Functions of heparan sulfate proteoglycans in cell signaling during development
Abstract
Heparan sulfate proteoglycans (HSPGs) are cell-surface and extracellular matrix macromolecules that are composed of a core protein decorated with covalently linked glycosaminoglycan (GAG) chains. In vitro studies have demonstrated the roles of these molecules in many cellular functions, and recent in vivo studies have begun to clarify their essential functions in development. In particular, HSPGs play crucial roles in regulating key developmental signaling pathways, such as the Wnt, Hedgehog, transforming growth factor-β, and fibroblast growth factor pathways. This review highlights recent findings regarding the functions of HSPGs in these signaling pathways during development.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
In the extra-cellular matrix, the Wnt proteins may be bound to and stabilized by heparan sulfate proteoglycans including Dally and glypican 3 which further limits their diffusion and modulate their signaling abilities.
“In the extra-cellular matrix, the Wnt proteins may be bound to and stabilized by heparan sulfate proteoglycans including Dally and glypican 3 which further limits their diffusion and modulate their signaling abilities.15”
From Wnt signal transduction pathways (2008) · cites this paper as [15]
Cites
Lipid rafts and signal transduction
Simons, K., & Toomre, D. K. (2000) · Nature Reviews Molecular Cell Biology · doi:10.1038/35036052 · Cited by 6,252 · see citing works
Hedgehog signaling in animal development: paradigms and principlesPreprint
Ingham, P. W., & McMahon, A. P. (2001) · Genes & Development · doi:10.1101/gad.938601 · Cited by 2,987 · see citing works
Functions of Cell Surface Heparan Sulfate Proteoglycans
Bernfield, M. R., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J. M., & Zako, M. (1999) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.68.1.729 · Cited by 2,689 · see citing works
MECHANISMS OF WNT SIGNALING IN DEVELOPMENT
Wodarz, A., & Nusse, R. (1998) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.14.1.59 · Cited by 2,017 · see citing works
Ornitz, D. M., & Itoh, N. (2001) · Genome biology · doi:10.1186/gb-2001-2-3-reviews3005 · Cited by 1,985 · see citing works
Order Out of Chaos: Assembly of Ligand Binding Sites in Heparan Sulfate
Esko, J. D., & Selleck, S. B. (2002) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.71.110601.135458 · Cited by 1,495 · see citing works
Veeman, M. T., Axelrod, J. D., & Moon, R. T. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00266-1 · Cited by 1,359 · see citing works
Schlessinger, J., Plotnikov, A. N., Ibrahimi, O. A., Eliseenkova, A. V., Yeh, B. K., Yayon, A., Linhardt, R. J., & Mohammadi, M. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00073-3 · Cited by 1,199 · see citing works
Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin
Pellegrini, L., Burke, D. F., von Delft, F., Mulloy, B., & Blundell, T. L. (2000) · Nature · doi:10.1038/35039551 · Cited by 704 · see citing works
Gradient Formation of the TGF-β Homolog Dpp
Entchev, E. V., Schwabedissen, A., & González‐Gaitán, M. (2000) · Cell · doi:10.1016/s0092-8674(00)00200-2 · Cited by 608 · see citing works
Ruppert, R., Hoffmann, E., & Sebald, W. (1996) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1996.0295n.x · Cited by 562 · see citing works
Identification of Hedgehog Pathway Components by RNAi in Drosophila Cultured Cells
Lum, L., Yao, S., Mozer, B. A., Rovescalli, A. C., von Kessler, D. P., Nirenberg, M. W., & Beachy, P. A. (2003) · Science · doi:10.1126/science.1081403 · Cited by 532 · see citing works
Bellaı̈che, Y., The, I., & Perrimon, N. (1998) · Nature · doi:10.1038/27932 · Cited by 502 · see citing works
A freely diffusible form of Sonic hedgehog mediates long-range signalling
Zeng, X., Goetz, J. A., Suber, L. M., Scott, W. J., Schreiner, C. M., & Robbins, D. J. (2001) · Nature · doi:10.1038/35079648 · Cited by 484 · see citing works
Dally cooperates with Drosophila Frizzled 2 to transduce Wingless signalling
Lin, X., & Perrimon, N. (1999) · Nature · doi:10.1038/22343 · Cited by 475 · see citing works
Self-citationRegulation of Wnt Signaling and Embryo Patterning by an Extracellular Sulfatase
Dhoot, G. K., Gustafsson, M. K., Ai, X., Sun, W., Standiford, D. M., & Emerson, C. P. (2001) · Science · doi:10.1126/science.293.5535.1663 · Cited by 473 · see citing works
Schlessinger, J., Lax, I., & Lemmon, M. A. (1995) · Cell · doi:10.1016/0092-8674(95)90112-4 · Cited by 465 · see citing works
Wingless gradient formation in the Drosophila wing
Strigini, M., & Cohen, S. M. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00378-x · Cited by 454 · see citing works
Topczewski, J., Sepich, D. S., Myers, D. C., Walker, C., Amores, A., Lele, Z., Hammerschmidt, M., Postlethwait, J. H., & Solnica‐Krezel, L. (2001) · Developmental Cell · doi:10.1016/s1534-5807(01)00005-3 · Cited by 454 · see citing works
Bullock, S. L., Fletcher, J. M., Beddington, R. S. P., & Wilson, V. A. (1998) · Genes & Development · doi:10.1101/gad.12.12.1894 · Cited by 453 · see citing works
Dpp Gradient Formation in the Drosophila Wing Imaginal Disc
Teleman, A. A., & Cohen, S. M. (2000) · Cell · doi:10.1016/s0092-8674(00)00199-9 · Cited by 452 · see citing works
Ai, X., Do, A.-T., Lozynska, O., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200212083 · Cited by 449 · see citing works
Morphogens, their identification and regulation
Tabata, T., & Takei, Y. (2004) · Development · doi:10.1242/dev.01043 · Cited by 447 · see citing works
Morimoto‐Tomita, M., Uchimura, K., Werb, Z., Hemmerich, S., & Rosen, S. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205131200 · Cited by 430 · see citing works
Greco, V., Hannus, M., & Eaton, S. (2001) · Cell · doi:10.1016/s0092-8674(01)00484-6 · Cited by 422 · see citing works
Hedgehog Creates a Gradient of DPP Activity in Drosophila Wing Imaginal Discs
Tanimoto, H., Itoh, S., ten Dijke, P., & Tabata, T. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80403-7 · Cited by 416 · see citing works
Chen, M.-H., Li, Y.-J., Kawakami, T., Xu, S.-M., & Chuang, P.-T. (2004) · Genes & Development · doi:10.1101/gad.1185804 · Cited by 407 · see citing works
Do Morphogen Gradients Arise by Diffusion?
Lander, A. D., Nie, Q. H., & Wan, F. Y. M. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00179-x · Cited by 402 · see citing works
The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila
Tsuda, M., Kamimura, K., Nakato, H., Archer, M., Staatz, W. D., Fox, B., Humphrey, M., Olson, S. K., Futch, T. A., Kaluza, V., et al. (1999) · Nature · doi:10.1038/22336 · Cited by 386 · see citing works
The, I., Bellaı̈che, Y., & Perrimon, N. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80214-2 · Cited by 372 · see citing works
Baeg, G., Lin, X., Khare, N. A., Baumgartner, S., & Perrimon, N. (2001) · Development · doi:10.1242/dev.128.1.87 · Cited by 371 · see citing works
Self-citationLin, X., Buff, E. M., Perrimon, N., & Michelson, A. M. (1999) · Development · doi:10.1242/dev.126.17.3715 · Cited by 368 · see citing works
Self-citationCrystal structure of human bone morphogenetic protein-2 at 2.7 Å resolution 1 1Edited by R. Huber
Scheufler, C., Sebald, W., & Hülsmeyer, M. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1999.2590 · Cited by 343 · see citing works
Nusse, R. (2003) · Development · doi:10.1242/dev.00821 · Cited by 337 · see citing works
Crystal structure of the BMP-2–BRIA ectodomain complex
Kirsch, T., Sebald, W., & Dreyer, M. (2000) · Nature Structural Biology · doi:10.1038/75903 · Cited by 323 · see citing works
TGF-β Family Signal Transduction in Drosophila Development: From Mad to Smads
Raftery, L. A., & Sutherland, D. J. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9282 · Cited by 322 · see citing works
Heparan sulfate proteoglycan as a plasma membrane carrier
Belting, M. (2003) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(03)00031-8 · Cited by 312 · see citing works
Reichsman, F., Smith, L., & Cumberledge, S. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.135.3.819 · Cited by 305 · see citing works
Belenkaya, T. Y., Han, C., Yan, D., Opoka, R. J., Khodoun, M. V., Liu, H., & Lin, X. (2004) · Cell · doi:10.1016/j.cell.2004.09.031 · Cited by 296 · see citing works
Self-citationHäcker, U., Lin, X., & Perrimon, N. (1997) · Development · doi:10.1242/dev.124.18.3565 · Cited by 292 · see citing works
Self-citationToyoda, H., Kinoshita‐Toyoda, A., & Selleck, S. B. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.4.2269 · Cited by 291 · see citing works
Takei, Y., Ozawa, Y., Sato, M., Watanabe, A., & Tabata, T. (2003) · Development · doi:10.1242/dev.00913 · Cited by 279 · see citing works
Role of heparan sulfate in fibroblast growth factor signalling: a structural view
Pellegrini, L. (2001) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(00)00258-x · Cited by 274 · see citing works
Nakato, H., Futch, T. A., & Selleck, S. B. (1995) · Development · doi:10.1242/dev.121.11.3687 · Cited by 264 · see citing works
Genetic evidence that heparin-like glycosaminoglycans are involved in wingless signaling
Binari, R. C., Staveley, B. E., Johnson, W. A., Godavarti, R., Sasisekharan, R., & Manoukian, A. S. (1997) · Development · doi:10.1242/dev.124.13.2623 · Cited by 256 · see citing works
Loss of HSulf-1 Up-regulates Heparin-binding Growth Factor Signaling in Cancer
Lai, J., CHIEN, J. R., Staub, J. K., Avula, R., Greene, E. L., Matthews, T. A., Smith, D. I., Kaufmann, S. H., Roberts, L. R., & Shridhar, V. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302203200 · Cited by 252 · see citing works
HSPG Modification by the Secreted Enzyme Notum Shapes the Wingless Morphogen Gradient
Giráldez, A. J., Copley, R. R., & Cohen, S. M. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00180-6 · Cited by 247 · see citing works
dally, a Drosophila glypican, controls cellular responses to the TGF-β-related morphogen, Dpp
Jackson, S. M., Nakato, H., Sugiura, M., et al. (1997) · Development · doi:10.1242/dev.124.20.4113 · Cited by 240 · see citing works
Drosophila glypicans control the cell-to-cell movement of Hedgehog by a dynamin-independent process
Han, C., Belenkaya, T. Y., Wang, B., & Lin, X. (2004) · Development · doi:10.1242/dev.00958 · Cited by 238 · see citing works
Self-citationHan, C., Belenkaya, T. Y., Khodoun, M. V., et al. (2004) · Development · doi:10.1242/dev.01051 · Cited by 236 · see citing works
Li, J., Gong, F., Hagner-McWhirter, Å., Forsberg, E., Åbrink, M., Kisilevsky, R., Zhang, X., & Lindahl, U. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.c300219200 · Cited by 234 · see citing works
Bornemann, D. J., Duncan, J. E., Staatz, W. D., et al. (2004) · Development · doi:10.1242/dev.01061 · Cited by 229 · see citing works
Dally regulates Dpp morphogen gradient formation in the Drosophila wing
Fujise, M., Takeo, S., Kamimura, K., Matsuo, T., Aigaki, T., Izumi, S., & Nakato, H. (2003) · Development · doi:10.1242/dev.00379 · Cited by 223 · see citing works
Opposing Activities of Dally-like Glypican at High and Low Levels of Wingless Morphogen Activity
Kreuger, J., Pérez, L., Giráldez, A. J., & Cohen, S. M. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.08.005 · Cited by 211 · see citing works
Influence of core protein sequence on glycosaminoglycan assembly
Esko, J. D., & Zhang, L. (1996) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(96)80034-0 · Cited by 208 · see citing works
Heparan Sulfate Proteoglycan Syndecan Promotes Axonal and Myotube Guidance by Slit/Robo Signaling
Steigemann, P., Molitor, A., Fellert, S., Jäckle, H., & Vorbrüggen, G. (2004) · Current Biology · doi:10.1016/j.cub.2004.01.006 · Cited by 199 · see citing works
Johnson, K. G., Ghose, A., Epstein, E., Lincecum, J. M., O’Connor, M. B., & Vactor, D. V. (2004) · Current Biology · doi:10.1016/j.cub.2004.02.005 · Cited by 198 · see citing works
Wang, S., Ai, X., Freeman, S. D., Pownall, M. E., Lu, Q., Kessler, D. S., & Emerson, C. P. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401028101 · Cited by 196 · see citing works
Hereditary multiple exostoses and heparan sulfate polymerization
Zak, B. M., Crawford, B. E., & Esko, J. D. (2002) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(02)00402-6 · Cited by 192 · see citing works
Defects in glucuronate biosynthesis disrupt Wingless signaling in Drosophila
Haerry, T. E., Heslip, T. R., Marsh, J. L., & O’Connor, M. B. (1997) · Development · doi:10.1242/dev.124.16.3055 · Cited by 190 · see citing works
Gallet, A., Rodriguez, R., Ruel, L., & Thérond, P. P. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00031-5 · Cited by 189 · see citing works
Cat, B. D., Muyldermans, S.-Y., Coomans, C., Degeest, G., Vanderschueren, B., Creemers, J. W. M., Biemar, F., Peers, B., & David, G. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302152 · Cited by 186 · see citing works
Ohkawara, B., Yamamoto, T. S., Tada, M., & Ueno, N. (2003) · Development · doi:10.1242/dev.00435 · Cited by 182 · see citing works
glypican-3 Controls Cellular Responses to Bmp4 in Limb Patterning and Skeletal Development
Paine‐Saunders, S., Viviano, B. L., Zupicich, J., Skarnes, W. C., & Saunders, S. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9831 · Cited by 176 · see citing works
The Molecular Phenotype of Heparan Sulfate in theHs2st−/− Mutant Mouse
Merry, C. L. R., Bullock, S. L., Swan, D., Backen, A. C., Lyon, M., Beddington, R. S. P., Wilson, V. A., & Gallagher, J. T. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100379200 · Cited by 175 · see citing works
Teleman, A. A., Strigini, M., & Cohen, S. M. (2001) · Cell · doi:10.1016/s0092-8674(01)00377-4 · Cited by 174 · see citing works
Drosophila Perlecan modulates FGF and Hedgehog signals to activate neural stem cell division
Park, Y., Rangel, C., Reynolds, M., Caldwell, M. C., Johns, M., Nayak, M. S., Welsh, C. J., McDermott, S., & Datta, S. (2003) · Developmental Biology · doi:10.1016/s0012-1606(02)00019-2 · Cited by 172 · see citing works
Spatial Regulation of Wingless Morphogen Distribution and Signaling by Dally-like Protein
Kirkpatrick, C. A., Dimitroff, B. D., Rawson, J. M., & Selleck, S. B. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.08.004 · Cited by 161 · see citing works
Toyoda, H., Kinoshita‐Toyoda, A., Fox, B., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m003540200 · Cited by 156 · see citing works
Heparan sulfate fine structure and specificity of proteoglycan functions
Nakato, H., & Kimata, K. (2002) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(02)00398-7 · Cited by 150 · see citing works
Molecular Cloning and Identification of 3′-Phosphoadenosine 5′-Phosphosulfate Transporter
Kamiyama, S., Suda, T., Ueda, R., Suzuki, M., Okubo, R., Kikuchi, N., Chiba, Y., Goto, S., Toyoda, H., Saigo, K., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302439200 · Cited by 150 · see citing works
Drosophila syndecan: conservation of a cell-surface heparan sulfate proteoglycan.
Spring, J., Paine‐Saunders, S., Hynes, R. O., & Bernfield, M. R. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.8.3334 · Cited by 148 · see citing works
Heparan sulfate proteoglycan modulation of developmental signaling in Drosophila
Nybakken, K. E., & Perrimon, N. (2002) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(02)00395-1 · Cited by 146 · see citing works
The glypican Dally-like is required for Hedgehog signalling in the embryonic epidermis ofDrosophila
Desbordes, S. C., & Sanson, B. (2003) · Development · doi:10.1242/dev.00874 · Cited by 146 · see citing works
The role of glypicans in mammalian development
Song, H. H., & Filmus, J. (2002) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(02)00390-2 · Cited by 145 · see citing works
Essential Role of Glycosaminoglycans in Fgf Signaling during Mouse Gastrulation
García‐García, M. J., & Anderson, K. V. (2003) · Cell · doi:10.1016/s0092-8674(03)00715-3 · Cited by 137 · see citing works
Wingful, an extracellular feedback inhibitor of WinglessPreprint
Gerlitz, O., & Basler, K. (2002) · Genes & Development · doi:10.1101/gad.991802 · Cited by 130 · see citing works
Perlecan participates in proliferation activation of quiescent Drosophila neuroblasts
Voigt, A., Pflanz, R., Schäfer, U., et al. (2002) · Developmental Dynamics · doi:10.1002/dvdy.10120 · Cited by 128 · see citing works
UDP–sugar transporter implicated in glycosylation and processing of Notch
Goto, S., Taniguchi, M., Muraoka, M., Toyoda, H., Sado, Y., Kawakita, M., & Hayashi, S. (2001) · Nature Cell Biology · doi:10.1038/ncb0901-816 · Cited by 123 · see citing works
Drosophila Heparan Sulfate 6-O-Sulfotransferase (dHS6ST) Gene
Kamimura, K., Fujise, M., Villa, F. A., Izumi, S., Habuchi, H., Kimata, K., & Nakato, H. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m011354200 · Cited by 121 · see citing works
Roles of FGF receptors in mammalian development and congenital diseases
Coumoul, X., & Deng, C. (2003) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.10025 · Cited by 121 · see citing works
Selva, E. M., Hong, K., Baeg, G., Beverley, S. M., Turco, S. J., Perrimon, N., & Häcker, U. (2001) · Nature Cell Biology · doi:10.1038/ncb0901-809 · Cited by 114 · see citing works
Creation of a Sog Morphogen Gradient in the Drosophila Embryo
Srinivasan, S., Rashka, K. E., & Bier, E. (2002) · Developmental Cell · doi:10.1016/s1534-5807(01)00097-1 · Cited by 110 · see citing works
Producing Cells Retain and Recycle Wingless in Drosophila Embryos
Pfeiffer, S., Ricardo, S. A. V., Manneville, J., Alexandre, C., & Vincent, J. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00867-9 · Cited by 107 · see citing works
Cholesterol modification of Hedgehog family proteins
Jeong, J., & McMahon, A. P. (2002) · Journal of Clinical Investigation · doi:10.1172/jci16506 · Cited by 103 · see citing works
Ohto, T., Uchida, H., Yamazaki, H., Keino‐Masu, K., Matsui, A., & Masu, M. (2002) · Genes to Cells · doi:10.1046/j.1356-9597.2001.00502.x · Cited by 94 · see citing works
Cholesterol modification of Hedgehog family proteins
Jeong, J., & McMahon, A. P. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0216506 · Cited by 93 · see citing works
Mechanisms Underlying Preferential Assembly of Heparan Sulfate on Glypican-1
Chen, R. L., & Lander, A. D. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008283200 · Cited by 90 · see citing works
Glypican 4 modulates FGF signalling and regulates dorsoventral forebrain patterning inXenopusembryos
Galli, A., Roure, A., Zeller, R., et al. (2003) · Development · doi:10.1242/dev.00706 · Cited by 85 · see citing works
Datta, S. (1995) · Development · doi:10.1242/dev.121.4.1173 · Cited by 85 · see citing works
Morphogen Transport along Epithelia, an Integrated Trafficking Problem
Vincent, J., & Dubois, L. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00323-4 · Cited by 82 · see citing works
Dally-like protein, a new Drosophila glypican with expression overlapping with wingless
Khare, N., & Baumgartner, S. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00502-5 · Cited by 78 · see citing works
Lüders, F., Segawa, H., Stein, D., et al. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg345 · Cited by 77 · see citing works
Fujise, M., Izumi, S., Selleck, S. B., et al. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0290 · Cited by 71 · see citing works
Genetic dissection of proteoglycan function in Drosophila and C. elegans
Selleck, S. B. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0242 · Cited by 70 · see citing works
Developmental roles of heparan sulfate proteoglycans in Drosophila
Lin, X., & Perrimon, N. (2002) · Glycoconjugate Journal · doi:10.1023/a:1025329323438 · Cited by 70 · see citing works
Self-citationPrincivalle, M., & de Agostini, A. (2002) · The International Journal of Developmental Biology · doi:10.1387/ijdb.12068947 · Cited by 57 · see citing works
Groppe, J. C., Rumpel, K., Economides, A. N., Stahl, N., Sebald, W., & Affolter, M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.44.29052 · Cited by 50 · see citing works
Kim, B.-T., Kitagawa, H., Tamura, J., et al. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111630200 · Cited by 39 · see citing works
Wingless, Hedgehog and Heparan Sulfate Proteoglycans
Perrimon, N., & Häcker, U. (2004) · Development · doi:10.1242/dev.01225 · Cited by 36 · see citing works
Baeg, G., Lin, X., & Perrimon, N. (2001) · Biochemical Society Transactions · doi:10.1042/bst029a010c · Cited by 35 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
The Fibroblast Growth Factor signaling pathway
Ornitz, D. M., & Itoh, N. (2015) · WIREs Developmental Biology · doi:10.1002/wdev.176 · Cited by 2,050 · see citing works
Wnt signal transduction pathways
Komiya, Y., & Habas, R. (2008) · Organogenesis · doi:10.4161/org.4.2.5851 · Cited by 1,528 · see citing works
FGF/FGFR signaling in health and disease
Xie, Y., Su, N., Yang, J., Tan, Q., Huang, S., Jin, M., Ni, Z., Zhang, B., Zhang, D., Luo, F., et al. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00222-7 · Cited by 904 · see citing works
Tao, Q., Yokota, C., Puck, H., Kofron, M., Birsoy, B., Yan, D., Asashima, M., Wylie, C. C., Lin, X., & Heasman, J. (2005) · Cell · doi:10.1016/j.cell.2005.01.013 · Cited by 510 · see citing works
Self-citationWnt signaling: complexity at the surface
Cadigan, K. M., & Liu, Y. I. (2006) · Journal of Cell Science · doi:10.1242/jcs.02826 · Cited by 486 · see citing works
Structural Insights into Biological Roles of Protein-Glycosaminoglycan Interactions
Raman, R., Sasisekharan, V., & Sasisekharan, R. (2005) · Chemistry & Biology · doi:10.1016/j.chembiol.2004.11.020 · Cited by 434 · see citing works
Si, W., Kang, Q., Luu, H. H., Park, J. K., Luo, Q., Song, W.-X., Jiang, W., Luo, X., Li, X., Yin, H., et al. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.8.2955-2964.2006 · Cited by 272 · see citing works
A Systems Biology Approach for the Investigation of the Heparin/Heparan Sulfate Interactome
Ori, A., Wilkinson, M. C., & Fernig, D. G. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.228114 · Cited by 251 · see citing works
Farach-Carson, M. C., Warren, C. R., Harrington, D. A., & Carson, D. D. (2014) · Matrix Biology · doi:10.1016/j.matbio.2013.08.004 · Cited by 155 · see citing works
Otx2-PNN interaction to regulate cortical plasticity
Bernard, C., & Prochiantz, A. (2016) · Neural Plasticity · doi:10.1155/2016/7931693 · Cited by 102 · see citing works
Nakano, Y., Kohno, T., Hibi, T., Kohno, S., Baba, A., Mikoshiba, K., Nakajima, K., & Hattori, M. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702300200 · Cited by 86 · see citing works
Chemistry and Function of Glycosaminoglycans in the Nervous System
Schwartz, N. B., & Domowicz, M. S. (2014) · Advances in Neurobiology · doi:10.1007/978-1-4939-1154-7_5 · Cited by 25 · see citing works
- Authors
- Lin, X.
- Affiliations
- Cincinnati Children's Hospital Medical Center (US)
- Corresponding author
- Lin, Xinhua
- ORCID
- Lin, Xinhua
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2004-12-15
- Volume
- 131
- Issue
- 24
- Pages
- 6009-6021
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2102091298
- Cited by
- 678
- References
- 102
- Citations by year
- 2026: 6 · 2025: 9 · 2024: 15 · 2023: 17 · 2022: 18 · 2021: 29 · 2020: 27 · 2019: 25 · 2018: 32 · 2017: 33 · 2016: 34 · 2015: 25 · 2014: 33 · 2013: 37 · 2012: 36
- FWCI
- 3.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Keywords
- heparan sulfate proteoglycans, signal transduction, developmental signaling pathways, Wnt signaling, Hedgehog signaling, TGF-beta signaling, FGF signaling, extracellular matrix, glycosaminoglycans, core protein
- MeSH terms
- Animals, Cell Membrane, Drosophila, Extracellular Matrix, Fibroblast Growth Factors, Glycosaminoglycans, Signal Transduction, Heparan Sulfate Proteoglycans, Intercellular Signaling Peptides and Proteins, Macromolecular Substances, Wnt 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