Transcription of laminin γ1 chain gene in rat mesangial cells: Constitutive and inducible RNA polymerase II recruitment and chromatin states

American Journal of Physiology - Renal Physiology

Volumn 294, Issue 3, 2008, Pages

  Nelson, Joel D ^a   Flanagin, Steve ^a   Kawata, Yasunobu ^a   Denisenko, Oleg ^a   Bomsztyk, Karol ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

egr 1; Elongation; Extracellular matrix; Fast ChIP; Histone; hnRNP K

Indexed keywords

HISTONE H3; LAMININ GAMMA1; LYSINE; PHORBOL 13 ACETATE 12 MYRISTATE; RNA POLYMERASE II; 12-O-UNDECADIENOYLPHORBOL-13-ACETATE; EARLY GROWTH RESPONSE FACTOR 1; EGR1 PROTEIN, RAT; HISTONE; LAMININ; MESSENGER RNA; PHORBOL 13 ACETATE 12 UNDECADIENOATE; PHORBOL ESTER;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE LOCUS; GENETIC TRANSCRIPTION; LIVER CELL CARCINOMA; MESANGIUM CELL; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; CELL LINE; COMPARATIVE STUDY; DRUG EFFECT; GENETICS; KINETICS; LIVER TUMOR; METABOLISM; TUMOR CELL LINE;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE; CELL LINE, TUMOR; CHROMATIN; EARLY GROWTH RESPONSE PROTEIN 1; HISTONES; KINETICS; LAMININ; LIVER NEOPLASMS; MESANGIAL CELLS; PHORBOL ESTERS; RATS; RNA POLYMERASE II; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 41149171670     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00299.2007     Document Type: Article

References (68)

1. Aberdam D, Virolle T, Simon-Assmann P. Transcriptional regulation of laminin gene expression. Microsc Res Tech 51: 228-237, 2000.
2. Abrass CK, Berfield AK, Ryan MC, Carter WG, Hansen KM. Abnormal development of glomerular endothelial and mesangial cells in mice with targeted disruption of the lama3 gene. Kidney Int 70: 1062-1071, 2006.
3. Aumailley M, Bruckner-Tuderman L, Carter WG, Deutzmann R, Edgar D, Ekblom P, Engel J, Engvall E, Hohenester E, Jones JC, Kleinman HK, Marinkovich MP, Martin GR, Mayer U, Meneguzzi G, Miner JH, Miyazaki K, Patarroyo M, Paulsson M, Quaranta V, Sanes JR, Sasaki T, Sekiguchi K, Sorokin LM, Talts JF, Tryggvason K, Uitto J, Virtanen I, von der Mark K, Wewer UM, Yamada Y, Yurchenco PD. A simplified laminin nomenclature. Matrix Biol 24: 326-332, 2005.
4. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837, 2007.
5. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D. FACT facilitates transcription-dependent nucleosome alteration. Science 301: 1090-1093, 2003.
6. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas EJ 3rd, Gingeras TR, Schreiber SL, Lander ES. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169-181, 2005.
7. Bernstein BE, Meissner A, Lander ES. The mammalian epigenome. Cell 128: 669-681, 2007.
8. Bomsztyk K, Denisenko O, Ostrowski J. hnRNP K: one protein multiple processes. Bioessays 26: 629-638, 2004.
9. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043, 2002.
10. Carey M, Li B, Workman JL. RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol Cell 24: 481-487, 2006.
11. Chen X, Wang J, Woltring D, Gerondakis S, Shannon MF. Histone dynamics on the interleukin-2 gene in response to T-cell activation. Mol Cell Biol 25: 3209-3219, 2005.
12. Chen Y, Keller JM. Transcriptional state and chromatin structure of the murine entactin and laminin gamma1 genes. J Cell Biochem 82: 225-233, 2001.
13. Denisenko O, Shnyreva M, Suzuki H, Bomsztyk K. Point mutations in the WD40 domain of eed block its interaction with ezh2. Mol Cell Biol 18: 5634-5642, 1998.
14. ENCODE. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816, 2007.
15. Fukui M, Nakamura T, Ebihara I, Shirato I, Tomino Y, Koide H. ECM gene expression and its modulation by insulin in diabetic rats. Diabetes 41: 1520-1527, 1992.
16. Gerber M, Shilatifard A. Transcriptional elongation by RNA polymerase II and histone methylation. J Biol Chem 278: 26303-26306, 2003.
17. Guenther MG, Jenner RG, Chevalier B, Nakamura T, Croce CM, Canaani E, Young RA. Global and Hox-specific roles for the MLL1 methyltransferase. Proc Natl Acad Sci USA 102: 8603-8608, 2005.
18. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318, 2007.
19. Higaki Y, Schullery D, Kawata Y, Shnyreva M, Abrass C, Bomsztyk K. Synergistic activation of the rat laminin gamma1 chain promoter by the gut-enriched Kruppel-like factor (GKLF/KLF4) and Sp1. Nucleic Acids Res 30: 2270-2279, 2002.
20. Johnson DS, Mortazavi A, Myers RM, Wold B. Genome-wide mapping of in vivo protein-DNA interactions. Science 316: 1497-1502, 2007.
21. Kawata Y, Suzuki H, Higaki Y, Denisenko ON, Schullery D, Abrass C, Bomsztyk K. Bcn-1-element-dependent activation of the laminin g1 chain gene by the cooperative action of TFE3 and Smad proteins. J Biol Chem 277: 11375-11384, 2002.
22. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, Boone C, Emili A, Weissman JS, Hughes TR, Strahl BD, Grunstein M, Greenblatt JF, Buratowski S, Krogan NJ. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123: 593-605, 2005.
23. Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, Richmond TA, Wu Y, Green RD, Ren B. A high-resolution map of active promoters in the human genome. Nature 436: 876-880, 2005.
24. Kizer KO, Phatnani HP, Shibata Y, Hall H, Greenleaf AL, Strahl BD. A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol Cell Biol 25: 3305-3316, 2005.
25. Koch CM, Andrews RM, Flicek P, Dillon SC, Karaoz U, Clelland GK, Wilcox S, Beare DM, Fowler JC, Couttet P, James KD, Lefebvre GC, Bruce AW, Dovey OM, Ellis PD, Dhami P, Langford CF, Weng Z, Birney E, Carter NP, Vetrie D, Dunham I. The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res 17: 691-707, 2007.
26. Kouzarides T. Chromatin modifications and their function. Cell 128: 693-705, 2007.
27. Kristjuhan A, Walker J, Suka N, Grunstein M, Roberts D, Cairns BR, Svejstrup JQ. Transcriptional inhibition of genes with severe histone h3 hypoacetylation in the coding region. Mol Cell 10: 925-933, 2002.
28. Krogan NJ, Dover J, Wood A, Schneider J, Heidt J, Boateng MA, Dean K, Ryan OW, Golshani A, Johnston M, Greenblatt JF, Shilatifard A. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell 11: 721-729, 2003.
29. Lee CK, Shibata Y, Rao B, Strahl BD, Lieb JD. Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat Genet 36: 900-905, 2004.
30. Liang G, Lin JC, Wei V, Yoo C, Cheng JC, Nguyen CT, Weisenberger DJ, Egger G, Takai D, Gonzales FA, Jones PA. Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc Natl Acad Sci USA 101: 7357-7362, 2004.
31. Lietard J, Musso O, Theret N, L'Helgoualc'h A, Campion JP, Yamada Y, Clement B. Sp1-mediated transactivation of LamC1 promoter and coordinated expression of Laminin-γ and Sp1 in human hepatocellular carcinomas. Am J Pathol 151: 1663-1672, 1997.
32. Mason PB, Struhl K. Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol Cell 17: 831-840, 2005.
33. Merchant JL, Iyer GR, Taylor BR, Kitchen JR, Mortensen ER, Wang Z, Flintoft RJ, Michel JB, Bassel-Duby R. ZBP-89, a Kruppel-like zinc finger protein, inhibits epidermal growth factor induction of the gastrin promoter. Mol Cell Biol 16: 6644-6653, 1996.
34. Miao F, Natarajan R. Mapping global histone methylation patterns in the coding regions of human genes. Mol Cell Biol 25: 4650-4661, 2005.
35. Milne TA, Dou Y, Martin ME, Brock HW, Roeder RG, Hess JL. MLL associates specifically with a subset of transcriptionally active target genes. Proc Natl Acad Sci USA 102: 14765-14770, 2005.
36. Miner JH, Li C, Mudd JL, Go G, Sutherland AE. Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development 131: 2247-2256, 2004.
37. Morillon A. Is histone loss a common feature of DNA metabolism regulation? Biochem Cell Biol 84: 450-462, 2006.
38. Morillon A, Karabetsou N, Nair A, Mellor J. Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol Cell 18: 723-734, 2005.
39. Morillon A, Karabetsou N, O'Sullivan J, Kent N, Proudfoot N, Mellor J. Isw1 chromatin remodeling ATPase coordinates transcription elongation and termination by RNA polymerase II. Cell 115: 425-435, 2003.
40. Murray P, Edgar D. Regulation of programmed cell death by basement membranes in embryonic development. J Cell Biol 150: 1215-1221, 2000.
41. Nelson JD, Denisenko O, Bomsztyk K. Protocol for fast chromatin immunoprecipitation (ChIP) method. Nat Protoc 1: 179-185, 2006.
42. Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, MacIsaac KD, Rolfe PA, Conboy CM, Gifford DK, Fraenkel E. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet 39: 730-732, 2007.
43. Okada Y, Feng Q, Lin Y, Jiang Q, Li Y, Coffield VM, Su L, Xu G, Zhang Y. hDOT1L links histone methylation to leukemogenesis. Cell 121: 167-178, 2005.
44. Okada Y, Jiang Q, Lemieux M, Jeannotte L, Su L, Zhang Y. Leukaemic transformation by CALM-AF10 involves upregulation of Hoxa5 by hDOT1L. Nat Cell Biol 8: 1017-1024, 2006.
45. O'Neill BO, Suzuki H, Loomis WP, Denisenko O, Bomsztyk K. Cloning of the rat laminin γ1-chain gene promoter reveals motifs for recognition of multiple transcription factors. Am J Physiol Renal Physiol 273: F411-F420, 1997.
46. Ostrowski J, Kawata Y, Schullery DS, Denisenko ON, Bomsztyk K. Transient recruitment of the hnRNP K protein to inducibly transcribed gene loci. Nucleic Acids Res 31: 3954-3962, 2003.
47. Phillips SL, DeRubertis FR, Craven PA. Regulation of the laminin C1 promoter in cultured mesangial cells. Diabetes 48: 2083-2089, 1999.
48. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y. Role of histone H3 lysine 27 methylation in X inactivation. Science 300: 131-135, 2003.
49. Polesskaya A, Naguibneva I, Fritsch L, Duquet A, Ait-Si-Ali S, Robin P, Vervisch A, Pritchard LL, Cole P, Harel-Bellan A. CBP/p300 and muscle differentiation: no HAT, no muscle. EMBO J 20: 6816-6825, 2001.
50. Pugliese G, Pricci F, Pugliese F, Mene P, Lenti L, Andreani D, Galli G, Casini A, Bianchi S, Rotella CM, Umberto DM. Mechanisms of glucose-enhanced extracellular matrix accumulation in rat glomerular mesangial cells. Diabetes 43: 478-490, 1994.
51. Rasmussen EB, Lis JT. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc Natl Acad Sci USA 90: 7923-7927, 1993.
52. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T. Active genes are tri-methylated at K4 of histone H3. Nature 419: 407-411, 2002.
53. Saunders A, Core LJ, Lis JT. Breaking barriers to transcription elongation. Nat Rev Mol Cell Biol 7: 557-567, 2006.
54. Schubeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F, Gottschling DE, O'Neill LP, Turner BM, Delrow J, Bell SP, Groudine M. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 18: 1263-1271, 2004.
55. Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, Moore IK, Wang JP, Widom J. A genomic code for nucleosome positioning. Nature 442: 772-778, 2006.
56. Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75: 243-269, 2006.
57. Shilatifard A. Transcriptional elongation control by RNA polymerase II: a new frontier. Biochim Biophys Acta 1677: 79-86, 2004.
58. Shilatifard A, Conaway RC, Conaway JW. The RNA polymerase II elongation complex. Annu Rev Biochem 72: 693-715, 2003.
59. Smyth N, Vatansever HS, Murray P, Meyer M, Frie C, Paulsson M, Edgar D. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J Cell Biol 144: 151-160, 1999.
60. Spencer CA, Groudine M. Transcription elongation and eukaryotic gene regulation. Oncogene 5: 777-785, 1990.
61. Studitsky VM, Walter W, Kireeva M, Kashlev M, Felsenfeld G. Chromatin remodeling by RNA polymerases. Trends Biochem Sci 29: 127-135, 2004.
62. Suzuki H, O'Neill BC, Suzuki Y, Denisenko ON, Bomsztyk K. Activation of a nuclear DNA-binding protein recognized by a transcriptional element, bcn-1, from the laminin B2 chain gene promoter. J Biol Chem 271: 18981-18988, 1996.
63. Thomas MC, Chiang CM. The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41: 105-178, 2006.
64. Tunggal P, Smyth N, Paulsson M, Ott MC. Laminins: structure and genetic regulation. Microsc Res Tech 51: 214-227, 2000.
65. Van Seuningen I, Ostrowski J, Bomsztyk K. Description of an IL-1-responsive kinase that phosphorylates the K protein. Enhancement of phosphorylation by sequence-selective DNA and RNA motifs. Biochemistry 34: 5644-5650, 1995.
66. Vanden Heuvel GB, Leardkamolkarn V, St. John PL, Abrahamson DR. Carboxy terminal sequence and synthesis of rat kidney laminin γ1 chain. Kidney Int 49: 752-760, 1996.
67. Vermeulen M, Mulder KW, Denissov S, Pijnappel WW, van Schaik FM, Varier RA, Baltissen MP, Stunnenberg HG, Mann M, Timmers HT. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131: 58-69, 2007.
68. Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, Wu C, Allis CD. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442: 86-90, 2006.