Rotation of photoreceptor clusters in the developing drosophila eye requires the nemo gene

Choi, Kwang-Wook; Benzer, Seymour

doi:10.1016/0092-8674(94)90579-7

Cited by 339Developmental Biology and Gene RegulationAxon Guidance and Neuronal SignalingNeurobiology and Insect Physiology Research

Rotation of photoreceptor clusters in the developing drosophila eye requires the nemo gene

Open access

Choi, Kwang-Wook, Benzer, Seymour·1994·Cell

DOI 10.1016/0092-8674(94)90579-7

Open this paper in CoChat — free account

Abstract

The Drosophila eye consists of a reiterative hexagonal array of photoreceptor cell clusters, the ommatidia. During normal morphogenesis, the clusters in the dorsal or ventral halves of the disc rotate 90 degrees in opposite directions, forming mirror images across a dorsoventral equator. In the mutant nemo (nmo), there is an initial turning of approximately 45 degrees, but further rotation is blocked. Genetic mosaic analysis indicates that the nmo gene acts upon each cluster as a whole; normal nmo function in one or more photoreceptor cells appears to be sufficient to induce full rotation. The nmo gene sequence encodes a serine/threonine protein kinase homolog, suggesting that the kinase is required to initiate the second step of rotation. In another mutant, roulette, excessive rotation through varying angles occurs in many ommatidia. This defect is suppressed by nmo, indicating that nmo acts upstream in a rotation-regulating pathway.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/0092-8674(94)90579-7

Cites

49 of 49 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

NLK is an evolutionarily conserved serine/threonine protein kinase.
“NLK is an evolutionarily conserved serine/threonine protein kinase (Choi and Benzer, 1994; Banfi et al., 1996; Brott et al., 1998; Meneghini et al., 1999).”
From Polyglutamine Disease Toxicity Is Regulated by Nemo-like Kinase in Spinocerebellar Ataxia Type 1 (2013) · cites this paper as Choi and Benzer, 1994
The Introduction (page not supplied) says that the Drosophila nemo (nmo) locus encodes a homolog of serine/threonine protein kinases. The passages do not establish that NLK is evolutionarily conserved across species, so they support the kinase description but not that qualifier. (LLM, conf=0.86)
Experimental — accuracy not yet measured
NLK was originally identified in 1994 as the Drosophila gene nemo required for proper rotation of photoreceptor cells in the eye during ommatidia morphogenesis.
“was originally identified in 1994 as the Drosophila gene nemo required for proper rotation of photoreceptor cells in the eye during ommatidia morphogenesis [14].”
From Nemo-Like Kinase in Development and Diseases: Insights from Mouse Studies (2020) · cites this paper as [14]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Improved tools for biological sequence comparison.
Pearson, W. R., & Lipman, D. J. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.8.2444 · Cited by 11,227 · see citing works
The Protein Kinase Family: Conserved Features and Deduced Phylogeny of the Catalytic Domains
Hanks, S. K., Quinn, A. M., & Hunter, T. R. (1988) · Science · doi:10.1126/science.3291115 · Cited by 5,040 · see citing works
The Genome of Drosophila Melanogaster
Lindsley, D. L., & Zimm, G. G. (1992) · Cited by 3,090 · see citing works
A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback
Tautz, D., & Pfeifle, C. (1989) · Chromosoma · doi:10.1007/bf00291041 · Cited by 2,535 · see citing works
ERKs: A family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF
Boulton, T. G., Nye, S. H., Robbins, D. J., Ip, N. Y., Radzlejewska, E., Morgenbesser, S. D., DePinho, R. A., Panayotatos, N., Cobb, M. H., & Yancopoulos, G. D. (1991) · Cell · doi:10.1016/0092-8674(91)90098-j · Cited by 1,876 · see citing works
Crystal Structure of the Catalytic Subunit of Cyclic Adenosine Monophosphate-Dependent Protein Kinase
Knighton, D. R., Zheng, J., Eyck, L. F. T., Ashford, V. A., Xuong, N., Taylor, S. S., & Sowadski, J. M. (1991) · Science · doi:10.1126/science.1862342 · Cited by 1,764 · see citing works
Scatter factor is a fibroblast-derived modulator of epithelial cell mobility
Stoker, M. G. P., Gherardi, E., Perryman, M., & Gray, J. (1987) · Nature · doi:10.1038/327239a0 · Cited by 1,316 · see citing works
Identification of the regulatory phosphorylation sites in pp42/mitogen‐activated protein kinase (MAP kinase).
Payne, D. M., Rossomando, A. J., Martino, P. A., Erickson, A. K., Her, J. H., Shabanowitz, J., Hunt, D. F., Weber, M. J., & Sturgill, T. W. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb08021.x · Cited by 1,041 · see citing works
Development of the Drosophila retina, a neurocrystalline lattice
Ready, D. F., Hanson, T. E., & Benzer, S. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90225-6 · Cited by 1,030 · see citing works
Self-citation
Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector.Preprint
Bier, E., Vaessin, H., Younger-Shepherd, S., Lee, K. J., McCall, K., Barbel, S., Ackerman, L. D., Carretto, R., Uemura, T., & Grell, E. H. (1989) · Genes & Development · doi:10.1101/gad.3.9.1273 · Cited by 679 · see citing works
Neuronal differentiation in the Drosophila ommatidium
Tomlinson, A., & Ready, D. F. (1987) · Developmental Biology · doi:10.1016/0012-1606(87)90239-9 · Cited by 543 · see citing works
Sequence, structure, and codon preference of theDrosophilaribosomal protein 49 gene
O'Connell, P., & Rosbash, M. (1984) · Nucleic Acids Research · doi:10.1093/nar/12.13.5495 · Cited by 519 · see citing works
Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development
Robinow, S., & White, K. (1991) · Journal of Neurobiology · doi:10.1002/neu.480220503 · Cited by 507 · see citing works
The emergence of order in the Drosophila pupal retina
Cagan, R. L., & Ready, D. F. (1989) · Developmental Biology · doi:10.1016/0012-1606(89)90261-3 · Cited by 443 · see citing works
Making a difference: The role of cell-cell interactions in establishing separate identities for equivalent cells
Greenwald, I., & Rubin, G. M. (1992) · Cell · doi:10.1016/0092-8674(92)90470-w · Cited by 441 · see citing works
Focal adhesion kinase (p125FAK): A point of convergence in the action of neuropeptides, integrins, and oncogenes
Zachary, I. C., & Rozengurt, E. (1992) · Cell · doi:10.1016/0092-8674(92)90385-p · Cited by 439 · see citing works
breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells.Preprint
Klämbt, C., Glazer, L., & Shilo, B. (1992) · Genes & Development · doi:10.1101/gad.6.9.1668 · Cited by 430 · see citing works
Neuronal development in the drosophila retina: Monoclonal antibodies as molecular probes
Zipursky, S. L., Venkatesh, T., Teplow, D. B., & Benzer, S. (1984) · Cell · doi:10.1016/0092-8674(84)90069-2 · Cited by 425 · see citing works
Self-citation
The Met receptor tyrosine kinase transduces motility, proliferation, and morphogenic signals of scatter factor/hepatocyte growth factor in epithelial cells.
Weidner, K. M., Sachs, M., & Birchmeier, W. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.1.145 · Cited by 407 · see citing works
Cell adhesion molecules in vertebrate neural development.
Rutishauser, U. S., & Jessell, T. M. (1988) · Physiological Reviews · doi:10.1152/physrev.1988.68.3.819 · Cited by 387 · see citing works
A genetic analysis of the determination of cuticular polarity during development inDrosophila melanogaster
Gubb, D., & Garcı́a-Bellido, A. (1982) · Development · doi:10.1242/dev.68.1.37 · Cited by 369 · see citing works
Primary structure homology between the product of yeast cell division control gene CDC28 and vertebrate oncogenes
Lorincz, A. T., & Reed, S. I. (1984) · Nature · doi:10.1038/307183a0 · Cited by 356 · see citing works
dishevelled is required during wingless signaling to establish both cell polarity and cell identity
Theisen, H., Purcell, J. M., Bennett, M. K., Kansagara, D., Syed, A., & Marsh, J. (1994) · Development · doi:10.1242/dev.120.2.347 · Cited by 339 · see citing works
seven in absentia, a gene required for specification of R7 cell fate in the Drosophila eye
Carthew, R. W., & Rubin, G. M. (1990) · Cell · doi:10.1016/0092-8674(90)90452-k · Cited by 310 · see citing works
Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phosphorylation of FUS3 and KSS1.Preprint
Gartner, A., Nasmyth, K., & Ammerer, G. (1992) · Genes & Development · doi:10.1101/gad.6.7.1280 · Cited by 289 · see citing works
Drosophila: A practical approach
Whittle, J. R. S. (1987) · FEBS Letters · doi:10.1016/0014-5793(87)80456-8 · Cited by 255 · see citing works
Patterns of cell division and cell movement in the formation of the imaginal nervous system in Drosophila melanogaster
White, K. A., & Kankel, D. R. (1978) · Developmental Biology · doi:10.1016/0012-1606(78)90029-5 · Cited by 255 · see citing works
Chaoptin, a cell surface glycoprotein required for Drosophila photoreceptor cell morphogenesis, contains a repeat motif found in yeast and human
Reinke, R., Krantz, D. E., Yen, D., & Zipursky, S. L. (1988) · Cell · doi:10.1016/0092-8674(88)90518-1 · Cited by 207 · see citing works
From white spots to stem cells: the role of the Kit receptor in mammalian development
Fleischman, R. A. (1993) · Trends in Genetics · doi:10.1016/0168-9525(93)90015-a · Cited by 205 · see citing works
A multifaceted approach to neural development
Ready, D. F. (1989) · Trends in Neurosciences · doi:10.1016/0166-2236(89)90166-5 · Cited by 200 · see citing works
Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo
Ingham, P. W. (1993) · Nature · doi:10.1038/366560a0 · Cited by 173 · see citing works
The cellular dynamics of pattern formation in the eye of Drosophila
Tomlinson, A. (1985) · Development · doi:10.1242/dev.89.1.313 · Cited by 170 · see citing works
Epithelial morphogenesis
Gumbiner, B. M. (1992) · Cell · doi:10.1016/0092-8674(92)90440-n · Cited by 169 · see citing works
The formation of somites in Xenopus
Hamilton, L. (1969) · Development · doi:10.1242/dev.22.2.253 · Cited by 168 · see citing works
Induction of cell fate in the Drosophila retina: the bride of sevenless protein is predicted to contain a large extracellular domain and seven transmembrane segments.Preprint
Hart, A. C., Krämer, H., Vactor, D. V., Paidhungat, M., & Zipursky, S. L. (1990) · Genes & Development · doi:10.1101/gad.4.11.1835 · Cited by 164 · see citing works
The role of cell-cell interaction in the development of the drosophila visual system
Banerjee, U. K., & Zipursky, S. L. (1990) · Neuron · doi:10.1016/0896-6273(90)90093-u · Cited by 163 · see citing works
Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginal discs
Baker, N. E., & Rubin, G. M. (1992) · Developmental Biology · doi:10.1016/0012-1606(92)90250-k · Cited by 133 · see citing works
MsERK1: A Mitogen-Activated Protein Kinase from a Flowering Plant
Duerr, B., Gawienowski, M., Ropp, T., & Jacobs, T. (1993) · The Plant Cell · doi:10.1105/tpc.5.1.87 · Cited by 132 · see citing works
The mechanism of evagination of imaginal discs of Drosophila melanogaster,
Fristrom, D. K. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90296-7 · Cited by 129 · see citing works
Cloning of Drosophila choline acetyltransferase cDNA.
Itoh, N., Slemmon, J. R., Hawke, D. H., Williamson, R., Morita, E. A., Itakura, K., Roberts, E. R., Shively, J. E., Crawford, G. D., & Salvaterra, P. M. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.11.4081 · Cited by 124 · see citing works
Primary structure, expression, and signal-dependent tyrosine phosphorylation of a Drosophila homolog of extracellular signal-regulated kinase.
Biggs, W., & Zipursky, S. L. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.14.6295 · Cited by 120 · see citing works
Embryonic head involution and rotation of male terminalia require the Drosophila locus head involution defective.
Abbott, M. K., & Lengyel, J. A. (1991) · Genetics · doi:10.1093/genetics/129.3.783 · Cited by 109 · see citing works
Zygotic expression of the pebble locus is required for cytokinesis during the postblastoderm mitoses of Drosophila
Hime, G. R., & Saint, R. B. (1992) · Development · doi:10.1242/dev.114.1.165 · Cited by 87 · see citing works
Raf‐1 is required for T cell IL2 production.
Owaki, H., Varma, R., Gillis, B. E., Bruder, J. T., Rapp, U. R., Davis, L. S., & Geppert, T. D. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb06121.x · Cited by 77 · see citing works
The fine structure of the eye imaginal disks in muscoid flies
Melamed, J., & Trujillo-Cenóz, O. (1975) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(75)80010-4 · Cited by 58 · see citing works
Sequence patterns in protein kinases
Bairoch, A., & Claverie, J. (1988) · Nature · doi:10.1038/331022a0 · Cited by 43 · see citing works
Allelic variation at the frizzled locus of Drosophila
Adler, P. N., Charlton, J., & Vinson, C. (1987) · Developmental Genetics · doi:10.1002/dvg.1020080206 · Cited by 42 · see citing works
The mechanism of axial rotation in the rat embryo: an experimental study in vitro
DEUCHAR, E. M. (1971) · Development · doi:10.1242/dev.25.2.189 · Cited by 33 · see citing works
Mutations on the Second Chromosome Affecting theDrosophilaEye
Baker, N. E., Moses, K., Nakahara, D., Ellis, M. C., Carthew, R. W., & Rubin, G. M. (1992) · Journal of Neurogenetics · doi:10.3109/01677069209084154 · Cited by 25 · see citing works

Flagged first, then by citations

Sorted by citations

Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases
Cargnello, M., & Roux, P. P. (2011) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00031-10 · Cited by 3,274 · see citing works
Pro-inflammatory Cytokines and Environmental Stress Cause p38 Mitogen-activated Protein Kinase Activation by Dual Phosphorylation on Tyrosine and Threonine
Raingeaud, J., Gupta, S., Rogers, J. S., Dickens, M., Han, J., Ulevitch, R. J., & Davis, R. J. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.13.7420 · Cited by 2,244 · see citing works
Signaling Through Scaffold, Anchoring, and Adaptor Proteins
Pawson, T., & Scott, J. D. (1997) · Science · doi:10.1126/science.278.5346.2075 · Cited by 2,256 · see citing works
The Transcriptional Program of Sporulation in Budding Yeast
Chu, S., DeRisi, J. L., Eisen, M. B., Mulholland, J., Botstein, D., Brown, P. O., & Herskowitz, I. (1998) · Science · doi:10.1126/science.282.5389.699 · Cited by 1,860 · see citing works
Signal Transduction through MAP Kinase Cascades
Lewis, T. S., Shapiro, P. S., & Ahn, N. G. (1998) · Advances in cancer research · doi:10.1016/s0065-230x(08)60765-4 · Cited by 1,746 · see citing works
Parallel signal processing among mammalian MAPKs
Cano, E., & Mahadevan, L. C. (1995) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(00)88978-1 · Cited by 1,009 · see citing works
MAPKs: new JNK expands the group
Davis, R. J. (1994) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(94)90132-5 · Cited by 944 · see citing works
G PROTEIN βγ SUBUNITS
Clapham, D. E., & Neer, E. J. (1997) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.37.1.167 · Cited by 842 · see citing works
Identification of a Dual Specificity Kinase That Activates the Jun Kinases and p38-Mpk2
Lin, A., Minden, A., Martinetto, H., Claret, F.-X., Lange, C. A., Mercurio, F., Johnson, G. L., & Karin, M. (1995) · Science · doi:10.1126/science.7716521 · Cited by 763 · see citing works
Protein Interaction Mapping in C. elegans Using Proteins Involved in Vulval Development
Walhout, A. J. M., Sordella, R., Lu, X., Hartley, J. L., Temple, G. F., Brasch, M. A., Thierry‐Mieg, N., & Vidal, M. (2000) · Science · doi:10.1126/science.287.5450.116 · Cited by 757 · see citing works
A Cytoplasmic Inhibitor of the JNK Signal Transduction Pathway
Dickens, M., Rogers, J. S., Cavanagh, J., Raitano, A., Xia, Z., Halpern, J. R., Greenberg, M. E., Sawyers, C. L., & Davis, R. J. (1997) · Science · doi:10.1126/science.277.5326.693 · Cited by 675 · see citing works
Structure and function of phosphoinositide 3-kinases
Wymann, M. P., & Pirola, L. (1998) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/s0005-2760(98)00139-8 · Cited by 662 · see citing works
A Mammalian Scaffold Complex That Selectively Mediates MAP Kinase Activation
Whitmarsh, A. J., Cavanagh, J., Tournier, C., Yasuda, J., & Davis, R. J. (1998) · Science · doi:10.1126/science.281.5383.1671 · Cited by 652 · see citing works
Cell Signaling in Space and Time: Where Proteins Come Together and When They’re Apart
Scott, J. D., & Pawson, T. J. (2009) · Science · doi:10.1126/science.1175668 · Cited by 648 · see citing works
The TAK1–NLK–MAPK-related pathway antagonizes signalling between β-catenin and transcription factor TCF
Ishitani, T., Ninomiya-Tsuji, J., Nagai, S.-I., Nishita, M., Meneghini, M., Barker, N., Waterman, M., Bowerman, B., Clevers, H., Shibuya, H., et al. (1999) · Nature · doi:10.1038/21674 · Cited by 624 · see citing works
AKAPs: from structure to function
Colledge, M., & Scott, J. D. (1999) · Trends in Cell Biology · doi:10.1016/s0962-8924(99)01558-5 · Cited by 611 · see citing works
Planar Cell Polarity Signaling: From Fly Development to Human Disease
Simons, M., & Mlodzik, M. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.42.110807.091432 · Cited by 570 · see citing works
Osmotic Activation of the HOG MAPK Pathway via Ste11p MAPKKK: Scaffold Role of Pbs2p MAPKK
Posas, F., & Saito, H. (1997) · Science · doi:10.1126/science.276.5319.1702 · Cited by 565 · see citing works
The role of RhoA in tissue polarity and Frizzled signalling
Strutt, D. I., Weber, U., & Mlodzik, M. (1997) · Nature · doi:10.1038/387292a0 · Cited by 560 · see citing works
Regulation of Myosin Phosphatase by a Specific Interaction with cGMP- Dependent Protein Kinase Iα
Surks, H. K., Mochizuki, N., Kasai, Y., Georgescu, S. P., Tang, K. M., Ito, M., Lincoln, T., & Mendelsohn, M. E. (1999) · Science · doi:10.1126/science.286.5444.1583 · Cited by 527 · see citing works
Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility
Seifert, J. R. K., & Mlodzik, M. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2042 · Cited by 513 · see citing works
Regulation of NMDA Receptors by an Associated Phosphatase-Kinase Signaling Complex
Westphal, R. S., Tavalin, S. J., Lin, J., Alto, N. M., Fraser, I. D. C., Langeberg, L. K., Sheng, M., & Scott, J. D. (1999) · Science · doi:10.1126/science.285.5424.93 · Cited by 492 · see citing works
Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties
Levchenko, A., Bruck, J., & Sternberg, P. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.11.5818 · Cited by 486 · see citing works
Regulation and function of the JNK subgroup of MAP kinases
Minden, A., & Karin, M. (1997) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/s0304-419x(97)00018-8 · Cited by 486 · see citing works
MP1: A MEK Binding Partner That Enhances Enzymatic Activation of the MAP Kinase Cascade
Schaeffer, H. J., Catling, A. D., Eblen, S. T., Collier, L. S., Krauss, A., & Weber, M. J. (1998) · Science · doi:10.1126/science.281.5383.1668 · Cited by 472 · see citing works
Domains, Motifs, and Scaffolds: The Role of Modular Interactions in the Evolution and Wiring of Cell Signaling Circuits
Bhattacharyya, R. P., Reményi, A., Yeh, B. J., & Lim, W. A. (2006) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.75.103004.142710 · Cited by 458 · see citing works
INITIATION AND PROCESSING OF SIGNALS FROM THE B CELL ANTIGEN RECEPTOR
Reth, M. G., & Wienands, J. (1997) · Annual Review of Immunology · doi:10.1146/annurev.immunol.15.1.453 · Cited by 436 · see citing works
Regulation of G Protein–Initiated Signal Transduction in Yeast: Paradigms and Principles
Dohlman, H. G., & Thorner, J. W. (2001) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.70.1.703 · Cited by 425 · see citing works
PSD-95 promotes Fyn-mediated tyrosine phosphorylation of the N -methyl- d -aspartate receptor subunit NR2A
Tezuka, T., Umemori, H., Akiyama, T., Nakanishi, S., & Yamamoto, T. S. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.2.435 · Cited by 377 · see citing works
Substrate recruitment to cyclin-dependent kinase 2 by a multipurpose docking site on cyclin A
Schulman, B. A., Lindstrom, D. L., & Harlow, E. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.18.10453 · Cited by 366 · see citing works
Rewiring MAP Kinase Pathways Using Alternative Scaffold Assembly Mechanisms
Park, S.-H., Zarrinpar, A., & Lim, W. A. (2003) · Science · doi:10.1126/science.1076979 · Cited by 355 · see citing works
Mechanistic Studies of the Dual Phosphorylation of Mitogen-activated Protein Kinase
Ferrell, J. E., & Bhatt, R. R. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.30.19008 · Cited by 344 · see citing works
Global Tissue Revolutions in a Morphogenetic Movement Controlling Elongation
Haigo, S. L., & Bilder, D. H. (2011) · Science · doi:10.1126/science.1199424 · Cited by 344 · see citing works
Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation?
Mlodzik, M. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(02)02770-1 · Cited by 341 · see citing works
strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila
Wolff, T., & Rubin, G. M. (1998) · Development · doi:10.1242/dev.125.6.1149 · Cited by 321 · see citing works
Comprehensive Analysis of Photoreceptor Gene Expression and the Identification of Candidate Retinal Disease Genes
Blackshaw, S., Fraioli, R. E., Furukawa, T., & Cepko, C. L. (2001) · Cell · doi:10.1016/s0092-8674(01)00574-8 · Cited by 303 · see citing works
Atypical mitogen-activated protein kinases: Structure, regulation and functions
Coulombe, P., & Meloche, S. (2007) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2006.11.001 · Cited by 298 · see citing works
MAP kinase and Wnt pathways converge to downregulate an HMG-domain repressor in Caenorhabditis elegans
Meneghini, M. D., Ishitani, T., Carter, J. C., Hisamoto, N., Ninomiya-Tsuji, J., Thorpe, C. J., Hamill, D. R., Matsumoto, K., & Bowerman, B. (1999) · Nature · doi:10.1038/21666 · Cited by 293 · see citing works
IKAP is a scaffold protein of the IκB kinase complex
Cohen, L., Henzel, W. J., & Baeuerle, P. A. (1998) · Nature · doi:10.1038/26254 · Cited by 288 · see citing works
WRM-1 Activates the LIT-1 Protein Kinase to Transduce Anterior/Posterior Polarity Signals in C. elegans
Rocheleau, C. E., Yasuda, J., Shin, T. H., Lin, R., Sawa, H., Okano, H., Priess, J. R., Davis, R. J., & Mello, C. C. (1999) · Cell · doi:10.1016/s0092-8674(00)80784-9 · Cited by 276 · see citing works
The Ste5 Scaffold Allosterically Modulates Signaling Output of the Yeast Mating Pathway
Bhattacharyya, R. P., Reményi, A., Good, M. C., Bashor, C. J., Falick, A. M., & Lim, W. A. (2006) · Science · doi:10.1126/science.1120941 · Cited by 276 · see citing works
Dishevelled: at the crossroads of divergent intracellular signaling pathways
Boutros, M., & Mlodzik, M. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00046-5 · Cited by 275 · see citing works
Protein Kinase A Anchoring
Dell’Acqua, M. L., & Scott, J. D. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.20.12881 · Cited by 271 · see citing works
CELL POLARITY AND MORPHOGENESIS IN BUDDING YEAST
Madden, K. T., & Snyder, M. P. (1998) · Annual Review of Microbiology · doi:10.1146/annurev.micro.52.1.687 · Cited by 266 · see citing works
Designing customized cell signalling circuits
Lim, W. A. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2904 · Cited by 257 · see citing works
Characterization of a Novel Giant Scaffolding Protein, CG-NAP, That Anchors Multiple Signaling Enzymes to Centrosome and the Golgi Apparatus
Takahashi, M., Shibata, H., Shimakawa, M., Miyamoto, M., Mukai, H., & Ono, Y. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.24.17267 · Cited by 251 · see citing works
Frizzled signalling and cell polarisation inDrosophilaand vertebrates
Strutt, D. I. (2003) · Development · doi:10.1242/dev.00695 · Cited by 243 · see citing works
The roles of MAPKs in disease
Lawrence, M. C., Jivan, A., Shao, C., Duan, L., Goad, D. L., Zaganjor, E., Osborne, J. K., McGlynn, K., Stippec, S., Earnest, S. A., et al. (2008) · Cell Research · doi:10.1038/cr.2008.37 · Cited by 233 · see citing works
Molecular Cloning of Mitogen-activated Protein/ERK Kinase Kinases (MEKK) 2 and 3
Blank, J. L., Gerwins, P., Elliott, E. M., Sather, S., & Johnson, G. L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.10.5361 · Cited by 230 · see citing works
More on target with protein phosphorylation: conferring specificity by location.
Faux, M. C., & Scott, J. D. (1996) · PubMed · Cited by 229 · see citing works
Planar polarity from flies to vertebrates
Fanto, M., & McNeill, H. (2004) · Journal of Cell Science · doi:10.1242/jcs.00973 · Cited by 224 · see citing works
The Role of Far1p in Linking the Heterotrimeric G Protein to Polarity Establishment Proteins During Yeast Mating
Butty, A.-C., Pryciak, P. M., Huang, L. S., Herskowitz, I., & Peter, M. (1998) · Science · doi:10.1126/science.282.5393.1511 · Cited by 227 · see citing works
frizzled regulates mirror-symmetric pattern formation in the Drosophila eye
Zheng, L., Zhang, J., & Carthew, R. W. (1995) · Development · doi:10.1242/dev.121.9.3045 · Cited by 227 · see citing works
Canonical and noncanonical Wnt signaling: Multilayered mediators, signaling mechanisms and major signaling crosstalk
Qin, K. H., Yu, M. S., Fan, J., Wang, H., Zhao, P., Zhao, G., Zeng, W., Chen, C., Wang, Y., Wang, A., et al. (2023) · Genes & Diseases · doi:10.1016/j.gendis.2023.01.030 · Cited by 236 · see citing works
Alternative Wnt Pathways and ReceptorsPreprint
van Amerongen, R. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a007914 · Cited by 220 · see citing works
wingless and patched are negative regulators of the morphogenetic furrow and can affect tissue polarity in the developing Drosophila compound eye
Ma, C., & Moses, K. (1995) · Development · doi:10.1242/dev.121.8.2279 · Cited by 210 · see citing works
Activation of the SAPK pathway by the human STE20 homologue germinal centre kinase
Pombo, C. M., Kehrl, J. H., Sánchez, I., Katz, P., Avruch, J., Zon, L. I., Woodgett, J. R., Force, T. L., & Kyriakis, J. M. (1995) · Nature · doi:10.1038/377750a0 · Cited by 210 · see citing works
Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait
Toma, D. P., White, K. P., Hirsch, J., & Greenspan, R. J. (2002) · Nature Genetics · doi:10.1038/ng893 · Cited by 204 · see citing works
Identification of Kinase-Phosphatase Signaling Modules Composed of p70 S6 Kinase-Protein Phosphatase 2A (PP2A) and p21-activated Kinase-PP2A
Westphal, R. S., Coffee, R. L., Marotta, A., Pelech, S., & Wadzinski, B. E. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.2.687 · Cited by 202 · see citing works
Reconstitution of Mitogen-activated Protein Kinase Phosphorylation Cascades in Bacteria
Khokhlatchev, A. V., Xu, S., English, J. M., Wu, P., SCHAEFER, E. M., & Cobb, M. H. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.17.11057 · Cited by 200 · see citing works
Unifying principles of bifunctional, proximity-inducing small molecules
Gerry, C. J., & Schreiber, S. L. (2020) · Nature Chemical Biology · doi:10.1038/s41589-020-0469-1 · Cited by 199 · see citing works
Hog1: 20 years of discovery and impact
Brewster, J. L., & Gustin, M. C. (2014) · Science Signaling · doi:10.1126/scisignal.2005458 · Cited by 197 · see citing works
Cascades in Compartments: En Route to Machine‐Assisted Biotechnology
Rabe, K. S., Müller, J., Skoupi, M., & Niemeyer, C. M. (2017) · Angewandte Chemie International Edition · doi:10.1002/anie.201703806 · Cited by 196 · see citing works
Nuclear signaling by Rac and Rho GTPases is required in the establishment of epithelial planar polarity in the Drosophila eye
Fanto, M., Weber, U., Strutt, D. I., & Mlodzik, M. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00645-x · Cited by 193 · see citing works
Isolation of ATMEKK1 (a MAP Kinase Kinase Kinase)-Interacting Proteins and Analysis of a MAP Kinase Cascade inArabidopsis
Ichimura, K., Mizoguchi, T., Irie, K., Morris, P. C., Giraudat, J., Matsumoto, K., & Shinozaki, K. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.9796 · Cited by 191 · see citing works
Cloning and Characterization of MEK6, a Novel Member of the Mitogen-activated Protein Kinase Kinase Cascade
Stein, B., Brady, H. A., Yang, M. X., Young, D. B., & Barbosa, M. S. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.19.11427 · Cited by 190 · see citing works
Binding Specificity for RACK1 Resides in the V5 Region of βII Protein Kinase C
Stebbins, E. G., & Mochly‐Rosen, D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m101044200 · Cited by 183 · see citing works
Frizzled signaling and the developmental control of cell polarity
Shulman, J. M., Perrimon, N., & Axelrod, J. D. (1998) · Trends in Genetics · doi:10.1016/s0168-9525(98)01584-4 · Cited by 181 · see citing works
Molecular Characterization of Ste20p, a Potential Mitogen-activated Protein or Extracellular Signal-regulated Kinase Kinase (MEK) Kinase Kinase from Saccharomyces cerevisiae
Wu, C., Whiteway, M. S., Thomas, D. Y., & Leberer, E. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.27.15984 · Cited by 180 · see citing works
mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye.Preprint
McNeill, H., Yang, C.-H., Brodsky, M., Ungos, J. M., & Simon, M. A. (1997) · Genes & Development · doi:10.1101/gad.11.8.1073 · Cited by 180 · see citing works
Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye
Cho, K.-O., & Choi, K. (1998) · Nature · doi:10.1038/24394 · Cited by 179 · see citing works
Self-citation
NEMO/NLK Phosphorylates PERIOD to Initiate a Time-Delay Phosphorylation Circuit that Sets Circadian Clock Speed
Chiu, J. C., Ko, H. W., & Edery, I. (2011) · Cell · doi:10.1016/j.cell.2011.04.002 · Cited by 178 · see citing works
MST/MLK2, a Member of the Mixed Lineage Kinase Family, Directly Phosphorylates and Activates SEK1, an Activator of c-Jun N-terminal Kinase/Stress-activated Protein Kinase
Hirai, S.-I., Katoh, M., Terada, M., Kyriakis, J. M., Zon, L. I., Rana, A., Avruch, J., & Ohno, S. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.24.15167 · Cited by 178 · see citing works
A Conserved Docking Site in MEKs Mediates High-affinity Binding to MAP Kinases and Cooperates with a Scaffold Protein to Enhance Signal Transmission
Bardwell, A. J., Flatauer, L. J., Matsukuma, K. E., Thorner, J. W., & Bardwell, L. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010271200 · Cited by 177 · see citing works
Raf induces NF-κB by membrane shuttle kinase MEKK1, a signaling pathway critical for transformation
Baumann, B., Weber, C. K., Troppmair, J., Whiteside, S. T., Israël, A., Rapp, U. R., & Wirth, T. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.080583397 · Cited by 177 · see citing works
Planar polarity in the Drosophila eye: a multifaceted view of signaling specificity and cross‐talk
Mlodzik, M. (1999) · The EMBO Journal · doi:10.1093/emboj/18.24.6873 · Cited by 172 · see citing works
Multiple intracellular MAP kinase signaling cascades
Bokemeyer, D., Sorokin, A., & Dunn, M. J. (1996) · Kidney International · doi:10.1038/ki.1996.172 · Cited by 173 · see citing works
Association of the Yeast Pheromone Response G Protein βγ Subunits with the Map Kinase Scaffold Ste5p
Whiteway, M. S., Wu, C., Leeuw, T., Clark, K., Fourest‐Lieuvin, A., Thomas, D. Y., & Leberer, E. (1995) · Science · doi:10.1126/science.7667635 · Cited by 170 · see citing works
Actin-biding Protein-280 Binds the Stress-activated Protein Kinase (SAPK) Activator SEK-1 and Is Required for Tumor Necrosis Factor-α Activation of SAPK in Melanoma Cells
Martí, A., Luo, Z., Cunningham, C. C., Ohta, Y., Hartwig, J. H., Stossel, T. P., Kyriakis, J. M., & Avruch, J. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.5.2620 · Cited by 169 · see citing works
Ste5 RING-H2 Domain: Role in Ste4-Promoted Oligomerization for Yeast Pheromone Signaling
Inouye, C. J., Dhillon, N., & Thorner, J. W. (1997) · Science · doi:10.1126/science.278.5335.103 · Cited by 168 · see citing works
Yeast two-hybrid: State of the art
Criekinge, W. V., & Beyaert, R. (1999) · Biological Procedures Online · doi:10.1251/bpo16 · Cited by 162 · see citing works
Cross-talk and decision making in MAP kinase pathways
McClean, M. N., Mody, A., Broach, J. R., & Ramanathan, S. (2007) · Nature Genetics · doi:10.1038/ng1957 · Cited by 159 · see citing works
MEKK2 Associates with the Adapter Protein Lad/RIBP and Regulates the MEK5-BMK1/ERK5 Pathway
Sun, W., Kesavan, K. P., Schaefer, B. C., Garrington, T. P., Ware, M. F., Johnson, N. L., Gelfand, E. W., & Johnson, G. L. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m003719200 · Cited by 159 · see citing works
The MAPKKK Ste11 regulates vegetative growth through a kinase cascade of shared signaling components
Lee, B. N., & Elion, E. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12679 · Cited by 156 · see citing works
Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion
Fleißner, A., Leeder, A. C., Roca, M. G., Read, N. D., & Glass, N. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907039106 · Cited by 155 · see citing works
SAM: A novel motif in yeast sterile anddrosophilapolyhomeotic proteins
Ponting, C. P. (1995) · Protein Science · doi:10.1002/pro.5560040927 · Cited by 152 · see citing works
OMTK1, a Novel MAPKKK, Channels Oxidative Stress Signaling through Direct MAPK Interaction
Nakagami, H., Kiegerl, S., & Heribert Hirt, A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m312662200 · Cited by 149 · see citing works
Hairy and Emc negatively regulate morphogenetic furrow progression in the drosophila eye
Brown, N. L., Sattler, C. A., Paddock, S. W., & Carroll, S. B. (1995) · Cell · doi:10.1016/0092-8674(95)90291-0 · Cited by 145 · see citing works
Identification of a Motif in the Carboxyl Terminus of β-Arrestin2 Responsible for Activation of JNK3
Miller, W. E., McDonald, P. H., Cai, S. F., Field, M. E., Davis, R. J., & Lefkowitz, R. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102264200 · Cited by 145 · see citing works
Protein interaction maps for model organisms
Walhout, A. J. M., & Vidal, M. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35048107 · Cited by 144 · see citing works
Phosphorylation by the β-Catenin/MAPK Complex Promotes 14-3-3-Mediated Nuclear Export of TCF/POP-1 in Signal-Responsive Cells in C. elegans
Lo, M.-C., Gay, F., Odom, R., Shi, Y., & Lin, R. (2004) · Cell · doi:10.1016/s0092-8674(04)00203-x · Cited by 138 · see citing works
MAP kinase dynamics in response to pheromones in budding yeast
van Drogen, F., Stucke, V. M., Jorritsma, G., & Peter, M. (2001) · Nature Cell Biology · doi:10.1038/ncb1201-1051 · Cited by 143 · see citing works
Dynamic analysis of MAPK signaling using a high-throughput microfluidic single-cell imaging platform
Taylor, R. J., Falconnet, D., Niemistö, A., Ramsey, S. A., Prinz, S., Ilya Shmulevich, C., Galitski, T., & Hansen, C. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813416106 · Cited by 141 · see citing works
JLP: A scaffolding protein that tethers JNK/p38MAPK signaling modules and transcription factors
Lee, C. M., Onésime, D., Reddy, C. D., Dhanasekaran, N., & Reddy, E. P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.232310199 · Cited by 139 · see citing works
Novel Signaling from the Peripodial Membrane Is Essential for Eye Disc Patterning in Drosophila
Cho, K.-O., Chern, J. J., Izaddoost, S. A., & Choi, K. (2000) · Cell · doi:10.1016/s0092-8674(00)00124-0 · Cited by 134 · see citing works
Self-citation
Mapping dynamic protein interactions in MAP kinase signaling using live-cell fluorescence fluctuation spectroscopy and imaging
Slaughter, B. D., Schwartz, J. W., & Li, R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710336105 · Cited by 131 · see citing works
Routing MAP Kinase Cascades
Elion, E. A. (1998) · Science · doi:10.1126/science.281.5383.1625 · Cited by 133 · see citing works
Nemo-like kinase suppresses Notch signalling by interfering with formation of the Notch active transcriptional complex
Ishitani, T., Hirao, T., Suzuki, M., Isoda, M., Ishitani, S., Harigaya, K., Kitagawa, M., Matsumoto, K., & Itoh, M. (2010) · Nature Cell Biology · doi:10.1038/ncb2028 · Cited by 131 · see citing works
Cell Cycle and Hormonal Control of Nuclear-Cytoplasmic Localization of the Serum- and Glucocorticoid-inducible Protein Kinase, Sgk, in Mammary Tumor Cells
Buse, P., Tran, S. H., Luther, E., Phu, P. T., Aponte, G. W., & Firestone, G. L. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.11.7253 · Cited by 131 · see citing works
Nlk is a murine protein kinase related to Erk/MAP kinases and localized in the nucleus
Brott, B. K., Pinsky, B. A., & Erikson, R. L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.3.963 · Cited by 130 · see citing works

Nemo is required in a subset of photoreceptors to regulate the speed of ommatidial rotation
Fiehler, R. W., & Wolff, T. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.10.034 · Cited by 26 · see citing works
Nemo regulates cell dynamics and represses the expression of miple, a midkine/pleiotrophin cytokine, during ommatidial rotation
Muñoz, V. F. L., Ruiz, C., Pérez‐Alonso, M., Mlodzik, M., & Paricio, N. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.02.006 · Cited by 11 · see citing works
The protein kinase Nemo integrates specification, proliferation and morphogenesis to shape the Drosophila eye
Braid, L. R. (2011) · Summit (Simon Fraser University)
Drosophila Nemo Promotes Eye Specification Directed by the Retinal Determination Gene Network
Braid, L. R., & Verheyen, E. M. (2008) · Genetics · doi:10.1534/genetics.108.092155 · Cited by 33 · see citing works
Nemo phosphorylates Eyes absent and enhances output from the Eya-Sine oculis transcriptional complex during Drosophila retinal determination
Morillo, S. A., Braid, L. R., Verheyen, E. M., & Rebay, I. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.02.030 · Cited by 22 · see citing works

Authors: Choi, K.-W., & Benzer, S.
Affiliations: California Institute of Technology (US)
ORCID: Choi, Kwang-Wook
Venue: Cell
Publisher: Elsevier BV
Published: 1994-07
Volume: 78
Issue: 1
Pages: 125-136
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/0092-8674(94)90579-7
OpenAlex: W1975803734
Cited by: 339
References: 49
Citations by year: 2025: 2 · 2024: 4 · 2023: 4 · 2022: 10 · 2021: 6 · 2020: 5 · 2019: 5 · 2018: 4 · 2017: 5 · 2016: 5 · 2015: 7 · 2014: 5 · 2013: 9 · 2012: 10
FWCI: 7.22
Type: journal article
Language: en
Open access: green
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
CaltechAUTHORS (California Institute of Technology) (submittedVersion)
Zenodo (CERN European Organization for Nuclear Research) (cc-by)
Funders: National Science Foundation (8908154)
James G. Boswell Foundation
National Institutes of Health
National Eye Institute (EY0 9278)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Keywords: NEMO gene, serine/threonine kinase
MeSH terms: Amino Acid Sequence, Animals, Base Sequence, Chromosome Mapping, Cloning, Molecular, Drosophila, Eye, Female, Male, Molecular Sequence Data, Mutation, Suppression, Genetic, Gene Expression, Genes, Insect, Protein Serine-Threonine Kinases, Sequence Homology, Amino Acid, Sequence Analysis, DNA, Photoreceptor Cells, Invertebrate, Mitogen-Activated Protein Kinases, Drosophila Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Rotation of photoreceptor clusters in the developing drosophila eye requires the nemo gene

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks