The Nuclear LIM Domain Interactor NLI Mediates Homo- and Heterodimerization of LIM Domain Transcription Factors
Open accessAbstract
LIM domain-containing transcription factors are required for embryonic survival and for the determination of many cell types. The combinatorial expression of the LIM homeodomain proteins Isl1, Isl2, Lhx1, and Lhx3 in subsets of developing motor neurons correlates with the future organization of these neurons into motor columns with distinct innervation targets, implying a functional role for LIM homeodomain protein combinations in the specification of neuronal identity. NLI is a widely expressed, dimeric protein that has been shown to specifically interact with the LIM domains of LIM domain-containing transcription factors. The present studies demonstrate that NLI mediates homo- and heteromeric complex formation between LIM domain transcription factors, requiring both the N-terminal dimerization and C-terminal LIM interaction domains of NLI. Although the interaction between most LIM homeodomain proteins is dependent on NLI, a direct interaction between the LIM domains of Lhx3 and the homeodomains of Isl1 and Isl2 was also observed. This interaction was disrupted by NLI, demonstrating that the conformational state of Lhx3-Isl1/Isl2 complexes is modified by NLI. Evidence indicating that NLI facilitates long range enhancer-promoter interactions suggests that NLI-dependent LIM domain transcription factor complexes are involved in communication between transcriptional control elements.
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LDB1 is a dimeric cofactor that does not have direct DNA-binding capacity, but interacts with the LIM domain of other TFs to form multi-protein complexes.
“LIM domain-binding protein 1 (LDB1) is a dimeric cofactor that does not have direct DNA-binding capacity, but interacts with the LIM domain of other TFs to form multi-protein complexes [370].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [370]
The Abstract identifies NLI as Ldb1 and describes its homodimerization and LIM-interaction domains. The Results report that NLI dimers link LIM-domain transcription factors in tetrameric complexes. Our copy does not establish the separate claim that Ldb1 has no direct DNA-binding capacity. (LLM, conf=0.84)
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Cites
Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes
Tsuchida, T., Ensini, M., Brenner‐Morton, S., Baldassare, M., Edlund, H., Jessell, T. M., & Pfaff, S. L. (1994) · Cell · doi:10.1016/0092-8674(94)90027-2 · Cited by 997 · see citing works
Self-citationCurrent Protocols in Molecular Biology
Hunt, T. (1989) · Journal of Cell Science · doi:10.1242/jcs.94.3.390 · Cited by 968 · see citing works
Requirement for LIml in head-organizer function
Shawlot, W., & Behringer, R. R. (1995) · Nature · doi:10.1038/374425a0 · Cited by 805 · see citing works
Pfaff, S., Mendelsohn, M., Stewart, C., Edlund, T., & Jessell, T. (1996) · Cell · doi:10.1016/s0092-8674(00)80985-x · Cited by 801 · see citing works
Self-citationDiversity and Pattern in the Developing Spinal Cord
Tanabe, Y., & Jessell, T. M. (1996) · Science · doi:10.1126/science.274.5290.1115 · Cited by 718 · see citing works
Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells
Ahlgren, U., Pfaff, S. L., Jessell, T. M., Edlund, H., & Edlund, H. (1997) · Nature · doi:10.1038/385257a0 · Cited by 688 · see citing works
Self-citationThe Oncogenic Cysteine-rich LIM domain protein Rbtn2 is essential for erythroid development
Warren, A. J., Colledge, W. H., Carlton, M. B. L., Evans, M. J., Smith, A. J. H., & Rabbitts, T. H. (1994) · Cell · doi:10.1016/0092-8674(94)90571-1 · Cited by 605 · see citing works
Histone acetylation: chromatin in action
Wade, P. A., Pruss, D., & Wolffe, A. P. (1997) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(97)01016-5 · Cited by 468 · see citing works
Specification of Pituitary Cell Lineages by the LIM Homeobox Gene Lhx3
SHENG, H. Z., Zhadanov, A. B., Mosinger, B. J., Fujii, T., Bertuzzi, S., Grinberg, A., Lee, E. J., Huang, S.-P., Mahon, K. A., & Westphal, H. (1996) · Science · doi:10.1126/science.272.5264.1004 · Cited by 456 · see citing works
Lai, J. S., & Herr, W. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.15.6958 · Cited by 451 · see citing works
German, M. S., Wang, J., Chadwick, R. B., & Rutter, W. J. (1992) · Genes & Development · doi:10.1101/gad.6.11.2165 · Cited by 390 · see citing works
Boehm, T. L. J., Foroni, L., Kaneko, Y., Perutz, M. F., & Rabbitts, T. H. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.10.4367 · Cited by 367 · see citing works
Thor, S., Ericson, J., Brännström, T., & Edlund, H. (1991) · Neuron · doi:10.1016/0896-6273(91)90334-v · Cited by 333 · see citing works
Interactions of the LIM-domain-binding factor Ldbl with LIM homeodomain proteins
Agulnick, A. D., Taira, M., Breen, J. J., Tanaka, T., Dawid, I. B., & Westphal, H. (1996) · Nature · doi:10.1038/384270a0 · Cited by 318 · see citing works
Bach, I., Rhodes, S. J., Pearse, R. V., Heinzel, T., Gloss, B. R., Scully, K. M., Sawchenko, P. E., & Rosenfeld, M. G. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2720 · Cited by 291 · see citing works
Bach, I., Carrière, C., Ostendorff, H. P., D, B. A. M., & Rosenfeld, M. G. (1997) · Genes & Development · doi:10.1101/gad.11.11.1370 · Cited by 285 · see citing works
Appel, B., Korzh, V. P., Glasgow, E. F., Thor, S., Edlund, H., Dawid, I. B., & Eisen, J. S. (1995) · Development · doi:10.1242/dev.121.12.4117 · Cited by 284 · see citing works
The Drosophila islet Gene Governs Axon Pathfinding and Neurotransmitter Identity
Thor, S., & Thomas, J. B. (1997) · Neuron · doi:10.1016/s0896-6273(00)81241-6 · Cited by 271 · see citing works
Jurata, L. W., Kenny, D. A., & Gill, G. N. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11693 · Cited by 228 · see citing works
Self-citationSpecificity of single LIM motifs in targeting and LIM/LIM interactions in situ.Preprint
Arber, S., & Caroni, P. (1996) · Genes & Development · doi:10.1101/gad.10.3.289 · Cited by 221 · see citing works
Morcillo, P., Rosen, C., Baylies, M. K., & Dorsett, D. (1997) · Genes & Development · doi:10.1101/gad.11.20.2729 · Cited by 208 · see citing works
Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous
Lundgren, S. E., Callahan, C. A., Thor, S., & Thomas, J. B. (1995) · Development · doi:10.1242/dev.121.6.1769 · Cited by 188 · see citing works
Functional Analysis of the Nuclear LIM Domain Interactor NLI
Jurata, L. W., & Gill, G. N. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.10.5688 · Cited by 169 · see citing works
Self-citationZhadanov, A. B., Bertuzzi, S., Taira, M., Dawid, I. B., & Westphal, H. (1995) · Developmental Dynamics · doi:10.1002/aja.1002020405 · Cited by 159 · see citing works
Li, H., Witte, D. P., Branford, W. W., Aronow, B. J., Weinstein, M. B., Kaur, S., Wert, S. E., Singh, G., Schreiner, C. M., & Whitsett, J. A. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06582.x · Cited by 124 · see citing works
McGuire, E. A., Rintoul, C. E., Sclar, G. M., & Korsmeyer, S. J. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.9.4186 · Cited by 114 · see citing works
Greenberg, J. M., Boehm, T. L. J., Sofroniew, M. V., Keynes, R. J., Barton, S. C., Norris, M. L., Surani, M. A., Spillantini, M. G., & Rabbitts, T. H. (1990) · Nature · doi:10.1038/344158a0 · Cited by 107 · see citing works
Foroni, L., Boehm, T. L. J., White, L., Forster, A. M., Sherrington, P. D., Liao, X., Brannan, C. I., Jenkins, N. A., Copeland, N. G., & Rabbitts, T. H. (1992) · Journal of Molecular Biology · doi:10.1016/0022-2836(92)90630-3 · Cited by 107 · see citing works
Fisch, P., Boehm, T. L. J., Lavenir, I., Larson, T., Arno, J., Forster, A. M., & Rabbitts, T. H. (1992) · PubMed · Cited by 105 · see citing works
Specificity of LIM Domain Interactions with Receptor Tyrosine Kinases
Wu, R.-Y., Durick, K., Songyang, Z., Cantley, L. C., Taylor, S. S., & Gill, G. N. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.27.15934 · Cited by 102 · see citing works
Self-citationSeidah, N. G., Barale, J.-C., MARCINKIEWICZ, M., Mattéi, M., Day, R. W., & Chrétien, M. (1994) · DNA and Cell Biology · doi:10.1089/dna.1994.13.1163 · Cited by 102 · see citing works
Johnson, J. D., Zhang, W., Rudnick, A., Rutter, W. J., & German, M. S. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.7.3488 · Cited by 92 · see citing works
Islet Cell and Extrapancreatic Expression of the LIM Domain Homeobox Geneisl-1
Dong, J., Asa, S. L., & Drucker, D. J. (1991) · Molecular Endocrinology · doi:10.1210/mend-5-11-1633 · Cited by 83 · see citing works
Taira, M., Hayes, W. P., Otani, H., & Dawid, I. B. (1993) · Developmental Biology · doi:10.1006/dbio.1993.1237 · Cited by 74 · see citing works
Gill, G. N. (1995) · Structure · doi:10.1016/s0969-2126(01)00265-9 · Cited by 72 · see citing works
Self-citationBoehm, T. L. J., Spillantini, M. G., Sofroniew, M. V., Surani, M. A., & Rabbitts, T. H. (1991) · PubMed · Cited by 49 · see citing works
Specifying the target identity of motoneurons
Tosney, K. W., Hotary, K. B., & Lance-Jones, C. C. (1995) · BioEssays · doi:10.1002/bies.950170503 · Cited by 32 · see citing works
Yamashita, T., Moriyama, K., SHENG, H. Z., & Westphal, H. (1997) · Genomics · doi:10.1006/geno.1997.4852 · Cited by 24 · see citing works
Insulin Gene Can Be Expressed in the Absence of Isl-1
Dandoy‐Dron, F., Deltour, L., Monthioux, E., Bucchini, D., & Jami, J. (1993) · Experimental Cell Research · doi:10.1006/excr.1993.1285 · Cited by 7 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- Boehm, T., Foroni, L., Kaneko, Y., Perutz, M. F., and Rabbitts, T. H. (1991) Proc. Natl. Acad. Sci. U. S. A. 88, 4367-4371
- Jurata, L. W., Kenny, D. A., and Gill, G. N. (1996) Proc. Natl. Acad. Sci.
- Lai, J. S., and Herr, W. (1992) Proc. Natl. Acad. Sci. U. S. A. 89, 6958 -6962
- Bach, I., Rhodes, S. J., Pearse, R. V., II, Heinzel, T., Gloss, B., Scully, K. M., Sawchenko, P. E., and Rosenfeld, M. G. (1995) Proc. Natl. Acad. Sci.
Cited by
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The LIM domain: from the cytoskeleton to the nucleus
Kadrmas, J. L., & Beckerle, M. C. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1499 · Cited by 741 · see citing works
The LIM domain: regulation by association
Bach, I. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00314-7 · Cited by 555 · see citing works
Kioussi, C., Briata, P., Baek, S. H., Rose, D. W., Hamblet, N. S., Herman, T., Ohgi, K. A., Lin, C. R., Gleiberman, A. S., Wang, J., et al. (2002) · Cell · doi:10.1016/s0092-8674(02)01084-x · Cited by 543 · see citing works
Transcriptional Codes and the Control of Neuronal Identity
Shirasaki, R., & Pfaff, S. L. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142916 · Cited by 522 · see citing works
Self-citationFunctions of LIM-homeobox genes
Hobert, O., & Westphal, H. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(99)01883-1 · Cited by 477 · see citing works
Thaler, J. P., Lee, S., Jurata, L. W., Gill, G. N., & Pfaff, S. L. (2002) · Cell · doi:10.1016/s0092-8674(02)00823-1 · Cited by 363 · see citing works
Self-citationThaler, J., Harrison, K., Sharma, K., Lettieri, K., Kehrl, J., & Pfaff, S. L. (1999) · Neuron · doi:10.1016/s0896-6273(01)80027-1 · Cited by 354 · see citing works
Self-citationSpecification of Motor Neuron Identity by the MNR2 Homeodomain Protein
Tanabe, Y., William, C. M., & Jessell, T. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81783-3 · Cited by 341 · see citing works
Rollins, R. A., Morcillo, P., & Dorsett, D. (1999) · Genetics · doi:10.1093/genetics/152.2.577 · Cited by 304 · see citing works
Transcriptional networks regulating neuronal identity in the developing spinal cord
Lee, S., & Pfaff, S. L. (2001) · Nature Neuroscience · doi:10.1038/nn750 · Cited by 290 · see citing works
Self-citationLee, S., & Pfaff, S. L. (2003) · Neuron · doi:10.1016/s0896-6273(03)00296-4 · Cited by 288 · see citing works
Self-citationA LIM-homeodomain combinatorial code for motor-neuron pathway selection
Thor, S., Andersson, S. G. E., Tomlinson, A., & Thomas, J. B. (1999) · Nature · doi:10.1038/16275 · Cited by 287 · see citing works
Dong, R., Yang, R., Zhan, Y., Lai, H., Ye, C., Yao, X.-Y., Luo, W., Cheng, X., Miao, J., Wang, J., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.08.014 · Cited by 268 · see citing works
Endosomal Transport of ErbB-2: Mechanism for Nuclear Entry of the Cell Surface Receptor
Giri, D. K., Ali‐Seyed, M., Li, L., Lee, D., Ling, P., Bartholomeusz, G. A., Wang, S., & Hung, M. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.24.11005-11018.2005 · Cited by 242 · see citing works
A positive role for NLI/Ldb1 in long-range β-globin locus control region function
Song, S.-H., Hou, C., & Dean, A. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.09.025 · Cited by 233 · see citing works
Distant liaisons: long-range enhancer–promoter interactions in Drosophila
Dorsett, D. (1999) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(99)00002-7 · Cited by 187 · see citing works
LIM‐domain‐binding protein 1: a multifunctional cofactor that interacts with diverse proteins
Matthews, J. M., & Visvader, J. E. (2003) · EMBO Reports · doi:10.1038/sj.embor.7400030 · Cited by 164 · see citing works
Sridhar, V. V., Surendrarao, A., González, D., Conlan, R. S., & Liu, Z. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403055101 · Cited by 158 · see citing works
Regulated subset of G 1 growth-control genes in response to derepression by the Wnt pathway
Baek, S. H., Kioussi, C., Briata, P., Wang, D., Nguyen, H., Ohgi, K. A., Glass, C. K., Wynshaw-Boris, A. J., Rose, D. W., & Rosenfeld, M. G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0330217100 · Cited by 148 · see citing works
LIM-domain-only proteins in cancer
Matthews, J. M., Lester, K. L., Joseph, S., & Curtis, D. J. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3418 · Cited by 137 · see citing works
Regulation of GATA1 levels in erythropoiesis
Gutiérrez, L., Caballero, N., Fernández‐Calleja, L., Karkoulia, E., & Strouboulis, J. (2019) · IUBMB Life · doi:10.1002/iub.2192 · Cited by 134 · see citing works
Lee, S.-K., Jurata, L., Funahashi, J., Ruiz, E. C., & Pfaff, S. (2004) · Development · doi:10.1242/dev.01179 · Cited by 142 · see citing works
Self-citationRole of LDB1 in the transition from chromatin looping to transcription activation
Krivega, I., Dale, R. K., & Dean, A. (2014) · Genes & Development · doi:10.1101/gad.239749.114 · Cited by 125 · see citing works
Rivella, S. (2015) · Haematologica · doi:10.3324/haematol.2014.114827 · Cited by 122 · see citing works
Regulation of LIM Homeodomain Activity In Vivo
Milán, M., & Cohen, S. M. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80374-3 · Cited by 120 · see citing works
LIM-homeodomain genes in mammalian development and human disease
Hunter, C. S., & Rhodes, S. J. (2005) · Molecular Biology Reports · doi:10.1007/s11033-004-7657-z · Cited by 118 · see citing works
Chip and Apterous Physically Interact to Form a Functional Complex during Drosophila Development
van Meyel, D. J., O’Keefe, D. D., Jurata, L. W., Thor, S., Gill, G. N., & Thomas, J. B. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80373-1 · Cited by 113 · see citing works
Self-citationGlenn, D. J., & Maurer, R. A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.51.36159 · Cited by 106 · see citing works
Ramain, P., Khechumian, R., Khetchoumian, K., Arbogast, N., Ackermann, C., & Heitzler, P. (2000) · Molecular Cell · doi:10.1016/s1097-2765(05)00079-1 · Cited by 104 · see citing works
LMX1B transactivation and expression in nail-patella syndrome
Dreyer, S. D. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.7.1067 · Cited by 102 · see citing works
Grütz, G., Bucher, K., Lavenir, I., Larson, T., Larson, R., & Rabbitts, T. H. (1998) · The EMBO Journal · doi:10.1093/emboj/17.16.4594 · Cited by 100 · see citing works
Kenny, D. A., Jurata, L. W., Saga, Y., & Gill, G. N. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.19.11257 · Cited by 99 · see citing works
Self-citationTandem LIM domains provide synergistic binding in the LMO4:Ldb1 complex
Deane, J. E., Ryan, D., Sunde, M., Maher, M. J., Guss, J. M., Visvader, J. E., & Matthews, J. M. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600376 · Cited by 98 · see citing works
Fernández-Fúnez, P., Lu, C.-H., Rincón-Limas, D. E., Garcı́a-Bellido, A., & Botas, J. (1998) · The EMBO Journal · doi:10.1093/emboj/17.23.6846 · Cited by 95 · see citing works
Sugihara, T. M., Bach, I., Kioussi, C., Rosenfeld, M. G., & D, B. A. M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15418 · Cited by 92 · see citing works
Tobacco WLIM1 Is a Novel F-Actin Binding Protein Involved in Actin Cytoskeleton Remodeling
Thomas, C., Hoffmann, C., Dieterle, M., Troys, M. V., Ampè, C., & Steinmetz, A. A. (2006) · The Plant Cell · doi:10.1105/tpc.106.040956 · Cited by 91 · see citing works
Specification ofDrosophilamotoneuron identity by the combinatorial action of POU and LIM-HD factors
Certel, S. J., & Thor, S. (2004) · Development · doi:10.1242/dev.01418 · Cited by 90 · see citing works
The role ofSEUSSin auxin response and floral organ patterning
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Sarafi-Reinach, T. R., Melkman, T., Hobert, O., & Sengupta, P. (2001) · Development · doi:10.1242/dev.128.17.3269 · Cited by 85 · see citing works
Neuronal diversification: development of motor neuron subtypes
Pfaff, S. L., & Kintner, C. R. (1998) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(98)80005-6 · Cited by 84 · see citing works
Self-citationSloop, K. W., Meier, B. C., Bridwell, J. L., Parker, G. E., McCutchan, A., & Rhodes, S. J. (1999) · Molecular Endocrinology · doi:10.1210/mend.13.12.0395 · Cited by 83 · see citing works
van Meyel, D. J., Thomas, J. B., & Agulnick, A. D. (2003) · Development · doi:10.1242/dev.00389 · Cited by 83 · see citing works
Chip interacts with diverse homeodomain proteins and potentiates Bicoid activity in vivo
Torigoi, E., Bennani-Baı̈ti, I. M., Rosen, C., Gonzalez, K. N., Morcillo, P., Ptashne, M., & Dorsett, D. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.050586397 · Cited by 83 · see citing works
Function and specificity of LIM domains in Drosophila nervous system and wing development
O’Keefe, D. D., Thor, S., & Thomas, J. B. (1998) · Development · doi:10.1242/dev.125.19.3915 · Cited by 82 · see citing works
Transcriptional enhancers and their communication with gene promoters
Ray-Jones, H., & Spivakov, M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03903-w · Cited by 81 · see citing works
Matthews, J. M., & Sunde, M. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3229-6_1 · Cited by 80 · see citing works
Lee, S., Cuvillier, J., Lee, B., Shen, R., Lee, J. W., & Lee, S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114515109 · Cited by 80 · see citing works
LMO4 Controls the Balance between Excitatory and Inhibitory Spinal V2 Interneurons
Joshi, K., Lee, S., Lee, J. W., Lee, S., & Lee, S. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.011 · Cited by 80 · see citing works
Lhx1 is required in Müllerian duct epithelium for uterine development
Huang, C.-C., Orvis, G. D., Kwan, K. M., & Behringer, R. R. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.01.025 · Cited by 78 · see citing works
Bhati, M., Lee, C., Nancarrow, A. L., Lee, M., Craig, V. J., Bach, I., Guss, J. M., Mackay, J. P., & Matthews, J. M. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.123 · Cited by 76 · see citing works
Song, M., Sun, Y., Bryson, A., Gill, G. N., Evans, S. Μ., & Pfaff, S. L. (2009) · Development · doi:10.1242/dev.037986 · Cited by 76 · see citing works
Self-citationLIM Genes Parcellate the Embryonic Amygdala and Regulate Its Development
Remedios, R., Subramanian, L., & Tole, S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0001-04.2004 · Cited by 74 · see citing works
Structural basis for the recognition of ldb1 by the N‐terminal LIM domains of LMO2 and LMO4
Deane, J. E., Mackay, J. P., Kwan, A. H., Sum, E. Y. M., Visvader, J. E., & Matthews, J. M. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg196 · Cited by 71 · see citing works
Wang, N., Lin, K., Lu, Z., Lam, K. S., Newton, R. H., Xu, X., Yu, Z., Gill, G. N., & D, B. A. M. (2007) · Oncogene · doi:10.1038/sj.onc.1210465 · Cited by 71 · see citing works
Self-citationSsdp1 regulates head morphogenesis of mouse embryos by activating the Lim1-Ldb1 complex
Nishioka, N., Nagano, S., Nakayama, R., Kiyonari, H., Ijiri, T. W., Taniguchi, K., Shawlot, W., Hayashizaki, Y., Westphal, H., Behringer, R. R., et al. (2005) · Development · doi:10.1242/dev.01844 · Cited by 68 · see citing works
The LIM domain-only protein LMO4 is required for neural tube closure
Lee, S., Jurata, L. W., Nowak, R. B., Lettieri, K., Kenny, D. A., Pfaff, S. L., & Gill, G. N. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.04.010 · Cited by 65 · see citing works
Self-citationThe N-terminal LIM domain negatively regulates the kinase activity ofLIM-kinase 1
NAGATA, K., Ohashi, K., Yang, N., & Mizuno, K. (1999) · Biochemical Journal · doi:10.1042/bj3430099 · Cited by 63 · see citing works
A Short History of LIM Domains (1993-2002): From Protein Interaction to Degradation
Rétaux, S., & Bachy, I. (2002) · Molecular Neurobiology · doi:10.1385/mn:26:2-3:269 · Cited by 61 · see citing works
Shoresh, M., Orgad, S., Shmueli, O., Werczberger, R., Gelbaum, D., Abiri, S., & Segal, D. (1998) · Genetics · doi:10.1093/genetics/150.1.283 · Cited by 59 · see citing works
Mouse GnRH Receptor Gene Expression Is Mediated by the LHX3 Homeodomain Protein
McGillivray, S. M., Bailey, J. S., Ramezani, R., Kirkwood, B. J., & Mellon, P. L. (2005) · Endocrinology · doi:10.1210/en.2004-1566 · Cited by 58 · see citing works
Michelson, R. J., Collard, M. W., Ziemba, A. J., Persinger, J., Bartholomew, B., & Huggenvik, J. I. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.43.30510 · Cited by 57 · see citing works
Granger, A., Bleux, C., Kottler, M., Rhodes, S. J., Counis, R., & Laverrière, J. (2006) · Molecular Endocrinology · doi:10.1210/me.2005-0184 · Cited by 54 · see citing works
Lhx6 and Lhx8: cell fate regulators and beyond
Zhou, C., Yang, G., Chen, M., He, L., Xiang, L., Ricupero, C. L., Mao, J. J., & Ling, J. (2015) · The FASEB Journal · doi:10.1096/fj.14-267500 · Cited by 53 · see citing works
Chip is an essential cofactor for Apterous in the regulation of axon guidance in Drosophila
van Meyel, D. J., O’Keefe, D. D., Thor, S., Jurata, L. W., Gill, G. N., & Thomas, J. B. (2000) · Development · doi:10.1242/dev.127.9.1823 · Cited by 52 · see citing works
Self-citationTranscriptional mechanisms in the development of motor control
Jurata, L. W., Thomas, J. B., & Pfaff, S. L. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00053-7 · Cited by 52 · see citing works
Self-citationHomeodomain transcription factors in the development of subsets of hindbrain reticulospinal neurons
Cepeda-Nieto, A. C., Pfaff, S. L., & Varela-Echavarría, A. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2004.06.016 · Cited by 50 · see citing works
Self-citationRincón-Limas, D. E., Lu, C., Canal, I., & Botas, J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.11.2602 · Cited by 50 · see citing works
Dubin, M., Stokes, P. H., Sum, E. Y. M., Williams, R. S., Valova, V. A., Robinson, P. J., Lindeman, G. J., Glover, J. N. M., Visvader, J. E., & Matthews, J. M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313974200 · Cited by 49 · see citing works
Failli, V., Rogard, M., Mattéi, M., Vernier, P., & Rétaux, S. (2000) · Genomics · doi:10.1006/geno.2000.6123 · Cited by 49 · see citing works
Regulation of Apterous activity inDrosophilawing development
Weihe, U., Milán, M., & Cohen, S. M. (2001) · Development · doi:10.1242/dev.128.22.4615 · Cited by 47 · see citing works
Mizunuma, H., MIYAZAWA, J., Sanada, K., & Imai, K. (2003) · British Journal of Cancer · doi:10.1038/sj.bjc.6600952 · Cited by 46 · see citing works
Multiple functions of LIM domain-binding CLIM/NLI/Ldb cofactors during zebrafish development
Becker, T., Ostendorff, H. P., Bossenz, M., Schlüter, A., Becker, C. G., Peirano, R. I., & Bach, I. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00178-8 · Cited by 45 · see citing works
Mundel, C., Baltz, R., Eliasson, Å., Bronner, R., Grass, N., Kräuter, R., Evrard, J., & Steinmetz, A. A. (2000) · Plant Molecular Biology · doi:10.1023/a:1006333611189 · Cited by 44 · see citing works
Cross, S. H., Macalinao, D. G., McKie, L., Rose, L., Kearney, A. L., Rainger, J., Thaung, C., Keighren, M., Jadeja, S., West, K. M., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004359 · Cited by 44 · see citing works
Rnf220 cooperates with Zc4h2 to specify spinal progenitor domains
Kim, J., Choi, T.-I., Park, S., Kim, M., Kim, C.-H., & Lee, S. (2018) · Development · doi:10.1242/dev.165340 · Cited by 35 · see citing works
Hiratani, I., Yamamoto, N., Mochizuki, T., Ohmori, S., & Taira, M. (2003) · Development · doi:10.1242/dev.00621 · Cited by 43 · see citing works
The LIM/Homeodomain Protein Islet-1 Modulates Estrogen Receptor Functions
Gay, F., Anglade, I., Gong, Z., & Salbert, G. (2000) · Molecular Endocrinology · doi:10.1210/mend.14.10.0538 · Cited by 43 · see citing works
A LIM-homeodomain code for development and evolution of forebrain connectivity
Bachy, I., Failli, V., & Rétaux, S. (2002) · Neuroreport · doi:10.1097/00001756-200202110-00002 · Cited by 43 · see citing works
Structure of Cysteine- and Glycine-rich Protein CRP2
Konrat, R., Kräutler, B., Weiskirchen, R., & Bister, K. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.36.23233 · Cited by 43 · see citing works
Enhancer long-range contacts: The multi-adaptor protein LDB1 is the tie that binds
Liu, G., & Dean, A. (2019) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2019.04.003 · Cited by 42 · see citing works
Aurelio, O. N., Boulin, T., & Hobert, O. (2003) · Development · doi:10.1242/dev.00277 · Cited by 39 · see citing works
Islet is a key determinant of ascidian palp morphogenesis
Wagner, E., Stolfi, A., Choi, Y. G., & Levine, M. (2014) · Development · doi:10.1242/dev.110684 · Cited by 39 · see citing works
Enkhmandakh, B., Makeyev, A. V., & Bayarsaihan, D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605209103 · Cited by 38 · see citing works
The LIM Homeodomain Transcription Factor LHX6
Zhang, Z., Gutierrez, D. K., Li, X., Bidlack, F. B., Cao, H., Wang, J., Andrade, K. C., Margolis, H. C., & Amendt, B. A. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.402933 · Cited by 36 · see citing works
Characterization of the porcine Lhx3/LIM-3/P-Lim LIM homeodomain transcription factor
Meier, B. C., Price, J. R., Parker, G. E., Bridwell, J. L., & Rhodes, S. J. (1999) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(98)00213-5 · Cited by 35 · see citing works
Dynamic expression of LIM cofactors in the developing mouse neural tube
Ostendorff, H. P., Tursun, B., Cornils, K., Schlüter, A., Drung, A., Güngör, C., & Bach, I. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20669 · Cited by 34 · see citing works
Pueyo, J. I., & Couso, J. P. (2004) · Development · doi:10.1242/dev.01161 · Cited by 34 · see citing works
Deane, J. E., Sum, E. Y. M., Mackay, J. P., Lindeman, G. J., Visvader, J. E., & Matthews, J. M. (2001) · Protein Engineering Design and Selection · doi:10.1093/protein/14.7.493 · Cited by 32 · see citing works
Parker, G. E., Sandoval, R. M., Feister, H. A., Bidwell, J. P., & Rhodes, S. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000377200 · Cited by 32 · see citing works
Chou, S., Hermesz, E., Hatta, T., Feltner, D. E., El‐Hodiri, H. M., Jamrich, M., & Mahon, K. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2005.12.053 · Cited by 31 · see citing works
Competition between LIM-binding domains
Matthews, J. M., Bhati, M., Craig, V. J., Deane, J. E., Jeffries, C. M., Lee, C., Nancarrow, A. L., Ryan, D., & Sunde, M. (2008) · Biochemical Society Transactions · doi:10.1042/bst0361393 · Cited by 31 · see citing works
Marquet, S., Lepage, P., Hudson, T. J., Musser, J. M., & Schurr, E. (2000) · Mammalian Genome · doi:10.1007/s003350010151 · Cited by 30 · see citing works
GATA4/FOG2 transcriptional complex regulates Lhx9 gene expression in murine heart development
Smagulova, F. O., Manuylov, N. L., Leach, L. L., & Tevosian, S. G. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-67 · Cited by 29 · see citing works
Decoding the LIM development code.
Gill, G. N. (2003) · PubMed Central · Cited by 29 · see citing works
Self-citationRoignant, J., Legent, K., Janody, F., & Treisman, J. E. (2009) · Development · doi:10.1242/dev.041244 · Cited by 28 · see citing works
Identification and characterization of LIM gene family in Brassica rapa
Park, J., Ahmed, N. U., Jung, H. J., Thamilarasan, S. K., Chung, M. Y., Cho, Y. G., Watanabe, M., & Nou, I. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-641 · Cited by 27 · see citing works
Chromatin looping as a target for altering erythroid gene expression
Krivega, I. V., & Dean, A. (2016) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13012 · Cited by 27 · see citing works
Crystal structure of human LDB1 in complex with SSBP2
Wang, H., Kim, J., Wang, Z., Yan, X., Dean, A., & Xu, W. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1914181117 · Cited by 26 · see citing works
The LIM-homeodomain transcription factor LMX1B regulates expression of NF-kappa B target genes
Rascle, A., Neumann, T., Raschta, A., Neumann, A., Heining, E., Kastner, J., & Witzgall, R. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.10.012 · Cited by 26 · see citing works
Biryukova, I., & Heitzler, P. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.09.033 · Cited by 24 · see citing works
- Authors
- Jurata, L. W., Pfaff, S. L., & Gill, G. N.
- Affiliations
- University of California San Diego (US)
- Salk Institute for Biological Studies (US)
- Corresponding author
- Gill, Gordon N.
- ORCID
- Pfaff, Samuel L.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 1998-02
- Volume
- 273
- Issue
- 6
- Pages
- 3152-3157
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2011115644
- Cited by
- 164
- References
- 39
- Citations by year
- 2025: 4 · 2024: 3 · 2023: 2 · 2022: 1 · 2021: 3 · 2020: 1 · 2019: 3 · 2018: 2 · 2017: 7 · 2016: 8 · 2015: 6 · 2014: 5 · 2013: 5 · 2012: 4
- FWCI
- 5.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- McKnight Foundation
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (DK13149, DK07541)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Keywords
- LIM domain, LIM-homeodomain transcription factor, protein dimerization, Isl1, ISL2, LHX3, Lhx1, motor neuron specification, enhancer-promoter interactions, transcriptional regulation, protein-protein interaction
- MeSH terms
- Cell Line, Cell Nucleus, DNA-Binding Proteins, Humans, Motor Neurons, Protein Binding, Recombinant Proteins, Transcription Factors, Homeodomain Proteins, Dimerization, LIM Domain Proteins
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