Tandem LIM domains provide synergistic binding in the LMO4:Ldb1 complex

EMBO Journal

Volumn 23, Issue 18, 2004, Pages 3589-3598

  Deane, Janet E ^a   Ryan, Daniel P ^a   Sunde, Margaret ^a   Maher, Megan J ^a   Guss, J Mitchell ^a   Visvader, Jane E ^b   Matthews, Jacqueline M ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Ldb1; LIM; LMO4 domains; Protein interactions; Tandem binding

Indexed keywords

ADAPTOR PROTEIN; BINDING PROTEIN; HOMEODOMAIN PROTEIN; NUCLEAR PROTEIN; ONCOPROTEIN; PROTEIN LDB1; PROTEIN LIM; PROTEIN LIM HD; PROTEIN LMO4; UNCLASSIFIED DRUG;

ARTICLE; CARCINOGENESIS; CELL FATE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR INTERACTION; MUTATION; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; TWO HYBRID SYSTEM; YEAST;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; DRUG SYNERGISM; FACTOR XA; HOMEODOMAIN PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; TANDEM REPEAT SEQUENCES; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 5044224710     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600376     Document Type: Article

References (58)

1. Bach I (2000) The LIM domain: regulation by association. Mech Dev 91: 5-17
2. Bach I, Rodriguez-Esteban C, Carriere C, Bhushan A, Krones A, Rose DW, Glass CK, Andersen B, Izpisua Belmonte JC, Rosenfeld MG (1999) RLIM inhibits functional activity of LIM homeodomain transcription factors via recruitment of the histone deacetylase complex. Nat Genet 22: 394-399
3. Becker T, Ostendorff HP, Bossenz M, Schluter A, Becker CG, Peirano RI, Bach I (2002) Multiple functions of LIM domain-binding CLIM/NLI/Ldb cofactors during zebrafish development. Mech Dev 117: 75-85
4. Breen JJ, Agulnick AD, Westphal H, Dawid IB (1998) Interactions between LIM domains and the LIM domain-binding protein Ldb1. J Biol Chem 273: 4712-4717
5. Castagnetto JM, Hennessy SW, Roberts VA, Getzoff ED, Tainer JA, Pique ME (2002) MDB: the Metalloprotein Database and Browser at The Scripps Research Institute. Nucleic Acids Res 30: 379-382
6. Curtiss J, Heilig JS (1998) DeLIMiting development. BioEssays 20: 58-69
7. Dawid IB, Breen JJ, Toyama R (1998) LIM domains: multiple roles as adapters and functional modifiers in protein interactions. Trends Genet 14: 156-162
8. Deane JE, Mackay JP, Kwan AH, Sum EY, Visvader JE, Matthews JM (2003a) Structural basis for the recognition of ldb1 by the N-terminal LIM domains of LMO2 and LMO4. EMBO J 22: 2224-2233
9. Deane JE, Maher MJ, Langley DB, Graham SC, Visvader JE, Guss JM, Matthews JM (2003b) Crystallization of FLINC4, an intramolecular LMO4-ldb1 complex. Acta Crystallogr D 59: 1484-1486
10. Deane JE, Sum E, Mackay JP, Lindeman GJ, Visvader JE, Matthews JM (2001) Design, production and characterization of FLIN2 and FLIN4: the engineering of intramolecular LMO/ldb1 complexes. Prot Eng 14: 493-494
11. Freyd G, Kim SK, Horvitz HR (1990) Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature 344: 876-879
12. Gill GN (1995) The enigma of LIM domains. Structure 3: 1285-1289
13. Grishin NV (2001) Treble clef finger-a functionally diverse zinc-binding structural motif. Nucleic Acids Res 29: 1703-1714
14. Grutz G, Forster A, Rabbitts TH (1998a) Identification of the LMO4 gene encoding an interaction partner of the LIM-binding protein LDB1/NLI1: a candidate for displacement by LMO proteins in T cell acute leukemia. Oncogene 17: 2799-2803
15. Grutz GG; Bucher K, Lavenir I, Larson T, Larson R, Rabbitts TH (1998b) The oncogenic T cell LIM protein Lmo2 forms part of a DNA-binding complex specifically in immature T cells. EMBO J 17: 4594-4605
16. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, McCormack MP, Wulffraat N, Leboulch P, Lim A, Osborne CS, Pawliuk R, Morillon E, Sorensen R, Foster A, Fraser P, Cohen JI, de Saint Basile G, Alexander I, Wintergerst U, Frebourg T, Aurias A, Stoppa-Lyonnet D, Romana S, Radford-Weiss I, Gross F, Valensi F, Delabesse E, Macintyre E, Sigaux F, Soulier J, Leiva LE, Wissler M, Prinz C, Rabbitts TH, Le Deist F, Fischer A, Cavazzana-Calvo M (2003) LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302: 415-419
17. Hahm K, Sum EYM, Fujiwara YJG, Lindeman GJ, Visvader JE, Orkin SH (2004) Defective neural tube closure and anteroposterior patterning in mice lacking the LIM protein Lmo4 or its interacting partner Deaf-1. Mol Cell Biol 24: 2074-2082
18. Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47: 110-119
19. Jurata LW, Gill GN (1997) Functional analysis of the nuclear LIM domain interactor NLI. Mol Cell Biol 17: 5688-5698
20. Jurata LW, Kenny DA, Gill GN (1996) Nuclear LIM interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development. Proc Natl Acad Sci USA 93: 11693-11698
21. Jurata LW, Pfaff SL, Gill GN (1998) The nuclear LIM domain interactor NLI mediates homo- and heterodimerization of LIM domain transcription factors. J Biol Chem 273: 3152-3157
22. Koradi R, Billeter M, Wüthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graphics 14: 51-55
23. Kowalski K, Czolij R, King GF, Crossley M, Mackay JP (1999) The solution structure of the N-terminal zinc finger of GATA-1 reveals a specific binding face for the transcriptional co-factor FOG. J Biomol NMR 13: 249-262
24. Lee B, Richards FM (1971) The interpretation of protein structures: estimation of static accessibility. J Mol Biol 55: 379-400
25. Matthews JM, Visvader JE (2003) LIM-domain-binding protein 1: a multifunctional cofactor that interacts with diverse proteins. EMBO Rep 4: 1132-1137
26. Milan M, Cohen SM (1999) Regulation of LIM homeodomain activity in vivo: a tetramer of dLDB and apterous confers activity and capacity for regulation by dLMO. Mol Cell 4: 267-273
27. Milan M, Diaz-Benjumea FJ, Cohen SM (1998) Beadex encodes an LMO protein that regulates apterous LIM-homeodomain activity in Drosophila wing development: a model for LMO oncogene function. Genes Dev 12: 2912-2920
28. Mizunuma H, Miyazawa J, Sanada K, Imai K (2003) The LIM-only protein, LMO4, and the LIM domain-binding protein, LDB1, expression in squamous cell carcinomas of the oral cavity. Br J Cancer 88: 1543-1548
29. Mukhopadhyay M, Teufel A, Yamashita T, Agulnick AD, Chen L, Downs KM, Schindler A, Grinberg A, Huang SP, Dorward D, Westphal H (2003) Functional ablation of the mouse Ldb1 gene results in severe patterning defects during gastrulation. Development 130: 495-505
30. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53: 240-255
31. Omichinski JG, Clore GM, Schaad O, Felsenfeld G, Trainor C, Appella E, Stahl SJ, Gronenborn AM (1993) NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science 261: 438-446
32. Perez-Alvarado GC, Miles C, Michelsen JW, Louis HA, Winge DR, Beckerle MC, Summers MF (1994) Structure of the carboxy-terminal LJM domain from the cysteine rich protein CRP. Nat Struct Biol 1: 388-398
33. Perrakis A, Morris R, Lamzin VS (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol 6: 458-463
34. Porter FD, Drago J, Xu Y, Cheema SS, Wassif C, Huang SP, Lee E, Grinberg A, Massalas JS, Bodine D, Alt F, Westphal H (1997) Lhx2, a LIM homeobox gene, is required for eye, forebrain, and definitive erythrocyte development. Development 124: 2935-2944
35. Rabbitts TH, Bucher K, Chung G, Grutz G, Warren A, Yamada Y (1999) The effect of chromosomal translocations in acute leukemias: the LMO2 paradigm in transcription and development. Cancer Res 59: 1794s-1798s
36. Racevskis J, Dill A, Sparano JA, Ruan H (1999) Molecular cloning of LMO41, a new human LIM domain gene. Biochim Biophys Acta 1445: 148-153
37. Remain P, Khechumian R, Khechumian K, Arbogast N, Ackermann C, Heitzler P (2000) Interactions between chip and the achaete/scute-daughterless heterodimers are required for pannier-driven proneural patterning. Mol Cell 6: 781-790
38. Schwarz-Linek U, Werner JM, Pickford AR, Gurusiddappa S, Kim JH, Pilka ES, Briggs JA, Gough TS, Hook M, Campbell ID, Potts JR (2003) Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423: 177-181
39. Shawlot W, Behringer RR (1995) Requirement for Lim1 in head-organizer function. Nature 374: 425-430
40. Sheng HZ, Zhadanov AB, Mosinger Jr B, Fujii T, Bertuzzi S, Grinberg A, Lee EJ, Huang SP, Mahon KA, Westphal H (1996) Specification of pituitary cell lineages by the LIM homeobox gene Lhx3. Science 272: 1004-1007
41. Shoresh M, Orgad S, Shmueli O, Werczberger R, Gelbaum D, Abiri S, Segal D (1998) Overexpression Beadex mutations and loss-of-function heldup-a mutations in Drosophila affect the 3′ regulatory and coding components, respectively, of the Dlmo gene. Genetics 150: 283-299
42. Sum EY, Peng B, Yu X, Chen J, Byrne J, Lindeman GJ, Visvader JE (2002) The LIM domain protein LMO4 interacts with the cofactor CtIP and the tumor suppressor BRCA1 and inhibits BRCA1 activity. J Biol Chem 277: 7849-7856
43. Terwilliger TC (2001) Maximum-likelihood density modification with pattern recognition of structural motifs. Acta Crystallogr D 57: 1755-1762
44. Thaler JP, Lee SK, Jurata LW, Gill GN, Pfaff SL, Bridwell JA, Price JR, Parker GE, McCutchan Schiller A, Sloop KW, Rhodes SJ (2002) LIM factor Lhx3 contributes to the specification of motor neuron and interneuron identity through cell-type-specific protein-protein interactions. Cell 110: 237-249
45. Tse E, Smith AJ, Hunt S, Lavenir I, Forster A, Warren AJ, Grutz G, Foroni L, Carlton MB, Colledge WH, Boehm T, Rabbitts TH (2004) Null mutation of the Lmo4 gene or a combined null mutation of the Lmo1/Lmo3 genes causes perinatal lethality, and Lmo4 controls neural tube development in mice. Mol Cell Biol 24: 2063-2073
46. Tu Y, Li F, Goicoechea S, Wu C (1999) The LIM-only protein PINCH directly interacts with integrin-linked kinase and is recruited to integrin-rich sites in spreading cells. Mol Cell Biol 19: 2425-2434
47. Turner J, Nicholas H, Bishop D, Matthews JM, Crossley M (2003) The LIM protein FHL3 binds basic Kruppel-like factor/Kruppel-like factor 3 and its co-repressor C-terminal-binding protein 2. J Biol Chem 278: 12786-12795
48. Valge-Archer V, Forster A, Rabbitts TH (1998) The LMO1 and Ldb1 proteins interact in human T cell acute leukaemia with the chromosomal translocation t(11;14)(p15;q11). Oncogene 17: 3199-3202
49. van Meyel DJ, O'Keefe DD, Jurata LW, Thor S, Gill GN, Thomas JB (1999) Chip and apterous physically interact to form a functional complex during Drosophila development. Mol Cell 4: 259-265
50. Velyvis A, Vaynberg J, Yang Y, Vinogradova O, Zhang Y, Wu C, Qin J (2003) Structural and functional insights into PINCH LIM4 domain-mediated integrin signaling. Nat Struct Biol 10: 558-564
51. Visvader JE, Mao X, Fujiwara Y, Hahm K, Orkin SH (1997) The LIM-domain binding protein Ldb1 and its partner LMO2 act as negative regulators of erythroid differentiation. Proc Natl Acad Sci USA 94: 13707-13712
52. Visvader JE, Venter D, Hahm K, Santamaria M, Sum EY, O'Reilly L, White D, Williams R, Armes J, Lindeman GJ (2001) The LIM domain gene LMO4 inhibits differentiation of mammary epithelial cells in vitro and is overexpressed in breast cancer. Proc Natl Acad Sci USA 98: 14452-14457
53. Wadman IA, Osada H, Grutz GG, Agulnick AD, Westphal H, Forster A, Rabbitts TH (1997) 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 16: 3145-3157
54. Wang N, Kudryavtseva E, Ch'en IL, McCormick J, Sugihara TM, Ruiz R, Andersen B, Kudryavtseva EI, Lasso RJ, Gudnason JF, Lipkin SM (2004) Expression of an engrailed-LMO4 fusion protein in mammary epithelial cells inhibits mammary gland development in mice. Oncogene 23: 1507-1513
55. Wei Y, Renard CA, Labalette C, Wu Y, Levy L, Neuveut C, Prieur X, Flajolet M, Prigent S, Buendia MA (2003) Identification of the LIM protein FHL2 as a coactivator of beta-catenin. J Biol Chem 278: 5188-5194
56. Yamada Y, Pannell R, Forster A, Rabbitts TH (2000) The oncogenic LIM-only transcription factor Lmo2 regulates angiogenesis but not vasculogenesis in mice. Proc Natl Acad Sci USA 97: 320-324
57. Yamada Y, Warren AJ, Dobson C, Forster A, Pannell R, Rabbitts TH (1998) The T cell leukemia LIM protein Lmo2 is necessary for adult mouse hematopoiesis. Proc Natl Acad Sci USA 95: 3890-3895
58. Zeng C, Justice NJ, Abdelilah S, Chan YM, Jan LY, Jan YN (1998) The Drosophila LIM-only gene, dLMO, is mutated in Beadex alleles and might represent an evolutionarily conserved function in appendage development. Proc Natl Acad Sci USA 95: 10637-10642