Cited by 103Hedgehog Signaling Pathway StudiesGenetic and Kidney Cyst DiseasesDevelopmental Biology and Gene Regulation

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Tubby-like protein 3 (TULP3) regulates patterning in the mouse embryo through inhibition of Hedgehog signaling

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Norman, Ryan X., Ko, Hyuk W., Huang, Viola, Eun, Christine M., Abler, Lisa L., Zhang, Zhen, Sun, Xin, Eggenschwiler, Jonathan T.·2009·Human Molecular Genetics

DOI 10.1093/hmg/ddp113PMC PMC2671991

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Abstract

Tubby-like protein 3 (TULP3) is required for proper embryonic development in mice. Disruption of mouse Tulp3 results in morphological defects in the embryonic craniofacial regions, the spinal neural tube and the limbs. Here, we show that TULP3 functions as a novel negative regulator of Sonic hedgehog (Shh) signaling in the mouse. In Tulp3 mutants, ventral cell types in the lumbar neural tube, which acquire their identities in response to Shh signaling, are ectopically specified at the expense of dorsal cell types. Genetic epistasis experiments show that this ventralized phenotype occurs independently of Shh and the transmembrane protein Smoothened, but it is dependent on the transcription factor Gli2. The ventralized phenotype is also dependent on the kinesin II subunit Kif3A, which is required for intraflagellar transport and ciliogenesis. In addition, TULP3 is required for proper Shh-dependent limb patterning and for maintaining the correct balance between differentiation and proliferation in the neural tube. Finally, the localization of TULP3 to the tips of primary cilia raises the possibility that it regulates the Hedgehog pathway within this structure.

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A Laboratory manual
Ashburner, M. (1989) · Cold Spring Harbor Laboratory eBooks · Cited by 6,756
Manipulating the mouse embryo: A laboratory manual
Hogan, B. L. M., Costantini, F. D., & Lacy, E. (1986) · Cited by 4,460
Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function
Chiang, C. C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H., & Beachy, P. A. (1996) · Nature · doi:10.1038/383407a0 · Cited by 3,062
Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity
Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A., & McMahon, A. P. (1993) · Cell · doi:10.1016/0092-8674(93)90627-3 · Cited by 2,154
Manipulating the Mouse Embryo: A Laboratory Manual
Behringer, R. R., Gertsenstein, M., Nagy, K. V., & Nagy, A. (2002) · Cited by 2,046
Vertebrate Smoothened functions at the primary cilium
Corbit, K. C., Aanstad, P., Singla, V., Norman, A. R., Stainier, D. Y. R., & Reiter, J. F. (2005) · Nature · doi:10.1038/nature04117 · Cited by 1,481
Patched1 Regulates Hedgehog Signaling at the Primary Cilium
Rohatgi, R., Milenkovic, L., & Scott, M. P. (2007) · Science · doi:10.1126/science.1139740 · Cited by 1,426
Hedgehog signalling in the mouse requires intraflagellar transport proteins
Huangfu, D., Liu, A., Rakeman, A. S., Murcia, N. S., Niswander, L., & Anderson, K. V. (2003) · Nature · doi:10.1038/nature02061 · Cited by 1,425
A Core Complex of BBS Proteins Cooperates with the GTPase Rab8 to Promote Ciliary Membrane Biogenesis
Nachury, M. V., Loktev, A. V., Zhang, Q., Westlake, C. J., Peränen, J., Merdes, A., Slusarski, D. C., Scheller, R. H., Bazan, J. F., Sheffield, V. C., et al. (2007) · Cell · doi:10.1016/j.cell.2007.03.053 · Cited by 1,384
Hedgehog: functions and mechanisms
Varjosalo, M., & Taipale, J. (2008) · Genes & Development · doi:10.1101/gad.1693608 · Cited by 1,217
A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes
Schaeren‐Wiemers, N., & Gerfin-Moser, A. (1993) · Histochemistry and Cell Biology · doi:10.1007/bf00267823 · Cited by 1,151
The bHLH Transcription Factors OLIG2 and OLIG1 Couple Neuronal and Glial Subtype Specification
Zhou, Q., & Anderson, D. J. (2002) · Cell · doi:10.1016/s0092-8674(02)00677-3 · Cited by 1,059
Cyclin D1 provides a link between development and oncogenesis in the retina and breast
Sicinski, P., Donaher, J. L., Parker, S. B., Li, T., Fazeli, A., Gardner, H., Haslam, S. Z., Bronson, R. T., Elledge, S. J., & Weinberg, R. A. (1995) · Cell · doi:10.1016/0092-8674(95)90034-9 · Cited by 1,021
Mutant sensory cilia in the nematode Caenorhabditis elegans
Perkins, L. A., Hedgecock, E. M., Thomson, J. N., & Culotti, J. G. (1986) · Developmental Biology · doi:10.1016/0012-1606(86)90314-3 · Cited by 907
Gli2 and Gli3 Localize to Cilia and Require the Intraflagellar Transport Protein Polaris for Processing and Function
Haycraft, C. J., Banizs, B., Aydin-Son, Y., Zhang, Q., Michaud, E. J., & Yoder, B. K. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010053 · Cited by 902
Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis
Roelink, H., Porter, J. A., Chiang, C. C., Tanabe, Y., Chang, D. T., Beachy, P. A., & Jessell, T. M. (1995) · Cell · doi:10.1016/0092-8674(95)90397-6 · Cited by 888
Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog.Preprint
Goodrich, L. V., Johnson, R. L., Milenković, L., McMahon, J. A., & Scott, M. P. (1996) · Genes & Development · doi:10.1101/gad.10.3.301 · Cited by 825
Cilia and Hedgehog responsiveness in the mouse
Huangfu, D., & Anderson, K. V. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0505328102 · Cited by 820
Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein
Chuang, P., & McMahon, A. P. (1999) · Nature · doi:10.1038/17611 · Cited by 798
Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects.Preprint
Ishibashi, M., Ang, S., Shiota, K., Nakanishi, S., Kageyama, R., & Guillemot, F. (1995) · Genes & Development · doi:10.1101/gad.9.24.3136 · Cited by 767
The Graded Response to Sonic Hedgehog Depends on Cilia Architecture
Caspary, T., Larkins, C. E., & Anderson, K. V. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.03.004 · Cited by 738
Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis
Siciński, P., Donaher, J. L., Geng, Y., Parker, S. B., Gardner, H., Park, M. Y., Robker, R. L., Richards, J. S., McGinnis, L. K., Biggers, J. D., et al. (1996) · Nature · doi:10.1038/384470a0 · Cited by 697
Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway
Bai, C. B., Auerbach, W., Lee, J. S., Stephen, D., & Joyner, A. L. (2002) · Development · doi:10.1242/dev.129.20.4753 · Cited by 692
Wnt signalling required for expansion of neural crest and CNS progenitors
Ikeya, M., Lee, S. M. K., Johnson, J. E. B., McMahon, A. P., & Takada, S. (1997) · Nature · doi:10.1038/40146 · Cited by 684
Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2
Novitch, B. G., Chen, A. I., & Jessell, T. M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00407-x · Cited by 615
Smoothened Mutants Reveal Redundant Roles for Shh and Ihh Signaling Including Regulation of L/R Asymmetry by the Mouse Node
Zhang, X. M., Ramalho‐Santos, M., & McMahon, A. P. (2001) · Cell · doi:10.1016/s0092-8674(01)00385-3 · Cited by 614
Sonic hedgehog controls stem cell behavior in the postnatal and adult brain
Palma, V., Lim, D. A., Dahmane, N., Sánchez‐Gómez, P., Brionne, T. C., Herzberg, C. D., Gitton, Y., Carleton, A., Álvarez-Buylla, A., & Altaba, A. R. I. (2004) · Development · doi:10.1242/dev.01567 · Cited by 610
Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development
Mo, R., Freer, A. M., Zinyk, D. L., Crackower, M. A., Michaud, J. L., Heng, H. H., Chik, K. W., Shi, X., Tsui, L., Cheng, S. H., et al. (1997) · Development · doi:10.1242/dev.124.1.113 · Cited by 607
Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease
Lin, F., Hiesberger, T., Cordes, K. R., Sinclair, A. M., Goldstein, L. S. B., Somlo, S., & Igarashi, P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0836980100 · Cited by 602
Regulation of lifespan by sensory perception in Caenorhabditis elegans
Apfeld, J., & Kenyon, C. (1999) · Nature · doi:10.1038/45544 · Cited by 573
Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II
Marszalek, J. R., Ruiz‐Lozano, P., Roberts, E. A., Chien, K. R., & Goldstein, L. S. B. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5043 · Cited by 542
Cilia and Developmental Signaling
Eggenschwiler, J. T., & Anderson, K. V. (2007) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.23.090506.123249 · Cited by 540
Self-citation
Sonic hedgehog Signaling Regulates Gli2 Transcriptional Activity by Suppressing Its Processing and Degradation
Pan, Y., Bai, C. B., Joyner, A. L., & Wang, B. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.9.3365-3377.2006 · Cited by 533
NEUROGENIN1 and NEUROGENIN2 control two distinct waves of neurogenesis in developing dorsal root gangliaPreprint
Ma, Q., Schuurmans, C. J., Guillemot, F., & Anderson, D. J. (1999) · Genes & Development · doi:10.1101/gad.13.13.1717 · Cited by 509
Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors
Liu, A., Wang, B., & Niswander, L. A. (2005) · Development · doi:10.1242/dev.01894 · Cited by 494
Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system
Matise, M. P., Epstein, D. J., Park, H. L., Platt, K. A., & Joyner, A. L. (1998) · Development · doi:10.1242/dev.125.15.2759 · Cited by 489
Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors
Kenney, A. M., Cole, M. D., & Rowitch, D. H. (2002) · Development · doi:10.1242/dev.00182 · Cited by 481
Expression of Three Mouse Homologs of the Drosophila Segment Polarity Gene cubitus interruptus, Gli, Gli-2, and Gli-3, in Ectoderm- and Mesoderm-Derived Tissues Suggests Multiple Roles during Postimplantation Development
Hui, C., Slusarski, D. C., Platt, K. A., Holmgren, R. A., & Joyner, A. L. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1097 · Cited by 480
Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons.
Mizuguchi, R., Sugimori, M., Takebayashi, H., Kosako, H., Nagao, M., Yoshida, S., Nabeshima, Y., Shimamura, K., & Nakafuku, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00413-5 · Cited by 471
Sonic Hedgehog-induced Activation of the Gli1Promoter Is Mediated by GLI3
Dai, P., Akimaru, H., Tanaka, Y., Maekawa, T., Nakafuku, M., & Ishii, S. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.12.8143 · Cited by 466
Loss of the retrograde motor for IFT disrupts localization of Smo to cilia and prevents the expression of both activator and repressor functions of Gli
May, S., Ashique, A. M., Karlén, M., Wang, B., Shen, Y., Zarbalis, K., Reiter, J. F., Ericson, J., & Peterson, A. S. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.08.050 · Cited by 437
Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function.
Chiang, C., Litingtung, Y., Harris, M. P., Simandl, B. K., Li, Y., Beachy, P. A., & Fallon, J. F. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0346 · Cited by 427
Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3
Litingtung, Y., & Chiang, C. C. (2000) · Nature Neuroscience · doi:10.1038/79916 · Cited by 392
G-Protein Signaling Through Tubby Proteins
Santagata, S., Boggon, T. J., Baird, C. L., Gomez, C. A., Zhao, J., Shan, W., Myszka, D. G., & Shapiro, L. S. (2001) · Science · doi:10.1126/science.1061233 · Cited by 387
A candidate gene for the mouse mutation tubby
Noben‐Trauth, K., Naggert, J. K., North, M. A., & Nishina, P. M. (1996) · Nature · doi:10.1038/380534a0 · Cited by 356
THM1 negatively modulates mouse sonic hedgehog signal transduction and affects retrograde intraflagellar transport in cilia
Tran, P. V., Haycraft, C. J., Besschetnova, T. Y., Turbe-Doan, A., Stottmann, R. W., Herron, B. J., Chesebro, A. L., Qiu, H., Scherz, P. J., Shah, J. V., et al. (2008) · Nature Genetics · doi:10.1038/ng.105 · Cited by 322
Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway
Eggenschwiler, J. T., Espinoza, E., & Anderson, K. V. (2001) · Nature · doi:10.1038/35084089 · Cited by 321
Self-citation
The left-right axis in the mouse: from origin to morphology
Shiratori, H., & Hamada, H. (2006) · Development · doi:10.1242/dev.02384 · Cited by 307
β-Arrestin–Mediated Localization of Smoothened to the Primary Cilium
Kovacs, J. J., Whalen, E. J., Liu, R., Xiao, K., Kim, J., Chen, M., Wang, J., Chen, W., & Lefkowitz, R. J. (2008) · Science · doi:10.1126/science.1157983 · Cited by 289
The Whereabouts of a Morphogen: Direct Evidence for Short- and Graded Long-Range Activity of Hedgehog Signaling Peptides
Gritli-Linde, A., Lewis, P. M., McMahon, A. P., & Linde, A. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0336 · Cited by 284
The mechanisms of dorsoventral patterning in the vertebrate neural tube
Wilson, L., & Maden, M. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.02.027 · Cited by 276
Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites
Liem, K. F., Jessell, T. M., & Briscoe, J. (2000) · Development · doi:10.1242/dev.127.22.4855 · Cited by 275
Evidence for the direct involvement of βTrCP in Gli3 protein processing
Wang, B., & Li, Y. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509927103 · Cited by 273
Notochord-derived Shh concentrates in close association with the apically positioned basal body in neural target cells and forms a dynamic gradient during neural patterning
Chamberlain, C. E., Jeong, J., Guo, C., Allen, B. L., & McMahon, A. P. (2008) · Development · doi:10.1242/dev.013086 · Cited by 263
Sonic hedgehog in CNS development: one signal, multiple outputs
Martı́, E. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02062-3 · Cited by 260
Crossregulation between Neurogenin2 and pathways specifying neuronal identity in the spinal cord.
Scardigli, R., Schuurmans, C., Gradwohl, G., & Guillemot, F. (2001) · Neuron · doi:10.1016/s0896-6273(01)00358-0 · Cited by 253
Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6
Scardigli, R., Bäumer, N., Gruss, P., Guillemot, F., & Roux, I. L. (2003) · Development · doi:10.1242/dev.00539 · Cited by 239
Divergence of Hedgehog Signal Transduction Mechanism between Drosophila and Mammals
Varjosalo, M. T., Li, S., & Taipale, J. (2006) · Developmental Cell · doi:10.1016/j.devcel.2005.12.014 · Cited by 230
Mutual genetic antagonism involving GLI3 and dHAND prepatterns the vertebrate limb bud mesenchyme prior to SHH signalingPreprint
Welscher, P. T., Fernandez‐Teran, M., Ros, M. A., & Zeller, R. (2002) · Genes & Development · doi:10.1101/gad.219202 · Cited by 226
Olig2 and Ngn2 function in opposition to modulate gene expression in motor neuron progenitor cells.Preprint
Lee, S.-K., Lee, B., Ruiz, E. C., & Pfaff, S. (2005) · Genes & Development · doi:10.1101/gad.1257105 · Cited by 226
elipsa is an early determinant of ciliogenesis that links the IFT particle to membrane-associated small GTPase Rab8
Omori, Y., Zhao, C., Saras, A., Mukhopadhyay, S., Kim, W., Furukawa, T., Sengupta, P., Veraksa, A. N., & Malicki, J. J. (2008) · Nature Cell Biology · doi:10.1038/ncb1706 · Cited by 225
Genome-wide transcriptional analysis of flagellar regeneration in Chlamydomonas reinhardtii identifies orthologs of ciliary disease genes
Štolc, V., Samanta, M. P., Tongprasit, W., & Marshall, W. F. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408358102 · Cited by 224
Growth and pattern of the mammalian neural tube are governed by partially overlapping feedback activities of the hedgehog antagonists patched 1 and Hhip1
Jeong, J., & McMahon, A. P. (2004) · Development · doi:10.1242/dev.01566 · Cited by 223
Implication of Tubby Proteins as Transcription Factors by Structure-Based Functional Analysis
Boggon, T. J., Shan, W., Santagata, S., Myers, S. C., & Shapiro, L. S. (1999) · Science · doi:10.1126/science.286.5447.2119 · Cited by 222
Gas1 extends the range of hedgehog action by facilitating its signaling
Martinelli, D. C., & Fan, C. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.03.166 · Cited by 217
Gas1extends the range of Hedgehog action by facilitating its signalingPreprint
Martinelli, D. C., & Fan, C. (2007) · Genes & Development · doi:10.1101/gad.1546307 · Cited by 215
Morphogens and the Control of Cell Proliferation and Patterning in the Spinal Cord
Ulloa, F., & Briscoe, J. (2007) · Cell Cycle · doi:10.4161/cc.6.21.4822 · Cited by 207
Recessive mutations in the gene encoding the tubby-like protein TULP1 in patients with Retinitis pigmentosa
Hagstrom, S. A., North, M. A., Nishina, P. M., Berson, E. L., & Dryja, T. P. (1998) · Nature Genetics · doi:10.1038/ng0298-174 · Cited by 204
Suppressor of Fused opposes Hedgehog signal transduction by impeding nuclear accumulation of the activator form of Cubitus interruptus
Méthot, N., & Basler, K. (2000) · Development · doi:10.1242/dev.127.18.4001 · Cited by 203
Stability and association of Smoothened, Costal2 and Fused with Cubitus interruptus are regulated by Hedgehog
Ruel, L., Rodriguez, R., Gallet, A., Staccini-Lavenant, L., & Thérond, P. P. (2003) · Nature Cell Biology · doi:10.1038/ncb1052 · Cited by 199
Polygenic control of Caenorhabditis elegans fat storage
Mak, H. Y., Nelson, L. S., Basson, M., Johnson, C. D., & Ruvkun, G. (2006) · Nature Genetics · doi:10.1038/ng1739 · Cited by 194
Analysis of xbx genes in C. elegans
Efimenko, E., Bubb, K. L., Mak, H. Y., Holzman, T., Leroux, M. R., Ruvkun, G., Thomas, J. H., & Swoboda, P. (2005) · Development · doi:10.1242/dev.01775 · Cited by 191
The Sonic hedgehog pathway independently controls the patterning,proliferation and survival of neuroepithelial cells by regulating Gli activity
Cayuso, J., Ulloa, F., Cox, B., Briscoe, J., & Martı́, E. (2006) · Development · doi:10.1242/dev.02228 · Cited by 186
Application of Active and Kinase-Deficient Kinome Collection for Identification of Kinases Regulating Hedgehog Signaling
Varjosalo, M. T., Björklund, M., Cheng, F., Syvänen, H., Kivioja, T., Kilpinen, S. K., Sun, Z., Kallioniemi, O., Stunnenberg, H. G., He, W.-W., et al. (2008) · Cell · doi:10.1016/j.cell.2008.02.047 · Cited by 183
ConditionalKif3aablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis
Koyama, E., Young, B. B., Nagayama, M., Shibukawa, Y., Enomoto‐Iwamoto, M., Iwamoto, M., MAEDA, Y. Y., Lanske, B., Song, B., Serra, R. A., et al. (2007) · Development · doi:10.1242/dev.001586 · Cited by 182
In vivo evidence that Patched and Smoothened constitute distinct binding and transducing components of a Hedgehog receptor complex
Chen, Y., & Struhl, G. (1998) · Development · doi:10.1242/dev.125.24.4943 · Cited by 178
Homeotic transformations in the mouse induced by overexpression of a human Hox3.3 transgene
Jegalian, B. G., & Robertis, E. M. D. (1992) · Cell · doi:10.1016/0092-8674(92)90387-r · Cited by 160
MIM/BEG4, a Sonic hedgehog-responsive gene that potentiates Gli-dependent transcriptionPreprint
Callahan, C. A., Ofstad, T. A., Horng, L. M.-S., Wang, J. K., Zhen, H. H., Coulombe, P. A., & Oro, A. E. (2004) · Genes & Development · doi:10.1101/gad.1221804 · Cited by 155
Signaling through BMP type 1 receptors is required for development of interneuron cell types in the dorsal spinal cord
Lee, L. W., Ahn, K. J., Richardson, R. D., Mishina, Y. M., Lyons, K. M., & Crenshaw, E. B. (2004) · Development · doi:10.1242/dev.01379 · Cited by 155
Hedgehog signaling and the retina: insights into the mechanisms controlling the proliferative properties of neural precursorsPreprint
Locker, M., Agathocleous, M., Amato, M. A., Parain, K., Harris, W. A., & Perron, M. (2006) · Genes & Development · doi:10.1101/gad.391106 · Cited by 155
Mouse Rab23 regulates Hedgehog signaling from Smoothened to Gli proteins
Eggenschwiler, J. T., Bulgakov, O. V., Qin, J., Li, T., & Anderson, K. V. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.09.022 · Cited by 147
Self-citation
Kinesin-2 is a motor for late endosomes and lysosomes
Brown, C. L., Maier, K. C., Stauber, T., Ginkel, L. M., Wordeman, L., Vernos, I., & Schroer, T. A. (2005) · Traffic · doi:10.1111/j.1600-0854.2005.00347.x · Cited by 140
Pathways and consequences: Hedgehog signaling in human disease
Mullor, J. L., Sánchez‐Gómez, P., & Altaba, A. R. I. (2002) · Trends in Cell Biology · doi:10.1016/s0962-8924(02)02405-4 · Cited by 137
Hoxd-12 differentially affects preaxial and postaxial chondrogenic branches in the limb and regulates Sonic hedgehog in a positive feedback loop
Knežević, V., Santo, R. J. D., Schughart, K., Huffstadt, U., Chiang, C. C., Mahon, K. A., & Mackem, S. (1997) · Development · doi:10.1242/dev.124.22.4523 · Cited by 131
Loss of the Serine/Threonine Kinase Fused Results in Postnatal Growth Defects and Lethality Due to Progressive Hydrocephalus
Merchant, M. A., Evangelista, M., Luoh, S.-M., Frantz, G. D., Chalasani, S., Carano, R. A. D., Hoy, M. V., Ramirez, J. C., Ogasawara, A. K., McFarland, L. M., et al. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.16.7054-7068.2005 · Cited by 131
C. elegans tubby regulates life span and fat storage by two independent mechanisms
Mukhopadhyay, A., Deplancke, B., Walhout, A. J. M., & Tissenbaum, H. A. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.06.004 · Cited by 125
Shifting paradigms in Hedgehog signaling
Wang, Y., McMahon, A. P., & Allen, B. L. (2007) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2007.02.005 · Cited by 124
The chicken talpid 3 gene encodesa novel protein essentialfor Hedgehog signalingPreprint
Davey, M. G., Paton, I. R., Yin, Y., Schmidt, M., Bangs, F. K., Morrice, D. R., Smith, T., BUXTON, P., Stamataki, D., Tanaka, M., et al. (2006) · Genes & Development · doi:10.1101/gad.369106 · Cited by 124
Microtubule-Dependent Movement of Late Endocytic Vesicles In Vitro: Requirements for Dynein and Kinesin
Bananis, E., Nath, S., Gordon, K. M., Satir, P., Stockert, R. J., Murray, J. W., & Wolkoff, A. W. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-04-0278 · Cited by 123
The on/off of Pax6 controls the tempo of neuronal differentiation in the developing spinal cord
Bel-Vialar, S., Médevielle, F., & Pituello, F. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.02.012 · Cited by 123
Differential requirement for Gli2 and Gli3 in ventral neural cell fate specification
Motoyama, J., Milenković, L., Iwama, M., Shikata, Y., Scott, M. P., & Hui, C. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00159-3 · Cited by 122
Mouse patched1 controls body size determination and limb patterning
Milenković, L., Goodrich, L. V., Higgins, K. M., & Scott, M. P. (1999) · Development · doi:10.1242/dev.126.20.4431 · Cited by 121
Distinct regulators ofShhtranscription in the floor plate and notochord indicate separate origins for these tissues in the mouse node
Jeong, Y., & Epstein, D. J. (2003) · Development · doi:10.1242/dev.00590 · Cited by 120
Identification of novel regulatory factor X (RFX) target genes by comparative genomics in Drosophila species
Laurençon, A., Dubruille, R., Efimenko, E., Grenier, G., Bissett, R., Cortier, E., Rolland, V., Swoboda, P., & Durand, B. (2007) · Genome biology · doi:10.1186/gb-2007-8-9-r195 · Cited by 117
A critical role for sonic hedgehog signaling in the early expansion of the developing brain
Britto, J. M., Tannahill, D., & Keynes, R. J. (2002) · Nature Neuroscience · doi:10.1038/nn797 · Cited by 116
ß-Arrestin 2 Regulates Zebrafish Development Through the Hedgehog Signaling Pathway
Wilbanks, A. M., Fralish, G. B., Kirby, M. L., Barak, L. S., Li, Y., & Caron, M. G. (2004) · Science · doi:10.1126/science.1104193 · Cited by 112
A role for the Tubby-like protein 1 in rhodopsin transport.
Hagstrom, S. A., Adamian, M., Scimeca, M. S., Pawlyk, B. S., Yue, G., & Li, T. (2001) · PubMed · Cited by 106
Protein Kinase A Deficiency Causes Axially Localized Neural Tube Defects in Mice
Huang, Y., Roelink, H., & McKnight, G. S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111412200 · Cited by 106
FKBP8 is a negative regulator of mouse sonic hedgehog signaling in neural tissues
Bulgakov, O. V., Eggenschwiler, J. T., Hong, D.-H., Anderson, K. V., & Li, T. (2004) · Development · doi:10.1242/dev.01122 · Cited by 106
Self-citation
The hedgehog-PKA pathway regulates two distinct steps of the differentiation of retinal ganglion cells: the cell-cycle exit of retinoblasts and their neuronal maturation
Masai, I., Yamaguchi, M., Tonou‐Fujimori, N., Komori, A., & Okamoto, H. (2005) · Development · doi:10.1242/dev.01714 · Cited by 105
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Mykytyn, K., & Sheffield, V. C. (2004) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2004.01.003 · Cited by 102
Decoding the Hedgehog signal in animal development
Jia, J., & Jiang, J. (2006) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-5519-z · Cited by 99
The tubby-like proteins, a family with roles in neuronal development and function
Ikeda, A., Nishina, P. M., & Naggert, J. Κ. (2002) · Journal of Cell Science · doi:10.1242/jcs.115.1.9 · Cited by 97
Specific regulation of cyclins D1 and D2 by FGF and Shh signaling coordinates cell cycle progression, patterning, and differentiation during early steps of spinal cord development
Lobjois, V., Bénazéraf, B., Bertrand, N., Médevielle, F., & Pituello, F. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.05.031 · Cited by 97
Mechanistic insight into how Shh patterns the vertebrate limb
McGlinn, E., & Tabin, C. J. (2006) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2006.06.013 · Cited by 94
Shh directs cell‐cycle exit by activating p57Kip2 in the zebrafish retina
Shkumatava, A., & Neumann, C. J. (2005) · EMBO Reports · doi:10.1038/sj.embor.7400416 · Cited by 85
Neural tube defects and neuroepithelial cell death in Tulp3 knockout mice
Ikeda, A. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.12.1325 · Cited by 77
A cell-autonomous requirement for Cip/Kip cyclin-kinase inhibitors in regulating neuronal cell cycle exit but not differentiation in the developing spinal cord
Gui, H., Li, S., & Matise, M. P. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.10.035 · Cited by 74
SoxB1 transcription factors and Notch signaling use distinct mechanisms to regulate proneural gene function and neural progenitor differentiation
Holmberg, J., Hansson, E. M., Malewicz, M., Sandberg, M., Perlmann, T., Lendahl, U., & Muhr, J. (2008) · Development · doi:10.1242/dev.020180 · Cited by 73
FKBP8 cell-autonomously controls neural tube patterning through a Gli2- and Kif3a-dependent mechanism
Cho, A., Ko, H. W., & Eggenschwiler, J. T. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.05.558 · Cited by 71
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He, W., Ikeda, S., Bronson, R. T., Yan, G., Nishina, P. M., North, M. A., & Naggert, J. Κ. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00164-9 · Cited by 47
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Oro, A. E. (2007) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2007.10.008 · Cited by 46
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Neumann, C. J. (2005) · Cell Cycle · doi:10.4161/cc.4.9.1999 · Cited by 35
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Authors: Norman, R. X., Ko, H. W., Huang, V., Eun, C. M., Abler, L. L., Zhang, Z., Sun, X., & Eggenschwiler, J. T.
Affiliations: Princeton University (US)
University of Wisconsin–Madison (US)
Corresponding author: Eggenschwiler, Jonathan T.
ORCID: Ko, Hyuk W.
Huang, Viola
Abler, Lisa L.
Zhang, Zhen
Sun, Xin
Eggenschwiler, Jonathan T.
Venue: Human Molecular Genetics
Publisher: Oxford University Press (OUP)
Published: 2009-03-12
Volume: 18
Issue: 10
Pages: 1740-1754
ISSN: 0964-6906 (ISSN-L)
1460-2083
DOI: 10.1093/hmg/ddp113
PMC: PMC2671991
OpenAlex: W2170193319
Cited by: 103
References: 125
Citations by year: 2026: 3 · 2025: 6 · 2024: 9 · 2023: 5 · 2022: 6 · 2021: 7 · 2020: 10 · 2019: 6 · 2018: 5 · 2017: 5 · 2016: 7 · 2015: 5 · 2014: 4 · 2013: 4 · 2012: 9
FWCI: 2.82
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Human Molecular Genetics (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: New Jersey Commission on Spinal Cord Research
National Institutes of Health (IA 52242)
Directorate for Biological Sciences
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD045522, HD045522, HD050761, R01HD050761)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Hedgehog Signaling Pathway Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: TULP3, Sonic hedgehog signaling, Hedgehog signaling, neural tube patterning, GLI2, KIF3A, kinesin-2, intraflagellar transport, ciliogenesis, primary cilia, limb patterning, craniofacial defects, Smoothened, mouse embryo
MeSH terms: Animals, Embryo, Mammalian, Female, Humans, Male, Mice, Inbred C3H, Mice, Transgenic, Mutation, Proteins, Spinal Cord, Signal Transduction, Down-Regulation, Gene Expression Regulation, Developmental, Body Patterning, Intercellular Signaling Peptides and Proteins, Embryonic Development, Intracellular Signaling Peptides and Proteins, Mice, Hedgehog Proteins, Neural Tube

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Tubby-like protein 3 (TULP3) regulates patterning in the mouse embryo through inhibition of Hedgehog signaling

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