Nucleolin binds specifically to an AP-1 DNA sequence and represses AP1-dependent transactivation of the matrix metalloproteinase-13 gene.

Samuel, Shaija; Twizere, Jean-Claude; Beifuss, Katherine K; Bernstein, Lori R

doi:10.1002/mc.20358

Article (Scientific journals)

Nucleolin binds specifically to an AP-1 DNA sequence and represses AP1-dependent transactivation of the matrix metalloproteinase-13 gene.

Samuel, Shaija; Twizere, Jean-Claude; Beifuss, Katherine K et al.

2008 • In Molecular Carcinogenesis, 47 (1), p. 34-46

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https://hdl.handle.net/2268/32296

DOI
10.1002/mc.20358

PubMed
17626252

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Keywords :

Adenocarcinoma; Amino Acid Sequence; Base Sequence; Cell Line, Tumor; DNA/chemistry/genetics/metabolism; Humans; Mass Spectrometry; Matrix Metalloproteinase 13/genetics; Molecular Sequence Data; Peptide Fragments/chemistry; Phosphoproteins/metabolism; Plasmids; Protein Binding; RNA-Binding Proteins/metabolism; Transcription Factor AP-1/genetics/metabolism; Transcriptional Activation

Abstract :

[en] Transcriptional regulation via activator protein-1 (AP-1) protein binding to AP-1 binding sites within gene promoter regions of AP-1 target genes plays a key role in controlling cellular invasion, proliferation, and oncogenesis, and is important to pathogenesis of arthritis and cardiovascular disease. To identify new proteins that interact with the AP-1 DNA binding site, we performed the DNA affinity chromatography-based Nucleotide Affinity Preincubation Specificity TEst of Recognition (NAPSTER) assay, and discovered a 97 kDa protein that binds in vitro to a minimal AP-1 DNA sequence element. Mass spectrometric fragmentation sequencing determined that p97 is nucleolin. Immunoblotting of DNA affinity-purified material with anti-nucleolin antibodies confirmed this identification. Nucleolin also binds the AP-1 site in gel shift assays. Nucleolin interacts in NAPSTER with the AP-1 site within the promoter sequence of the metalloproteinase-13 gene (MMP-13), and binds in vivo in chromatin immunoprecipitation assays in the vicinity of the AP-1 site in the MMP-13 promoter. Overexpression of nucleolin in human HeLa cervical carcinoma cells significantly represses AP-1 dependent gene transactivation of a minimal AP-1 reporter construct and of an MMP-13 promoter reporter sequence. This is the first report of nucleolin binding and transregulation at the AP-1 site.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Samuel, Shaija

Twizere, Jean-Claude ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Gembloux Agro-Bio Tech

Beifuss, Katherine K

Bernstein, Lori R

Language :

English

Title :

Nucleolin binds specifically to an AP-1 DNA sequence and represses AP1-dependent transactivation of the matrix metalloproteinase-13 gene.

Publication date :

2008

Journal title :

Molecular Carcinogenesis

ISSN :

0899-1987

eISSN :

1098-2744

Publisher :

Wiley Liss, Inc., New York, United States - New York

Volume :

Issue :

Pages :

34-46

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 11 December 2009

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Bibliography

Wisdom R. AP-1: One switch for many signals. Exp Cell Res 1999;253:180-185.
Eferl R, Wagner EF. AP-1: A double-edged sword in tumorigenesis. Nat Rev Cancer 2003;3:859-868.
Shaulian E, Karin M. AP-1 as a regulator of cell life and death. Nat Cell Biol 2002;4:E131-E136.
Ozanne BW, Spence HJ, McGarry LC, Hennigan RF. Transcription factors control invasion: AP-1 the first among equals. Oncogene 2006;26:1-10.
De Bosscher K, Vanden Berghe W, Haegeman G. The interplay between the glucocorticoid receptor and nuclear factor-kappaB or activator protein-1: Molecular mechanisms for gene repression. Endocr Rev 2003;24:488-522.
Rannou F, Francois M, Corvol MT, Berenbaum F. Cartilage breakdown in rheumatoid arthritis. Joint Bone Spine 2005;73:29-36.
Zenz R, Eferl R, Kenner L, et al. Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature 2005;437:369-375.
Zou Y, Hu Y, Metzler B, Xu Q. Signal transduction in arteriosclerosis: Mechanical stress-activated MAP kinases in vascular smooth muscle cells. Int J Mol Med 1998;1:827-834.
Herdegen T, Waetzig V. AP-1 proteins in the adult brain: Facts and fiction about effectors of neuroprotection and neurodegeneration. Oncogene 2001;20:2424-2437.
Milde-Langosch K, The Fos family of transcription factors and their role in tumourigenesis. Eur J Cancer 2005;41:2449-2461.
Lee W, Mitchell P, Tjian R. Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell 1987;49:741-752.
Angel P, Imagawa M, Chiu R, et al. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans acting factor. Cell 1987;49:729-739.
Przybylo JA, Radisky DC. Matrix metalloproteinase-induced epithelial-mesenchymal transition: Tumor progression at Snail's pace. Int J Biochem Cell Biol 2007;31:1082-1088.
Tardif G, Reboul P, Pelletier JP, Martel-Pelletier J. Ten years in the life of an enzyme: The story of the human MMP-13 (collagenase-3). Mod Rheumatol 2004;14:197-204.
Mongelard F, Bouvet P. Nucleolin: A multiFACeTed protein. Trends Cell Biol 2006;17:80-86.
Ginisty H, Sicard H, Roger B, Bouvet P. Structure and functions of nucleolin. J Cell Sci 1999;112:761-772.
Huddleson JP, Ahmad N, Lingrel JB. Up-regulation of the KLF2 transcription factor by fluid shear stress requires nucleolin. J Biol Chem 2006;281:15121-15128.
Tuteja R, Tuteja N. Nucleolin: A multifunctional major nucleolar phosphoprotein, Review. Crit Rev Biochem Mol Biol 1998;33:407-436.
Srivastava M, Pollard HB. Molecular dissection of nucleolin's role in growth and cell proliferation: New insights. FASEB J 1999;13:1911-1922.
Jiang Y, Xu XS, Russell JE. A nucleolin-binding 3′ untranslated region element stabilizes beta-globin mRNA in vivo. Mol Cell Biol 2006;26:2419-2429.
Fahling M, Steege A, Perlewitz A, et al. Role of nucleolin in posttranscriptional control of MMP-9 expression. Biochim Biophys Acta 2005;1731:32-40.
Rickards B, Flint SJ, Cole MD, Leroy G. Nucleolin is required for RNA polymerase I transcription in vivo. Mol Cell Biol 2006;27:937-948.
Masumi A, Fukazawa H, Shimazu T, et al. Nucleolin is involved in interferon regulatory factor-2-dependent transcriptional activation. Oncogene 2006;25:5113-5124.
Kumar NV, Bernstein LR. A new analytical scale DNA affinity binding assay for analyses of specific protein-DNA interactions. Anal Biochem 2001;299:203-210.
Samuel S, Twizere JC, Bernstein LR. YB-1 represses AP1-dependent gene transactivation and interacts with an AP-1 DNA sequence. Biochem J 2005;388:921-928.
Kumar NV, Bernstein LR. Ten ERK-related proteins in three distinct classes associate with AP-1 proteins and/or AP-1 DNA. J Biol Chem 2001;276:32362-32372.
Ala-aho R, Ahonen M, George SJ, et al. Targeted inhibition of human collagenase-3 (MMP-13) expression inhibits squamous cell carcinoma growth in vivo. Oncogene 2004;23:5111-5123.
Chu CY, Cha ST, Chang CC, et al. Involvement of matrix metalloproteinase-13 in stromal-cell-derived factor 1alpha-directed invasion of human basal cell carcinoma cells. Oncogene 2006;26:2491-2501.
Bernstein LR, Walker SE. Tumor promotion resistant cells are deficient in AP-1 DNA binding, JunD DNA binding, and JunD expression and form different AP-1 DNA complexes than promotion sensitive cells. Biochim Biophys Acta 1999;1489:263-280.
Mengshol JA, Vincenti MP, Brinckerhoff CE. IL-1 induces collagenase-3 (MMP-13) promoter activity in stably transfected chondrocytic cells: Requirement for Runx-2 and activation by p38 MAPK and JNK pathways. Nucleic Acids Res 2001;29:4361-4372.
Dickinson LA, Kohwi-Shigematsu T. Nucleolin is a matrix attachment region DNA-binding protein that specifically recognizes a region with high base-unpairing potential. Mol Cell Biol 1995;15:456-465.
Galande S. Chromatin (dis)organization and cancer: BUR-binding proteins as biomarkers for cancer. Curr Cancer Drug Targets 2002;2:157-190.
Ala-aho R, Kahari VM. Collagenases in cancer. Biochimie 2005;87:273-286.
Winchester SK, Selvamurugan N, D'Alonzo RC, Partridge NC. Developmental regulation of collagenase-3 mRNA in normal, differentiating osteoblasts through the activator protein-1 and the runt domain binding sites. J Biol Chem 2000;275:23310-23318.
Yang TH, Tsai WH, Lee YM, et al. Purification and characterization of nucleolin and its identification as a transcription repressor. Mol Cell Biol 1994;14:6068-6074.
Hoffmann H, Green J, van Wijnen AJ, Stein JL, Stein GS, Lian JB. Expression screening of factors binding to the osteocalcin bone-specific promoter element OC Box I: Isolation of a novel osteoblast differentiation- specific factor. J Cell Biochem 2000;80:156-168.
Hanakahi LA, Bu Z, Maizels N. The C-terminal domain of nucleolin accelerates nucleic acid annealing. Biochemistry 2000;39:15493-15499.
Grinstein E, Wernet P, Snijders PJ, et al. Nucleolin as activator of human papillomavirus type 18 oncogene transcription in cervical cancer. J Exp Med 2002;196:1067-1078.
Angelov D, Bondarenko VA, Almagro S, et al. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J 2006;25:1669-1679.
Farrell PJ, Rowe DT, Rooney CM, Kouzarides T. Epstein-Barr virus BZLF1 trans-activator specifically binds to a consensus AP-1 site and is related to c-fos. EMBO J 1989;8:127-132.
Kouzarides T, Packham G, Cook A, Farrell PJ. The BZLF1 protein of EBV has a coiled coil dimerisation domain without a heptad leucine repeat but with homology to the C/EBP leucine zipper. Oncogene 1991;6:195-204.
Masquilier D, Sassone-Corsi P. Transcriptional cross-talk: Nuclear factors CREM and CREB bind to AP-1 sites and inhibit activation by Jun. J Biol Chem 1992;267:22460-22466.
Hasegawa H, Utsunomiya Y, Kishimoto K, Tange Y, Yasukawa M, Fujita S. SFA-2, a novel bZIP transcription factor induced by human T-cell leukemia virus type I, is highly expressed in mature lymphocytes. Biochem Biophys Res Commun 1996;222:164-170.
Aronheim A, Zandi E, Hennemann H, Elledge SJ, Karin M. Isolation of an AP-1 repressor by a novel method for detecting protein-protein interactions. Mol Cell Biol 1997;17:3094-3102.
Iacobelli M, Wachsman W, McGuire KL. Repression of IL-2 promoter activity by the novel basic leucine zipper p21 SNFT protein. J Immunol 2000;165:860-868.
Chinekov Y, Kerppola TK. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 2001;20:2438-2452.
Motohashi H, O'Connor T, Katsuoka F, Engel JD, Yamamoto M. Integration and diversity of the regulatory network composed of Maf and CNC families of transcription factors. Gene 2002;294:1-12.
Bower KE, Zeller RW, Wachsman W, Martinez T, McGuire KL. Correlation of transcriptional repression by p21 (SNFT) with changes in DNA. NF-AT complex interactions. J Biol Chem 2002;277:34967-34977.
Bengal E, Ransone L, Scharfmann R, et al. Functional antagonism between c-Jun and MyoD proteins: A direct physical association. Cell 1992;68:507-519.
Goldberg Y, Treier M, Ghysdael J, Bohmann D. Repression of AP-1-stimulated transcription byc-Ets-1. J Biol Chem 1994;269:16566-16573.
Lee JS, See RH, Deng T, Shi Y. Adenovirus E1A downregulates cJun- and JunB-mediated transcription by targeting their coactivator p300. Mol Cell Biol 1996;16:4312-4326.
Min W, Ghosh S, Lengyel P. The interferon-inducible p202 protein as a modulator of transcription: Inhibition of NF-kappa B, c-Fos, and c-Jun activities. Mol Cell Biol 1996;16:359-368.
Ye J, Cippitelli M, Dorman L, Ortaldo JR, Young HA. The nuclear factor YY1 suppresses the human gamma interferon promoter through two mechanisms: Inhibition of AP1 binding and activation of a silencer element. Mol Cell Biol 1996;16:4744-4753.
Agarwal SK, Guru SC, Heppner C, et al. Menin interacts with the AP1 transcription factor JunD and represses JunD-activated transcription. Cell 1999:143-152.
Delerive P, De Bosscher K, Besnard S, et al. Peroxisome proliferator-activated receptor alpha negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-kappaB and AP-1. J Biol Chem 1999;274:32048-32054.
Bidder M, Loewy AP, Latifi T, et al. Ets domain transcription factor PE1 suppresses human interstitial collagenase promoter activity by antagonizing protein-DNA interactions at a critical AP1 element. Biochemistry 2000;39:8917-8928.
Benkoussa M, Brand C, Delmotte MH, Formstecher P, Lefebvre P. Retinoic acid receptors inhibit AP1 activation by regulating extracellular signal-regulated kinase and CBP recruitment to an AP1-responsive promoter. Mol Cell Biol 2002;22:4522-4534.
Vasanwala FH, Kusam S, Toney LM, Dent AL. Repression of AP-1 function: A mechanism for the regulation of Blimp-1 expression and B lymphocyte differentiation by the B cell lymphoma-6 protooncogene. J Immunol 2002;169:1922-1929.
Smoak KA, Cidlowski JA. Mechanisms of glucocorticoid receptor signaling during inflammation. Mech Ageing Dev 2004;125:697-706.
Ceman S, Nelson R, Warren ST. Identification of mouse YB1/p50 as a component of the FMRP-associated mRNP particle. Biochem Biophys Res Commun 2000;279:904-908.
Yanagida M, Shimamoto A, Nishikawa K, Furuichi Y, Isobe T, Takahashi N. Isolation and proteomic characterization of the major proteins of the nucleolin-binding ribonucleoprotein complexes. Proteomics 2001;1:1390-1404.
Gaudreault I, Guay D, Lebel M. YB-1 promotes strand separation in vitro of duplex DNA containing either mispaired bases or cisplatin modifications, exhibits endonucleolytic activities and binds several DNA repair proteins. Nucleic Acids Res 2004;32:316-327.
Marshak DR, Kadonaga JT, Burgess RR, Knuth MW, Brennan WA, Lin S-H. Strategies for protein purification and characterization, a laboratory course manual. New York: Cold Spring Harbor Press; 1996.
Ala-Aho R, Johansson N, Baker AH, Kahari VM. Expression of collagenase-3 (MMP-13) enhances invasion of human fibrosarcoma HT-1080 cells. Int J Cancer 2002;97:283-289.
Poole AR, Nelson F, Dahlberg L, et al. Proteolysis of the collagen fibril in osteoarthritis. Biochem Soc Symp 2003;70:115-123.
Schmidt-Hansen B, Ornas D, Grigorian M, et al. Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity. Oncogene 2004;23:5487-5495.
Licht AH, Pein OT, Florin L, et al. JunB is required for endothelial cell morphogenesis by regulating core-binding factor beta. J Cell Biol 2006;175:981-991.
Blavier L, Lazaryev A, Dorey F, Shackleford GM, DeClerck YA. Matrix metalloproteinases play an active role in Wnt1-induced mammary tumorigenesis. Cancer Res 2006;66:2691-2699.
Vincenti MP, Brinckerhoff CE. Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: Integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res 2002;4:157-164.
Milde-Langosch K, Roder H, Andritzky B, et al. The role of the AP-1 transcription factors c-Fos, FosB, Fra-1 and Fra-2 in the invasion process of mammary carcinomas. Breast Cancer Res Treat 2004;86:139-152.
Tuckermann JP, Vallon R, Gack S, et al. Expression of collagenase-3 (MMP-13) in c-fos-induced osteosarcomas and chondrosarcomas is restricted to a subset of cells of the osteo-/chondrogenic lineage. Differentiation 2001;1:49-57.
Onodera S, Nishihira J, Iwabuchi K, et al. Macrophage migration inhibitory factor up-regulates matrix metalloproteinase-9 and -13 in rat osteoblasts. Relevance to intracellular signaling pathways. J Biol Chem 2001;277:7865-7874.