PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of molcellbPermissionsJournals.ASM.orgJournalMCB ArticleJournal InfoAuthorsReviewers
 
Mol Cell Biol. 1997 September; 17(9): 5275–5287.
PMCID: PMC232378

The matrix attachment region-binding protein SATB1 participates in negative regulation of tissue-specific gene expression.

Abstract

The nuclear matrix has been implicated in several cellular processes, including DNA replication, transcription, and RNA processing. In particular, transcriptional regulation is believed to be accomplished by binding of chromatin loops to the nuclear matrix and by the concentration of specific transcription factors near these matrix attachment regions (MARs). A number of MAR-binding proteins have been identified, but few have been directly linked to tissue-specific transcription. Recently, we have identified two cellular protein complexes (NBP and UBP) that bind to a region of the mouse mammary tumor virus (MMTV) long terminal repeat (LTR) previously shown to contain at least two negative regulatory elements (NREs) termed the promoter-proximal and promoter-distal NREs. These NREs are absent from MMTV strains that cause T-cell lymphomas instead of mammary carcinomas. We show here that NBP binds to a 22-bp sequence containing an imperfect inverted repeat in the promoter-proximal NRE. Previous data showed that a mutation (p924) within the inverted repeat elevated basal transcription from the MMTV promoter and destabilized the binding of NBP, but not UBP, to the proximal NRE. By using conventional and affinity methods to purify NBP from rat thymic nuclear extracts, we obtained a single major protein of 115 kDa that was identified by protease digestion and partial sequencing analysis as the nuclear matrix-binding protein special AT-rich sequence-binding protein 1 (SATB1). Antibody ablation, distamycin inhibition of binding, renaturation and competition experiments, and tissue distribution data all confirmed that the NBP complex contained SATB1. Similar types of experiments were used to show that the UBP complex contained the homeodomain protein Cux/CDP that binds the MAR of the intronic heavy-chain immunoglobulin enhancer. By using the p924 mutation within the MMTV LTR upstream of the chloramphenicol acetyltransferase gene, we generated two strains of transgenic mice that had a dramatic elevation of reporter gene expression in lymphoid tissues compared with reporter gene expression in mice expressing wild-type LTR constructs. Thus, the 924 mutation in the SATB1-binding site dramatically elevated MMTV transcription in lymphoid tissues. These results and the ability of the proximal NRE in the MMTV LTR to bind to the nuclear matrix clearly demonstrate the role of MAR-binding proteins in tissue-specific gene regulation and in MMTV-induced oncogenesis.

Full Text

The Full Text of this article is available as a PDF (3.7M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Adachi Y, Käs E, Laemmli UK. Preferential, cooperative binding of DNA topoisomerase II to scaffold-associated regions. EMBO J. 1989 Dec 20;8(13):3997–4006. [PubMed]
  • Andres V, Nadal-Ginard B, Mahdavi V. Clox, a mammalian homeobox gene related to Drosophila cut, encodes DNA-binding regulatory proteins differentially expressed during development. Development. 1992 Oct;116(2):321–334. [PubMed]
  • Archer TK, Lefebvre P, Wolford RG, Hager GL. Transcription factor loading on the MMTV promoter: a bimodal mechanism for promoter activation. Science. 1992 Mar 20;255(5051):1573–1576. [PubMed]
  • Ball JK, Arthur LO, Dekaban GA. The involvement of a type-B retrovirus in the induction of thymic lymphomas. Virology. 1985 Jan 15;140(1):159–172. [PubMed]
  • Ball JK, Dekaban GA, McCarter JA, Loosmore SM. Molecular biological characterization of a highly leukaemogenic virus isolated from the mouse. III. Identity with mouse mammary tumour virus. J Gen Virol. 1983 Oct;64(Pt 10):2177–2190. [PubMed]
  • Ball JK, Diggelmann H, Dekaban GA, Grossi GF, Semmler R, Waight PA, Fletcher RF. Alterations in the U3 region of the long terminal repeat of an infectious thymotropic type B retrovirus. J Virol. 1988 Aug;62(8):2985–2993. [PMC free article] [PubMed]
  • Barberis A, Superti-Furga G, Busslinger M. Mutually exclusive interaction of the CCAAT-binding factor and of a displacement protein with overlapping sequences of a histone gene promoter. Cell. 1987 Jul 31;50(3):347–359. [PubMed]
  • Belgrader P, Dey R, Berezney R. Molecular cloning of matrin 3. A 125-kilodalton protein of the nuclear matrix contains an extensive acidic domain. J Biol Chem. 1991 May 25;266(15):9893–9899. [PubMed]
  • Berezney R, Coffey DS. Identification of a nuclear protein matrix. Biochem Biophys Res Commun. 1974 Oct 23;60(4):1410–1417. [PubMed]
  • Berezney R, Coffey DS. Nuclear protein matrix: association with newly synthesized DNA. Science. 1975 Jul 25;189(4199):291–293. [PubMed]
  • Berrios M, Osheroff N, Fisher PA. In situ localization of DNA topoisomerase II, a major polypeptide component of the Drosophila nuclear matrix fraction. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4142–4146. [PubMed]
  • Beutner U, Kraus E, Kitamura D, Rajewsky K, Huber BT. B cells are essential for murine mammary tumor virus transmission, but not for presentation of endogenous superantigens. J Exp Med. 1994 May 1;179(5):1457–1466. [PMC free article] [PubMed]
  • Blochlinger K, Jan LY, Jan YN. Transformation of sensory organ identity by ectopic expression of Cut in Drosophila. Genes Dev. 1991 Jul;5(7):1124–1135. [PubMed]
  • Bramblett D, Hsu CL, Lozano M, Earnest K, Fabritius C, Dudley J. A redundant nuclear protein binding site contributes to negative regulation of the mouse mammary tumor virus long terminal repeat. J Virol. 1995 Dec;69(12):7868–7876. [PMC free article] [PubMed]
  • Bresnick EH, Rories C, Hager GL. Evidence that nucleosomes on the mouse mammary tumor virus promoter adopt specific translational positions. Nucleic Acids Res. 1992 Feb 25;20(4):865–870. [PMC free article] [PubMed]
  • Choi YW, Henrard D, Lee I, Ross SR. The mouse mammary tumor virus long terminal repeat directs expression in epithelial and lymphoid cells of different tissues in transgenic mice. J Virol. 1987 Oct;61(10):3013–3019. [PMC free article] [PubMed]
  • Cockerill PN, Garrard WT. Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell. 1986 Jan 31;44(2):273–282. [PubMed]
  • Cockerill PN, Yuen MH, Garrard WT. The enhancer of the immunoglobulin heavy chain locus is flanked by presumptive chromosomal loop anchorage elements. J Biol Chem. 1987 Apr 15;262(11):5394–5397. [PubMed]
  • Cordingley MG, Riegel AT, Hager GL. Steroid-dependent interaction of transcription factors with the inducible promoter of mouse mammary tumor virus in vivo. Cell. 1987 Jan 30;48(2):261–270. [PubMed]
  • Corley RB, Lund FE, Randall TD, King LB, Doerre S, Woodland DL. Mouse mammary tumor proviral gene expression in cells of the B lineage. Semin Immunol. 1992 Oct;4(5):287–296. [PubMed]
  • Cunningham JM, Purucker ME, Jane SM, Safer B, Vanin EF, Ney PA, Lowrey CH, Nienhuis AW. The regulatory element 3' to the A gamma-globin gene binds to the nuclear matrix and interacts with special A-T-rich binding protein 1 (SATB1), an SAR/MAR-associating region DNA binding protein. Blood. 1994 Aug 15;84(4):1298–1308. [PubMed]
  • Davie JR. The nuclear matrix and the regulation of chromatin organization and function. Int Rev Cytol. 1995;162A:191–250. [PubMed]
  • Diamond MI, Miner JN, Yoshinaga SK, Yamamoto KR. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science. 1990 Sep 14;249(4974):1266–1272. [PubMed]
  • Dickinson LA, Dickinson CD, Kohwi-Shigematsu T. An atypical homeodomain in SATB1 promotes specific recognition of the key structural element in a matrix attachment region. J Biol Chem. 1997 Apr 25;272(17):11463–11470. [PubMed]
  • Dickinson LA, Joh T, Kohwi Y, Kohwi-Shigematsu T. A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell. 1992 Aug 21;70(4):631–645. [PubMed]
  • 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 Jan;15(1):456–465. [PMC free article] [PubMed]
  • Dignam JD, Martin PL, Shastry BS, Roeder RG. Eukaryotic gene transcription with purified components. Methods Enzymol. 1983;101:582–598. [PubMed]
  • Dudley J, Risser R. Amplification and novel locations of endogenous mouse mammary tumor virus genomes in mouse T-cell lymphomas. J Virol. 1984 Jan;49(1):92–101. [PMC free article] [PubMed]
  • Dufort D, Nepveu A. The human cut homeodomain protein represses transcription from the c-myc promoter. Mol Cell Biol. 1994 Jun;14(6):4251–4257. [PMC free article] [PubMed]
  • Dworetzky SI, Fey EG, Penman S, Lian JB, Stein JL, Stein GS. Progressive changes in the protein composition of the nuclear matrix during rat osteoblast differentiation. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4605–4609. [PubMed]
  • Dworetzky SI, Wright KL, Fey EG, Penman S, Lian JB, Stein JL, Stein GS. Sequence-specific DNA-binding proteins are components of a nuclear matrix-attachment site. Proc Natl Acad Sci U S A. 1992 May 1;89(9):4178–4182. [PubMed]
  • Forrester WC, Takegawa S, Papayannopoulou T, Stamatoyannopoulos G, Groudine M. Evidence for a locus activation region: the formation of developmentally stable hypersensitive sites in globin-expressing hybrids. Nucleic Acids Res. 1987 Dec 23;15(24):10159–10177. [PMC free article] [PubMed]
  • Forrester WC, van Genderen C, Jenuwein T, Grosschedl R. Dependence of enhancer-mediated transcription of the immunoglobulin mu gene on nuclear matrix attachment regions. Science. 1994 Aug 26;265(5176):1221–1225. [PubMed]
  • Gabrielsen OS, Hornes E, Korsnes L, Ruet A, Oyen TB. Magnetic DNA affinity purification of yeast transcription factor tau--a new purification principle for the ultrarapid isolation of near homogeneous factor. Nucleic Acids Res. 1989 Aug 11;17(15):6253–6267. [PMC free article] [PubMed]
  • Gabrielsen OS, Huet J. Magnetic DNA affinity purification of yeast transcription factor. Methods Enzymol. 1993;218:508–525. [PubMed]
  • Georgatos SD, Meier J, Simos G. Lamins and lamin-associated proteins. Curr Opin Cell Biol. 1994 Jun;6(3):347–353. [PubMed]
  • Gerdes MG, Carter KC, Moen PT, Jr, Lawrence JB. Dynamic changes in the higher-level chromatin organization of specific sequences revealed by in situ hybridization to nuclear halos. J Cell Biol. 1994 Jul;126(2):289–304. [PMC free article] [PubMed]
  • Getzenberg RH. Nuclear matrix and the regulation of gene expression: tissue specificity. J Cell Biochem. 1994 May;55(1):22–31. [PubMed]
  • Gilead Z, Jeng YH, Wold WS, Sugawara K, Rho HM, Harter ML, Green M. Immunological identification of two adenovirus 2-induced early proteins possibly involved in cell transformation. Nature. 1976 Nov 18;264(5583):263–266. [PubMed]
  • Golovkina TV, Chervonsky A, Dudley JP, Ross SR. Transgenic mouse mammary tumor virus superantigen expression prevents viral infection. Cell. 1992 May 15;69(4):637–645. [PubMed]
  • Guo B, Odgren PR, van Wijnen AJ, Last TJ, Nickerson J, Penman S, Lian JB, Stein JL, Stein GS. The nuclear matrix protein NMP-1 is the transcription factor YY1. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10526–10530. [PubMed]
  • Hager DA, Burgess RR. Elution of proteins from sodium dodecyl sulfate-polyacrylamide gels, removal of sodium dodecyl sulfate, and renaturation of enzymatic activity: results with sigma subunit of Escherichia coli RNA polymerase, wheat germ DNA topoisomerase, and other enzymes. Anal Biochem. 1980 Nov 15;109(1):76–86. [PubMed]
  • Held W, Waanders GA, Shakhov AN, Scarpellino L, Acha-Orbea H, MacDonald HR. Superantigen-induced immune stimulation amplifies mouse mammary tumor virus infection and allows virus transmission. Cell. 1993 Aug 13;74(3):529–540. [PubMed]
  • Held W, Acha-Orbea H, MacDonald HR, Waanders GA. Superantigens and retroviral infection: insights from mouse mammary tumor virus. Immunol Today. 1994 Apr;15(4):184–190. [PubMed]
  • Herrscher RF, Kaplan MH, Lelsz DL, Das C, Scheuermann R, Tucker PW. The immunoglobulin heavy-chain matrix-associating regions are bound by Bright: a B cell-specific trans-activator that describes a new DNA-binding protein family. Genes Dev. 1995 Dec 15;9(24):3067–3082. [PubMed]
  • Hsu CL, Fabritius C, Dudley J. Mouse mammary tumor virus proviruses in T-cell lymphomas lack a negative regulatory element in the long terminal repeat. J Virol. 1988 Dec;62(12):4644–4652. [PMC free article] [PubMed]
  • Huang M, Lee JW, Peterson DO. Functional redundancy of octamer elements in the mouse mammary tumor virus promoter. Nucleic Acids Res. 1993 Nov 11;21(22):5235–5241. [PMC free article] [PubMed]
  • Jarman AP, Higgs DR. Nuclear scaffold attachment sites in the human globin gene complexes. EMBO J. 1988 Nov;7(11):3337–3344. [PubMed]
  • Karapetian O, Shakhov AN, Kraehenbuhl JP, Acha-Orbea H. Retroviral infection of neonatal Peyer's patch lymphocytes: the mouse mammary tumor virus model. J Exp Med. 1994 Oct 1;180(4):1511–1516. [PMC free article] [PubMed]
  • Käs E, Izaurralde E, Laemmli UK. Specific inhibition of DNA binding to nuclear scaffolds and histone H1 by distamycin. The role of oligo(dA).oligo(dT) tracts. J Mol Biol. 1989 Dec 5;210(3):587–599. [PubMed]
  • Kohwi-Shigematsu T, Kohwi Y. Torsional stress stabilizes extended base unpairing in suppressor sites flanking immunoglobulin heavy chain enhancer. Biochemistry. 1990 Oct 16;29(41):9551–9560. [PubMed]
  • Kusk P, Carlson KE, Warren BS, Hager GL. Role of the TATA box in transcription of the mouse mammary tumor virus long terminal repeat. Mol Endocrinol. 1995 Sep;9(9):1180–1192. [PubMed]
  • Lee WT, Prakash O, Klein D, Sarkar NH. Structural alterations in the long terminal repeat of an acquired mouse mammary tumor virus provirus in a T-cell leukemia of DBA/2 mice. Virology. 1987 Jul;159(1):39–48. [PubMed]
  • Lowenthal JW, Ballard DW, Bogerd H, Böhnlein E, Greene WC. Tumor necrosis factor-alpha activation of the IL-2 receptor-alpha gene involves the induction of kappa B-specific DNA binding proteins. J Immunol. 1989 May 1;142(9):3121–3128. [PubMed]
  • Lydersen BK, Pettijohn DE. Human-specific nuclear protein that associates with the polar region of the mitotic apparatus: distribution in a human/hamster hybrid cell. Cell. 1980 Nov;22(2 Pt 2):489–499. [PubMed]
  • Mailly F, Bérubé G, Harada R, Mao PL, Phillips S, Nepveu A. The human cut homeodomain protein can repress gene expression by two distinct mechanisms: active repression and competition for binding site occupancy. Mol Cell Biol. 1996 Oct;16(10):5346–5357. [PMC free article] [PubMed]
  • Maxam AM, Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. [PubMed]
  • Michalides R, Wagenaar E. Site-specific rearrangements in the long terminal repeat of extra mouse mammary tumor proviruses in murine T-cell leukemias. Virology. 1986 Oct 15;154(1):76–84. [PubMed]
  • Michalides R, Wagenaar E, Hilkens J, Hilgers J, Groner B, Hynes NE. Acquisition of proviral DNA of mouse mammary tumor virus in thymic leukemia cells from GR mice. J Virol. 1982 Sep;43(3):819–829. [PMC free article] [PubMed]
  • Michalides R, Wagenaar E, Weijers P. Rearrangements in the long terminal repeat of extra mouse mammary tumor proviruses in T-cell leukemias of mouse strain GR result in a novel enhancer-like structure. Mol Cell Biol. 1985 Apr;5(4):823–830. [PMC free article] [PubMed]
  • Nakagomi K, Kohwi Y, Dickinson LA, Kohwi-Shigematsu T. A novel DNA-binding motif in the nuclear matrix attachment DNA-binding protein SATB1. Mol Cell Biol. 1994 Mar;14(3):1852–1860. [PMC free article] [PubMed]
  • Neufeld EJ, Skalnik DG, Lievens PM, Orkin SH. Human CCAAT displacement protein is homologous to the Drosophila homeoprotein, cut. Nat Genet. 1992 Apr;1(1):50–55. [PubMed]
  • Nickerson JA, Blencowe BJ, Penman S. The architectural organization of nuclear metabolism. Int Rev Cytol. 1995;162A:67–123. [PubMed]
  • Nicolas JF, Wegmann D, Lebrun P, Kaiserlian D, Tovey J, Glasebrook AL. Relationship of B cell Fc receptors to T cell recognition of Mls antigen. Eur J Immunol. 1987 Nov;17(11):1561–1565. [PubMed]
  • Noller HF, Hoffarth V, Zimniak L. Unusual resistance of peptidyl transferase to protein extraction procedures. Science. 1992 Jun 5;256(5062):1416–1419. [PubMed]
  • Olnes MI, Kurl RN. Isolation of nuclear extracts from fragile cells: a simplified procedure applied to thymocytes. Biotechniques. 1994 Nov;17(5):828–829. [PubMed]
  • Phi-Van L, von Kries JP, Ostertag W, Strätling WH. The chicken lysozyme 5' matrix attachment region increases transcription from a heterologous promoter in heterologous cells and dampens position effects on the expression of transfected genes. Mol Cell Biol. 1990 May;10(5):2302–2307. [PMC free article] [PubMed]
  • Piña B, Brüggemeier U, Beato M. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell. 1990 Mar 9;60(5):719–731. [PubMed]
  • Richard-Foy H, Hager GL. Sequence-specific positioning of nucleosomes over the steroid-inducible MMTV promoter. EMBO J. 1987 Aug;6(8):2321–2328. [PubMed]
  • Ringold GM, Yamamoto KR, Bishop JM, Varmus HE. Glucocorticoid-stimulated accumulation of mouse mammary tumor virus RNA: increased rate of synthesis of viral RNA. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2879–2883. [PubMed]
  • Roberts MS, Fragoso G, Hager GL. Nucleosomes reconstituted in vitro on mouse mammary tumor virus B region DNA occupy multiple translational and rotational frames. Biochemistry. 1995 Sep 26;34(38):12470–12480. [PubMed]
  • Ross SR, Choy L, Graves RA, Fox N, Solevjeva V, Klaus S, Ricquier D, Spiegelman BM. Hibernoma formation in transgenic mice and isolation of a brown adipocyte cell line expressing the uncoupling protein gene. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7561–7565. [PubMed]
  • Ross SR, Graves RA, Greenstein A, Platt KA, Shyu HL, Mellovitz B, Spiegelman BM. A fat-specific enhancer is the primary determinant of gene expression for adipocyte P2 in vivo. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9590–9594. [PubMed]
  • Ross SR, Hsu CL, Choi Y, Mok E, Dudley JP. Negative regulation in correct tissue-specific expression of mouse mammary tumor virus in transgenic mice. Mol Cell Biol. 1990 Nov;10(11):5822–5829. [PMC free article] [PubMed]
  • Saitoh N, Goldberg IG, Wood ER, Earnshaw WC. ScII: an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure. J Cell Biol. 1994 Oct;127(2):303–318. [PMC free article] [PubMed]
  • Scheuermann RH, Chen U. A developmental-specific factor binds to suppressor sites flanking the immunoglobulin heavy-chain enhancer. Genes Dev. 1989 Aug;3(8):1255–1266. [PubMed]
  • Sharma S, King LB, Corley RB. Molecular events during B lymphocyte differentiation. Induction of endogenous mouse mammary tumor proviral envelope transcripts after B cell stimulation. J Immunol. 1988 Oct 1;141(7):2510–2518. [PubMed]
  • Skalnik DG, Strauss EC, Orkin SH. CCAAT displacement protein as a repressor of the myelomonocytic-specific gp91-phox gene promoter. J Biol Chem. 1991 Sep 5;266(25):16736–16744. [PubMed]
  • Staudt LM, Lenardo MJ. Immunoglobulin gene transcription. Annu Rev Immunol. 1991;9:373–398. [PubMed]
  • Stein GS, van Wijnen AJ, Stein JL, Lian JB, Bidwell JP, Montecino M. Nuclear architecture supports integration of physiological regulatory signals for transcription of cell growth and tissue-specific genes during osteoblast differentiation. J Cell Biochem. 1994 May;55(1):4–15. [PubMed]
  • Stief A, Winter DM, Strätling WH, Sippel AE. A nuclear DNA attachment element mediates elevated and position-independent gene activity. Nature. 1989 Sep 28;341(6240):343–345. [PubMed]
  • Tang Y, DeFranco DB. ATP-dependent release of glucocorticoid receptors from the nuclear matrix. Mol Cell Biol. 1996 May;16(5):1989–2001. [PMC free article] [PubMed]
  • Tremethick DJ, Molloy PL. High mobility group proteins 1 and 2 stimulate transcription in vitro by RNA polymerases II and III. J Biol Chem. 1986 May 25;261(15):6986–6992. [PubMed]
  • Truss M, Chalepakis G, Piña B, Barettino D, Brüggemeier U, Kalff M, Slater EP, Beato M. Transcriptional control by steroid hormones. J Steroid Biochem Mol Biol. 1992 Mar;41(3-8):241–248. [PubMed]
  • Valarché I, Tissier-Seta JP, Hirsch MR, Martinez S, Goridis C, Brunet JF. The mouse homeodomain protein Phox2 regulates Ncam promoter activity in concert with Cux/CDP and is a putative determinant of neurotransmitter phenotype. Development. 1993 Nov;119(3):881–896. [PubMed]
  • van Wijnen AJ, Bidwell JP, Fey EG, Penman S, Lian JB, Stein JL, Stein GS. Nuclear matrix association of multiple sequence-specific DNA binding activities related to SP-1, ATF, CCAAT, C/EBP, OCT-1, and AP-1. Biochemistry. 1993 Aug 24;32(33):8397–8402. [PubMed]
  • Vieira J, Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. [PubMed]
  • von Kries JP, Buhrmester H, Strätling WH. A matrix/scaffold attachment region binding protein: identification, purification, and mode of binding. Cell. 1991 Jan 11;64(1):123–135. [PubMed]
  • Wang R, Kobayashi R, Bishop JM. Cellular adherence elicits ligand-independent activation of the Met cell-surface receptor. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8425–8430. [PubMed]
  • Webb CF, Das C, Eaton S, Calame K, Tucker PW. Novel protein-DNA interactions associated with increased immunoglobulin transcription in response to antigen plus interleukin-5. Mol Cell Biol. 1991 Oct;11(10):5197–5205. [PMC free article] [PubMed]
  • Webb CF, Das C, Eneff KL, Tucker PW. Identification of a matrix-associated region 5' of an immunoglobulin heavy chain variable region gene. Mol Cell Biol. 1991 Oct;11(10):5206–5211. [PMC free article] [PubMed]
  • Wilson CJ, Chao DM, Imbalzano AN, Schnitzler GR, Kingston RE, Young RA. RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling. Cell. 1996 Jan 26;84(2):235–244. [PubMed]
  • Yamamoto KR. Steroid receptor regulated transcription of specific genes and gene networks. Annu Rev Genet. 1985;19:209–252. [PubMed]
  • Yanagawa S, Kakimi K, Tanaka H, Murakami A, Nakagawa Y, Kubo Y, Yamada Y, Hiai H, Kuribayashi K, Masuda T, et al. Mouse mammary tumor virus with rearranged long terminal repeats causes murine lymphomas. J Virol. 1993 Jan;67(1):112–118. [PMC free article] [PubMed]
  • Yang JN, Dudley J. Endogenous Mtv-8 or a closely linked sequence stimulates rearrangement of the downstream V kappa 9 gene. J Immunol. 1992 Aug 15;149(4):1242–1251. [PubMed]
  • Zaret KS, Yamamoto KR. Reversible and persistent changes in chromatin structure accompany activation of a glucocorticoid-dependent enhancer element. Cell. 1984 Aug;38(1):29–38. [PubMed]
  • Zong RT, Scheuermann RH. Mutually exclusive interaction of a novel matrix attachment region binding protein and the NF-muNR enhancer repressor. Implications for regulation of immunoglobulin heavy chain expression. J Biol Chem. 1995 Oct 13;270(41):24010–24018. [PubMed]

Articles from Molecular and Cellular Biology are provided here courtesy of American Society for Microbiology (ASM)