/ejhg.2009.35, 19337313.
28. Shovlin CL, Guttmacher AE, Buscarini E, Faughnan ME, Hyland RH, Westermann CJ, Kjeldsen AD, Plauchu H. Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu-Osler-Weber syndrome). Am J Med Genet 2000, 91:66-67. 10.1002/(SICI)1096-8628(20000306)91:1<66::AID-AJMG12>3.0.CO;2-P, 10751092.
29. Abdalla SA, Pece-Barbara N, Vera S, Tapia E, Paez E, Bernabeu C, Letarte M. Analysis of ALK-1 and endoglin in newborns from families with hereditary hemorrhagic telangiectasia type 2. Hum Mol Genet 2000, 9:1227-1237. 10.1093/hmg/9.8.1227, 10767348.
30. Rius C, Smith JD, Almendro N, Langa C, Botella LM, Marchuk DA, Vary CP, Bernabeu C. Cloning of the promoter region of human endoglin, the target gene for hereditary hemorrhagic telangiectasia type 1. Blood 1998, 92:4677-4690.
31. Botella LM, Sanchez-Elsner T, Rius C, Corbi A, Bernabeu C. Identification of a critical Sp1 site within the endoglin promoter and its involvement in the transforming growth factor-beta stimulation. J Biol Chem 2001, 276:34486-34494. 10.1074/jbc.M011611200, 11432852.
32. Botella LM, Sanchez-Elsner T, Sanz-Rodriguez F, Kojima S, Shimada J, Guerrero-Esteo M, Cooreman MP, Ratziu V, Langa C, Vary CP, et al. Transcriptional activation of endoglin and transforming growth factor-beta signaling components by cooperative interaction between Sp1 and KLF6: their potential role in the response to vascular injury. Blood 2002, 100:4001-4010. 10.1182/blood.V100.12.4001, 12433697.
33. Sanchez-Elsner T, Botella LM, Velasco B, Langa C, Bernabeu C. Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-beta pathways. J Biol Chem 2002, 277:43799-43808. 10.1074/jbc.M207160200, 12228247.
34. Berg JN, Gallione CJ, Stenzel TT, Johnson DW, Allen WP, Schwartz CE, Jackson CE, Porteous ME, Marchuk DA. The activin receptor-like kinase 1 gene: genomic structure and mutations in hereditary hemorrhagic telangiectasia type 2. Am J Hum Genet 1997, 61:60-67. 10.1086/513903, 1715857, 9245985.
35. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J 2002, 21:1743-1753. 10.1093/emboj/21.7.1743, 125949, 11927558.
36. Sanchez-Elsner T, Ramirez JR, Sanz-Rodriguez F, Varela E, Bernabeu C, Botella LM. A cross-talk between hypoxia and TGF-beta orchestrates erythropoietin gene regulation through SP1 and Smads. J Mol Biol 2004, 336:9-24. 10.1016/j.jmb.2003.12.023, 14741200.
37. Pimanda JE, Chan WY, Wilson NK, Smith AM, Kinston S, Knezevic K, Janes ME, Landry JR, Kolb-Kokocinski A, Frampton J, et al. Endoglin expression in blood and endothelium is differentially regulated by modular assembly of the Ets/Gata hemangioblast code. Blood 2008, 112:4512-4522. 10.1182/blood-2008-05-157560, 2682356, 18805961.
38. Wasylyk B, Hagman J, Gutierrez-Hartmann A. Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem Sci 1998, 23:213-216. 10.1016/S0968-0004(98)01211-0, 9644975.
39. Bloom BB, Humphries DE, Kuang PP, Fine A, Goldstein RH. Structure and expression of the promoter for the R4/ALK5 human type I transforming growth factor-beta receptor: regulation by TGF-beta. Biochim Biophys Acta 1996, 1312:243-248. 10.1016/0167-4889(96)00043-2, 8703994.
40. Lania L, Majello B, De Luca P. Transcriptional regulation by the Sp family proteins. Int J Biochem Cell B 1997, 29:1313-1323.
41. Clark SJ, Harrison J, Molloy PL. Sp1 binding is inhibited by (m)Cp(m)CpG methylation. Gene 1997, 195:67-71. 10.1016/S0378-1119(97)00164-9, 9300822.
42. Siegfried Z, Eden S, Mendelsohn M, Feng X, Tsuberi BZ, Cedar H. DNA methylation represses transcription in vivo. Nat Genet 1999, 22:203-206. 10.1038/9727, 10369268.
43. Simonsson S, Gurdon J. DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat Cell Biol 2004, 6:984-990. 10.1038/ncb1176, 15448701.
44. Cao YX, Jean JC, Williams MC. Cytosine methylation of an Sp1 site contributes to organ-specific and cell-specific regulation of expression of the lung epithelial gene t1alpha. Biochem J 2000, 350:883-890. 10.1042/0264-6021:3500883, 1221323, 10970805.
45. Almendro N, Bellon T, Rius C, Lastres P, Langa C, Corbi A, Bernabeu C. Cloning of the human platelet endothelial cell adhesion molecule-1 promoter and its tissue-specific expression. Structural and functional characterization. J Immunol 1996, 157:5411-5421.
46. Patterson C, Perrella MA, Hsieh CM, Yoshizumi M, Lee ME, Haber E. Cloning and functional analysis of the promoter for KDR/flk-1, a receptor for vascular endothelial growth factor. J Biol Chem 1995, 270:23111-23118. 10.1074/jbc.270.39.23111, 7559454.
47. Gory S, Dalmon J, Prandini MH, Kortulewski T, de Launoit Y, Huber P. Requirement of a GT box (Sp1 site) and two Ets binding sites for vascular endothelial cadherin gene transcription. J Biol Chem 1998, 273:6750-6755. 10.1074/jbc.273.12.6750, 9506975.
48. Zhang R, Min W, Sessa WC. Functional analysis of the human endothelial nitric oxide synthase promoter. Sp1 and GATA factors are necessary for basal transcription in endothelial cells. J Biol Chem 1995, 270:15320-15326. 10.1074/jbc.270.25.15320, 7541039.
49. Dube A, Akbarali Y, Sato TN, Libermann TA, Oettgen P. Role of the Ets transcription factors in the regulation of the vascular-specific Tie2 gene. Circ Res 1999, 84:1177-1185.
50. Seki T, Hong KH, Yun J, Kim SJ, Oh SP. Isolation of a regulatory region of activin receptor-like kinase 1 gene sufficient for arterial endothelium-specific expression. Circ Res 2004, 94:e72-77. 10.1161/01.RES.0000127048.81744.31, 15059937.
51. Butta N, Larrucea S, Alonso S, Rodriguez RB, Arias-Salgado EG, Ayuso MS, Gonzalez-Manchon C, Parrilla R. Role of transcription factor Sp1 and CpG methylation on the regulation of the human podocalyxin gene promoter. BMC Mol Biol 2006, 7:17. 10.1186/1471-2199-7-17, 1481587, 16684343.
52. Korchynskyi O, ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 2002, 277:4883-4891. 10.1074/jbc.M111023200, 11729207.
53. Sanchez-Elsner T, Botella LM, Velasco B, Corbi A, Attisano L, Bernabeu C. Synergistic cooperation between hypoxia and transforming growth factor-beta pathways on human vascular endothelial growth factor gene expression. J Biol Chem 2001, 276:38527-38535. 10.1074/jbc.M104536200, 11486006.