A Brg1 mutation that uncouples ATPase activity from chromatin remodeling reveals an essential role for SWI/SNF-related complexes in β-globin expression and erythroid development

Genes and Development

Volumn 19, Issue 23, 2005, Pages 2849-2861

  Bultman, Scott J ^a   Gebuhr, Thomas C ^a,b   Magnuson, Terry ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

globin; ATPase; Brg1; Chromatin remodeling; Locus control region; SWI SNF

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BETA GLOBIN; DEOXYRIBONUCLEASE I; ETHYLNITROSOUREA; HISTONE;

ANEMIA; ANIMAL CELL; ARTICLE; BETA CHAIN; BLASTOCYTE; BRAHMA RELATED 1 GENE; CELL DEATH; CELL LINEAGE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ERYTHROPOIESIS; FEMALE; GENE; GENE LOCUS; GENE MUTATION; GESTATIONAL AGE; HOMOZYGOSITY; MALE; MOUSE; MUTAGENIC ACTIVITY; NONHUMAN; NULL ALLELE; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; TRANSCRIPTION INITIATION;

ACETYLATION; ADENOSINE TRIPHOSPHATASES; ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA HELICASES; DNA METHYLATION; EMBRYO; ERYTHROPOIESIS; GLOBINS; HISTONES; MICE; MICE, MUTANT STRAINS; MULTIPROTEIN COMPLEXES; MUTATION; NUCLEAR PROTEINS; ORGANOGENESIS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 28444439242     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1364105     Document Type: Article

References (54)

1. Armstrong, J.A., Bieker, J.J., and Emerson, B.M. 1998. A SWI/SNF-related chromatin remodeling complex, E-RC1, is required for tissue-specific transcriptional regulation by EKLF in vitro. Cell 95: 93-104.
2. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. 1992. Current protocols in molecular biology. Greene Publishing Associates/Wiley Interscience, New York.
3. Banine, F., Bartlett, C., Gunawardena, R., Muchardt, C., Yaniv, M., Knudsen, E.S., Weissman, B.E., and Sherman, L.S. 2005. SWI/SNF chromatin-remodeling factors induce changes in DNA methylation to promote transcriptional activation. Cancer Res. 65: 3542-3547.
4. Bender, M.A., Reik, A., Close, J., Telling, A., Epner, E., Fiering, S., Hardison, R., and Groudine, M. 1998. Description and targeted deletion of 5′ hypersensitive site 5 and 6 of the mouse β-globin locus control region. Blood 92: 4394-4403.
5. Bultman, S., Gebuhr, T., Yee, D., La Mantia, C., Nicholson, J., Gilliam, A., Randazzo, F., Metzger, D., Chambon, P., Crabtree, G., et al. 2000. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6: 1287-1295.
6. Chi, T.H., Wan, M., Lee, P.P., Akashi, K., Metzger, D., Chambon, P., Wilson, C.B., and Crabtree, G.R. 2003. Sequential roles of Brg, the ATPase subunit of BAF chromatin remodeling complexes, in thymocyte development. Immunity 19: 169-182.
7. Dennis, K., Fan, T., Geiman, T., Yan, Q., and Muegge, K. 2001. Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes & Dev. 15: 2940-2944.
8. Drissen, R., von Lindern, M., Kolbus, A., Driegen, S., Steinlein, P., Beug, H., Grosveld, F., and Philipsen, S. 2005. The erythroid phenotype of EKLF-null mice: Defects in hemoglobin metabolism and membrane stability. Mol. Cell. Biol. 25: 5205-5214.
9. Duan, Z., Stamatoyannopoulos, G., and Li, Q. 2001. Role of NF-Y in in vivo regulation of the γ-globin gene. Mol. Cell. Biol. 21: 3083-3095.
10. Durr, H., Korner, C., Muller, M., Hickmann, V., and Hopfner, K.P. 2005. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 121: 363-373.
11. Eisen, J.A., Sweder, K.S., and Hanawalt, P.C. 1995. Evolution of the SNF2 family of proteins: Subfamilies with distinct sequences and functions. Nucleic Acids Res. 23: 2715-2723.
12. Falconer, D.S. and Isaacson, J.H. 1966. Curly-whiskers and its linkage with tail-kinks in linkage group II of the mouse. Genet. Res. 8: 111-113.
13. Forsberg, E.C., Downs, K.M., Christensen, H.M., Im, H., Nuzzi, P.A., and Bresnick, E.H. 2000. Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc. Natl. Acad. Sci. 97: 14494-14499.
14. Fry, C.J. and Peterson, C.L. 2001. Chromatin remodeling enzymes: Who's on first? Curr. Biol. 11: R185-R197.
15. Fujiwara, Y., Browne, C.P., Cunniff, K., Goff, S.C., and Orkin, S.H. 1996. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc. Natl. Acad. Sci. 93: 12355-12358.
16. Gebuhr, T.C., Kovalev, G.I., Bultman, S., Godfrey, V., Su, L., and Magnuson, T. 2003. The role of Brg1, a catalytic subunit of mammalian chromatin-remodeling complexes, in T cell development. J. Exp. Med. 198: 1937-1949.
17. Gibbons, R.J., McDowell, T.L., Raman, S., O'Rourke, D.M., Garrick, D., Ayyub, H., and Higgs, D.R. 2000. Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat. Genet. 24: 368-371.
18. Guidi, C.J., Sands, A.T., Zambrowicz, B.P., Turner, T.K., Demers, D.A, Webster, W., Smith, T.W., Imbalzano, A.N., and Jones, S.N. 2001. Disruption of Ini1 leads to peri-implantation lethality and tumorigenesis in mice. Mol. Cell. Biol. 21: 3598-3603.
19. Holstege, F.C., Jennings, E.G., Wyrick, J.J., Lee, T.I., Hengartner, C.J., Green, M.R., Golub, T.R., Lander, E.S., and Young, R.A. 1998. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95: 717-728.
20. Horak, C.E., Mahajan, M.C., Luscombe, N.M., Gerstein, M., Weissman, S.M., and Snyder, M. 2002. GATA-1 binding sites mapped in the β-globin locus by using mammalian chIp-chip analysis. Proc. Natl. Acad. Sci. 99: 2924-2929.
21. Kadam, S. and Emerson, B.M. 2003. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol. Cell 11: 377-389.
22. Kim, J.K., Huh, S.O., Choi, H., Lee, K.S., Shin, D., Lee, C., Nam, J.S., Kim, H., Chung, H., Lee, H.W., et al. 2001. Srg3, a mouse homolog of yeast SWI3, is essential for early embryogenesis and involved in brain development. Mol. Cell. Biol. 21: 7787-7795.
23. Kina, T., Ikuta, K., Takayama, E., Wada, K., Majumdar, A.S., Weissman, I.L., and Katsura, Y. 2000. The monoclonal antibody TER-119 recognizes a molecule associated with glycophorin A and specifically marks the late stages of murine erythroid lineage. Br. J. Haematol. 109: 280-287.
24. Klochendler-Yeivin, A., Fiette, L., Barra, J., Muchardt, C., Babinet, C., and Yaniv, M. 2000. The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. EMBO Rep. 1: 500-506.
25. Krebs, J.E., Fry, C.J., Samuels, M.L., and Peterson, C.L. 2000. Global role for chromatin remodeling enzymes in mitotic gene expression. Cell 102: 587-598.
26. Lee, J.S., Ngo, H., Kim, D., and Chung, J.H. 2000. Erythroid Kruppel-like factor is recruited to the CACCC box in the β-globin promoter but not to the CACCC box in the γ-globin promoter: The role of the neighboring promoter elements. Proc. Natl. Acad. Sci. 97: 2468-2473.
27. Lemon, B. and Tjian, R. 2000. Orchestrated response: A symphony of transcription factors for gene control. Genes & Dev. 14: 2551-2569.
28. Levings, P.P. and Bungert, J. 2002. The human β-globin locus control region. Eur. J. Biochem. 269: 1589-1599.
29. McArthur, M., Gerum, S., and Stamatoyannopoulos, G. 2001. Quantification of DNaseI-sensitivity by real-time PCR: Quantitative analysis of DNaseI-hypersensitivity of the mouse β-globin LCR. J. Mol. Biol. 313: 27-34.
30. McDevitt, M.A., Shivdasani, R.A., Fujiwara, Y., Yang, H., and Orkin, S.H. 1997. A 'knockdown' mutation created by cis-element gene targeting reveals the dependence of erythroid cell maturation on the level of transcription factor GATA-1. Proc. Natl. Acad. Sci. 94: 6781-6785.
31. Medina, P.P., Carretero, J., Fraga, M.F., Esteller, M., Sidransky, D., and Sanchez-Cespedes, M. 2004. Genetic and epigenetic screening for gene alterations of the chromatin-remodeling factor, SMARCA4/BRG1, in lung tumors. Genes Chromosomes Cancer 41: 170-177.
32. Meehan, R.R., Pennings, S., and Stancheva, I. 2001. Lashings of DNA methylation, forkfuls of chromatin remodeling. Genes & Dev. 15: 3231-3236.
33. Mohrmann, L. and Verrijzer, C.P. 2005. Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim. Biophys. Acta 1681: 59-73.
34. Mucenski, M.L., McLain, K., Kier, A.B., Swerdlow, S.H., Schreiner, C.M., Miller, T.A., Pietryga, D.W., Scott Jr., W.J., and Potter, S.S. 1991. A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell 65: 677-689.
35. Narlikar, G.J., Fan, H.Y., and Kingston, R.E. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108: 475-487.
36. O'Neill, D., Yang, J., Erdjument-Bromage, H., Bornschlegel, K., Tempst, P., and Bank, A. 1999. Tissue-specific and developmental stage-specific DNA binding by a mammalian SWI/ SNF complex associated with human fetal-to-adult globin gene switching. Proc. Natl. Acad. Sci. 96: 349-354.
37. Pray-Grant, M.G., Daniel, J.A., Schieltz, D., Yates III, J.R., and Grant, P.A. 2005. Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433: 434-438.
38. Reyes, J.C., Barra, J., Muchardt, C., Camus, A., Babinet, C., and Yaniv, M. 1998. Altered control of cellular proliferation in the absence of mammalian brahma (SNF2α). EMBO J. 17: 6979-6991.
39. Richmond, E. and Peterson, C.L. 1996. Functional analysis of the DNA-stimulated ATPase domain of yeast SWI2/SNF2. Nucleic Acids Res. 24: 3685-3692.
40. Roberts, C.W., Galusha, S.A., McMenamin, M.E., Fletcher, C.D., and Orkin, S.H. 2000. Haploinsufficiency of Snf5 (integrase interactor 1) predisposes to malignant rhabdoid tumors in mice. Proc. Natl. Acad. Sci. 97: 13796-13800.
41. Smith, C.L. and Peterson, C.L. 2005. A conserved swi2/snf2 ATPase motif couples ATP hydrolysis to chromatin remodeling. Mol. Cell. Biol. 25: 5880-5892.
42. Smith, C.L., Horowitz-Scherer, R., Flanagan, J.F., Woodcock, C.L., and Peterson, C.L. 2003. Structural analysis of the yeast SWI/SNF chromatin remodeling complex. Nat. Struct. Biol. 10: 141-145.
43. Struhl, K. 1999. Fundamentally different logic of gene regulation in eukaryotes and prokaryotes. Cell 98: 1-4.
44. Sudarsanam, P. and Winston, F. 2000. The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet. 16: 345-351.
45. Sudarsanam, P., Iyer, V.R., Brown, P.O., and Winston, F. 2000. Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 97: 3364-3369.
46. Tamkun, J.W. 1995. The role of brahma and related proteins in transcription and development. Curr. Opin. Genet. Dev. 5: 473-477.
47. Tamkun, J.W., Deuring, R., Scott, M.P., Kissinger, M., Pattatucci, A.M., Kaufman, T.C., and Kennison, J.A. 1992. brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68: 561-572.
48. Thoma, N.H., Czyzewski, B.K., Alexeev, A.A., Mazin, A.V., Kowalczykowski, S.C., and Pavletich, N.P. 2005. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nat. Struct. Mol. Biol. 12: 350-356.
49. Trimborn, T., Gribnau, J., Grosveld, F., and Fraser, P. 1999. Mechanisms of developmental control of transcription in the murine α- and β-globin loci. Genes & Dev. 13: 112-124.
50. Uetsuki, T., Takagi, K., Sugiura, H., and Yoshikawa, K. 1996. Structure and expression of the mouse necdin gene. Identification of a postmitotic neuron-restrictive core promoter. J. Biol. Chem. 271: 918-924.
51. Uoshima, N., Ozawa, M., Kimura, S., Tanaka, K., Wada, K., Kobayashi, Y., and Kondo, M. 1995. Changes in c-Kit expression and effects of SCF during differentiation of human erythroid progenitor cells. Br. J. Haematol. 91: 30-36.
52. Wang, W., Cote, J., Xue, Y., Zhou, S., Khavari, P.A., Biggar, S.R., Muchardt, C., Kalpana, G.V., Goff, S.P., Yaniv, M., et al. 1996. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 15: 5370-5382.
53. Wojda, U., Noel, P., and Miller, J.L. 2002. Fetal and adult hemoglobin production during adult erythropoiesis: Coordinate expression correlates with cell proliferation. Blood 99: 3005-3013.
54. Wong, A.K., Shanahan, F., Chen, Y., Lian, L., Ha, P., Hendricks, K., Ghaffari, S., Iliev, D., Penn, B., Woodland, A.M., et al. 2000. BRG1, a component of the SWI-SNF complex, is mutated in multiple human tumor cell lines. Cancer Res. 60: 6171-6177.