Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity

Kalus I, Salmen B, Viebahn C, von Figura K, Schmitz D, D'Hooge R, Dierks T (2009)
JOURNAL OF CELLULAR AND MOLECULAR MEDICINE 13(11-12): 4505-4521.

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The extracellular sulfatases Sulf1 and Sulf2 remove specific 6-O-sulfate groups from heparan sulfate, thereby modulating numerous signalling pathways underlying development and homeostasis. In vitro data have suggested that the two enzymes show functional redundancy. To elucidate their in vivo functions and to further address the question of a putative redundancy, we have generated Sulf1- and Sulf2-deficient mice. Phenotypic analysis of these animals revealed higher embryonic lethality of Sulf2 knockout mice, which can be associated with neuroanatomical malformations during embryogenesis. Sulf1 seems not to be essential for developmental or postnatal viability, as mice deficient in this sulfatase show no overt phenotype. However, neurite outgrowth deficits were observed in hippocampal and cerebellar neurons of both mutant mouse lines, suggesting that not only Sulf2 but also Sulf1 function plays a role in the developing nervous system. Behavioural analysis revealed differential deficits with regard to cage activity and spatial learning for Sulf1- and Sulf2-deficient mouse lines. In addition, Sulf1-specific deficits were shown for synaptic plasticity in the CA1 region of the hippocampus, associated with a reduced spine density. These results reveal that Sulf1 and Sulf2 fulfil non-redundant functions in vivo in the development and maintenance of the murine nervous system.
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Kalus I, Salmen B, Viebahn C, et al. Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity. JOURNAL OF CELLULAR AND MOLECULAR MEDICINE. 2009;13(11-12):4505-4521.
Kalus, I., Salmen, B., Viebahn, C., von Figura, K., Schmitz, D., D'Hooge, R., & Dierks, T. (2009). Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity. JOURNAL OF CELLULAR AND MOLECULAR MEDICINE, 13(11-12), 4505-4521.
Kalus, I., Salmen, B., Viebahn, C., von Figura, K., Schmitz, D., D'Hooge, R., and Dierks, T. (2009). Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity. JOURNAL OF CELLULAR AND MOLECULAR MEDICINE 13, 4505-4521.
Kalus, I., et al., 2009. Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity. JOURNAL OF CELLULAR AND MOLECULAR MEDICINE, 13(11-12), p 4505-4521.
I. Kalus, et al., “Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity”, JOURNAL OF CELLULAR AND MOLECULAR MEDICINE, vol. 13, 2009, pp. 4505-4521.
Kalus, I., Salmen, B., Viebahn, C., von Figura, K., Schmitz, D., D'Hooge, R., Dierks, T.: Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity. JOURNAL OF CELLULAR AND MOLECULAR MEDICINE. 13, 4505-4521 (2009).
Kalus, Ina, Salmen, Benedikt, Viebahn, Christoph, von Figura, Kurt, Schmitz, Dietmar, D'Hooge, Rudi, and Dierks, Thomas. “Differential involvement of the extracellular 6-O-endosulfatases Sulf1 and Sulf2 in brain development and neuronal and behavioural plasticity”. JOURNAL OF CELLULAR AND MOLECULAR MEDICINE 13.11-12 (2009): 4505-4521.
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Data provided by Europe PubMed Central.

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Kalus I, Rohn S, Puvirajesinghe TM, Guimond SE, Eyckerman-Kolln PJ, Ten Dam G, van Kuppevelt TH, Turnbull JE, Dierks T., PLoS ONE 10(10), 2015
PMID: 26448642
Sulf1 and Sulf2 expression in the nervous system and its role in limiting neurite outgrowth in vitro.
Joy MT, Vrbova G, Dhoot GK, Anderson PN., Exp. Neurol. 263(), 2015
PMID: 25448158
SULF2, a heparan sulfate endosulfatase, is present in the blood of healthy individuals and increases in cirrhosis.
Singer MS, Phillips JJ, Lemjabbar-Alaoui H, Wang YQ, Wu J, Goldman R, Rosen SD., Clin. Chim. Acta 440(), 2015
PMID: 25444749
Choroid plexus in developmental and evolutionary perspective.
Bill BR, Korzh V., Front Neurosci 8(), 2014
PMID: 25452709
Human genetic disorders and knockout mice deficient in glycosaminoglycan.
Mizumoto S, Yamada S, Sugahara K., Biomed Res Int 2014(), 2014
PMID: 25126564
Heparan sulfotransferases Hs6st1 and Hs2st keep Erk in check for mouse corpus callosum development.
Clegg JM, Conway CD, Howe KM, Price DJ, Mason JO, Turnbull JE, Basson MA, Pratt T., J. Neurosci. 34(6), 2014
PMID: 24501377
Sugar glues for broken neurons.
Swarup VP, Mencio CP, Hlady V, Kuberan B., Biomol Concepts 4(3), 2013
PMID: 25285176
Cooperation of binding sites at the hydrophilic domain of cell-surface sulfatase Sulf1 allows for dynamic interaction of the enzyme with its substrate heparan sulfate.
Milz F, Harder A, Neuhaus P, Breitkreuz-Korff O, Walhorn V, Lubke T, Anselmetti D, Dierks T., Biochim. Biophys. Acta 1830(11), 2013
PMID: 23891937
Proteoglycans and their roles in brain cancer.
Wade A, Robinson AE, Engler JR, Petritsch C, James CD, Phillips JJ., FEBS J. 280(10), 2013
PMID: 23281850
Genomic variation in seven Khoe-San groups reveals adaptation and complex African history.
Schlebusch CM, Skoglund P, Sjodin P, Gattepaille LM, Hernandez D, Jay F, Li S, De Jongh M, Singleton A, Blum MG, Soodyall H, Jakobsson M., Science 338(6105), 2012
PMID: 22997136
Laser-capture microdissection and transcriptional profiling of the dorsomedial nucleus of the hypothalamus.
Lee S, Bookout AL, Lee CE, Gautron L, Harper MJ, Elias CF, Lowell BB, Elmquist JK., J. Comp. Neurol. 520(16), 2012
PMID: 22473294
Roles of heparan sulfate sulfation in dentinogenesis.
Hayano S, Kurosaka H, Yanagita T, Kalus I, Milz F, Ishihara Y, Islam MN, Kawanabe N, Saito M, Kamioka H, Adachi T, Dierks T, Yamashiro T., J. Biol. Chem. 287(15), 2012
PMID: 22351753
Heparan sulfate sulfatase SULF2 regulates PDGFRα signaling and growth in human and mouse malignant glioma.
Phillips JJ, Huillard E, Robinson AE, Ward A, Lum DH, Polley MY, Rosen SD, Rowitch DH, Werb Z., J. Clin. Invest. 122(3), 2012
PMID: 22293178
SULFs in human neoplasia: implication as progression and prognosis factors.
Bret C, Moreaux J, Schved JF, Hose D, Klein B., J Transl Med 9(), 2011
PMID: 21599997
Sulfatase 1 and sulfatase 2 in hepatocellular carcinoma: associated signaling pathways, tumor phenotypes, and survival.
Yang JD, Sun Z, Hu C, Lai J, Dove R, Nakamura I, Lee JS, Thorgeirsson SS, Kang KJ, Chu IS, Roberts LR., Genes Chromosomes Cancer 50(2), 2011
PMID: 21104785
Sulf-2: an extracellular modulator of cell signaling and a cancer target candidate.
Rosen SD, Lemjabbar-Alaoui H., Expert Opin. Ther. Targets 14(9), 2010
PMID: 20629619
Expression patterns of sulfatase genes in the developing mouse embryo.
Ratzka A, Mundlos S, Vortkamp A., Dev. Dyn. 239(6), 2010
PMID: 20503373

60 References

Data provided by Europe PubMed Central.

Identification of neurite outgrowth promoting sites on the laminin alpha 3 chain G domain.
Kato K, Utani A, Suzuki N, Mochizuki M, Yamada M, Nishi N, Matsuura H, Shinkai H, Nomizu M., Biochemistry 41(35), 2002
PMID: 12196012
The heparan sulfate proteoglycan agrin modulates neurite outgrowth mediated by FGF-2.
Kim MJ, Cotman SL, Halfter W, Cole GJ., J. Neurobiol. 55(3), 2003
PMID: 12717697
Glypican-2 binds to midkine: the role of glypican-2 in neuronal cell adhesion and neurite outgrowth.
Kurosawa N, Chen GY, Kadomatsu K, Ikematsu S, Sakuma S, Muramatsu T., Glycoconj. J. 18(6), 2001
PMID: 12084985
The extracellular matrix and synapses.
Dityatev A, Schachner M., Cell Tissue Res. 326(2), 2006
PMID: 16767406
Reg1ulatory role and molecular interactions of a cell-surface heparan sulfate proteoglycan (N-syndecan) in hippocampal long-term potentiation.
Lauri SE, Kaukinen S, Kinnunen T, Ylinen A, Imai S, Kaila K, Taira T, Rauvala H., J. Neurosci. 19(4), 1999
PMID: 9952400
Differences in behavioural test battery performance between mice with hippocampal and cerebellar lesions.
Goddyn H, Leo S, Meert T, D'Hooge R., Behav. Brain Res. 173(1), 2006
PMID: 16860407
Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory.
Kaksonen M, Pavlov I, Voikar V, Lauri SE, Hienola A, Riekki R, Lakso M, Taira T, Rauvala H., Mol. Cell. Neurosci. 21(1), 2002
PMID: 12359158
Role of heparin-binding growth-associated molecule (HB-GAM) in hippocampal LTP and spatial learning revealed by studies on overexpressing and knockout mice.
Pavlov I, Voikar V, Kaksonen M, Lauri SE, Hienola A, Taira T, Rauvala H., Mol. Cell. Neurosci. 20(2), 2002
PMID: 12093164
Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration.
Cornelison DD, Wilcox-Adelman SA, Goetinck PF, Rauvala H, Rapraeger AC, Olwin BB., Genes Dev. 18(18), 2004
PMID: 15371336

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