FTY720 requires vitamin B12-TCN2-CD320 signaling in astrocytes to reduce disease in an animal model of multiple sclerosis

Vitamin B12 (B12) deficiency causes neurological manifestations resembling multiple sclerosis (MS); however, a molecular explanation for the similarity is unknown. FTY720 (fingolimod) is a sphingosine 1-phosphate (S1P) receptor modulator and sphingosine analog approved for MS therapy that can functi...

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Published inCell reports (Cambridge) Vol. 42; no. 12; p. 113545
Main Authors Jonnalagadda, Deepa, Kihara, Yasuyuki, Groves, Aran, Ray, Manisha, Saha, Arjun, Ellington, Clayton, Lee-Okada, Hyeon-Cheol, Furihata, Tomomi, Yokomizo, Takehiko, Quadros, Edward V., Rivera, Richard, Chun, Jerold
Format Journal Article
LanguageEnglish
Published Elsevier Inc 26.12.2023
Elsevier
Subjects
cobalamin
CP: Neuroscience
demyelination
inflammation
lysophospholipid receptor
neurology
ozanimod
ponesimod
siponimod
sphingolipid
sphingosine kinase
ozanimod
cobalamin
inflammation
sphingolipid
CP: Neuroscience
demyelination
sphingosine kinase
ponesimod
lysophospholipid receptor
neurology
siponimod
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Abstract Vitamin B12 (B12) deficiency causes neurological manifestations resembling multiple sclerosis (MS); however, a molecular explanation for the similarity is unknown. FTY720 (fingolimod) is a sphingosine 1-phosphate (S1P) receptor modulator and sphingosine analog approved for MS therapy that can functionally antagonize S1P1. Here, we report that FTY720 suppresses neuroinflammation by functionally and physically regulating the B12 pathways. Genetic and pharmacological S1P1 inhibition upregulates a transcobalamin 2 (TCN2)-B12 receptor, CD320, in immediate-early astrocytes (ieAstrocytes; a c-Fos-activated astrocyte subset that tracks with experimental autoimmune encephalomyelitis [EAE] severity). CD320 is also reduced in MS plaques. Deficiency of CD320 or dietary B12 restriction worsens EAE and eliminates FTY720’s efficacy while concomitantly downregulating type I interferon signaling. TCN2 functions as a chaperone for FTY720 and sphingosine, whose complex induces astrocytic CD320 internalization, suggesting a delivery mechanism of FTY720/sphingosine via the TCN2-CD320 pathway. Taken together, the B12-TCN2-CD320 pathway is essential for the mechanism of action of FTY720. [Display omitted] •CD320 expression is suppressed in MS and EAE astrocytes•S1P1 inhibition upregulates CD320 expression in astrocytes•Fingolimod and sphingosine directly bind to TCN2•Fingolimod-bound TCN2 promotes CD320 internalization in astrocytes Jonnalagadda et al. find fingolimod-mediated maintenance of vitamin B12 homeostasis in the CNS. Fingolimod binds directly to TCN2 to form a complex that promotes vitamin B12 availability in astrocytes through internalization of CD320, followed by phosphorylation of fingolimod, which functionally antagonizes S1P1, resulting in upregulation of CD320 in astrocytes.
AbstractList Vitamin B12 (B12) deficiency causes neurological manifestations resembling multiple sclerosis (MS); however, a molecular explanation for the similarity is unknown. FTY720 (fingolimod) is a sphingosine 1-phosphate (S1P) receptor modulator and sphingosine analog approved for MS therapy that can functionally antagonize S1P1. Here, we report that FTY720 suppresses neuroinflammation by functionally and physically regulating the B12 pathways. Genetic and pharmacological S1P1 inhibition upregulates a transcobalamin 2 (TCN2)-B12 receptor, CD320, in immediate-early astrocytes (ieAstrocytes; a c-Fos-activated astrocyte subset that tracks with experimental autoimmune encephalomyelitis [EAE] severity). CD320 is also reduced in MS plaques. Deficiency of CD320 or dietary B12 restriction worsens EAE and eliminates FTY720's efficacy while concomitantly downregulating type I interferon signaling. TCN2 functions as a chaperone for FTY720 and sphingosine, whose complex induces astrocytic CD320 internalization, suggesting a delivery mechanism of FTY720/sphingosine via the TCN2-CD320 pathway. Taken together, the B12-TCN2-CD320 pathway is essential for the mechanism of action of FTY720.
Vitamin B12 (B12) deficiency causes neurological manifestations resembling multiple sclerosis (MS); however, a molecular explanation for the similarity is unknown. FTY720 (fingolimod) is a sphingosine 1-phosphate (S1P) receptor modulator and sphingosine analog approved for MS therapy that can functionally antagonize S1P1. Here, we report that FTY720 suppresses neuroinflammation by functionally and physically regulating the B12 pathways. Genetic and pharmacological S1P1 inhibition upregulates a transcobalamin 2 (TCN2)-B12 receptor, CD320, in immediate-early astrocytes (ieAstrocytes; a c-Fos-activated astrocyte subset that tracks with experimental autoimmune encephalomyelitis [EAE] severity). CD320 is also reduced in MS plaques. Deficiency of CD320 or dietary B12 restriction worsens EAE and eliminates FTY720’s efficacy while concomitantly downregulating type I interferon signaling. TCN2 functions as a chaperone for FTY720 and sphingosine, whose complex induces astrocytic CD320 internalization, suggesting a delivery mechanism of FTY720/sphingosine via the TCN2-CD320 pathway. Taken together, the B12-TCN2-CD320 pathway is essential for the mechanism of action of FTY720. [Display omitted] •CD320 expression is suppressed in MS and EAE astrocytes•S1P1 inhibition upregulates CD320 expression in astrocytes•Fingolimod and sphingosine directly bind to TCN2•Fingolimod-bound TCN2 promotes CD320 internalization in astrocytes Jonnalagadda et al. find fingolimod-mediated maintenance of vitamin B12 homeostasis in the CNS. Fingolimod binds directly to TCN2 to form a complex that promotes vitamin B12 availability in astrocytes through internalization of CD320, followed by phosphorylation of fingolimod, which functionally antagonizes S1P1, resulting in upregulation of CD320 in astrocytes.
ArticleNumber 113545
Author Lee-Okada, Hyeon-Cheol
Yokomizo, Takehiko
Quadros, Edward V.
Rivera, Richard
Jonnalagadda, Deepa
Chun, Jerold
Kihara, Yasuyuki
Groves, Aran
Saha, Arjun
Ray, Manisha
Ellington, Clayton
Furihata, Tomomi
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  organization: Department of Biochemistry, Graduate School of Medicine, Juntendo University, Hongo 2-1-1, Bunkyo-ku, Tokyo 113-8421, Japan
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  givenname: Tomomi
  surname: Furihata
  fullname: Furihata, Tomomi
  organization: Laboratory of Clinical Pharmacy and Experimental Therapeutics, School of Pharmacy, Tokyo University of Pharmacy and Life Sciences, Tokyo 192-0392, Japan
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  surname: Yokomizo
  fullname: Yokomizo, Takehiko
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  givenname: Edward V.
  surname: Quadros
  fullname: Quadros, Edward V.
  organization: Department of Medicine, SUNY-Downstate Medical Center, 450 Clarkson Avenue, Brooklyn, NY 11203, USA
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  givenname: Richard
  surname: Rivera
  fullname: Rivera, Richard
  organization: Sanford Burnham Prebys Medical Discovery Institute, 10901 N. Torrey Pines Road, La Jolla, CA 92037, USA
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  givenname: Jerold
  surname: Chun
  fullname: Chun, Jerold
  email: jchun@sbpdiscovery.org
  organization: Sanford Burnham Prebys Medical Discovery Institute, 10901 N. Torrey Pines Road, La Jolla, CA 92037, USA
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Issue 12
Keywords ozanimod
cobalamin
inflammation
sphingolipid
CP: Neuroscience
demyelination
sphingosine kinase
ponesimod
lysophospholipid receptor
neurology
siponimod
Language English
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Snippet Vitamin B12 (B12) deficiency causes neurological manifestations resembling multiple sclerosis (MS); however, a molecular explanation for the similarity is...
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SubjectTerms cobalamin
CP: Neuroscience
demyelination
inflammation
lysophospholipid receptor
neurology
ozanimod
ponesimod
siponimod
sphingolipid
sphingosine kinase
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Title FTY720 requires vitamin B12-TCN2-CD320 signaling in astrocytes to reduce disease in an animal model of multiple sclerosis
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Volume 42
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