Identification of SVIP as an endogenous inhibitor of endoplasmic reticulum-associated degradation
Open accessAbstract
Misfolded proteins in the endoplasmic reticulum (ER) are eliminated by a process known as ER-associated degradation (ERAD), which starts with misfolded protein recognition, followed by ubiquitination, retrotranslocation to the cytosol, deglycosylation, and targeting to the proteasome for degradation. Actions of multisubunit protein machineries in the ER membrane integrate these steps. We hypothesized that regulation of the multisubunit machinery assembly is a mechanism by which ERAD activity is regulated. To test this hypothesis, we investigated the potential regulatory role of the small p97/VCP-interacting protein (SVIP) on the formation of the ERAD machinery that includes ubiquitin ligase gp78, AAA ATPase p97/VCP, and the putative channel Derlin1. We found that SVIP is anchored to microsomal membrane via myristoylation and co-fractionated with gp78, Derlin1, p97/VCP, and calnexin to the ER. Like gp78, SVIP also physically interacts with p97/VCP and Derlin1. Overexpression of SVIP blocks unassembled CD3delta from association with gp78 and p97/VCP, which is accompanied by decreases in CD3delta ubiquitination and degradation. Silencing SVIP expression markedly enhances the formation of gp78-p97/VCP-Derlin1 complex, which correlates with increased degradation of CD3delta and misfolded Z variant of alpha-1-antitrypsin, established substrates of gp78. These results suggest that SVIP is an endogenous inhibitor of ERAD that acts through regulating the assembly of the gp78-p97/VCP-Derlin1 complex.
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?
Disturbance of ER homeostasis in cEDS is suggested by the decreased transcription of SVIP.
“The disturbance of ER homeostasis in cEDS is also suggested by the decreased transcription of the small VCP/p97-interacting protein (SVIP), which is a modulator of the ER-associated degradation pathway [86,87].”
From Cellular and Molecular Mechanisms in the Pathogenesis of Classical, Vascular, and Hypermobile Ehlers‒Danlos Syndromes (2019) · cites this paper as [87]
Cites
Travers, K. J., Patil, C. K., Wodicka, L. M., Lockhart, D. J., Weissman, J. S., & Walter, P. (2000) · Cell · doi:10.1016/s0092-8674(00)80835-1 · Cited by 1,994 · see citing works
Protein Sensors for Membrane Sterols
Goldstein, J. L., DeBose‐Boyd, R. A., & Brown, M. S. (2006) · Cell · doi:10.1016/j.cell.2005.12.022 · Cited by 1,677 · see citing works
ERAD: the long road to destruction
Meusser, B., Hirsch, C., Jarosch, E., & Sommer, T. (2005) · Nature Cell Biology · doi:10.1038/ncb0805-766 · Cited by 1,221 · see citing works
A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol
Ye, Y., Shibata, Y., Yun, C., Ron, D., & Rapoport, T. A. (2004) · Nature · doi:10.1038/nature02656 · Cited by 963 · see citing works
Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation
Haglund, K., Sigismund, S., Polo, S., Szymkiewicz, I., Fiore, P. P. D., & Đikić, I. (2003) · Nature Cell Biology · doi:10.1038/ncb983 · Cited by 813 · see citing works
How the ubiquitin–proteasome system controls transcription
Muratani, M., & Tansey, W. P. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1049 · Cited by 803 · see citing works
Distinct Ubiquitin-Ligase Complexes Define Convergent Pathways for the Degradation of ER Proteins
Carvalho, P., Goder, V., & Rapoport, T. A. (2006) · Cell · doi:10.1016/j.cell.2006.05.043 · Cited by 726 · see citing works
Retro-translocation of proteins from the endoplasmic reticulum into the cytosol
Tsai, B., Ye, Y., & Rapoport, T. A. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm780 · Cited by 647 · see citing works
Hampton, R. Y., Gardner, R. G., & Rine, J. (1996) · Molecular Biology of the Cell · doi:10.1091/mbc.7.12.2029 · Cited by 569 · see citing works
ER-associated degradation in protein quality control and cellular regulation
Hampton, R. Y. (2002) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(02)00358-7 · Cited by 475 · see citing works
Younger, J. M., Chen, L., Ren, H.-Y., Rosser, M. F. N., Turnbull, E. L., Fan, C., Patterson, C., & Cyr, D. (2006) · Cell · doi:10.1016/j.cell.2006.06.041 · Cited by 440 · see citing works
A Luminal Surveillance Complex that Selects Misfolded Glycoproteins for ER-Associated Degradation
Denic, V., Toyama, E. Q., & Weissman, J. S. (2006) · Cell · doi:10.1016/j.cell.2006.05.045 · Cited by 419 · see citing works
Fang, S., Ferrone, M. L., Yang, C., Jensen, J. P., Tiwari, S., & Weissman, A. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.251401598 · Cited by 413 · see citing works
Self-citationKikkert, M., Doolman, R., Dai, M., Avner, R., Hassink, G., van Voorden, S., Thanedar, S., Roitelman, J., Chau, V., & Wiertz, E. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m307453200 · Cited by 384 · see citing works
Oda, Y., Okada, T., Yoshida, H., Kaufman, R. J., Nagata, K., & Mori, K. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200507057 · Cited by 380 · see citing works
Song, B., Sever, N., & DeBose‐Boyd, R. A. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.08.009 · Cited by 368 · see citing works
Lilley, B. N., & Ploegh, H. L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0505014102 · Cited by 315 · see citing works
Ye, Y., Shibata, Y., Kikkert, M., van Voorden, S., Wiertz, E. J. H. J., & Rapoport, T. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0505006102 · Cited by 311 · see citing works
Cytoplasmic destruction of p53 by the endoplasmic reticulum‐resident ubiquitin ligase ‘Synoviolin’
Yamasaki, S., Yagishita, N., Sasaki, T., Nakazawa, M., Kato, Y., Yamadera, T., Bae, E.-K., Toriyama, S., Ikeda, R., Zhang, L., et al. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601490 · Cited by 275 · see citing works
Endoplasmic reticulum stress compromises the ubiquitin–proteasome system
Menéndez-Benito, V., Verhoef, L. G. G. C., Masucci, M. G., & Dantuma, N. P. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi312 · Cited by 221 · see citing works
Chen, B., Mariano, J. M., Tsai, Y. C., Chan, A. H., Cohen, M. M., & Weissman, A. M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506618103 · Cited by 213 · see citing works
SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER
Mueller, B., Lilley, B. N., & Ploegh, H. L. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200605196 · Cited by 210 · see citing works
Zhong, X., Shen, Y., Ballar, P., Apostolou, A., Agami, R., & Fang, S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m409034200 · Cited by 209 · see citing works
Self-citationSchulze, A., Standera, S., Buerger, E., Kikkert, M., van Voorden, S., Wiertz, E. J. H. J., Koning, F., Kloetzel, P., & Seeger, M. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.10.020 · Cited by 204 · see citing works
Wu, Y., Swulius, M. T., Moremen, K. W., & Sifers, R. N. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1430537100 · Cited by 172 · see citing works
TEB4 is a C4HC3 RING finger-containing ubiquitin ligase of the endoplasmic reticulum
Hassink, G. C., Kikkert, M., van Voorden, S., Lee, S., Spaapen, R. M., van Laar, T., Coleman, C. S., Bartee, E., Früh, K., Chau, V., et al. (2005) · Biochemical Journal · doi:10.1042/bj20041241 · Cited by 172 · see citing works
Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase
Deng, M., & Hochstrasser, M. (2006) · Nature · doi:10.1038/nature05170 · Cited by 161 · see citing works
Ballar, P., Shen, Y., Yang, H., & Fang, S. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m603355200 · Cited by 129 · see citing works
Self-citationYang, H., Zhong, X., Ballar, P., Luo, S., Shen, Y., Rubinsztein, D. C., Monteiro, M. J., & Fang, S. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.10.031 · Cited by 114 · see citing works
Self-citationMbonye, U. R., Wada, M., Rieke, C. J., Tang, H.-Y., DeWitt, D. L., & Smith, W. L. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m608281200 · Cited by 109 · see citing works
The RBCC GeneRFP2(Leu5) Encodes a Novel Transmembrane E3 Ubiquitin Ligase Involved in ERAD
Lerner, M., Corcoran, M., Cepeda, D., Nielsen, M. L., Zubarev, R. A., Pontén, F., Uhlén, M., Hober, S., Grandér, D., & Sangfelt, O. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-03-0248 · Cited by 109 · see citing works
SVIP is a novel VCP/p97-interacting protein whose expression causes cell vacuolation
Nagahama, M., Suzuki, M., Hamada, Y., Hatsuzawa, K., Tani, K., Yamamoto, A., & Tagaya, M. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.02-07-0115 · Cited by 95 · see citing works
Self-citationArteaga, M. F., Wang, L., Ravid, T., Hochstrasser, M., & Canessa, C. M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604816103 · Cited by 85 · see citing works
Shen, Y., Ballar, P., & Fang, S. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.08.173 · Cited by 60 · see citing works
Self-citationNadler, M. J. S., Harrison, M. L., Ashendel, C. L., Cassady, J. M., & Geahlen, R. L. (1993) · Biochemistry · doi:10.1021/bi00086a034 · Cited by 52 · see citing works
ER stress differentially regulates the stabilities of ERAD ubiquitin ligases and their substrates
Shen, Y., Ballar, P., Apostolou, A., Doong, H., & Fang, S. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.11.121 · Cited by 48 · see citing works
Self-citationAlzayady, K. J., Panning, M. M., Kelley, G. G., & Richard Wojcikiewicz, J. H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508890200 · Cited by 47 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Protein Folding and Quality Control in the ERPreprint
Araki, K., & Nagata, K. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a007526 · Cited by 422 · see citing works
Armet, a UPR-upregulated protein, inhibits cell proliferation and ER stress-induced cell death
Apostolou, A., Shen, Y., Liang, Y., Luo, J., & Fang, S. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.05.001 · Cited by 288 · see citing works
Self-citationThe AAA-ATPase p97 is essential for outer mitochondrial membrane protein turnover
Xu, S., Peng, G., Wang, Y., Fang, S., & Karbowski, M. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-09-0748 · Cited by 243 · see citing works
Self-citationControl of p97 function by cofactor binding
Buchberger, A., Schindelin, H., & Hänzelmann, P. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.08.028 · Cited by 219 · see citing works
Martins‐de‐Souza, D., Guest, P. C., Harris, L. W., Vanattou‐Saïfoudine, N., Webster, M. J., Rahmoune, H., & Bahn, S. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.13 · Cited by 202 · see citing works
Mechanisms of substrate processing during ER-associated protein degradation
Christianson, J. C., Jarosch, E., & Sommer, T. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00633-8 · Cited by 189 · see citing works
A Mighty “Protein Extractor” of the Cell: Structure and Function of the p97/CDC48 ATPase
Ye, Y., Tang, W. K., Zhang, T., & Xia, D. (2017) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2017.00039 · Cited by 181 · see citing works
Ubiquilin and p97/VCP bind erasin, forming a complex involved in ERAD
Lim, P. J., Danner, R., Liang, J., Doong, H., Harman, C. A., Srinivasan, D., Rothenberg, C., Wang, H., Ye, Y., Fang, S., et al. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200903024 · Cited by 169 · see citing works
Self-citationStructure and function of the AAA+ ATPase p97/Cdc48p
Xia, D., Tang, W. K., & Ye, Y. (2016) · Gene · doi:10.1016/j.gene.2016.02.042 · Cited by 159 · see citing works
Hänzelmann, P., & Schindelin, H. (2017) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2017.00021 · Cited by 152 · see citing works
Insights into adaptor binding to the AAA protein p97
Yeung, H. O., Kloppsteck, P., Niwa, H., Isaacson, R. L., Matthews, S., Zhang, X., & Freemont, P. S. (2008) · Biochemical Society Transactions · doi:10.1042/bst0360062 · Cited by 139 · see citing works
The evolving role of ubiquitin modification in endoplasmic reticulum-associated degradation
Preston, G. M., & Brodsky, J. L. (2017) · Biochemical Journal · doi:10.1042/bcj20160582 · Cited by 138 · see citing works
Distinct mechanisms controlling rough and smooth endoplasmic reticulum-mitochondria contacts
Wang, P. T. C., Garcin, P. O., Fu, M., Masoudi, M., St-Pierre, P., Panté, N., & Nabi, I. R. (2015) · Journal of Cell Science · doi:10.1242/jcs.171132 · Cited by 111 · see citing works
Fairbank, M., St-Pierre, P., & Nabi, I. R. (2009) · Molecular BioSystems · doi:10.1039/b820820b · Cited by 88 · see citing works
Chiarelli, N., Ritelli, M., Zoppi, N., & Colombi, M. (2019) · Genes · doi:10.3390/genes10080609 · Cited by 82 · see citing works
AAA ATPase p97/VCP: cellular functions, disease and therapeutic potential
Vij, N. (2008) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2008.00462.x · Cited by 82 · see citing works
Hänzelmann, P., & Schindelin, H. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.274506 · Cited by 80 · see citing works
Dargemont, C., & Ossareh‐Nazari, B. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.07.011 · Cited by 76 · see citing works
New ATPase regulators—p97 goes to the PUB
Madsen, L., Seeger, M., Semple, C. A. M., & Hartmann‐Petersen, R. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.05.017 · Cited by 72 · see citing works
Differential regulation of CFTRΔF508 degradation by ubiquitin ligases gp78 and Hrd1
Ballar, P., Örs, A. U., Yang, H., & Fang, S. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.10.005 · Cited by 71 · see citing works
Self-citationThe complexities of p97 function in health and disease
Chapman, E., Fry, A. N., & Kang, M. (2010) · Molecular BioSystems · doi:10.1039/c0mb00176g · Cited by 67 · see citing works
Stapf, C., Cartwright, E. J. P., Bycroft, M., Hofmann, K., & Buchberger, A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.274472 · Cited by 65 · see citing works
Bao, D., Cheng, C., Lan, X., Xing, R., Chen, Z., Zhao, H., Sun, J., Wang, Y., Niu, C., Zhang, B., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.15509 · Cited by 63 · see citing works
Self-citationBraxton, J. R., & Southworth, D. R. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.105182 · Cited by 61 · see citing works
Gp78 E3 Ubiquitin Ligase: Essential Functions and Contributions in Proteostasis
Joshi, V., Upadhyay, A., Kumar, A., & Mishra, A. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00259 · Cited by 61 · see citing works
Chu, S., Xie, X., Payan, C., & Stochaj, U. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00639-y · Cited by 58 · see citing works
Erzurumlu, Y., & Ballar, P. (2017) · Scientific Reports · doi:10.1038/srep40719 · Cited by 57 · see citing works
Self-citationTargeting p97 to Disrupt Protein Homeostasis in Cancer
Vekaria, P., Home, T., Weir, S. J., Schoenen, F. J., & Rao, R. (2016) · Frontiers in Oncology · doi:10.3389/fonc.2016.00181 · Cited by 56 · see citing works
Clearance of RhodopsinP23H aggregates requires the ERAD effector VCP
Griciuc, A., Aron, L., Piccoli, G., & Ueffing, M. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.01.008 · Cited by 50 · see citing works
Exploring the proteasome system: A novel concept of proteasome inhibition and regulation
Wang, X., Meul, T., & Meiners, S. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107526 · Cited by 50 · see citing works
SVIP is a molecular determinant of lysosomal dynamic stability, neurodegeneration and lifespan
Johnson, A. E., Orr, B. O., Fetter, R. D., Moughamian, A. J., Primeaux, L. A., Geier, E. G., Yokoyama, J. S., Miller, B. L., & Davis, G. W. (2021) · Nature Communications · doi:10.1038/s41467-020-20796-8 · Cited by 46 · see citing works
SVIP Induces Localization of p97/VCP to the Plasma and Lysosomal Membranes and Regulates Autophagy
Wang, Y., Ballar, P., Zhong, Y., Zhang, X., Liu, C., Zhang, Y., Monteiro, M. J., Li, J., & Fang, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024478 · Cited by 45 · see citing works
Self-citationSun, X., & Qiu, H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113842 · Cited by 42 · see citing works
Hwang, J., Walczak, C. P., Shaler, T. A., Olzmann, J. A., Zhang, L., Elias, J. E., & Kopito, R. R. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.785055 · Cited by 43 · see citing works
Morreale, G., Conforti, L., Coadwell, J., Wilbrey, A. L., & Coleman, M. P. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2008.06858.x · Cited by 43 · see citing works
Chen, Z., Du, S., & Fang, S. (2012) · Current Protein and Peptide Science · doi:10.2174/138920312802430590 · Cited by 36 · see citing works
Self-citationChiarelli, N., Carini, G., Zoppi, N., Ritelli, M., & Colombi, M. (2019) · PLOS ONE · doi:10.1371/journal.pone.0211647 · Cited by 35 · see citing works
UBXD1 is a VCP-interacting protein that is involved in ER-associated degradation
Nagahama, M., Ohnishi, M., Kawate, Y., Matsui, T., Miyake, H., Yuasa, K., Tani, K., Tagaya, M., & Tsuji, A. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.03.012 · Cited by 33 · see citing works
Self-citationSoetandyo, N., & Ye, Y. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.131649 · Cited by 34 · see citing works
Live Cell Imaging of Protein Dislocation from the Endoplasmic Reticulum
Zhong, Y., & Fang, S. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.381798 · Cited by 33 · see citing works
Self-citationRegulation of ER-associated degradation via p97/VCP-interacting motif
Ballar, P., & Fang, S. (2008) · Biochemical Society Transactions · doi:10.1042/bst0360818 · Cited by 32 · see citing works
Self-citationZhong, Y., Wang, Y., Yang, H., Ballar, P., Lee, J., Ye, Y., Monteiro, M. J., & Fang, S. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.272906 · Cited by 30 · see citing works
Self-citationThe AAA-ATPase p97 facilitates degradation of apolipoprotein B by the ubiquitin-proteasome pathway
Fisher, E. A., Lapierre, L. R., Junkins, R. D., & McLeod, R. S. (2008) · Journal of Lipid Research · doi:10.1194/jlr.m800108-jlr200 · Cited by 29 · see citing works
Zhong, Y., Shen, H., Wang, Y., Yang, Y., Yang, P., & Fang, S. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.01.133 · Cited by 27 · see citing works
Self-citationSubstrate Insolubility Dictates Hsp104-Dependent Endoplasmic-Reticulum-Associated Degradation
Preston, G. M., Guerriero, C. J., Metzger, M. B., Michaelis, S., & Brodsky, J. L. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.03.016 · Cited by 26 · see citing works
Peripheral Endoplasmic Reticulum Localization of Gp78 Ubiquitin Ligase Activity
St-Pierre, P., Dang, T. T. P., Joshi, B., & Nabi, I. R. (2012) · Journal of Cell Science · doi:10.1242/jcs.096396 · Cited by 25 · see citing works
Llinàs‐Arias, P., Rosselló-Tortella, M., López-Serra, P., Pérez-Salvia, M., Setién, F., Marín, S., Muñoz, J. P., Junza, A., Capellades, J., Calleja-Cervantes, M. E., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.125888 · Cited by 24 · see citing works
Tiwari, S., Siddiqi, S., Zhelyabovska, O., & Siddiqi, S. A. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.705269 · Cited by 24 · see citing works
Liu, S., Fu, Q., Zhao, J., & Hu, H. (2013) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2013.09.021 · Cited by 22 · see citing works
Yahiro, K., Tsutsuki, H., Ogura, K., Nagasawa, S., Moss, J., & Noda, M. (2012) · Infection and Immunity · doi:10.1128/iai.06164-11 · Cited by 22 · see citing works
Erzurumlu, Y., & Muhammed, M. T. (2023) · Cellular Signalling · doi:10.1016/j.cellsig.2023.110745 · Cited by 21 · see citing works
Structural and functional deviations in disease-associated p97 mutants
Tang, W. K., & Xia, D. (2012) · Journal of Structural Biology · doi:10.1016/j.jsb.2012.04.024 · Cited by 20 · see citing works
Ebrahimi, A., Jung, M.-H., Dreyfuss, J., Pan, H., Sgroi, D., Bonner-Weir, S., & Weir, G. (2017) · Islets · doi:10.1080/19382014.2017.1283083 · Cited by 18 · see citing works
Structure and expression of a novel compact myelin protein – Small VCP-interacting protein (SVIP)
Wu, J., Peng, D., Voehler, M., Sanders, C. R., & Li, J. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.09.056 · Cited by 19 · see citing works
Chen, Z., Zhong, Y., Wang, Y., Xu, S., Liu, Z., Baskakov, I. V., Monteiro, M. J., Karbowski, M., Shen, Y., & Fang, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073482 · Cited by 18 · see citing works
Self-citationAkcan, G., Alimoğulları, E., Abu‐Issa, R., & Çaylı, S. (2020) · Reproductive Biology · doi:10.1016/j.repbio.2020.01.006 · Cited by 17 · see citing works
UBXN2A regulates nicotinic receptor degradation by modulating the E3 ligase activity of CHIP
Teng, Y., Rezvani, K. S., & Biasi, M. D. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.08.084 · Cited by 17 · see citing works
You, H., Wen, X., Wang, X., Zhu, C., Chen, H., Bu, L., Zhang, J., & Qu, S. (2023) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2023.07.026 · Cited by 15 · see citing works
SVIP regulates Z variant alpha-1 antitrypsin retro-translocation by inhibiting ubiquitin ligase gp78
Khodayari, N., Wang, R. L., Marek, G. W., Krotova, K. Y., Kirst, M. E., Liu, C., Rouhani, F. N., & Brantly, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172983 · Cited by 12 · see citing works
İlhan, R., Üner, G., Yılmaz, S., Şahar, E. A., Çaylı, S., Erzurumlu, Y., Gözen, O., & Ballar, P. (2022) · Scientific Reports · doi:10.1038/s41598-022-04821-y · Cited by 11 · see citing works
Self-citationErzurumlu, Y., Doğan, H. K., & Çataklı, D. (2023) · Steroids · doi:10.1016/j.steroids.2023.109238 · Cited by 10 · see citing works
Zheng, X., Li, A., Qiu, J., Yan, G., Ji, Y., & Wang, G. (2024) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2024.135301 · Cited by 10 · see citing works
Endoplasmic Reticulum-Associated Degradation (ERAD)
Tepedelen, B. E., & Ballar, P. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.82043 · Cited by 10 · see citing works
Self-citationLiu, D., Hong, Z., Gui, L., Zhao, L., Zhou, W., Wang, Y., Sun, S., & Li, M. (2023) · Biomolecules · doi:10.3390/biom13030460 · Cited by 8 · see citing works
Çaylı, S., Alimoğulları, E., Pişkin, İ., Bilginoğlu, A., & Nakkaş, H. (2021) · Journal of Molecular Histology · doi:10.1007/s10735-021-10013-1 · Cited by 7 · see citing works
Turnover of EDEM1 , an ERAD ‐enhancing factor, is mediated by multiple degradation routes
Katsuki, R., Kanuka, M., Ohta, R., Yoshida, S., & Tamura, T. (2024) · Genes to Cells · doi:10.1111/gtc.13117 · Cited by 5 · see citing works
Adapter-mediated Substrate Selection for Endoplasmic Reticulum-associated Degradation
Corcoran, K., Wang, X., & Lybarger, L. P. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808258200 · Cited by 6 · see citing works
Fatty links between multisystem proteinopathy and small VCP-interacting protein
Ramzan, F., Kumar, A., Abrar, F., Gray, R. A. V., Campbell, Z. E., Liao, L. M. Q., Dang, A., Akanni, O., Guyn, C., & Martin, D. D. O. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-02118-9 · Cited by 5 · see citing works
Nguyen, Q.-A. T., Choi, J., Yang, J. K., & Lee, S. Y. (2019) · Biochemical Journal · doi:10.1042/bcj20190254 · Cited by 4 · see citing works
Şahar, E. A., & Ballar, P. (2023) · Cells · doi:10.3390/cells12101362 · Cited by 4 · see citing works
Self-citationAlimoğulları, E., & Çaylı, S. (2024) · TURKISH JOURNAL OF MEDICAL SCIENCES · doi:10.55730/1300-0144.5894 · Cited by 5 · see citing works
Alimoğulları, E., Akcan, G., Arı, O., & Çaylı, S. (2022) · Molecular Biology Reports · doi:10.1007/s11033-022-07740-3 · Cited by 3 · see citing works
Proteomics Analysis of Pregnancy in Ewes under Heat Stress Conditions and Melatonin Administration
Bouroutzika, E. V., Proikakis, S., Theodosiadou, E. K., Vougas, K. N., Katsafadou, A. I., Tsangaris, G. T., & Valasi, I. (2024) · Animals · doi:10.3390/ani14030400 · Cited by 2 · see citing works
Braxton, J. R., Altobelli, C. R., Tucker, M. R., Tse, E., Thwin, A. C., Arkin, M. R., & Southworth, D. R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.15.540864 · Cited by 2 · see citing works
The immunoexpression of valosin‐containing protein and small VCP ‐interacting protein in rat ovaries
Kartal, B., Alimoğulları, E., & Çaylı, S. (2023) · Anatomia Histologia Embryologia · doi:10.1111/ahe.12914 · Cited by 1 · see citing works
Arıcı, A., & Erdemır, F. (2023) · Medicina · doi:10.3390/medicina59061079 · Cited by 1 · see citing works
Sekhar, V., Andl, T., & Siddiqi, S. A. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26157465 · Cited by 1 · see citing works
Chen, Z., Zhong, Y., Wang, Y., Xu, S., Liu, Z., Baskakov, I. V., Monteiro, M. J., Karbowski, M., Shen, Y., & Fang, S. (2013) · PLoS ONE · doi:10.1371/annotation/65881dc3-5bce-4f0b-9060-7079e16b1877 · Cited by 1 · see citing works
Self-citationYamanishi, H. (1998) · International Journal of Molecular Medicine · doi:10.3892/ijmm_00000001
The p97 ATPase and the Drosophila Proteasome : Protein Unfolding and Regulation
Grimberg, K. B. (2010)
Li, L. (2015) · cIRcle (University of British Columbia) · doi:10.14288/1.0167674
Wang, P. T. C. (2015) · cIRcle (University of British Columbia) · doi:10.14288/1.0166455
Tiwari, S. (2013) · Journal of International Crisis and Risk Communication Research
Şahar, E. A., & Ballar, P. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.03.530947
Self-citationAlimoğulları, E., & Kartal, B. (2024) · Uludağ Üniversitesi Tıp Fakültesi Dergisi · doi:10.32708/uutfd.1524387
Alimoğulları, E., Kartal, B., Bozkurt, M. F., Demir, H., Saçık, U., & Bhaya, M. N. (2024) · Turkish Journal of Biochemistry · doi:10.1515/tjb-2024-0154
Kartal, B., Alimoğulları, E., & Çaylı, S. (2025) · Pathology - Research and Practice · doi:10.1016/j.prp.2025.155929
Regulation of hepatic ER stress by the E3 ubiquitin ligase gp78 in zebrafish
Chen, Z. (2012) · University Libraries (University of Maryland)
Processes and therapeutic perspectives of acylation modifications of lysine and cysteine in tumors
Jiang, J., Chen, J., Huang, S., Tian, Y., Liu, L., Yao, J., Zhang, Y., Jiang, C., Zhang, X., Han, N., et al. (2026) · Cell Communication and Signaling · doi:10.1186/s12964-026-02707-4
VCP at the crossroads of UPS and autophagy in cancer
Hitchman, C. J., Phillips, J. I., Park, H.-W., & Lu, H. (2026) · Genes & Diseases · doi:10.1016/j.gendis.2026.102264
Lu, G., Shan, H., Yin, Y., Chen, L., Yu, K., Wei, Z. H., Chen, H., Hu, L. X., Qi, Y., Wu, T., et al. (2026) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2026.1781331
Alimoğulları, E., Kartal, B., Pişkin, İ., KARATAY, M., & Saçık, U. (2026) · European Journal of Therapeutics · doi:10.58600/eurjther3030
- Authors
- Ballar, P., Zhong, Y., Nagahama, M., Tagaya, M., Shen, Y., & Fang, S.
- Affiliations
- University of Maryland, Baltimore (US)
- Tokushima University (JP)
- Tokyo University of Pharmacy and Life Sciences (JP)
- Corresponding author
- Fang, Shengyun
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2007-11
- Volume
- 282
- Issue
- 47
- Pages
- 33908-33914
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2073337768
- Cited by
- 93
- References
- 37
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 7 · 2023: 12 · 2022: 2 · 2021: 2 · 2020: 3 · 2019: 5 · 2018: 1 · 2017: 9 · 2016: 3 · 2015: 6 · 2013: 6 · 2012: 7
- FWCI
- 2.34
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institute of General Medical Sciences (R01-GM69967, R01GM069967)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- ER-associated degradation, gp78, VCP/p97, protein misfolding, ubiquitination, retrotranslocation, proteasomal degradation, protein complex formation, myristoylation, calnexin, endoplasmic reticulum
- MeSH terms
- Valosin Containing Protein, Adenosine Triphosphatases, alpha 1-Antitrypsin, Carrier Proteins, Cell Line, Endoplasmic Reticulum, Humans, Membrane Proteins, Nuclear Proteins, Protein Processing, Post-Translational, CD3 Complex, Protein Folding, Receptors, Cytokine, Cell Cycle Proteins, Gene Silencing, Phosphate-Binding Proteins, Calnexin, Ubiquitin-Protein Ligases, Proteasome Endopeptidase Complex, Ubiquitination, Receptors, Autocrine Motility Factor, Proteasome Inhibitors
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