|
|
Metabolic Regulation on Myelination and Remyelination |
LI Pingping, JIANG Xinyue, HU Xinyue, LI Yawen, SONG Yixuan, ZHANG Mingliang |
Department of Histoembryology, Genetics, and Developmental Biology, Shanghai Jiao Tong University School of Medicine, Shanghai Key Laboratory of Reproductive Medicine, Shanghai 200025, China |
|
|
Abstract In the central nervous system (CNS), oligodendrocyte precursor cells (OPCs) proliferate, migrate, and differentiate into oligodendrocytes (OLs), which subsequently form myelin structure that ensheathes the axons of neurons. Myelin enables fast saltatory impulse propagation, provides energy and nutrition for neurons, and facilitates the establishment and maintenance of cognition. Notably, the (re) generation of myelin requires substantial energy consumption. Glucose, the preferred energy resource for many biological processes, plays a vital role in (re) myelination. Thus, we review the recent progress in the regulation of glucose metabolism on myelination to extend our understanding of myelination and to provide insights into the potential strategy for treating diseases of demyelination and neurodegeneration.
|
Received: 03 February 2024
|
|
|
|
|
[1] NAVE K A.Myelination and support of axonal integrity by glia[J]. Nature, 2010, 468(7321) : 244-252. [2] BARNES-VÉLEZ J A, YASAR F B A, HU J. Myelin lipid metabolism and its role in myelination and myelin maintenance[J]. Innovation (Camb) , 2023, 4(1) : 100360. [3] DIENEL G A.Brain Glucose Metabolism: Integration of Energetics with Function[J]. Physiol Rev, 2019, 99(1) : 949-1045. [4] MERGENTHALER P, LINDAUER U, DIENEL G A, et al.Sugar for the brain: the role of glucose in physiological and pathological brain function[J]. Trends Neurosci, 2013, 36(10) : 587-597. [5] LIU X, BLAŽENOVIĆ I, CONTRERAS A J, et al. Hexosamine biosynthetic pathway and O-GlcNAc-processing enzymes regulate daily rhythms in protein O-GlcNAcylation[J]. Nat Commun, 2021, 12(1) : 4173. [6] SUNG Y, YU Y C, HAN J M.Nutrient sensors and their crosstalk[J]. Exp Mol Med, 2023, 55(6) : 1076-1089. [7] ZHAO J, LANG M.New insight into protein glycosylation in the development of Alzheimer's disease[J]. Cell Death Discov, 2023, 9(1) : 1-14. [8] ROWITCH D H, KRIEGSTEIN A R.Developmental genetics of vertebrate glial-cell specification[J]. Nature, 2010, 468(7321) : 214-222. [9] TSAI H H, NIU J, MUNJI R, et al.Oligodendrocyte precursors migrate along vasculature in the developing nervous system[J]. Science, 2016, 351(6271) : 379-384. [10] FAME R M, SHANNON M L, CHAU K F, et al. A concerted metabolic shift in early forebrain alters the CSF proteome and depends on MYC downregulation for mitochondrial maturation[J]. Development, 2019, 146 (20) : dev182857. [11] WANG F, YANG Y J, YANG N, et al. Enhancing Oligodendrocyte Myelination Rescues Synaptic Loss and Improves Functional Recovery after Chronic Hypoxia[J]. Neuron, 2018, 99 (4) : 689-701. e5. [12] ZIABREVA I, CAMPBELL G, RIST J, et al.Injury and differentiation following inhibition of mitochondrial respiratory chain complex IV in rat oligodendrocytes[J]. Glia, 2010, 58(15) : 1827-1837. [13] FORSTON M D, WEI G Z, CHARIKER J H, et al.Enhanced oxidative phosphorylation, re-organized intracellular signaling, and epigenetic de-silencing as revealed by oligodendrocyte translatome analysis after contusive spinal cord injury[J]. Sci Rep, 2023, 13(1) : 21254. [14] RINHOLM J E, VERVAEKE K, TADROSS M R, et al.Movement and structure of mitochondria in oligodendrocytes and their myelin sheaths[J]. Glia, 2016, 64(5) : 810-825. [15] FÜNFSCHILLING U, SUPPLIE L M, MAHAD D, et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity[J]. Nature, 2012, 485(7399) : 517-521. [16] SAAB A S, TZVETAVONA I D, TREVISIOL A, et al.Oligodendroglial NMDA Receptors Regulate Glucose Import and Axonal Energy Metabolism[J]. Neuron, 2016, 91(1) : 119-132. [17] FRANKLIN R J M, FFRENCH-CONSTANT C. Remyelination in the CNS: from biology to therapy[J]. Nat Rev Neurosci, 2008, 9(11) : 839-855. [18] MOLINA-GONZALEZ I, MIRON V E, ANTEL J P.Chronic oligodendrocyte injury in central nervous system pathologies[J]. Commun Biol, 2022, 5(1) : 1-11. [19] CHANG A, TOURTELLOTTE W W, RUDICK R, et al.Premyelinating Oligodendrocytes in Chronic Lesions of Multiple Sclerosis[J]. N Engl J Med, 2002, 346(3) : 165-173. [20] RONE M B, CUI Q L, FANG J, et al.Oligodendrogliopathy in Multiple Sclerosis: Low Glycolytic Metabolic Rate Promotes Oligodendrocyte Survival[J]. J Neurosci, 2016, 36(17) : 4698-4707. [21] PERUZZOTTI-JAMETTI L, PLUCHINO S.Targeting Mitochondrial Metabolism in Neuroinflammation: Towards a Therapy for Progressive Multiple Sclerosis[J]. Trends Mol Med, 2018, 24(10) : 838-855. [22] ASSINCK P, DUNCAN G J, HILTON B J, et al.Cell transplantation therapy for spinal cord injury[J]. Nat Neurosci, 2017, 20(5) : 637-647. [23] WU Y QING, XIONG J, HE Z LI, et al.Metformin promotes microglial cells to facilitate myelin debris clearance and accelerate nerve repairment after spinal cord injury[J]. Acta Pharmacol Sin, 2022, 43(6): 1360-1371. [24] WU H, CHEN X, YU B, et al.Deficient deposition of new myelin impairs adult optic nerve function in a murine model of diabetes[J]. Glia, 2023, 71(5) : 1333-1345. [25] LI J X, HUNG Y T, BAIR H, et al.Sodium-glucose co-transporter 2 inhibitor add-on therapy for metformin delays diabetic retinopathy progression in diabetes patients: a population-based cohort study[J]. Sci Rep, 2023, 13(1) : 17049. [26] ZHANG P, KISHIMOTO Y, GRAMMATIKAKIS I, et al.Senolytic therapy alleviates Aβ-associated oligodendrocyte progenitor cell senescence and cognitive deficits in an Alzheimer's disease model[J]. Nat Neurosci, 2019, 22(5) : 719-728. [27] BALANA A T, LEVINE P M, CRAVEN T W, et al.O-GlcNAc modification of small heat shock proteins enhances their anti-amyloid chaperone activity[J]. Nat Chem, 2021, 13(5) : 441-450. [28] DING J, JI J, RABOW Z, et al.A metabolome atlas of the aging mouse brain[J]. Nat Commun, 2021, 12(1) : 6021. [29] OH J, LEE Y D, WAGERS A J.Stem cell aging: mechanisms, regulators and therapeutic opportunities[J]. Nat Med, 2014, 20(8) : 870-880. [30] NEUMANN B, BAROR R, ZHAO C, et al. Metformin Restores CNS Remyelination Capacity by Rejuvenating Aged Stem Cells[J]. Cell Stem Cell, 2019, 25 (4) : 473-485. e8. [31] MA X R, ZHU X, XIAO Y, et al.Restoring nuclear entry of Sirtuin 2 in oligodendrocyte progenitor cells promotes remyelination during ageing[J]. Nat Commun, 2022, 13(1) : 1225. [32] REILY C, STEWART T J, RENFROW M B, et al.Glycosylation in health and disease[J]. Nat Rev Nephrol, 2019, 15(6) : 346-366. [33] VARKI A, CUMMINGS R D, ESKO J D, et al.Essentials of Glycobiology[M]. 3rd ed. Cold Spring Harbor (NY) : Cold Spring Harbor Laboratory Press, 2015. [34] SY M, BRANDT A U, LEE S U, et al.N-acetylglucosamine drives myelination by triggering oligodendrocyte precursor cell differentiation[J]. J Biol Chem, 2020, 295(51) : 17413-17424. [35] CONROY L R, HAWKINSON T R, YOUNG L E A, et al. Emerging roles of N-linked glycosylation in brain physiology and disorders[J]. Trends Endocrinol Metab, 2021, 32(12) : 980-993. [36] ABAD-RODRÍGUEZ J, DÍEZ-REVUELTA N. Axon glycoprotein routing in nerve polarity, function, and repair[J]. Trends Biochem Sci, 2015, 40(7) : 385-396. [37] SANTOS M, DAMÁSIO J, KUN-RODRIGUES C, et al. Novel MAG Variant Causes Cerebellar Ataxia with Oculomotor Apraxia: Molecular Basis and Expanded Clinical Phenotype[J]. J Clin Med, 2020, 9(4) : 1212. [38] BRANDT A U, SY M, BELLMANN-STROBL J, et al.Association of a Marker of N-Acetylglucosamine With Progressive Multiple Sclerosis and Neurodegeneration[J]. JAMA Neurol, 2021, 78(7) : 842-852. [39] LAU K S, PARTRIDGE E A, GRIGORIAN A, et al.Complex N-Glycan Number and Degree of Branching Cooperate to Regulate Cell Proliferation and Differentiation[J]. Cell, 2007, 129(1) : 123-134. [40] PASQUINI L A, MILLET V, HOYOS H C, et al.Galectin-3 drives oligodendrocyte differentiation to control myelin integrity and function[J]. Cell Death Differ, 2011, 18(11) : 1746-1756. [41] ZHANG Y, YU X, ICHIKAWA M, et al. Autosomal recessive phosphoglucomutase 3 (PGM3) mutations link glycosylation defects to atopy, immune deficiency, autoimmunity,neurocognitive impairment[J]. J Allergy Clin Immunol, 2014, 133 (5) : 1400-1409. e5. [42] KANEKIYO K, INAMORI K ICHIRO, KITAZUME S, et al.Loss of Branched O-Mannosyl Glycans in Astrocytes Accelerates Remyelination[J]. J Neurosci, 2013, 33(24) : 10037-10047. [43] FEHL C, HANOVER J A.Tools, tactics and objectives to interrogate cellular roles of O-GlcNAc in disease[J]. Nat Chem Biol, 2022, 18(1) : 8-17. [44] KIM S, MAYNARD J C, SASAKI Y, et al.Schwann Cell O-GlcNAc Glycosylation Is Required for Myelin Maintenance and Axon Integrity[J]. J Neurosci, 2016, 36(37) : 9633-9646. [45] WHITE C W, FAN X, MAYNARD J C, et al.Age-related loss of neural stem cell O-GlcNAc promotes a glial fate switch through STAT3 activation[J]. Proc Natl Acad Sci USA, 2020, 117(36) : 22214-22224. [46] CHEN L, LI Y, SONG Z, et al.O-GlcNAcylation promotes cerebellum development and medulloblastoma oncogenesis via SHH signaling[J]. Proc Natl Acad Sci USA, 2022, 119(34) : e2202821119. [47] LAGERLÖF O, HART G W, HUGANIR R L. O-GlcNAc transferase regulates excitatory synapse maturity[J]. Proc Natl Acad Sci USA, 2017, 114(7) : 1684-1689. [48] LEE B E, SUH P G, KIM J I.O-GlcNAcylation in health and neurodegenerative diseases[J]. Exp Mol Med, 2021, 53(11) : 1674-1682. [49] YOU Y, JOSEPH C, WANG C, et al.Demyelination precedes axonal loss in the transneuronal spread of human neurodegenerative disease[J]. Brain, 2019, 142(2) : 426-442. [50] 李蕾, 郑海霞, 戴欧阳, 等. 阿尔兹海默症发生机制及脂质代谢在其中的作用[J]. 湖南师范大学学报 (医学版) , 2023, 20(3) : 1-9. [51] CHEN J F, LIU K, HU B, et al. Enhancing myelin renewal reverses cognitive dysfunction in a murine model of Alzheimer's disease[J]. Neuron, 2021, 109 (14) : 2292-2307. e5. |
|
|
|