Astrocyte-Derived BDNF supports myelin protein synthesis after cuprizone-induced demyelination

Journal of Neuroscience

Volumn 34, Issue 24, 2014, Pages 8186-8196

  Fulmer, Clifton G ^a,b   VonDran, Melissa W ^a,b,c   Stillman, Althea A ^a   Huang, Yangyang ^a   Hempstead, Barbara L ^c   Dreyfus, Cheryl F ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

ACPD; Astrocytes; BDNF; Cuprizone; Metabotropic receptors; Oligodendrocytes

Indexed keywords

1 AMINO 1, 3 CYCLOPENTANEDICARBOXYLIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYTOCHROME C1; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 5; METABOTROPIC RECEPTOR; MYELIN PROTEIN; TAMOXIFEN; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ACPD; ASTROCYTES; BDNF; CUPRIZONE; METABOTROPIC RECEPTORS; OLIGODENDROCYTES;

ANIMALS; ASTROCYTES; BRAIN-DERIVED NEUROTROPHIC FACTOR; CUPRIZONE; DEMYELINATING DISEASES; DIOXOLANES; DISEASE MODELS, ANIMAL; ESTROGEN ANTAGONISTS; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELIN PROTEINS; PURINES; RECEPTORS, METABOTROPIC GLUTAMATE; RNA, UNTRANSLATED; SIGNAL TRANSDUCTION; TAMOXIFEN;

EID: 84902125139     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4267-13.2014     Document Type: Article

References (45)

1. Agari T, Yasuhara T, Matsui T, Kuramoto S, Kondo A, Miyoshi Y, Shingo T, Borlongan CV, Date I (2008) Intrapallidal metabotropic glutamate receptor activation in a rat model of Parkinson's disease: behavioral and histological analyses. Brain Res 1203:189-196. CrossRef Medline
2. Aharoni R, Eilam R, Domev H, Labunskay G, Sela M, Arnon R (2005) The immunomodulator glatiramer acetate augments the expression of neurotrophic factors in brains of experimental autoimmune encephalomyelitis mice. Proc Natl Acad Sci U S A 102:19045-19050. CrossRef Medline
3. Aktas O, Küry P, Kieseier B, Hartung HP (2010) Fingolimod is a potential novel therapy for multiple sclerosis. Nat Rev Neurol 6:373-382. CrossRef Medline
4. Arnett HA, Mason J, Marino M, Suzuki K, Matsushima GK, Ting JP (2001) TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci 4:1116-1122. CrossRef Medline
5. Aronica E, Catania MV, Geurts J, Yankaya B, Troost D (2001) Immunohistochemical localization of group I and II metabotropic glutamate receptors in control and amyotrophic lateral sclerosis human spinal cord: upregulation in reactive astrocytes. Neuroscience 105:509-520. CrossRef Medline
6. Aronica E, Gorter JA, Rozemuller AJ, Yankaya B, Troost D (2005) Activation of metabotropic glutamate receptor 3 enhances interleukin (IL)-1beta-stimulated release of IL-6 in cultured human astrocytes. Neuroscience 130:927-933. CrossRef Medline
7. Azoulay D, Vachapova V, Shihman B, Miler A, Karni A (2005) Lower brainderived neurotrophic factor in serum of relapsing remitting MS: reversal by glatiramer acetate. J Neuroimmunol 167:215-218. CrossRef Medline
8. Balázs R, Miller S, Romano C, de Vries A, Chun Y, Cotman CW (1997) Metabotropic glutamate receptor m Glu R5 in astrocytes: pharmacological properties and agonist regulation. J Neurochem 69:151-163. Medline
9. Bruno V, Battaglia G, Casabona G, Copani A, Caciagli F, Nicoletti F (1998) Neuroprotection by glial metabotropic glutamate receptors is mediated by transforming growth factor-beta. J Neurosci 18:9594-9600. Medline
10. Canals JM, Checa N, Marco S, Akerud P, Michels A, Pérez-Navarro E, Tolosa E, Arenas E, Alberch J (2001) Expression of brain-derived neurotrophic factor in cortical neurons is regulated by striatal target area. J Neurosci 21:117-124. Medline
11. Casper KB, McCarthy KD (2006) GFAP-positive progenitor cells produce neurons and oligodendrocytes throughout the CNS. Mol Cell Neurosci 31:676-684. CrossRef Medline
12. Casper KB, Jones K, McCarthy KD (2007) Characterization of astrocytespecific conditional knockouts. Genesis 45:292-299. CrossRef Medline
13. Chow LM, Zhang J, Baker SJ (2008) Inducible Cre recombinase activity in mouse mature astrocytes and adult neural precursor cells. Transgenic Res 17:919-928. CrossRef Medline
14. Chung IY, Benveniste EN (1990) Tumor necrosis factor-alpha production by astrocytes. Induction by lipopolysaccharide, IFN-gamma, and IL-1beta. J Immunol 144:2999-3007. Medline
15. Ciccarelli R, Di Iorio P, Bruno V, Battaglia G, D'Alimonte I, D'Onofrio M, Nicoletti F, Caciagli F (1999) Activation of A(1) adenosine or m Glu3 metabotropic glutamate receptors enhances the release of nerve growth factor and S-100beta protein from cultured astrocytes. Glia 27:275-281. CrossRef Medline
16. Dai X, Lercher LD, Clinton PM, Du Y, Livingston DL, Vieira C, Yang L, Shen MM, Dreyfus CF (2003) The trophic role of oligodendrocytes in the basal forebrain. J Neurosci 23:5846-5853. Medline
17. Deogracias R, Yazdani M, Dekkers MP, Guy J, Ionescu MC, Vogt KE, Barde YA (2012) Fingolimod, a sphingosine-1 phosphate receptor modulator, increases BDNF levels and improves symptoms of a mouse model of Rett syndrome. Proc Natl Acad Sci U S A109:14230-14235. CrossRef Medline
18. Di Liberto V, Bonomo A, Frinchi M, Belluardo N, Mudò G (2010) Group II metabotropic glutamate receptor activation by agonist LY379268 treatment increases the expression of brain derived neurotrophic factor in the mouse brain. Neuroscience 165:863-873. CrossRef Medline
19. Dougherty KD, Dreyfus CF, Black IB (2000) Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiol Dis 7:574-585. CrossRef Medline
20. Du Y, Lercher LD, Zhou R, Dreyfus CF (2006) Mitogen-activated protein kinase pathway mediates effects of brain-derived neurotrophic factor on differentiation of basal forebrain oligodendrocytes. J Neurosci Res 84: 1692-1702. CrossRef Medline
21. Fazio F, Notartomaso S, Aronica E, Storto M, Battaglia G, Vieira E, Gatti S, Bruno V, Biagioni F, Gradini R, Nicoletti F, Di Marco R (2008) Switch in the expression of m Glu1 and m Glu5 metabotropic glutamate receptors in the cerebellum of mice developing experimental autoimmune encephalomyelitis and in autoptic cerebellar samples from patients with multiple sclerosis. Neuropharmacology 55:491-499. CrossRef Medline
22. Geurts JJ, Wolswijk G, Bö L, van der Valk P, Polman CH, Troost D, Aronica E (2003) Altered expression patterns of group I and II metabotropic glutamate receptors in multiple sclerosis. Brain 126:1755-1766. CrossRef Medline
23. Guo L, Sawkar A, Zasadzki M, Watterson DM, Van Eldik LJ (2001) Similar activation of glial cultures from different rat brain regions by neuroinflammatory stimuli and downregulation of the activation by a new class of small molecule ligands. Neurobiol Aging 22:975-981. CrossRef Medline
24. Halassa MM, Haydon PG (2010) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu Rev physiol 72: 335-355. CrossRef Medline
25. Hashimoto R, Udagawa J, Kagohashi Y, Matsumoto A, Hatta T, Otani H (2011) Direct and indirect effects of neuropeptide Y and neurotrophin 3 on myelination in the neonatal brains. Brain Res 1373:55-66. CrossRef Medline
26. Huang YT, Lai PC, Wu CC, Hsu SH, Cheng CC, Lan YF, Chiu TH (2010) BDNF mediated Trk B activation is a survival signal for transitional cell carcinoma cells. Int J Oncol 36:1469-1476. CrossRef Medline
27. Jean YY, Lercher LD, Dreyfus CF (2008) Glutamate elicits release of BDNF from basal forebrain astrocytes in a process dependent on metabotropic receptors and the PLC pathway. Neuron Glia Biol 4:35-42. CrossRef Medline
28. Komoly S, Hudson LD, Webster HD, Bondy CA (1992) Insulin-like growth factor I gene expression is induced in astrocytes during experimental demyelination. Proc Natl Acad Sci U S A 89:1894-1898. CrossRef Medline
29. Makar TK, Bever CT, Singh IS, Royal W, Sahu SN, Sura TP, Sultana S, Sura KT, Patel N, Dhib-Jalbut S, Trisler D (2009) Brain-derived neurotrophic factor gene delivery in an animal model of multiple sclerosis using bone marrow stem cells as a vehicle. J Neuroimmunol 210:40-51. CrossRef Medline
30. Mason JL, Ye P, Suzuki K, D'Ercole AJ, Matsushima GK (2000) Insulin-like growth factor-1 inhibits mature oligodendrocyte apoptosis during primary demyelination. J Neurosci 20:5703-5708. Medline
31. Mason JL, Suzuki K, Chaplin DD, Matsushima GK (2001) Interleukin-1beta promotes repair of the CNS. J Neurosci 21:7046-7052. Medline
32. Mason JL, Xuan S, Dragatsis I, Efstratiadis A, Goldman JE (2003) Insulinlike growth factor (IGF) signaling through type 1 IGF receptor plays an important role in remyelination. J Neurosci 23:7710-7718. Medline
33. Matsumoto T, Rauskolb S, Polack M, Klose J, Kolbeck R, Korte M, Barde YA (2008) Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat Neurosci 11:131-133. CrossRef Medline
34. Nakahara K, Okada M, Nakanishi S (1997) The metabotropic glutamate receptor m Glu R5 induces calcium oscillations in cultured astrocytes via protein kinase C phosphorylation. J Neurochem 69:1467-1475. Medline
35. Poduslo JF, Curran GL (1996) Permeability at the blood-brain and bloodnerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF. Brain Res Mol Brain Res 36:280-286. CrossRef Medline
36. Rios M, Fan G, Fekete C, Kelly J, Bates B, Kuehn R, Lechan RM, Jaenisch R (2001) Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol Endocrinol 15: 1748-1757. CrossRef Medline
37. Van't Veer A, Du Y, Fischer TZ, Boetig DR, Wood MR, Dreyfus CF (2009) Brain-derived neurotrophic factor effects on oligodendrocyte progenitors of the basal forebrain are mediated through trk B and the MAP kinase pathway. J Neurosci Res 87:69-78. CrossRef Medline
38. Vondran MW, Clinton-Luke P, Honeywell JZ, Dreyfus CF (2010) BDNF mice exhibit deficits in oligodendrocyte lineage cells of the basal forebrain. Glia 58:848-856. CrossRef Medline
39. Von Dran MW, Singh H, Honeywell JZ, Dreyfus CF (2011) Levels of BDNF impact oligodendrocyte lineage cells following a cuprizone lesion. J Neurosci 31:14182-14190. CrossRef Medline
40. Wake H, Lee PR, Fields RD (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333:1647-1651. CrossRef Medline
41. Wong AW, Xiao J, Kemper D, Kilpatrick TJ, Murray SS (2013) Oligodendroglial expression of Trk B independently regulates myelination and progenitor cell proliferation. J Neurosci 33:4947-4957. CrossRef Medline
42. Woodruff RH, Fruttiger M, Richardson WD, Franklin RJ (2004) Plateletderived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol Cell Neurosci 25:252-262. CrossRef Medline
43. Wu H, Friedman WJ, Dreyfus CF (2004) Differential regulation of neurotrophin expression in basal forebrain astrocytes by neuronal signals. J Neurosci Res 76:76-85. CrossRef Medline
44. Yang J, Siao CJ, Nagappan G, Marinic T, Jing D, McGrath K, Chen ZY, Mark W, Tessarollo L, Lee FS, Lu B, Hempstead BL (2009) Neuronal release of pro BDNF. Nat Neurosci 12:113-115. CrossRef Medline
45. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG, Barres BA (2012) Genomic analysis of reactive astrogliosis. J Neurosci 32:6391-6410. CrossRef Medline