Diversity in Tissue Expression, Substrate Binding, and SCF Complex Formation for a Lectin Family of Ubiquitin Ligases
Open accessAbstract
Post-translational modification of proteins regulates many cellular processes. Some modifications, including N-linked glycosylation, serve multiple functions. For example, the attachment of N-linked glycans to nascent proteins in the endoplasmic reticulum facilitates proper folding, whereas retention of high mannose glycans on misfolded glycoproteins serves as a signal for retrotranslocation and ubiquitin-mediated proteasomal degradation. Here we examine the substrate specificity of the only family of ubiquitin ligase subunits thought to target glycoproteins through their attached glycans. The five proteins comprising this FBA family (FBXO2, FBXO6, FBXO17, FBXO27, and FBXO44) contain a conserved G domain that mediates substrate binding. Using a variety of complementary approaches, including glycan arrays, we show that each family member has differing specificity for glycosylated substrates. Collectively, the F-box proteins in the FBA family bind high mannose and sulfated glycoproteins, with one FBA protein, FBX044, failing to bind any glycans on the tested arrays. Site-directed mutagenesis of two aromatic amino acids in the G domain demonstrated that the hydrophobic pocket created by these amino acids is necessary for high affinity glycan binding. All FBA proteins co-precipitated components of the canonical SCF complex (Skp1, Cullin1, and Rbx1), yet FBXO2 bound very little Cullin1, suggesting that FBXO2 may exist primarily as a heterodimer with Skp1. Using subunit-specific antibodies, we further demonstrate marked divergence in tissue distribution and developmental expression. These differences in substrate recognition, SCF complex formation, and tissue distribution suggest that FBA proteins play diverse roles in glycoprotein quality control.
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
Cites
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?
FBXO44 is enriched in some tissues but not specific to any.
“F-box protein 44 (FBXO44)150 that is enriched in some tissues but not specific to any151.”
From PROTAC targeted protein degraders: the past is prologue (2022) · cites this paper as [151]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Pruitt, K. D., Tatusova, T. A., & Maglott, D. R. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl842 · Cited by 4,441 · see citing works
The Ubiquitin-Proteasome Proteolytic Pathway: Destruction for the Sake of Construction
Glickman, M. H., & Ciechanover, A. J. (2002) · Physiological Reviews · doi:10.1152/physrev.00027.2001 · Cited by 4,216 · see citing works
Intracellular Functions of N-Linked Glycans
Helenius, A., & Aebi, A. M. (2001) · Science · doi:10.1126/science.291.5512.2364 · Cited by 2,405 · see citing works
Quality control in the endoplasmic reticulum
Ellgaard, L., & Helenius, A. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1052 · Cited by 2,130 · see citing works
Roles of N-Linked Glycans in the Endoplasmic Reticulum
Helenius, A., & Aebi, M. (2004) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.73.011303.073752 · Cited by 2,037 · see citing works
Rapid degradation of a large fraction of newly synthesized proteins by proteasomes
Schubert, U., Antón, L. C., Gibbs, J. S., Norbury, C. C., Yewdell, J. W., & Bennink, J. R. (2000) · Nature · doi:10.1038/35008096 · Cited by 1,536 · see citing works
Structure of the Cul1–Rbx1–Skp1–F boxSkp2 SCF ubiquitin ligase complex
Zheng, N., Schulman, B. A., Song, L., Miller, J. J., Jeffrey, P. D., Wang, P., Chu, C., Koepp, D. M., Elledge, S. J., Pagano, M., et al. (2002) · Nature · doi:10.1038/416703a · Cited by 1,507 · see citing works
Bai, C., Sen, P., Hofmann, K., Ma, L., Goebl, M. G., Harper, J. W., & Elledge, S. J. (1996) · Cell · doi:10.1016/s0092-8674(00)80098-7 · Cited by 1,421 · see citing works
The ubiquitin–proteasome pathway: on protein death and cell life
Ciechanover, A. J. (1998) · The EMBO Journal · doi:10.1093/emboj/17.24.7151 · Cited by 1,419 · see citing works
SCF and Cullin/RING H2-Based Ubiquitin Ligases
Deshaies, R. J. (1999) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.15.1.435 · Cited by 1,238 · see citing works
Printed covalent glycan array for ligand profiling of diverse glycan binding proteins
Blixt, O., Head, S., Mondala, T. S., Scanlan, C. N., Huflejt, M. E., Alvarez, R., Bryan, M. C., Fazio, F., Calarese, D. A., Stevens, J., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407902101 · Cited by 1,106 · see citing works
Kipreos, E. T., & Pagano, M. (2000) · Genome biology · doi:10.1186/gb-2000-1-5-reviews3002 · Cited by 743 · see citing works
Systematic analysis and nomenclature of mammalian F-box proteinsPreprint
Jin, J., Cardozo, T. J., Lovering, R. C., Elledge, S. J., Pagano, M., & Harper, J. W. (2004) · Genes & Development · doi:10.1101/gad.1255304 · Cited by 716 · see citing works
U Box Proteins as a New Family of Ubiquitin-Protein Ligases
Hatakeyama, S., Yada, M., Matsumoto, M., Ishida, N., & Nakayama, K. I. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102755200 · Cited by 580 · see citing works
A Novel Mechanism of Carbohydrate Recognition by the C-type Lectins DC-SIGN and DC-SIGNR
Mitchell, D. A., Fadden, A. J., & Drickamer, K. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104565200 · Cited by 502 · see citing works
All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases
Hagen, K. G. T. (2002) · Glycobiology · doi:10.1093/glycob/cwg007 · Cited by 498 · see citing works
Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation
Bays, N. W., Gardner, R. G., Seelig, L. P., Joazeiro, C. A. P., & Hampton, R. Y. (2000) · Nature Cell Biology · doi:10.1038/35050524 · Cited by 465 · see citing works
Werner, E. D., Brodsky, J. L., & McCracken, A. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13797 · Cited by 463 · see citing works
Dermatan sulfate: new functions from an old glycosaminoglycan
Trowbridge, J. M., & Gallo, R. L. (2002) · Glycobiology · doi:10.1093/glycob/cwf066 · Cited by 459 · see citing works
Spik, G. (1975) · FEBS Letters · doi:10.1016/0014-5793(75)80513-8 · Cited by 360 · see citing works
A family of mammalian F-box proteins
Winston, J. T., Koepp, D. M., Zhu, C., Elledge, S. J., & Harper, J. W. (1999) · Current Biology · doi:10.1016/s0960-9822(00)80021-4 · Cited by 357 · see citing works
E3 ubiquitin ligase that recognizes sugar chains
Yoshida, Y., Chiba, T., Tokunaga, F., Kawasaki, H., Iwaï, K., Suzuki, T., Ito, Y., Matsuoka, K., Yoshida, M., Tanaka, K., et al. (2002) · Nature · doi:10.1038/nature00890 · Cited by 351 · see citing works
Endoplasmic Reticulum Degradation Requires Lumen to Cytosol Signaling
Gardner, R. G., Swarbrick, G. M., Bays, N. W., Cronin, S. R., Wilhovsky, S., Seelig, L. P., Kim, C. G., & Hampton, R. Y. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.1.69 · Cited by 317 · see citing works
Ubiquitin-dependent degradation of multiple F-box proteins by an autocatalytic mechanism
Galan, J., & Peter, M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.16.9124 · Cited by 269 · see citing works
Biochemistry, molecular biology, and genetics of the oligosaccharyltransferase
Silberstein, S., & Gilmore, R. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.8.8666161 · Cited by 256 · see citing works
Detecting and Measuring Cotranslational Protein Degradation in Vivo
Turner, G. C., & Varshavsky, A. J. (2000) · Science · doi:10.1126/science.289.5487.2117 · Cited by 245 · see citing works
Croft, L., Schandorff, S., Clark, F., Burrage, K., Arctander, P., & Mattick, J. S. (2000) · Nature Genetics · doi:10.1038/74153 · Cited by 221 · see citing works
Fbs2 Is a New Member of the E3 Ubiquitin Ligase Family That Recognizes Sugar Chains
Yoshida, Y., Tokunaga, F., Chiba, T., Iwaï, K., Tanaka, K., & Tai, T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304157200 · Cited by 176 · see citing works
(1975) · FEBS Letters · doi:10.1016/0014-5793(75)90053-8 · Cited by 154 · see citing works
Townsend, R. R., Hilliker, E., Li, Y. T., Laine, R. A., Bell, W. R., & Lee, Y. C. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)34130-9 · Cited by 142 · see citing works
Arias, E. B., Kim, J., & Cartee, G. D. (2004) · Diabetes · doi:10.2337/diabetes.53.4.921 · Cited by 139 · see citing works
The Comparative Proteomics of Ubiquitination in MousePreprint
Semple, C. A. M., RIKEN GER Group, & Members, G. (2003) · Genome Research · doi:10.1101/gr.980303 · Cited by 135 · see citing works
Moremen, K. W., & Molinari, M. (2006) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2006.08.005 · Cited by 134 · see citing works
Kijimoto‐Ochiai, S., Katagiri, Y. U., & Ochiai, H. (1985) · Analytical Biochemistry · doi:10.1016/0003-2697(85)90031-4 · Cited by 133 · see citing works
cbl-3: a new mammalian cbl family protein
Keane, M., Ettenberg, S. A., Nau, M. M., Banerjee, P., Cuello, M. A., Penninger, J. M., & Lipkowitz, S. (1999) · Oncogene · doi:10.1038/sj.onc.1202753 · Cited by 120 · see citing works
Using a Small Molecule Inhibitor of Peptide: N-Glycanase to Probe Its Role in Glycoprotein Turnover
Misaghi, S., Pacold, M. E., Blom, D., Ploegh, H. L., & Korbel, G. A. (2004) · Chemistry & Biology · doi:10.1016/j.chembiol.2004.11.010 · Cited by 116 · see citing works
Cabral, C. M., Liu, Y., Moremen, K. W., & Sifers, R. N. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-02-0068 · Cited by 109 · see citing works
Shiyan, S. D., & Bovin, N. V. (1997) · Glycoconjugate Journal · doi:10.1023/a:1018544711767 · Cited by 106 · see citing works
A window of opportunity: timing protein degradation by trimming of sugars and ubiquitins.
Lederkremer, G., & Glickman, M. (2005) · TIBS -Trends in Biochemical Sciences. Regular ed · doi:10.1016/j.tibs.2005.04.010 · Cited by 106 · see citing works
Shaper, N. L., Wright, W. W., & Shaper, J. H. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.2.791 · Cited by 102 · see citing works
Manzella, S. M., Hooper, L. V., & Baenziger, J. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.21.12117 · Cited by 98 · see citing works
Sequence analysis of heparan sulphate and heparin oligosaccharides
Vivès, R. R., Pye, D. A., Salmivirta, M., Hopwood, J. J., Lindahl, U., & Gallagher, J. T. (1999) · Biochemical Journal · doi:10.1042/bj3390767 · Cited by 95 · see citing works
Harduin‐Lepers, A., Shaper, J. H., & Shaper, N. L. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)85247-x · Cited by 92 · see citing works
Yamashita, K., Liang, C. J., Funakoshi, S., & Kobata, A. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)69961-8 · Cited by 89 · see citing works
Structural basis for the selection of glycosylated substrates by SCF Fbs1 ubiquitin ligase
Mizushima, T., Yoshida, Y., Kumanomidou, T., Hasegawa, Y., Suzuki, A., Yamane, T., & Tanaka, K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610312104 · Cited by 85 · see citing works
Nelson, R. F., Glenn, K. A., Zhang, Y., Wen, H., Knutson, T. M., Gouvion, C. M., Robinson, B. K., Zhou, Z., Yang, B., Smith, R. J., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0206-07.2007 · Cited by 82 · see citing works
Self-citationStructural basis of sugar-recognizing ubiquitin ligase
Mizushima, T., Hirao, T., Yoshida, Y., Lee, S. J., Chiba, T., Iwaï, K., Yamaguchi, Y., Kato, K., Tomitake Tsukihara, A., & Tanaka, K. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb732 · Cited by 82 · see citing works
Glycoprotein‐specific ubiquitin ligases recognize N‐glycans in unfolded substrates
Yoshida, Y., Adachi, E., Fukiya, K., Iwaï, K., & Tanaka, K. (2005) · EMBO Reports · doi:10.1038/sj.embor.7400351 · Cited by 81 · see citing works
Carbohydrate in Pancreatic Ribonucleases
Beintema, J. J., Gaastra, W., Scheffer, A. J., & Welling, G. W. (1976) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1976.tb10246.x · Cited by 71 · see citing works
A Novel F Box Protein, NFB42, Is Highly Enriched in Neurons and Induces Growth Arrest
Erhardt, J. A., Hynicka, W. P., DiBenedetto, A. J., Shen, N., Stone, N. L., Paulson, H. L., & Pittman, R. N. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.52.35222 · Cited by 66 · see citing works
Self-citationMehtani, S., Gong, Q., Panella, J. R., Subbiah, S., Peffley, D. M., & Frankfater, A. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.21.13236 · Cited by 66 · see citing works
Characterization of the mouse gene for the U-box-type ubiquitin ligase UFD2a
Kaneko, C., Hatakeyama, S., Matsumoto, M., Yada, M., Nakayama, K., & Nakayama, K. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02834-6 · Cited by 60 · see citing works
The coiled-coil domain of TRAF6 is essential for its auto-ubiquitination
Yang, K. S., Zhu, J., Sun, S., Tang, Y., Zhang, B., Diao, L., & Wang, C. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.09.070 · Cited by 57 · see citing works
Endo, M., Suzuki, K., Schmid, K., Fournet, B., Karamanos, Y., Montreuil, J., DORLAND, L., van HALBEEK, H., & Vliegenthart, J. F. G. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)34193-0 · Cited by 55 · see citing works
A Novel Route for F-box Protein-mediated Ubiquitination Links CHIP to Glycoprotein Quality Control
Nelson, R. F., Glenn, K. A., Miller, V. M., Wen, H., & Paulson, H. L. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602423200 · Cited by 51 · see citing works
Self-citationThe cochlear F-box protein OCP1 associates with OCP2 and connexin 26
Henzl, M. T., Thalmann, I., Larson, J. D., Ignatova, E. G., & Thalmann, R. (2004) · Hearing Research · doi:10.1016/j.heares.2004.01.005 · Cited by 51 · see citing works
Zhou, X., Zhao, G., Truglio, J. J., Wang, L., Li, G., Lennarz, W. J., & Schindelin, H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602954103 · Cited by 48 · see citing works
WEST, C. (2004) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2004.04.007 · Cited by 44 · see citing works
Baici, A., Müntener, K., Willimann, A., & Zwicky, R. (2006) · Biological Chemistry · doi:10.1515/bc.2006.125 · Cited by 42 · see citing works
Thermodynamic Analysis of Interactions between N-Linked Sugar Chains and F-Box Protein Fbs1
Hagihara, S., Totani, K., Matsuo, I., & Ito, Y. (2005) · Journal of Medicinal Chemistry · doi:10.1021/jm0489511 · Cited by 40 · see citing works
A Neural-specific F-box Protein Fbs1 Functions as a Chaperone Suppressing Glycoprotein Aggregation
Yoshida, Y., Murakami, A., Iwaï, K., & Tanaka, K. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m611168200 · Cited by 37 · see citing works
A new subfamily of structurally related human F-box proteins
Ilyin, G. P., Sérandour, A., Pigeon, C., Rialland, M., Glaise, D., & Guguen‐Guillouzo, C. (2002) · Gene · doi:10.1016/s0378-1119(02)00867-3 · Cited by 34 · see citing works
OCP1, an F-box protein, co-localizes with OCP2/SKP1 in the cochlear epithelial gap junction region
Henzl, M. T., O’Neal, J., Killick, R., Thalmann, I., & Thalmann, R. (2001) · Hearing Research · doi:10.1016/s0378-5955(01)00285-4 · Cited by 34 · see citing works
Exploring the Role of 5’ Alternative Splicing and of the 3’-Untranslated Region of Cathepsin B mRNA
Zwicky, R., Müntener, K., Csúcs, G., Goldring, M. B., & Baici, A. (2003) · Biological Chemistry · doi:10.1515/bc.2003.113 · Cited by 30 · see citing works
Fbs1 protects the malfolded glycoproteins from the attack of peptide:N-glycanase
Yamaguchi, Y., Hirao, T., Sakata, E., Kamiya, Y., Kurimoto, E., Yoshida, Y., Suzuki, T., Tanaka, K., & Kato, K. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.08.056 · Cited by 27 · see citing works
Characterization of Glycans in a Lactoferrin Isoform, Lactoferrin-a
Wei, Z., Nishimura, T., & Yoshida, S. (2001) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(01)74712-1 · Cited by 25 · see citing works
Parkin expression in the developing mouse
Kühn, K., Zhu, X., Lübbert, H., & Stichel, C. C. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2004.02.001 · Cited by 25 · see citing works
West, C. M. (2003) · Cellular and Molecular Life Sciences · doi:10.1007/s000180300018 · Cited by 25 · see citing works
Expression analysis of the gene encoding for the U-box-type ubiquitin ligase UBE4A in human tissues
Contino, G., Amati, F., Pucci, S., Pontieri, E., Pichiorri, F., Novelli, A., Botta, A., Mango, R., Nardone, A. M., Sangiuolo, F. C., et al. (2004) · Gene · doi:10.1016/j.gene.2003.11.017 · Cited by 24 · see citing works
Microsatellite structures in the context of human evolution
Wiegand, P., Meyer, E., & Brinkmann, B. (2000) · Electrophoresis · doi:10.1002/(sici)1522-2683(20000301)21:5 · Cited by 21 · see citing works
OCP2 exists as a dimer in the organ of Corti
Henzl, M. T., Thalmann, I., & Thalmann, R. (1998) · Hearing Research · doi:10.1016/s0378-5955(98)00148-8 · Cited by 17 · see citing works
Thalmann, R., Henzl, M. T., Killick, R., Ignatova, E. G., & Thalmann, I. (2003) · Acta Oto-Laryngologica · doi:10.1080/0036554021000028100 · Cited by 17 · see citing works
Groisman, B., Avezov, E., & Lederkremer, G. Z. (2006) · Israel Journal of Chemistry · doi:10.1560/2qpd-9wp9-ncyk-58x3 · Cited by 12 · see citing works
Flagged first, then by citations
Research works printed but not linked: 6
- Werner, E. D., Brodsky, J. L., and McCracken, A. A. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 13797-13801
- Zhou, X., Zhao, G., Truglio, J. J., Wang, L., Li, G., Lennarz, W. J., and Schindelin, H. (2006) Proc. Natl. Acad. Sci. U. S. A. 103, 17214 -17219
- Blixt, O., Head, S., Mondala, T., Scanlan, C., Huflejt, M. E., Alvarez, R., Bryan, M. C., Fazio, F., Calarese, D., Stevens, J., Razi, N., Stevens, D. J., Skehel, J. J., van Die, I., Burton, D. R., Wilson, I. A., Cummings, R., Bovin, N., Wong, C.-H., and Paulson, J. C. (2004) Proc. Natl. Acad. Sci. U. S. A. 101, 17033-17038
- Mizushima, T., Yoshida, Y., Kumanomidou, T., Hasegawa, Y., Suzuki, A., Yamane, T., and Tanaka, K. (2007) Proc. Natl. Acad. Sci. U. S. A. 104, 5777-5781
- Galan, J.-M., and Peter, M. (1999) Proc. Natl. Acad. Sci. U. S. A. 96, 9124 -9129
- Shaper, N., Wright, W., and Shaper, J. (1990) Proc. Natl. Acad. Sci. U. S. A. 87, 791-795
Cited by
Sorted by citations
PROTAC targeted protein degraders: the past is prologue
Békés, M., Langley, D. R., & Crews, C. M. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00371-6 · Cited by 3,395 · see citing works
Mechanisms and function of substrate recruitment by F-box proteins
Skaar, J. R., Pagan, J. K., & Pagano, M. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3582 · Cited by 671 · see citing works
Galectin-3 Coordinates a Cellular System for Lysosomal Repair and Removal
Jia, J., Claude-Taupin, A., Gu, Y., Choi, S. W., Peters, R., Bissa, B., Mudd, M. H., Allers, L., Pallikkuth, S., Lidke, K. A., et al. (2020) · Developmental Cell · doi:10.1016/j.devcel.2019.10.025 · Cited by 434 · see citing works
Damme, E. J. M. V., Lannoo, N., & Peumans, W. J. (2008) · Advances in botanical research · doi:10.1016/s0065-2296(08)00403-5 · Cited by 237 · see citing works
Repair or Lysophagy: Dealing with Damaged Lysosomes.
Papadopoulos, C., Kravić, B., & Meyer, H. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.08.010 · Cited by 183 · see citing works
Wong, E., Vaaje‐Kolstad, G., Ghosh, A., Hurtado‐Guerrero, R., Konarev, P. V., Ibrahim, A. F. M., Svergun, D. I., Eijsink, V. G. H., Chatterjee, N. S., & van Aalten, D. M. F. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002373 · Cited by 176 · see citing works
Ubiquitination of exposed glycoproteins by SCF FBXO27 directs damaged lysosomes for autophagy
Yoshida, Y., Yasuda, S., Fujita, T., Hamasaki, M., Murakami, A., Kawawaki, J., Iwaï, K., Saeki, Y., Yoshimori, T., Matsuda, N., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1702615114 · Cited by 147 · see citing works
CpG island methylation profiling in human salivary gland adenoid cystic carcinoma
Bell, A., Bell, D., Weber, R. S., & El‐Naggar, A. K. (2011) · Cancer · doi:10.1002/cncr.25818 · Cited by 126 · see citing works
F-box protein interactions with the hallmark pathways in cancer
Randle, S. J., & Laman, H. (2015) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.09.013 · Cited by 95 · see citing works
Wang, G., Chen, S., Xie, Z., Shen, S., Xu, W., Chen, W., Li, X., Wu, Y., Li, L., Liu, B., et al. (2020) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2019-216911 · Cited by 97 · see citing works
Convergent and divergent mechanisms of sugar recognition across kingdoms
Taylor, M. E., & Drickamer, K. (2014) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2014.07.003 · Cited by 82 · see citing works
Human Lectins, Their Carbohydrate Affinities and Where to Find Them
Raposo, C. D. D. C. B. G., Canelas, A. B., & Barros, M. T. (2021) · Biomolecules · doi:10.3390/biom11020188 · Cited by 82 · see citing works
Plant F-box Proteins – Judges between Life and Death
Stefanowicz, K., Lannoo, N., & Damme, E. J. M. V. (2015) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2015.1024566 · Cited by 67 · see citing works
The F-box Protein FBXO44 Mediates BRCA1 Ubiquitination and Degradation
Lu, Y., Li, J., Cheng, D., Parameswaran, B., Zhang, S., Jiang, Z., Yew, P. R., Peng, J., Ye, Q., & Hu, Y. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.407106 · Cited by 65 · see citing works
Buso, A., Comelli, M., Picco, R., Isola, M., Magnesa, B., Pišot, R., Rittweger, J., Salvadego, D., Šimunič, B., Grassi, B., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00474 · Cited by 63 · see citing works
Lectin-like ERAD players in ER and cytosol
Yoshida, Y., & Tanaka, K. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.07.029 · Cited by 59 · see citing works
Lectins of living organisms. The overview
Lakhtin, V. M., Lakhtin, M., & Aleshkin, V. A. (2011) · Anaerobe · doi:10.1016/j.anaerobe.2011.06.004 · Cited by 59 · see citing works
Stefanowicz, K., Lannoo, N., Zhao, Y., Eggermont, L., Hove, J. V., Atalah, B. A., & Damme, E. J. M. V. (2016) · BMC Plant Biology · doi:10.1186/s12870-016-0905-2 · Cited by 50 · see citing works
Liu, B., Zheng, Y., Wang, T., Xu, H., Li, X., Zhang, J., Wu, Y., Chen, G., & Wang, L. (2012) · Journal of Proteome Research · doi:10.1021/pr2010204 · Cited by 49 · see citing works
Atkin, G., Moore, S. J., Lü, Y., Nelson, R. F., Tipper, N., Rajpal, G., Hunt, J. F. V., Tennant, W., Hell, J. W., Murphy, G. G., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3013-14.2015 · Cited by 46 · see citing works
Self-citationLiu, E. A., Schultz, M., Mochida, C., Chung, C., Paulson, H., & Lieberman, A. (2020) · JCI Insight · doi:10.1172/jci.insight.136676 · Cited by 42 · see citing works
Self-citationChen, M., Shi, X., Duke, R. M., Ruse, C. I., Dai, N., Taron, C. H., & Samuelson, J. C. (2017) · Nature Communications · doi:10.1038/ncomms15487 · Cited by 46 · see citing works
F-box Only Protein 2 (Fbxo2) Regulates Amyloid Precursor Protein Levels and Processing
Atkin, G., Hunt, J. F. V., Minakawa, E. N., Sharkey, L. M., Tipper, N., Tennant, W., & Paulson, H. L. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.515056 · Cited by 44 · see citing works
Self-citationLiu, B., Han, L., Li, D., Xiong, X., Gao, L., Wu, Z., & Lu, Y. (2016) · Diabetes · doi:10.2337/db16-1104 · Cited by 42 · see citing works
Zhang, H.-J., Tian, J., Qi, X.-K., Xiang, T., He, G.-P., Zhang, H., Yu, X., Zhang, X., Zhao, B., Feng, Q.-S., et al. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007208 · Cited by 42 · see citing works
Stefanowicz, K., Lannoo, N., Proost, P., & Damme, E. J. M. V. (2012) · FEBS Open Bio · doi:10.1016/j.fob.2012.06.002 · Cited by 40 · see citing works
FBXO2, a novel marker for metastasis in human gastric cancer
Sun, X., Wang, T., Guan, Z., Zhang, C., Chen, Y., Jin, J., & Hua, D. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.12.097 · Cited by 39 · see citing works
Che, X., Jian, F., Wang, Y., Zhang, J., Shen, J., Cheng, Q., Wang, X., Jia, N., & Feng, W. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00843 · Cited by 40 · see citing works
FBXO6-mediated RNASET2 ubiquitination and degradation governs the development of ovarian cancer
Ji, M., Zhao, Z., Li, Y., Xu, P., Shi, J., Li, Z., Wang, K., Huang, X., & Liu, B. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03580-4 · Cited by 39 · see citing works
Lectins as potential tools for cancer biomarker discovery from extracellular vesicles
Islam, M. K., Khan, M., Gidwani, K., Witwer, K. W., Lamminmäki, U., & Leivo, J. (2023) · Biomarker Research · doi:10.1186/s40364-023-00520-6 · Cited by 36 · see citing works
Skp1 stabilizes the conformation of F-box proteins
Yoshida, Y., Murakami, A., & Tanaka, K. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.05.098 · Cited by 36 · see citing works
Kallio, H. M. L., Tolvanen, M. E. E., Jänis, J., Pan, P., Laurila, E. M., Kallioniemi, A. H., Kilpinen, S. K., Tuominen, V. J., Isola, J. J., Valjakka, J., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027152 · Cited by 35 · see citing works
FBXO44-Mediated Degradation of RGS2 Protein Uniquely Depends on a Cullin 4B/DDB1 Complex
Sjögren, B., Swaney, S. M., & Neubig, R. R. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123581 · Cited by 33 · see citing works
Peng, D., Wang, Z., Huang, A., Zhao, Y. B., & Qin, F. X.-F. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1601009 · Cited by 32 · see citing works
FBXO2/SCF ubiquitin ligase complex directs xenophagy through recognizing bacterial surface glycan
Yamada, A., Hikichi, M., Nozawa, T., & Nakagawa, I. (2021) · EMBO Reports · doi:10.15252/embr.202152584 · Cited by 30 · see citing works
Chen, W., Xiong, S., Li, J., Li, X., Liu, Y., Zou, C., & Mallampalli, R. K. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.01185-14 · Cited by 30 · see citing works
Suber, T. L., Wei, J., Jacko, A. M., Nikolli, I., Zhao, Y., Zhao, J., & Mallampalli, R. K. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.771667 · Cited by 30 · see citing works
Lannoo, N., Peumans, W. J., & Damme, E. J. M. V. (2008) · Biochemical Society Transactions · doi:10.1042/bst0360843 · Cited by 29 · see citing works
Chen, X., Duan, L.-H., Luo, P., Hu, G., Yu, X., Liu, J., Han, L., & Liu, B. (2016) · Cellular Physiology and Biochemistry · doi:10.1159/000452517 · Cited by 28 · see citing works
Su, S.-B., Tian, R.-J., Jiao, Y., Zheng, S., Liang, S., Liu, T., Tian, Z., Cao, X., Xing, Y., Ma, C., et al. (2024) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2024.09.011 · Cited by 29 · see citing works
Linear ubiquitination at damaged lysosomes induces local NF-κB activation and controls cell survival
Zein, L., Dietrich, M., Balta, D., Bader, V., Scheuer, C., Zellner, S., Weinelt, N., Vandrey, J., Mari, M., Behrends, C., et al. (2023) · bioRxiv · doi:10.1080/15548627.2024.2443945 · Cited by 27 · see citing works
Sugar-Recognizing Ubiquitin Ligases: Action Mechanisms and Physiology
Yoshida, Y., Mizushima, T., & Tanaka, K. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00104 · Cited by 25 · see citing works
Kumanomidou, T., Nishio, K., Takagi, K., Nakagawa, T., Suzuki, A., Yamane, T., Tokunaga, F., Iwai, K., Murakami, A., Yoshida, Y., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0140366 · Cited by 21 · see citing works
Clinical significance of FBXO17 gene expression in high-grade glioma
Du, D., Yuan, J., Ma, W., Ning, J., Weinstein, J. N., Yuan, X., Fuller, G. N., & Liu, Y. (2018) · BMC Cancer · doi:10.1186/s12885-018-4680-3 · Cited by 18 · see citing works
Gee, R. R. F., Huber, A. D., Wu, J., Bajpai, R., Loughran, A. J., Pruett‐Miller, S. M., & Chen, T. (2023) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2023.07.014 · Cited by 15 · see citing works
Cytosolic N‐Glycans: Triggers for Ubiquitination Directing Proteasomal and Autophagic Degradation
Yoshida, Y., & Tanaka, K. (2018) · BioEssays · doi:10.1002/bies.201700215 · Cited by 14 · see citing works
Folding and Quality Control of Glycoproteins
Suzuki, T., Tanabe, K., & Funakoshi, Y. (2007) · Elsevier eBooks · doi:10.1016/b978-044451967-2/00046-5 · Cited by 12 · see citing works
Lectin-Type Ubiquitin Ligase Subunits: Fbs Proteins and Their Applications for Use
Yoshida, Y. (2020) · Methods in molecular biology · doi:10.1007/978-1-0716-0430-4_22 · Cited by 11 · see citing works
Precision oncology revolution: CRISPR-Cas9 and PROTAC technologies unleashed
Kanbar, K., Darzi, R. E., & Jaalouk, D. E. (2024) · Frontiers in Genetics · doi:10.3389/fgene.2024.1434002 · Cited by 17 · see citing works
McNabb, H. J., González, S., Muli, C. S., & Sjögren, B. (2020) · Molecular Pharmacology · doi:10.1124/molpharm.120.000061 · Cited by 11 · see citing works
FBXW10 is negatively regulated in transcription and expression level by protein O-GlcNAcylation
Feng, Z., Yan, H., Li, L., Xiaoyan, L., Yuqiu, W., Peng, W., & Lianwen, Z. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.07.091 · Cited by 11 · see citing works
Using a ubiquitin ligase as an unfolded protein sensor
Mallinger, A., Wen, H., Dankle, G., & Glenn, K. A. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.12.109 · Cited by 10 · see citing works
Self-citationGupta, S., Garg, V., & Bhatia, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0121100 · Cited by 10 · see citing works
Gordon, K. L., Glenn, K. A., Bode, N. M., Wen, H. M., Paulson, H. L., & Gonzalez‐Alegre, P. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.023 · Cited by 10 · see citing works
Self-citationFBG1 is a promiscuous ubiquitin ligase that sequesters APC2 and causes S-phase arrest
Wen, H., Kim, N., Fuentes, E. J., Mallinger, A., Gonzalez‐Alegre, P., & Glenn, K. A. (2010) · Cell Cycle · doi:10.4161/cc.9.22.13743 · Cited by 9 · see citing works
Self-citationFunctional identification of a novel F‐box/FBA gene in tomato
Xing, L., Li, Z., Khalil, R., Ren, Z., & Yang, Y. (2011) · Physiologia Plantarum · doi:10.1111/j.1399-3054.2011.01543.x · Cited by 9 · see citing works
The Nogo receptor 2 is a novel substrate of Fbs1
Kern, F., Sarg, B., Stasyk, T., Heß, D., & Lindner, H. H. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.12.050 · Cited by 8 · see citing works
Wu, M., Li, S., Han, J., Liu, R., Yuan, H., Xu, X., Li, X., & Liu, Z. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.606327 · Cited by 7 · see citing works
Miller, R. G., Mychaleckyj, J., Onengut-Gumuscu, S., Feingold, E., Orchard, T., & Costacou, T. (2023) · Clinical Epigenetics · doi:10.1186/s13148-023-01539-0 · Cited by 5 · see citing works
Identification of SNPs and Candidate Genes for Milk Production Ability in Yorkshire Pigs
Shi, L., Yang, L., Liu, Q., Zhang, L., Wang, L., Liu, X., Gao, H., Hou, X., Zhao, F., Yan, H., et al. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.724533 · Cited by 5 · see citing works
Folding and Quality Control of Glycoproteins
Suzuki, T., & Fujihira, H. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-409547-2.14947-9 · Cited by 5 · see citing works
Dong, L., Wang, H., Miao, Z., Yu, Y., Gai, D., Zhang, G., Ge, L., & Shen, X. (2023) · Hematology · doi:10.1080/16078454.2023.2246268 · Cited by 5 · see citing works
FBG1 Is the Final Arbitrator of A1AT-Z Degradation
Wen, J. H., Wen, H., Gibson-Corley, K. N., & Glenn, K. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135591 · Cited by 5 · see citing works
Self-citationGözütok, Ö., Helmold, B., & Özdi̇nler, P. H. (2021) · Brain Sciences · doi:10.3390/brainsci11050578 · Cited by 4 · see citing works
Krey, K., Risso-Ballester, J., Hamad, S., Maidl, S., Bilekova, S., Emslander, Q., Verin, M., Mundigl, S., Cernat, A., Piras, A., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-72732-x · Cited by 4 · see citing works
Nie, H., Xu, H., Yang, S., Tian, C., Wang, T., Jin, C., Chen, Z., Wang, X., Tang, J., Feng, Y., et al. (2025) · Advanced Science · doi:10.1002/advs.202415458 · Cited by 2 · see citing works
Lectins of ERAD Pathway: F-Box Proteins and M-Type Lectins
Gupta, G. (2012) · Springer eBooks · doi:10.1007/978-3-7091-1065-2_6 · Cited by 2 · see citing works
Palacios, F., Cota, G., Horjales, S., Lima, A. E., Battistoni, J., Sotelo-Silveira, J. R., & Marı́n, M. (2010) · Biotechnology Journal · doi:10.1002/biot.200900106 · Cited by 2 · see citing works
Wang, Z., Li, X., Tang, Z., Yang, S., Ying, Z., Fu, T., Fan, B., Mu, Y., Ao, H., & Li, K. (2009) · Molecular Biology Reports · doi:10.1007/s11033-009-9928-1 · Cited by 2 · see citing works
Tissue Standards Using Stain Free Gels as a Superior Approach for Aging Research
Wen, H., Dankle, G., & Glenn, K. A. (2014) · International Journal of Biochemistry Research & Review · doi:10.9734/ijbcrr/2015/8940 · Cited by 1 · see citing works
Self-citationToti-N-glycan Recognition Enables Universal Multiplexed Single-Nucleus RNA Sequencing
Guo, Y., Zhang, L., Zhao, X., Chang, X., Li, Y., Gao, Z., Ou, G., Chen, P., Zheng, W., Pei, H., et al. (2025) · Research · doi:10.34133/research.0678 · Cited by 1 · see citing works
N-Glycans and Quality Control of Proteins
Hosokawa, N., & Suzuki, T. (2014) · Springer eBooks · doi:10.1007/978-4-431-55381-6_1 · Cited by 1 · see citing works
Saritas‐Yildirim, B. (2013) · DigitalGeorgetown (Georgetown University Library)
Regulation and Roles of Carbonic Anhydrases IX and XII
Kallio, H. M. L. (2011) · Tampere University Institutional Repository (Tampere University)
Identification of the genetic alterations in prostate cancer metastases
Stankiewicz, E. (2017) · Queen Mary Research Online (Queen Mary University of London)
Identification of SNPs and Candidate Genes for Milk Produce Ability in Yorkshire PigPreprint
Shi, L., Li, Y., Liu, Q., Zhang, L., Wang, L., Liu, X., Gao, H., Hou, X., Zhao, F., Yan, H., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-585023/v1
Xue, C., Yang, F., Bao, G., Yan, J., Fu, R., Zhang, M., Ding, J., Feng, J., Han, J., Qin, X., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.28.586926
Xin, Z., Gao, H., Ren, Z., & Tan, H. (2025) · Asian Journal of Surgery · doi:10.1016/j.asjsur.2025.03.213
McNabb, H. J., Cho, E., Pitman, M., Rushton, P. S., Mobley, D. L., & Sjögren, B. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.110757
Miller, R. G., Mychaleckyj, J. C., Onengut-Gumuscu, S., Feingold, E., Orchard, T., & Costacou, T. (2024) · Figshare · doi:10.6084/m9.figshare.26608066
Saifi, M. A., Marguerie, F., Kamiya, M., Nguyen, H. N., Knipe, R. S., Kim, E. Y., & Ho, I. (2026) · The Journal of Physiology · doi:10.1113/jp290391
Salkovski, M., Suarez, A. A., Gao, Q., Hippman, R. S., Petros, Z. A., Korkmaz, M. A., Gerlach, E. M., Alvarado-Cartagena, Y. M., Nguyen, T. T. A., Pavlinov, I., et al. (2026) · ACS Chemical Biology · doi:10.1021/acschembio.6c00039
Wu, Y., Li, Y., Chen, T., Xia, W., Wang, Y., Yan, X., & Hu, J. (2026) · Animals · doi:10.3390/ani16101510
Reyimu, A., Rahman, M., Abudurousuli, A., Cheng, X., Liu, X., Xu, A., & Zou, X. (2026) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2026.1885489
- Authors
- Glenn, K. A., Nelson, R. F., Wen, H. M., Mallinger, A. J., & Paulson, H. L.
- Affiliations
- Veterans Health Administration (US)
- University of Iowa Hospitals and Clinics (US)
- Kansas City University (US)
- Michigan Medicine (US)
- Corresponding author
- Glenn, Kevin A.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2008-05
- Volume
- 283
- Issue
- 19
- Pages
- 12717-12729
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC2442310
- OpenAlex
- W2007169599
- Cited by
- 86
- References
- 73
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 5 · 2023: 4 · 2022: 1 · 2021: 7 · 2020: 6 · 2019: 4 · 2018: 3 · 2017: 6 · 2016: 4 · 2015: 8 · 2014: 4 · 2013: 3 · 2012: 6
- FWCI
- 1.92
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (T32GM007337)
- National Institute of Neurological Disorders and Stroke (R01NS047535, F30NS047872, NS047872, R01 NS47535-01)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
- Keywords
- ubiquitin ligase, F-box protein, substrate specificity, glycan binding, high-mannose glycans, sulfated glycoproteins, G-domain, SCF ubiquitin ligase, CUL1, Skp1, RBX1, tissue expression, developmental gene expression, glycoprotein quality control, N-glycosylation, retrotranslocation, proteasomal degradation
- MeSH terms
- Animals, Cell Line, Chlorocebus aethiops, Multigene Family, Glycoproteins, Humans, Mannose, Models, Biological, Polysaccharides, Protein Binding, Substrate Specificity, Gene Expression Regulation, Enzymologic, Lectins, F-Box Proteins, SKP Cullin F-Box Protein Ligases, Mice, Hydrophobic and Hydrophilic Interactions
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