Glucocerebrosidases catalyze a transgalactosylation reaction that yields a newly-identified brain sterol metabolite, galactosylated cholesterol

β-Glucocerebrosidase (GBA) hydrolyzes glucosylceramide (GlcCer) to generate ceramide. Previously, we demonstrated that lysosomal GBA1 and nonlysosomal GBA2 possess not only GlcCer hydrolase activity, but also transglucosylation activity to transfer the glucose residue from GlcCer to cholesterol to f...

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Veröffentlicht in:The Journal of biological chemistry 2020-04, Vol.295 (16), p.5257-5277
Hauptverfasser: Akiyama, Hisako, Ide, Mitsuko, Nagatsuka, Yasuko, Sayano, Tomoko, Nakanishi, Etsuro, Uemura, Norihito, Yuyama, Kohei, Yamaguchi, Yoshiki, Kamiguchi, Hiroyuki, Takahashi, Ryosuke, Aerts, Johannes M.F.G., Greimel, Peter, Hirabayashi, Yoshio
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container_end_page 5277
container_issue 16
container_start_page 5257
container_title The Journal of biological chemistry
container_volume 295
creator Akiyama, Hisako
Ide, Mitsuko
Nagatsuka, Yasuko
Sayano, Tomoko
Nakanishi, Etsuro
Uemura, Norihito
Yuyama, Kohei
Yamaguchi, Yoshiki
Kamiguchi, Hiroyuki
Takahashi, Ryosuke
Aerts, Johannes M.F.G.
Greimel, Peter
Hirabayashi, Yoshio
description β-Glucocerebrosidase (GBA) hydrolyzes glucosylceramide (GlcCer) to generate ceramide. Previously, we demonstrated that lysosomal GBA1 and nonlysosomal GBA2 possess not only GlcCer hydrolase activity, but also transglucosylation activity to transfer the glucose residue from GlcCer to cholesterol to form β-cholesterylglucoside (β-GlcChol) in vitro. β-GlcChol is a member of sterylglycosides present in diverse species. How GBA1 and GBA2 mediate β-GlcChol metabolism in the brain is unknown. Here, we purified and characterized sterylglycosides from rodent and fish brains. Although glucose is thought to be the sole carbohydrate component of sterylglycosides in vertebrates, structural analysis of rat brain sterylglycosides revealed the presence of galactosylated cholesterol (β-GalChol), in addition to β-GlcChol. Analyses of brain tissues from GBA2-deficient mice and GBA1- and/or GBA2-deficient Japanese rice fish (Oryzias latipes) revealed that GBA1 and GBA2 are responsible for β-GlcChol degradation and formation, respectively, and that both GBA1 and GBA2 are responsible for β-GalChol formation. Liquid chromatography–tandem MS revealed that β-GlcChol and β-GalChol are present throughout development from embryo to adult in the mouse brain. We found that β-GalChol expression depends on galactosylceramide (GalCer), and developmental onset of β-GalChol biosynthesis appeared to be during myelination. We also found that β-GlcChol and β-GalChol are secreted from neurons and glial cells in association with exosomes. In vitro enzyme assays confirmed that GBA1 and GBA2 have transgalactosylation activity to transfer the galactose residue from GalCer to cholesterol to form β-GalChol. This is the first report of the existence of β-GalChol in vertebrates and how β-GlcChol and β-GalChol are formed in the brain.
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Previously, we demonstrated that lysosomal GBA1 and nonlysosomal GBA2 possess not only GlcCer hydrolase activity, but also transglucosylation activity to transfer the glucose residue from GlcCer to cholesterol to form β-cholesterylglucoside (β-GlcChol) in vitro. β-GlcChol is a member of sterylglycosides present in diverse species. How GBA1 and GBA2 mediate β-GlcChol metabolism in the brain is unknown. Here, we purified and characterized sterylglycosides from rodent and fish brains. Although glucose is thought to be the sole carbohydrate component of sterylglycosides in vertebrates, structural analysis of rat brain sterylglycosides revealed the presence of galactosylated cholesterol (β-GalChol), in addition to β-GlcChol. Analyses of brain tissues from GBA2-deficient mice and GBA1- and/or GBA2-deficient Japanese rice fish (Oryzias latipes) revealed that GBA1 and GBA2 are responsible for β-GlcChol degradation and formation, respectively, and that both GBA1 and GBA2 are responsible for β-GalChol formation. Liquid chromatography–tandem MS revealed that β-GlcChol and β-GalChol are present throughout development from embryo to adult in the mouse brain. We found that β-GalChol expression depends on galactosylceramide (GalCer), and developmental onset of β-GalChol biosynthesis appeared to be during myelination. We also found that β-GlcChol and β-GalChol are secreted from neurons and glial cells in association with exosomes. In vitro enzyme assays confirmed that GBA1 and GBA2 have transgalactosylation activity to transfer the galactose residue from GalCer to cholesterol to form β-GalChol. 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Previously, we demonstrated that lysosomal GBA1 and nonlysosomal GBA2 possess not only GlcCer hydrolase activity, but also transglucosylation activity to transfer the glucose residue from GlcCer to cholesterol to form β-cholesterylglucoside (β-GlcChol) in vitro. β-GlcChol is a member of sterylglycosides present in diverse species. How GBA1 and GBA2 mediate β-GlcChol metabolism in the brain is unknown. Here, we purified and characterized sterylglycosides from rodent and fish brains. Although glucose is thought to be the sole carbohydrate component of sterylglycosides in vertebrates, structural analysis of rat brain sterylglycosides revealed the presence of galactosylated cholesterol (β-GalChol), in addition to β-GlcChol. Analyses of brain tissues from GBA2-deficient mice and GBA1- and/or GBA2-deficient Japanese rice fish (Oryzias latipes) revealed that GBA1 and GBA2 are responsible for β-GlcChol degradation and formation, respectively, and that both GBA1 and GBA2 are responsible for β-GalChol formation. Liquid chromatography–tandem MS revealed that β-GlcChol and β-GalChol are present throughout development from embryo to adult in the mouse brain. We found that β-GalChol expression depends on galactosylceramide (GalCer), and developmental onset of β-GalChol biosynthesis appeared to be during myelination. We also found that β-GlcChol and β-GalChol are secreted from neurons and glial cells in association with exosomes. In vitro enzyme assays confirmed that GBA1 and GBA2 have transgalactosylation activity to transfer the galactose residue from GalCer to cholesterol to form β-GalChol. 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Ide, Mitsuko ; Nagatsuka, Yasuko ; Sayano, Tomoko ; Nakanishi, Etsuro ; Uemura, Norihito ; Yuyama, Kohei ; Yamaguchi, Yoshiki ; Kamiguchi, Hiroyuki ; Takahashi, Ryosuke ; Aerts, Johannes M.F.G. ; Greimel, Peter ; Hirabayashi, Yoshio</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c447t-1bf0969463dcc8b2bab9528f2a146dc8eaa207e9bffd82ae30bede02f82f7b0f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>brain</topic><topic>Brain - cytology</topic><topic>Brain - metabolism</topic><topic>Cell Line, Tumor</topic><topic>Cells, Cultured</topic><topic>cholesterol</topic><topic>Cholesterol - analogs &amp; derivatives</topic><topic>Cholesterol - metabolism</topic><topic>Female</topic><topic>Galactose - metabolism</topic><topic>galactosylated cholesterol</topic><topic>Galactosylceramides - metabolism</topic><topic>glucocerebrosidase</topic><topic>Glucosylceramidase - genetics</topic><topic>Glucosylceramidase - metabolism</topic><topic>glycolipid</topic><topic>Humans</topic><topic>Lipids</topic><topic>Male</topic><topic>mass spectrometry (MS)</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Inbred ICR</topic><topic>Myelin Sheath - metabolism</topic><topic>Neuroglia - metabolism</topic><topic>Neurons - metabolism</topic><topic>Oryzias</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>sterol</topic><topic>sterylglycoside</topic><topic>transglycosylation</topic><topic>β-cholesterylgalactoside</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Akiyama, Hisako</creatorcontrib><creatorcontrib>Ide, Mitsuko</creatorcontrib><creatorcontrib>Nagatsuka, Yasuko</creatorcontrib><creatorcontrib>Sayano, Tomoko</creatorcontrib><creatorcontrib>Nakanishi, Etsuro</creatorcontrib><creatorcontrib>Uemura, Norihito</creatorcontrib><creatorcontrib>Yuyama, Kohei</creatorcontrib><creatorcontrib>Yamaguchi, Yoshiki</creatorcontrib><creatorcontrib>Kamiguchi, Hiroyuki</creatorcontrib><creatorcontrib>Takahashi, Ryosuke</creatorcontrib><creatorcontrib>Aerts, Johannes M.F.G.</creatorcontrib><creatorcontrib>Greimel, Peter</creatorcontrib><creatorcontrib>Hirabayashi, Yoshio</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Akiyama, Hisako</au><au>Ide, Mitsuko</au><au>Nagatsuka, Yasuko</au><au>Sayano, Tomoko</au><au>Nakanishi, Etsuro</au><au>Uemura, Norihito</au><au>Yuyama, Kohei</au><au>Yamaguchi, Yoshiki</au><au>Kamiguchi, Hiroyuki</au><au>Takahashi, Ryosuke</au><au>Aerts, Johannes M.F.G.</au><au>Greimel, Peter</au><au>Hirabayashi, Yoshio</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Glucocerebrosidases catalyze a transgalactosylation reaction that yields a newly-identified brain sterol metabolite, galactosylated cholesterol</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2020-04-17</date><risdate>2020</risdate><volume>295</volume><issue>16</issue><spage>5257</spage><epage>5277</epage><pages>5257-5277</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>β-Glucocerebrosidase (GBA) hydrolyzes glucosylceramide (GlcCer) to generate ceramide. 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Analyses of brain tissues from GBA2-deficient mice and GBA1- and/or GBA2-deficient Japanese rice fish (Oryzias latipes) revealed that GBA1 and GBA2 are responsible for β-GlcChol degradation and formation, respectively, and that both GBA1 and GBA2 are responsible for β-GalChol formation. Liquid chromatography–tandem MS revealed that β-GlcChol and β-GalChol are present throughout development from embryo to adult in the mouse brain. We found that β-GalChol expression depends on galactosylceramide (GalCer), and developmental onset of β-GalChol biosynthesis appeared to be during myelination. We also found that β-GlcChol and β-GalChol are secreted from neurons and glial cells in association with exosomes. In vitro enzyme assays confirmed that GBA1 and GBA2 have transgalactosylation activity to transfer the galactose residue from GalCer to cholesterol to form β-GalChol. 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subjects Animals
brain
Brain - cytology
Brain - metabolism
Cell Line, Tumor
Cells, Cultured
cholesterol
Cholesterol - analogs & derivatives
Cholesterol - metabolism
Female
Galactose - metabolism
galactosylated cholesterol
Galactosylceramides - metabolism
glucocerebrosidase
Glucosylceramidase - genetics
Glucosylceramidase - metabolism
glycolipid
Humans
Lipids
Male
mass spectrometry (MS)
Mice
Mice, Inbred BALB C
Mice, Inbred C57BL
Mice, Inbred ICR
Myelin Sheath - metabolism
Neuroglia - metabolism
Neurons - metabolism
Oryzias
Rats
Rats, Wistar
sterol
sterylglycoside
transglycosylation
β-cholesterylgalactoside
title Glucocerebrosidases catalyze a transgalactosylation reaction that yields a newly-identified brain sterol metabolite, galactosylated cholesterol
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