Desulfation of Heparan Sulfate by Sulf1 and Sulf2 Is Required for Corticospinal Tract Formation

Heparan sulfate (HS) has been implicated in a wide range of cell signaling. Here we report a novel mechanism in which extracellular removal of 6- O -sulfate groups from HS by the endosulfatases, Sulf1 and Sulf2, is essential for axon guidance during development. In Sulf1/ 2 double knockout (DKO) mic...

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Veröffentlicht in:	Scientific reports 2017-10, Vol.7 (1), p.13847-14, Article 13847
Hauptverfasser:	Okada, Takuya, Keino-Masu, Kazuko, Nagamine, Satoshi, Kametani, Fuyuki, Ohto, Tatsuyuki, Hasegawa, Masato, van Kuppevelt, Toin H., Kunita, Satoshi, Takahashi, Satoru, Masu, Masayuki
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Schlagworte:	13 14 14/19 42 42/109 42/35 45 59 631/378/2571/2576 631/45/221 631/80/221 64 64/60 82 82/29 82/51 96 96/63 Animals Axon Guidance Axonogenesis Electroporation Glial cells Heparan sulfate Heparitin Sulfate - chemistry Heparitin Sulfate - metabolism Humanities and Social Sciences Hypothalamus Mesencephalon Mice Mice, Inbred C57BL Mice, Knockout multidisciplinary Phenotype Proteomics Pyramidal tracts Pyramidal Tracts - metabolism Pyramidal Tracts - pathology Radial glial cells Science Science (multidisciplinary) Signal Transduction Spinal Cord Injuries - metabolism Spinal Cord Injuries - pathology Sulfatases - physiology Sulfates Sulfates - chemistry Sulfates - metabolism Sulfotransferases - physiology Ventricle Ventricles (cerebral)
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creator	Okada, Takuya Keino-Masu, Kazuko Nagamine, Satoshi Kametani, Fuyuki Ohto, Tatsuyuki Hasegawa, Masato van Kuppevelt, Toin H. Kunita, Satoshi Takahashi, Satoru Masu, Masayuki
description	Heparan sulfate (HS) has been implicated in a wide range of cell signaling. Here we report a novel mechanism in which extracellular removal of 6- O -sulfate groups from HS by the endosulfatases, Sulf1 and Sulf2, is essential for axon guidance during development. In Sulf1/ 2 double knockout (DKO) mice, the corticospinal tract (CST) was dorsally displaced on the midbrain surface. In utero electroporation of Sulf1/ 2 into radial glial cells along the third ventricle, where Sulf1/ 2 mRNAs are normally expressed, rescued the CST defects in the DKO mice. Proteomic analysis and functional testing identified Slit2 as the key molecule associated with the DKO phenotype. In the DKO brain, 6- O -sulfated HS was increased, leading to abnormal accumulation of Slit2 protein on the pial surface of the cerebral peduncle and hypothalamus, which caused dorsal repulsion of CST axons. Our findings indicate that postbiosynthetic desulfation of HS by Sulfs controls CST axon guidance through fine-tuning of Slit2 presentation.
doi_str_mv	10.1038/s41598-017-14185-3
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Here we report a novel mechanism in which extracellular removal of 6- O -sulfate groups from HS by the endosulfatases, Sulf1 and Sulf2, is essential for axon guidance during development. In Sulf1/ 2 double knockout (DKO) mice, the corticospinal tract (CST) was dorsally displaced on the midbrain surface. In utero electroporation of Sulf1/ 2 into radial glial cells along the third ventricle, where Sulf1/ 2 mRNAs are normally expressed, rescued the CST defects in the DKO mice. Proteomic analysis and functional testing identified Slit2 as the key molecule associated with the DKO phenotype. In the DKO brain, 6- O -sulfated HS was increased, leading to abnormal accumulation of Slit2 protein on the pial surface of the cerebral peduncle and hypothalamus, which caused dorsal repulsion of CST axons. Our findings indicate that postbiosynthetic desulfation of HS by Sulfs controls CST axon guidance through fine-tuning of Slit2 presentation.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-017-14185-3</identifier><identifier>PMID: 29062064</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13 ; 14 ; 14/19 ; 42 ; 42/109 ; 42/35 ; 45 ; 59 ; 631/378/2571/2576 ; 631/45/221 ; 631/80/221 ; 64 ; 64/60 ; 82 ; 82/29 ; 82/51 ; 96 ; 96/63 ; Animals ; Axon Guidance ; Axonogenesis ; Electroporation ; Glial cells ; Heparan sulfate ; Heparitin Sulfate - chemistry ; Heparitin Sulfate - metabolism ; Humanities and Social Sciences ; Hypothalamus ; Mesencephalon ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; multidisciplinary ; Phenotype ; Proteomics ; Pyramidal tracts ; Pyramidal Tracts - metabolism ; Pyramidal Tracts - pathology ; Radial glial cells ; Science ; Science (multidisciplinary) ; Signal Transduction ; Spinal Cord Injuries - metabolism ; Spinal Cord Injuries - pathology ; Sulfatases - physiology ; Sulfates ; Sulfates - chemistry ; Sulfates - metabolism ; Sulfotransferases - physiology ; Ventricle ; Ventricles (cerebral)</subject><ispartof>Scientific reports, 2017-10, Vol.7 (1), p.13847-14, Article 13847</ispartof><rights>The Author(s) 2017</rights><rights>2017. 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Here we report a novel mechanism in which extracellular removal of 6- O -sulfate groups from HS by the endosulfatases, Sulf1 and Sulf2, is essential for axon guidance during development. In Sulf1/ 2 double knockout (DKO) mice, the corticospinal tract (CST) was dorsally displaced on the midbrain surface. In utero electroporation of Sulf1/ 2 into radial glial cells along the third ventricle, where Sulf1/ 2 mRNAs are normally expressed, rescued the CST defects in the DKO mice. Proteomic analysis and functional testing identified Slit2 as the key molecule associated with the DKO phenotype. In the DKO brain, 6- O -sulfated HS was increased, leading to abnormal accumulation of Slit2 protein on the pial surface of the cerebral peduncle and hypothalamus, which caused dorsal repulsion of CST axons. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Okada, Takuya</au><au>Keino-Masu, Kazuko</au><au>Nagamine, Satoshi</au><au>Kametani, Fuyuki</au><au>Ohto, Tatsuyuki</au><au>Hasegawa, Masato</au><au>van Kuppevelt, Toin H.</au><au>Kunita, Satoshi</au><au>Takahashi, Satoru</au><au>Masu, Masayuki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Desulfation of Heparan Sulfate by Sulf1 and Sulf2 Is Required for Corticospinal Tract Formation</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2017-10-23</date><risdate>2017</risdate><volume>7</volume><issue>1</issue><spage>13847</spage><epage>14</epage><pages>13847-14</pages><artnum>13847</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Heparan sulfate (HS) has been implicated in a wide range of cell signaling. Here we report a novel mechanism in which extracellular removal of 6- O -sulfate groups from HS by the endosulfatases, Sulf1 and Sulf2, is essential for axon guidance during development. In Sulf1/ 2 double knockout (DKO) mice, the corticospinal tract (CST) was dorsally displaced on the midbrain surface. In utero electroporation of Sulf1/ 2 into radial glial cells along the third ventricle, where Sulf1/ 2 mRNAs are normally expressed, rescued the CST defects in the DKO mice. Proteomic analysis and functional testing identified Slit2 as the key molecule associated with the DKO phenotype. In the DKO brain, 6- O -sulfated HS was increased, leading to abnormal accumulation of Slit2 protein on the pial surface of the cerebral peduncle and hypothalamus, which caused dorsal repulsion of CST axons. Our findings indicate that postbiosynthetic desulfation of HS by Sulfs controls CST axon guidance through fine-tuning of Slit2 presentation.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>29062064</pmid><doi>10.1038/s41598-017-14185-3</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-9125-7001</orcidid><oa>free_for_read</oa></addata></record>
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subjects	13 14 14/19 42 42/109 42/35 45 59 631/378/2571/2576 631/45/221 631/80/221 64 64/60 82 82/29 82/51 96 96/63 Animals Axon Guidance Axonogenesis Electroporation Glial cells Heparan sulfate Heparitin Sulfate - chemistry Heparitin Sulfate - metabolism Humanities and Social Sciences Hypothalamus Mesencephalon Mice Mice, Inbred C57BL Mice, Knockout multidisciplinary Phenotype Proteomics Pyramidal tracts Pyramidal Tracts - metabolism Pyramidal Tracts - pathology Radial glial cells Science Science (multidisciplinary) Signal Transduction Spinal Cord Injuries - metabolism Spinal Cord Injuries - pathology Sulfatases - physiology Sulfates Sulfates - chemistry Sulfates - metabolism Sulfotransferases - physiology Ventricle Ventricles (cerebral)
title	Desulfation of Heparan Sulfate by Sulf1 and Sulf2 Is Required for Corticospinal Tract Formation
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