Cited by 812

Neurotransmitter-Triggered Transfer of Exosomes Mediates Oligodendrocyte–Neuron Communication

Frühbeis, Carsten, Fröhlich, Dominik, Kuo, Wen Ping, Amphornrat, Jesa, Thilemann, Sebastian, Saab, Aiman S., Kirchhoff, Frank, Möbius, Wiebke +7 more·2013·PLoS Biology

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pbio.1001604

Cites

9 of 9 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Exosomes released by Schwann cells and oligodendrocytes can be taken up by neuronal axons to increase neurite growth, enhance axonal regeneration and improve neuronal survival.

    “Exosomes released by Schwann cells and oligodendrocytes can be taken up by neuronal axons to increase neurite growth, enhance axonal regeneration and improve neuronal survival49,50.”
  • EV fusion allows direct retrieval of EV cargo in the cytosol of neurons, avoiding degradation in late endosome or lysosomes, where EVs may accumulate after endocytosis.

    “EV fusion allows direct retrieval of EV cargo in the cytosol of neurons, avoiding degradation in late endosome or lysosomes, where EVs may accumulate after endocytosis [13, 26, 28].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 80

  1. [1]Sherman DL, Brophy PJ (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6: 683– 690. 16136172
  2. [2]Nave KA (2010) Myelination and support of axonal integrity by glia. Nature 468: 244– 252. 21068833
  3. [4]Fields RD, Burnstock G (2006) Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7: 423– 436. 16715052 PMC2062484
  4. [6]Nave KA, Trapp BD (2008) Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 31: 535– 561. 18558866
  5. [7]Nave KA (2010) Myelination and the trophic support of long axons. Nat Rev Neurosci 11: 275– 283. 20216548
  6. [10]Krämer-Albers EM, Bretz N, Tenzer S, Winterstein C, Möbius W, et al (2007) Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: Trophic support for axons? Proteomics Clin Appl 1446– 1461. 21136642
  7. [11]Bakhti M, Winter C, Simons M (2010) Inhibition of myelin membrane sheath formation by oligodendrocyte-derived exosome-like vesicles. J Biol Chem 286: 787– 796. 20978131 PMC3013037
  8. [12]Simons M, Raposo G (2009) Exosomes–vesicular carriers for intercellular communication. Curr Opin Cell Biol 21: 575– 581. 19442504
  9. [13]Raposo G, Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. The Journal of Cell Biology 200: 373– 383. 23420871 PMC3575529
  10. [14]Cocucci E, Racchetti G, Meldolesi J (2009) Shedding microvesicles: artefacts no more. Trends Cell Biol 19: 43– 51. 19144520
  11. [15]Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, et al (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654– 659. 17486113
  12. [16]Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, et al (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470– 1476. 19011622 PMC3423894
  13. [17]Zhang Y, Liu D, Chen X, Li J, Li L, et al (2010) Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39: 133– 144. 20603081
  14. [18]Fevrier B, Vilette D, Archer F, Loew D, Faigle W, et al (2004) Cells release prions in association with exosomes. Proc Natl Acad Sci U S A 101: 9683– 9688. 15210972 PMC470735
  15. [19]Thery C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581– 593. 19498381
  16. [20]Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, et al (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nature Medicine 18: 883– 891. PMC3645291 22635005
  17. [21]Savina A, Furlan M, Vidal M, Colombo MI (2003) Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem 278: 20083– 20090. 12639953
  18. [22]Lachenal G, Pernet-Gallay K, Chivet M, Hemming FJ, Belly A, et al (2011) Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol Cell Neurosci 46: 409– 418. 21111824
  19. [24]Hovelmeyer N, Hao Z, Kranidioti K, Kassiotis G, Buch T, et al (2005) Apoptosis of oligodendrocytes via Fas and TNF-R1 is a key event in the induction of experimental autoimmune encephalomyelitis. Journal of Immunology 175: 5875– 5884. 16237080
  20. [25]Locatelli G, Wortge S, Buch T, Ingold B, Frommer F, et al (2012) Primary oligodendrocyte death does not elicit anti-CNS immunity. Nat Neurosci 15: 543– 550. 22366759
  21. [26]Butt AM (2006) Neurotransmitter-mediated calcium signalling in oligodendrocyte physiology and pathology. Glia 54: 666– 675. 17006895
  22. [27]Oka A, Belliveau MJ, Rosenberg PA, Volpe JJ (1993) Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J Neurosci 13: 1441– 1453. 8096541 PMC6576718
  23. [28]Yoshioka A, Hardy M, Younkin DP, Grinspan JB, Stern JL, et al (1995) Alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptors mediate excitotoxicity in the oligodendroglial lineage. Journal of Neurochemistry 64: 2442– 2448. 7539052
  24. [29]Hsu C, Morohashi Y, Yoshimura S, Manrique-Hoyos N, Jung S, et al (2010) Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J Cell Biol 189: 223– 232. 20404108 PMC2856897
  25. [30]Li S, Stys PK (2000) Mechanisms of ionotropic glutamate receptor-mediated excitotoxicity in isolated spinal cord white matter. J Neurosci 20: 1190– 1198. 10648723 PMC6774174
  26. [31]Karadottir R, Cavelier P, Bergersen LH, Attwell D (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438: 1162– 1166. 16372011 PMC1416283
  27. [32]Salter MG, Fern R (2005) NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438: 1167– 1171. 16372012
  28. [33]Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, et al (2006) NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439: 988– 992. 16372019
  29. [34]Karadottir R, Attwell D (2007) Neurotransmitter receptors in the life and death of oligodendrocytes. Neuroscience 145: 1426– 1438. 17049173 PMC2173944
  30. [35]Mothet JP, Parent AT, Wolosker H, Brady RO Jr, Linden DJ, et al (2000) D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc Natl Acad Sci U S A 97: 4926– 4931. 10781100 PMC18334
  31. [36]Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, et al (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33: 366– 374. 12590258
  32. [38]Chiu SY, Kriegler S (1994) Neurotransmitter-mediated signaling between axons and glial cells. Glia 11: 191– 200. 7927647
  33. [39]Butt AM, Pugh M, Hubbard P, James G (2004) Functions of optic nerve glia: axoglial signalling in physiology and pathology. Eye (Lond) 18: 1110– 1121. 15534596
  34. [40]Stevens B, Porta S, Haak LL, Gallo V, Fields RD (2002) Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36: 855– 868. 12467589 PMC1201407
  35. [41]Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, et al (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A 107: 6328– 6333. 20304794 PMC2851954
  36. [42]Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, et al (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319: 1244– 1247. 18309083
  37. [43]Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, et al (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839– 850. 16740485
  38. [44]von Kleist L, Stahlschmidt W, Bulut H, Gromova K, Puchkov D, et al (2011) Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146: 471– 484. 21816279
  39. [46]Guggenhuber S, Monory K, Lutz B, Klugmann M (2010) AAV vector-mediated overexpression of CB1 cannabinoid receptor in pyramidal neurons of the hippocampus protects against seizure-induced excitoxicity. PLoS One 5: e15707 doi: 10.1371/journal.pone.0015707 21203567 PMC3006205 · DOI
  40. [47]Ziskin JL, Nishiyama A, Rubio M, Fukaya M, Bergles DE (2007) Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10: 321– 330. 17293857 PMC2140234
  41. [48]Kukley M, Capetillo-Zarate E, Dietrich D (2007) Vesicular glutamate release from axons in white matter. Nat Neurosci 10: 311– 320. 17293860
  42. [49]Li S, Mealing GA, Morley P, Stys PK (1999) Novel injury mechanism in anoxia and trauma of spinal cord white matter: glutamate release via reverse Na+-dependent glutamate transport. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 19: RC16. 10407058 PMC6783104
  43. [50]Kolodziejczyk K, Saab AS, Nave KA, Attwell D (2010) Why do oligodendrocyte lineage cells express glutamate receptors? F1000 Biol Rep 2: 57. 21173873 PMC2990618
  44. [51]Matute C (2011) Glutamate and ATP signalling in white matter pathology. Journal of Anatomy 219: 53– 64. 21250988 PMC3130160
  45. [52]Rosin C, Bates TE, Skaper SD (2004) Excitatory amino acid induced oligodendrocyte cell death in vitro: receptor-dependent and -independent mechanisms. Journal of Neurochemistry 90: 1173– 1185. 15312172
  46. [53]Alberdi E, Sanchez-Gomez MV, Torre I, Domercq M, Perez-Samartin A, et al (2006) Activation of kainate receptors sensitizes oligodendrocytes to complement attack. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 26: 3220– 3228. 16554473 PMC6674098
  47. [54]Domercq M, Etxebarria E, Perez-Samartin A, Matute C (2005) Excitotoxic oligodendrocyte death and axonal damage induced by glutamate transporter inhibition. Glia 52: 36– 46. 15892126
  48. [55]Barres BA, Raff MC (1993) Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361: 258– 260. 8093806
  49. [56]Demerens C, Stankoff B, Logak M, Anglade P, Allinquant B, et al (1996) Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci U S A 93: 9887– 9892. 8790426 PMC38524
  50. [57]Coman I, Barbin G, Charles P, Zalc B, Lubetzki C (2005) Axonal signals in central nervous system myelination, demyelination and remyelination. Journal of the Neurological Sciences 233: 67– 71. 15894333
  51. [58]Bergles DE, Roberts JD, Somogyi P, Jahr CE (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405: 187– 191. 10821275
  52. [59]De Biase LM, Kang SH, Baxi EG, Fukaya M, Pucak ML, et al (2011) NMDA receptor signaling in oligodendrocyte progenitors is not required for oligodendrogenesis and myelination. J Neurosci 31: 12650– 12662. 21880926 PMC3179911
  53. [60]Guo F, Maeda Y, Ko EM, Delgado M, Horiuchi M, et al (2012) Disruption of NMDA receptors in oligodendroglial lineage cells does not alter their susceptibility to experimental autoimmune encephalomyelitis or their normal development. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 32: 639– 645. 22238099 PMC3403747
  54. [61]Fitzner D, Schnaars M, van Rossum D, Krishnamoorthy G, Dibaj P, et al (2011) Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J Cell Sci 124: 447– 458. 21242314
  55. [62]Meckes DG Jr, Shair KH, Marquitz AR, Kung CP, Edwards RH, et al (2010) Human tumor virus utilizes exosomes for intercellular communication. Proc Natl Acad Sci U S A 107: 20370– 20375. 21059916 PMC2996715
  56. [63]Hergenreider E, Heydt S, Treguer K, Boettger T, Horrevoets AJ, et al (2012) Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 14: 249– 256. 22327366
  57. [64]Brown IR (2007) Heat shock proteins and protection of the nervous system. Annals of the New York Academy of Sciences 1113: 147– 158. 17656567
  58. [65]Tytell M, Greenberg SG, Lasek RJ (1986) Heat shock-like protein is transferred from glia to axon. Brain Res 363: 161– 164. 3947949
  59. [66]Eyman M, Cefaliello C, Ferrara E, De Stefano R, Lavina ZS, et al (2007) Local synthesis of axonal and presynaptic RNA in squid model systems. Eur J Neurosci 25: 341– 350. 17284174
  60. [67]Shrager P, Chiu SY, Ritchie JM (1985) Voltage-dependent sodium and potassium channels in mammalian cultured Schwann cells. Proc Natl Acad Sci U S A 82: 948– 952. 2579384 PMC397165
  61. [68]Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, et al (1998) Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280: 1610– 1613. 9616125
  62. [69]Court FA, Hendriks WT, MacGillavry HD, Alvarez J, van Minnen J (2008) Schwann cell to axon transfer of ribosomes: toward a novel understanding of the role of glia in the nervous system. J Neurosci 28: 11024– 11029. 18945910 PMC6671360
  63. [70]Court FA, Midha R, Cisterna BA, Grochmal J, Shakhbazau A, et al (2011) Morphological evidence for a transport of ribosomes from Schwann cells to regenerating axons. Glia 59: 1529– 1539. 21656857
  64. [72]Chivet M, Hemming F, Pernet-Gallay K, Fraboulet S, Sadoul R (2012) Emerging role of neuronal exosomes in the central nervous system. Frontiers in Physiology 3: 145. 22654762 PMC3361079
  65. [73]Schneider A, Simons M (2012) Exosomes: vesicular carriers for intercellular communication in neurodegenerative disorders. Cell and Tissue Research 352 ((1)) 33– 47. 22610588 PMC3602607
  66. [74]Antonucci F, Turola E, Riganti L, Caleo M, Gabrielli M, et al (2012) Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism. Embo J 31: 1231– 1240. 22246184 PMC3297996
  67. [75]Verderio C, Muzio L, Turola E, Bergami A, Novellino L, et al (2012) Myeloid microvesicles are a marker and therapeutic target for neuroinflammation. Annals of Neurology 72: 610– 624. 23109155
  68. [76]Bellingham SA, Guo BB, Coleman BM, Hill AF (2012) Exosomes: vehicles for the transfer of toxic proteins associated with neurodegenerative diseases? Frontiers in Physiology 3: 124. 22563321 PMC3342525
  69. [77]Rajendran L, Honsho M, Zahn TR, Keller P, Geiger KD, et al (2006) Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc Natl Acad Sci U S A 103: 11172– 11177. 16837572 PMC1544060
  70. [78]Gomes C, Keller S, Altevogt P, Costa J (2007) Evidence for secretion of Cu,Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis. Neurosci Lett 428: 43– 46. 17942226
  71. [80]Strauss K, Goebel C, Runz H, Mobius W, Weiss S, et al (2010) Exosome secretion ameliorates lysosomal storage of cholesterol in Niemann-Pick type C disease. J Biol Chem 285: 26279– 26288. 20554533 PMC2924046
  72. [81]Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, et al (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol 29: 341– 345. 21423189
  73. [82]Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, et al (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4. 11299042 PMC31338
  74. [83]Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genetics 21: 70– 71. 9916792
  75. [84]Krämer EM, Koch T, Niehaus A, Trotter J (1997) Oligodendrocytes direct glycosyl phosphatidylinositol-anchored proteins to the myelin sheath in glycosphingolipid-rich complexes. J Biol Chem 272: 8937– 8945. 9083015
  76. [85]Feldmann A, Amphornrat J, Schonherr M, Winterstein C, Mobius W, et al (2011) Transport of the major myelin proteolipid protein is directed by VAMP3 and VAMP7. J Neurosci 31: 5659– 5672. 21490207 PMC6622839
  77. [86]Klugmann M, Symes CW, Leichtlein CB, Klaussner BK, Dunning J, et al (2005) AAV-mediated hippocampal expression of short and long Homer 1 proteins differentially affect cognition and seizure activity in adult rats. Mol Cell Neurosci 28: 347– 360. 15691715
  78. [87]Austyn JM, Gordon S (1981) F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol 11: 805– 815. 7308288
  79. [88]Sommer I, Schachner M (1981) Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol 83: 311– 327. 6786942
  80. [89]Krämer-Albers EM, Gehrig-Burger K, Thiele C, Trotter J, Nave KA (2006) Perturbed interactions of mutant proteolipid protein/DM20 with cholesterol and lipid rafts in oligodendroglia: implications for dysmyelination in spastic paraplegia. J Neurosci 26: 11743– 11752. 17093095 PMC6674790

Cited by

Sorted by citations

Authors
Frühbeis, C., Fröhlich, D., Kuo, W. P., Amphornrat, J., Thilemann, S., Saab, A. S., Kirchhoff, F., Möbius, W., Goebbels, S., Nave, K.-A., Schneider, A., Simons, M., Klugmann, M., Trotter, J., & Krämer-Albers, E.-M.
Venue
PLoS Biology
Published
2013-07-09
Volume
11
Issue
7
Pages
e1001604
ISSN
1545-7885
Cited by
812
References
9
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review