The Ajuba LIM domain protein is a corepressor for SNAG domain-mediated repression and participates in nucleocytoplasmic shuttling

Cancer Research

Volumn 67, Issue 19, 2007, Pages 9097-9106

  Ayyanathan, Kasirajan ^a,d   Peng, Hongzhuang ^a   Hou, Zhaoyuan ^a   Fredericks, William J ^a   Goyal, Rakesh K ^c   Langer, Ellen M ^b   Longmore, Gregory D ^b   Rauscher III, Frank J ^a  

^a WISTAR INSTITUTE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^d FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; GROWTH FACTOR INDEPENDENCE 1; HISTONE; LIM PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN SNAG; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AJUBA; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; ASSAY; CARCINOGENESIS; CELL NUCLEUS; CHROMATIN IMMUNOPRECIPITATION; CYTOPLASM; EPITHELIUM; GENE REPRESSION; IN VITRO STUDY; IN VIVO STUDY; MESENCHYME; MESENCHYME CELL; METASTASIS; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; ONCOGENE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTO ONCOGENE; REPORTER GENE; SIGNAL TRANSDUCTION; T CELL LYMPHOMA; TWO HYBRID ASSAY; YEAST;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL NUCLEUS; CYTOPLASM; HOMEODOMAIN PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; PAIRED BOX TRANSCRIPTION FACTORS; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 35148851978     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-2987     Document Type: Article

References (53)

1. Hamilton AT, Huntley S, Kim J, Branscomb E, Stubbs L. Lineage-specific expansion of KRAB zinc-finger transcription factor genes: implications for the evolution of vertebrate regulatory networks. Cold Spring Harb Symp Quant Biol 2003;68:131-40.
2. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007;447:407-12.
3. Kim S, Na JG, Hampsey M, Reinberg D. The Dr1/DRAP1 heterodimer is a global repressor of transcription in vivo. Proc Natl Acad Sci U S A 1997;94:820-5.
4. Fisher AL, Ohsako S, Caudy M. The WRPW motif of the hairy-related basic helix-loop-helix repressor proteins acts as a 4-amino-acid transcription repression and protein-protein interaction domain. Mol Cell Biol 1996;16:2670-7.
5. You A, Tong JK, Grozinger CM, Schreiber SL. CoREST is an integral component of the CoREST-human histone deacetylase complex. Proc Natl Acad Sci U S A 2001;98:1454-8.
6. Friedman JR, Fredericks WJ, Jensen DE, et al. KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev 1996;10:2067-78.
7. Hemavathy K, Guru SC, Harris J, Chen JD, Ip YT. Human Slug is a repressor that localizes to sites of active transcription. Mol Cell Biol 2000;20:5087-95.
8. Nakakura EK, Watkins DN, Schuebel KE, et al. Mammalian Scratch: a neural-specific Snail family transcriptional repressor. Proc Natl Acad Sci U S A 2001;98:4010-5.
9. Nibu Y, Zhang H, Bajor E, Barolo S, Small S, Levine M. dCtBP mediates transcriptional repression by Knirps, Kruppel and Snail in the Drosophila embryo. EMBO J 1998;17:7009-20.
10. Grimes HL, Chan TO, Zweidler-McKay PA, Tong B, Tsichlis PN. The Gfi-1 proto-oncoprotein contains a novel transcriptional repressor domain, SNAG, inhibits G1 arrest induced by interleukin-2 withdrawal. Mol Cell Biol 1996;16:6263-72.
11. Gilks CB, Bear SE, Grimes HL, Tsichlis PN. Progression of interleukin-2 (IL-2)-dependent rat T cell lymphoma lines to IL-2-independent growth following activation of a gene (Gfi-1) encoding a novel zinc finger protein. Mol Cell Biol 1993;13:1759-68.
12. Zornig M, Schmidt T, Karsunky H, Grzeschiczek A, Moroy T. Zinc finger protein GFI-1 cooperates with myc and pim-1 in T-cell lymphomagenesis by reducing the requirements for IL-2. Oncogene 1996;12:1789-801.
13. Zweidler-Mckay PA, Grimes HL, Flubacher MM, Tsichlis PN. Gfi-1 encodes a nuclear zinc finger protein that binds DNA and functions as a transcriptional repressor. Mol Cell Biol 1996;16:4024-34.
14. Grimes HL, Gilks CB, Chan TO, Porter S, Tsichlis PN. The Gfi-1 protooncoprotein represses Bax expression and inhibits T-cell death. Proc Natl Acad Sci U S A 1996;93:14569-73.
15. Karsunky H, Zeng H, Schmidt T, et al. Inflammatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1. Nat Genet 2002;30:295-300.
16. Saleque S, Cameron S, Orkin SH. The zinc-finger proto-oncogene Gfi-1b is essential for development of the erythroid and megakaryocytic lineages. Gene s Dev 2002;16:301-6.
17. Hock H, Hamblen MJ, Rooke HM, et al. Intrinsic requirement for zinc finger transcription factor Gfi-1 in neutrophil differentiation. Immunity 2003;18:109-20.
18. Manzanares M, Locascio A, Nieto MA. The increasing complexity of the Snail gene superfamily in metazoan evolution. Trend s Genet 2001;17:178-81.
19. Mayor R, Morgan R, Sargent MG. Induction of the prospective neural crest of Xenopus. Development 1995;121:767-77.
20. Inukai T, Inoue A, Kurosawa H, et al. SLUG, a ces-1-related zinc finger transcription factor gene with antiapoptotic activity, is a downstream target of the E2A-HLF oncoprotein. Mol Cell 1999;4:343-52.
21. Cano A, Perez-Moreno MA, Rodrigo I, et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000;2:76-83.
22. Batlle E, Sancho E, Franci C, et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2000;2:84-9.
23. Goyal RK, Lin P, Kanungo J, Payne AS, Muslin AJ, Longmore GD. Ajuba, a novel LIM protein, interacts with Grb2, augments mitogen-activated protein kinase activity in fibroblasts, and promotes meiotic maturation of Xenopus oocytes in a Grb2- and Ras-dependent manner. Mol Cell Biol 1999;19:4379-89.
24. Kanungo J, Pratt SJ, Marie H, Longmore GD. Ajuba, a cytosolic LIM protein, shuttles into the nucleus and affects embryonal cell proliferation and fate decisions. Mol Biol Cell 2000;11:3299-313.
25. Kiss H, Kedra D, Yang Y, et al. A novel gene containing LIM domains (LIMD1) is located within the common eliminated region 1 (C3CER1) in 3p21.3. Hum Genet 1999;105:552-9.
26. Ayyanathan K, Lechner MS, Bell P, et al. Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. Genes Dev 2003;17:1855-69.
27. Ayyanathan K, Fredericks WJ, Berking C, et al. Hormone-dependent tumor regression in vivo by an inducible transcriptional repressor directed at the PAX3-FKHR oncogene. Cancer Res 2000;60:5803-14.
28. Ryan RF, Schultz DC, Ayyanathan K, et al. KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Kruppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol Cell Biol 1999;19:4366-78.
29. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ III. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 2002;16:919-32.
30. Fredericks WJ, Ayyanathan K, Herlyn M, Friedman JR, Rauscher FJ III. An engineered PAX3-KRAB transcriptional repressor inhibits the malignant phenotype of alveolar rhabdomyosarcoma cells harboring the endogenous PAX3-FKHR oncogene. Mol Cell Biol 2000;20:5019-31.
31. Hollenberg SM, Sternglanz R, Cheng PF, Weintraub H. Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol Cell Biol 1995;15:3813-22.
32. Freyd G, Kim SK, Horvitz HR. Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature 1990;344:876-9.
33. Kadrmas JL, Beckerle MC. The LIM domain: from the cytoskeleton to the nucleus. Nat Rev Mol Cell Biol 2004;5:920-31.
34. Nix DA, Beckerle MC. Nuclear-cytoplasmic shuttling of the focal contact protein, zyxin: a potential mechanism for communication between sites of cell adhesion and the nucleus. J Cell Biol 1997;138:1139-47.
35. Peng H, Begg GE, Schultz DC, et al. Reconstitution of the KRAB-KAP-1 repressor complex: a model system for defining the molecular anatomy of RING-B box-coiled-coil domain-mediated protein-protein interactions. J Mol Biol 2000;295:1139-62.
36. Peng H, Begg GE, Harper SL, Friedman JR, Speicher DW, Rauscher FJ III. Biochemical analysis of the Kruppel-associated box (KRAB) transcriptional repression domain. J Biol Chem 2000;275:18000-10.
37. Peng H, Gibson LC, Capili AD, et al. The structurally disordered KRAB repression domain is incorporated into a protease resistant core upon binding to KAP-1-RBCC domain. J Mol Biol 2007;370:269-89.
38. Li X, Peng H, Schultz DC, Lopez-Guisa JM, Rauscher FJ III, Marmorstein R. Structure-function studies of the BTB/POZ transcriptional repression domain from the promyelocytic leukemia zinc finger oncoprotein. Cancer Res 1999;59:5275-82.
39. Wadman IA, Osada H, Grutz GG, et al. The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J 1997;16:3145-57.
40. Visvader JE, Mao X, Fujiwara Y, Hahm K, Orkin SH. The LIM-domain binding protein Ldb1 and its partner LMO2 act as negative regulators of erythroid differentiation. Proc Natl Acad Sci U S A 1997;94:13707-12.
41. McLoughlin P, Ehler E, Carlile G, Licht JD, Schafer BW. The LIM-only protein DRAL/FHL2 interacts with and is a corepressor for the promyelocytic leukemia zinc finger protein. J Biol Chem 2002;277:37045-53.
42. Morlon A, Sassone-Corsi P. The LIM-only protein FHL2 is a serum-inducible transcriptional coactivator of AP-1. Proc Natl Acad Sci U S A 2003;100:3977-82.
43. Sugihara TM, Bach I, Kioussi C, Rosenfeld MG, Andersen B. Mouse deformed epidermal autoregulatory factor 1 recruits a LIM domain factor, LMO-4, and CLIM coregulators. Proc Natl Acad Sci U S A 1998;95:15418-23.
44. Howard PW, Maurer RA. A point mutation in the LIM domain of Lhx3 reduces activation of the glycoprotein hormone α-subunit promoter. J Biol Chem 2001;276:19020-6.
45. Chang DF, Belaguli NS, Iyer D, et al. Cysteine-rich LIM-only proteins CRP1 and CRP2 are potent smooth muscle differentiation cofactors. Dev Cell 2003;4:107-18.
46. Muller JM, Metzger E, Greschik H, et al. The transcriptional coactivator FHL2 transmits Rho signals from the cell membrane into the nucleus. EMBO J 2002;21:736-48.
47. Ng EK, Chan KK, Wong CH, et al. Interaction of the heart-specific LIM domain protein, FHL2, with DNA-binding nuclear protein, hNP220. J Cell Biochem 2002;84:556-66.
48. Taniguchi Y, Furukawa T, Tun T, Han H, Honjo T. LIM protein KyoT2 negatively regulates transcription by association with the RBP-J DNA-binding protein. Mol Cell Biol 1998;18:644-54.
49. Brown S, McGrath MJ, Ooms LM, Gurung R, Maimone MM, Mitchell CA. Characterization of two isoforms of the skeletal muscle LIM protein 1, SLIM1. Localization of SLIM1 at focal adhesions and the isoform slimmer in the nucleus of myoblasts and cytoplasm of myotubes suggests distinct roles in the cytoskeleton and in nuclear-cytoplasmic communication. J Biol Chem 1999;274:27083-91.
50. Degenhardt YY, Silverstein S. Interaction of zyxin, a focal adhesion protein, with the e6 protein from human papillomavirus type 6 results in its nuclear translocation. J Virol 2001;75:11791-802.
51. Petit MM, Fradelizi J, Golsteyn RM, et al. LPP, an actin cytoskeleton protein related to zyxin, harbors a nuclear export signal and transcriptional activation capacity. Mol Biol Cell 2000;11:117-29.
52. Peinado H, Ballestar E, Esteller M, Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol 2004;24:306-19.
53. Bach I, Rodriguez-Esteban C, Carriere C, et al. RLIM inhibits functional activity of LIM homeodomain transcription factors via recruitment of the histone deacetylase complex. Nat Genet 1999;22:394-9.