A role for a lithium-inhibited Golgi nucleotidase in skeletal development and sulfation
Open accessAbstract
Sulfation is an important biological process that modulates the function of numerous molecules. It is directly mediated by cytosolic and Golgi sulfotransferases, which use 3′-phosphoadenosine 5′-phosphosulfate to produce sulfated acceptors and 3′-phosphoadenosine 5′-phosphate (PAP). Here, we identify a Golgi-resident PAP 3′-phosphatase (gPAPP) and demonstrate that its activity is potently inhibited by lithium in vitro . The inactivation of gPAPP in mice led to neonatal lethality, lung abnormalities resembling atelectasis, and dwarfism characterized by aberrant cartilage morphology. The phenotypic similarities of gPAPP mutant mice to chondrodysplastic models harboring mutations within components of the sulfation pathway lead to the discovery of undersulfated chondroitin in the absence of functional enzyme. Additionally, we observed loss of gPAPP leads to perturbations in the levels of heparan sulfate species in lung tissue and whole embryos. Our data are consistent with a model that clearance of the nucleotide product of sulfotransferases within the Golgi plays an important role in glycosaminoglycan sulfation, provide a unique genetic basis for chondrodysplasia, and define a function for gPAPP in the formation of skeletal elements derived through endochondral ossification.
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?
Lithium treatment was shown in rodents to facilitate enzymatic CSPG digestion.
“lithium treatment was shown in rodents to facilitate enzymatic CSPG digestion.71, 72”
From Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala (2015) · cites this paper as [72]
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
Theory and Practice of Histological Techniques
Bancroft, J. D., & Gamble, M. (1990) · Cited by 6,986 · see citing works
Theory and Practice of Histological Techniques
Warren, B. A. (1996) · Pathology · doi:10.1016/s0031-3025(16)35146-7 · Cited by 1,572 · 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
Hallcher, L. M., & Sherman, W. R. (1980) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)70391-3 · Cited by 1,102 · see citing works
Goldring, M. B., Tsuchimochi, K., & Ijiri, K. (2005) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20652 · Cited by 1,062 · see citing works
Human Sulfotransferases and Their Role in Chemical Metabolism
Gamage, N., Barnett, A., Hempel, N., Duggleby, R. G., Windmill, K. F., Martin, J. L., & McManus, M. E. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfj061 · Cited by 703 · see citing works
Knudson, C. B., & Knudson, W. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0243 · Cited by 601 · see citing works
Sulfation patterns of glycosaminoglycans encode molecular recognition and activity
Gama, C. I., Tully, S. E., Sotogaku, N., Clark, P. M., Rawat, M., Vaidehi, N., Goddard, W. A., Nishi, A., & Hsieh‐Wilson, L. C. (2006) · Nature Chemical Biology · doi:10.1038/nchembio810 · Cited by 561 · see citing works
Molecular Targets of Lithium Action
Phiel, C. J., & Klein, P. S. (2001) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.41.1.789 · Cited by 513 · see citing works
Sulfonation and molecular action
Strott, C. A. (2002) · Endocrine Reviews · doi:10.1210/er.2001-0040 · Cited by 487 · see citing works
Transcriptional control of chondrocyte fate and differentiation
Lefebvre, V., & Smits, P. J. (2005) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20048 · Cited by 477 · see citing works
Functional analysis of secreted and transmembrane proteins critical to mouse development.
Mitchell, K. J., Pinson, K. I., Kelly, O. G., Brennan, J., Zupicich, J., Scherz, P., Leighton, P. A., Goodrich, L. V., Lu, X., Avery, B. J., et al. (2001) · Nature Genetics · doi:10.1038/90074 · Cited by 400 · see citing works
Defining brain wiring patterns and mechanisms through gene trapping in mice
Leighton, P. A., Mitchell, K. J., Goodrich, L. V., Lu, X., Pinson, K. I., Scherz, P., Skarnes, W. C., & Tessier‐Lavigne, M. (2001) · Nature · doi:10.1038/35065539 · Cited by 391 · see citing works
Hirschberg, C. B., Robbins, P. W., & Abeijón, C. (1998) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.67.1.49 · Cited by 385 · see citing works
The new bone biology: Pathologic, molecular, and clinical correlates
Cohen, M. M. (2006) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.31368 · Cited by 332 · see citing works
Biosynthesis of Chondroitin/Dermatan Sulfate
Silbert, J. E., & Sugumaran, G. (2002) · IUBMB Life · doi:10.1080/15216540214923 · Cited by 330 · see citing works
Sulfotransferases in glycosaminoglycan biosynthesis
Kusche‐Gullberg, M. (2003) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2003.08.002 · Cited by 314 · see citing works
Heparan Sulfate Structure in Mice with Genetically Modified Heparan Sulfate Production
Ledin, J., Staatz, W. D., Li, J.-P., Götte, M., Selleck, S. B., Kjellén, L., & Spillmann, D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405382200 · Cited by 257 · see citing works
Lithium toxicity in yeast is due to the inhibition of RNA processing enzymes
Dichtl, B., Stevens, A., & Tollervey, D. (1997) · The EMBO Journal · doi:10.1093/emboj/16.23.7184 · Cited by 256 · see citing works
Ringvall, M., Ledin, J., Holmborn, K., Kuppevelt, T. H. V., Ellin, F., Eriksson, I., Olofsson, A.-M., Kjellén, L., & Forsberg, E. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.c000359200 · Cited by 244 · see citing works
Gould, T. D., Quiroz, J. A., Singh, J. B., Zarate, C. A., & Manji, H. K. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001518 · Cited by 238 · see citing works
Mutations in orthologous genes in human spondyloepimetaphyseal dysplasia and the brachymorphic mouse
Haque, M. F. U., King, L. M., Krakow, D., Cantor, R. M., Rusiniak, M. E., Swank, R. T., Superti‐Furga, A., Haque, S., Abbas, H., Ahmad, W., et al. (1998) · Nature Genetics · doi:10.1038/2458 · Cited by 217 · see citing works
MacArthur, J. M., Bishop, J. R., Stanford, K. I., Wang, L., Bensadoun, A., Witztum, J. L., & Esko, J. D. (2007) · Journal of Clinical Investigation · doi:10.1172/jci29154 · Cited by 216 · see citing works
Lithium and bipolar mood disorder: the inositol-depletion hypothesis revisited
Harwood, A. J. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001618 · Cited by 208 · see citing works
A Salt-Sensitive 3′(2′),5′-Bisphosphate Nucleotidase Involved in Sulfate Activation
Murguía, J. R., Bellés, J. M., & Serrano, R. (1995) · Science · doi:10.1126/science.7809627 · Cited by 203 · see citing works
Klüppel, M., Wight, T. N., Chan, C. K., Hinek, A., & Wrana, J. L. (2005) · Development · doi:10.1242/dev.01948 · Cited by 198 · see citing works
Thiele, H., Sakano, M., Kitagawa, H., Sugahara, K., Rajab, A., Höhne, W., Ritter, H., Leschik, G., Nürnberg, P., & Mundlos, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400334101 · Cited by 190 · see citing works
Cerebral hypoplasia and craniofacial defects in mice lacking heparan sulfate Ndst1 gene function
Grobe, K., Inatani, M., Pallerla, S. R., Castagnola, J., Yamaguchi, Y., & Esko, J. D. (2005) · Development · doi:10.1242/dev.01935 · Cited by 184 · see citing works
Mundlos, S., & Olsen, B. R. (1997) · The FASEB Journal · doi:10.1096/fasebj.11.2.9039954 · Cited by 179 · see citing works
Fan, G., Xiao, L., Cheng, L., Wang, X., Sun, B., & Hu, G. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01111-x · Cited by 165 · see citing works
York, J. D., Ponder, J. W., & Majerus, P. W. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.11.5149 · Cited by 159 · see citing works
Self-citationMundlos, S., & Olsen, B. R. (1997) · The FASEB Journal · doi:10.1096/fasebj.11.4.9068611 · Cited by 158 · see citing works
A member of a family of sulfate-activating enzymes causes murine brachymorphism
Kurima, K., Warman, M. L., Krishnan, S., Domowicz, M. S., Krueger, R. C., Deyrup, A. T., & Schwartz, N. B. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.15.8681 · Cited by 156 · see citing works
Capasso, J. M., & Hirschberg, C. B. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.22.7051 · Cited by 148 · see citing works
Molecular-pathogenetic classification of genetic disorders of the skeleton
Superti‐Furga, A., Bonafé, L., & Rimoin, D. L. (2001) · American Journal of Medical Genetics · doi:10.1002/ajmg.10233 · Cited by 146 · see citing works
Lawrence, R., Lu, H., ROSENBERG, R. D., Esko, J. D., & Zhang, L. (2008) · Nature Methods · doi:10.1038/nmeth0408-291 · Cited by 146 · see citing works
Gläser, H.-U., Thomas, D., Gaxiola, R. A., Montrichard, F., Surdin-Kerjan, Y., & Serrano, R. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb05979.x · Cited by 141 · see citing works
Frederick, J. P., Mattiske, D., Wofford, J. A., Megosh, L. C., Drake, L. Y., Chiou, S.-T., Hogan, B. L. M., & York, J. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503706102 · Cited by 139 · see citing works
Self-citationForlino, A. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi079 · Cited by 137 · see citing works
Inhorn, R. C., & Majerus, P. W. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47680-6 · Cited by 129 · see citing works
Chondrodysplasias due to proteoglycan defects
Schwartz, N. B., & Domowicz, M. S. (2002) · Glycobiology · doi:10.1093/glycob/12.4.57r · Cited by 129 · see citing works
Evolution of carbohydrate antigens—microbial forces shaping host glycomes?
Bishop, J. R., & Gagneux, P. (2007) · Glycobiology · doi:10.1093/glycob/cwm005 · Cited by 126 · see citing works
Cellular functions of proteoglycans—an overview
Perrimon, N., & Bernfield, M. R. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0237 · Cited by 125 · see citing works
Sulfotransferases and sulfated oligosaccharides
Honke, K., & Taniguchi, N. (2002) · Medicinal Research Reviews · doi:10.1002/med.10020 · Cited by 121 · see citing works
Properties of inositol polyphosphate 1-phosphatase.
Inhorn, R. C., & Majerus, P. W. (1988) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)68256-0 · Cited by 89 · see citing works
Spiegelberg, B. D., Xiong, J.-P., Smith, J. J., Gu, R. F., & York, J. D. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.19.13619 · Cited by 84 · see citing works
Self-citationLópez-Coronado, J., Bellés, J. M., Lesage, F., Serrano, R., & Rodrı́guez, P. L. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.23.16034 · Cited by 68 · see citing works
Mandon, E. C., Milla, M. E., Kempner, E. S., & Hirschberg, C. B. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.22.10707 · Cited by 61 · see citing works
Allison, J. H., Boshans, R. L., Hallcher, L. M., Packman, P. M., & Sherman, W. R. (1980) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1980.tb06619.x · Cited by 60 · see citing works
Acharya, J., Labarca, P. P., Delgado, R., Jalink, K., & Zuker, C. S. (1998) · Neuron · doi:10.1016/s0896-6273(00)80502-4 · Cited by 59 · see citing works
Mouse models of abnormal skeletal development and homeostasis
McLean, W., & Olsen, B. R. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02458-1 · Cited by 58 · see citing works
Inhibition of M and P Phenol Sulfotransferase by Analogues of 3′‐Phosphoadenosine‐5′‐Phosphosulfate
Rens‐Domiano, S., & Roth, J. A. (1987) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1987.tb05679.x · Cited by 47 · see citing works
JAWS coordinates chondrogenesis and synovial joint positioning
Sohaskey, M. L., Yu, J. A., Diaz, M. A., Plaas, A., & Harland, R. M. (2008) · Development · doi:10.1242/dev.019950 · Cited by 45 · see citing works
Scheijen, B., Bronk, M., van der Meer, T., & Bernards, R. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.10.3656-3668.2003 · Cited by 45 · see citing works
A high-throughput induction gene trap approach defines C4ST as a target of BMP signaling
Klüppel, M., Vallis, K. A., & Wrana, J. L. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00198-3 · Cited by 37 · see citing works
Kinetics of PAPS Translocase: Evidence for an Antiport Mechanism
Ozeran, J. D., WESTLEY, J. W., & Schwartz, N. B. (1996) · Biochemistry · doi:10.1021/bi951302u · Cited by 33 · see citing works
Alteration of Lithium Pharmacology through Manipulation of Phosphoadenosine Phosphate Metabolism
Spiegelberg, B. D., Cruz-Racelis, J. D., Law, T.-H., & York, J. D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407890200 · Cited by 33 · see citing works
Self-citation(2')3',5'-Bisphosphate nucleotidase.
Ramaswamy, S. G., & Jakoby, W. B. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)61072-5 · Cited by 25 · see citing works
The evolving definition of a chondrodysplasia?
Horton, W. A. (2003) · Fetal and Pediatric Pathology · doi:10.1080/pdp.22.1.47.52 · Cited by 6 · see citing works
Flagged first, then by citations
1 of the 60 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Kusche-Gullberg M, Kjellen L (2003) Sulfotransferases in glycosaminoglycan biosyn- thesis. Curr Opin Struct Biol 13:605-611.
Cited by
Sorted by citations
The Regulation of Steroid Action by Sulfation and Desulfation
Mueller, J. W., Gilligan, L. C., Idkowiak, J., Arlt, W., & Foster, P. A. (2015) · Endocrine Reviews · doi:10.1210/er.2015-1036 · Cited by 419 · see citing works
Heparan Sulfate: Biosynthesis, Structure, and Function
Li, J.-P., & Kusche‐Gullberg, M. (2016) · International review of cytology · doi:10.1016/bs.ircmb.2016.02.009 · Cited by 302 · see citing works
Chapter 3 Interactions Between Heparan Sulfate and Proteins—Design and Functional Implications
Lindahl, U., & Li, J. (2009) · International review of cytology · doi:10.1016/s1937-6448(09)76003-4 · Cited by 274 · see citing works
Cortes, M., Baria, A. T., & Schwartz, N. B. (2009) · Development · doi:10.1242/dev.030742 · Cited by 167 · see citing works
Validating GSK3 as an in vivo target of lithium action
O'Brien, W. T., & Klein, P. S. (2009) · Biochemical Society Transactions · doi:10.1042/bst0371133 · Cited by 157 · see citing works
Pantazopoulos, H., Markota, M., Jaquet, F., Ghosh, D., Wallin, A., Santos, A., Caterson, B., & Berretta, S. (2015) · Translational Psychiatry · doi:10.1038/tp.2014.128 · Cited by 153 · see citing works
Sulfation pathways from red to green
Günal, S., Hardman-Kavanaugh, R. E., Kopřiva, S., & Mueller, J. W. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.rev119.007422 · Cited by 117 · see citing works
In Sickness and in Health: Perineuronal Nets and Synaptic Plasticity in Psychiatric Disorders
Pantazopoulos, H., & Berretta, S. (2015) · Neural Plasticity · doi:10.1155/2016/9847696 · Cited by 118 · see citing works
Regulation of coenzyme A levels by degradation: the ‘Ins and Outs’
Naquet, P., Kerr, E. W., Vickers, S. D., & Leonardi, R. (2020) · Progress in Lipid Research · doi:10.1016/j.plipres.2020.101028 · Cited by 115 · see citing works
Vissers, L. E. L. M., Lausch, E. U., Unger, S., Campos‐Xavier, B., Gilissen, C., Rossi, A., del Rosario, M., Venselaar, H., Knoll, U., Nampoothiri, S., et al. (2011) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2011.04.002 · Cited by 100 · see citing works
Chondroitin sulfate synthase 1 (Chsy1) is required for bone development and digit patterning
Wilson, D. G., Phamluong, K., Lin, W. Y., Barck, K. H., Carano, R. A. D., Diehl, L. J., Peterson, A. S., Martin, F., & Solloway, M. J. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.01.005 · Cited by 94 · see citing works
Secondary sulfur metabolism in cellular signalling and oxidative stress responses
Chan, K. X., Phua, S. Y., & Breusegem, F. V. (2019) · Journal of Experimental Botany · doi:10.1093/jxb/erz119 · Cited by 93 · see citing works
Bozzelli, P. L., Alaiyed, S., Kim, E., Villapol, S., & Conant, K. E. (2018) · Neural Plasticity · doi:10.1155/2018/5735789 · Cited by 90 · see citing works
Molecular signature of extracellular matrix pathology in schizophrenia
Pantazopoulos, H., Katsel, P., Haroutunian, V. H., Chelini, G., Klengel, T., & Berretta, S. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.15009 · Cited by 79 · see citing works
Ashrafizadeh, M., Mirzaei, S., Hushmandi, K., Rahmanian, V., Zabolian, A., Raei, M., Farahani, M. V., Goharrizi, M. A. S. B., Khan, H. Z., Zarrabi, A., et al. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119649 · Cited by 80 · see citing works
Paganini, C., Costantini, R., Superti‐Furga, A., & Rossi, A. (2019) · FEBS Journal · doi:10.1111/febs.14984 · Cited by 70 · see citing works
Carlsson, P., & Kjellén, L. (2011) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-23056-1_2 · Cited by 64 · see citing works
UDP xylose synthase 1 is required for morphogenesis and histogenesis of the craniofacial skeleton
Eames, B. F., Singer, A., Smith, G. A., Wood, Z. A., Yan, Y., He, X., Polizzi, S. J., Catchen, J., Rodríguez‐Marí, A., Linbo, T. H., et al. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.02.035 · Cited by 63 · see citing works
Biosynthesis of glycosaminoglycans: associated disorders and biochemical tests
Sasarman, F., Maftei, C., Campeau, P. M., Brunel‐Guitton, C., Mitchell, G. A., & Allard, P. (2015) · Journal of Inherited Metabolic Disease · doi:10.1007/s10545-015-9903-z · Cited by 59 · see citing works
Hui, W., Litherland, G. J., Jefferson, M. A., Barter, M. J., Elias, M. S., Cawston, T. E., Rowan, A. D., & Young, D. A. (2010) · Lara D. Veeken · doi:10.1093/rheumatology/keq217 · Cited by 57 · see citing works
Human genetic disorders and knockout mice deficient in glycosaminoglycan
Mizumoto, S., Yamada, S., & Sugahara, K. (2014) · BioMed Research International · doi:10.1155/2014/495764 · Cited by 54 · see citing works
Osteopotentia regulates osteoblast maturation, bone formation, and skeletal integrity in mice
Sohaskey, M. L., Jiang, Y., Zhao, J. J., Mohr, A., Roemer, F. W., & Harland, R. M. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201003006 · Cited by 54 · see citing works
Congenital Disorders of Deficiency in Glycosaminoglycan Biosynthesis
Mizumoto, S., & Yamada, S. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.717535 · Cited by 55 · see citing works
van den Boom, J., Heider, D., Martin, S. R., Pastore, A., & Mueller, J. W. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.325498 · Cited by 50 · see citing works
Chan, W. L., Steiner, M., Witkos, T. M., Egerer, J., Busse, B., Mizumoto, S., Pestka, J. M., Zhang, H., Haußer, I., Khayal, L. A., et al. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007242 · Cited by 49 · see citing works
From direct to indirect lithium targets: a comprehensive review of omics data
Roux-Rouquié, M., & Dosseto, A. (2017) · Metallomics · doi:10.1039/c7mt00203c · Cited by 48 · see citing works
Gualeni, B., Facchini, M., Leonardis, F. D., Tenni, R., Cetta, G., Viola, M., Passi, A. G., Superti‐Furga, A., Forlino, A., & Rossi, A. (2010) · Matrix Biology · doi:10.1016/j.matbio.2010.05.001 · Cited by 48 · see citing works
Enhanced Endothelial Cell Senescence by Lithium-induced Matrix Metalloproteinase-1 Expression
Struewing, I. T., Durham, S. N., Barnett, C. D., & Mao, C. D. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.001735 · Cited by 47 · see citing works
Zheng, C., Lin, X., Xu, X., Wang, C., Zhou, J., Gao, B., Fan, J., Lu, W., Hu, Y., Jie, Q., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.01.010 · Cited by 45 · see citing works
IMPAD1 and KDELR2 drive invasion and metastasis by enhancing Golgi-mediated secretion
Bajaj, R., Kundu, S. T., Grzeskowiak, C. L., Fradette, J. J., Scott, K. L., Creighton, C. J., & Gibbons, D. L. (2020) · Oncogene · doi:10.1038/s41388-020-01410-z · Cited by 41 · see citing works
Mizumoto, S., & Yamada, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.764781 · Cited by 41 · see citing works
Skeletal Dysplasias Caused by Sulfation Defects
Paganini, C., Tota, C. G., Superti‐Furga, A., & Rossi, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082710 · Cited by 39 · see citing works
Wang, H., Chen, R. B., Zhang, S. N., & Zhang, R. F. (2022) · BMC Genomics · doi:10.1186/s12864-021-08188-8 · Cited by 34 · see citing works
IMPAD1 mutations in two Catel‐Manzke like patients
Nizon, M., Alanay, Y., Tüysüz, B., Şimşek‐Kiper, P. Ö., Geneviève, D., Sillence, D. O., Huber, C., Münnich, A., & Cormier‐Daire, V. (2012) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.35504 · Cited by 30 · see citing works
Thompson, C. L., Yasmin, H., Varone, A., Wiles, A. K., Poole, C. A., & Knight, M. M. (2015) · Journal of Orthopaedic Research® · doi:10.1002/jor.22913 · Cited by 28 · see citing works
Meisel, J. D., & Kim, D. H. (2016) · Current Biology · doi:10.1016/j.cub.2016.05.050 · Cited by 27 · see citing works
Matrix Disruptions, Growth, and Degradation of Cartilage with Impaired Sulfation
Mertz, E. L., Facchini, M., Pham, A. T., Gualeni, B., Leonardis, F. D., Rossi, A., & Forlino, A. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.116467 · Cited by 26 · see citing works
Mondal, S., Hsiao, K., & Goueli, S. A. (2017) · Assay and Drug Development Technologies · doi:10.1089/adt.2017.815 · Cited by 25 · see citing works
Roles for nucleotide phosphatases in sulfate assimilation and skeletal disease
Hudson, B. H., & York, J. D. (2011) · Advances in Biological Regulation · doi:10.1016/j.advenzreg.2011.11.002 · Cited by 25 · see citing works
Self-citationYang, Y., Wang, Y., Hsiao, M., Lo, S. J., Chang, Y., Jan, Y., Lai, T., Lee, Y.-C., Hsieh, Y.-C., & Yuan, S. F. (2020) · Cancer Letters · doi:10.1016/j.canlet.2020.04.025 · Cited by 24 · see citing works
Schibler, L., Gibbs, L., Benoist-Lasselin, C., Decraene, C., Martinovic, J., Loget, P., Delezoide, A., Gonzalès, M., Münnich, A., Jaïs, J., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007633 · Cited by 24 · see citing works
Roles of Chondroitin Sulfate Proteoglycans as Regulators of Skeletal Development
Schwartz, N. B., & Domowicz, M. S. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.745372 · Cited by 23 · see citing works
Role for cytoplasmic nucleotide hydrolysis in hepatic function and protein synthesis
Hudson, B. H., Frederick, J. P., Drake, L. Y., Megosh, L. C., Irving, R. P., & York, J. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205001110 · Cited by 23 · see citing works
Self-citationDejima, K., Murata, D., Mizuguchi, S., Nomura, K. H., Izumikawa, T., Kitagawa, H., Gengyo‐Ando, K., Yoshina, S., Ichimiya, T., Nishihara, S., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.088229 · Cited by 22 · see citing works
Golgi-resident PAP-specific 3′-phosphatase-coupled sulfotransferase assays
Prather, B., Ethen, C. M., Machacek, M. E., & Wu, Z. L. (2012) · Analytical Biochemistry · doi:10.1016/j.ab.2012.01.003 · Cited by 16 · see citing works
Chondrodysplasias With Multiple Dislocations Caused by Defects in Glycosaminoglycan Synthesis
Dubail, J., & Cormier‐Daire, V. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.642097 · Cited by 15 · see citing works
A structural basis for lithium and substrate binding of an inositide phosphatase
Dollins, D. E., Xiong, J.-P., Endo-Streeter, S., Anderson, D. E., Bansal, V. S., Ponder, J. W., Ren, Y., & York, J. D. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.014057 · Cited by 15 · see citing works
Self-citationBajaj, R., Rodriguez, B. L., Russell, W. K., Warner, A. N., Diao, L., Wang, J., Raso, M. G., Lü, W., Khan, K. B., Solis, L. S., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111429 · Cited by 14 · see citing works
Modulation of intestinal sulfur assimilation metabolism regulates iron homeostasis
Hudson, B. H., Hale, A. T., Irving, R. P., Li, S., & York, J. D. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1715302115 · Cited by 14 · see citing works
Self-citationLi, W., Jia, H., Li, Q., Cui, J., Li, R., Zou, Z., & Hong, X. (2018) · Scientific Reports · doi:10.1038/s41598-018-32847-8 · Cited by 14 · see citing works
Eisele, B. S., Luka, Z., Wu, A. J., Yang, F., Hale, A. T., & York, J. D. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101293 · Cited by 10 · see citing works
Self-citationTissue-specific regulation of 3′-nucleotide hydrolysis and nucleolar architecture
Hudson, B. H., & York, J. D. (2013) · Advances in Biological Regulation · doi:10.1016/j.jbior.2013.11.002 · Cited by 9 · see citing works
Self-citationKoosha, E., Brenna, C. T. A., Ashique, A. M., Jain, N., Ovens, K. L., Koike, T., Kitagawa, H., & Eames, B. F. (2023) · Development · doi:10.1242/dev.201716 · Cited by 9 · see citing works
Testing the Cre-mediated genetic switch for the generation of conditional knock-in mice
Capulli, M., Costantini, R., Sonntag, S., Maurizi, A., Paganini, C., Monti, L., Forlino, A., Shmerling, D., Teti, A. M., & Rossi, A. (2019) · PLoS ONE · doi:10.1371/journal.pone.0213660 · Cited by 7 · see citing works
Modulation of sulfur assimilation metabolic toxicity overcomes anemia and hemochromatosis in mice
Hale, A. T., Brown, R. E., Luka, Z., Hudson, B. H., Matta, P., Williams, C. S., & York, J. D. (2020) · Advances in Biological Regulation · doi:10.1016/j.jbior.2020.100694 · Cited by 6 · see citing works
Self-citationThe growth plate: Zonal architecture, plasticity, and endocrine control of linear growth
Barba‐Ostria, C., & Yakar, S. (2026) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2026.101679 · Cited by 4 · see citing works
Eisele, B. S., Wu, A. J., Luka, Z., Hale, A. T., & York, J. D. (2021) · Advances in Biological Regulation · doi:10.1016/j.jbior.2021.100858 · Cited by 3 · see citing works
Self-citationAndrássy, L., Maros, G., Kovács, I. J., Horváth, Á., Gulyás, K., Bertalan, É., Besnyi, A., Füri, J., Fancsik, T., Szekanecz, Z., et al. (2014) · Orvosi Hetilap · doi:10.1556/oh.2014.30010 · Cited by 2 · see citing works
Venkatapuram, V. S., Aggarwal, S., Kulkarni, A., Vineeth, V. S., Dalal, A. B., Bhat, V. S., Kiran, L., & Patil, S. J. (2022) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.62622 · Cited by 2 · see citing works
Biological effects of lithium – fundamental and medical aspects
As, M., Ковзун, О. І., & Tronko, M. D. (2017) · The Ukrainian Biochemical Journal · doi:10.15407/ubj89.03.005 · Cited by 2 · see citing works
Skeletal Disorders Linked to GAG Synthesis
Huber, C., Guasto, A., Dubail, J., & Cormier‐Daire, V. (2024) · Biology of extracellular matrix · doi:10.1007/978-3-031-70835-0_5 · Cited by 1 · see citing works
Wang, H., Chen, R. B., Zhang, S. N., & Zhang, R. F. (2022) · Figshare · doi:10.6084/m9.figshare.18070769
Wang, H., Chen, R. B., Zhang, S. N., & Zhang, R. F. (2022) · Figshare · doi:10.6084/m9.figshare.18070772
Jiang, J., Sun, Y., Sun, Y., Lu, F., Liu, F., & Zhang, H. (2024) · The Journal of General and Applied Microbiology · doi:10.2323/jgam.2024.05.006
Skeletal Dysplasias Caused by Defects in Glycosaminoglycan Sulfation
Tota, C. G., Leone, A., Paganini, C., Khan, A., Rossi, A., & Superti‐Furga, A. (2024) · Biology of extracellular matrix · doi:10.1007/978-3-031-70835-0_6
Reduction of Charged Glycoconjugates in Tango2 KO Mouse Brain
Moh, E. S. X., Stentenbach, M., McCubbin, T., & Packer, N. H. (2026) · Proteoglycan Research · doi:10.1002/pgr2.70042
MESH1 functions as a metazoan PAPS phosphatase to regulate sulfation
Lin, C., Rose, J. S., Zhang, A., Mirando, A. J., Mestre, A. A., Ding, C. C., Liao, Y., Chen, S.-Y., Setayeshpour, Y., Wu, J., et al. (2026) · Nature Chemical Biology · doi:10.1038/s41589-026-02190-5
- Authors
- Frederick, J. P., Tafari, A. T., Wu, S.-M., Megosh, L. C., Chiou, S.-T., Irving, R. P., & York, J. D.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- York, John D.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2008-08-19
- Volume
- 105
- Issue
- 33
- Pages
- 11605-11612
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2575314
- OpenAlex
- W2038088062
- Cited by
- 67
- References
- 60
- Citations by year
- 2026: 3 · 2024: 3 · 2023: 1 · 2022: 4 · 2021: 7 · 2020: 7 · 2019: 5 · 2018: 4 · 2017: 3 · 2016: 2 · 2015: 5 · 2014: 2 · 2013: 2 · 2012: 5
- FWCI
- 2.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (R01‐grant)
- University of California, San Diego
- National Heart, Lung, and Blood Institute (R01 HL-55672, R01HL055672)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Health Sciences › Medicine › Physiology › Lysosomal Storage Disorders Research
- Health Sciences › Medicine › Rheumatology › Osteoarthritis Treatment and Mechanisms
- Keywords
- lithium inhibition, sulfation, sulfotransferase, 3'-phosphoadenosine 5'-phosphate, heparan sulfate, chondrodysplasia, skeletal development, endochondral ossification, atelectasis, dwarfism, glycosaminoglycan sulfation, Golgi apparatus
- MeSH terms
- Animals, Animals, Newborn, Bone and Bones, Cartilage, Cells, Cultured, Chondrodysplasia Punctata, Chondroitin, Embryo, Nonmammalian, Enzyme Inhibitors, Golgi Apparatus, Growth Plate, Heparitin Sulfate, Heparan Sulfate, Lithium, Male, Mice, Transgenic, Nucleotidases, Phylogeny, Sulfur, Gene Expression Regulation, Enzymologic, Gene Expression Regulation, Developmental, Body Patterning, Mice
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