Sp1/Sp3 and DNA-methylation contribute to basal transcriptional activation of human podoplanin in MG63 versus Saos-2 osteoblastic cells

BMC Molecular Biology

Volumn 8, Issue , 2007, Pages

  Hantusch, Brigitte ^a   Kalt, Romana ^a   Krieger, Sigurd ^a   Puri, Christina ^a   Kerjaschki, Dontscho ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE; CCAAT ENHANCER BINDING PROTEIN; DEOXYRIBONUCLEASE I; DNA METHYLTRANSFERASE INHIBITOR; GENOMIC DNA; MESSENGER RNA; NUCLEAR FACTOR I; PODOPLANIN; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3; TRICHOSTATIN A; MEMBRANE PROTEIN; PDPN PROTEIN, HUMAN; SP3 PROTEIN, HUMAN; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA FLANKING REGION; DNA FOOTPRINTING; DNA METHYLATION; DOWN REGULATION; GC RICH SEQUENCE; GEL MOBILITY SHIFT ASSAY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOLECULAR CLONING; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PROMOTER REGION; PROTEIN FUNCTION; REPORTER GENE; SOUTHERN BLOTTING; TRANSCRIPTION INITIATION; BIOSYNTHESIS; METABOLISM; OSTEOSARCOMA; PHYSIOLOGY; TRANSACTIVATION; TUMOR CELL LINE;

CELL LINE, TUMOR; DNA METHYLATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HUMANS; MEMBRANE GLYCOPROTEINS; OSTEOBLASTS; OSTEOSARCOMA; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; SP1 TRANSCRIPTION FACTOR; SP3 TRANSCRIPTION FACTOR; TRANS-ACTIVATION (GENETICS);

EID: 35148882985     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-8-20     Document Type: Article

References (65)

1. Nose K Saito H Kuroki T Isolation of a gene sequence induced later by tumor-promoting 12-O-tetradecanoylphorbol-13-acetate in mouse osteoblastic cells (MC3T3-E1) and expressed constitutively in ras-transformed cells Cell Growth Differ 1990, 1(11):511-518. 2088477
2. Watanabe M Sugimoto Y Tsuruo T Expression of a Mr 41,000 glycoprotein associated with thrombin-independent platelet aggregation in high metastatic variants of murine B16 melanoma Cancer Res 1990, 50(20):6657-6662. 2208129
3. Farr AG Berry ML Kim A Nelson AJ Welch MP Aruffo A Characterization and cloning of a novel glycoprotein expressed by stromal cells in T-dependent areas of peripheral lymphoid tissues J Exp Med 1992, 176(5):1477-1482. 10.1084/jem.176.5.1477 1402691
4. Wetterwald A Hoffstetter W Cecchini MG Lanske B Wagner C Fleisch H Atkinson M Characterization and cloning of the E11 antigen, a marker expressed by rat osteoblasts and osteocytes Bone 1996, 18(2):125-132. 10.1016/8756-3282(95)00457-2 8833206
5. Zimmer G Oeffner F Von Messling V Tschernig T Groness HJ Klenk HD Herrler G Cloning and characterization of gp36, a human mucin-type glycoprotein preferentially expressed in vascular endothelium Biochem J 1999, 341(Pt 2):277-284. 1220357 10393083 10.1042/0264-6021:3410277
6. Williams MC Cao Y Hinds A Rishi AK Wetterwald A T1 alpha protein is developmentally regulated and expressed by alveolar type I cells, choroid plexus, and ciliary epithelia of adult rats Am J Respir Cell Mol Biol 1996, 14(6):577-585. 8652186
7. Gandarillas A Scholl FG Benito N Gamallo C Quintanilla M Induction of PA2.26, a cell-surface antigen expressed by active fibroblasts, in mouse epidermal keratinocytes during carcinogenesis Mol Carcinog 1997, 20(1):10-18. 10.1002/ (SICI)1098-2744(199709)20:1<10::AID-MC3>3.0.CO;2-M 9328432
8. Kotani M Osanai T Tajima Y Kato H Imada M Kaneda H Kubo H Sakuraba H Identification of neuronal cell lineage-specific molecules in the neuronal differentiation of P19 EC cells and mouse central nervous system J Neurosci Res 2002, 67(5):595-606. 10.1002/jnr.10150 11891772
9. Breiteneder-Geleff S Matsui K Soleiman A Meraner P Poczewski H Kalt R Schaffner G Kerjaschki D Podoplanin, novel 43-kd membrane protein of glomerular epithelial cells, is down-regulated in puromycin nephrosis Am J Pathol 1997, 151(4):1141-1152. 9327748
10. Kriehuber E Breiteneder-Geleff S Groeger M Soleiman A Schoppmann SF Stingl G Kerjaschki D Maurer D Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages J Exp Med 2001, 194(6):797-808. 10.1084/ jem.194.6.797 11560995
11. Rishi AK Joyce-Brady M Fisher J Dobbs LG Floros J VanderSpek J Brody JS Williams MC Cloning, characterization, and development expression of a rat lung alveolar type I cell gene in embryonic endodermal and neural derivatives Dev Biol 1995, 167(1):294-306. 10.1006/dbio.1995.1024 7851650
12. Kato Y Fujita N Kunita A Sato S Kaneko M Osawa M Tsuruo T Molecular identification of Aggrus/T1alpha as a platelet aggregation-inducing factor expressed in colorectal tumors J Biol Chem 2003, 278(51):51599-51605. 10.1074/jbc.M309935200 14522983
13. Vanderbilt JN Dobbs LG Characterization of the gene and promoter for RTI40, a differentiation marker of type I alveolar epithelial cells Am J Respir Cell Mol Biol 1998, 19(4):662-671. 9761764
14. Zimmer G Klenk HD Herrler G Identification of a 40-kDa cell surface sialoglycoprotein with the characteristics of a major influenza C virus receptor in a Madin-Darby canine kidney cell line J Biol Chem 1995, 270(30):17815-17822. 10.1074/jbc.270.30.17815 7629082
15. Watanabe M Okochi E Sugimoto Y Tsuruo T Identification of a platelet-aggregating factor of murine colon adenocarcinoma 26: Mr 44,000 membrane protein as determined by monoclonal antibodies Cancer Res 1988, 48(22):6411-6416. 3180058
16. Schacht V Ramirez MI Hong YK Hirakawa S Feng D Harvey N Williams M Dvorak AM Dvorak HF Oliver G Detmar M T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema EMBO J 2003, 22(14):3546-3556. 165612 12853470 10.1093/emboj/cdg342
17. Kerjaschki D Regele HM Moosberger I Nagy-Bojarski K Watschinger B Soleiman A Birner P Krieger S Hovorka A Silberhumer G Laakkonen P Petrova T Langer B Raab I Lymphatic neoangiogenesis in human kidney transplants is associated with immunologically active lymphocytic infiltrates J Am Soc Nephrol 2004, 15(3):603-612. 10.1097/ 01.ASN.0000113316.52371.2E 14978162
18. Martin-Villar E Scholl FG Gamallo C Yurrita MM Munoz-Guerra M Cruces J Quintanilla M Characterization of human PA2.26 antigen (T1alpha-2, podoplanin), a small membrane mucin induced in oral squamous cell carcinomas Int J Cancer 2005, 113(6):899-910. 10.1002/ijc.20656 15515019
19. Ohizumi I Harada N Taniguchi K Tsutsumi Y Nakagawa S Kaiho S Mayumi T Association of CD44 with OTS-8 in tumor vascular endothelial cells Biochim Biophys Acta 2000, 1497(2):197-203. 10.1016/ S0167-4889(00)00063-X 10903424
20. Scholl FG Gamallo C Quintanilla M Ectopic expression of PA2.26 antigen in epidermal keratinocytes leads to destabilization of adherens junctions and malignant progression Lab Invest 2000, 80(11):1749-1759. 11092535
21. Kato Y Sasagawa I Kaneko M Osawa M Fujita N Tsuruo T Aggrus: A diagnostic marker that distinguishes seminoma from embryonal carcinoma in testicular germ cell tumors Oncogene 2004, 23(52):8552-8556. 10.1038/ sj.onc.1207869 15361850
22. Wicki A Lehembre F Wick N Hantusch B Kerjaschki D Christofori G Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton Cancer Cell 2006, 9(4):261-272. 10.1016/j.ccr.2006.03.010 16616332
23. Sevetson B Taylor S Pan Y Cbfa1/RUNX2 directs specific expression of the sclerosteosis gene (SOST) J Biol Chem 2004, 279(14):13849-13858. 10.1074/ jbc.M306249200 14739291
24. Ramirez MI Rishi AK Cao YX Williams MC TGT3, thyroid transcription factor I, and Sp1 elements regulate transcriptional activity of the 1.3-kilobase pair promoter of T1alpha, a lung alveolar type I cell gene J Biol Chem 1997, 272(42):26285-26294. 10.1074/jbc.272.42.26285 9334198
25. 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(Pt 3):883-890. 1221323 10970805 10.1042/0264-6021:3500883
26. Hong YK Harvey N Noh YH Schacht V Hirakawa S Detmar M Oliver G Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate Dev Dyn 2002, 225(3):351-357. 10.1002/dvdy.10163 12412020
27. Groger M Loewe R Holnthoner W Embacher R Pillinger M Herron GS Wolff K Petzelbauer P IL-3 induces expression of lymphatic markers Prox-1 and podoplanin in human endothelial cells J Immunol 2004, 173(12):7161-7169. 15585837
28. Gardiner-Garden M Frommer M CpG islands in vertebrate genomes J Mol Biol 1987, 196(2):261-282. 10.1016/0022-2836(87)90689-9 3656447
29. Frommer M McDonald LE Millar DS Collis CM Watt F Grigg GW Molloy PL Paul CL A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands Proc Natl Acad Sci U S A 1992, 89(5):1827-1831. 48546 1542678 10.1073/pnas.89.5.1827
30. Azizkhan JC Jensen DE Pierce AJ Wade M Transcription from TATA-less promoters: Dihydrofolate reductase as a model Crit Rev Eukaryot Gene Expr 1993, 3(4):229-254. 8286846
31. Singal R Ferris R Little JA Wang SZ Ginder GD Methylation of the minimal promoter of an embryonic globin gene silences transcription in primary erythroid cells Proc Natl Acad Sci U S A 1997, 94(25):13724-13729. 28373 9391093 10.1073/pnas.94.25.13724
32. Rundlof AK Carlsten M Arner ES The core promoter of human thioredoxin reductase 1: Cloning, transcriptional activity, and Oct-1, Sp1, and Sp3 binding reveal a housekeeping-type promoter for the AU-rich element-regulated gene J Biol Chem 2001, 276(32):30542-30551. 10.1074/ jbc.M101452200 11375392
33. Kadonaga JT Carner KR Masiarz FR Tjian R Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain Cell 1987, 51(6):1079-1090. 10.1016/0092-8674(87)90594-0 3319186
34. Lania L Majello B De Luca P Transcriptional regulation by the Sp family proteins Int J Biochem Cell Biol 1997, 29(12):1313-1323. 10.1016/ S1357-2725(97)00094-0 9570130
35. De Luca P Majello B Lania L Sp3 represses transcription when tethered to promoter DNA or targeted to promoter proximal RNA J Biol Chem 1996, 271(15):8533-8536. 10.1074/jbc.271.15.8533 8621476
36. Lai CF Feng X Nishimura R Teitelbaum SL Avioli LV Ross FP Cheng SL Transforming growth factor-beta up-regulates the beta 5 integrin subunit expression via Sp1 and Smad signaling J Biol Chem 2000, 275(46):36400-36406. 10.1074/jbc.M002131200 10964912
37. Stains JP Lecanda F Screen J Towler DA Civitelli R Gap junctional communication modulates gene transcription by altering the recruitment of Sp1 and Sp3 to connexin-response elements in osteoblast promoters J Biol Chem 2003, 278(27):24377-24387. 10.1074/jbc.M212554200 12700237
38. Goto T Matsui Y Fernandes RJ Hanson DA Kubo T Yukata K Michigami T Komori T Fujita T Yang L Eyre DR Yasui N Sp1 family of transcription factors regulates the human alpha2 (XI) collagen gene (COL11A2) in Saos-2 osteoblastic cells J Bone Miner Res 2006, 21(5):661-673. 10.1359/ jbmr.020605 16734381
39. Ye X Liu SF Lipopolysaccharide down-regulates Sp1 binding activity by promoting Sp1 protein dephosphorylation and degradation J Biol Chem 2002, 277(35):31863-31870. 10.1074/jbc.M205544200 12089157
40. Cao YX Ramirez MI Williams MC Enhanced binding of Sp1/Sp3 transcription factors mediates the hyperoxia-induced increased expression of the lung type I cell gene T1alpha J Cell Biochem 2003, 89(5):887-901. 10.1002/ jcb.10555 12874823
41. Ahlgren R Suske G Waterman MR Lund J Role of Sp1 in cAMP-dependent transcriptional regulation of the bovine CYP11A gene J Biol Chem 1999, 274(27):19422-19428. 10.1074/jbc.274.27.19422 10383457
42. Liu A Hoffman PW Lu W Bai G NF-kappaB site interacts with Sp factors and up-regulates the NR1 promoter during neuronal differentiation J Biol Chem 2004, 279(17):17449-17458. 10.1074/jbc.M311267200 14970236
43. Karlseder J Rotheneder H Wintersberger E Interaction of Sp1 with the growth- and cell cycle-regulated transcription factor E2F Mol Cell Biol 1996, 164:1659-1667. 231152 8657141
44. Nakashima K Zhou X Kunkel G Zhang Z Deng JM Behringer RR de Crombrugghe B The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation Cell 2002, 108(1):17-29. 10.1016/S0092-8674(01)00622-5 11792318
45. Milona MA Gough JE Edgar AJ Expression of alternatively spliced isoforms of human Sp7 in osteoblast-like cells BMC Genomics 2003, 4(1):43. 280673 14604442 10.1186/1471-2164-4-43
46. Cao Y Zhou Z de Crombrugghe B Nakashima K Guan H Duan X Jia SF Kleinerman ES Osterix, a transcription factor for osteoblast differentiation, mediates antitumor activity in murine osteosarcoma Cancer Res 2005, 65(4):1124-1128. 10.1158/0008-5472.CAN-04-2128 15734992
47. Kudo S Methyl-CpG-binding protein MeCP2 represses Sp1-activated transcription of the human leukosialin gene when the promoter is methylated Mol Cell Biol 1998, 18(9):5492-5499. 109134 9710633
48. Alikhani-Koopaei R Fouladkou F Frey FJ Frey BM Epigenetic regulation of 11 beta-hydroxysteroid dehydrogenase type 2 expression J Clin Invest 2004, 114(8):1146-1157. 522246 15489962 10.1172/JCI200421647
49. Cameron EE Bachman KE Myohanen S Herman JG Baylin SB Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer Nat Genet 1999, 21(1):103-107. 10.1038/5047 9916800
50. Prokhortchouk A Hendrich B Jorgensen H Ruzov A Wilm M Georgiev G Bird A Prokhortchouk E The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor Genes Dev 2001, 15(13):1613-1618. 312733 11445535 10.1101/gad.198501
51. Rodova M Kelly KF VanSaun M Daniel JM Werle MJ Regulation of the rapsyn promoter by kaiso and delta-catenin Mol Cell Biol 2004, 24(16):7188-7196. 479716 15282317 10.1128/MCB.24.16.7188-7196.2004
52. Klose RJ Bird AP Genomic DNA methylation: The mark and its mediators Trends Biochem Sci 2006, 31(2):89-97. 10.1016/j.tibs.2005.12.008 16403636
53. Murrell A Heeson S Bowden L Constancia M Dean W Kelsey G Reik W An intragenic methylated region in the imprinted Igf2 gene augments transcription EMBO Rep 2001, 2(12):1101-1106. 1084166 11743023 10.1093/ embo-reports/kve248
54. Jones PA The DNA methylation paradox Trends Genet 1999, 15(1):34-37. 10.1016/S0168-9525(98)01636-9 10087932
55. Liang G Salem CE Yu MC Nguyen HD Gonzales FA Nguyen TT Nichols PW Jones PA DNA methylation differences associated with tumor tissues identified by genome scanning analysis Genomics 1998, 53(3):260-268. 10.1006/ geno.1998.5502 9799591
56. Weber M Davies JJ Wittig D Oakeley EJ Haase M Lam WL Schubeler D Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells Nat Genet 2005, 37(8):853-862. 10.1038/ng1598 16007088
57. Keshet I Schlesinger Y Farkash S Rand E Hecht M Segal E Pikarski E Young RA Niveleau A Cedar H Simon I Evidence for an instructive mechanism of de novo methylation in cancer cells Nat Genet 2006, 38(2):149-153. 10.1038/ng1719 16444255
58. Jackson-Grusby L Beard C Possemato R Tudor M Fambrough D Csankovszki G Dausman J Lee P Wilson C Lander E Jaenisch R Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation Nat Genet 2001, 27(1):31-39. 10.1038/83730 11137995
59. Jones PA Baylin SB The fundamental role of epigenetic events in cancer Nat Rev Genet 2002, 3(6):415-428. 12042769
60. Osoegawa K Woon PY Zhao B Frengen E Tateno M Catanese JJ de Jong PJ An improved approach for construction of bacterial artificial chromosome libraries Genomics 1998, 52(1):1-8. 10.1006/geno.1998.5423 9740665
61. Quandt K Frech K Karas H Wingender E Werner T MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data Nucleic Acids Res 1995, 23(23):4878-4884. 307478 8532532 10.1093/nar/23.23.4878
62. EMBOSS CpGPlot/CpGReport/Isochore http://www.ebi.ac.uk/emboss/cpgplot/ index.html
63. Sapetschnig A Koch F Rischitor G Mennenga T Suske G Complexity of translationally controlled transcription factor Sp3 isoform expression J Biol Chem 2004, 279(40):42095-42105. 10.1074/jbc.M404989200 15247228
64. Dignam JD Lebovitz RM Roeder RG Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei Nucleic Acids Res 1983, 11(5):1475-1489. 325809 6828386 10.1093/nar/ 11.5.1475
65. Sambrook J Russell, D.W. Molecular Cloning: A Laboratory Manual Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press 3rd Ed. 2001