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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Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Abstract / Bemerkung
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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Zeitschriftentitel
JOURNAL OF CELLULAR AND MOLECULAR MEDICINE
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13
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11-12
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4505-4521
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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. doi:10.1111/j.1582-4934.2008.00558.x
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.

33 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Flexible Roles for Proteoglycan Sulfation and Receptor Signaling.
Yu P, Pearson CS, Geller HM., Trends Neurosci 41(1), 2018
PMID: 29150096
Heparan Sulfate Proteoglycans as Emerging Players in Synaptic Specificity.
Condomitti G, de Wit J., Front Mol Neurosci 11(), 2018
PMID: 29434536
Multiple roles of epithelial heparan sulfate in stomach morphogenesis.
Huang M, He H, Belenkaya T, Lin X., J Cell Sci 131(10), 2018
PMID: 29700203
Heparan Sulfate Organizes Neuronal Synapses through Neurexin Partnerships.
Zhang P, Lu H, Peixoto RT, Pines MK, Ge Y, Oku S, Siddiqui TJ, Xie Y, Wu W, Archer-Hartmann S, Yoshida K, Tanaka KF, Aricescu AR, Azadi P, Gordon MD, Sabatini BL, Wong ROL, Craig AM., Cell 174(6), 2018
PMID: 30100184
Sulfatase-mediated manipulation of the astrocyte-Schwann cell interface.
O'Neill P, Lindsay SL, Pantiru A, Guimond SE, Fagoe N, Verhaagen J, Turnbull JE, Riddell JS, Barnett SC., Glia 65(1), 2017
PMID: 27535874
The "in and out" of glucosamine 6-O-sulfation: the 6th sense of heparan sulfate.
El Masri R, Seffouh A, Lortat-Jacob H, Vivès RR., Glycoconj J 34(3), 2017
PMID: 27812771
Decreased Expression of Sulfatase 2 in the Brains of Alzheimer's Disease Patients: Implications for Regulation of Neuronal Cell Signaling.
Roberts RO, Kang YN, Hu C, Moser CD, Wang S, Moore MJ, Graham RP, Lai JP, Petersen RC, Roberts LR., J Alzheimers Dis Rep 1(1), 2017
PMID: 30035253
Desulfation of Heparan Sulfate by Sulf1 and Sulf2 Is Required for Corticospinal Tract Formation.
Okada T, Keino-Masu K, Nagamine S, Kametani F, Ohto T, Hasegawa M, van Kuppevelt TH, Kunita S, Takahashi S, Masu M., Sci Rep 7(1), 2017
PMID: 29062064
Expression of the extracellular sulfatase SULF2 is associated with squamous cell carcinoma of the head and neck.
Flowers SA, Zhou X, Wu J, Wang Y, Makambi K, Kallakury BV, Singer MS, Rosen SD, Davidson B, Goldman R., Oncotarget 7(28), 2016
PMID: 27223083
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
Heparan sulfate proteoglycans: a sugar code for vertebrate development?
Poulain FE, Yost HJ., Development 142(20), 2015
PMID: 26487777
Sulf1 and Sulf2 Differentially Modulate Heparan Sulfate Proteoglycan Sulfation during Postnatal Cerebellum Development: Evidence for Neuroprotective and Neurite Outgrowth Promoting Functions.
Kalus I, Rohn S, Puvirajesinghe TM, Guimond SE, Eyckerman-Kölln PJ, Ten Dam G, van Kuppevelt TH, Turnbull JE, Dierks T., PLoS One 10(10), 2015
PMID: 26448642
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
Human genetic disorders and knockout mice deficient in glycosaminoglycan.
Mizumoto S, Yamada S, Sugahara K., Biomed Res Int 2014(), 2014
PMID: 25126564
Choroid plexus in developmental and evolutionary perspective.
Bill BR, Korzh V., Front Neurosci 8(), 2014
PMID: 25452709
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
HSulf sulfatases catalyze processive and oriented 6-O-desulfation of heparan sulfate that differentially regulates fibroblast growth factor activity.
Seffouh A, Milz F, Przybylski C, Laguri C, Oosterhof A, Bourcier S, Sadir R, Dutkowski E, Daniel R, van Kuppevelt TH, Dierks T, Lortat-Jacob H, Vivès RR., FASEB J 27(6), 2013
PMID: 23457216
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, Lübke T, Anselmetti D, Dierks T., Biochim Biophys Acta 1830(11), 2013
PMID: 23891937
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
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
Genomic variation in seven Khoe-San groups reveals adaptation and complex African history.
Schlebusch CM, Skoglund P, Sjödin 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
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
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
Expression patterns of sulfatase genes in the developing mouse embryo.
Ratzka A, Mundlos S, Vortkamp A., Dev Dyn 239(6), 2010
PMID: 20503373
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
Characterization of the human sulfatase Sulf1 and its high affinity heparin/heparan sulfate interaction domain.
Frese MA, Milz F, Dick M, Lamanna WC, Dierks T., J Biol Chem 284(41), 2009
PMID: 19666466

60 References

Daten bereitgestellt von Europe PubMed Central.

Proteoglycans in the developing brain: new conceptual insights for old proteins.
Bandtlow CE, Zimmermann DR., Physiol. Rev. 80(4), 2000
PMID: 11015614
Nervous system proteoglycans as modulators of neurite outgrowth.
Bovolenta P, Fernaud-Espinosa I., Prog. Neurobiol. 61(2), 2000
PMID: 10704995
When sugars guide axons: insights from heparan sulphate proteoglycan mutants.
Lee JS, Chien CB., Nat. Rev. Genet. 5(12), 2004
PMID: 15573124
Heparan sulfate proteoglycans and the emergence of neuronal connectivity.
Van Vactor D, Wall DP, Johnson KG., Curr. Opin. Neurobiol. 16(1), 2006
PMID: 16417999
Functions of cell surface heparan sulfate proteoglycans.
Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M., Annu. Rev. Biochem. 68(), 1999
PMID: 10872465
Molecular diversity of heparan sulfate.
Esko JD, Lindahl U., J. Clin. Invest. 108(2), 2001
PMID: 11457867
Heparan sulfate: decoding a dynamic multifunctional cell regulator.
Turnbull J, Powell A, Guimond S., Trends Cell Biol. 11(2), 2001
PMID: 11166215
Mammalian brain morphogenesis and midline axon guidance require heparan sulfate.
Inatani M, Irie F, Plump AS, Tessier-Lavigne M, Yamaguchi Y., Science 302(5647), 2003
PMID: 14605369
Substrate specificity and domain functions of extracellular heparan sulfate 6-O-endosulfatases, QSulf1 and QSulf2.
Ai X, Do AT, Kusche-Gullberg M, Lindahl U, Lu K, Emerson CP Jr., J. Biol. Chem. 281(8), 2005
PMID: 16377625
Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans.
Morimoto-Tomita M, Uchimura K, Werb Z, Hemmerich S, Rosen SD., J. Biol. Chem. 277(51), 2002
PMID: 12368295
Heparan sulfate 6-O-endosulfatases: discrete in vivo activities and functional co-operativity.
Lamanna WC, Baldwin RJ, Padva M, Kalus I, Ten Dam G, van Kuppevelt TH, Gallagher JT, von Figura K, Dierks T, Merry CL., Biochem. J. 400(1), 2006
PMID: 16901266
The heparanome--the enigma of encoding and decoding heparan sulfate sulfation.
Lamanna WC, Kalus I, Padva M, Baldwin RJ, Merry CL, Dierks T., J. Biotechnol. 129(2), 2007
PMID: 17337080
SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation.
Ai X, Kitazawa T, Do AT, Kusche-Gullberg M, Labosky PA, Emerson CP Jr., Development 134(18), 2007
PMID: 17720696
Secreted sulfatases Sulf1 and Sulf2 have overlapping yet essential roles in mouse neonatal survival.
Holst CR, Bou-Reslan H, Gore BB, Wong K, Grant D, Chalasani S, Carano RA, Frantz GD, Tessier-Lavigne M, Bolon B, French DM, Ashkenazi A., PLoS ONE 2(6), 2007
PMID: 17593974
Gene trap disruption of the mouse heparan sulfate 6-O-endosulfatase gene, Sulf2.
Lum DH, Tan J, Rosen SD, Werb Z., Mol. Cell. Biol. 27(2), 2006
PMID: 17116694
Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase.
Dhoot GK, Gustafsson MK, Ai X, Sun W, Standiford DM, Emerson CP Jr., Science 293(5535), 2001
PMID: 11533491
Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer.
Lai J, Chien J, Staub J, Avula R, Greene EL, Matthews TA, Smith DI, Kaufmann SH, Roberts LR, Shridhar V., J. Biol. Chem. 278(25), 2003
PMID: 12686563
HSulf-1 modulates HGF-mediated tumor cell invasion and signaling in head and neck squamous carcinoma.
Lai JP, Chien J, Strome SE, Staub J, Montoya DP, Greene EL, Smith DI, Roberts LR, Shridhar V., Oncogene 23(7), 2004
PMID: 14973553
Domain-specific modification of heparan sulfate by Qsulf1 modulates the binding of the bone morphogenetic protein antagonist Noggin.
Viviano BL, Paine-Saunders S, Gasiunas N, Gallagher J, Saunders S., J. Biol. Chem. 279(7), 2003
PMID: 14645250
QSulf1, a heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis.
Wang S, Ai X, Freeman SD, Pownall ME, Lu Q, Kessler DS, Emerson CP Jr., Proc. Natl. Acad. Sci. U.S.A. 101(14), 2004
PMID: 15051888
The proprotein convertase PC5A and a metalloprotease are involved in the proteolytic processing of the neural adhesion molecule L1.
Kalus I, Schnegelsberg B, Seidah NG, Kleene R, Schachner M., J. Biol. Chem. 278(12), 2003
PMID: 12529374
Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation.
Schmitz D, Mellor J, Breustedt J, Nicoll RA., Nat. Neurosci. 6(10), 2003
PMID: 12947409
Congenital hydrocephalus: nosology and guidelines for clinical approach and genetic counselling.
Schrander-Stumpel C, Fryns JP., Eur. J. Pediatr. 157(5), 1998
PMID: 9625330
Expression of a heparan sulfate remodeling enzyme, heparan sulfate 6-O-endosulfatase sulfatase FP2, in the rat nervous system.
Nagamine S, Koike S, Keino-Masu K, Masu M., Brain Res. Dev. Brain Res. 159(2), 2005
PMID: 16139897
Identification of a novel nonlysosomal sulphatase expressed in the floor plate, choroid plexus and cartilage.
Ohto T, Uchida H, Yamazaki H, Keino-Masu K, Matsui A, Masu M., Genes Cells 7(2), 2002
PMID: 11895481
Role of L1 in neural development: what the knockouts tell us.
Kamiguchi H, Hlavin ML, Lemmon V., Mol. Cell. Neurosci. 12(1-2), 1998
PMID: 9770339
Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses.
Dityatev A, Dityateva G, Sytnyk V, Delling M, Toni N, Nikonenko I, Muller D, Schachner M., J. Neurosci. 24(42), 2004
PMID: 15496673
Neuroscience. Organizing the source of memory.
Grove EA., Science 319(5861), 2008
PMID: 18202278
Sulf1 expression pattern and its role in cartilage and joint development.
Zhao W, Sala-Newby GB, Dhoot GK., Dev. Dyn. 235(12), 2006
PMID: 17061267
Regulation of vascular smooth muscle cell proliferation, migration and death by heparan sulfate 6-O-endosulfatase1.
Sala-Newby GB, George SJ, Bond M, Dhoot GK, Newby AC., FEBS Lett. 579(28), 2005
PMID: 16289059
Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase.
Bullock SL, Fletcher JM, Beddington RS, Wilson VA., Genes Dev. 12(12), 1998
PMID: 9637690
Defective heparan sulfate biosynthesis and neonatal lethality in mice lacking N-deacetylase/N-sulfotransferase-1.
Ringvall M, Ledin J, Holmborn K, van Kuppevelt T, Ellin F, Eriksson I, Olofsson AM, Kjellen L, Forsberg E., J. Biol. Chem. 275(34), 2000
PMID: 10852901
Mice deficient in heparan sulfate 3-O-sulfotransferase-1: normal hemostasis with unexpected perinatal phenotypes.
Shworak NW, HajMohammadi S, de Agostini AI, Rosenberg RD., Glycoconj. J. 19(4-5), 2002
PMID: 12975616
HSulf-2, an extracellular endoglucosamine-6-sulfatase, selectively mobilizes heparin-bound growth factors and chemokines: effects on VEGF, FGF-1, and SDF-1.
Uchimura K, Morimoto-Tomita M, Bistrup A, Li J, Lyon M, Gallagher J, Werb Z, Rosen SD., BMC Biochem. 7(), 2006
PMID: 16417632
Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin.
Pellegrini L, Burke DF, von Delft F, Mulloy B, Blundell TL., Nature 407(6807), 2000
PMID: 11069186
Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization.
Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, Mohammadi M., Mol. Cell 6(3), 2000
PMID: 11030354
Fibroblast growth factor receptor-1 (FGFR-1) is essential for normal neural tube and limb development.
Deng C, Bedford M, Li C, Xu X, Yang X, Dunmore J, Leder P., Dev. Biol. 185(1), 1997
PMID: 9169049
Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice.
Dono R, Texido G, Dussel R, Ehmke H, Zeller R., EMBO J. 17(15), 1998
PMID: 9687490
Perlecan is essential for cartilage and cephalic development.
Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell JR, Yamada Y., Nat. Genet. 23(3), 1999
PMID: 10545953
Perlecan controls neurogenesis in the developing telencephalon.
Giros A, Morante J, Gil-Sanz C, Fairen A, Costell M., BMC Dev. Biol. 7(), 2007
PMID: 17411441
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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